Prenatal and perinatal exposure of acrylamide disrupts the development of spinal cord in rats

Abstract

Acrylamideis neurotoxic to the experimental animals and humans. Also, it has mutagenic and carcinogenic effects. Acrylamide was orally administered to non-anesthetized pregnant females by gastric intubation (10 mg/kg/day). The animals were divided into three groups as follows: 1) Group A, newborn from control animals; 2) Group B, newborns from mothers treated with acrylamide from day 7 (D7) of gestation till birth (prenatal intoxicated group); 3) Group C, newborns from mothers treated with acrylamide from D7 of gestation till D28 after birth (perinatally intoxicated group). In the present study acrylamide-induced histopathological and histochemical changes in brachial and lumber regions of spinal cord, including some pyknotic neurons and marked decrease of colour intensity of DNA contents as well as obvious retardation of sensorimotor reflexes of rat newborns. Thus acrylamide and its toxic metabolites resulted in teratogenicity in the rat newborns if their mother exposed to them chronically during gestation and lactation periods. As the spinal motor neurons are the final output neurons of motor systems, so a detailed developmental study is important for a greater understanding motor reflexes development. Moreover, the data on the acrylamide-induced effects on the embryonic and postnatal development is relatively rare. So, the present study was carried out to examine its effects on the development of spinal cord.

Share and Cite:

El-Bakry, A. , Abdul-Hamid, M. and Allam, A. (2013) Prenatal and perinatal exposure of acrylamide disrupts the development of spinal cord in rats. World Journal of Neuroscience, 3, 17-31. doi: 10.4236/wjns.2013.31003.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Friedman, M. (2003) Chemistry, biochemistry, and safety of acrylamide. A review. Journal of Agricultural and Food Chemistry, 51, 4504-4526. doi:10.1021/jf030204+
[2] Dixit, R., Seth, P.K. and Mukjtar, H. (1982) Metabolism of acrylamide into urinary mercapturic acid and cysteine conjugates in rats. Drug Metabolism and Disposition, 10, 196-197.
[3] Miller, M.J., Carter, D.E. and Sipes, I.G. (1982) Pharmacokinetics of acrylamide in Fisher-334 rats. Toxicology and Applied Pharmacology, 63, 36-44. doi:10.1016/0041-008X(82)90024-2
[4] Calleman, C.J., Bergmark, E. and Costa, L. (1990) Acrylamide is metabolized to glycidamide in the rat, evidence from hemoglobin adducts formation. Chemical Research in Toxicology, 3, 406-412. doi:10.1021/tx00017a004
[5] Sumner, S.C.J., MacNeela, J.P. and Fennell, T.R. (1992) Characterization and quantitation of urinary metabolites of [1,2,3-13C]acrylamide in rats and mice using carbon-13 nuclear magnetic resonance spectroscopy. Chemical Research in Toxicology, 5, 81-89. doi:10.1021/tx00025a014
[6] Das, M., Mukhtar, H. and Seth, P. (1982) Effect of acrylamide on brain and hepatic mixed function oxidases. Toxicology and Applied Pharmacology, 66, 420-426. doi:10.1016/0041-008X(82)90308-8
[7] Sumner, S.C.J., Selvaraj, L. and Nauhaus, S.K. (1997) Urinary metabolites from F344 rats and B6C3F1 mice coadministered acrylamide and acrylonitrile for 1 or 5 days. Chemical Research in Toxicology, 10, 1152-1160. doi:10.1021/tx9602123
[8] Spencer, P.S. and Schaumburg, H.H. (1979) Clinical and experimental studies of distal axonopathy, a frequent form of brain and nerve damage produced by environmental chemical hazards. Annals of the New York Academy of Sciences, 329, 14-29. doi:10.1111/j.1749-6632.1979.tb15331.x
[9] LoPachin, R.M. (2004) The changing view of acrylamide neurotoxicity. Neurotoxicology, 25, 617-630. doi:10.1016/j.neuro.2004.01.004
[10] Allam, A., El-Ghareeb, A., Abdul-Hamid, M., Baikry, A. and Sabri, M. (2011) Prenatal and perinatal acrylamide disrupts the development of cerebellum in rat, Biochemical and morphological studies. Toxicology and Industrial Health, 27, 291-306. doi:10.1177/0748233710386412
[11] Takahashi, S., Tanaka, H. and Oki, J. (1999) Development of spinal motorneurons in rats after aneonatal hypoxic insult. Pediatric Neurology, 21, 715-720. doi:10.1016/S0887-8994(99)00080-6
[12] Delcomyn, F. (1980) Neural basis of rhythmic behavior in animals. Science, 210, 492-498. doi:10.1126/science.7423199
[13] Grillner, S. (1985) Neurobiological bases of rhythmic motor acts in vertebrates. Science, 228, 143-149. doi:10.1126/science.3975635
[14] Sakurai, M., Tayashi, H., Abe, K., Itoyama, Y. and Tabayashi, K. (2000) Cyclin D1 and Cdk4 protein induction in motor neurons after transient spinal cord ischemia in rabbits. Stroke, 31, 200-207. doi:10.1161/01.STR.31.1.200
[15] Sinkjaer, T., Toft, E. and Hansen, H.J. (1995) H-reflex modulation during gait in multiple sclerosis patients with spasticity. Acta Neurologica Scandinavica, 91, 239-264. doi:10.1111/j.1600-0404.1995.tb06997.x
[16] Dubowitz, V. (1995) Musle Disorders of Childhood. W.B. Saunders, Co. Ltd., London.
[17] Williams, B.Y., Vinnakota, S., Sawyer, C.A., Woldrep, J.C., Hamilton, S.L. and Sarkar, H.K. (1999) Differential subcellular localization of the survival motor neuron protein in spinal cord and skeletal muscle. Biochemical and Biophysical Research Communications, 254, 10-14.
[18] Dalia, M.S. (2002) Comparative studies on the ontogeny of sensorimotor reflexes and locomotive activity in small mammals and their applications on infants. Ph.D. Thesis, Mansour University, Mansour.
[19] Zehr, E.P. and Stein, R.B. (1999) What functions do reflexes serve during human locomotion. Progress in Neurobiology, 58, 185-205. doi:10.1016/S0301-0082(98)00081-1
[20] Rossignol, S. (1996) Neural control of stereotypic limb movement. In: Rowell, L.B. and Sheperd, J.T., Eds., Integration of Motor Circulatory, Respiretory and Metabolic Control during Exercise, Oxford University Press, New York, 173-216.
[21] Seale, S.M., Feng, Q., Agarwal, A.K and El-Alfy, A.T. (2012) Neurobehavioral and transcriptional effects of acrylamide in juvenile rats. Pharmacology Biochemistry and Behavior, 1, 84.
[22] Nicholls, J.G., Martin, A.R. and Wallace, B.G. (1992) From neuron to brain. 3rd Editon, Sinauer Associates Inc., Sunderland.
[23] Cassidy, G., Boudrias, D., Pflieger, J.F. and Cabana, T. (1994) The development of sensorimotor reflexes in the Brazilian opossum (Monodelphis domestica). Brain, Behavior and Evolution, 43, 244-253. doi:10.1159/000113638
[24] Smart, J.L. and Dobbing, J. (1971) Vulnerability of developing brain. II. Effects of early nutritional deprivation on reflex ontogeny and development of behaviour in the rat. Brain Research, 28, 85-95. doi:10.1016/0006-8993(71)90526-9
[25] Garey, J., Sherry, A.F. and Merle, G.P. (2005) Developmental and behavioral effects of acrylamide in Fischer 344 rats. Neurotoxicology and Teratology, 27, 3-563. doi:10.1016/j.ntt.2005.03.007
[26] Zhang, L., Gavin, T., Barber, D.S. and LoPachin, R.M. (2011) Role of the Nrf2-ARE pathway in acrylamide neurotoxicity. Toxicology Letters, 5, 7-11. doi:10.1016/j.toxlet.2011.08.017
[27] Jennekens, F.G., Veldman, H., Schotman, P. and Gispen, W.H. (1979) Sequence of motor nerve terminal involvement in acrylamide neuropathy. Acta Neuropathologica, 46, 57-63. doi:10.1007/BF00684805
[28] Agrawal, A.K. and Squibb, R.E. (1981) Effects of acrylamide given during gestation on dopamine receptor binding in rat pups. Toxicology Letters, 7, 233-238. doi:10.1016/0378-4274(81)90074-6cvc
[29] Kinnard, W.J. and Watzman, N. (1966) Techniques used in the evaluation of psychotropic drugs on animal activity. Journal of Pharmaceutical Sciences, 55, 995-1012. doi:10.1002/jps.2600551002
[30] Bouet, V., Wubbels, R.J., De-Jong, H.A.A. and Gramsbergen, A. (2004) Behavioral consequences of hyper-gravity in developing rats. Developmental Brain Research, 153, 69-78. doi:10.1016/j.devbrainres.2004.03.022
[31] Cassidy, G., Pflieger, J.F. and Cabana, T., (1992) The ontogenesis of sensorimotor reflexes in the Mongolian gerbil (Meriones unguicatas). Behavioural Brain Research, 52, 143-151. doi:10.1016/S0166-4328(05)80224-4
[32] Mallory, F.B. (1988) Pathological Techénique. W.B. Saunders, Philadelphia.
[33] Feulgen, R. and Rossenbeck, H. (1924) Mikroskopisch-chemischer Nachweis einer Nucleinsaure vom Typus der Thymonucleinsaure und die-darauf beruhende elektive Farbung von Zellkernen in mikroskopischen Praparat. Zeitschrift für Physikalische Chemie, 135, 203-248. doi:10.1515/bchm2.1924.135.5-6.203
[34] Carleton, H., Drury, R., Willington, E. and Conergon, H. (1967) Cited from Carleton. Histological techniques. Oxford University Press, Toronto.
[35] Rao, M. and Blane, K. (1995) PC-STAT. One way analysis of variance procedure. University of Georgia, Atlanta.
[36] Cabana, T., Cassidy, G., Pflieger, J.F. and Baron, G. (1993) The ontogenic development of sensorimotor reflexes and spontaneous locomotion in the Mongolian gerbil (Meriones unguicutas). Brain Research Bulletin, 30, 291-301. doi:10.1016/0361-9230(93)90257-C
[37] Shaheed, I.B., Kawkab, A.A. and Makhlouf, M.M. (2006) Toxicicological and pathological studies on acrylamide neurotoxicity in albino rats. Egyptian Veterinary Medical Society for Pathology and Clinical Pathology, 19, 63-82.
[38] Crofton, K.M., Padilla, S., Tilson, H.A., Anthony, D.C., Raymer, J.H. and MacPhail, R.C. (1996) The impact of dose rate on the neurotoxicity of acrylamide, the interacttion of administered dose, target tissue concentrations, tissue damage, and functional effects. Toxicology and Applied Pharmacology, 139, 163-176. doi:10.1006/taap.1996.0155
[39] Lehning, E.J., Balaban, C.D., Ross, J.F., Reid, M.A. and LoPachin, R.M. (2002) Acrylamide neuropathy. I. Spatiotemporal characteristics of nerve cell damage in rat cerebellum. Neurotoxicology, 23, 397-416. doi:10.1016/S0161-813X(02)00083-9
[40] Goodlett, C.R., Marcussen, B.L. and West, J.R. (1992) A single day of alcohol exposure during the brain growth spurt induce brain weight restriction and cerebellar Purkinje cell loss. Alcohol, 7, 107-114. doi:10.1016/0741-8329(90)90070-S
[41] Daniel, J.B., Nancy, E.B., Ruth, M.A.N., Susan, J.A. and West, J.R. (1996) Purkinje cell deficits in nonhuman primates following weekly exposure to ethanol during gestation. Teratology, 53, 230-236. doi:10.1002/(SICI)1096-9926(199604)53:4<230::AID-TERA5>3.0.CO;2-6
[42] LoPachin, R.M., Ross, J.F., Reid, M.L., Dasgupta, S., Mansukhani, S. and Lehning, E.J. (2002) Neurological evaluation of toxic axonopathies in rats, acrylamide and 2,5-hexanedione. Neurotoxicology, 23, 95-110. doi:10.1016/S0161-813X(02)00003-7
[43] Abdul-Hamid, M., Allam, A. and Hussein, M.B. (2007) Effect of ethanol administration during gestation on the cerebral cortex and spinal cord of albino rat newborns and on the development of their sensorimotor reflexes. Egyptian Journal of Zoology, 48, 137-162.
[44] Fox, M.W. (1964) A phylogenetic analysis of behavioral neuro-ontogeny in precocial and non-precocial mammals. Canadian Journal of Comparative Medicine and Veterinary Science, 28, 197-202.
[45] Guo, C., Li, B. and Xiao, J. (2010) General survey of mechanisms of acrylamide neurotoxicity. Journal of Hygiene Research, 39, 282-285.
[46] Garey, J. and Paule, M.G. (2010) Effects of chronic oral acrylamide exposure on incremental repeated acquisition (learning) task performance in Fischer 344 rats. Neurotoxicology and Teratology, 32, 20-25. doi:10.1016/j.ntt.2009.10.001
[47] Wise, L.D., Gordon, L.R., Soper, K.A., Duchai, D.M. and Morrissey, R.E. (1995) Developmental neurotoxicity evaluation of acrylamide in Sprague-Dawley rats. Neurotoxicology and Teratology, 17, 189-198. doi:10.1016/0892-0362(94)00071-K
[48] Stevens, A. and Lowe, J. (1997) Human Histology. 2nd Edition, Grafos S.A., Barcelona.
[49] Sridevi, B., Reddy, K.V. and Reddy, S.L.N. (1998) Effect of trivalent and hexavalent chromium on antioxidant enzyme activities and lipid peroxidation in a freshwater field crab, Barytelphusa guerini. Bulletin of Environmental Contamination and Toxicology, 61, 384-390. doi:10.1007/s001289900774
[50] Frieda, S.G. and William, P.R. (1999) Effects of lactational administration of acrylamide on rat dams and offspring. Reproductive Toxicology, 13, 511-520. doi:10.1016/S0890-6238(99)00043-X
[51] LoPachin, R.M., Lehning, E.J., Opanashuk, L.A. and Jortner, B.S. (2000) Rate of neurotoxicant exposure determines morphologic manifestations of distal axonopathy. Toxicology and Applied Pharmacology, 167, 75-86. doi:10.1006/taap.2000.8984
[52] Lehning, E.J., Balaban, C.D., Ross, J.F. and LoPachin, R.M. (2003) Acrylamide neuropathy, III. Spatiotemporal charcteristics of nerve cell damage in forebrain. Neurotoxicology, 24, 125-136. doi:10.1016/S0161-813X(02)00155-9
[53] Ko, M.H., Chen, W.P., Linshiau, S.Y. and Hsieh, S.T. (1999) Age-dependent acrylamide neurotoxicity in mice, morphology, physiology and function. Experimental Neurology, 158, 37-46. doi:10.1006/exnr.1999.7102
[54] Laouris, Y., Kalli-Laouris, J. and Schwartze, P. (1990) The influence of altered head, thorax and pelvis mass on the postnatal development of air-righting reaction in albino rats. Behavioural Brain Research, 38, 185-190. doi:10.1016/0166-4328(90)90016-8
[55] Stelzner, D.J. (1971) The normal postnatal development of synaptic end-feet in the lumbosacral spinal cord and responses in the hind limbs of the albino rat. Experimental Neurology, 31, 337-357. doi:10.1016/0014-4886(71)90237-8
[56] Tanaka, H., Takahashi, S. and Oki, J. (1997) Developmental regulation of spinal motorneurons by monoaminergic nerve fibers. Urnal of the Peripheral Nervous System, 2, 323-332.
[57] Rajaoftra, N., Sandillon, F., Geffard, M. and Privat, A. (1989) Pre- and postnatal ontogeny of serotonergic projections to the rat spinal cord. Journal of Neuronscience Research, 22, 305-321.
[58] Lehning, E.J., Balaban, C.D., Ross, J.F. and LoPachin, R.M. (2003) Acrylamide neuropathy, II. Spatiotemporal charcteristics of nerve cell damage in brainstem and spinal cord. Neurotoxicology, 24, 109-123. doi:10.1016/S0161-813X(02)00192-4
[59] Klaunig, J.E. and Kamendulis, L.M. (2005) Mechanism of acrylamide induced rodent carcinogensis. Advances in Experimental Medicine and Biology, 561, 49-62. doi:10.1007/0-387-24980-X_4
[60] Yousef, M.I. and El-Demerdash, F.M. (2006) Acryla- mide-induced oxidative stress and biochemical perturbations in rats. Toxicology, 219, 133-141. doi:10.1016/j.tox.2005.11.008
[61] Sorgel, F., Weissenbacher, R., Kinzig-Schippers, M., Hofmann, A., Illauer, M., Skott, A. and Landersdorfer, C. (2002) Acrylamide, increased concen-trations in homemade food and first evidence of its variable absorption from food, variable metabolism and placental and breast milk transfer in humans. Chemotherapy, 48, 267-274. doi:10.1159/000069715
[62] Tyl, R.W., Marr, M.C., Myers, C.B., Ross, W.P. and Friedman, M.A. (2000) Relationship between acrylamide reproductive and neurotoxicity in male rats. Reproductive Toxicology, 14, 147-57. doi:10.1016/S0890-6238(00)00066-6
[63] Tyl, R.W., Friedman, M.A., Losco, P.E. and Ross, W.P. (2000) Rat two-generation reproduction and dominant lethal study of acrylamide in drinking water. Reproductive Toxicology, 14, 385-401. doi:10.1002/em.2850160302
[64] Sega, G.A., Generoso, E. and Brimer, P. (1990) Acrylamide exposure delayed unscheduled DNA synthesis in germ cells of mal mice that is correlated with the temproal pattern of adduct formation in testis DNA. Environmental and Molecular Mutagenesis, 16, 1161-1165.
[65] Warr, T., Parry, J. and Callander, R. (1990) Methyl vinyl sulphone, a new class of Michael-type genotoxin. Mutation Research, 245, 191-199. doi:10.1016/0165-7992(90)90049-P

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.