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Table of Contents
ORIGINAL ARTICLE
Year : 2019  |  Volume : 30  |  Issue : 4  |  Page : 177-183

The impact of the fine ambient particle on infertile male's sperm quality


1 Department of Urology, National Taiwan University Hospital; Department of Surgery, Division of Urology, Cardinal Tien Hospital, Taipei, Taiwan
2 Department of Urology, National Taiwan University Hospital, Taipei, Taiwan
3 Department of Surgery, Division of Urology, Cardinal Tien Hospital; Department of Surgery, Division of Urology, Fu Jen Catholic University Hospital, Taipei, Taiwan
4 Department of Surgery, Division of Urology, Cardinal Tien Hospital, Taipei, Taiwan

Date of Submission02-Feb-2019
Date of Decision08-Mar-2019
Date of Acceptance03-May-2019
Date of Web Publication29-Jul-2019

Correspondence Address:
Hong-Chiang Chang
No- 7, Zhongshang South Road, Department of Urology, National Taiwan University, Taipei City 100
Taiwan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/UROS.UROS_6_19

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  Abstract 


Introduction: Infertility has been a major problem for several years. Previously, infertility was often attributed to female factors. Recently, however, male factors have been found to contribute to 50% of the infertility cases overall. Male infertility is a multifactorial issue. A genetic disorder, abnormal endocrine system, structural anomaly, and environmental causes could lead to male infertility. Studies have revealed a link between fine air particles and decreased fertility. The aim of this study was to discover the effect of particulate matter 2.5 (PM2.5), representing environmental fine particles, on male infertility. Materials and Methods: We retrospectively collected data from patients diagnosed as having infertility and visited National Taiwan University Hospital from January 2015 to October 2017. We recorded each patient's body weight, height, basic blood test, sperm analysis, and sex hormone profile. Air quality data, especially PM2.5 concentration, were acquired from the Environmental Protection Administration of Taiwan. A total of 78 monitoring stations throughout Taiwan record PM2.5 concentrations (μg/m3) each hour automatically. Multivariate linear regression was used to detect independent factors affecting sperm count, concentration, motility, and morphology and sex hormone profile. Results:We observed regional and seasonal differences in the distributions of PM2.5 concentrations. In nearly all cities in Taiwan, the PM2.5 concentrations increased during early winter and continued to increase until next spring, with a peak around January and February. In particular, regional differences were observed in winter. The peak PM2.5 concentrations in southern and northern cities in Taiwan ranged between 35 and 40 μg/m3 and between 18 and 23 μg/m3, respectively. PM2.5 in central Taiwan reached as high as 30 μL/m3. By contrast, the eastern part of Taiwan had the lowest peak PM2.5, which was mostly <15 μg/m3. The average 24-month PM2.5 concentration had a negative effect on sperm count, but the result was nonsignificant. Additionally, the effect of PM2.5 on sperm motility and morphology was minimal. Conclusion: In infertile Taiwanese men, there is a trend of a negative association between exposure to PM2.5 and sperm concentration and total sperm count. Exposure to ambient fine particles, especially PM2.5, might have a negative correlation with sperm quality, sex hormone balance, and the testicular microenvironment through different mechanisms.

Keywords: Air pollution, infertility, particulate matter 2.5, sperm quality


How to cite this article:
Chen Y, Chang HC, Liao CH, Chiang BJ, Chang YK. The impact of the fine ambient particle on infertile male's sperm quality. Urol Sci 2019;30:177-83

How to cite this URL:
Chen Y, Chang HC, Liao CH, Chiang BJ, Chang YK. The impact of the fine ambient particle on infertile male's sperm quality. Urol Sci [serial online] 2019 [cited 2019 Oct 13];30:177-83. Available from: http://www.e-urol-sci.com/text.asp?2019/30/4/177/263652




  Introduction Top


Infertility is a distressing problem that has been a concern for several years. Despite advancements in novel technology for fertility, infertility is still a major clinical problem faced not only by patients but also by doctors.

According to statistics, 9%–15% of couples are affected by infertility.[1],[2] Previously, female factors were thought to contribute to most cases of infertility. Nonetheless, the rate of infertility is complicated by the will to conceive and the use of contraception. Moreover, female factors are somewhat overemphasized. In particular, in patriarchal societies, women are often blamed for infertility, whereas their male partners rarely resort to medical advice.

A meta-analysis in 2015 showed that male factors contributed to 50% of infertility cases overall.[3] Many factors play a role in male infertility, including poor sperm quality, chromosomal errors, lifestyle and habits (constituting environmental factors), and hypogonadism.[4],[5] Nonetheless, sperm quality is almost always the first item assessed in a male with fecundity, and male infertility is commonly attributed to abnormal semen quality. In certain instances, semen parameters may serve as the measurement tool for male fertility.[6] Aberrant chromosomes, hypogonadism, and environmental factors could lead to poor spermatogenesis. With industrialization and the accompanying pollution, environmental factors are attracting increasing attention.[7],[8],[9],[10]

Particulate matter 2.5 (PM2.5), referring to fine air particles with a diameter of <2.5 μm, can enter the respiratory system and lodge in different organ systems; PM2.5 has thus become a major health concern.[11] PM2.5 has been linked to many diseases, including cancers, cardiovascular disease, and pulmonary diseases; it also increases humans' vulnerability to infection.[12],[13],[14],[15] In addition to causing subtle molecular alterations, which contribute to the vulnerability to the aforementioned diseases, the link between air pollution and fertility rates has also been reported. According to US birth statistics, the birth rate had dropped from 120 (per 1000 women aged 15–44 years) in the 1960s to 60 (per 1000 women aged 15–44 years) in 2013. In the past 3 years, the rate declined by 1% annually.[16] Nieuwenhuijsen et al. discovered an association between traffic-related air pollution and a decrease in fertility rates.[17] Moreover, a systematic review showed a negative effect of air pollution on pregnancy rate and successful implantation rate (in vitro fertilization).[18] Nonetheless, a decreased pregnancy rate may be a result of either impaired male or impaired female fecundity or both.

A few theories have been proposed to explain the possible detrimental effects of fine ambient particles on male infertility. First, PM2.5 may have negative impact on sperm maturation which was seen in murine models. Fewer mature sperms were observed in the testes of male mice after exposure to fine ambient particles. Second, testicular biopsy of male mice revealed structural changes including the disruption of tight junction and blood–testes barrier.[19] Third, PM2.5 could cause increased oxidative stress in the gonad, which was illustrated by altered expression levels of pro-inflammatory cytokine genes.[20],[21]

The current study focused on the effect of air pollution, as measured by the concentration of PM2.5, on semen quality and sex hormone profiles in infertile male individuals.


  Materials and Methods Top


We retrospectively collected data from patients diagnosed as having infertility, which was defined as an inability to conceive under unprotected sexual encounter in 12 months or longer, as defined by the World Health Organization.[6] We visited National Taiwan University Hospital from January 2015 to October 2017 for data collection. Body weight, height, basic blood test, sperm analysis, and sex hormone profiles were examined at the clinic. In addition, age and smoking status were recorded.

If a patient had undergone >1 semen analysis or had >1 clinical visit, the first data collected before any treatment were recorded and analyzed. Patients who were found to have aberrant chromosomes, received previous chemotherapy/radiotherapy due to malignancy, or had undergone bone marrow transplantation were excluded. Patients who were diagnosed as having obstructive azoospermia – which is the absence of bilateral vas deferens – or had received vasectomies or orchiectomy were also excluded.

Semen analysis was performed by an experienced team. Patients were asked for abstinence for 3–5 days. Subsequently, sperm samples were collected from the patients by masturbation and then sent to our laboratory within 2 h of collection. Microscopic examination was then performed to record semen volume, sperm concentration, and sperm morphology.

Particulate matter 2.5 concentration acquisition

Data were acquired from the Environmental Protection Administration of Taiwan. PM2.5 concentrations (μg/m 3) are automatically recorded at 78 monitoring stations throughout Taiwan. The data collected from the stations are recorded by equipment that automatically analyzes PM2.5 concentrations. The measures were previously validated by manually checking concentrations using linear regression. Data are collected at the monitoring stations hourly. In this study, individual exposure to air pollution was estimated by the current residential addresses reported by the study participants and the mean concentrations of air pollutants in the study period (2016 January to 2017 December).

Statistical analysis

Statistical analysis was performed using SPSS Version 12 (SPSS Inc., Chicago, IL, USA).

Multivariate linear regression was used to detect independent factors for sperm count, concentration, motility, and morphology. Smoking habit and medical comorbidity, including obesity and the status of varicocele were adjusted in the multivariate regression model.

Varicocele was graded from 1 to 3. Grade 1: The varicose vein was palpable when the patient performs a Valsalva maneuver. Grade 2: Palpable with the patient standing, without a Valsalva maneuver. Grade 3: Visible through scrotal skin, with grade 0 denoting no varicocele.

Multivariate linear regression analysis was conducted for independent risk factors for sex hormone profile. The level of significance was set at P < 0.05.


  Results Top


Patient distribution

A total of 283 patients were included in the final analysis. Their mean age (standard deviation) was 36.96 (7.34) years [Table 1]. The sperm parameters were within the normal range, with the sperm concentration and total sperm count being in the lower quartile of the reference range. The mean body mass index (BMI) was 24.83, indicating that more than half of the patients were overweight according to the Taiwanese definition.[22] Moreover, 264 (93.3%) patients lived in northern Taiwan; 3.2%, 2.5%, and 1.4% of the patients were from central, southern, and eastern and other parts of Taiwan, respectively. To the best of our knowledge, after enrolling in the study, 5 patients received in vitro fertilization and 2 received medication, but whether the others received medication or treatment was unknown.
Table 1: Baseline characteristics of study population (n=283)

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Particulate matter 2.5 seasonal and regional distributions

We acquired PM2.5 data from the Environmental Protection Administration of Taiwan (https://www.epa.gov.tw/). The distributions of PM2.5 concentrations were regionally and seasonally different [Figure 1] and [Figure 2]. In most cities in Taiwan, the PM2.5 concentrations were highest from early winter to next spring, with a peak concentration between January and February. Regional difference was generally observed during winter. During winter, the highest concentrations of PM2.5 for cities in southwestern, northern, and central Taiwan were 35–40, 18–23, and 30 μg/m 3, respectively. The eastern part of Taiwan had the lowest concentration of PM2.5, which was in general <15 μL/m 3 (pic 1–5). During summer, however, no significant difference in PM2.5 concentration was noted. Nearly all cities in Taiwan had concentrations between 5 and 15 μg/m 3. We calculated the average concentration of PM2.5 from January 2016 to December 2017.
Figure 1: Particulate matter 2.5 concentration (μg/m3) in Taiwan from January 2016 to December 2017

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Figure 2: Distributions of particulate matter 2.5 concentration in a: January 2016; b: July 2016; c: January 2017; and d: July 2017

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Multivariable linear regression was conducted to identify the contributing factors to sperm quality and sex hormone profile, with PM2.5 being one of the independent variables [Table 3],[Table 4] and [Table 5].
Table 3: Multivariable linear regression analysis for serum testosterone

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Table 4: Multivariable linear regression analysis for serum follicle-stimulating hormone

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Table 5: Multivariable linear regression analysis for serum-luteinizing hormone

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The average 24-month PM2.5 concentration had a negative effect on the sperm count and sperm concentration; however, this result was nonsignificant. The effect of PM2.5 on sperm motility and morphology was minimal [Table 2] and [Table 3]. In addition, BMI was observed to be an independent factor predicting lower total sperm count (P = 0.042) and lower serum testosterone (P < 0.01) in infertile Taiwanese men.
Table 2: Multivariable linear regression analysis for total sperm parameters

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  Discussion Top


In our study, we found a negative, although nonsignificant, association between the average 24-month PM2.5 concentration and sperm concentration, motility, and morphology. We adjusted for age, BMI, status of varicocele, smoking habit, and blood glucose, which may serve as confounders.

Some large observational studies have shown that ambient particles are negatively associated with fertility rate. Using country-level satellite remote sensing to detect PM2.5 concentrations in China, Xue and Zhang observed a 2% decrease in fertility rate when the PM2.5 concentration was increased by 10 μg/m 3, after adjusting for socioeconomic factors.[23] In Spain, Nieuwenhuijsen et al. reported a negative correlation between estimated air pollutant concentrations, including NO2 and NOx, and the fertility rate of women aged between 15 and 44 years.[17] Similarly, Mahalingaiah et al. demonstrated an association between lowered female fertility and air pollution (hazard ratio = 1.11; 95% confidence interval [CI]: 1.02, 1.20).[24]

In addition to affecting women's ability to conceive, fine particles have been revealed to be associated with alterations in semen quality in the general male population.[9],[25],[26],[27] Although existing results are still inconsistent and no consensus has been reached, Lao et al. reported that a 5 μg/m 3 increase in the average 24-month PM2.5 concentration was associated with a significant 1.29% decrease in normal sperm morphology and a 26% increased risk of being in the worst 10% of sperm morphology. However, a 5 μg/m 3 increase in PM2.5 was found to be associated with a 1.03 × 106/mL increase in sperm concentration.[27] By contrast, Li reported a negative correlation between PM2.5 exposure and sperm count and sperm concentration in Wuhan, China. Another study revealed that sperm motility was not significantly affected by PM2.5, but the semen morphology was not recorded.[26] Hammoud et al. found a negative correlation between the concentration of PM2.5 and sperm motility in Salt Lake City.[28]

Although some studies have reported a negative effect of PM2.5 on sperm parameters, Santi et al. reported a positive correlation between PM2.5 and sperm count and sperm volume in Italy.[29] Zhou et al. also reported a positive correlation of PM10 with sperm concentration, motility, and morphology; however, only sperm concentration showed a significant positive correlation with PM 10 (β = 0.075; 95% CI: 0.021, 0.109). By contrast, Hansen et al. conducted a study on 228 fertile male individuals and found that air pollution was not correlated with sperm concentration, count, and morphology.[25],[30]

Possible explanations for these inconsistent results are as follows:First, the studies may have involved selection bias for the study populations. In one of the aforementioned studies, most semen samples were obtained from male volunteers, most of whom may be fertile, which compromised the chances of detecting the effect of PM2.5 on sperm parameters. However, our study population comprised male individuals diagnosed as having infertility, which was different from that of the previous cross-sectional study. Due to a small patient number and the inability to follow up patients, the observed effect of PM2.5 on sperm parameters may not be significant. Second, the seasonal variations in temperature and humidity were found to be associated with sperm quality.[31] A 6-year observational study conducted by Santi et al. reported that both maximum and minimum temperatures were inversely correlated with sperm count, motility, and morphology. Moreover, the length of daytime was negatively correlated with sperm count, signifying that in summer, the sperm count may be lower. In our study, we could not adjust for the effects of temperature and daytime on sperm profile. Third, sperm development is a 3-month process; therefore, an average 24-month PM2.5 exposure may not ideally reflect the effect of the ambient fine particles on spermatogenesis.

Ambient PM2.5 was shown to decrease fertility rate.[17] However, the correlation between PM2.5 and sperm quality is still under investigation, with some studies suggesting a positive correlation and others indicating negative correlation. PM2.5 may affect human fertility through other mechanisms, not by merely compromising semen quality, in terms of altered concentration, motility, or morphology.

In murine models, Pires et al. reported a decrease in spermatogenesis; through testicular biopsy, they also observed less mature sperm cells after prenatal or postnatal exposure to air pollutants, particularly PM2.5.[20] Qiu et al. exposed male mice to an environment with concentrated PM2.5 for 4 months. Although they observed no marked structural change in seminiferous tubule biopsy, they reported Sertoli cell vacuolization and derangement. Moreover, after a long-term exposure to PM2.5, the number of normal forms was reduced, and the average number of spermatocytes was not significantly reduced. This observation suggests that exposure to PM2.5 may affect germ cells at the microbiological level, with an alteration of testicular biochemistry.[21]

In addition to microstructural changes in the gonads, an inflammatory response can be triggered by exposure to fine ambient particles. Exposing mice to a high concentration of PM2.5 through intratracheal injection resulted in spermatocytes with decreased viability, a higher level of lactate dehydrogenase, and impaired mitochondrial structure and adenosine triphosphate production. Furthermore, reactive oxygen species (ROS)-induced cell cycle arrest and inhibition of cell proliferation have been observed.[19],[20],[32] Qiu et al. reported that after long-term exposure to PM2.5 in a murine model, the expression of tumor necrosis factor alpha and interleukin-1 beta mRNA increased and that of GnRH mRNA decreased in the hypothalamus; this demonstrates the existence of a pro-inflammatory state in the hypothalamus–pituitary axis triggered by the fine ambient particles. Consequently, decreases in serum follicle-stimulating hormone (FSH) and testosterone levels were observed. PM2.5 affects male fertility by affecting both sperm quality and the balance between the hypothalamus–pituitary axis and endocrine system.[21]

In our multivariable linear regression model, when serum testosterone served as the dependent variable, PM2.5 exposure was negatively correlated with sex hormone profiles, which is consistent with the finding of Qiu et al.[21] Higher BMI was the only significant factor predicting low serum testosterone, which has already been demonstrated in previous studies and is thus not discussed further herein.[33],[34]

Possible explanations for the nonsignificant effect of PM2.5 on serum sex hormone profile, which is inconsistent with the finding of Qiu et al., are outlined as follows: first, murine responses to PM2.5 could be different from those of humans. Second, because our study was retrospective, we could not follow up the patients who had a heavy exposure to fine ambient particles to evaluate the long-term effects of PM2.5 on hormones. If those patients were followed up for a longer period, lower serum FSH and testosterone levels may be observed. A future study including a longer follow-up period and considering patients' GnRH levels may be conducted to evaluate the long-term effect of PM2.5 on sex hormone profile.

The blood–testis barrier (BTB) serves as both a barrier against exogenous toxins and a barrier for preventing immunological disruption in the testicular microenvironment.[35] In murine models, increased exposure to PM2.5 resulted in decreased tight junction, adherent junction, and gap junction proteins in testicular tissues, which were regulated by the TGF-β3 and p38 MAPK cascade.[19],[36],[37],[38] The connection between exposure to PM2.5 and the decreased expression of tight-junction and gap-junction proteins may be explained by elevations of autophagy activity. Wei et al. reported an increase in the number of autophagosomes and the levels of autophagy markers Microtubule-associated protein 1A/1B-light chain 3 (LC3)-II and p62, suggesting that altered autophagy activity may play a role in decreased tight-junction and gap-junction expression.

Additionally, exposure to PM2.5, even in low dose, could result in increased oxidative stress in the testicular microenvironment. Wei et al. reported a decrease in superoxide dismutase (SOD), which is one of the most important enzymes protecting cells from ROS. Furthermore, an increase in heme oxygenase (HO) was observed. HO plays a role in metabolizing ROS, serving as an indicator of oxidative stress. In addition, marked altered expression levels of SOD and HO-1 have been observed in mouse testicular biopsy.[19],[35] Notably, administration of Vitamin C and Vitamin E could neutralize the harmful effects of ambient particles, reversing the altered expression of oxidative markers. Altogether, PM2.5 and fine ambient particles could compromise male infertility by not only reducing sperm quality but also altering the testicular microenvironment, including induction of oxidative stress, elevation of pro-inflammatory cytokines, and disruption of the BTB.

Our study was limited by several aspects. First, our study was retrospective in design; we had a relatively small study population, and some data were missing. Therefore, the statistical power to detect the effect of PM2.5 on sperm quality and sex hormone profile may be weakened. Furthermore, selection bias was inevitable. Because our center is located in Taipei, most of our patients were also located in northern Taiwan. To recruit more patients from the other parts of Taiwan and strengthen our study results, future cross-institute research is recommended. Second, although we recorded the patients' residential addresses, they may not reside at the addresses provided or may have traveled around the country and exposed themselves to different levels of PM2.5, which may be a confounder. Third, it was difficult to record whether patients had fathered a child, because patients were frequently lost to follow-up when their partners became pregnant. Therefore, we could not translate sperm quality into clinical outcome. Nevertheless, this is the first study focusing on the effect of PM2.5 on infertile men. The results from the multivariable linear regression analysis show that PM2.5 has a negative effect on semen concentration and total sperm count. A larger prospective study may be conducted in the future to further establish the correlations between ambient fine particles and sperm quality, sex hormone profile, and male infertility.


  Conclusion Top


In infertile Taiwanese men, there is a trend of a negative association between exposure to PM2.5 and sperm concentration and total sperm count. Exposure to ambient fine particles, particularly PM2.5, may be negatively correlated with sperm quality, sex hormone balance, and the testicular microenvironment through different mechanisms.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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