10970274, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ajim.23439 by Nat Prov Indonesia, Wiley Online Library on [11/02/2023].

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Received: 27 June 2022 | Revised: 26 October 2022 | Accepted: 26 October 2022

DOI: 10.1002/ajim.23439

RESEARCH ARTICLE

Transmission factors and exposure to infections at work and

invasive pneumococcal disease

Kjell Torén MD, PhD1,2,3 | Maria Albin MD, PhD4,5 | Magnus Alderling PhD5 |
Linus Schiöler PhD1 | Maria Åberg MD, PhD1,6

1
School of Public Health and Community
Medicine, Institute of Medicine, The Abstract
Sahgrenska Academy, University of
Background: Working in close contacts with coworkers or the general public may be
Gothenburg, Gothenburg, Sweden
2
Department of Medicine, Occupational and
associated with transmission of invasive pneumococcal disease (IPD). We
Environmental Medicine, Sahlgrenska investigated whether crowded workplaces, sharing surfaces, and exposure to
University Hospital, Gothenburg, Sweden
infections were factors associated with IPD.
3
Discipline of Occupational and
Environmental Health, University of Methods: We studied 3,968 cases of IPD, and selected six controls for each case
KwaZulu‐Natal, Durban, South Africa from the Swedish population registry with each control being assigned the index
4
Division of Occupational and Environmental date of their corresponding case. We linked job histories to job‐exposure matrices to
Medicine, Lund University, Lund, Sweden
5
assess different transmission dimensions of pneumococci, as well as occupational
Unit of Occupational Medicine, Institute of
Environmental Medicine, Karolinska Institutet, exposure to fumes. We used adjusted conditional logistic analyses to estimate the
Stockholm, Sweden
odds ratios (ORs) for IPD with 95% confidence intervals (95% CI).
6
Region Västra Götaland, Regionhälsan,
Results: ORs for IPD for the different transmission dimensions were increased
Gothenburg, Sweden
moderately but were statistically significant. Compared to home‐working or working
Correspondence alone, the highest odds was for Working mostly outside, or partly inside (OR 1.19, 95%
Kjell Torén, MD, PhD, Sahlgrenska Academy,
University of Gothenburg, Box 414, SE‐405 CI 1.04−1.38). Estimates were higher in men for all dimensions, compared to women.
30 Gothenburg, Sweden. The odds for IPD for Working mostly outside, or partly inside were 1.33 (95% CI
Email: Kjell.Toren@amm.gu.se
1.13−1.56) and 0.79 (95% CI 0.55−1.14) for men and women, respectively. Higher
Funding information odds were seen for all transmission dimensions among those exposed to fumes,
2021‐00304; Forskningsrådet om Hälsa,
although CIs included unity. Contact with ill or infected patients did not increase the
Arbetsliv och Välfärd
odds for IPD.
Conclusion: IPD was associated with working in close contact with coworkers or the
general public, and with outside work, especially for men. Contact with infected
patients or persons was not associated with IPD.

KEYWORDS
case‐control, COVID‐19, job‐exposure matrix, pneumococci

This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial‐NoDerivs License, which permits use and distribution in any
medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
© 2022 The Authors. Analyses of Social Issues and Public Policy published by Wiley Periodicals LLC on behalf of Society for the Psychological Study of Social Issues.

Am J Ind Med. 2023;66:65–74. wileyonlinelibrary.com/journal/ajim | 65


66 | TORÉN
1 | INTRODUCTION
Streptococcus pneumoniae is a Gram‐positive bacterium that is part of
the normal flora of the upper respiratory tract.1S. pneumoniae can
invade tissues locally to cause sinusitis, otitis media or lobar
pneumonia.2−3 Pneumonia due to S. pneumoniae is often accompa-
nied by invasive pneumococcal disease (IPD), which is defined as
pneumococcal bacterial growth cultured from a normally sterile site
such as the blood, cerebrospinal fluid or joint fluid.
Transmission of pneumococci occurs through droplets, from either
persons with the disease or healthy carriers. Around 10% of the adult
population are asymptomatic carriers of S. pneumoniae. Transmission
requires close contact, and is more likely to occur after viral infections.
Person‐to‐person spread can also occur via contaminated surfaces.
Therefore, numerous outbreaks have been reported in different types of
closed settings, and in the preantibiotic area outbreaks were quite
common.3−6
In many workplaces, welders, construction workers, dockers, miners,
health care workers, and daycare personnel may work in crowded
settings and, sometimes, also live part‐time in crowded guest houses. The
latter, is often the case for contract workers in certain professions who
are working far from home. This phenomenon was observed already in
the late 1890s when pneumococcal pneumonia was epidemic among
South African miners living far from their homes.7−8 Systematic reviews
have concluded that workers in closed settings have an increased risk of
pneumococcal pneumonias, and especially those who work in hospital
3,6
wards, oil rigs, military units and prisons. A recent example of such an
outbreak is from a large Finnish shipyard with numerous short‐term
employees with multinational background.9 Similar observations have
been made in Norwegian and French shipyards, and on Swedish
construction sites.10−12 In all these studies, the working conditions were
described as crowded, with workers of many different nationalities, and
combined with occupational exposure to irritants, metal fumes, dust and
chemicals. In the outbreaks in Norway and Finland, the same genetically
distinct and uncommon variant of S. pneumoniae was identified.13 It has
been proposed that the circulation of this specific genotype is facilitated
by crowded conditions. In workplaces, occupational exposures to
inorganic dust, silica dust, and metal fumes are also risk factors for
14−16
pneumococcal pneumonia.
The ongoing COVID‐19 pandemic has focused attention on the
possibility that the work‐place is key setting for the spread of severe
acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2).17−18 To
study this, several job‐exposure matrices have been developed to
assess the risk of exposure to SARS‐CoV‐2.19−20 While these
matrices have been developed for SARS‐CoV‐2, we assume that in
slightly modified form they also can be applied to studying risks for
bacterial infections, likeS. pneumoniae. Thus, we hypothesized that in
a working population, in addition to occupational exposures to dust
and fumes, the situation of working in close contact with coworkers,
or the general public would be associated with increased odds for
IPD. We tested this hypothesis by applying newly developed job‐
exposure matrices that classify occupations according to transmission
and mitigation dimensions.19−20
10970274, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ajim.23439 by Nat Prov Indonesia, Wiley Online Library on [11/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ET AL.
2 | M A T E R I A L S AN D M E T H O D S
2.1 | Establishment of study population
The study population included all cases of IPD obtained through the
system of mandatory reporting of communicable diseases in Sweden,
the SmiNet registry, as previously reported by us.15 The potentially
eligible cases for inclusion (N = 6,335) with IPD were those aged 20−65
years with a reported positive culture of S. pneumoniae in blood,
cerebrospinal fluid, joint fluid, or other normally sterile body fluids. We
extracted from the SmiNet registry the Swedish personal identity
number of each case and the date (index date) when the positive sample
was obtained. We selected six living controls for each case, matched for
gender, age (case year of birth), and region of residency (four urban
areas and three rural areas) at index date from the Swedish Historical
National Population Registry (N = 38,076). We limited the study to
reports received from July 1, 2006 through December 31, 2019.
We extracted information from the Swedish national socio-
economic database, called LISA (Longitudinal integration database for
health insurance and labor market studies), for the highest
educational level attained, categorized as: pre‐high school (up to
9 years); completed high school; or university examination. We used
this as a surrogate for socioeconomic status. From LISA, we also
obtained information about the annual occupational history from
2005 until 2019. From the initial population of cases (N = 6335), we
excluded those with no reported occupation or no reported income
(N = 2367) resulting in a final population of 3968 cases for the
analysis. All controls linked to excluded cases were also excluded
(N = 14,202). In addition, controls with no reported occupation or no
reported income (N = 5906) were excluded. This generated a final
population of 17,968 matched controls. Cases and controls were
linked with the Swedish National Hospital Discharge Registry and the
Swedish Cause of Death Registry to identify hospitalizations and
deaths due to pneumonia (ICD10 J10−J18), including any hospital
stay that at least included the index date ± 7 days. This resulted in
2887 cases with IPD and pneumonia and 13,099 matched controls.
Thus, we defined two overlapping groups of cases; all cases with IPD
(N = 3968) and cases with IPD with pneumonia (pneumococcal
pneumonia) (N = 2887).
2.2 | Comorbidities
We used the Swedish National Hospital Discharge Registry and the
Swedish Prescribed Drug Registry to identify the following comor-
bidities based on ICD‐10 coding: chronic obstructive pulmonary
disease (COPD) (ICD10 J43‐J44); and ischemic heart disease (ICD10
I20‐I25) during 5 years preceding the index date. We defined the use
of drugs according to the Anatomical Therapeutic Chemical (ATC)
codes. Diabetes mellitus was defined according to prescriptions
dispensed for diabetes drugs (ATC A10), and ethanol‐containing
substance abuse disorders were defined according to the medications
dispensed for such disorders (ATC N07B), at any time within the

TORÉN ET AL.
5 years preceding the index date. We also used information on
prescriptions for oral corticosteroids (ATC H02A) and immuno-
suppressive medications (ATC L03−L04), but only if these drugs were
dispensed at any time within the 5 years preceding the index date.
2.3 | Classification of occupational exposures
The occupation in the year preceding the index date was classified at
the four‐digit level according to the ISCO‐88 and ISCO‐08
21−22
codes.
Ten experts in occupational epidemiology and exposure assess-
ment from The Netherlands, Denmark and UK constructed a job‐
exposure matrix (JEM) for assessing the risk of becoming infected
with the SARS‐CoV‐2 virus.20 The JEM was designed to capture eight
dimensions that were judged as being important for the risk of being
infected, divided into; no risk, low risk, elevated risk, and high risk.
For the present study we refined this to the following three levels;
No risk, homeworker or working alone; medium risk (low and
elevated); and high risk.
For the present study we applied the following categories of
dimensions:
1. Number. High risk: Number of fellow workers in close proximity
to each other, divided into >30 workers per day in close proximity;
Medium risk: ≤30 workers per day in close proximity, as compared
to homeworking or not working with others.
2. Nature of contacts. High risk: Working in workspaces with regular
contacts with suspected or diagnosed COVID‐19 (for this
application, infected patients); Medium risk; Working with cow-
orkers only or with the general public, compared to homeworkers
or not working with others.
3. Contaminated workspaces. High risk: Frequently (≥10 times/day)
sharing materials or surfaces with the general public; Medium risk:
Sometimes (<10 times/day) sharing material or surfaces with the
general public but frequently (≥10 times/day) sharing materials or
surfaces with co‐workers, as compared to homeworkers or not
working with others.
4. Location. High risk: Working mostly inside (>4 h/day); Medium
risk: Working mostly outside or partly inside (<4 h/day); as
compared to homeworkers or not working with others.
5. Social distancing. High risk; Maintaining a distancing of ≥1 meter
between coworkers or the public while at work can never be
maintained; Medium risk: Social distancing cannot always be
maintained, as compared to homeworkers or not working with
others.
We did not include the dimension of face covering, which has
been defined differently in recent years than it was during our study
period. In addition, we did not include the dimensions of income
insecurity or migrant background, as individual data on socioeconomic
status and migrant status were to be obtained from our national
registries. We used the Danish application of the JEM, which we
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| 67
assumed was the application that was most likely to reflect Swedish
conditions.
We also applied a Swedish JEM that mapped physical proximity
and exposure to diseases or infections.19 The classifications of all
occupations were based on information from answers to the
questionnaire that the US Bureau of Labor Statistics have collected,
as reported in the Occupational Information Network (O*NET).23 The
two main questions were phrased as follows.How physically close to
other people are you when you perform your current work? The
response options were: I do not work near other people (>30 m),
I work with others but not closely (e.g. private office), slightly close
(e.g., shared office), moderately close (at arm's length), and very close
(near touching). The other main question was: How often does your
current work require that you be exposed to diseases or infections? The
response alternatives were: Never; At least once a year, but not every
month; At least once a month, but not every week; At least once a
week, but not daily; and Daily. The O*NET reports standardized
scores for each occupational group, resulting in scores in the range
of 0−100.
Thus, the scale for physical proximity was:
0—I do not work near other people (>30 m)
25—I work with others but not closely (e.g., private office)
50—I work slightly close (e.g., shared office) to other persons
75—I work moderately close (at arm's length) to other persons
100—I work very close (near touching) to other persons
The scale for exposure to diseases or infections—based on the
question: How often does your current work require that you be exposed
to diseases or infections? was as follows:
0—Never
25—At least once a year, but not every month
50—At least once a month, but not every week
75—At least once a week, but not daily
100—Daily
We divided the material into four groups, 0−24, 25−49, 50−74,
and 75−100. Of note, this JEM is based on a US questionnaire, which
did not include military personnel.
To assess airborne occupational exposures to vapor, gas, dust
and fumes and specifically fumes, we used a previously established
JEM.15,24
2.4 | Statistical methods
We used conditional logistic multivariable regression to calculate
the ORs for IPD or IPD with pneumonia associated with the
JEM‐defined categories of exposures tested as indicator vari-
ables. As the likelihood of the conditional model is formed as the
product over all matching strata the conditional model is always
adjusted for the matching variables, although not by the usual
covariate adjustment. The basic model (Model 1) was only
adjusted for matching strata (i.e., equivalent to adjusting for
gender, age and geographic region, and index date). The adjusted
model (Model 2) include, in addition, COPD, ethanol abuse (based
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68 | TORÉN ET AL.

on prescribed drugs) and prescribed immunosuppressive All statistical analyses were performed using the SAS version 9.4
drugs. We did not adjust for diabetes or ischemic heart disease, M5 software (SAS Inc.). Statistical significance was defined as
as we did not consider these to be confounders. All the JEM‐ p < 0.05 and 95% confidence intervals (95% CI) were calculated.
defined categories of exposures were tested in separate models
for each exposure. We also analyzed interactions with regard to
gender, migrant status, and airborne occupational exposure to 3 | RESULTS
fumes.
We also performed unconditional logistic multivariable The prevalence of the different transmission and mitigation dimen-
regression analysis (Model 3).25 We did not exclude sions are listed in Table 1. The differences between the cases and
controls linked to excluded cases in the unconditional logistic controls were, in general, rather small. The most common dimension
regression models, as controls with complete occupational was Working mostly inside, accounting for 68.8% of the cases and
information were always retained in the data set. Thus, in the 67.7% of the controls. Diabetes mellitus was a common comorbidity
unconditional models we had 3968 cases and 23,874 controls. seen in 9.6% of the cases and 4.0% of the controls. Use of oral
The unconditional models were adjusted for all matching steroids or immunosuppressive drugs was found in 21.2% of the
variables and COPD, use of alcohol and prescribed immuno- cases and in 5.6% of the controls. Additional descriptive data are
suppressive drugs. presented in Table 1.

T A B L E 1 Characteristics of cases with

Controls
IPD (N = 3968) (N = 17,968) invasive pneumococcal disease (IPD) and
matched controls from the general
Men 52.8% (N = 2097) 53.3% (N = 9576) population of Sweden aged 20−65 years
Age, years (SD) 51.4 (11.3) 51.0 (11.1)

Born outside Sweden 9.8% (N = 390) 12.7% (N = 2290)

Post‐high‐school examination 33.0% (N = 1308) 38.5% (N = 6919)

a
Chronic obstructive pulmonary disease (COPD) 2.2% (N = 87) 0.3% (N = 49)
a
Bronchial asthma 3.1% (N = 124) 0.9% (N = 154)

Diabetes mellitusa 9.6% (N = 381) 4.0% (N = 719)

Ischemic heart diseasea 2.3% (N = 90) 1.4% (N = 243)

Ethanol abuse 4.8% (N = 192) 1.7% (N = 309)

Oral steroids 15.7% (N = 621) 4.3% (N = 769)

Immunosuppressive drugs 5.5% (N = 218) 1.3% (N = 228)

Occupational exposures or dimensions of transmission and mitigation factors

Number; Workers (>30) in close proximity of each 24.6% (N = 976) 23.7% (N = 4252)
other

Nature; Regular contacts with infected patients 15.6% (N = 619) 14.9% (N = 2678)

Contaminated workspaces; Frequently sharing 37.2% (N = 1475) 35.6% (N = 6402)

material/surfaces with general public

Location; Working mostly inside 68.8% (N = 2729) 67.7% (N = 12,166)

Social distancing; Can never be maintained 22.3% (N = 886) 21.5% (N = 3868)

b
Physical proximity, highest group 75−100 22.8% (N = 903) 21.6% (N = 3873)

Exposure to diseases or infections, highest group 9.5% (N = 377) 9.2% (N = 1650)

75−100

Airborne occupational exposures

Exposure to vapor, gas, dust, or fumes 39.7% (N = 1574) 35.2% (N = 6321)

Exposure to fumes 19.2% (N = 763) 16.5% (N = 2964)

Abbreviation: SD, standard deviation.

a
Hospital‐based diagnoses.
b
Military personnel not included.
 10970274, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ajim.23439 by Nat Prov Indonesia, Wiley Online Library on [11/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
TORÉN ET AL. | 69

T A B L E 2 Logistic multivariable
Invasive pneumococcal disease (IPD)
regression models of invasive (N = 3968)
pneumococcal disease (IPD) in relation to Odds ratios with 95% confidence intervals
relation to the different dimensions of Dimensions of transmission and
transmission and mitigation factors mitigation factors Model 1a Model 2b Model 3c
Number of workers in close proximity to
each otherd

≤30 per day 1.11 (1.02−1.22) 1.11 (1.01−1.22) 1.11 (1.02−1.21)

>30 per day 1.12 (1.01−1.25) 1.14 (1.02−1.26) 1.12 (1.02−1.24)

d
Nature of contacts

With coworkers/general public 1.10 (1.01−1.21) 1.11 (1.01−1.21) 1.10 (1.01−1.19)

Regular contacts with infected patients 1.13 (1.01−1.27) 1.13 (1.00−1.27) 1.14 (1.02−1.27)
d
Contaminated workspaces

Sharing material/surfaces with 1.10 (1.00−1.20) 1.09 (0.99−1.20) 1.09 (1.00−1.19)

coworkers/general public

Frequently sharing material/surfaces 1.13 (1.02−1.24) 1.13 (1.02−1.24) 1.12 (1.03−1.23)

with general public

Locationd

Mostly outside, or partly inside 1.20 (1.04−1.38) 1.19 (1.04−1.38) 1.18 (1.03−1.35)

Mostly inside 1.10 (1.01−1.20) 1.10 (1.01−1.20) 1.10 (1.01−1.19)

Social distancingd

Not always 1.11 (1.01−1.21) 1.11 (1.01−1.21) 1.10 (1.01−1.20)

Never 1.12 (1.00−1.24) 1.11 (1.00−1.24) 1.12 (1.01−1.23)

Note: Model 1 and Model 2 are conditional logistic regression models and Model 3 is an unconditional
logistic regression model.
a
Model adjusted for gender, age geographic region.
b
Model adjusted for gender, age geographic region, chronic obstructive pulmonary disease, alcoholism,
and use of immunosuppressive drugs.
c
Unconditional logistic regression adjusted for gender, age geographic region, chronic obstructive
pulmonary disease, alcoholism, and use of immunosuppressive drugs.
d
Compared with homeworkers or working alone.

The ORs for IPD in relation to the different transmission dimensions
were, in general, moderately increased (Table 2). The differences between
the basic models (Model 1) and adjusted models (Model 2) were also
small. The highest odds in the adjusted models were for the dimension of
Working mostly outside or partly inside (<4 h/day) (odd ratio [OR] 1.19, 95%
CI 1.04−1.38). Besides that, the odds were around 1.10 in relation to the
different numbers of coworkers, contact with infected patients, shared
surfaces and social distancing, and nearly all the CIs did not include unity.
The results of the unconditional analysis were similar to those obtained
when retaining the matching. As expected, the CIs were marginally
narrower, and the point estimates were almost identical (Table 2, Model
3). The ORs for pneumococcal pneumonia (IPD with pneumonia) were
similar to the results for All IPD (Online Supporting Information: Table S1).
In Table 3 are shown the resulting odds when considering the
interactions. For all the dimensions, there were statistically significant
interactions with gender (Table 3). For Migrant status, born in Sweden, and
Occupational exposure to fumes there were significant interactions with
Contaminated workspaces. In general, the odds for men increased and the
odds decreased for women. Working mostly outside or partly inside (<4 h/
day) resulted in increased odds for men, but not for women. Further, for
men contact with coworkers or the general public increased the odds,
whereas work with infected patients did not increase the odds. Men, but
not women, had elevated odds for the Not always category of Social
distancing. For persons born outside Sweden (migrant status), there was
an interaction with Contaminated workspaces, and this resulted in a slightly
higher odds for persons born in Sweden for the dimension Frequently
sharing material/surfaces with general public (OR 1.19, 95% CI 1.07−1.32).
Among the fume exposed persons, the dimension Sharing material/
surfaces with co‐workers/general public (note, not “frequently sharing”) had
a high OR (OR 1.69, 95% CI 0.72−3.95). Small working groups (≤30
persons/day) seemed to have higher odds (OR 1.58, 95%
CI 0.68−3.67) compared to meeting or working with more people (OR
1.22, 95% CI 0.50−2.97).
To increase the understanding of possible risk factors, we listed
in Table 4 the five most common occupations among the cases, as
compared with the controls, in the stratum with the highest odds (OR
 10970274, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ajim.23439 by Nat Prov Indonesia, Wiley Online Library on [11/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
70 | TORÉN ET AL.

T A B L E 3 Logistic multivariable regression models of invasive pneumococcal disease (IPD) in relation to different dimensions of transmission
and mitigation factors

Invasive pneumococcal disease (IPD)

(N = 3968)
Odds ratios with 95% confidence intervals
Gender Born in Sweden Exposed to fumes
Transmission and mitigation factors Men Women Yes No Yes No

Number of workers in close proximity to each othera

≤30 per day 1.25b 0.97b 1.14 1.05 1.58 1.03

(1.10−1.12) (0.86−1.10) (1.04−1.25) (0.77−1.44) (0.68−3.67) (0.94−1.14)

b b
>30 per day 1.16 1.05 1.17 1.09 1.22 1.15

(0.97−1.38) (0.92−1.19) (1.04−1.30) (0.77−1.55) (0.50−2.97) (1.03−1.27)

Nature of contactsa

With coworkers or general public 1.24b 0.97b 1.13 1.06 1.53 1.07

(1.10−1.41) (0.86−1.09) (1.03−1.24) (0.77−1.45) (0.66−3.57) (0.97−1.17)

Regular contacts with infected patients 1.11 1.04 1.16 1.13 1.54 1.08

(0.86−1.42) (0.91−1.19) (1.02−1.31) (0.77−1.64) (0.65−3.62) (0.95−1.23)

Contaminated workspacesa

Sharing material/surface with coworkers or general 1.24b 0.90b 1.09c 1.23 1.69 1.03
public
(1.09−1.41) (0.78−1.05) (0.99−1.21) (0.88−1.71) (0.72−3.95) (0.94−1.14)

Frequently sharing material/surface with general 1.22 1.03 1.19 0.96 1.42 1.31
public
(1.05−1.42) (0.92−1.16) (1.07−1.32) (0.69−1.33) (0.61−3.31) (1.00−1.23)
a
Location

Mostly outside, or partly inside 1.33 0.79 1.20 1.28 1.26 1.23

(1.13−1.57) (0.55−1.14) (1.04−1.39) (0.78−2.10) (0.52−3.07) (1.06−1.43)

b b
Mostly inside 1.22 1.00 1.13 1.06 1.56 1.05

(1.07−1.38) (0.89−1.12) (1.03−1.24) (0.78−1.44) (0.67−3.64) (0.96−1.15)

a
Social distancing

Not always 1.25b 0.96b 1.13 1.10 1.54 1.07

(1.10−1.42) (0.85−1.09) (1.03−1.24) (0.80−1.51) (0.66−3.60) (0.97−1.17)

Never 1.14 1.03 1.16 1.01 1.51 1.07

(0.94−1.37) (0.91−1.17) (1.04−1.30) (0.71−1.44) (0.64−3.55) (0.96−1.20)

Note: Conditional model adjusted for gender, age, geographical region, chronic obstructive pulmonary disease, alcoholism and use of immunosuppressive drugs.
a
Compared to homeworking or working alone.
b
Interaction with gender, p < 0.05.
c
Interaction with Born in Sweden, p < 0.05.

1.33, 95% CI 1.13−1.57), that is, men working Mostly outside, or partly
inside according to the dimension Location.
The Swedish JEM showed in general moderately increased odds
(Table 5). Of note, exposures to disease or infections were not
associated with increased odds. With men and women combined,
ORs for Physical proximity were elevated and statistically significant.
Women had higher odds than men in all models for the Physical
proximity comparison of 4th versus 2nd/1st quartiles, with ORs =
1.22 and CIs that did not include unity. These were the highest ORs
from analyses that used the Swedish JEM.
In the unconditional analysis, Model 3, the results were similar to
the conditional analysis, the CIs were slightly narrower and, the point
estimates were almost identical (Table 5, Model 3).
4 | D IS CU SS IO N
This case‐control study confirmed our hypothesis that IPD was
associated with working in close contact with coworkers or the
general public. Similarly, elevated odds for IPD were observed
 10970274, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ajim.23439 by Nat Prov Indonesia, Wiley Online Library on [11/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
TORÉN ET AL. | 71

T A B L E 4 The prevalence of the five most common occupations with Not always maintaining social distance and with close
for the cases and the corresponding prevalence for the controls proximity to others at work, and these results varied by gender.
Prevalence; % (N) In addition, we observed especially high odds for IPD among men
Occupations Cases (N = 328) Controls (N = 1327) working outside. The other dimensions of Number of coworkers
Building caretakers 16.2% (N = 53) 12.7% (N = 168) and Contaminated workspaces had modest increases in the odds

Carpenters and joiners 15.9% (N = 52) 18.3% (N = 243)

for IPD. Importantly, we observed that for all the dimensions of
the international COVID‐19 JEM, men had higher odds for IPD
Earth‐moving and related 8.2% (N = 27) 5.7% (N = 76)
than the women. The major gender‐related difference in results
plant operators
with the Swedish JEM was the higher odds for women with the
Civil engineers 6.1% (N = 20) 6.6% (N = 88)
4th quartile of Physical proximity. Of interest is that, applying both
Concrete placers, finishers 5.5% (N = 18) 2.6% (N = 35) JEMs, contact with infected or ill patients or persons, was not
and related workers
clearly associated with IPD.
Note: Data shown are for men Working mostly outside, and partly inside S. pneumoniae is part of the normal flora of the upper
according to the dimension Location. respiratory tract, and the microorganism is mainly found in the

T A B L E 5 Logistic multivariable
Invasive pneumococcal disease (IPD)
regression models of invasive (n = 3968)
pneumococcal disease (IPD) in relation to Odds ratios with 95% confidence intervals
the different dimensions of physical Dimensions of transmission and
proximity and exposure to disease or mitigation factors Model 1a Model 2b Model 3c
infections. d
Physical proximity

3rd versus 2nd and 1st 1.13 (1.03−1.24) 1.12 (1.02−1.24) 1.12 (1.03−1.23)

4th versus 2nd and 1st 1.18 (1.05−1.32) 1.16 (1.03−1.30) 1.18 (1.06−1.31)

Exposure to diseases or infections

2nd versus 1st 1.09 (0.99–1.21) 1.09 (0.98–1.21) 1.10 (1.00–1.22)

3rd versus 1st 1.07 (0.95–1.20) 1.08 (0.96–1.21) 1.08 (0.96–1.20)

4th versus 1st 1.08 (0.95–1.23) 1.09 (0.96–1.24) 1.06 (0.94–1.20)

Men physical proximityd

3rd versus 2nd and 1st 1.14 (1.02−1.28) 1.13 (1.00−1.26) 1.14 (1.02−1.27)

4th versus 2nd and 1st 1.07 (0.90−1.28) 1.05 (0.88−1.26) 1.06 (0.90−1.26)

Exposure to diseases or infections

2nd versus 1st 1.08 (0.93−1.25) 1.09 (0.94−1.27) 1.09 (0.95−1.25)

3rd versus 1st 1.10 (0.87−1.38) 1.12 (0.89−1.41) 1.10 (0.88−1.37)

4th versus 1st 0.90 (0.67−1.19) 0.88 (0.66−1.18) 0.87 (0.66−1.15)

d
Women physical proximity

3rd versus 2nd and 1st 1.12 (0.95−1.31) 1.13 (0.96−1.33) 1.10 (0.95–1.28)

4th versus 2nd and 1st 1.22 (1.04−1.44) 1.22 (1.03−1.44) 1.22 (1.05−1.43)

Exposure to diseases or infections

2nd versus 1st 1.11 (0.96–1.27) 1.09 (0.95−1.26) 1.13 (0.99−1.29)

3rd versus 1st 1.07 (0.93−1.23) 1.07 (0.93−1.24) 1.09 (0.95−1.24)

4th versus 1st 1.14 (0.98−1.31) 1.15 (0.99−1.33) 1.12 (0.98−1.29)

a
Conditional model adjusted for gender, age, geographic region.
b
Conditional model matched for gender (except for gender specific estimates), age, geographic region,
chronic obstructive pulmonary disease, alcoholism and use of immunosuppressive drugs.
c
Unconditional logistic regression adjusted for gender (except for gender specific estimates), age,
geographic region.
d
The first (0‐24) and second group (25‐49) are merged due to lack of observations.

72 | TORÉN
nasopharynx.1 Transmission of pneumococci occurs through
droplets, either from diseased persons or from healthy carriers.
Around 10% of the adult population are asymptomatic carriers ofS.
pneumoniae. Transmission requires close contact, and is also more
likely to occur after viral infections. Person‐to‐person spread can
also occur via contaminated surfaces. With this background our
results showing quite modestly increased odds for both working in
close proximity and frequently sharing material surfaces with the
general public, are surprising. The dimension Working mostly
outside or partly inside (<4 h/day), may provide some clue to why
this is the case. These occupations are dominated by construction
workers and cleaners, often men, who are exposed to dust and
fumes.
It is known that in addition to transmission, pneumococcal
disease occurs if the asymptomatically carried S. pneumoniae
13,26
transforms into a more virulent form. A factor that can initiate
such a transformation is living in crowded settings, as the bacteria
are spread between persons and prone to mutation leading to
increased strain diversity.13 Other factors that increase the
virulence of the bacteria involve exposures of the airways to
irritants, fumes and toxic metals.13 The latter is the probable
mechanism for welders and similar workers to have an increased
14
risk for pneumococcal disease. Our results showing that men
working outside have clear risk for IPD may indicate that if the
airways are exposed to harsh conditions, the sensitivity for
different contact dimensions increases. The underlying assumption
is that men are more exposed to fumes, dust, and irritants, which
has been observed in both industrial cohorts and in general‐
population‐based studies.27−28 Another possible reason why men
have an increased risk is that there are physiological differences
between the genders, which affect both hormonal activities and
the and immune system.29
Of interest is that we observed that in all the dimensions of the
international COVID‐19 JEM there were higher odds for men
compared to the women. In the Swedish JEM there was the higher
odds for women with the 4th quartile of Physical proximity. This was
an unexpected finding. In the international COVID‐19 JEM Social
distancing was defined as maintaining a distance ≥1 m. The Swedish
JEM defines close proximity as “I work very close (near touching) to
other persons.” This may be one explanation to the observed
difference, as many occupations with very close contact to other
persons have a high percentage of women. Examples of that could be
different groups of health care workers, hair‐dressers, and
cosmetologists.
It is also of interest that regular contacts with infected patients
were not clearly associated with increased odds for IPD. Of note, the
JEM is based on the COVID‐19 paradigm or experience, although we
assume that the same personnel have similar contacts with infected
patients of other causes. It is important to remember that the study
covers the period 2006−2019, which is a pre‐COVID‐19 period.
Similar results were obtained when applying a Swedish JEM;
10970274, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ajim.23439 by Nat Prov Indonesia, Wiley Online Library on [11/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ET AL.
exposure to diseases or infections was not associated with increased
odds for IPD. This is different from the experience with COVID‐19,
and may be explained by the fact that transmission of pneumococci
occurs via droplets, such that very close contact is required for it to
be contagious. Moreover, health care workers who are dealing with
severely infected patients wear face masks.
A major strength of this analysis is it uses national registry data
with high and accurate case capture to define the outcome of interest,
IPD, in a registry with well‐established validity.30 Another strength of
the study is the use of randomly selected population‐based controls.
Furthermore, we were able to consider potential confounders using
Swedish national health records.30 The study design was a matched
case‐control study. An analysis adjusting for the matching variables by
conditional logistic regression was applied and we also performed
unconditional with the matching variables included as covariates.24
This resulted in almost identical point estimates, albeit with nar-
rower CIs.
A key analytic strength of this study is our approach of
categorizing occupational exposure. It is generally acknowledged
that the JEM approach avoids recall bias inherent to respondent
elicited exposure histories. Furthermore, we were limited to analyzing
occupational exposures during the year preceding the disease, as that
period has been shown to be critical for increased risk.31 The
“Swedish” JEM for proximity and exposure to diseases was based on
data collected in the United States. We do not consider this to be a
problem, besides that US military personnel was not included.
Military personnel make up a very small fraction of the Swedish
working‐age population.
Limitations associated with the study also should be consid-
ered. Swedish health records do not provide cigarette smoking
data, although we could address this in part through including
COPD as a covariate. The adjustments for educational achieve-
ment, capturing lower educational level and ethanol abuse, both of
which are also linked to smoking status, served to take the smoking
issue into account.32 Nonetheless, residual confounding due to
smoking cannot be excluded entirely. We did not adjust for
diabetes mellitus or ischemic heart disease, even if these
conditions showed higher prevalence among the cases. The reason
for this is that we do not believe that these two conditions are
linked to the exposure or the transmission dimensions. We
adjusted for use of immunosuppressive medications as these
drugs increase the risk for IPD and probably cause persons to
change their behaviors in relation to other people or to avoid
contacts. COPD was adjusted for because we consider it a proxy
for smoking habits. We consider smoking as a confounder as it is
linked to increased risk for disease and it probably also affects
contacts and interactions with the general public and coworkers.
In conclusion, we confirmed our hypothesis that IPD was
associated with working in close contact with coworkers or
with the general public. Outside work was associated with
increased odds for IPD, especially for men. We did not observe

TORÉN ET AL.
that contact with infected or ill patients or persons was
associated with IPD.
A U T H O R C O N TR I B U T I O N S
Kjell Torén and Maria Åberg designed the study, Linus Schiöler
analyzed the data, and all the authors interpreted the data. Kjell
Torén wrote the first draft of the manuscript, and is the guarantor
of the manuscript. Maria Åberg transferred the US occupational
codes to Swedish codes, Kjell Torén and Linus Schiöler have full
access to the data, and Kjell Torén had the final responsibility to
submit the manuscript. All authors interpreted the data and assisted
in the drafting of the manuscript. All authors approved the final
version of the manuscript.
A C KN O W L E D G M E N T S
Funding was provided by the Swedish Heart and Lung Foundation,
the Swedish Council for Working Life, Health, and Welfare (FORTE)
(no 2021‐00304), and the Swedish State under the agreement
between the Swedish government and the County Councils
(ALF‐agreements, 74570 and 965149).
CO NFL I CTS OF I NTEREST
The authors declare that there are no conflicts of interest.
D I S C L O S U R E B Y A JI M E D I T O R O F R E C O R D
John Meyer declares that he has no conflict of interest in the review
and publication decision for this article.
D A TA A C C E S S I B I L I T Y
The data that support the findings of this study are available from the
corresponding author upon reasonable request.
ETHICS APPROV AL AND I NFORMED CONSE NT
The Gothenburg Committee of Ethics approved this registry study
(Dnr 04792‐19).
ORCID
Kjell Torén http://orcid.org/0000-0001-8509-7603
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