Environmental Toxins and Male Fertility

Andrology and Infertility (L Lipshultz, Section Editor)
  • 39 Downloads
Part of the following topical collections:
  1. Topical Collection on Andrology and Infertility

Abstract

Purpose of Review

Global industrialization has increased population exposure to environmental toxins. A global decline in sperm quality over the last few decades raises questions about the adverse impact of environmental toxins on male reproductive health.

Recent Findings

Multiple animal- and human-based studies on exposure to environmental toxins suggest a negative impact on semen quality, in terms of sperm concentration, motility, and/or morphology. These toxins may exert estrogenic and/or anti-androgenic effects, which in turn alter the hypothalamic-pituitary-gonadal axis (HPGA), induce sperm DNA damage, or cause sperm epigenetic changes.

Summary

This chapter will discuss the most recent literature about the most common environmental toxins and their impact on spermatogenesis and its consequences on male fertility. Understanding the presence and underlying mechanism of these toxins will help us preserve the integrity of the male reproduction system and formulate better regulations against their indiscriminate use.

Keywords

Environment Environmental toxins Male infertility Sperm Endocrine disrupting chemicals Thermotoxicity 

Notes

Compliance with Ethical Standards

Conflict of Interest

Mahmoud Mima, David Greenwald, and Samuel Ohlander each declare no potential conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

  1. 1.
    Levine H, Jørgensen N, Martino-Andrade A, Mendiola J, Weksler-Derri D, Mindlis I, et al. Temporal trends in sperm count: a systematic review and meta-regression analysis. Hum Reprod Update. 2017;23(6):646–59.CrossRefPubMedGoogle Scholar
  2. 2.
    Jenardhanan P, Panneerselvam M, Mathur PP. Effect of environmental contaminants on spermatogenesis. Semin Cell Dev Biol. 2016;59:126–40.CrossRefPubMedGoogle Scholar
  3. 3.
    Kavlock RJ, Daston GP, DeRosa C, Fenner-Crisp P, Gray LE, Kaattari S, et al. Research needs for the risk assessment of health and environmental effects of endocrine disruptors: a report of the U.S. EPA-sponsored workshop. Environ Health Perspect. 1996;104(Suppl 4):715–40.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Kabir ER, Rahman MS, Rahman I. A review on endocrine disruptors and their possible impacts on human health. Environ Toxicol Pharmacol. 2015;40(1):241–58.CrossRefPubMedGoogle Scholar
  5. 5.
    Krieg SA, Shahine LK, Lathi RB. Environmental exposure to endocrine-disrupting chemicals and miscarriage. Fertil Steril. 2016;106(4):941–7.CrossRefPubMedGoogle Scholar
  6. 6.
    Hauser R, Skakkebaek NE, Hass U, Toppari J, Juul A, Andersson AM, et al. Male reproductive disorders, diseases, and costs of exposure to endocrine-disrupting chemicals in the European Union. J Clin Endocrinol Metab. 2015;100(4):1267–77.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Attina TM, Hauser R, Sathyanarayana S, Hunt PA, Bourguignon JP, Myers JP, et al. Exposure to endocrine-disrupting chemicals in the USA: a population-based disease burden and cost analysis. Lancet Diabetes Endocrinol. 2016;4(12):996–1003.CrossRefPubMedGoogle Scholar
  8. 8.
    Conka K, et al. Simple solid-phase extraction method for determination of polychlorinated biphenyls and selected organochlorine pesticides in human serum. J Chromatogr A. 2005;1084(1–2):33–8.CrossRefPubMedGoogle Scholar
  9. 9.
    Sifakis S, Androutsopoulos VP, Tsatsakis AM, Spandidos DA. Human exposure to endocrine disrupting chemicals: effects on the male and female reproductive systems. Environ Toxicol Pharmacol. 2017;51:56–70.CrossRefPubMedGoogle Scholar
  10. 10.
    Jiang LG, Cheng LY, Kong SH, Yang Y, Shen YJ, Chen C, et al. Toxic effects of polychlorinated biphenyls (Aroclor 1254) on human sperm motility. Asian J Androl. 2017;19(5):561–6.CrossRefPubMedGoogle Scholar
  11. 11.
    Mumford SL, Kim S, Chen Z, Gore-Langton RE, Boyd Barr D, Buck Louis GM. Persistent organic pollutants and semen quality: the LIFE study. Chemosphere. 2015;135:427–35.CrossRefPubMedGoogle Scholar
  12. 12.
    Petersen MS, Halling J, Weihe P, Jensen TK, Grandjean P, Nielsen F, et al. Spermatogenic capacity in fertile men with elevated exposure to polychlorinated biphenyls. Environ Res. 2015;138:345–51.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Vitku J, Heracek J, Sosvorova L, Hampl R, Chlupacova T, Hill M, et al. Associations of bisphenol A and polychlorinated biphenyls with spermatogenesis and steroidogenesis in two biological fluids from men attending an infertility clinic. Environ Int. 2016;89-90:166–73.CrossRefPubMedGoogle Scholar
  14. 14.
    Yurdakok B, Tekin K, Daskin A, Filazi A. Effects of polychlorinated biphenyls 28, 30 and 118 on bovine spermatozoa in vitro. Reprod Domest Anim. 2015;50(1):41–7.CrossRefPubMedGoogle Scholar
  15. 15.
    Sugantha Priya E, Sathish Kumar T, Balaji S, Bavithra S, Raja Singh P, Sakthivel D, et al. Lactational exposure effect of polychlorinated biphenyl on rat Sertoli cell markers and functional regulators in prepuberal and puberal F1 offspring. J Endocrinol Investig. 2017;40(1):91–100.CrossRefGoogle Scholar
  16. 16.
    Fiandanese N, Borromeo V, Berrini A, Fischer B, Schaedlich K, Schmidt JS, et al. Maternal exposure to a mixture of di(2-ethylhexyl) phthalate (DEHP) and polychlorinated biphenyls (PCBs) causes reproductive dysfunction in adult male mouse offspring. Reprod Toxicol. 2016;65:123–32.CrossRefPubMedGoogle Scholar
  17. 17.
    Aydin Y, Erkan M. The toxic effects of polychlorinated biphenyl (Aroclor 1242) on Tm3 Leydig cells. Toxicol Ind Health. 2017;33(8):636–45.CrossRefPubMedGoogle Scholar
  18. 18.
    Perry MJ, Young HA, Grandjean P, Halling J, Petersen MS, Martenies SE, et al. Sperm aneuploidy in Faroese men with lifetime exposure to Dichlorodiphenyldichloroethylene (p,p -DDE) and polychlorinated biphenyl (PCB) pollutants. Environ Health Perspect. 2016;124(7):951–6.PubMedGoogle Scholar
  19. 19.
    Hsu P-C, Li MC, Lee YC, Kuo PL, Guo YL. Polychlorinated biphenyls and dibenzofurans increased abnormal sperm morphology without alterations in aneuploidy: the Yucheng study. Chemosphere. 2016;165:294–7.CrossRefPubMedGoogle Scholar
  20. 20.
    Goldstone AE, Chen Z, Perry MJ, Kannan K, Louis GMB. Urinary bisphenol A and semen quality, the LIFE Study. Reprod Toxicol. 2015;51:7–13.CrossRefPubMedGoogle Scholar
  21. 21.
    Richter CA, Taylor JA, Ruhlen RL, Welshons WV, vom Saal FS. Estradiol and bisphenol a stimulate androgen receptor and estrogen receptor gene expression in fetal mouse prostate mesenchyme cells. Environ Health Perspect. 2007;115(6):902–8.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Qiu LL, Wang X, Zhang XH, Zhang Z, Gu J, Liu L, et al. Decreased androgen receptor expression may contribute to spermatogenesis failure in rats exposed to low concentration of bisphenol A. Toxicol Lett. 2013;219(2):116–24.CrossRefPubMedGoogle Scholar
  23. 23.
    Wisniewski P, Romano RM, Kizys MML, Oliveira KC, Kasamatsu T, Giannocco G, et al. Adult exposure to bisphenol A (BPA) in Wistar rats reduces sperm quality with disruption of the hypothalamic–pituitary–testicular axis. Toxicology. 2015;329:1–9.CrossRefPubMedGoogle Scholar
  24. 24.
    Lassen TH, Frederiksen H, Jensen TK, Petersen JH, Joensen UN, Main KM, et al. Urinary bisphenol A levels in young men: association with reproductive hormones and semen quality. Environ Health Perspect. 2014;122(5):478–84.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Liu X, Miao M, Zhou Z, Gao E, Chen J, Wang J, et al. Exposure to bisphenol-A and reproductive hormones among male adults. Environ Toxicol Pharmacol. 2015;39(2):934–41.CrossRefPubMedGoogle Scholar
  26. 26.
    Manfo FP, Jubendradass R, Nantia EA, Moundipa PF, Mathur PP. Adverse effects of bisphenol A on male reproductive function. Rev Environ Contam Toxicol. 2014;228:57–82.PubMedGoogle Scholar
  27. 27.
    Dirtu AC, Geens T, Dirinck E, Malarvannan G, Neels H, van Gaal L, et al. Phthalate metabolites in obese individuals undergoing weight loss: urinary levels and estimation of the phthalates daily intake. Environ Int. 2013;59:344–53.CrossRefPubMedGoogle Scholar
  28. 28.
    Pant N, Pant AB, Shukla M, Mathur N, Gupta YK, Saxena DK. Environmental and experimental exposure of phthalate esters: the toxicological consequence on human sperm. Hum Exp Toxicol. 2011;30(6):507–14.CrossRefPubMedGoogle Scholar
  29. 29.
    Prevention, C.f.D.C.a. Second National Report on Human Exposure to Environmental Chemicals. NCEH publication 02–0716. National Center for Environmental Health [report] 2003. February 4, 2003.Google Scholar
  30. 30.
    Cai H, Zheng W, Zheng P, Wang S, Tan H, He G, et al. Human urinary/seminal phthalates or their metabolite levels and semen quality: a meta-analysis. Environ Res. 2015;142:486–94.CrossRefPubMedGoogle Scholar
  31. 31.
    Wang YX, Zeng Q, Sun Y, You L, Wang P, Li M, et al. Phthalate exposure in association with serum hormone levels, sperm DNA damage and spermatozoa apoptosis: a cross-sectional study in China. Environ Res. 2016;150:557–65.CrossRefPubMedGoogle Scholar
  32. 32.
    Watkins DJ, Sánchez BN, Téllez-Rojo MM, Lee JM, Mercado-García A, Blank-Goldenberg C, et al. Impact of phthalate and BPA exposure during in utero windows of susceptibility on reproductive hormones and sexual maturation in peripubertal males. Environ Health. 2017;16:69.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Dobrzynska MM. Phthalates—widespread occurrence and the effect on male gametes. Part 2. The effects of phthalates on male gametes and on the offspring. Rocz Panstw Zakl Hig. 2016;67(3):209–21.PubMedGoogle Scholar
  34. 34.
    Ahmad R, Gautam AK, Verma Y, Sedha S, Kumar S. Effects of in utero di-butyl phthalate and butyl benzyl phthalate exposure on offspring development and male reproduction of rat. Environ Sci Pollut Res. 2014;21(4):3156–65.CrossRefGoogle Scholar
  35. 35.
    Hsu PC, Kuo YT, Leon Guo Y, Chen JR, Tsai SS, Chao HR, et al. The adverse effects of low-dose exposure to Di(2-ethylhexyl) phthalate during adolescence on sperm function in adult rats. Environ Toxicol. 2016;31(6):706–12.CrossRefPubMedGoogle Scholar
  36. 36.
    Svechnikov K, Savchuk I, Morvan ML, Antignac JP, le Bizec B, Söder O. Phthalates exert multiple effects on Leydig cell steroidogenesis. Horm Res Paediatr. 2016;86(4):253–63.CrossRefPubMedGoogle Scholar
  37. 37.
    Thurston SW, Mendiola J, Bellamy AR, Levine H, Wang C, Sparks A, et al. Phthalate exposure and semen quality in fertile US men. Andrology. 2016;4(4):632–8.CrossRefPubMedGoogle Scholar
  38. 38.
    Specht IO, Toft G, Hougaard KS, Lindh CH, Lenters V, Jönsson BAG, et al. Associations between serum phthalates and biomarkers of reproductive function in 589 adult men. Environ Int. 2014;66:146–56.CrossRefPubMedGoogle Scholar
  39. 39.
    Jurewicz J, Radwan M, Sobala W, Ligocka D, Radwan P, Bochenek M, et al. Human urinary phthalate metabolites level and main semen parameters, sperm chromatin structure, sperm aneuploidy and reproductive hormones. Reprod Toxicol. 2013;42:232–41.CrossRefPubMedGoogle Scholar
  40. 40.
    Chen Q, Yang H, Zhou N, Sun L, Bao H, Tan L, et al. Phthalate exposure, even below US EPA reference doses, was associated with semen quality and reproductive hormones: prospective MARHCS study in general population. Environ Int. 2017;104:58–68.CrossRefPubMedGoogle Scholar
  41. 41.
    Nassan FL, Coull BA, Skakkebaek NE, Andersson AM, Williams MA, Mínguez-Alarcón L, et al. A crossover-crossback prospective study of dibutyl-phthalate exposure from mesalamine medications and serum reproductive hormones in men. Environ Res. 2018;160:121–31.CrossRefPubMedGoogle Scholar
  42. 42.
    Mostafalou S, Abdollahi M. Pesticides: an update of human exposure and toxicity. Arch Toxicol. 2017;91(2):549–99.CrossRefPubMedGoogle Scholar
  43. 43.
    Hernández AF, Parrón T, Tsatsakis AM, Requena M, Alarcón R, López-Guarnido O. Toxic effects of pesticide mixtures at a molecular level: their relevance to human health. Toxicology. 2013;307:136–45.CrossRefPubMedGoogle Scholar
  44. 44.
    Yolanda Pico, G.f.a.J.m., Handbook of Food Analysis, Organophosphate Pesticides Residues in Food. 2nd edn, vol. 2. 2004, New York, USA.Google Scholar
  45. 45.
    Bjørling-Poulsen M, Andersen HR, Grandjean P. Potential developmental neurotoxicity of pesticides used in Europe. Environ Health. 2008;7:50.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Mnif W, Hassine AIH, Bouaziz A, Bartegi A, Thomas O, Roig B. Effect of endocrine disruptor pesticides: a review. Int J Environ Res Public Health. 2011;8(6):2265–303.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Mehrpour O, Karrari P, Zamani N, Tsatsakis AM, Abdollahi M. Occupational exposure to pesticides and consequences on male semen and fertility: a review. Toxicol Lett. 2014;230(2):146–56.CrossRefPubMedGoogle Scholar
  48. 48.
    Miranda-Contreras L, Gómez-Pérez R, Rojas G, Cruz I, Berrueta L, Salmen S, et al. Occupational exposure to organophosphate and carbamate pesticides affects sperm chromatin integrity and reproductive hormone levels among Venezuelan farm workers. J Occup Health. 2013;55(3):195–203.CrossRefPubMedGoogle Scholar
  49. 49.
    Melgarejo M, Mendiola J, Koch HM, Moñino-García M, Noguera-Velasco JA, Torres-Cantero AM. Associations between urinary organophosphate pesticide metabolite levels and reproductive parameters in men from an infertility clinic. Environ Res. 2015;137:292–8.CrossRefPubMedGoogle Scholar
  50. 50.
    Cremonese C, Piccoli C, Pasqualotto F, Clapauch R, Koifman RJ, Koifman S, et al. Occupational exposure to pesticides, reproductive hormone levels and sperm quality in young Brazilian men. Reprod Toxicol. 2017;67:174–85.CrossRefPubMedGoogle Scholar
  51. 51.
    ATSDR. Toxic Substances and Disease Registry. Toxicological Profile for DDT, DDE, and DDD. Atlanta: Agency for Toxic Substances and Disease Registr; 2002.Google Scholar
  52. 52.
    Consales C, Toft G, Leter G, Bonde JPE, Uccelli R, Pacchierotti F, et al. Exposure to persistent organic pollutants and sperm DNA methylation changes in Arctic and European populations. Environ Mol Mutagen. 2016;57(3):200–9.CrossRefPubMedGoogle Scholar
  53. 53.
    Campagna M, Satta G, Fadda D, Pili S, Cocco P. Male fertility following occupational exposure to dichlorodiphenyltrichloroethane (DDT). Environ Int. 2015;77:42–7.CrossRefPubMedGoogle Scholar
  54. 54.
    Pant N, Shukla M, Upadhyay AD, Chaturvedi PK, Saxena DK, Gupta YK. Association between environmental exposure to p, p’-DDE and lindane and semen quality. Environ Sci Pollut Res Int. 2014;21(18):11009–16.CrossRefPubMedGoogle Scholar
  55. 55.
    Rana SVS. Perspectives in endocrine toxicity of heavy metals—a review. Biol Trace Elem Res. 2014;160(1):1–14.CrossRefPubMedGoogle Scholar
  56. 56.
    Carette D, Perrard MH, Prisant N, Gilleron J, Pointis G, Segretain D, et al. Hexavalent chromium at low concentration alters Sertoli cell barrier and connexin 43 gap junction but not claudin-11 and N-cadherin in the rat seminiferous tubule culture model. Toxicol Appl Pharmacol. 2013;268(1):27–36.CrossRefPubMedGoogle Scholar
  57. 57.
    de Angelis C, Galdiero M, Pivonello C, Salzano C, Gianfrilli D, Piscitelli P, et al. The environment and male reproduction: the effect of cadmium exposure on reproductive function and its implication in fertility. Reprod Toxicol. 2017;73:105–27.CrossRefPubMedGoogle Scholar
  58. 58.
    Cosselman KE, Navas-Acien A, Kaufman JD. Environmental factors in cardiovascular disease. Nat Rev Cardiol. 2015;12(11):627–42.CrossRefPubMedGoogle Scholar
  59. 59.
    Lemjabbar-Alaoui H, Hassan OUI, Yang YW, Buchanan P. Lung cancer: biology and treatment options. Biochim Biophys Acta Rev Cancer. 2015;1856(2):189–210.CrossRefGoogle Scholar
  60. 60.
    Loomis D, Grosse Y, Lauby-Secretan B, el Ghissassi F, Bouvard V, Benbrahim-Tallaa L, et al. The carcinogenicity of outdoor air pollution. Lancet Oncol. 2013;14(13):1262–3.CrossRefPubMedGoogle Scholar
  61. 61.
    Lafuente R, García-Blàquez N, Jacquemin B, Checa MA. Outdoor air pollution and sperm quality. Fertil Steril. 2016;106(4):880–96.CrossRefPubMedGoogle Scholar
  62. 62.
    Radwan M, et al. Air Pollution and Human Sperm Sex Ratio. Am J Men’s Health. 0(0):1557988317752608.Google Scholar
  63. 63.
    Zhang M-H, Shi ZD, Yu JC, Zhang YP, Wang LG, Qiu Y. Scrotal heat stress causes sperm chromatin damage and cysteinyl aspartate-spicific proteinases 3 changes in fertile men. J Assist Reprod Genet. 2015;32(5):747–55.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Garolla A, Torino M, Sartini B, Cosci I, Patassini C, Carraro U, et al. Seminal and molecular evidence that sauna exposure affects human spermatogenesis. Hum Reprod. 2013;28(4):877–85.CrossRefPubMedGoogle Scholar
  65. 65.
    Liu Y, Li X. Molecular basis of cryptorchidism-induced infertility. Sci China Life Sci. 2010;53(11):1274–83.CrossRefPubMedGoogle Scholar
  66. 66.
    Garolla A, Torino M, Miola P, Caretta N, Pizzol D, Menegazzo M, et al. Twenty-four-hour monitoring of scrotal temperature in obese men and men with a varicocele as a mirror of spermatogenic function. Hum Reprod. 2015;30(5):1006–13.CrossRefPubMedGoogle Scholar
  67. 67.
    Kim J-H, Park SJ, Kim TS, Kim JM, Lee DS. Testosterone production by a Leydig tumor cell line is suppressed by hyperthermia-induced endoplasmic reticulum stress in mice. Life Sci. 2016;146:184–91.CrossRefPubMedGoogle Scholar
  68. 68.
    Lin C, et al. Enhanced Protective Effects of Combined Treatment with β-Carotene and Curcumin against Hyperthermic Spermatogenic Disorders in Mice. BioMed Res Int. 2016;2016:2572073.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Zhang M-H, Zhang AD, Shi ZD, Wang LG, Qiu Y. Changes in levels of seminal nitric oxide synthase, macrophage migration inhibitory factor, sperm DNA integrity and caspase-3 in fertile men after scrotal heat stress. PLoS One. 2015;10(10):e0141320.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Rao M, Xia W, Yang J, Hu LX, Hu SF, Lei H, et al. Transient scrotal hyperthermia affects human sperm DNA integrity, sperm apoptosis, and sperm protein expression. Andrology. 2016;4(6):1054–63.CrossRefPubMedGoogle Scholar
  71. 71.
    Kesari KK, Kumar S, Nirala J, Siddiqui MH, Behari J. Biophysical evaluation of radiofrequency electromagnetic field effects on male reproductive pattern. Cell Biochem Biophys. 2013;65(2):85–96.CrossRefPubMedGoogle Scholar
  72. 72.
    Elmas O. Effects of electromagnetic field exposure on the heart: a systematic review. Toxicol Ind Health. 2016;32(1):76–82.CrossRefPubMedGoogle Scholar
  73. 73.
    Morgan LL, et al. Mobile phone radiation causes brain tumors and should be classified as a probable human carcinogen (2A) (Review). Vol. 46. 2015.Google Scholar
  74. 74.
    Oftedal G, Wilen J, Sandstrom M, Mild KH. Symptoms experienced in connection with mobile phone use. Occup Med. 2000;50(4):237–45.CrossRefGoogle Scholar
  75. 75.
    Braune S, Wrocklage C, Raczek J, Gailus T, Lücking CH. Resting blood pressure increase during exposure to a radio-frequency electromagnetic field. Lancet. 1998;351(9119):1857–8.CrossRefPubMedGoogle Scholar
  76. 76.
    Danker-Hopfe H, Dorn H, Bolz T, Peter A, Hansen ML, Eggert T, et al. Effects of mobile phone exposure (GSM 900 and WCDMA/UMTS) on polysomnography based sleep quality: an intra- and inter-individual perspective. Environ Res. 2016;145:50–60.CrossRefPubMedGoogle Scholar
  77. 77.
    Ghanbari M, Mortazavi SB, Khavanin A, Khazaei M. The effects of cell phone waves (900 MHz-GSM band) on sperm parameters and total antioxidant capacity in rats. Int J Fertil Steril. 2013;7(1):21–8.PubMedPubMedCentralGoogle Scholar
  78. 78.
    Kumar S, et al. Effect of electromagnetic irradiation produced by 3G mobile phone on male rat reproductive system in a simulated scenario. 2014;52:890–7.Google Scholar
  79. 79.
    Pandey N, Giri S, Das S, Upadhaya P. Radiofrequency radiation (900 MHz)-induced DNA damage and cell cycle arrest in testicular germ cells in swiss albino mice. Toxicol Ind Health. 2017;33(4):373–84.CrossRefPubMedGoogle Scholar
  80. 80.
    Adams JA, Galloway TS, Mondal D, Esteves SC, Mathews F. Effect of mobile telephones on sperm quality: a systematic review and meta-analysis. Environ Int. 2014;70:106–12.CrossRefPubMedGoogle Scholar
  81. 81.
    Liu K, Li Y, Zhang G, Liu J, Cao J, Ao L, et al. Association between mobile phone use and semen quality: a systemic review and meta-analysis. Andrology. 2014;2(4):491–501.CrossRefPubMedGoogle Scholar
  82. 82.
    Zhang G, Yan H, Chen Q, Liu K, Ling X, Sun L, et al. Effects of cell phone use on semen parameters: results from the MARHCS cohort study in Chongqing, China. Environ Int. 2016;91:116–21.CrossRefPubMedGoogle Scholar
  83. 83.
    Sheynkin Y, Jung M, Yoo P, Schulsinger D, Komaroff E. Increase in scrotal temperature in laptop computer users. Hum Reprod. 2005;20(2):452–5.CrossRefPubMedGoogle Scholar
  84. 84.
    Sheynkin Y, et al. Protection from scrotal hyperthermia in laptop computer users. 2010;95:647–51.Google Scholar
  85. 85.
    McGill JJ, Agarwal A. The impact of cell phone, laptop computer, and microwave oven usage on male fertility. In: du Plessis SS, Agarwal A, Sabanegh JES, editors. Male Infertility: A Complete Guide to Lifestyle and Environmental Factors. New York: Springer New York; 2014. p. 161–77.Google Scholar
  86. 86.
    Dasdag S, Taş M, Akdag MZ, Yegin K. Effect of long-term exposure of 2.4 GHz radiofrequency radiation emitted from Wi-Fi equipment on testes functions. Electromagn Biol Med. 2015;34(1):37–42.CrossRefPubMedGoogle Scholar
  87. 87.
    Shokri S, et al. Effects of Wi-Fi (2.45 GHz) exposure on apoptosis, sperm parameters and testicular histomorphometry in rats: a time course study. Cell J (Yakhteh). 2015;17(2):322–31.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Mahmoud Mima
    • 1
  • David Greenwald
    • 1
  • Samuel Ohlander
    • 1
  1. 1.University of Illinois at ChicagoChicagoUSA

Personalised recommendations