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Sperm Changes in Men Exposed to Polychlorinated Biphenyls and Dibenzofurans
To the Editor: Between 1978 and 1979, more than 2000 people in Taiwan ingested rice oil contaminated with polychlorinated biphenyls (PCBs) and their pyrolytic product, mainly polychlorinated dibenzofurans (PCDFs). This event has been referred to as the "Yucheng exposure."1 A previous study of the sperm of young men born to Yucheng women exposed to PCBs/PCDFs showed increased abnormal morphology, reduced motility, and reduced capacity to penetrate hamster oocytes.2 Effects of postnatal exposure to PCBs/PCDFs on sperm quality, however, are less well documented. We assessed the sperm quality of men directly exposed to PCBs/PCDFs in the Yucheng exposure.
Methods
In 1991, a matched control group was identified for members of a registry of individuals exposed to the Yucheng event.3 We used the 1979 addresses of the registry members as index addresses and attempted to identify persons who lived nearby in 1979 from the archives of the registration offices. We began with a higher- or lower-numbered dwelling at random, locating the record of the current household. If that family had not been there in 1979, we worked through the archived records until we found the record of the family who had lived there at the time. We then identified the members of each family and attempted to identify a control within it. Controls had to be of the same sex, within 3 years of age of the index registry member, and not in the registry themselves. If a household contained no eligible control, the next closest household was tried. We identified 3 controls for each registry member and attempted to contact the control living nearest to the index address in 1979. Our study was approved by the local institutional review board.
In 1999-2002, exposed men and their controls aged 37 to 50 years were recruited for physical examination followed by semen analysis. A total of 40 men exposed to PCBs/PCDFs and 28 unexposed matched controls participated in the study. Participants were instructed to abstain from ejaculation for at least 4 days prior to providing semen specimens. Evaluations of sperm counts, morphology, motility, and velocity were measured according to World Health Organization guidelines.4 Hamster oocyte penetration was assessed after 1 cycle of storage in liquid nitrogen. All interview, examination, and laboratory tests were computed in a blinded fashion. P values for all comparisons were made by the Fisher exact test.
Results
Age, body weight, percentage of smokers, frequency of erection, number of children, and frequency of intercourse were not different between exposed and control men. Exposed men were found to have higher abnormal morphology and oligospermia rate than controls (Table 1). Semen volume, sperm count, motility, velocity, amplitude of lateral displacement, and beat-cross frequency were similar in sperm of exposed and control men. The ability of sperm to penetrate hamster oocytes and the number of sperm bound to hamster oocytes, however, were significantly reduced in exposed men.
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Table. Age, Physical Examination, History Relevant to Reproductive System, and Semen Characteristics in Men Directly Exposed to PCBs/PCDFs and Unexposed Controls*
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Comment
To our knowledge, this is the first report on sperm changes in PCB/PCDF-exposed men. Exposed men had a higher percentage of oligospermia, abnormal morphology, and reduced sperm capability of binding and penetration. These findings are compatible with animal studies in which postnatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin reduced sperm motility and daily production.5 Sperm findings in this study were similar to the second-generation young men prenatally exposed to PCBs/PCDFs2 in reduced normal morphology and reduced capability of oocyte penetration. The prenatally exposed young men had the additional finding of reduced sperm motility. The male to female offspring ratio was reduced in Yucheng men exposed to PCBs/PCDFs before age 20 years.6 It is unclear whether the reduced capability of oocyte penetration found in this study was specific to Y chromosome–bearing sperm.
The fact that reduced capability of sperm-oocyte binding and penetration and an increased oligospermia rate were found 20 years after exposure suggests long-lasting damage to the male reproductive system. Whether fecundity and integrity of Y chromosome–bearing sperm are reduced in exposed men and how these effects can be extrapolated to the general population exposed to background levels of PCBs, PCDFs, and dioxinlike chemicals warrant further investigation.
Funding/Support: This study was funded by grant NSC88-2314-B-006-117 from the National Science Council of Taiwan, grant NHRI-EX90-9025PL from the National Health Research Institute, Taiwan, grant R82939101 from the US Environmental Protection Agency, and grant ES11256 from the US National Institute for Environmental Health Science.
AUTHOR INFORMATION
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Ping-Chi Hsu, PhD
National Kaohsiung First University of Science and Technology
Kaohsiung, Taiwan
Wenya Huang, PhD;
Wei-Jen Yao, MD;
Meng-Hsing Wu, MD;
Yueliang Leon Guo, MD, MPH, PhD
National Cheng Kung University Medical College
Tainan, Taiwan
George H. Lambert, MD
Environmental and Occupational Health Service Institute
Robert Wood Johnson Medical School
University of Medicine and Dentistry of New Jersey
Piscataway
Corresponding Author: Yueliang Leon Guo, MD, MPH, PhD, Department of Occupational & Environmental Health, National Cheng Kung University Medical College, 138 Sheng Li Rd, Tainan 70428, Taiwan (e-mail: leonguo{at}mail.ncku.edu.tw).
1. Hsu ST, Ma CI, Hsu SK, et al. Discovery and epidemiology of PCB poisoning in Taiwan: a four-year followup. Environ Health Perspect. 1985;59:5-10.
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2. Guo YL, Hsu PC, Hsu CC, et al. Sperm changes in humans prenatally exposed to polychlorinated biphenyls and dibenzofurans. Lancet. 2000;356:1240-1241.
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3. Guo YL, Yu ML, Hsu CC, et al. Goiter, skin diseases, arthralgia, and anemia after PCB/PCDF poisoning: 14 year follow-up of the Taiwan Yucheng cohort. Environ Health Perspect. 1999;107:715-719.
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4. World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Seminal-Cervical Mucus Interaction. Cambridge, England: Cambridge University Press; 1992.
5. Faqi AS, Dalsenter PR, Merker HJ, et al. Reproductive toxicity and tissue concentrations of low doses of 2,3,7,8-tetrachlorodibenzo-p-dioxin in male offspring rats exposed throughout pregnancy and lactation. Toxicol Appl Pharmacol. 1998;150:383-392.
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6. del Rio Gomez I, Marshall T, Tsai PC, et al. Number of boys born to men exposed to polychlorinated biphenyls. Lancet. 2002;360:143-144.
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Letters Section Editor: Stephen J. Lurie, MD, PhD, Senior Editor.
JAMA. 2003;289:2943-2944.
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