Environmental factors and semen quality.

IJOMEH 2009;22(4) 305
R E v I E w P a P E R s
International Journal of Occupational Medicine and Environmental Health 2009;22(4):305 – 329
DOI 10.2478/v10001-009-0036-1
ENVIRONMENTAL FACTORS AND SEMEN QUALITY
JOANNA JUREWICZ1, WOJCIECH HANKE1,2, MICHAŁ RADWAN3, and JENS PETER BONDE4
1 Nofer Institute of Occupational Medicine, Łódź, Poland
Department of Environmental Epidemiology
2 Medical University of Lodz, Łódź, Poland
Department of Informatics and Medical Statistics
3 Polish Mother’s Memorial Hospital — Research Institute, Łódź, Poland
Department of Operative and Endoscopic Gynecology
4 Bispebjerg Universty Hospital, Copenhagen, Denmark
Department of Occupational and Environmental Medicine
Abstract
Objectives: An increasing number of reports suggest that chemical and physical agents in the environment, introduced
and spread by human activity, may affect male fertility in humans. This article aims at evaluating the impact of environ-
mental exposures (pesticides, phthalates, PCBs, air pollution, trihalomethanes (THMs), mobile phones) on semen quality,
by reviewing most recent published literature. Materials and Methods: Epidemiological studies focusing on exposure to
environmental factors and semen quality for the last ten years were identified by a search of the Pubmed, Medline, Ebsco,
Agricola and Toxnet literature bases. Results: The results from the presented studies suggest that there are strong and
rather consistent indications that some pesticides besides DBCP (e.g. DDT/Dichlorodiphenyldichloroethylene [DDE], eth-
ylenedibromide, organophosphates) affects sperm count. PCBs are detrimental to sperm motility. In case of air pollution,
studies suggest a link between ambient air pollutants and various semen characteristics. Additional research is needed to
corroborate this association and to establish the causal agents. Results of few studies on subfertile men demonstrate associ-
ations between phthalate levels commonly experienced by the public and impaired sperm quality (impact on sperm concen-
tration, morphology, motility), but the findings have not been corroborated in studies of men from the general population.
Mobile phones might adversely affect the quality of semen by decreasing mostly motility but also the sperm counts, viability
and morphology. In spite of their consistent results, most of the studies are rather small. Association between exposure to
THMs and poor semen quality was not observed. Conclusions: Epidemiological studies suggest awareness of environ-
mental factors which may affect semen quality. In case both of well proven and disputable reproductive and developmental
hazards, it is necessary to prevent parental exposure to the agents associated with those hazards.
Key words:
Environmental factors, Semen quality, Environmental exposure
This study was performed under the project “Exposure to environmental hazards and the risk of male infertility — multicenter national study in Poland.” supported by
the Ministry of Science and Higher Education, Poland, from grant no. PBZ-MEiN-/8/2//2006; contract no. K140/P01/2007/1.2.1.2.
Received: September 4, 2009. Accepted: October 12, 2009.
Address reprint request to J. Jurewicz, Department of Environmental Epidemiology, Nofer Institute of Occupational Health, św. Teresy 8, 91-348, Łódź, Poland
(e-mail: joannaj@imp.lodz.pl).
INTRODUCTION
Male reproductive function in the general population has
attracted increasing attention due to reports indicating
increased occurrence of testicular cancer, cryptorchid-
ism and hypospadias across some time periods in some
populations past 50 years [1,2]. Reports indicating declin-
ing sperm counts in some regions [3,4] have also greatly
stimulated hypotheses that environmental pollutants may
impair male fertility [5].
The discovery in 1977 of the severe spermatotoxic effect of
the nematocide dibromochloropropane (DBCP) among
workers at a chemical plant [6] initiated several studies of
occupational and environmental risks to male reproduc-
tive function. Although for several decades semen qual-
ity has been used as a marker of male reproductive func-

R E v I E w P a P E R s J. JUREwICZ ET aL.
IJOMEH 2009;22(4)306
between a given environmental exposure and measures of
male reproductive function in terms of semen quality for
the last ten years. The period was chosen to reflect find-
ings over the past ten years during which new techniques
have emerged for measuring exposures and health effects
in reproductive and environmental epidemiology studies.
RESULTS
Air pollution
The major air pollutants in Europe and North America
are sulphur dioxide (SO2), nitrogen oxides (NOx), particu-
late matter (PM) and ozone (O3). Air pollutants can be
in the form of solid particles, liquid droplets, or gases. In
addition, they may be natural or man-made. Sources of air
pollution refer to the various locations, activities or factors
which are responsible for the releasing of pollutants into
the atmosphere.
Several studies addressing links between ambient air pol-
lution and semen quality have been published past few
years in the Czech Republic [13–15] and in USA, Los
Angeles [16] (Table 1). Two hundred seventy two young
Czech men exposed to high levels of air contaminants
in the Teplice region were more likely to have abnormal
sperm morphology and sperm chromatin structure than
were those who lived in a city (Prachatice) with less air
pollution. The authors observed a reduced percentage of
sperm with normal morphology and proportionately more
sperm with abnormal chromatin in men from Teplice re-
gion [13]. The other study conducted in the same region
of Czech Republic investigated whether the polluted air
in the Teplice district is related to abnormal morphology
in males living in this district [14]. More than 300 men
living in the Teplice district and in the control district of
Prachatice were examined between 1992 and 1994, in au-
tumn and at the end of winter. Significantly increased fre-
quency of sperm with abnormal morphology and reduced
motility was observed in men with medium and high expo-
sure to air pollution. More intensively exposed males also
had significantly higher frequency of disomy in chromo-
somes X, XY, and Y [14]. The same young men from Tep-
lice were sampled up to seven times over 2 years, allowing
tion in case of environmental exposure, the data are still
limited [7,8].
An obvious consequence of exposure to reproductive
toxicants is infertility. Infertility is defined as inability to
conceive after a year of sexual intercourse without the use
of contraceptives. A male contributory factor is involved
in approximately half of these cases [9], but most of the
causes of reduced semen quality and other disturbances of
male reproductive function are unknown [10].
Current studies, as reviewed by Sheiner et al. (2003) [11]
and Jensen et al. (2006) [12] show that variety of envi-
ronmental and occupational exposures may impair male
fertility. During past years male reproductive function has
been addressed in relation to a number of environmen-
tal exposures that have only to a very limited extent been
investigated or reviewed earlier. These exposures and
conditions include air pollution and drinking water pol-
lutants, biopersistent organochlorines, trihalomethanes,
phthalates and high frequency electromagnetic radiation
related to use of mobile phones. The objective of this pa-
per is to review the literature in order to update current
state of the art knowledge on hazards to male reproduc-
tive function.
MATERIALS AND METHODS
Epidemiological studies focused on the environmental
factors and male fertility were identified by a search of
the Pubmed, Medline, Ebsco, Agricola and Toxnet litera-
ture databases. Hand search was a second search method
used to explore the references of retrieved articles. The
combination of key words used were: semen quality, en-
vironmental exposure, air pollution, exposure to: phtha-
lates, persistent organochlorine pollutants, tap water,
mobile phones and pesticides. From each study, the fol-
lowing information was abstracted: study population, type
of outcome (sperm count, volume, concentration, sperm
density, semen motility, morphology, aneuploidy, level of
sexual hormones), type of exposure and methods used for
its assessment (including biomarkers). Finally in this re-
view were included human studies published in English in
peer reviewed journals with original information on links

ENvIRONMENTaL FaCTORs aND sEMEN QUaLITY R E v I E w P a P E R s
IJOMEH 2009;22(4) 307
Ta
bl
e
1.
S
em
en
q
ua
lit
y
an
d
ai
r p
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tio
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21
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(in
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32
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[1
5]
U
ni
te
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St
at
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al
ifo
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48
se
m
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do
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C
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A
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po
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ni
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fr
om
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co
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m
ot
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ph
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D
at
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irt
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se
as
on
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ge
a
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co
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be
tw
ee
n
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on
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le
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ls
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0
–9
, 1
0–
14

an
d
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–9
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b
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an
d
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sp
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c
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tio
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wa
s
ob
se
rv
ed
[1
6]

R E v I E w P a P E R s J. JUREwICZ ET aL.
IJOMEH 2009;22(4)308
(POCs), has been hypothesized. In animal studies, POCs
were found to have adverse effects on male reproductive
function. The studies on exposure to organochlorine com-
pounds and semen quality suggested association between
polychlorinated biphenyls (PCBs) exposure and poor
sperm quality. The findings of the pilot study carried out in
the Boston area population were also indicative of an as-
sociation between PCBs and p,p’-dichlorodiphenyldichloro-
ethylene (p,p’-DDE) and abnormal sperm count, motility
and morphology [19]. The total motile sperm counts were
inversely proportional to the PCB concentrations and
were significantly lower among infertile male than those
of the controls [20]. Also, in a study performed by Dallinga
et al. among 65 males with fertility problems, sperm count
and motility were inversely related to the sum of PCB con-
geners [21] (Table 2).
A strong and monotonically increasing DNA fragmentation
index with increasing serum levels of 2,2’,4,4’,5,5’-hexa-
chlorobiphenyl (CB-153) was found in a study performed
by Spanò et al. (2005) [22]. Sperm motility was also in-
versely related to the lipid adjusted serum concentration
of CB-153 among men in each of four regions (Greenland,
Sweden, Warsaw and Ukrania), which is consistent with
several earlier findings and results of animal studies [23]
(Table 2). Thus, there is fairly strong evidence to suggest
that persistent organic pollutants interfere with sperm
motility, although the causal agent cannot be identified
because of a strong correlation in serum concentration of
a wide number of biopersistent pollutants [24].
In a study of young fishermen from the coastal stretch-
es of Sweden prostate-specific antigen (PSA), neutral
α-glucosidase (NAG), fructose and zinc levels were anal-
ysed. There was a significant linear association between
CB-153 and total amount of PSA. With age, abstinence
time and smoking included in the model the associa-
tion became non-significant [25]. The same author per-
formed also study among 176 Swedish fishermen (with
low and high consumption of fatty fish). A significantly
lower % DNA fragmentation index (DFI) was found in
the lowest CB-153 quintile (<113 ng/g lipid) compared
with the other quintiles; there was a similar tendency, al-
though not statistically significant, between % DFI and
evaluation of semen quality after periods of exposure to
both low and high air pollution. Using repeated measures
analysis, a significant association was found between ex-
posure to periods of high air pollution (at or above the
upper limit of US air quality standards) and the percent-
age of sperm with DNA fragmentation according to sperm
chromatin structure assay (SCSA). Other semen measures
were not associated with air pollution [15]
The relationship between air pollutant levels and semen
quality was also evaluated over 2-year period in Los An-
geles, by analysing repeated semen samples collected by
sperm donors. Semen analysis data derived from 48 semen
samples provided by sperm donors were correlated with
air pollution level (ozone, nitrogen dioxide, carbon mon-
oxide, particulate matter). There was a significant negative
correlation between ozone levels at 0–9, 10–14 and 70–
90 days before donation and average sperm concentration,
which was adjusted for donor’s birth date, age at donation,
temperature and seasonality [16]. However, several occu-
pational studies of TIG (tungsten inert gas) welders with
exposure levels to ozone that are several orders of mag-
nitude higher have not revealed reduced sperm counts in
exposed men [18].
Summing up, while some studies suggest a link between
ambient air pollutants and various semen characteristics
like reduced percentage of sperm with normal morphol-
ogy and proportionately more sperm with abnormal chro-
matin and reduction of motility, additional research is
needed to corroborate this association and to establish the
causal agents.
Organochlorine contaminants, dioxins
and polychlorinated biphenyls
Organochlorines were widely used worldwide
from 1940 through 1970s, but most have been eliminated
or restricted in use after recognition of their persistence in
the environment, bioaccumulation in animals and humans
and toxicity in laboratory animals and wildlife.
Exposure mainly occurs through ingestion of contaminated
food, but can also occur through dermal contact and inha-
lation. A time-related deterioration in male reproductive
function caused by exposure to persistent organochlorines

ENvIRONMENTaL FaCTORs aND sEMEN QUaLITY R E v I E w P a P E R s
IJOMEH 2009;22(4) 309
to DBPs. Exposure to DBPs was evaluated by incorporat-
ing data on water consumption, bathing and showering
with concentrations measured in tap water. No consistent
pattern was found of increased abnormal semen quality
(sperm concentration and sperm count) with elevated ex-
posure to trihalomethanes or haloacetic acids [34]. In the
second study the relationship between THMs and semen
quality was examined in 157 healthy men from couples
without known risk factors for infertility. Total THM levels
were assigned based on water utility measurements taken
during the 90 days preceding semen collection. THM level
was not associated with decrements in semen quality. Only
for motility, a small decrease for every unit increase in
bromodichloromethane exposure level was found [35].
Based on presented results, there seems to be no associa-
tion between exposure to THMs and poor semen quality
(sperm concentration and sperm count). As the number of
studies is limited, further studies of the effect of THMs on
semen quality are needed.
Pesticides
Pesticides form a large group of heterogeneous chemicals,
which are used to kill insects, weed, fungi and rodents. On
the one hand these substances bring a significant public
health benefit by increasing productivity in the food indus-
try and decreasing the incidence of diseases.
Pesticides in general may directly damage spermato-
zoa, alter Steroli cell or Laydig cell function, or disrupt
the endocrine function in any stage of hormone regula-
tion (hormone synthesis, release, storage, transport and
clearance, receptor recognition and binding) [36]. Clear
effects on male fertility have been demonstrated for
some pesticides: dibromochloropropane [4], ethylene
dibromide [37], organophosphorus [38,39], alochlor, me-
tochlor, 2,4-D, atrazine [40], fenvalerate [41], carbaryl,
chlorpyrifos [42].
The results of the recent studies performed in Denmark,
China and Mexico indicated that exposure to pesticides
(however not confirmed by exposure measurements) in-
creased the risk of specific morphological abnormalities
of the sperm and decreased sperm count per ejaculate and
the percentage of viable sperm. No effects of pesticide
p,p’-DDE [26]. In the other cross-sectional study in Swe-
den, negative correlations between CB-153 levels and
both the testosterone and sperm motility were found [27]
(Table 2).
The results of the presented studies suggest that there is
an association between exposure and poor sperm qual-
ity, especially an inverse relationship was found between
sperm motility and the concentration of PCBs, while other
effects (sperm count and morphology) are rather uncer-
tain. Increasing DNA fragmentation index with increasing
serum levels of CB-153 was also found. On the other hand,
no effects of concentration of CB-153 and p,p’-DDE on
sperm concentration and prostate-specific antigen (PSA)
were observed.
Trihalomethanes in tap water
Trihalomethanes (THMs) are a byproduct of the water
treatment process. They are formed when natural organic
material reacts with chlorine used to treat the water. This
reaction produces “disinfection by-products” (DBPs) the
most common of which are trihalomethanes (THMs).
THMs such as chloroform, bromoform, chlorodibro-
momethane, bromodichloromethane, are the most preva-
lent and routinely measured class of DBPs found in the
water [27]. Routes of exposure to THMs include dermal
absorption during hand washing and bathing, inhalation
during showering and ingestion of drinking water [28].
Animal studies have consistently demonstrated an as-
sociation between oral exposure to DBPs including ha-
loacetic acids (HAAs) and trihalomethanes and adverse
effects in male reproductive system: acute spermatoxicity,
impaired reproductive competence, sperm quality [29],
delayed spermiation and distorted sperm motility and
morphology [30], histopathologic changes in testis and
epididymis [31], transient subfertility [32], altered sperm
production and epididymal tubule changes [33].
Contrary to large amount of evidences on the detrimental
effects of DBPs on male reproductive function in animals,
two so far completed human studies have not supported
these findings [34,35] (Table 3). In one cohort study per-
formed in United States the semen quality was evaluated
among 228 fertile men with different profiles of exposure