Key Points
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Downward trends in sperm concentrations have been described in several geographical areas during this century
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In several countries, sperm concentration of a considerable proportion of young men has been described to be on a level that has been associated with prolonged time to pregnancy
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Longitudinal studies suggest that almost full sperm production capacity is achieved around the age of 20 years, which points to the importance of earlier developmental phases in establishment of spermatogenic capacity
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Environmental factors are likely to have contributed to the declining trends in sperm concentrations; however, identifying the most important factors causing adverse effects remains a challenge
Abstract
Although semen quality is an important determinant of fertility, defining clear thresholds for normal ranges has proven difficult. According to 'time to pregnancy' studies, fecundity starts to decline when sperm concentrations fall below 30–55 × 106/ml, whereas the WHO criterion for normal values is currently 15 × 106/ml. Multiple studies over the past 15 years have reported median sperm concentrations of 41–55 × 106/ml in young men (mean age 18–21 years) from the general population, suggesting that many of them have suboptimal semen quality. Sperm numbers remain fairly constant between 19 and 29 years of age, which points to the importance of developmental effects. Discussion on whether population semen quality has declined has continued for decades, as regional differences in trends have been noted. The reasons for poor semen quality and adverse trends are not well established, but some associations suggest a causal relationship, for example, with maternal smoking during pregnancy. The role of chemical exposures leading to endocrine disruption and detrimental reproductive effects has been in the focus of research during the past 20 years. Identification of exposures that affect fertility could provide opportunities for effective prevention of reproductive health problems.
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References
Mendiola, J. et al. Sperm counts may have declined in young university students in southern Spain. Andrology 1, 408–413 (2013).
Jørgensen, N. et al. Recent adverse trends in semen quality and testis cancer incidence among Finnish men. Int. J. Androl. 34, e37–48 (2011).
Lackner, J. et al. Constant decline in sperm concentration in infertile males in an urban population: experience over 18 years. Fertil. Steril. 84, 1657–1661 (2005).
Sripada, S. et al. Trends in semen parameters in the northeast of Scotland. J. Androl. 28, 313–319 (2007).
Feki, N. C. et al. Semen quality decline among men in infertile relationships: experience over 12 years in the south of Tunisia. J. Androl. 30, 541–547 (2009).
Geoffroy-Siraudin, C. et al. Decline of semen quality among 10 932 males consulting for couple infertility over a 20-year period in Marseille, France. Asian J. Androl. 14, 584–590 (2012).
Rolland, M., Le Moal, J., Wagner, V., Royère, D. & De Mouzon, J. Decline in semen concentration and morphology in a sample of 26,609 men close to general population between 1989 and 2005 in France. Hum. Reprod. 28, 462–470 (2013).
Adiga, S. K., Jayaraman, V., Kalthur, G., Upadhya, D. & Kumar, P. Declining semen quality among south Indian infertile men: a retrospective study. J. Hum. Reprod. Sci. 1, 15–18 (2008).
Romero-Otero, J. et al. Semen quality assessment in fertile men in Madrid during the last 3 decades. Urology 85, 1333–1338 (2015).
Jiang, M. et al. Semen quality evaluation in a cohort of 28213 adult males from Sichuan area of south-west China. Andrologia 46, 842–847 (2014).
Haimov-Kochman, R. et al. Is the quality of donated semen deteriorating? Findings from a 15 year longitudinal analysis of weekly sperm samples. Isr. Med. Assoc. J. 14, 372–377 (2012).
Rao, M. et al. Evaluation of semen quality in 1808 university students, from Wuhan, central China. Asian J. Androl. 17, 111–116 (2015).
Wang, L. et al. Decline of semen quality among Chinese sperm bank donors within 7 years (2008–2014). Asian J. Androl. http://dx.doi.org/10.4103/1008-682X.179533 (2016).
Shine, R., Peek, J. & Birdsall, M. Declining sperm quality in New Zealand over 20 years. N. Z. Med. J. 121, 50–56 (2008).
Splingart, C. et al. Semen variation in a population of fertile donors: evaluation in a French centre over a 34-year period. Int. J. Androl. 35, 467–474 (2012).
Centola, G. M., Blanchard, A., Demick, J., Li, S. & Eisenberg, M. L. Decline in sperm count and motility in young adult men from 2003 to 2013: observations from a U. S. sperm bank. Andrology 4, 270–276 (2016).
Huang, C. et al. Decline in semen quality among 30,636 young Chinese men from 2001 to 2015. Fertil. Steril. http://dx.doi.org/10.1016/j.fertnstert.2016.09.035 (2016).
Chen, Z. et al. Temporal trends in human semen parameters in New England in the United States, 1989–2000. Arch. Androl. 49, 369–374 (2003).
Axelsson, J., Rylander, L., Rignell-Hydbom, A. & Giwercman, A. No secular trend over the last decade in sperm counts among Swedish men from the general population. Hum. Reprod. 26, 1012–1016 (2011).
Jørgensen, N. et al. Human semen quality in the new millennium: a prospective cross-sectional population-based study of 4867 men. BMJ Open 2, e000990 (2012).
Costello, M. F., Sjoblom, P., Haddad, Y., Steigrad, S. J. & Bosch, E. G. No decline in semen quality among potential sperm donors in Sydney, Australia, between 1983 and 2001. J. Assist. Reprod. Genet. 19, 284–290 (2002).
Mukhopadhyay, D. et al. Semen quality and age-specific changes: a study between two decades on 3,729 male partners of couples with normal sperm count and attending an andrology laboratory for infertility-related problems in an Indian city. Fertil. Steril. 93, 2247–2254 (2010).
Marimuthu, P., Kapilashrami, M. C., Misro, M. M. & Singh, G. Evaluation of trend in semen analysis for 11 years in subjects attending a fertility clinic in India. Asian J. Androl. 5, 221–225 (2003).
Birdsall, M. A., Peek, J. & Valiapan, S. Sperm quality in New Zealand: is the downward trend continuing? N. Z. Med. J. 128, 50–56 (2015).
Johnson, S. L., Dunleavy, J., Gemmell, N. J. & Nakagawa, S. Consistent age-dependent declines in human semen quality: a systematic review and meta-analysis. Ageing Res. Rev. 19, 22–33 (2015).
Jørgensen, N. et al. Regional differences in semen quality in Europe. Hum. Reprod. 16, 1012–1019 (2001).
Jørgensen, N. et al. East-West gradient in semen quality in the Nordic-Baltic area: a study of men from the general population in Denmark, Norway, Estonia and Finland. Hum. Reprod. 17, 2199–2208 (2002).
Richthoff, J., Rylander, L., Hagmar, L., Malm, J. & Giwercman, A. Higher sperm counts in southern Sweden compared with Denmark. Hum. Reprod. 17, 2468–2473 (2002).
Andersen, A. G. et al. High frequency of sub-optimal semen quality in an unselected population of young men. Hum. Reprod. 15, 366–372 (2000).
Punab, M. et al. Regional differences in semen qualities in the Baltic region. Int. J. Androl. 25, 243–252 (2002).
Tsarev, I., Gagonin, V., Giwercman, A. & Erenpreiss, J. Sperm concentration in Latvian military conscripts as compared with other countries in the Nordic-Baltic area. Int. J. Androl. 28, 208–214 (2005).
Fernandez, M. F. et al. Semen quality and reproductive hormone levels in men from southern Spain. Int. J. Androl. 35, 1–10 (2012).
Iwamoto, T. et al. Semen quality of 1559 young men from four cities in Japan: a cross-sectional population-based study. BMJ Open 3, e002222 (2013).
Paasch, U. et al. Semen quality in sub-fertile range for a significant proportion of young men from the general German population: a co-ordinated, controlled study of 791 men from Hamburg and Leipzig. Int. J. Androl. 31, 93–102 (2008).
Halling, J. et al. Semen quality and reproductive hormones in Faroese men: a cross-sectional population-based study of 481 men. BMJ Open 3, e001946 (2013).
Mendiola, J. et al. Reproductive parameters in young men living in Rochester, New York. Fertil. Steril. 101, 1064–1071 (2014).
Hart, R. J. et al. Testicular function in a birth cohort of young men. Hum. Reprod. 30, 2713–2724 (2015).
Perheentupa, A. et al. Semen quality improves marginally during young adulthood: a longitudinal follow-up study. Hum. Reprod. 31, 502–510 (2016).
Carlsen, E., Swan, S. H., Petersen, J. H. & Skakkebaek, N. E. Longitudinal changes in semen parameters in young Danish men from the Copenhagen area. Hum. Reprod. 20, 942–949 (2005).
Swan, S. H. et al. Geographic differences in semen quality of fertile U. S. males. Environ. Health Perspect. 111, 414–420 (2003).
Redmon, J. B. et al. Semen parameters in fertile US men: the Study for Future Families. Andrology 1, 806–814 (2013).
Swan, S. H. et al. Semen quality in relation to biomarkers of pesticide exposure. Environ. Health Perspect. 111, 1478–1484 (2003).
Iwamoto, T. et al. Semen quality of 324 fertile Japanese men. Hum. Reprod. 21, 760–765 (2006).
Iwamoto, T. et al. Semen quality of fertile Japanese men: a cross-sectional population-based study of 792 men. BMJ Open 3, e002223 (2013).
Stewart, T. M. et al. Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output. Hum. Reprod. 24, 1561–1568 (2009).
Haugen, T. B., Egeland, T. & Magnus, O. Semen parameters in Norwegian fertile men. J. Androl. 27, 66–71 (2006).
Skakkebaek, N. E., Rajpert-De Meyts, E. & Main, K. M. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum. Reprod. 16, 972–978 (2001).
Skakkebaek, N. E. et al. Male reproductive disorders and fertility trends: influences of environment and genetic susceptibility. Physiol. Rev. 96, 55–97 (2016).
Vine, M. F., Margolin, B. H., Morrison, H. I. & Hulka, B. S. Cigarette smoking and sperm density: a meta-analysis. Fertil. Steril. 61, 35–43 (1994).
Li, Y., Lin, H. & Cao, J. Association between socio-psycho-behavioral factors and male semen quality: systematic review and meta-analyses. Fertil. Steril. 95, 116–123 (2011).
Sharma, R., Harlev, A., Agarwal, A. & Esteves, S. C. Cigarette smoking and semen quality: a new meta-analysis examining the effect of the 2010 World Health Organization laboratory methods for the examination of human semen. Eur. Urol. 70, 635–645 (2016).
Rubes, J. et al. Smoking cigarettes is associated with increased sperm disomy in teenage men. Fertil. Steril. 70, 715–723 (1998).
Taha, E. A., Ez-Aldin, A. M., Sayed, S. K., Ghandour, N. M. & Mostafa, T. Effect of smoking on sperm vitality, DNA integrity, seminal oxidative stress, zinc in fertile men. Urology 80, 822–825 (2012).
Robbins, W. A. et al. Effect of lifestyle exposures on sperm aneuploidy. Cytogenet. Genome Res. 111, 371–377 (2005).
Storgaard, L. et al. Does smoking during pregnancy affect sons' sperm counts? Epidemiology 14, 278–286 (2003).
Jensen, T. K. et al. Association of in utero exposure to maternal smoking with reduced semen quality and testis size in adulthood: a cross-sectional study of 1,770 young men from the general population in five European countries. Am. J. Epidemiol. 159, 49–58 (2004).
Jensen, M. S., Mabeck, L. M., Toft, G., Thulstrup, A. M. & Bonde, J. P. Lower sperm counts following prenatal tobacco exposure. Hum. Reprod. 20, 2559–2566 (2005).
Ramlau-Hansen, C. H. et al. Is prenatal exposure to tobacco smoking a cause of poor semen quality? A follow-up study. Am. J. Epidemiol. 165, 1372–1379 (2007).
Ravnborg, T. L. et al. Prenatal and adult exposures to smoking are associated with adverse effects on reproductive hormones, semen quality, final height and body mass index. Hum. Reprod. 26, 1000–1011 (2011).
Virtanen, H. E., Sadov, S. & Toppari, J. Prenatal exposure to smoking and male reproductive health. Curr. Opin. Endocrinol. Diabetes Obes. 19, 228–232 (2012).
Gundersen, T. D. et al. Association between use of marijuana and male reproductive hormones and semen quality: a study among 1,215 healthy young men. Am. J. Epidemiol. 182, 473–481 (2015).
Dai, J. B., Wang, Z. X. & Qiao, Z. D. The hazardous effects of tobacco smoking on male fertility. Asian J. Androl. 17, 954–960 (2015).
Jensen, T. K. et al. Alcohol and male reproductive health: a cross-sectional study of 8344 healthy men from Europe and the USA. Hum. Reprod. 29, 1801–1809 (2014).
Jensen, T. K. et al. Habitual alcohol consumption associated with reduced semen quality and changes in reproductive hormones; a cross-sectional study among 1221 young Danish men. BMJ Open 4, e005462 (2014).
Pajarinen, J. et al. Moderate alcohol consumption and disorders of human spermatogenesis. Alcohol Clin. Exp. Res. 20, 332–337 (1996).
Ramlau-Hansen, C. H. et al. Maternal alcohol consumption during pregnancy and semen quality in the male offspring: two decades of follow-up. Hum. Reprod. 25, 2340–2345 (2010).
Anifandis, G. et al. The impact of cigarette smoking and alcohol consumption on sperm parameters and sperm DNA fragmentation (SDF) measured by Halosperm(®). Arch. Gynecol. Obstet. 290, 777–782 (2014).
Martini, A. C. et al. Effects of alcohol and cigarette consumption on human seminal quality. Fertil. Steril. 82, 374–377 (2004).
WHO. Obesity. Situation and trends. Global Health Observatory (GHO) data [online], http://www.who.int/gho/ncd/risk_factors/obesity_text/en/ (2016).
Sermondade, N. et al. BMI in relation to sperm count: an updated systematic review and collaborative meta-analysis. Hum. Reprod. Update 19, 221–231 (2013).
Macdonald, A. A., Stewart, A. W. & Farquhar, C. M. Body mass index in relation to semen quality and reproductive hormones in New Zealand men: a cross-sectional study in fertility clinics. Hum. Reprod. 28, 3178–3187 (2013).
Eisenberg, M. L. et al. The relationship between male BMI and waist circumference on semen quality: data from the LIFE study. Hum. Reprod. 29, 193–200 (2014).
Tsao, C. W. et al. Exploration of the association between obesity and semen quality in a 7630 male population. PLoS ONE 10, e0119458 (2015).
Andersen, J. M. et al. Body mass index is associated with impaired semen characteristics and reduced levels of anti-Müllerian hormone across a wide weight range. PLoS ONE 10, e0130210 (2015).
Belloc, S. et al. High body mass index has a deleterious effect on semen parameters except morphology: results from a large cohort study. Fertil. Steril. 102, 1268–1273 (2014).
Ehala-Aleksejev, K. & Punab, M. The different surrogate measures of adiposity in relation to semen quality and serum reproductive hormone levels among Estonian fertile men. Andrology 3, 225–234 (2015).
Lu, J. C. et al. Body mass index, waist-to-hip ratio, waist circumference and waist-to-height ratio cannot predict male semen quality: a report of 1231 subfertile Chinese men. Andrologia 47, 1047–1054 (2015).
Nordkap, L. et al. Psychological stress and testicular function: a cross-sectional study of 1,215 Danish men. Fertil. Steril. 105, 174–187.e2 (2016).
Janevic, T. et al. Effects of work and life stress on semen quality. Fertil. Steril. 102, 530–538 (2014).
Li, Y. et al. Socio-psycho-behavioural factors associated with male semen quality in China: results from 1346 healthy men in Chongqing. J. Fam. Plann. Reprod. Health Care 39, 102–110 (2013).
Mojtabai, R. & Jorm, A. F. Trends in psychological distress, depressive episodes and mental health treatment-seeking in the United States: 2001–2012. J. Affect. Disord. 174, 556–561 (2015).
Bergman, Å., Heindel, J., Jobling, S., Kidd, K. & Zoeller, R. State of the science of endocrine disrupting chemicals 2012. (United Nations Environment Programme and the World Health Organization, 2013).
Gore, A. C. et al. EDC-2: the Endocrine Society's second scientific statement on endocrine-disrupting chemicals. Endocr. Rev. 36, E1–E150 (2015).
Vested, A., Giwercman, A., Bonde, J. P. & Toft, G. Persistent organic pollutants and male reproductive health. Asian J. Androl. 16, 71–80 (2014).
Guo, Y. L., Hsu, P. C., Hsu, C. C. & Lambert, G. H. Semen quality after prenatal exposure to polychlorinated biphenyls and dibenzofurans. Lancet 356, 1240–1241 (2000).
Mocarelli, P. et al. Perinatal exposure to low doses of dioxin can permanently impair human semen quality. Environ. Health Perspect. 119, 713–718 (2011).
Mocarelli, P. et al. Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality. Environ. Health Perspect. 116, 70–77 (2008).
Vested, A. et al. Associations of in utero exposure to perfluorinated alkyl acids with human semen quality and reproductive hormones in adult men. Environ. Health Perspect. 121, 453–458 (2013).
Vested, A. et al. In utero exposure to persistent organochlorine pollutants and reproductive health in the human male. Reproduction 148, 635–646 (2014).
Buck Louis, G. M. et al. Persistent environmental pollutants and couple fecundity: the LIFE study. Environ. Health Perspect. 121, 231–236 (2013).
Axelsson, J. et al. Prenatal phthalate exposure and reproductive function in young men. Environ. Res. 138, 264–270 (2015).
Cai, H. et al. Human urinary/seminal phthalates or their metabolite levels and semen quality: a meta-analysis. Environ. Res. 142, 486–494 (2015).
Phthalate exposure and reproductive parameters in young men from the general Swedish population. Environ. Int. 85, 54–60 (2015).
Thurston, S. W. et al. Phthalate exposure and semen quality in fertile US men. Andrology 4, 623–628 (2016).
Mínguez-Alarcón, L., Hauser, R. & Gaskins, A. J. Effects of bisphenol A on male and couple reproductive health: a review. Fertil. Steril. 106, 864–870 (2016).
Christiansen, S. et al. Synergistic disruption of external male sex organ development by a mixture of four antiandrogens. Environ. Health Perspect. 117, 1839–1846 (2009).
Rider, C. V., Furr, J. R., Wilson, V. S. & Gray, L. E. J. Cumulative effects of in utero administration of mixtures of reproductive toxicants that disrupt common target tissues via diverse mechanisms of toxicity. Int. J. Androl. 33, 443–462 (2010).
Dama, M. S. & Bhat, M. N. Mobile phones affect multiple sperm quality traits: a meta-analysis. F1000Res 2, 40 (2013).
Adams, J. A., Galloway, T. S., Mondal, D., Esteves, S. C. & Mathews, F. Effect of mobile telephones on sperm quality: a systematic review and meta-analysis. Environ. Int. 70, 106–112 (2014).
Liu, K. et al. Association between mobile phone use and semen quality: a systemic review and meta-analysis. Andrology 2, 491–501 (2014).
NTP. Cell phones. National Toxicology Program [online], https://ntp.niehs.nih.gov/results/areas/cellphones/ (2016).
Avendaño, C., Mata, A., Sanchez Sarmiento, C. A. & Doncel, G. F. Use of laptop computers connected to internet through Wi-Fi decreases human sperm motility and increases sperm DNA fragmentation. Fertil. Steril. 97, 39–45.e32 (2012).
Guzick, D. S. et al. Sperm morphology, motility, and concentration in fertile and infertile men. N. Engl. J. Med. 345, 1388–1393 (2001).
Bonde, J. P. et al. Relation between semen quality and fertility: a population-based study of 430 first-pregnancy planners. Lancet 352, 1172–1177 (1998).
Menkveld, R., Stander, F. S., Kotze, T. J., Kruger, T. F. & van Zyl, J. A. The evaluation of morphological characteristics of human spermatozoa according to stricter criteria. Hum. Reprod. 5, 586–592 (1990).
Slama, R. et al. Time to pregnancy and semen parameters: a cross-sectional study among fertile couples from four European cities. Hum. Reprod. 17, 503–515 (2002).
Zinaman, M. J., Brown, C. C., Selevan, S. G. & Clegg, E. D. Semen quality and human fertility: a prospective study with healthy couples. J. Androl. 21, 145–153 (2000).
Buck Louis, G. M. et al. Semen quality and time to pregnancy: the Longitudinal Investigation of Fertility and the Environment Study. Fertil. Steril. 101, 453–462 (2014).
Patel, C. J., Sundaram, R. & Buck Louis, G. M. A data-driven search for semen-related phenotypes in conception delay. Andrology http://dx.doi.org/10.1111/andr.12288 (2016).
Zhao, J., Zhang, Q., Wang, Y. & Li, Y. Whether sperm deoxyribonucleic acid fragmentation has an effect on pregnancy and miscarriage after in vitro fertilization/intracytoplasmic sperm injection: a systematic review and meta-analysis. Fertil. Steril. 102, 998–1005.e1008 (2014).
Evenson, D. P. et al. Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum. Reprod. 14, 1039–1049 (1999).
Spanò, M. et al. Sperm chromatin damage impairs human fertility. Fertil. Steril. 73, 43–50 (2000).
WHO. WHO laboratory manual for the examination of human semen and sperm – cervical mucus interaction. (Press Concern, 1980).
WHO. WHO laboratory manual for the examination and processing of human semen. 5th edn, (WHO press, 2010).
MacLeod, J. & Heim, L. M. Characteristics and variations in semen specimens in 100 normal young men. J. Urol. 54, 474–482 (1945).
Acknowledgements
The authors thank Dr. Wiwat Rodprasert for drawing the figures and Ms. Johanna Järvi for technical assistance with this article. This work was supported by the European Commission (FP7), the Academy of Finland, Sigrid Juselius Foundation, Novo Nordisk Foundation, Turku University Hospital Special Governmental Research Fund, and The Research Fund of Rigshospitalet (grant no. R42-A1326).
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Virtanen, H., Jørgensen, N. & Toppari, J. Semen quality in the 21st century. Nat Rev Urol 14, 120–130 (2017). https://doi.org/10.1038/nrurol.2016.261
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DOI: https://doi.org/10.1038/nrurol.2016.261