Abstract
About a quarter of the human diseases occurs for exposure to air pollution. The male reproductive system, and especially spermatogenesis, seems to be particularly sensitive. As result, male infertility is increasing in industrial countries becoming a top priority for public health. In addition to psychological distress and economic constraints, poorer semen quality may have trans-generational effects including congenital malformations in the offspring and predispose to later onset adult diseases. Genetic and epigenetic alterations are involved in the failure of spermatogenesis. In this paper, we reviewed the major evidences of the effects of air pollutants on male infertility as well as the role of sperm DNA damage and epigenetic changes in affecting spermatogenesis. A better knowledge on the effects of air contaminants on the molecular mechanisms leading to infertility is of huge importance to help clinicians in identifying the cause of infertility but above all, in defining preventive and therapeutic protocols.
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References
Agarwal A, Prabakaran SA, Said TM (2005) Prevention of oxidative stress injury to sperm. J Androl 26:654–660
Agarwal A, Saleh RA, Bedaiwy MA (2003) Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79:829–843
Aitken RJ, Baker MA (2004) Oxidative stress and male reproductive biology. Reprod Fertil Dev 16:581–588
Anawalt BD (2013) The silent spermatozoon: are man-made endocrine disruptors killing male fertility? Asian J Androl 15:165–168
Andersson AM, Jorgensen N, Main KM, Toppari J, Rajpert-De Meyts E, Leffers H, Juul A, Jensen TK, Skakkebaek NE (2008) Adverse trends in male reproductive health: we may have reached a crucial ‘tipping point. Int J Androl 31:74–80
Apostoli P, Telišman S, Sager PR (2007) Reproductive and developmental toxicity of metals. In: Nordberg GF, Fowler BA, Nordberg M, Friberg LT (eds) Handbook on the toxicology of metals. Academic Press Elsevier, Amsterdam, pp. 213–249
Asklund C, Jorgensen N, Skakkebaek NE, Jensen TK (2007) Increased frequency of reproductive health problems among fathers of boys with hypospadias. Hum Reprod 22:2639–2646
Auger J, Kunstmann JM, Czyglik F, Jouannet P (1995) Decline in semen quality among fertile men in Paris during the past 20 years. N Engl J Med 332:281–285
Baccarelli A, Bollati V (2009) Epigenetics and environmental chemicals. Curr Opin Pediatr 21:243–251
Baker JA, Buck GM, Vena JE, Moysich KB (2005) Fertility patterns prior to testicular cancer diagnosis. Cancer Causes Control 16:295–299
Barakat TS, Jonkers I, Monkhorst K, Gribnau J (2010) X-changing information on X inactivation. Exp Cell Res 316:679–687
Barazani Y, Katz BF, Nagler HM, Stember DS (2014) Lifestyle, environment, and male reproductive health. Urol Clin North Am 41:55–66
Barroso G, Morshedi M, Oehninger S (2000) Analysis of DNA fragmentation, plasma membrane translocation of phosphatidylserine and oxidative stress in human spermatozoa. Hum Reprod 15:1338–1344
Benchaib M, Braun V, Lornage J, Hadj S, Salle B, Lejeune H, Guérin JF (2003) Sperm DNA fragmentation decreases the pregnancy rate in an assisted reproductive technique. Hum Reprod 18:1023–1028
Benoff S, Jacob A, Hurley IR (2000) Male infertility and environmental exposure to lead and cadmium. Hum Reprod Update 6:107–121
Bergamo P, Volpe MG, Lorenzetti S, Mantovani A Notari T, Cocca E, Cerullo S, Di Stasio M, Cerino P, Montano L. Human semen as an early, sensitive biomarker of highly polluted living environment in healthy men: a pilot biomonitoring study on trace elements in blood and semen and their relationship with sperm quality and RedOx status. Reprod Toxicol 2016. in press
Berger R (1975) The incidence of constitutional chromosome aberrations. J Genet Hum 23:42–49
Bollati V, Marinelli B, Apostoli P, Bonzini M, Nordio F, Hoxha M, Pegoraro V, Motta V, Tarantini L, Cantone L, Schwartz J, Bertazzi PA, Baccarelli A (2010) Exposure to metal-rich particulate matter modifies the expression of candidate microRNAs in peripheral blood leukocytes. Environ. Health Perspect 118:763–768
Brugnon F, Van Assche E, Verheyen G, Sion B, Boucher D, Pouly JL, Janny L, Devroey P, Liebaers I, Van Steirteghem A (2006) Study of two markers of apoptosis and meiotic segregation in ejaculated sperm of chromosomal translocation carrier patients. Hum Reprod 21:685–693
Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, Giwercman A (2007) Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Human Reprod 22:174–179
Calogero AE, La Vignera S, Condorelli RA, Perdichizzi A, Valenti D, Asero P, Carbone U, Boggia B, De Rosa N, Lombardi G, D’Agata R, Vicari LO, Vicari E, De Rosa M (2011) Environmental car exhaust pollution damages human sperm chromatin and DNA. J Endocrinol Investig 34:e139–e143
Carlsen E, Giwercman A, Keiding N, Skakkebaek NE (1992) Evidence for decreasing quality of semen during past 50 years. BMJ 305:609–613
Carrell DT (2012) Epigenetics of the male gamete. Fertil Steril 97:267–274
Carrell DT, Liu L, Peterson CM, Jones KP, Hatasaka HH, Erickson L, Campbell B (2003) Sperm DNA fragmentation is increased in couple with unexplained recurrent pregnancy loss. Arch Androl 1:49–55
Dada R, Kumar M, Jesudasan R, Fernández JL, Gosálvez J (2012) Agarwal a (2006) epigenetics and its role in male infertility. J Assist Reprod Genet 29:213–223
De Lamirande E, Gagnon C (1999) The dark and bright sides of reactive oxygen species on sperm function. In: Gagnon C (ed) The male gamete: from basic science to clinical applications. Cache River Press, IL, pp. 455–467
De Rosa M, Zarrilli S, Paesano L, Carbone U, Boggia B, Petretta M, Maisto A, Cimmino F, Puca G, Colao A, Lombardi G (2003) Traffic pollutants affect fertility in men. Hum Reprod 18:1055–1061
Deng Z, Chen F, Zhang M, Lan L, Qiao Z, Cui Y, An J, Wang N, Fan Z, Zhao X, Li X (2016) Association between air pollution and sperm quality: a systematic review and meta-analysis. Environ Pollut 208:663–669
Derijck A, van der Heijden G, Giele M, Philippens M, de Boer P (2008) DNA double-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. Hum Mol Genet 17:1922–1937
Dolk H (2004) Epidemiological approaches to identifying environmental causes of birth defects. Am J Med Genet C Semin Med Genet 125C:4–11
Du Y, Li M, Chen J, Duan Y, Wang X, Qiu Y, Cai Z, Gui Y, Jiang H (2016) Promoter targeted bisulfite sequencing reveals DNA methylation profiles associated with low sperm motility in asthenozoospermia. Hum Reprod 31:24–33
Erenpreiss J, Spano M, Erenpreisa J, Bungum M, Giwercman A (2006) Sperm chromatin structure and male fertility: biological and clinical aspects. Asian J Androl 8:11–29
Esteves SC (2013) A clinical appraisal of the genetic basis in unexplained male infertility. J Hum Reprod Sci 6:176–182
Evenson DP, Wixon R (2006a) Meta-analysis of sperm DNA fragmentation using the sperm chromatin structure assay. Reprod BioMed Online 12:466–472
Evenson DP, Wixon R (2006b) Clinical aspects of sperm DNA fragmentation detection and male infertility. Theriogenology 65:979–991
Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330:622–627
Ferlin A, Raicu F, Gatta V, Zuccarello D, Palka G, Foresta C (2007) Male infertility: role of genetic background. Reprod BioMed Online 14:734–745
Flanagan JM, Popendikyte V, Pozdniakovaite N, Sobolev M, Assadzadeh A, Schumacher A, Zangeneh M, Lau L, Virtanen C, Wang SC, Petronis A (2006) Intra- and interindividual epigenetic variation in human germ cells. Am J Hum Genet 79:67–84
Foster WG, McMahon A, Rice DC (1996) Sperm chromatin structure is altered in cynomolgus monkeys with environmentally relevant blood lead levels. Toxicol Ind Health 12:723–735
Giaccio L, Cicchella D, De Vivo B, Lombardi G, De Rosa M (2012) Does heavy metals pollution affects semen quality in men? A case of study in the metropolitan area of Naples (Italy). J Geochem Expl 112:218–225
Gianicolo EA, Mangia C, Cervino M, Bruni A, Andreassi MG, Latini G (2014) Congenital anomalies among live births in a high environmental risk area—a case-control study in Brindisi (southern Italy. Environ Res 128:9–14
Guo YL, Hsu PC, Hsu CC, Lambert GH (2000) Semen quality after prenatal exposure to polychlorinated biphenyls and dibenzofurans. Lancet 356:1240–1241
Guo YL, Lambert GH, Hsu CC, Hsu MM (2004) Yucheng: health effects of prenatal exposure to polychlorinated biphenyls and dibenzofurans. Int Arch Occup Environ Health 77:153–158
Guven A, Kayikci A, Cam K, Arbak P, Balbay O, Cam M (2008) Alterations in semen parameters of toll collectors working at motorways: does diesel exposure induce detrimental effects on semen? Andrologia 40:346–351
Hammoud A, Carrell DT, Gibson M, Sanderson M, Parker-Jones K, Peterson CM (2010a) Decreased sperm motility is associated with air pollution in salt Lake City. Fertil Steril 93:1875–1879
Hammoud SS, Nix DA, Hammoud AO, Gibson M, Cairns BR, Carrell DT (2011) Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men. Hum Reprod 26:2558–2569
Hammoud SS, Purwar J, Pflueger C, Cairns BR, Carrell DT (2010b) Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility. Fertil Steril 94:1728–1733
Hauser R, Sokol R (2008) Science linking environmental contaminant exposures with fertility and reproductive health impacts in the adult male. Fertil Steril 89:e59–e65
Hayashi K, Chuva de Sousa Lopes SM, Kaneda M, Tang F, Hajkova P, Lao K, O’Carroll D, Das PP, Tarakhovsky A, Miska EA, Surani MA (2008) MicroRNA, biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One 3:e1738
Hernández-Ochoa I, Sánchez-Gutiérrez M, Solís-Heredia MJ, Quintanilla-Vega B (2006) Spermatozoa nucleus takes up lead during the epididymal maturation altering chromatin condensation. Reprod Toxicol 21:171–178
Hikim AP, Lue Y, Yamamoto CM, Vera Y, Rodriguez S, Yen PH, Soeng K, Wang C, Swerdloff RS (2003) Key apoptotic pathways for heat-induced programmed germ cell death in the testis. Endocrinology 144:3167–3175
Hou L, Wang D, Baccarelli A (2011) Environmental chemicals and microRNAs. Mutat Res 714:105–112
Hsu PC, Chang HY, Guo YL, Liu YC, Shih TS (2009) Effect of smoking on blood lead levels in workers and role of reactive oxygen species in lead-induced sperm chromatin DNA damage. Fertil Steril 91:1096–1103
Hughes IA, Martin H, Jaaskelainen J (2006) Genetic mechanisms of fetal male undermasculinization: a background to the role of endocrine disruptors. Environ Res 100:44–49
Huszar JM, Payne CJ (2013) MicroRNA 146 (Mir146) modulates spermatogonial differentiation by retinoic acid in mice. Biol Reprod 88:15
Ichiyanagi K, Li Y, Watanabe T, Ichiyanagi T, Fukuda K, Kitayama J, Yamamoto Y, Kuramochi-Miyagawa S, Nakano T, Yabuta Y, Seki Y, Saitou M, Sasaki H (2011) Locus- and domain- dependent control of DNA methylation at mouse B1 retrotransposons during male germ cell development. Genome Res 21:2058–2066
Irvine S, Cawood E, Richardson D, MacDonald E, Aitken J (1996) Evidence of deteriorating semen quality in the United Kingdom: birth cohort study in 577 men in Scotland over 11 years. Br Med J 312:467–471
Irvine DS, Twigg JP, Gordon EL, Fulton N, Milne PA, Aitken RJ (2000) DNA integrity in human spermatozoa: relationships with semen quality. J Androl 21:33–44
Jardim MJ (2011) microRNAs: implications for air pollution research. Mutat Res 717:38–45
Jardim MJ, Fry RC, Jaspers I, Dailey L, Diaz-Sanchez D (2009) Disruption of microRNA expression in human airway cells by diesel exhaust particles is linked to tumorigenesis-associated pathways. Environ. Health Perspect 117:1745–1751
Jeng HA, Yu L (2008) Alteration of sperm quality and hormone levels by polycyclic aromatic hydrocarbons on airborne particulate particles. J Environ Sci Health A Tox Hazard Subst Environ Eng 43:675–681
Jensen TK, Jacobsen R, Christensen K, Nielsen NC, Bostofte E (2009) Good semen quality and life expectancy: a cohort study of 43,277 men. Am J Epidemiol 170:559–565
Jorgensen N, Vierula M, Jacobsen R, Pukkala E, Perheentupa A, Virtanen HE, Skakkebaek NE, Toppari J (2011) Recent adverse trends in semen quality and testis cancer incidence among Finnish men. Int J Androl 34:e37–e48
Jurewicz J, Radwan M, Sobala W, Polańska K, Radwan P, Jakubowski L, Ulańska A, Hanke W (2015) The relationship between exposure to air pollution and sperm disomy. Environ Mol Mutagen 56:50–59
Khazaie Y, Nasr Esfahani MH (2014) MicroRNA and male infertility: a potential for diagnosis. Int J Fertil Steril 8:113–18e
Khazamipour N, Noruzinia M, Fatehmanesh P, Keyhanee M, Pujol P (2009) MTHFR promoter hypermethylation in testicular biopsies of patients with non-obstructive azoospermia: the role of epigenetics in male infertility. Hum Reprod 24:2361–2364
Kleene KC (2003) Patterns, mechanisms, and functions of translation regulation in mammalian spermatogenic cells. Cytogenet Genome Res 103:217–224
Kobayashi H, Sato A, Otsu E, Hiura H, Tomatsu C, Utsunomiya T, Utsunomiya T, Sasaki H, Yaegashi N, Arima T (2007) Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet 16:2542–2551
Kotaja N (2014) MicroRNAs and spermatogenesis. Fertil Steril 101:1552–1562
Laberge RM, Boissonneault G (2005) On the nature and origin of DNA strand breaks in elongating spermatids. Biol Reprod 73:289–296
Laurentino SS, Borgmann J, Gromoll J (2016) On the origin of sperm epigenetic heterogeneity. Reproduction 151:R71–R78
Lee J, Richburg JH, Younkin SC, Boekelheide K (1997) The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 138:2081–2088
Lopes S, Sun JG, Jurisicova A, Meriano J, Casper RF (1998) Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril 69:528–532
Maatouk DM, Loveland KL, McManus MT, Moore K, Harfe BD (2008) Dicer1 is required for differentiation of the mouse male germline. Biol Reprod 79:696–703
Manfo FP, Nantia EA, Mathur PP (2014) Effect of environmental contaminants on mammalian testis. Curr Mol Pharmacol 7:119–135
Marcon L, Boissonneault G (2004) Transient DNA strand breaks during mouse and human spermiogenesis new insights in stage specificity and link to chromatin remodeling. Biol Reprod 70:910–918 85
Marques CJ, Costa P, Vaz B, Carvalho F, Fernandes S, Barros A, Sousa M (2008) Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod 14:67–74
Martin RH (2008) Meiotic errors in human oogenesis and spermatogenesis. Reprod BioMed Online 16:523–531
Mazza A, Piscitelli P, Neglia C, Della Rosa G, Iannuzzi L (2015) Illegal dumping of toxic waste and its effect on human health in Campania, Italy. Int J Environ Res Public Health 12:6818–6831
McPherson S, Longo FJ (1993) Chromatin structure-function alterations during mammalian spermatogenesis: DNA nicking and repair in elongating spermatids. Eur J Histochem 37:109–128
Mendiola J, Jorgensen N, Andersson AM, Stahlhut RW, Liu F, Swan SH (2014) Reproductive parameters in young men living in Rochester, New York. Fertil Steril 101:1064–1071
Ménézo Y, Dale B, Cohen M (2010) DNA damage and repair in human oocytes and embryos: a review. Zygote 18:357–65
Merritt MA, De Pari M, Vitonis AF, Titus LJ, Cramer DW, Terry KL (2013) Reproductive characteristics in relation to ovarian cancer risk by histologic pathways. Hum Reprod 28:1406–1417
Moldan B, Schnoor JL (1992) Czechoslovakia: examining a critically ill environment. Environ Sci Technol 26:14–21
Montano L, Iannuzzi L, Rubes J, Avolio C, Pistos C, Gatti A, Notari T, Raimondo S (2014) EcoFoodFertility—environmental and food impact assessment on male reproductive function. Andrology 2:69
Muratori M, Marchiani S, Maggi M, Forti G, Baldi E (2006) Origin and biological significance of DNA fragmentation in human spermatozoa. Front Biosci 11:1491–1499
Muratori M, Piomboni P, Baldi E, Filimberti E, Pecchioli P, Moretti E, Gambera L, Baccetti B, Biagiotti R, Forti G, Maggi M (2000) Functional and ultrastructural features of DNA fragmented human sperm. J Androl 21:903–912
Navarro-Costa P, Nogueira P, Carvalho M, Leal F, Cordeiro I, Calhaz-Jorge C, Gonçalves J, Plancha CE (2010) Incorrect DNA methylation of the DAZL promoter CpG island associates with defective human sperm. Hum Reprod 25:2647–2654
Nicholls PK, Harrison CA, Walton KL, McLachlan RI, O’Donnell L, Stanton PG (2011) Hormonal regulation of sertoli cell micro-RNAs at spermiation. Endocrinology 152:1670–1683
Page H (1989) Estimation of the prevalence and incidence of infertility in a population: a pilot study. Fertil Steril 51:57l–577
Paradowska AS, Miller D, Spiess AN, Vieweg M, Cerna M, Dvorakova-Hortova K, Bartkuhn M, Schuppe HC, Weidner W, Steger K (2012) Genome wide identification of promoter binding sites for H4K12ac in human sperm and its relevance for early embryonic development. Epigenetics 7:1057–1070
Park CJ, Nah WH, Lee JE et al (2012) Butyl paraben-induced changes in DNA methylation in rat epididymal spermatozoa. Andrologia 44:187–193
Pinborg A, Henningsen AK, Malchau SS, Loft A (2013) Congenital anomalies after assisted reproductive technology. Fertil Steril 99:327–332
Poplinski A, Tüttelmann F, Kanber D, Horsthemke B, Gromoll J (2010) Idiopathic male infertility is strongly associated with aberrant methylation of MEST and IGF2/H19 ICR1. Int J Androl 33:642–649
Quintanilla-Vega B, Hoover D, Bal W, Silbergeld EK, Waalkes MP, Anderson LD (2000a) Lead effects on protamine-DNA binding. Am J Ind Med 38:324–329
Quintanilla-Vega B, Hoover DJ, Bal W, Silbergeld EK, Waalkes MP, Anderson LD (2000b) Lead interaction with human protamine (HP2) as a mechanism of male reproductive toxicity. Chem Res Toxicol 13:594–600
Radwan M, Jurewicz J, Polańska K, Sobala W, Radwan P, Bochenek M, Hanke W (2016) Exposure to ambient air pollution—does it affect semen quality and the level of reproductive hormones? Ann Hum Biol 43:50–56
Rajender S, Avery K, Agarwal A (2011) Epigenetics, spermatogenesis and male infertility. Mutat Res 727:62–71
Rives N, Perdrix A, Hennebicq S, Saias-Magnan J, Melin MC, Berthaut I, Barthélémy C, Daudin M, Szerman E, Bresson JL, Brugnon F, Bujan L (2012) The semen quality of 1158 men with testicular cancer at the time of cryopreservation: results of the French national CECOS network. J Androl 33:1394–1401
Robbins WA, Rubes J, Selevan SG, Perreault SD (1999) Air pollution and sperm aneuploidy in healthy young men. Environ Epidemiol Toxicol 1:125–131
Rolland M, Le Moal J, Wagner V, Royère D, De Mouzon J (2013) Decline in semen concentration and morphology in a sample of 26,609 men close to general population between 1989 and 2005 in France. Hum Reprod 28:462–470
Röösli M (2011) Non-cancer effects of chemical agents on children’s health. Prog Biophys Mol Biol 107:315–322
Rousseaux S, Caron C, Govin J, Lestrat C, Faure AK, Khochbin S (2005) Establishment of male-specific epigenetic information. Gene 345:139–153
Rubes Y, Dale B, Cohen M (2010a) DNA damage and repair in human oocytes and embryos: a review. Zygote 18:357–365
Rubes J, Rybar R, Prinosilova P, Veznik Z, Chvatalova I, Solansky I, Sram RJ (2010b) Genetic polymorphisms influence the susceptibility of men to sperm DNA damage associated with exposure to air pollution. Mutat Res 683:9–15
Rubes J, Selevan SG, Evenson DP, Zudova D, Vozdova M, Zudova Z, Robbins WA, Perreault SD (2005) Episodic air pollution is associated with increased DNA fragmentation in human sperm without other changes in semen quality. Hum Reprod 20:2776–2783
Rybar R, Markova P, Veznik Z, Faldikova L, Kunetkova M, Zajicova A, Kopecka V, Rubes J (2009) Sperm chromatin integrity in young men with no experiences of infertility and men from idiopathic infertility couples. Andrologia 41:141–149
Sakkas D, Mariethoz E, St John JC (1999a) Abnormal sperm parameters in humans are indicative of an abortive apoptotic mechanism linked to the Fas-mediated pathway. Exp Cell Res 251:350–355
Sakkas D, Mariethoz E, Manicardi G, Bizzaro D, Bianchi PG, Bianchi U (1999b) Origin of DNA damage in ejaculated human spermatozoa. Rev Reprod 4:31–37
Sakkas D, Seli E, Bizzaro D, Tarozzi N, Manicardi GC (2003) Abnormal spermatozoa in the ejaculate: abortive apoptosis and faulty nuclear remodelling during spermatogenesis. Reprod BioMed Online 7:428–432
Salas-Huetos A, Blanco J, Vidal F, Godo A, Grossmann M, Pons MC, F-Fernández S, Garrido N, Anton E (2015) Spermatozoa from patients with seminal alterations exhibit a differential micro-ribonucleic acid profile. Fertil Steril 104:591–601
Selevan SG, Borkovec L, Slott VL, Zudova Z, Rubes J, Evenson DP, Perreault SD (2000) Semen quality and reproductive health of young Czech men exposed to seasonal air pollution. Environ Health Perspect 108:887–894
Shanker S, Hu Z, Wilkinson MF (2008) Epigenetic regulation and downstream targets of the Rhox5 homeobox gene. Int J Androl 31:462–470
Sharma R, Biedenharn KR, Fedor JM, Agarwal A (2013) Lifestyle factors and reproductive health: taking control of your fertility. Reprod Biol Endocrinol 11:66
Shi Q, Martin RH (2000) Aneuploidy in human sperm: a review of the frequency and distribution of aneuploidy, effects of donor age and lifestyle factors. Cytogenet Cell Genet 90:219–226
Shufaro Y, Laufer N (2013) Epigenetic concerns in assisted reproduction: update and critical review of the current literature. Fertil Steril 99:605–606
Sikka SC, Rajasekaran M, Hellstrom WJ (1995) Role of oxidative stress and antioxidants in male infertility. J Androl 166:464–468
Sinha Hikim AP, Swerdloff RS (1999) Hormonal and genetic control of germ cell apoptosis in the testis. Rev Reprod 4:38–47
Skinner MK (2011) Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenetics 6:838–842
Skinner MK, Manikkam M, Guerrero-Bosagna C (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21:214–222
Sokol RZ, Kraft P, Fowler IM, Mamet R, Kim E, Berhane KT (2006) Exposure to environmental ozone alters semen quality. Environ Health Perspect 114:360–365
Sram RJ, Benes I, Binkova B, Dejmek J, Horstman D, Kotesovec F, Otto D, Perreault SD, Rubes J, Selevan SG, Skalík I, Stevens RK, Lewtas J (1996) Teplice program—the impact of air pollution on human health. Environ Health Perspect 104:699–714
Stouder C, Somm E, Paoloni-Giacobino A (2011) Prenatal exposure to ethanol: a specific effect on the H19 gene in sperm. Reprod Toxicol 31:507–512
Stuppia L, Franzago M, Ballerini P, Gatta V, Antonucci I (2015) Epigenetics and male reproduction: the consequences of paternal lifestyle on fertility, embryo development, and children lifetime health. Clin Epigenetics 7
Swan SH, Elkin EP, Fenster L (1997) Have sperm densities declined? A reanalysis of global trend data. Environ Health Perspect 105:1228–1232
Swan SH, Elkin EP, Fenster L (2000) The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ. Health Perspect 108:961–966
Tamburrino L, Marchiani S, Montoya M, Elia Marino F, Natali I, Cambi M, Forti G, Baldi E, Muratori M (2012) Mechanisms and clinical correlates of sperm DNA damage. Asian Journal of Andrology 14:24–31
Thompson ST (1993) Preventable causes of male infertility. World J Urol 11:111–119
Thompson, Forti G, Krausz C (1998) Clinical review 100: evaluation and treatment of the infertile couple. J Clin Endocrinol Metab 83:4177–4188
Tremellen K (2008) Oxidative stress and male infertility—a clinical perspective. Hum Reprod Update 14:243–258
Tsatsanis C, Bobjer J, Rastkhani H, Dermitzaki E, Katrinaki M, Margioris AN, Giwercman YL, Giwercman A (2015) Serum miR-155 as a potential biomarker of male fertility. Hum Reprod 30:853–860
Urdinguio RG, Bayón GF, Dmitrijeva M, Toraño EG, Bravo C, Fraga MF, Bassas L, Larriba S, Fernández AF (2015) Aberrant DNA methylation patterns of spermatozoa in men with unexplained infertility. Hum Reprod 30:1014–1028
Vecoli C, Pulignani S, Foffa I, Andreassi MG (2014) Congenital heart disease: the crossroads of genetics, epigenetics and environment. Curr Genomics 15:390–399
Vrijens K, Bollati V, Nawrot TS (2015) MicroRNAs as potential signatures of environmental exposure or effect: a systematic review. Environ Health Perspect 123:399–411
Wang C, Yang C, Chen X, Yao B, Yang C, Zhu C, Li L, Wang J, Li X, Shao Y, Liu Y, Ji J, Zhang J, Zen K, Zhang CY, Zhang C (2011) Altered profile of seminal plasma microRNAs in the molecular diagnosis of male infertility. Clin Chem 57:1722–1731
Wigle DT, Arbuckle TE, Turner MC, Bérubé A, Yang Q, Liu S, Krewski D (2008) Epidemiologic evidence of relationships between reproductive and child health outcomes and environmental chemical contaminants. J Toxicol Environ Health B Crit Rev 11:373–517
Wong EW, Cheng CY (2011) Impacts of environmental toxicants on male reproductive dysfunction. Trends Pharmacol Sci 32:290–299
Wu W, Hu Z, Qin Y, Dong J, Dai J, Lu C, Zhang W, Shen H, Xia Y, Wang X (2012) Seminal plasma microRNAs: potential biomarkers for spermatogenesis status. Mol Hum Reprod 18:489–497
Wu W, Shen O, Qin Y, Niu X, Lu C, Xia Y, Song L, Wang S, Wang X (2010) Idiopathic male infertility is strongly associated with aberrant promoter methylation of methylenetetrahydrofolate reductase (MTHFR. PLoS One 5:e13884
Yamauchi Y, Riel JM, Ward MA (2012) Paternal DNA damage resulting from various sperm treatments persists after fertilization and is similar prior and after DNA replication. J Androl 33:229–238
Zhang B, Pan X (2009) RDX induces aberrant expression of microRNAs in mouse brain and liver environ. Health Perspect 117:231–240
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Vecoli, C., Montano, L. & Andreassi, M.G. Environmental pollutants: genetic damage and epigenetic changes in male germ cells. Environ Sci Pollut Res 23, 23339–23348 (2016). https://doi.org/10.1007/s11356-016-7728-4
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DOI: https://doi.org/10.1007/s11356-016-7728-4