Systems Biology in Reproductive Medicine

ISSN: 1939-6368 (Print) 1939-6376 (Online) Journal homepage: https://www.tandfonline.com/loi/iaan20

Effects of occupational exposure - is there a link

between exposure based on an occupational
questionnaire and semen quality?

Joanna Jurewicz, Michał Radwan, Wojciech Sobala, Paweł Radwan, Michał

Bochenek & Wojciech Hanke

To cite this article: Joanna Jurewicz, Michał Radwan, Wojciech Sobala, Paweł Radwan, Michał
Bochenek & Wojciech Hanke (2014) Effects of occupational exposure - is there a link between
exposure based on an occupational questionnaire and semen quality?, Systems Biology in
Reproductive Medicine, 60:4, 227-233, DOI: 10.3109/19396368.2014.907837

To link to this article: https://doi.org/10.3109/19396368.2014.907837

Published online: 07 Apr 2014.

Submit your article to this journal

Article views: 426

View Crossmark data

Citing articles: 5 View citing articles

Full Terms & Conditions of access and use can be found at

https://www.tandfonline.com/action/journalInformation?journalCode=iaan20
 http://informahealthcare.com/aan
ISSN: 1939-6368 (print), 1939-6376 (electronic)

Syst Biol Reprod Med, 2014; 60(4): 227–233

! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/19396368.2014.907837

RESEARCH ARTICLE

Effects of occupational exposure - is there a link between exposure

based on an occupational questionnaire and semen quality?
Joanna Jurewicz1*, Michał Radwan2, Wojciech Sobala1, Paweł Radwan2, Michał Bochenek3, and Wojciech Hanke1
1
Department of Environmental Epidemiology, Nofer Institute of Occupational Medicine, Lodz, Poland, 2Department of Gynecology and
Reproduction, Gameta Hospital, Rzgów, Poland, and 3Department of Biotechnology of Animal Reproduction, National Research Institute of
Animal Production, Kraków-Balice, Poland

Abstract Keywords
Several studies have suggested that human semen quality has declined over past decades and Occupational factors, semen quality, sperm
some have associated decline with occupational exposures. Many studies have been conducted chromatin structure, work setting
in occupational settings, where exposure to occupational pollutants is intense. Our objective
was to examine the association between exposure to occupational factors based on an History
occupational exposure questionnaire, and semen quality parameters (sperm concentration,
motility, sperm morphology) and sperm chromatin structure. The study population consisted of Received 21 November 2013
336 men who were attending an infertility clinic for diagnostic purposes and who had a normal Revised 21 February 2014
semen concentration of 15 mln/ml according to WHO criteria. All participants were Accepted 23 February 2014
interviewed and provided a semen sample. Additionally, a detailed questionnaire about the Published online 7 April 2014
exposure to occupational factors was performed among the study participants. The results of
the study suggest that occupational factors may affect semen quality. The exposure to noise
during work was associated with decreased motility and increased DNA damage (p ¼ 0.005 and
p ¼ 0.02, respectively). Exposure to polyvinyl chloride (PVC) decreased sperm concentration and
motility (p ¼ 0.02 and p ¼ 0.03, respectively). Whereas exposure to high temperatures and
sitting for more than 6 hours during work was positively associated with DNA fragmentation
index (DFI) (p ¼ 0.03 and p ¼ 0.001, respectively). After applying the correction for multiple
comparisons only the exposure to noise and sitting 6 hours during work was associated with
poorer semen quality (decreased motility and increased DFI, respectively). This study showed
associations between self-reported occupational exposures and impaired semen parameters.
The occupational exposure questionnaire may be useful in clinical practice for patients and
physicians to identify the work factors associated with poorer semen quality.

Introduction occupational activities involving exposure to specific chem-

The first information regarding the occupational factor
exposure and poor semen quality was stimulated by the
1977 report that dibromochloropropane (DBCP) caused
severe damage to spermatogenesis among workers in several
industrial plants producing pesticides in California [Whorton
et al. 1977]. This raised the concern regarding other
occupational exposures and their impact on semen quality.
Since then a number of occupational exposure semen reports
have contributed to understanding the impact of chemical and
physical exposures on male reproductive function [Bonde and
Storgaard 2002; Lahdetie 1995]. Studies suggest that
*Address correspondence to Joanna Jurewicz, Nofer Institute of
Occupational Medicine, Department of Environmental Epidemiology,
8 Teresy St; 91-362 Lodz, Poland. Tel: +48516073517, E-mail:
joannaj@imp.lodz.pl
icals may impair male reproductive health and cause infer-
tility in humans [Bonde 1993; Irgnes et al. 1999; Lerda 1992;
Mortensen 1988; Ng et al. 1991; Wyrobek et al. 1997].
Several pesticides have been studied in various occupational
settings and the results show that they may interfere with
spermatogenesis [Padungtod et al. 2000; Ratcliffe et al. 1987].
Exposure to electromagnetic radiation, metals (lead, chro-
mium, manganese, mercury), and organic solvents also affect
semen quality (concentration, motility, viability, and morph-
ology) and interfere with male reproductive function through
various mechanisms [Bonde and Giwercman 1995; Figa-
Talamanca et al. 2001]. Rapid industrialization, along with
changes in living conditions caused that new exposure at the
workplace started to be number one. During the last decade
there have been widespread growing concerns over potential
adverse effects that may result from a sedentary work
position, long hours driving during work, or the use of
computers at work. A sedentary position has become the
prevalent cause of testicular warming [Bujan et al. 2000;
228 J. Jurewicz et al. Syst Biol Reprod Med, 2014; 60(4): 227–233

Hjollund et al. 2000] affecting human spermatogenesis Table 1. Characteristics of the study population (n ¼ 336).
(sperm concentration, sperm count, FSH, and inhibin B)
Characteristics
[Figa-Talamanca et al. 1996; Laven et al. 1988; Sas and
Szollosi 1979]. The results of the studies on the use of a Education n (%)
computer at work and semen quality are inconsistent. Some Primary and vocational 72 (21.43)
Secondary 126 (37.50)
studies have indicated that computer managers or operators Higher 138 (41.07)
had a higher risk of infertility than service and clerical Smoking determined by cotinine level n (%)
workers [Chia and Tay 2001; Fracki et al. 1994] whereas No 235 (69.94)
others found no risk for poorer semen quality [Sun et al. Yes 101 (30.06)
2005]. BMI (kg/m2) n (%)
Most of the studies have been focused on a single specific 525 116 (34.52)
25 220 (65.48)
factor (physical or chemical) [Chia et al. 1996; Thonneau Mean (sd) 27.2 ± 3.7
et al. 1996; Stoy et al. 2004] or occupation [Figa-Talamanca Median (min–max) 27.3 (18.3–39.5)
et al. 1992; Kurinczuk and Clarke 2001] where exposure to Duration of couple’s infertility (years) n (%)
occupational pollutants are usually more intense. In such 1–2 125 (37.20)
studies, the collection of the data is very accurate regarding 2–3 110 (32.74)
3–5 51 (15.18)
one risk factor or level of exposure using biomarkers for that 45 50 (14.88)
exposure. This approach is not generally useful in clinical *Past diseases, which may have impact on semen quality n (%)
practice to identify the reason for poorer semen quality as the No 292 (86.91)
patients often represent different occupations with different Yes 44 (13.09)
work characteristics. It is not possible to accurately assess the Abstinence (days) n (%)
whole range of work exposures. To identify occupational risk 53 17 (5.06)
3–7 248 (73.81)
factors for poorer semen quality in clinical settings general 47 20 (5.95)
occupational exposure information (based on the question- Missing data 51 (15.18)
naire about occupational exposures) may be useful Mean (sd) 5.0 ± 2.3
[De Fleurian et al. 2009; Garcia et al. 2005; Tielemans Median (min–max) 5.0 (0.0–20.0)
et al. 1999; Wong et al. 2003]. Our objective was to examine Age (years)
Mean (sd) 32.24 (4.43)
the association between exposure to occupational factors Median (min–max) 31.70 (22.01–44.26)
(existing in contemporary work settings) among patients in Coffee (days/week) n (%)
clinical settings, based on an occupational exposure ques- 51/week 80 (23.80)
tionnaire, and semen quality parameters (sperm concentra- 1–6/week 78 (23.20)
tion, motility, sperm morphology) and sperm chromatin Everyday 178 (53.00)
structure. Leisure time activity (MET) n (%)
No 103 (30.65)
Yes 233 (69.35)
Results Cell phone (years) n (%)
Study population 0–5 53 (15.77)
6–10 177 (52.68)
The study population consisted of 336 men who attended 11–25 80 (23.81)
Missing data 26 (7.74)
infertility clinics for diagnostic purposes. The mean age of
Boxer shorts n (%)
men participating in this study was 32.2 years. Most of them
No 199 (59.20)
had higher (41.1%) or secondary (37.5%) education, while Yes 137 (40.80)
about 21% had only vocational education (Table 1). A total of Alcohol use n (%)
65% of the examined men had a BMI  25 kg/m2. Most of the None or 51 drink/week 111 (33.05)
participants were non smokers (69.9%) (Table 1). Past 1–3 drinks/week 171 (50.89)
Everyday 54 (16.06)
diseases which may impact semen quality (e.g. mumps,
cryptorchidism, testes surgery, testes trauma) were reported Level of occupational stress n (%)
Low (65–80 points) 108 (32.14)
by 13% of the participants. The period of abstinence before Medium (81–101 points) 117 (34.82)
the semen collection and analysis was about 5 days (Table 1). High (102–152 points) 102 (30.36)
The duration of the couple’s infertility could be divided into Missing data 9 (2.68)
two major groups from 1 to 2 years (37.2%) and from 2–3 *Past diseases which may have impact on semen quality – mumps,
years (32.7%). Most of the study men reported a medium level cryptorchidism, testes surgery, testes trauma.
of occupational stress (35%). The leisure time physical
activity was reported by 69.4% of the study population
(Table 1). Cell phone usage varied from 6 to 10 years and was
Occupational factors among study participants
documented among 53% of study subjects. Approximately
24% of the men used the cell phone for more than 10 years The occupational risk factors are presented in Table 2. Most
(Table 1) and 41% wore loose underwear (boxer shorts). As of the study men worked as office workers (33.63%), physical
summarized in Table 1, everyday coffee drinking was workers (22.62%), farmers (7.14%), drivers (6.85%), and
reported by 53% of study participants and most of the study salesman (5.36%). The number of work hours during the week
men drank 1–3 drinks per week (50.9%). was about 47 and during the day about 9 (Table 2). Most of
DOI: 10.3109/19396368.2014.907837 Occupational factors and semen quality 229
Table 2. Occupational risk factors among study participants. Table 3. Distribution of semen parameters.

Occupation, n (%) Statistical variables n ¼ 336

Farmer 24 (7.14) Semen quality Mean ± SD Median Range n
Physical worker 76 (22.62)
Office worker 113 (33.63) Semen concentration 50.49 ± 52.33 32.60 15.00–360.00 334
Driver 23 (6.85) (mln/ml)
Car repair worker 11 (3.27) Motility (%) 56.00 ± 20.05 56.00 4.00–99.00 330
Teacher 7 (2.08) Sperm with abnormal 53.24 ± 23.78 50.00 11.00–98.00 331
Salesman 18 (5.36) morphology (%)
Physician 5 (1.49) DFI (%) 15.88 ± 10.79 13.30 2.72–71.23 279
Policeman 7 (2.08)
DFI – DNA fragmentation index; SD – standard deviation.
Laboratory worker 5 (1.49)
Photographer 2 (0.60)
Housekeeper 2 (0.60)
Other 43 (12.80) Occupational factors and semen quality
Work time during week (hours) Table 3 presents the semen quality among the study subjects.
Mean ± SD 46.62 (11.84) Semen quality among the study participants was in the normal
Median (min–max) 40.00 (10.00–105.00)
range of the WHO [1999; 2010] indicators [Jurewicz et al.
Work time during day (hours)
Mean ± SD 8.80 (1.79) 2013]. The mean semen concentration was 50.49 mln/ml and
Median (min–max) 8.00 (4.00–18.00) the percentages of motile sperm cells, abnormal morphology,
Sitting during work (hours), n (%) and DNA fragmentation were 56, 53, and 16, respectively
6 hours 116 (34.52) (Table 3). As shown in Table 4, a reduction in semen
Mean (SD) 3.82 (3.11) concentration was observed when the study participants were
Median (min–max) 4.00 (0.00–14.00)
driving a car (to work or during work) more than 120 minutes
Driving a car (min), n (%)
4120 min 84 (25.00) a day (p ¼ 0.04) and when the person was exposed to noise
Mean (SD) 35 (28.13) (p ¼ 0.04). Additionally, exposure to noise decreased the
Median (min–max) 32 (5–200) percentage of motile sperm cells (p ¼ 0.01). A positive
Computer use during work, n (%) association was observed between exposure to high tempera-
Almost the whole work time 142 (42.26) tures and keeping a laptop on the knees with the level of DNA
Keeping laptop on knees 56 (16.67)
fragmentation (p ¼ 0.05 and p ¼ 0.05, respectively).
Exposure at the work position, n (%)
Noise 108 (32.14)
After adjusting for age, smoking, BMI, past diseases, time
Vibration* 60 (17.85) of sexual abstinence, alcohol consumption, occupational
Electromagnetic fields 189 (56.25) stress, cell phone use, boxer short use, coffee drinking, and
Solvents 77 (22.92) physical activity (Table 5) a negative association was
Pesticides 37 (11.01)
Heavy metals 12 (3.57) observed between exposure to PVC and semen concentration
PVC 18 (5.36) (p ¼ 0.02) and motility (p ¼ 0.03). The exposure to noise
High temperatures 53 (15.77) during work was associated with a decrease in motility and an
increase in DNA damage (p ¼ 0.005 and p ¼ 0.02, respect-
* – Vibration on a whole body 40 (11.90%); Vibration on hands
20 (5.95%) ively). Whereas exposure to high temperatures and sitting for
more than 6 hours during work was positively associated with
DNA damage (p ¼ 0.03 and p ¼ 0.001, respectively). After
the study men sat for about 4 hours at work, about 35 % of applying the correction for multiple comparisons the exposure
participants sat more than 6 hours. Approximately 25% of the to noise decreased motility and sitting 6 hours increased the
men drove more than 120 minutes to work or during work DNA fragmentation index.
(Table 2). A total of 42.26 % of the study participants used a
Discussion
computer almost the whole time during work. Keeping a
laptop on the knees was declared by about 17% of the men. Results from the cross-sectional study of 336 men suggests
About 32% of participants were exposed to noise in the work that several of the occupational factors that were analyzed are
environment (Table 2). Men were exposed to vibration on related to poor semen quality including: sperm concentration,
work position (18%), with whole body vibration declared by motility, and DNA fragmentation index (DFI) after adjusting
11.90% and vibration on hands by 5.95%. In addition to the for potential confounders. Strong associations were found
above, 22.9% of the study participants were exposed during between sitting 6 hours during work and exposure to noise
work to solvents, e.g. 2-bromochloropropane, trichloroethyl- and increased DNA damage and decreased motility. These
ene, tetrachloroethylene, 56.25% to electromagnetic fields, findings are in line with studies showing that sedentary work
11.01% to pesticides, fungicides (such as mancozeb, chlor- leads to an increase in scrotal temperature [Bujan et al. 2000;
othalonil, captan), herbicides (MCPA (4-chloro-2-methylphe- Hjollund et al. 2000] that is strongly associated with
noxy acetic acid), 2,4-D (2,4-Dichlorophenoxyacetic acid), decreased sperm concentration [Hjollund et al. 2000].
linuron), insecticides (delthametrin, lambda-cyhalothrin; Similar results were found for total sperm count, FSH, and
acaricide: spirodiclofen), 3.57% to heavy metals (lead, inhibin B. In contrast, motility, morphology, pH, and
cadmium, mercury), 5.36% to polyvinyl chloride (PVC), and testosterone were not significantly associated with tempera-
15.77% to high temperatures (Table 2). ture [Hjollund et al. 2002]. While Magnusdottir et al. [2005]
230 J. Jurewicz et al. Syst Biol Reprod Med, 2014; 60(4): 227–233

Table 4. The association between occupational factors and main semen parameters (concentration, motility, morphology) and sperm chromatin
structure-univariate analysis.

Semen concentration Sperm with abnormal

(mln/ml) Motility (%) morphology (%) DFI (%)
Variables coef 95% CI p coef 95% CI p coef 95% CI p coef 95% CI p
Sitting during work; (6 hours) 0.11 0.20–0.44 0.50 0.32 4.14–3.27 0.88 0.12 0.08–4.31 0.97 0.08 0.55–0.68 0.14
Driving a car; (4120 min) 0.39 1.32–1.55 0.04 1.23 4.07–7.55 0.73 1.89 4.32–8.55 0.64 0.22 0.46–0.13 0.38
Computer use during work 0.01 0.28–0.14 0.80 3.55 9.38–1.55 0.20 0.95 6.44–3.21 0.89 0.09 0.14–0.36 0.89
(Almost the whole work time)
Keeping laptop on knees 0.24 0.31–0.82 0.44 1.22 6.13–8.74 0.78 4.37 5.66–12.34 0.54 0.04 1.05–3.37 0.05
Noise on work position 0.28 1.05–2.05 0.04 6.55 2.11–9.21 0.01 1.78 4.55–6.33 0.58 0.02 0.23–0.33 0.07
Vibration on work position 0.15 0.02–0.56 0.62 4.55 2.11–9.34 0.21 2.33 4.30–9.27 0.64 0.09 0.32–0.18 0.62
Exposure to solvents 0.20 0.23–0.45 0.48 4.28 0.25–8.77 0.08 1.89 7.33–2.89 0.39 0.05 0.11–0.23 0.63
Exposure to electromagnetic fields 0.10 0.12–0.34 0.55 0.33 4.55–1.85 0.15 1.58 5.55–2.70 0.52 0.03 0.23–0.15 0.65
Exposure to heavy metals 0.55 0.17–0.34 0.34 0.88 11.25–11.33 0.93 7.31 4.25–13.26 0.32 0.34 0.08–0.65 0.15
Exposure to pesticides 0.23 0.38–0.48 0.55 1.62 4.55–7.33 0.78 2.45 5.33–11.53 0.65 0.10 0.18–0.42 0.55
Exposure to PVC 0.46 0.23–0.97 0.15 4.33 3.21–15.55 0.09 1.84 8.22–12.30 0.85 0.21 0.52–0.21 0.43
Exposure to high temperature 0.19 0.45–0.35 0.70 2.72 2.58–6.44 0.58 2.88 4.96–11.55 0.45 0.22 1.27–5.82 0.05

Reference categories: Sitting during work – less than 3 hours; Driving a car – less than 60 minutes; Computer use during work- not using at all, rarely
use; Keeping laptop on knees – No; Noise on work position – No; Vibration on work position – No; Exposure to solvents – No; Exposure to
electomagnetic fields – No; Exposure to heavy metals – No; Exposure to pesticides – No; Exposure to PVC – No; Exposure to high temperature – No
DFI – DNA fragmentation index; SD – standard deviation; coef – b coefficient
Significance level 0.05 was used for statistical interference.

Table 5. The association between occupational factors and main semen parameters (concentration, motility, morphology) and sperm chromatin
structure-multivariate analysis.

Semen concentration Sperm with abnormal

(mln/ml) Motility (%) morphology (%) DFI (%)
Variables coef 95% CI p coef 95% CI p coef 95% CI p coef 95% CI p
Sitting during work; (6 hours) 0.27 0.33–0.68 0.55 0.44 1.68–1.58 0.44 0.44 1.44–4.25 0.87 0.78 0.33–0.85 0.001*
Driving a car; (4120 min) 0.15 0.23–1.89 0.30 0.33 2.33–6.21 0.69 1.55 1.29–8.33 0.59 1.22 0.78–0.12 0.12
Computer use during work
(Almost the whole work time) 1.33 0.55–0.78 0.33 1.13 2.57–1.42 0.87 1.22 2.78–1.25 0.65 0.56 0.47–0.95 0.48
Keeping laptop on knees 0.58 0.25–0.78 0.75 1.65 1.24–9.74 0.89 3.33 0.78–10.42 0.33 1.46 0.21–1.25 0.15
Noise on work position 0.28 0.15–0.69 0.25 2.21 1.23–8.27 0.005* 0.89 3.39–7.22 0.18 1.22 0.39–0.78 0.02
Vibration on work position 2.88 0.28–1.78 0.63 1.34 1.58–8.32 0.24 1.36 1.12–5.48 0.32 0.35 0.44–0.15 0.29
Exposure to solvents 2.55 0.55–1.25 0.77 1.55 0.45–1.78 0.25 1.54 4.44–1.59 0.69 1.64 1.55–1.89 0.45
Exposure to electromagnetic fields 0.99 0.78–0.22 0.57 1.33 1.56–3.28 0.26 1.59 2.17–1.48 0.42 0.55 0.12–0.48 0.78
Exposure to heavy metals 1.02 0.78–0.58 0.36 1.78 7.42–5.69 0.74 1.98 0.64–7.89 0.69 0.33 0.58–1.78 0.27
Exposure to pesticides 0.55 0.55–0.78 0.55 1.38 2.17–4.24 0.59 1.78 3.36–5.87 0.43 0.98 0.14–1.32 0.45
Exposure to PVC 0.78 0.28–0.65 0.02 0.89 1.23–2.32 0.03 1.05 2.36–8.73 0.64 1.44 0.59–0.75 0.74
Exposure to high temperature 2.01 0.78–1.74 0.69 0.78 2.78–4.33 0.37 0.77 0.42–5.13 0.57 1.21 1.44–1.89 0.03

Reference categories: Sitting during work – less than 3 hours; Driving a car – less than 60 minutes; Computer use during work – not using at all, rarely
use; Keeping laptop on knees – No; Noise on work position – No; Vibration on work position – No; Exposure to solvents – No; Exposure to
electomagnetic fields – No; Exposure to heavy metals – No; Exposure to pesticides – No; Exposure to PVC – No; Exposure to high temperature – No
Model was adjusted for: age, smoking, BMI, past diseases, time of sexual abstinence, alcohol consumption, occupational stress, cell phone use, boxer
shorts use, coffee drinking, physical activity
DFI – DNA fragmentation index; SD – standard deviation; coef – b coefficient
* – significant association after control for multiple comparisions
Significance level 0.05 was used for statistical interference.

noticed that prevalence of sedentary work was the lowest
among men with the best semen quality, Stoy et al. [2004] did
not find a harmful effect of sedentary work on sperm density
among Danish men from infertility centers.
Impairment of spermatogenesis has been observed in a high
prevalence among professional drivers [Figa-Talamanca et al.
1996; Sas and Szollosi 1979; Thonneau et al. 1996]. The study
among taxi drivers in Rome found that taxi drivers, compared
to the controls, had a significantly lower prevalence of normal
sperm forms [Figa-Talamanca et al. 1996]. The result was more
pronounced in those who had been working as taxi drivers for a
long time. In other studies, workers coming from the ‘‘trans-
port and communication’’ industries were reported to be at
higher risk of abnormal sperm motility [Chia et al. 1994] or to
have lower sperm count [Henderson et al. 1986] than other
occupational groups. Bujan et al. [2000] found that scrotal
temperature increased significantly (p50.0001) after 2 hours
of driving as compared to walking. Our findings suggest that
exposure to work place noise decreases sperm motility
(p ¼ 0.005) and increases sperm DNA damage (p ¼ 0.02) No
previous data were found in the literature regarding a possible
relationship between exposure to noise and sperm parameter
alteration. The explanation for this may be that work place
noise caused stress which can be negatively associated with
semen quality [Clarke et al. 1999; Eskiocak et al. 2006; Fenster
et al. 1997; Jurewicz et al. 2013a].
DOI: 10.3109/19396368.2014.907837
Other tendencies observed in our study suggest that
exposure to high temperatures may be associated with an
increase in DNA damage. As the active production of sperm
requires a temperature of about 3–4  C lower than normal
body temperature [Sheiner et al. 2003] the effect of chronic
occupational exposure to high temperatures has been
examined, in addition to semen quality in the ceramics
industry [Figa-Talamanca et al. 1992]. The study indicated a
higher prevalence of pathologic sperm profiles among the
exposed subjects [Figa-Talamanca et al. 1992]. Bonde [1990]
studied metal arc alloyed steel welders with moderate
exposure to radiant heat and noticed a decrease in sperm
morphology during six weeks of exposure. Velez de la Calle
et al. [2001] investigated infertility risk factors in a French
military population and found heat exposure as an independ-
ent risk factor for male infertility (OR 4.5, 95%CI 1.9–10.6),
using a multivariate analysis.
In the present study, PVC exposure decreases sperm
concentration and motility. This may reflect exposure to
DEHP (di-(2-ethylhexyl) phthalate) that is the dominant
plasticizer used in PVC due to its low cost. The recent review
of the studies of the health effect associated with exposure to
phthalate demonstrated negative associations between phthal-
ate levels commonly experienced by the public and impaired
sperm quality (concentration, morphology, motility)
[Jurewicz and Hanke 2011].
Mechanisms underlying reproductive toxic alteration
caused by occupational exposure are complex. Effects of
chemicals on reproduction may be induced directly by the
chemical itself on reproductive organs (e.g. testes) or
indirectly by altering hormonal regulation. Toxicants that
damage the Leydig cells can lead to reduced secretion of
testosterone, which in turn affects Sertoli cell function and
spermatogenesis [Kumar 2004]. Also elevated testicular
temperature is a well-documented mechanism of abnormal
spermatogenesis in common diseases associated with male
infertility, e.g. varicocele and undescended testis [Lerchl et al.
1993; Wright et al. 1997].
The occupational exposure documented in the present
study was based on a detailed occupational questionnaire
design of the Nofer Institue of Occupational Medicine. As the
questionnaire was administrated to men attending an infertil-
ity clinic for diagnostic purposes we can assume that
exposures in this population may be limited. A different
study which was based on self-reported physical or chemical
occupational exposures and its’ impact on semen quality was
performed by De Fleurian and co-workes [2009]. Significant
associations were found between semen impairment and
occupational risk factors such as: heavy metals, solvents,
fumes, polycyclic aromatic hydrocarbons, mechanical vibra-
tions, and extended sitting, which is in line with our findings.
Our study had several strengths. First, a detailed descrip-
tion of occupational exposure based on a face to face
questionnaire was performed, which can be used to identify
occupational risk factors for poorer semen quality in clinical
settings. The questionnaire was prepared based on years of
experience of Nofer Institute of Occupational Medicine,
Lodz, Poland. Second, the results were adjusted for many
factors that may be associated with semen quality. This
included smoking status that was verified using the level of
Occupational factors and semen quality 231
cotinine in saliva. A third strength arises from the fact that
many different semen parameters were included in the
analysis: main semen parameters (concentration, motility,
morphology) and sperm chromatin structure.
On one hand, the study does have weaknesses. First, we
were not able to examine a representative sample of the
general male population. We tried to overcome this
disadvantage by selecting only men with normal semen
parameters (WHO 2010) classification among the male
infertility patients. Also analysis of a single semen sample
per subject does not allow for physiological variability of
semen parameters. On the other hand, all subjects were
recruited in the same center, and all semen samples were
collected and analyzed using a standardized protocol. The
second limitation arises from the fact that to assess the
occupational factors and exposure a questionnaire was used.
The information which is included in such a questionnaire
may not be sufficient to study the different exposures.
However, the questionnaire which was used in the present
study was standardized and prepared in the center, which is
engaged in occupational health and medicine. Exposure based
data collection using interviews in relation to such agents as
pesticides and solvents may not be reliable. However, we
assumed that the men (most of them had higher education)
had reasonable information about their working conditions.
In conclusion, our findings support the results of previous
studies regarding the association between occupational factors
(sedentary work, exposure to high temperature, noise, and
PVC) and semen quality (semen concentration, motility, and
sperm DNA damage). The study showed associations between
self-reported occupational exposures and impaired semen
parameters. This approach allows patients and physicians to
become aware of the relationships between some occupations
and altered semen parameters. Further research is necessary
to evaluate the observed associations in this study and the use
of this information to ascribe appropriate interventions.
Materials and Methods
Study population
The study population consisted of 344 men who attended the
infertility clinic for diagnostic purposes with a normal semen
concentration of 15 mln/ml [WHO 2010] recruited between
2007–2011. They were all healthy and under 45 years of age.
Out of 580 men who fulfill the inclusion criteria (based on
semen analysis) 344 (59%) of the men agreed to participate in
the study and signed the written agreement. The Nofer
Institute of Occupational Medicine Bioethical Committee
Board approved the study (Resolution No 9/2007
(04.06.2007)) and written informed consent was obtain from
all subjects before their participation. All men completed a
questionnaire that included questions about demographics,
socio-economic status, medical history, and lifestyle factors.
Smoking status was verified by measurement of cotinine level
in saliva using high performance liquid chromatography
coupled with tandem mass spectrometry/positive electrospray
ionization (LC-ESI + MS/MS) and isotope dilution method.
A detailed description of this study population has been
presented elsewhere [Jurewicz et al. 2013a; Jurewicz et al.
2014]. The work during the time of questionnaire was
232 J. Jurewicz et al.
declared by 336 (98% of original study sample) and the
association between occupational factors and semen quality
was studied in this group of men.
Information about occupational factors
To assess the occupational exposure in a contemporary work
setting the detailed questionnaire was administered among the
study participants by trained interviewers. The questionnaire
included job title, tasks performed at work, position of body
during work and time in each position, carrying heavy things
and transmitting of these things, heavy physical effort, mainly
standing or sedentary posture during work, and driving a car
during work or work commute. Also the questionnaire
included information about occupational exposures to chem-
icals (solvents, pesticides, heavy metals, dyes, paints,
varnishes, and PVC), biological substances (blood, urine),
and physical agents (ionizing radiation, X radiation, exposure
to electromagnetic fields, noise, high temperature, and
mechanical vibrations).
Semen collection and analysis
All men provided a semen sample. The ejaculation abstinence
time and time between sample collection and analysis were
recorded. The ejaculate was obtained by masturbation into a
sterile standard plastic container as a part of fertility
investigation. Semen analysis was performed after 30 min of
liquefaction at 37  C. The samples were examined by trained
laboratory technicians. The semen analysis included deter-
mination of ejaculate volume, sperm concentration, and
sperm motility according to WHO [1999] guidelines. Sperm
morphology was quantified using strict Kruger criteria
[Kruger et al. 1988]; the semen smears were air-dried,
fixed, and stained according to Papanicolaou.
The assessment of the sperm chromatin structure assay
(SCSA) was performed using flow cytometry (DAKO
Galaxym DAKO, Denmark) [ASRM 2006] as described
elsewhere [Jurewicz et al. 2013b]. The cells with abnormal
chromatin structure (i.e. fragmented DNA) showed a distinct
shift of alpha t parameter value (alpha-t ¼ red/(red + green)
fluorescence). The DFI was calculated according to the
formula:
DFI ¼ ðcells with shift of alpha  t parameter=all cellsÞ  100
Statistical analysis
Statistical inference was based on two-sided tests at a 0.05
significance level. A linear regression model was used for the
analysis of dependence between occupational factors and
semen quality parameters (concentration, motility, morph-
ology) and sperm chromatin structure. First, we compared
semen quality for men in relation to work characteristics.
Then we compared the distributions of other variables from
the questionnaire among men with different work character-
istics by chi-square test in order to identify potential
confounders. Finally, data were analyzed using multiple
linear regressions. Normally distributed outcome variables
were entered directly as continuous variables in the model,
whereas sperm concentration (mln/ml) and DFI (%) were
Syst Biol Reprod Med, 2014; 60(4): 227–233
transformed by use of the natural logarithm to obtain the
normality. The qqnorm plot was used to visually assess the
normality of distribution. Covariates initially included factors
possibly associated with semen parameters or work charac-
teristics but were then excluded stepwise if they did not
change the estimate by more than 10%. The same set of
confounders was used for all outcomes: age (continuous
variable), smoking, physical activity and boxer shorts wearing
(Yes/No), past diseases (e.g. mumps, cryptorchidism, tes-
tes surgery, testes trauma) (Yes/No), BMI (25 kg/m2 and
25 kg/m2), sexual abstinence time (continuous variable-
days), alcohol (None or 51 drink/week, 1–3 drinks/week, 4–7
drinks per week), coffee drinking (51/week, 1–6/week,
everyday), cell phone use (0–5 years, 6–10 years, 11–25
years), and occupational stress (low, medium, high level).
Univariate and multivariate analyses were performed to
assess the relationship between occupational factors and
semen quality. Benjamini and Hochberg [1995] method (False
Discovery Rate) was used to correct p values for multiple
comparisons. Statistical analyses were performed using
R software, version 2.15.1 (http://www.R-project.org) [R
Core TeamR 2013]. The results were presented as regression
coefficients with 95 percent confidence intervals and p value.
Declaration of interest
We declare no conflict of interest. This study was performed
under the project ‘‘Epidemiology of reproductive hazards in
Poland — multicentre study in Poland’’ supported by the
National Center for Research and Development in Poland,
from grant no. PBZ-MEiN-/8/2//2006; contract no. K140/P01/
2007/1.2.1.2.
Author contributions
Involved in study concept and design: JJ, WH, MR; Data
analysis: WS; Drafted the manuscript: JJ; Responsible for
recruitment of men to the study and analysis of main semen
parameters: MR, PR; Responsible for analysis of sperm
chromatin structure: MB. All authors provided substantial
intellectual contributions and approved the final version of
manuscript.
References
ASRM. (2006) ASRM Practice Committee Report on optimal evaluation
of the infertile male. Fertil Steril 86:202–9.
Benjamini Y. and Hochberg Y. (1995) Controlling the false discovery
rate: A practical and powerful approach to multiple testing. J R Stat
Soc Ser B 57:289–300.
Bonde, J.P. and Giwercman, A. (1995) Occupational hazards to male
fecundity. Reprod Med Rev 4:59–73.
Bonde, J.P. (1990) Semen quality in welders exposed to radiant heat.
Br J Indust Med 49:515–8.
Bonde, J.P. (1993) The risk of male subfecundity attributable to welding
of metals. Studies of semen quality, infertility, fertility, adverse
pregnancy outcome and childhood malignancy. Int J Androl 16:1–29.
Bonde, J.P. and Storgaard, L. (2002) How work-place conditions,
environmental toxicants and lifestyle affect male reproductive func-
tion. Int J Androl 25:262–8.
Bujan, L., Daudin, M., Charlet, J.P., Thonneau, P., and Mieusset, R.
(2000) Increase in scrotal temperature in car drivers. Hum Reprod 15:
1355–7.
Chia, S.E., Ong, G.N., and Tsakok, F.M.H. (1994) Study of the effects of
occupation and industry on sperm quality. Am Acad Med Singapore
23:645–9.
DOI: 10.3109/19396368.2014.907837
Chia, S.E., Ong, C.N., Tsakok, M.F.H., and Ho, A. (1996) Semen
parameters in workers exposed to trichloroethylene. Reprod Toxicol
10:295–9.
Chia, S.E., and Tay, S.K. (2001) Occupational risk for male infertility:
A case-control study of 218 infertile and 227 fertile men. J Occup
Environ Med 43:946–51.
Clarke, R.N., Klock, S.C., Geoghegan, A., and Travasson, D.E. (1999)
Relationship between psychological stress and semen quality among
in-vitro fertilization patients. Hum Reprod 14:753–8.
De Fleurian, G., Perrin, J., Ecochard, R., Dantony, E., Lanteaume, A.,
and Achard, V. (2009) Occupational exposures obtained by question-
naire in clinical practice and their association with semen quality.
J Androl 30:566–79.
Eskiocak, S., Gozen, A.S., Taskiran, A., Kilic, A.S., Eskiocak, M., and
Gulen, S. (2006) Effects of psychological stress on the L-arginine-
nitric oxide pathway and semen quality. Braz J Med Biol Res 39:
581–858.
Fenster, L., Katz, D.F., Wyrobek, A.J., Pieper, C., Rempel, D.M.,
Oman, D., et al. (1997) Effects of psychological stress on human
semen quality. J Androl 18:194–202.
Figa Talamanca, I., Dell’Orco, V., Pupi, A., Dondero, F., Gandini, L.,
Lenzi, A., et al. (1992) Fertility and semen quality of workers exposed
to high temperatures in the ceramics industry. Reprod Toxicol 6:
517–23.
Figà-Talamanca, I., Cini, C., Varricchio, G.C., Dondero, F., Gandini, L.,
Lenzi, A., et al. (1996) Effects of prolonged autovehicle driving on
male reproduction function: A study among taxi drivers. Am J Ind
Med 30:750–8.
Figà-Talamanca, I., Traina, M.E., and Urbani, E. (2001) Occupational
exposures to metals, solvents and pesticides: Recent evidence on male
reproductive effects and biological markers. Occup Med (Lond) 51:
174–88.
Fracki, S., Bablok, L. and Mezynski, J. (1994) Fertility disturbances in
males working as professional computer operators. Ginekol Pol 65:
41–4.
Gracia, C.R., Sammel, M.D., Coutifaris, C., Guzik, D.S., and
Barnhart, K.T. (2005) Occupational exposures and male infertility.
Am J Epidemiol 162:729–33.
Henderson, J., Rennie, C.G., and Baker, H.W.G. (1986) Association
between occupational group and sperm concentration in infertile men.
Clin Reprod Fertil 4:275–81.
Hjollund, N.H., Bonde, J.P., Jensen, T.K., and Olsen, J. (2000) Diurnal
scrotal skin temperature and semen quality. The Danish First
Pregnancy Planner Study Team. Int J Androl 23:309–18.
Hjollund, N.H., Storgaard, L., Ernst, E., Bonde, J.P., and Olsen, J. (2002)
The relation between daily activities and scrotal temperature. Reprod
Toxicol 16:209–14.
Irgens, A., Krüger, K., and Ulstein, M. (1999) The effect of male
occupational exposure in infertile couples in Norway. J Occup Environ
Med 41:1116–20.
Jurewicz, J., and Hanke, W. (2011) Exposure to phthalates: reproductive
outcome and children health. A review of epidemiological studies.
Int J Occup Med Environ Health 24(2):115–141.
Jurewicz, J., Hanke, W., Radwan, M., Sobala, W., Ligocka, D.,
Radwan, P., et al. (2013b) Human urinary phthalate metabolites
level and main semen parameters, sperm chromatin structure, sperm
aneuploidy and reproductive hormones. Reprod Toxicol 42:232–41.
Jurewicz, J., Radwan, M., Merecz-Kot, D., Sobala, W., Ligocka, D.,
Radwan, P., et al. (2013a) Occupational, life stress and family
functioning-does it affect semen quality? Ann Hum Biol (2013 Nov 4.
Epub ahead of print); DOI: 10.3109/03014460.2013.849755.
Jurewicz, J., Radwan, M., Sobala, W., Ligocka, D., Radwan, P.,
Bochenek, M., et al. (2014) Lifestyle and semen quality- role of
modifiable risk factors. Syst Biol Reprod Med 60:43–51.
Kumar, S. (2004) Occupational exposure associated with reproductive
dysfunction. J Occup Health 46:1–19.
Kruger, T.F., Acosta, A.A., Simmons, K.F., Swanson, R.J., Matta, J.F.,
and Oehninger, S. (1988) Predictive value of abnormal sperm
morphology in in vitro fertilization. Fertil Steril 49:112–7.
Kurinczuk, J.J. and Clarke, M. (2001) Case-control study of leatherwork
and male infertility. Occup Environ Med 58:217–24.
Occupational factors and semen quality 233
Lahdetie, J. (1995) Occupation- and exposure-related studies on human
sperm. J Occup Environ Med 37:922–30.
Lerchl, A., Keck, C., Spiteri-Grech, J., and Nieschlag, E. (1993) Diural
variations in scrotal temperature˛ of normal men and patients with
varicocele before and after treatment. Int J Androl 16:195–200.
Laven, J.S., Haverkorn, M.J., and Bots, R.S. (1988) Influence of
occupation and living habits on semen quality in men (scrotal
insulation and semen quality). Eur J Obstet Gynecol Reprod Biol 29:
137–41.
Lerda, D. (1992) Study of sperm characteristics in sperm in persons
occupationally exposed to lead. Am J Ind Med 22:567–71.
Magnusdottir, E.V., Thorsteinsson, T., Thorsteinsdottir, S.,
Heimisdottir, M., and Olafsdottir, K. (2005) Persistent organochlor-
ines, sedentary occupation, obesity and human male subfertility. Hum
Reprod 20:208–15.
Mortensen, J.T. (1988) Risk for reduced sperm quality among metal
workers, with special reference to welders. Scand J Work Environ
Health 14:27–30.
Ng, T.P., Goh, H.N., Ng, Y.L., Ong, H.Y., Ong, C.N., Chia, K.S., et al.
(1991) Male endocrine functions in workers with moderate exposure
to lead. Br J Ind Med 48:485–91.
Padungtod, C., Savitz, D.A., Overstreet, J.W., Christiani, D.C.,
Ryan, L.M., and Xu, X. (2000) Occupational pesticide exposure and
semen quality among Chinese workers. J Occup Environ Med 42:
982–92.
R Core TeamR (2013) A language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna, Austria.
URL http://www.R-project.org/.
Ratcliffe, J., Schrader, S.M., Steenland, K., Clapp, D.E., Turner, T., and
Hornung, R.W. (1987) Semen quality in papaya workers with long
term exposure to ethylene dibromide. Br J Ind Med 44:317–26.
Sas, M. and Szollosi, J. (1979) Impaired spermiogenesis as a common
finding among professional drivers. Arch Androl 3:57–60.
Sheiner, E.K., Sheiner, E., Hammel, R.D., Potashnik, G., and Carel, R.
(2003) Effect of occupational exposures on male fertility: Literature
review. Ind Health 41:55–62.
Stoy, J., Hjollund, N.H., Mortensen, J.T., Burr, H., and Bonde, J.P.
(2004) Semen quality and sedentary work position. Int J Androl 27:
5–11.
Sun, Y.L., Zhou, W.J., Wu, J.Q., and Gao, E.S. (2005) Does exposure to
computers affect the routine parameters of semen quality? Asian J
Androl 7:263–6.
Thonneau, P., Ducot, D., Bujan, L., Mieusset, R., and Spira, A. (1996)
Heat exposure as a hazard to male fertility. Lancet 347:204–5.
Tielemans, E., Burdorf, A., te Velde, E.R., Weber, R.F., Van Kooij, R.J.,
Veulemans, H., et al. (1999) Occupationally related exposures
and reduced semen quality: A case control study. Fertil Steril 71:
690–6.
Velez de la Calle, J.F., Rachou, E., le Martelot, M.T., Ducot, B.,
Multigner, L., and Thonneau, P.F. (2001) Male infertility risk factors
in a French military population. Hum Reprod 16:481–6.
WHO. (1999) WHO laboratory manual for the examination of human
semen and sperm-cervical mucus interaction. 4th edn. World Health
Organization. Cambridge University Press, Cambridge, UK.
WHO. (2010) WHO laboratory manual for the examination of human
semen and sperm-cervical mucus interaction. 5th edn. World Health
Organization. Cambridge University Press, Cambridge, UK.
Whorton, D., Krauss, R.M., Marshall, S., and Milby, T.H. (1977)
Infertility in male pesticide workers. Lancet 17;2:1259–61.
Wong, W.Y., Zielhuis, G.A., Thomas, C.M., Merkus, H.M., and
Steegers-Theunissen, R.P. (2003) New evidence of the influence of
exogenous and endogenous factors on sperm count in man. Eur J
Obstet Reprod Biol 110:49–54.
Wright, E.J., Young, G.P.H., and Goldstein, M. (1997) Reduction in
testicular temperature after varicocelectomy in infertile men. Urology
2:257–9.
Wyrobek, A.J., Schrader, S.M., Perreault, S.D., Fenster, L., Huszar, G.,
Katz, D.F., et al. (1997) Assessment of reproductive disorders and
birth defects in communities near hazardous chemical sites. III
Guidelines for field studies of male reproductive disorders. Reprod
Toxicol 11:243–59.