Influence of subchronic exposure to manganese carried by female rats during pregnancy on the behavioral and cognitive abilities of their offspring at later stages of postnatal development

Authors

  • Tatiana Kazakova Federal Research Centre for Biological Systems and Agrotechnologies, Russian Academy of Sciences, ul. 9 Yanvarya, 29, Orenburg, 460000, Russian Federation https://orcid.org/0000-0003-3717-4533
  • Olga Marshinskaya Federal Research Centre for Biological Systems and Agrotechnologies, Russian Academy of Sciences, ul. 9 Yanvarya, 29, Orenburg, 460000, Russian Federation https://orcid.org/0000-0002-5611-5128
  • Svetlana Notova Federal Research Centre for Biological Systems and Agrotechnologies, Russian Academy of Sciences, ul. 9 Yanvarya, 29, Orenburg, 460000, Russian Federation https://orcid.org/0009-0006-3644-3585

DOI:

https://doi.org/10.21638/spbu03.2024.102

Abstract

The study evaluated the effects of prenatal exposure to manganese (Mn) on the functional state of offspring at later stages of postnatal development (PND). Female rats were treated with MnSO4·5H2O in the diet at a dose of 1433 mg/kg starting 28 days prior to breeding and through gestation. The pregnancy proceeded normally, no physical abnormalities were observed. There was a lag in physical development of the offspring, which was characterized by a later opening of the eyes, the formation of a coat and the eruption of incisors, the weight gain was attenuated from PND 0-84. Offspring had hyperactive behavior and deterioration in spatial learning and memory. The level of Mn in the blood serum and cerebral cortex was higher than the control values by 11 % and 53 % respectively. The acetylcholinesterase level in the serum was higher by 47 %. These findings highlight the risk of prenatal exposure to subchronic doses of Mn.

Keywords:

heavy metals, manganese, toxicity, prenatal influence, behavior, cognitive abilities, acetylcholinesterase, biomarker

Downloads

Download data is not yet available.
 

References

Amos-Kroohs, R. M., Davenport, L. L., Gutierrez, A., Hufgard, J. R., Vorhees, C. V., and Williams, M. T. 2016. Developmental manganese exposure in combination with developmental stress and iron deficiency: Effects on behavior and monoamines. Neurotoxicology and Teratology 56:55–67. https://doi.org/10.1016/j.ntt.2016.06.004

Andiarena, A., Irizar, A., Molinuevo, A., Urbieta, N., Babarro, I., Subiza-Pérez, M., Santa-Marina, L., Ibarluzea, J., and Lertxundi A. 2020. Prenatal manganese exposure and long-term neuropsychological development at 4 years of age in a population-based birth cohort. International Journal of Environmental Research and Public Health 17(5):1665. https://doi.org/10.3390/ijerph17051665

Andrade, V. M., Mateus, M. L., Batoréu, M. C., Aschner, M., and Marreilha dos Santos, A. P. 2015. Lead, arsenic, and manganese metal mixture exposures: Focus on biomarkers of effect. Biological Trace Element Research 166(1):13–23. https://doi.org/10.1007/s12011-015-0267-x

Ashley-Martin, J., Dodds, L., Arbuckle, T. E., Ettinger, A. S., Shapiro, G. D., Fisher, M., Monnier, P., Morisset, A. S., Fraser, W. D., and Bouchard, M. F. 2018. Maternal and cord blood manganese (Mn) levels and birth weight: The MIREC birth cohort study. International Journal of Hygiene and Environmental Health 221(6):876–882. https://doi.org/10.1016/j.ijheh.2018.05.015

Bakulski, K. M., Seo, Y. A., Hickman, R. C., Brandt, D., Vadari, H. S., Hu, H., and Park, S. K. 2020. Heavy metals exposure and Alzheimer’s disease and related dementias. Journal of Alzheimer’s Disease 76(4):1215–1242. https://doi.org/10.3233/JAD-200282

Bałasz, M., Szkilnik, R., Brus, R., Malinowska-Borowska, J., Kasperczyk, S., Nowak, D., Kostrzewa, R. M., and Nowak, P. 2015. Perinatal manganese exposure and hydroxyl radical formation in rat brain. Neurotoxicity Research 27(1):1–14. https://doi.org/10.1007/s12640-014-9474-z

Beasley, T. E., McDaniel, K. L., Oshiro, W. M., Moser, V. C., MacMillan, D. K., and Herr, D. W. 2022. Impacts of a perinatal exposure to manganese coupled with maternal stress in rats: Maternal somatic measures and the postnatal growth and development of rat offspring. Neurotoxicology and Teratology 90:107061. https://doi.org/10.1016/j.ntt.2021.107061

Betharia, S. and Maher, T. J. 2012. Neurobehavioral effects of lead and manganese individually and in combination in developmentally exposed rats. Neurotoxicology 33(5):1117–11127. https://doi.org/10.1016/j.neuro.2012.06.002

Brenneman, K. A., Cattley, R. C., Ali, S. F., and Dorman, D. C. 1999. Manganese-induced developmentalтneurotoxicity in the CD rat: Is oxidative damage a mechanism of action. Neurotoxicology 20:477–487.

Campanari, M. L., García-Ayllón, M. S., Blazquez-Llorca, L., Luk, W. K., Tsim, K., and Sáez-Valero, J. 2014. Acetylcholinesterase protein level is preserved in the Alzheimer’s brain. Journal of Molecular Neuroscience 53(3):446–453. https://doi.org/10.1007/s12031-013-0183-5

Campanari, M. L., Navarrete, F., Ginsberg, S. D., Manzanares, J., Sáez-Valero, J., and García-Ayllón, M. S. 2016. Increased expression of readthrough acetylcholinesterase variants in the brains of Alzheimer’s disease patients. Journal of Alzheimer’s Disease 53(3):831–841. https://doi.org/10.3233/JAD-160220

Cendrowska-Pinkosz, M., Krauze, M., Juśkiewicz, J., and Ognik, K. 2021. The effect of the use of copper carbonate and copper nanoparticles in the diet of rats on the level of β-amyloid and acetylcholinesterase in selected organs. Journal of Trace Elements in Medicine and Biology 67:126777. https://doi.org/10.1016/j.jtemb.2021.126777

Chandra, S. V., Shukla, G. S., and Saxena, D. K. 1979. Manganese-induced behavioral dysfunction and itsneurochemical mechanism in growing mice. Journal of Neurochemistry 33:1217–1221. https://doi.org/10.1111/j.1471-4159.1979.tb05267.x

Chernogaeva, G. M., Zhuravleva, L. R., Malevanov, Y. A., Peshkov, Y. V., Kotlyakova, M. G., and Krasilnikova, T. A. 2022. Overview of the state and pollution of the environment in the Russian Federation for 2021. Federalnaya sluzhba po gidrometeorologii i monitoringu okruzhayushchej sredy (Rosgidromet) Publ., Moscow. (In Russian)

Cheung, J., Rudolph, M. J., Burshteyn, F., Cassidy, M. S., Gary, E. N., Love, J., Franklin, M. C., and Height, J. J. 2012. Structures of human acetylcholinesterase in complex with pharmacologically important ligands. Journal of Medicinal Chemistry 55(22):10282–10286. https://doi.org/10.1021/jm300871x

Chtourou, Y., Fetoui, H., Garoui, M., Boudawara, T., and Zeghal, N. 2012. Improvement of cerebellum redox states and cholinergic functions contribute to the beneficial effects of silymarin against manganese-induced neurotoxicity. Neurochemical Research 37(3):469–479. https://doi.org/10.1007/s11064-011-0632-x

Dorman, D. C., Struve, M. F., Vitarella, D., Byerly, F. L., Goetz, J., and Miller, R. 2000. Neurotoxicity of manganese chloride in neonatal and adult CD rats following subchronic (21-day) high-dose oral exposure. Journal of Applied Toxicology 20:179–187. https://doi.org/10.1002/(SICI)1099-1263(200005/06)20:3%3C179::AID-JAT631%3E3.0.CO;2-C

Dutta, S. and Bahadur, M. 2019. Effect of pesticide exposure on the cholinesterase activity of the occupationally exposed tea garden workers of northern part of West Bengal, India. Biomarkers 24(4):317–324. https://doi.org/10.1080/1354750X.2018.1556342

Dziak, L. A. and Tsurkalenko, O. S. 2019.The role of cholinergic deficiency in the pathogenesis of neuropsychiatric diseasest. International Neurological Journal 3(105):39–47. https://doi.org/10.22141/2224-0713.3.105.2019.169917

Ellman, G. L., Courtney, K. D., Andres, V. Jr., and Feather-Stone, R. M. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9

Erikson, K. M., Dobson, A. W., Dorman, D. C., and Aschner, M. 2004. Manganese exposure and induced oxidative stress in the rat brain. Science of the Total Environment 334–335:409–416. https://doi.org/10.1016/j.scitotenv.2004.04.044

Fernández-Olmo, I., Mantecón, P., Markiv, B., Ruiz-Azcona, L., and Santibáñez, M. A. 2021. Review on the environmental exposure to airborne manganese, biomonitoring, and neurological/neuropsychological outcomes. Reviews of Environmental Contamination and Toxicology 254:85–130. https://doi.org/10.1007/398_2020_46

Finkelstein, Y., Milatovic, D., and Aschner, M. 2007. Modulation of cholinergic systems by manganese. Neurotoxicology 28(5):1003–1014. https://doi.org/10.1016/j.neuro.2007.08.006

Fishman, E. B., Siek, G. C., MacCallum, R. D., Bird, E. D., Volicer, L., and Marquis, J. K. 1986. Distribution of the molecular forms of acetylcholinesterase in human brain, alterations in dementia of the Alzheimer type. Annals of Neurology 19(3):246–252. https://doi.org/10.1002/ana.410190305

Fu, H., Xia, Y., Chen, Y., Xu, T., Xu, L., Guo, Z., Xu, H., Xie, H. Q., and Zhao, B. 2018. Acetylcholinesterase is a potential biomarker for a broad spectrum of organic environmental pollutants. Environmental Science and Technology 52(15):8065–8074. https://doi.org/10.1021/acs.est.7b04004

Garcia, S. J., Gellein, K., Syversen, T., and Aschner, M. 2006. A manganese-enhanced diet alters brain metals and transporters in the developing rat. Toxicological Sciences 92(2):516–525. https://doi.org/10.1093/toxsci/kfl017

Garcia, S. J., Gellein, K., Syversen, T., and Aschner, M. 2007. Iron deficient and manganese supplemented diets alter metals and transporters in the developing rat brain. Toxicological Sciences 95(1):205–214. https://doi.org/10.1093/toxsci/kfl139

García-Ayllón, M. S., Riba-Llena, I., Serra-Basante, C., Alom, J., Boopathy, R., and Sáez-Valero, J. 2010. Altered levels of acetylcholinesterase in Alzheimer plasma. PLoS One. 5(1):e8701. https://doi.org/10.1371/journal.pone. 0008701

Gonzalez-Casanova, I., Stein, A. D., Barraza-Villarreal, A., Feregrino, R. G., DiGirolamo, A., Hernandez-Cadena, L., Rivera, J. A., Romieu, I., and Ramakrishnan, U. 2018. Prenatal exposure to environmental pollutants and child development trajectories through 7 years. International Journal of Hygiene and Environmental Health 221(4):616–622. https://doi.org/10.1016/j.ijheh.2018.04.004

Gould, T. D., Dao, D. T., and Kovacsics, C. E. 2009. The Open Field Test; pp. 1–20 in T. Gould (ed.), Mood and Anxiety Related Phenotypes in Mice. Neuromethods. Humana Press, Totowa. https://doi.org/10.1007/978-1-60761-303-9_1

Gurol, K. C., Aschner, M., Smith, D. R., and Mukhopadhyay, S. 2022. Role of excretion in manganese homeostasis and neurotoxicity: A historical perspective. American Journal of Physiology. Gastrointestinal and Liver Physiology 322(1):G79–G92. https://doi.org/10.1152/ajpgi.00299.2021

Han, S. H., Park, J. C, Byun, M. S., Yi, D., Lee, J. H., Lee, D. Y., and Mook-Jung, I. 2019. Blood acetylcholinesterase level is a potential biomarker for the early detection of cerebral amyloid deposition in cognitively normal individuals. Neurobiology of Aging 73:21–29. https://doi.org/10.1016/j.neurobiolaging.2018.09.001

Hu, J., Wu, C., Zheng, T., Zhang, B., Xia, W., Peng, Y., Liu, W., Jiang, M., Liu, S., Buka, S. L., Zhou, A., Zhang, Y., Jiang, Y., Hu, C., Chen, X., Zeng, Q., Chen, X., Xu, B., Zhang, X., Truong, A., Shi, K., Qian, Z., Li, Y., and Xu, S. 2018. Critical windows for associations between manganese exposure during pregnancy and size at birth: A longitudinal cohort study in Wuhan, China. Environmental Health Perspectives 126(12):127006. https://doi.org/10.1289/EHP3423

Kalaria, R. N. 1999. The blood-brain barrier and cerebrovascular pathology in Alzheimer’s disease. Annals of the New York Academy of Sciences 893:113–125. https://doi.org/10.1111/j.1749-6632.1999.tb07821.x

Kern, C. H., Stanwood, G. D., and Smith, D. R. 2010. Preweaning manganese exposure causes hyperactivity, disinhibition, and spatial learning and memory deficits associated with altered dopamine receptor and transporter levels. Synapse 64(5):363–378. https://doi.org/10.1002/syn.20736

Kontur, P. J. and Fechter, L. D. 1985. Brain manganese, catecholamine turnover, and the development of startle in rats prenatally exposed to manganese. Teratology 32(1):1–11. https://doi.org/10.1002/tera.1420320102

Koroleva, A. A. 2023. The effect of manganese on the nervous system: New research. Trace Elements in Medicine 24(2):48–52. https://doi.org/10.19112/2413-6174-2023-24-2-48-52 (In Russian)

Korchina, T. Ya., Minyaylo, L. A., and Korchin, V. I. 2018. Excessive concentration of manganese in drinking water and risk to the health of the population of the northern region. Public Health and Life Environment — PH&LE 2:28–33. (In Russian)

Kostina, N. N., Veterkova, Z. A., Reshetnikova, O. V., Ibragimova, N. V., Alaeva, S. E., Kichaeva, T. G., Khusnullina, G. G., and Rachkova, N. I. 2017. Risk factors for the birth and structure of morbidity of children with extremely low and very low body weight. Orenburg Medical Herald 2(18):15–21. (In Russian)

Kraeuter, A. K., Guest, P. C., and Sarnyai, Z. 2019. The open field test for measuring locomotor activity and anxiety-like behavior. Methods in Molecular Biology 1916:99–103. https://doi.org/10.1007/978-1-4939-8994-2_9

Kuvacheva, N. V., Salmina, A. B., Komleva, Yu. K., Malinovskaya, N. A., Morgun, A. V., Pozhilenkova, E. A., Zamai, G. S., Yauzina, N. A., and Petrova, M. M. 2013. Permeability of the hematoencephalic barrier in normalcy, brain development pathology and neurodegeneration. S. S. Korsakov Journal of Neurology and Psychiatry 113(4):80–85. (In Russian)

Lai, J., Leung, T., and Lim, L. 1984. Differences in neurotoxic effects of manganese during development and aging: Some observations on brain regional neurotransmitter and non-neurotransmitter metabolism in a developmental rat model of chronic manganese encephalopathy. NeuroToxicology 5(1):37–47.

Lehner, C., Gehwolf, R., Tempfer, H., Krizbai, I., Hennig, B., Bauer, H. C., and Bauer, H. 2011. Oxidative stress and blood-brain barrier dysfunction under particular consideration of matrix metalloproteinases. Antioxidants and Redox Signaling 15(5):1305–1323. https://doi.org/10.1089/ars.2011.3923

Lin, M., Colon-Perez, L. M., Sambo, D. O., Miller, D. R., and Lebowitz, J. J. 2020. Mechanism of manganese dysregulation of dopamine neuronal activity. Journal of Neuroscience 40(30):5871–5891. https://doi.org/10.1523/JNEUROSCI.2830-19.2020

Lionetto, M. G., Caricato, R., Calisi, A., Giordano, M. E., and Schettino, T. 2013. Acetylcholinesterase as a biomarker in environmental and occupational medicine: New insights and future perspectives. BioMed Research International 2013:321213. https://doi.org/10.1155/2013/321213

Lømo, T., Massoulié, J., and Vigny, M. 1985. Stimulation of denervated rat soleus muscle with fast and slow activity patterns induces different expression of acetylcholinesterase molecular forms. The Journal of Neuroscience 5(5):1180–1187. https://doi.org/10.1523/JNEUROSCI.05-05-01180.1985

Martinez, H. and Bonilla, E. 1981. Water intake and brain choline-acetyltransferase and acetylcholinesterase activities in manganese treated rats. Neurobehavioral Toxicology and Teratology 3(3):277–280.

Molina, R. M., Phattanarudee, S., Kim, J., Thompson, K., Wessling-Resnick, M., Maher, T. J., and Brain, J. D. 2011. Ingestion of Mn and Pb by rats during and after pregnancy alters iron metabolism and behavior in offspring. Neurotoxicology 32(4):413–422. https://doi.org/10.1016/j.neuro.2011.03.010

Nørgaard-Pedersen, B., Hangaard, J., and Bjerrum, O. J. 1983. Quantitative enzyme antigen immunoassay of acetylcholinesterase in amniotic fluid. Clinical Chemistry 29(6):1061–1064.

Notova, S. V., Karimov, I. F., Kazakova, T. V., and Marshinskaya, O. V. 2021. Prenatal effect of manganese on the serum level of acetylcholinesterase in rats. Journal of Medical and Biological Research 9(2):163–170. https://doi.org/10.37482/2687-1419-Z054 (In Russian)

Nyarko-Danquah, I., Pajarillo, E., Digman, A., Soliman, K. F. A., Aschner, M., and Lee, E. 2020. Manganese accumulation in the brain via various transporters and its neurotoxicity mechanisms. Molecules 25(24):5880. https://doi.org/10.3390/molecules25245880

Oberlis, D., Harland, B., and Skalny, A. 2018. The biological role of macro- and microelements in humans and animals. Nauka Publ., Saint Petersburg. (In Russian)

Okada, M. A., Neto, F. F, Noso, C. H., Voigt, C. L., Campos, S. X., and Ribeiro, C. A. O. 2016. Brain effects of manganese exposure in mice pups during prenatal and breastfeeding periods. Neurochemistry International 97(2016):109–116. https://doi.org/10.1016/j.neuint.2016.03.009

Othman, M. Z., Hassan, Z., and Che Has, A. T. 2022. Morris water maze: A versatile and pertinent tool for assessing spatial learning and memory. Experimental Animals 71(3):264–280. https://doi.org/10.1538/expanim.21-0120

Pappas, B. A., Zhang, D., Davidson, C. M., Crowder, T., Park, G. A., and Fortin, T. 1997. Perinatal manganese exposure: Behavioral, neurochemical, and histopathological effects in the rat. Neurotoxicology and Teratology 19(1):17–25. https://doi.org/10.1016/s0892-0362(96)00185-7

Pizzino, G., Irrera, N., Cucinotta, M., Pallio, G., Mannino, F., Arcoraci, V., Squadrito, F., Altavilla, D., and Bitto, A. 2017. Oxidative stress: Harms and benefits for human health. Oxidative Medicine and Cellular Longevity 2017:8416763. https://doi.org/10.1155/2017/8416763

Racette, B. A., Nelson, G., Dlamini, W. W., Prathibha, P., Turnerm, J. R., Ushem, M., Checkoway, H., Sheppard, L., and Nielsen, S. S. 2021. Severity of Parkinsonism associated with environmental manganese exposure. Environmental Health 20(1):27. https://doi.org/10.1186/s12940-021-00712-3

Radysh, I. V., Skalny, A. V., Notova, S. V., Marshinskaya, O. V., and Kazakova, T. V. 2017. Introduction to Elementology. Izdatel'stvo Orenburgskogo gosudarstvennogo universiteta Publ., Orenburg. (In Russian)

Rasmussen Loft, A. G., Nanchahal, K., Cuckle, H. S., Wald, N. J., Hulten, M., Leedham, P., and Nørgaard-Pedersen, B. 1990. Amniotic fluid acetylcholinesterase in the prenatal diagnosis of open neural tube defects and abdominal wall defects: A comparison of gel electrophoresis and a monoclonal antibody immunoassay. Prenatal Diagnosis Journal 10(7):449–459. https://doi.org/10.1002/pd.1970100707

Rodriguez, A., Zhang, H., Klaminder, J., Brodin, T., Andersson, P. L., and Andersson, M. 2018. ToxTrac: A fast and robust software for tracking organisms. Methods in Ecology and Evolution 9(3):460–464. https://doi.org/10.1111/2041-210x.12874

Rotundo, R. L. 2003. Expression and localization of acetylcholinesterase at the neuromuscular junction. Journal of Neurocytology 32(5–8):743–766. https://doi.org/10.1023/B:NEUR.0000020621.58197.d4

Rotundo, R. L., Ruiz, C. A., Marrero, E., Kimbell, L. M., Rossi, S. G., Rosenberry, T., Darr, A., and Tsoulfa, P. 2008. Assembly and regulation of acetylcholinesterase at the vertebrate neuromuscular junctions. Chemico-Biological Interactions 175(1–3):26–29. https://doi.org/10.1016/j.cbi.2008.05.025

Santos, D., Milatovic, D., Andrade, V., Batoreu, M. C., Aschner, M., and Marreilha dos Santos, A. P. 2012. The inhibitory effect of manganese on acetylcholinesterase activity enhances oxidative stress and neuroinflammation in the rat brain. Toxicology 292(2–3):90–98. https://doi.org/10.1016/j.tox.2011.11.017

Schetinger, M. R. C., Peres, T. V., Arantes, L. P., Carvalho, F., Dressler, V., Heidrich, G., Bowman, A. B., and Aschner, M. 2019. Combined exposure to methylmercury and manganese during L1 larval stage causes motor dysfunction, cholinergic and monoaminergic up-regulation and oxidative stress in L4 Caenorhabditis elegans. Toxicology 411:154–162. https://doi.org/10.1016/j.tox.2018.10.006

Scott-Goodwin, A. C., Puerto, M., and Moreno, I. 2016. Toxic effects of prenatal exposure to alcohol, tobacco and other drugs. Reproductive Toxicology 61:120–130. https://doi.org/10.1016/j.reprotox.2016.03.043

Sengupt, P., Banerjee, R., Nath, S., Das, S., and Banerjee, S. 2015. Metals and female reproductive toxicity. Human and Experimental Toxicology 34(7):679–697. https://doi.org/10.1177/0960327114559611

Sharp, P. and Regina, M. L. 1998. The Laboratory Rat. CRC Press, Boca Raton.

Skalny, A. V., Aftanas, L. I., Berezkina, E. S., Bonitenko, E. Yu., Varenik, V. I., Grabeklis, A. R., Demidov, V. A., Kiselev, M. F., Nechiporenko, S. P., Nikolaev, V. A., and Skalnaya, M. G. 2011. Element status of Russian population. Part 2. Element status of population of the Central Federal District. Medkniga ELBI-SPb Publ., Saint Petersburg. (In Russian)

Skalny, A. V., Aftanas, L. I., Berezkina, E. S., Bonitenko, E. Yu., Varenik, V. I., Grabeklis, A. R., Demidov, V. A., Kiselev, M. F., Nechiporenko, S. P., Nikolaev, V. A., and Skalnaya, M. G. 2012. Element status of Russian population. Part 3. Element status of population of the North-West, South and North-Caucasian Federal Districts. Medkniga ELBI-SPb Publ., Saint Petersburg. (In Russian)

Skalny, A. V., Aftanas, L. I., Berezkina, E. S., Bonitenko, E. Yu., Varenik, V. I., Grabeklis, A. R., Demidov, V. A., Kiselev, M. F., Nechiporenko, S. P., Nikolaev, V. A., and Skalnaya, M. G. 2013. Element status of Russian population. Part 4. Elemental status of the population of the Volga and Ural Federal Districts. Medkniga ELBI-SPb Publ., Saint Petersburg. (In Russian)

Skalny, A. V., Aftanas, L. I., Berezkina, E. S., Bonitenko, E. Yu., Varenik, V. I., Grabeklis, A. R., Demidov, V. A., Kiselev, M. F., Nechiporenko, S. P., Nikolaev, V. A., and Skalnaya, M. G. 2014. Element status of Russian population. Part 5. The elemental status of the population of the Siberian and Far Eastern Federal Districts. Medkniga ELBI-SPb Publ., Saint Petersburg. (In Russian)

Souza, T. L., Batschauer, A. R., Brito, P. M., Oliveira Ribeiro, C. A., Martino-Andrade, A. J., and Ortolani-Machado, C. F. 2019. Multigenerational analysis of the functional status of male reproductive system in mice after exposure to realistic doses of manganese. Food and Chemical Toxicology 133:110763. https://doi.org/10.1016/j.fct.2019.110763

Spitznagel, B. D., Buchanan, R. A., Consoli, D. C., Thibert, M. K., Bowman, A. B., Nobis, W. P., and Harrison, F. E. 2023.Acute manganese exposure impairs glutamatergic function in a young mouse model of Alzheimer’s disease. Neurotoxicology 95:1–11. https://doi.org/10.1016/j.neuro.2023.01.002

Starostina, V. K. and Degteva, S. A. 2008. Holinesteraza: Metody analiza i diagnosticheskoe znachenie: Informacionno-metodicheskoe posobie. Vektor-Best Publ., Novosibirsk. (In Russian)

Strizhakov, A. N., Ignatko, I. V., Timohina, E. V., and Kardanova, M. A. 2019. Critical fetal condition: Diagnostic criteria, obstetric tactics, perinatal outcomes. GEOTAR-Media Publ., Moscow. (In Russian)

Su, C., Chen, K., Zou, Y., Shen, Y., Xia, B., Liang, G., Lv, Y., Wang, F., Huang, D., and Yang, X. 2016. Chronic exposure to manganese sulfate leads to adverse dose-dependent effects on the neurobehavioral ability of rats. Environmental Toxicology 31(11):1571–1579. https://doi.org/10.1002/tox.22161

Tran, T. T., Chowanadisai, W., Crinella, F. M., Chicz-Demet, A., and Lonnerdal, B. 2002. Effect of high dietary manganese intake of neonatal rats on tissue mineral accumulation, striatal dopamine levels, and neurodevelopmental status. Neurotoxicology 23(4–5):635–643. https://doi.org/10.1016/s0161-813x(02)00091-8

Vladimirskaya, T. E., Shved, I. A., Kryvorot, S. G., Veyalkina, N. N., and Adamovich, A. V. 2011. Determination of the estrous cycle phases of white rats according to cellular makeup of vaginal smears. Proceedings of the National Academy of Sciences of Belarus Biological Series 4:99–91.

Vorhees, C. V., Graham, D. L., Amos-Kroohs, R. M., Braun, A. A., Grace, C. E., Schaefer, T. L., Skelton, M. R., Erikson, K. M., Aschner, M., and Williams, M. T. 2014. Effects of developmental manganese, stress, and the combination of both on monoamines, growth, and corticosterone. Toxicology Reports 1:1046–1061. https://doi.org/10.1016/j.toxrep.2014.10.004

Yamamoto, M., Sakurai, K., Eguchi, A., Yamazaki, S., Nakayama, S. F., Isobe, T., Takeuchi, A., Sato, T., Hata, A., Mori, C., and Nitta, H. 2019. Association between blood manganese level during pregnancy and birth size: The Japan environment and children’s study (JECS). Environmental Research 172:117–126. https://doi.org/10.1016/j.envres.2019.02.007

Yoon, M., Nong, A., Clewell, H. J., Taylor, M. D., Dorman, D. C., and Andersen, M. E. 2009. Evaluating placental transfer and tissue concentrations of manganese in the pregnant rat and fetuses after inhalation exposures with a PBPK model. Toxicological Sciences 112(1):44–58. https://doi.org/10.1093/toxsci/kfp198

Yousefi Babadi, V., Sadeghi, L., Shirani, K., Malekirad, A. A., and Rezaei, M. 2014. The toxic effect of manganese on the acetylcholinesterase activity in rat brains. International Journal of Toxicology 2014:946372. https://doi.org/10.1155/2014/946372

Zavadenko, N. N. and Davydova, L. A. 2018. Prematurity and low birth weight as risk factors for neurodevelopmental disorders in children. Rossiyskiy vestnik perinatologii i pediatrii 63(4):43–51. https://doi.org/10.21508/1027-4065-2018-63-4-43-51 (In Russian)

Zhang, D., He, X., Huang, S., and Li, Y. 2001. Effect of manganese exposure on brain development in postnatal mice. Journal of Hygiene Research 30(5):260–262.

Zhang, D., He, X., Huang, S., and Li, Y. 2002. Toxicity of manganese exposure on the postnatal development of brain in mice. Journal of Hygiene Research 31(2):73–75.

Zhang, D., He, X., Zhang, W., and Tan, J. 1998. Effect of manganese on the growth and development of rat offspring. Journal of Hygiene Research 27(4):237–240.

Downloads

Published

2024-05-31

How to Cite

Kazakova, T., Marshinskaya, O., & Notova, S. (2024). Influence of subchronic exposure to manganese carried by female rats during pregnancy on the behavioral and cognitive abilities of their offspring at later stages of postnatal development. Biological Communications, 69(1), 12–25. https://doi.org/10.21638/spbu03.2024.102

Issue

Section

Full communications

Categories