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. 2003 Sep;111(12):1505–1511. doi: 10.1289/ehp.6175

The relationship between human semen parameters and environmental exposure to polychlorinated biphenyls and p,p'-DDE.

Russ Hauser 1, Zuying Chen 1, Lucille Pothier 1, Louise Ryan 1, Larisa Altshul 1
PMCID: PMC1241654  PMID: 12948891

Abstract

Scientific and public concern exists about potential reproductive health effects of persistent chlorinated organic chemicals, such as polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane (DDT), and dichlorodiphenyldichloroethylene (DDE, the most stable daughter compound of DDT). To explore the hypothesis that environmental exposures to PCBs and DDE are associated with altered semen parameters, we conducted a cross-sectional study of 212 male partners of subfertile couples who presented to the Massachusetts General Hospital Andrology Laboratory. Semen parameters were analyzed as both a continuous measure and dichotomized based on World Health Organization reference values for sperm concentration (< 20 million/mL), motility (< 50% motile), and Kruger strict criteria for morphology (< 4% normal). The comparison group for the dichotomized analysis was men with all three semen parameters above the reference values. In serum, 57 PCB congeners and p,p -DDE were measured by congener-specific analysis using gas chromatography with electron capture detection. There were dose-response relationships among PCB-138 and sperm motility (odds ratio per tertile, adjusted for age, abstinence, and smoking, and p-value for trend were, respectively, 1.00, 1.68, 2.35, and p-value = 0.03) and morphology (1.00, 1.36, 2.53, p-value = 0.04). There was limited evidence of an inverse relationship between sum of PCBs, as well as those PCBs classified as cytochrome P450 enzyme inducers, with sperm motility and sperm morphology, as well as limited evidence of an inverse association between p,p -DDE and sperm motility. The lack of a consistent relationship among semen parameters and other individual PCB congeners and groupings of congeners may indicate a difference in spermatotoxicity between congeners.

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Selected References

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  1. Andersen A. G., Jensen T. K., Carlsen E., Jørgensen N., Andersson A. M., Krarup T., Keiding N., Skakkebaek N. E. High frequency of sub-optimal semen quality in an unselected population of young men. Hum Reprod. 2000 Feb;15(2):366–372. doi: 10.1093/humrep/15.2.366. [DOI] [PubMed] [Google Scholar]
  2. Auger J., Kunstmann J. M., Czyglik F., Jouannet P. Decline in semen quality among fertile men in Paris during the past 20 years. N Engl J Med. 1995 Feb 2;332(5):281–285. doi: 10.1056/NEJM199502023320501. [DOI] [PubMed] [Google Scholar]
  3. Ayotte P., Giroux S., Dewailly E., Hernández Avila M., Farias P., Danis R., Villanueva Díaz C. DDT spraying for malaria control and reproductive function in Mexican men. Epidemiology. 2001 May;12(3):366–367. doi: 10.1097/00001648-200105000-00022. [DOI] [PubMed] [Google Scholar]
  4. Berman N. G., Wang C., Paulsen C. A. Methodological issues in the analysis of human sperm concentration data. J Androl. 1996 Jan-Feb;17(1):68–73. [PubMed] [Google Scholar]
  5. Blackwell J. M., Zaneveld L. J. Effect of abstinence on sperm acrosin, hypoosmotic swelling, and other semen variables. Fertil Steril. 1992 Oct;58(4):798–802. doi: 10.1016/s0015-0282(16)55330-8. [DOI] [PubMed] [Google Scholar]
  6. Bonde J. P., Ernst E., Jensen T. K., Hjollund N. H., Kolstad H., Henriksen T. B., Scheike T., Giwercman A., Olsen J., Skakkebaek N. E. Relation between semen quality and fertility: a population-based study of 430 first-pregnancy planners. Lancet. 1998 Oct 10;352(9135):1172–1177. doi: 10.1016/S0140-6736(97)10514-1. [DOI] [PubMed] [Google Scholar]
  7. Bonde J. P., Giwercman A., Ernst E. Identifying environmental risk to male reproductive function by occupational sperm studies: logistics and design options. Occup Environ Med. 1996 Aug;53(8):511–519. doi: 10.1136/oem.53.8.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bujan L., Mansat A., Pontonnier F., Mieusset R. Time series analysis of sperm concentration in fertile men in Toulouse, France between 1977 and 1992. BMJ. 1996 Feb 24;312(7029):471–472. doi: 10.1136/bmj.312.7029.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bush B., Bennett A. H., Snow J. T. Polychlorobiphenyl congeners, p,p'-DDE, and sperm function in humans. Arch Environ Contam Toxicol. 1986 Jul;15(4):333–341. doi: 10.1007/BF01066399. [DOI] [PubMed] [Google Scholar]
  10. Bush B., Snow J., Koblintz R. Polychlorobiphenyl (PCB) congeners, p,p'-DDE, and hexachlorobenzene in maternal and fetal cord blood from mothers in Upstate New York. Arch Environ Contam Toxicol. 1984 Sep;13(5):517–527. doi: 10.1007/BF01056331. [DOI] [PubMed] [Google Scholar]
  11. Carlsen E., Giwercman A., Keiding N., Skakkebaek N. E. Evidence for decreasing quality of semen during past 50 years. BMJ. 1992 Sep 12;305(6854):609–613. doi: 10.1136/bmj.305.6854.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dallinga Jan W., Moonen Edwin J. C., Dumoulin John C. M., Evers Johannes L. H., Geraedts Joep P. M., Kleinjans Jos C. S. Decreased human semen quality and organochlorine compounds in blood. Hum Reprod. 2002 Aug;17(8):1973–1979. doi: 10.1093/humrep/17.8.1973. [DOI] [PubMed] [Google Scholar]
  13. DeVoto E., Fiore B. J., Millikan R., Anderson H. A., Sheldon L., Sonzogni W. C., Longnecker M. P. Correlations among human blood levels of specific PCB congeners and implications for epidemiologic studies. Am J Ind Med. 1997 Dec;32(6):606–613. doi: 10.1002/(sici)1097-0274(199712)32:6<606::aid-ajim6>3.0.co;2-n. [DOI] [PubMed] [Google Scholar]
  14. Fisch H., Goluboff E. T. Geographic variations in sperm counts: a potential cause of bias in studies of semen quality. Fertil Steril. 1996 May;65(5):1044–1046. doi: 10.1016/s0015-0282(16)58284-3. [DOI] [PubMed] [Google Scholar]
  15. Fisch H., Goluboff E. T., Olson J. H., Feldshuh J., Broder S. J., Barad D. H. Semen analyses in 1,283 men from the United States over a 25-year period: no decline in quality. Fertil Steril. 1996 May;65(5):1009–1014. doi: 10.1016/s0015-0282(16)58278-8. [DOI] [PubMed] [Google Scholar]
  16. Giwercman A., Carlsen E., Keiding N., Skakkebaek N. E. Evidence for increasing incidence of abnormalities of the human testis: a review. Environ Health Perspect. 1993 Jul;101 (Suppl 2):65–71. doi: 10.1289/ehp.93101s265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Irvine S., Cawood E., Richardson D., MacDonald E., Aitken J. Evidence of deteriorating semen quality in the United Kingdom: birth cohort study in 577 men in Scotland over 11 years. BMJ. 1996 Feb 24;312(7029):467–471. doi: 10.1136/bmj.312.7029.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jansen H. T., Cooke P. S., Porcelli J., Liu T. C., Hansen L. G. Estrogenic and antiestrogenic actions of PCBs in the female rat: in vitro and in vivo studies. Reprod Toxicol. 1993 May-Jun;7(3):237–248. doi: 10.1016/0890-6238(93)90230-5. [DOI] [PubMed] [Google Scholar]
  19. Jensen T. K., Vierula M., Hjollund N. H., Saaranen M., Scheike T., Saarikoski S., Suominen J., Keiski A., Toppari J., Skakkebaek N. E. Semen quality among Danish and Finnish men attempting to conceive. The Danish First Pregnancy Planner Study Team. Eur J Endocrinol. 2000 Jan;142(1):47–52. doi: 10.1530/eje.0.1420047. [DOI] [PubMed] [Google Scholar]
  20. Kelce W. R., Stone C. R., Laws S. C., Gray L. E., Kemppainen J. A., Wilson E. M. Persistent DDT metabolite p,p'-DDE is a potent androgen receptor antagonist. Nature. 1995 Jun 15;375(6532):581–585. doi: 10.1038/375581a0. [DOI] [PubMed] [Google Scholar]
  21. Kidd S. A., Eskenazi B., Wyrobek A. J. Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril. 2001 Feb;75(2):237–248. doi: 10.1016/s0015-0282(00)01679-4. [DOI] [PubMed] [Google Scholar]
  22. Korach K. S., Sarver P., Chae K., McLachlan J. A., McKinney J. D. Estrogen receptor-binding activity of polychlorinated hydroxybiphenyls: conformationally restricted structural probes. Mol Pharmacol. 1988 Jan;33(1):120–126. [PubMed] [Google Scholar]
  23. Korrick S. A., Altshul L. M., Tolbert P. E., Burse V. W., Needham L. L., Monson R. R. Measurement of PCBs, DDE, and hexachlorobenzene in cord blood from infants born in towns adjacent to a PCB-contaminated waste site. J Expo Anal Environ Epidemiol. 2000 Nov-Dec;10(6 Pt 2):743–754. doi: 10.1038/sj.jea.7500120. [DOI] [PubMed] [Google Scholar]
  24. Kruger T. F., Acosta A. A., Simmons K. F., Swanson R. J., Matta J. F., Oehninger S. Predictive value of abnormal sperm morphology in in vitro fertilization. Fertil Steril. 1988 Jan;49(1):112–117. doi: 10.1016/s0015-0282(16)59660-5. [DOI] [PubMed] [Google Scholar]
  25. Longnecker M. P., Rogan W. J., Lucier G. The human health effects of DDT (dichlorodiphenyltrichloroethane) and PCBS (polychlorinated biphenyls) and an overview of organochlorines in public health. Annu Rev Public Health. 1997;18:211–244. doi: 10.1146/annurev.publhealth.18.1.211. [DOI] [PubMed] [Google Scholar]
  26. Murphy R., Harvey C. Residues and metabolites of selected persistent halogenated hydrocarbons in blood specimens from a general population survey. Environ Health Perspect. 1985 May;60:115–120. doi: 10.1289/ehp.8560115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Paulsen C. A., Berman N. G., Wang C. Data from men in greater Seattle area reveals no downward trend in semen quality: further evidence that deterioration of semen quality is not geographically uniform. Fertil Steril. 1996 May;65(5):1015–1020. [PubMed] [Google Scholar]
  28. Phillips D. L., Pirkle J. L., Burse V. W., Bernert J. T., Jr, Henderson L. O., Needham L. L. Chlorinated hydrocarbon levels in human serum: effects of fasting and feeding. Arch Environ Contam Toxicol. 1989 Jul-Aug;18(4):495–500. doi: 10.1007/BF01055015. [DOI] [PubMed] [Google Scholar]
  29. Phillips D. L., Smith A. B., Burse V. W., Steele G. K., Needham L. L., Hannon W. H. Half-life of polychlorinated biphenyls in occupationally exposed workers. Arch Environ Health. 1989 Nov-Dec;44(6):351–354. doi: 10.1080/00039896.1989.9935905. [DOI] [PubMed] [Google Scholar]
  30. Richthoff Jonas, Rylander Lars, Jönsson Bo A. G., Akesson Heléne, Hagmar Lars, Nilsson-Ehle Peter, Stridsberg Mats, Giwercman Aleksander. Serum levels of 2,2',4,4',5,5'-hexachlorobiphenyl (CB-153) in relation to markers of reproductive function in young males from the general Swedish population. Environ Health Perspect. 2003 Apr;111(4):409–413. doi: 10.1289/ehp.5767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Safe S. Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Crit Rev Toxicol. 1990;21(1):51–88. doi: 10.3109/10408449009089873. [DOI] [PubMed] [Google Scholar]
  32. Sharpe R. M., Skakkebaek N. E. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet. 1993 May 29;341(8857):1392–1395. doi: 10.1016/0140-6736(93)90953-e. [DOI] [PubMed] [Google Scholar]
  33. Sherins R. J. Are semen quality and male fertility changing? N Engl J Med. 1995 Feb 2;332(5):327–328. doi: 10.1056/NEJM199502023320510. [DOI] [PubMed] [Google Scholar]
  34. Stehr-Green P. A. Demographic and seasonal influences on human serum pesticide residue levels. J Toxicol Environ Health. 1989;27(4):405–421. doi: 10.1080/15287398909531312. [DOI] [PubMed] [Google Scholar]
  35. Sun J. G., Jurisicova A., Casper R. F. Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod. 1997 Mar;56(3):602–607. doi: 10.1095/biolreprod56.3.602. [DOI] [PubMed] [Google Scholar]
  36. Swan S. H., Elkin E. P., Fenster L. Have sperm densities declined? A reanalysis of global trend data. Environ Health Perspect. 1997 Nov;105(11):1228–1232. doi: 10.1289/ehp.971051228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Vine M. F., Margolin B. H., Morrison H. I., Hulka B. S. Cigarette smoking and sperm density: a meta-analysis. Fertil Steril. 1994 Jan;61(1):35–43. [PubMed] [Google Scholar]
  38. Wolff M. S., Camann D., Gammon M., Stellman S. D. Proposed PCB congener groupings for epidemiological studies. Environ Health Perspect. 1997 Jan;105(1):13–14. doi: 10.1289/ehp.9710513. [DOI] [PMC free article] [PubMed] [Google Scholar]

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