Effects of Maternal Lead Acetate Exposure during Lactation on Postnatal Development of Testis in Offspring Wistar Rats

Document Type: Original Article

Authors

1 Department of Biology, Faculty of Sciences, Shahid Chamran University of Ahwaz, Ahwaz, Iran

2 Department of Anatomical Sciences, Faculty of Medicine, Jondishapour Medical Sciences University of Ahwaz, Ahwaz, Iran

Abstract

Objective(s)
During recent years, there has been an increasing interest in contribution of environmental pollutants as heavy metals to human male infertility. Present study was aimed to investigate the effects of maternal lead acetate exposure during lactation on postnatal development of testis in offspring rats.
Materials and Methods
A total of 60 female rats randomly divided into four equal groups; control and three treatment groups received 20, 100 and 300 mg/kg/day lead acetate via drinking water from day 2 to day 21 of lactation. At 7, 14, 21, 28, 60, 90 and 120 days after birth, the testis weight and volume of offspring were measured and their epididymal semen analyzed. Following tissue processing, 5 μm sections were stained with haematoxylineosin and evaluated with quantitative techniques. Testicular parameters in different groups were compared by one-way ANOVA.
Results
Testis weight and volume of offspring decreased significantly in a dose-related manner in moderate (P< 0.05) and high (P< 0.01) doses groups. Dose-dependent significant reductions were seen in seminiferous tubules diameter and germinal epithelium height during neonatal, prepubertal and postpubertal periods in moderate (P< 0.05) and high (P< 0.01) doses groups until 90 and 120 days after birth, respectively. Significant decreases were observed in mean sperm density of offspring at puberty in moderate and high doses groups until 90 and 120 days after birth, respectively. Testosterone levels decreased significantly in a dose-related manner at puberty in moderate and high doses groups.
Conclusion
Present study showed maternal lead acetate exposure during lactation caused dose-related and long-term alterations of testicular parameters in offspring rats.

Keywords


1. Adamopoulos DA, Pappa A, Nicopoulou S, Andreou E, Karamertzanis M, Michopoulos J, et al. Seminal volume and total sperm number trends in men attending subfertility clinics in the greater Athens area during the period 1977-1993. Hum Reprod 1996; 11:1936-1941.

2. Auger J, Kunstmann JM, Czyglik F, Jouannet P. Decline in semen quality among fertile men in Paris during the past 20 years. N Engl J Med 1995; 332:281-285.

3. Becker S, Berhane K. Ameta-analysis of 61 sperm count studies revisited. Fertil Steril 1997; 67:1103-1108.

4. Carlsen E, Giwercman A, Keiding N, Skakkebaek NE. Evidence for decreasing quality of semen during the past 50 years. Br Med J 1992; 305: 609-613.

5. Bonde JE. The risk of male subfertility attributable to the welding of metals. Int J Androl 1993; 16:1-23.

6. Spinelli A, Figa-Talamanca I, Osborn I. Time to pregnancy and occupation in a group of Italian women. Int J Epidemiol 1997; 26: 601-609.

7. Benoff S, Jacob A, Hurley IR. Male infertility and environmental exposure to lead and cadmium. Hum Reprod Update 2000; 6:107-121.

8. Benoff S, Centola GM, Millan C, Napolitano B, Marmar JL, Hurley IR. Increased seminal plasma lead levels adversely affect the fertility potential of sperm in IVF. Hum Reprod 2003; 18: 374-383.

9. Wong WY, Thomas CMG, Merkus JMWM, Zielhuis GA, Steegers-Theunissen RPM. Male factor subfertility: possible causes and the impact of nutritional factor. Fertil Steril 2000; 73:435-442.

10. Cullen M, R, Kayne RD, Robins JM. Endocrine and reproductive dysfunction in men associated with occupational inorganic lead intoxication. Arch Environ Health 1984; 39:431-440.

11. Foster WG, McMahon A, Younglai EV, Hughes EG, Rice EC. Reproductive endocrine effects of chronic lead exposure in the male cynomolgus monkey. Reprod Toxicol 1993; 7:203-209.

12. Singh A, Cullen C, Dykeman A, Rice D, Foster W. Chronic lead exposure induces ultrastructural alterations in the monkey testis. J Submicrosc Cytol Pathol 1993; 25:479-486.

13. Sokol RZ. Hormonal effects of lead acetate in the male rat: mechanism of action. Biol Reprod 1987; 37:1135-1138.

14. McGivern RF, Sokol RZ, Berman NG. Prenatal lead exposure in the rat during the third week of gestation: Long-term behavioral, physiological, and anatomical effects associated with reproduction. Toxicol Appl Pharmacol 1991; 110:206-215.

15. Bogden JD, Gertner SB, Christakos S, Kemp FW, Yang Z, Katz SR, et al. Dietary calcium modifies concentrations of lead and other metals and renal calbindin in rats. J Nutr 1992; 122:1351-1360.

16. Corpas I, Castillo M, Marquina D, Benito MJ. Lead intoxication in gestational and lactation periods alters the development of male reproductive organs.Ecotoxicol Environ Saf 2002; 53:259-266.

17. Mann DR, Frase HM. The neonatal period: a critical interval in male primate development. J Endocinol 1996; 149:191-197.

18. Barratt C, Davies A, Bansal M, Williams M. The effects of lead on the male rat reproductive system. Andrologiam 1989; 21:161–166.

19. Petrusz P, Weaver CM, Grant LD, Mushak P, Krigman MR. Lead poisoning and reproduction effects on pituitary and serum gonadotropins in neonatal rats. Environ Res 1979; 19:383–391.

20. Abdel Moniem AE, Dkhil MA, Al-Quraishy S. Protective role of flaxseed oil against lead acetate induced oxidative stress in testes of adult rats. AJB 2010; 9:7216-7223.

21. Sprando RL. Perfusion of the rat testis through the heart using heparin. In: Russell LD, Ettlin RA, Sinha HAP, Clegg ED, editors. Histological and Histopathological Evaluation of the Testis. Clearwater:Cache River Press;1990.p.277-280.

22. Howard CV, Reed MG. Unbiased Stereology. 1st ed. Guilford: Bios Scientific Publishers; 1998.

23. Seed J, Chapin RE, Clegg ED, Dostal LA, Foote RH, Hurtt ME, et al. Methods for assessing sperm motility, morphology and counts in the rat, rabbit and dog: a consensus report. ILSI Risk Science Institute Expert Working Group on Sperm Evaluation. Reprod Toxicol 1996; 10:237–244.

24. Narayana K, Prashanthi N, Nayanatara A, Kumar HH, Abhilash K, Bairy KL. Effects of methyl parathion (o,odimethyl o-4-nitrophenyl phosphorothioate) on rat sperm morphology and sperm count, but not fertility, are associated with decreased ascorbic acid level in the testis. Mutat Res 2005; 588:28-34.

25. Gagnon C. The roles of environmental toxins in unexplained male infertility. Sem Reprod Endocrinol 1988; 6: 369-376.

26. Barry PSI. A comparison of concentration of lead in human tissues. Br J Ind Med 1975; 32: 19-136.

27. Ahmad I, Sabir M, Yasin KF. Study of the effects of lead poisoning on the testes in albino rats. Pak J Med Res 2003; 42:256-262.

28. Acharya UR, Acharya S, Mishra M. Lead acetate induced cytotoxicity in male germinal cells of Swiss mice. Ind Health 2003; 41:291–294.

29. Graça A, Ramalho-Santos J, Pereira ML. Effect of lead chloride on spermatogenesis and sperm parameters in mice. Asian J Androl 2004; 6:237–241.

30. Allouche L, Hamadouche M, Touabti A. Chronic effects of low lead levels on sperm quality, gonadotropins and testosterone in albino rats. Exp Toxicol Pathol 2009; 61:503-510.

31. Al-Omar MA, Abbas AK, Al-Obaidy SA. Combined effect of exposure to lead and chlordane on the testicular tissues of Swiss mice. Toxicol lett 2000; 10:1-8.

32. Coogan TP, Shiraishi N, Waalkes MP. Apparent quiescence of the metallothionein gene in the rat ventral prostate: Association with cadmium-induced prostate tumours in rats. Environ Health Perspect 1994; 102: 137-139.

33. Sokol RZ, Madding CE, Swerdloff RS. Lead toxicity and the hypothalamic-pituitary-testicular axis. Biol Reprod 1985; 33:722-778.

34. Moorman WJ, Skaggs SR, Clark JC, Turner TW, Sharpnack DD, Murrell JA, et al. Male reproductive effects of lead, including species extrapolation for the rabbit model. Reprod Toxicol 1998; 12:333-346.

35. Sokol RZ. Reversibility of the toxic effect of lead on the male reproductiv eaxis. Reprod Toxicol 1989; 3:175- 180.

36. Sokol RZ, Berman N. The effect of age of exposure on lead-induced testicular toxicity. Toxicology 1991; 69:269- 278.

37. Camoratto AM. Inhibition of rat pituitary growth hormone release by subclinical levels of lead. Toxicologists 1990; 10:641.

38. Assennato G, Paci C, Baser ME, Molinini R, Candela, RG, Altamura BM, et al. Sperm count suppression without endocrine dysfunction in lead-exposed men. Arch Environ Health 1987; 42:124-127.

39. Murthy RC. Lead induced ultrastructural changes in the testis of rats. Exp Pathol 1991; 42:95-100.