Abstract

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 environmental exposures (pesticides, phthalates, PCBs, air pollution, trihalomethanes (THMs), mobile phones) on semen quality, by reviewing most recent published literature. 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. 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], ethylenedibromide, 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 associations between phthalate levels commonly experienced by the public and impaired sperm quality (impact on sperm concentration, 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. Epidemiological studies suggest awareness of environmental 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.
IJOMEH 2009;22(4) 305
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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 JUREWICZ
1
, WOJCIECH HANKE
1,2
, MICHAŁ RADWAN
3
, and JENS PETER BONDE
4
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 identied 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 ndings 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-
REvIEw PaPERs 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 reect nd-
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 (SO
2
), nitrogen oxides (NOx), particu-
late matter (PM) and ozone (O
3
). 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. Signicantly 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 signicantly 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 dened 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-(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 identied 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
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IJOMEH 2009;22(4) 307
Table 1. Semen quality and air pollution
Study population Type of study Denition of exposure Semen analysis Confounders Results References
Czech Republic
215 young men
(18 years of age)
from Teplice region
(industrialized district)
and 193 from Prachatice
region (rural district)
Prospective
cohort
Air pollution data
were obtained from air
monitoring stations
Semen volume, sperm
concentration, total
number of sperm per
sample, percentage of
motile sperm, percentage
of sperm with normal
morphology and
percentage with normal
head morphology
Seasonality, age at
donation, smoking
Reduced percentage of sperm
with normal morphology and
proportionately more sperm with
abnormal chromatin in men from
Teplice region was observed
[13]
Czech Republic
325 males 18-year-old
living in the Teplice district
(industrialized district)
and in the control region
of Prachatice (rural
district)
Prospective
cohort
Air pollution data
were obtained from air
monitoring stations
Semen volume, pH,
motility, number
and morphology of
spermatozoa, aneuploidy
Seasonality, age at
donation, smoking
Signicantly increased frequency of
sperm with abnormal morphology
and reduced motility was observed in
men with medium and high exposure
for air pollution. More intensively
exposed males also had signicantly
higher frequency of disomy in
chromosomes X, XY, and Y
[14]
Czech Republic
36 young men (18 years of
age) from Teplice region
(industrialized district)
Prospective
cohort
Air pollution data
were obtained from air
monitoring stations
Sperm concentration,
sperm count, volume,
motility, sperm
morphology, aneuploidy
Seasonality, age at
donation, smoking
A signicant association was found
between exposure to periods of high
air pollution (at or above the upper
limit of US air quality standards) and
the percentage of sperm with DNA
fragmentation according to sperm
chromatin structure assay (SCSA).
Other semen measures were not
associated with air pollution.
[15]
United States, California
48 semen samples
collected from sperm
donors
Cross-sectional Air pollution levels (ozone,
nitrogen dioxide, carbon
monoxide and particulate
matter) were obtained
from air monitoring
stations
Semen volume, sperm
concentration, motility,
sperm morphology
Date of birth,
seasonality, age at
donation
A signicant negative correlation
between ozone levels at 0–9, 10–14
and 70–90 days before donation and
average sperm concentration was
observed
[16]
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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 ndings 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 signicantly 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 ndings 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 identied
because of a strong correlation in serum concentration of
a wide number of biopersistent pollutants [24].
In a study of young shermen from the coastal stretch-
es of Sweden prostate-specic antigen (PSA), neutral
α-glucosidase (NAG), fructose and zinc levels were anal-
ysed. There was a signicant 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-signicant [25]. The same author per-
formed also study among 176 Swedish shermen (with
low and high consumption of fatty sh). A signicantly
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 signicant, between % DFI and
evaluation of semen quality after periods of exposure to
both low and high air pollution. Using repeated measures
analysis, a signicant 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 signicant 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
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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 signicant public
health benet 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 conrmed by exposure measurements) in-
creased the risk of specic 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-specic 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 ndings [34,35] (Table 3). In one cohort study per-
formed in United States the semen quality was evaluated
among 228 fertile men with different proles of exposure
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IJOMEH 2009;22(4)310
Table 2. Exposure to organochlorine contaminants, dioxins, polychlorinated biphenyls and semen quality
Study population Type of study Denition of exposure Semen analysis Confounders Results References
United States
29 subjects from
Massachusetts General
Hospital Andrology
Laboratory including 18
subjects with normal
spermatozoa
Cross-sec-
tional
pilot study
Blood serum samples were analysed
for PCB, p,p-DDE and HCB
Sperm concentration,
sperm count, volume,
motility, sperm
morphology
Age, smoking,
abstinence time
An association between PCBs and
p,p’-DDE and abnormal sperm
count, motility and morphology was
detected
[19]
India
21 infertile men with
“unexplained male factor”
and 32 fertile controls
were examined
Cross-sec-
tional
PCBs were estimated in seminal
plasma
Total motile sperm count Age, smoking,
abstinence time,
diet
PCBs were detected in seminal
plasma of infertile men but absent
from controls. Sperm quantity and
quality were signicantly lower in
infertile men compared to controls.
The highest average PCB concen-
trations were found in sh-eating
urban dwellers, followed in succes-
sion by sh-eating rural dwellers,
non sh-eating urban dwellers and
non sh-eating rural dwellers. The
total motile sperm counts were
inversely proportional to the PCB
concentrations and were signicant-
ly lower than those of the respective
controls
[20]
Netherlands
A total of 65 male
counterparts of couples
visiting the Maastricht
University Hospital for
fertility treatment were
selected for this study. 31
men with normal sperm
quality and 34 with very
poor semen quality
Cross-sec-
tional
Blood samples were investigated with
regard to organochlorine compounds:
hexachlorobenzene (HCB),
p,p’-DDE:1,1-dichloro-2,2-bis
(p-chlorophenyl)ethylene p,p’-DDT:
1,1,1-trichloro-2,2-bis(p-chlorophenyl)
ethylene, 2,3’,4,4’,5-pentachlorobiphe-
nyl (PCB-118), 2,2’,4,4’,5,5’-hexachlo-
robiphenyl (PCB-153),
2,2’,3,4,4’,5-hexachlorobiphenyl
(PCB-138) and 2,2’,3,4,4’,5,5’-hepta-
chlo robiphenyl (PCB-180)
Sperm volume, sperm
concentration (sperm
count), overall and pro-
gressive motility and mor-
phology
Age, smoking,
abstinence time,
diet,
Focusing on the subgroup of men
with normal semen quality showed
that sperm count and sperm pro-
gressive motility were inversely re-
lated to the concentrations of PCB
metabolites within that group
[21]
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Greenland, Sweden, Poland,
Ukraine
707 adult males
(193 Inuits from
Greenland, 178 Swedish
shermen, 141 men from
Warsaw, Poland,
and 195 men from
Kharkiv, Ukraine)
Cross-sec-
tional
Serum levels of 2,2’,4,4’,5,5’-hexa-
chlorobiphenyl (CB-153), as a proxy
of the total PCB burden, and
of p,p’-DDE were determined
Sperm chromatin struc-
ture assay (SCSA) was
used to assess sperm
DNA/chromatin integrity
Lifestyle, diet,
abstinence
Increasing DNA fragmentation
index with increasing serum levels
of CB-153 among European but
not Inuit men, reaching a 60%
higher average level in the highest
exposure group. No signicant asso-
ciations were found between SCSA-
derived parameters and p,p’-DDE
serum concentrations
[22]
Greenland, Sweden, Poland,
Ukraine
763 men from all regions
in Greenland (n = 194),
shermen from Sweden
(n = 185), inhabitants
of the city of Kharkiv,
Ukraine (n = 195), and
inhabitants of the city of
Warsaw, Poland (n = 189)
Cross-sec-
tional
Serum concentrations
of 2,2′,4,4′,5,5′-hexachlorobiphenyl
(CB-153) and 1,1-dichloro-2,2-bis
(p-chlorophenyl)-ethylene
(p,p′-DDE) were examined
Sperm chromatin struc-
ture assay (SCSA) was
used to assess sperm
DNA/chromatin integrity
Lifestyle, diet,
abstinence
Sperm motility was inversely related
to CB-153 concentration in Green-
land and the Swedish shermen
population. Across all 4 regions,
the sperm motility decreased on
average by 3.6% (95% condence
interval = 1.7% to 5.6%) per one-
unit increase in the log of blood
CB-153 (ng/g lipid). The concentra-
tion of p,p′-DDE was negatively
associated with sperm motility in
the Greenlandic population and in
the compiled dataset
[23]
Sweden
157 shermen from
the coastal stretches of
Sweden, aged 27-67 years
Serum levels of CB-153 and
p’p-DDE were determined.
Prostate-specic an-
tigen (PSA), neutral
α-glucosidase (NAG),
fructose and zinc levels
Age, abstinence
time, smoking
There was a signicant linear as-
sociation between CB-153 and total
amount of PSA. With age, absti-
nence time and smoking included in
the model the association became
non-signicant
[25]
Sweden
176 Swedish shermen
(with low and high
consumption of fatty sh)
Serum levels of 2,2’,4,4’,5,5’-hexa-
chlorobiphenyl (CB-153) and
p,p’-DDE were examined
Sperm chromatin struc-
ture assay (SCSA) was
used to assess sperm
DNA/chromatin integrity
Lifestyle, diet,
abstinence
A signicantly lower %DFI was
found in the lowest CB-153 quin-
tile (< 113 ng/g lipid) compared
with the other quintiles; there was
a similar tendency, although not
statistically signicant, between
%DFI and p,p’-DDE
[26]
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IJOMEH 2009;22(4)312
Study population Type of study Denition of exposure Semen analysis Confounders Results References
Sweden
305 young Swedish
men 18-21 years old from
the general population
Serum levels of 2,2’,4,4’,5,5’-hexa-
chlorobiphenyl (CB-153)
Sperm concentration,
total sperm count, sperm
motility assessed manu-
ally and with a computer-
aided sperm analyser
(CASA), and serum levels
of follicle-stimulating hor-
mone, inhibin b, testos-
terone, sexual hormone-
binding globulin (SHBG),
luteinizing hormone, and
estradiol
Lifestyle, diet,
abstinence
Negative correlations between
CB-153 levels, testosterone
and sperm motility
[27]
Table 3. Exposure to trihalomethane (THM) and semen quality
Study population Type of study Denition of exposure Semen analysis Confounders Results References
United States
228 fertile men
Cohort study Water was sampled
at frequent intervals
(weekly or biweekly)
at a representative
location and analysed for
THM4, HAA9 and TOX
concentrations that were
indeed representative of
the entire system on that
day
Sperm concentration,
count, morphology, DNA
integrity, chromatin
maturity
Age, smoking,
alcohol drinking,
education level,
season, vitamin
intake, coffee
drinking, race
No consistent pattern was found of
increased abnormal semen quality (sperm
concentration and sperm count) with
elevated exposure to trihalomethanes
[34]
United States
157 healthy men from
couples without known
risk factor for infertility
Cross-sectional Total THM (TTHM) levels
were assigned based on
water utility measurements
taken during the 90 days
preceding semen collection
Sperm concentration,
sperm count, volume,
motility, sperm
morphology
Age, smoking,
alcohol drinking,
education level,
season, coffee
drinking
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]
Table 2. Exposure to organochlorine contaminants, dioxins, polychlorinated biphenyls and semen quality — cont.
ENvIRONMENTaL FaCTORs aND sEMEN QUaLITY REvIEw PaPERs
IJOMEH 2009;22(4) 313
methamidophos or endosulfan were conducted. In China,
male workers at a large pesticide-manufacturing plant had
an excess risk of aneuploidy and the risk of specic chro-
mosome abnormalities: disomy for chromosome 18 and
the three different types of sex chromosome disomy
(XX, XY, YY) [39]. In the Mexico study, aneuploidies
were found in 0.67% of total sperm nuclei. The authors
concluded that exposure to organophosphates could inter-
fere with sperm chromosome segregation and increase the
risk of Turner’s syndrome [38]. The next study performed
in Mexico showed the poorest semen quality among the
subjects with the highest OP exposure and the highest uri-
nary OP levels. Seasonal variations in sperm concentra-
tion and sperm count were registered. The results showed
a signicant decrease in total sperm count among subjects
with the highest exposure to OP [47] (Table 4).
The rst study which demonstrates links between specic
biomarkers of environmental exposure to pesticides and
biomarkers of male reproduction in humans was per-
formed in United States [40]. Men with high exposure lev-
el of alachlor (> 0.15 μg/g creatinine) had poorer semen
parameters (concentration, percentage sperm with normal
morphology, percentage motile sperm) than those less
exposed. The exposure to herbicide 2,4-D, metolachlor
and atrazine was associated with poorer sperm quality as
well [40]. The next study where the exposure to carbaryl
and chlorpyrifos was analysed by detecting the urinary
metabolites showed an associated between exposure and
lower sperm concentration and motility among men at-
tending an infertility clinic [42] (Table 4).
Yucra et al. [48] reported a signicant reduction of semen
volume and an increase in semen pH in men with organo-
phosphate metabolites in urine in the study performed in
Peru [48]. The poorest semen quality was found among
farmers with the highest OP exposure and the highest uri-
nary OP levels. The results showed a signicant decrease
in total sperm count among subjects with the highest ex-
posure to OP [48] (Table 4). In summary, there are several
indications that some pesticides may impair semen quality
in humans, but weak exposure assessment in most studies
precludes proper identication of responsible agents and
evaluation of exposure-response relations.
exposure on sexual hormones were observed [39,43,44]
(Table 4). However, this approach rarely provided any in-
dications of cause-effect relationship.
Among Danish greenhouse workers exposed to pesticides,
the median values of sperm concentration and proportion
of normal spermatozoa were lower by 60% and 14%, re-
spectively, in the high- and low-level exposure groups. The
median sperm concentration was lower by 40% for men
with over 10 years’ work experience in a greenhouse than for
those with experience below 5 years [43]. Also signicantly
lower sperm count was found in pesticide plant workers ex-
posed to fenvalerate compared with non-exposed controls
in the study performed in China [41] (Table 4).
Some studies assessed the levels of reproductive hormones.
Farmers exposed to pesticides in Argentina had higher se-
rum oestradiol concentrations and lower luteinizing hor-
mone (LH) concentrations than non-exposed men [45]. In
Japan, pesticide sprayers had the serum testosterone con-
centration in winter higher than the controls (p < 0.05),
though luteinizing hormone and follicle stimulating hor-
mone concentrations were not signicantly different. The
sperm counts and vitality were comparable between the
groups, but detailed sperm motility analysis in summer re-
vealed that the percentages of slow progressive and non-
progressive motile sperm were twice as high in the sprayers
(p < 0.05), and that of rapid progressive sperm tended to
be lower (p = 0.06). Such differences were not observed
in winter [46]. Semen quality and reproductive hormones
across a spraying season were examined among Danish
farmers (using and not using pesticides) and controls (non
farmers) that were asked to give two semen samples [44].
The median sperm concentration declined signicantly
from the rst to the second sample in both groups, but
there was no statistical difference in the decline between
the two groups. It was concluded that semen quality did
not change across a spraying season as a result of pesticide
exposure. Sprayers and non-sprayers had an equal decline
in sperm concentration from the rst to the second semen
sample [44] (Table 4).
In China and Mexico, studies of the prevalence of sperm
aneuploidy [38,39] in agricultural workers exposed to
organophosphorous pesticides like ethyl parathion,
REvIEw PaPERs J. JUREwICZ ET aL.
IJOMEH 2009;22(4)314
Table 4. Exposure to pesticides and semen quality
Study population Type of study Denition of exposure Semen analysis Confounders Results References
Hawaii
46 men employed in
the papaya fumigation
industry, exposed to
ethylene dibromide
43 non-exposed men from
sugar renery
Cross-sectional Based on job title ‘workers
working in production of
pesticides’.
No biomarker
Sperm count, concentra-
tion, viability, motility,
morphology
Lifestyle: smok-
ing, drinking
Exposure to pesticides signicantly de-
creased sperm count per ejaculate, the
percentage of viable and motile sperm.
Increase in the proportion of sperm with
specic morphological abnormalities (ta-
pered heads, absent heads and abnormal
tails) was observed among exposed men
compared with controls. No effect of expo-
sure to ethylene dibromide on sperm veloc-
ity, the overall proportion of sperm with
normal morphology was observed
[37]
Mexico
agricultural workers
exposed to pesticides
Cross-sectional Metabolites of organo-
phosphate pesticides in
urine were determined.
Sperm concentration,
aneuploidy
Lifestyle: smok-
ing, drinking
Exposure to organophosphate pesticides
was associated with sperm hyperploidy/
polyploidy. There was a signicant asso-
ciation between the concentration of or-
ganophosphate metabolites and increased
frequency of sperm aneuploidies
[38]
China
32 workers from pesticide-
manufacturing plant
43 workers from a nearby
textile factory free of
pesticides
Cross-sectional Based on job title ‘workers
manufacturing pesticides’.
No biomarker
Aneuploidy, motility,
sperm concentration, pro-
portion of sperm with nor-
mal morphology
Age, smoking,
alcohol drinking,
education level,
season, coffee
drinking
Exposure to organophosphate pesticides
(parathion, methamidophos) increased
the prevalence of sperm aneuploidy giving
the ratio of 1.56 (95% CI: 1.06–2.31). The
specic chromosome abnormalities were
disomy for chromosome 18 and the three
different types of sex chromosome disomy
(XX, XY, YY).
Median semen parameters for the exposed
(and non-exposed) men were as follows:
— proportion of sperm with normal motil-
ity — 50.5% (61.3%)
— proportion of sperm with normal mor-
phology — 59% (61.5%)
— sperm concentration was lower in the
exposed group compared with the non-
exposed one
[39]
ENvIRONMENTaL FaCTORs aND sEMEN QUaLITY REvIEw PaPERs
IJOMEH 2009;22(4) 315
United States
50 men in whom all
semen parameters
(concentration,
percentage sperm with
normal morphology, and
percentage motile sperm)
were low (cases)
and 36 men in whom all
semen parameters were
within normal limits
(controls) within Missouri
and Minnesota
Cross-sectional Metabolites of eight
current-use pesticides in
urine: alachlor, 2,4-D,
metalochlor, atrazine,
diazinon [2-isopropoxy-
4-methyl-pyrimidinol
(IMPY)], malathion,
acetochlor, DEET- (N,N-
diethyl-m-toluamide)
were determined
Cases: all semen param-
eters (concentration,
percentage sperm with
normal morphology, and
percentage motile sperm)
were low
controls: all semen param-
eters were within normal
limits
Education level,
season, coffee
drinking
Pesticide metabolite levels were
elevated in Missouri cases, compared
with controls, for the herbicides
alachlor and atrazine and for the
insecticide diazinon [2-isopropoxy-
4-methyl-pyrimidinol (IMPY)].
Men from Missouri with high
levels of alachlor or IMPY were
signicantly more likely to be
cases than were men with low
levels. The herbicides 2,4-D
(2,4-dichlorophenoxyacetic acid) and
metolachlor were also associated
with poor semen quality in some
analyses, whereas acetochlor
levels were lower in cases than in
controls (p = 0.04). No signicant
associations were seen for any
pesticides within Minnesota, where
levels of agricultural pesticides were
low, or for the insect repellant DEET
(N,N-diethyl-m-toluamide) or the
malathion metabolite (malathion
dicarboxylic acid)
[40]
China
32 male workers
who were exposed to
fenvalerate and 46 male
administrators in the ofce
in the same pesticide
factory
Cross-sectional The amount of fenvalerate
in individual sampling and
dermal contamination was
evaluated
Sperm concentration, mo-
tility, morphology, sperm
progression, beat cross
frequency
Age, education,
smoking
Sperm motion parameters through
routine semen analysis in the
exposure group were decreased
signicantly, and the abnormality
rate of viscidity and coagulation was
increased signicantly as compared
with the internal and the external
control groups. Furthermore, sperm
progression and beat cross frequency
(BCF) in the exposure group were also
signicantly lower than those in the
external control group
[41]
REvIEw PaPERs J. JUREwICZ ET aL.
IJOMEH 2009;22(4)316
Study population Type of study Denition of exposure Semen analysis Confounders Results References
United States
272 males were recruited
through Massachusetts
infertility clinic.
Urinary concentrations
of 1-naphthol (1N),
a metabolite of car-
baryl and naphthalene,
and 3,5,6-trichloro-2-
pyridinol (TCPY), a me-
tabolite of chlorpyrifos
and chlorpyrifos-methyl
were determined
Sperm concentration,
percent motile sperm, and
percent sperm with normal
morphology, along with
sperm motion parameters
Education, sea-
sonality
For increasing 1N tertiles, adjusted odds
ratios (ORs) were signicantly elevated
for below-reference sperm concentra-
tion (OR for low, medium, and high ter-
tiles = 1.0, 4.2, 4.2, respectively; p-value
for trend = 0.01) and percent motile sperm
(1.0, 2.5, 2.4; p-value for trend = 0.01). The
sperm motion parameter most strongly
associated with 1N was straight-line veloc-
ity. There were suggestive, borderline-sig-
nicant associations for TCPY with sperm
concentration and motility, whereas sperm
morphology was weakly and nonsignicant-
ly associated with both TCPY and 1N
[42]
Denmark
122 greenhouse workers
exposed to pesticide:
44 with low exposure
65 with medium exposure
13 with high exposure
Cross-sectional Based on job title ‘green-
house workers exposed to
pesticides’ with: low, me-
dium and high exposure
No biomarker
Sperm concentration,
proportion of normal sper-
matozoa, viability, velocity,
sexual hormones
Age, education,
smoking
The median values of sperm concentration
and the concentration and proportion of
normal spermatozoa were 60% and 14%
in the high- and low-level groups, respec-
tively. No differences were observed for the
viability and velocity of sperm and sexual
hormones. The median sperm concentra-
tion was 40% lower for the men with > 10
years’ period of work in a greenhouse than
for those with < 5 years’ period
[43]
Denmark
161 agricultural workers
exposed to pesticides
87 agricultural workers not
using pesticides
Cross-sectional Based on job title ‘agri-
cultural workers using
pesticides’
No biomarker
Sperm morphology, vi-
tality, motility, sperm
chromatin denaturation
(SCSA) and reproductive
hormones
Age, education,
smoking
The median sperm concentration declined
signicantly from the rst to the second
sample for the men spraying pesticides and
the men not spraying pesticides, but there
was no statistical difference in the decline
between the two groups. Only minor chang-
es were found in the sperm morphology,
vitality, motility, sperm chromatin denatur-
ation (SCSA) and reproductive hormones
[44]
Table 4. Exposure to pesticides and semen quality — cont.
ENvIRONMENTaL FaCTORs aND sEMEN QUaLITY REvIEw PaPERs
IJOMEH 2009;22(4) 317
Argentina
225 male partners from
consecutively recruited
couples, who had their
rst infertility consultation
between 1995 and 1998
Cross-sectional Based on job title
“farmers”
No biomarker
Sperm concentration,
sperm motility,
morphology, reproductive
hormones
Education,
seasonality
Men exposed to pesticides had higher
serum oestradiol concentrations, and
those exposed to solvents had lower LH
concentrations than non-exposed men
[45]
Japan
18 male pesticide sprayers
out of 54 working for 9
companies in central
Japan and 18 age-matched
students
Cross-sectional Based on job title
“pesticide sprayer”
No biomarker
Sperm concentration,
sperm motility,
morphology, reproductive
hormones
Age, smoking,
alcohol drinking,
education level
Serum testosterone concentration in
winter in the sprayers was higher than in
the controls (p < 0.05), though luteinizing
hormone and follicle stimulating hormone
concentrations were not signicantly
different. Sperm counts and vitality were
comparable between the groups, but
detailed sperm motility analysis in summer
revealed that the percentages of slow
progressive and nonprogressive motile
sperm were twice as high in the sprayers
(p < 0.05), and that of rapid progressive
sperm tended to be lower (p = 0.06). Such
differences were not observed in winter
[46]
Mexico
52 volunteers
Longitudinal
follow-up study
Urinary organophosphate
metabolities
Education level,
season
The results revealed that the poorest semen
quality was found among the subjects with
the highest OP exposure and the highest
urinary OP levels. Seasonal variations in
sperm concentration and sperm count were
registered. The results showed a signicant
decrease in total sperm count among
subjects with the highest exposure to OP
[47]
Peru
31 pesticide
applicators exposed to
organophosphate (OP)
pesticides and 31 non-
exposed were recruited
(age, 20–60 years)
Cross-sectional Urinary levels of OP me-
tabolites (dimethyl and
diethyl phosphates and
thiophosphates)
Sperm concentration,
percentage of sperm motil-
ity, percentage of normal
morphology, semen leuco-
cytes and concentrations of
fructose and zinc
Age, smoking,
alcohol drinking,
education level
Semen analysis revealed a signicant re-
duction of semen volume and an increase
in semen pH in men with OP metabolites.
Multiple regression analysis showed that
both occupational exposure to pesticides
and the time of exposure to pesticides were
more closely related to alterations in semen
quality parameters than the single mea-
surement of OP metabolites in urine
[48]
REvIEw PaPERs J. JUREwICZ ET aL.
IJOMEH 2009;22(4)318
Table 5. Exposure to phthalates and semen quality
Study population Type of study Denition of exposure Semen analysis Confounders Results References
United States
168 men who were part of
subfertile couples and who
presented to Massachusetts
General Hospital
andrology laboratory for
semen analysis between
January 2000 and
April 2001
Cross-sectional Eight phthalate
metabolites were
measured
Sperm concentration,
motility, morphology
Age, abstinence
time, and smoking
status
A dose-response relation between
tertiles of mono-butyl phthalate and
sperm motility and sperm concentration
was observed. In addition, there was
a dose-response relation between tertiles
of mono-benzyl phthalate and sperm
concentration
[53]
United States
295 male partners of
subfertile couples who
presented for semen
analysis to Massachusetts
General Hospital
between 1999 and 2003
Cross-sectional Selected phthalate
metabolites were
measured in urine
Sexual hormones Educational level,
age, abstinence
time, smoking
status
An interquartile range (IQR) change
in monobenzyl phthalate (MBzP)
exposure was signicantly associated with
a 10% decrease in FSH concentration.
Additionally, an IQR change in
monobutyl phthalate (MBP) exposure
was associated with a 4.8% increase
in inhibin B but this was of borderline
signicance
[54]
United States
463 males in subfertile
couples who presented
for semen analysis to
Massachusetts General
Hospital between
January 2000 and May 2004
Cross-sectional Eight phthalate
metabolites were
measured
Sperm concentration,
motility, morphology
Age, abstinence
time, smoking
status
There were dose-response relationships
of mono-butyl phthalate (MBP) with low
sperm concentration and motility. There
was suggestive evidence of an association
between the highest mono-benzyl
phthalate (MBzP) quartile and low sperm
concentration
[55]
Sweden
234 young Swedish men
Cross-sectional Urinary concentrations
of phthalate metabolites
were determined
Semen volume, sperm
concentration and motility
were measured, together
with sperm chromatin
integrity (sperm chromatin
structure assay) and
biochemical markers of
epididymal and prostatic
function, reproductive
hormones in serum
Education level,
age, abstinence
time, smoking
status
Subjects within the highest quartile for
monoethyl phthalate (MEP) had fewer
motile sperm, more immotile sperms, and
lower luteinizing hormone values, but
there was no suggestion of harmful effects
for most other endpoints
[56]
ENvIRONMENTaL FaCTORs aND sEMEN QUaLITY REvIEw PaPERs
IJOMEH 2009;22(4) 319
United States
Males (N = 45) of
subfertile couples
presenting to Michigan
infertility clinic
Cross-sectional
pilot study
Urinary concentrations
of phthalate metabolites
were measured
Motility, concentration,
morphology
Education level,
age, abstinence
time
Low sperm concentration was
signicantly associated with elevated
median concentrations of monoethyl
phthalate (MEP) and low morphology
with elevated median concentrations
of mono-3-carboxypropyl
phthalate. Increased odds for low
concentration and elevated median
concentrations of metabolites of
di(2-ethylhexyl) phthalate (DEHP)
(OR = 5.4, 95% CI: 0.9–30.8)
and low morphology and elevated
median concentrations of MEP
(OR = 3.4, 95% CI: 0.9–13.8) were
also found
[57]
India
The study was conducted
in the urban/rural
population of Lucknow
visiting Obstetrics and
Gynecology Department
Cross-sectional Urinary concentrations
of phthalate metabolites
were measured
Motility, concentration,
morphology
Age, abstinence
time, smoking
status
Infertile men showed statistically
signicant (p < 0.05) higher levels of
pollutants in the semen than fertile
men. A negative correlation between
semen phthalate level viz DEHP and
sperm quality and positive association
with depolarised mitochondria,
elevation in ROS production and
LPO, DNA fragmentation was
established
[58]
China
Participants residing in
Shanghai were surveyed
in 2002. Semen species
of 52 men (aged from 23
to 48 years) were collected
from outpatients of
Shanghai Institute of
Planned Parenthood
Research
Cross-sectional Concentrations of three
kinds of commonly used
phthalates (di-ethyl
phthalate, DEP; di-n-
butyl phthalate, DBP;
di-2-ethylhexyl phthalate,
DEHP
Sperm density, viability,
concentration
There was a signicant positive
association between liqueed time of
semen and phthalate concentrations
of semen. There was no signicant
difference between phthalate
concentrations of semen and sperm
density or viability
[59]
REvIEw PaPERs J. JUREwICZ ET aL.
IJOMEH 2009;22(4)320
level (DEHP) and sperm concentration, motility, % of
abnormal sperm was found in a population of men that
visited an infertility clinic [58].
Another study performed by Duty and co-workers [54]
to explore the association between environmental levels
of phthalates and altered reproductive hormone levels
in adult men showed that an interquartile range (IQR)
change in monobenzyl phthalate (MBzP) exposure was
signicantly associated with a 10% decrease in follicle-
stimulating hormone (FSH) concentration. Additionally,
an IQR change in monobutyl phthalate (MBP) exposure
was associated with a 4.8% increase in inhibin B, but this
was of borderline signicance [54].
On other hand, in a Swedish study, Jonsson et al.
(2005) [56] reported that only subjects within the highest
quartile for monoethyl phthalate (MEP) had fewer mo-
tile sperms, more immotile sperms, and lower luteinizing
hormone values, but there was no suggestion of harmful
effects for most other endpoints. In the study in China
there was no signicant difference between phthalate
concentrations of semen and sperm density and liveabil-
ity, while there was a signicant positive association be-
tween liqueed time of semen and phthalate concentra-
tions of semen [59].
Summing up, results of few studies of subfertile men dem-
onstrate associations between phthalate levels commonly
experienced by the public and impaired sperm quality
(impact on sperm concentration, morphology, motility),
but ndings have not been corroborated in studies of men
from the general population. Effects of phthalates in sexu-
ally mature rodents have only been seen at much higher
exposures levels but perhaps the human male is more sus-
ceptible to the class of chemicals. It remains to be investi-
gated if maternal exposures to phthalates have bearings as
to semen quality in the offspring.
Mobile phones
There has been a tremendous increase in the use of mo-
bile phones in the past decade and concerns are growing
about the possible detrimental effects of high-frequency
electromagnetic elds (EMF) emitted by these devices on
Phthalates
Phthalates are among the most widely used man-made
chemicals released to the environment over the last sev-
eral decades [49]. Phthalates are used as plasticizers to
increase the exibility of PCV products like: toys, vinyl
ooring and electricity cables or medical devices. The
main plasticizer used in PVC based medical devices is
di(2-ethylhexyl) phthalate (DEHP). Phthalates are also
used as solvents or xing agents in perfumes, body lotions
and other cosmetics. Humans are mainly exposed to these
compounds through the diet, medical devices and consum-
er products. In spite of short half times in the organism,
the compounds or their metabolites have been detected in
urine in more than 95% of men and women that have been
investigated [50].
There are numerous animal studies on the risk of infer-
tility related to phthalates exposure. Laboratory experi-
ments with rodents have shown repeatedly that phthalate
at very high doses (g/kg in gavage range) can adversely af-
fect sperm quality. Ge et al. (2007) [51] found that at lower
doses phthalates increase testosterone production either
by increasing Leyding cell numbers or by directly stimulat-
ing testosterone production [51]. However, inhibition of
testosterone was noticed in both foetal and adult Leyding
cells when rats were exposed to higher doses [51]. Other
studies in animals showed reduction of protein levels in
foetal Leyding cells and deregulation of cholesterol trans-
port and steroid synthesis [52].
Several recent epidemiological studies have addressed the
male reproductive toxicity of phthalates [53–59] (Table 5).
Duty et al. (2003) [53] compared levels of eight phthalate
metabolites in urine among men with normal and abnor-
mal semen quality recruited from 168 subfertile couples.
They observed an inverse dose-response relationship be-
tween 2 phthalate metabolites (monobutyl- and monoben-
zyl phthalate (MBP, MbzP)) on the one side and sperm
concentration and motility on the other. These ndings
were corroborated in a subsequent study of 463 infertile
men using same study design [55] and to some extent by
a smaller study including 45 infertility clients from the
Great Lakes Region in US [57]. Also in a study performed
in India, a negative correlation between semen phthalate
ENvIRONMENTaL FaCTORs aND sEMEN QUaLITY REvIEw PaPERs
IJOMEH 2009;22(4) 321
In the study performed in Poland, 304 males attending
an infertility clinic were divided into three groups: 99 pa-
tients who did not use mobile phones, 157 males who
had used GSM equipment sporadically for the period
of 1–2 years, 48 patients who had been regularly using mo-
bile phones for more than 2 years. In the analysis of the
effect of GSM equipment on the semen, an increase was
noted in the percentage of sperm cells of abnormal mor-
phology with the duration of exposure to GSM phone [66]
(Table 6).
The results of the presented studies provide limited sup-
port to the hypothesis that use of mobile phones may ad-
versely affect semen quality, but most of the presented
studies are small [60–63] only three [64–66] were conduct-
ed on the sample of about 300 men. So there is a need for
future studies in this area.
DISCUSSION
The results of the reviewed studies suggest that expo-
sure to environmental factors (air pollution, pesticides,
phthalates, PCB and the use of mobile phones) may af-
fect semen quality. However, when reviewing the epi-
demiological studies on the inuence of environmental
hazards on semen quality, it is important to take into ac-
count the current limitations of these studies resulting
from inadequacies in semen analysis, exposure evalua-
tion and design of studies. The studies conducted in the
general population are very rare mainly because of the
difculties in collecting the semen samples. The fact
that most of the studies are drawn from infertility clin-
ics may introduce a selection bias. Some of the subjects
are classied as fertile; they belong to a population of
men seeking medical care, which is probably different
from the general population in terms of other exposure
factors, because these men are more health-concerned
and therefore less exposed to other agents such as alco-
hol or drugs. In addition, subjects may underreport their
lifestyle habits, especially for smoking and drinking, thus
biasing the results. Another possible variable that needs
to be considered is the simultaneous presence of other
exposure factors. In reviewed studies authors collected
human health. Although many studies have recently been
published on this topic, the effects of the EMF emitted
by cell phones on living cells and organs are still unclear.
Here we review the few studies addressing possible effects
of cellular phone usage on human semen quality.
In a small prospective study involving 13 men with nor-
mal sperm, GSM phone usage in 5 days for 6 hours per
day decreased the rapid progressive motility of sperm [60]
(Table 6). Interesting results were obtained in a pilot study
performed in Australia; men who carried their mobile
phone in their hip pocket or on their belt had lower sperm
motility than men who did not carry a mobile phone or who
carried their mobile phone elsewhere on the body [61].
There are also two small studies where semen sample
was exposed to cellular phone radiation [62,63] (Table 6).
The rst study was performed in Turkey where statisti-
cally signicant changes were observed in the rapid pro-
gressive, slow progressive and no-motility categories of
sperm movement. Electromagnetic radiation (EMR) ex-Electromagnetic radiation (EMR) ex- (EMR) ex-
posure caused a subtle decrease in the rapid progressive
and slow progressive sperm movement. It also caused
an increase in the no-motility category of sperm move-
ment. There was no statistically signicant difference in
the sperm concentration between two groups [62]. The
second study was performed in United States where sam-
ples exposed to radiofrequency electromagnetic waves
(RF-EMW) showed a signicant decrease in sperm mo-
tility and viability, increase in reactive oxygen species
(ROS) level, and decrease in ROS-TAC (Total Antioxi-
dant Capacity) score. Levels of TAC and DNA damage
showed no signicant differences from the non-exposed
group [63].
A recent study involving 361 men attending an infer-
tility clinic suggested that use of cell phones for lon-
ger durations adversely affected the quality of semen
by decreasing the sperm counts, motility, viability and
morphology [64]. In Hungary a study was performed
among 371 male patients of infertility clinics. The dura-
tion of mobile phone use was correlated negatively with
the proportion of rapid progressive motile sperm, and
positively with the proportion of slow progressive motile
sperm [65] (Table 6).
REvIEw PaPERs J. JUREwICZ ET aL.
IJOMEH 2009;22(4)322
Table 6. Mobile phones and semen quality
Study population Type of study Denition of exposure Semen analysis Confounders Results References
United States
361 men undergoing
infertility evaluation
Cross-sectional Four groups according to their
active cell phone use:
group A: no use;
group B: < 2 h/day;
group C: 2–4 h/day;
group D: > 4 h/day
Sperm parameters
(volume, liquefaction
time, pH, viscosity,
sperm count,
motility, viability,
and morphology)
Controlling for
lifestyle factors,
education level
The comparisons of mean sperm
count, motility, viability, and normal
morphology among four different cell
phone user groups showed statistically
signicant differences. Mean sperm
motility, viability, and normal
morphology were signicantly different in
cell phone user groups within two sperm
count groups. The laboratory values
of the above four sperm parameters
decreased in all four cell phone user
groups as the duration of daily exposure
to cell phones increased
[64]
Hungary
371 males
from infertility clinic
Cross-sectional Group 1 was subdivided into
those who used a cell phone
for less than 15 min/day
(low transmitters) and those
who used it for over 60 min/day
(high transmitters).
Group 2 was subdivided into
those patients who kept their cell
phone in the standby position
within a distance of 50 cm for
less than 1 h daily (short-standby
group) and those who kept
their cell phone in the standby
position within a distance
of 50 cm for more than 20 h
daily (long-standby group)
Sperm concentration,
motility, morphology,
volume, count
Controlling for
lifestyle factors
The duration of possession and the daily
transmission time correlated negatively
with the proportion of rapid progressive
motile sperm and positively with the
proportion of slow progressive motile
sperm. The low and high transmitter
groups also differed in the proportion
of rapid progressive motile sperm. The
prolonged use of cell phones may have
adverse effects on the sperm motility
characteristics
[65]
Germany
13 men
with normal sperm
Prospective
study
GSM phone usage
5 days/week, 6 h/day
Sperm concentration,
motility, morphology,
volume, count
Controlling for
lifestyle factors
A reduction in the rapid progressive
motility of sperm
[60]
ENvIRONMENTaL FaCTORs aND sEMEN QUaLITY REvIEw PaPERs
IJOMEH 2009;22(4) 323
Australia
52 men between the
ages of 18 and 35 years
from the campus of the
University of Western
Australia
Percentage of motile
sperm and the number
of sperm per ml of
ejaculate
Controlling for
lifestyle factors
Interestingly, men who carried their
mobile phone in their hip pocket or on
their belt had lower sperm motility than
men who did not carry a mobile phone or
who carried their mobile phone elsewhere
on the body
[61]
Turkey
27 males
The semen sample obtained
from each participant was
divided equally into two parts.
One of the specimens was
exposed to EMR emitted by
an activated 900 MHz cellular
phone, whereas the other was
not
Sperm concentration,
motility, morphology,
volume, count
Controlling for
lifestyle factors
Statistically signicant changes were
observed in the rapid progressive, slow
progressive and no-motility categories of
sperm movement. EMR exposure caused
a subtle decrease in the rapid progressive
and slow progressive sperm movement. It
also caused an increase in the no-motility
category of sperm movement. There was
no statistically signicant difference in
sperm concentration between two groups.
[62]
United States
healthy donors (n = 23)
and infertile patients
(n = 9)
Prospective
pilot study
After liquefaction, neat semen
samples were divided into
two aliquots. One aliquot
(experimental) from each
patient was exposed
to cellular phone radiation
(in talk mode) for 1 h, and the
second aliquot (non-exposed)
served as the control
sample under identical
conditions
Evaluation of sperm
parameters (motility,
viability), reactive
oxygen species (ROS),
total antioxidant
capacity (TAC) of
semen, ROS-TAC
score, and sperm
DNA damage
Controlling for
lifestyle factors
Samples exposed to RF-EMW showed
a signicant decrease in sperm motility
and viability, increase in ROS level, and
decrease in ROS-TAC score. Levels
of TAC and DNA damage showed no
signicant differences from the non-
exposed group
[63]
Poland
304 males
Cross-sectional Group A: 99 patients who did
not use mobile phones, Group
B: 157 males who have used
GSM equipment sporadically
for the period of 1–2 years, and
Group C: 48 people who have
been regularly using mobile
phone for more than 2 years
Sperm concentration,
motility, morphology,
volume, count
Controlling for
lifestyle factors,
age, place of
residence
In the analysis of the effect of GSM
equipment on the semen it was noted that
an increase in the percentage of abnormal
morphology sperm cells was associated
with the duration of exposure to the waves
emitted by the GSM phone
[66]
REvIEw PaPERs J. JUREwICZ ET aL.
IJOMEH 2009;22(4)324
Exposure assessment
Exposure assessment is a crucial part of any area of envi-
ronmental epidemiology. The best assessment of exposure
usually provide measurements of contaminants in ambient
air samples, or in blood, urine, semen or other biological
specimens that might be appropriate.
Exposure in several of the presented studies was based on
specic biomarkers of exposure or the assessment of expo-
sure was performed. Phthalates were assessed in urine, air
pollution measurement was also taken. However, in the
studies on pesticide exposure and semen quality the expo-
sure was based in almost all studies on the job titles. Only
Swan et al. and Yucra et al. [40,48] used specic biomark-
ers of pesticide exposure [40,48]. It is well known that mis-
classication of exposure may occur if the type of exposure
is based solely on subject’s memory.
Biological assessment of exposure is the most precise indi-
cator, but sometimes it can be limited by the cost and the
large number of suspected chemicals that individuals were
exposed to, what usually is the case in relation to pesti-
cides exposure.
It is not only the type of exposure but also the timing in
relation to the development of the reproductive system
that is important for the assessment of type and magni-
tude of the harmful effect. The period between the 8th
and the 10th gestational week seems to be critical for
the development of male gonads [70]. It has been hy-
pothesised that even relatively insignificant exposures
acting at this period of prenatal life may have serious
consequences for the future reproductive capability
of men [5]. So the studies of environmental effects on
male reproduction should not only focus on exposures
during the reproductive life, but should also include
the foetal periods of male reproductive system devel-
opment.
Type of study design
With few exceptions, all studies comparing the distribu-
tions of seminal variables in an exposed populations with
those of an non-exposed reference population were cross-
sectional. The participation rate was about 40–60% and
there was tendency towards lower participation rates
information on age, alcohol and coffee drinking, tobacco
smoking, occupational exposure, and conducted a multi-
variate analysis.
Sometimes, like in case of trihalomethanes [34,35] or mo-
bile phones [63–66] there are just a few studies so it is dif-
cult to reach the conclusion. The next problem is also the
size of study population. In case of PCBs there are lots of
small pilot studies [19–21] but the bigger, well designed
studies [22,23,25–27] conrmed the ndings derived from
those studies.
It is a challenge for future studies to overcome the expe-
rienced limitations but also to focus more on mechanistic
aspects of reproductive toxicity.
Semen analysis
Presented studies usually have used classical human se-
men parameters (concentration, motility and morphol-
ogy), other markers have been used to get a more compre-
hensive evaluation of spermatogenesis and the function of
accessory sex organs (hormone levels, aneuploidy).
A signicant factor impeding the interpretation of stud-
ies concerning semen quality is great variation in the same
semen variables — in particular, ejaculate volume, sperm
density and motility. The uctuations across time within
a man are nearly as great as the variation between men
and can only partly be explained by the duration of the
period of abstinence [8]. The concentration and probably
also the sperm motility seem to be subject to seasonal
variation, the best quality in the northern hemisphere be-
ing registered during the winter and spring [67]. Seasonal
variation accounts only for a part of total variation which,
thus, remains largely unknown [8]. Experiments with rhe-
sus monkeys suggest that the seasonal changes in semen
quality may be driven by an inherent circannual biological
clock reset annually by seasonal changes in the length of
daylight [67].
Although there are some guidelines under WHO to intro-
duce standardization and quality control in sperm labora-
tory work [68], the assessment of semen quality even
within the same laboratory — may be subject to variation
between technicians and related to time [69].
ENvIRONMENTaL FaCTORs aND sEMEN QUaLITY REvIEw PaPERs
IJOMEH 2009;22(4) 325
(1995) [72] showed that p,p’-DDE had an antiandrogenic
activity.
Some pesticides are now suspected of being endocrine dis-
rupting chemicals (EDCs). These chemicals might cause
an adverse effect by interfering in some way with the
body’s hormones or chemical messengers. Many of these
endocrine disrupters have been linked to adverse effects
on either embryonic development or reproductive func-
tion in humans and wildlife [73–75].
Challenges for future studies
It is necessary to conduct longitudinal studies. These stud-
ies should take into account other factors which may in-
terfere with male reproductive health and include other
sperm characteristics. Future studies should have suf-
cient power and homogenous groups with an appropriate
non-exposed control group.
When the inuence of confounding factors is possible,
these should be taken into account during the stage of
study design and data collection and nally in the statisti-
cal analysis. Further evaluation of male reproductive tox-
icity of commonly used substances or those that are likely
to be in contact with human population is highly recom-
mended.
The longitudinal design option is a rational answer to
several of the main limitations in the cross sectional ap-
proach. Imprecision of measurement and variation be-
tween observers can be reduced by implementing good
laboratory practice and by computerised methods for ob-
jective assessment of sperm motility.
Also exposure assessment based on biomarkers of expo-
sure should be used. As little is known about the basic
mechanisms by which environmental exposures exert their
effect, current studies should focus more on the explana-
tion of the biological mechanism.
CONCLUSIONS
The results from the presented studies suggest that there
are strong and rather consistent indications that some
pesticides besides DBCP (as DDT/DDE, ethylenedibro-
mide, organophosphates) affect sperm count. PCBs are
among controls. So, the possibility that the men available
for the study may not truly reect the source population is
also the matter of concern.
The cross-sectional approach is most often associated with
considerable differential dropout and uncertainty about
the comparability of exposed and non-exposed groups.
It may be possible to overcome some of the major limi-
tations of studies by choosing a longitudinal design with
sampling before and during exposure and with a follow-up
of intraindividual changes.
Epidemiological models seem to have played increasing
role in the risk assessment of reproductive health effects
due to exposure to environmental factors. To be more
informative, epidemiological studies should focus on ex-
posure to single factors which were known from animal
studies that they might bring health consequences. The
factors which may inuence the sperm count and explain
part of the variability comprise the characteristics of the
men included in the study, the methodologies used to
analyse the semen or external factors inuencing sperm
production.
Mechanisms
Exposure to environmental toxicants that disrupt sperm
production or the function of reproductive hormones or
sperm may increase the risk of male infertility. On the oth-
er hand, chronic exposures to reproductive toxins are not
well documented and mechanisms of toxicity are either
poorly understood or unknown. Some evidences from ani-
mal studies suggest that some pesticides and PCBs belong
to the substances known as endocrine disrupters.
PCBs and DDT are well known chemicals with estrogen-
like characteristics and are referred to as estrogen disrupt-
ers. Animal studies suggest that these chemicals readily
penetrate the blood-testis barrier and can directly affect
spermatogenesis. It was also documented that PCB me-
tabolites bind to estrogen receptors. Jansen has hypoth-
esized that adverse reproductive effects of PCBs may re-
sult from PCB congeners increasing gonadotropin-releas-
ing hormone or affecting the production and release of
luteinizing hormone from the pituitary [71]. Kelce et al.
REvIEw PaPERs J. JUREwICZ ET aL.
IJOMEH 2009;22(4)326
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... Moreover, phthalates have been proven to impact, in a dose-dependent manner, sperm quality by affecting diverse parameters, such as concentration, morphology, and motility. Similarly, PCB resulted in being detrimental to sperm count and motility, exerting toxicity on reproductive processes on aquatic life, especially those of freshwater organisms [52][53][54][55]. Despite the high level of attention given to the toxic impact of BPA, only a few studies have evaluated its effect on human gamete quality [56]. ...
... A close relationship between air pollutants and sperm quality impairment has been reported in the last few decades [54,63]. In particular, airborne particulate matters resulted in being genotoxic to male germ cells, inducing DNA damage and alterations in sperm functionality and fertilization potential [64]. ...
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Reproductive health is progressively declining due to multiples endogenous and exogenous factors, such as environmental contaminants, diet and behavior. Accumulated evidences confirm that fertility and reproductive function have been adversely affected by exposure to chemical contaminants released in the environment. Today, the impact of diet and behavior on reproductive processes is also receiving special attention from the scientific community. Indeed, a close relationship between diet and fertility has been proven. Furthermore, a combination of unhealthy behavior, such as exposure to hazardous compounds and stress factors, poses living organisms at higher risk of reprotoxic effects. In particular, it has been described that poor life behaviors are associated with reduced male and female fertility due to decreased gamete quality and function. Most of the erroneous behaviors are, furthermore, a source of oxidative stress that, leading to epigenetic alterations, results in an impaired reproductive fitness. This review reports the detrimental impact of the most common environmental chemical stressors, diet, and behavior on reproductive functionality and success. Although clear evidences are still scarce, reassuring data are provided that a healthy diet and reverting unhealthy lifestyles may be of help to recover physiological reproductive conditions.
... Low levels of exposure may cause endocrine or reproductive disorders [20]. These are substances that may disrupt the functioning of the endocrine system and, consequently, affect the fertility of men and women [21][22][23][24][25][26]. Compared to studies evaluating the link between persistent endocrine-disrupting chemical exposure and endometriosis studies on the effects of exposure to nonpersistent chemicals are rare. ...
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Abstract: Endometriosis is a disease characterized by the presence of the uterine endometrium outside of its normal location. As the etiology of endometriosis is not well known and hormonal imbalance is central to disease pathogenesis, the potential contribution of exposure to endocrine�disrupting chemicals (EDCs) has been hypothesized in endometriosis. A systematic search of the literature was carried out to identify relevant studies using: PubMed, Scopus, Elsevier, Springer; EBSCO, and Web of Science. A total of 22 studies were considered. Most of the studies reviewed in this paper showed an association between exposure to BPA and phthalates and endometriosis. In the case of phthalate exposure, the reviewed studies found an association between the concentration of at least one phthalate metabolite and endometriosis. Only one study was performed to assess the exposure to parabens and a significant relationship with endometriosis was found. Additionally, only one study assessed the relationship of non-persistent pesticide exposure with endometriosis, observing a significant association between endometriosis and the urinary concentration of diazinon, chlorpyrifos, and chlorpyrifos-methyl. Studies struggled to provide a conclusion on the effect of exposure to benzophenones on endometriosis. Despite the numerous limitations of the results, the re�viewed studies suggest that exposure to non-persistent endocrine disruptors, especially bisphenol A and phthalates may affect endometriosis. The results of the studies on exposure to parabens, benzophenones, and non-persistent insecticides are inconclusive. Keywords: environmental exposure; non-persistent endocrine-disrupting chemicals; endometriosis; phthalates; bisphenol A; parabens; benzophenones
... . Polusi tanah dapat menyebabkan kerusakan jangka panjang atau jangka pendek dengan menurunnya pertumbuhan tanaman atau hewan, dapat mengganggu kesehatan lingkungan yang berdampak pada kesehatan manusia (Jurewicz et al. 2010;Havugimana et al. 2017). ...
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Soil pollution is a common environmental problem. It refers to the presence of exceeding concentration of chemicals or substances than the normal limit that harm living things and environment. Sources of soil pollution are mining activities, household waste, agricultural activities, and many more. Preventive or remediation activities are important to avoid the negative impacts on environment, especially on human health. Various scientific-based remediation methods can be applied such as increasing microbial activity (bioremediation) and the use of vegetation to remove contaminants (phytoremediation). These are more preferred methods for controlling soil pollutant because easier and economically applicable. Another preventive method is pesticides application. Activated charcoal can also be used to solve soil pollution caused by pesticide residues. Activated charcoal has high ability to absorb pesticide residue. Hopefully, this paper could provide information about soil pollution and its impact on human health as well as the preventive methods.
... A significant decline in human semen quality has been observed over the past 70 years, even in fertile men [2,3]. Exposures that have been associated with reduced semen quality include air pollutants, smoking, and heavy metals [4][5][6]. The World Health Organization (WHO) reports that 1.4 billion urban residents live in areas with air quality that does not meet WHO air quality guidelines [7]. ...
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Background Several studies have suggested adverse effects of particulate matter (PM) exposure on male reproductive health; few have investigated the association between PM exposure and semen quality in a large population of fertile men. Methods We evaluated 14 parameters of semen quality in 1554 fertile men in Nanjing from 2014 to 2016. Individual exposure to particular matter ≤10 μm in diameter (PM 10 ) and ≤ 2.5 μm in diameter (PM 2.5 ) during key periods of sperm development (0-90, 0-9, 10-14, 15-69, and 70-90 days before semen collection) were estimated by inverse distance weighting interpolation. Associations between PM exposure and semen quality were estimated using multivariable linear regression. Results Higher 90-days average PM 2.5 was in association with decreased sperm motility (2.21% for total motility, 1.93% for progressive motility per 10 μg/m ³ increase, P < 0.001) and four quantitative aspects of sperm motion (curvilinear velocity (VCL), straight line velocity (VSL), average path velocity (VAP), and amplitude of lateral head displacement (ALH), P < 0.01). The association between PM 2.5 exposure and semen quality were generally stronger for the earlier exposure window (70-90 days prior to ejaculation) than for recent exposure (0-9, 10-14, or 15-69 days). In the subgroup of men who had normal sperm parameters ( n = 1019), similar results were obtained. Ninety-days PM 10 exposure was associated only with decreased VCL and VAP and was not related to sperm concentration. Conclusions Exposure to PM 2.5 adversely affects semen quality, specifically lower sperm motility, in fertile men. Graphical abstract
... Cigarettes are made up of Nicotiana tabacum along with vaporized drugs and harmful substances, where cigarette smoke consists of carbon monoxide, tar, formaldehyde, nicotine, lead, cadmium, and many other substances [7,8]. Previous studies reported that cigarette smoking impact negatively on spermatogenesis process and functions of spermatozoa [9,10]. Additionally, several studies reported that the oxygen deficiency produced by cigarette smoking influences testicular function and impairs spermatogenesis, which ultimately leads to impaired sperm morphology, a decline in the progressive sperm, and increased sperm death [11][12][13]. ...
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Background Tobacco smoking is considered as one of the lifestyles factors that influence the sperm DNA methylation and global sperm DNA methylation and that may affect the sperm phenotype. This study was performed to investigate whether tobacco cigarette heavy smoking influences sperm DNA methylation patterns and semen parameters and to determine whether there is an alteration in the transcription level of MAPK8IP3 , GAA , ANXA2 , PRRC2A , and PDE11A genes in heavy smokers compared to non-smokers. Thirty samples were subjected to 450K arrays as a screening study to assess the variation in sperm DNA methylation levels between heavy smokers and non-smokers. Five CpG sites have the highest difference in methylation levels (cg07869343, cg05813498, cg09785377, cg06833981, and cg02745784), which are located in the MAPK8IP3 , GAA , ANXA2 , PRRC2A , and PDE11A genes, respectively, and were selected for further analysis using deep bisulfite sequencing in 280 independent samples (120 proven non-smokers and 160 heavy smokers) with a mean age of 33.8 ± 8.4 years. The global sperm DNA methylation, sperm DNA fragmentation, and chromatin non-condensation were evaluated also. Results A significant increase was found in the methylation level at seven, three, and seventeen CpGs within the GAA , ANXA2 , and MAPK8IP3 genes amplicon, respectively ( P < 0.01) in heavy smokers compared to non-smokers. Additionally, a significant increase was found in the methylation levels at all CpGs within PRRC2A and PDE11A gene amplicon ( P < 0.01). A significant increase was found in the level of sperm chromatin non-condensation, DNA fragmentation, and global DNA methylation ( P < 0.001) in heavy smokers compared to non-smokers. Conclusion These results indicate that tobacco cigarette smoking can alter the DNA methylation level at several CpGs, the status of global DNA methylation, and transcription level of the following genes “ MAPK8IP3 , GAA, ANXA2, PRRC2A , and PDE11A ” in human spermatozoa. These findings may affect negatively semen parameters and men’s fertility.
... There has been a growing concern about the decrease in sperm quality observed in recent decades and its possible association with environmental factors. Semen consists of spermatozoa, seminal fluid, and prostatic fluid, and any changes induced in these constituents can result in changes in the spermogram (Hauser, 2006;Jurewicz et al., 2009). All the phthalate effects in the spermogram described below are summarized in Table 2. ...
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Phthalate esters are synthetic chemicals used in the plastic industry as plasticizers and consumable products. According to United Nations, about 400 million tons of plastic are produced every year. In parallel with increased production, the concerns about its effects on human health have increased because phthalates are endocrine-disrupting compounds. Humans are continuously exposed to phthalates through different routes of exposure. Experimental data have associated the phthalates exposure to adverse effects on development and reproduction in women (e.g., earlier puberty, primary ovarian insufficiency, endometriosis, preterm birth, or in vitro fertilization) and men (e.g., anogenital distance, cryptorchidism, hypospadias, and changes in adult reproductive function) although there is no consensus. Therefore, one question arises: could the increase in infertility be related to phthalates exposure? To answer this question, we aimed to assess the disrupting-effects of phthalates on the human reproductive system. For this, we reviewed the current literature based on epidemiological and experimental data and experimental studies in humans. The phthalate effects were discussed in a separate mode for female and male reproductive systems. In summary, phthalates induce toxicity in the reproductive system and human development. The increased plastic production may be related to the increase in human infertility.
... In which additionally similar effect was in military population that heat exposure as an independent risk factor for male infertility [15]. Certain research works have also reported that psychological stress [33], Obesity [34] affects male infertility by influencing the hypothalamic-pituitarygonadal axis, thus causing detrimental effects upon spermatogenesis and subsequent fertility.On other hand several studies have been done on exposure to environmental toxicants that disrupt sperm production or the function of reproductive hormones or sperm may increase the risk of male infertility [16]. Recent studies illustrate that nutrition and lifestyle factors play a critical role in the normal function of the reproductive system [21,22]. ...
... Therefore, assessing the relationship between residential environment and semen quality would expand our understanding of the potential role of environmental factors in human reproductive health. Prior studies found that exposure to ubiquitous chemicals including endocrine disruptive chemicals and air pollutants is associated with reduced semen quality [14][15][16]. Given the association of physical environment with human fertility, male reproductive potential represented by semen quality may be associated with features of the built environment. ...
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This study explored the association between built environment and semen parameters among men who sought fertility evaluation. We used a data of 5,886 men living in the Seoul capital area whose semen was tested at a single fertility center during 2016–2018. Distance to fresh water, the coast, major roadways, and neighborhood greenness measured by Normalized Difference Vegetation Index (NDVI) were evaluated. Outcome indicators were semen volume, sperm concentration, percentage of progressive motility, vitality, normal morphology, and total motile sperm count. Linear regression models were fitted to standardized values of six semen indicators. Majority of men were white-collar, clerical, and service workers. Linear associations between built environment features and semen quality indicators were not evident except for NDVI within 500 m and sperm vitality (β = 0.05; 95% confidence interval (CI): 0.01, 0.09). The 2 nd quartile of distance to fresh water was associated with lower progressive motility compared to the 1 st quartile (β = −0.10; 95% CI: −0.17, −0.03). Proportion of vitality was higher among men in the 2 nd quartile of distance to roadways than those in the 1 st quartile (0.08; 95% CI: 0.01, 0.15). Men in the 2 nd quartile of NDVI had higher total motile sperm count (0.09; 95% CI: 0.01, 0.17). In the multi-exposure model, the positive association between NDVI and vitality remained (0.03; 95% CI: 0.00, 0.06). We observed potential evidence regarding the impact of built environment on male fertility, specifically a positive association between residential greenness and sperm vitality among men with a history of infertility.
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In vertebrates dysregulation of the antioxidant defense system has a detrimental impact on male fertility and reproductive physiology. However, in insects, especially mosquitoes the importance of sperm quality has been poorly studied. Since long-term storage of healthy and viable sperm earmarks male reproductive competency, we tested whether the heme peroxidase, a member of antioxidant enzyme family proteins, and abundantly expressed in the testis, also influence male fertility in the mosquito An. stephensi. Here, we show that a heme peroxidase 12 (HPX12), is an important cellular factor to protect the sperms from oxidative stress, and maintains semen quality in the male mosquito reproductive organ. We demonstrate that knockdown of the HPX12 not only impairs the sperm parameters such as motility, viability but also causes a significant down-regulation of MAG expressing transcripts such as ASTEI02706, ASTEI00744, ASTEI10266, likely encoding putative Accessory gland proteins. Mating with HPX12 knockdown male mosquitoes, resulted in ~ 50% reduction in egg-laying, coupled with diminished larval hatchability of a gravid female mosquito. Our data further outlines that increased ROS in the HPX12 mRNA depleted mosquitoes is the ultimate cause of sperm disabilities both qualitatively as well as quantitatively. Our data provide evidence that testis expressing AsHPX12 is crucial for maintaining optimal homeostasis for storing and protecting healthy sperms in the male mosquito’s reproductive organs. Since, high reproductive capacity directly influences the mosquito population, manipulating male mosquito reproductive physiology could be an attractive tool to combat vector-borne diseases.
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The association between polycyclic aromatic hydrocarbons (PAHs) and male reproductive dysfunction has attracted increasing attention. The purpose of this study was to compare the male reproductive toxicity of multiple PAHs and to investigate the underlying molecular mechanisms. TM4 cells (mouse testicular Sertoli cells, SCs) were treated with benzo(a)pyrene (BaP), pyrene (Py), fluoranthene (Fl) and phenanthrene (Phe) (0, 0.1, 1, 10, 50, or 100 μM) for varying time points (4, 12, 24, or 48 h), and male C57BL/6 mice were administered BaP and Py (0, 10, 50, or 100 mg/kg body weight) for 14 days based on the cell experimental results. Histopathological examination, western blotting, ELISA, biochemical assays, RT–PCR, flow cytometry, JC-1 staining and trans-epithelium electrical resistance (TEER) measurements were used to assess apoptosis, blood-testis barrier (BTB) integrity, intracellular calcium ([Ca²⁺]i) concentrations and oxidative stress (OS). The results revealed that the mRNA levels and enzymatic activities of CYP450 and GST family members; levels of ROS, MDA, cleaved caspase 3 (c-caspase 3), caspase 9, Bax, and cytochrome C (CytC); and numbers of TUNEL-positive cells were significantly increased by BaP and Py, while levels of AhR, GSH, SOD, CAT, Bcl-2 and ΔΨm were decreased. Additionally, BaP and Py notably interfered with tight junctions (TJs) and adherens junctions (AJs) in the BTB. Intriguingly, BaP, but not Py, induced [Ca²⁺]i overload and gap junction (GJ) destruction. There was no dramatic effect of Fl and/or Phe on any of the above parameters except that slight cytotoxicity was observed with higher doses of Fl. Collectively, these findings showed that BaP and Py elicited SC apoptosis and BTB disruption involving mitochondrial dysfunction and OS, but [Ca²⁺]i fluctuation and GJ injury were only observed with BaP-induced reproductive toxicity. The male reproductive toxicity of the selected PAHs was ranked in the order of BaP > Py > Fl > Phe.
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Malfunction of the male reproductive system might be a sensitive marker of environmental hazards, the effects of which may extend beyond reproductive function. The testis is more vulnerable to heat and ionising radiation than any other organ of the body and several xenobiotics are known to disrupt spermatogenesis after low level exposure. Studies of environmental impact on human health are often most informative and accurate when carried out in the workplace where exposures can be high and easy to document. Semen analysis provides readily obtainable information on testicular function. The main advantages in comparison with functional measures such as fertility rates and time taken to conceive are the possibilities to examine men independently of marriage and pregnancy, to find changes of fecundity with different exposures within the same person and to detect adverse effects when no alteration of fertility is yet taking place. In the implementation of an occupational sperm study considerable attention must be paid to logistic issues. A mobile laboratory unit for initial semen preparation and processing may in some situations increase worker compliance and the quality of sperm cell motility. The cross sectional design which has been used in almost all male reproductive studies so far has several severe limitations including selection bias because of differential participation, difficulties in defining a suitable reference group, and lack of information about the time dimension of the cause-effect relation. The longitudinal design deals adequately with most of these constraints. Semen samples are collected before, during, and possibly after exposure to the risk factor of interest and causal inferences are based upon change of semen variables within a man over time rather than upon differences between men. The logistics of the longitudinal study may benefit from pre-employment health examinations to enrol newly hired workers and require fewer participants to obtain comparable statistical power. In conclusion, andrological methods and epidemiological designs are available for the implementation of valid studies concerned with environmental impact on human testicular function. Occupational sperm studies should probably not be the first choice when the objective is initial screening of environmental impact on fertility but should be implemented when their is a need to corroborate or refuse earlier evidence that specific exposures have impact on testicular function.
Conference Paper
Infertility is a common problem, affecting perhaps one couple in six, the majority of whom now seek medical care. Although diagnostic problems make it difficult to establish the extent of the male partner's contribution with certainty, a number of studies suggest that male problems represent the commonest single defined cause of infertility, The World Health Organization has proposed a scheme for the diagnostic classification of male infertility, based upon a standardized approach to clinical assessment and to the assessment of semen quality. Some of these classifications are now controversial, and many are descriptive, rather than aetiological, Increasingly, the importance of occupation, environmental and particularly genetic factors in the causation of male infertility is being recognized.
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Dibromoacetic Acid Affects Reproductive Competence and Sperm Quality in the Male Rat. Linder, R. E., Klinefelter, G. R., Strader, L, F., Narotsky, M. G., Suarez, J. D., Roberts, N. L, and Perreault, S. D. (1995). Fundam. Appl. Toxicol. 28, 9-17.
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A time-related deterioration in male reproductive function caused by exposure to endocrine disrupters, including persistent organochlorines (POCs), has been hypothesized. In animal studies, POCs were found to have adverse effects on male reproductive function. However, little is known about the impact of POC exposure on reproductive parameters in men. In a study of 305 young Swedish men 18-21 years old from the general population, we correlated lipid-adjusted serum levels of 2,2',4,4',5,5'-hexachlorobiphenyl (CB-153)-an index substance for POC exposure-to markers of male reproductive function: testis size assessed by ultrasound, sperm concentration, total sperm count, sperm motility assessed manually and with a computer-aided sperm analyzer (CASA), and serum levels-of follicle-stimulating hormone, inhibin B, testosterone, sexual hormone-binding globulin (SHBG), luteinizing hormone, and estradiol. We found weak but statistically significant, negative correlations between CB-153 levels and both the testosterone:SHBG ratio (r = -0.25, P < 0.001)-a measure of the biologically active free testosterone fraction-and CASA sperm motility (r = -0.13, p = 0.02). No statistically significant association with other seminal, hormonal, or clinical markers of male reproductive function was found. In previous studies of more highly POC-exposed groups of adult men, the correlation between POC exposure, including CB-153, and free testosterone, levels was not statistically significant. The present study gives some tentative support for weak, negative effects of CB-153 exposure on sperm motility and free testosterone levels in young men, but further semen studies on more highly exposed groups may give more firm conclusions on the hazard for male reproductive function from dietary POC exposure.
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Research methods and knowledge in the field of male reproductive toxicology have gradually improved since reports in the late 1970s on severe impairment of spermatogenesis in workers with occupational exposure to certain chlorinated hydrocarbon pesticides (the nematocide 1,2-dibromochloropropan and the insecticide and fungicide chlordecone, but still we have only vague answers to basic questions about the overall significance of the environmental and occupational impact of these compounds on male reproductive capability.
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Trihalomethanes (THMs) are byproducts of drinking water chlorination whose effects on semen quality have not been previously studied in humans. We examined the relationship of THMs to semen quality in 157 healthy men from couples without known risk factors for infertility. Total THM (TTHM) levels were assigned based on water utility measurements taken during the 90 days preceding semen collection. We analyzed continuous semen parameters in relation to total and individual THMs, adjusting for potential confounders by using repeated measures analyses. TTHM level was not associated with decrements in semen quality. Percent normal morphology decreased and percent head defects increased at higher levels of an ingestion metric (TTHM multiplied by cold home tap water consumption). At the highest level of the ingestion metric (>160 mug/L x glasses/day, which is equivalent to >2 glasses/day of water containing 80 mug/L) we observed a difference of -7.1 (95% confidence interval = -12.7 to -1.6) for percent morphologically normal sperm compared with the lowest level (</= 40 mug/L x glasses/day). Of the individual THMs, bromodichloromethane exposure was inversely related to linearity (a motility parameter); we observed a small decrease (beta = -0.09, SE 0.04) for every unit increase in bromodichloromethane. Although our study had a limited exposure assessment and a selective sample, our results suggest the need for further study of the effects of THMs on semen quality.
Article
In a retrospective human biomonitoring study we analyzed 24h urine samples taken from the German Environmental Specimen Bank for Human Tissues (ESBHum), which were collected from 634 subjects (predominantly students, age range 20-29 years, 326 females, 308 males) in 9 years between 1988 and 2003 (each n >or= 60), for the concentrations of primary and/or secondary metabolites of di-n-butyl phthalate (DnBP), di-iso-butyl phthalate (DiBP), butylbenzyl phthalate (BBzP), di(2-ethylhexyl) phthalate (DEHP) and di-iso-nonyl phthalate (DiNP). Based on the urinary metabolite excretion we estimated daily intakes of the parent phthalates and investigated the chronological course of the phthalate exposure. In over 98% of the urine samples metabolites of all five phthalates were detectable indicating a ubiquitous exposure of the German population to all five phthalates throughout the last 20 years. The median daily intakes in the subsets between 1988 and 1993 were quite constant for DnBP (approx. 7 microg/kg bw/d) and DEHP (approx. 4 microg/kg bw/d). However, from 1996 the median levels of both phthalates decreased continuously until 2003 (DnBP 1.9 microg/kg bw/d; DEHP 2.4 microg/kg bw/d). By contrast, the daily intake values for DiBP were slightly increasing over the whole time frame investigated (median 1988: 1.1 microg/kg bw/d; median 2003: 1.4 microg/kg bw/d), approximating the levels for DnBP and DEHP. For BBzP we observed slightly decreasing values, even though the medians as of 1998 levelled off at around 0.2 microg/kg bw/d. Regarding daily DiNP exposure we found continuously increasing values, with the lowest median being 0.20 microg/kg bw/d for the subset of 1988 and the highest median for 2003 being twice as high. The trends observed in phthalate exposure may be associated with a change in production and usage pattern. Female subjects exhibited significantly higher daily intakes for the dibutyl phthalates (DnBP p=0.013; DiBP p=0.004). Compared to data from US National Health and Nutrition Examination Surveys (NHANES) exposure levels of the dibutyl phthalates were generally higher in our German study population, while levels of BBzP were somewhat lower. Overall, for a considerable 14% of the subjects we observed daily DnBP intakes above the tolerable daily intake (TDI) value deduced by the European Food Safety Authority (EFSA) (10 microg/kg bw/d). However, the frequency of exceedance decreased during the years and was beneath 2% in the 2003 subset. Even though transgressions of the exposure limit values of the EFSA and the US Environmental Protection Agency (US EPA) occurred only in a relatively small share of the subjects, one has to take into account the cumulative exposure to all phthalates investigated and possible dose-additive endocrine effects of these phthalates.
Phthalates are used in commercial products as softners of plastics, solvents in perfumes and additives to hair sprays, lubricants and insect repellents. The wide spread use of phthalate results in multiple human exposure routes i.e., ingestion, inhalation and dermal exposure. In the present review, a detailed account of respiratory toxicity, reproductive toxicity, developmental toxicity, endocrine disruptors and genotoxicity of human exposure to phthalate is mentioned in detail.
Article
A number of studies indicated a clear decline in semen quality in the past 30-50 years and there is accumulating evidence that this decline might result from exposure to high levels of air pollution. To examine the impact of environment on male reproductive ability, we undertook for the first time a pilot study on semen quality of infertile men exposed to purification of indoor air. Ten subjects with a history of unexplained male infertility and poor semen quality were exposed for at least 1 year to a cleaning indoor air system (Koala technology). The key feature of this air purifier is the unique innovative multiple filtering system. The treatment of total purification of indoor air showed neither improvements in semen parameters nor variation in reproductive hormones (P = N.S.), but induced an evident increase (P < 0.03 and more) in seminal leucocytic concentrations. Within the limits due to the small sample of subjects recruited, the sole purification of indoor air does not seem enough to improve semen quality, although the increase in leucocytic concentrations could indicate an activation of the role of immunosurveillance in a purified indoor air environment.
Article
To evaluate effects of cellular phone radiofrequency electromagnetic waves (RF-EMW) during talk mode on unprocessed (neat) ejaculated human semen. Prospective pilot study. Center for reproductive medicine laboratory in tertiary hospital setting. Neat semen samples from normal healthy donors (n = 23) and infertile patients (n = 9). After liquefaction, neat semen samples were divided into two aliquots. One aliquot (experimental) from each patient was exposed to cellular phone radiation (in talk mode) for 1 h, and the second aliquot (unexposed) served as the control sample under identical conditions. Evaluation of sperm parameters (motility, viability), reactive oxygen species (ROS), total antioxidant capacity (TAC) of semen, ROS-TAC score, and sperm DNA damage. Samples exposed to RF-EMW showed a significant decrease in sperm motility and viability, increase in ROS level, and decrease in ROS-TAC score. Levels of TAC and DNA damage showed no significant differences from the unexposed group. Radiofrequency electromagnetic waves emitted from cell phones may lead to oxidative stress in human semen. We speculate that keeping the cell phone in a trouser pocket in talk mode may negatively affect spermatozoa and impair male fertility.