Abstract
Purpose
We carried out a case–control study to investigate the possible role of occupational and environmental exposure to endocrine disruptors in the onset of testicular cancer (TC).
Methods
We evaluated 125 TC patients and 103 controls. Seminal fluid examination and organochlorine analysis were performed in all subjects. Cases and controls were also interviewed using a structured questionnaire to collect demographic information, residence, andrological medical history and dietary information.
Results
We found that a higher level of reproductive tract birth defects was associated with a higher risk of TC. With regard to diet, cases reported a higher consumption of milk and dairy products than controls. Overall, there was a statistically significant increase in TC risk in cases with detectable values of total polychlorinated organic compounds against controls (14.4 vs. 1.0 %; p < 0.001). TC patients with detectable levels of organochlorines had lower mean semen parameters than those with undetectable levels, although this difference was not statistically significant.
Conclusion
The International Agency for Research on Cancer recently included dioxin-like polychlorinated biphenyls (PCBs) in Group 1 of known human carcinogens. Our study confirmed and identified various risk factors for testicular cancer: cryptorchidism, consumption of milk and dairy products, parents’ occupation and serum concentration of hexachlorobenzene and PCBs and, for the first time, we showed the correlation between semen quality and the serum concentration of these pollutants.
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References
Crocetti E, AIRTUM Working Group. Numbers (2009) Testis cancer is the most frequent neoplasia among young men. Epidemiol Prev 33:145
Le Cornet C, Lortet-Tieulent J, Forman D et al (2014) Testicular cancer incidence to rise by 25 % by 2025 in Europe? Model-based predictions in 40 countries using population-based registry data. Eur J Cancer 50:831–839
Weir HK, Marrett LD, Kreiger N, Darlington GA, Sugar L (2000) Pre-natal and peri-natal exposures and risk of testicular germ-cell cancer. Int J Cancer 87:438–443
Monograph IARC Working Group (2013) Carcinogenicity of polychlorinated biphenyls and polybrominated biphenyls. Lancet Oncol 14:287–288
Hardell L, van Bavel B, Lindström G et al (2003) Increased concentrations of polychlorinated biphenyls, hexachlorobenzene, and chlordanes in mothers of men with testicular cancer. Environ Health Perspect 111:930–934
Hardell L, Van Bavel B, Lindström G et al (2004) Concentrations of polychlorinated biphenyls in blood and the risk for testicular cancer. Int J Androl 27:282–290
Hardell L, Bavel B, Lindström G, Eriksson M, Carlberg M (2006) In utero exposure to persistent organic pollutants in relation to testicular cancer risk. Int J Androl 29:228–234
McGlynn KA, Quraishi SM, Graubard BI, Weber JP, Rubertone MV, Erickson RL (2008) Persistent organochlorine pesticides and risk of testicular germ cell tumors. J Natl Cancer Inst 100:663–671
Biggs ML, Davis MD, Eaton DL et al (2008) Serum organochlorine pesticide residues and risk of testicular germ cell carcinoma: a population-based case–control study. Cancer Epidemiol Biomarkers Prev 17:2012–2018
McGlynn KA, Quraishi SM, Graubard BI, Weber JP, Rubertone MV, Erickson RL (2009) Polychlorinated biphenyls and risk of testicular germ cell tumors. Cancer Res 69:1901–1909
Purdue MP, Engel LS, Langseth H et al (2009) Prediagnostic serum concentrations of organochlorine compounds and risk of testicular germ cell tumors. Environ Health Perspect 117:1514–1519
Giannandrea F, Gandini L, Paoli D, Turci R, Figà-Talamanca I (2011) Pesticide exposure and serum organochlorine residuals among testicular cancer patients and healthy controls. Environ Sci Health B 46:780–787
Van Tongeren M, Nieuwenhuijsen MJ, Gardiner K et al (2002) A job-exposure matrix for potential endocrine-disrupting chemicals developed for a study into the association between maternal occupational exposure and hypospadias. Ann Occup Hyg 46:465–477
World Health Organisation (2010) WHO laboratory manual for the examination and processing of human semen, 5th edn. WHO Press, Geneva
Turci R, Balducci C, Brambilla G et al (2010) A simple and fast method for the determination of selected organohalogenated compounds in serum samples from the general population. Toxicol Lett 192:66–71
Del Mazo J, Brieño-Enríquez MA, García-López J, López-Fernández LA, De-Felici M (2013) Endocrine disruptors, gene deregulation and male germ cell tumors. Int J Dev Biol 57:225–239
Youngson NA, Whitelaw E (2008) Transgenerational epigenetic effects. Annu Rev Genomics Hum Genet 9:233–257
Cook MB, Graubard BI, Rubertone MV, Erickson RL, McGlynn KA (2008) Perinatal factors and the risk of testicular germ cell tumors. Int J Cancer 122:2600–2606
Cook MB, Akre O, Forman D, Madigan MP, Richiardi L, McGlynn KA (2010) A systematic review and meta-analysis of perinatal variables in relation to the risk of testicular cancer-experiences of the son. Int J Epidemiol 39:1605–1618
Garner MJ, Birkett NJ, Johnson KC, Shatenstein B, Ghadirian P, Kreswski D (2003) Dietary risk factors for testicular carcinoma. Int J Cancer 106:934–941
Stang A, Ahrens W, Baumgardt-Elms C et al (2006) Adolescent milk fat and galactose consumption and testicular germ cell cancer. Cancer Epidemiol Biomark Prev 15:2189–2195
McGlynn KA, Trabert B (2012) Adolescent and adult risk factors for testicular cancer. Nat Rev Urol 9:339–349
Arisawa K, Uemura H, Hiyoshi M et al (2011) Dietary patterns and blood levels of PCDDs, PCDFs, and dioxin-like PCBs in 1656 Japanese individuals. Chemosphere 82:656–662
Boada LD, Sangil M, Alvarez-León EE et al (2014) Consumption of foods of animal origin as determinant of contamination by organochlorine pesticides and polychlorobiphenyls: results from a population-based study in Spain. Chemosphere 114:121–128
Sharpe RM, Skakkebaek NE (1993) Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet 341:1392–1395
Giannandrea F, Paoli D, Figà-Talamanca I, Lombardo F, Lenzi A, Gandini L (2013) Effect of endogenous and exogenous hormones on testicular cancer: the epidemiological evidence. Int J Dev Biol 57:255–263
Béranger R, Le Cornet C, Schüz J, Fervers B (2013) Occupational and environmental exposures associated with testicular germ cell tumours: systematic review of prenatal and life-long exposures. PLoS One 8:e77130
Carlsen E, Giwercman A, Keiding N, Skakkebaek NE (1992) Evidence for decreasing quality of semen during past 50 years. BMJ 305:609–613
Gandini L, Lombardo F, Culasso F, Dondero F, Lenzi A (2000) Myth and reality of the decline in semen quality: an example of the relativity of data interpretation. J Endocrinol Invest 23:402–411
Shine R, Peek J, Birdsall M (2008) Declining sperm quality in New Zealand over 20 years. N Z Med J 121:50–56
Feki NC, Abid N, Rebai A et al (2009) Semen quality decline among men in infertile relationships: experience over 12 years in the South of Tunisia. J Androl 30:541–547
Geoffroy-Siraudin C, Loundou AD, Romain F et al (2012) Decline of semen quality among 10,932 males consulting for couple infertility over a 20-year period in Marseille, France. Asian J Androl 14:584–590
Dama MS, Rajender S (2012) Secular changes in the semen quality in India during the past 33 years. J Androl 33:740–744
Haimov-Kochman R, Har-Nir R, Ein-Mor E et al (2012) Is the quality of donated semen deteriorating? Findings from a 15 year longitudinal analysis of weekly sperm samples. Isr Med Assoc J 14:372–377
Martenies SE, Perry MJ (2013) Environmental and occupational pesticide exposure and human sperm parameters: a systematic review. Toxicology 307:66–73
Messaros BM, Rossano MG, Liu G et al (2009) Negative effects of serum p, p′-DDE on sperm parameters and modification by genetic polymorphisms. Environ Res 109:457–464
Acknowledgments
The authors wish to thank Marie-Hélène Hayles for her assistance in the English translation of the manuscript and Prof. Irene Figà Talamanca for her helpful discussions of the data. This work was supported by a grant from the Italian Ministry of Education and Research (MIUR-PRIN) and the University of Rome “La Sapienza” Faculty of Medicine.
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The authors have no conflicts of interest.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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Informed consent was obtained from all individual participants included in the study.
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Paoli, D., Giannandrea, F., Gallo, M. et al. Exposure to polychlorinated biphenyls and hexachlorobenzene, semen quality and testicular cancer risk. J Endocrinol Invest 38, 745–752 (2015). https://doi.org/10.1007/s40618-015-0251-5
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DOI: https://doi.org/10.1007/s40618-015-0251-5