Skip to main content
Environmental Sciences Europe
Download PDF

Impact of environmental factors on human semen quality and male fertility: a narrative review

Environmental Sciences Europe volume 34, Article number: 6 (2022) Cite this article

Abstract

Background

Worldwide rising trend in infertility has been observed in the past few years with male infertility arising as a major problem. One main reason for the rise in male infertility cases is declining semen quality. It was found that any factor that affects semen quality can affect male fertility. There are several modifiable factors affecting semen quality including air pollution, use of pesticides and harmful chemicals, exposure to excessive heat, and can lead to decreased male fertility.

Main body

The present review focuses on some of these environmental factors that affect semen quality and hence, can cause male infertility. The literature from 2000 till June 2021 was searched from various English peer-reviewed journals and WHO fact sheets using the USA National Library of Medicine (PubMed) database, the regional portal of Virtual Health Library, and Scientific Electronic Library Online. The search terms used were: “Air pollution and male fertility”, “Chemicals and male infertility”, “Heat exposure and infertility”, “heavy metals and male fertility”.

Conclusion

Adverse environmental factors have a significant impact on semen quality, leading to decreased sperm concentration, total sperm count, motility, viability, and increased abnormal sperm morphology, sperm DNA fragmentation, ultimately causing male infertility. However, all these factors are modifiable and reversible, and hence, by mere changing of lifestyle, many of these risk factors can be avoided.

Background

Worldwide infertility affects around 8–12% of couples, with male-factors identified as the primary cause in 50% of cases [1]. Furthermore, around 7% of all men are affected by male infertility all over the world [2]. Many factors predispose to male infertility including congenital malformations, hormonal, genetic, behavioral, iatrogenic, environmental, and lifestyle factors [3]. Environmental pollution has emerged as a major cause for the rising trend of male infertility in today’s era all over the world due to the universal presence of environmental contaminants. Recent studies have revealed that air pollution has a significant impact on human fertility and sperm quality [4, 5].

Semen quality is the major predictor of male fertility outcome [6]. It was observed that environmental pollution unfavorably affects semen quality by impairing the process of spermatogenesis, steroidogenesis, Sertoli cell, and sperm functions, thereby leading to decreased male fertility [7, 8]. Furthermore, there are numerous natural and man-made chemicals that are released into the environment daily and have deleterious impacts on human fertility. Despite, the adverse impacts of environmental chemicals such as industrial waste, pesticides, insecticides, herbicides, food additives, etc. on spermatogenesis in adult men, there is very scarce data available on the direct impact of these chemicals in humans. The available studies are usually in an occupational setting, where the population is exposed to these substances at very high concentrations and not for the general population [9, 10].

The present review briefs the impact of various environmental factors that affect male fertility including air pollution, working environment, increased risk of exposure to chemicals, radiation, and heat. All these factors are modifiable and can hence, provide opportunities for the treatment of male infertility. Figure 1 Summarizes the effects of environmental factors on semen quality. Some of these environmental factors and their impact on semen quality, sperm, and overall male fertility are discussed in detail as under:

Fig. 1
figure 1

Impact of environmental and lifestyle factors on semen quality and male fertility

Full size image

Environmental factors

Air pollution

Nowadays alarming rise in air pollution in many cities of the world has affected human health to a large extent and has also led to a rise in the number of diseases including respiratory [11], cardiovascular [12], skin-related [13], cancers [14] and reproductive diseases [15,16,17]. Furthermore, India is the second most populated country and the third most air polluted country all over the world [18].

The main sources of air pollution include motor vehicle exhaust, factories, fire, household, agriculture, waste treatment, oil refineries, natural sources, such as volcanic eruptions, wind, etc. The major air pollutants affecting human health are particulate matter, volatile organic compounds, ozone, nitrogen oxides, sulfur dioxide, carbon monoxide, polycyclic aromatic hydrocarbons (PAH), and radiations, such as X-ray exposure [15, 19]. The particulate matter present in the air in form of tiny liquid or solid droplets can be inhaled and can result in serious health effects [20] Furthermore, particles < 10 μm in diameter (PM10) are very harmful and after inhalation are known to invade the lungs and can even reach the bloodstream causing numerous deleterious impacts. Finer particles, such as PM2.5, are even more dangerous and pose a greater risk to health [21].

Numerous recent researches have shown the adverse effect of air pollution on reproductive outcomes in both males and females. It seriously affects the semen quality in males. It was observed that air pollution causes increased sperm Deoxyribonucleic acid (DNA) fragmentation, sperm morphological changes, and reduced sperm motility [22]. A systematic meta-analysis reported that the level of air pollution was significantly associated with decreased semen volume, sperm concentration, progressive and total sperm motility, and normal sperm morphology rate. It also results in increased sperm DNA fragmentation index, further leading to decreased fertility in males [23]. A recent study evaluated the association between various gaseous pollutants and semen quality and reported that Sulfur dioxide (SO2) exposure has significant negative impacts on sperm parameters during all exposure windows. They also observed that both SO2 and nitrogen dioxide (NO2) had significant adverse impacts on sperm concentration and motility which was found to be more aggressive in the initial phase of spermatogenesis. Hence, concluding that gaseous pollutants have a significant adverse impact on semen quality especially during the sperm development period [24]. Findings of original research reported that in motorway tollgate workers the total sperm motility, forward progression, and sperm kinetics were significantly lesser as compared to other men living in that area. It was found that the nitrogen oxide and lead released from automobile exhaust severely affected the overall semen quality in these men as compared to their controls [25]. A study reported that tollgate workers who are exposed to large amounts of automobile exhaust had an increased quantity of damaged sperm chromatin and fragmented DNA as compared to their unexposed healthy men, and hence, concluded that car exhaust exposure can lead to a significant genotoxic effect on human spermatozoa [26].

One major air pollutant is ozone. Ozone can result in decreased percentages of sperm with normal sperm morphology and hence, can explain the rising trend of males reporting to infertility clinics with abnormal sperm morphology [27]. Recent studies have proposed the role of particulate matter 2.5 (PM2.5), a fine particulate matter that is the main component of haze and an important indicator of air pollution in causing male infertility [28, 29]. It was observed that exposure to PM2.5 results in an increased number of sperm cells with cytoplasmic drop and morphological abnormalities in sperm heads [30]. Other similar studies have also found a significant inverse relationship between PM2.5 and sperm motility, sperm concentration, total sperm count, sperm head morphology, and overall semen quality [31, 32].

The exact mechanism by which air pollutants result in male infertility is not clear, but it can be explained to some extent by the facts that air pollution leads to: a). Hormonal disruption: The heavy metals such as lead, zinc, copper, and PAH present in the exhaust of automobiles have estrogenic, antiestrogenic, and antiandrogenic actions, which in turn can result in abnormal gonadal steroidogenesis and gametogenesis, thereby leading to infertility [33, 34]. Another recently studied particulate matter PM2.5 gets accumulated in the reproductive organs through blood-testis, epithelial, or placental barrier and can disrupt hormone levels, leading to infertility [28]; b). Increased production of reactive oxygen species due to oxidative stress, leading to lipid peroxidation, sperm DNA fragmentation, and infertility [33, 35]; c). Sperm DNA alteration due to the formation of DNA adducts especially with PAH results in changes in gene expression and DNA methylation causing male infertility [33, 36]. Hence, air pollution is one major factor in today’s era resulting in defective spermatogenesis, increased sperm DNA fragmentation, reduced motility, and abnormal morphological changes, leading to a rise in male infertility.

Exposure to harmful chemicals

Human beings all over the world are exposed to a wide variety of chemicals in their day-to-day life. Many of these chemicals have serious ill effects on the functioning of the human body, especially reproductive organs. Recent studies have shown that male reproductive organs are one of the major sites for insults resulting from exposure to environmental chemicals leading to male infertility [37]. A recent large cross-sectional study on maternal occupational exposure to potential endocrine-disrupting chemicals during pregnancy, especially to pesticides, phthalates, and heavy metals on the semen quality of their sons in adulthood reported a significant correlation between maternal occupational exposure with low semen volume and total sperm count in their sons. Furthermore, a significant association was found between maternal heavy metal exposure and low sperm concentration. Hence, they concluded that there is need to inform pregnant women about the potential hazards of chemicals during pregnancy that can impair their child's fertility, though further studies are needed to confirm the impact of endocrine disrupting chemicals on fertility [38]. Some of the chemicals that significantly affects male fertility are summarized as under:

Dioxins

Dioxins are a group of highly persistent lipophilic chemicals produced as a by-product to several industrial and natural processes including smelting, chlorine bleaching of paper and pulp, in production of some pesticides, biomedical and plastic waste incineration [39,40,41]. Chemically it is 2,3,7,8- tetrachlorodibenzo para dioxin (TCDD) and is considered a “dirty dozen” that is a cluster of hazardous chemicals also known as persistent organic pollutants (POPs) as they resist biological and environmental degradation. They are of concern because of their highly toxic nature and ability to get absorbed by fat tissue and stored in the body for long periods (7–11 years) [36]. They are known to cause serious reproductive, developmental, and cancer problems [42]. Dioxins act as endocrine disruptors and mediate their effects by binding to the aryl hydrocarbon receptor (AHR)/aryl hydrocarbon receptor nuclear translocator (ARNT) receptor complex present over human testicular cells to mediate their toxic effects [43]. The exact mechanism by which it affects the reproductive functions in humans is not clear. A recent study in male Zebrafish proposed DNA methylation as a possible mechanism of reproductive effects of dioxins [44]. Since DNA methylation pattern in zebrafish is carried down paternally through the sperm [45], inheritance of epimutations in the DNA methylome is a promising mechanism of transgenerational male-mediated reproductive defects resulting from TCDD exposure. Furthermore, early disruption of DNA methylation during gonad development can result in reproductive and epigenetic gene changes leading to impaired reproductive functions [46]. A study on 135 human males exposed to dioxin at three age groups (prepuberty, puberty, and adulthood), and 184 healthy males as control reported that exposure to dioxin in prepubertal males was significantly associated with reduced sperm concentration and motility [47]. Only available human study on dioxin exposure during the developmental stage reported that male babies fed on breast milk of women exposed to high concentrations of dioxins at the time of conception had significantly decreased sperm concentration, total sperm count, and total sperm motility [48]. Another retrospective study also reported that the dioxin and furan content was 2.2–2.3 times higher in the ejaculate of infertile males as compared to the fertile ones [49]. A recent study in male mice reported a significant fall in sperm motility and count, in mice exposed to dioxin. Furthermore, on testicular histopathology, they observed necrotic degeneration and reduced epithelium thickness in mice exposed to dioxin as compared to the controls [50]. Furthermore, supporting the fact that dioxin exposure seriously affects the sperm functions in males resulting in poor quality semen and hence, male infertility.

Plastic contaminants (Bisphenols): Plastic use has become indispensable in our daily lives, but being non-biodegradable, it has now become a major cause of concern all over the world. Bisphenol A (BPA) a major component of plastic is released into the environment during the process of production, use, or disposal of plastics and from break-down of industrial plastic-related wastes [51]. In a recent study in the United States, adults and children reported that Bisphenols substitutes such as Bisphenol F, bisphenol S, and bisphenol A are almost universal [52]. It is nowadays considered hazardous to human health, because of its universal presence, prolonged persistence in the environment, and as an endocrine disruptor. It has been linked to numerous health problems including cardiovascular diseases, metabolic disorders, infertility, and cancers [53,54,55]. It was found that BPA has estrogenic, antiandrogenic, and antithyroid activities and hence, can disrupt the hypothalamic–pituitary–gonadal axis, resulting in altered reproductive system functions [54]. Increased exposure to BPA results in sperm DNA damage, mitochondrial dysfunction, and degeneration, decreased sperm motility, sperm count, and increased risk of aneuploidies in sperm [54, 56]. Numerous studies on rodents have shown that BPA exposure in male rodents results in a significant decrease in sperm motility, count, normal sperm morphology, increased sperm DNA damage, and adversely affects the spermatogenesis process resulting in male infertility [53, 57,58,59]. Another recent study reported that excessive exposure to BPA results in impaired sperm motility by reducing the sperm Adenosine Triphosphate (ATP) levels and premature acrosome reaction resulting in poor fertilization and embryonic developmental problems [60]. Other studies have also found a close association between increased BPA exposure and poor semen quality and parameters including sperm quality and motility [61,62,63]. The exact mechanism by which BPA affects human sperm quality is still under research but it was found that BPA is an endocrine disruptor that results in inhibition of anti-apoptotic pathways such as Bcl-2 and causes activation of pro-apoptotic signaling pathways including mitogen-activated protein kinase (MAPK), Fas/FasL, Caspase 3 and 9, Bax leading to diminished proliferation, increased reactive oxygen species-mediated damage and enhanced apoptosis of male gametes [64]. It acts as an Androgen receptor (AR) antagonist resulting in reduced AR translocation and increases AR transcriptional corepressors thereby resulting in suppression of Sertoli cell proliferation [65]. A study in mice reported that BPA inhibits testosterone synthesis in male pups [66]. This decreased testosterone levels in plasma results in reduced expressions of steroidogenic enzymes, cholesterol carrier protein in Leydig cells, and plasma Luteinizing hormone (LH) levels. BPA also results in decreased Leydig cell numbers in the testis [67]. All leading to male reproductive dysfunction. Hence, prolonged exposure to BPA in excessive concentrations can affect male fertility.

Pesticides and herbicides

Pesticides especially dibromochloropropane, ethylene dibromide which has been extensively studied is known to cause direct spermatozoa damage, Sertoli or Leydig cell function alteration, disordered endocrine function during hormonal regulation of processes, such as synthesis, release, storage, transport, and clearance of hormones; binding of hormones to their receptors, thyroid function, etc. leading to male infertility [68]. Organochlorine pesticides which are widely used, including DDT and its metabolites, act as endocrine-disrupting chemicals [69]. The main metabolite of DDT, p,p′-Dichlorodiphenyl-dichloroethylene (p,p′-DDE), is an anti-androgenic and binds to androgen receptors and hence, inhibits the action of testosterone [70]. Furthermore, it was observed that p,p′-DDE may have an additive or multiplicative effect with other endocrine-disrupting environmental pollutants leading to adverse impacts on reproductive functions [69]. Pesticide exposure can result in defective spermatogenesis leading to reduced sperm concentration, sperm motility, an increased number of morphologically abnormal sperms, causing poor semen quality and reduced male fertility [71]. A recent study on the in-vitro impact of Herbicide Roundup on human sperm motility and sperm mitochondria reported that the direct exposure of semen samples to the active component of this herbicide even at a very low concentration of 1 mg/L can result in adverse effects on sperm motility and in sperm mitochondrial dysfunction [72]. At low doses, Roundup herbicide also induces oxidative stress and causes Sertoli cell death [73]. Another commonly used pesticide is DDT. Its main metabolite is 1,1-dichloro-2,2-bis(4-chlorophenyl) ethylene and direct exposure to this metabolite was found to be strongly associated with sperm immobility and mitochondrial dysfunction in a concentration-dependent manner [74, 75]. Furthermore, it’s been 49 years, since organochlorine chemicals such as DDT and polychlorinated biphenyls (PCB) have been banned in the USA, but that doesn’t mean that they are gone. They persist in the environment for years after use and are known as ‘legacy pesticide’ and still can produce deleterious impacts on male fertility. Organochlorine chemicals show resistance to breakdown, can bioaccumulate, enter the food chain, and can be transported over long distances [76, 77]. The use of DDT has been restricted in many nations across the world as a result of the Stockholm Convention, 2004 as a measure to protect human and environmental health from the side effects of exposure to specific persistent organic pollutants. Although its use in South Africa continued for malaria vector control and a cross-sectional study from this area reported a statistically significant positive correlation between the percentage of sperm with cytoplasmic droplets, teratozoospermia, asthenospermia, and oligospermia with blood plasma concentration of DDT and an inverse correlation with semen volume. Hence, they concluded that nonoccupational exposure to DDT results in impaired seminal parameters in healthy men [78]. A recent study observed that pesticide exposure also results in erectile dysfunctions in males, by causing apoptosis of Leydig cells, thereby decreasing the overall concentration of circulating testosterone in the body [79]. Many environmental pollutants including pesticides, polybrominated diphenyl ethers, BPA, phthalates act as endocrine-disrupting compounds. These chemicals are known to induce the MAPK signaling pathway in the testis. Three MAPK signaling pathways are known to be involved in pesticides related testicular injury. The testicular Erk1/2, p38 MAPK result in disruption of the blood testes barrier by blocking gap junction communications leading to germ cell depletion from the seminiferous epithelium [80]. Hence, prolonged, and excessive exposure to various pesticides and herbicides in our daily life can be a cause of compromised male fertility.

Phthalates

Phthalates, also known as Phthalic acid diesters are a group of man-made chemicals that are used in several consumer and industrial goods [81]. They are universally present environmental chemicals commonly found in many consumer products such as toys, pharmaceuticals, cosmetic products, building and construction materials, scent retainers, some medications, personal care products, etc. [82] and are known for their anti-androgenic activity. Phthalate gets easily absorbed in the human body through ingestion, skin, or inhalation of contaminated air. It causes a wide array of male reproductive organ dysfunction known as “phthalate syndrome” comprising of diminished anogenital distance, infertility, low sperm count, undescended testes, hypospadias, and many other reproductive-tract anomalies [83]. Phthalates, especially mono-(2-ethyl-hexyl) phthalate (MEHP), an active metabolite of Di-2-ethylhexyl phthalate (DEHP) causes activation of both PPAR (peroxisome proliferator-activated receptor) α and γ pathways [84], which in turn stimulates PPAR: RXR (retinoid X receptor) heterodimers that compete for DNA binding sites required for gene transcription, thus stopping the transcription of aromatase enzyme involved in sexual development. Furthermore, MEHP decreases the production of steroidogenic proteins including steroidogenic acute regulatory (StAR), and cytochrome P450 side-chain cleavage (P450scc), thereby adversely affecting male reproductive health. At high levels, it inhibits the activity of 3β-hydroxysteroid dehydrogenases (3β-HSD) and 17β-hydroxysteroid dehydrogenases (17β-HSD) specific to Leydig cell function in addition to the steroidogenic proteins by causing increased oxidative stress in Leydig cells, and hence, decreases testosterone synthesis [85]. A recent study conducted on male partners of infertile couples found that males who were exposed to ortho-phthalate drugs had poor semen quality as compared to unexposed ones [86]. Several other studies have also reported that phthalate exposure in humans has a significant adverse impact on overall semen quality [87, 88]. It causes reduced semen volume, total sperm counts, sperm concentration, morphological abnormalities of sperm head including large sperm head sizes, and other variations [61, 87]. Furthermore, it was observed that exposure to mono-methyl phthalate (MMP) and mono-cyclohexyl phthalate (MCPP) results in reduced sperm motility [87, 89]. Another recent study on the impact of eight phthalate metabolites measured in urine samples of 599 men attending an in-vitro fertilization clinic on the male reproductive functions and semen parameters reported an inverse correlation between serum testosterone and mono-isobutyl phthalate, FSH, and mono-(2-ethyl-5-hydroxyhexyl) phthalate, and prolactin and mono-(2-ethyl-5-oxohexyl) phthalate. Furthermore, they reported a positive correlation between sperm concentration and mono-(2-ethyl-5-carboxypentyl) phthalate, mono-(2-ethyl-5-hydroxyhexyl) phthalate, mono-(2-ethyl-5-oxohexyl) phthalate, and DHEP, but a negative correlation with the percentage of MEHP to molar sum of DHEP metabolites, hence indicating the need for further studies on the role of phthalates in male fertility [90]. Several mechanisms have been proposed for how phthalates affect male fertility by causing testicular damage, impairing normal testicular tissue structure, decreasing levels of circulating testosterone and other reproductive hormones, increasing sperm abnormalities, and by decreasing Sertoli cell viability [61, 91, 92]. A study reported that fetal exposure of male rats to di (n-butyl) phthalate results in testicular changes that are very similar to testicular dysgenesis syndrome observed in humans, characterized by focal areas of dysgenetic tubules in normal testes. di (n-butyl) phthalate exposure leads to abnormal accumulation of significantly small Leydig cells centrally in the fetal testis. The testosterone levels were also reduced. These Leydig cell collections did not exhibit features of focal proliferation as observed normally and have trapped isolated Sertoli cells within them resulting in the formation of dysgenetic tubules. These centrally located dysgenetic tubules have germ cells in early puberty, but have only Sertoli cells by adulthood, indicating that the presence of intratubular Leydig cells adversely affects spermatogenesis [93]. Hence, exposure to phthalates, a common component of many products used in daily life can affect male fertility.

Heavy metals

Another widespread environmental pollutant that can affect male fertility are non-essential heavy metals, such as lead, cadmium, arsenic, mercury, barium, etc. These heavy metals can adversely affect the semen and sperm quality in men. It was observed that the presence of Cadmium and Barium in blood, and Lead, Cadmium, Barium, and Uranium in seminal plasma were closely linked with increased risk for reduced sperm viability and normal sperm morphology [94]. Heavy metals affect male fertility by inducing reactive oxygen species generation, which in turn cause lipid peroxidation, sperm DNA damage, leading to infertility [95]. Lead and cadmium are known reproductive toxicants and are suspected endocrine disruptor compounds, which can alter hormonal levels in men and cause impaired semen quality and male infertility [96]. A study reported that exposure to high concentrations of copper sulphate (CuSO4—250 µg/ml) and Cadmium chloride (CdCl2—500 µg/ml) was associated with significantly reduced sperm motility parameters [97]. This was supported by the findings of another study which reported the association of heavy metals, such as lead, cadmium, mercury, zinc with oligospermia and male infertility [98]. Many other studies have also proposed the role of heavy metals in male infertility [99, 100].

Heat exposure

Another major factor that may contribute to male infertility is exposure to excessive heat at the workplace or due to climate change. Temperature plays a crucial role in maintaining normal spermatogenesis in testes. The scrotal temperature is 2–4 °C lower than the core body temperature [101, 102] and any factor that causes a rise in scrotal temperature will affect the spermatogenesis process resulting in male infertility [103]. Furthermore, it was observed that 1–1.5 °C elevation in scrotal temperature can result in impaired sperm production (oligozoospermia, azoospermia, teratozoospermia), and sperm morphological abnormalities [104]. Environmental stresses, such as a temperature rise, resulting in the activation of heat shock protein (HSP). Of these the most important is HSP70s, one of the major classes of proteins induced by elevated temperatures. They are responsible for the folding, assembly, and disassembly of other proteins [105] and are known to play a crucial role in spermatogenesis [106]. Hence, any factor that perturbs their normal expression and regulation results in an adverse impact on male fertility [107]. A study on 37 infertile men (cases) and 13 fertile men (controls) reported that HSP 70 levels were significantly increased in the infertile group as compared to fertile males, thereby concluding that HSP 70 expression increases in spermatozoa of infertile men as a protective mechanism against apoptosis [108]. Constant exposure to high temperatures as seen in cases of occupational exposure to radiant heat in people working in furnaces, bakeries, welding or ceramic factories, those working for long hours in kitchens, laundries, dry cleaning shops, or drivers can result in loss of thermoregulatory function of scrotum affecting one or more component of semen quality in males [103, 109]. This fact was further supported by a study that revealed that tight undergarments in men also lead to a rise in scrotal temperature resulting in decreased sperm concentration, total sperm count, motility, and hence, male infertility [110]. It was observed that higher scrotal temperatures result in a rise in testicular metabolism without the surge in blood supply, leading to local tissue hypoxia and oxidative stress [111]. Human spermatozoa are very susceptible to oxidative stress-induced lipid peroxidation because of high levels of polyunsaturated fatty acids (PUFAs) in their plasma membrane [112]. This in turn causes increased production of reactive oxygen species (ROS) which causes increased sperm DNA fragmentation and male infertility [113, 114]. It was demonstrated recently that excessive heat exposure causes decreased sperm motility by downregulating mitochondrial activity and reducing ATP levels [115]. Furthermore, a transient rise in scrotal temperature results in a reversible drop in proteins essential for the spermatogenesis process, gamete interaction, and sperm motility [116]. A recent study on male rats reported that exertional heatstroke can cause erectile dysfunctions, disruption of testicular temperature, poorly differentiated seminiferous tubules, diminished sperm quality, loss of interstitial Leydig cells, Sertoli cells, leading to azoospermia and infertility [117]. Another similar study conducted on bovine sperm also reported that heat stress in bulls induces seminal plasma oxidative stress thereby affecting the sperm mitochondrial function, motility, plasma membrane integrity, and DNA fragmentation, ultimately leading to infertility [118]. Another study observed the impact of wet heat exposure in the forms of hot tubs, Jacuzzi or hot baths in infertile male partners and concluded that the toxic effects of wet heat exposure are reversible, and withdrawal of hyperthermia resulted in increased sperm motility and quality in these patients, further supporting the fact that excessive heat exposure affects sperm parameters and can cause infertility in males [119]. A large longitudinal study including 10,802 Chinese men in Wuhan was conducted to quantitatively evaluate the exposure–response relationship between ambient temperature exposure and semen quality and observed that exposure to extremes of temperature, both high and low was found to be associated with decreased semen quality including reduced sperm concentration, total sperm count, total motility, progressive motility [120]. Another similar study reported that seasonal and monthly temperature variation has a significant impact on the human semen parameters. It was observed in their study that sperm concentration and total amount per ejaculate was significantly lower in summer and higher in winter, whereas the sperm progressive and total motility was found to be higher in spring and summer and lower in autumn and winter [121]. A large data analysis study in Northern Italy to evaluate the impact of environmental temperature and air pollution on semen parameters also reported that total sperm number was significantly lower in summer/autumn and was found to be inversely related with the duration of daylight [122]. Hence, though the data related to the impact of season or climate change on human semen quality is very little, pieces of evidence have been found to link extreme changes of temperature with poor semen quality. Other studies have also reported the impact of seasonal and environmental temperature variation on sperm quality [123,124,125]. Furthermore, many animal studies have also shown that a rise in testicular temperature results in reduced testicular size, decreased sperm production, increased abnormal sperm forms, and reduced motility leading to male infertility [115, 126, 127]. Hence, exposure to high temperatures both due to occupation or environmental factors has a deleterious impact on overall semen quality and can cause male infertility.

Table 1 depicts the impact of various environmental factors on male fertility in human and animal studies.

Table 1 Effect of Environmental Factors on Semen Quality and Male Fertility: A Comparison of Human and Animal Studies
Full size table

Conclusion

Hence, the environment plays a crucial role in male fertility. Adverse environmental factors can result in poor semen quality with decreased sperm concentration, sperm motility, viability, normal morphological forms, and increased sperm DNA fragmentation index, mitochondrial dysfunction, all leading to male infertility. However, all these factors can be prevented or modified, allowing us to decrease the risk associated with them. Decreasing air, chemical pollution, heat exposure and bringing positive changes in our daily lifestyle can prevent these adverse impacts on semen quality to a large extent, thereby reducing the overall incidence of male infertility.

Availability of data and materials

Not applicable.

Abbreviations

AR:

Androgen receptor

AHR:

Aryl hydrocarbon receptor

ARNT:

Aryl hydrocarbon receptor nuclear translocator

ATP:

Adenosine triphosphate

BPA:

Bisphenol A

CdCl2 :

Cadmium chloride

CuSO4 :

Copper sulphate

DDT:

Dichlorodiphenyltrichloroethane

p,p DDE:

p,p′-Dichlorodiphenyl-dichloroethylene

DEHP:

Di-2-ethylhexyl phthalate

DNA:

Deoxyribonucleic acid

FSH:

Follicle stimulating hormone

HSD:

Hydroxysteroid dehydrogenases

HSP:

Heat shock proteins

LH:

Luteinizing hormone

MAPK:

Mitogen-activated protein kinase

MCPP:

Mono-cyclohexyl phthalate

MEHP:

Mono-(2-ethylhexyl) phthalate

MMP:

Mono-methyl phthalate

MnBP:

Mono n-butylphthalate

NO2 :

Nitrogen dioxide

PAH:

Polycyclic aromatic hydrocarbons

PCB:

Polychlorinated biphenyls

PM:

Particulate matter

POP:

Persistent organic pollutants

PPAR:

Peroxisome proliferator-activated receptor

PUFAs:

Polyunsaturated fatty acids

P450scc:

Cytochrome P450 side-chain cleavage

ROS:

Reactive oxygen species

RXR:

Retinoid X receptor

SO2 :

Sulfur dioxide

StAR:

Steroidogenic acute regulatory

TCDD:

Tetrachlorodibenzo para dioxin

WHO:

World Health Organization

References

  1. Agarwal A, Baskaran S, Parekh N, Cho CL, Henkel R, Vij S, Arafa M, Panner Selvam MK, Shah R (2021) Male infertility. Lancet (London, England) 397(10271):319–333. https://doi.org/10.1016/S0140-6736(20)32667-2

    Article  Google Scholar 

  2. Krausz C (2011) Male infertility: pathogenesis and clinical diagnosis Best practice & research. Clin Endocrinol Metab 25(2):271–285. https://doi.org/10.1016/j.beem.2010.08.006

    Article  Google Scholar 

  3. Karavolos S, Panagiotopoulou N, Alahwany H, Martins da Silva S (2020) An update on the management of male infertility. TOG 22(4):267–274. https://doi.org/10.1111/tog.12688

    Article  Google Scholar 

  4. Checa Vizcaíno MA, González-Comadran M, Jacquemin B (2016) Outdoor air pollution and human infertility: a systematic review. Fertil Steril 106(4):897-904.e1. https://doi.org/10.1016/j.fertnstert.2016.07.1110

    Article  CAS  Google Scholar 

  5. Zhang G, Jiang F, Chen Q, Yang H, Zhou N, Sun L, Zou P, Yang W, Cao J, Zhou Z, Ao L (2020) Associations of ambient air pollutant exposure with seminal plasma MDA, sperm mtDNA copy number, and mtDNA integrity. Environ Int 136:105483. https://doi.org/10.1016/j.envint.2020.105483

    Article  CAS  Google Scholar 

  6. Blay RM, Pinamang AD, Sagoe AE, Owusu E, Koney NK, Arko-Boham B (2020) Influence of lifestyle and environmental factors on semen quality in ghanaian men. Int J Reprod Med 2020:6908458. https://doi.org/10.1155/2020/6908458

    Article  Google Scholar 

  7. Nateghian Z, Aliabadi E (2020) Aspects of Environmental Pollutants on Male Fertility and Sperm Parameters. J Environ Treat Tech 8(1):299–309. http://www.jett.dormaj.com

  8. Selvaraju V, Baskaran S, Agarwal A, Henkel R (2021) Environmental contaminants and male infertility: effects and mechanisms. Andrologia 53(1):e13646. https://doi.org/10.1111/and.13646

    Article  CAS  Google Scholar 

  9. Oliva A, Spira A, Multigner L (2001) Contribution of environmental factors to the risk of male infertility. Hum Reprod 16(8):1768–1776. https://doi.org/10.1093/humrep/16.8.1768

    Article  CAS  Google Scholar 

  10. Sharpe RM (2010) Environmental/lifestyle effects on spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365(1546):1697–1712. https://doi.org/10.1098/rstb.2009.0206

    Article  CAS  Google Scholar 

  11. Atkinson RW, Kang S, Anderson HR, Mills IC, Walton HA (2014) Epidemiological time series studies of PM2.5 and daily mortality and hospital admissions: a systematic review and meta-analysis. Thorax 69(7):660–665. https://doi.org/10.1136/thoraxjnl-2013-204492

    Article  CAS  Google Scholar 

  12. Cosselman KE, Navas-Acien A, Kaufman JD (2015) Environmental factors in cardiovascular disease. Nat Rev Cardiol 12(11):627–642. https://doi.org/10.1038/nrcardio.2015.152

    Article  CAS  Google Scholar 

  13. Ahn K (2014) The role of air pollutants in atopic dermatitis. J Allergy Clin Immunol 134(5):993–1000. https://doi.org/10.1016/j.jaci.2014.09.023

    Article  CAS  Google Scholar 

  14. Lemjabbar-Alaoui H, Hassan OU, Yang YW (1856) Lung cancer: Biology and treatment options. Biochem Biophys Acta 2:189–210. https://doi.org/10.1016/j.bbcan.2015.08.002

    Article  CAS  Google Scholar 

  15. Chiang C, Mahalingam S, Flaws JA (2017) Environmental contaminants affecting fertility and somatic health. Semin Reprod Med 35(3):241–249. https://doi.org/10.1055/s-0037-1603569

    Article  CAS  Google Scholar 

  16. Deng Z, Chen F, Zhang M, Lan L, Qiao Z, Cui Y, An J, Wang N, Fan Z, Zhao X, Li X (2016) Association between air pollution and sperm quality: a systematic review and meta-analysis. Environ Pollution 208(Pt B):663–669. https://doi.org/10.1016/j.envpol.2015.10.044

    Article  CAS  Google Scholar 

  17. Giudice LC (2016) Environmental toxicants: hidden players on the reproductive stage. Fertil Steril 106(4):791–794. https://doi.org/10.1016/j.fertnstert.2016.08.019

    Article  CAS  Google Scholar 

  18. World's most polluted countries 2020 (PM2.5) https://www.iqair.com/in-en/world-most-polluted-countries.

  19. Rengaraj D, Kwon WS, Pang MG (2015) Effects of motor vehicle exhaust on male reproductive function and associated proteins. J Proteome Res 14(1):22–37. https://doi.org/10.1021/pr500939c

    Article  CAS  Google Scholar 

  20. Cheung K, Daher N, Kam W, Shafer MM, Ning Z, Schauer JJ, Constantinos S (2011) Spatial and temporal variation of chemical composition and mass closure of ambient coarse particulate matter (PM10–2.5) in the Los Angeles area. Atmos Environ 45(16):2651–2662. https://doi.org/10.1016/j.atmosenv.2011.02.066

    Article  CAS  Google Scholar 

  21. Zhang L, Yang Y, Li Y, Qian ZM, Xiao W, Wang X, Rolling CA, Liu E, Xiao J, Zeng W, Liu T, Li X, Yao Z, Wang H, Ma W, Lin H (2019) Short-term and long-term effects of PM2.5 on acute nasopharyngitis in 10 communities of Guangdong. China Sci Total Environ 688:136–142. https://doi.org/10.1016/j.scitotenv.2019.05.470

    Article  CAS  Google Scholar 

  22. Jurewicz J, Dziewirska E, Radwan M, Hanke W (2018) Air pollution from natural and anthropic sources and male fertility. Reprod Biol Endocrinol 16(1):109. https://doi.org/10.1186/s12958-018-0430-2

    Article  CAS  Google Scholar 

  23. Zhang J, Cai Z, Ma C, Xiong J, Li H (2020) Impacts of outdoor air pollution on human semen quality: a meta-analysis and systematic review. Biomed Res Int 2020:7528901. https://doi.org/10.1155/2020/7528901

    Article  CAS  Google Scholar 

  24. Wang X, Tian X, Ye B, Zhang Y, Li C, Liao J, Zou Y, Zhang S, Zhu Y, Yang J, Ma L (2020) Gaseous pollutant exposure affects semen quality in central China: a cross-sectional study. Andrology 8(1):117–124. https://doi.org/10.1111/andr.12655

    Article  CAS  Google Scholar 

  25. De Rosa M, Zarrilli S, Paesano L, Carbone U, Boggia B, Petretta M, Maisto A, Cimmino F, Puca G, Colao A, Lombardi G (2003) Traffic pollutants affect fertility in men. Human Reprod (Oxford, England) 18(5):1055–1061. https://doi.org/10.1093/humrep/deg226

    Article  CAS  Google Scholar 

  26. Calogero AE, La Vignera S, Condorelli RA, Perdichizzi A, Valenti D, Asero P, Carbone U, Boggia B, De Rosa N, Lombardi G, D’Agata R, Vicari LO, Vicari E, De Rosa M (2011) Environmental car exhaust pollution damages human sperm chromatin and DNA. J Endocrinol Invest 34(6):e139–e143. https://doi.org/10.1007/BF03346722

    Article  CAS  Google Scholar 

  27. Wdowiak A, Wdowiak E, Bień A, Bojar I, Iwanowicz-Palus G, Raczkiewicz D (2019) Air pollution and semen parameters in men seeking fertility treatment for the first time. Int J Occup Med Environ Health 32(3):387–399. https://doi.org/10.13075/ijomeh.1896.01355

    Article  Google Scholar 

  28. Wang L, Luo D, Liu X, Zhu J, Wang F, Li B, Li L (2021) Effects of PM2.5 exposure on reproductive system and its mechanisms. Chemosphere 264(Pt 1):128436. https://doi.org/10.1016/j.chemosphere.2020.128436

    Article  CAS  Google Scholar 

  29. Zhang J, Liu J, Ren L, Wei J, Duan J, Zhang L, Zhou X, Sun Z (2018) PM2.5 induces male reproductive toxicity via mitochondrial dysfunction, DNA damage and RIPK1 mediated apoptotic signaling pathway. Sci Total Environ 634:1435–1444. https://doi.org/10.1016/j.scitotenv.2018.03.383

    Article  CAS  Google Scholar 

  30. Hansen C, Luben TJ, Sacks JD, Olshan A, Jeffay S, Strader L, Perreault SD (2010) The effect of ambient air pollution on sperm quality. Environ Health Perspect 118(2):203–209. https://doi.org/10.1289/ehp.0901022

    Article  CAS  Google Scholar 

  31. Chen Y, Chang HC, Liao CH, Chiang BJ, Chang YK (2019) The impact of the fine ambient particle on infertile male's sperm quality. Urol Sci 30:177–83. https://www.e-urol-sci.com/text.asp?2019/30/4/177/263652.

  32. Hammoud A, Carrell DT, Gibson M, Sanderson M, Parker-Jones K, Peterson CM (2010) Decreased sperm motility is associated with air pollution in Salt Lake City. Fertil Steril 93(6):1875–1879. https://doi.org/10.1016/j.fertnstert.2008.12.089

    Article  Google Scholar 

  33. Carré J, Gatimel N, Moreau J, Parinaud J, Léandri R (2017) Does air pollution play a role in infertility?: a systematic review. Environ Health 16(1):82. https://doi.org/10.1186/s12940-017-0291-8

    Article  CAS  Google Scholar 

  34. Takeda K, Tsukue N, Yoshida S (2004) Endocrine-disrupting activity of chemicals in diesel exhaust and diesel exhaust particles. Environ Sci 11(1):33–45

    CAS  Google Scholar 

  35. Sklorz M, Briedé JJ, Schnelle-Kreis J, Liu Y, Cyrys J, de Kok TM, Zimmermann R (2007) Concentration of oxygenated polycyclic aromatic hydrocarbons and oxygen free radical formation from urban particulate matter. J Toxicol Environ Health A 70(21):1866–1869. https://doi.org/10.1080/15287390701457654

    Article  CAS  Google Scholar 

  36. Gaspari L, Chang SS, Santella RM, Garte S, Pedotti P, Taioli E (2003) Polycyclic aromatic hydrocarbon-DNA adducts in human sperm as a marker of DNA damage and infertility. Mutat Res 535(2):155–160. https://doi.org/10.1016/s1383-5718(02)00297-8

    Article  CAS  Google Scholar 

  37. Dissanayake DMIH, Keerthirathna WLR, Peiris LDC (2019) Male infertility problem: a contemporary review on present status and future perspective. Gender Genome 3:1–7. https://doi.org/10.1177/2470289719868240

    Article  Google Scholar 

  38. Istvan M, Rahban R, Dananche B, Senn A, Stettler E, Multigner L, Nef S, Garlantézec R (2021) Maternal occupational exposure to endocrine-disrupting chemicals during pregnancy and semen parameters in adulthood: results of a nationwide cross-sectional study among Swiss conscripts. Hum Reprod 36(7):1948–1958. https://doi.org/10.1093/humrep/deab034

    Article  CAS  Google Scholar 

  39. Pilsner JR, Parker M, Sergeyev O, Suvorov A (2017) Spermatogenesis disruption by dioxins: epigenetic reprograming and windows of susceptibility. Reprod Toxicol 69:221–229. https://doi.org/10.1016/j.reprotox.2017.03.002

    Article  CAS  Google Scholar 

  40. Foster WG, Maharaj-Briceño S, Cyr DG (2010) Dioxin-induced changes in epididymal sperm count and spermatogenesis. Environ Health Perspect 118(4):458–464. https://doi.org/10.1289/ehp.0901084

    Article  CAS  Google Scholar 

  41. Hewitt LM, Parrott JL, McMaster ME (2006) A decade of research on the environmental impacts of pulp and paper mill effluents in Canada: sources and characteristics of bioactive substances. J Toxicol Environ Health B Crit Rev 9(4):341–356. https://doi.org/10.1080/15287390500195976

    Article  CAS  Google Scholar 

  42. World Health Organization (2016) Dioxins and their effects on human health. Fact Sheet. https://www.who.int/news-room/fact-sheets/detail/dioxins-and-their-effects-on-human-health.

  43. Schultz R, Suominen J, Värre T, Hakovirta H, Parvinen M, Toppari J, Pelto-Huikko M (2003) Expression of aryl hydrocarbon receptor and aryl hydrocarbon receptor nuclear translocator messenger ribonucleic acids and proteins in rat and human testis. Endocrinology 144(3):767–776. https://doi.org/10.1210/en.2002-220642

    Article  CAS  Google Scholar 

  44. Akemann C, Meyer DN, Gurdziel K, Baker TR (2019) Developmental dioxin exposure alters the methylome of adult male zebrafish gonads. Front Genet 9:719. https://doi.org/10.3389/fgene.2018.00719

    Article  CAS  Google Scholar 

  45. Jiang L, Zhang J, Wang JJ, Wang L, Zhang L, Li G, Yang X, Ma X, Sun X, Cai J, Zhang J, Huang X, Yu M, Wang X, Liu F, Wu CI, He C, Zhang B, Ci W, Liu J (2013) Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos. Cell 153(4):773–784. https://doi.org/10.1016/j.cell.2013.04.041

    Article  CAS  Google Scholar 

  46. Ribas L, Vanezis K, Imués MA, Piferrer F (2017) Treatment with a DNA methyltransferase inhibitor feminizes zebrafish and induces long-term expression changes in the gonads. Epigenetics Chromatin 10:59. https://doi.org/10.1186/s13072-017-0168-7

    Article  CAS  Google Scholar 

  47. Mocarelli P, Gerthoux PM, Patterson DG Jr, Milani S, Limonta G, Bertona M, Signorini S, Tramacere P, Colombo L, Crespi C, Brambilla P, Sarto C, Carreri V, Sampson EJ, Turner WE, Needham LL (2008) Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality. Environ Health Perspect 116(1):70–77. https://doi.org/10.1289/ehp.10399

    Article  CAS  Google Scholar 

  48. Barrett JR (2011) Window for dioxin damage: sperm quality in men born after the Seveso disaster. Environ Health Perspect 119(5):A219. https://doi.org/10.1289/ehp.119-a219b

    Article  Google Scholar 

  49. Galimova EF, Amirova ZK, Galimov S (2015) Dioxins in the semen of men with infertility. Environ Sci Pollut Res Int 22(19):14566–14569. https://doi.org/10.1007/s11356-014-3109-z

    Article  CAS  Google Scholar 

  50. Mohammadi S, Rahmani F, Hasanian SM, Beheshti F, Akbari Oryani M, Ebrahimzadeh A, Farzadfar S (2019) Effects of dioxin on testicular histopathology, sperm parameters, and CatSper2 gene and protein expression in Naval Medical Research Institute male mice. Andrologia 51(11):e13411. https://doi.org/10.1111/and.13411

    Article  Google Scholar 

  51. Manfo FP, Jubendradass R, Nantia EA, Moundipa PF, Mathur PP (2014) Adverse effects of bisphenol A on male reproductive function. Rev Environ Contam Toxicol 228:57–82. https://doi.org/10.1007/978-3-319-01619-1_3

    Article  CAS  Google Scholar 

  52. Lehmler HJ, Liu B, Gadogbe M, Bao W (2018) Exposure to Bisphenol A, Bisphenol F, and Bisphenol S in U.S. Adults and Children: The National Health and Nutrition Examination Survey 2013–2014. ACS Omega 3(6):6523–6532. https://doi.org/10.1021/acsomega.8b00824

    Article  CAS  Google Scholar 

  53. Castellini C, Totaro M, Parisi A, D’Andrea S, Lucente L, Cordeschi G, Francavilla S, Francavilla F, Barbonetti A (2020) Bisphenol A and male fertility: myths and realities. Front Endocrinol 11:353. https://doi.org/10.3389/fendo.2020.00353

    Article  Google Scholar 

  54. Cariati F, D’Uonno N, Borrillo F, Iervolino S, Galdiero G, Rb T (2019) Bisphenol a: an emerging threat to male fertility. Reprod Biol Endocrinol 17(1):6. https://doi.org/10.1186/s12958-018-0447-6

    Article  Google Scholar 

  55. Rochester JR (2013) Bisphenol A and human health: a review of the literature. Reproduct Toxicol 42:132–155. https://doi.org/10.1016/j.reprotox.2013.08.008

    Article  CAS  Google Scholar 

  56. Barbonetti A, Castellini C, Di Giammarco N, Santilli G, Francavilla S, Francavilla F (2016) In vitro exposure of human spermatozoa to bisphenol A induces pro-oxidative/apoptotic mitochondrial dysfunction. Reprod Toxicol 66:61–67. https://doi.org/10.1016/j.reprotox.2016.09.014

    Article  CAS  Google Scholar 

  57. Grami D, Rtibi K, Hammami I, Selmi S, De Toni L, Foresta C, Marzouki L, Sebai H (2020) Protective action of eruca sativa leaves aqueous extracts against bisphenol A-caused in vivo testicular damages. J Med Food 23(6):600–610. https://doi.org/10.1089/jmf.2019.0170

    Article  CAS  Google Scholar 

  58. Wisniewski P, Romano RM, Kizys MM, Oliveira KC, Kasamatsu T, Giannocco G, Chiamolera MI, Dias-da-Silva MR, Romano MA (2015) Adult exposure to bisphenol A (BPA) in Wistar rats reduces sperm quality with disruption of the hypothalamic-pituitary-testicular axis. Toxicology 329:1–9. https://doi.org/10.1016/j.tox.2015.01.002

    Article  CAS  Google Scholar 

  59. Dobrzyńska MM, Radzikowska J (2013) Genotoxicity and reproductive toxicity of bisphenol A and X-ray/bisphenol A combination in male mice. Drug Chem Toxicol 36(1):19–26. https://doi.org/10.3109/01480545.2011.644561

    Article  CAS  Google Scholar 

  60. Rahman MS, Kwon WS, Lee JS, Yoon SJ, Ryu BY, Pang MG (2015) Bisphenol-A affects male fertility via fertility-related proteins in spermatozoa. Sci Rep 5:9169. https://doi.org/10.1038/srep09169

    Article  CAS  Google Scholar 

  61. Caporossi L, Alteri A, Campo G, Paci E, Tranfo G, Capanna S, Papaleo E, Pigini D, Viganò P, Papaleo B (2020) Cross sectional study on exposure to BPA and phthalates and semen parameters in men attending a fertility center. Int J Environ Res Public Health 17(2):489. https://doi.org/10.3390/ijerph17020489

    Article  CAS  Google Scholar 

  62. Radwan M, Wielgomas B, Dziewirska E, Radwan P, Kałużny P, Klimowska A, Hanke W, Jurewicz J (2018) Urinary bisphenol a levels and male fertility. Am J Mens Health 12(6):2144–2151. https://doi.org/10.1177/1557988318799163

    Article  Google Scholar 

  63. Tomza-Marciniak A, Stępkowska P, Kuba J, Pilarczyk B (2018) Effect of bisphenol A on reproductive processes: A review of in vitro, in vivo and epidemiological studies. J Appl Toxicol 38(1):51–80. https://doi.org/10.1002/jat.3480

    Article  CAS  Google Scholar 

  64. Murata M, Kang JH (2018) Bisphenol A (BPA) and cell signaling pathways. Biotechnol Adv 36(1):311–327. https://doi.org/10.1016/j.biotechadv.2017.12.002

    Article  CAS  Google Scholar 

  65. Wang H, Ding Z, Shi QM, Ge X, Wang HX, Li MX, Chen G, Wang Q, Ju Q, Zhang JP, Zhang MR, Xu LC (2017) Anti-androgenic mechanisms of Bisphenol A involve androgen receptor signaling pathway. Toxicology 387:10–16. https://doi.org/10.1016/j.tox.2017.06.007

    Article  CAS  Google Scholar 

  66. Xi W, Lee CK, Yeung WS, Giesy JP, Wong MH, Zhang X, Hecker M, Wong CK (2011) Effect of perinatal and postnatal bisphenol A exposure to the regulatory circuits at the hypothalamus-pituitary-gonadal axis of CD-1 mice. Reprod Toxicol 31(4):409–417. https://doi.org/10.1016/j.reprotox.2010.12.002

    Article  CAS  Google Scholar 

  67. Nakamura D, Yanagiba Y, Duan Z, Ito Y, Okamura A, Asaeda N, Tagawa Y, Li C, Taya K, Zhang SY, Naito H, Ramdhan DH, Kamijima M, Nakajima T (2010) Bisphenol A may cause testosterone reduction by adversely affecting both testis and pituitary systems similar to estradiol. Toxicol Lett 194(1–2):16–25. https://doi.org/10.1016/j.toxlet.2010.02.002

    Article  CAS  Google Scholar 

  68. Bretveld R, Brouwers M, Ebisch I, Roeleveld N (2007) Influence of pesticides on male fertility. Scand J Work Environ Health 33(1):13–28. https://doi.org/10.5271/sjweh.1060

    Article  CAS  Google Scholar 

  69. Turusov V, Rakitsky V, Tomatis L (2002) Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence, and risks. Environ Health Perspect 110(2):125–128. https://doi.org/10.1289/ehp.02110125

    Article  CAS  Google Scholar 

  70. Bhatia R, Shiau R, Petreas M, Weintraub JM, Farhang L, Eskenazi B (2005) Organochlorine pesticides and male genital anomalies in the child health and development studies. Environ Health Perspect 113(2):220–224. https://doi.org/10.1289/ehp.7382

    Article  CAS  Google Scholar 

  71. Roeleveld N, Bretveld R (2008) The impact of pesticides on male fertility. Curr Opin Obstet Gynecol 20(3):229–233. https://doi.org/10.1097/GCO.0b013e3282fcc334

    Article  Google Scholar 

  72. Anifandis G, Amiridis G, Dafopoulos K, Daponte A, Dovolou E, Gavriil E, Gorgogietas V, Kachpani E, Mamuris Z, Messini CI, Vassiou K, Psarra AG (2017) The in vitro impact of the herbicide roundup on human sperm motility and sperm mitochondria. Toxics 6(1):2. https://doi.org/10.3390/toxics6010002

    Article  CAS  Google Scholar 

  73. de Liz Oliveira Cavalli VL, Cattani D, Heinz Rieg CE, Pierozan P, Zanatta L, Benedetti Parisotto E, Wilhelm Filho D, Mena Barreto Silva FR, Pessoa-Pureur R, Zamoner A, (2013) Roundup disrupts male reproductive functions by triggering calcium-mediated cell death in rat testis and Sertoli cells. Free Radic Biol Med 65:335–346. https://doi.org/10.1016/j.freeradbiomed.2013.06.043

    Article  CAS  Google Scholar 

  74. Tavares RS, Amaral S, Paiva C, Baptista M, Ramalho-Santos J (2015) In vitro exposure to the organochlorine p, p’-DDE affects functional human sperm parameters. Chemosphere 120:443–446. https://doi.org/10.1016/j.chemosphere.2014.08.075

    Article  CAS  Google Scholar 

  75. Pant N, Shukla M, Upadhyay AD, Chaturvedi PK, Saxena DK, Gupta YK (2014) Association between environmental exposure to p, p’-DDE and lindane and semen quality. Environ Sci Pollut Res Int 21(18):11009–11016. https://doi.org/10.1007/s11356-014-2965-x

    Article  CAS  Google Scholar 

  76. ATSDR (2002) Toxicological Profile for DDT, DDE, and DDD. Atlanta, GA: Agency for Toxic Substances and Disease Registry.

  77. Longnecker MP (2005) Invited commentary: why DDT matters now. Am J Epidemiol 162(8):726–728. https://doi.org/10.1093/aje/kwi277

    Article  Google Scholar 

  78. Aneck-Hahn NH, Schulenburg GW, Bornman MS, Farias P, de Jager C (2007) Impaired semen quality associated with environmental DDT exposure in young men living in a malaria area in the Limpopo Province. South Africa J Androl 28(3):423–434. https://doi.org/10.2164/jandrol.106.001701

    Article  CAS  Google Scholar 

  79. Kaur RP, Gupta V, Christopher AF, Bansal P (2015) Potential pathways of pesticide action on erectile function—a contributory factor in male infertility. Asian Pacific J Reprod 4(4):322–330. https://doi.org/10.1016/j.apjr.2015.07.012

    Article  Google Scholar 

  80. Cheng CY, Wong EW, Lie PP, Li MW, Su L, Siu ER, Yan HH, Mannu J, Mathur PP, Bonanomi M, Silvestrini B, Mruk DD (2011) Environmental toxicants and male reproductive function. Spermatogenesis 1(1):2–13. https://doi.org/10.4161/spmg.1.1.13971

    Article  Google Scholar 

  81. Radke EG, Braun JM, Meeker JD, Cooper GS (2018) Phthalate exposure and male reproductive outcomes: a systematic review of the human epidemiological evidence. Environ Int 121(Pt 1):764–793. https://doi.org/10.1016/j.envint.2018.07.029

    Article  CAS  Google Scholar 

  82. Lioy PJ, Hauser R, Gennings C, Koch HM, Mirkes PE, Schwetz BA, Kortenkamp A (2015) Assessment of phthalates/phthalate alternatives in children’s toys and childcare articles: Review of the report including conclusions and recommendation of the Chronic Hazard Advisory Panel of the Consumer Product Safety Commission. J Expo Sci Environ Epidemiol 25(4):343–353. https://doi.org/10.1038/jes.2015.33

    Article  CAS  Google Scholar 

  83. National Academies of Sciences, Engineering, and Medicine; Division on Earth and Life Studies; Board on Environmental Studies and Toxicology; Committee on Endocrine-Related Low-Dose Toxicity (2017) Application of Systematic Review Methods in an Overall Strategy for Evaluating Low-Dose Toxicity from Endocrine Active Chemicals. Washington (DC): National Academies Press (US), 3, Phthalates and Male Reproductive-Tract Development. https://www.ncbi.nlm.nih.gov/books/NBK453249/

  84. Lovekamp-Swan T, Jetten AM, Davis BJ (2003) Dual activation of PPARalpha and PPARgamma by mono-(2-ethylhexyl) phthalate in rat ovarian granulosa cells. Mol Cell Endocrinol 201(1–2):133–141. https://doi.org/10.1016/s0303-7207(02)00423-9

    Article  CAS  Google Scholar 

  85. Zhao Y, Ao H, Chen L, Sottas CM, Ge RS, Li L, Zhang Y (2012) Mono-(2-ethylhexyl) phthalate affects the steroidogenesis in rat Leydig cells through provoking ROS perturbation. Toxicol In Vitro 26(6):950–955. https://doi.org/10.1016/j.tiv.2012.04.003

    Article  CAS  Google Scholar 

  86. Broe A, Pottegård A, Hallas J, Ahern TP, Fedder J, Damkier P (2018) Association between use of phthalate-containing medication and semen quality among men in couples referred for assisted reproduction. Hum Reprod 33(3):503–511. https://doi.org/10.1093/humrep/dey009

    Article  CAS  Google Scholar 

  87. Bloom MS, Whitcomb BW, Chen Z, Ye A, Kannan K, Buck Louis GM (2015) Associations between urinary phthalate concentrations and semen quality parameters in a general population. Hum Reprod 30(11):2645–2657. https://doi.org/10.1093/humrep/dev219

    Article  CAS  Google Scholar 

  88. Cai H, Zheng W, Zheng P, Wang S, Tan H, He G, Qu W (2015) Human urinary/seminal phthalates or their metabolite levels and semen quality: a meta-analysis. Environ Res 142:486–494. https://doi.org/10.1016/j.envres.2015.07.008

    Article  CAS  Google Scholar 

  89. Thurston SW, Mendiola J, Bellamy AR, Levine H, Wang C, Sparks A, Redmon JB, Drobnis EZ, Swan SH (2016) Phthalate exposure and semen quality in fertile US men. Andrology 4(4):632–638. https://doi.org/10.1111/andr.12124

    Article  CAS  Google Scholar 

  90. Al-Saleh I, Coskun S, Al-Doush I, Al-Rajudi T, Abduljabbar M, Al-Rouqi R, Palawan H, Al-Hassan S (2019) The relationships between urinary phthalate metabolites, reproductive hormones and semen parameters in men attending in vitro fertilization clinic. Sci Total Environ 658:982–995. https://doi.org/10.1016/j.scitotenv.2018.12.261

    Article  CAS  Google Scholar 

  91. Wang H, Zhou W, Zhang J, Li H (2019) Role of JNK and ERK1/2 MAPK signaling pathway in testicular injury of rats induced by di-N-butyl-phthalate (DBP). Biol Res 52(1):41. https://doi.org/10.1186/s40659-019-0248-1

    Article  CAS  Google Scholar 

  92. Yin X, Ma T, Han R, Ding J, Zhang H, Han X, Li D (2018) MiR-301b-3p/3584-5p enhances low-dose mono-n-butyl phthalate (MBP)-induced proliferation by targeting Rasd1 in Sertoli cells. Toxicol In Vitro 47:79–88. https://doi.org/10.1016/j.tiv.2017.11.009

    Article  CAS  Google Scholar 

  93. Mahood IK, Hallmark N, McKinnell C, Walker M, Fisher JS, Sharpe RM (2005) Abnormal Leydig Cell aggregation in the fetal testis of rats exposed to di (n-butyl) phthalate and its possible role in testicular dysgenesis. Endocrinology 146(2):613–623. https://doi.org/10.1210/en.2004-0671

    Article  CAS  Google Scholar 

  94. Sukhn C, Awwad J, Ghantous A, Zaatari G (2018) Associations of semen quality with non-essential heavy metals in blood and seminal fluid: data from the Environment and Male Infertility (EMI) study in Lebanon. J Assist Reprod Genet 35(9):1691–1701. https://doi.org/10.1007/s10815-018-1236-z

    Article  Google Scholar 

  95. Jamalan M, Ghaffari MA, Hoseinzadeh P, Hashemitabar M, Zeinali M (2016) Human sperm quality and metal toxicants: protective effects of some flavonoids on male reproductive function. Int J Fertil Steril 10(2):215–223. https://doi.org/10.22074/ijfs.2016.4912

    Article  CAS  Google Scholar 

  96. Mendiola J, Moreno JM, Roca M, Vergara-Juárez N, Martínez-García MJ, García-Sánchez A, Elvira-Rendueles B, Moreno-Grau S, López-Espín JJ, Ten J, Bernabeu R, Torres-Cantero AM (2011) Relationships between heavy metal concentrations in three different body fluids and male reproductive parameters: a pilot study. Environ Health 10(1):6. https://doi.org/10.1186/1476-069X-10-6

    Article  CAS  Google Scholar 

  97. Hardneck F, Israel G, Pool E, Maree L (2018) Quantitative assessment of heavy metal effects on sperm function using computer-aided sperm analysis and cytotoxicity assays. Andrologia 50(10):e13141. https://doi.org/10.1111/and.13141

    Article  CAS  Google Scholar 

  98. Rispoli AF, Stabile G, Ingenito CM, Stabile M (2018) Heavy metals in semen of oligospermic patients without known etiologic factors. Biol Med (Aligarh) 10(2):434. https://doi.org/10.4172/0974-8369.1000432

    Article  Google Scholar 

  99. Ali HM, Kanaem QA, Selman MO (2020) Relation of Some Heavy Metals with Male Infertility. Medico-legal Update 20(1):1140–1145. https://doi.org/10.37506/mlu.v20i1.578

    Article  Google Scholar 

  100. Pant N, Kumar G, Upadhyay AD, Gupta YK, Chaturvedi PK (2015) Correlation between lead and cadmium concentration and semen quality. Andrologia 47(8):887–891. https://doi.org/10.1111/and.12342

    Article  CAS  Google Scholar 

  101. Ivell R (2007) Lifestyle impact and the biology of the human scrotum. Reprod Biol Endocrinol 5:15. https://doi.org/10.1186/1477-7827-5-15

    Article  Google Scholar 

  102. Garolla A, Torino M, Miola P, Caretta N, Pizzol D, Menegazzo M, Bertoldo A, Foresta C (2015) Twenty-four-hour monitoring of scrotal temperature in obese men and men with a varicocele as a mirror of spermatogenic function. Hum Reprod 30(5):1006–1013. https://doi.org/10.1093/humrep/dev057

    Article  CAS  Google Scholar 

  103. Al-Otaibi ST (2018) Male infertility among bakers associated with exposure to high environmental temperature at the workplace. J Taibah Univ Med Sci 13(2):103–107. https://doi.org/10.1016/j.jtumed.2017.12.003

    Article  Google Scholar 

  104. Hamerezaee M, Dehghan SF, Golbabaei F, Fathi A, Barzegar L, Heidarnejad N (2018) Assessment of semen quality among workers exposed to heat stress: a cross-sectional study in a steel industry. Saf Health Work 9(2):232–235. https://doi.org/10.1016/j.shaw.2017.07.003

    Article  Google Scholar 

  105. Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670–684. https://doi.org/10.1007/s00018-004-4464-6

    Article  CAS  Google Scholar 

  106. Huang SY, Tam MF, Hsu YT, Lin JH, Chen HH, Chuang CK, Chen MY, King YT, Lee WC (2005) Developmental changes of heat-shock proteins in porcine testis by a proteomic analysis. Theriogenology 64(9):1940–1955. https://doi.org/10.1016/j.theriogenology.2005.04.024

    Article  CAS  Google Scholar 

  107. Rockett JC, Mapp FL, Garges JB, Luft JC, Mori C, Dix DJ (2001) Effects of hyperthermia on spermatogenesis, apoptosis, gene expression, and fertility in adult male mice. Biol Reprod 65(1):229–239. https://doi.org/10.1095/biolreprod65.1.229

    Article  CAS  Google Scholar 

  108. Erata GO, Koçak Toker N, Durlanik O, Kadioğlu A, Aktan G, Aykaç Toker G (2008) The role of heat shock protein 70 (Hsp 70) in male infertility: is it a line of defense against sperm DNA fragmentation? Fertil Steril 90(2):322–327. https://doi.org/10.1016/j.fertnstert.2007.06.021

    Article  CAS  Google Scholar 

  109. Barazani Y, Katz BF, Nagler HM, Stember DS (2014) Lifestyle, environment, and male reproductive health. Urol Clin North Am 41(1):55–66. https://doi.org/10.1016/j.ucl.2013.08.017

    Article  Google Scholar 

  110. Mínguez-Alarcón L, Gaskins AJ, Chiu YH, Messerlian C, Williams PL, Ford JB, Souter I, Hauser R, Chavarro JE (2018) Type of underwear worn and markers of testicular function among men attending a fertility center. Hum Reprod 33(9):1749–1756. https://doi.org/10.1093/humrep/dey259

    Article  CAS  Google Scholar 

  111. Reyes JG, Farias JG, Henríquez-Olavarrieta S, Madrid E, Parraga M, Zepeda AB, Moreno RD (2012) The hypoxic testicle: physiology and pathophysiology. Oxid Med Cell Longev 2012:929285. https://doi.org/10.1155/2012/929285

    Article  CAS  Google Scholar 

  112. Vernet P, Aitken RJ, Drevet JR (2004) Antioxidant strategies in the epididymis. Mol Cell Endocrinol 216(1–2):31–39. https://doi.org/10.1016/j.mce.2003.10.069

    Article  CAS  Google Scholar 

  113. Hamilton TR, Mendes CM, de Castro LS, de Assis PM, Siqueira AF, Delgado Jde C, Goissis MD, Muiño-Blanco T, Cebrián-Pérez JÁ, Nichi M, Visintin JA, Assumpção ME (2016) Evaluation of lasting effects of heat stress on sperm profile and oxidative status of ram semen and epididymal sperm. Oxid Med Cell Longev 2016:1687657. https://doi.org/10.1155/2016/1687657

    Article  CAS  Google Scholar 

  114. Mahfouz R, Sharma R, Thiyagarajan A, Kale V, Gupta S, Sabanegh E, Agarwal A (2010) Semen characteristics and sperm DNA fragmentation in infertile men with low and high levels of seminal reactive oxygen species. Fertil Steril 94(6):2141–2146. https://doi.org/10.1016/j.fertnstert.2009.12.030

    Article  CAS  Google Scholar 

  115. Gong Y, Guo H, Zhang Z, Zhou H, Zhao R, He B (2017) Heat Stress reduces sperm motility via activation of glycogen synthase kinase-3α and inhibition of mitochondrial protein import. Front Physiol 8:718. https://doi.org/10.3389/fphys.2017.00718

    Article  Google Scholar 

  116. Rao M, Xia W, Yang J, Hu LX, Hu SF, Lei H, Wu YQ, Zhu CH (2016) Transient scrotal hyperthermia affects human sperm DNA integrity, sperm apoptosis, and sperm protein expression. Andrology 4(6):1054–1063. https://doi.org/10.1111/andr.12228

    Article  CAS  Google Scholar 

  117. Lin PH, Huang KH, Tian YF, Lin CH, Chao CM, Tang LY, Hsieh KL, Chang CP (2021) Exertional heat stroke on fertility, erectile function, and testicular morphology in male rats. Sci Rep 11(1):3539. https://doi.org/10.1038/s41598-021-83121-3

    Article  CAS  Google Scholar 

  118. Garcia-Oliveros LN, de Arruda RP, Batissaco L, Gonzaga VHG, Nogueira VJM, Florez-Rodriguez SA, Almeida FDS, Alves MBR, Pinto SCC, Nichi M, Losano JDA, Kawai GKV, Celeghini ECC (2020) Heat stress effects on bovine sperm cells: a chronological approach to early findings. Int J Biometeorol 64(8):1367–1378. https://doi.org/10.1007/s00484-020-01917-w

    Article  Google Scholar 

  119. Hassun Filho PA (2007) Re: Wet heat exposure: a potentially reversible cause of low semen quality in infertile men. Int Braz J Urol 33(2):269–270. https://doi.org/10.1590/s1677-55382007000200023

    Article  Google Scholar 

  120. Zhou Y, Meng T, Wu L, Duan Y, Li G, Shi C, Zhang H, Peng Z, Fan C, Ma J, Xiong C, Bao W, Liu Y (2020) Association between ambient temperature and semen quality: a longitudinal study of 10 802 men in China. Environ Int 135:105364. https://doi.org/10.1016/j.envint.2019.105364

    Article  Google Scholar 

  121. Mao H, Feng L, Yang WX (2017) Environmental factors contributed to circannual rhythm of semen quality. Chronobiol Int 34(3):411–425. https://doi.org/10.1080/07420528.2017.1280046

    Article  Google Scholar 

  122. Santi D, Magnani E, Michelangeli M, Grassi R, Vecchi B, Pedroni G, Roli L, De Santis MC, Baraldi E, Setti M, Trenti T, Simoni M (2018) Seasonal variation of semen parameters correlates with environmental temperature and air pollution: A big data analysis over 6 years. Environ Pollut 235:806–813. https://doi.org/10.1016/j.envpol.2018.01.021

    Article  CAS  Google Scholar 

  123. Wang X, Tian X, Ye B, Zhang Y, Zhang X, Huang S, Li C, Wu S, Li R, Zou Y, Liao J, Yang J, Ma L (2020) The association between ambient temperature and sperm quality in Wuhan. China Environ Health 19(1):44. https://doi.org/10.1186/s12940-020-00595-w

    Article  CAS  Google Scholar 

  124. Levitas E, Lunenfeld E, Weisz N, Friger M, Har-Vardi I (2013) Seasonal variations of human sperm cells among 6455 semen samples: a plausible explanation of a seasonal birth pattern. Am J Obstet Gynecol 208:406.e1–6. https://doi.org/10.1016/j.ajog.2013.02.010

    Article  Google Scholar 

  125. Santi D, Vezzani S, Granata AR, Roli L, De Santis MC, Ongaro C, Donati F, Baraldi E, Trenti T, Setti M, Simoni M (2016) Sperm quality and environment: A retrospective, cohort study in a Northern province of Italy. Environ Res 150:144–153. https://doi.org/10.1016/j.envres.2016.05.053

    Article  CAS  Google Scholar 

  126. Ilacqua A, Izzo G, Emerenziani GP, Baldari C, Aversa A (2018) Lifestyle and fertility: the influence of stress and quality of life on male fertility. Reprod Biol Endocrinol 16(1):115. https://doi.org/10.1186/s12958-018-0436-9

    Article  CAS  Google Scholar 

  127. Sieber MH, Thomsen MB, Spradling AC (2016) Electron transport chain remodeling by GSK3 during oogenesis connects nutrient state to reproduction. Cell 164(3):420–432. https://doi.org/10.1016/j.cell.2015.12.020

    Article  CAS  Google Scholar 

  128. Wu L, Jin L, Shi T, Zhang B, Zhou Y, Zhou T, Bao W, Xiang H, Zuo Y, Li G, Wang C, Duan Y, Peng Z, Huang X, Zhang H, Xu T, Li Y, Pan X, Xia Y, Gong X, Chen W, Liu Y (2017) Association between ambient particulate matter exposure and semen quality in Wuhan, China. Environ Int 98:219–228. https://doi.org/10.1016/j.envint.2016.11.013

    Article  CAS  Google Scholar 

  129. Radwan M, Jurewicz J, Polańska K, Sobala W, Radwan P, Bochenek M, Hanke W (2016) Exposure to ambient air pollution–does it affect semen quality and the level of reproductive hormones? Ann Hum Biol 43(1):50–56. https://doi.org/10.3109/03014460.2015.1013986

    Article  Google Scholar 

  130. Yang Y, Yang T, Liu S, Cao Z, Zhao Y, Su X, Liao Z, Teng X, Hua J (2019) Concentrated ambient PM2.5 exposure affects mice sperm quality and testosterone biosynthesis. PeerJ 7:e8109. https://doi.org/10.7717/peerj.8109

    Article  CAS  Google Scholar 

  131. Cao XN, Yan C, Liu DY, Peng JP, Chen JJ, Zhou Y, Long CL, He DW, Lin T, Shen LJ, Wei GH (2015) Fine particulate matter leads to reproductive impairment in male rats by overexpressing phosphatidylinositol 3-kinase (PI3K)/protein kinase B (Akt) signaling pathway. Toxicol Lett 237(3):181–190. https://doi.org/10.1016/j.toxlet.2015.06.015

    Article  CAS  Google Scholar 

  132. Rehman H, Ullah I, David M, Ullah A, Jahan S (2019) Neonatal exposure to furan alters the development of reproductive systems in adult male Sprague Dawley rats. Food Chem Toxicol 130:231–241. https://doi.org/10.1016/j.fct.2019.05.020

    Article  CAS  Google Scholar 

  133. Al-Griw MA, Alghazeer RO, Salama NM, Lwaleed BA, Eskandrani AA, Alansari WS, Alnajeebi AM, Babteen NA, Shamlan G, Elnfati AH (2021) Paternal bisphenol A exposure induces testis and sperm pathologies in mice offspring: Possibly due to oxidative stress? Saudi J Biol Sci 28(1):948–955. https://doi.org/10.1016/j.sjbs.2020.11.003

    Article  CAS  Google Scholar 

  134. Lwin TZ, Than AA, Min AZ, Robson MG, Siriwong W (2018) Effects of pesticide exposure on reproductivity of male groundnut farmers in Kyauk Kan village, Nyaung-U, Mandalay region, Myanmar. Risk Manag Healthc Policy 11:235–241. https://doi.org/10.2147/RMHP.S175230

    Article  Google Scholar 

  135. Hossain F, Ali O, D’Souza UJ, Naing DK (2010) Effects of pesticide use on semen quality among farmers in rural areas of Sabah. Malaysia J Occup Health 52(6):353–360. https://doi.org/10.1539/joh.l10006

    Article  CAS  Google Scholar 

  136. Bae JW, Kwon WS (2020) Investigating the effects of fipronil on male fertility: Insight into the mechanism of capacitation. Reprod Toxicol 94:1–7. https://doi.org/10.1016/j.reprotox.2020.04.002

    Article  CAS  Google Scholar 

  137. Dahamna S, Bencheikh F, Harzallah D, Boussahel S, Belgeit A, Merghem M, Bouriche H (2010) Cypermetherin toxic effects on spermatogenesis and male mouse reproductive organs. Commun Agric Appl Biol Sci 75(2):209–216 (PMID: 21542485)

    CAS  Google Scholar 

  138. Amjad S, Rahman MS, Pang WK, Ryu DY, Adegoke EO, Park YJ, Pang MG (2021) Effects of phthalates on the functions and fertility of mouse spermatozoa. Toxicology 454:152746. https://doi.org/10.1016/j.tox.2021.152746

    Article  CAS  Google Scholar 

  139. Sumner RN, Tomlinson M, Craigon J, England G, Lea R (2019) Independent and combined effects of diethylhexyl phthalate and polychlorinated biphenyl 153 on sperm quality in the human and dog. Sci Rep 9:3409. https://doi.org/10.1038/s41598-019-39913-9

    Article  CAS  Google Scholar 

  140. Wang HF, Chang M, Peng TT, Yang Y, Li N, Luo T, Cheng YM, Zhou MZ, Zeng XH, Zheng LP (2017) Exposure to cadmium impairs sperm functions by reducing CatSper in mice. Cell Physiol Biochem 42(1):44–54. https://doi.org/10.1159/000477113

    Article  CAS  Google Scholar 

  141. Heidari AH, Zamiri MJ, Nazem MN, Jafarzadeh Shirazi MR, Akhlaghi A, Ansari Pirsaraei Z (2021) Detrimental effects of long-term exposure to heavy metals on histology, size and trace elements of testes and sperm parameters in Kermani Sheep. Ecotoxicol Environ Saf 207:111563. https://doi.org/10.1016/j.ecoenv.2020.111563

    Article  CAS  Google Scholar 

  142. Zhao J, Zhang Y, Hao L, Wang J, Zhang J, Liu S, Ren B (2010) Effects of a mild heat treatment on mouse testicular gene expression and sperm quality. Anim Cells Syst 14(4):267–274. https://doi.org/10.1080/19768354.2010.525830

    Article  CAS  Google Scholar 

  143. Rizzoto G, Boe-Hansen G, Klein C, Thundathil JC, Kastelic JP (2020) Acute mild heat stress alters gene expression in testes and reduces sperm quality in mice. Theriogenology 158:375–381. https://doi.org/10.1016/j.theriogenology.2020.10.002

    Article  CAS  Google Scholar 

  144. Sales K, Vasudeva R, Dickinson ME, Godwin JL, Lumley AJ, Michalczyk Ł, Hebberecht L, Thomas P, Franco A, Gage MJG (2018) Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect. Nat Commun 9(1):4771. https://doi.org/10.1038/s41467-018-07273-z

    Article  CAS  Google Scholar 

Download references

Acknowledgements

I Thank Amrita Kumar, Dr. Namit Kant Singh, Adhvan Singh and Nutty Singh for their constant support and guidance.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, All India Institute of Medical Sciences, Hyderabad Metropolitan Region, Bibinagar, 508126, Telangana, India

    Naina Kumar

  2. Department of Physiology, U.P. University of Medical Sciences, Saifai, Etawah, Uttar Pradesh, India

    Amit Kant Singh

Authors
  1. Naina Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amit Kant Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NK: Conceptualization, Literature search, Methodology, Analysis of data, Preparation and Final review of manuscript. AKS: literature search, Methodology, Analysis of data, Preparation and Final review of manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Naina Kumar.

Ethics declarations

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors have no competing interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, N., Singh, A.K. Impact of environmental factors on human semen quality and male fertility: a narrative review. Environ Sci Eur 34, 6 (2022). https://doi.org/10.1186/s12302-021-00585-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12302-021-00585-w

Keywords