BEU, Alm.del - 2023-24 - Bilag 61: Orientering om svensk undersøgelse af luftmålinger om krom-6 på svenske virksomheder

Beskæftigelsesudvalget 2023-24
BEU Alm.del Bilag 61
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International Journal of Hygiene and Environmental Health 256 (2024) 114298

Contents lists available at

ScienceDirect

International Journal of Hygiene and Environmental Health

journal homepage:

www.elsevier.com/locate/ijheh

Hexavalent chromium still a concern in Sweden

–

Evidence from a

cross-sectional study within the SafeChrom project

Zheshun Jiang

, Linda Schenk

, Eva Assarsson

, Maria Albin

a, b

, Helen Bertilsson

Eva Dock

a, d

, Jessika Hagberg

, Lovisa E. Karlsson

, Pete Kines

, Annette M. Krais

Stefan Ljunggren

, Thomas Lundh

, Lars Modig

, Rickie Moller

, Daniela Pineda

Niklas Ricklund , Anne T. Saber , Tobias Storsjo , Evana Taher Amir

, Håkan Tinnerberg

i, k

l, m

Martin Tondel , Ulla Vogel , Pernilla Wiebert

b, j

, Karin Broberg

a, b, g, *

, Malin Engfeldt

a, d

Division of Occupational and Environmental Medicine, Department of Laboratory Medicine, Lund University, Lund, Sweden

Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden

Department of Public Health and Clinical Medicine, Sustainable Health, Umeå University, Umeå, Sweden

Occupational and Environmental Medicine, Region Skåne, Lund, Sweden

Department of Occupational and Environmental Health, Faculty of Business, Science and Engineering, Orebro University, Orebro, Sweden

Department of Occupational and Environmental Medicine, Orebro University Hospital, Region Orebro County, Sweden

National Research Centre for the Working Environment, Copenhagen, Denmark

Occupational and Environmental Medicine Center in Link

ping, Department of Health, Medicine and Caring Sciences, Link

ping University, Link

ping, Sweden

Occupational and Environmental Medicine, Sahlgrenska University Hospital, Gothenburg, Sweden

Centre for Occupational and Environmental Medicine, Region Stockholm, Stockholm, Sweden

Occupational and Environmental Medicine, School of Public Health and Community Medicine, Institute of Medicine, University of Gothenburg, Gothenburg, Sweden

Occupational and Environmental Medicine, Department of Medical Sciences, Uppsala University, Uppsala, Sweden

Occupational and Environmental Medicine, Uppsala University Hospital, Uppsala, Sweden

A R T I C L E I N F O

Keywords:

Hexavalent chromium

Occupational cancer

Inhalable

Biomonitoring

Occupational exposure limits

A B S T R A C T

Objectives:

Hexavalent chromium (Cr(VI)) is classified as a human carcinogen. Occupational Cr(VI) exposure can

occur during different work processes, but the current exposure to Cr(VI) at Swedish workplaces is unknown.

Methods:

This cross-sectional study (SafeChrom) recruited non-smoking men and women from 14 companies with

potential Cr(VI) exposure (n

113) and controls from 6 companies without Cr(VI) exposure (n

72). Inhalable

Cr(VI) was measured by personal air sampling (outside of respiratory protection) in exposed workers. Total Cr

was measured in urine (pre- and post-shift, density-adjusted) and red blood cells (RBC) (reflecting Cr(VI)) in

exposed workers and controls. The Bayesian tool Expostats was used to assess risk and evaluate occupational

exposure limit (OEL) compliance.

Results:

The exposed workers performed processing of metal products, steel production, welding, plating, and

various chemical processes. The geometric mean concentration of inhalable Cr(VI) in exposed workers was 0.15

g/m

(95% confidence interval: 0.11–0.21). Eight of the 113 exposed workers (7%) exceeded the Swedish OEL

of 5

g/m

, and the Bayesian analysis estimated the share of OEL exceedances up to 19.6% for stainless steel

welders. Median post-shift urinary (0.60

g/L, 5th-95th percentile 0.10–3.20) and RBC concentrations (0.73

L, 0.51–2.33) of Cr were significantly higher in the exposed group compared with the controls (urinary 0.10

L, 0.06–0.56 and RBC 0.53

g/L, 0.42–0.72). Inhalable Cr(VI) correlated with urinary Cr (r

0.64) and RBC-Cr

0.53). Workers within steel production showed the highest concentrations of inhalable, urinary and RBC Cr.

Workers with inferred non-acceptable local exhaustion ventilation showed significantly higher inhalable Cr(VI),

urinary and RBC Cr concentrations compared with those with inferred acceptable ventilation. Furthermore,

workers with inferred correct use of respiratory protection were exposed to significantly higher concentrations of

Cr(VI) in air and had higher levels of Cr in urine and RBC than those assessed with incorrect or no use. Based on

the Swedish job-exposure-matrix, approximately 17 900 workers were estimated to be occupationally exposed to

Cr(VI) today.

* Corresponding author. Division of Occupational and Environmental Medicine, Department of Laboratory Medicine, Lund University, SE-221 85, Lund, Sweden.

E-mail address:

[email protected]

(K. Broberg).

https://doi.org/10.1016/j.ijheh.2023.114298

Received 11 September 2023; Received in revised form 24 November 2023; Accepted 24 November 2023

BEU, Alm.del - 2023-24 - Bilag 61: Orientering om svensk undersøgelse af luftmålinger om krom-6 på svenske virksomheder

Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

Conclusions:

Our study demonstrates that some workers in Sweden are exposed to high levels of the non-threshold

carcinogen Cr(VI). Employers and workers seem aware of Cr(VI) exposure, but more efficient exposure control

strategies are required. National strategies aligned with the European strategies are needed in order to eliminate

this cause of occupational cancer.

Abbreviations

8-h TWA 8-h time-weighted average

BLV

Biological limit value

BMI

Body mass index

Confidence interval

CIS

Conical inhalable sampler

Chromium

Cr(III)

Trivalent chromium

Cr(VI)

Hexavalent chromium

The European Union

European Commission

EPA

Environmental Protection Agency

G-EQUAS German External Quality Assessment Scheme

Geometric mean

GSP

Gesamtstaubprobenahme sampler

HBM4EU The European Human Biomonitoring Initiative

IARC

International Agency for Research on Cancer

ICP-MS Inductively coupled plasma mass spectrometry

ISCO-08 International Standard Classification of Occupation 2008

JEM

Job-Exposure-Matrix

LEV

Local exhaustion ventilation

LOD

LOQ

MAG

MIG

MMA

NIOSH

OEL

P25

P75

P95

RBC

RBC-Cr

REACH

RPE

SNI

SOP

SSYK

TIG

WBC

Limit of detection

Limit of quantification

Metal active gas

Metal inert gas

Manual metal arc

National Institute for Occupational Safety and Health

Occupational exposure limit

5th percentile

25th percentile

75th percentile

95th percentile

Red blood cells

Chromium concentration in red blood cells

The Registration, Evaluation, Authorisation and

Restriction of Chemicals

Respiratory protective equipment

Swedish Standard Industrial Classification

Standard operating procedure

Swedish Standard Classification of Occupations

Tungsten inert gas

White blood cells

1. Introduction

The element chromium (Cr) is primarily present as trivalent chro-

mium (Cr(III)) and hexavalent chromium (Cr(VI)) in occupational set-

tings (Pan

et al., 2018).

Cr(VI) and its compounds are used in industrial

applications like electroplating and chromate production and Cr(VI) can

also be formed during steel production and welding (IARC,

2012).

Occupational exposure to Cr(VI) can occur through inhalation, dermal

contact and hand-to-mouth exposure (Beattie

et al., 2017).

Cr(VI) is considered to be thousand times more toxic than Cr(III) due

to its oxidizing ability and high solubility, resulting in increased cell

membrane permeability (Saha

et al., 2011; ATSDR, 2011).

Cr(VI) is

classified as a human carcinogen (Group 1) by the International Agency

for Research on Cancer (IARC) and causes lung cancer (IARC,

2012).

Epidemiological evidence suggests that workers exposed to Cr(VI) also

have an increased risk of nose and nasal sinus cancer, and non-cancer

effects, especially in the respiratory and reproductive systems, skin,

kidneys, stomach and liver (IARC,

2018).

Cr(VI) is considered a

non-threshold carcinogen and the guiding principle is that the exposure

should be ‘as low as reasonably achievable’ (Mahiout

et al., 2022).

It is

worth noting that Cr(VI) exposed workers can be occupationally

exposed to other toxic metals, such as nickel and lead, and co-exposure

could play a crucial role in development of adverse health effects

(Muller

et al., 2022).

Exposure to Cr(VI) is often assessed by measurements in air, urine or

blood (Viegas

et al., 2022).

Urinary Cr is a common biomarker with a

half-life of approximately 7 h and post-shift urine is often compared with

pre-shift urine to identify possible work-related Cr exposure (Viegas

et al., 2022).

However, urinary Cr represents total Cr and is therefore not

specific for occupational Cr(VI) exposure (Viegas

et al., 2022; Welinder

et al., 1983).

Red blood cells (RBC) take up Cr(VI) but not Cr(III), and the

Cr concentration in RBC (RBC-Cr) thus reflects the amount of Cr(VI) that

has entered the bloodstream in its non-reduced form (Goldoni

et al.,

2010a).

Since Cr is bound to haemoglobin within the RBC, it is assumed

that the half-life of RBC-Cr in humans corresponds to the half-life of RBC

(Franco,

2012; Ndaw et al., 2022).

It is suggested that RBC-Cr values

reflect the exposure to Cr(VI) over the past four months (Ndaw

et al.,

2022).

In the European Union (EU), the use of Cr(VI) compounds is autho-

rized under the Registration, Evaluation, Authorisation and Restriction

of Chemicals (REACH) regulation (Viegas

et al., 2022).

The current

binding occupational exposure limit (OEL) set under EU Directive

2004/37/EC is 10

g/m

(8-h time-weighted average, 8-h TWA) until

January 17, 2025; after that, the OEL will be 5

g/m

(8-h TWA)

(Santonen

et al., 2022).

In France and the Netherlands, OELs of 1

g/m

have already been set for Cr(VI) (Viegas

et al., 2022).

Denmark has also

implemented an OEL of 1

g/m

and will consider lowering it further to

0.25

g/m (Beattie

et al., 2017; Santonen et al., 2022; Beskæfti-

gelsesministeriet, 2020).

It has been estimated that exposure to air

concentrations of 5

g/m

, the current OEL in Sweden, corresponds to

20 extra lung cancer cases per 1000 exposed workers after 40 years of

occupational exposure (i.e. lifetime risk) (C.

European, 2017).

In Ger-

many and the Netherlands, acceptable risk is considered to be an addi-

tional risk of

cases per 100,000 after 40 years, and tolerable risk

(during a transitional period) is considered to be

4/1000 (Ding

et al.,

2014).

In the 1990s, it was estimated that around 21 000 workers in

Sweden were occupationally exposed to Cr(VI) (Kauppinen

et al., 2000).

However, despite the strong carcinogenicity of Cr(VI), it is not known

how many workers are exposed today and at what levels.

In order to characterize and minimize occupational Cr(VI) exposure

and toxicity in Sweden, all seven Occupational and Environmental

Medicine clinics in Sweden, in collaboration with the Danish National

Research Centre for the Working Environment and the Finnish Institute

of Occupational Health, initiated the SafeChrom project. Specifically,

SafeChrom aims to: 1. characterize Cr(VI) exposure at different

BEU, Alm.del - 2023-24 - Bilag 61: Orientering om svensk undersøgelse af luftmålinger om krom-6 på svenske virksomheder

Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

workplaces by air monitoring of inhalable Cr(VI) and biomonitoring of

Cr in urine and RBC and to identify adequate monitoring methods for Cr

(VI) exposure; 2. investigate toxicity of current exposure levels by

measuring early markers of Cr(VI)-related chromosome damage and

DNA modifications; 3. evaluate the perception of regulations and risk

management strategies at workplaces using Cr(VI); 4. take advantage of

the Nordic expertise and increase the study base for examining occu-

pational Cr(VI) exposure; 5. develop guidelines for minimizing Cr(VI)

exposure. Here we present the results of the first study aim of

SafeChrom.

2. Material and methods

2.1. Study participants and recruitment

This cross-sectional study of Cr(VI) exposure in the Swedish work

environment (SafeChrom) was carried out by all seven Occupational and

Environmental Medicine clinics in Sweden (Lund, Gothenburg, Link-

oping, Orebro, Stockholm, Uppsala, and Umeå) in collaboration with

their corresponding university divisions. The occupational exposure

assessment, along with the sampling of air, blood, and urine were per-

formed by standard operating procedures (SOPs) used by all partners.

The study and the questionnaire were designed to be as similar as

possible to The European Human Biomonitoring Initiative (HBM4EU)

chromates study protocol (Santonen

et al., 2019).

The recruitment of

study participants in the exposed group was performed between June

2021 and May 2022. Identification of suitable companies was done

either by a) request of interest sent out to customers of Cr analyses

(mainly occupational health care services or occupational safety and

health consultants distributed all over Sweden) informing about the

study or b) occupational hygienists at each clinic that identified com-

panies with potential Cr(VI) exposure in the respective region.

Recruitment was performed by each clinic in a harmonized way: 1.

occupational hygienists contacted the companies via e-mail or phone,

and invited the companies to join the project; 2. managers received an

information leaflet about the background and aim of the project and the

sampling plan; 3. managers informed employees about the study and

identified workers willing to participate in the project; 4. a work site

visit was conducted before the measurements to plan the sampling and

to provide further information about the study; and 5. finally, a visit was

scheduled to the company for air measurement, along with collecting

blood and urine samples from workers who agreed to participate. Bio-

logical sampling was performed when the study participants had worked

for at least three previous consecutive days (for those who worked

Monday to Friday, sampling was carried out on Wednesday at the

earliest).

Controls were recruited between March 2022 to October 2022 from

occupational groups that were considered to have the same gender, a

similar socioeconomic status, education, and exposure to physical

workload but no genotoxic exposures (e.g. from metals, particles or

organic chemicals) as exposed workers. The recruitment procedure of

controls was the same as for the exposed workers. The sampling for

controls was the same as for the exposed workers except that no air

measurement was performed, and biological sampling was possible each

working day. The recruitment of controls took place in southern and

middle Sweden.

The inclusion criteria for the exposed workers were potential expo-

sure to Cr(VI), being 20–68 years of age, and non-smoker

months (as

tobacco smoke may contain Cr(VI) (Rowbotham

et al., 2000)).

The in-

clusion criteria of the control group were the same as the exposed group

except that they should not have a potential exposure to Cr(VI) or other

genotoxic agents via work. All study participants answered the same

questionnaire, except for questions relating to work tasks that differed

between exposed workers and controls. All study participants gave

informed written consent to participate in the study. The study was

approved by the Swedish Ethical Review Authority (Dnr 2021-00641).

2.2. Categorisation of companies and work tasks for exposed workers

Based on the expertise of the occupational hygienists, a catego-

risation of the companies was carried out according to the Swedish

Standard Industrial Classification (SNI 2007). In addition, companies

were categorised into four groups: manufacture/processing of metal

products, steel production, bath plating and non-categorised (two

companies that could not be classified into any of the previous cate-

gories) (Supplementary

Table 1).

One of the included companies had

two different divisions and was thus categorised into both steel pro-

duction and manufacture/processing of metal products. Based on the

expertise of the occupational hygienists and the work tasks performed

on the sampling day, a descriptive categorisation of the work tasks was

carried out according to the Swedish Standard Classification of Occu-

pations 2012 (SSYK 2012, 4-digit), which is based on the International

Standard Classification of Occupation 2008 (ISCO-08). In addition, work

tasks were categorised into four groups: welding, process operation,

machining, and others (Supplementary

Table 2).

2.3. Air monitoring

2.3.1. Sampling

The inhalable Cr(VI) fraction was collected using a conical inhalable

sampler (CIS) (Casella, Rutland, United States) mounted with a 37 mm

polyvinyl chloride filter, pore size 5

m (Merck Millipore, Cork, Ireland).

Battery-powered sampling pumps were used to provide a flow rate of

3.5 L/min, which was regularly checked with a digital flow meter

before, during, and after sampling. Due to a temporary shortage of CIS

from Casella, another type of CIS was used: ten individuals were

sampled with a Gesamtstaubprobenahme sampler (GSP) mounted with

the same filter and run at the same flow rate. Measurements were

generally performed during full-shift work, with an average measure-

ment time of 6.7 h. The sampler was placed within the breathing zone.

For workers who were wearing respiratory protection equipment (RPE)

(e.g powered air-purifying respirators, full- or half mask, or filtering half

mask) during sampling, the air outside the RPE was sampled. At least

one field blank was collected per sampling day. If the number of sampled

individuals per day exceeded 10, two field blanks were collected. Field

blanks were sampled by connecting the sampler to the pump without

drawing any air through it whilst mounting and dismounting the

equipment used for the participants at the beginning and the end of the

day. Field blanks were analysed in parallel with the samples.

2.3.2. Chemical analysis

Filter samples of inhalable Cr(VI) were sent for analysis to the

Occupational and Environmental Medicine Laboratory, University

Hospital, Orebro. The samples were analysed by a method modified

from the National Institute for Occupational Safety and Health (NIOSH)

(NIOSH,

2003).

The samples were placed in glass tubes and a 5 ml so-

lution containing sodium hydroxide (1 g/L) and sodium carbonate (1.5

g/L) was added to each tube. The filters were then extracted in an ul-

trasonic bath for 35 min at 40

◦

C. Solid residues were separated from the

samples by centrifugation at 2000 rpm for 10 min. Cationic metals were

removed from the samples by solid phase extraction using Dionex

OnGuardTM II M columns (Thermo Fisher Scientific, GmbH, Bremen,

Germany) and vacuum filtration. The liquid samples were transferred to

autosampler vials. Calibration solutions in six different concentrations

(30–2000 ng/ml) were diluted from a 1000

g/ml certified stock solu-

tion (Spectrascan, Ski, Norway). The calibration solutions were diluted

with the same extraction solution used for the samples. The samples

were analysed by ion chromatography with conductivity detection

(Thermo Fisher Scientific, GmbH, Bremen, Germany, Dionex ICS-2100).

The guard and separation columns used were model Dionex IonPacTM

AG15-5

m and AS15-5

m, respectively. Ten filter blanks (i.e.

non-exposed PVC filters) were extracted and analysed for the calculation

of limit of detection (LOD). Mean value and standard deviation were

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Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

calculated. The LOD was calculated using the following formula: LOD

mean value

standard deviation. The LOD was 0.08

g/sample. The

laboratory regularly participates in LGC AXIO proficiency testing

scheme for air and stack emissions (LGC AXIO PT AIR). During the

measurement campaign, proficiency tests showed good agreement be-

tween measured Cr(VI) concentrations in quality control samples and

assigned concentrations.

Due to delayed delivery of solid phase extraction columns, four

samples were analysed by ALS Scandinavia AB in Luleå by a method

based upon SS-EN ISO 17294-2:2016 (CEN) and EPA Method

200.8:1994 (EPA

US, 1994)

using inductively coupled plasma mass

spectrometry (ICP-MS) after alkaline leaching of Cr(VI) according to ISO

15192:2006 (CEN,

2006).

The ALS laboratory used the limit of quanti-

fication (LOQ) as limit of the applied method and six filter blank samples

were extracted and analysed for the calculation of LOQ. Mean value and

standard deviation were calculated. The LOD was calculated using the

following formula: LOQ

mean value

standard deviation. The

LOQ was 0.3

g/sample.

2.4. Biological monitoring

2.4.1. Sampling

An informed consent form and a urine sampling kit (including in-

struction, two acid-washed tubes, and one acid-washed cup) for the pre-

shift urine was sent out to every participant before the sampling day. On

the day of the visit, trained nurses collected the signed informed con-

sent, the pre-shift urine sample and sampled blood and post-shift urine

(after the workers had worked at least 4 h). The biological sampling was

performed on the same day as the measurements of inhalable Cr(VI)

fraction. Blood samples were collected in four vacutainer tubes (Becton,

Dickinson and Company, Plymouth, UK): one sodium-heparin tube for

analysis of metals, one lithium-heparin tube for micronuclei, one

vacutainer EDTA tube for other biomarkers of genotoxicity, and one

PAXgene blood RNA tube for RNA (the last three tubes were not

included in this study). Urine and blood samples were kept at 4

◦

C and

transported to the laboratory at the Div. of Occupational and Environ-

mental Medicine, Lund University. After separating blood cells and

plasma from whole blood in the sodium-heparin tubes (details described

below), all blood and urine samples were stored at 20

◦

C until analysis.

In the exposed group, three participants abstained from providing

blood samples, and one abstained from providing pre-shift urine sample.

2.4.2. Chemical analysis

Tubes and tips used in the chemical analysis were washed with acid

(5% HNO

and 5% HCl) to remove potential metal contamination. To

avoid haemolysis, plasma and RBC separation was conducted following

the method described by

Devoy et al. (2016).

Blood samples were

separated for 10 min at 1300 g, and the plasma supernatant was

removed. After the separation, a wash step was conducted by adding

0.9% isotonic saline (with a volume corresponding to the initial blood

volume) to the RBC, gently rocked for 5–10 min, separated for 10 min at

1300 g, whereafter the supernatant was removed. The wash was per-

formed two more times before the RBC were processed for metal

analysis.

Cr(VI) exposed workers can be exposed to other toxic metals during

work, thus manganese, cobalt, nickel, copper, zinc, selenium, cadmium,

antimony, mercury, and lead were measured along with Cr. All de-

terminations were performed with ICP-MS (iCAP Q, Thermo Fisher

Scientific, Bremen, accuracy GmbH) equipped with collision cell with

kinetic energy discrimination and helium as collision gas. A sample

volume of 100

L (RBC) and 250

L (urine) was diluted 20 times with an

alkaline solution according to

Barany et al. (1997)

and analysed in

peak-jumping mode, with scandium, rhodium, terbium, and iridium

used as internal standards. The detection limits were calculated as three

times the standard deviation (SD) of the blank and were 0.20

g/L both

for Cr in blood and urine. All analysed samples were prepared and

measured in duplicate, and the mean value was used in subsequent

statistical analyses. During the measurement campaign, the laboratory

participated in the German External Quality Assessment Scheme

(G-EQUAS), with good agreement between obtained element concen-

trations in quality control samples used and expected values. The

analytical accuracy was verified towards certified reference materials

from G-EQUAS and SERO AS, Billingstad, Norway (Seronorm). The re-

sults (

g/L, mean

SD) obtained for Seronorm (Lot. 2011920) were for

Cr in blood 0.63

0.06 vs. recommended 0.48–0.75 and for G-EQUAS

Cr in blood (Lot. R64 1A) 1.80

0.21 (n

49) vs. recommended

1.1–2.3. For G-EQUAS Cr in urine (Lot. R64 8A and R64 2A) the results

obtained were 0.22

0.03 vs. recommended 0.16–0.34 and 3.67

0.28

vs. recommended 2.8–4.0, respectively. Quality data for the other

metals analysed are shown in

Supplementary Table 3.

2.5. Measurement of creatinine and density in urine

Density and creatinine were measured in all urine samples for

correction of dilution. The density was measured with a hand-held

refractometer (30PX; Mettler Toledo, USA). The density adjustment

was calculated using the following formula: C(

density-adjusted

)

(1-

mean

)/(1-

sample density

), where C

the determined Cr concentration in

the sample,

mean

the mean of the urinary density of all participants,

and

sample density

the density of the urine sample. Creatinine was

measured with Atellica (Siemens Healthcare Diagnostics, Munich, Ger-

many; accredited analysis) at the Clinical Chemistry University Hospital,

Lund. Since creatinine excretion often is higher in men (due to gender

differences in muscle mass (Thomas

et al., 2012)),

density adjustment

was more appropriate for the correction of urinary dilution. Neverthe-

less, we also present the creatinine-adjusted urinary Cr for comparison

with other studies.

2.6. Questionnaire and occupational hygienist protocol

A questionnaire was sent to each participant in advance. On the day

of the visit, trained nurses checked that the questionnaires were

completed. The questionnaire contained questions about birth year,

height, weight, residential area, smoking (current smoker, former

smoker, party smoker, and non-smoker), use of electronic cigarettes and

snuff, consumption of alcoholic beverages, coffee, tea, energy drinks,

and supplements, diet, implants, and any leisure activities that may

result in exposure to Cr (e.g. welding, spray painting and metal work).

Moreover, the questionnaire inquired about the respondent’s working

situation, including working years, working tasks, working place (out-

door or indoor), working shift, and hygiene options (changing rooms

and opportunity to shower and wash hands). In addition, the question-

naire given to the exposed group enquired about the details of their

working tasks (i.e.

“plating”, “painting”, “grinding”, “welding”, “ther-

mal spraying”,

“metal

production”, and

“working

in close connection

with the tasks above”), working hour (5 categories, from never to about

3/4 of the working time), performing tasks manually or automatically,

and use of personal protective equipment (nothing, compressed air or

fresh air supplied breathing apparatus, fan-assisted respiratory protec-

tion, reusable respirators (half mask or full mask), disposable protection

(filtering half mask), full protective overalls, gloves, apron), and use of

stationary fume extraction.

During air sampling, the occupational hygienist filled in an obser-

vation protocol for the workplace, as well as an individual observation

protocol for each sampled individual. The occupational hygienist asked

about details of the company (number of employees, production, num-

ber of Cr exposed workers, working shift and working hours), produc-

tion conditions during measurement (3 categories; low, normal, high),

description of the design of the premises, general ventilation (mechan-

ical, windows, doors, and no ventilation), and process ventilation

(containment of emission source and point extraction at emission

source) were recorded. Further, the occupational hygienist made an

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Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

ocular assessment of the use and standard of local exhaustion ventilation

(LEV) and RPE on sampling day. Based on these ocular observations LEV

was categorised as either

“inferred

acceptable” or

“inferred

non-

acceptable” while use of RPE was categorised as

“yes

and correctly”,

“yes

but not correctly” or

“no”.

Acceptable LEV was defined as working

conditions inferred as providing air quality in which additional RPE was

not needed. The workplaces where LEV was considered as not adding

additional value beyond the general ventilation were also categorised as

“inferred

acceptable” LEV for the analyses herein. Inferred correct use of

RPE was defined as: 1. using RPE when needed; 2. using the correct type

of filter; 3. regular filter changes, and 4. correct storage of RPE when not

used.

2.7. Risk assessment

In order to assess risk and evaluate OEL compliance, the Bayesian

tool Expostats (Tool 1) was employed to assess the expected extent of

OEL exceedances in the sampled population (Lavou

et al., 2019).

The

occupational and workplace categories were used in the present work to

identify similar exposure groups. The category ‘other work tasks’ was

not included as it does not represent the same work tasks across com-

panies. We evaluated compliance with the current Swedish OEL (5

g/m

) and also estimated the share that would be expected to exceed 1

g/m

and 0.25

g/m

, respectively. We defined overexposure as 5% of

the population exceeding the exposure limit, and evaluated the proba-

bility of overexposure using the thresholds 30% (as proposed by e.g.

CEN 2019 (CEN).

The estimations of workers exposed to Cr(VI) in Sweden was per-

formed using a job-exposure-matrix (JEM) linked to register data on

occupation from Statistics Sweden. The JEM was originally based on the

Finnish JEM (Kauppinen

et al., 1998)

and later updates (Kauppinen

et al., 2014).

The estimated prevalence is for workers ever exposed

during a year, meaning that some of them can have very low prevalence,

maybe one time per year. Adaptions to Swedish working conditions have

been made by Wiebert and Tinnerberg et al. (Gustavsson

et al., 2022).

2.8. Statistical analysis

For inhalable Cr(VI), 51 samples analysed in Orebro (concentrations

below the LOD (0.08

g/sample)) and 2 samples analysed in Luleå

(below the LOQ (0.3

g/sample)) were substituted by values equal to

half of the LOD (0.04

g/sample) or LOQ (0.15

g/sample) (Hornung

and Reed, 1990).

Age was calculated based on birth and recruitment

dates. Body mass index (BMI) was obtained using the formula BMI

weight in kilograms/(height in meters) (IARC,

2012).

Descriptive sta-

tistics including geometric mean (GM), 95% confidence interval (CI),

median, 5th and 95th percentiles (P5, P95) were calculated.

Mann-Whitney

test, Kruskal-Wallis test and Wilcoxon signed ranks

test were used to compare differences between continuous variables.

The Chi-square test and Fisher’s exact test were used to compare dif-

ferences in distribution of categorical variables between groups.

Spearman’s correlation was used to examine correlations between

variables.

Multiple regression models were built to evaluate differences in Cr

concentration between the exposure group and controls, adjusting for

potential covariates and confounders. Possible confounders of exposure

¨¨ ¨

to Cr(VI) or Cr(III) were: smoking (P

aakko et al., 1989),

coffee (Olechno

et al., 2021)

and tea (Barman

et al., 2020)

drinking, diet (Smart

and

Sherlock, 1985),

supplement (Saper

et al., 2004),

implant (Campbell

and

Estey, 2013)

and leisure activity with Cr. Three models were built:

model 1 without adjustment; model 2 adjusted for variables that had a

significant difference in the bivariate analysis between exposed workers

and controls; model 3 adjusted for all potential confounders. To deal

with skewed data, log transformation was used for the urinary and RBC

Cr.

The statistical analyses above were conducted with SPSS 28.0 (IBM

SPSS Statistics, NY) and statistical significance (two-tailed) was denoted

value

0.05.

3. Results

3.1. Characteristics of the study participants

A total number of 44 companies with potential occupational expo-

sure to Cr(VI) were contacted by the occupational hygienists, and 14

companies, geographically distributed from north to south of Sweden,

agreed to participate (company participation rate 31.8%). Companies

that did not participate did either: 1. not reply to the occupational hy-

gienists; 2. not want to participate; or 3. not fulfill the inclusion criteria

because of ceased or sporadic exposure to Cr(VI). The tasks performed

by workers at the participating companies included production of

stainless steel, welding, grinding, plating, surface treatment, and various

chemical processes. The volunteers in the control group were recruited

from one agricultural operator, one care home, two construction com-

panies, one storage company, and one restaurant (company participa-

tion rate 66.7%).

One hundred and sixteen air samples were collected, but one pump

did not work, thus 115 valid inhalable Cr(VI) results were obtained.

Three exposed workers only provided air samples, and the remaining

113 workers completed the questionnaire and donated biological sam-

ples. Categorisation, number of individuals for each company, and their

work tasks are shown in

Table 1.

The demographic characteristics, lifestyle, and work-related factors

of the exposed workers and controls are summarised in

Table 2.

The

exposed workers and controls were similar in BMI, smoking history,

coffee drinking, use of supplements, presence of implants, and leisure

activities with Cr. However, significant differences (P

0.05) were

found with respect to age, sex, and tea drinking between the two groups.

Participants in the exposed group were younger, more likely to be male

and less likely to drink tea than those in the control group. There were

35.4% exposed workers with inferred non-acceptable LEV, and 54% did

not use RPE on the sampling day. Fifteen exposed workers (13.2%) had

non-acceptable LEV and did not use RPE.

3.2. Cr(VI) in air

The inhalable Cr(VI) concentrations are presented in

Table 3.

There

were 74 samples below 0.25

g/m

, 20 samples between 0.25 and 1

, 13 samples between 1 and 5

g/m

and eight samples higher than 5

g/m

(Fig.

1A).

The GM and 95% CI of inhalable Cr(VI) in the exposed

group were 0.15 and 0.11–0.21

g/m

, but the P95 was 8.03

g/m

(Table

3).

At company level, steel production had the highest GM and

non-categorised companies had the lowest (P

0.05). In relation to

work tasks, process operators had the highest GM, and machining

workers the lowest GM, but no significant difference was found between

work tasks (Table

and

Fig. 1B).

Workers with inferred non-acceptable

LEV were exposed to around two times higher levels of inhalable Cr(VI)

compared with those with inferred acceptable LEV (P

0.05), and

workers with inferred correct use of RPE on the sampling day were

exposed to significantly higher inhalable Cr(VI) compared with those

who did not use RPE or had inferred incorrect use (P

0.001) (Fig.

2A).

Stratified analysis showed that among workers with acceptable LEV, a

significant difference in inhalable Cr(VI) was found between different

usage of RPE. A significant difference was also found between different

usage of RPE among the workers with non-acceptable LEV (Supple-

mentary Fig. 1A).

3.3. Risk assessment

Table 4

shows the estimated likelihood of overexposure when using

the Bayesian analysis performed by Expostats. The estimated fractions of

exceedances over the Swedish OEL ranged from 0.02 % for machining in

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Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

Table 1

Categorisation in SafeChrom of 14 companies (15 work sites) and work task for individuals (n

116, exposed group) for whom air sampling was performed.

SafeChrom Categorisation

Manufacture/processing of metal products

Steel production

Bath plating

Non-categorised

Total

Companies

Work task on sampling day

Welding

Process operation

Machining

Others

Total individuals n

116

One company with two different work sites was categorised into both steel production and manufacture/processing of metal products.

Two companies that could not be classified in manufacture/processing of metal products, steel production or bath plating were classified as non-categorised

(details in

Supplementary Table 1).

Table 2

Characteristics of the study groups in SafeChrom.

Exposed group

113

Age, median (P5, P95)

Female, n (%)

BMI

, median (P5, P95)

Smoking, n (%)

Never smoker

Previous smoker

Party smoker

Current smoker

Coffee drinking (yes/no), n (%)

Tea drinking (yes/no), n (%)

Diet (mix, vegetarian, vegan), n

(%)

Supplement (yes/no), n (%)

Implant (yes/no), n (%)

Leisure activity with Cr (yes/

no), n (%)

LEV

(inferred acceptable/non-

acceptable), n (%)

RPE

(yes and correctly/yes but

not correctly/no), n (%)

Controls group

43.5 (27.7,60.4)

22 (30.6)

27.2 (20.6,

35.1)

45 (62.5)

23 (31.9)

2 (2.8)

56/16 (77.8/

22.2)

34/38 (47.2/

52.8)

70/1/1 (97.2/

1.4/1.4)

21/51 (29.2/

70.8)

12/60 (16.7/

83.3)

4/68 (5.6/94.4)

0.016

<0.001

0.368

0.854

Table 3

Concentrations of inhalable hexavalent chromium (Cr(VI);

g/m

) measured in

the exposed group and stratified by company and work task.

<LOD/

LOQ n

(%)

Exposed group, N

115

Company

Manufacture/

processing of metal

products, n

Steel production, n

Bath plating, n

Non-categorised, n

Work task

Welding, n

Process operation,

Machining, n

Others, n

GM (CI)

b,c

Median

39 (21.7, 60.3)

15 (13.3)

27.9 (20, 37.6)

68 (60.2)

35 (31)

6 (5.3)

4 (3.5)

96/17 (85/15)

35/77 (31.9/

68.1)

113/0/0 (100/

0/0)

32/81 (27.4/

72.6)

11/102 (11.5/

88.5)

10/103 (8.8/

91.2)

73/40 (64.6/

35.4)

30/22/61

(26.5/19.5/54)

P5,

P95

0.02,

8.03

0.02,

13.58

0.03,

9.78

0.03,

1.92

0.02,

0.28

0.02,

14.73

0.02,

6.93

0.02,

0.44

0.02,

2.55

54 (47)

0.15

(0.11–0.21)

0.12

(0.07–0.21)

0.30

(0.17–0.55)

0.15

(0.07–0.29)

0.04

(0.02–0.08)

0.17

(0.08–0.37)

0.19

(0.12–0.31)

0.05

(0.03–0.11)

0.09

(0.04–0.21)

0.1

(57.9)

8 (25)

7 (38.9)

6 (75)

0.03

0.25

0.10

0.02

0.001

0.24

0.042

0.205

0.177

0.571

(48.4)

(37.9)

8 (72.7)

9 (60)

0.10

0.16

0.04

0.151

Mann-Whitney

test.

Chi-square test.

Fisher’s exact test.

BMI, body mass index.

LEV, Local exhaustion ventilation.

Using respiratory protective equipment (RPE) on sampling day.

Kruskal-Wallis test.

GM, Geometric mean, CI: 95% confidence interval of the geometric mean.

Concentrations below the limit of detection (LOD) and limit of quantification

(LOQ) were substituted by a value equal to half of the LOD/LOQ.

manufacture/processing to 8.8 % for welding in manufacture/process-

ing with the 95% credible interval ranging up to 19.6% for the welders.

Only three groups had less than 30% probability of overexposure of the

Swedish OEL (shown by the shading in

Table 4),

defined as 5% or more

exceeding the OEL. All groups had more than 30% probability of over-

exposure for the upcoming Danish OEL (0.25

g/m3).

In order to identify how many workers are at risk for exceeding the

Swedish OEL, the total number of workers exposed to Cr(VI) in Sweden

was estimated. Initially, different branch organizations were contacted

but no information on numbers of exposed workers could be retrieved.

Thus, estimations were done using the Swedish JEM: in 2021, approx-

imately 16 000 men and 1900 women distributed within 14 different

occupations were estimated to be exposed to Cr(VI). Among those, 2570

were welders.

3.4. Cr in urine and red blood cells

The Cr concentrations in urine and RBC are presented in

Table 5.

Both pre-shift and post-shift urinary Cr in the exposed group were

significantly higher compared with controls (P

0.001). In the exposed

group, but not among the controls, Cr concentrations in after-work urine

were statistically significantly higher than in the pre-shift urine. In

addition, the difference between post-shift and pre-shift urinary Cr

concentrations in the exposed group were significantly higher than the

controls (Supplementary

Table 4).

The median RBC-Cr in the exposed

group was significantly higher than in the controls.

The workers in non-categorised companies had the lowest post-shift

urinary Cr/density and RBC-Cr, while those working in steel production

had the highest urinary and RBC Cr (P

0.01). Among different work

tasks, machining workers had the lowest post-shift urinary Cr/density. It

was significantly lower than the welders, but non-significantly higher

than the controls (P

0.068). For RBC-Cr, machining workers had

significantly higher concentrations than the controls, but not signifi-

cantly different from exposed workers doing other work tasks

(Fig.

1C–D).

Regarding using LEV and RPE, urinary and RBC Cr concentrations

showed a similar trend as the inhalable Cr(VI). Workers with inferred

non-acceptable LEV had higher urinary and RBC concentrations than

those with inferred acceptable LEV. Contrarily, workers who were

assessed to use RPE correctly on the sampling day had higher concen-

trations of Cr in urinary and RBC than workers who did not (Fig.

2B–C).

Stratified analysis for acceptable and non-acceptable LEV, showed that

BEU, Alm.del - 2023-24 - Bilag 61: Orientering om svensk undersøgelse af luftmålinger om krom-6 på svenske virksomheder

Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

Fig. 1. Inhalable hexavalent chromium (Cr(VI)), urinary and red blood

cells (RBC) Cr in controls and exposed workers across company and work

task.

A. Frequency distribution histogram for inhalable Cr(VI). B. Inhalable Cr

(VI). Kruskal-Wallis Test, *P

0.05. C. Post-shift urinary Cr/density. Kruskal-

Wallis Test and Mann-Whitney

test, **P

0.01, ***P

0.001. D. RBC-Cr.

Kruskal-Wallis Test and Mann-Whitney

test, **P

0.01, ***P

0.001. The

data are presented as geometric mean and 95% CI for inhalable Cr(VI), median

and interquartile range for post-shift urinary Cr/density and RBC-Cr. (For

interpretation of the references to colour in this figure legend, the reader is

referred to the Web version of this article.)

Fig. 2. Inhalable hexavalent chromium (Cr(VI)), urinary and red blood

cells (RBC) Cr in exposed group according to the local exhaustion venti-

lation (LEV) and using respiratory protective equipment (RPE).

A. Inhal-

able Cr(VI). B. Post-shift urinary Cr/density. C. RBC-Cr. Mann-Whitney

test,

0.05, **P

0.01, ***P

0.001. The data are presented as geometric mean

and 95% CI for inhalable Cr(VI), median and interquartile range for post-shift

urinary Cr/density and RBC-Cr. LEV and RPE centered under inferred

acceptable/non-acceptable and yes, and correctly/yes, but not correctly/no,

respectively. (For interpretation of the references to colour in this figure legend,

the reader is referred to the Web version of this article.)

among workers with acceptable LEV, there were less pronounced dif-

ferences in urinary and RBC Cr between usage of RPE. However, with

non-acceptable LEV, workers using RPE correctly still showed the

highest urinary and RBC Cr (Supplementary

Figs. 1B–C).

When urinary and RBC Cr concentrations were compared to the P95

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Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

Table 4

Estimated exceedance fractions of hexavalent chromium for 5, 1 and 0.25

g/m

across the different expo-

sure groups using Expostats.

The shading indicates that the probability of overexposure (defined as an exceedance fraction

>5%)

is more

than 30%.

Table 5

Chromium (Cr) concentration in urine and red blood cells.

Median (P5, P95)

Pre-shift urine

Post-shift urine

Red blood cells

3.6. Further elements in red blood cells and post-shift urine

Control group

0.10 (0.01, 0.45)

0.08 (0.01, 0.54)

0.10 (0.01, 0.84)

0.11 (0.04, 0.30)

0.10 (0.03, 0.58)

0.10 (0.06, 0.56)

0.53 (0.42, 0.72)

Exposed group

0.54 (0.08, 2.91)

0.33 (0.05, 1.75)

0.51 (0.07, 2.44)

0.55 (0.10, 3.83)

d, e

0.41 (0.08, 2.12)

d, g

0.60 (0.10, 3.20)

d, f

0.73 (0.51, 2.33)

Cr (

g/L)

Cr (

g/g creatinine)

Cr/density

Cr (

g/L)

Cr (

g/g creatinine)

Cr/density

Cr (

g/L)

Pre-shift urine (exposed group n

112, control group n

72).

Post-shift urine (exposed group n

113, control group n

72).

Red blood cells sample was collected with post-shift urine (exposed group n

110, control group n

72).

Exposed group vs. control group, Mann-Whitney

test,

0.001.

Post-shift urine vs. pre-shift urine in exposed group, Wilcoxon signed ranks

test, P

0.05

Post-shift urine vs. pre-shift urine in exposed group, Wilcoxon signed ranks

test, P

0.01

Post-shift urine vs. pre-shift urine in exposed group, Wilcoxon signed ranks

test, P

0.001

of controls (reference value), 42 exposed workers were below the P95 of

controls’ urinary and RBC Cr; 10 exceeded the P95 of urinary Cr but

were below the P95 of RBC-Cr; 13 exceeded P95 of RBC-Cr but were

below the P95 of urinary Cr; 45 exceeded both P95 of urinary and RBC

Cr. Among the latter 45 individuals, 15 had exposure measurements of

less than 0.25

g/m

of inhalable Cr(VI) (Supplementary

Table 5).

3.5. Inhalable Cr(VI), urinary and RBC Cr in welders

Four types of welding processes (manual metal arc (MMA), metal

active gas (MAG), metal inert gas (MIG) and tungsten inert gas (TIG))

were performed by 30 welders, including 14 welders that performed

more than one type of welding (data not shown). The most common

welding process reported was TIG (n

24). Workers using TIG had the

lowest level of inhalable Cr(VI) (GM 0.11

g/m

) and workers welding

using MMA had the highest (GM 1.13

g/m

) (P

0.02). The same

pattern was found in urinary and RBC Cr: workers using TIG had the

lowest (median 0.54 and 0.74 for urinary and RBC Cr, respectively) and

workers using MMA had the highest (median 1.45 and 0.82 for urinary

and RBC Cr, respectively), but without significant difference between

types of welding (P

0.41 for urinary Cr and

0.33 for RBC-Cr).

For workers exposed to Cr(VI), they might be exposed to other

metals. Hence manganese, cobalt, nickel, copper, zinc, selenium, cad-

mium, antimony, mercury, and lead were also measured in urine (den-

sity-adjusted) and RBC (Supplementary

Table 6).

Post-shift urinary

copper concentrations were significantly higher in Cr(VI)-exposed

workers (median 9.77

g/L) compared with controls (8.41

g/L). Uri-

nary nickel and lead were non-significantly higher in Cr(VI)-exposed

workers. In RBC, copper and zinc concentrations were significantly

higher in the Cr(VI)-exposed workers (571

g/L for copper and 10728

g/L for zinc) compared with the controls (525

g/L for copper and

10496

g/L for zinc). Cr(VI)-exposed workers had higher RBC concen-

trations of cobalt and lead than controls, but not statistically significant.

Controls had significantly higher antimony concentrations both in urine

(0.57

g/L) and RBC (5.30

g/L) compared with Cr(VI)-exposed workers

(0.08

g/L in urine and 4.46

g/L in RBC).

Similar to Cr, we divided other metals in urine and RBC according to

the company and work task (Supplementary

Table 7).

There were sig-

nificant differences between companies in median urinary concentra-

tions of nickel (highest in steel production and lowest in bath plating),

copper (highest in non-categorised and lowest in bath plating), zinc

(highest in non-categorised and lowest in bath plating), and lead

(highest in steel production and lowest in manufacture/processing of

metal products. There were significant differences between companies

in median RBC concentrations of antimony (highest in manufacture/

processing of metal products and lowest in non-categorised) and lead

(highest in steel production and lowest in non-categorised). Further-

more, for work tasks, there was a significant difference in urinary me-

dian concentrations of cobalt (highest in welding and lowest in

machining). For work tasks median RBC concentrations differed for

nickel (highest in others and lowest in machining) and mercury (highest

in others and lowest in process operation).

Correlations between metals in RBC in Cr(VI)-exposed workers are

presented in

Supplementary Fig. 2.

The strongest correlations were

found between cobalt and nickel (r

0.53). Positive correlations be-

tween zinc and copper as well as between zinc and selenium were also

observed (r

0.46 and r

0.44, respectively). The strongest corre-

lation with Cr was observed with nickel (r

0.37) and other moderate

correlations were found between Cr and cobalt, copper, zinc, selenium

and lead (0.2< r

0.4).

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Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

3.7. Correlations between exposure biomarkers and multivariate analysis

There were strong correlations between pre-shift and post-shift uri-

nary Cr concentrations in exposed workers (r

0.89 both for

creatinine-adjusted Cr and density-adjusted Cr,

Supplementary Table 8).

Inhalable Cr(VI) correlated with urinary Cr (density-adjusted) (r

0.64) and RBC (r

0.53). Urinary Cr (density-adjusted) correlated with

RBC-Cr (r

0.72) (Supplementary

Table 8

and

Supplementary Fig. 3).

In multivariate regression analysis, post-shift urinary and RBC Cr

concentrations were significantly higher in the exposed group compared

with the controls (Table

A, model 1). After adjustment for sex, age and

tea drinking (model 2), and further adjustment for smoking, coffee

drinking, supplements consumption, implants, and leisure activities

exposed to Cr (model 3), the results remained statistically significant.

Regression analysis showed that post-shift urinary Cr was higher after

welding, process operation and other work tasks, than after machining

0.05). Workers doing other work tasks also had higher RBC-Cr than

machining workers (Table

B). At company level, urinary and RBC Cr

for workers in steel production companies were higher than for workers

in non-categorised companies (P

0.05) (Table

B).

4. Discussion

We have, by short-term and long-term markers of Cr(VI) exposure,

identified workplaces and various occupations throughout Sweden

where employees are exposed to Cr(VI).

4.1. Comparison with previous studies and risk assessment

Our study was designed to be similar to the HBM4EU chromates

study, hence the results of our study and HBM4EU chromates study are

comparable. However, it should be noted that differences in methods of

Table 6

Linear regression models for logarithm-transformed red blood cells (RBC) and

density adjusted post-shift urinary chromium (Cr).

A. Multiple linear regression models with beta coefficient (β) were to evaluate

differences between exposed group and controls.

Model 1

(95% CI)

Exposed

group

Urinary

RBCCr

1.57 (1.26,

1.89)

0.40 (0.30,

0.50)

Model 2

(95% CI)

1.63 (1.30,

1.96)

0.41 (0.30,

0.51)

Model 3

(95% CI)

1.60 (1.26,

1.93)

0.40 (0.30,

0.51)

air-sampling and biomonitoring could potentially influence compara-

bility with other studies.

4.1.1. Inhalable Cr(VI)

Airborne Cr has been commonly measured as inhalable total Cr,

inhalable Cr(VI), respirable total Cr or respirable Cr(VI). Several studies

have measured airborne Cr(VI) without specifying which particle frac-

tion has been measured. A study conducted in Iran reported a mean

value of 2

g/m

for welding and 5

g/m

for back welding (welding

inside pipes as confined space) (Golbabaei

et al., 2012).

Studies in India

and Egypt measured airborne Cr(VI) in the leather tanning industry with

a mean value of 21

g/m

(Balachandar

et al., 2010)

and 10.4

g/m

(Abdel

Rasoul et al., 2017),

respectively. HBM4EU carried out a study on

occupational exposure to Cr(VI) and involving nine countries (Belgium,

Finland, France, Italy, Luxembourg, the Netherlands, Poland, Portugal,

and United Kingdom) (Santonen

et al., 2022).

The median concentration

of inhalable Cr(VI) in HBM4EU chromates study (0.43

g/m

) was

higher compared with our study (0.1

g/m

), but their P95 value was

lower (5.13

g/m

versus 8.03

g/m

). The same trend was also

observed if only welders were considered. The median and P95 of

inhalable Cr(VI) for welders in HBM4EU chromates study were 0.5 and

4.06

g/m

, while in our study they were 0.1 and 14.73

g/m

. The

lower median value in our study suggests that, on average, the inhalable

Cr(VI) concentrations among exposed workers were relatively low in

Sweden. However, the higher P95 value indicates a higher upper range

of exposure. These studies clearly show that the distribution and range

of inhalable Cr(VI) concentrations among Cr(VI) exposed workers vary

between different countries, and further, the necessity to perform na-

tional exposure assessment.

4.1.2. Risk assessment

In our study, 5 individuals (4.3%) exceeded 10

g/m

of inhalable Cr

(VI) (i.e. current EU OEL), 8 (7.0%) exceeded 5

g/m

(the current

Swedish OEL), 22 (19.1%) exceeded 1

g/m

(the current Danish,

French and Dutch OEL) and 42 (36.5%) exceeded 0.25

g/m

(the ex-

pected future Danish OEL). Further, the Bayesian tool Expostats analysis

indicates that there is a non-negligible, and often high, probability that

the Swedish OEL is exceeded for at least 5% of the occupational groups

we investigated, assuming similar conditions as during the performed

measurements. However, the broad definitions of and the low number of

samples in our similar exposure groups contribute to the variability and

hence the high estimates of probability of overexposure.

In the present study, 7% of workers exceeded the current Swedish

OEL of 5

g/m

and we estimated that 17 900 workers were exposed to

Cr(VI) in Sweden. Therefore, we can speculate that around 1250

workers in Sweden are at risk of exceeding the Swedish OEL (17 900 *

≈

1250). However, it should be noted that the Swedish JEM includes

everyone exposed to Cr(VI) regardless of exposure level. Thus, occupa-

tions with low and/or very intermittent exposure are also included. On

the other hand, a recent time trend study of exposure to respirable

crystalline silica, welding fumes, wood dust, and chlorinated hydro-

carbon solvents in Sweden showed that occupational exposures tended

to shift from large companies to small companies (Gustavsson

et al.,

2022).

Technological progress and automatization have eliminated

many hazards in large companies, however, without supervision by an

occupational physician and limited resources for preventive work in

many small and middle-sized companies, high-risk workplaces may still

prevail (Funke,

2007).

Most participated companies (86%) in our study are considered big

companies (more than 100 employees), and this could be the reason that

the inhalable Cr(VI) concentrations among exposed workers were rela-

tively low. However, the working situation in small companies and the

shifting of the exposure indicative of more serious negative health ef-

fects on the individual level even though the exposure level and prev-

alence overall diminished. Thereby, one can speculate that the

exceedance of the OEL in the participating companies is an

B. Linear regression model with

were to evaluate differences between companies in

exposed group. All analyses are unadjusted.

Urinary Cr

(95% CI)

Work task

Welding

Process operation

Others

Company

Manufacture/processing of

metal products

Steel production

Bath plating

RBC-Cr

(95% CI)

0.08 ( 0.19,

0.36)

0.04 ( 0.22,

0.30)

0.33 (0.02,

0.64)

0.24 ( 0.05,

0.52)

0.53 (0.23,

0.82)

0.29 ( 0.04,

0.61)

1.15 (0.31,

1.98)

0.90 (0.12,

1.68)

1.06 (0.12,

2.00)

0.83 ( 0.06,

1.71)

1.42 (0.50,

2.34)

0.95 ( 0.06,

1.94)

Model 1 is unadjusted; model 2 is adjusted for sex, age and tea drinking;

model 3 is adjusted for sex, age, tea drinking, smoking, coffee drinking, using of

supplements, implants, and leisure activities exposed to Cr. The reference is

controls.

The reference is machining.

The reference is non-categorised companies.

0.05

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Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

underestimation in comparison with companies without resources for

preventive work. Our estimate of the number of workers currently

exposed to Cr(VI) is lower than the numbers estimated in the 1990s, 17

900 today vs. 21 000 in the 1990s (Kauppinen

et al., 2000).

Comparison

is somewhat difficult since it is not known if the former estimation also

included low or intermittently exposed occupations. However, as

pointed out above although the prevalence of exposure to Cr(VI) has

decreased it does not mean the exposure level also has declined.

In our study, exposure was assessed according to four work tasks

(welding, machining, process operation and others). Welder was the

only homogenous occupation with known Cr(VI) exposure that could be

easily assessed in the register from Statistics Sweden (Statistikdataba-

sen, 2021).

In 2021, there were 12 703 registered welders (SSYK code

7212) in Sweden and based on the estimation in the Swedish JEM that

20% of welders are exposed to Cr(VI), we estimate that approximately

2570 welders are exposed to Cr(VI) today. However, many workers

perform welding without having the job title welder. Sjogren and Gus-

tavsson estimated that in 2013 there were 20 000–25 000 workers

welding in their profession (Sj

ogren, 2013)

but 70 306 workers exposed

to welding fumes (Gustavsson

et al., 2022).

In the present study, 12.5%

of welders exceeded the Swedish OEL of inhalable Cr(VI). Therefore, in

the case of conservative estimation (exposure of non-welders to welding

fumes was not considered), around 625 welders are at risk of exceeding

the Swedish OEL nationally (25 000 welders * 20% * 12.5%

625

welders) when welding. The Bayesian analysis’ 95% credible interval for

welders’ overexposure of the Swedish OEL was 3.1%–19.6%. This

translates to between 155 and 980 welders being at risk of exceeding the

Swedish OEL nationally (25000 welders * 20% * 3.1%

155 welders;

25000 * 20% * 19.6%

980 welders).

The current OEL for Cr(VI) in Sweden corresponds to 20 extra lung

cancer cases per 1000 exposed after 40 years of exposure (i.e. lifetime

risk) (C.

European, 2017).

In Germany and the Netherlands, acceptable

risk is considered to be an additional risk of

cases per 100,000 after

40 years and tolerable risk (during a transitional period) is considered to

4/1000 (Ding

et al., 2014).

It should be noted that the Swedish OEL

corresponds to much higher levels of Cr(VI) and thus substantially

higher risks. Further, the fact that 7.0% of workers in our study exceeded

the Swedish OEL and 4.3% exceeded the EU OEL, suggests that a sub-

population of the Cr(VI)-exposed workers may be at even higher risk of

lung cancer in Sweden. To lower the Cr(VI) exposure, there is a need for

more effective risk management measures and increased incentives for

workplaces to implement them. Important actions towards this aim are

reduction of the current OEL and subsequent enforcement of it,

including directed information campaigns supporting the adoption of

proper risk management.

4.1.3. Urinary Cr

In a recent systematic review of biomonitoring data on occupational

exposure to Cr(VI) (Verdonck

et al., 2021),

the median or mean urinary

Cr levels were lower in European countries (ranging from 0.96

g/L to

5.81

g/L) compared with non-European countries (ranging from 1.66

g/L to 48.4

g/L). In HBM4EU chromates study, the median and P95

concentration of post-shift urinary Cr in exposed workers were 1.7 and

5.1

g/g creatinine. In our study, the median urinary Cr was 0.55

g/L,

and after creatinine adjustment, the median and P95 were 0.41 and 2.12

g/g creatinine, which are lower than all studies above. In HBM4EU

chromates study, reference values were obtained by recruiting controls

from the same companies as the exposed workers (within company

controls) or from other companies without associated with Cr(VI)

exposure (outwith (external) company controls). The values of the

controls’ urinary Cr in our study (median and P95, 0.08 and 0.54

g/g

creatinine) are similar with the outwith company controls in HBM4EU

chromates study (0.1 and 0.4

g/g creatinine) (Viegas

et al., 2022).

France and the Netherlands have set a biological limit value (BLV) of

2.5

g/L of Cr in urine based on their OEL of 1

g/m

for Cr(VI) in air,

and Finland has derived a BLV of 0.2

mol/L (ca. 10

g/L) in urine

corresponding to its OEL of 5

g/m

in air (Verdonck

et al., 2021).

In our

study, two participants (1.8%) exceeded 10

g/L of urinary Cr and 13

(11.5%) exceeded 2.5

g/L.

4.1.4. RBC-Cr

RBC-Cr (median, 0.73

g/L and mean, 0.89

g/L) was lower in our

study compared to welders in a German study (median, 1.95

g/L)

(Weiss

et al., 2013),

electroplaters in Italy (median, 3.4

g/L) (Goldoni

et al., 2010a)

and China (median, 4.41

g/L) (Zhang

et al., 2011),

and

chromate production workers in China (mean, 12.45

g/L). The median

value of RBC-Cr in HBM4EU chromates study (0.73

g/L) was the same

as in our study but they had higher P95 (5.83

g/L versus 2.33

g/L)

(Ndaw

et al., 2022).

With respect to controls, one study in China

measured RBC-Cr in 93 controls (median, 1.54

g/L) (Zhang

et al.,

2011)

and HBM4EU chromates study measured 175 controls (median,

0.63

g/L) (Ndaw

et al., 2022).

The median concentration of RBC-Cr in

our controls was 0.53

g/L, similar to in HBM4EU chromates study.

Despite that Cr in RBC is considered a specific biomarker of Cr(VI),

there is no established BLV for RBC-Cr. It is worth mentioning that, in

our study, plasma was removed from whole blood, and the blood cells

were washed to eliminate interfering residual plasma-Cr. However,

white blood cells (WBC) were retained along with RBC, which might

increase the background level of RBC-Cr from Cr(III) accumulated in

WBC.

4.2. Efficiency of using LEV and RPE

In earlier studies, LEV significantly influenced exposure to Cr(VI)

during welding, resulting in a 68% reduction in median Cr(VI) con-

centrations (Meeker

et al., 2010).

In the HBM4EU chromates study, the

use of LEV corresponded to about one third lower airborne Cr concen-

trations (Viegas

et al., 2022).

In our study, the reduction was around

50%. An inferred acceptable LEV also led to a reduction to half of the

urinary Cr and corresponded to a statistically significantly lower con-

centration of RBC-Cr.

Compared to other preventive and protective measures (e.g., elimi-

nation of the high-risk substance, substitution by a less toxic alternative

or separating the substance from the workers), RPE should be regarded

as the last resort in the hierarchy of controls (Viegas

et al., 2022).

HBM4EU chromates study, the use of RPE was associated with lower

urinary Cr (except for machining workers). In addition, in

chrome-platers, a stronger correlation between internal Cr and airborne

Cr(VI) was observed in the group without RPE (Ndaw

et al., 2022).

our study, workers who correctly used RPE were exposed to around four

times higher inhalable Cr(VI) compared with those who did not, and

higher concentrations of urinary and RBC Cr were found in workers who

used RPE correctly. Stratified analysis showed that LEV had a greater

protective effect compared with RPE, and among workers with

non-acceptable LEV, the correct usage of RPE was still associated with

the highest level of inhalable Cr(VI), and urinary and RBC Cr. There may

be several explanations for the dysfunction of RPE: the exposed workers

may have irregularly worn RPE over time; they may have been exposed

to Cr(VI) via the skin; or workers may have been subject to secondary

exposure. Furthermore, RPE only guarantees protection if no leaking

occurs, and only works when it fits properly to the wearer’s face (Viegas

et al., 2022).

Fit test is not formally required in Sweden as opposed to

many other countries. Only around half of the workers who correctly

used RPE used loose-fitting powered air-purifying respirators, which

does not require the fit test. For the other workers, a reason for the low

efficiency of RPE protection could be that no fit test was performed.

Our findings show that most employers and workers are aware of the

risk of high levels of Cr(VI) in the air and thus use RPE, but that this is

not enough to reduce the Cr(VI) exposure and more efficient exposure

control strategies are needed.

BEU, Alm.del - 2023-24 - Bilag 61: Orientering om svensk undersøgelse af luftmålinger om krom-6 på svenske virksomheder

Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

4.3. Other metals

Apart from Cr, workers may be exposed to other toxic metals in their

working environment. It was reported that urinary (Golbabaei

et al.,

2012; Stanislawska et al., 2020),

serum (El

Safty et al., 2018)

and blood

(Muller

et al., 2022)

nickel in Cr(VI)-exposed workers were significantly

higher than controls. In our study, post-shift urinary nickel in the Cr

(VI)-exposed group was non-significantly higher than controls (P

0.09), and nickel concentrations in RBC showed no significant difference

between the two groups (P

0.36). However, nickel concentrations in

RBC was significantly higher in welders than in controls (P

0.02). In

addition, among all metals in RBC, we observed the strongest correlation

with Cr for nickel (r

0.37). The finding of co-exposure to nickel

among some Cr(VI)-exposed workers indicate exposure to multiple

carcinogens. We found some differences in urinary and RBC metal

concentrations between companies and work tasks as well. This may

lead to more serious health consequences than exposure only to one

carcinogen, and thus, a more complex risk assessment is needed

including monitoring of multiple carcinogens.

We also found significantly higher concentrations of post-shift uri-

nary and RBC copper in Cr(VI)-exposed workers compared with con-

trols. On the contrary, Song et al. reported significantly lower levels of

copper in whole blood in chromate production workers in China (Song

et al., 2012).

Besides that, our result for zinc concentrations in RBC was

in line with Song et al., i.e. higher zinc among Cr(VI)-exposed workers.

Unexpectedly, antimony was found to be significantly higher in urine

and RBC in the control group. A potential explanation for the higher

levels of antimony in controls could be exposure to antimony trisulfide; a

lubricant in friction material and widely used in disc brake pads (Uex-

küll et al., 2005).

In our study, 33 controls (45.8%) had the work task of

car driving car, truck, forklift truck, or excavator. Other controls

recruited from the same company as drivers may share the same work

environment and be exposed to antimony-containing dust as well.

4.4. Correlations between exposure markers and monitoring strategy

The positive correlation between airborne Cr(VI) and urinary Cr

concentrations (r

0.64) in our study indicates that exposures to Cr(VI)

occurred mainly via inhalation (Were,

2013).

Moderate correlations

were also found between inhalable Cr(VI) and urinary Cr in welders in

Poland (r

0.58) (Stanislawska

et al., 2020),

electroplaters in Great

Britain (r

0.62) (Beattie

et al., 2017)

and in the HBM4EU chromates

study (r

0.46) (Viegas

et al., 2022).

Regression analyses are

commonly used to study the relationship between airborne Cr(VI) levels

and urinary Cr levels. Published regression formulas could be used to

convert the measured biomonitoring data, representing internal expo-

sure, into corresponding Cr(VI) air levels (Mahiout

et al., 2022),

and

conversely set BLVs corresponding to OELs. The regression analysis

published by Lindberg and Vesterberg has been used as a basis for

deriving a BLV for Cr(VI) in bath plating where a value of 13

g/g

creatinine (an average creatinine excretion of 1.36 g/L was used) cor-

responds to the OEL of 5

g/m

(Lindberg

and Vesterberg, 1983).

Another widely used regression analysis for Cr(VI) in electroplating was

published by Chen et al. in which the same OEL corresponds to urinary

Cr of 8.8

g/g creatinine (Chen

et al., 2002).

HBM4EU chromates study

reported two regression analysis (Viegas

et al., 2022),

for platers the

OEL of 5

g/m

corresponds to a urinary Cr level of 6.9

g/g creatinine

and for welders it corresponds to 3.4

g/g creatinine. In our study the

Swedish OEL corresponds to 2.44

g/g creatinine for all exposed

workers and 1.26

g/g creatinine for welders, respectively. It should be

noted that we observed a low goodness-of-fit value (0.02) for all exposed

workers. Furthermore, 21 workers exceeded the reference P95 of uri-

nary Cr but had less than 0.25

g/m

of inhalable Cr(VI) (Supplementary

Table 5B).

This indicates that the Cr(VI) exposure might not have

occurred only via inhalation. Thus, aspects to asses for the relationships

between exposure via air and biomarkers are sources and variations in

Cr(VI) emissions, but also solubility of Cr(VI) compounds in water and

particle size, which are expected to impact the toxicokinetic of Cr and

subsequently influence the levels of chromium excreted in the urine

(Wilbur

et al., 2012).

More studies are needed to establish the most

suitable regression analysis to set up the BLV.

A few studies investigated the correlation between urinary and RBC

Cr. A significant positive correlation between urinary and RBC Cr (r

0.74) was found in chrome-platers in Italy (Goldoni

et al., 2010a)

However, in chromate production workers in China, the correlation was

weak (r

0.21) (Wang

et al., 2011).

Also, poor correlation between

urinary and RBC Cr was found in HBM4EU chromates study, but when

only considering chrome-platers, the r

coefficient became higher (only

shown in figure, approximately r

0.1 for all workers and r

0.5 for

chrome-platers) (Santonen

et al., 2022).

The correlation between uri-

nary and RBC Cr in our study is relatively strong (r

0.72). To date,

only a few studies have investigated the correlation between inhalable

Cr(VI) and RBC-Cr concentrations. No correlation (r

0.06;

0.73)

was reported for Polish welders (Stanislawska

et al., 2020).

In HBM4EU

chromates study, no correlation was also reported for all worker groups

combined, but among chrome-platers, the correlation between inhalable

Cr(VI) and RBC-Cr was stronger (r

0.54) (Ndaw

et al., 2022).

similar correlation was found in our study for all exposed workers (r

0.53). RBC-Cr may primarily reflect exposure to water-soluble Cr and

less to welding fumes, but there is also evidence that stainless steel

welding fumes are retained in the lungs longer than mild steel welding

fumes (Antonini

et al., 2004).

In our project, 97% of welders were

welding stainless steel, and this could be a plausible explication of the

high correlation observed between inhalable Cr(VI) and RBC-Cr. How-

ever, it should be noted that 27 workers exceeded the reference P95 of

RBC-Cr but had less than 0.25

g/m

of inhalable Cr(VI), among them,

12 workers even had normal levels of urinary Cr (Supplementary

Table 5B).

This indicates that RBC-Cr reflects elevated exposure in air

prior to our exposure measurements. Since the air monitoring is tran-

sient and the short-term nature of total urinary Cr may mislead exposure

to Cr(VI), a better strategy when assessing long-term Cr(VI) exposure

would be repeated air measurement combined with biomonitoring of

RBC-Cr.

4.5. Strengths and limitations

This is a comprehensive study of occupational exposure to Cr(VI),

and, to the best of our knowledge, the very first in Sweden. The

nationwide cover allowed us to obtain a more complete dataset of

different types of companies across the country. Additionally, this study

included environmental and biological monitoring information at the

individual level. Overall, our results corroborate with previous pub-

lished studies. The study design and the questionnaire were adapted

from HBM4EU chromates study, and therefore our data should be

directly comparable to the data from HBM4EU chromates study. In the

present study, statistically significant relationships between RBC-Cr and

different exposure biomarkers provided evidence that RBC-Cr is an

appropriate biomarker for monitoring occupational Cr(VI) exposure.

This study has the potential to enhance the significance of different

biological indicators in monitoring Cr levels and contributes valuable

data to bolster regulatory risk assessment and decision-making

processes.

There were several limitations of the present study. The relatively

low company participation rate indicates that the participating com-

panies may not be representative for Cr(VI) exposure in Sweden. There

may be bias due to unbalanced covariates in the exposed and control

groups. Airborne Cr(VI) was measured only for one working day. There

were higher Cr concentrations in pre-shift urine since pre-shift urine was

sampled when workers had worked for at least three days. The wide

range of work tasks and sectors has, because of different emission

sources and exposure routes, influenced the analysis of correlations

between inhalable Cr(VI) and biomarkers. Further, this study only

BEU, Alm.del - 2023-24 - Bilag 61: Orientering om svensk undersøgelse af luftmålinger om krom-6 på svenske virksomheder

Z. Jiang et al.

International Journal of Hygiene and Environmental Health 256 (2024) 114298

measured inhalable Cr(VI), and dermal exposure was not assessed

although dermal contamination is considered an important Cr(VI)

exposure route. Finally, there may be uncertainties about usage of RPE

over time.

5. Conclusions

Our study showed that although a majority of the individual air

measurements were relatively low, some workers are exposed to high

levels of Cr(VI), and 7.0% of participants’ measured exposures exceeded

the current Swedish OEL. Furthermore, the existing protective measures

implemented at workplaces are inadequate and insufficient, and sig-

nificant action to lower Cr(VI) exposure is warranted. Several workers

showed higher concentrations of Cr in urine and RBC, but not in air,

suggesting that a combination of workplace environmental and biolog-

ical monitoring is necessary to assess Cr(VI) exposure. LEV showed

promising protection efficiency, while further studies are needed to

evaluate how RPE best should be used in preventing Cr(VI) exposure

when other exposure control measures have been exhausted. Risk

assessment and risk reduction need to be improved at the companies and

supplemented with national policies to support risk awareness for non-

threshold carcinogens as well as surveillance of exposure levels, in order

to eliminate occupational cancer. Further studies are needed to clarify

the health consequences of the current Cr(VI) exposure.

CRediT authorship contribution statement

Zheshun Jiang:

Data curation, Formal analysis, Investigation,

Visualization, Writing

–

original draft, Writing

–

review

editing.

Linda

Schenk:

Formal analysis, Investigation, Methodology, Writing

–

original

draft, Writing

–

review

editing.

Eva Assarsson:

Investigation, Writing

–

review

editing.

Maria Albin:

Conceptualization, Funding acquisi-

tion, Project administration, Resources, Supervision, Writing

–

review

editing.

Helen Bertilsson:

Investigation, Writing

–

review

editing.

Eva Dock:

Investigation, Writing

–

review

editing.

Jessika Hagberg:

Investigation, Resources, Writing

–

review

editing.

Lovisa E. Karls-

son:

Formal analysis, Methodology, Writing

–

review

editing.

Pete

Kines:

Investigation, Writing

–

review

editing.

Annette M. Krais:

Investigation, Writing

–

review

editing.

Stefan Ljunggren:

Data

curation, Investigation, Methodology, Writing

–

review

editing.

Thomas Lundh:

Formal analysis, Investigation, Methodology, Super-

vision, Writing

–

review

editing.

Lars Modig:

Funding acquisition,

Investigation, Writing

–

review

editing.

Rickie Moller:

Investigation,

Writing

–

review

editing.

Daniela Pineda:

Formal analysis, Meth-

odology, Project administration, Writing

–

review

editing.

Niklas

Ricklund:

Data curation, Investigation, Writing

–

review

editing.

Anne T. Saber:

Investigation, Writing

–

review

editing.

Tobias

Storsjo:

Investigation, Writing

–

review

editing.

Evana Taher Amir:

Investigation, Writing

–

review

editing.

Håkan Tinnerberg:

Conceptualization, Investigation, Methodology, Writing

–

review

editing.

Martin Tondel:

Investigation, Methodology, Writing

–

review

editing.

Ulla Vogel:

Conceptualization, Investigation, Writing

–

re-

view

editing.

Pernilla Wiebert:

Data curation, Investigation, Writing

–

review

editing.

Karin Broberg:

Conceptualization, Funding acqui-

sition, Investigation, Methodology, Project administration, Resources,

Supervision, Writing

–

review

editing.

Malin Engfeldt:

Conceptuali-

zation, Data curation, Formal analysis, Investigation, Methodology,

Project administration, Resources, Supervision, Validation, Writing

–

review

editing.

Declaration of Competing interest

The authors declare no conflicts of interest.

Acknowledgments

This study has received funding from Forskningsrådet for halsa,

lfard (Forte) (2020-00208) and Afa Forsakring

¨ ¨

arbetsliv och va

(200279).

The project team would like to thank all the companies and workers

who participated in the SafeChrom study.

Appendix A. Supplementary data

Supplementary data to this article can be found online at

https://doi.

org/10.1016/j.ijheh.2023.114298.

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