Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-23T21:26:40.022Z Has data issue: false hasContentIssue false
  • English
  • Français

Prenatal exposure to an environmentally relevant mixture of Canadian Arctic contaminants decreases male reproductive function in an aging rat model

Part of: A Canadian perspective on DOHaD

Published online by Cambridge University Press:  13 August 2018

C. Maurice ,
M. Kaczmarczyk ,
N. Côté ,
Y. Tremblay ,
S. Kimmins  and
J. L. Bailey
C. Maurice
Affiliation:
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle, Département des Sciences Animales, Université Laval, Québec, QC, Canada
M. Kaczmarczyk
Affiliation:
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle, Centre de recherché du CHUQ, Unité d’ontogénie-reproduction, Université Laval, Québec, QC, Canada
N. Côté
Affiliation:
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle, Département des Sciences Animales, Université Laval, Québec, QC, Canada
Y. Tremblay
Affiliation:
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle, Centre de recherché du CHUQ, Unité d’ontogénie-reproduction, Université Laval, Québec, QC, Canada
S. Kimmins
Affiliation:
Department of Animal Sciences, McGill University, Ste. Anne de Bellevue, Quebec, H9X 3V9 Canada Department of Pharmacology and Therapeutics, McGill University, Montréal, QC, Canada
J. L. Bailey*
Affiliation:
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle, Département des Sciences Animales, Université Laval, Québec, QC, Canada
*
*Address for correspondence: J. L. Bailey, Ph.D., Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle, Département des Sciences Animales, Faculté des Sciences de l’Agriculture et de l’Alimentation, Pavillon Paul Comtois, 2425 rue de l’Agriculture, Université Laval, Québec, QC, Canada G1V 0A6. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Elevated levels of organochlorines (OC) have been reported in Inuit populations in the Arctic. We hypothesized that prenatal exposure to a Canadian Arctic OC mixture adversely affects male reproductive function and health with age. Sprague–Dawley female rats (F0) were gavaged with an environmentally relevant concentration of an Arctic OC mixture or corn oil (Control) during mating with untreated males until parturition (F1 litters). After postnatal day (PND) 90, the weights of the OC F1 males differed dramatically relative to Controls (P<0.05; n=10) and they exhibited respiratory distress. Except for possible thinning of the alveolar barrier, histological observation of the lungs revealed no apparent pathology to explain the respiratory distress. At PND 365, OC F1 males had reduced relative reproductive organ weights and lower sperm quality than Controls (P<0.05). At PND 90, OC F1 males were subfertile (P<0.05), but were infertile at PND 365. In conclusion, environmentally relevant prenatal OC exposure reduced reproductive function and health in aging male rats, providing new insight into the effects of early-life exposures to these contaminants.

Keywords

contaminantfertilitylungmaleprenatal exposure
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 5 , October 2018 , pp. 511 - 518
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Muir, DCG, Wagemann, R, Hargrave, BT, et al. Arctic marine ecosystem contamination. Sci Total Environ. 1992; 122, 75–134.Google Scholar
2. National Research Council. Hormonally Active Agents in the Environment, 1999; pp. 54–81. National Academies Press: Washington, DC.Google Scholar
3. Van Oostdam, J, Donaldson, SG, Feeley, M, et al. Human health implications of environmental contaminants in Arctic Canada: a review. Sci Total Environ. 2005; 351-352, 165–246.Google Scholar
4. Bjerregaard, P, Dewailly, É, Ayotte, P, et al. Exposure of Inuit in Greenland to OCs through the marine diet. J Toxicol Environ Health, Part A. 2001; 62, 69–81.Google Scholar
5. Ayotte, P, Muckle, G, Jacobson, JL, et al. Assessment of pre- and postnatal exposure to polychlorinated biphenyls: lessons from the Inuit cohort study. Environ Health Perspect. 2003; 111, 1253–1258.Google Scholar
6. Bonde, JP, Toft, G, Rylander, L, et al. Fertility and markers of male reproductive function in Inuit and European populations spanning large contrasts in blood Levels of persistent OCs. Environ Health Perspect. 2007; 116, 269–277.Google Scholar
7. De Jager, C, Farias, P, Barraza-Villarreal, A, et al. Reduced seminal parameters associated with environmental DDT exposure and p,p'-DDE concentrations in men in Chiapas, Mexico: a cross-sectional study. J Androl. 2006; 27, 16–27.Google Scholar
8. De Jager, C, Aneck-Hahn, NH, Bornman, MS, et al. Sperm chromatin integrity in DDT-exposed young men living in a malaria area in the Limpopo Province, South Africa. Hum Reprod. 2009; 24, 2429–2438.Google Scholar
9. Medehouenou, TCM, Ayotte, P, Carmichael, P-H, et al. Polychlorinated biphenyls and OC pesticides in plasma of older Canadians. Environ Res. 2011; 111, 1313–1320.Google Scholar
10. Flurkey, K, Currer, JM, Harrison, DE. Mouse models in aging research. In The Mouse in Biomedical Research. (eds. Fox JG, Davisson MT, Quimby FW, Barthold SW, Newcomer CE, and Smith AL), 2007; pp. 627–672. Elsevier, San Diego, CA.Google Scholar
11. Anas, M-K I, Guillemette, C, Ayotte, P, et al. In utero and lactational exposure to an environmentally relevant OC mixture disrupts reproductive development and function in male rats. Biol Reprod. 2005; 73, 414–426.Google Scholar
12. Burri, PH, Dbaly, J, Weibel, ER. The postnatal growth of the rat lung. I. Morphometry. Anat Rec. 1974; 178, 711–730.Google Scholar
13. Haberthur, D, Barré, SF, Tschanz, SA, et al. Visualization and stereological characterization of individual rat lung acini by high-resolution X-ray tomographic microscopy. J Appl Physiol. 1985; 115, 1379–1387.Google Scholar
14. Boucher, E, Provost, PR, Plante, J, et al. Androgen receptor and 17beta-HSD type 2 regulation in neonatal mouse lung development. Mol Cell Endocrinol. 2009; 311, 109–119.Google Scholar
15. Weibel, ER. Morphometric and stereological methods in respiratory physiology, including fixation techniques. In: Techniques in the Life Sciences, Part 1: Respiratory Physiology. (ed. Otis AB), 1984; pp. 1–35. Elsevier, Ireland.Google Scholar
16. Weibel, ER. Morphometric estimation of pulmonary diffusion capacity. Respir Physiol. 1970; 11, 54–75.Google Scholar
17. Nyengaard, JR, Gundensen, HJG. Sampling for stereology in lungs. Eur Respir Rev. 2006; 15, 107–114.Google Scholar
18. Seung, H, Wolfe, G, Rocca, M. Performing a testicular spermatid head count. Curr Protoc Toxicol. 2003; 16, 16.7.1–16.7.6.Google Scholar
19. Oberländer, G, Yeung, CH, Cooper, TG. Influence of oral administration of ornidazole on capacitation and the activity of some glycolytic enzymes of rat spermatozoa. J Reprod Fertil. 1996; 106, 231–239.Google Scholar
20. Donaldson, SG, Van Oostdam, J, Tikhonov, C, et al. Environmental contaminants and human health in the Canadian. Arctic Sci Total Environ. 2010; 408, 5165–5234.Google Scholar
21. Toft, G, Axmon, A, Giwercman, A, et al. Fertility in four regions spanning large contrasts in serum levels of widespread persistent organochlorines: a cross-sectional study. Environ Health. 2005; 4, 26.Google Scholar
22. Auger, N, Park, AL, Zoungrana, H, et al. Rates of stillbirth by gestional age and cause in Inuit and First Nations populations in Quebec. CMAJ. 2013; 185, E256–E262.Google Scholar
23. Stajkovic, S, Aitken, EM, Holroyd-Leduc, J. Unintentional weight loss in older adults. CMAJ. 2011; 183, 443–449.Google Scholar
24. Ochs, M, Mühlfeld, C. Quantitative microscopy of the lung: a problem-based approach. Part 1: basic principles of lung stereology. Am J Physiol Lung Cell Mol Physiol. 2013; 305, L15–L22.Google Scholar
25. Ye, M, Beach, J, Martin, JW, et al. Association between lung function in adults and plasma DDT and DDE levels: Results from the Canadian health measures survey. Environ Health Perspect. 2015; 123, 422–427.Google Scholar
26. Karmaus, W, Kuehr, J, Kruse, H. Infections and atopic disorders in childhood and organochlorine exposure. Arch Environ Health. 2001; 56, 485–492.Google Scholar
27. Gascon, M, Vrijheid, M, Martinez, D, et al. Prenatal exposure to dichlorodiphenydichloroethylene and infant lower respiratory tract infections and wheeze. Eur Respir J. 2012; 39, 1188–1196.Google Scholar
28. Dallaire, F, Dewailly, E, Muckle, G, et al. Acute infections and environmental exposure to organochlorines in Inuit infants from Nunavik. Environ Health Perspect. 2004; 112, 1359–1364.Google Scholar
29. Dallaire, F, Dewailly, E, Vézina, C, et al. Effect of prenatal exposure to polychlorinated bisphenyls on incidence of acute respiratory infections in preschool Inuit children. Environ Health Perspect. 2006; 114, 1301–1305.Google Scholar
30. Bozkurt, B, Mann, DL. Shortness of breath. Circulation. 2003; 108, e11–e13.Google Scholar
31. Scanga, CB, Verde, TJ, Paolone, AM, et al. Effect of weight loss and exercise training on natural killer cell activity in obese women. Med Sci Sports Exerc. 1998; 30, 1666–1669.Google Scholar
32. Bilrha, H, Roy, R, Wagner, E, et al. Effects of gestational and lactational exposure to organochlorine compounds on cellular, humoral, and innate immunity in swine. Toxicol Sci. 2003; 77, 41–50.Google Scholar
33. Sheppard, AJ, Hetherington, R. A decade of research in Inuit children, youth, and maternal health in Canada: areas of concentrations and scarcities. Int J Circumpolar Health. 2012; 71, 12.Google Scholar
34. De Roos, AJ, Ulrich, CM, Sjödin, A, et al. Adiposity, body composition, and weight change in relation to organochlorine pollutant plasma concentrations. J Expo Sci Environ Epidemiol. 2012; 22, 617–624.Google Scholar
35. Kidd, SA, Eskenazi, B, Wyrobek, AJ. Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril. 2001; 75, 237–248.Google Scholar
36. Bailey, JL. Factors regulating sperm capacitation. Sys Biol Reprod Med. 2010; 56, 334–348.Google Scholar
37. Liu, DY, Baler, HWG. Disordered zona pellucida-induced acrosome reaction and failure of in vitro fertilization in patients with unexplained infertility. Fertil Steril. 2003; 79, 74–80.Google Scholar
38. Skakkebaek, NE, Jorgensen, N, Main, KM, et al. Is human fecundity declining? Int J Androl. 2006; 29, 2–11.Google Scholar