Environmental PAH exposure and male idiopathic infertility: a review on early life exposures and adult diagnosis

References

1. Martinez G, Daniels K, Chandra A. Fertility of men and women aged 15–44 years in the United States: National Survey of Family Growth, 2006–2010. Natl Health Stat Report 2012;51:1–28.Search in Google Scholar

2. Barker DJ. Fetal origins of coronary heart disease. Br Med J 1995;311(6998):171–4.10.1002/9780470986882.ch22Search in Google Scholar

3. De Boo HA, Harding JE. The developmental origins of adult disease (Barker) hypothesis. Aust NZ J Obstet Gyn 2006;46(1):4–14.10.1111/j.1479-828X.2006.00506.xSearch in Google Scholar

4. IARC, Monographs on the Evaluation of Carcinogenic Risks to Humans, in Polynuclear aromatic compounds, Part 1: chemical, environmental, and experimental data. 1983, World Health Organization International Agency For Research On Cancer: Lyon, France.Search in Google Scholar

5. Menzie CA, Potocki BB, Santodonato J. Exposure to carcinogenic PAHs in the environment. Environ Sci Technol 1992;26(7):1278–84.10.1021/es00031a002Search in Google Scholar

6. Zhang YY, Dong S, Wang H, Tao S, Kiyama R. Biological impact of environmental polycyclic aromatic hydrocarbons (ePAHs) as endocrine disruptors. Environ Pollut 2016;213:809–24.10.1016/j.envpol.2016.03.050Search in Google Scholar

7. Peterson BS, Rauh VA, Bansal R, Hao X, Toth Z, et al. Effects of prenatal exposure to air pollutants (polycyclic aromatic hydrocarbons) on the development of brain white matter, cognition, and behavior in later childhood. JAMA Psychiatry 2015;72(6):531–40.10.1001/jamapsychiatry.2015.57Search in Google Scholar

8. Nakamura BN, Mohar I, Lawson GW, Cortés MM, Hoang YD, et al. Increased sensitivity to testicular toxicity of transplacental benzo [a] pyrene exposure in male glutamate cysteine ligase modifier subunit knockout (Gclm-/-) mice. Toxicol Sci 2012;126(1):227–41.10.1093/toxsci/kfs017Search in Google Scholar

9. Gaspari L, Chang SS, Santella RM, Garte S, Pedotti P, et al. Polycyclic aromatic hydrocarbon-DNA adducts in human sperm as a marker of DNA damage and infertility. Mutat Res 2003;535(2):155–60.10.1016/S1383-5718(02)00297-8Search in Google Scholar

10. Jungwirth A, Diemer T, Dohle GR, Giwercman A, Kopa Z, et al. Guidelines on male infertility. Euro Assoc Urol 2015. Available at: http://uroweb.org/wp-content/uploads/17-Male-Infertility_LR1.pdf.Search in Google Scholar

11. Pierik FH, Van Ginneken AM, Dohle GR, Vreeburg JT, Weber RF. The advantages of standardized evaluation of male infertility. Int J Androl 2000;23(6):340–6.10.1046/j.1365-2605.2000.00250.xSearch in Google Scholar

12. Nuti F, Krausz C. Gene polymorphisms/mutations relevant to abnormal spermatogenesis. Reprod Biomed Online 2008;16(4):504–13.10.1016/S1472-6483(10)60457-9Search in Google Scholar

13. Krausz C, Giachini C. Genetic risk factors in male infertility. Arch Androl 2007;53(3):125–33.10.1080/01485010701271786Search in Google Scholar PubMed

14. Tuttelmann F, Rajpert-De Meyts E, Nieschlag E, Simoni M. Gene polymorphisms and male infertility – a meta-analysis and literature review. Reprod Biomed Online 2007;15(6):643–58.10.1016/S1472-6483(10)60531-7Search in Google Scholar

15. Jeng HA, Pan C-H, Chao M-R, Lin W-Y. Sperm DNA oxidative damage and DNA adducts. Mutat Res 2015;794:75–82.10.1016/j.mrgentox.2015.09.002Search in Google Scholar

16. Jeng HA, Pan CH, Lin WY, Wu MT, Taylor S, et al. Biomonitoring of polycyclic aromatic hydrocarbons from coke oven emissions and reproductive toxicity in nonsmoking workers. J Hazard Mater 2013;244:436–43.10.1016/j.jhazmat.2012.11.008Search in Google Scholar

17. Anderson L, Anderson LM, Coulson M, McIntyre BS, Boekelheide K, et al. Sperm MRNAs are molecular markers of minimal testicular injury in rats. Andrology 2013;1:85–5.Search in Google Scholar

18. Ji GX, Yan L, Wu S, Liu J, Wang L, et al. Bulky DNA adducts in human sperm associated with semen parameters and sperm DNA fragmentation in infertile men: a cross-sectional study. Environ Health 2013;12:82.10.1186/1476-069X-12-82Search in Google Scholar

19. Cooke PS, Young P, Cunha GR. Androgen receptor expression in developing male reproductive-organs. Endocrinology 1991;128(6):2867–73.10.1210/endo-128-6-2867Search in Google Scholar

20. Reisert I, Pilgrim C. Sexual-differentiation of monanimergic neurons – genetic or epigenetic. Trends Neurosci 1991;14(10):468–73.10.1016/0166-2236(91)90047-XSearch in Google Scholar

21. Takeda H, Chang C. Immunoistochemical and insitu hybridizatin analysis of androgen receptor expression during the development of the mouse prostate gland. J Endocrinol 1991;129(1):83–9.10.1677/joe.0.1290083Search in Google Scholar PubMed

22. Murashima A, Kishigami S, Thomson A, Yamada G. Androgens and mammalian male reproductive tract development. Biochim Biophys Acta 2015;1849(2):163–70.10.1016/j.bbagrm.2014.05.020Search in Google Scholar PubMed

23. De Bellis MD, Keshavan MS, Beers SR, Hall J, Frustaci K, et al. Sex differences in brain maturation during childhood and adolescence. Cereb Cortex 2001;11(6):552–7.10.1093/cercor/11.6.552Search in Google Scholar PubMed

24. Hutchison JB. Gender-specific steroid metabolism in neural differentiation. Cell Mol Neurobiol 1997;17(6):603–26.10.1023/A:1022581902880Search in Google Scholar

25. Goldstein JM, Seidman LJ, Horton NJ, Makris N, Kennedy DN, et al. Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb Cortex 2001;11(6):490–7.10.1093/cercor/11.6.490Search in Google Scholar

26. Segovia S, Guillamón A, del Cerro MC, Ortega E, Pérez-Laso C, et al. The development of brain sex differences: a multisignaling process. Behav Brain Res 1999;105(1):69–80.10.1016/S0166-4328(99)00083-2Search in Google Scholar

27. Arnold AP, Gorski RA. Gonadal steroid induction of structural sex – differences in the central nervous system. Annu Rev Neurosci 1984;7:413–42.10.1146/annurev.ne.07.030184.002213Search in Google Scholar

28. Pilgrim C, Reisert I. Differences between male and female brains – developmental mechanisms and implications. Horm Metab Res 1992;24(8):353–9.10.1055/s-2007-1003334Search in Google Scholar

29. Roselli CE, Abdelgadir SE, Resko JA. Regulation of aromatase gene expression in the adult rat brain. Brain Res Bull 1997;44(4):351–7.10.1016/S0361-9230(97)00214-1Search in Google Scholar

30. BeyerC, Pilgrim C, Reisert I. Dopamine content and metabolism in mesencephalic and diencephalic cell cultures – sex differences and effects on sex steriods. J Neurosci 1991;11(5):1325–33.10.1523/JNEUROSCI.11-05-01325.1991Search in Google Scholar

31. Phoenix CH, Goy RW, Gerall AA, Young WC. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 1959;65(3):369–82.10.1016/j.yhbeh.2009.01.004Search in Google Scholar

32. Dewing P, Shi T, Horvath S, Vilain E. Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Mol Brain Res 2003;118(1–2):82–90.10.1016/S0169-328X(03)00339-5Search in Google Scholar

33. Rodier PM. Developing brain as a target of toxicity. Environ Health Perspect 1995;103:73–6.Search in Google Scholar

34. Grova N, Salquèbre G, Schroeder H, Appenzeller BM. Determination of PAHs and OH-PAHs in rat brain by gas chromatography tandem (triple quadrupole) mass spectrometry. Chem Res Toxicol 2011;24(10):1653–67.10.1021/tx2003596Search in Google Scholar PubMed

35. Brown LA, Khousbouei H, Goodwin JS, Irvin-Wilson CV, Ramesh A, et al. Down-regulation of early ionotrophic glutamate receptor subunit developmental expression as a mechanism for observed plasticity deficits following gestational exposure to benzo(a)pyrene. Neurotoxicology 2007;28(5):965–78.10.1016/j.neuro.2007.05.005Search in Google Scholar PubMed PubMed Central

36. Perera FP, Jedrychowski W, Butscher M, Camann D, Kieltyka A, et al. Prenatal airborne polycyclic aromatic hydrocarbon exposure and child IQ at age 5 years. Pediatrics 2009;124(2):E195–202.10.1542/peds.2008-3506Search in Google Scholar

37. Jedrychowski WA, Perera FP, Camann D, Spengler J, Butscher M, et al. Prenatal exposure to polycyclic aromatic hydrocarbons and cognitive dysfunction in children. Environ Sci Pollut Res 2015;22(5):3631–9.10.1007/s11356-014-3627-8Search in Google Scholar

38. Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Taylor K, et al. Fetal testosterone influences sexually dimorphic gray matter in the human brain. J Neurosci 2012;32(2):674–80.10.1523/JNEUROSCI.4389-11.2012Search in Google Scholar

39. Lin PP, Chang JT, Ko JL, Liao SH, Lo WS. Reduction of androgen receptor expression by benzo a pyrene and 7,8-dihydro-9,10-epoxy-7,8,9,10-tetrahydrobenzo a pyrene in human lung cells. Biochem Pharmacol 2004;67(8):1523–30.10.1016/j.bcp.2003.12.018Search in Google Scholar

40. Li F, Wu H, Li L, Li X, Zhao J, et al. Docking and QSAR study on the binding interactions between polycyclic aromatic hydrocarbons and estrogen receptor. Ecotox Environ Safe 2012;80:273–9.10.1016/j.ecoenv.2012.03.009Search in Google Scholar

41. Srivastava VK, Li L, Li X, Zhao J, Peijnenburg WJGM. Fetal translocation and metabolism of PAH obtained from cola fly-ash given intratracheally to pregnant rats. J Toxicol Environ Health 1986;18(3):459–69.10.1080/15287398609530885Search in Google Scholar

42. Hatch MC, Warburton D, Santella RM. Polycyclic aromatic hydrocarbons-DNA adducts in spontaneously aborted fetal tissue. Carcinogenesis 1990;11(9):1673–5.10.1093/carcin/11.9.1673Search in Google Scholar

43. Sinko I, Sinkó I, Mórocz M, Zádori J, Kokavszky K. Effect of cigarette smoking on DNA damage of human cumulus cells analyzed by comet assay. Reprod Toxicol 2005;20(1):65–71.10.1016/j.reprotox.2004.12.007Search in Google Scholar

44. Georgellis A, Toppari J, Veromaa T, Rydström J, Parvinen M. Inhibition of meitoic divisions of rat spermatocytes in vitro by polycyclic aromatic hydrocarbons. Mutat Res 1990;231(2):125–35.10.1016/0027-5107(90)90019-ZSearch in Google Scholar

45. Pedersen RA, Meneses J, Spindle A, Wu K, Galloway SM. Cytochrome P450 metabolic activity in embryonic and extraembryonic tissue liearges of mouse embryos. Proc Natl Acad Sci USA 1985;82(10):3311–5.10.1073/pnas.82.10.3311Search in Google Scholar PubMed PubMed Central

46. Jensen TK, Jørgensen N, Punab M, Haugen TB, Suominen J, 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 2004;159(1):49–58.10.1093/aje/kwh002Search in Google Scholar

47. Storgaard L, Bonde JP, Ernst E, Spanô M, Andersen CY, et al. Does smoking during pregnancy affect sons’ sperm counts? Epidemiology 2003;14(3):278–86.10.1097/01.EDE.0000059922.73864.3ESearch in Google Scholar

48. Fukuda M, Fukuda K, Shimizu T, Andersen CY, Byskov AG. Periconceptual parental smoking and sex ratio of offspring – Reply. Lancet 2002;360(9344):1515–6.10.1016/S0140-6736(02)11455-3Search in Google Scholar

49. Viloria T, Rubio MC, Rodrigo L, Calderon G, Mercader A, et al. Smoking habits of parents and male: female ratio in spermatozoa and preimplantation embryos. Hum Reprod 2005;20(9):2517–22.10.1093/humrep/dei087Search in Google Scholar PubMed

50. Mackenzie KM, Angevine DM. Infertility in mice exposed in utero to benzo[a]pyene. Biol Reprod 1981;24(1):183–91.10.1095/biolreprod24.1.183Search in Google Scholar PubMed

51. Mohamed ES, Song WH, Oh SA, Park YJ, You YA, et al. The transgenerational impact of benzo(a)pyrene on murine male fertility. Hum Reprod 2010;25(10):2427–33.10.1093/humrep/deq205Search in Google Scholar PubMed

52. Kim A, Park M, Yoon TK, Lee WS, Ko JJ, et al. Maternal exposure to benzo b fluoranthene disturbs reproductive performance in male offspring mice. Toxicol Lett 2011;203(1):54–61.10.1016/j.toxlet.2011.03.003Search in Google Scholar PubMed

53. Shorey LE, Castro DJ, Baird WM, Siddens LK, Löhr CV, et al. Transplacental carcinogenesis with dibenzo def,p chrysene (DBC): timing of maternal exposures determines target tissue response in offspring. Cancer Lett 2012;317(1):49–55.10.1016/j.canlet.2011.11.010Search in Google Scholar PubMed PubMed Central

54. Jedrychowski WA, Perera FP, Tang D, Rauh V, Majewska R, et al. The relationship between prenatal exposure to airborne polycyclic aromatic hydrocarbons (PAHs) and PAH-DNA adducts in cord blood. J Expo Sci Environ Epidemiol 2013;23(4):371–7.10.1038/jes.2012.117Search in Google Scholar PubMed PubMed Central

55. Vishnevetsky J, Tang D, Chang HW, Roen EL, Wang Y, et al. Combined effects of prenatal polycyclic aromatic hydrocarbons and material hardship on child IQ. Neurotoxicol Teratol 2015;49:74–80.10.1016/j.ntt.2015.04.002Search in Google Scholar PubMed PubMed Central

56. Perera FP, Rauh V, Tsai WY, Kinney P, Camann D, et al. Effects of transplacental exposure to environmental pollutants on birth outcomes in a multiethnic population. Environ Health Perspect 2003;111(2):201–5.10.1289/ehp.5742Search in Google Scholar

57. Dennis MJ, Massey RC, Cripps G, Venn I, Howarth N, et al. Factors affecting the polycyclic aromatic hydrocarbon content of cereals, fats and other food-products. Food Addit Contam 1991;8(4):517–30.10.1080/02652039109374004Search in Google Scholar

58. Jakszyn P, Agudo A, Ibáñez R, García-Closas R, Pera G, et al. Development of a food database of nitrosamines, heterocyclic amines, and polycyclic aromatic hydrocarbons. J Nutr 2004;134(8)2011–4.10.1093/jn/134.8.2011Search in Google Scholar

59. Domingo JL, Nadal M. Human dietary exposure to polycyclic aromatic hydrocarbons: a review of the scientific literature. Food Chem Toxicol 2015;86:144–53.10.1016/j.fct.2015.10.002Search in Google Scholar

60. Kazerouni N, Sinha R, Hsu CH, Greenberg A, Rothman N. Analysis of 200 food items for benzo a pyrene and estimation of its intake in an epidemiologic study. Food Chem Toxicol 2001;39(5):423–36.10.1016/S0278-6915(00)00158-7Search in Google Scholar

61. Boehmer TK, Foster SL, Henry JR, Woghiren-Akinnifesi EL, Yip FY. Residential proximity to major highways – United States, 2010. Morb Mortal Wkly Rep 2013;62(3):46–50.Search in Google Scholar

62. Gustafson P, Ostman C, Sallsten G. Indoor levels of polycyclic aromatic hydrocarbons in homes with or without wood burning for heating. Environ Sci Technol 2008;42(14):5074–80.10.1021/es800304ySearch in Google Scholar

63. Raiyani CV, Shah SH, Desai NM, Venkaiah K, Patel JS, et al. Characterization and problems of indoor pollution due to cooking stove smoke. Atmos Environ 1993;27(11):1643–55.10.1016/0960-1686(93)90227-PSearch in Google Scholar

64. Ezzati M, Kammen DM. The health impacts of exposure to indoor air pollution from solid fuels in developing countries: knowledge, gaps, and data needs. Environ Health Perspec 2002;110(11):1057–68.10.1289/ehp.021101057Search in Google Scholar PubMed PubMed Central

65. Huang L, Bohac SV, Chernyak SM, Batterman SA. Composition and integrity of PAHs, nitro-PAHs, hopanes, and steranes in diesel exhaust particulate matter. Water Air Soil Poll 2013;224(8):1630–1.10.1007/s11270-013-1630-1Search in Google Scholar PubMed PubMed Central

66. Lafontaine S, Schrlau J, Butler J, Jia Y, Harper B, et al. Relative influence of trans-Pacific and regional atmospheric transport of PAHs in the Pacific Northwest, US. Environ Sci Technol 2015;49(23):13807–16.10.1021/acs.est.5b00800Search in Google Scholar PubMed PubMed Central

67. Lundstedt S, White PA, Lemieux CL, Lynes KD, Lambert IB, et al. Sources, fate, and toxic hazards of oxygenated polycyclic aromatic hydrocarbons (PAHs) at PAH-contaminated sites. Ambio 2007;36(6):475–85.10.1579/0044-7447(2007)36[475:SFATHO]2.0.CO;2Search in Google Scholar

68. Heeb NV, Schmid P, Kohler M, Gujer E, Zennegg M, et al. Secondary effects of catalytic diesel particulate filters: conversion of PAHs versus formation of nitro-PAHs. Environ Sci Technol 2008;42(10):3773–9.10.1021/es7026949Search in Google Scholar

69. Sienra MD. Oxygenated polycyclic aromatic hydrocarbons in urban air particulate matter. Atmos Environ 2006;40(13):2374–84.10.1016/j.atmosenv.2005.12.009Search in Google Scholar

70. Sram RJ, Benes I, Binková B, Dejmek J, Horstman D, et al. Teplice program – The impact of air pollution on human health. Environ Health Perspect 1996;104:699–714.Search in Google Scholar

71. Lewtas J. Air pollution combustion emissions: characterization of causative agents and mechanisms associated with cancer, reproductive, and cardiovascular effects. Mutat Res 2007;636(1–3):95–133.10.1016/j.mrrev.2007.08.003Search in Google Scholar

72. Sram RJ, Binková B, Rössner P, Rubes J, Topinka J, et al. Adverse reproductive outcomes from exposure to environmental mutagens. Mutat Res 1999;428(1–2):203–15.10.1016/S1383-5742(99)00048-4Search in Google Scholar

73. Dejmek J, Solanský I, Benes I, Lenícek J, Srám RJ. The impact of polycyclic aromatic hydrocarbons and fine particles on pregnancy outcome. Environ Health Perspect 2000;108(12):1159–64.10.1289/ehp.001081159Search in Google Scholar

74. Sram RJ. Impact of air pollution on reproductive health. Environ Health Perspect 1999;107(11):A542–3.10.1289/ehp.99107a542Search in Google Scholar

75. Agarwal A, Mulgund A, Hamada A, Chyatte MR. A unique view on male infertility around the globe. Reprod Biol Endocrinol 2015;13:37.10.1186/s12958-015-0032-1Search in Google Scholar

76. Bablok L, Dziadecki W, Szymusik I, Wolczynski S, Kurzawa R, et al. Patterns of infertility in Poland – multicenter study. Neuroendocrinol Lett 2011;32(6):799–804.Search in Google Scholar

77. Sanocka D, Kurpisz M. Infertility in Poland-present status, reasons, and prognosis as a reflection of Central and Eastern Europe problems with reproduction. Med Sci Monit 2003;9:16–20.Search in Google Scholar

78. Shimada T. Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab Pharmacokinet 2006;21(4):257–76.10.2133/dmpk.21.257Search in Google Scholar

79. Shahid A, Ali R, Ali N, Hasan SK, Bernwal P, et al. Modulatory effects of catechin hydrate against genotoxicity, oxidative stress, inflammation and apoptosis induced by benzo(a)pyrene in mice. Food Chem Toxicol 2016;92:64–74.10.1016/j.fct.2016.03.021Search in Google Scholar

80. Rushmore TH, Kong AN. Pharmacogenomics, regulation and signaling pathways of phase I and II drug metabolizing enzymes. Curr Drug Metab 2002;3(5):481–90.10.2174/1389200023337171Search in Google Scholar PubMed

81. Salehi Z, Gholizadeh L, Vaziri H, Madani AH. Analysis of GSTM1, GSTT1, and CYP1A1 in idiopathic male infertility. Reprod Sci 2012;19(1):81–5.10.1177/1933719111413302Search in Google Scholar PubMed

82. Lu NX, Wu B, Xia Y, Wang W, Gu A, et al. Polymorphisms in CYP1A1 gene are associated with male infertility in a Chinese population. Int J Androl 2008;31(5):527–33.10.1111/j.1365-2605.2007.00804.xSearch in Google Scholar PubMed

83. Vani GT, Mukesh N, Siva Prasad B, Rama Devi P, Hema Prasad M, et al. Association of CYP1A1*2A polymorphism with male infertility in Indian population. Clin Chim Acta 2009;410(1–2):43–7.10.1016/j.cca.2009.09.019Search in Google Scholar PubMed

84. Aydos SE, Taspinar M, Sunguroglu A, Aydos K. Association of CYP1A1 and glutathione S-transferase polymorphisms with male factor infertility. Fertil Steril 2009;92(2):541–7.10.1016/j.fertnstert.2008.07.017Search in Google Scholar PubMed

85. Yarosh SL, Kokhtenko EV, Starodubova NI, Churnosov MI, Polonikov AV. Smoking status modifies the relation between CYP1A1*2C gene polymorphism and idiopathic male infertility: the importance of gene-environment interaction analysis for genetic studies of the disease. Reprod Sci 2013;20(11):1302–7.10.1177/1933719113483013Search in Google Scholar PubMed

86. O’Connell SG, Kind LD, Anderson KA. Silicone wristbands as personal passive samplers. Environ Sci Technol 2014;48(6):3327–35.10.1021/es405022fSearch in Google Scholar PubMed PubMed Central

87. Penning TM. Human aldo-keto reductases and the metabolic activation of polycyclic aromatic hydrocarbons. Chem Res Toxicol 2014;27(11):1901–17.10.1021/tx500298nSearch in Google Scholar PubMed PubMed Central

88. Palackal NT, Burczynski ME, Harvey RG, Penning TM. The ubiquitous aldehyde reductase (AKR1A1) oxidizes proximate carcinogen trans-dihydrodiols to o-quinones: potential role in polycyclic aromatic hydrocarbon activation. Biochemistry 2001;40(36):10901–10.10.1021/bi010872tSearch in Google Scholar PubMed

89. Sharma RK, Pasqualotto FF, Nelson DR, Thomas AJ Jr, Agarwal A. The reactive oxygen species – total antioxidant capacity score is a new measure of oxidative stress to predict male infertility. Hum Reprod 1999;14(11):2801–7.10.1093/humrep/14.11.2801Search in Google Scholar PubMed

90. Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol 2008;59(1):2–11.10.1111/j.1600-0897.2007.00559.xSearch in Google Scholar

91. Penning TM, Ohnishi ST, Ohnishi T, Harvey RG. Generation of reactive oxygen species during the enzymatic oxidation of polycyclic aromatic hydrocarbon trans-dihydrodiols catalyzed by dihydrodiol dehydrogenase. Chem Res Toxicol 1996;9(1):84–92.10.1021/tx950055sSearch in Google Scholar

92. Eskenazi B, Kidd SA, Marks AR, Sloter E, Block G, et al. Antioxidant intake is associated with semen quality in healthy men. Hum Reprod 2005;20(4):1006–12.10.1093/humrep/deh725Search in Google Scholar

93. Hecht SS, Carmella SG, Yoder A, Chen M, Li ZZ, et al. Comparison of polymorphisms in genes involved in polycyclic aromatic hydrocarbon metabolism with urinary phenanthrene metabolite ratios in smokers. Cancer Epidemiol Biomarkers Prev 2006;15(10):1805–11.10.1158/1055-9965.EPI-06-0173Search in Google Scholar

94. Hakkola J, Pelkonen O, Pasanen M, Raunio H. Xenobiotic-metabolizing cytochrome P450 enzymes in the human feto-placental unit: role in intrauterine toxicity. Crit Rev Toxicol 1998;28(1):35–72.10.1080/10408449891344173Search in Google Scholar

95. Fraga CG, Motchnik PA, Wyrobek AJ, Rempel DM, Ames BN. Smoking and low antioxidant levels increase oxidative damage to sperm DNA. Mutat Res 1996;351(2):199–203.10.1016/0027-5107(95)00251-0Search in Google Scholar

96. Mostafa T, Tawadrous G, Roaia MM, Amer MK, Kader RA, et al. Effect of smoking on seminal plasma ascorbic acid in infertile and fertile males. Andrologia 2006;38(6):221–4.10.1111/j.1439-0272.2006.00744.xSearch in Google Scholar

97. Saleh RA, Agarwal A, Sharma RK, Nelson DR, Thomas AJ Jr. Effect of cigarette smoking on level of seminal oxidative stress in fertile men: a prospective study. Fertil Steril 2002;78(3):491–9.10.1016/S0015-0282(02)03294-6Search in Google Scholar

98. Kao SH, Chao HT, Chen HW, Hwang TI, Liao TL, et al. Increase of oxidative stress in human sperm with lower motility. Fertil Steril 2008;89(5):1183–90.10.1016/j.fertnstert.2007.05.029Search in Google Scholar PubMed

99. Aydemir B, Onaran I, Kiziler AR, Alici B, Akyolcu MC. The influence of oxidative damage on viscosity of seminal fluid in infertile men. J Androl 2008;29(1):41–6.10.2164/jandrol.107.003046Search in Google Scholar PubMed

100. Sharma RK, Pasqualotto AE, Nelson DR, Thomas AJ Jr, Agarwal A. Relationship between seminal white blood cell counts and oxidative stress in men treated at an infertility clinic. J Androl 2001;22(4):575–83.Search in Google Scholar

101. Tremellen K. Oxidative stress and male infertility – a clinical perspective. Hum Reprod Update 2008;14(3):243–58.10.1007/978-1-61779-776-7_16Search in Google Scholar

102. Tavilani H, Doosti M, Saeidi H. Malondialdehyde levels in sperm and seminal plasma of asthenozoospermic and its relationship with semen parameters. Clin Chim Acta 2005;356(1–2):199–203.10.1016/j.cccn.2005.01.017Search in Google Scholar

103. Li K, Shang XJ, Chen YG. High-performance liquid chromatographic detection of lipid peroxidation in human seminal plasma and its application to male infertility. Clin Chim Acta 2004;346(2):199–203.10.1016/j.cccn.2004.03.013Search in Google Scholar

104. Ko EY, Sabanegh ES, Agarwal A. Male infertility testing: reactive oxygen species and antioxidant capacity. Fertil Steril 2014;102(6):1518–27.10.1016/j.fertnstert.2014.10.020Search in Google Scholar

105. Gharagozloo P, Aitken RJ. The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Hum Reprod 2011;26(7):1628–40.10.1093/humrep/der132Search in Google Scholar

106. Inyang F, Ramesh A, Kopsombut P, Niaz MS, Hood DB, et al. Disruption of testicular steroidogenesis and epididymal function by inhaled benzo(a)pyrene. Reprod Toxicol 2003;17(5):527–37.10.1016/S0890-6238(03)00071-6Search in Google Scholar

107. Arafa HM, Aly HA, Abd-Ellah MF, El-Refaey HM. Hesperidin attenuates benzo alpha pyrene-induced testicular toxicity in rats via regulation of oxidant/antioxidant balance. Toxicol Ind Health 2009;25(6):417–27.10.1177/0748233709106624Search in Google Scholar PubMed

108. Peretti-Watel P, L’Haridon O, Seror V. Time preferences, socioeconomic status and smokers’ behaviour, attitudes and risk awareness. Eur J Public Health 2013;23(5):783–8.10.1093/eurpub/cks189Search in Google Scholar PubMed

109. Winkleby MA, Jatulis DE, Frank E, Fortmann SP. Socioeconomic-status and health-How education, income, and occupation contribute to risk-factors for cardiovascualr-disease. Am J Public Health 1992;82(6):816–20.10.2105/AJPH.82.6.816Search in Google Scholar PubMed PubMed Central

110. Gilman SE, Breslau J, Subramanian SV, Hitsman B, Koenen KC. Social factors psychopathology, and maternal smoking during pregnancy. Am J Public Health 2008;98(3):448–53.10.2105/AJPH.2006.102772Search in Google Scholar PubMed PubMed Central

111. Williams DR. Race, socioeconomic status, and health – The added effects of racism and discrimination. Ann NY Acad Sci 1999;896:173–88.10.1111/j.1749-6632.1999.tb08114.xSearch in Google Scholar PubMed