Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Semen quality in the 21st century

Key Points

  • Downward trends in sperm concentrations have been described in several geographical areas during this century

  • 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

  • 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

  • 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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Median sperm concentration of young men in different geographical areas in studies using similar study protocols.
Figure 2: Median sperm concentration of fertile men in different geographical areas in studies using similar study protocols.

References

  1. 1

    Mendiola, J. et al. Sperm counts may have declined in young university students in southern Spain. Andrology 1, 408–413 (2013).

    PubMed  Article  Google Scholar 

  2. 2

    Jørgensen, N. et al. Recent adverse trends in semen quality and testis cancer incidence among Finnish men. Int. J. Androl. 34, e37–48 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  3. 3

    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).

    PubMed  Article  Google Scholar 

  4. 4

    Sripada, S. et al. Trends in semen parameters in the northeast of Scotland. J. Androl. 28, 313–319 (2007).

    PubMed  Article  Google Scholar 

  5. 5

    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).

    PubMed  Article  Google Scholar 

  6. 6

    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).

    PubMed  PubMed Central  Article  Google Scholar 

  7. 7

    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).

    CAS  PubMed  Article  Google Scholar 

  8. 8

    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).

    Article  Google Scholar 

  9. 9

    Romero-Otero, J. et al. Semen quality assessment in fertile men in Madrid during the last 3 decades. Urology 85, 1333–1338 (2015).

    PubMed  Article  Google Scholar 

  10. 10

    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).

    CAS  PubMed  Article  Google Scholar 

  11. 11

    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).

    PubMed  Google Scholar 

  12. 12

    Rao, M. et al. Evaluation of semen quality in 1808 university students, from Wuhan, central China. Asian J. Androl. 17, 111–116 (2015).

    PubMed  Article  Google Scholar 

  13. 13

    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).

  14. 14

    Shine, R., Peek, J. & Birdsall, M. Declining sperm quality in New Zealand over 20 years. N. Z. Med. J. 121, 50–56 (2008).

    PubMed  Google Scholar 

  15. 15

    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).

    CAS  PubMed  Article  Google Scholar 

  16. 16

    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).

    CAS  PubMed  Article  Google Scholar 

  17. 17

    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).

  18. 18

    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).

    CAS  PubMed  Article  Google Scholar 

  19. 19

    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).

    CAS  PubMed  Article  Google Scholar 

  20. 20

    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).

    PubMed  PubMed Central  Article  Google Scholar 

  21. 21

    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).

    PubMed  PubMed Central  Article  Google Scholar 

  22. 22

    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).

    PubMed  Article  Google Scholar 

  23. 23

    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).

    CAS  PubMed  Google Scholar 

  24. 24

    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).

    PubMed  Google Scholar 

  25. 25

    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).

    PubMed  Article  Google Scholar 

  26. 26

    Jørgensen, N. et al. Regional differences in semen quality in Europe. Hum. Reprod. 16, 1012–1019 (2001).

    PubMed  Article  Google Scholar 

  27. 27

    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).

    PubMed  Article  Google Scholar 

  28. 28

    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).

    CAS  PubMed  Article  Google Scholar 

  29. 29

    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).

    CAS  PubMed  Article  Google Scholar 

  30. 30

    Punab, M. et al. Regional differences in semen qualities in the Baltic region. Int. J. Androl. 25, 243–252 (2002).

    PubMed  Article  Google Scholar 

  31. 31

    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).

    PubMed  Article  Google Scholar 

  32. 32

    Fernandez, M. F. et al. Semen quality and reproductive hormone levels in men from southern Spain. Int. J. Androl. 35, 1–10 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. 33

    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).

    PubMed  PubMed Central  Article  Google Scholar 

  34. 34

    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).

    PubMed  Article  Google Scholar 

  35. 35

    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).

    PubMed  PubMed Central  Article  Google Scholar 

  36. 36

    Mendiola, J. et al. Reproductive parameters in young men living in Rochester, New York. Fertil. Steril. 101, 1064–1071 (2014).

    PubMed  Article  Google Scholar 

  37. 37

    Hart, R. J. et al. Testicular function in a birth cohort of young men. Hum. Reprod. 30, 2713–2724 (2015).

    CAS  PubMed  Google Scholar 

  38. 38

    Perheentupa, A. et al. Semen quality improves marginally during young adulthood: a longitudinal follow-up study. Hum. Reprod. 31, 502–510 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  39. 39

    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).

    PubMed  Article  Google Scholar 

  40. 40

    Swan, S. H. et al. Geographic differences in semen quality of fertile U. S. males. Environ. Health Perspect. 111, 414–420 (2003).

    PubMed  PubMed Central  Article  Google Scholar 

  41. 41

    Redmon, J. B. et al. Semen parameters in fertile US men: the Study for Future Families. Andrology 1, 806–814 (2013).

    CAS  PubMed  Article  Google Scholar 

  42. 42

    Swan, S. H. et al. Semen quality in relation to biomarkers of pesticide exposure. Environ. Health Perspect. 111, 1478–1484 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. 43

    Iwamoto, T. et al. Semen quality of 324 fertile Japanese men. Hum. Reprod. 21, 760–765 (2006).

    CAS  PubMed  Article  Google Scholar 

  44. 44

    Iwamoto, T. et al. Semen quality of fertile Japanese men: a cross-sectional population-based study of 792 men. BMJ Open 3, e002223 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  45. 45

    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).

    CAS  PubMed  Article  Google Scholar 

  46. 46

    Haugen, T. B., Egeland, T. & Magnus, O. Semen parameters in Norwegian fertile men. J. Androl. 27, 66–71 (2006).

    PubMed  Article  Google Scholar 

  47. 47

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  48. 48

    Skakkebaek, N. E. et al. Male reproductive disorders and fertility trends: influences of environment and genetic susceptibility. Physiol. Rev. 96, 55–97 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. 49

    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).

    CAS  PubMed  Article  Google Scholar 

  50. 50

    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).

    PubMed  Article  Google Scholar 

  51. 51

    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).

    PubMed  Article  Google Scholar 

  52. 52

    Rubes, J. et al. Smoking cigarettes is associated with increased sperm disomy in teenage men. Fertil. Steril. 70, 715–723 (1998).

    CAS  PubMed  Article  Google Scholar 

  53. 53

    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).

    PubMed  Article  Google Scholar 

  54. 54

    Robbins, W. A. et al. Effect of lifestyle exposures on sperm aneuploidy. Cytogenet. Genome Res. 111, 371–377 (2005).

    CAS  PubMed  Article  Google Scholar 

  55. 55

    Storgaard, L. et al. Does smoking during pregnancy affect sons' sperm counts? Epidemiology 14, 278–286 (2003).

    PubMed  Google Scholar 

  56. 56

    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).

    PubMed  Article  Google Scholar 

  57. 57

    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).

    CAS  PubMed  Article  Google Scholar 

  58. 58

    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).

    PubMed  Article  Google Scholar 

  59. 59

    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).

    CAS  PubMed  Article  Google Scholar 

  60. 60

    Virtanen, H. E., Sadov, S. & Toppari, J. Prenatal exposure to smoking and male reproductive health. Curr. Opin. Endocrinol. Diabetes Obes. 19, 228–232 (2012).

    PubMed  Article  Google Scholar 

  61. 61

    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).

    PubMed  Article  Google Scholar 

  62. 62

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. 63

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. 64

    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).

    PubMed  PubMed Central  Article  Google Scholar 

  65. 65

    Pajarinen, J. et al. Moderate alcohol consumption and disorders of human spermatogenesis. Alcohol Clin. Exp. Res. 20, 332–337 (1996).

    CAS  PubMed  Article  Google Scholar 

  66. 66

    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).

    CAS  PubMed  Article  Google Scholar 

  67. 67

    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).

    CAS  PubMed  Article  Google Scholar 

  68. 68

    Martini, A. C. et al. Effects of alcohol and cigarette consumption on human seminal quality. Fertil. Steril. 82, 374–377 (2004).

    PubMed  Article  Google Scholar 

  69. 69

    WHO. Obesity. Situation and trends. Global Health Observatory (GHO) data [online], http://www.who.int/gho/ncd/risk_factors/obesity_text/en/ (2016).

  70. 70

    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).

    CAS  PubMed  Article  Google Scholar 

  71. 71

    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).

    CAS  PubMed  Article  Google Scholar 

  72. 72

    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).

    PubMed  Article  Google Scholar 

  73. 73

    Tsao, C. W. et al. Exploration of the association between obesity and semen quality in a 7630 male population. PLoS ONE 10, e0119458 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  74. 74

    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).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  75. 75

    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).

    PubMed  Article  Google Scholar 

  76. 76

    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).

    CAS  PubMed  Article  Google Scholar 

  77. 77

    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).

    CAS  PubMed  Article  Google Scholar 

  78. 78

    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).

    PubMed  Article  Google Scholar 

  79. 79

    Janevic, T. et al. Effects of work and life stress on semen quality. Fertil. Steril. 102, 530–538 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  80. 80

    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).

    CAS  PubMed  Article  Google Scholar 

  81. 81

    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).

    PubMed  Article  Google Scholar 

  82. 82

    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).

    Google Scholar 

  83. 83

    Gore, A. C. et al. EDC-2: the Endocrine Society's second scientific statement on endocrine-disrupting chemicals. Endocr. Rev. 36, E1–E150 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  84. 84

    Vested, A., Giwercman, A., Bonde, J. P. & Toft, G. Persistent organic pollutants and male reproductive health. Asian J. Androl. 16, 71–80 (2014).

    PubMed  Article  CAS  Google Scholar 

  85. 85

    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).

    CAS  PubMed  Article  Google Scholar 

  86. 86

    Mocarelli, P. et al. Perinatal exposure to low doses of dioxin can permanently impair human semen quality. Environ. Health Perspect. 119, 713–718 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  87. 87

    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).

    CAS  PubMed  Article  Google Scholar 

  88. 88

    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).

    PubMed  PubMed Central  Article  Google Scholar 

  89. 89

    Vested, A. et al. In utero exposure to persistent organochlorine pollutants and reproductive health in the human male. Reproduction 148, 635–646 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  90. 90

    Buck Louis, G. M. et al. Persistent environmental pollutants and couple fecundity: the LIFE study. Environ. Health Perspect. 121, 231–236 (2013).

    PubMed  Article  CAS  Google Scholar 

  91. 91

    Axelsson, J. et al. Prenatal phthalate exposure and reproductive function in young men. Environ. Res. 138, 264–270 (2015).

    CAS  PubMed  Article  Google Scholar 

  92. 92

    Cai, H. et al. Human urinary/seminal phthalates or their metabolite levels and semen quality: a meta-analysis. Environ. Res. 142, 486–494 (2015).

    CAS  PubMed  Article  Google Scholar 

  93. 93

    Phthalate exposure and reproductive parameters in young men from the general Swedish population. Environ. Int. 85, 54–60 (2015).

  94. 94

    Thurston, S. W. et al. Phthalate exposure and semen quality in fertile US men. Andrology 4, 623–628 (2016).

    Article  CAS  Google Scholar 

  95. 95

    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).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  96. 96

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  97. 97

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. 98

    Dama, M. S. & Bhat, M. N. Mobile phones affect multiple sperm quality traits: a meta-analysis. F1000Res 2, 40 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  99. 99

    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).

    PubMed  Article  Google Scholar 

  100. 100

    Liu, K. et al. Association between mobile phone use and semen quality: a systemic review and meta-analysis. Andrology 2, 491–501 (2014).

    CAS  PubMed  Article  Google Scholar 

  101. 101

    NTP. Cell phones. National Toxicology Program [online], https://ntp.niehs.nih.gov/results/areas/cellphones/ (2016).

  102. 102

    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).

    PubMed  Article  Google Scholar 

  103. 103

    Guzick, D. S. et al. Sperm morphology, motility, and concentration in fertile and infertile men. N. Engl. J. Med. 345, 1388–1393 (2001).

    CAS  PubMed  Article  Google Scholar 

  104. 104

    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).

    CAS  PubMed  Article  Google Scholar 

  105. 105

    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).

    CAS  PubMed  Article  Google Scholar 

  106. 106

    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).

    CAS  PubMed  Article  Google Scholar 

  107. 107

    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).

    CAS  PubMed  Google Scholar 

  108. 108

    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).

    PubMed  Article  Google Scholar 

  109. 109

    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).

  110. 110

    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).

    CAS  PubMed  Article  Google Scholar 

  111. 111

    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).

    CAS  PubMed  Article  Google Scholar 

  112. 112

    Spanò, M. et al. Sperm chromatin damage impairs human fertility. Fertil. Steril. 73, 43–50 (2000).

    PubMed  Article  Google Scholar 

  113. 113

    WHO. WHO laboratory manual for the examination of human semen and sperm – cervical mucus interaction. (Press Concern, 1980).

  114. 114

    WHO. WHO laboratory manual for the examination and processing of human semen. 5th edn, (WHO press, 2010).

  115. 115

    MacLeod, J. & Heim, L. M. Characteristics and variations in semen specimens in 100 normal young men. J. Urol. 54, 474–482 (1945).

    CAS  PubMed  Article  Google Scholar 

Download references

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).

Author information

Affiliations

Authors

Contributions

All authors researched data for article, made substantial contributions to discussion of content, wrote the article, and reviewed and edited the manuscript before submission.

Corresponding author

Correspondence to Jorma Toppari.

Ethics declarations

Competing interests

J.T. has received honoraria for speaking and acted as a consultant for Merck and Mylan. The other authors declare no competing interests.

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing