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Trends in Male Reproductive Health and Decreasing Fertility: Possible Influence of Endocrine Disrupters

  • Tina Harmer Lassen
  • Teruaki Iwamoto
  • Tina Kold Jensen
  • Niels E. SkakkebækEmail author
Chapter
Part of the International Studies in Population book series (ISIP, volume 11)

Abstract

Within recent decades, adverse trends in male reproductive health have become increasingly evident. In many countries the incidence of testicular cancer has been growing along with an apparent increase in incidences of congenital malformations in the male reproductive tract and a decline in sperm quality. There are, however, large geographical variations in these trends. At the same time, fertility rates have declined drastically and are now below replacement level in many parts of the world. This decline is, without doubt, due primarily to changes in social and economic conditions, but it may also be partly due to a decrease in the ability to conceive. The rapid increase in male reproductive problems and the geographical variations indicate that environmental exposures, lifestyle factors, or both, rather than genetic factors, are important contributors. In particular, there is concern about environmental chemicals with endocrine-disrupting properties, which are suspected of having the ability to disturb the development of reproductive organs during fetal life.

Keywords

Testicular Cancer Prenatal Exposure Endocrine Disrupter Sperm Concentration Semen Quality 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Akre, O., Lipworth, L., Cnattingius, S., Sparen, P., & Ekbom, A. (1999). Risk factor patterns for cryptorchidism and hypospadias. Epidemiology, 10(4), 364–369.Google Scholar
  2. Andersen, A. N., & Erb, K. (2006). Register data on assisted reproductive technology (ART) in Europe including a detailed description of ART in Denmark. International Journal of Andrology, 29(1), 12–16.Google Scholar
  3. Andersen, A. G., Jensen, T. K., Carlsen, E., Jørgensen, N., Andersson, A. M., Krarup, T., et al. (2000). High frequency of sub-optimal semen quality in an unselected population of young men. Human Reproduction, 15(2), 366–372.Google Scholar
  4. Andersen, A. N., Carlsen, E., & Loft, A. (2008a). Trends in the use of intracytoplasmatic sperm injection marked variability between countries. Human Reproduction Update, 14(6), 593–604.Google Scholar
  5. Andersen, H. R., Schmidt, I. M., Grandjean, P., Jensen, T. K., Budtz-Jørgensen, E., Kjaerstad, M. B., et al. (2008b). Impaired reproductive development in sons of women occupationally exposed to pesticides during pregnancy. Environmental Health Perspectives, 116(4), 566–572.Google Scholar
  6. Andersson, A. M., Jørgensen, N., Main, K. M., Toppari, J., Rajpert-De Meyts, E., Leffers, H., et al. (2008). Adverse trends in male reproductive health: We may have reached a crucial ‘tipping point’. International Journal of Andrology, 31(2), 74–80.Google Scholar
  7. Asklund, C., Jensen, T. K., Main, K. M., Sobotka, T., Skakkebæk, N. E., & Jørgensen, N. (2010). Semen quality, reproductive hormones and fertility of men operated for hypospadias. International Journal of Andrology, 33(1), 80–87.Google Scholar
  8. Birnbaum, L. S., & Tuomisto, J. (2000). Non-carcinogenic effects of TCDD in animals. Food Additives & Contaminants, 17(4), 275–288.Google Scholar
  9. Boisen, K. A., Kaleva, M., Main, K. M., Virtanen, H. E., Haavisto, A. M., Schmidt, I. M., et al. (2004). Difference in prevalence of congenital cryptorchidism in infants between two Nordic countries. Lancet, 363(9417), 1264–1269.Google Scholar
  10. Bonde, J. P., Ernst, E., Jensen, T. K., Hjollund, N. H., Kolstad, H., Henriksen, T. B., et al. (1998). Relation between semen quality and fertility: A population-based study of 430 first-pregnancy planners. Lancet, 352(9135), 1172–1177.Google Scholar
  11. Bonefeld-Jørgensen, E. C., Andersen, H. R., Rasmussen, T. H., & Vinggaard, A. M. (2001). Effect of highly bioaccumulated polychlorinated biphenyl congeners on estrogen and androgen receptor activity. Toxicology, 158(3), 141–153.Google Scholar
  12. Caballero, B. (2007). The global epidemic of obesity: An overview. Epidemiologic Reviews, 29, 1–5.Google Scholar
  13. Carlsen, E., Giwercman, A., Keiding, N., & Skakkebæk, N. E. (1992). Evidence for decreasing quality of semen during past 50 years. British Medical Journal, 305(6854), 609–613.Google Scholar
  14. Chia, S. E., Tay, S. K., & Lim, S. T. (1998). What constitutes a normal seminal analysis? semen parameters of 243 fertile men. Human Reproduction, 13(12), 3394–3398.Google Scholar
  15. Christiansen, S., Scholze, M., Axelstad, M., Boberg, J., Kortenkamp, A., & Hass, U. (2008). Combined exposure to anti-androgens causes markedly increased frequencies of hypospadias in the rat. International Journal of Andrology, 31(2), 241–248.Google Scholar
  16. Damgaard, I. N., Skakkebæk, N. E., Toppari, J., Virtanen, H. E., Shen, H., Schramm, K. W., et al. (2006). Persistent pesticides in human breast milk and cryptorchidism. Environmental Health Perspectives, 114(7), 1133–1138.Google Scholar
  17. Danish Fertility Society. (2010). www.fertilitetsselskab.dk. Accessed 6 Sept 2010.
  18. Dodds, E. C., & Lawson, W. (1936). Synthetic oestrogenic agents without the phenanthrene nucleus. Nature, 137, 996.Google Scholar
  19. Dunphy, B. C., Barratt, C. L., & Cooke, I. D. (1991). Male alcohol consumption and fecundity in couples attending an infertility clinic. Andrologia, 23(3), 219–221.Google Scholar
  20. Edwards, T. M., Moore, B. C., & Guillette, L. J., Jr. (2006). Reproductive dysgenesis in wildlife: A comparative view. International Journal of Andrology, 29(1), 109–121.Google Scholar
  21. Fernandez, M. F., Olmos, B., Granada, A., Lopez-Espinosa, M. J., Molina-Molina, J. M., Fernandez, J. M., et al. (2007). Human exposure to endocrine-disrupting chemicals and prenatal risk factors for cryptorchidism and hypospadias: A nested case-control study. Environmental Health Perspectives, 115(Suppl 1), 8–14.Google Scholar
  22. Fisher, J. S., Macpherson, S., Marchetti, N., & Sharpe, R. M. (2003). Human ‘testicular dysgenesis syndrome’: A possible model using in-utero exposure of the rat to dibutyl phthalate. Human Reproduction, 18(7), 1383–1394.Google Scholar
  23. Foster, P. M. (2006). Disruption of reproductive development in male rat offspring following in utero exposure to phthalate esters. International Journal of Andrology, 29(1), 140–147.Google Scholar
  24. Giwercman, A., Kledal, T., Schwartz, M., Giwercman, Y. L., Leffers, H., Zazzi, H., et al. (2000). Preserved male fertility despite decreased androgen sensitivity caused by a mutation in the ligand-binding domain of the androgen receptor gene. Journal of Clinical Endocrinology and Metabolism, 85(6), 2253–2259.Google Scholar
  25. Giwercman, A., Rylander, L., Hagmar, L., & Giwercman, Y. L. (2006). Ethnic differences in occurrence of TDS—genetics and/or environment? International Journal of Andrology, 29(1), 291–297.Google Scholar
  26. Gray, L. E., Jr., Wilson, V. S., Stoker, T., Lambright, C., Furr, J., Noriega, N., et al. (2006). Adverse effects of environmental antiandrogens and androgens on reproductive development in mammals. International Journal of Andrology, 29(1), 96–104.Google Scholar
  27. Guo, Y. L., Hsu, P. C., Hsu, C. C., & Lambert, G. H. (2000). Semen quality after prenatal exposure to polychlorinated biphenyls and dibenzofurans. Lancet, 356(9237), 1240–1241.Google Scholar
  28. Hammoud, A. O., Wilde, N., Gibson, M., Parks, A., Carrell, D. T., & Meikle, A. W. (2008). Male obesity and alteration in sperm parameters. Fertility and Sterility, 90(6), 2222–2225.Google Scholar
  29. Hardell, L., Van Bavel, B., Lindstrom, G., Carlberg, M., Eriksson, M., Dreifaldt, A. C., et al. (2004). Concentrations of polychlorinated biphenyls in blood and the risk for testicular cancer. International Journal of Andrology, 27(5), 282–290.Google Scholar
  30. Hauser, R. (2006). The environment and male fertility: Recent research on emerging chemicals and semen quality. Seminars in Reproductive Medicine, 24(3), 156–167.Google Scholar
  31. Hemminki, K., & Li, X. (2002). Cancer risks in Nordic immigrants and their offspring in Sweden. European Journal of Cancer, 38(18), 2428–2434.Google Scholar
  32. Huyghe, E., Matsuda, T., & Thonneau, P. (2003). Increasing incidence of testicular cancer worldwide: A review. Journal of Urology, 170(1), 5–11.Google Scholar
  33. Huyghe, E., Plante, P., & Thonneau, P. F. (2007). Testicular cancer variations in time and space in Europe. European Urology, 51(3), 621–628.Google Scholar
  34. Iwamoto, T., Nozawa, S., Yoshiike, M., Hoshino, T., Baba, K., Matsushita, T., et al. (2006). Semen quality of 324 fertile Japanese men. Human Reproduction, 21(3), 760–765.Google Scholar
  35. Jacobsen, R., Bostofte, E., Engholm, G., Hansen, J., Olsen, J. H., Skakkebæk, N. E., et al. (2000). Risk of testicular cancer in men with abnormal semen characteristics: Cohort study. British Medical Journal, 321(7264), 789–792.Google Scholar
  36. Jensen, T. K., Andersson, A. M., Jørgensen, N., Andersen, A. G., Carlsen, E., Petersen, J. H., et al. (2004a). Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men. Fertility and Sterility, 82(4), 863–870.Google Scholar
  37. Jensen, T. K., Jørgensen, N., Punab, M., Haugen, T. B., Suominen, J., Zilaitiene, B., et al. (2004b). 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. American Journal of Epidemiology, 159(1), 49–58.Google Scholar
  38. Jensen, T. K., Sobotka, T., Hansen, M. A., Pedersen, A. T., Lutz, W., & Skakkebæk, N. E. (2008). Declining trends in conception rates in recent birth cohorts of native Danish women: A possible role of deteriorating male reproductive health. International Journal of Andrology, 31(2), 81–92.Google Scholar
  39. Jørgensen, N., Andersen, A. G., Eustache, F., Irvine, D. S., Suominen, J., Petersen, J. H., et al. (2001). Regional differences in semen quality in Europe. Human Reproduction, 16(5), 1012–1019.Google Scholar
  40. Jørgensen, N., Carlsen, E., Nermoen, I., Punab, M., Suominen, J., Andersen, A. G., et al. (2002). 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. Human Reproduction, 17(8), 2199–2208.Google Scholar
  41. Jørgensen, N., Asklund, C., Carlsen, E., & Skakkebæk, N. E. (2006). Coordinated European investigations of semen quality: Results from studies of Scandinavian young men is a matter of concern. International Journal of Andrology, 29(1), 54–61.Google Scholar
  42. Jørgensen, N., Joensen, U. N., Jensen, T. K., Jensen, M. B., Almstrup, K., Olesen, I. A., Juul, A., Andersson, A.-M., Carlsen, E., Petersen, J. H., Toppari, J., & Skakkebæk, N. E. (2012). Human semen quality in the new millennium: A prospective cross-sectional population-based study of 4867 men. BMJ Open, 2, e000990.Google Scholar
  43. Jouannet, P., Wang, C., Eustache, F., Kold-Jensen, T., & Auger, J. (2001). Semen quality and male reproductive health: The controversy about human sperm concentration decline. Acta Pathologica, Microbiologica et Immunologica Scandinavica, 109(5), 333–344.Google Scholar
  44. Kelce, W. R., & Wilson, E. M. (1997). Environmental antiandrogens: Developmental effects, molecular mechanisms, and clinical implications. Journal of Molecular Medicine, 75(3), 198–207.Google Scholar
  45. Koloszar, S., Fejes, I., Zavaczki, Z., Daru, J., Szollosi, J., & Pal, A. (2005). Effect of body weight on sperm concentration in normozoospermic males. Archives of Andrology, 51(4), 299–304.Google Scholar
  46. Kort, H. I., Massey, J. B., Elsner, C. W., Mitchell-Leef, D., Shapiro, D. B., Witt, M. A., et al. (2006). Impact of body mass index values on sperm quantity and quality. Journal of Andrology, 27(3), 450–452.Google Scholar
  47. Krysiak-Baltyn, K., Toppari, J., Skakkebæk, N. E., Jensen, T. S., Virtanen, H. E., Schramm, K. W., et al. (2010). Country-specific chemical signatures of persistent environmental compounds in breast milk. International Journal of Andrology, 33(2), 270–278.Google Scholar
  48. Lassen, T. H., Sobotka, T., Jensen, T. K., Jacobsen, R., Erb, K., & Skakkebæk, N. E. (2012). Trends in rates of natural conceptions among Danish women born during 1960–1984. Human Reproduction, 27, 2815–2822.Google Scholar
  49. Lee, P. A., & Coughlin, M. T. (2001). Fertility after bilateral cryptorchidism: Evaluation by paternity, hormone, and semen data. Hormone Research, 55(1), 28–32.Google Scholar
  50. Lund, L., Engebjerg, M. C., Pedersen, L., Ehrenstein, V., Nørgaard, M., & Sørensen, H. T. (2009). Prevalence of hypospadias in Danish boys: A longitudinal study, 1977–2005. European Urology, 55(5), 1022–1026.Google Scholar
  51. Lundkvist, U. (1990). Clinical and reproductive effects of clophen A50 (PCB) administered during gestation on pregnant guinea pigs and their offspring. Toxicology, 61(3), 249–257.Google Scholar
  52. Lutke Holzik, M. F., Rapley, E. A., Hoekstra, H. J., Sleijfer, D. T., Nolte, I. M., & Sijmons, R. H. (2004). Genetic predisposition to testicular germ-cell tumours. Lancet Oncology, 5(6), 363–371.Google Scholar
  53. Lutz, W. (2006). Fertility rates and future population trends: Will Europe’s birth rate recover or continue to decline? International Journal of Andrology, 29(1), 25–33.Google Scholar
  54. Magnusdottir, E. V., Thorsteinsson, T., Thorsteinsdottir, S., Heimisdottir, M., & Olafsdottir, K. (2005). Persistent organochlorines, sedentary occupation, obesity and human male subfertility. Human Reproduction, 20(1), 208–215.Google Scholar
  55. Main, K. M., Kiviranta, H., Virtanen, H. E., Sundqvist, E., Tuomisto, J. T., Tuomisto, J., et al. (2007). Flame retardants in placenta and breast milk and cryptorchidism in newborn boys. Environmental Health Perspectives, 115(10), 1519–1526.Google Scholar
  56. Marshburn, P. B., Sloan, C. S., & Hammond, M. G. (1989). Semen quality and association with coffee drinking, cigarette smoking, and ethanol consumption. Fertility and Sterility, 52(1), 162–165.Google Scholar
  57. Martíni, A. C., Molina, R. I., Estofan, D., Senestrari, D., Fiol, D. C. M., & Ruiz, R. D. (2004). Effects of alcohol and cigarette consumption on human seminal quality. Fertility and Sterility, 82(2), 374–377.Google Scholar
  58. Matsuda, T., & Saika, K. (2008). Comparison of time trends in testicular cancer incidence (1973–97) in East Asia, Europe and USA, from cancer incidence in five continents, vols. IV–VIII. Japanese Journal of Clinical Oncology, 38(8), 578–579.Google Scholar
  59. McElreavey, K., & Quintana-Murci, L. (2003). Y chromosome haplogroups: A correlation with testicular dysgenesis syndrome? Acta Pathologica Microbiologica et Immunologica Scandinavica, 111(1), 106–113.Google Scholar
  60. McGlynn, K. A., Quraishi, S. M., Graubard, B. I., Weber, J. P., Rubertone, M. V., & Erickson, R. L. (2008). Persistent organochlorine pesticides and risk of testicular germ cell tumors. Journal of the National Cancer Institute, 100(9), 663–671.Google Scholar
  61. Mocarelli, P., Gerthoux, P. M., Patterson, D. G., Jr., Milani, S., Limonta, G., Bertona, M., et al. (2008). Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality. Environmental Health Perspectives, 116(1), 70–77.Google Scholar
  62. Mokdad, A. H., Bowman, B. A., Ford, E. S., Vinicor, F., Marks, J. S., & Koplan, J. P. (2001). The continuing epidemics of obesity and diabetes in the United States. Journal of the American Medical Association, 286(10), 1195–1200.Google Scholar
  63. Mol, N. M., Sorensen, N., Weihe, P., Andersson, A. M., Jørgensen, N., Skakkebæk, N. E., et al. (2002). Spermaturia and serum hormone concentrations at the age of puberty in boys prenatally exposed to polychlorinated biphenyls. European Journal of Endocrinology, 146(3), 357–363.Google Scholar
  64. Molarius, A., Parsons, R. W., Dobson, A. J., Evans, A., Fortmann, S. P., Jamrozik, K., et al. (2001). Trends in cigarette smoking in 36 populations from the early 1980s to the mid-1990s: Findings from the WHO MONICA Project. American Journal of Public Health, 91(2), 206–212.Google Scholar
  65. Møller, H., & Skakkebæk, N. E. (1999). Risk of testicular cancer in subfertile men: Case-control study. British Medical Journal, 318(7183), 559–562.Google Scholar
  66. Morohoshi, K., Yamamoto, H., Kamata, R., Shiraishi, F., Koda, T., & Morita, M. (2005). Estrogenic activity of 37 components of commercial sunscreen lotions evaluated by in vitro assays. Toxicology in Vitro, 19(4), 457–469.Google Scholar
  67. Muthusami, K. R., & Chinnaswamy, P. (2005). Effect of chronic alcoholism on male fertility hormones and semen quality. Fertility and Sterility, 84(4), 919–924.Google Scholar
  68. Myrup, C., Westergaard, T., Schnack, T., Oudin, A., Ritz, C., Wohlfahrt, J., et al. (2008). Testicular cancer risk in first- and second-generation immigrants to Denmark. Journal of the National Cancer Institute, 100(1), 41–47.Google Scholar
  69. Oldereid, N. B., Rui, H., & Purvis, K. (1992). Life styles of men in barren couples and their relationship to sperm quality. International Journal of Fertility, 37(6), 343–349.Google Scholar
  70. Paulozzi, L. J. (1999). International trends in rates of hypospadias and cryptorchidism. Environmental Health Perspectives, 107(4), 297–302.Google Scholar
  71. Phillips, K. P., & Tanphaichitr, N. (2008). Human exposure to endocrine disrupters and semen quality. Journal of Toxicology and Environmental Health. Part B, Critical Reviews, 11(3–4), 188–220.Google Scholar
  72. Prener, A., Engholm, G., & Jensen, O. M. (1996). Genital anomalies and risk for testicular cancer in Danish men. Epidemiology, 7(1), 14–19.Google Scholar
  73. Priskorn, L., Holmboe, S. A., Jacobsen, R., Jensen, T. K., Lassen, T. H., & Skakkebæk, N. E. (2012). Increasing trends in childlessness in recent birth cohorts—a registry-based study of the total Danish male population born from 1945 to 1980. International Journal of Andrology, 35, 449–455.Google Scholar
  74. Rajpert-De Meyts, E. (2006). Developmental model for the pathogenesis of testicular carcinoma in situ: Genetic and environmental aspects. Human Reproduction Update, 12(3), 303–323.Google Scholar
  75. Ramlau-Hansen, C. H., Thulstrup, A. M., Aggerholm, A. S., Jensen, M. S., Toft, G., & Bonde, J. P. (2007a). Is smoking a risk factor for decreased semen quality? A cross-sectional analysis. Human Reproduction, 22(1), 188–196.Google Scholar
  76. Ramlau-Hansen, C. H., Thulstrup, A. M., Storgaard, L., Toft, G., Olsen, J., & Bonde, J. P. (2007b). Is prenatal exposure to tobacco smoking a cause of poor semen quality? A follow-up study. American Journal of Epidemiology, 165(12), 1372–1379.Google Scholar
  77. Richiardi, L., Bellocco, R., Adami, H. O., Torrang, A., Barlow, L., Hakulinen, T., et al. (2004). Testicular cancer incidence in eight northern European countries: Secular and recent trends. Cancer Epidemiology, Biomarkers & Prevention, 13(12), 2157–2166.Google Scholar
  78. Richter, C. A., Birnbaum, L. S., Farabollini, F., Newbold, R. R., Rubin, B. S., Talsness, C. E., et al. (2007). In vivo effects of bisphenol a in laboratory rodent studies. Reproductive Toxicology, 24(2), 199–224.Google Scholar
  79. Richthoff, J., Rylander, L., Jonsson, B. A., Akesson, H., Hagmar, L., Nilsson-Ehle, P., et al. (2003). Serum levels of 2,2',4,4',5,5'-hexachlorobiphenyl (CB-153) in relation to markers of reproductive function in young males from the general Swedish population. Environmental Health Perspectives, 111(4), 409–413.Google Scholar
  80. Schettler, T. (2006). Human exposure to phthalates via consumer products. International Journal of Andrology, 29(1), 134–139.Google Scholar
  81. Schlumpf, M., Schmid, P., Durrer, S., Conscience, M., Maerkel, K., Henseler, M., et al. (2004). Endocrine activity and developmental toxicity of cosmetic UV filters—an update. Toxicology, 205(1–2), 113–122.Google Scholar
  82. Schnack, T. H., Zdravkovic, S., Myrup, C., Westergaard, T., Christensen, K., Wohlfahrt, J., et al. (2008a). Familial aggregation of hypospadias: A cohort study. American Journal of Epidemiology, 167(3), 251–256.Google Scholar
  83. Schnack, T. H., Zdravkovic, S., Myrup, C., Westergaard, T., Wohlfahrt, J., & Melbye, M. (2008b). Familial aggregation of cryptorchidism—a nationwide cohort study. American Journal of Epidemiology, 167(12), 1453–1457.Google Scholar
  84. Shah, M. N., Devesa, S. S., Zhu, K., & McGlynn, K. A. (2007). Trends in testicular germ cell tumours by ethnic group in the United States. International Journal of Andrology, 30(4), 206–213.Google Scholar
  85. Shen, H., Main, K. M., Andersson, A. M., Damgaard, I. N., Virtanen, H. E., Skakkebæk, N. E., et al. (2008). Concentrations of persistent organochlorine compounds in human milk and placenta are higher in Denmark than in Finland. Human Reproduction, 23(1), 201–210.Google Scholar
  86. Skakkebæk, N. E., Berthelsen, J. G., Giwercman, A., & Müller, J. (1987). Carcinoma-in-situ of the testis: Possible origin from gonocytes and precursor of all types of germ cell tumours except spermatocytoma. International Journal of Andrology, 10(1), 19–28.Google Scholar
  87. Skakkebæk, N. E., Rajpert-De Meyts, E., & Main, K. M. (2001). Testicular dysgenesis syndrome: An increasingly common developmental disorder with environmental aspects. Human Reproduction, 16(5), 972–978.Google Scholar
  88. Sobreiro, B. P., Lucon, A. M., Pasqualotto, F. F., Hallak, J., Athayde, K. S., & Arap, S. (2005). Semen analysis in fertile patients undergoing vasectomy: Reference values and variations according to age, length of sexual abstinence, seasonality, smoking habits and caffeine intake. São Paulo Medical Journal, 123(4), 161–166.Google Scholar
  89. Storgaard, L., Bonde, J. P., Ernst, E., Spano, M., Andersen, C. Y., Frydenberg, M., et al. (2003). Does smoking during pregnancy affect sons’ sperm counts? Epidemiology, 14(3), 278–286.Google Scholar
  90. Suzuki, T., Kitamura, S., Khota, R., Sugihara, K., Fujimoto, N., & Ohta, S. (2005). Estrogenic and antiandrogenic activities of 17 benzophenone derivatives used as UV stabilizers and sunscreens. Toxicology and Applied Pharmacology, 203(1), 9–17.Google Scholar
  91. Swan, S. H., Elkin, E. P., & Fenster, L. (1997). Have sperm densities declined? A reanalysis of global trend data. Environmental Health Perspectives, 105(11), 1228–1232.Google Scholar
  92. Swan, S. H., Elkin, E. P., & Fenster, L. (2000). The question of declining sperm density revisited: An analysis of 101 studies published 1934–1996. Environmental Health Perspectives, 108(10), 961–966.Google Scholar
  93. Swan, S. H., Brazil, C., Drobnis, E. Z., Liu, F., Kruse, R. L., Hatch, M., et al. (2003). Geographic differences in semen quality of fertile U.S. Males. Environmental Health Perspectives, 111(4), 414–420.Google Scholar
  94. Swan, S. H., Main, K. M., Liu, F., Stewart, S. L., Kruse, R. L., Calafat, A. M., et al. (2005). Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environmental Health Perspectives, 113(8), 1056–1061.Google Scholar
  95. Toppari, J. (2008). Environmental endocrine disrupters. Sexual Development, 2(4–5), 260–267.Google Scholar
  96. Toppari, J., Larsen, J. C., Christiansen, P., Giwercman, A., Grandjean, P., Guillette, L. J., Jr., et al. (1996). Male reproductive health and environmental xenoestrogens. Environmental Health Perspectives, 104(Supplement 4), 741–803.Google Scholar
  97. Toppari, J., Kaleva, M., & Virtanen, H. E. (2001). Trends in the incidence of cryptorchidism and hypospadias, and methodological limitations of registry-based data. Human Reproduction Update, 7(3), 282–286.Google Scholar
  98. Tuomisto, J., Holl, K., Rantakokko, P., Koskela, P., Hallmans, G., Wadell, G., et al. (2009). Maternal smoking during pregnancy and testicular cancer in the sons: A nested case-control study and a meta-analysis. European Journal of Cancer, 45(9), 1640–1648.Google Scholar
  99. United Nations. (2007). World population prospects: The 2006 revision. New York: United Nations.Google Scholar
  100. Vine, M. F., Margolin, B. H., Morrison, H. I., & Hulka, B. S. (1994). Cigarette smoking and sperm density: A meta-analysis. Fertility and Sterility, 61(1), 35–43.Google Scholar
  101. Vine, M. F., Setzer, R. W., Jr., Everson, R. B., & Wyrobek, A. J. (1997). Human sperm morphometry and smoking, caffeine, and alcohol consumption. Reproductive Toxicology, 11(2–3), 179–184.Google Scholar
  102. Vinggaard, A. M., Hass, U., Dalgaard, M., Andersen, H. R., Bonefeld-Jørgensen, E., Christiansen, S., et al. (2006). Prochloraz: An imidazole fungicide with multiple mechanisms of action. International Journal of Andrology, 29(1), 186–192.Google Scholar
  103. Weidner, I. S., Møller, H., Jensen, T. K., & Skakkebæk, N. E. (1999). Risk factors for cryptorchidism and hypospadias. Journal of Urology, 161(5), 1606–1609.Google Scholar
  104. Welsh, M., Saunders, P. T., Fisken, M., Scott, H. M., Hutchison, G. R., Smith, L. B., et al. (2008). Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. Journal of Clinical Investigation, 118(4), 1479–1490.Google Scholar
  105. Welshons, W. V., Nagel, S. C., & vom Saal, F. S. (2006). Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol a at levels of human exposure. Endocrinology, 147(Suppl 6), S56–S69.Google Scholar
  106. WHO (World Health Organisation). (2010). WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction (5th ed.). http://whqlibdoc.who.int/publications/2010/9789241547789_eng.pdf

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© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Tina Harmer Lassen
    • 1
  • Teruaki Iwamoto
    • 2
  • Tina Kold Jensen
    • 1
    • 3
  • Niels E. Skakkebæk
    • 1
    Email author
  1. 1.University Department of Growth and Reproduction, RigshospitaletCopenhagenDenmark
  2. 2.Division of Male Infertility, Center for Infertility and IVFInternational University of Health and Welfare HospitalNasushiobaraJapan
  3. 3.Department of Environmental MedicineUniversity of Southern DenmarkOdenseDenmark

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