MOF, Alm.del - 2022-23 (2. samling) - Bilag 251: Orientering om opdaterede vurderinger om COVID-19 og mink

Miljø- og Fødevareudvalget 2022-23 (2. samling)
MOF Alm.del Bilag 251
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SCIENTIFIC OPINION

ADOPTED: 19 January 2023

doi: 10.2903/j.efsa.2023.7822

SARS-CoV-2 in animals: susceptibility of animal species, risk

for animal and public health, monitoring, prevention and

control

EFSA Panel on Animal Health and Welfare (AHAW),

Søren Saxmose Nielsen, Julio Alvarez, Dominique Joseph Bicout, Paolo Calistri,

Elisabetta Canali, Julian Ashley Drewe, Bruno Garin-Bastuji, Jose Luis Gonzales Rojas,

Christian Gortazar, Mette Herskin, Virginie Michel, Miguel Angel Miranda Chueca,

Barbara Padalino, Paolo Pasquali, Helen Clare Roberts, Hans Spoolder, Antonio Velarde,

Arvo Viltrop, Christoph Winckler, Cornelia Adlhoch, Inmaculada Aznar, Francesca Baldinelli,

Anette Boklund, Alessandro Broglia, Nora Gerhards, Lina Mur, Priyanka Nannapaneni and

Karl St

ahl

Abstract

The epidemiological situation of SARS-CoV-2 in humans and animals is continually evolving. To date,

animal species known to transmit SARS-CoV-2 are American mink, raccoon dog, cat, ferret, hamster,

house mouse, Egyptian fruit bat, deer mouse and white-tailed deer. Among farmed animals, American

mink have the highest likelihood to become infected from humans or animals and further transmit

SARS-CoV-2. In the EU, 44 outbreaks were reported in 2021 in mink farms in seven MSs, while only six

in 2022 in two MSs, thus representing a decreasing trend. The introduction of SARS-CoV-2 into mink

farms is usually via infected humans; this can be controlled by systematically testing people entering

farms and adequate biosecurity. The current most appropriate monitoring approach for mink is the

outbreak conﬁrmation based on suspicion, testing dead or clinically sick animals in case of increased

mortality or positive farm personnel and the genomic surveillance of virus variants. The genomic

analysis of SARS-CoV-2 showed mink-speciﬁc clusters with a potential to spill back into the human

population. Among companion animals, cats, ferrets and hamsters are those at highest risk of SARS-

CoV-2 infection, which most likely originates from an infected human, and which has no or very low

impact on virus circulation in the human population. Among wild animals (including zoo animals),

mostly carnivores, great apes and white-tailed deer have been reported to be naturally infected by

SARS-CoV-2. In the EU, no cases of infected wildlife have been reported so far. Proper disposal of

human waste is advised to reduce the risks of spill-over of SARS-CoV-2 to wildlife. Furthermore,

contact with wildlife, especially if sick or dead, should be minimised. No speciﬁc monitoring for wildlife

is recommended apart from testing hunter-harvested animals with clinical signs or found-dead. Bats

should be monitored as a natural host of many coronaviruses.

2023 European Food Safety Authority.

EFSA Journal

published by Wiley-VCH GmbH on behalf of

European Food Safety Authority.

Keywords:

SARS-CoV-2, mink, wildlife, public health, monitoring, prevention, control

Requestor:

European Commission

Question number:

EFSA-Q-2022-00139

Correspondence:

[email protected]

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EFSA Journal 2023;21(2):7822

MOF, Alm.del - 2022-23 (2. samling) - Bilag 251: Orientering om opdaterede vurderinger om COVID-19 og mink

SARS-CoV-2 in animals

Panel members:

Saxmose Nielsen, Julio Alvarez, Dominique Joseph Bicout, Paolo Calistri, Elisabetta

Canali, Julian Ashley Drewe, Bruno Garin-Bastuji, Jose Luis Gonzales Rojas, Christian Gortazar, Mette

Herskin, Virginie Michel, Miguel Angel Miranda Chueca, Barbara Padalino, Paolo Pasquali, Helen Clare

Roberts, Hans Spoolder, Karl St

Antonio Velarde, Arvo Viltrop and Christoph Winckler.

ahl,

Declarations of interest:

If you wish to access the declaration of interests of any expert

contributing to an EFSA scientiﬁc assessment, please contact

[email protected].

Acknowledgements:

The Panel on Animal Health and Welfare of EFSA wishes to thank the following

for the support provided to this scientiﬁc output:

•

Verena Oswaldi, Anna Karagiannis, Marzia Gnocchi, trainees at BIOHAW Unit of EFSA; Erik Alm,

Maja Vukovikj, Diamantis Plachouras, Kate Olsson (European Center for Disease Prevention and

Control, ECDC); Member State representatives who provided data about SARS-CoV-2 outbreaks and

€

monitoring: Finland: Riikka-Elina Lahdenpera, Terhi Laaksonen and Ari Kauppinen (Finnish Food

Authority); Greece: Sokratis Perdikaris (Ministry of Rural Development and Food); Italy: Andrea

Maroni Ponti, Luigi Ruocco (General Directorate of animal health, Ministry of Health); Latvia: Edvins

Olsevskis (Food and Veterinary Service); Lithuania:- Marius Masiulis, Paulius Bu

auskas and Vilija

Grigaliuniene (Emergency Response Division, State Food and Veterinary Service); Poland: Agnieszka

Warda and Anna Hoffman (General Veterinary Inspectorate) and Katarzyna Domanska-Blicharz

(National Veterinary Research Institute); Spain: Luis Jose Romero Gonzalez, German Caceres

Garrido, Sergio Bonilla Garc

(Ministry of Agriculture, Fisheries and Food); Sweden: Emelie

ıa

Pettersson and Siamak Zohari (National Veterinary Institute, SVA). Noemi Garcia del Blanco, Ewa

Shaw, Alberto Contreras Fuentetaja, Jordi Torren (EMA, European Medicine Agency, Amsterdam);

One Health European Joint Programme, project COVRIN. European Union’s Horizon 2020 Research

and Innovation programme, grant agreement No 773830; Joanna Korpela and Jussi Peura from

FiFur

–

Fur Farming in Finland.

Suggested citation:

EFSA AHAW Panel (EFSA Panel on Animal Health and Animal Welfare), Nielsen

SS, Alvarez J, Bicout DJ, Calistri P, Canali E, Drewe JA, Garin-Bastuji B, Gonzales Rojas JL, Gortazar C,

Herskin M, Michel M, Miranda Chueca MA, Padalino B, Pasquali P, Roberts HC, Spoolder H, Velarde A,

Viltrop A, Winckler C, Adlhoch C, Aznar I, Baldinelli F, Boklund A, Broglia A, Gerhards N, Mur L,

Nannapaneni P and St

K, 2023. SARS-CoV-2 in animals: susceptibility of animal species, risk for

ahl

animal and public health, monitoring, prevention and control. EFSA Journal 2023;21(2):7822, 108 pp.

https://doi.org/10.2903/j.efsa.2023.7822

ISSN:

1831-4732

2023 European Food Safety Authority.

EFSA Journal

published by Wiley-VCH GmbH on behalf of

European Food Safety Authority.

This is an open access article under the terms of the

Creative Commons Attribution-NoDerivs

License,

which permits use and distribution in any medium, provided the original work is properly cited and no

modiﬁcations or adaptations are made.

EFSA may include images or other content for which it does not hold copyright. In such cases, EFSA

indicates the copyright holder and users should seek permission to reproduce the content from the

original source.

The EFSA Journal is a publication of the European Food Safety

Authority, a European agency funded by the European Union.

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EFSA Journal 2023;21(2):7822

MOF, Alm.del - 2022-23 (2. samling) - Bilag 251: Orientering om opdaterede vurderinger om COVID-19 og mink

SARS-CoV-2 in animals

Summary

Since the entry into force of the Commission Implementing Decision (EU) 2021/788 laying down

the monitoring measures in the EU for mink, other animals of the family

Mustelidae

and raccoon dog,

the epidemiological situation and scientiﬁc knowledge of COVID-19 in the EU has evolved and

improved both in humans and animals. Therefore, the risks for animals and humans need to be

reassessed based on new scientiﬁc

ﬁndings

and on the availability of control measures. In this opinion,

EFSA was asked to review the scientiﬁc literature related to animal species susceptible to SARS-CoV-2

infection that play a role in its epidemiology. An assessment of the current epidemiological situation

and of the risk for human and animal health posed by SARS-CoV-2 infection in animal species of

concern was also conducted, which should serve to recommend options for reviewing the monitoring

strategies for SARS-CoV-2 infection in animal species of concern. Finally, the main possible options for

the prevention and control of COVID-19 in both humans and susceptible animals were explored,

highlighting their strengths and drawbacks.

The criterion used to classify the animal species of concern for SARS-CoV-2 epidemiology was the

ability to shed infectious virus and to transmit SARS-CoV-2 to other individuals. The species assessed

were American mink (Neogale

vison),

raccoon dog (Nyctereutes

procyonoides),

cat (Felis

catus),

Syrian

hamster (Mesocricetus

auratus),

ferret (Mustela

furo),

house mouse (Mus

musculus,

for some virus

variants only), Egyptian fruit bat (Rousettus

aegyptiacus),

deer mouse species (Peromyscus

spp.,

not

present in Europe) and white-tailed deer (Odocoileus

virginianus).

Since SARS-CoV-2 variants continue

to arise, new animal species fulﬁlling the above-mentioned criterion may be detected over time with

the continuous potential emergence of new host species.

Since the current assessment covers a range of points that deserve speciﬁc considerations in

different contexts

–

i.e. susceptibility to the virus, risk for animal and public health, monitoring

approach and preventive and control measures

–

the animal species considered were grouped

according to the categories reﬂecting those contexts: farmed animals, companion animals, wildlife

(referring to free-ranging wildlife, thus excluding for example captive wild animals such as in zoo), and

animals kept in zoos (from now on referred to as zoo animals).

Among farmed animals, American mink farmed for fur production have the highest likelihood to

become infected from humans or animals and transmit SARS-CoV-2 within animal populations and to

in-contact humans. This is due to both the inherent susceptibility to SARS-CoV-2 infection of this

species and the characteristics of the mink farming system, with a high density of animals kept in

contiguous cages. During the still ongoing COVID-19 pandemic, a vast majority of the reported

outbreaks of SARS-CoV-2 in animals globally were from farmed mink. In the period, the present

document refers to (February 2021 to November 2022), 50 outbreaks of SARS-CoV-2 were reported,

of those 44 were reported in 2021 in seven MSs, while only six were reported in 2022 in two MSs, thus

representing a decreasing trend. The genomic analysis of SARS-CoV-2 sequences showed major mink-

speciﬁc clusters, high rates of virus evolution within the mink population and emergence of mink-

speciﬁc variants with a potential to spill back into the human population.

The introduction of SARS-CoV-2 into mink farms is usually from infected humans; thus, this

probability is associated with the SARS-CoV-2 level of circulation in the surrounding human population.

Continuous and proper implementation of biosecurity measures in mink farms including the use of

non-pharmaceutical interventions (NPI) for all humans accessing mink farms can reduce the probability

of introduction. Once introduced into a mink farm, SARS-CoV-2 spreads efﬁciently within the animal

population, resulting in extensive virus circulation and risk of spill-over to humans in contact with the

mink, as well as to other susceptible animals with access to mink and their local environment.

The public health impact of the possible spill-over of SARS-CoV-2 from mink farms to humans

depends on the respective virus variant, effectiveness of the vaccine for this variant in vaccinated

people including the time period after the vaccination, previous exposure to other SARS-CoV-2 variants

and health status of the individual person. While the risk, determined by the probability of infection

and the impact of the disease, for an occupationally exposed person to a SARS-CoV-2 infected mink

has been assessed as low to moderate, in persons without or with limited exposure to farmed mink is

estimated to be negligible to very low.

Concerning the monitoring of SARS-CoV-2 in mink farms, given the current epidemiological situation

in the EU, where a substantial decrease of outbreaks in mink farms was reported in 2022 compared to

2020 and 2021, and where the majority of the human population has acquired some level of immunity

to SARS-CoV-2, the most appropriate monitoring approach on animals would be the one based on

testing dead animals with a suspicion of SARS-CoV-2 infection or animals showing clinical signs

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SARS-CoV-2 in animals

compatible with SARS-CoV-2 infection, with sampling triggered by increased mortality (compared to

the baseline mortality rate) or morbidity in mink, or farm personnel testing positive. In fact, the

primary purposes of monitoring of mink farms are to conﬁrm outbreaks based on suspicion in order to

apply preventive measures. In addition, genomic surveillance of circulating variants in mink and other

species is also considered relevant to monitor virus evolution.

Regarding prevention and control of SARS-CoV-2 introduction into mink farms, since the most

important source of introduction of SARS-CoV-2 into mink farms is via infected humans, systematic

and frequent testing of people entering mink farms for SARS-CoV-2 infection using rapid antigen test

and/or PCR is a prerequisite for the early detection of infected humans that may come into contact

with mink. Also, the ban of non-essential visits to farms and the use of personal protective equipment

will reduce the exposure of animals to potentially infected people and reduce the probability of

introduction of the virus. Biosecurity measures such as cleaning, disinfection, pest control (e.g.

rodents) and restricted access to other animals on the farm (such as cats, dogs, bats, etc.) can also

reduce the risk of virus introduction into the farm, and its further spread within and from the farm.

The risk of further virus spread and secondary outbreaks to other farms can be reduced by restriction

of mink movement and/or by testing for SARS CoV-2 in mink prior to movement, especially in mink

farms located in areas with known infected farms. Vaccines against COVID-19 are protective against

severe disease, hospitalisation and death, however, do not fully prevent virus transmission to and from

humans as well as between humans and mink. In general, preventive and control measures applied to

reduce the risk of transmission between mink and humans will only be effective if implemented

consistently.

Among companion animal species, cats, ferrets and several hamster species are those most at risk

of SARS-CoV-2 infection, which most likely originates from an infected human; in such situations, there

is a very low risk of spillback infection to humans, and little or no animal-to-animal transmission, as

indicated by genomic analysis. Categories of people with high contact rates to companion animals from

different households (e.g. veterinarians) may have a higher risk of infection from companion animals.

Under

ﬁeld

conditions, cats and hamsters have been associated with mild to moderate respiratory,

gastrointestinal or systemic signs of disease and they can shed virus. In general, SARS-CoV-2

transmitted by companion animals to humans are considered to have no or very low probability of

having impact on virus circulation in the general population, and there is a low frequency of species-

adapted mutations.

Therefore, there is no need for speciﬁc monitoring programmes of SARS-CoV-2 infection in

companion animals; some testing activity can be generally limited to owners, zoo workers or

veterinarians in contact with these animals. In case of clinical signs compatible with SARS-CoV-2

disease, animal testing may be important for possible quarantine measures or application of proper

therapies. Moreover, testing of individuals in stray communities (especially cats) could be justiﬁed,

apart from research objectives, in case of suspected SARS-CoV-2 clinical cases or abnormal mortality

rates in these communities.

The number of wildlife species that are globally reported to be naturally infected by SARS-CoV-2

grows steadily, also due to the active research in this

ﬁeld,

which should be promoted. These include

several wild carnivores and the white-tailed deer in North America. Only the latter has been

demonstrated, both free living or captive in game reserves, to maintain and possibly spill back the

virus to humans. Nevertheless, in the EU, no cases of infected wildlife (with viral or RNA isolation)

have been reported so far.

The situation of white-tailed deer in the EU is very different from that in North America: The

abundance of this deer species in the EU is very limited (less than 1% of the total deer population)

and it is present only in two countries (Czechia and Finland); thus, it is unknown whether these

animals may be able to support the persistence of SARS-CoV-2 infection in the European context.

Moreover, white-tailed deer are also kept farmed in some places in North America, which may increase

the risk of transmission to and from any susceptible species, but this practice is not seen in the EU.

Therefore, the risk of transmission of SARS CoV-2 infection from humans to white-tailed deer and

backward, causing a severe disease, is considered very low.

Regarding wild carnivores, due to their elusive and solitary behaviour, to their low density and to

the low numbers hunted, there is a very low probability for these species of maintaining the infection

or representing a risk for other animal species or for public health. The latter is also due to limited

human exposure, even for occupationally exposed people (rangers, hunters, researchers, etc.).

In any case, as a preventive measure, humans dealing with wildlife should follow biosecurity

measures to minimise direct contact with wild animals, especially sick and dead animals. Furthermore,

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SARS-CoV-2 in animals

safe disposal of garbage and waste from human communities in both urban and rural settings is

advised to reduce the risks of SARS-CoV-2 spillover to wildlife.

The probability of transmission from bats to humans or the emergence of SARS-CoV-2-related or

new coronaviruses has been assessed as none to very low, since transmission of SARS-CoV-2 or other

coronaviruses from bats to humans and backwards has not been observed and there is a limited

human population having direct contact with these animals in Europe. However, since bats are a

natural host of many coronaviruses, the monitoring of these species remains important.

As a result of the above-mentioned arguments, for wild species that may be considered as possible

targets for SARS-CoV-2 monitoring (such as white-tailed deer, wild carnivores, bats, rodents such as

wild synanthropic mice and rats), no speciﬁc regulated monitoring activities would be needed, apart

from testing of hunter-harvested animals showing clinical signs or dead-found individuals and

sequencing the virus isolates to monitor its evolution.

Regarding animal species kept in zoos, there are reports of both experimental and natural infection

with SARS CoV-2, mainly felids and non-human great apes. In zoos, susceptible species can acquire

the infection mainly from in-contact infected zoo workers; however, this is still at very low risk and

there is no report of spillback transmission from animals to humans. Transmission between susceptible

animals in the same enclosure could occur at moderate probability once an animal is infected,

although transmission between animals kept in zoos is difﬁcult to prove, because they are usually

exposed to the same infectious source (e.g. infectious caretaker). Overall, animals kept in zoos do not

represent a major public health risk in relation to SARS-CoV-2, the risk being considered very low for

occupationally or activity-related exposed people and negligible to very low for the general population.

No speciﬁc regulated monitoring activities on animals are needed in this animal category, apart

from suspicion-based testing and isolation of animals with clinical signs or testing in the frame of other

veterinary checks. The main prevention is based on regular testing of zoo workers, self-isolation when

positive, use of PPE and good hygiene practice (e.g. avoiding close contact, tool disinfection, etc.) is

expected to signiﬁcantly reduce the risk of transmission from humans to animals.

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SARS-CoV-2 in animals

Table of contents

Abstract......................................................................................................................................................

Summary....................................................................................................................................................

Introduction.................................................................................................................................

1.1.

Background and terms of reference as provided by the EC

..............................................................

1.2.

Interpretation of the terms of reference.........................................................................................

Data and methodologies

...............................................................................................................

Assessment..................................................................................................................................

3.1.

Animal species susceptible to SARS-CoV-2 under experimental conditions.........................................

3.1.1.

Companion animals (cat, dog, ferret, rabbit, mice and several hamster species)

...............................

3.1.2.

Farmed animals............................................................................................................................

3.1.3.

Zoo and wild animals....................................................................................................................

3.1.4.

Time to detection of infection following experimental infection

........................................................

3.2.

Animal species detected infected with SARS CoV-2 under

ﬁeld

conditions

.........................................

3.2.1.

Farmed animals detected infected with SARS CoV-2 under

ﬁeld

conditions

.......................................

3.2.1.1.

Fur animals

..................................................................................................................................

3.2.1.1.1.

Finland

........................................................................................................................................

3.2.1.1.2.

France

.........................................................................................................................................

3.2.1.1.3.

Greece.........................................................................................................................................

3.2.1.1.4.

Italy

............................................................................................................................................

3.2.1.1.5.

Latvia

..........................................................................................................................................

3.2.1.1.6.

Lithuania......................................................................................................................................

3.2.1.1.7.

Poland

.........................................................................................................................................

3.2.1.1.8.

Spain...........................................................................................................................................

3.2.1.1.9.

Sweden

.......................................................................................................................................

3.2.1.2.

Natural infection in other livestock species

......................................................................................

3.2.2.

Companion animals detected as infected with SARS-CoV-2 under

ﬁeld

conditions..............................

3.2.2.1.

Cat

..............................................................................................................................................

3.2.2.2.

Dog

.............................................................................................................................................

3.2.2.3.

Hamster

.......................................................................................................................................

3.2.3.

Wild animals detected as infected with SARS CoV-2 under

ﬁeld

conditions........................................

3.2.4.

Zoo animals detected as infected with SARS-CoV-2 under

ﬁeld

conditions.........................................

3.3.

Sequence data of animal species infected with SARS-CoV-2.............................................................

3.3.1.

Sequence data of farmed animals infected with SARS CoV-2 (mink)

.................................................

3.3.2.

Sequence data of companion animals infected with SARS CoV-2

......................................................

3.3.3.

Sequence data of wild animals infected with SARS CoV-2

................................................................

3.4.

Probability of transmission between animals, and between animals and humans, posed by SARS-

CoV-2 infection in animal species of concern

..................................................................................

3.4.1.

Farmed animals............................................................................................................................

3.4.2.

Companion animals

......................................................................................................................

3.4.3.

Wild animals

................................................................................................................................

3.4.4.

Zoo animals

.................................................................................................................................

3.5.

Risk for human health posed by SARS-CoV-2 infection in animal species and preventive measures

.....

3.5.1.

Overview of variant viruses in humans by cases over time...............................................................

3.5.2.

Measures to prevent and control infection or spread of SARS-CoV-2 at the animal–human interface:

monitoring

...................................................................................................................................

3.5.2.1.

SARS-CoV-2 surveillance in people

.................................................................................................

3.5.2.2.

Genomic surveillance.....................................................................................................................

3.5.2.3.

Wastewater surveillance

................................................................................................................

3.5.2.4.

Testing.........................................................................................................................................

3.5.2.5.

Hygiene measure

..........................................................................................................................

3.5.2.6.

Keeping distance

..........................................................................................................................

3.5.2.7.

Personal protective equipment (PPE)

..............................................................................................

3.5.2.8.

Face masks

..................................................................................................................................

3.5.2.9.

Ventilation

....................................................................................................................................

3.5.2.10.

Stay-at-home/isolation.................................................................................................................

3.5.3.

Measures to prevent and control infection or spread of SARS-CoV-2 at the animal–human interface

–

vaccination of humans as protective and control measure

...............................................................

3.5.4.

Treatment and pharmaceutical prophylaxis of COVID-19

.................................................................

3.5.5.

Risk assessment

...........................................................................................................................

3.6.

Revision of monitoring strategies

...................................................................................................

3.6.1.

Current legislative requirements of monitoring SARS-CoV-2 in mustelids and raccoon dogs

................

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SARS-CoV-2 in animals

3.6.2.

Animal categories and monitoring approach

...................................................................................

3.6.2.1.

Farmed animals

............................................................................................................................

3.6.2.2.

Companion animals.......................................................................................................................

3.6.2.3.

Wild animals.................................................................................................................................

3.6.2.4.

Zoo animals..................................................................................................................................

3.6.3.

New development in diagnostics/sample matrices for SARS-CoV-2 in animals....................................

3.7.

Options for disease prevention and control measures......................................................................

3.7.1.

Farmed animals............................................................................................................................

3.7.1.1.

Farm personnel and visitors

...........................................................................................................

3.7.1.1.1.

Health self-assessment (‘stay-at-home/isolation’).............................................................................

3.7.1.1.2.

Systematic testing of personnel/visitors at predetermined frequency.................................................

3.7.1.1.3.

Temperature screening..................................................................................................................

3.7.1.1.4.

Use of personal protective equipment (PPE) for farm personnel and visitors

......................................

3.7.1.1.5.

Vaccination of personnel................................................................................................................

3.7.1.2.

General on-farm biosecurity measures

............................................................................................

3.7.1.2.1.

Restricted access for animals and visitors to farm, including tracing of visitors...................................

3.7.1.2.2.

Changing work clothes for farm personnel

......................................................................................

3.7.1.2.3.

Cleaning and disinfection equipment/vehicles..................................................................................

3.7.1.2.4.

Rodent control..............................................................................................................................

3.7.1.3.

Animal movement control, including pre-movement testing and tracing.............................................

3.7.1.4.

Awareness raising

.........................................................................................................................

3.7.1.5.

Culling and disposal of animal in an infected farm

...........................................................................

3.7.1.6.

Zoning around infected farms

........................................................................................................

3.7.1.7.

Vaccination of animals

...................................................................................................................

3.7.2.

Options for public health response.................................................................................................

Conclusions and recommendations

................................................................................................

References..................................................................................................................................................

Abbreviations

..............................................................................................................................................

Annexes

.....................................................................................................................................................

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SARS-CoV-2 in animals

1.1.

Introduction

Background and terms of reference as provided by the EC

The scientiﬁc report of January 2021 produced by EFSA, in collaboration with ECDC, on

‘Monitoring

of SARS-CoV-2 infection in mustelids’ (EFSA, 2021), along with the rapid risk assessment of November

2020 by ECDC have been the basis for the current monitoring measures in the EU for mink, other

animals of the family

Mustelidae

and raccoon dogs as provided by Commission Implementing Decision

(EU) 2021/788

The epidemiological situation has evolved in the EU since the adoption of these measures in May

2021 along with the scientiﬁc knowledge on the spread of SARS-CoV-2 in both humans and animals

and what role individual epidemiological units play for the disease spread. This includes availability of

new measures such as vaccination (for both animals and humans), reﬁned diagnostic techniques,

better understanding of biosecurity requirements and the risks related to genetic mutations of SARS-

CoV-2. The risks for humans need to be reassessed based on new scientiﬁc

ﬁndings

and on the

availability of control measures.

SARS-CoV-2 infections in mink have been reported by Member States to the Commission in line

with the monitoring requirements. Further data has been collected by the OIE via the notiﬁcation by

its Member Countries.

The adequacy of the current monitoring system in the EU should be reviewed in light of the above

to ensure proportionate measures are put in place to address the signiﬁcant risks which could exist.

Terms of Reference

There is a need to revise and update the measures put in place by Member States to face the

challenges posed by the epidemiological situation of SARS-CoV-2 in mink, other animals of the family

Mustelidae

and raccoon dogs.

The coordinated monitoring provided by Implementing Decision (EU) 2021/788 may need to be

reviewed in view of the control measures available in response to the different epidemiological

scenarios and possible evolution of the disease agent.

In view of the above, and in accordance with Article 29 of Regulation (EC) No 178/2002, the

Commission asks EFSA for scientiﬁc opinion about:

•

1.2.

Reviewing updated relevant scientiﬁc literature available globally related to SARS-CoV-2

infection in animal species of concern in the epidemiology of SARS-CoV2.

Assess the current epidemiological situation in the EU and elsewhere as regards the risk for

human and animal health posed by SARS-CoV-2 infection in animal species of concern with a

view to review the design of the existing monitoring performed by the Member States for

minks, other animals of the family

Mustelidae

and raccoon dogs.

In different epidemiological scenarios, recommend options for reviewing the monitoring

strategies indicating possible objectives and suitable methodologies, in particular as regards

scope, sampling, frequencies and testing methods taking into account existing risk mitigating

measures.

Explore the main possible options for disease prevention and control measures suitable to

address the risks under different plausible scenarios indicating the strengths and drawbacks of

each set of measures.

Interpretation of the terms of reference

Regarding term of reference (ToR) 1, i.e. reviewing scientiﬁc literature related to SARS-CoV-2

infection in animal species of concern in the epidemiology of SARS-CoV2, an extensive literature review

has been conducted, focusing on susceptibility of wild and domestic animal species reported under

ﬁeld

and laboratory conditions, considering different diagnostic tests (e.g. virus isolation, RNA and

antibody detection), infection dynamic, pathogenesis, immunity and further transmission of the virus.

The results are presented in Sections 5.1 and 5.2, where the animal species are grouped in the

following categories: (1) farmed animals, (2) companion animals, (3) wildlife (including feral animals)

and (4) animals kept in zoos (from now one referred as

‘zoo

animals’). The phylogenetic analysis of

Commission Implementing Decision (EU) 2021/788 of 12 May 2021 laying down rules for the monitoring and reporting of

infections with SARS-CoV-2 in certain animal species (OJ L 173, 17.5.2021, p. 6).

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sequence data from animal isolates deposited in GISAID until October 2022 is reported in Section 5.3,

and this has been conducted by ECDC. Given the high rate and continuous publication of studies about

potential new susceptible species along 2022, the evidence collected by the literature review has been

complemented by that from new studies indicated by the experts of the established EFSA ad-hoc

working group, up to November 2022.

Concerning ToR 2, an updated epidemiological situation in the above-mentioned animal categories

is presented in Section

3.4.

In particular, for fur farmed animals, mostly mink, the situation of reported

outbreaks and related monitoring in MSs where mink are still bred is discussed. The risk for human

and animal health posed by SARS-CoV-2 infection in animal species, which is also a part of ToR2, is

addressed in Section

3.4,

where, for the animal species considered as susceptible and relevant in the

epidemiology of SARS-CoV-2, the probability of transmission in different pathways between animals

and between animals and humans is assessed. A dedicated section about public health aspects is

Section

3.5,

which has been drafted by ECDC. Here, besides an overview of the virus variants

circulating in the human population, the measures to prevent and control infection or spread of SARS-

CoV-2 at the animal–human interface are discussed as well as the risk assessment for public health

represented by animals infected by SARS-CoV-2.

The options for reviewing the monitoring strategies for SARS Cov-2 (ToR 3) are discussed in

Section

3.6.

Here, keeping the current legislative requirements of the EC Decision 2021/788 as a

reference, the monitoring approaches for SARS-CoV-2 in the different categories of animals and in

different scenarios are discussed. An update about diagnostic tools that could be used for monitoring

purposes, compared to what was already assessed in a previous EFSA report (EFSA, 2021), is

reported.

The main disease prevention and control measures in humans and in the different animal

categories are discussed in Sections

3.5

and

3.7,

respectively, based on information provided by MSs

and based on expert knowledge (ToR 4). The measures include, among others, biosecurity, movement

controls, vaccination and non-pharmaceutical interventions; the strengths and drawbacks of each of

those are discussed.

Further details about problem formulation are provided in Annex

A.1.

Data and methodologies

A systematic literature review was performed by an external contractor with stringent inclusion

criteria (literature search protocol available at this link:

https://doi.org/10.5281/zenodo.7559990)

retrieve a list of wild and domestic mammals that are susceptible to SARS-CoV-2 under laboratory

conditions. Due to the stringent inclusion criteria and to the constantly and rapidly evolving results

from the research about SARS-CoV-2 in animals, the presented lists are not exhaustive, and therefore,

only publications published between 1 January 2020 and 15 February 2022 were included. Therefore,

in order to provide the most up-to-date information, additional publications on various animal species

issued up to December 2022 were added by the expert panel, to ensure that all relevant animal

species were listed. Literature protocol and data extraction tables are available at this link:

https://doi.

org/10.5281/zenodo.7559990.

Data about the current epidemiological situation in the EU were retrieved from the literature as well

as from outbreak reports submitted by MSs to the European Commission, from the World Organisation

for Animal Health (WOAH) database

and from ProMedmail

notiﬁcations and they were analysed and

presented by descriptive epidemiology.

The probability of transmission of SARS-CoV-2 from the different animal categories considered in

the present opinion (i.e. farmed animals, companion animals, wildlife, zoo animals) to humans or other

animals and vice versa and scenarios were assessed by consensus agreement among experts. In order

to make a proper assessment of the likelihood of an event, it is necessary to come up with a well-

deﬁned question or quantity of interest (QoI), such that the true answer or value could be determined,

at least in principle. By doing so, ambiguities that could contribute to uncertainty are minimised. In

addition, it helps to ensure that the range of probabilities provided in the assessment are reﬂecting

only uncertainty and not also variability (that could be interpreted differently by the different experts if

not made explicit). This assessment does not imply making

‘additional

judgements’ (for which

insufﬁcient knowledge exists), but rather to translate the judgements already done into transparent

https://www.woah.org/en/what-we-offer/emergency-preparedness/covid-19/

https://promedmail.org/

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and clear statements that can be unambiguously understood by the readers (and risk managers). With

this approach, once a range of probabilities is agreed, uncertainty becomes evident as will be reﬂected

by the width of the interval (EFSA, 2014). Proposed probability ranges used alone or in combination

were:

•

Very high:

90%

High: 66–90%

Moderate: 33–< 66%

Low: 10–< 33%

Very low

10%

The risk assessment for human health posed by SARS-CoV-2 infection in animals is based on

evidence available to ECDC at the time of publication. It follows the ECDC rapid risk assessment

methodology, where the overall risk is determined by a combination of the probability of infection

(taking into consideration the assessment of the probability of transmission of SARS-CoV-2 for the

different animal categories, as explained above) and the level of impact of the disease on the affected

individuals or general population and it is assessed on a qualitative scale as in ECDC (2019), as

displayed below in Figure

Figure 1:

Risk ranking matrix as in ECDC (2019)

The revision of monitoring approaches and the assessment on strengths and drawbacks of

preventive and control measures were done based on data retrieved from MSs and literature and

addressed based on expert knowledge.

3.1.

Assessment

Animal species susceptible to SARS-CoV-2 under experimental

conditions

Susceptibility to SARS-CoV-2 infection can be determined by detection of indicators of productive

infection such as isolation of infectious virus or viral RNA from host’s secretions/excretions (ante-

mortem) or organs (post-mortem) and/or seroconversion. Based on these indicators, animal species

that were described in the literature (see literature protocol and data extraction at this link

https://doi.

org/10.5281/zenodo.7559990)

as susceptible to SARS-CoV-2 experimental infection (see also Table

A.1

in Annex

A.2)

were grouped in three categories: (1) companion animals, (2) farmed animals, (3)

wildlife and (4) zoo animals (Figure

2).

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Detection of viral RNA refers to either detection in at least two consecutive ante-mortem respiratory samples, or

any post-mortem sample. A black cross indicates the absence of a feature, while a red check mark indicates the

presence of a feature. Both signs mean disagreement among studies considered;

‘nd’

means that this feature was

not determined. Please note that for some species for which extensive literature is available (e.g. ferrets and Syrian

hamsters), only a selection of a few representative references were included.

Figure 2:

Animal species that are susceptible to SARS-CoV-2 infection under experimental conditions

based on seroconversion and/or detection of viral RNA and ability of further transmit SARS-

CoV-2 virus (as of literature search carried out on 15 February 2022)

3.1.1.

Companion animals (cat, dog, ferret, rabbit, mice and several hamster

species)

Chinese, Djungarian, Roborovski and Syrian hamsters displayed clinical signs post infection, while

Campbell’s dwarf hamsters remained without clinical signs (Chan et al., 2020; Imai et al., 2020; Sia

et al., 2020; Trimpert et al., 2020; Bertzbach et al., 2021; Gerhards et al., 2021). In cats and ferrets,

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both the presence and absence of clinical signs were reported (such as fever, diarrhoea, sneezing,

arching of back) (Bosco-Lauth et al., 2020; Gaudreault et al., 2020; Halfmann et al., 2020; Kim

et al., 2020; Richard et al., 2020; Schlottau et al., 2020; Shi et al., 2020; Bao et al., 2021; Chiba

et al., 2021; Gaudreault et al., 2021; Kutter et al., 2021; Marsh et al., 2021; Ryan et al., 2021;

Ciurkiewicz et al., 2022). No clinical signs were reported for other companion animals such as dogs

and rabbits (Bosco-Lauth et al., 2020; Shi et al., 2020; Montagutelli et al., 2021; Pan et al., 2021),

neither for laboratory animals such as mice (laboratory mouse strains C54BL/6 and BALB/c).

Nevertheless, animals usually recover from the experimental infection with the exception of Roborovski

hamsters, for which infection with SARS-CoV-2 is severe, requiring euthanasia.

Viral RNA was detected in all investigated companion animal species except in dogs, and virus

could be isolated from hamsters, cats, ferrets, rabbits and laboratory mice. Noteworthy, for laboratory

mice, this was only the case for B.1.1.7, B.1.351 and P.1 isolates.

Cats, dogs, ferrets, laboratory mice, rabbits and Syrian hamsters developed antibodies against

SARS-CoV-2. For ferrets, one report did not detect antibodies post infection while Campbell’s, Chinese,

Djungarian and Roborovski hamsters were not tested for the presence of antibodies.

Transmission of SARS-CoV-2 from a donor animal to a recipient by direct contact has been

demonstrated for cats, ferrets, laboratory mice and Syrian hamsters. There was no evidence of virus

transmission between dogs. Rabbits, Campbell’s dwarf, Chinese, Djungarian and Roborovski hamsters

were not investigated for virus transmission.

A large number of publications are available describing the susceptibility of ferrets and hamsters. In

another literature review, performed within the project COVRIN of the One Health European Joint

program (Grant agreement 773830), efﬁcient direct contact as well as indirect contact transmission

between ferrets and between hamsters was widely reported (de Vries et al., 2021; Dowall et al., 2021;

Kutter et al., 2021; Mok et al., 2021; Neary et al., 2021; Page et al., 2021; Patel et al., 2021; Peacock

et al., 2021; Cox et al., 2021a,b; Kim et al., 2022).

3.1.2.

Farmed animals

For cattle, mink and pigs, reports disagree concerning the presence of clinical signs post SARS-

CoV-2 infection (Schlottau et al., 2020; Shi et al., 2020; Meekins et al., 2020; Ulrich et al., 2020;

Buckley et al., 2021; Falkenberg et al., 2021; Pickering et al., 2021; Shuai et al., 2021; Sikkema et al.,

2022; Virtanen et al., 2022). One out of two references describe fever in cattle; one out of two

references describe anorexia, diarrhoea, lethargy and respiratory signs in mink; and fever and ocular

discharge was described for pigs in two independent references out of six in total. No clinical signs

were observed in raccoon dogs (Freuling et al., 2020).

Viral RNA was detected in ante-mortem and/or post-mortem samples of cattle, mink and raccoon

dogs, while for pigs, both detection as well as the absence of viral RNA post infection were reported.

Virus could be isolated from raccoon dogs and mink, while for pigs and cattle, virus isolation was not

undertaken.

Seroconversion was observed in racoon dogs, mink and cattle, while for pigs, antibodies were

detected only in three out of six references.

Transmission of SARS-CoV-2 was observed for mink and raccoon dogs, and no transmission was

observed for cattle and pigs.

Goats, sheep, alpacas and horses are not included in the

ﬁgure,

because the available publications

did not pass the inclusion criteria of the systematic literature review (time of publication and use of

animals to model human infections). No viral RNA could be detected in ante-mortem respiratory

samples from sheep, alpacas and horses and no virus could be isolated and no neutralising antibodies

could be detected on day 14 post infection. For goats, viral RNA could be detected in swabs from the

respiratory tract in some animals, but no virus could be isolated and no antibodies were detected post

infection (Bosco-Lauth et al., 2021b). In a study published in September 2022, SARS-CoV-2 was

detected in experimentally infected goats in nasal swabs and tissues by PCR, and seroneutralisation

was conﬁrmed via ELISA. However, the viral amount and tissue distribution suggest a low susceptibility

of goats, thus no relevant role of goats in the epidemiology of SARS-Cov-2 (Fernandez-Bastit et al.,

2022).

3.1.3.

Zoo and wild animals

In this category, we refer to African green monkey

(Chlorocebus

sabaeus),

bank vole (Myodes

glareolus),

bushy-tailed woodrat (Neotoma

cinerea),

Chinese tree shrew (Tupaia

belangeri chinensis),

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cynomolgus macaques (Macaca

fascicularis),

deer mouse (Peromyscus

maniculatus),

Egyptian fruit bat

(Rousettus

aegyptiacus),

raccoon (Procyon

lotor),

red fox (Vulpes

vulpes),

rhesus macaque (Macaca

mulatta),

skunk (Mephitis

mephitis)

and white-tailed deer (Odocoileus

virginianus).

Clinical signs were

observed in African green monkeys (fever and reduced appetite or hypothermia and respiratory

distress; (Blair et al., 2021; Woolsey et al., 2021)), cynomolgus macaques (nasal discharge; (Rockx

et al., 2020)) and white-tailed deer (fever or ocular discharge; (Palmer et al., 2021; Cool et al., 2022))

post experimental infection with SARS-CoV-2. Reports disagree regarding clinical signs in Chinese tree

shrews (fever in one out of two references (Xu et al., 2020; Zhao et al., 2020)) and rhesus macaques

(no signs in two references; fever, respiratory distress, weight loss, hunched posture and nasal

discharge or reduced appetite and weight loss in two out of four references (Munster et al., 2020;

Shan et al., 2020; Blair et al., 2021; Yadav et al., 2021)). No clinical signs were observed in bank voles

(Ulrich et al., 2021), bushy-tailed woodrats (Bosco-Lauth et al., 2021a), deer mice (Fagre et al., 2021;

Grifﬁn et al., 2021), Egyptian fruit bats (Schlottau et al., 2020), raccoons (Bosco-Lauth et al., 2021a;

Francisco et al., 2022) and skunks (Bosco-Lauth et al., 2021a; Francisco et al., 2022).

Viral RNA was detected and virus could be isolated in all investigated zoo and wild animal species,

except raccoons. For Chinese tree shrews, virus isolations were not performed.

Seroconversion was observed in all animals. One out of four references did not observe antibodies

in rhesus macaques post-infection, and antibodies were not assessed for Chinese tree shrews.

Transmission of SARS-CoV-2 was successfully demonstrated in deer mice, Egyptian fruit bats and

white-tailed deer. No transmission took place in bank voles, raccoons and skunks. For all other animal

species, transmission was not investigated.

Common marmosets (Callithrix

jacchus)

and hamadryas baboons (Papio

hamadryas)

are listed in

Figure

although the publications did not pass the inclusion criteria of the systematic literature

review. In both species, viral RNA was detected post-infection (Singh et al., 2021).

In a study published in September 2022, two red foxes (Vulpes

vulpes)

and coyotes (Canis

latrans)

were tested for susceptibility to SARS-CoV-2 at experimental inoculation. Only red foxes became

infected and shed infectious virus. The authors concluded that the role of red foxes in SARS CoV-2

transmission should be carefully evaluated, given the wide distribution of this species, its frequent

proximity to humans, and that it preys, scavenges upon or otherwise interacts with species

demonstrated to be susceptible to SARS-CoV-2, including felids, skunks, rodents and white-tailed deer

(Porter et al., 2022).

3.1.4.

Time to detection of infection following experimental infection

The period from inoculation until viral RNA detection varied between 1 and 3 days post-inoculation

for most species. Longer incubation periods were observed for animals infected by direct contact (up

to 8 days), for Chinese tree shrews (6–8 days), African green monkeys and rhesus macaques (up to

7 days).

Seroconversion took place within the following days post-inoculation: 3–11 (pigs), 5–11 (cats), 6–14

(deer mice), 7–12 (cattle), 7 (white-tailed deer), 7–14 (African green monkey), 7–17 (ferrets), 8 (bank

voles, bats, raccoon dogs), 8–28 (skunks), 9–28 (raccoons), 10–14 (rhesus macaques), 12–14 (mice),

7–16 (Syrian hamsters), 14 (dogs, cynomolgus macaques), 18 (mink), 21 (rabbits).

Noteworthy, the above-mentioned time from infection to seroconversion depends on the individual

study designs and sampling schemes, leaving the possibility that, e.g. antibodies would have been

detectable at earlier time points post-infection, if an earlier blood sample would have been taken.

Sequence or structure-based predictions of animal susceptibility due to homology of human ACE2

receptor and their agreement with

in vivo

data has been systematically assessed by Fischhoff et al.

(2021). Sequence-based predictions revealed a low afﬁnity of SARS-CoV-2 to mink and ferret ACE2, for

instance, while, in fact, these species were highly susceptible. The agreement between structure-based

predictions of species susceptibility and factual susceptibility is high, although not always accurate.

Furthermore, the following animal species were experimentally infected with SARS-CoV-2, but did

not seroconvert, and neither viral RNA nor infectious virus could be isolated post-infection: big brown

bats, black-tailed prairie dogs, cottontail rabbits, coyotes, fox squirrels and Wyoming ground squirrels.

These species are therefore considered not susceptible to SARS-CoV-2.

Red foxes are not reported in Figure

since the investigation was carried out after the date of literature review (until Feb

2022).

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3.2.

Animal species detected infected with SARS CoV-2 under

ﬁeld

conditions

In the present section, the information obtained by literature review,

from WOAH database and

from ProMEDmail about animal species that have been detected as positive for SARS-CoV-2 worldwide,

either as PCR positive or serologically positive, are presented. The animal species are grouped as

farmed animals, companion animals and zoo and wild animals.

Figures

and

show animal species that were found to be susceptible to SARS-CoV-2 under

ﬁeld

(natural) conditions, based on the literature review done on 15 February 2022. Moreover, in Annex

A.3

(Table

A.2),

the results obtained from literature review about

ﬁeld

infection of different animal species

to SARS CoV-2 are shown, as proportion of positive animals in each epidemiological unit, tested by

PCR/virus isolation or serological test.

Figure 3:

Companion and farm animal species that have been reported as being susceptible to SARS-

CoV-2 infection under

ﬁeld

conditions based on seroconversion and/or detection of viral

RNA and able to further transmit (based on the literature search carried out on 15 February

2022)

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Figure 4:

Zoo and wild animal species that are susceptible to SARS-CoV-2 infection under

ﬁeld

conditions based on seroconversion and/or detection of viral RNA (based on literature

search carried out on 15 February 2022)

Based on the extensive literature review, the following animal species were tested with PCR test

and/or serological test but results were negative (Table

1).

Table 1:

Animal species under

ﬁeld

conditions tested with PCR test and/or serological test with

negative results

PCR

neg

Davoust et al. (2022)

Cerino et al. (2021)

Reference

Serological

test

neg

Reference

Deng et al. (2020)

Davoust et al. (2022)

Deng et al. (2020)

Moreira-Soto (2022)

Species

Alpaca (Vicugna

pacos)

Bamboo rat (Rhizomys spp.)

Bear (Ursus spp.)

Beech marten (Martes

foina)

Buffalo (Bubalus

bubalis)

Camel (Camelus

dromedarius)

Deer (red deer, roe deer, fallow deer)

(Cervus

elaphus, Capreolus capreolus,

Dama dama)

Giant panda (Ailuropoda

melanoleuca)

neg

Deng et al. (2020)

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Species

Goat (Capra

hircus)

Guinea pig (Cavia

porcellus)

Horse (Equus

ferus caballus)

Leopard cat (Prionailurus

bengalensis)

Masked civet (Paguma

larvata)

Mouse (Mus

musculus)

Non-human primates of genera

Callithrix, Callicebus

and

Alouatta

spp.

Pig (Sus

scrofa domesticus)

Polecat (Mustela

putorius)

Porcupine (Hystrix spp.)

Raccoon (Procyon

lotor)

Rat (Rattus

rattus)

Red panda (Ailurus

fulgens)

Rhinoceros (Rhinoceros spp.)

Sheep (Ovis

aries)

PCR

neg

Reference

Cerino et al. (2021)

Ruiz-Arrondo et al.

(2021)

Cerino et al. (2021)

Serological

test

neg

Reference

Deng et al. (2020)

Ip et al. (2021)

Sacchetto et al.

(2021)

Cerino et al. (2021)

Davoust et al. (2022)

Ip et al. (2021)

neg

Deng et al. (2020)

Davoust et al. (2022)

Deng et al. (2020)

Colombo et al. (2021)

Deng et al. (2020)

Deng et al. (2020);

Villanueva-Saz et

al. (2021a)

Colombo et al. (2021) neg

neg

Cerino et al. (2021)

neg

Skunk (Mephitis

mephitis)

Tamarin (Saguinus spp.)

Weasel (Mustela

nivalis)

neg: tested negative; na: not available.

neg

Ip et al. (2021)

Sacchetto et al.

(2021)

neg

Deng et al. (2020)

3.2.1.

Farmed animals detected infected with SARS CoV-2 under

ﬁeld

conditions

To date, the only farmed animals that were tested positive following natural infection (detection of

SARS-CoV-2 RNA by PCR) are mink (Molenaar et al., 2020; Oreshkova et al., 2020; Domanska-Blicharz

et al., 2021; EFSA, 2021; Hammer et al., 2021; Rabalski et al., 2021; Rasmussen et al., 2021), raccoon

dogs (one outbreak reported in Poland in 2021), and to a certain extent also ferrets (Shi et al., 2020;

Giner et al., 2021; Gortazar et al., 2021; Ra

nik et al., 2021). The former two species are bred mainly

in the fur industry, while ferrets are bred mainly as companion, research or as work animals for rabbit

hunting and rabbit control. The size of ferret breeding centres may be between 10 and 100 ferrets per

facility.

In the following section, the epidemiological situation in farmed mink is reported in MSs where mink

farming is still practiced, also considering molecular epidemiology and monitoring scheme applied.

3.2.1.1. Fur animals

EU data

From the beginning of the pandemics up to 31 January 2021 (the reporting period which the

ﬁrst

EFSA report refers to (EFSA, 2021)), 401 outbreaks of SARS-CoV-2 in mink farms were reported in

Europe (Table

3),

mostly in Denmark (290) and the Netherlands (69), where around 60% of the total

mink farms in EU were until the end of 2020, then the mink farming was stopped in those two MSs.

From 1 February 2021 until 30 November 2022, period in which the number of mink farms was

approximately stable in EU (around 700 farms), 50 SARS-CoV-2 outbreaks were detected in farmed

mink and raccoon dogs in the EU, of those 44 were reported in 2021 in seven MSs, while only six were

reported in 2022 in two MSs (Figure

6).

In all the affected establishments, farmed mink were raised,

apart from one Polish farm where both raccoon dogs (300 animals) and mink (5,000 animals) were

raised (detection in December 2021).

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The geographical distribution of the affected mink establishments is presented in Figure

and the

monthly distribution of outbreaks is presented in Figure

Clinical signs of SARS-CoV-2 infections were

detected in 4 out of 50 affected mink establishments, and humans were identiﬁed as the possible

source of virus introduction in 12 mink establishments, whereas the source of the infection was not

identiﬁed in the other 38 SARS-CoV-2 outbreaks. No clinical signs of SARS-CoV-2 infections were

detected in the affected raccoon dog establishment and the source of the virus introduction was not

identiﬁed.

*: This designation is without prejudice to positions on status and is in line with United Nations Security Council

Resolution 1,244 and the International Court of Justice Opinion on the Kosovo Declaration of Independence.

Figure 5:

Geographical distribution of SARS-CoV-2 outbreaks in mink establishments (green circles)

and of mink establishments by country (grey areas) in Europe, from 1 February 2021 to 30

November 2022

Disclaimer: The designations employed and the presentation of material on this map do not imply the expression of any

opinion whatsoever on the part of the European Food Safety Authority concerning the legal status of any country, territory,

city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries.

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SARS-CoV-2 in animals

Source: EC, EFSA

The vertical grey line indicates when the Commission Implementing Decision (EU) 2021/788 of 12 May 2021 laying

down rules for the monitoring and reporting of infections with SARS-CoV-2 in certain animal species (OJ L 173,

17.5.2021, p. 6) entered into force.

Figure 6:

Distribution of SARS-CoV-2 reported outbreaks in mink establishments in the EU by month

of conﬁrmation and affected countries from February 2021 to November 2022

In Tables

and

data on number of mink farms in the MS, number of infected farms, with clinical

signs and where likely human source was conﬁrmed, in the two reporting periods (February 2021 until

November 2022, and 2020, until 31 January 2021, respectively) are reported.

Table 2:

Data on outbreaks of SARS-CoV-2 in mink farms in the EU from February 2021 to

November 2022

Number of Number of

mink farms infected

in the MS mink farms

in the

as of

reporting

January

period

2022

133

261

Date of

ﬁrst

and last SARS-

Cov-2 virus

detection in

mink farms in

the reporting

period

–

February 2021 to

August 2021

–

April 2021

November–

December 2021

June 2021–July

2022

Number of

outbreaks with

outbreaks

likely human

where clinical

source of virus

signs of

origin in the

SARS-CoV-2

reporting period

were

(if known)

observed

–

Unknown

Country

Start of

systematic

monitoring

Finland

Greece

Italy

Latvia

Lithuania

Poland

January 2021

November

2020

February 2021

January 2021

November

2021

December 2020

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SARS-CoV-2 in animals

Country

Number of Number of

mink farms infected

in the MS mink farms

in the

as of

reporting

January

period

2022

Date of

ﬁrst

and last SARS-

Cov-2 virus

detection in

mink farms in

the reporting

period

March–October

2021

August 2021

Start of

systematic

monitoring

Number of

outbreaks with

outbreaks

likely human

where clinical

source of virus

signs of

origin in the

SARS-CoV-2

reporting period

were

(if known)

observed

Spain

Sweden

May 2021

October 2020

Table 3:

Data on outbreaks of SARS-CoV-2 in mink farms in the EU in 2020 until January 2021

(EFSA, 2021)

Number of mink

Number of

farms in the

infected

country at the time

mink

of SARS-Cov-2 virus

farms

ﬁrst

detection

1,147

290

Number of

Date of

ﬁrst

and last SARS- farms where

Likely source of

clinical signs of

CoV-2 virus

virus origin

SARS-CoV-2

detection in

were observed

mink farms

15 June to 7

December

145

Human-to-animal

transmission suspected

or conﬁrmed in some

outbreaks. Unclear in

most outbreaks

Undetermined, but

most probably humans

on the farm

Human-to-animal

transmission suspected

in most outbreaks

Human-to-animal

transmission

Human-to-animal

transmission

Partly human to mink

transmission and partly

unclear, but with a

strong spatial

component

Unknown

Human-to-animal

transmission

suspected

Human-to-animal

transmission

Country

Denmark

France

20 November

Greece

13 November to

8 January

10 October

24 November

24 April to 4

November

Italy

Lithuania

Netherlands

126

Poland

Spain

272

27 January 2021

22 June to 22

January

23 October to 11

November

Sweden

No information

In the following section, we present the epidemiological situation and monitoring activities

(reporting period February 2021–March 2022) carried out in MSs where mink farming is still present.

3.2.1.1.1. Finland

Fur-farmed animals

In Finland, the farmed species targeted by SARS-CoV-2 monitoring were mink, raccoon dogs and

sable (Martes

zibellina).

Up to January 2022, 133 mink farms were registered, including a total of

190,500 breeding animals and around 500,000 production stocks as well as 50 farms with raccoon

dogs, including a total of 13,700 breeding animals, and one sable farm with 310 breeding animals.

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Epidemiological situation

Finland has not reported any outbreaks of SARS-CoV-2 in mink or other fur animal farms. A

voluntary preventive vaccination scheme in mink (implemented in November 2021) was in place on

January–February 2022 covering approximately 95% of breeding females. The vaccination campaign is

currently not active.

Monitoring scheme

In December 2020, monitoring of SARS-CoV-2 infection started in all fur farms (mink and other

animals of the family

Mustelidae),

and at the beginning of 2021, raccoon dog farms were included in

the monitoring, although the sampling scheme was not completely harmonised among farms. Since

June 2021, a harmonised active monitoring scheme foresees that all fur farms submit

ﬁve

dead

animals every 2 weeks for SARS-CoV-2 testing to the laboratory of the Finnish Food Authority. Throat

swab samples from dead animals are taken by laboratory staff and samples are analysed by RT-PCR. If

the number of dead animals is insufﬁcient to reach the threshold of

ﬁve

animals per 2 weeks, further

live animals are sampled by municipal veterinarians. So far, 14,165 samples from 229 farms have been

tested, all negative.

Furthermore, passive monitoring is carried out in all farms. Suspicion is triggered if farmed fur

animals show clinical signs, in which case 30 samples are taken from the animals of the farm, or if a

person tested positive at SARS-CoV-2 has been in contact with fur animals, in which case 60 samples

are taken from the animals of the farm. Until March 2022, a total of 568 samples from 11 farms were

tested, all negative.

Other species

Wild mustelids or wild raccoon dog: Those animals found dead or hunted animals with clinical signs

associated with SARS-CoV-2 are sampled for SARS-CoV-2 tests. From wild animals, mostly oral swabs

or organ samples are used and tested by PCR (E gene). In total, 278 raccoon dogs, three otters and

three badgers have been tested for SARS-CoV-2, all negative.

Wild white-tailed deer: In total, 36 samples from oral swab/lymph node have been tested by PCR

(E gene), all negative for SARS-CoV-2.

Companion animals: Six cats and three dogs have been sampled in case of a suspicion of SARS-

CoV-2 (e.g. a pet had SARS-CoV-2 signs and had been in contact with a person having COVID-19).

Oral swabs have been tested by PCR (E gene). One cat and one dog were found positive in 2021

(Delta variant) and 2022 (Omicron variant), respectively.

3.2.1.1.2. France

In France, there is currently only one mink farm left, where passive monitoring is carried out. No

outbreaks have been reported in the period from February 2021 to September 2022.

3.2.1.1.3. Greece

By 2022, in Greece, the only farmed species targeted by SARS-CoV-2 monitoring are mink. There

are 91 mink farms, 89 of which are located in the region of Western Macedonia (Regional Units

Kastoria, Kozani, Grevena). In March 2022, the total population was 470,000 breeding animals and

approximately 1.6 million production stock that are pelted annually. As 90% of Greece’s fur production

is exported to Russia, following the sanctions, the above-mentioned numbers can decrease. Raccoon

dogs are not bred in Greece.

Epidemiological situation

Until 29 January 2021, the reporting period to which the previous EFSA report refers (EFSA, 2021),

SARS-CoV-2 was detected on 21 out of the 91 mink farms currently present in Greece. Until November

2022, four more outbreaks were reported, two in February 2021 in the regional Units of Kastoria and

Grevena, and two more in August 2021 in the regional Unit of Kozani.

The

ﬁrst

one in Kastoria was suspected based on the

ﬁrst

observation of reduced feed intake on 26

January 2021, while respiratory symptoms and increased mortality were

ﬁrst

detected on 29 January

2021. It was estimated that around 70% of all 716 farmed animals showed respiratory symptoms, and

55 minks died since the estimated date of virus introduction. The outbreak was conﬁrmed on 5

February by RT-PCR, but it was not possible to relate it to human infection, as none of the farm

personnel or owners was found positive in either molecular or antibody testing.

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The second outbreak reported in February 2021 was in Grevena. It was detected in minks, which

were tested because two positive workers were positive in the framework of the early warning system

(weekly testing) for farm personnel in place since November 2020. Animals showed no clinical signs

and mortality appeared in line with baseline mortality. There was no conclusive evidence on the

possible source of the virus, although transmission from infected workers is suspected.

The third outbreak was reported in Kozani, in August 2021, on a farm with 30,000 animals, of

which 25,600 were juveniles, and it was detected because an increase in daily deaths (80 juvenile)

followed by respiratory symptoms in 50 juvenile animals was noticed. Based on that, the owner

notiﬁed veterinary authorities on 8 November 2021, and samples from dead animals were collected

and conﬁrmed positive by RT-PCR. Farm personnel were vaccinated and tested all negative.

Similarly, the fourth outbreak, reported in the same regional unit as the third at the end of August

2021, was suspected due to death (180 animals) and respiratory signs in animals, approx. 50% of

them (total 14,200 animals, out of which 2,700 breeders). One worker, who was vaccinated 2 weeks

before, tested positive by PCR.

In Greece, the control measures applied included movement control inside the country, zoning,

traceability, quarantine, monitoring biosecurity measures including mandatory use of PPE. Affected

animals are not culled.

Genomic analysis

The analysis of genomes isolated in 20 infected farms showed that B.1.1.305 in the prefecture of

Kastoria and B.1.1.218 in the prefectures of Kozani and Grevena are the two main lineages detected in

mink and farm personnel, as it is the case in the general population. In each distinct farm, the same

lineage was identiﬁed in mink and farm personnel.

The most frequent mutations in the S protein are the D614G, N501T and P812L, both for the

general human population and minks. Preliminary data indicate that mink were infected by humans in

most of the cases. Mink-related mutations in the S protein have been detected (Y453F) in six human

cases directly related to farms and in animals from four establishments, but it has not been detected in

the small sample of the general population. None of the other mutations described on by ECDC

(ECDC, 2020a) has been found so far, neither in humans (farm personnel/owners and community) nor

animals. Although spillback into the local community has not been observed, further investigation in

the general population by extending the number of sequenced genomes is ongoing.

Monitoring scheme

Since the

ﬁrst

case of SARS-CoV-2 in mink in Greece in November 2020, a monitoring plan has

been implemented as follows:

•

Mink farm personnel were regularly tested with PCR and rapid antigen tests during the

reporting period (February 2001–March 2022), by PCR weekly until May 2021, PCR every

14 days from June to December 2021 and rapid antigen tests weekly from January 2022 to

March 2022; and results are notiﬁed to veterinary authorities.

As regards mink, passive monitoring was implemented by clinical investigations and laboratory

testing (oropharyngeal swabs tested by RT-PCR) upon notiﬁcation of clinical signs related to SARS-

CoV-2 or increased mortality in mink, or in case humans in the establishment tested positive.

Under this scheme, 24 of 29 samples from three mink farms and 14 out of 40 samples from farm

personnel from two farms tested positive. From February 2021 to May 2021, when the 2021/788

Decision entered into force, 10 samples were collected from farms with increased mortality and 20

from establishments, where SARS-CoV-2 cases in workers or their families were notiﬁed. The

sampling scheme has been adjusted to the Decision since it was adopted in May 2021.

Mink farms were subjected also to active monitoring whenever animals were moved. In these

cases, 20 samples were taken for testing (oropharyngeal swabs-real-time PCR) from the

establishment of origin prior to each movement (design prevalence: 15%); no positive cases

were detected.

Sequencing was conducted on samples from both human (100% samples) and animals (30%

samples) that were tested positive at farm level during the reporting period (February 2021–

March 2022). Moreover, sequencing was performed on positive samples from the community in

the workers’ places of residence. All sequencing results were compared and no mink variants

were detected in samples collected from the community in the areas where mink farms are

located, and no spillover infection to the community was detected.

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•

Since the 2021/788 Decision entered into force, also other kept and wild animals belonging to

mustelids have been monitored according to the section 2 of Annex III of Decision 2021/788.

3.2.1.1.4. Italy

As of January 2022, in Italy, there were

ﬁve

mink farms with 6,055 breeding stock, mainly

concentrated in northern Italy (two farms in Lombardy and two in Emilia Romagna region) and one

farm in central Italy (Abruzzo). No other animal species is object of systematic monitoring for SARS-

CoV-2 infection.

Epidemiological situation

So far, only one positive animal in one farm was detected by PCR in Italy, in January 2021, out of

10,823 samples tested from six farms, up to March 2022. No clinical signs were observed in the farm.

No other animals in the farm were tested positive at PCR, while seropositive animals were detected. A

further outbreak was reported in November 2022 in a mink farm composed of breeding 1,523 animals

in Emilia Romagna region; this was detected within the surveillance plan, which provides controls on

live and dead animals. In this regard two animals tested positive at RT-PCR, one out of 55 live animals

tested and one out of four dead animals, both asymptomatic.

Monitoring scheme

There is a weekly control of all dead animals in mink farms, coupled with 60 oropharyngeal swab

(target prevalence 5%) every 15 days (in 2022, it is on weekly frequency) as random sampling to be

tested by PCR.

3.2.1.1.5. Latvia

In Latvia, the only farmed species targeted by SARS-CoV-2 monitoring are mink. As of January

2022, there are four mink farms with a total of 117,954 breeding animals and an estimated production

stock of 250,000 animals to be pelted by the end of 2022.

Epidemiological situation

The only outbreak in mink in Latvia was reported in April 2021, conﬁrmed on 10 April 2021 in

Iecava county, approximately 50 km south from Riga, in a farm with 64,000 female breeders. No

clinical signs nor unusual mortality was reported in the farm in the period around detection until the

pelting season in November. The disease was detected in the frame of monitoring programme, i.e.

weekly sampling of at least one dead mink from the each farm. For the conﬁrmation, 10 additional

samples (dead mink) were taken, and the presence of SARS-CoV-2 virus was conﬁrmed in nine dead

minks by RT-PCR. After conﬁrmation of the outbreak, weekly sampling of

ﬁve

dead minks was

established to monitor the epidemiological situation in the affected farm. The epidemiological

investigation showed that SARS-CoV-2 was introduced in the mink farm by an infected worker.

From July 2021, the number of dead minks to be tested weekly was increased to 10 to get more

isolates for sequencing, as from July all PCR-positive mink samples were sequenced. Apart from dead

mink testing, also 20 live mink were sampled every month (for PCR and serological testing). After

pelting, up to 19 dead minks were sampled every week. In total, more than 500 dead minks and

around 200 live minks were tested from April 2021 to the beginning of March 2022. In the second

week of March 2022, the weekly testing was stopped due to the absence of PCR-positive results.

Interestingly, the continuous surveillance in the affected farm showed

ﬂuctuating

virus circulation in

animals: the seroprevalence in samples taken from live minks was around 70%, and three infection

waves were observed during the period of April–November 2021, when animals were pelted. After

pelting, a signiﬁcant reduction in virus prevalence in the affected mink farm was observed. The

interpretation by Latvian authorities was that the reduction of animal numbers and density also might

have an impact on virus circulation.

Since outbreak detection, weekly screening tests were performed also on farm personnel, who did

not experience any serious clinical signs, nor were they hospitalised. Until the beginning of pelting

season in November, all farm personnel were fully vaccinated against SARS-Cov-2, and, among those,

no positive cases were reported in 2022 (32 workers were tested positive in 2021).

Genomic analysis

The results of the phylogenetic analysis in mink showed that the genome sequences belong to the

Pangolin lineages B.1, B.1.177, B.1.177.60 (SARS-CoV-2 Alpha variant), which were also the dominant

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lineages in the Latvian human population at the beginning of 2021. Some mutations in spike protein

gene (e.g. Y453F, F486I, N501T, P681R, T478K, L452R) in virus isolates obtained from mink were also

identiﬁed.

The phylogenetic analysis of the virus isolated from farm personnel showed eight cases in which

virus mutations were related to those from infected minks, indicating backward transmission of the

virus from animals to humans in the affected holding. However, the circulating type of SARS-CoV-2

virus detected in the mink farm was not detected in human population living close to the farm, nor

elsewhere in Latvia.

Monitoring scheme

•

From January until October 2021, weekly sampling and testing of one dead mink from every

mink farm to SARS-CoV-2, oropharyngeal swabs by RT-PCR.

From July 2021, weekly screening (saliva laboratory testing by RT-PCR) of mink farm

personnel.

From September 2021, following the risk assessment done by the Food and Veterinary Service

(FVS), the active monitoring based on weekly testing in all mink farms was changed to passive

surveillance based on suspicion in mink and conﬁrmed SARS-CoV-2 cases in farm personnel.

The risk assessment included:

–

the results of the laboratory tests performed so far on the mink regarding the presence of

SARS-CoV-2 in the farm;

the active monitoring in all mink farms based on oropharyngeal swabs to be tested by RT-PCR

targeting 25% prevalence with 95% conﬁdence. Samples were chosen from dead mink, but if

they were not sufﬁciently available to achieve the required sample size, additional samples

were taken from live mink.

the vaccination status of the persons working in the holding, the procedures for laboratory

examinations (screening) and the results of the examinations regarding the SARS-CoV-2;

compliance of the biosecurity measures implemented in the farm as set by national legislation.

The owner or keeper of the mink farm continue to send to FVS electronically data:

number of minks in the holding.

number of minks that have died and been killed in the farm weekly.

In accordance with national legislation, the owner or keeper of minks must immediately notify the

FVS about suspicion of SARS-CoV-2 in minks, e.g. if the animals show symptoms of acute respiratory

infection, digestive system dysfunction, depression, immobility, withdrawal from food or water or

increased animal mortality.

Other animals

SARS-CoV-2 monitoring was implemented also on wild animals of the family

Mustelidae,

as well as

raccoon dogs. For this purpose, dead animal carcasses were submitted for laboratory testing in the

frame of rabies passive surveillance; no positive results were found.

3.2.1.1.6. Lithuania

In Lithuania, the only animal species targeted by SARS-CoV-2 monitoring are mink. As of January

2022, there are 120 registered mink farms, of which 71 (62 in January 2021) were active (animals

were present) with a total of 277,043 breeding animals, and an estimated production stock of 600,000

animals to be pelted by end of 2022.

Epidemiological situation

In Lithuania, the

ﬁrst

two outbreaks were reported in mink farms in November and December

2020, and, under an intensiﬁed active monitoring, 13 further outbreaks were detected in November

and December 2021. As it was the pelting season, 10 of the infected herds with more than 78,000

animals in total only pelted young animals and kept breeding stock. In the other three infected mink

herds, all animals were killed and pelted. However, the mink mortality and morbidity did not increase

and remained within the norm or even below; thus, no clinical signs were observed on farms. The

disease was very mild, and it was detected only due to intensiﬁed targeted sampling.

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Monitoring scheme

Passive monitoring is conducted based on suspicion due to increased morbidity or mortality. During

the pelting season in November and December 2021, the veterinary authority decided to implement

also an active monitoring campaign on mink farms over the country, 1,219 samples from 57 out of 62

farms were tested and 41 samples from 13 farms were found as positive. Blood samples were also

taken from 19 farms for antibody detection, by targeting 10% prevalence with 95% of conﬁdence. Out

of 19 tested farms, 16 were found with antibodies (300/570 samples, 52%).

From 2021 until March 2022, 621 samples from 14 farms were tested and 24 samples from two

farms were positive by PCR (oral swabs). In addition to passive surveillance, the veterinary authority is

notiﬁed in case of positive farm personnel (currently in 2022 most of the farm personnel are

vaccinated, and vaccinated workers are not tested anymore on a regular basis) or increased mink

mortality, and following an epidemiological investigation is conducted. Furthermore, not less than the

last

ﬁve

dead animals per week are sampled for testing. Samples in case of suspicion are collected

from dead animals, pelted animals and clinically affected animals.

Genomic analysis

For all virus positive samples, sequencing was performed, and the results indicated that for almost

all samples, SARS-CoV-2 virus Delta mutation was dominant.

3.2.1.1.7. Poland

In Poland, the farmed species targeted by SARS-CoV-2 monitoring are mink and raccoon dogs. As

of January 2022, there are 261 mink farms (272 in January 2021), with a total of 1,988,272 breeding

animals, and an estimated production stock of 344,958 animals to be pelted by the end of 2022.

Besides, there are 28 raccoon dog farms, with 4,701 animals in total.

Epidemiological situation

The

ﬁrst

outbreak in farmed mink in Poland was conﬁrmed in January 2021, followed by another

one in June 2021. During the months of November and December 2021, through active surveillance,

further nine outbreaks were reported in mink farms, without clinical signs. In 2022, four additional

outbreaks have been reported, in January, July, September and October, respectively.

Genomic analysis

Molecular tests are conducted on E gene fragments of Sarbecoviruses for virus monitoring; positive

samples are conﬁrmed in tests aimed at N and RdRp genes fragments by using in-house PCR based on

Corman et al. (Euro surveillance, 2019), and NGS sequencing is done on positive samples.

Monitoring scheme

In 2021, monitoring was carried out in accordance with the monitoring rules in the Polish

legislation, i.e. throat or nasopharyngeal swabs were taken from at least 10 dead mink or mink with

clinical signs. In the absence of clinical symptoms, the tests were carried out twice a year (20 live

mink) with a minimum of 8 weeks sampling interval on the farm.

In 2022, in accordance with the provisions of Commission Implementing Decision (EU) 2021/788,

passive surveillance is carried out, in all mink and raccoon dog farms in Poland. In addition, active

monitoring is carried out on farms with over 500 adult livestock at the beginning of the production

cycle. Between February 2021 until March 2022, 11,853 samples from 594 farms were tested by PCR,

and 104 positive samples from 11 farms were detected.

Farm personnel monitoring is carried out when the second alternative sampling scheme is in place

as of (EU) 2021/788.

Other animals

Other kept (other than farmed) or wild animals are subject to passive surveillance in accordance

with Annex III, Section 2, of Commission Implementing Decision (EU) 2021/788. Samples are taken

from all dead animals or animals with clinical signs related to SARS-CoV-2. In 2022, six badgers, one

ferret and one marten (road kills) were tested for SARS-CoV-2, all with negative results.

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3.2.1.1.8. Spain

As of January 2022, there are 27 mink farms in Spain with 104,000 breeding animals and around

340,000 animals for pelting.

Epidemiological situation

In 2021 and up to November 2022, there have been 17 outbreaks reported in Spain in mink farms;

14 were reported in summer 2021, between June and October 2021, most linked to the

implementation of a new monitoring scheme (see below).

Monitoring scheme

In accordance with Commission Implementing Decision (EU) 2021/788 of 12 May 2021, a National

Program for Prevention, Surveillance and Control of SARS-CoV-2 in American mink farms was

developed by the Spanish Ministry of Agriculture, Fisheries and Food (MAPA) in collaboration with the

Coordination Centre for Health Alerts and Emergencies (CCAES) and the Autonomous Communities

with mink farms.

The programme comprises (i) the prevention measures for SARS-CoV-2 infection, (ii) the

surveillance and early detection of SARS-CoV-2 infection and (iii) SARS-CoV-2 control activities.

The surveillance on animals is based on two components:

•

A passive surveillance component focused on the detection and communication to the Ofﬁcial

Veterinary Services (OVS) of any clinical sign compatible with SARS-CoV-2 infection, followed

by sampling of sick animals and PCR test carried out in the NRL;

A targeted active surveillance component including the PCR testing of oropharyngeal swabs

from 8 found dead animals on the farm every 2 weeks.

Through passive surveillance, 2,043 samples from 21 farms were tested from February 2021 to

March 2022, 21 samples from

ﬁve

farms were tested positive at PCR; in these the infection was

detected after the detection of positive workers, but without signs or abnormal mortalities in mink. So

far, no positive farms have been detected in 2022.

By the active surveillance, tests on 740 samples from 27 farms identiﬁed 63 positive animals from

10 farms.

Moreover, a monitoring is conducted on positive farms as follow-up. Every 2 weeks, oropharyngeal

swabs are taken from 30 adult animals (older than 13 months) and from 60 offspring. This monitoring

is maintained until a negative result is obtained by RT-PCR in two consecutive samplings.

Monitoring of infection in farm personnel is also in place with two components:

•

A passive surveillance component for the early detection of cases, consisting of communication

of any compatible clinical symptom to the human health authorities.

An active surveillance where farm personnel are subject to regular random screening tests.

In case of detection of virus in a farm, positive samples are subjected to sequencing processes to

investigate genetic variants and possible mutations.

Passive surveillance for detection of cases compatible with SARS-CoV-2 is conducted in other

domestic and wild mustelids and raccoon dogs as foreseen in Annex I of Commission Implementing

Decision (EU) 2021/788 with no detection of cases of infection.

Independently from the governmental monitoring scheme, wildlife research groups and rescue

centres have performed some research activities of SARS-CoV-2 infection in susceptible species, mainly

wild mink. Two infected wild mink were initially suspected to be positive (Aguilo-Gisbert et al., 2021),

which they turned out to be negative according to conﬁrmatory analysis in ofﬁcial accredited

laboratory.

Infection was detected in dogs and cats from positive households (Barroso-Arevalo et

al., 2021a,b; Miro et al., 2021).

Genomic analysis

The sequencing conducted in the isolates from Spain revealed that the most frequent lineage

detected was B.1.1.7 (Alpha variant). The mutations identiﬁed were D614G, N501T (a site related to

an adaptation to the host and to antigenic drift), A222V (characteristic of the human cases), Y453F

(very rarely, detected in Galicia in March 2021

–

described in samples from several Danish mink farms

https://www.woah.org/ﬁleadmin/Home/MM/Spain_mink_09.04.21.pdf

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SARS-CoV-2 in animals

(Hammer et al., 2021; Rasmussen et al., 2021)), and F486V and D796H (the two changes that always

appear together, detected in 2020).

3.2.1.1.9. Sweden

During the current reporting period (February 2021–November 2022), mink is the only farmed

species targeted by SARS-CoV-2 monitoring in Sweden. In February 2022, there were 22 mink farms

with approximately 60,000 breeding animals. Breeding was banned during the season 2021 as a

preventive measure after the outbreaks of SARS-CoV-2 that affected large parts of the Swedish mink

industry in 2020 but is again allowed during the season 2022. There is no racoon dog breeding in the

country.

Epidemiological situation

During the previous reporting period (until January 2021), SARS-CoV-2 was detected in mink in 13

farms. Moreover, a serological screening conducted during fall 2020, which covered the majority of

mink fur farms active at the time, suggested that most of them had been exposed to the virus. During

the current reporting period, movement restrictions and strict biosecurity measures have been in place

for all mink farms in Sweden.

During the present reporting period, one outbreak of SARS-CoV-2 in mink has been conﬁrmed and

reported in August 2021. The farm in question, with 11,000 breeding animals at that time, was located

in Skara municipality in the southwest of Sweden. No increased morbidity or mortality had been

observed on the farm, and samples were taken for analysis within the surveillance programme

covering all mink farms in Sweden in accordance with Commission Implementing Decision (EU) 2021/

788. At the time of the outbreak, all people associated with the farm had either had the infection

(COVID-19 conﬁrmed in farm personnel in November 2020) or been vaccinated, or both. Moreover, a

serological screening carried out in December 2020 demonstrated that also the mink on the farm had

been exposed to SARS-CoV-2 although virus could not be detected at that time. In spite of this, SARS-

CoV-2 might have been introduced again to the farm, most likely through one of the farm personnel,

although this was never conﬁrmed.

Genomic analysis

Whole genome sequencing of the virus demonstrated that the virus belonged to sublineage

B.1.1.464 (clade 20B) of SARS-CoV-2. None of the amino acid mutations described on the spike

protein and considered associated with adaptation to mink was present in the sequence. At the time,

matching sequences from sublineage B.1.1.464 had previously been described from at least 14

countries globally in samples originating from people. Moreover, this sublineage had also been

detected in mink in two other countries. B1.1.464 had not been detected previously in Sweden.

Monitoring scheme

A monitoring scheme has been in place in Sweden since fall 2020, which foresees that all fur farms

submit animals found dead, or throat swabs from animals found dead, to the National Veterinary

Institute for SARS-CoV-2 testing using RT-PCR. The scheme was initially run on a voluntary basis but

has been compulsory since 2021-05-12 in accordance with Implementing Decision (EU) 2021/788.

Based on a risk assessment with positive outcome, the monitoring has been based on the alternative

sampling scheme for the monitoring of animals provided by Annex III in the decision.

During this reporting period, 1,143 samples from 28 farms have been tested, with positive results

only in one out of six samples submitted from the outbreak farm described above.

To have a better overview of the situation, the monitoring scheme described above has been

complemented with two serological screenings during 2020 and 2021, respectively. During this

reporting period, 30 mink serum samples from each of 25 farms (out of the 28 farms active at that

time) were submitted to the National Veterinary Institute between June and November 2021, and

analysed by indirect ELISA (IDvet, ID Screen SARS-CoV-2 Double Antigen Multi-species ELISA).

Samples from 12 farms tested positive in the screening, 11 of which were positive also during the

screening conducted during the previous reporting period. In these 11 farms, the proportion of

positive samples were lower (in 10 farms) or equal in this screening compared to the previous

screening. In one farm, which was negative in the screening in 2020, 16 of 30 samples tested positive

suggesting that the animals on the farm had been exposed to the virus during this reporting period.

No increased morbidity or mortality had been observed on the farm.

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3.2.1.2. Natural infection in other livestock species

By screening the scientiﬁc literature and WOAH outbreak dashboard,

camel, cattle, horse, chicken,

swine, goat, sheep and rabbit have never been detected positive for SARS CoV-2 infection at PCR

under

ﬁeld

conditions (Deng et al., 2020; Cerino et al., 2021; Pomorska-Mol et al., 2021; Ruiz-Arrondo

et al., 2021; Villanueva-Saz et al., 2021a). Serological evidence was detected in rabbit and cattle in a

limited number of studies (Fritz et al., 2022; Wernike et al., 2022).

3.2.2.

Companion animals detected as infected with SARS-CoV-2 under

ﬁeld

conditions

3.2.2.1. Cat

In general, cases in cats have been associated with mild to moderate respiratory (e.g. coughing,

sneezing, shortness of breath, increased respiratory rate, congestion and eye discharge) or

gastrointestinal (e.g. vomiting, mouth ulcers, diarrhoea) or general non-speciﬁc syndromes (e.g.

lethargy, fever, lack of appetite, cardiac or neural signs). The analysis of available global data shows 51

references reporting 725 suspected cases of cats based on clinical signs or epidemiological links with

SARS-CoV-2 infections. Several of these studies were case reports of detected infected cats associated

with infected households and showing clinical signs. A systematic review on clinical presentation of

infection in cats identiﬁed 70 cases (out of a total 124 reviewed cases) with clear data on clinical

presentation. Out of these reviewed cases, 38 (54%) were asymptomatic and 32 (46%) were

symptomatic. From all cases reviewed, there were six severe cases, where cats died or were

euthanised due to disease complications (Giraldo-Ramirez et al., 2021).

For cases where infection was conﬁrmed by virus isolation or identiﬁcation of virus genome in

respiratory and/or anal samples, high levels of virus loads, indirectly measured by detection of virus

genome (10^6.8 RNA copies/ml sample or RT-PCR cycle threshold, (CT) values

21) were observed,

particularly in some symptomatic cases (Gonzales et al., 2021; Piewbang et al., 2022; Sila et al., 2022).

From all articles identiﬁed in the SLR, a subset (N = 28) was selected where observational studies

were reported. These studies were either random or opportunistic surveys, which reported serological

results. Data on the proportion of infected cats grouped by their habitat conditions (household pets,

feral/stray (free roaming cats) or cats kept in shelters) were collected from each selected study. A

summary of the distribution of the reported percentage of seropositive cats among the studies is

presented in Table

While there is large heterogeneity in the study approach (study design,

diagnostic methods and timing of sampling) and the reported

ﬁndings,

it could be seen that the

observed percent of seropositive cats among the studies was higher (two to three times) in those cats

–

household pets or feral

–

which were exposed to a known infected source (e.g. infected household

member(s), infected mink farms (Boklund et al., 2021; van Aart et al., 2021; Zhao et al., 2021; Amman

et al., 2022)),than in those cats whose close environment reported no infection (e.g. household

members not infected) or this information (e.g. infection situation in the household) was unknown

(Fritz et al., 2020; Patterson et al., 2020; Bessiere et al., 2022; Kannekens-Jager et al., 2022; Oliveira

et al., 2022). Observed levels of seropositivity in shelters with an unknown source of infection (median

10.4% [interquartile range (IQR): 1.7–13.0]) appear to be higher than seropositive levels observed in

feral/stray cats with unknown source of exposure (median 2.5% [IQR: 0–9]) (Table

4),

which could

reﬂect exposure of shelter cats to infection via contact with infected humans in the shelter or contact

with infected cats (Piewbang et al., 2022).

Overall, it is possible to infer that cats are highly susceptible to the infection and that they could

shed virus in comparable levels to those reported for people, which may lead to efﬁcient cat-to-cat

direct-contact transmission (R0

1) (Gonzales et al., 2021; Gerhards et al., 2022; Piewbang et

al., 2022) and potential cat-to-human transmission events (Piewbang et al., 2022; Sila et al., 2022).

Cats from households with infected people have the highest risk of infection, and if these cats are

allowed outdoor roaming, they may represent a risk for transmission to other cats (domestic or stray/

feral cats) they contact outdoors. Similarly, feral cats with access to infected sources, such as infected

mink farms, may represent a risk for transmission to both the feral cat population and household cats

they would encounter when roaming around residential neighbourhoods in the vicinity of mink farms

(Amman et al., 2022). The low levels of infection observed in stray/feral cats with unknown source of

exposure may be a result of limited contact with potential sources of infection, such as contact with

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household cats, and even between feral cat colonies. The latter would limit spread of infection within

feral cats. However, feral colonies and household cats nearby mink farms may appear to represent the

cat population with the highest risk of becoming infected.

3.2.2.2. Dog

The SLR identiﬁed 34 studies evaluating the presence of infection in dogs. As done for cats, most

studies were opportunistic, which followed infected households, reported individual case reports or

random surveys, mostly involving clients from veterinary clinics. A crude overview of the reports from

the studies identiﬁed in the SLR shows that the frequency of reported virus (genome) detections in

dogs is lower than that in cats (data not shown) and that infections in dogs were mainly

asymptomatic. Observational studies where data on detection of infection (assessed by serological

tests) could be extracted are summarised in Table

As observed for cats, the percentage of positives

detected was higher in dogs exposed to an infected source (mainly a household with infected people).

Studies where both dogs and cats were sampled, reported higher percent of positivity in cats than in

dogs, with one study in particular reporting the odds for infection in cats being 7.6 (95% CI: 1.9–44.4)

higher than in dogs (Colitti et al., 2021).

In summary, dogs are susceptible to infection; if infected, they are mostly asymptomatic and may

shed low levels of virus, which may limit between-dog transmission.

Table 4:

Summary of apparent seroprevalence (%) observed in observational studies reported in

the literature

Epidemiological Source of

exposure

(b)

unit

(a)

Feral/stray

Household

Shelter

Vet clinic

Dogs

Feral/stray

Household

shelter

Vet clinic

Infected

(c)

unknown

Infected

Not_infected

Unknown

Infected

Not_infected

Unknown

Infected

(c)

Infected

Not_infected

Unknown

Infected

Not_infected

Unknown

Distribution of

Distribution of apparent

number of

Number

prevalence

animals sampled

of Studies

Median Q1 Q2 Median Min Q1 Q2 Max

133

238

251

50.0

2.5

20.0

2.6

6.3

10.4

7.7

0.0

62.5

12.8

1.5

0.4

0.0

12.5

0.0

0.8

17.7 22.7 53.3 64.3

0.0

0.1

0.0

5.2

0.0

0.4

7.9

3.2

1.7

3.8

0.0

9.2 19.2

23.5 52.1

6.3

Species

Cats

16 385

46 102

15 56

24 127

13.0 22.5

11.5 15.4

3.3

1.2

6.7

22.9

11.4 17.1 40.7

0.0

6.3

0.0

0.2

1.9

4.9

22 454

0.0 0.0

18.8 25.0

0.0

1.8

0.0

9.1

55 500

(a): Within each selected study, one or multiple epidemiological units (households, veterinary clinics and/or feral cats from

different geographical locations) were sampled. Only epidemiological units where equal or more than 10 animals were

sampled were selected for data extraction. Data on number of animals sampled and number of positives were collected per

epidemiological unit. Percentage of seropositive animals (apparent prevalence) was estimated per epidemiological unit.

(b): The source of exposure to infection is known:

‘infected’

source (e.g. infected humans in the household),

‘not_infected’

source (e.g. animals coming from households where no infection in humans was conﬁrmed) or

‘unknown’

(no information

was available or not provided about the situation regarding infection in humans or other pets in the epidemiological unit).

(c): These are feral/stray companion animals living nearby affected settings, e.g. hospitals (Farnia et al., 2020) or infected mink

farms (Boklund et al., 2021; Zhao et al., 2021).

3.2.2.3. Hamster

There is evidence that hamsters can be naturally infected with SARS-CoV-2 and cause human

infections (Kok et al., 2022; Yen et al., 2022). Kok et al. (2022) reported that following a case of an

infected worker in a pet shop in Hong Kong, 7 out of 69 swab specimens collected from hamsters

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were conﬁrmed positive for SARS-CoV-2 infection by RT-PCR. The warehouse supplying this pet-shop

chain was investigated on 17 January 2022, with 511 swabs randomly collected from hamsters

(n = 137), rabbits (n = 204), guinea pigs (n = 52), chinchillas (n = 116) and mice (n = 2). One Syrian

hamster swab was positive for SARS-CoV-2 infection by RT-PCR.

As follow-up investigation, swabs and serum samples were collected from the Syrian and dwarf

hamsters in the pet shop and the warehouse. Eight (50%) of 16 Syrian hamsters had evidence of

infection, with four animals positive by both serology and RT-PCR, three animals tested positive by RT-

PCR alone and one animal tested positive by serology alone. In the warehouse, 7 (58%) out of 12

Syrian hamsters had evidence of infection by serology. Of those, two were also positive by RT-PCR.

None of the dwarf hamsters were conﬁrmed positive for SARS-CoV-2. Genetic and phylogenetic

analysis of the viruses suggested that importation of SARS-CoV-2-infected hamsters to Hong Kong was

a likely source of this outbreak. Eighty-two human cases with an epidemiological link to hamsters were

detected leading to multiple zoonotic transmission events to humans. SARS-CoV-2 viral genomes from

human and hamster cases in this cluster belong to the Delta variant of concern (AY.127) that had not

been circulating locally before the outbreak.

Further investigations were then performed on 100 randomly selected euthanised dwarf hamsters

housed in the warehouse, as the small number of rabbits and chinchillas had already been removed

from the warehouse prior to the warehouse visit. The lung tissues of three of these 100 (3.0%)

hamsters tested positive for the SARS-CoV-2 by RT-PCR (Kok et al., 2022).

3.2.3.

Wild animals detected as infected with SARS CoV-2 under

ﬁeld

conditions

Among wildlife, white-tailed deer in North America, where it is very abundant with over 30 million

animals (EAZWV, 2022), as free living or kept in game reserves, is one of the species raising most

concern in SARS-CoV-2 epidemiology. Detection of SARS-CoV-2 in white-tailed deer has been described

in seven publications, all describing surveys in different areas of USA or Canada (Chandler et al., 2021;

Hale et al., 2021; Cool et al., 2022; Kotwa et al., 2022; Palermo et al., 2022; Vandegrift et al., 2022;

Pickering et al., 2022a). The surveys cover in total 72 areas (7 states in USA and a high and low

density region in Canada) from which in total 962 animals have been sampled for PCR-test, leading to

a median of 16 animals (IQR: 9–32%) per sampled area, and 821 (median 27 animals, IQR: 5–21%)

have been sampled for serology. The median percentage of PCR positives was 27% (IQR: 9–62%),

while the median percentage of serologically positives was 16% (IQR: 0–67%). From the Canadian

Animal Health Surveillance System’s (CAHSS) dashboard, it appears that infection with SARS-CoV-2 has

been detected in 47 white-tailed deer across Canada (seven states). From USDA’s dashboard,

appears that SARS-CoV-2 has been detected in white-tailed deer in 24 states. Furthermore, detections

of SARS-CoV-2 in mule deer have been reported in USA as well as in Canada.

3,10

From Germany and

Austria, 232 samples from hunted red deer and roe deer were collected for SARS-CoV-2 surrogate

virus neutralisation test (sVNT), with none of them found positive (Moreira-Soto et al., 2022). White-

tailed deer are not native in Europe; some individuals were imported from North America in the last

century, but the abundance in Europe is very limited; currently few individuals are present in Czechia

(700 animals) and a more consistent population in Finland, approx. 100,000 individuals (EFSA, 2021).

White-tailed deer are also kept farmed in some places in North America, while this practice is not seen

in the EU. Farming may increase the contact between animals and humans, so it may increase the risk

of transmission to and from any susceptible species.

SARS-CoV-2 has been detected in wild American mink (or mink escaped from farms) in USA

(Shriner et al., 2021). In a study from Spain, 162 European or American mink were tested by ELISA

and/or RT-qPCR, and none were found positive (Villanueva-Saz et al., 2022). Furthermore,

ﬁve

seropositive mustelids (three martens and two badgers) have been detected in France (Davoust et

al., 2022). One PCR-positive juvenile wild leopard (Panthera

pardus)

was reported in India (Mahajan et

al., 2022).

Large numbers of red foxes, jackals and wild boar have been tested in Croatia, all with negative

results at PCR. Few results were serologically positive (6/153 wild boar, 3/65 jackals and 6/204 red

foxes); however, this was considered as false-positive results, due to negative or weak positive results

in VNT (Jemer

et al., 2021).

https://www.aphis.usda.gov/aphis/dashboards/tableau/sars-dashboard

https://app.powerbi.com/view?r=eyJrIjoiMGNhYjU0ODItNWFmYy00NTQ4LTk0OGMtOTRhZjIyODFjY2VmIiwidCI6IjE4YjVhNWVk

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In August 2022, the detection of RNA and antibodies against the SARS-CoV-2 Gamma variant

infection was reported in four specimens of

Chaetophractus villosus

(big hairy armadillo) in Argentina

(Arteaga et al., 2022).

From a study performed in Eastern USA, 18 different wildlife species were sampled, with SARS-

CoV-2 detected by PCR in the Virginia opossum (Didelphis

virginiana)

and equivocal detections in

additional species red fox (Vulpes

vulpes),

white-tailed deer (Odocoileus

virginianus)

Eastern grey

squirrel (Sciurus

carolinensis),

Eastern cottontail rabbit (Sylvilagus

ﬂoridanus)

and bobcat (Lynx

rufus).

Species considered human commensals like squirrels and raccoons had seroprevalence ranging

between 62 and71%, and sites with high human use had three times higher seroprevalence than low

human-use areas (Goldberg et al., 2022).

3.2.4.

Zoo animals detected as infected with SARS-CoV-2 under

ﬁeld

conditions

Detection of SARS-CoV-2 in lions, tigers and pumas in zoos was described in 10 publications, of

which four described multispecies outbreaks. In total, SARS-CoV-2 was detected by PCR in 25 lions, 15

tigers and 1 puma. The median percentage of PCR positives was 100% in all three species; however,

for lions, the 25-percentile was 22%, while 73% for tigers. And pumas were only reported in one

reference, with two pumas included, of which one puma was tested and found positive. The median

group size for lion and tiger was 2–4, with a maximum of 18, and 8, respectively.

In reports by WOAH,

detections of SARS-CoV-2 by PCR have been described in numerous zoo or

captive wild species, most often felines (tiger, lion, puma, leopard,

ﬁshing

cat, Eurasian lynx and,

Canada lynx), but also in other families (South American coati (Nasua

nasua),

spotted hyena (Crocuta

crocuta),

hippopotamus, giant anteater (Myrmecophaga

tridactyla),

West Indian manatee (Trichechus

manatus),

black-tailed marmoset (Mico

melanurus),

common squirrel monkey (Saimiri spp.), mandrill

(Mandrillus

sphinx),

otter (Lutra

lutra)

and gorilla (Gorilla

gorilla)).

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SARS-CoV-2 in animals

3.3.

Sequence data of animal species infected with SARS-CoV-2

As of 13 October 2022 (week 39/2022), there are 2093 sequences collected from animal hosts deposited in the GISAID EpiCoV database (Figure

Table

5).

Inclusion criteria were non-human and non-environmental host sources, collection dates from January 2020 and excluding non-SARS-CoV-2

sequences from bats. The sequences related to the Variants of Concern (VOC), belonging to the Ancestral (pre-Alpha), Alpha, Beta, Delta, Gamma and

Omicron clades, are indicated speciﬁcally. The microreact site, a web application to visualise data and sharing genomic epidemiology of the sequences is

available.

Table 5:

Host

Neogale vison

Odocoileus virginianus

Felis catus

Canis lupus familiaris

Panthera leo

Mus musculus

Panthera tigris

Mesocricetus auratus

Panthera tigris jacksoni

Gorilla gorilla

Panthera uncia

Aonyx cinereus

Panthera tigris

Chlorocebus sabaeus

Rhinolophus malayanus

Gorilla gorilla gorilla

Phodopus roborovskii

Rhinolophus pusillus

Cygnus columbianus

Number of deposited SARS-CoV-2 sequences from animal sources by animal host from GISAID database,

January 2020–13 October 2022

(week 39/2022)

Common name

Mink/American Mink

White-tailed deer

Cat

Dog

Lion

House mouse

Tiger

Golden (syn. Syrian) Hamster

Malayan Tiger

Western Gorilla

Snow Leopard

Asian small-clawed otter

Mainland Asian Tiger

Green Monkey

Malayan horseshoe bat

Lowland Gorilla

Dwarf Hamster

Least horseshoe bat

Tundra Swan

Number of sequences

1,323

323

133

https://microreact.org/project/7SSAQ1zRZ9CaJNJDYKm4xD-20,221,026-animal-sc2-publication-country

https://gisaid.org/

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Host

Mustela putorius furo

Panthera tigris sondaica

Arctictis binturong

Crocuta crocuta

Hippopotamus amphibius

Manis javanica

Mustela furo

Nasua nasua

Prionailurus bengalensis euptilurus

Prionailurus viverrinus

Puma concolor

Rhinolophus marshalli

Rhinolophus stheno

Common name

Domestic Ferret

Sumatran Tiger/Javan Tiger

Bearcat

Spotted Hyena

Hippopotamus

Sunda Pangolin

Ferret

South American Coati

Leopard Cat

Fishing Cat

Cougar

Marshall’s horseshoe bat

Lesser brown horseshoe bat

Number of sequences

The tree is constructed using Animal sequences from GISAID EpiCoV, using Nextclade tool by including clade speciﬁc reference genomes from Nextclade (link). Human reference

genomes are coloured Lavender blue in the tree, whereas the colouring patterns for Animal sequences are based on their hosts. Mainly, mink sequences (yellow), companion animals

–

cats, dogs and hamsters (shades of blue), wild cats

–

lions, tigers, mainland Asian tiger, leopard cats,

ﬁshing

cat and bear cats (shades of orange) and white-tailed deer (green).

Figure 7:

Phylogenetic analysis of SARS-CoV-2 Animal sequences along with the human clade-speciﬁc reference genomes

Source of

ﬁgure

https://microreact.org/project/7SSAQ1zRZ9CaJNJDYKm4xD-20221026-animal-sc2-publication-country

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SARS-CoV-2 in animals

3.3.1.

Sequence data of farmed animals infected with SARS CoV-2 (mink)

More than half of the total animal sequence depositions in GISAID EpiCoV database are derived from mink (1,323 sequences). Mink sequences cluster

into distinct major mink-speciﬁc clusters and most of them are located in ancestral clades (pre-alpha clades, Figure

8).

These clusters show high intra-

cluster variability, indicating mink-to-mink transmission, high rates of virus evolution within the mink population and emergence of mink-speciﬁc variants with

potential to spill back into the human population, which has previously been described (ECDC, 2020d; Oude Munnink et al., 2021). Sequence data within

clusters exhibit high intra-cluster variability, which indicates high level of transmission and accelerated evolution within the cluster. The latest pre-alpha virus

sample collected from mink belongs to clade 20C in Lithuania, collected on 26 November 2021, and there are no pre-alpha viruses detected in 2022 and

only six mink-related sequences were reported in 2022. Fewer smaller mink clusters have been detected in VOC clades, but mostly sporadic mink sequences

are reported in these VOC clades

–

belonging to Alpha, Delta and Omicron. Only two mink-related Omicron sequences have been reported indicating that

human-to-mink transmission has been probably mitigated over time if testing has been continued. No sequences of SARS-CoV-2 originating from raccoon

dogs have been uploaded to GISAID.

Mutations identiﬁed in outbreaks of SARS-CoV-2 in mink and related human cases:

SARS-CoV-2 variants detected in mink outbreaks and related human cases were part of at least

ﬁve

closely related clusters; each cluster was

characterised by a speciﬁc mink-related variant, identiﬁed in humans and animals from infected mink farms. Some mutations, such as Y453F in the

receptor-binding domain (RBD) of the spike protein, have been suggested as an adaptation of the virus to mink and has been observed in many of the

SARS-CoV-2 strains in different countries, independently of the clustering (ECDC, 2020d). To note, the Y453F mutation has also been observed in human

cases not related to mink. One of the clusters (Cluster 5 variant strains), which was reported as circulating in August and September 2020, carried a

deletion of two amino acids (69–70) and two additional mutations in the S protein (I692V, M1229I) in addition to the Y453F mutation in the RBD.

Spillover of SARS-CoV-2 from mink to humans

The majority of spill-over events from animals is related to mink and in some occasions, this spill-over caused circulation of mink-related viruses in the

general population, as observed in Denmark (ECDC, 2020d; EFSA, 2021). Also other countries (e.g. The Netherlands) reported transmission of SARS-CoV-2

from mink to people (Larsen and Paludan, 2020; Oreshkova et al., 2020; Devaux et al., 2021; Hammer et al., 2021; Larsen et al., 2021; Lassauniere et

al., 2021; Lu et al., 2021; Oude Munnink et al., 2021; Sharun et al., 2021; Wang et al., 2021; Rabalski et al., 2022).

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SARS-CoV-2 in animals

The tree is constructed using Animal sequences from GISAID EpiCoV, using Nextclade tool by including clade speciﬁc reference genomes from Nextclade (link).

Figure 8:

Phylogenetic analysis of SARS-CoV-2 sequences from mink along with the human clade-speciﬁc reference genomes and other animal sequences

(not marked). Clusters are coloured by country of reporting.

3.3.2.

Sequence data of companion animals infected with SARS CoV-2

In total, 247 sequences have been deposited for companion animals, divided into cats (133), dogs (93) and hamsters (21) (Figures

9, 10, 11).

These

sequences are spread all over the SARS-CoV-2 clades and have much less tendency of clustering together. There is one Syrian hamster cluster (12

sequences) in the Delta clade mixed with human sequences reported from Hong Kong and previously described (Kok et al., 2022). Otherwise, companion

animal sequences mostly spread within human sequences. However, some sequences cluster within mink clusters, indicating some spillover from the minks.

Little to no tendency in terms of clustering indicates sporadic transmission from humans, with little or no animal-to-animal transmission among companion

animals. Furthermore, unlike mink, which are farmed and kept in large numbers, accelerated evolution and emergence of species-speciﬁc variants was not

observed in companion animal sequences. Some cat sequences cluster within mink clusters pointing to sporadic transmission events either during outbreaks

or from infected humans, possibly from cats visiting mink farms, or from households of mink workers.

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SARS-CoV-2 in animals

The tree is constructed using Animal sequences from GISAID EpiCoV, using Nextclade tool by including clade-speciﬁc reference genomes from Nextclade (link).

Figure 9:

Phylogenetic analysis of SARS-CoV-2 sequences from cats (blue dots) along with the human clade-speciﬁc reference genomes and other animal

sequences (not marked)

The tree is constructed using Animal sequences from GISAID EpiCoV, using Nextclade tool by including clade-speciﬁc reference genomes from Nextclade (link).

Figure 10:

Phylogenetic analysis of SARS-CoV-2 sequences from dogs (light blue dots) along with the human clade-speciﬁc reference genomes and other

animal sequences (not marked)

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SARS-CoV-2 in animals

The tree is constructed using Animal sequences from GISAID EpiCoV, using Nextclade tool by including clade-speciﬁc reference genomes from Nextclade (link).

Figure 11:

Phylogenetic analysis of SARS-CoV-2 sequences from hamster (dark blue dots) along with the human clade-speciﬁc reference genomes and

other animal sequences (not marked)

3.3.3.

Sequence data of wild animals infected with SARS CoV-2

Around 130 sequences have been deposited in the GISAID EpiCoV database for wild cats (lions, tigers, Mainland Asian Tiger, Leopard Cats, Fishing Cat

and Bear Cats, Figure

12).

These wild felids sequences have a higher tendency of clustering than companion animals. There is one lion-associated cluster

from Spain from November 2020 (19 sequences). This cluster also contains one sequence from dog and two human sequences and has previously been

described (Fernandez-Bellon et al., 2021). Another lion-related cluster was identiﬁed in sequences deposited from the USA in October 2021, also containing

one spotted Hyena-related sequence. Another cluster containing several different wild cats, collected in September–November 2021, uploaded from the

USA, also containing human sequences. These clustering patterns indicates animal-to-animal transmission for wild cats in zoo settings, but there is no clear

sign of species-speciﬁc evolution suggesting viral adaptation in these cats in these settings. These wild-cat-related sequences are spread all over the clades

except the Omicron clade.

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SARS-CoV-2 in animals

The tree is constructed using Animal sequences from GISAID EpiCoV, using Nextclade tool by including clade-speciﬁc reference genomes from Nextclade (link).

Figure 12:

Phylogenetic analysis of SARS-CoV-2 sequences from wild animals along with the human clade-speciﬁc reference genomes

White-tailed deer

In total, 323 white-tailed deer-related sequences have been deposited in GISAID EpiCoV database, originating from studies performed in the USA and

Canada (Figure

13)

(Hale et al., 2021; Caserta et al., 2022). Similar to mink, these white-tailed deer sequences form a signiﬁcant number of animal-speciﬁc

clusters indicating intra-species transmission and there are signs of accelerated evolution within these clusters. Some of the clusters include human

sequences, but not all of them. Sequences are spread across all clades including Omicron, except the index virus clade (Lineage A, clade 19). There were

two sampling periods for white-tailed deer sequences, the

ﬁrst

in autumn–winter 2020 (shown in light green colour dots, Figure

12)

and the second in

autumn 2021 (shown in dark green colour dots, Figure

12).

For the

ﬁrst

season, mostly all the sequences belong to the ancestral clades, except one

sequence in the Alpha clade. One small cluster (four sequences) previously described (Caserta et al., 2022) was highly divergent, indicating adaptation of

the virus to new host species, and there is one reference human sequence in this cluster which indicates limited spill-back to the human population for this

variant. During the second season, the sequences are spread over all the VOC clades, mainly Alpha and Delta clades, with few sequences in the Omicron

clade. Some ancestral divergent clade sequences were observed in this second season. This indicates new SARS-CoV-2 introductions to deer population in

2022, with remaining ancestral variants circulating for a longer period and at least one novel deer-adapted variant still circulating. It also indicates a

continuous transmission from humans to deer populations with deer-related intra-host evolution resulting in divergent clusters. The

ﬁndings

of sequence

data analysis have been also described in a recent publication (Pickering et al., 2022b).

As only very few sequences from other wild animals have been deposited in GISAID EpiCoV compared to white-tailed deer, it is difﬁcult to ascertain

whether the spread of SARS-CoV-2 within the white-tailed deer population in North America is unique, or if other similar events are ongoing in other animal

species and geographic regions.

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SARS-CoV-2 in animals

The tree is constructed using Animal sequences from GISAID EpiCoV, using Nextclade tool by including clade-speciﬁc reference genomes from Nextclade (link).

Figure 13:

Phylogenetic analysis of SARS-CoV-2 animal sequences from white-tailed deer along with the human clade-speciﬁc reference genomes. Clusters

are coloured by the hunting season.

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SARS-CoV-2 in animals

3.4.

Probability of transmission between animals, and between animals

and humans, posed by SARS-CoV-2 infection in animal species of

concern

In this section, for the animal species considered as particularly susceptible (Section

3.1)

and thus

potentially important in the epidemiology of SARS-CoV-2, the probability of SARS CoV-2 transmission

between animals and between animals and humans is addressed, as requested in ToR 2.

The possible epidemiological scenarios and related transmission pathways in farmed animals,

companion animals, zoo animals and wildlife are presented in diagrams, tables and supported by

explanatory text. The probability of transmission of the virus in each single pathway is qualitatively

assessed by consensus of the experts based on the risk and exposure factors identiﬁed and supported

by the evidence provided in Section

3.1.

The reasoning is further explained either in the tables or in

the text below the tables in Section

3.3.1.

The probability of transmission is estimated assuming no

preventive and control measures speciﬁc to SARS-CoV-2 in the animal species and in the human

exposed groups are applied (e.g. no use of non -pharmaceutical interventions (NPI), nor infection

prevention and control (see Section

3.5.3)).

An additional characterisation of the risk assessment is

composed by the amount or quality of evidence available (categorised as low, moderate, high) as

explained in Table

The possible preventive and control measures and monitoring approaches are

also indicated for each transmission pathway, and next to each, it is indicated in brackets, whether the

measure may affect the susceptibility or the exposure.

Table 6:

Name

High

Moderate

Low

Ratings used to describe the amount or quality of the evidence available (EFSA AHAW

Panel, 2015)

Explanation

No or limited information or data are lacking, incomplete, inconsistent or conﬂicting. No subjective

judgement is introduced. No unpublished data are used.

Some information or data are lacking, incomplete, inconsistent or conﬂicting. Subjective judgement

is introduced with supporting evidence. Unpublished data are sometimes used.

The majority of information or data are lacking, incomplete, inconsistent or conﬂicting.

Subjective judgement may be introduced without supporting evidence. Unpublished data are

frequently used.

3.4.1.

Farmed animals

This section refers to probability of transmission between farmed animals susceptible to SARS-

CoV-2, and from them to humans and vice versa. Farmed animals include fur-farmed animals such as

mink, raccoon dogs, sable, ferrets, foxes, but from now on we refer to mink, which is used as the type

animal in the category, given that it is considered the worst case. In Figure

14,

the pathways of

transmission (both direct and indirect transmission, the former as by direct contact with infected

animals or humans, the latter as transmission, e.g. by contaminated environment and fomites, etc.)

within and between mink farms are presented, while in Table

the probability of transmission (P),

possible control measures and monitoring approach are presented. The reasoning is described more

extensively in the text below the table.

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Figure 14:

Diagram of transmission pathways of SARS-CoV-2 in mink

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SARS-CoV-2 in animals

Table 7:

Transmission pathways of SARS-CoV-2 for different scenarios in mink farms, related preventive and control measures and probability of

transmission. Mink is used as a worst-case example of farmed animals

Probability of

transmission (in the

absence of control

measures speciﬁc

to animals in

question)

Potential preventive and

control measures in

animals/farm (in brackets Potential preventive and

control measures in humans

is indicated inﬂuence on

probability of exposure or

susceptibility)

Possible monitoring

approaches to reduce the

probability of

transmission

Transmission

Risk factors/

pathways (quantity of

exposure factors

interest)

•

Epidemiological

situation in the

‘What

proportion of mink

local/regional

farms in the EU will be

human population

infected in the next

•

No. of farm

12 months due to

personnel/visitors

contact with an infectious

visiting farms

human?’

•

No. of contacts

between farm

worker/visitor to

animals

•

No. of contacts

between farms

Human to mink (P

h-m

)

•

Low to moderate

•

Vaccination of mink may

(from 10 to 66% of

reduce the probability of

all farms)* see text

transmission to the

below the table.

individual mink, but likely

•

Quality of evidence:

not on farm level

moderate (PAFF

(susceptibility).

reports from

•

Duration of the immunity

affected

in mink is not well

countries)

described, and following,

varying effects of

vaccination are expected.

•

Regular (at least weekly)

•

Testing, symptom

testing of farm personnel,

monitoring;

•

Testing of other visitors

•

NPI e.g. FFP respirators,

before visit (exposure) (for

goggles or face shields,

both points above assuming

gowns, hand hygiene,

that a positive test is

respiratory etiquette, keeping

followed by, e.g. denied

distance, stay-at home when

access to farm)

sick

•

No entrance for positive

tested people, no entrance

for workers with SARS-CoV-

2-like symptoms or who have

had close contact with

conﬁrmed cases,

•

Limitation of access to farm,

•

Quarantine between visits to

farms (exposure)

•

Vaccination of workers could

protect against severe

outcomes of infection;

•

Training and information to

farm personnel in their own

language

The monitoring approaches listed here are examples of which approach can be taken, but are not necessarily linked with what is discussed in the Section

3.5

on monitoring revision.

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SARS-CoV-2 in animals

Transmission

Risk factors/

pathways (quantity of

exposure factors

interest)

Mink to mink (intra-farm)

•

Farms size

•

Period when young

m-m

)

animals are born

What is the proportion of

•

Immunity status of

mink that will become

animals

infected in infected mink

•

Mink density within

farms in the EU in the

the farm

next 12 months?

•

Within-farm

biosecurity and

movement

Mink to humans (P

m-h

)

Probability of

transmission (in the

absence of control

measures speciﬁc

to animals in

question)

Potential preventive and

control measures in

animals/farm (in brackets Potential preventive and

is indicated inﬂuence on

control measures in humans

probability of exposure or

susceptibility)

Possible monitoring

approaches to reduce the

probability of

transmission

•

Regular testing of mink

(exposure)

•

Vaccination (susceptibility

•

High to very high

and exposure),

(from 66 to

90%)

•

reduction of the within-

•

Quality of evidence:

farm density (exposure)

High

•

Within-farm biosecurity

•

(Field evidence,

(exposure)

several reports, see

Section

3.2)

•

Vaccination, within farm

•

Seasonality related

•

Very low to very

density and time of

high (from

10 to

to pelting, which

What is the proportion of

detection can inﬂuence

90%)

inﬂuences no. of

people entering/present

virus load on farm

•

Quality of evidence:

farm personnel*

in infected mink farms in

(exposure)

Moderate

and contacts

the EU next 12 months

between farms; an

•

Evidence on spread

that will become infected

from mink to

increased number

from mink?

humans,

of workers increase

uncertainty related

the risk.

to spread between

workers or from

mink to workers

•

Vaccination of workers could

protect against severe

outcomes of infection;

•

FFP respirators, goggles or

face shields, gowns, gloves

•

Regular testing of mink,

direct or indirect (air

samples, environmental

samples) (exposure)

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SARS-CoV-2 in animals

Transmission

Risk factors/

pathways (quantity of

exposure factors

interest)

•

Farm density

•

Distance

What proportion of

•

Low level

infected mink farms in

implementation of

the EU will generate at

biosecurity

least one secondary case

measures

through direct or indirect

farm-to-farm

transmission of SARS-

CoV-2 in the next

12 months?

Farm to farm (P

f-f

)

Probability of

transmission (in the

absence of control

measures speciﬁc

to animals in

question)

Potential preventive and

control measures in

animals/farm (in brackets Potential preventive and

is indicated inﬂuence on

control measures in humans

probability of exposure or

susceptibility)

•

Restricted access and

movement of workers,

visitors.

•

Vaccination of workers

decreases disease severity;

•

PPE such as FFP respirators,

goggles or face shields,

gowns, gloves;

•

NPI: hand and respiratory

hygiene, keeping distance,

stay at home when sick;

•

Testing, symptom

monitoring;

•

limitation of access to farm,

quarantine between visits to

farms (exposure)

Possible monitoring

approaches to reduce the

probability of

transmission

•

Regular testing of mink, test

of animals or farm

personnel, testing before

movement (exposure)

•

Moderate (from 33

•

Movement restrictions of

animals, equipment

to 66%)

between farms,

•

Quality of evidence:

quarantine, test of

Moderate (from

animals/farm before

reported outbreaks

movement (exposure)

and reports, see

•

Vaccination (exposure &

Section

3.2)

susceptibility)

Spread from farm to

general population

farm- general pop

)

What proportion of

infected mink farms in

the EU will generate

circulation (i.e. not

limited to sporadic

detections) of mink

adapted SARS-CoV-2

strains in general

population to people not

associated with mink

farms in the next

12 months?

•

Farm density

•

Distance to general

population

•

Low level

implementation of

biosecurity

measures

•

Very low (< 10%)

•

Quality of evidence:

Low (limited

information on how

many samples are

sequenced in

different countries,

making it difﬁcult to

follow the spread in

the general

population).

•

To limit access of visitors

to the farm

•

Farm biosecurity

•

Lowering virus

concentration in the air

during outbreaks e.g. by

ventilation and

interventions on the animal

side

(compartmentalisation)

•

Vaccination and acquired

immunity from previous

SARS-CoV-2 infection to

lower the risk of getting

infected and also reduce

the period of infectiousness

•

Testing, symptom monitoring

•

Regular testing of farm

personnel, testing of other

of workers;

visitors after visit (exposure)

•

Vaccination of workers

•

Genetic monitoring of viruses

decreases disease severity;

at mink farms and

•

NPI: hand and respiratory

population level

hygiene, keeping distance,

stay at home when sick;

•

Genetic monitoring of SARS-

CoV-2 to identify mink-

associated viruses to be able

to follow up and limit further

spread in the affected

population

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SARS-CoV-2 in animals

Transmission

Risk factors/

pathways (quantity of

exposure factors

interest)

•

Farm biosecurity

Mink to companion

animals /other animals at

farm

In the next 12 months,

out of the mink farms

becoming infected in the

EU what is the

proportion in which at

least one pet or other

animal of susceptible

species (including wild

animals) in the farm will

become infected (due to

transmission from the

mink), given such

animals are present on

the farms?

Probability of

transmission (in the

absence of control

measures speciﬁc

to animals in

question)

Potential preventive and

control measures in

animals/farm (in brackets Potential preventive and

is indicated inﬂuence on

control measures in humans

probability of exposure or

susceptibility)

Possible monitoring

approaches to reduce the

probability of

transmission

–

•

Fencing, automatic closure

–

•

Low to moderate

of gates/doors, closed halls

(from 10 to 66%)

vs. open sheds, restricted

•

Quality of evidence:

access for companion

Moderate (Surveys

animals (dogs/cats, etc.)

conducted during

(exposure)

epidemics in

Denmark (Boklund

et al., 2021), in the

Netherlands (van

Aart et al., 2021),

and in the USA

(Amman et al.,

2022). See also

Table

NPI: non-pharmaceutical interventions; PPE: personal protective equipment.

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SARS-CoV-2 in animals

Human to mink (P

h-m

The epidemiological situation, and in particular the level of virus activity and the respective virus

variant circulating in the general population in the area is expected to be a driving force in the

probability of transmission from humans to mink. However, despite a relatively low incidence in the

general population in 2020, the

ﬁrst

outbreaks in mink occurred, most likely caused by a mixture of

low awareness, limited testing and control measures in the early phases of the pandemic, and a

prolonged infectious pressure from infected humans to mink. In addition, introduction likely occurred

via people with asymptomatic infection during times when testing was limited or not performed.

Lower testing volumes in the general population will also add limitation to the available data about

the level of SARS-CoV-2 circulation in the population locally and beyond. This will limit the assessment

of when more stringent measures are needed on a farm to prevent virus introduction.

An increase in numbers of workers and visitors will lead to an increased probability of transmission

between humans and mink, for example as result of seasonal increase of workload, e.g. during pelting

operations.

Non-pharmaceutical intervention (NPI) measures (Section

3.5.3)

such as maintaining distance, hand

and respiratory hygiene, wearing face masks, testing and isolating positive tested people and their

contacts have been shown to effectively reduce the transmission rate between humans, and most

likely from humans to mink. However, experience shows that it is difﬁcult to ensure compliance to all

measures during full working days. Limitation of access for visitors and testing for workers and visitors

can effectively reduce the risk of virus introduction, if the time from testing to test results is short and

the sensitivity of tests is high. However, in many countries, at the time of writing this opinion, SARS-

CoV-2 is no longer considered such a threat to the population, and such that health care is

overwhelmed and would require testing, and public health measures such as wearing facemasks in

public places or indoor areas. Indeed, vaccination against SARS-CoV-2 reduced hospitalisations,

intensive care units (ICU) admissions and deaths due to SARS-CoV-2.

Vaccination in humans has shown to be a powerful tool to prevent severe and fatal disease during

the SARS-CoV-2 pandemic, reduce disease overall, lower virus load and reduce the time of infectivity in

infected people; however, vaccination cannot be considered a control measure of the viral spread e.g.

to prevent the introduction into a farm.

Explanation about estimation of probability of transmission

(low to moderate, from 10 to

66% of all farms): the assessment by the experts indicated a high uncertainty regarding the potential

number of adequate contacts between infected humans in the next 12 months, mostly due to possible

variation in the incidence of infection in humans (which will inﬂuence that of workers/visitors of mink

farms). This is expected to be the case even if human transmission to mink (i.e. an infected human

entering a mink farm) is very likely, given adequate contact (evidence is available for this as observed

in past epidemics in DK and NL).

Mink to mink (intra-farm) (P

m-m

)

Experience from outbreaks in mink shows that the virus spreads rapidly throughout the farm

(Boklund et al., 2021; Hammer et al., 2021), and from two farms, an R0 of 2.9 and a growth rate of

0.293 during a within-farm epidemic have been estimated (Chaintoutis et al., 2021). In periods with

kits (young mink), the density in farms increases, which may lead to even higher transmission rates.

However, as virus has been often detected in air within 1 m from mink and may be present up to 3 m

away, even reduced density can result in high probability of spread between mink, although likely at a

lower speed. Experimental studies on ferrets have shown a higher probability of transmission between

animals by direct contact than by airborne transmission, although airborne transmission up to 1 metre

has been described (Richard et al., 2020; Kutter et al., 2021).

Previous exposure or vaccination of mink is likely to reduce the transmission rate, but experience is

scarce and data lacking. One vaccine study with mink showed that one of three vaccinated mink

became infectious, and that vaccinated mink were PCR-positive for a shorter time period (Shuai et

al., 2021). Vaccination has been used in mink in USA and Finland. No farms have been tested positive

in Finland, neither before nor after vaccination.

Within-farm biosecurity may reduce the probability of spread between sections of a farm. However,

it is likely that introductions from workers will occur into several sections of the farm (Chaintoutis et

al., 2021), leading to a limited effect of within-farm biosecurity.

Explanation about estimation of probability of transmission (high

to very high, from 66 to

90%): While there is a large uncertainty on the proportion of mink farms becoming infected, mink

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SARS-CoV-2 in animals

can readily transmit the virus (R0

1) and thus, given the close contact between animals in mink

farms, once the infection is present in at least one animal, it is very likely that it will reach a large

proportion of the exposed mink population within farm.

Mink to humans (P

m-h

)

Evidence from previous outbreaks shows an increased incidence among mink workers (Larsen and

Paludan, 2020; Lu et al., 2021; Oude Munnink et al., 2021). Moreover, characterisation of virus

circulating in mink and farm personnel has demonstrated transmission from humans to mink as well as

from mink to humans (Hammer et al., 2021; Lu et al., 2021). The probability of transmission from

mink to humans will vary with the number of persons exposed on the farm (farm personnel, visitors

including family members) as well as applied personal protective measures. Farm size is likely to have

an effect on the virus load in the environment, leading to increased risk of transmission in large farms

depending on number of animals and in seasons with increased animal density. Testing does not

reduce the risk of infection of the individuals tested, but reduces the risk of further spread by early

detection of infection/contamination. NPIs instead reduce the risk of individual infection and of further

spread to others (depending on the NPI measure). Early detection will in theory increase the

effectiveness of PPE by reducing the exposure before detection if PPE is not worn routinely. In

practise, it can be difﬁcult to detect outbreaks early enough to have the optimal effect of additional

PPE. However, the effect will be inﬂuenced by several factors, such as animal density, transmission rate

and frequency of contact between workers/visitor and animals. Similar effects can be obtained by

measures reducing the spread between mink (P

m-m

). Monitoring infections with the purpose of early

detection is described (EFSA, 2021).

Explanation about estimation of probability of transmission (very

low to very high, from

10 to

90%): in infected mink farms, there is a large uncertainty regarding the risk for workers due

to future circulating strains, biosecurity measures, etc. Furthermore, the average proportion of people

infected from mink on an infected farm, varies with farm size and thereby with the numbers of

workers/visitors of the farm.

Farm to farm (P

f-f

)

Experience from previous outbreaks indicates that spread between farms occur and that farms size

and distance between farms is associated with the risk of occurrence (Boklund et al., 2021; Lu et

al., 2021). Direct or indirect transmission by humans is believed to be the main route of transmission

(Lu et al., 2021). However, from other contagious husbandry diseases, it is well known that the extent

of movement between farms of animals, people and equipment inﬂuence the risk of spread of disease.

Therefore, movement restrictions, limited access to farms for visitors and quarantine time between

visits for workers and visitors can reduce the probability of transmission.

Explanation about estimation of probability of transmission

(Moderate, from 33 to 66%):

multiple factors may play a role here (particularly biosecurity), but assuming possible exposure (e.g.

close distance or high farm density and/or movement of animals) the probability of transmission is

considered moderate. In some situations, where only antibodies are detected, phylogenetic analyses

are not possible, and therefore, the relations between farms can be difﬁcult to describe and, as such,

it is a source of uncertainty.

Spread to general population (P

f-society

)

Experience from Denmark showed that the SARS-CoV-2 variant related to mink spread from farm

personnel to the general population. After the

ﬁrst

three outbreaks on mink farms in June 2020, its

spread led to at least 90 people infected with this mink-related variant (Larsen et al., 2021). However,

after all mink were culled in the country, this variant was no longer found in the sequenced samples

from Denmark. In the Netherlands, three human community cases infected with a mink strain were

found (Lu et al., 2021). Furthermore, SARS-CoV-2 was not detected in air samples outside farms in the

Netherlands (de Rooij et al., 2021) or in Denmark (Boklund et al., 2021).

Explanation about estimation of probability of transmission:

(very low

10%) The

probability that mink-related strains establish in the general population can be assumed to depend on

how well adapted these viruses are for transmission between humans, and on the level and viral

ﬁtness

of other circulating strains at the time. The risk of spread to the general population can be

reduced by minimising the risk of mink outbreaks and the risk of transmitting the mink-adapted viruses

to workers at mink farms and thereby lowering the risk of transmission to the general population in

the local area of the affected mink farm and beyond. Also, interventions on the animal side, if feasible

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SARS-CoV-2 in animals

(e.g. compartmentalisation, etc.), to reduce the spread among the animal population will reduce the

risk of workers to be exposed to infected animals (and consequently to the general population) as well

as to aerosol or contaminated environment such as surfaces or dust particles in the air. Vaccination

and acquired immunity in human population from previous SARS-CoV-2 infection have shown to lower

the risk of getting infected and also reduce the period of infectiousness, which contributes to reduce

the spread to the general population, but this effect is decreasing over time and with any new variant.

Frequent testing of farm personnel and visitors on farms could be a useful monitoring approach, the

latter with the purpose of early detection.

Mink to other animals at farm (companion animals, wild, feral animals)

The probability of transmission from mink to companion animals (e.g. cats, dogs) will vary with the

number of the latter at risk on the farm and the viral load. Companion animals are considered at risk if

they have access to the farm area. Similarly, animals of susceptible species living in the surroundings

of the farm can be at risk, if they have access to the farm area (e.g. feral cats). Wild mink in

surroundings of farms in USA have tested positive, and virus was found in two escaped mink in the

Netherlands, 450 and 650 m from culled farms

(Lu et al., 2021). Furthermore, several cats (many

feral) and dogs living on infected Danish, Dutch and Utah (USA) farms have been tested positive, for

either virus or antibodies (van Aart et al., 2021; Amman et al., 2022) (Table

4).

High levels of biosecurity, efﬁcient fencing and closed farms, including automated closure of gates

and doors, can reduce the risk of companion animals as well as wildlife entering the farms, and

thereby the probability of transmission. Monitoring of wildlife and feral cats cannot reduce the

probability of transmission; however, it can help supporting information on potential spread between

species.

Explanation about estimation of probability of transmission (Low

to moderate, from 10 to

66%): Mink are likely highly infectious and effective contact with other animals in the farm is

considered likely if the latter are present. However, as few animals of other species have been tested

on infected mink farms, there is uncertainty on the probability of each susceptible animal getting

infected.

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SARS-CoV-2 in animals

3.4.2.

Companion animals

This section refers to probability of transmission between companion animals and humans. Examples are given for cats and hamsters, as these are

considered the species at highest risk, and include cats living in households having access to outdoor, stray (feral) cats (cats without owners that may often

live in colonies and roam freely), dogs and hamsters in pet shops or at breeding centre. In Figures

and

16,

the pathways of transmission are presented,

while in Tables

and

the probability of transmission (P), possible control measures and monitoring approach are shown, respectively, for cats and

hamsters.

Cats and dogs

Figure 15:

Diagram of transmission pathways of SARS-CoV-2 between dogs or cats and humans

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SARS-CoV-2 in animals

Table 8:

Transmission pathways of SARS CoV-2 for different scenarios in cats (referring to EU), probability of transmission and related preventive and

control measures

Risk factors

Potential preventive

Probability of transmission (P) and control

measures in animals

•

Not applicable

•

Low to moderate (10–66%)

•

Quality of evidence: High,

several reports and studies

indicating higher risk of

infection in cats from infected

households (Table

Reasoning:

•

Reported median prevalence of

infected cats in households with

infected humans is 20% (IQR:

8–23) with a maximum

reported prevalence of 50%

(Table

4).

•

Very low to low (< 10% to

33%)

Quality of evidence: low

Reasoning:

•

Some infected cats, in particular

those with clinical signs, can

shed high levels of virus

(Gonzales et al., 2021), which

can be sufﬁcient to infect

humans following close contact

(Sila et al., 2022; Piewbang et

al., 2022).

•

Restrict movements

of infected cat and

possibly isolate it.

Potential preventive

and control measures

in humans

Possible monitoring

approach

Pathways

Human

cat

•

Household habits

•

Number of household

In the next 12 months,

members and/or cats

out of the households with

•

Awareness of

at least one SARS-CoV-2

probability of

infected person living with

transmission to

one or more cats in the

companion animals

EU, what is the proportion

in which at least one of

the cats in the household

will become infected?

•

PPE and good hygiene

•

If investigation is

planned, target sampling

practices.

cats from infected

•

If tested positive, to

households

avoid close contact

with cats, and if

possible keep animals

outside of affected

households

•

To raise awareness to

animal owners

•

Household habits

•

Number of household

In the next 12 months,

member and/or cats

out of the cats that will

•

Awareness of

become infected with

probability of

SARS-CoV-2 in the EU,

transmission to

what is the proportion that

companion animals

will transmit the infection

•

Clinical condition and

to one or more humans in

shedding levels of

the same household?

infected cats

Cat

Human

•

PPE and good hygiene

•

If infected cat is

practices.

detected, investigate

other companion

•

Avoid close contact

with cats

animals and humans at

risk (exposed to the

cat)

Cat

cat (in same

household, shelter)

In the next 12 months,

out of SARS-CoV-2

infected cats in the EU,

what is the proportion that

•

Numbers and densities

•

Moderate

–

high (33–90%)

of cats

Quality of evidence: moderate

•

Type of contact and

Reasoning:

duration of contact

•

Transmission between cats can

be sustained; R0

1 (Gonzales

•

Not applicable

•

Isolate infected cat

•

Restrict movement of

infected cat

•

If infected cat is

detected, investigate

other companion

animals and humans at

risk (exposed to the

cat)

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SARS-CoV-2 in animals

Pathways

Risk factors

Potential preventive

Probability of transmission (P) and control

measures in animals

et al., 2021; Gerhards et

al., 2022).

Potential preventive

and control measures

in humans

Possible monitoring

approach

will transmit the infection

•

Clinical condition and

to at least one other cat in

shedding levels of

the same household or

infected cats

shelter?

Cat -> other household

•

Cats’ habits

•

Household cats with

cats, stray cats

outdoor access

In the next 12 months,

•

Frequency of contact

out of SARS-CoV-2

with other cats

infected household cats in

•

Clinical condition and

the EU, what is the

shedding levels of

proportion that will

infected cats

transmit the infection to

one or more cats that do

not live in the same

household (including stray

cats)?

•

Cats habits

Stray cat

other

•

Number of cat colonies

animals

•

Household cats

In the next 12 months,

allowed outside/street

out of SARS-CoV-2

access

infected stray cats in the

•

Frequency of contact

EU, what is the proportion

with other animals

that will transmit the

•

Clinical condition and

infection to one or more

shedding levels of

‘non-stray’

cats or other

infected cats

animals?

Very Low to low (< 10–33%)

Reasoning:

Transmission between cats can be

sustained (Gonzales et al., 2021;

Gerhards et al., 2022), however,

the duration and intensity of the

contact between cats inﬂuences

the transmission.

Quality of evidence: low

•

Restrict movement of

•

Not applicable

household cat, when

infected

•

Not applicable

Very low to low (< 10–33%)

Reasoning:

The duration and intensity of the

contact between a cat and another

animal inﬂuences the transmission

probability.

Quality of evidence: low

•

Not applicable

•

Not applicable

Other cats here means cats living in households having access to outdoor, and stray cats are those without owners that may live in colonies.

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Figure 16:

Diagram of transmission pathways of SARS-CoV-2 between hamsters

and humans

It could apply also for cat or dog or other susceptible animals in a pet shop or breeding center.

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SARS-CoV-2 in animals

Hamsters

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SARS-CoV-2 in animals

Table 9:

Transmission pathways of SARS CoV-2 for different scenarios in hamsters (referring to EU), probability of transmission and related preventive

and control measures

Risk factors/periods/

areas

Potential

preventive and

control measures

in animals

•

Not available/

applicable

Possible

Potential preventive

and control measures monitoring

in humans

approach

•

Investigation in

•

Testing

pet shop workers

•

PPE and good hygiene

or breeders

practices

•

Avoid direct contact if

infected.

Pathways

Human

hamster

Probability of transmission (P)

•

Close contact with pet

•

very low to low (< 10–33%)

•

Contamination of cage

Reasoning:

In the next 12 months, what

equipment (Port et

proportion of hamsters in

al., 2021)

•

Hamsters are highly susceptible to

pet shops in the EU

will be

•

No PPE or good hygiene

SARS-CoV-2 (Yen et al., 2022)

infected with SARS-CoV-2

practices when handling

Quality of evidence: low to moderate,

due to contact with infected

animals or equipment

there is only one publication describing

people?

natural infection of hamsters (Yen et

al.). Hamsters however are used

frequently as animal models for SARS-

CoV-2 and high susceptibility to infection

has been demonstrated by numerous

publications.

•

Group size per cage

Hamster

hamster

•

High (> 90%)

•

Density of hamsters

Reasoning:

In the next 12 months, out

•

Hygiene measures

of SARS-CoV-2 infected

between cages

•

Transmission of SARS-CoV-2 can take

hamsters in the EU, what is

place via contact, aerosol, fomites

the proportion that will

and air (Port et al., 2021)

transmit the infection to at

•

Quality of evidence: high, there is a

least one other hamster?

plethora of publications

demonstrating transmission of SARS-

CoV-2 between hamsters

–

by direct

contact or via fomites or air/aerosol.

Hamster

human

In the next 12 months, out

of SARS-CoV-2 infected

hamsters in the EU, what is

the proportion that will

•

Reduce group size

•

PPE and good hygiene

•

Not applicable

in cages.

practices.

•

Reduce hamster

density/increase

distance between

cages

•

Use

ﬁlter-top

cages

•

Limit movement of

animals with

clinical signs and/

or quarantine after

movement

•

Close contact with pet

•

Use

ﬁlter-top

cages

•

PPE and good hygiene

•

Monitor pet shop

Low (10–33%)

workers or

•

No PPE or good hygiene

Reasoning:

practices.

breeders

practices when handling

•

If animals tested

Hamsters shed high levels of virus.

animals

positive wearing PPE

•

Limit direct contact.

Quality of evidence:

low to moderate,

because there is only one publication

describing the transmission of SARS-

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SARS-CoV-2 in animals

Pathways

transmit the infection to one

or more humans?

Risk factors/periods/

areas

Probability of transmission (P)

CoV-2 from hamsters to humans (Yen et

al.). Considering that hamsters shed

high levels of virus, which can be

detected in the air, and that virus

transmits rapidly among hamsters, high

amounts of infectious virus can be

reached in situations where several

hamsters are kept.

Potential

preventive and

control measures

in animals

Possible

Potential preventive

and control measures monitoring

approach

in humans

3.4.3.

Wild animals

and

18,

the pathways of transmission are presented.

or as captive in game reserves) found positive at a

and the related table. However, the assessment and

susceptibility to infection and potential for sustained

This section refers to probability of transmission between wild animals and humans. In Figures

The white-tailed deer is until now the only wildlife species in North America (either as free ranging

signiﬁcant prevalence. Therefore, only white-tailed deer is indicated in the

ﬁgure

(indicated as

deer)

considerations done for white-tailed deer might be extrapolated to other wildlife species with a high

infectivity if identiﬁed in the future (Table

10).

Figure 17:

Diagram of transmission pathways of SARS-CoV-2 between white-tailed deer (or other wildlife species with high susceptibility to infection and

potential for sustained infectivity) and humans

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SARS-CoV-2 in animals

Table 10:

Transmission pathways of SARS CoV-2 for different scenarios in white-tailed deer (WTD), probability of transmission and related preventive

and control measures

Risk factors/periods/

areas

•

Hunting season (e.g.

contaminated baiting,

feeding)

•

Outdoor activity

•

Occupational exposure

(e.g. forest workers,

deer farmers)

•

Proximity to urban

settings (wastewater,

rubbish)

•

Epidemiological

situation (level of

infection) in general

population

P of transmission

Very low to low,

10%–33%

Possible

monitoring

approach

Potential preventive

and control measures

in/for animals

Potential preventive

and control measures

in humans

Possible transmission

pathways

Human

deer

In the next 12 months,

what

proportion of the WTD in the EU

will get infected with SARS-CoV-2

due to contact with infected

people?

To set up

integrated

quality of evidence: moderate

monitoring of

(Palmer et al., 2021; Vandegrift

relevant species

et al., 2022)

(Cardoso et

al., 2021)

•

Good hunting practices

•

Testing and symptom

monitoring

(avoid feeding or

•

PPE for close contact

baiting)

(e.g. face masks)

•

Safe disposal of

•

No contact with live

garbage and use of

wild animals for people

animal-proof containers

with symptoms

•

Wastewater

management

•

Avoid unnecessary

contact in general.

•

Vaccination of people

in contact with live

animals

Reasoning to support estimation of P of transmission: several variants circulating among humans spilled over to deer, although no case in EU, the majority of white-tailed

deer WTD in the EU are in Finland, where the circulation of SARS-CoV-2 has been among the lowest in the EU all through the pandemic. Nevertheless, this could be linked

to the diversity of hosts and the limited and generally non-systematic sampling.

Deer

deer

Not applicable

•

Population density

•

Avoid aggregation of

•

Monitoring

•

Low to high, 33–99%;

•

Mating season

susceptible animals at

group sizes and

•

quality of evidence:

In the next 12 months, out of

•

Epidemiological

focal points such as

contact rates

moderate for WTD (Hale et

SARS-CoV-2 infected WTD in the

situation (level of

feeding sites (Gortazar

al., 2021; Kotwa et

EU, what is the proportion that will

infection) in general

et al., 2015)

al., 2022), but very limited

transmit the infection to one or

population

•

To avoid situations of

evidence for European wild

WTD?

overabundance of

ruminants

susceptible wildlife

•

Reasoning: there is clear

maintenance of infection in

WTD populations in North

America

Deer

humans

In the next 12 months, out of

SARS-CoV-2 infected WTD in the

EU, what is the proportion that will

•

Hunting season

•

Hunting practices and

carcass handling

•

Outdoor activity

•

Very low,

10%

•

quality of evidence:

moderate

•

Reasoning: a report of

SARS-CoV-2 WTD-adapted

•

Testing of found

•

same as above

pathway, human to

dead animals, or

deer

shot/road kill

animals

•

PPE when managing

fresh carcasses

•

Hand hygiene

•

Testing

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SARS-CoV-2 in animals

Possible transmission

pathways

transmit the infection to one or

more humans?

Risk factors/periods/

areas

•

Population density of

deer

•

Closer/more frequent

contacts in protected

or urban areas

•

Epidemiological

situation (level of

infection) in general

population

P of transmission

lineage with epidemiological

link to a human case may

support the hypothesis of

deer to human transmission

(Pickering et al., 2022b)

Possible

monitoring

approach

•

Integrated

monitoring

Potential preventive

and control measures

in/for animals

Potential preventive

and control measures

in humans

•

Vaccination of people

in contact with live

animals (hunters,

visitors, etc.)

3.4.4.

Zoo animals

This section refers to probability of transmission between zoo animals and humans. In Figure

18,

the pathways of transmission are presented (Table

11).

Figure 18:

Diagram of transmission pathways of SARS-CoV-2 between zoo animals and humans

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SARS-CoV-2 in animals

Table 11:

Transmission pathways of SARS-CoV-2 for different scenarios in the EU in zoo animals (e.g. great apes, felines), probability of transmission

and related preventive and control measures

Risk factors

Probability of

transmission (P)

Very low to low, 10–33%

Quality of evidence:

moderate

Reasoning:

few case

reports available, although

susceptible species present

in zoos has not been

regularly tested for contact

with SARS-CoV-2.

Potential preventive and

control measures in

animals

•

Reduce probability of

contact between persons

and animals

•

increase distance from

workers to animals

Potential preventive

and control measures

in humans

Possible monitoring

approach

Pathways

Human

animals

•

Zoo workers, training/

handling of zoo animals

In the next 12 months,

•

Ventilation (e.g. closed

what is the proportion of

buildings for carnivores or

zoos in the EU with

primates, and aerosols)

susceptible animal species

•

visitors do not usually

in which at least one animal

have close contact with

will become infected with

susceptible zoo animals

SARS-CoV-2 due to contact

like felines or great apes,

with infected people?

so do not represent a

major risk.

•

Regular testing of

•

Testing

people in contact with

•

‘Stay

at home’ when

susceptible animals

sick or tested positive

(animal keepers and

•

Good hygiene practice

personnel, mainly). If

by zoo personnel

needed, non-invasive

•

Vaccination of workers

monitoring of animals

decreases disease

could be done by air

severity;

sampling or rope-based

•

PPE for people (zoo

oral

ﬂuid

sampling

workers, visitors), in

contact with

susceptible animals

•

Ensure sufﬁcient

distance

•

Good hygiene practice

by zoo personnel

•

Testing of susceptible

animals with clinical

signs

Animal

animal (same

species, same

enclosure)

In the next 12 months,

SARS-CoV-2 infected zoo

animals in the EU, what is

the proportion that transmit

the virus to at least one

more zoo animal in the

same enclosure?

•

Density of susceptible

animals in enclosure

Moderate, 33–66%

Quality of evidence:

moderate

Reasoning:

case reports

available, close contact

between animals, although

difﬁcult to be proven,

because the animals

belonging to the same

outbreak were usually

exposed to the same

infectious source (e.g.

positive caretaker

(EAZWV, 2022)).

•

Isolation/quarantine of

susceptible animals with

clinical signs

•

Reduction of contact

between animals

A non-invasive sampling method consisting of a cotton rope, often with a bait, that is hung and let chewed by animals, out of which oral

ﬂuid

can be collected and tested.

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SARS-CoV-2 in animals

Pathways

Animal

animal (in

other enclosures)

Risk factors

Probability of

transmission (P)

Very low

10%

Potential preventive and

control measures in

animals

Potential preventive

and control measures

in humans

Possible monitoring

approach

•

Testing of susceptible

animals with clinical

signs

•

Screening of exposure

to SARS-CoV-2

•

Isolation/quarantine of

•

Good hygiene practice

susceptible animals with

by zoo personnel

Quality of evidence:

clinical signs

moderate

•

Disinfection/hygiene of

tools used with animals

Reasoning:

no conﬁrmed

•

Avoid different enclosures

cases, low chance of

sharing the same surface

transmission, difﬁcult to

water and same

conﬁrm, whether spread

ventilation system

between enclosures, or

multiple introduction. For

infection maintenance, zoo

populations are usually too

small

•

Zoo workers, training/

•

Reduce probability of

•

Good hygiene practice

Very low

10%

Animal

human

handling of zoo animals

contact between persons

by zoo personnel

Quality of evidence:

In the next 12 months, out

•

Ventilation (e.g. closed

and animals

high

of SARS-CoV-2 infected zoo

buildings for carnivores or

animals in the EU, what is

primates, and aerosols)

Reasoning:

no reported

the proportion that will

cases

transmit the infection to

one or more humans?

•

Good hygiene practice by

zoo personnel

•

Ventilation in shared

In the next 12 months, out

buildings

of SARS-CoV-2 infected zoo

•

Shared surface water

animals in the EU, what is

•

Shared feeders and other

the proportion that will

equipment

transmit the infection to at

•

Indirect contact through

least one other zoo animal

wildlife

in another enclosure in the

same zoo?

•

Good hygiene practice

by zoo personnel

•

Vaccination of workers

decreases disease

severity;

•

PPE for people (zoo

workers, veterinarian),

in contact with infected

animals

•

Ensure sufﬁcient

distance

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SARS-CoV-2 in animals

3.5.

3.5.1.

Risk for human health posed by SARS-CoV-2 infection in animal

species and preventive measures

Overview of variant viruses in humans by cases over time

On 30 January 2020, the World Health Organization (WHO) declared that the outbreak of

COVID-19 constitutes a Public Health Emergency of International Concern (PHEIC). On 11 March

2020, the Director-General of WHO declared the COVID-19 outbreak a pandemic. As of 4

December 2022, 179 million COVID-19 cases and 1.18 million COVID-19-related deaths have been

reported from EU/EEA countries. The last Rapid Risk Assessment by ECDC was published 27

January 2022 (ECDC, 2022a).

Different SARS-CoV-2 variants have emerged over the course of the pandemic, and variants of

concern (VOC) which have been dominant in the EU/EEA countries are shown in Figure

below by

number of human cases. The emergence and circulation of VOC clades of the Ancestral (pre-Alpha),

Alpha, Beta, Delta, Gamma and Omicron variants with sublineage (BA.1–BA.5) clades are indicated in

Figure

19.

Information on variants that ECDC is currently monitoring is available on a dedicated

webpage,

together with a timeline about the Omicron variant emergence.

The proportion of the circulating variant viruses was estimated from the SARS-CoV-2 sequences submitted to

GISAID EpiCov database based on the collection date of the submissions. The average proportions of variants

were plotted for the EU/EEA countries. Omicron variants are depicted based on its sublineages (BA.1–BA.5) in

the

ﬁgure,

‘other’

indicates the lineages that are other than Alpha, Beta, Gamma, Delta and Omicron. In the pre-

Alpha period,

‘other’

includes ancestral lineages belonging to nextclade A and B clades whereas now during

Omicron circulation,

‘other’

includes recombinants and unassigned lineages.

Figure 19:

Number of weekly conﬁrmed COVID-19 cases reported from EU/EEA countries

3.5.2.

Measures to prevent and control infection or spread of SARS-CoV-2 at the

animal–human interface: monitoring

3.5.2.1. SARS-CoV-2 surveillance in people

Information from comprehensive testing of SARS-CoV-2 was used to monitor the circulation in the

general population during the

ﬁrst

2 years of the COVID-19 pandemic. With countries moving into

more routine monitoring approaches of SARS-CoV-2, also surveillance systems are being adapted and

combined with other respiratory viruses.

These integrated respiratory virus surveillance systems should be able to monitor the spread and

intensity of SARS-CoV-2 transmission to guide control measures and mitigate the impact of COVID-19.

Integrated surveillance systems for respiratory viruses should also monitor the possible emergence of

https://www.ecdc.europa.eu/en/covid-19/variants-concern

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new variants as well as other relevant events. Countries are encouraged to integrate SARS-CoV-2 into

existing surveillance frameworks, such as those for inﬂuenza, where representative sentinel

surveillance systems in primary and secondary care are already established and remain the central

surveillance method for acute respiratory infections. These sentinel systems rely on common syndromic

case deﬁnitions that combine epidemiological data and virological testing that can cover multiple

respiratory viruses such as inﬂuenza, COVID-19, and potentially other respiratory virus infections.

Indicators of severity such as hospitalisations, admissions to ICU and mortality are key parameters for

risk assessments and public health decision as well as assess the impact of vaccination in the

population over time (ECDC/WHO, 2022b).

With the shift from comprehensive testing to sentinel surveillance, data on SARS-CoV-2 circulation

in the population, particularly at local or regional level, might be limited, impacting also the

assessment about the risk for animal settings through available data. Over the course of the COVID-19

pandemic, different other parameters such as hospital or ICU admissions, outbreaks in long-term care

or health-care facilities might be other parameters that have been used for situational assessments

instead of the reported incidence in the populations. These parameters focus on severity and burden

on health care and not on the overall circulation in the population. These parameters, however, are

delayed indicators of the actual virus circulation in the population.

3.5.2.2. Genomic surveillance

Genomic monitoring is a key part of SARS-CoV-2 surveillance with the objective to monitor

circulation, evolution and dominance of known and emerging variant viruses in the population,

describe key mutations and relevant sites during evolutionary processes, inform vaccine composition

decisions or outbreak analyses, and identify new emerging SARS-CoV-2 variant viruses early. This

should also include the analysis of viruses from animal sources and their relation to viruses circulating

in humans in a One Health approach. Genetic surveillance needs to be integrated into the national

surveillance strategies for respiratory viruses.

Whole genome sequencing (WGS), or at least complete or partial spike (S)-gene sequencing, is the

best method for characterising a speciﬁc variant. Alternative methods, such as diagnostic screening

nucleic acid ampliﬁcation technique (NAAT)-based assays, have been developed for early detection and

pre-screening to allow prevalence calculation of variants of concern (VOC), variants of interest (VOI)

and variants under monitoring (VUM). Many of these methods can accurately identify the different

variants, while others will require conﬁrmation by sequencing of at least the complete or partial S-gene

genomic region in a subset of samples.

Timely sharing of SARS-CoV-2 consensus sequences is crucial. Sequences should be deposited in

the Global Initiative on Sharing All Inﬂuenza Data (GISAID) database, or other public databases.

Related sequencing raw data should be deposited in the European Nucleotide Archive (ENA) and raw

data, if available (ECDC/WHO, 2022a).

3.5.2.3. Wastewater surveillance

Wastewater monitoring is a tool to monitor the overall situation of SARS-CoV-2 in the population

without speciﬁc testing of individuals and has been useful to identify upsurges of infections. Viruses

from wastewater surveillance can be sequenced to identify the currently circulating variant but also to

identify new or emerging viruses. The European Commission adopted a recommendation asking EU

MSs to establish wastewater monitoring to track COVID-19 and its variants.

The Joint Research

Centre (JRC) coordinates this network on wastewater surveillance with the aim to build on the EU

capacities to detect future threats and trends arising from emerging pathogens and pollutants of

emerging concern for public health. At the time of writing this document, wastewater or sewage

testing for SARS-CoV-2 has been implemented in 1370 wastewater plants across the EU for the

monitoring of the activity levels in a community and has shown promising results with timely data as

well as the identiﬁcation of new and emerging variants in the population.

Variant monitoring through WGS can also be applied in wastewater, sewage or environmental

samples but requires specialised bioinformatic analyses. The value of this surveillance covers also the

One Health area (ECDC/WHO, 2022a).

https://ec.europa.eu/environment/pdf/water/recommendation_covid19_monitoring_wastewaters.pdf

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3.5.2.4. Testing

For the testing, different commercial detection assays for SARS-CoV-2 RNA or antigen, and

serological assays for SARS-CoV-2 speciﬁc antibodies are available on the market with CE-IVD (in

vitro

diagnostic device) marking. More information on CE-IVD-marked COVID-19 rapid antigen tests can be

found in ECDC’s technical report (ECDC, 2021). Information on these assays can be found in the test

directory of the Foundation for Innovative New Diagnostics (FIND) and in the JRC COVID-19

In Vitro

Diagnostic Devices and Test Methods Database

of the European Commission. The characteristic

amino acid substitutions of variants can be found in ECDC’s updated list of variants of concern (VOC),

variants of Interest (VOI) and variants under monitoring (VUM).

The speciﬁc tests currently recommended by the WHO for the diagnosis and conﬁrmation of SARS-

CoV-2 are described at WHO webpages.

Testing strategies of symptomatic or people exposed to infected contacts have been successfully

applied over the course of the pandemic to identify SARS-CoV-2-infected people and prevent further

transmission through the implementation of public health measures like isolation at home. Population-

based testing strategies have been recently revised in several EU/EEA countries with a focused

approach on targeted testing of patients with respiratory illness in secondary health care or selected

other groups e.g. risk groups in long-term care facilities or health-care workers. Different occupational

settings are also part of a more risk based or targeted testing approach.

Testing at the workplace needs to be embedded in the occupational safety and health management

approach. There are different legal frameworks and requirements in the different EU/EEA countries

concerning testing in the workplace and many countries have lifted the requirements for testing at

occupational settings. When testing strategies are designed and implemented at enterprise level,

workers (or their representatives) should be consulted and clearly informed, in a language, they can

understand, about the procedures set out in the enterprise.

The use of rapid antigen detection tests (RADTs) and/or self-test RADTs in occupational settings

can complement, but not replace, occupational safety and health measures including existing non-

pharmaceutical interventions aimed at preventing the introduction and spread of SARS-CoV-2 (ECDC/

EUOSHA, 2021).

Measures to prevent and control infection or spread of SARS-CoV-2 at the animal–human interface

–

non-pharmaceutical interventions (NPI)

Non-pharmaceutical interventions (NPI) are public health measures that aim to prevent and/or

control transmission of communicable diseases such as respiratory virus infections e.g. SARS-CoV-2 in

the community. NPIs are more effective to reduce transmission than vaccination, while COVID-19

vaccination is clearly the most effective measure to reduce the health impact. NPIs have played a

critical role in reducing transmission rates and the impact of COVID-19 in the EU/EEA. NPIs will

continue to be one public health tool against COVID-19, however, based on the national situation,

countries have lifted requirements following the SARS-CoV-2 vaccine roll-out that prevents those

vaccinated from severe disease and avert deaths in the population.

Most important NPIs relevant for the animal–human interface are detailed below.

3.5.2.5. Hygiene measure

Coughing and sneezing hygiene, frequent washing of hands with soap and water for at least 20 s,

or applying hand hygiene solutions, such as alcohol-based hand rub or gels are recommended in all

settings and are simple measures to reduce the spread and exposure.

3.5.2.6. Keeping distance

Keeping physical distance (e.g. 1–2 m) to other people or animals likely infected with SARS-CoV-2

as well as avoiding physical contact reduce the risk to spread the infection or get infected. This is also

applicable for occupational environments and contact between farm/shop/zoo personnel and visitors as

well as animals takes place. However, some working duties might not be possible without contact to

animals.

https://covid-19-diagnostics.jrc.ec.europa.eu/

https://www.who.int/publications/i/item/diagnostic-testing-for-sars-cov-2

https://www.ecdc.europa.eu/en/covid-19/prevention-and-control/non-pharmaceutical-interventions

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3.5.2.7. Personal protective equipment (PPE)

Personal protective equipment (PPE) prevents from contact, droplet and airborne transmission of

pathogens but also provides protection from physical harm and other hazards. PPE includes respiratory

protection e.g.

ﬁltering

facepiece (FFP) respirators, goggles or face shields for eye, gowns for body

and gloves for hand protection. PPE need to be available and worn appropriately according to the

situation and risk. PPE might be different based on situation and needs, e.g. for a mink farm worker, a

ranger or a veterinarian. Also, the recommended PPE may differ in regular working situations,

compared to situations where SARS-CoV-2 has been conﬁrmed at an establishment and its personnel

has to continue working on the premises to feed and take care of the animals (ECDC, 2020b).

3.5.2.8. Face masks

Coronaviruses are transmitted primarily from person to person via respiratory droplets, either by

being inhaled or deposited on mucosal surfaces, including aerosols produced when coughing and

speaking. A public health policy for wearing a face mask in public spaces should be considered in areas

with community transmission when the public health objective is to limit community transmission

(ECDC, 2022b).

FFP respirators should be worn by all people in contact to SARS-CoV-2 positive tested animals at

the workplace.

People tested positive for SARS-CoV-2 could also consider limiting the contact and wearing a face

mask when in close contact to companion animals in the household to limit the spread of the infection

to the respective animal.

3.5.2.9. Ventilation

Based on evidence from several SARS-CoV-2 outbreak investigations that transmission also occurs

in closed, poorly ventilated spaces, even without close proximity to the source, improved ventilation

minimises the role of aerosols in transmission of SARS-CoV-2. This could be considered in occupational

settings, especially in closed animal facilities such as pet shops and other indoor facilities where

animals are kept in close distance and where SARS-CoV-2 outbreaks would lead to high virus presence

in the environment including air (ECDC, 2020c, 2022b).

3.5.2.10. Stay-at-home/isolation

In general, people are advised to stay at home when feeling sick or having COVID-19-like

respiratory symptoms. Countries have lifted the requirement of COVID-19 positive tested people to

isolate at home for a particular period of time until the infectivity is considered low. However, in special

circumstances, it might be requested for people to self-isolate after a positive test to avoid either the

introduction into a farm, e.g. when a new SARS-CoV-2 variant circulates in the population, or to avoid

spread of new variants to the general population, if the infection was likely acquired at the work place

through close contact with animals.

3.5.3.

Measures to prevent and control infection or spread of SARS-CoV-2 at the

animal–human interface

–

vaccination of humans as protective and control

measure

National authorities in the EU make

ﬁnal

decisions on the roll-out of vaccines, including booster doses

and type of vaccines, considering factors such as the spread of infection, the impact of COVID-19 in

different populations and the emergence of new variants. These elements will determine which vaccines

people receive and when, based on their level of risk and the epidemiological situation.

The latest ECDC report on vaccination strategies and deployment plans in the EU/EEA countries is

available.

Some countries have particular recommendations for occupational settings related to

nursing home staff, healthcare and social–health personnel but not related to groups working at the

animal–human interface. The report also details the respective vaccines and timing of vaccinations.

Currently recommendations for booster doses are usually targeted to risk group and the elderly

https://www.ecdc.europa.eu/en/publications-data/overview-implementation-covid-19-vaccination-strategies-and-deployment-

plans

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population to prevent severe disease and deaths in a population at risk, see also ECDC and EMA joint

statement.

Detailed and up-to-date information on the vaccine rollout and country-speciﬁc

disclaimers on the data may be found in the ECDC Vaccine Tracker.

As of December 2022, eight COVID-19 vaccines have received conditional marketing authorisation

in the EU/EEA, following evaluation by the European Medicines Agency (EMA), and are part of the EU

Coronavirus Vaccines Strategy Portfolio including most recently authorised adapted COVID-19 vaccines

including the bivalent original/Omicron BA.1 and the bivalent original/BA.4–5.

Safe and effective COVID-19 vaccines are a powerful tool for ensuring public health and controlling

the pandemic. Results from observational studies carried out to date have shown that the vaccines

authorised in the EU/EEA are highly protective against severe COVID-19, hospitalisation and death.

Overall, vaccines against COVID-19 have shown to substantially lower the risk of severe disease

and death and to lower the risk of infection and symptomatic illness. In addition, the risk of exposure

is lowered due to a shorter infectious period and lower virus titres in vaccinated people. Vaccination

and natural immunity from exposure to the circulating virus has increased the level of protection

across the population in many countries across the EU/EEA. However, the emergence of different

SARS-CoV-2 variants with different antigenic properties over the course of the pandemic has impacted

the effectiveness of available vaccines. In addition, waning immunity has also contributed to declining

protection over time.

With newly available adapted vaccines and newly emerging immune-evasive variants, vaccines are

still the measure of choice to prevent severe disease and reduce somewhat risk of infection but are

not a measure that alone can grant full control of the spread of SARS-CoV-2. This is also true for

possibly antigenically modiﬁed SARS-CoV-2 viruses that originate from animal sources.

Published literature indicates that vaccine effectiveness (VE) against severe outcomes caused by

Omicron remains high, including among older age groups, with continuous strong protection generally

at around 80–90% about 2–3 months after receiving the

ﬁrst

booster. Results of studies with a follow-

up period of 3–6 months after the

ﬁrst

booster dose are heterogenous, but generally show a gradual

decrease in effectiveness against severe COVID-19 outcomes (VE estimates in the range of 53–100%).

The available studies indicate that a

ﬁrst

booster dose provides strong protection against severe

disease in all the investigated age groups, and there are no clear signs of a more rapid waning in

elderly groups.

VE following a second booster dose against severe disease remains high during the short follow-up

period covered in the studies available so far and appears to restore the slightly reduced protection

seen 4 months after the

ﬁrst

booster dose. Depending on the speciﬁc outcome and study, protection is

in the range of 40–77% when compared to the third dose (incremental or relative VE) and in the

range of 66–86%, when compared to the unvaccinated. Recent analysis of VE from the UK shows

some waning of protection following a fourth dose.

This analysis estimated VE against the Omicron

variant for several sub-lineages (BA.1, BA.2, BA.4 and BA.5) and found that VE against hospitalisation

was enhanced by a fourth dose and the incremental VE after 2–4 weeks was 58.6%. This incremental

VE decreased to 19.2% at 15 or more weeks after receiving the fourth dose.

In summary, studies conducted during the period when the Omicron subvariants BA.1 and BA.2

were dominant have found that VE against infection with the Omicron variant wanes over time,

starting from around 2–3 months after completing the primary series. Similarly, the effectiveness

against documented infection wanes after the administration of a

ﬁrst

mRNA vaccine booster dose,

from estimates within the range of 45–66% in the

ﬁrst

3 months to around 25–45% between 3 and

6 months after the booster dose. A second booster improves VE against infection, but this seems to

wane rapidly, as seen within the short follow-up period available so far after the second booster dose.

Studies suggest that booster doses in general have a modest effect and limited duration in

preventing Omicron transmission in the population.

Duration of immunity is a complex issue and, to date, the correlation between measured immunity

(e.g. levels of antibodies) and clinical protection from SARS-CoV-2 infection has yet to be established.

The presence of memory T cells could prevent severe disease in infected individuals for a long period

https://www.ecdc.europa.eu/en/news-events/covid-19-recommendations-use-adapted-vaccines

https://vaccinetracker.ecdc.europa.eu/public/extensions/COVID-19/vaccine-tracker.html#uptake-tab

https://www.ema.europa.eu/en/human-regulatory/overview/public-health-threats/coronavirus-disease-covid-19/treatments-

vaccines/vaccines-covid-19/covid-19-vaccines-authorised#authorised-covid-19-vaccines-section

https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/ﬁle/1101870/vaccine-surveillance-

report-week-35.pdf

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of time, although the durability of these cells and role in protecting from infection (and onward

transmission) remains unclear.

Recent studies from the UK, Denmark and South Africa have not found a big difference in VE

against different outcomes, including against severe disease, between sublineages BA.1/BA.2

compared with BA.4/BA.5. However, some other studies have found that protection following third or

fourth doses against severe outcomes was lower for BA.5 compared to BA.1/BA.2 (Collie et al., 2022;

Davies et al., 2022; Hansen et al., 2022; Kirsebom et al., 2022; Kislaya et al., 2022).

A recent analysis from the UK found that, overall, there was no evidence of reduced VE against

hospitalisation for the Omicron sublineage BA.4.6 as compared to other BA.4 or BA.5 sublineages.

Real-world evidence is essential to measure the impact that the new Omicron-adapted bivalent

vaccines have in preventing infection and disease, since the approval of these adapted vaccines was

based on studies collecting data related to safety and immunogenicity. The

ﬁrst

VE estimates following

vaccination with mRNA bivalent BA.4/BA.5 vaccines against infection have recently been published

from the USA (Link-Gelles, 2022). This study shows that bivalent boosters provided additional

protection against symptomatic infection in individuals who had previously received 2, 3 or 4

monovalent vaccine doses. They found that for 18- to 49-year-olds, the bivalent vaccines were 42%

effective against infection, for 50- to 64-year-olds, 28% effective against infection and for those over

65 years, the bivalent vaccine was 22% effective against infection (see also other topic page on

COVID-19 vaccination by ECDC).

33,34,35

Vaccine effectiveness against transmission of the Omicron variant

One study from the UK, that compared VE against transmission of Omicron and Delta variants after

vaccination, found a protective effect in contacts (adjusted risk ratio (aRR) 0.88, 95% CI: 0.79–0.97,

p = 0.0129) or index cases (aRR 0.78 (95% CI: 0.69–0.88)) having received three doses (compared to

two doses) in household settings (Allen et al., 2022). In non-household settings, a protective effect

was observed for contacts having received three doses compared to two doses (0.76 (95% CI: 0.61–

0.94)), but there was no evidence of differences in protection based on the number of doses received

by those exposing the contacts (Allen et al., 2022). This protective effect of a

ﬁrst

booster dose was

less pronounced for Omicron compared to Delta. Data from a Danish household study showed a

secondary attack rate (SAR) of 31% related to Omicron and 21% for the Delta variant (Lyngse

et al., 2021). For unvaccinated household members SAR secondary attack rates of 29% and 28% were

observed for Omicron and Delta, respectively, while the SAR were 32% (Omicron) and 19% (Delta) for

fully vaccinated, respectively. For booster-vaccinated individuals, Omicron was associated with a SAR

was 25% for Omicron and 11% for Delta, while the corresponding estimate for Delta was only 11%,

thus indicating that Omicron is generally 2.7–3.7 times more infectious than the Delta among

vaccinated individuals (Lyngse et al., 2021). The secondary attack rate in a household study conducted

in Norway for Omicron was estimated at 51% (95% CI: 48–54) compared to 36% (95% CI: 33–40)

with Delta giving a signiﬁcantly higher risk of infection in households with Omicron relative to Delta

(Jalali et al., 2022). Generally, the SAR in households with booster vaccinated primary cases and

contacts was lower than in households with unvaccinated primary cases and contacts, however

primary cases who were booster vaccinated were found to have a considerably higher risk (RR: 4.34;

95% CI: 1.52–25.16) of transmitting SARS-CoV-2 to their household contacts with Omicron compared

to Delta (Jalali et al., 2022). Moreover, booster vaccinated primary cases with Delta have 80% lower

risk of Delta transmission (RR: 0.18; 95% CI: 0.01–0.70) relative to the unvaccinated primary cases

(Jalali et al., 2022).

A study using the epidemiologic data from the SARS-CoV-2 surveillance within the California state

prison system found that vaccination and prior infection were each associated with comparable

reductions in infectiousness during SARS-CoV-2 infection and additional doses of vaccination against

SARS-CoV-2 and more recent vaccination led to greater reductions in infectiousness (Tan et al., 2023).

https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/ﬁle/1115385/Vaccine_surveillance_

report___week-44.pdf

https://www.ecdc.europa.eu/en/publications-data/preliminary-public-health-considerations-covid-19-vaccination-strategies-

second

https://www.ecdc.europa.eu/en/covid-19/latest-evidence/vaccines

https://www.ecdc.europa.eu/en/covid-19/prevention-and-control/vaccines

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Protection against infections in vaccinated people by the different variants (data for the

different variants)

The data from a systematic review and meta-analysis of 18 peer-reviewed studies has shown that

the pooled mean vaccine effectiveness for all vaccines and ages against symptomatic COVID-19 was

87% (95% CI: 86–87%) with variation based on vaccine type; for mRNA-1,273 and BNT162b2, VE

were 92% (95% CI: 88–96%) and 85% (95% CI: 85–86%), respectively (Ssentongo et al., 2022).

Mean vaccine effectiveness (VE) declined over time and reached 94% (95% CI: 93–94%), 78% (95%

CI, 55–100%) and 64% (95% CI: 24–100%) 1, 3 and 4 months after vaccination (Ssentongo et al.,

2022). Pooled results from another meta-analysis demonstrated a 71% (OR = 0.3, 95% CI: 0.2–0.5)

reduction in SARS-CoV-2 infection rates among subjects who received a booster shot compared with

those who did not receive a booster shot of COVID-19 vaccine (Zhu et al., 2022).

A large meta-analysis has shown that the VE of full vaccination against any infection and

symptomatic infection with the Alpha variant was 88.0% (95% CI: 83.0–91.5) (Zeng et al., 2022). In a

multicentre cohort study, VE against SARS-CoV-2 infection with the Alpha variant was estimated at

70% 21 days or more following the

ﬁrst

dose and 85% 7 days or more after the second dose of

BNT162b2 vaccination, respectively (Hall et al., 2021). In another study during the predominance of

both Alpha (B.1.1.7) and Beta (B.1.351), vaccine effectiveness (VE) of BNT162b2 was estimated at

90% for Alpha infection and 75% for Beta infection (Abu-Raddad et al., 2021).

The effectiveness of vaccination against symptomatic disease after vaccination with one dose was

notably lower among persons with the Delta variant (30.7%; 95% CI: 25.2–35.7) than among those

with the Alpha variant (48.7%; 95% CI: 45.5–51.7) (Bernal et al., 2021). In a case–control study, the

effectiveness of two doses of BNT162b2 was 94% against B.1.1.7 and 88% against Delta (B.1.617.2)

(Bernal et al., 2021). A meta-analysis, involving

~17.2

million people of whom 61.1% fully vaccinated

with two doses of COVID-19 vaccines demonstrated that vaccines signiﬁcantly lower the risk of

exposure (RR = 0.2, 95% CI: 0.1–0.5) against the Delta variant among the fully vaccinated population

by 80% compared to the unvaccinated population (Mahumud et al., 2022). Overall, the effectiveness

of COVID-19 vaccines against the Delta variant was 86% (RR = 0.1, 95% CI: 0.1–0.5) (Mahumud et

al., 2022). During the dominance period of the Delta variant, the booster-vaccinated subjects

demonstrated a signiﬁcant reduction in infection rates compared with non-booster-vaccinated subjects

(Zhu et al., 2022).

During the period of dominance of the Omicron variant, the pooled results of studies with a total

sample of around one hundred million participants showed that full vaccination signiﬁcantly lowered

the risk of infection (odds ratio (OR) = 0.6, 95% CI: 0.6–0.7) against the Omicron variant (Zou et

al., 2022). Additionally, the results indicated that a two-dose vaccination plus booster signiﬁcantly

lowered the risk of infection (OR = 0.4, 95% CI: 0.4–0.5) against the Omicron variant compared to

the unvaccinated group (Zou et al., 2022). The pooling of these same studies also showed that the

standard two-dose vaccination plus a booster signiﬁcantly lowered the risk of infection (OR = 0.6, 95%

CI: 0.5–0.7) against the Omicron variant compared to the two-dose vaccination without booster (Zou

et al., 2022). Another meta-analysis demonstrated that booster-vaccinated subjects displayed a 47%

reduction in infection rates compared with those who did not receive the booster vaccine (OR = 0.5,

95% CI: 0.4–0.8).

€

Bjork et al. (2022) showed that the VE for the Omicron subvariants BA.1 and BA.2, after at least

three doses remained above 80%, however, the VE after two doses declined substantially from 90%

(95% CI: 78–95) during Omicron BA.1 dominance to 54% (95% CI: 13–75) during BA.2 dominance.

Furthermore, there was a marked decline in protection against severe COVID-19 during the Omicron

€

BA.2 dominance among persons with two vaccine doses only (Bjork et al., 2022). A vaccine

effectiveness study has shown that among those who received two doses of any vaccine, VE against

symptomatic disease was 64% (95% CI: 59–68%) and 67% (95% CI: 54–76%) for BA.1 and BA.2,

respectively, within the

ﬁrst

2 weeks of receiving the second dose (Kirsebom et al., 2022). The

numbers drop to 17% (95% CI: 15–19%) and 24% (95% CI: 20–28%) after 25 or more weeks for

BA.1 and BA.2, respectively. Additionally, among those who received any booster dose following

immunisation with a primary course of any vaccine, VE increased to 71% (70–73%) and 72% (67–

77%) for BA.1 and BA.2 respectively, after a week. Over time, this waned to 46% (95% CI: 44–47%)

and 48% (95% CI: 45–51%), respectively, at 15 or more weeks after receiving the booster dose

(Kirsebom et al., 2022). A different VE study demonstrated that the effectiveness of a three-dose

(booster) vaccination with BNT162b2 for BA.1 was 60% (95% CI: 53–65%), while the VE for BA.2 was

52% (95% CI: 48–56%) (Altarawneh et al., 2022). A recently published study, investigating the VE of

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four vs. three doses of mRNA-based vaccines reported a VE estimate of 47% (95% CI: 44–47) against

Omicron infection at 12 or more days after the fourth dose (Bar-On et al., 2022).

Full vaccination with the currently available vaccines provides a statistically signiﬁcant protection

against the Omicron variant (OR = 0.6, 95% CI: 0.6–0.7) within a period of time, but it is not as

effective as it was against the Delta variant (RR = 0.15, 95% CI: 0.1–0.3) (Mahumud et al., 2022).

The booster provides additional protection against Omicron (OR = 0.4, 95% CI: 0.4–0.5); however, it

is also less effective compared to the reported protection effectiveness against Delta (OR = 0.065,

95% CI: 0.06–0.07) (Accorsi et al., 2022). Additionally, those who received the two-dose vaccination

plus booster were also reported to have fewer hospitalisations and lower disease severity compared to

the unvaccinated population (Lauring et al., 2022). The new bivalent vaccines have been shown to

induce an increase in neutralisation of the B.1.1.529 Omicron variant (Regev-Yochay et al., 2022).

A living systematic review is being carried out on the efﬁcacy, effectiveness and safety of COVID-19

vaccines that are currently, or soon to be, authorised in the EU/EEA.

The aim of the review is to

provide a living, continuously updated overview on the evidence by speciﬁc vaccine product, age

groups and SARS-CoV-2 variants. Overall, COVID-19 vaccines continue to provide a high level of

protection against severe outcomes of SARS-CoV-2 but lower and relatively fast-waning protection

against infection by the virus. Effectiveness of newer vaccines against infection is still under

investigation. The virus continuously evolves and new variants or sub-lineages with immunity-evading

€

properties may emerge at any time (Kulper-Schiek et al., 2022).

If vaccinated people are infected, can they still transmit the virus? How does this differ

between vaccinated and non-vaccinated? How is this related to the different variants?

Overall, COVID-19 vaccines, due to the new immune escape variants, have not shown to be

anymore an effective tool at individual level to prevent infection and onward transmission of the virus

although the COVID-19 vaccines, still maintain high effectiveness against severe disease.

The results from a cohort study have demonstrated that even though the initial genomic viral load

between vaccinated and unvaccinated individuals was similar, fully vaccinated individuals had a shorter

duration of viable viral shedding and a lower secondary attack rate than partially vaccinated or

unvaccinated individuals (Jung et al., 2022). This implies that COVID-19 vaccinations lead to a more

rapid virus clearance, thus shortening the infectious period.

Household studies have shown that vaccination reduced onward transmission of the Alpha variant

from infected and previously vaccinated people (Harris et al., 2021; Layan et al., 2022; Prunas et

al., 2022; Salo et al., 2022). Another study showed transmission of the Alpha variant was 68% (95%

CI: 52–79) lower from SARS-CoV-2 infected index person 2 weeks after the second vaccination with

BNT162b2 than from unvaccinated index patients (Eyre et al., 2022).

Although viral loads were similar in vaccinated and unvaccinated people infected with the Delta

variant (Brown et al., 2021), the duration of viral shedding may have been shorter for vaccinated (Chia

et al., 2022). This was also shown in another study where 2 weeks after the second BNT162b2

vaccination, transmission of the Delta variant was reduced by 50% (95% Cl: 35–61) and by 24%

(95% CI: 20–28) after 12 weeks (Eyre et al., 2022).

In a study conducted in Switzerland from April 2020 to February 2022, it was shown that full

vaccination signiﬁcantly reduced infectious viral load in Delta breakthrough infection cases compared to

unvaccinated individuals (Puhach et al., 2022). Fully vaccinated individuals with Delta variant infection

had a faster mean rate of viral load decline than did unvaccinated individuals with pre-Alpha, Alpha or

Delta variant infections (Singanayagam et al., 2022).

Vaccine-associated reductions in onward transmission of the Alpha and Delta variants declined over

time after the second vaccination in index patients (Eyre et al., 2022).

For Omicron, an increased transmission rate for unvaccinated individuals and a reduced

transmission for booster-vaccinated individuals was observed, compared to fully vaccinated individuals.

These

ﬁndings

show that vaccinated individuals, particularly those recently having received a booster

dose, do not transmit the virus to the same extent as unvaccinated individuals (Lyngse et al., 2021).

For Omicron BA.1 breakthrough infections in patients with completed primary course vaccination

resulted in signiﬁcantly lower infectious viral loads (Puhach et al., 2022). Moreover, a signiﬁcantly lower

infectious viral load was observed for booster-vaccinated individuals compared to fully vaccinated

subjects (Puhach et al., 2022). Similarly, for infections occurring 7–30 days after the booster

vaccination, a more than sixfold reduction in viral load was noted; however, this booster-associated

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viral-load reducing effectiveness rapidly declined for breakthrough infections occurring 31–60 and 61–

120 days after the booster shot, respectively (Levine-Tiefenbrun et al., 2022).

How long are vaccinated vs. non-vaccinated able to transmit the virus or at least have

detectable virus (period of infectiousness) also by variant?

Duration of infectiousness and peak viral load may differ among virus variants. Even though viral

load is a common proxy for infectiousness, a correlation between viral loads and infectiousness is not

fully established (Owusu et al., 2021).

One study found that the duration of virus shedding (median) was shorter in vaccinated compared

to unvaccinated participants, but this was only effective from day six of the infection (Garcia-Knight

et al., 2022). Overall, the study identiﬁed a more rapid decrease of the viral RNA level and a shorter

detection of infectious virus in fully vaccinated compared to unvaccinated (Garcia-Knight et al., 2022).

Even though full vaccination may be inefﬁcient at reducing infectiousness during the early phase of the

infection, it likely leads to a reduction in the duration of infectiousness (Accorsi et al., 2022; Garcia-

Knight et al., 2022; Singanayagam et al., 2022).

For people infected with the Delta variant similar levels of genome copy numbers were detected in

vaccinated compared to unvaccinated during the

ﬁrst

3 days of infection but after this period, the

detected genome copy numbers declined faster in vaccinated patients (Puhach et al., 2022) In

contrast, infectious virus levels for Delta were substantially lower in vaccinated patients at all days

after symptom onset with the biggest effect at days 3–5 and 5 days after onset of symptoms

infectious virus was detectable in 54% vaccinated and 85% unvaccinated patients, indicating a shorter

period of infectiousness for vaccinated individuals (Puhach et al., 2022).

Bouton et al. (2022) found that the median time for Omicron culture conversion was 2 days for

boosted participants with Omicron, 3 days for vaccinated, unboosted participants with Omicron, and

3 days for participants with Delta. Moreover, only 17% of their study cohort failed to culture-convert

by day six and no major differences in culture conversion or viral load decay between the Delta and

Omicron variants were found. These results are consistent with previous data that showed no major

differences in Omicron infection duration when compared with Delta (Hay et al., 2022). A different

study observed that the median time from initial positive PCR assay to culture conversion was 4 days

in the Delta virus group and 5 days in the Omicron group, whereas the median time from symptom

onset to culture conversion was 6 and 8 days, respectively, for Delta and Omicron (Boucau et al.,

2022).

Immunity in the population acquired over time through vaccination and natural infection with SARS-

CoV-2 is described at ECDC pages.

3.5.4.

Treatment and pharmaceutical prophylaxis of COVID-19

Different medicinal products have been studied to assess their safety and efﬁcacy as potential

agents for pharmaceutical prophylaxis or treatment of COVID-19. These include corticosteroids,

immunomodulatory agents, monoclonal antibodies, antivirals, COVID-19 convalescent plasma and

other therapeutic agents.

Some antiviral monoclonal antibodies (bamlanivimab/etesevimab,

casirivimab/imdevimab) have been studied for post-exposure prophylaxis (PEP) but none has been

recommended so far due to low effectiveness against Omicron.

3.5.5.

Risk assessment

This assessment is based on information available to ECDC at the time of publication and, unless

otherwise stated, the assessment of risk refers to the risk that existed at the time of writing. It follows

the ECDC rapid risk assessment methodology, with relevant adaptations (ECDC, 2019). The overall risk

for public health was determined by a combination of the probability of transmission, taking into

consideration the assessment presented in Section

3.4,

and its consequences (impact of the disease)

for individuals or the population (ECDC, 2019). Limitations have been described in the previous rapid

risk assessment and EFSA document on mink (EFSA, 2021).

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Which detailed threats to humans exist related to SARS-CoV-2 in animals?

SARS-CoV-2 has the ability to transmit between humans, but also transmit from humans to

animals, between animals and from animals back to humans. Not all animal species are susceptible to

be infected or can spread the virus back to humans. The relevant animal species that may play a role

in SARS-CoV-2 epidemiology are discussed in Sections

3.1–3.4

and in the following section.

1) SARS-CoV-2 can adapt in animals and undergo evolutionary processes that result in viral

characteristics that may have a public health impact; however, this has not been observed

so far (Tan et al., 2022). These animal species-speciﬁc mutations might be located in similar

but also different genome sites compared to humans. Mink-speciﬁc mutations have been

described with characteristic amino acid changes not observed in humans before,

establishing a

‘ﬁnger-print’

in SARS-CoV-2 viruses, which could be traced in humans

following animal exposure and infection with mink-speciﬁc viruses.

2) Another threat is related to the creation of a reservoir in animals where for instance slightly

different animal-adapted SARS-CoV-2 viruses could co-circulate while being related to the

SARS-CoV-2 viruses circulating in the human population at the same time.

a) However, a SARS-CoV-2 variant virus could also circulate among the animal population

over a longer period that does not or very little relate to the respective virus variant in

the human population. Such variants in animals would also undergo evolutionary

mechanisms in the animal host, which could lead to infecting a more na

€

human

ıve

population with the evolved variants and reintroduction into the general population. This

could equally have an impact on vaccine effectiveness, disease severity and viral

transmission.

3) Spill-over of SARS-CoV-2 from one animal species to another species could introduce

different evolutionary and species-related mutations and processes that could lead to viruses

with altered genetic and antigenic proﬁle, as described in point 2. However, to consider

continuous animal-to-animal transmission, a large susceptible population might be needed

to maintain the infection over a longer time period time.

4) A speciﬁc susceptible species may be an intermediate host/vector in the transmission

process but not represent a reservoir.

How does SARS-CoV-2 in animals represents a threat for individual people/speciﬁc

exposed groups and the general public?

SARS-CoV-2 infected animals do pose a threat to those people in direct unprotected contact with

them. This threat could be related to single individuals of the populations, e.g. in a household, or to

speciﬁc occupationally exposed groups in the animal sector (e.g. mink farm personnel, rangers,

veterinarians, zoo or pet shop workers, etc.). Not only a single person but also a larger group of

people could be considered occupationally exposed to the animal species identiﬁed as a source of

potential transmission (see below and in Section

3.5.5).

A wider spread of animal-related viruses can occur when viruses transmitted to those primarily

exposed are further transmitted to local contacts, and then they are transferred to a wider group

reaching the general population causing the replacement of the circulating variant with an animal-

derived SARS-CoV-2 virus.

Therefore, the risk for the individual and general population will be discussed separately in the risk

assessment part.

How is the probability of transmitting SARS-CoV-2 from infected animals to individual

people/speciﬁc exposed groups and the general public evaluated?

The probability of humans to get infected with animal-derived SARS-CoV-2 is dependent of the

speciﬁc animal species to which the person is exposed, the level and intensity of exposure, as well as

the likelihood of the animal to get infected and to become infectious. As outlined in Section

3.4,

not

every animal species is susceptible and can transmit the virus to the same or another species. In

addition, the level of infectiousness (correlated with virus load) as well its duration in the animal

species determines the probability of infection.

The likelihood of exposure is dependent of the setting (e.g. workplace, household, zoo, wildlife,

etc.), level, and quality of exposure, which is determined by the kind and level of protection of the

human, the number and frequency of exposure events over time, as well as the duration of exposure.

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Long repeated unprotected exposure of people (e.g. mink farm personnel activity over longer periods

of time) increases the probability to be exposed to infected animals and acquire the infection.

How is SARS-CoV-2 in animals transmitted to humans?

Transmission pathways from animals to humans and vice versa as well as between animals likely

occur similarly to the identiﬁed routes between people, e.g. through droplets or aerosol in close

proximity to infected animals as well as through contaminated hands, surfaces or other materials and

the environment. Aerosol sampling around cages of infected mink showed that virus particles were

detectable up to 3 m away.

Which animal species are more likely to pose a threat for a human and for public health in

relation to SARS-CoV-2?

Farmed animals:

Among farmed animals in the EU, farmed mink are the most likely to get infected and transmit

SARS-CoV-2 among the animal population and onwards to humans. Transmission events within these

populations as well as between farm personnel and the animals and back have been observed over

the course of the COVID-19 pandemic. In addition, species-related evolution of

‘older’

SARS-CoV-2

variants that are not anymore circulating in the general human population has been observed, e.g. in

Latvia.

No sequence data from SARS-CoV-2 infected raccoon dogs has been provided to GISAID EpiCoV

database indicating possibly very limited infections in this animal species and raccoon dogs would not

be considered a risk species based on these data.

For other farmed animals screened by the literature review (Sections

3.1

and

3.2)

such as cattle

and pigs, the evidence that these species can be infected is limited, no further transmission has been

described including to humans and very few sequences have been reported. Therefore, they are not

an animal species that represents a public health risk.

Risk assessment for individual people/groups and general public:

Mink farms have restricted access and are conﬁned in speciﬁc areas or regions that minimise the

possibility of exposure to potentially infected mink for individuals not associated with the mink farm.

The risk for a person without or with limited exposure to farmed mink based on the probability to get

infected and develop severe disease from farmed animals is estimated to be none to very low.

Transmission events from farmed mink to humans as well as humans to farmed mink concern directly

exposed individuals with unprotected close contact with the animal or with the environment within a farm

in the presence of ongoing virus circulation. Exposed individuals are part of different occupational groups

working at the premises such as farm owners, veterinarians, workers or seasonal workers involved in,

e.g. culling or pelting activities. The risk for an occupationally exposed individual of this deﬁned group to

get infected when in unprotected contact to an infected farmed mink (highest probability to be infected)

and impact of this infection (probability to develop severe disease) is estimated to be low-to-moderate

dependent and subjected to uncertainty in relation to the respective virus variant, the effectiveness of

the vaccine for this variant in vaccinated people including the time period after the vaccination, previous

exposure to other SARS-CoV-2 variants and the health status of the individual (i.e. presence of comorbid

conditions). The use of PPE and other measures can reduce the risk.

Mink-related variants transmission from farmed mink to occupationally exposed groups and further

spread to the local and even general population have been observed in 2020 and 2021 before the

implementation of measures in mink farms. Transmission events from humans to mink and vice versa

have been reported only sporadically in 2022. The risk of the spread of a virus variant with mink-

speciﬁc mutations or of the re-introduction of an older variant virus that circulated in minks into the

general population causing severe disease is estimated to be very low-to-low. This is, however,

dependent on the implemented measures at farm level, the follow-up of exposed people, the

respective virus variant, the effectiveness of the vaccine for this variant (in those vaccinated) and the

previous exposure to other SARS-CoV-2 variants.

Companion animals:

Among companion animals, hamsters, cats and ferrets are considered the most probable to get

infected as well as transmit the virus to the same species, to other animal species and to humans.

Since the emergence of the Omicron variant, also mice and rats have been identiﬁed to get infected

and possibly be able to further spread the virus. Dogs are able to get infected but do not transmit the

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virus further very consistently indicating a lower risk associated with this species. An outbreak involving

humans and forming a larger cluster among companion animals has only been observed in a pet shop

setting with hamsters in Hong Kong (Kok et al., 2022). Limited clustering and sporadic transmission to

humans has been observed for companion animals overall has been reported with viruses lacking

species-speciﬁc separate evolution.

The assessment is based on experimental evidence, observational studies as well as available

sequence data.

Risk assessment for individual people/groups and general public:

Cats represent the species with the highest number of animals living in close contact to humans

across all EU/EEA MSs and have the highest contact frequency with humans. As displayed in

Section

3.4.2,

the contact between different cats can occur between those living in the same

household, with other family cats in the neighbourhood as well as to stray cats when having outdoor

access and to other cats in holiday shelters. This contact pattern, including to humans, is unlikely to be

sufﬁcient to result in a long or even permanent circulation of the virus or to establish a virus reservoir.

The probability of cats to get infected is dependent on humans in the same household being

infected and transmitting the virus to the cat (see Section

3.4.2).

In a household, an infected person is the main source of infection both for other persons as well as

for companion animals, due to similar and more timely exposure.

The probability for a human to get infected from a cat with outdoor access that got infected from

another cat outside the household is very low. This probability is higher (very low-to-low) for

occupationally exposed groups with higher number of close contacts to different cats from different

households such as veterinarians. The related disease severity is estimated to be equal to the situation

in human-to-human transmission.

Similarly, the risk is estimated to be very low for non-occupationally exposed individuals in close

contact with hamsters and higher (very low-to-low) for groups occupationally exposed to hamsters.

The probability of companion animals to have an impact on the virus circulation in the general

population is none to-very low although smaller outbreaks related to hamsters have been observed

outside the EU; the related disease severity is estimated to be equal to the situation in human-to-

human transmission and therefore the overall risk (determined by the probability and severity) is

considered very low.

Zoo and wild animals:

Of animals kept in zoos, primates (apes) as well as feline species have been identiﬁed to be

susceptible and to transmit the virus to other animals.

In wildlife, carnivores such as foxes, skunks, raccoon dogs, etc., have been found infected but so

far there is no evidence that the virus was transmitted among the same species, to other species or to

humans. Wild carnivores are mostly solitary living animals, which limits the circulation and spread of

SARS-CoV-2 among a wild carnivore population of, e.g. wild mink, ferrets or foxes (EFSA, 2021).

A different situation has been reported for white-tailed deer in the USA and Canada, which has

been shown to have become a possible reservoir species with longer circulation among deer herds and

is also able to potentially transmit the virus back to humans (Pickering et al., 2022b). Species-speciﬁc

virus evolution has been observed in white-tailed deer. However, white-tailed deer might not play a

major role in establishing a reservoir in Europe as there is a much smaller local population compared

to North America.

Rodents, such as wild synanthropic mice and rats in urban settings, are widespread susceptible

species, often living in colonies close or even inside human settlements. The virus could spread in

these populations over a longer period, thus species-speciﬁc mutations could emerge and potentially

represent a public health risk. However, such a scenario has not been observed so far, also with limited

sequence data reported from those populations, and the evidence for this is limited at the moment.

Bats are a classical animal reservoir for coronaviruses and are also susceptible to SARS-CoV-2.

However, very little is known about the possible role of European bats in the emergence of potential

zoonotic viruses. Bats of the family

Rhinolophidae

were identiﬁed in the previous EFSA report as of

possible concern (EFSA, 2021) since SARS-CoV-related Betacoronaviruses were identiﬁed in

Rhinolophus ferrumequinum.

Bats of the

Rhinolophidae

family, from which SARS-CoV-2

(betacoronavirus) is thought to have originated, are present in central and southern Europe.

Risk assessment for individual people/speciﬁc groups and general public:

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The probability for an individual person to get infected from an animal in a zoo or from an animal

in the wilderness is considered to be none to very low and the disease severity associated with such

an infection estimated to be similar to the one observed among the human population. The risk is

therefore estimated to be none to very low.

The probability for occupationally or activity-related exposed people or groups such as zoo workers,

hunters, rangers or forest workers to be in contact with infected animals or their droppings and get

infected might be slightly higher with a similar level of disease severity as for viruses circulating in the

general human population. The risk is therefore estimated to be very low.

The probability to have an emerging virus from zoo or wild animals circulating in the general

population in the EU/EEA is considered none to very low. The associated disease severity is expected

to be comparable to viruses circulating among the general human population. The overall risk is

estimated to be none to very low.

Wild carnivores do not represent a public health risk also due to limited human exposure and lack

of continuous circulation in such wildlife populations.

Transmission of SARS-CoV-2 or other coronaviruses from bats to humans and backwards has not

been observed in Europe. The probability of transmission from bats to humans or the emergence of

SARS-CoV-2-related or new coronaviruses has been assessed as none to very low for the time period

of the next 12 months according to the description in previous sections. This assessment is based also

on the limited human population having direct contact with these animals. However, since bats are

natural host of many coronaviruses, the monitoring of these species is still important.

Table

shows the assessment of public health risk for different animal categories and species, for

individuals, occupationally exposed and general population.

Table 12:

Overview of assessment of public health risk for different animal categories and species,

for individuals, occupationally exposed and general population

Risk for an

individual

None to very low

Very low

None to very low

Risk for occupationally Risk for general

exposed

population

Low to moderate

very low to low

Very low

Very low to low

none to very low

None to very low

Category and animal species

Farmed animals (mink)

Companion animals (Cat, hamster,

mouse, rat and ferret)

Wildlife (White-tailed deer, bats)

Zoo animals

3.6.

Revision of monitoring strategies

In this section, the monitoring approaches for SARS-Cov-2 in animals are discussed for different

categories of animals to be targeted, in the light of the changing and evolving epidemiological situation

and new control measures for both animal and public health. As baseline, the current legislative

requirements are presented, as well as the information about monitoring plans of SARS-CoV-2 in

farmed mink in place in MSs, which is reported Section

3.2.1.1.

3.6.1.

Current legislative requirements of monitoring SARS-CoV-2 in mustelids

and raccoon dogs

The current legislation in force for the monitoring and reporting of infections with SARS-CoV-2 in

animals is the Commission Decision 788/2021. The target species are mink (Neogale

vison

and other

animals belonging to the family

Mustelidae)

and raccoon dogs, because these species are susceptible

to SARS-CoV-2 infection and often farmed in large numbers, thus potentially supporting the

transmission of infection in the farms at high rates and probability of variant emergence. In addition,

although the introduction of the infection into the farms is usually caused by infected farm personnel,

the transmission of the SARS-CoV-2 virus back to humans (by American mink) has been observed

(Oude Munnink et al., 2021). The sampling scheme is applied in establishments with more than 500

adult breeders at the beginning of the cycle and it is summarised in Table

13.

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Table 13:

Sampling scheme alternatives as foreseen by EC Decision 788/2021

Default scheme

1st alternative

scheme

2nd alternative scheme

Prerequisites

–

Favourable outcome of Risk assessment + risk mitigating

a risk assessment + risk measures + testing employees

mitigating measures

–

Detection of

Increased mortality

SARS-CoV-2 in

compared to the

baseline mortality rate employees

or animals with clinical

signs related to SARS-

CoV-2

Only dead and sick animals from each

epidemiological unit

Events triggering

–

sampling

Sampling

population

Dead and sick animals

from each

epidemiological unit. If

no dead or sick animals

> >

randomly from live

animals to reach the

expected sample size.

Weekly

Oropharyngeal swabs

from live or dead

animals

Detection of SARS-CoV-

2 virus genome.

5% prevalence with

95% conﬁdence.

Dead and sick animals

from each

epidemiological unit. If

no dead or sick animals

> >

randomly from live

animals to reach the

expected sample size.

Every 2 weeks

Sampling

frequency

Sample matrix

Following

‘events’

as above

Oropharyngeal swabs or Oropharyngeal swabs from live or dead

expiration air

animals

Detection of SARS-CoV-

2 virus genome.

20% prevalence with

95% conﬁdence.

Detection of SARS-CoV-2 virus

genome.

50% prevalence with

5% prevalence

95% conﬁdence.

with 95%

conﬁdence.

Diagnostic test

Design

prevalence

Estimated

amount of

samples required

(e.g. in a 5,000

mink farm)

3.6.2.

Animal categories and monitoring approach

The general aim of SARS-CoV-2 monitoring is to provide relevant information for planning and

implementing appropriate preventive and control measures for preserving public and animal health.

However, the changes of the epidemiological situation of SARS-CoV-2 at global and EU levels have

led the countries to modify the objectives and the approaches followed for the monitoring of SARS-

CoV-2 infection in humans. The reduction of mortality and severe disease in the human population due

to COVID-19 following the implementation of the COVID-19 vaccination led to the relaxation of public

health and social control measures as well as a modiﬁed overall testing strategy in the countries with

decreasing testing intensity for the early detection of the infection in the general population.

Nevertheless, genomic surveillance of the emergence of new variants of the virus remains a relevant

objective, especially in relation to the possible emergence of variants more capable of escaping the

immune response induced by the vaccines. The World Health Organization (WHO) together with the

Food and Agriculture Organization of the United Nations (FAO) and the World Organisation for Animal

Health (WOAH) have recently raised concern about the risk of the establishment of animal reservoirs

and virus evolution in novel hosts, potentially leading to the emergence of new SARS-CoV-2 variants

(WHO-FAO-WOAH, 2022).

In this context, the information coming from monitoring programs in animal populations can

support the assessment of risks of SARS-CoV-2 transmission from animals to humans, with particular

regard to the possible selection and emergence of new variants in animal populations, for which

humans might be more susceptible or available vaccines less effective.

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However, it must be highlighted that humans currently represent the main population maintaining the

circulation of SARS-CoV-2 virus, and that the introduction of the virus into animal populations is caused in

almost all cases by infected people. Spillback of infection, from animals to humans, has been identiﬁed

only in farmed minks, white-tailed deer and hamsters (Oude Munnink et al., 2020; Yen et al., 2022).

Therefore, considering the different purposes and opportunities of human exposure, the four animal

categories considered in this opinion (farmed animals, companion animals, wild animals and zoo animals)

will be considered separately.

In particular, based on the results of the assessment of susceptible species and their ability of

transmitting SARS-CoV-2 (Sections

3.1

and

3.2),

the following species are considered in each animal

category:

•

farmed animals: minks, raccoon dogs;

companion animals: cats, hamsters, ferrets;

wild animals: white-tailed deer and other susceptible wildlife including carnivores and bats;

zoo animals: wild

Felidae,

great apes.

Concerning the main possible objectives of monitoring programmes of SARS-CoV-2 infection in

animals, the four objectives already reported in a previous EFSA report (EFSA, 2021) have been

considered (early detection of SARS-CoV-2, measuring exposure to SARS-CoV-2, conﬁrmation of SARS-

CoV-2 infection in suspected animals, monitoring virus evolution). The monitoring scenarios are

reported in Table

14.

As explained in Section

3.6.2.1

below, the objective of early detection being no

longer considered relevant according to the current epidemiological situation, but kept in the table for

comparison.

Table 14:

Monitoring scenarios for animal categories and monitoring objective

Measuring

Conﬁrmation of

Early detection

exposure to SARS- SARS-CoV-2 infection

of SARS-CoV-2

CoV-2

in suspected animals

Farmed animals (minks,

raccoon dogs)

Companion animals

(household cats, hamsters,

ferrets)

Stray cats

Wild animals

Zoo animals

Monitoring

virus

evolution

3.6.2.1. Farmed animals

In the EU context, this category includes mainly mink and other

Mustelidae

and carnivores (e.g. sable,

raccoon dogs, farmed for fur production). The current legislation is aiming at the early detection of the

infection in farmed animals, especially in establishments with a high number of individuals, to quickly

apply all measures needed to halt the transmission and prevent potential risk for humans in the

establishments. Given the current epidemiological situation of SARS-CoV-2 in the EU, this objective has

lost its original importance. In fact, from 44 outbreaks reported in 2021 in the whole EU, in 2022 only six

were reported (Section

3.2.1).

This improvement may be linked to several factors, among those the

general reduced population of mink in the EU, and the measures in place to prevent the virus introduction

into farms through farm personnel, like the application of a repeated testing regime of workers, use of

PPE and possibly vaccination of farm personnel. On the other hand, the genomic surveillance of viruses

circulating in this category of animals is still important, given the possibility of selection and emergence of

new genetic variants of the virus, especially in farms with a large number of animals.

Likewise, the conﬁrmation of SARS-CoV-2 infection in suspected animals remains a potentially

relevant objective, in order to allow the farmers to apply some preventive measures (quarantine,

targeted culling, vaccination, etc.) in the effort to reduce the virus circulation within the farm and

prevent health consequences for the animals kept.

For the above-reported reasons, a surveillance approach following the 2nd alternative scheme

foreseen in the Commission Decision 788/2021, based on the investigation of dead animals or animals

showing clinical signs compatible with SARS-CoV-2 infection, with sampling triggered by increased

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mortality (compared to the baseline mortality rate) or morbidity in mink, or farm personnel testing

positive, would be the most appropriate for conﬁrming the infection in the farms and monitoring the

virus evolution.

In case of conﬁrmation of infection in farm personnel or other persons in close contact with the

animals, and in the absence of observable clinical signs in the animals, a random sample of individuals

should be tested with the purpose to detect the infection, assuming a 20% prevalence (with 95%

conﬁdence). Considering the time needed to establish the infection in 20% of subjects, it could be

preferable to wait for or to repeat sampling after 8–10 days (according to the epidemic model reported

in the previous EFSA report (EFSA et al., 2021)), according to the presumable time of exposure of the

worker, in order to have a higher chance to detect the infection in the animals, if present. However, in

case the veterinary authorities intend to reduce the time for the veriﬁcation of the health status of the

animals and, therefore, the impact of the disease, a larger sample of individuals should be tested,

considering the expected prevalence in the farm in relation to the most probable time of virus

introduction, in line with the epidemic model reported in the previous EFSA report (EFSA, 2021).

Simultaneous testing of workers (rapid test or PCR) would improve the sensitivity and detect infected

workers, especially if no PPE, in particular face masks or FFP respirators, are worn in the premises.

National veterinary authorities might also voluntarily consider to periodically assess the situation in

the farms, following a more active monitoring scheme. In this situation, sampling during pelting can be

a reasonable approach to reduce logistic difﬁculties and sampling costs. Serological assays and PCR

tests can be used for assessing the level of exposure and infection, respectively, of the farmed mink

population.

In any case, regardless of the type of objective, a representative sample of PCR-positive samples

should be subjected to genomic characterisation through genome sequencing in order to ensure a

proper surveillance on the circulating genetic variants of the virus. If many positive animals are

detected and the sequencing capacity is limited, a subset should be selected, at least to represent

each positive farm or epidemiological unit. Samples metadata (e.g. epidemiological link, spatial data,

temporal information) should be collected, also to properly select the samples to be sequenced and

allow comparative analysis.

3.6.2.2. Companion animals

Companion animals (dogs, cats and ferrets) may be infected by SARS-CoV-2 virus when in close

contact with infected people. Cats may also develop clinical signs (see Section

3.1).

Concerning the

possibility of back transmission to humans, two reports from Thailand singled out this possibility

(Piewbang et al., 2022; Sila et al., 2022).

It must be assumed, therefore, that infected companion animals in households may coexist with

infected owners. In this circumstance, testing the animals in the household, especially those showing

severe clinical signs, may be relevant to conﬁrm the SARS-CoV-2 infection and, if needed, to apply

proper therapy.

In any case, when cats coexist with infected persons in the same household, the outdoor access of

these animals should be limited and possibly avoided to reduce any possible risk of further

transmission. In addition, genome sequencing on positive samples taken from these animals may be

useful, especially when the sequences were not obtained from the owner’s samples or in case other

epidemiological circumstances (e.g. unusual clinical picture observed) may suggest a more in-depth

characterisation of the virus involved.

Concerning the possible circulation and persistence of the SARS-CoV-2 virus in stray cat and stray

dog communities, available literature reports contrasting results. According to some published surveys,

serological evidence of SARS-CoV-2 infection was detected in stray cat and stray dog populations in

Spain, and northern Italy (Farnia et al., 2020; Spada et al., 2021; Villanueva-Saz et al., 2021b),

whereas other surveys in Italy in stray cats failed to

ﬁnd

any evidence of virus circulation (Stranieri

et al., 2022). Surveys in feral cats frequenting infected mink farms in Denmark, the Netherlands and

Utah (Boklund et al., 2021; van Aart et al., 2021, Amman et al., 2022) or with access to hospital’s

waste in Iran (Farnia et al., 2020) have reported a seroprevalence ranging from 17.7% to 64.3%.

Amman et al. (2022) used trackers to follow the roaming activity of cats frequenting infected mink

farms in Utah and observed that these cats would freely move between farms and the surrounding

residential properties. To date, it is rather difﬁcult to evaluate the importance of these studies in

relation to the possibility of circulation of virus and its persistence in stray cat communities. More

research studies on the possible persistence of the infection in stray animal communities should be

performed to better clarify the possible role of these populations in the maintenance and evolution of

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the virus. However, apart from research objectives, testing of individual animals in stray communities

could be justiﬁed when suspected SARS-CoV-2 clinical cases or abnormal mortality rates possibly due

to infectious diseases are observed.

3.6.2.3. Wild animals

The wild animal species that may be considered as possible targets for SARS-CoV-2 monitoring are

white-tailed deer, as well as other susceptible wildlife, including carnivores, bats and rodents such as

wild synanthropic mice and rats (those living in or close to human settlements).

Given the low number of white-tailed deer in the EU (Finland and Czech Republic), compared to

USA and Canada, it is unknown whether white-tailed deer under the European conditions may be able

to sustain the persistence of SARS-CoV-2 infection and circulation (in terms of ecology, population

density, likelihood of exposure by contacts with humans, etc.), as it seems possible in North America.

Therefore, no speciﬁc regulated monitoring activities, apart from testing hunter-harvested showing

signs related to SARS CoV2 infection or dead-found individual animals, would be needed for white-

tailed deer populations.

Monitoring based on suspicion can be conducted in other wildlife species, including found dead

individuals (especially carnivores) and animals showing respiratory signs suggesting possible SARS-

CoV-2 infection. Further research studies might be relevant to monitor the possible introduction and

persistence of the virus into the white-tailed deer population in Europe, as well as in other potential

susceptible European deer species, in particular roe deer and red deer. A similar approach can be

followed for wild

Mustelidae

and wild canids (e.g. fox that has been found susceptible in one

experimental study (Porter et al., 2022)), for which no evidence of a role in the circulation and

maintenance of the SARS-CoV-2 infection currently exists. In case of increased mortality in these

wildlife populations, SARS-CoV-2 infection should be included as a differential diagnosis. In addition,

research studies should investigate the possible role of bats in the European context, especially those

belonging to the family

Rhinolophidae

(Delahay et al., 2021; EFSA, 2021).

From all types of surveillance of wildlife for SARS-CoV-2, positive samples should be subjected to

genomic characterisation to monitor the circulating virus genetic characteristics.

3.6.2.4. Zoo animals

The infection of zoo animals with SARS-CoV-2 can be considered an accidental and sporadic event

from infected workers, with little relevance from the epidemiological point of view. Therefore, no

speciﬁc systematic monitoring activities are considered necessary in these animals; only testing

sporadic mortality cases and animals showing clinical signs or in contact with positive tested workers

or animals may be relevant to conﬁrm the SARS-CoV-2 infection and, in case needed, to apply a

proper therapy, especially for high-value individuals. Usual preventive measures (quarantine, isolation,

etc.) should be then foreseen for infected animals, especially if kept in enclosure with other susceptible

species or individuals. A repeated testing scheme could be justiﬁed for zoo workers in order to prevent

the transmission to these animals.

3.6.3.

New development in diagnostics/sample matrices for SARS-CoV-2 in

animals

Depending on the various objectives of the surveillance, different testing method approaches have

to be considered: viral nucleic acid detection tests for acute infection and serological tests for

population studies. Relevant aspects regarding diagnostic tests are described in a previous EFSA report

(EFSA, 2021) and are still applicable. In particular, caution needs to be taken if new variants arise that

may not be detected by previously validated tests.

The limitations of diagnostic tests must be taken into account. Very few diagnostic tests have been

validated in animals, especially in wild populations. Direct diagnostic assays (e.g. RT-PCR) may be

affected by a low sensitivity due to the limited knowledge of the viral loads and routes of virus

shedding as well as the temporal window during which the virus can be detected on animal samples.

Antigen tests, as used for humans, are not recommended for use in animals due to the unknown

speciﬁcity and sensitivity in animal samples.

Serological tests (e.g. neutralisation tests or ELISAs), so relevant for retrospective or prospective

population studies, may be seriously affected by a low speciﬁcity, due to potential cross reaction with

antibodies against other coronaviruses frequently present in animal populations. Noteworthy, some

animals can also have antibodies against coronaviruses to which they are not susceptible.

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Samples from the environment of animals can also be collected for surveillance studies. This could

include water, air or surface sampling for environmental SARS-CoV-2 RNA.

3.7.

Options for disease prevention and control measures

In this chapter, the main possible measure for prevention and control of SARS-CoV-2 infection in

farmed animals are presented and their advantages and drawbacks discussed based on feedback

gathered from MSs, assessment by ECDC (for the measures to be applied on humans) and on expert

knowledge. The control measures to be applied in the scenarios for companion animals in the

household, wild and feral animals and zoo animals are indicated in Section

3.4;

because these are

driven by general principles of good hygiene practice, an assessment about their advantages and

limitations is not conducted.

3.7.1.

Farmed animals

This section refers to main control measures applied in MSs, where farmed animals susceptible to

SARS-CoV-2 are bred (i.e. mink, raccoon dogs, sable, ferrets, foxes). Humans are considered to be the

most important source of introduction of SARS-CoV-2 into the farm, with 12 reported occurrences of

human introductions to fur farms in the current reporting period, up to November 2022

(Section

3.2.1.1).

3.7.1.1. Farm personnel and visitors

3.7.1.1.1. Health self-assessment (‘stay-at-home/isolation’)

In general, the risk of transmission from persons (workers/visitors) to mink can be reduced by

staying at home when feeling sick or testing positive for SARS-CoV-2 or other pathogens that could be

transmitted to animals, e.g. inﬂuenza. For details, see Section

3.5.3.

3.7.1.1.2. Systematic testing of personnel/visitors at predetermined frequency

To prevent introduction of infection from humans, systematic frequent testing using rapid antigen

test and/or PCR of personnel and visitors for SARS-CoV-2 infection has been recommended as an

option. As already indicated in the previous report by EFSA (2021), this is a prerequisite for the early

detection of infection in people that may enter the farm and come into contact with animals, and

therefore considered a key measure to prevent introduction of SARS-CoV-2 into the farm. Early

detection of infection in people is only efﬁcient if followed by restricted access to the farm for people

tested positive. More details are provided in Section

3.5.3.

•

Advantages:

○

Theoretically good effectiveness

Limited costs

Easy application and veriﬁcation (a record of test results can be kept)

Relatively early detection of infected workers including the asymptomatic ones.

•

Challenges and drawbacks

○

Limited (and depending on the type of test) sensitivity of the test during early stages of

infection and potentially for emerging variants

High frequency of testing necessary to ensure early detection

Additional cost for farm or workers might decrease compliance

Possible organisational difﬁculties (e.g. to train people for properly making nasopharyngeal

swabs or to recruit sanitary personnel)

Some personnel/visitors may

‘escape’

testing at sampling locations (farmers may not have

the authority to impose testing) or skip mandatory self-tests.

3.7.1.1.3. Temperature screening

The systematic testing has sometimes been coupled with temperature screening and health check

for clinical signs for whoever enters the farm at any time (personnel, visitors, etc.), in combination with

a SARS-CoV-2 rapid antigen test.

Nevertheless, based on the experience with different diseases over the past outbreaks and

pandemics, temperature screening is an ineffective, unspeciﬁc and resource-intensive measure that

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adds little beneﬁt. Fever is not a speciﬁc symptom that clearly identiﬁes a SARS-CoV-2 infection. A

proportion of COVID-19 cases will not be identiﬁed through temperature measurement because of

being asymptomatic- or pre-symptomatic or under antipyretic medication. Furthermore, a proportion of

transmission happens before symptom onset. In addition, the technical implementation of this

measure is quite complex (equipment, calibration, thresholds, performance, sensitivity and speciﬁcity,

etc.).

Compared to the application of screening by COVID-19 rapid test, this measure does not provide

any advantage in such settings nor prevents introduction of SARS-CoV-2 into the facilities.

3.7.1.1.4. Use of personal protective equipment (PPE) for farm personnel and visitors

Personal protective equipment (PPE) impacts the risk of transmission from infected persons to

animals or vice versa. PPE will help to limit the exposure to and spread of pathogens but is dependent

on the level of applied PPE. To reduce the risk of transmission, people in contact with SARS-CoV-2-

infected animals should wear FFP masks or respirators as well as goggles.

The wearing of speciﬁc clothing, aprons, rubber boots and additional protective equipment needs to

be considered according to the work area in consultation with the respective occupational safety and

health authorities. Limitations in the preventive effect could be due to difﬁculties in maintaining

compliance for a long period, working conditions could be difﬁcult especially when temperatures are

high or in case of chronic respiratory disorders of farm personnel. It may also require long-term

awareness from farm personnel and work environment rules/regulations might require special types of

masks or limited time working with masks. See also ECDC’s scientiﬁc evidence basis assessment for

the considerations for the use of face masks in the community in the context of the SARS-CoV-2

Omicron variant of concern (ECDC, 2022b).

3.7.1.1.5. Vaccination of personnel

Vaccines continue to provide high levels of protection against severe COVID-19, hospitalisation and

death. Vaccination of personnel may inﬂuence the risk of spread from personnel and visitors to mink

and vice versa, however, with waning immunity against infection and the possible emergence of new

immune-escape variants, protection against infection and onward transmission could be limited in time

and magnitude. Vaccination recommendations need to be in line with the national recommendations

and discussed with occupational health and safety authorities. For details, please see Section

3.5.4.

3.7.1.2. General on-farm biosecurity measures

Biosecurity measures aim at reducing the risk of introduction of pathogens into the farm and its

further spread in and from the farm. The measures described in this section are focused on

mechanical transmission, or transmission between farmed animals and other species, while

transmission from infected persons to mink and vice versa is described in Section

3.7.1.1.

Application of biosecurity measures can be veriﬁed by ofﬁcial controls and record keeping, although

the level of on-farm biosecurity and the compliance may vary between farms and may change over

time in the individual farm, according to what has been reported by MSs.

3.7.1.2.1. Restricted access for animals and visitors to farm, including tracing of visitors

To reduce the risk of introduction of pathogens, non-essential visits of people to the farm should

not be allowed. Farm personnel or visitors with symptoms compatible with SARS-CoV-2 or having

tested positive should not be permitted to enter fur farm premises (see Section

3.7.1.1).

To allow tracing of introduction of SARS-CoV-2 from persons entering farms, records (electronic or

physical) of all workers and visitors entering should be kept and be up to date. To reduce the risk of

spread between farms, rotation of farm workers between farms should be limited and farm personnel

should be discouraged to breed or keep other mink at home.

In closed farms, openings (doors, windows, holes, enclosures) should be

ﬁxed

to prevent animals

from escaping and entering the farm. Ventilation would represent an issue only for indoor farms,

although mink farms are generally structures covered with a roof but open on the sides, so natural air

circulation is sufﬁcient. In all farms, but especially in open farms, efﬁcient fencing can reduce the

access of other animals to the farm area. Automatic closure of gates and doors can help keeping the

openings closed.

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•

Advantages

○

Basic biosecurity measures reduce the risk of introduction of pathogens in general. Each

individual measure might not be highly effective by itself, while in combination, they can

reduce the overall risk.

○

Fences and locked doors can reduce the risk of uninvited persons to enter the farm and

reduce the risk of pets and wildlife to enter the farm area.

○

Reducing the numbers of events (e.g. visits by persons or animals) will reduce the overall

risk of disease introduction.

Challenges and drawbacks

○

Availability of trained personnel might be limited in certain periods of the year with high

workloads in mink farms.

○

It might be difﬁcult to control whether visitors have visited other farms previously.

○

Fences and doors require proper facilities (e.g. fences, which, in some countries, such as

Finland, are mandatory in raccoon dog farms as a rule for invasive alien species).

○

Building and maintenance costs.

○

Difﬁcult to ensure daily compliance of closed doors/fences.

○

Requires long-term awareness from farm personnel.

○

In case of restricted/delayed access of workers, this may delay operations at farm.

•

3.7.1.2.2. Changing work clothes for farm personnel

Changing clothes will reduce the risk of mechanical transmission of infectious pathogens from and

to the farm. In a situation, where the worker or person entering the farm is infected, the effect of

changing clothes will be limited. However, if for example the personnel entering a farm have had

contact with an infected family or other persons, the risk of introduction can be reduced by changing

of clothes, boots, washing hands, etc. In some farms, changing room or areas are available, where

clean clothes and boots, a sink for hand wash, disinfectants, etc. are available.

•

Advantages

○

Basic biosecurity measures reduce the risk of introduction of pathogens in general. Each

individual measure might not be highly effective by itself, while in combination, they can

reduce the overall risk.

○

Relatively limited costs, as some level of biosecurity is often already in place in farms.

Challenges and drawbacks

○

Supply costs (if not already implemented).

○

Proper facilities are required (e.g. locker rooms, washing machine on farm).

○

Building and maintenance costs (if not in place).

○

Requires long-term awareness from farm personnel.

•

3.7.1.2.3. Cleaning and disinfection equipment/vehicles

For other pathogens, transport vehicles are often considered a risk, and cleaning disinfection and tracing

is used as general biosecurity measures. For SARS-CoV-2, the transmission of SARS-CoV-2 through

transport vehicles has not been described. Furthermore, sharing equipment between farms might pose a

risk of mechanical transmission of pathogens. Avoiding sharing equipment and vehicles, and proper

cleaning and disinfection, if sharing is needed, can reduce the risk of potential mechanical transmission.

•

Advantages

○

Basic biosecurity measures reduce the risk of introduction of pathogens in general. Each

individual measure might not be highly effective by itself, while in combination, they can

reduce the overall risk.

Challenges and drawbacks

○

Requires proper facilities, and efﬁcient disinfectants.

○

Especially during winter months, temperatures can be a challenge in relation to cleaning,

and disinfection of equipment and vehicles.

○

Difﬁcult to ensure daily and sufﬁcient compliance.

○

Requires long-term awareness from farm personnel.

•

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3.7.1.2.4. Rodent control

The use of rodent control is a basic biosecurity measure often used in farms to reduce the risk of

spread of pathogens, although in the case of SARS-CoV-2, spread of the virus by rodents has not been

reported.

•

Advantages

○

Basic biosecurity measures reduce the risk of introduction of pathogens in general. Each

individual measure might not be highly effective by itself, while in combination, they can

reduce the overall risk.

○

Prevention of entry and presence of rodents can be based also on keeping the area where

mink are as clean as possible, reducing feed rests and having a clear, open zone between

the fence and the animal cages.

Challenges and drawbacks

○

Requires suitable equipment and rodenticides.

○

Supply costs.

○

Risk for animals and humans if misused, due to rodenticides toxicity.

•

3.7.1.3. Animal movement control, including pre-movement testing and tracing

In known infected farms and surrounding areas, restriction of movements can prevent or reduce

the risk of further virus spread and secondary outbreaks. By testing prior to movements, the risk of

moving infected animals can be reduced. Furthermore, keeping records of movements can make easy

the tracing after detections of infected farms.

•

Advantages

○

Potentially effective in preventing spread to other holdings.

○

Ease of implantation, since not many movements are performed in farmed mink, and

movements most often occur in restricted time periods.

Challenges and drawbacks

○

Only efﬁcient if early detection occurs in infected farms.

○

Negative impact on trade and potential

ﬁnancial

losses can limit compliance.

○

Negative impact on farm management and productivity (e.g. inability to replace breeding

animals or transfer animals in order to decrease density following increased litter sizes).

○

If testing is required prior to movements, additional costs are incurred.

○

Records (electronic or physical) must be kept and be up to date, which might be a

challenge for small farms.

○

At certain times (pelting), movement restrictions may cause problems in the removal of

skins or transfer of carcasses for pelting.

•

3.7.1.4. Awareness raising

This is to increase awareness about how to prevent and control SARS-CoV-2 infection, and it is

considered a very important measure. Especially among farm personnel, it is important to remind

about how SARS-CoV-2 in animals spreads and how to prevent animal and human infection and

routinely remind them about biosafety and biosecurity measures against SARS-CoV-2 on the farm.

Authorities and fur industry usually spread information and operating instructions through different

channels to farm personnel. Workers from other countries should be provided information in their own

language for regular work arrangements as well as during outbreak situations with speciﬁcally targeted

information leaﬂets.

•

Advantages

○

Potentially enhances and improves application of biosecurity measures.

○

Potentially increases reporting of abnormal morbidity and mortality (already foreseen by

the legislation).

Challenges and drawbacks

○

May cause disquiet due to possible economic losses and public health concerns.

○

Translation in different languages may be needed, especially in case of farm personnel

from abroad.

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3.7.1.5. Culling and disposal of animal in an infected farm

In the case of an infected farm, the veterinary authorities may order the immediate killing of all

farmed animals under ofﬁcial surveillance with the aim of preventing the spread of the disease.

•

Advantages

○

It can reduce the virus load thus reducing the risk of spread, if the infection is detected

early.

○

If infection is detected early, culling all animals on the farm will prevent extensive virus

circulation and consequently the risk of mutations that might pose a risk to public health.

Challenges and drawbacks

○

Only efﬁcient, if early detection can be ensured.

○

Extensive secondary spread from infected farms have only been reported from areas with

very dense population, meaning that the probability is not always high.

○

High costs, large need of resources, human resources and equipment (ofﬁcial vets,

dedicated companies).

○

Costs for infected farms (entire loss of breeding and production animals) as well as for the

administrations for the compensation to farmers and for the destruction of skins and other

possibly contaminated by products.

○

Emotional impairment for farmers and other involved people.

○

Public concerns about culling animals.

○

Increased exposure to humans involved in culling activities, however, no or very limited

number of infections have been observed in people related to culling activities likely due to

the wearing of PPE.

•

3.7.1.6. Zoning around infected farms

Implementation of zones around infected farms is a general preventive measure used for outbreaks

of other pathogens. In the zones, increased surveillance and movement restrictions are typically

implemented. The effect of movement restrictions is described in Section

3.7.1.3,

while the effect of

surveillance is described in Section

3.6.

For SARS-CoV-2, distance to infected farms was described as a risk factor (EFSA, 2021). However,

as introductions from infected persons is considered the highest risk of transmission, the effect of

zoning on the risk of SARS-CoV-2 transmission is considered to be limited. While airborne transmission

is one of several pathways that in general might increase the risk in zones around infected farms,

which might be managed by zoning restrictions, SARS-CoV-2 has not been detected in air samples in

distances

3 m from infected mink. Moreover, zoning is a way to delimitate and differentiate

geographical zones with a different health status. Here, since SARS-CoV-2 is present everywhere

outside the outbreak, zoning would not be a meaningful measure.

3.7.1.7. Vaccination of animals

In the EU, vaccination of animals against SARS-CoV-2 was only applied in mink in Finland with a

product developed by the Finnish Fur Breeders’ Association (FIFUR), whose usage permit was granted

by the Finnish Food Authority according to national procedures that foresee a provisional authorisation

of a vaccine in the event of a serious animal disease epidemic. Approximately 95% of breeding

females in all farms were vaccinated early in 2022 when only breeding animals were present at farm.

The vaccine product contains subunits of the SARS-CoV-2 bivalent RBD-mFc fusion protein

produced in mammalian cells as antigen and aluminium hydroxide as adjuvant.

Data provided by the producer showed that the vaccine was well tolerated in mink and it was able

to induce a humoral immune response characterised,

inter alia,

by virus-neutralising antibodies, tested

5 weeks after vaccination.

Regarding the protection induced by vaccination, the experimental studies performed by the

producer suggested that the symptoms (sneezing, anorexia and diarrhoea) were less common and

severe in vaccinated than in control animals. Data regarding other possible impact of the vaccination,

such as the spread of the virus, the efﬁcacy versus infection and the onset or duration of immunity

were not complete to allow a reliable assessment. Overall, it is possible to conclude that the vaccine

was able to provide a certain degree of protection against severe disease caused by Delta-variant of

SARS-CoV-2 in mink, but it did not prevent infection. Vaccination of mink is no longer in use in Finland,

due to its limited effectiveness against Omicron variant, as reported by the producer.

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SARS-CoV-2 in animals

Another vaccine product was submitted to the European Medicines Agency (EMA) for a centralised

procedure of authorisation, but they have been withdrawn during the process.

3.7.2.

Options for public health response

A close collaboration and communication between animal and public health sectors as well as

occupational safety and health authorities in a One Health approach is crucial to identify transmission

events at the human–animal interface and prevent further spread.

Testing approaches together with genetic monitoring of virus samples from people exposed to

animals with conﬁrmed SARS-Cov-2 infection as well as from animal sources are key to understand

factors related to transmission as well as evolutionary host-driven mechanisms. It is important to

collect representative samples for further characterisation of viruses from the general population as

well as from animals infected with SARS-CoV-2.

PPE is a crucial measure for workers to prevent exposure to SARS-CoV-2-infected animals or

contaminated workplaces. Information about outbreaks should be immediately shared with public and

occupational safety and health authorities to enable appropriate follow-up of exposed people and the

implementation of control measures.

Conclusions and recommendations

Based on the aspects to be assessed as indicated in the ToRs (susceptibility, risk for animal and

public health, monitoring approach and preventive and control measures), the current assessment is

structured according to different animal categories: farmed animals (mink), companion animals,

wildlife and animals kept in zoos, and the conclusions are presented accordingly.

General conclusions about animal species of concern in the epidemiology of SARS-CoV2

•

This scientiﬁc opinion classiﬁed animal species of potential epidemiological concern to be those

that shed infectious virus and are able to transmit SARS-CoV-2 to other animals or humans.

Such species of epidemiological concern assessed here are American mink (Neogale

vison),

raccoon dog (Nyctereutes

procyonoides),

cat (Felis

catus),

Syrian hamster (Mesocricetus

auratus),

ferret (Mustela

furo),

house mouse (Mus

musculus,

for some virus variants only),

Egyptian fruit bat (Rousettus

aegyptiacus),

deer mouse species (Peromyscus

spp.,

not present

in Europe) and white-tailed deer (Odocoileus

virginianus).

Of note, there is uncertainty on the list provided in the previous bullet: most experimental

infections to determine species susceptibility were performed with ancestral (pre-Alpha clades)

virus isolates. Furthermore, as variants continue to arise, and new host species are being

detected over time, species susceptibility and virus transmission capacity may change, with the

continuous potential emergence of new host species.

Farmed animals (mink)

Susceptibility, epidemiological situation

•

American mink is a highly susceptible species, and outbreaks have occurred in MSs from April

2020 until the end of the reporting period considered in this document, although with a

decreasing number of outbreaks in 2022 compared to 2021. Species-speciﬁc viral evolution of

SARS-CoV-2 has been observed in this species.

Among animals in the EU, mink farmed for fur production have the highest likelihood to

become infected and transmit SARS-CoV-2 within animal populations and to in-contact humans

e.g. farm personnel, and subsequently to the general population. This can be explained by the

inherent susceptibility to SARS-CoV-2 infection of the species, in combination with the

characteristics of the systems in which farmed mink are kept, with large numbers of animals in

a limited area.

During the still ongoing SARS-CoV-2 pandemic, a vast majority of the outbreaks of SARS-CoV-2

reported globally in animals have occurred in mink for fur production. In the reporting period

(February 2021–November 2022), 50 outbreaks of SARS-CoV-2 were reported, of those 44

were reported in 2021 in 7 MSs, while only 6 were reported in 2022 in 2 MSs, thus

representing a decreasing trend.

https://www.ema.europa.eu/en/medicines/veterinary/withdrawn-applications/versiguard-sars-cov2

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SARS-CoV-2 in animals

•

Most sequenced mink isolates grouped into distinct major mink-speciﬁc clusters, were

geographically clustered and showed high intra-cluster variability, indicating mink-to-mink

transmission, high rates of virus evolution within the mink population and emergence of mink-

speciﬁc variants with a potential to spill back into the human population.

Risk for animal and public health

•

SARS-CoV-2 can spread from humans to mink and from mink to humans during exposure.

The probability of introduction of SARS-CoV-2 from humans to mink farms is associated with

the SARS-CoV-2 level of circulation in the surrounding general human population. This

probability can be reduced through continuous and proper implementation of biosecurity

measures in mink farms including the use of non-pharmaceutical interventions (NPI) for all

humans accessing mink farms (Section

3.5.3).

Once introduced into a mink farm, SARS-CoV-2 spreads efﬁciently within the farm from animal to

animal, resulting in extensive virus circulation and risk of spill-over to humans in contact with the

mink, as well as to other susceptible animals with access to mink and their local environment.

The extensive circulation of SARS-CoV-2 in an infected mink farm drives virus adaptation,

resulting in the potential generation of mink-adapted virus variants.

In general and for all animal species, the public health impact of the possible spill-over of

SARS-CoV-2 from mink farms to humans depends on several factors: the respective virus

variant, effectiveness of the vaccine for this variant in vaccinated people including the time

period after the vaccination, previous exposure to other SARS-CoV-2 variants and health status

of the individual person:

○

The risk (determined by probability of infection and impact of the disease), for an

occupationally exposed person to a SARS-CoV-2-infected mink is assessed as low to

moderate. This assessment is subjected to uncertainty related to the impact of variants

potentially emerging in mink.

The risk based on the probability to get infected and develop severe disease for a person

without or with limited exposure to farmed mink is estimated to be none to very low.

The risk of the spread of a SARS-CoV-2 variant with mink-speciﬁc mutations, or re-

introduction of an older variant virus that circulated in mink, into the general human

population causing severe COVID-19 is estimated to be very low-to-low.

○

Monitoring approach at farm level

•

In the current epidemiological situation in the EU, where a substantial decrease of outbreaks in

mink farms has been reported in 2022 compared to 2020 and 2021, and where the majority of

the human population has acquired some level of immunity to SARS-CoV-2, the risk for the

general population represented by infected mink is considered very low-to-low; therefore:

○

The primary purposes of monitoring of mink farms are to conﬁrm outbreaks based on

suspicion and monitor virus evolution (sequencing isolates).

The conﬁrmation of SARS-CoV-2 infection in suspected animals remains a relevant

objective, in order to allow the farmers to apply preventive measures in terms of reducing

the risk of secondary outbreaks.

A monitoring approach based on testing of dead animals or with clinical signs suggesting

possible SARS-CoV-2 infection is considered appropriate, with sampling triggered by

increased mortality or morbidity in mink, or farm personnel testing positive.

•

The genomic surveillance of viruses circulating in mink and in general in all animal species is

considered relevant to monitor the circulating genetic variants of the virus and comparing the

genetic type from mink to currently circulating variants in humans. Virus isolates from positive

samples representing at least every epidemiological unit should be subjected to genomic

characterisation and genome sequences shared with the scientiﬁc community.

As an additional monitoring strategy, sampling at pelting and use of serological tests can help

in assessing the number of mink farms that have been infected to monitor possible changes in

prevalence.

Decreasing testing for SARS-CoV-2 in the human population and testing with sequencing of

specimens from severely ill COVID-19 patients in hospital may delay the early detection of

animal-associated SARS-CoV-2 variant viruses. It is therefore important to expand and increase

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SARS-CoV-2 in animals

the national sentinel surveillance for SARS-CoV-2 in primary (as well as secondary) health care

units to achieve higher representativeness across the population and higher number of

available specimens for genomic analysis. This will also enable the detection of new virus

variants in the population.

Options for preventive and control measures

•

Humans are considered the most important source of introduction of SARS-CoV-2 into a farm.

○

Systematic frequent (e.g. at least weekly) testing for SARS-CoV-2 infection using rapid

antigen test and/or PCR of personnel and visitors is a prerequisite for the early detection of

infection in humans that may enter the farm and come into contact with mink and is

therefore a key measure to prevent introduction of SARS-CoV-2 into the farm.

Similarly, the limitation or ban of non-essential visits of humans to farms will reduce the

frequency of contacts and thereby the risk of transmission from visitors.

○

•

The risk of transmission from persons (e.g. workers, visitors) to farmed mink can be reduced

by staying at home when feeling sick or testing positive for SARS-CoV-2.

Measures applied to reduce the risk of transmission between mink and humans will only have

effect if used consistently. The level of on-farm biosecurity and the compliance can be veriﬁed

by ofﬁcial controls and record keeping, although may vary between farms and may change

over time in an individual farm.

Wearing of personal protective equipment for persons in contact with mink is a useful measure

to reduce the probability of introduction and transmission of SARS-CoV-2 virus into farms from

people. These measures also may reduce the risk for people of being infected by mink.

Biosecurity measures applied at farm (cleaning, disinfection, pest control and restricted access to

other animals than mink that may be present at farm) aim at reducing the risk of virus introduction

into the farm, and its further spread in and from the farm (e.g. transmission between farmed

animals and other susceptible or possibly susceptible species such as cats, dogs, bats, etc.).

The risk of further virus spread and secondary outbreaks to other farms can be reduced by

restriction of mink movement and/or by testing for SARS CoV-2 prior to movement, especially

in farms located in areas with known infected farms.

Current vaccines against SARS-CoV-2 do not fully prevent virus transmission to and from

vaccinated humans as well as between humans and mink. Vaccines are protective against

severe disease, hospitalisation and death. Experimental vaccines for mink conferred a certain

degree of protection against severe disease caused by Delta-variant of SARS-CoV-2 but they

did not prevent infection, and they not effective against Omicron variants.

Recommendation:

Equally important in relation to farm personnel is the provision of

information material and training to all farmworkers, including guest workers, in mink farms

about biosafety and biosecurity measures against SARS-CoV-2 on the farm in their own

language, as well as providing them access to health care.

Companion animals

Susceptibility, epidemiological situation

•

Among companion animal species, cats, ferrets and hamsters are the species most at risk of

infection. In these species, serious illness from SARS-CoV-2 has sporadically been observed.

In experimental infections, hamsters, ferrets and cats can display clinical signs. Usually, they

recover spontaneously. No clinical signs have been reported for dogs, rabbits, rats and mice.

Transmission of SARS-CoV-2 from a donor animal to a recipient of the same species by direct

contact has been demonstrated for cats, ferrets, hamsters and mice, while no evidence exists

for virus transmission between dogs.

Under

ﬁeld

conditions, cats and hamsters have been associated with mild to moderate

respiratory, gastrointestinal or systemic signs of disease and they can shed virus.

Deposited sequences of SARS-CoV-2 obtained from infected companion animals are spread all

over the SARS-CoV-2 clades and have limited tendency of clustering together, indicating

sporadic transmission from humans, with little or no animal-to-animal transmission among

companion animals.

Viral sequence analysis indicates low frequency of species-adapted mutations.

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SARS-CoV-2 in animals

Risk for animal and public health and related control measures

SARS-CoV-2 infection of companion animals is most likely originating from an infected human.

The risk for cats and hamsters of spreading SARS-CoV-2 back to humans (probability of infection and

severity of disease of a pet owner as well as in the general population) is assessed as very low.

•

Humans with high contact rates to companion animals from different households (e.g.

veterinarians) have a higher risk (very low to low) to get infected from a companion animal.

•

The probability of companion animals to have an impact on the virus circulation in the general

population is none to very low.

Monitoring approach

•

–

For companion animals, there is no need for speciﬁc monitoring programmes, taking into

consideration that sporadic cases of transmission to humans may occur, but generally limited

to owners, zoo workers or veterinarians in contact with these animals.

○

In some companion animal species, in case of clinical signs compatible with SARS-CoV-2

disease, animal testing may be important for possible quarantine measures or application

of proper therapies.

In addition, apart from research objectives, testing of individuals in stray communities

(especially cats) could be justiﬁed, in case of suspected SARS-CoV-2 clinical cases or

abnormal mortality rates in these communities.

Wildlife

Susceptibility, epidemiological situation

The number of wildlife species that have been reported naturally SARS-CoV-2 infected grows

steadily, also due to the active research in this

ﬁeld,

including several wild carnivores and the

white-tailed deer in North America.

•

The epidemiological role of susceptible wildlife in the EU context for the maintenance of virus

circulation, and as a possible public health risk, depends on their abundance and the level of

exposure to human population and to other wild or domesticated animals.

•

In the EU, no cases of infected wildlife (with viral isolation or RNA detection) have been

reported so far.

•

So far, only North American white-tailed deer, both free living or captive in game reserves,

have been demonstrated to maintain and possibly spill back the infection to humans.

•

Recommendation:

Further epidemiological research should be promoted in a broad range of

wildlife species, including feral species, and geographical regions.

Risk for animal and public health

•

Differently from the situation in North America, very low numbers of white-tailed deer are

present in the EU (less than 1% of the total EU deer population) only in two countries. It is

unknown whether these animals may be able to support the persistence of SARS-CoV-2

infection in the European context. Population density, aggregation and mating season can

facilitate this possible occurrence.

In the EU, the risk of transmission of SARS CoV-2 infection from humans to white-tailed deer

and backward causing severe disease is considered very low. Risk factors are events that

increase exposure of white-tailed deer to humans, such as hunting. In general, any activities

that bring animals close to humans or even proximity of animals to urban settings and

likelihood of exposure to contaminated wastewater or garbage.

○

Recommendation:

Action should be taken to avoid overabundance or aggregation of

white-tailed deer, and in general all game species (such as by avoiding feeding sites,

monitoring group size) to control this transmission pathway.

Recommendations:

Further research studies might be relevant to monitor the possible

role of white-tailed deer and other deer or other wildlife populations in Europe for the

presence and eventual persistence of SARS-CoV-2 infection.

Recommendation:

Good hunting practices (avoiding feeding or baiting) are advised.

Humans dealing with wildlife should follow biosecurity measures in general minimising

direct contact with wild animals, especially sick and dead animals. Furthermore, safe

disposal of garbage and waste from human communities in both urban and rural settings

is advised to reduce the risks of SARS-CoV-2 spill-over to wildlife.

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•

Regarding wild carnivores, due to their elusive and solitary behaviour, to their low density and

to the low numbers hunted, there is a very low probability of maintaining the infection or

representing a risk for other animal species or for public health also due to limited human

exposure, even for occupationally exposed people (rangers, hunters, researchers, etc.).

The probability of transmission of viruses from bats to humans or the emergence of SARS-CoV-

2-related or new coronaviruses has been assessed as none to very low for the next 12 months,

since transmission of SARS-CoV-2 or other coronaviruses from bats to humans and backwards

has not been observed in Europe and on the limited human population having direct contact

with these animals. However, since bats are natural hosts of many coronaviruses, the

monitoring of these species is still important.

Monitoring approach

–

Based on the current knowledge, the main wild animal species that may be considered as

possible targets for SARS-CoV-2 monitoring are white-tailed deer, wild carnivores (e.g. wild

mustelids, felids and canids), bats and rodents such as wild synanthropic mice and rats (those

living in or close to human settlements).

○

No speciﬁc regulated monitoring activities would be needed for wildlife in the EU, apart

from monitoring based on suspicion, i.e. testing of animals showing clinical signs

suggesting possible SARS-CoV-2 infection or dead-found animals. Positive samples should

be subjected to genomic analysis to monitor virus evolution and genome sequences shared

with the scientiﬁc community.

–

Insectivorous bats, especially those belonging to the genus

Rhinolophus,

are hosts for a range

of betacoronaviruses and thus also of potential relevance for SARS-CoV-2 monitoring.

Recommendations:

Research studies should investigate the possible role of bats in the

European context, especially those belonging to the family

Rhinolophidae.

Zoo animals

Susceptibility and epidemiological situation

•

There are reports of both experimental and natural infection of animal species kept in zoos

with SARS CoV-2, mainly felids and great apes.

Risk for animal and public health and related control measures

Zoo animals, such as felids and great apes, can acquire the infection mainly from infected zoo

workers in contact with them, still at very low risk. There is no report of spillback transmission

from animals to humans in zoos.

Regular testing of workers, self-isolation when positive, use of PPE and good hygiene practice

(e.g. avoiding close contact, disinfection of tools), as well as good ventilation in closed

enclosures can signiﬁcantly reduce the risk of transmission from humans to animals.

Transmission between susceptible animals in the same enclosure could occur once an animal is

infected, although transmission between animals kept in zoos is difﬁcult to be proven, because

if they belong to the same outbreak they are usually exposed to the same infectious source

(e.g. positive caretaker). The probability of transmission to animals in other enclosures is

considered very low.

Testing and isolation of animals with clinical signs, even by non-invasive monitoring by air

sampling or rope-based oral

ﬂuid

sampling, or testing in the frame of other veterinary checks,

as well as reducing animal density and avoiding sharing same air in ventilation systems, might

reduce the risk of further transmission.

Animals kept in zoos overall do not represent a major public health risk in relation to SARS-

CoV-2.

○

The risk for occupationally or activity-related exposed people or groups such as zoo

workers, rangers or forest workers to be in contact with infected animals or their

droppings and get infected and develop severe is estimated to be very low.

The risk (probability to be infected and develop severe disease) for an individual person to

get infected from an animal in a zoo as well as the probability to have an emerging virus from

zoo or wild animals circulating in the general population is considered to be none to very low.

•

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Monitoring approach

•

The same conclusions as those indicated for companion animals are valid for zoo animals.

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940956

Abbreviations

COVID-19

ECDC

ELISA

EMA

EWS

PPE

RADT

Coronavirus disease 2019

European Centre for Disease Prevention and Control

Enzyme-linked immunosorbent assay

European Medicines Agency

Early Warning System

Fusion peptide

Member State

Personal protective equipment

rapid antigen detection tests

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Reverse transcription polymerase chain reaction

Receptor-binding domain

Severe acute respiratory syndrome coronavirus 2

Term of Reference

Virus neutralisation test

World Health Organization

www.efsa.europa.eu/efsajournal

SARS-CoV-2 in animals

RT-PCR

RBD

SARS-CoV-2

ToR

VNT

WHO

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SARS-CoV-2 in animals

Annexes

–

A.1.

A.1.1.

Protocol for the assessment of the SARS-CoV-2 in animals:

susceptibility of animal species, monitoring, prevention and control

Background and ToRs as provided by the requestor

See Section

1.1.

A.1.2.

Problem formulation

Here, a summary of the initial considerations are described. With this mandate, the European

Commission requests EFSA’s support in assessing the adequacy of the current monitoring system for

SARS-CoV-2 in mustelids and raccoon dogs in the EU, which should be reviewed in light of the evolvement

of the epidemiological situation and along with the new scientiﬁc knowledge on the spread of SARS-CoV-2

in both humans and animals. For the assessment of the following problems are formulated:

1) susceptibility of animals

a) susceptibility in natural and laboratory conditions, species where SARS-CoV-2 or its RNA

or antibodies to SARS-CoV-2 been detected in experimental studies or in the

ﬁeld,

and

their geographical distribution;

b) dynamic of infection and pathogenesis;

c) role in inter and intra-species transmission;

d) genetic analysis of the virus variants in each species where it is isolated;

e) The group animal species to be considered.

2) Risk for animals posed by SARS-CoV-2 infection in animals species of concern

a) Once susceptible species or group of species susceptible to SARS -CoV-2 are identiﬁed,

the possible exposure and transmission pathways and related risk between these species

and other species are assessed.

3) Risk for humans posed by SARS-CoV-2 infection in animal species of concern

a) Which species identiﬁed in ToR 1 to whom humans may be exposed and the following:

b) Exposure assessment: social groups exposed to which relevant animal species;

c) Genetic variants and assessment of the possibility that virus can persist in animal

population with the emergence of new variants potentially able to escape vaccine efﬁcacy;

d) Circulation, severity;

e) Diagnostics, immunity, vaccination, treatment;

f) Options for public health response for each social groups.

4) Revision of the monitoring system

The main problem is to assess which monitoring approach in mink/raccoon dogs should be applied

and whether it should be extended to other species. The monitoring scenarios is depicted by animal

category and the related monitoring objective.

5) Possible options for disease prevention and control measures

1) Identiﬁcation and assessment of effectiveness of main preventive and control options in

place in EU, highlighting strengths and drawbacks.

A.1.3.

Clariﬁcations of the scope of the request: framework, population

and geographical area of concern, deﬁnitions

Scope: to assess health risk in animals and humans and to provide recommendations for revision of

the current monitoring system for SARS-CoV-2 in mustelids and raccoon dogs in the EU.

Geographical area: EU for the monitoring approach; worldwide for screening the literature.

Population: mustelids and raccoon dogs as population target for the current monitoring system and

assessment of any other species considered susceptible to SARS-CoV-2 that may represent a risk for

animals and humans and should be considered in the monitoring plans.

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SARS-CoV-2 in animals

A.1.4.

Translation of ToRs into assessment questions and subquestions

ToR 1

‘Reviewing

updated relevant scientiﬁc literature available globally related to SARS-CoV-2

infection in animals species of concern in the epidemiology of SARS-CoV2’ has been translated in the

following assessment questions:

•

Which mammal species have been reported test positive to SARS-CoV-2 in the

ﬁeld

(either at

RNA, isolated virus, antibodies), and their geographical distribution?

Which wild and domestic mammal species are susceptible to SARS-CoV-2 in laboratory

conditions?

Dynamic of infection and pathogenesis:

What are conﬁrmed infection routes for these species?

What is the length of the incubation period in these species?

What are the clinical signs, if any, their severity, duration, etc.?

Which species are able to shed the virus (even in the absence of clinical signs)?

Do these species develop protective immunity?

Which of these species can further transmit the disease to same/other species?

What are the genetic virus variants in each species where it is isolated?

In which animals vaccines against SARS-CoV-2 have been tested, and what are the results in

terms of immunogenicity, protection to challenge or safety?

Which diagnostic tests are used in animals to detect SARS CoV-2?

Type of test

Test performance (Se, Sp)

Sample matrix used

ToR2

‘Assess

the current epidemiological situation in the EU and elsewhere as regards the risk for

human and animal health posed by SARS-CoV-2 infection in animals species of concern with a view to

review the design of the existing monitoring performed by the Member States for minks, other animals

of the family

Mustelidae

and raccoon dogs’ is addressed the

ﬁrst

part as descriptive epidemiology of

SARS-CoV-2 outbreaks in animals in EU and worldwide, while the second part is translated into the

question what is the possible exposure and transmission pathways and related risk between the

species assessed as susceptible and other species, mainly due to their capacity of being infected and

further transmit the virus?

ToR 3 about recommending options for reviewing the monitoring strategies in different

epidemiological scenarios,

ﬁrst

the scenarios are deﬁned by the question:

Which monitoring objectives should be set for each susceptible animal category?

For each deﬁned scenario, the following subquestions should be answered:

○

What type of surveillance would be needed (active/passive)?

What type of Diagnostic test?

What type of Sample matrix?

What type of Target population?

What is the sampling frequency?

What is the duration of active monitoring plan?

where applicable, what would be the design prevalence and sample size?

The ToR 4 about disease prevention and control measures can be translated into the following

questions:

•

A.1.5.

What are the preventive measures for SARS-CoV-2 in animals, and their pros and cons?

What are the control measures for SARS-CoV-2 in animals, and their pros and cons?

Assessing and synthesising evidence (including uncertainty

analysis)

Details of the methodology used for the analysis of the data retrieved by the literature review as

well as data from other sources will be provided in the methodology section of the opinion.

All sources of uncertainty identiﬁed during the assessment will be recorded, and their impact on the

scientiﬁc assessment will be assessed collectively.

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SARS-CoV-2 in animals

A.2.

Table A.1:

Animal species considered susceptible to SARS-CoV-2 based on detection of viral RNA in ante-mortem or

post-mortem samples or based on seroconversion

Animal species considered susceptible to SARS-CoV-2 based on detection of viral RNA in

ante-mortem

post-mortem

samples, or based on

seroconversion (please note that some references contain multiple studies)

Route of

inoculation

[IN =

intranasal;

IT =

SARS-CoV-2 isolate Clinical signs

intratracheal;

PO = per

oral; IV =

intravenous]

IN and IT

Aerosol

IN, PO, IT and

conjunctival

SARS-CoV-2/INMI1-

Isolate/2020/Italy

2019-nCoV/USA-WA

1/2020

2019_nCoV Muc-IMB-

WA1/2020WY96

Detection of

viral RNA in

ante-

mortem

samples of

airways (at

least 2

consecutive

days)

Speciﬁcation

animal

Animal species

species and

age

Detection of

viral RNA or

Isolation of

antigen in

infectious

any post

virus

mortem

samples

Seroconversion

(ELISA or

Neutralisation

assay)

Direct

References

transmission

African Green

Monkey

Adult

16 years

Fever and

Yes

reduced appetite

Hypothermia and

respiratory

distress

Yes

Not

investigated

Yes

Not

investigated

Yes

Not

investigated

Woolsey et al.

(2021)

Blair et al.

(2020)

Chlorocebus

aethiops

Bank vole

7–9 weeks

Yes

No evidence

Myodes

glareolus

Bushy-tailed

woodrat

Not reported

Ulrich et al.

(2021)

Bosco-Lauth

et al. (2021)

Yes

Not

investigated

Neotoma

cinerea

Campbell’s

dwarf hamster

Phodopus

campbelli

Cat

5–7 weeks

BetaCoV/Germany/

BavPat1/2020

Yes

Not investigated

Not

investigated

Trimpert et al.

(2020)

15–18 weeks

5–7 months

6–9 months

4.5–5 months

Felis catus

IN, IT, PO and

ocular

IN and PO

UT-NCGM02/Human/

2020/Tokyo

USA-WA1/2020

SARS-CoV-2/Ctan/

human/2020/Wuhan

SARS-CoV-2 USA-

WA1/2020

Yes

Not

investigated

Yes

Halfmann et al.

(2020)

Gaudreault

et al. (2021)

Shi et al.

(2020)

Gaudreault

et al. (2020)

Yes

Mild fever

Not

investigated

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EFSA Journal 2023;21(2):7822

MOF, Alm.del - 2022-23 (2. samling) - Bilag 251: Orientering om opdaterede vurderinger om COVID-19 og mink

SARS-CoV-2 in animals

Speciﬁcation

animal

Animal species

species and

age

Route of

inoculation

[IN =

intranasal;

IT =

SARS-CoV-2 isolate Clinical signs

intratracheal;

PO = per

oral; IV =

intravenous]

IN, IT, PO and

ocular

WA1/2020WY96

UT-NCGM02/Human/

2020/Tokyo

SARS-CoV-2/WH-09/

human/2020/CHN/

MT093631.2

TGR1/NY/20

Detection of

viral RNA in

ante-

mortem

samples of

airways (at

least 2

consecutive

days)

Detection of

viral RNA or

Isolation of

antigen in

infectious

any post

virus

mortem

samples

Seroconversion

(ELISA or

Neutralisation

assay)

Direct

References

transmission

5–8 years

19 weeks

8 months

–

1.5 years

Cattle

6 weeks

4–6 months

Chinese hamster 5–7 weeks

Yes

Not investigated

Bosco-Lauth

et al. (2020)

Chiba et al.

(2021)

Bao et al.

(2021)

Not

investigated

No evidence

Falkenberg et al.

(2021)

Ulrich et al.

(2020)

Bertzbach et al.

(2020)

Xu et al. (2020)

Zhao et al.

(2020)

Arching of back,

diarrhoea

Fever

Yes

Not

investigated

Yes

Not

investigated

Not

investigated

Yes

Bos taurus

Yes

2019 nCoV Muc-IBM-1 No

BetaCoV/Germany/

BavPat1/2020

SARS-CoV-2 strain

107

Not reported

Weight loss

Yes

Not investigated

Cricetulus

griseus

Chinese tree

shrew

1 year and 5–

6 years

6–12 months

and 2–4 years

and 5–7 years

4–20 years

IN, PO and

ocular

Not

investigated

Not

investigated

Fever

Yes

Not

investigated

Not investigated

Tupaia

belangeri

chinensis

Cynomolgus

macaque

IT and IN

BetaCoV/Munich/

BavPat1/2020

Nasal discharge

Yes

Not

investigated

Rockx et al.

(2020)

Macaca

fascicularis

Deer mouse

6 months

8–32 weeks

2019-nCoV/USA-WA1

GISAID #

ID_EPI_ISL_425177

Yes

Peromyscus

maniculatus

nebrascensis

Fagre et al.

(2021)

Grifﬁn et al.

(2021)

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SARS-CoV-2 in animals

Speciﬁcation

animal

Animal species

species and

age

Route of

inoculation

[IN =

intranasal;

IT =

SARS-CoV-2 isolate Clinical signs

intratracheal;

PO = per

oral; IV =

intravenous]

BetaCoV/Germany/

BavPat1/2020

Weight loss

Detection of

viral RNA in

ante-

mortem

samples of

airways (at

least 2

consecutive

days)

Yes

Detection of

viral RNA or

Isolation of

antigen in

infectious

any post

virus

mortem

samples

Seroconversion

(ELISA or

Neutralisation

assay)

Direct

References

transmission

Djungarian

hamster

Phodopus

sungorus

Dog

5–7 weeks

Yes

Not investigated

Not

investigated

Trimpert et al.

(2020)

3 months

5–6 years

1–5 years old

Canis lupus

familiaris

Egyptian fruit

bat

SARS-CoV-2/Ctan/

human/2020/Wuhan

WA1/2020WY96

Yes

No evidence

Not

investigated

Shi et al.

(2020)

Bosco-Lauth

et al. (2020)

Schlottau et al.

(2020)

2019-nCoV Muc-IMB-1 No

Yes

Rousettus

aegyptiacus

Ferret

6–9 months

3–4 months

2019-nCoV Muc-IMB-1 No

SARS-CoV-2/F13/

environment/2020/

Wuhan

BavPat1/2020

hCoV-19/Australia/

VIC01/2020

BetaCoV/Munich/

BavPat1/2020

Victoria/01/2020

BetaCoV/Munich/

BavPat1/2020

MNC-nCoV02

Reduced activity,

sneezing

Fever

Anorexia

Yes

Not

investigated

Not

investigated

Not investigated

Yes

Not

investigated

Yes

Mustela furo

Schlottau et al.

(2020)

Shi et al.

(2020)

Ciurkiewicz

et al. (2022)

Marsh et al.

(2021)

Kutter et al.

(2021)

Ryan et al.

(2021)

Richard et al.

(2020)

Kim et al.

(2020)

8 mtonhs

4 months

6 months

7 months

12–20 months

Not

investigated

Yes

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SARS-CoV-2 in animals

Speciﬁcation

animal

Animal species

species and

age

Route of

inoculation

[IN =

intranasal;

IT =

SARS-CoV-2 isolate Clinical signs

intratracheal;

PO = per

oral; IV =

intravenous]

SARS-CoV-2 HRB25

No signs

Detection of

viral RNA in

ante-

mortem

samples of

airways (at

least 2

consecutive

days)

Yes

Detection of

viral RNA or

Isolation of

antigen in

infectious

any post

virus

mortem

samples

Seroconversion

(ELISA or

Neutralisation

assay)

Direct

References

transmission

Mink

–

Not reported

Yes

Not investigated

Neogale vison

hCoV-19/Finland/THL- Anorexia,

202126660/2021

diarrhoea,

lethargy,

respiratory signs

19 nCoV-CDC-Tan-

GDPCC

Not

investigated

Yes

Shuai et al.

(2021)

Virtanen et al.

(2022)

Mouse

Strain C54BL/6: IN

Mus musculus

8 weeks

Strain BALB/c:

Not

investigated

Yes

Not

investigated

Yes

Not investigated

Yes

Not

investigated

Pan et al.

(2021)

8 weeks

Strain C54BL/6:

8 weeks

France/GES-1973/

2020

France/IDF-IPP11324/

2020

France/IDF-IPP05174/

2021

France/IDF-IPP00078/

2021

FrenchGuiana/

IPP03772/2021

France/IDF-IPP02260/

2021

France/HDF-

IPP11602/2021

Yes

Montagutelli et

al. (2021)

Strain BALB/c:

8 weeks

France/GES-1973/

2020

France/IDF-IPP11324/

2020

France/IDF-IPP05174/

2021

Yes

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SARS-CoV-2 in animals

Speciﬁcation

animal

Animal species

species and

age

Route of

inoculation

[IN =

intranasal;

IT =

SARS-CoV-2 isolate Clinical signs

intratracheal;

PO = per

oral; IV =

intravenous]

France/IDF-IPP00078/

2021

FrenchGuiana/

IPP03772/2021

France/IDF-IPP02260/

2021

France/HDF-

IPP11602/2021

SARS-CoV-2/Ctan/

human/2020/Wuhan

SARS-CoV-2/human/

NL/Lelystad/2020

TGR/NY/20

Detection of

viral RNA in

ante-

mortem

samples of

airways (at

least 2

consecutive

days)

Detection of

viral RNA or

Isolation of

antigen in

infectious

any post

virus

mortem

samples

Seroconversion

(ELISA or

Neutralisation

assay)

Direct

References

transmission

Yes

Not investigated

Yes

Not

investigated

Yes

Fever

Yes

Not

investigated

Yes

Not

investigated

Yes

No evidence

Not

investigated

No evidence

Shi et al.

(2020)

Sikkema et al.

(2022)

Buckley et al.

(2021)

Pickering et al.

(2021)

Schlottau et al.

(2020)

Meekins et al.

(2020)

Mykytyn et al.

(2021)

Francisco et al.

(2022)

Bosco-Lauth et

al. (2021)

Freuling et al.

(2020)

Pig

6 weeks

3 months

3 weeks

IT and aerosol

Sus scrofa

domesticus

8 weeks

9 weeks

5 weeks

Rabbit

3 months

IN and PO

PO, IN and IT

hCoV-19/Canada/ON- Ocular discharge

VIDO-01/2020

2019-nCoV Muc-IMB-1 No

USA-WA1/2020

BetaCoV/Munich/

BavPatl/2020

USA-WA1/2020

WA1/2020WY96

Yes

Not

investigated

Yes

Oryctolagus

cuniculus

Raccoon

10 weeks

Not stated

Raccoon dog

Adult

No (on DPI 1 Yes

only)

Yes

Not

investigated

No evidence

Not

investigated

Procyon lotor

Nyctereutes

procyonoides

2019_nCoV Muc-IMB-

Yes

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SARS-CoV-2 in animals

Speciﬁcation

animal

Animal species

species and

age

Route of

inoculation

[IN =

intranasal;

IT =

SARS-CoV-2 isolate Clinical signs

intratracheal;

PO = per

oral; IV =

intravenous]

IN and IT

IN, IT, PO and

ocular

WA1/2020WY96

Not reported

nCoV-WA1-2020

Lethargy

Fever, respiratory

distress, weight

loss, hunched

posture, nasal

discharge

Reduced

appetite, weight

loss

Detection of

viral RNA in

ante-

mortem

samples of

airways (at

least 2

consecutive

days)

Yes

Detection of

viral RNA or

Isolation of

antigen in

infectious

any post

virus

mortem

samples

Seroconversion

(ELISA or

Neutralisation

assay)

Direct

References

transmission

Red fox

3–5 months

Yes

Vulpes vulpes

Rhesus macaque 7–12 years

Not

investigated

Not

investigated

Porter et al.

(2022)

Yadav et al.

(2021)

Munster et al.

(2020)

Macaca

mulatta

4–6 years

6–11 years

SARS-CoV-2 IVCAS

6.7512

2019-nCoV/USA-WA

1/2020

BetaCoV/Germany/

BavPat1/2020

Not

investigated

Not

investigated

Yes

Not investigated

Not

investigated

Shan et al.

(2020)

Blair et al.

(2020)

Trimpert et al.

(2020)

13–15 years

Aerosol

PO, IN, IT and

conjunctival

Roborovski

dwarf hamster

5–7 weeks

Phodopus

roborovskii

Humane

euthanasia 3–5

DPI due to

severe clinical

symptoms

(weight loss,

respiratory

distress,

hypothermia,

rufﬂed fur)

Skunk

Not reported

10 weeks

WA1/2020WY96

USA-WA1/2020

Yes

Mephitis

mephitis

Not

investigated

No evidence

Bosco-Lauth

et al. (2021)

Francisco et al.

(2022)

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SARS-CoV-2 in animals

Speciﬁcation

animal

Animal species

species and

age

Route of

inoculation

[IN =

intranasal;

IT =

SARS-CoV-2 isolate Clinical signs

intratracheal;

PO = per

oral; IV =

intravenous]

IN and ocular

BetaCoV/Hong Kong/

VM20001061/2020

SARS-CoV-2/UT-

NCGM02/Human/

2020/Tokyo

SARS-CoV-2 isolated

from human patient

TGR/NY/2

SARS-CoV-2/human/

USA/WA1/2020

lineage A and SARS-

CoV-2/human/USA/

CA_CDC_5574/2020

lineage B.1.1.7

Weight loss

Detection of

viral RNA in

ante-

mortem

samples of

airways (at

least 2

consecutive

days)

Yes

Not

investigated

Not

investigated

Yes

Detection of

viral RNA or

Isolation of

antigen in

infectious

any post

virus

mortem

samples

Seroconversion

(ELISA or

Neutralisation

assay)

Direct

References

transmission

Syrian hamster

4–5 weeks

1 months and

7–8 months

6–10 weeks

Yes

Not

investigated

Mesocricetus

auratus

Sia et al.

(2020)

Imai et al.

(2020)

Chan et al.

(2020)

Palmer et al.

(2021)

Cool et al.

(2022)

IN and PO

Not investigated

Yes

White-tailed

deer

6 weeks

2 years

Fever

Ocular discharge

Odocoileus

virginianus

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SARS-CoV-2 in animals

A.3.

Proportion of animals positive (as median and inter-quartile range

(IQR)) to SARS CoV-2 infection in the

ﬁeld

Table

A.2

summarises all mammal species in which SARS-CoV-2 positivity either at virus detection,

PCR or serologically was reported in peer-reviewed literature (based on the SLR), or reported to the

World Animal Health Organisation (OIE), by country. OIE reports were queried in the WAHIS system

on 8 April 2022.

Based on passive (following evidence of clinical signs or epidemiological links to human or animal

cases of SARS CoV-2 infections, suspicion-based) or active (e.g. random sampling) monitoring, in Table

17, the results obtained from SLR about

ﬁeld

infection of different species to SARS CoV-2 are shown,

as proportion of positive animals in each epidemiological unit, tested by PCR/virus isolation or

serological test.

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SARS-CoV-2 in animals

Table A.2:

Proportion of animals positive (as median and inter-quartile range (IQR)) to SARS CoV-2 infection in the

ﬁeld,

per species and epidemiological

unit following passive or active monitoring and according to virus detection/isolation or serological tests. Based on literature screening, only

species found positive are included in the table, and studies including only one animal of this species are excluded from the calculations of

proportions of positives

Passive monitoring (suspicion-based)

Active monitoring (random sampling)

Species

% positive

% positive tested

tested animals

% serologically

animals in each

in each

positive animals

Total no. reference (virus

reference

Total

in each

No. of

isolation or PCR-

no. of (virus isolation

reference

references

positive)

animal

or PCR-

animal

(Median;

(median;

positive)

min–max

min–max)

25th–75th)

(median;

min–max)

Felis catus

725

100%; 0–100%)

(33.33%;

0–100%)

12,531

(0%; 0–2,48%)

(1.79%;

0–22.4%)

Companion

animals/

farmed

animals

Cat

Cattle

Bos taurus

(0%)

1,144

10,971

198

1,121

(0%)

7/3542 (0%;

0–1.32%)

(7.04%)

(16.48%;

0.68–33.44%)

White-tailed

Odocoileus

deer (farmed)

virginianus

Dog

Ferret

American

mink

Syrian

Hamster

Rabbit

zoo animals

Lion

Tiger

Canis familiaris

Mustela furo

Neogale vison

Mesocricetus

auratus

Oryctolagus

cuniculus

Panthera leo

Panthera tigris

823

22,611

(1.95%;

0–100%)

(50.0%;

0–100%)

(61.26%;

0.26–100%)

16.55%

(0%)

(100%;

1166.6–100%)

(100%;

62.5–100%)

(100%;

11%–100%)

(100%;

100%–100%)

(19.16%;

0–100%)

(87.93%;

80.0–100%)

(78.34%;

2–100%)

12.4%

(1.1%;

0–36.36%)

(95.24%;

90.47–100%)

(1.47%;

0–33.33%)

(1.57%)

98.7%;

7.7%–100.0%)

173

(0.69%;

0–1.38%)

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SARS-CoV-2 in animals

Passive monitoring (suspicion-based)

Active monitoring (random sampling)

Species

% positive

% positive tested

tested animals

% serologically

animals in each

in each

positive animals

Total no. reference (virus

reference

Total

in each

No. of

isolation or PCR-

no. of (virus isolation

reference

references

positive)

animal

or PCR-

animal

(Median;

(median;

positive)

min–max

min–max)

25th–75th)

(median;

min–max)

Gorilla gorilla

Prionailurus

bengalensis

Puma concolor

Meles meles

Rhinolophus

acuminatus

Odocoileus

virginianus

Canis aureus

Panthera pardus

Martes

spp.

Neogale vison

Manis javanica

Sus scrofa

Felis catus

Canis familiaris

(100%)

108

247

332

(0%)

(64,29%)

(62.5%)

(0%; 0–25.0%)

(21.42%)

(0%)

(10%)

(1.95%;

0%–3.9%)

(0.95%;

0–3.51%)

(50.0%;

37.5–62.5%)

50%

100%

208

1,464

(13%)

62 (24%;

0%–100%

(0%)

(20%)

(0.46%)

(24%;

0%–100%)

(2.3%; 0–4.6%)

Gorilla

Amur

Leopard cat

Puma

wild animals

Badger

Bat

White-tailed

deer

Jackal

Leopard

Marten

American

mink

Pangolin

Wild boar

Stray animals

cat

dog

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