The Prenatal Toxic Effect of Methylmercury on the Development of the Appendicular Skeleton of Rat Fetuses and the Protective Role of Vitamin E

Anatomical Record

Volumn 295, Issue 6, 2012, Pages 939-949

  Abd El Aziz, Gamal S ^a   El Fark, Magdy M O ^a   Saleh, Hamid A M ^a  

^a KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Appendicular skeleton; Methylmercury; Vitamin E

Indexed keywords

ALPHA TOCOPHEROL; METHYLMERCURY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DEVELOPMENT; CONTROLLED STUDY; DNA DAMAGE; FEMALE; FETOTOXICITY; FETUS; FETUS DEVELOPMENT; FETUS GROWTH; FORELIMB; GESTATIONAL AGE; HINDLIMB; LIMB DEVELOPMENT; LIPID PEROXIDATION; MALE; MERCURIALISM; NONHUMAN; OSSIFICATION; OXIDATIVE STRESS; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT;

ABNORMALITIES, DRUG-INDUCED; ANIMALS; ANTIOXIDANTS; BONE AND BONES; CROWN-RUMP LENGTH; DRUG ANTAGONISM; EXTREMITIES; FEMALE; FETAL WEIGHT; HEAD; MATERNAL EXPOSURE; MERCURY POISONING; METHYLMERCURY COMPOUNDS; OSTEOGENESIS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; VITAMIN E;

RATTUS;

EID: 84860918303     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.22485     Document Type: Article

References (88)

1. Ali SF, LeBel CP, Bondy SC. 1992. Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity. Neurotoxicology 13: 637-648.
2. Aliverti V, Bonanomi L, Giavini E, Leone VG, Mariani L. 1979. The extent of fetal ossification as an index of delayed development in teratogenic studies on the rat. Teratology 20: 237-242.
3. Ariyuki F, Ishihara H, Higaki K, Yasuda M. 1982. A study of fetal growth retardation in teratological tests: relationship between body weight and ossification of the skeleton in rat fetuses. Teratology 26: 263-267.
4. Bakir F, Damluji SF, Amin-Zaki L, Murtadha M, Khalidi A, Al-Rawi NY, Tikriti S, Dhahir HI, Clarkson TW, Smith JC, Doherty RA. 1973. Methylmercury poisoning in Iraq. Science 181: 230-241.
5. Beck SL. 1989. Prenatal ossification as an indicator of exposure to toxic agents. Teratology 40: 365-374.
6. Beyrouty P, Chan HM. 2006. Co-consumption of selenium and vitamin E altered the reproductive and developmental toxicity of methylmercury in rats. Neurotoxicol Teratol 28: 49-58.
7. Beytut E, Yuce A, Kamiloglu NN, Aksakal M. 2003. Role of dietary vitamin E in cadmium-induced oxidative damage in rabbit's blood, liver and kidneys. Int J Vitam Nutr Res 73: 351-355.
8. Björnberg KA, Vahter M, Petersson-Grawé K, Glynn A, Cnattingius S, Darnerud PO, Atuma S, Aune M, Becker W, Berglund M. 2003. Methylmercury and inorganic mercury in Swedish pregnant women and in cord blood: influence of fish consumption. Environ Health Perspect 111: 637-641.
9. Bland M. 2000. An introduction to medical statistics. 3rd ed. Oxford UK: Oxford University Press. p 137-265.
10. Bornhausen M, Müsch H, Greim H. 1980. Operant behavior performance changes in rats after prenatal methylmercury exposure. Toxicol Appl Pharmacol 56: 305-310.
11. Carney EW, Kimmel CA. 2007. Interpretation of skeletal variations for human risk assessment: delayed ossification and wavy ribs. Birth Defects Res B Dev Reprod Toxicol 80: 473-496.
12. Chahoud I, Paumgartten FJR. 2005. Relationships between fetal body weight of Wistar rats at term and the extent of skeletal ossification. Braz J Med Biol Res 38: 565-575.
13. Chahoud I, Paumgartten FJR. 2009. Dose-response relationships of rat fetal skeleton variations: relevance for risk assessment. Environ Res 109: 922-929.
14. Chahoud I, Buschmann J, Clark R, Druga A, Falke H, Faqi A, Hansen E, Heinrich-Hirsch B, Hellwig J, Lingk W, Parkinson M, Paumgartten FJR, Pfeil R, Platzek T, Scialli AR, Seed J, Stahlmann R, Ulbrich B, Wu X, Yasuda M, Younes M, Solecki R. 1999. Classification terms in developmental toxicology: need for harmonisation. Reprod Toxicol 13: 77-82.
15. Chang LW, Gilbert M, Sprecher J. 1978. Modification of methylmercury neurotoxicity by vitamin E. Environ Res 17: 356-366.
16. Cooper C, Westlake S, Harvey N, Javaid K, Dennison E, Hanson M. 2006. Review: developmental origins of osteoporotic fracture. Osteoporos Int 17: 337-347.
17. Cox C, Clarkson TW, Marsh DO, Amin-Zaki L, Tikriti S, Myers GG. 1989. Dose-response analysis of infants prenatally exposed to methyl mercury: an application of a single compartment model to single-strand hair analysis. Environ Res 49: 318-332.
18. Danielson M, Kihlström I. 1986. Calcification of the rabbit fetal skeleton. Growth 50: 378-384.
19. Dreiem A, Gertz CC, Seegal RF. 2005. The effects of methylmercury on mitochondrial function and reactive oxygen species formation in rat striatal synaptosomes are age-dependent. Toxicol Sci 87: 156-162.
20. Eccles CU, Annau Z. 1982. Prenatal methyl mercury exposure. I. Alterations in neonatal activity. Neurobehav Toxicol Teratol 4: 371-376.
21. Eisler R. 2004. Mercury hazards from gold mining to humans, plants, and animals. Rev Environ Contam Toxicol 181: 139-198.
22. El-Gharieb MA, El-Masry TA, Emara AM, Hashem MA. 2010. Potential hepatoprotective effects of vitamin E and Nigella sativa oil on hepatotoxicity induced by chronic exposure to malathion in human and male albino rats. Toxicol Environ Chem 2: 391-407.
23. El-Hage S, Singh SM. 1990a. Temporal expression of genes encoding free radical-metabolizing enzymes is associated with higher mRNA levels during in utero development in mice. Dev Genet 11: 149-159.
24. El-Hage SS, Singh M. 1990b. A 5-fold reduction in sister-chromatid exchange following implantation of mouse embryos is not directly related to the expression of embryonic genes responsible for oxygen radical metabolism. Mutat Res 232: 217-226.
25. Evstigneeva RP, Volkov IM, Chudinova VV. 1998. Vitamin E as a universal antioxidant and stabilizer of biological membranes. Membr Cell Biol 12: 151-172.
26. Fantel AG. 1996. Reactive oxygen species in developmental toxicity: review and hypothesis. Teratology 53: 196-217.
27. Fiore G, Capasso A. 2008. Effects of vitamin E and C on placental oxidative stress: an in vitro evidence for the potential therapeutic or prophylactic treatment of preeclampsia. Med Chem 4: 526-530.
28. Fredriksson A, Gårdlund A, Bergman K, Oskarsson A, Ohlin B, Danielsson B, Archer T. 1993. Effects of maternal dietary supplementation with selenite on the postnatal development of rat offspring exposed to methyl mercury in-utero. Pharmacol Toxicol 72: 377-382.
29. Fritz H. 1975. Prenatal ossification in rabbits as indicative of fetal maturity. Teratology 11: 313-319.
30. Fuyuta M, Fujimoto T, Hirata S. 1978. Embryotoxic effects of methylmercuric chloride administered to mice and rats during orangogenesis. Teratology 18: 353-365.
31. Ganther HE, Goudie C, Sunde ML, Kopecky MJ, Wagner P. 1972. Selenium: relation to decreased toxicity of methylmercury added to diets containing tuna. Science 175: 1122-1124.
32. Gilbert SG, Grant-Webster KS. 1995. Neurobehavioral effects of developmental methylmercury exposure. Environ Health Perspect 103: 135-142.
33. Goldman LR, Shannon MW. 2001. American Academy of Pediatrics: Committee on Environmental Health. Technical report: mercury in the environment: implications for pediatricians. Pediatrics 108: 197-205.
34. Grandjean P, Weihe P, White R F, Debes F, Araki S, Yokoyama K, Murata K, Sørensen N, Dahl R, Jørgensen PJ. 1997. Cognitive deficits in 7-year old children with prenatal exposure to methylmercury. Neurotoxicol Teratol 19: 417-428.
35. Harada M. 1995. Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Crit Rev Toxicol 25: 1-24.
36. Hare MF, Atchison WD. 1992. Comparative action of methylmercury and divalent inorganic mercury on nerve terminal and intraterminal mitochondrial membrane potentials. J Pharmacol Exp Ther 261: 166-172.
37. Harvey N, Cooper C. 2004. The developmental origins of osteoporotic fracture. J Br Menopause Soc 10: 14-15, 29.
38. Horlick M, Wang J, Pierson RN Jr, Thornton JC. 2004. Prediction models for evaluation of total-body bone mass with dual-energy X-ray absorptiometry among children and adolescents. Pediatrics 114: e337-e345.
39. Hoskins BB, Hupp EW. 1978. Methylmercury effects in rat, hamster, and squirrel monkey. Environ Res 15: 5-19.
40. Ibrahim W, Chow CK. 2005. Dietary vitamin E reduces labile iron in rat tissues. J Biochem Mol Toxicol 19: 298-303.
41. Igarashi E, Kawamura N, Okumura H, Hotta K, Okamoto T, Inaoka M, Takeshita S, Tasuda M. 1992. Frequency of spontaneous axial skeletal variations detected by the double staining technique for ossified and cartilaginous skeleton in rat fetuses. Congenit Anom 32: 381-391.
42. Jalili Sh, Ilkhanipour M, Heydari R, Farshid AA, Salehi S. 2007. The effects of vitamin E on endosulfan-induced oxidative stress in rat heart. Pakistan J Nutr 6: 375-380.
43. Jansson T, Powell TL. 2007. Role of the placenta in fetal programming: underlying mechanisms and potential interventional approaches. Clin Sci (Lond) 113: 1-13.
44. Javaid MK, Cooper C. 2002. Prenatal and childhood influences on osteoporosis. Best Pract Res Clin Endocrinol Metab 16: 349-367.
45. Komulainen H, Bondy SC. 1987. Increased free intrasynaptosomal Ca2+ by neurotoxic organometals: distinctive mechanisms. Toxicol Appl Pharmacol 88: 77-86.
46. Kunimoto M. 1994. Methylmercury induces apoptosis of rat cerebellar neurons in primary culture. Biochem Biophys Res Commun 204: 310-317.
47. Lee JH, Han DH. 1995. Maternal and fetal toxicity of methylmercuric chloride administered to pregnant Fischer 344 rats. J Toxicol Environ Health 45: 415-425.
48. Lee DE, Kehlenbrink S, Lee H, Hawkins M, Yudkin JS. 2009. Getting the message across: mechanisms of physiological cross talk by adipose tissue. Am J Physiol Endocrinol Metab 296: E1210-E1229.
49. Liang C, Oest ME, Jones JC, Prater MR. 2009. Gestational high saturated fat diet alters C57BL/6 mouse perinatal skeletal formation. Birth Defects Res B Dev Reprod Toxicol 86: 362-369.
50. Limke TL, Atchison WD. 2002. Acute exposure to methylmercury opens the mitochondrial permeability transition pore in rat cerebellar granule cells. Toxicol Appl Pharmacol 178: 52-61.
51. Mahaffey KR, Clickner RP, Bodurow CC. 2004. Blood organic mercury and dietary mercury intake: National Health and Nutrition Examination Survey, 1999 and 2000. Environ Health Perspect 112: 562-570.
52. Marsh DO, Clarkson TW, Cox C, Myers GJ, Amin-Zaki L, Al-Tikriti S. 1987. Fetal methylmercury poisoning. Relationship between concentration in single strands of maternal hair and child effects. Arch Neurol 44: 1017-1022.
53. Marty MS, Atchison WD. 1997. Pathways mediating Ca2+ entry in rat cerebellar granule cells following in vitro exposure to methyl mercury. Toxicol Appl Pharmacol 147: 319-330.
54. Menegola E, Broccia ML, Giavini E. 2001. Atlas of rat fetal skeleton double stained for bone and cartilage. Teratology 64: 125-133.
55. Murata K, Weihe P, Budtz-Jørgensen E, Jørgensen PJ, Grandjean P. 2004. Delayed brainstem auditory evoked potential latencies in 14-year-old children exposed to methylmercury. J Pediatr 144: 177-183.
56. Navarro F, Arroyo A, Martin SF, Bello RI, Cabo R, Burgess JR, Navas P, Villalba JM. 1999. Protective role of ubiquinone in vitamin E and selenium-deficient plasma membranes. Biofactors 9: 163-170.
57. Newland MC, Reed MN, LeBlanc A, Donlin WD. 2006. Brain and blood mercury and selenium after chronic and developmental exposure to methylmercury. Neurotoxicology 27: 710-720.
58. Norazlina M, Ima-Nirwana S, Gapor MT, Khalid BA. 2000. Palm vitamin E is comparable to alpha-tocopherol in maintaining bone mineral density in ovariectomised female rats. Exp Clin Endocrinol Diabetes 108: 305-310.
59. Ornoy A. 2007. Embryonic oxidative stress as a mechanism of teratogenesis with special emphasis on diabetic embryopathy. Reprod Toxicol 24: 31-41.
60. Packer L. 1991. Protective role of vitamin E in biological systems. Am J Clin Nutr 53: 1050S-1055S.
61. Patrick T, Roberts JM. 1999. Current concepts in preeclampsia. MCN Am J Matern Child Nurs 24: 193-200.
62. Pillai A, Gupta S. 2005. Antioxidant enzyme activity and lipid peroxidation in liver of female rats co-exposed to lead and cadmium: effects of vitamin E and Mn2+. Free Radic Res 39: 707-712.
63. Roda-Moreno JA, Pascual-Morenilla MT, Roda-Murillo O, Lopez-Soler M, Arrebola-Nacle F. 2000. Action of ethanol on different skull and brain parameters in the chick embryo. J Craniofac Genet Dev Biol 20: 44-48.
64. Rodier PM, Aschner M, Sager PR. 1984. Mitotic arrest in the developing CNS after prenatal exposure to methylmercury. Neurobehav Toxicol Teratol 6: 379-385.
65. Rugh R. 1968. The mouse: its reproduction and development. Minneapolis: Burgess Publishing Company.
66. Scifres CM, Nelson DM. 2009. Intrauterine growth restriction, human placental development and trophoblast cell death. J Physiol 587: 3453-3458.
67. Siciliano SD, Sangster A, Daughney CJ, Loseto L, Germida JJ, Rencz AN, O'Driscoll NJ, Lean DR. 2003. Are methylmercury concentrations in the wetlands of Kejimkujik National Park, Nova Scotia, Canada, dependent on geology? J Environ Qual 32: 2085-2094.
68. Sikorski R, Paszkowski T, Szprengier-Juszkiewicz T. 1986. Mercury in neonatal scalp hair. Sci Total Environ 57: 105-110.
69. Sikorski R, Juszkiewicz T, Paszkowski T, Szprengier-Juszkiewicz T. 1987. Women in dental surgeries: reproductive hazards in occupational exposure to metallic mercury. Int Arch Occup Environ Health 59: 551-557.
70. Stern AH, Gochfeld M, Weisel C, Burger J. 2001. Mercury and methylmercury exposure in the New Jersey pregnant population. Arch Environ Health 56: 4-10.
71. Tollefson L, Cordle F. 1986. Methylmercury in fish: a review of residue levels, fish consumption and regulatory action in the United States. Environ Health Perspect 68: 203-208.
72. Trasande L, Schechter CB, Haynes KA, Landrigan PJ. 2006. Mental retardation and prenatal methylmercury toxicity. Am J Ind Med 49: 153-158.
73. United Nations Environmental Programme. 2002. Global Mercury Assessment Report. Available at:.
74. Vahter M, Akesson A, Lind B, Björs U, Schütz A, Berglund M. 2000. Longitudinal study of methylmercury and inorganic mercury in blood and urine of pregnant and lactating women, as well as in umbilical cord blood. Environ Res 84: 186-194.
75. Vorhees CV. 1985. Behavioral effects of prenatal methylmercury in rats: a parallel trial to the collaborative behavioral teratology study. Neurobehav Toxicol Teratol 7: 717-725.
76. Walker DG, Wirtschafter ZT. 1957. The Genesis of the rat skeleton. A laboratory Atlas. Springfield Illinois USA: Charles C Thomas Publishers.
77. Warren S, Patel S, Kapron CM. 2000. The effect of vitamin E exposure on cadmium toxicity in mouse embryo cells in vitro. Toxicology 142: 119-126.
78. Weiss B. 1995. Perspectives on methylmercury as a global health hazard. Neurotoxicology 16: 577-578.
79. Welsh SO. 1979. The protective effect of vitamin E and N, N′-diphenyl-p-phenylenediamine (DPPD) against methyl mercury toxicity in the rat. J Nutr 109: 1673-1681.
80. Welsh SO, Soares JH, Jr. 1976. The protective effect of vitamin E and selenium against methyl mercury toxicity in the Japanese quail. Nutr Rep Int 13: 43-51.
81. Wright HV, Asling CW, Dougherty HL, Nelson MM, Evans HM. 1958. Prenatal development of the skeleton in Long-Evans rats. Anat Rec 130: 673-689.
82. Xu H, Watkins BA, Seifert MF. 1995. Vitamin E stimulates trabecular bone formation and alters epiphyseal cartilage morphometry. Calcif Tissue Int 57: 293-300.
83. Yamashita T, Ando Y, Nakamura M, Obayashi K, Terazaki H, Haraoka K, Guo SX, Ueda M, Uchino M. 2004. Inhibitory effect of α-tocopherol on methylmercury-induced oxidative stress. Environ Health Prev Med 9: 111-117.
84. Yee JK, Ima-Nirwana S. 1998. Palm vitamin E protects against ferric nitrilotriacetate-induced impairment of bone calcification. Asia Pacific J Pharmacol 13: 1-7.
85. Yee S, Choi BH. 1994. Methylmercury poisoning induces oxidative stress in the mouse brain. Exp Mol Pathol 60: 188-196.
86. Yee S, Choi BH. 1996. Oxidative stress in neurotoxic effects of methylmercury poisoning. Neurotoxicology 17: 17-26.
87. Zahir F, Rizwi SJ, Haq SK, Khan RH. 2005. Low dose mercury toxicity and human health. Environ Toxicol Pharmacol 20: 351-360.
88. Zahir F, Rizvi SJ, Haq SK, Khan RH. 2006. Effect of methyl mercury induced free radical stress on nucleic acids and protein: implications on cognitive and motor functions. Indian J Clin Biochem 21: 149-152.