Impact of Paternal Exposure to Gonadotoxins on Embryo and Offspring and the Male Evaluation

  • Kathleen Hwang
  • Paul Gittens
  • Desiderio AvilaJr.
  • Larry I. Lipshultz
Chapter

Abstract

There are several routes of exposure to gonadotoxins for the male. Exposures originate from lifestyle choices, medications, and treatment for malignancies, as well as occupational and chemical hazards. Regardless of the route, the impact of paternal exposure to gonadotoxins on subsequent fertility is significant as it not only affects the individual, but may also affect future offspring. Given the increasing popularity of in vitro fertilization (IVF)/intracytoplasmic sperm injection (ICSI) and the vast numbers of procedures performed each year throughout the world, continued research on the safety of IVF/ICSI and IVF itself is crucial. Patients can only truly give informed consent when they are properly educated as to all the associated risks.

Keywords

Gonadotoxin effect on embryo and offspring Chemotherapy and radiation effects on male fertility Cancer treatment effects on gonads 

References

  1. 1.
    Thonneau P, Marchand S, Tallec A, et al. Incidence and main causes of infertility in a resident population (1,850,000) of three French regions (1988–1989). Hum Reprod. 1991;6:811.PubMedGoogle Scholar
  2. 2.
    Padron OF, Sharma RK, Thomas Jr AJ, et al. Effects of cancer on spermatozoa quality after cryopreservation: a 12-year experience. Fertil Steril. 1997;67:326.PubMedCrossRefGoogle Scholar
  3. 3.
    Costabile RA, Spevak M. Cancer and male factor infertility. Oncology (Williston Park). 1998;12:557.Google Scholar
  4. 4.
    Shukla AR, Woodard C, Carr MC, et al. Experience with testis sparing surgery for testicular teratoma. J Urol. 2004;171:161.PubMedCrossRefGoogle Scholar
  5. 5.
    Petersen PM, Skakkebaek NE, Rorth M, et al. Semen quality and reproductive hormones before and after orchiectomy in men with testicular cancer. J Urol. 1999;161:822.PubMedCrossRefGoogle Scholar
  6. 6.
    Halstead LS, VerVoort S, Seager SW. Rectal probe electrostimulation in the treatment of anejaculatory spinal cord injured men. Paraplegia. 1987;25:120.PubMedCrossRefGoogle Scholar
  7. 7.
    Kamischke A, Nieschlag E. Treatment of retrograde ejaculation and anejaculation. Hum Reprod Update. 1999;5:448.PubMedCrossRefGoogle Scholar
  8. 8.
    Thomson AB, Critchley HO, Kelnar CJ, et al. Late reproductive sequelae following treatment of childhood cancer and options for fertility preservation. Best Pract Res Clin Endocrinol Metab. 2002;16:311.PubMedCrossRefGoogle Scholar
  9. 9.
    Stahl O, Eberhard J, Jepson K, et al. Sperm DNA integrity in testicular cancer patients. Hum Reprod. 2006;21:3199.PubMedCrossRefGoogle Scholar
  10. 10.
    Shalet SM, Tsatsoulis A, Whitehead E, et al. Vulnerability of the human Leydig cell to radiation damage is dependent upon age. J Endocrinol. 1989;120:161.PubMedCrossRefGoogle Scholar
  11. 11.
    Howell SJ, Shalet SM. Spermatogenesis after cancer treatment: damage and recovery. J Natl Cancer Inst Monogr. 2005;34:12–7.PubMedCrossRefGoogle Scholar
  12. 12.
    Giwercman A, Petersen PM. Cancer and male infertility. Baillieres Best Pract Res Clin Endocrinol Metab. 2000;14:453.PubMedCrossRefGoogle Scholar
  13. 13.
    Lee SJ, Schover LR, Partridge AH, et al. American Society of Clinical Oncology recommendations on fertility preservation in cancer patients. J Clin Oncol. 2006;24:2917.PubMedCrossRefGoogle Scholar
  14. 14.
    Pryzant RM, Meistrich ML, Wilson G, et al. Long-term reduction in sperm count after chemotherapy with and without radiation therapy for non-Hodgkin’s lymphomas. J Clin Oncol. 1993;11:239.PubMedGoogle Scholar
  15. 15.
    Fossa SD, Magelssen H. Fertility and reproduction after chemotherapy of adult cancer patients: malignant lymphoma and testicular cancer. Ann Oncol. 2004;15 Suppl 4:iv259.PubMedCrossRefGoogle Scholar
  16. 16.
    Martin RH, Ernst S, Rademaker A, et al. Analysis of sperm chromosome complements before, during, and after chemotherapy. Cancer Genet Cytogenet. 1999;108:133.PubMedCrossRefGoogle Scholar
  17. 17.
    De Mas P, Daudin M, Vincent MC, et al. Increased aneuploidy in spermatozoa from testicular tumour patients after chemotherapy with cisplatin, etoposide and bleomycin. Hum Reprod. 2001;16:1204.PubMedCrossRefGoogle Scholar
  18. 18.
    Tempest HG, Ko E, Chan P, et al. Sperm aneuploidy frequencies analysed before and after chemotherapy in testicular cancer and Hodgkin’s lymphoma patients. Hum Reprod. 2008;23:251.PubMedCrossRefGoogle Scholar
  19. 19.
    Carlsen E, Giwercman A, Keiding N, et al. Evidence for decreasing quality of semen during past 50 years. BMJ. 1992;305:609.PubMedCrossRefGoogle Scholar
  20. 20.
    Paulozzi LJ. International trends in rates of hypospadias and cryptorchidism. Environ Health Perspect. 1999;107:297.PubMedCrossRefGoogle Scholar
  21. 21.
    Huyghe E, Matsuda T, Thonneau P. Increasing incidence of testicular cancer worldwide: a review. J Urol. 2003;170:5.PubMedCrossRefGoogle Scholar
  22. 22.
    Whorton D, Krauss RM, Marshall S, et al. Infertility in male pesticide workers. Lancet. 1977;2:1259.PubMedCrossRefGoogle Scholar
  23. 23.
    Anway MD, Cupp AS, Uzumcu M, et al. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005;308:1466.PubMedCrossRefGoogle Scholar
  24. 24.
    Wittassek M, Wiesmuller GA, Koch HM, et al. Internal phthalate exposure over the last two decades – a retrospective human biomonitoring study. Int J Hyg Environ Health. 2007;210:319.PubMedCrossRefGoogle Scholar
  25. 25.
    Duty SM, Silva MJ, Barr DB, et al. Phthalate exposure and human semen parameters. Epidemiology. 2003;14:269.PubMedGoogle Scholar
  26. 26.
    Hauser R, Meeker JD, Singh NP, et al. DNA damage in human sperm is related to urinary levels of phthalate monoester and oxidative metabolites. Hum Reprod. 2007;22:688.PubMedCrossRefGoogle Scholar
  27. 27.
    Kamijima M, Hibi H, Gotoh M, et al. A survey of semen indices in insecticide sprayers. J Occup Health. 2004;46:109.PubMedCrossRefGoogle Scholar
  28. 28.
    Swan SH, Kruse RL, Liu F, et al. Semen quality in relation to biomarkers of pesticide exposure. Environ Health Perspect. 2003;111:1478.PubMedCrossRefGoogle Scholar
  29. 29.
    Recio R, Robbins WA, Borja-Aburto V, et al. Organophosphorous pesticide exposure increases the frequency of sperm sex null aneuploidy. Environ Health Perspect. 2001;109:1237.PubMedCrossRefGoogle Scholar
  30. 30.
    Smith JL, Garry VF, Rademaker AW, et al. Human sperm aneuploidy after exposure to pesticides. Mol Reprod Dev. 2004;67:353.PubMedCrossRefGoogle Scholar
  31. 31.
    vom Saal FS, Cooke PS, Buchanan DL, et al. A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol Ind Health. 1998;14:239.PubMedGoogle Scholar
  32. 32.
    Steinmetz R, Brown NG, Allen DL, et al. The environmental estrogen bisphenol A stimulates prolactin release in vitro and in vivo. Endocrinology. 1997;138:1780.PubMedCrossRefGoogle Scholar
  33. 33.
    Krishnan AV, Stathis P, Permuth SF, et al. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology. 1993; 132:2279.PubMedCrossRefGoogle Scholar
  34. 34.
    Calafat AM, Kuklenyik Z, Reidy JA, et al. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect. 2005;113:391.PubMedCrossRefGoogle Scholar
  35. 35.
    Ikezuki Y, Tsutsumi O, Takai Y, et al. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod. 2002;17:2839.PubMedCrossRefGoogle Scholar
  36. 36.
    Sun Y, Irie M, Kishikawa N, et al. Determination of bisphenol A in human breast milk by HPLC with column-switching and fluorescence detection. Biomed Chromatogr. 2004;18:501.PubMedCrossRefGoogle Scholar
  37. 37.
    Takeuchi T, Tsutsumi O, Ikezuki Y, et al. Positive relationship between androgen and the endocrine disruptor, bisphenol A, in normal women and women with ovarian dysfunction. Endocr J. 2004;51:165.PubMedCrossRefGoogle Scholar
  38. 38.
    Yamada H, Furuta I, Kato EH, et al. Maternal serum and amniotic fluid bisphenol A concentrations in the early second trimester. Reprod Toxicol. 2002;16:735.PubMedCrossRefGoogle Scholar
  39. 39.
    Sugiura-Ogasawara M, Ozaki Y, Sonta S, et al. Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod. 2005;20:2325.PubMedCrossRefGoogle Scholar
  40. 40.
    Bagchi G, Hurst CH, Waxman DJ. Interactions of methoxyacetic acid with androgen receptor. Toxicol Appl Pharmacol. 2009;238:101.PubMedCrossRefGoogle Scholar
  41. 41.
    Miller RR, Carreon RE, Young JT, et al. Toxicity of methoxyacetic acid in rats. Fundam Appl Toxicol. 1982;2:158.PubMedCrossRefGoogle Scholar
  42. 42.
    Welch LS, Schrader SM, Turner TW, et al. Effects of exposure to ethylene glycol ethers on shipyard painters: II. Male reproduction. Am J Ind Med. 1988;14:509.PubMedCrossRefGoogle Scholar
  43. 43.
    Cherry N, Moore H, McNamee R, et al. Occupation and male infertility: glycol ethers and other exposures. Occup Environ Med. 2008;65:708.PubMedCrossRefGoogle Scholar
  44. 44.
    Emanuele MA, Emanuele NV. Alcohol’s effects on male reproduction. Alcohol Health Res World. 1998;22:195.PubMedGoogle Scholar
  45. 45.
    Muthusami KR, Chinnaswamy P. Effect of chronic alcoholism on male fertility hormones and semen quality. Fertil Steril. 2005;84:919.PubMedCrossRefGoogle Scholar
  46. 46.
    Vicari E, Arancio A, Giuffrida V, et al. A case of reversible azoospermia following withdrawal from alcohol consumption. J Endocrinol Invest. 2002;25:473.PubMedGoogle Scholar
  47. 47.
    Villalta J, Ballesca JL, Nicolas JM, et al. Testicular function in asymptomatic chronic alcoholics: relation to ethanol intake. Alcohol Clin Exp Res. 1997;21:128.PubMedGoogle Scholar
  48. 48.
    Donnelly GP, McClure N, Kennedy MS, et al. Direct effect of alcohol on the motility and morphology of human spermatozoa. Andrologia. 1999;31:43.PubMedGoogle Scholar
  49. 49.
    Emanuele NV, LaPagli N, Steiner J, et al. Peripubertal paternal EtOH exposure. Endocrine. 2001;14:213.PubMedCrossRefGoogle Scholar
  50. 50.
    Orleans CT. Increasing the demand for and use of effective smoking-cessation treatments reaping the full health benefits of tobacco-control science and policy gains – in our lifetime. Am J Prev Med. 2007;33:S340.PubMedCrossRefGoogle Scholar
  51. 51.
    Kulikauskas V, Blaustein D, Ablin RJ. Cigarette smoking and its possible effects on sperm. Fertil Steril. 1985;44:526.PubMedGoogle Scholar
  52. 52.
    Sepaniak S, Forges T, Fontaine B, et al. Negative impact of cigarette smoking on male fertility: from spermatozoa to the offspring. J Gynecol Obstet Biol Reprod (Paris). 2004;33:384.CrossRefGoogle Scholar
  53. 53.
    Trummer H, Habermann H, Haas J, et al. The impact of cigarette smoking on human semen parameters and hormones. Hum Reprod. 2002;17:1554.PubMedCrossRefGoogle Scholar
  54. 54.
    Saleh RA, Agarwal A, Sharma RK, et al. Effect of cigarette smoking on levels of seminal oxidative stress in infertile men: a prospective study. Fertil Steril. 2002;78:491.PubMedCrossRefGoogle Scholar
  55. 55.
    Hull MG, North K, Taylor H, et al. Delayed conception and active and passive smoking. The Avon Longitudinal Study of Pregnancy and Childhood Study Team. Fertil Steril. 2000;74:725.PubMedCrossRefGoogle Scholar
  56. 56.
    Zenzes MT, Puy LA, Bielecki R, et al. Detection of benzo[a]pyrene diol epoxide-DNA adducts in embryos from smoking couples: evidence for transmission by spermatozoa. Mol Hum Reprod. 1999;5:125.PubMedCrossRefGoogle Scholar
  57. 57.
    Compton WM, Grant BF, Colliver JD, et al. Prevalence of marijuana use disorders in the United States: 1991–1992 and 2001–2002. JAMA. 2004;291:2114.PubMedCrossRefGoogle Scholar
  58. 58.
    Close CE, Roberts PL, Berger RE. Cigarettes, alcohol and marijuana are related to pyospermia in infertile men. J Urol. 1990;144:900.PubMedGoogle Scholar
  59. 59.
    Rossato M, Pagano C, Vettor R. The cannabinoid system and male reproductive functions. J Neuro­endocrinol. 2008;20 Suppl 1:90.PubMedCrossRefGoogle Scholar
  60. 60.
    Robbins WA, Elashoff DA, Xun L, et al. Effect of lifestyle exposures on sperm aneuploidy. Cytogenet Genome Res. 2005;111:371.PubMedCrossRefGoogle Scholar
  61. 61.
    Robbins WA, Vine MF, Truong KY, et al. Use of fluorescence in situ hybridization (FISH) to assess effects of smoking, caffeine, and alcohol on aneuploidy load in sperm of healthy men. Environ Mol Mutagen. 1997;30:175.PubMedCrossRefGoogle Scholar
  62. 62.
    Rubes J, Lowe X, Moore II D, et al. Smoking cigarettes is associated with increased sperm disomy in teenage men. Fertil Steril. 1998;70:715.PubMedCrossRefGoogle Scholar
  63. 63.
    Tidd MJ, Horth CE, Ramsay LE, et al. Endocrine effects of spironolactone in man. Clin Endocrinol Oxf. 1978;9:389.PubMedCrossRefGoogle Scholar
  64. 64.
    Benoff S, Cooper GW, Hurley I, et al. The effect of calcium ion channel blockers on sperm fertilization potential. Fertil Steril. 1994;62:606.PubMedGoogle Scholar
  65. 65.
    Nelson WO, Bunge RG. The effect of therapeutic dosages of nitrofurantoin (furadantin) upon spermatogenesis in man. J Urol. 1957;77:275.PubMedGoogle Scholar
  66. 66.
    Hargreaves CA, Rogers S, Hills F, et al. Effects of co-trimoxazole, erythromycin, amoxycillin, tetracycline and chloroquine on sperm function in vitro. Hum Reprod. 1998;13:1878.PubMedCrossRefGoogle Scholar
  67. 67.
    Birnie GG, McLeod TI, Watkinson G. Incidence of sulphasalazine-induced male infertility. Gut. 1981; 22:452.PubMedCrossRefGoogle Scholar
  68. 68.
    Sarica K, Suzer O, Gurler A, et al. Urological evaluation of Behcet patients and the effect of colchicine on fertility. Eur Urol. 1995;27:39.PubMedGoogle Scholar
  69. 69.
    Baumgartner A, Schmid TE, Schuetz CG, et al. Detection of aneuploidy in rodent and human sperm by multicolor FISH after chronic exposure to diazepam. Mutat Res. 2001;490:11.PubMedCrossRefGoogle Scholar
  70. 70.
    Collodel G, Scapigliati G, Moretti E. Spermatozoa and chronic treatment with finasteride: a TEM and FISH study. Arch Androl. 2007;53:229.PubMedCrossRefGoogle Scholar
  71. 71.
    Carlsen E, Petersen JH, Andersson AM, et al. Effects of ejaculatory frequency and season on variations in semen quality. Fertil Steril. 2004;82:358.PubMedCrossRefGoogle Scholar
  72. 72.
    Guzick DS, Overstreet JW, Factor-Litvak P, et al. Sperm morphology, motility, and concentration in ­fertile and infertile men. N Engl J Med. 2001;345:1388.PubMedCrossRefGoogle Scholar
  73. 73.
    World Health Organization. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction, 4th ed. Cambridge: World Health Organization, Published on behalf of the World Health Organization by Cambridge University Press; 1999, p. 128.Google Scholar
  74. 74.
    Cooper TG, Noonan E, von Eckardstein S, et al. World Health Organization reference values for human semen characteristics. Hum Reprod Update. 2010;16:231.PubMedCrossRefGoogle Scholar
  75. 75.
    Keck C, Gerber-Schafer C, Clad A, et al. Seminal tract infections: impact on male fertility and treatment options. Hum Reprod Update. 1998;4:891.PubMedCrossRefGoogle Scholar
  76. 76.
    Colpi GM, Lange A. Diagnostic usefulness of study of the round cells in seminal fluid. Acta Eur Fertil. 1984;15:265.PubMedGoogle Scholar
  77. 77.
    Wolff H. The biologic significance of white blood cells in semen. Fertil Steril. 1995;63:1143.PubMedGoogle Scholar
  78. 78.
    Prathalingam NS, Holt WW, Revell SG, et al. The precision and accuracy of six different methods to determine sperm concentration. J Androl. 2006;27:257.PubMedCrossRefGoogle Scholar
  79. 79.
    Tomlinson M, Turner J, Powell G, et al. One-step disposable chambers for sperm concentration and motility assessment: how do they compare with the World Health Organization’s recommended methods? Hum Reprod. 2001;16:121.PubMedCrossRefGoogle Scholar
  80. 80.
    World-Health-Organization. WHO laboratory manual for the examination and processing of human semen. 5th ed. Geneva: World-Health-Organization; 2010.Google Scholar
  81. 81.
    Bostofte E, Bagger P, Michael A, et al. Fertility prognosis for infertile men: results of follow-up study of semen analysis in infertile men from two different populations evaluated by the Cox regression model. Fertil Steril. 1990;54:1100.PubMedGoogle Scholar
  82. 82.
    Mayaux MJ, Schwartz D, Czyglik F, et al. Conception rate according to semen characteristics in a series of 15 364 insemination cycles: results of a multivariate analysis. Andrologia. 1985;17:9.PubMedCrossRefGoogle Scholar
  83. 83.
    Kruger TF, Menkveld R, Stander FS, et al. Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil Steril. 1986;46:1118.PubMedGoogle Scholar
  84. 84.
    Mortimer D, Menkveld R. Sperm morphology assessment – historical perspectives and current opinions. J Androl. 2001;22:192.PubMedGoogle Scholar
  85. 85.
    Celik-Ozenci C, Jakab A, Kovacs T, et al. Sperm selection for ICSI: shape properties do not predict the absence or presence of numerical chromosomal aberrations. Hum Reprod. 2004;19:2052.PubMedCrossRefGoogle Scholar
  86. 86.
    Ryu HM, Lin WW, Lamb DJ, et al. Increased chromosome X, Y, and 18 nondisjunction in sperm from infertile patients that were identified as normal by strict morphology: implication for intracytoplasmic sperm injection. Fertil Steril. 2001;76:879.PubMedCrossRefGoogle Scholar
  87. 87.
    Aitken RJ. A free radical theory of male infertility. Reprod Fertil Dev. 1994;6:19.PubMedCrossRefGoogle Scholar
  88. 88.
    Aitken RJ, Baker MA, Sawyer D. Oxidative stress in the male germ line and its role in the aetiology of male infertility and genetic disease. Reprod Biomed Online. 2003;7:65.PubMedCrossRefGoogle Scholar
  89. 89.
    Griveau JF, Le Lannou D. Reactive oxygen species and human spermatozoa: physiology and pathology. Int J Androl. 1997;20:61.PubMedCrossRefGoogle Scholar
  90. 90.
    Henkel R, Hajimohammad M, Stalf T, et al. Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil Steril. 2004;81:965.PubMedCrossRefGoogle Scholar
  91. 91.
    Iwasaki A, Gagnon C. Formation of reactive oxygen species in spermatozoa of infertile patients. Fertil Steril. 1992;57:409.PubMedGoogle Scholar
  92. 92.
    Aitken RJ, Irvine DS, Wu FC. Prospective analysis of sperm-oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am J Obstet Gynecol. 1991;164:542.PubMedGoogle Scholar
  93. 93.
    Sukcharoen N, Keith J, Irvine DS, et al. Prediction of the in-vitro fertilization (IVF) potential of human spermatozoa using sperm function tests: the effect of the delay between testing and IVF. Hum Reprod. 1996;11:1030.PubMedCrossRefGoogle Scholar
  94. 94.
    Hammadeh ME, Radwan M, Al-Hasani S, et al. Comparison of reactive oxygen species concentration in seminal plasma and semen parameters in partners of pregnant and non-pregnant patients after IVF/ICSI. Reprod Biomed Online. 2006;13:696.PubMedCrossRefGoogle Scholar
  95. 95.
    McKinney KA, Lewis SE, Thompson W. Reactive oxygen species generation in human sperm: luminol and lucigenin chemiluminescence probes. Arch Androl. 1996;36:119.PubMedCrossRefGoogle Scholar
  96. 96.
    Aitken RJ, West KM. Analysis of the relationship between reactive oxygen species production and ­leucocyte infiltration in fractions of human semen separated on Percoll gradients. Int J Androl. 1990; 13:433.PubMedCrossRefGoogle Scholar
  97. 97.
    Saleh RA, Agarwal A, Kandirali E, et al. Leukocytospermia is associated with increased reactive oxygen species production by human spermatozoa. Fertil Steril. 2002;78:1215.PubMedCrossRefGoogle Scholar
  98. 98.
    Aitken RJ, Buckingham DW, West K, et al. On the use of paramagnetic beads and ferrofluids to assess and eliminate the leukocytic contribution to oxygen radical generation by human sperm suspensions. Am J Reprod Immunol. 1996;35:541.PubMedCrossRefGoogle Scholar
  99. 99.
    Shekarriz M, DeWire DM, Thomas Jr AJ, et al. A method of human semen centrifugation to minimize the iatrogenic sperm injuries caused by reactive oxygen species. Eur Urol. 1995;28:31.PubMedGoogle Scholar
  100. 100.
    Aitken RJ, Baker MA, O’Bryan M. Shedding light on chemiluminescence: the application of chemiluminescence in diagnostic andrology. J Androl. 2004;25:455.PubMedGoogle Scholar
  101. 101.
    Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil. 1987;81:459.PubMedCrossRefGoogle Scholar
  102. 102.
    Kobayashi H, Gil-Guzman E, Mahran AM, et al. Quality control of reactive oxygen species measurement by luminol-dependent chemiluminescence assay. J Androl. 2001;22:568.PubMedGoogle Scholar
  103. 103.
    Kodama H, Yamaguchi R, Fukuda J, et al. Increased oxidative deoxyribonucleic acid damage in the spermatozoa of infertile male patients. Fertil Steril. 1997;68:519.PubMedCrossRefGoogle Scholar
  104. 104.
    Spano M, Bonde JP, Hjollund HI, et al. Sperm chromatin damage impairs human fertility. The Danish First Pregnancy Planner Study Team. Fertil Steril. 2000;73:43.PubMedCrossRefGoogle Scholar
  105. 105.
    Evenson DP, Jost LK, Marshall D, et al. Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod. 1999;14:1039.PubMedCrossRefGoogle Scholar
  106. 106.
    Duran EH, Morshedi M, Taylor S, et al. Sperm DNA quality predicts intrauterine insemination outcome: a prospective cohort study. Hum Reprod. 2002;17:3122.PubMedCrossRefGoogle Scholar
  107. 107.
    Sun JG, Jurisicova A, Casper RF. Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod. 1997;56:602.PubMedCrossRefGoogle Scholar
  108. 108.
    Lopes S, Sun JG, Jurisicova A, et al. Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril. 1998;69:528.PubMedCrossRefGoogle Scholar
  109. 109.
    Bungum M, Humaidan P, Axmon A, et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod. 2007;22:174.PubMedCrossRefGoogle Scholar
  110. 110.
    Huang CC, Lin DP, Tsao HM, et al. Sperm DNA fragmentation negatively correlates with velocity and fertilization rates but might not affect pregnancy rates. Fertil Steril. 2005;84:130.PubMedCrossRefGoogle Scholar
  111. 111.
    Gandini L, Lombardo F, Paoli D, et al. Full-term pregnancies achieved with ICSI despite high levels of sperm chromatin damage. Hum Reprod. 2004;19:1409.PubMedCrossRefGoogle Scholar
  112. 112.
    Jurisicova A, Varmuza S, Casper RF. Programmed cell death and human embryo fragmentation. Mol Hum Reprod. 1996;2:93.PubMedCrossRefGoogle Scholar
  113. 113.
    Tesarik J, Mendoza C, Greco E. Paternal effects acting during the first cell cycle of human preimplantation development after ICSI. Hum Reprod. 2002;17:184.PubMedCrossRefGoogle Scholar
  114. 114.
    Sakkas D, Mariethoz E, St John JC. Abnormal sperm parameters in humans are indicative of an abortive apoptotic mechanism linked to the Fas-mediated pathway. Exp Cell Res. 1999;251:350.PubMedCrossRefGoogle Scholar
  115. 115.
    Sakkas D, Moffatt O, Manicardi GC, et al. Nature of DNA damage in ejaculated human spermatozoa and the possible involvement of apoptosis. Biol Reprod. 2002;66:1061.PubMedCrossRefGoogle Scholar
  116. 116.
    Aoki VW, Moskovtsev SI, Willis J, et al. DNA integrity is compromised in protamine-deficient human sperm. J Androl. 2005;26:741.PubMedCrossRefGoogle Scholar
  117. 117.
    Iguchi N, Yang S, Lamb DJ, et al. An SNP in protamine 1: a possible genetic cause of male infertility? J Med Genet. 2006;43:382.PubMedCrossRefGoogle Scholar
  118. 118.
    Tremellen K. Oxidative stress and male infertility – a clinical perspective. Hum Reprod Update. 2008;14:243.PubMedCrossRefGoogle Scholar
  119. 119.
    Greco E, Iacobelli M, Rienzi L, et al. Reduction of the incidence of sperm DNA fragmentation by oral antioxidant treatment. J Androl. 2005;26:349.PubMedCrossRefGoogle Scholar
  120. 120.
    Smith R, Kaune H, Parodi D, et al. Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod. 2006;21:986.PubMedCrossRefGoogle Scholar
  121. 121.
    Werthman P, Wixon R, Kasperson K, et al. Significant decrease in sperm deoxyribonucleic acid fragmentation after varicocelectomy. Fertil Steril. 2008;90:1800.PubMedCrossRefGoogle Scholar
  122. 122.
    Zini A, Blumenfeld A, Libman J, et al. Beneficial effect of microsurgical varicocelectomy on human sperm DNA integrity. Hum Reprod. 2005;20:1018.PubMedCrossRefGoogle Scholar
  123. 123.
    Smit M, Romijn JC, Wildhagen MF, et al. Decreased sperm DNA fragmentation after surgical varicocelectomy is associated with increased pregnancy rate. J Urol. 2010;183:270.PubMedCrossRefGoogle Scholar
  124. 124.
    Potts RJ, Newbury CJ, Smith G, et al. Sperm chromatin damage associated with male smoking. Mutat Res. 1999;423:103.PubMedCrossRefGoogle Scholar
  125. 125.
    Pasqualotto FF, Sharma RK, Potts JM, et al. Seminal oxidative stress in patients with chronic prostatitis. Urology. 2000;55:881.PubMedCrossRefGoogle Scholar
  126. 126.
    O’Connell M, McClure N, Lewis SE. Mitochondrial DNA deletions and nuclear DNA fragmentation in testicular and epididymal human sperm. Hum Reprod. 2002;17:1565.PubMedCrossRefGoogle Scholar
  127. 127.
    Greco E, Scarselli F, Iacobelli M, et al. Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. Hum Reprod. 2005;20:226.PubMedCrossRefGoogle Scholar
  128. 128.
    Dohle GR. Male infertility in cancer patients: review of the literature. Int J Urol. 2010;17:327.PubMedCrossRefGoogle Scholar
  129. 129.
    van der Horst-Schrivers AN, van Ieperen E, Wymenga AN, et al. Sexual function in patients with metastatic midgut carcinoid tumours. Neuroen­docrinology. 2009;89:231.PubMedCrossRefGoogle Scholar
  130. 130.
    The practice Committee of the Society for Assisted Reproductive Technology and the Practice committee of the American Society for Reproductive Medicine. Preimplantation genetic testing: a Practice Committee opinion. Fertil Steril. 2007;88:1497.CrossRefGoogle Scholar
  131. 131.
    Helmerhorst FM, Perquin DA, Donker D, et al. Perinatal outcome of singletons and twins after assisted conception: a systematic review of controlled studies. BMJ. 2004;328:261.PubMedCrossRefGoogle Scholar
  132. 132.
    Jackson RA, Gibson KA, Wu YW, et al. Perinatal outcomes in singletons following in vitro fertilization: a meta-analysis. Obstet Gynecol. 2004; 103:551.PubMedCrossRefGoogle Scholar
  133. 133.
    The ESHRE Capri Workshop Group. Intracytoplasmic sperm injection (ICSI) in 2006: evidence and evolution. Hum Reprod Update. 2007;13:515.CrossRefGoogle Scholar
  134. 134.
    Schlegel PN, Shin D, Goldstein M. Urogenital anomalies in men with congenital absence of the vas deferens. J Urol. 1996;155:1644.PubMedCrossRefGoogle Scholar
  135. 135.
    Anguiano A, Oates RD, Amos JA, et al. Congenital bilateral absence of the vas deferens. A primarily genital form of cystic fibrosis. JAMA. 1992;267: 1794.PubMedCrossRefGoogle Scholar
  136. 136.
    McCallum T, Milunsky J, Munarriz R, et al. Unilateral renal agenesis associated with congenital bilateral absence of the vas deferens: phenotypic findings and genetic considerations. Hum Reprod. 2001;16:282.PubMedCrossRefGoogle Scholar
  137. 137.
    O’Flynn O’Brien KL, Varghese AC, Agarwal A. The genetic causes of male factor infertility: a review. Fertil Steril. 2010;93:1.PubMedCrossRefGoogle Scholar
  138. 138.
    Ferlin A, Raicu F, Gatta V, et al. Male infertility: role of genetic background. Reprod Biomed Online. 2007;14:734.PubMedCrossRefGoogle Scholar
  139. 139.
    Denschlag D, Tempfer C, Kunze M, et al. Assisted reproductive techniques in patients with Klinefelter syndrome: a critical review. Fertil Steril. 2004;82:775.PubMedCrossRefGoogle Scholar
  140. 140.
    Nielsen J, Wohlert M. Chromosome abnormalities found among 34,910 newborn children: results from a 13-year incidence study in Arhus, Denmark. Hum Genet. 1991;87:81.PubMedCrossRefGoogle Scholar
  141. 141.
    Engels H, Eggermann T, Caliebe A, et al. Genetic counseling in Robertsonian translocations der(13;14): frequencies of reproductive outcomes and infertility in 101 pedigrees. Am J Med Genet A. 2008; 146A:2611.PubMedCrossRefGoogle Scholar
  142. 142.
    Kuroda-Kawaguchi T, Skaletsky H, Brown LG, et al. The AZFc region of the Y chromosome features massive palindromes and uniform recurrent deletions in infertile men. Nat Genet. 2001;29:279.PubMedCrossRefGoogle Scholar
  143. 143.
    Hopps CV, Mielnik A, Goldstein M, et al. Detection of sperm in men with Y chromosome microdeletions of the AZFa, AZFb and AZFc regions. Hum Reprod. 2003;18:1660.PubMedCrossRefGoogle Scholar
  144. 144.
    Kaufman GE, Malone FD, Harvey-Wilkes KB, et al. Neonatal morbidity and mortality associated with triplet pregnancy. Obstet Gynecol. 1998;91:342.PubMedCrossRefGoogle Scholar
  145. 145.
    Pinborg A. IVF/ICSI twin pregnancies: risks and prevention. Hum Reprod Update. 2005;11:575.PubMedCrossRefGoogle Scholar
  146. 146.
    Klemetti R, Gissler M, Sevon T, et al. Children born after assisted fertilization have an increased rate of major congenital anomalies. Fertil Steril. 2005; 84:1300.PubMedCrossRefGoogle Scholar
  147. 147.
    Reddy UM, Wapner RJ, Rebar RW, et al. Infertility, assisted reproductive technology, and adverse ­pregnancy outcomes: executive summary of a National Institute of Child Health and Human Development workshop. Obstet Gynecol. 2007; 109:967.PubMedCrossRefGoogle Scholar
  148. 148.
    Hansen M, Kurinczuk JJ, Bower C, et al. The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization. N Engl J Med. 2002;346:725.PubMedCrossRefGoogle Scholar
  149. 149.
    Zhu JL, Basso O, Obel C, et al. Infertility, infertility treatment, and congenital malformations: Danish national birth cohort. BMJ. 2006;333:679.PubMedCrossRefGoogle Scholar
  150. 150.
    Koivurova S, Hartikainen AL, Gissler M, et al. Neonatal outcome and congenital malformations in children born after in-vitro fertilization. Hum Reprod. 2002;17:1391.PubMedCrossRefGoogle Scholar
  151. 151.
    Ludwig M, Katalinic A. Malformation rate in fetuses and children conceived after ICSI: results of a prospective cohort study. Reprod Biomed Online. 2002;5:171.PubMedCrossRefGoogle Scholar
  152. 152.
    Anthony S, Buitendijk SE, Dorrepaal CA, et al. Congenital malformations in 4224 children conceived after IVF. Hum Reprod. 2002;17:2089.PubMedCrossRefGoogle Scholar
  153. 153.
    Ericson A, Kallen B. Congenital malformations in infants born after IVF: a population-based study. Hum Reprod. 2001;16:504.PubMedCrossRefGoogle Scholar
  154. 154.
    Sutcliffe AG, D’Souza SW, Cadman J, et al. Minor congenital anomalies, major congenital malformations and development in children conceived from cryopreserved embryos. Hum Reprod. 1995; 10:3332.PubMedGoogle Scholar
  155. 155.
    Olson CK, Keppler-Noreuil KM, Romitti PA, et al. In vitro fertilization is associated with an increase in major birth defects. Fertil Steril. 2005;84:1308.PubMedCrossRefGoogle Scholar
  156. 156.
    Lie RT, Lyngstadaas A, Orstavik KH, et al. Birth defects in children conceived by ICSI compared with children conceived by other IVF-methods; a meta-analysis. Int J Epidemiol. 2005;34:696.PubMedCrossRefGoogle Scholar
  157. 157.
    Hansen M, Bower C, Milne E, et al. Assisted reproductive technologies and the risk of birth defects – a systematic review. Hum Reprod. 2005;20:328.PubMedCrossRefGoogle Scholar
  158. 158.
    Bonduelle M, Ponjaert I, Steirteghem AV, et al. Developmental outcome at 2 years of age for children born after ICSI compared with children born after IVF. Hum Reprod. 2003;18:342.PubMedCrossRefGoogle Scholar
  159. 159.
    Zadori J, Kozinszky Z, Orvos H, et al. Dilemma of increased obstetric risk in pregnancies following IVF-ET. J Assist Reprod Genet. 2003;20:216.PubMedCrossRefGoogle Scholar
  160. 160.
    Simpson JL, Lamb DJ. Genetic effects of intracytoplasmic sperm injection. Semin Reprod Med. 2001;19:239.PubMedCrossRefGoogle Scholar
  161. 161.
    Alukal JP, Lipshultz LI. Safety of assisted reproduction, assessed by risk of abnormalities in children born after use of in vitro fertilization techniques. Nat Clin Pract Urol. 2008;5(3):140–50.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Kathleen Hwang
    • 1
  • Paul Gittens
    • 1
  • Desiderio AvilaJr.
    • 1
  • Larry I. Lipshultz
    • 2
  1. 1.Scott Department of UrologyBaylor College of MedicineHoustonUSA
  2. 2.Scott Department of UrologyBaylor College of MedicineHoustonUSA

Personalised recommendations