Zinc Sulfate and α-tocopherol Supplementation Enhance Reproductive Performance in Male Albino Rats (Rattus norvegicus) With Lead Acetate Toxicity
Keywords:
Antioxidant prevention, Lead acetate toxicity, Oxidative stress, Reproductive health, Vitamin E (α-tocopherol) and Zinc sulfate
Abstract
Metal toxicity from lead affects reproductive organ function by activating reactive oxygen species processes. This study aims to see how α-tocopherol and zinc sulfate (ZnSO4) affect gonads, liver, follicle-stimulating hormone, luteinizing hormone, spermatogenesis (the amount of spermatogonia, spermatocytes, and spermatids), and Leydig cells in male albino rats (Rattus norvegicus) exposed to lead acetate Pb(CH3COO)2. The samples used were 25 male Wistar rats aged 4 months, separated into five groups. For 30 days, all treatment groups were exposed to Pb(CH3COO)2 at a level of 50-mg/kg body weight (BW). The T1 group was given a dosage of 100-mg/kg BW of α-tocopherol. The ZnSO4 was given to the T2 group at a dose of 0.54-mg/kg BW. Meanwhile, the T3 group was given a mixture of ZnSO4 at 0.54-mg/kg BW and α-tocopherol at 100-mg/kg BW orally. ELISA test was carried out to determine the level of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in a blood plasma sample of 100 μl / 1 mg. Histopathological observations made on the liver included counting damaged cells and seminiferous tubules that included counting the amount of spermatogonia, spermatocytes, spermatids, Sertoli cells, and Leydig cells. Using SPSS 20 software, the collected data were analyzed using analysis of variance, followed by Duncan’s test with a 95% simultaneous confidence level. The highest average levels of FSH and LH in the T3 group were 3.6162 mIU/mL and 14.9658 mIU/mL. The finding showed that Pb(CH3COO)2 caused disruptions in the spermatogenesis and Leydig cell processes. Exogenous antioxidants in combination with ZnSO4 and α-tocopherol had significant effect on enhancing reproductive performance in animals exposed to Pb(CH3COO)2.
References
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Hasanein, P., Fazeli, F., Parviz, M., & Roghani, M. (2018). Ferulic acid prevents lead‐induced testicular oxidative stress and suppressed spermatogenesis in rats. Andrologia, 50(1), e12798.
Huang, H., An, Y., Jiao, W., Wang, J., Li, S., & Teng, X. (2018). CHOP/caspase-3 signal pathway involves in mitigative effect of selenium on lead-induced apoptosis via endoplasmic reticulum pathway in chicken testes. Environmental Science and Pollution Research, 25, 18838-18845.
Ibanescu, I., Siuda, M., & Bollwein, H. (2020). Motile sperm subpopulations in bull semen using different clustering approaches–Associations with flow cytometric sperm characteristics and fertility. Animal Reproduction Science, 215, 106329.
Jegede, A. I., Offor, U., Azu, O. O., & Akinloye, O. (2015). Red Palm Oil attenuates lead acetate induced testicular damage in adult male Sprague-Dawley rats. Evidence-Based Complementary and Alternative Medicine, 2015.
Jungwirth, A., Diemer, T., Dohle, G. R., Giwercman, A., Kopa, Z., Tournaye, H., & Krausz, C. (2013). EAU guidelines on male infertility. Eur Urol, 7, 226-241.
Jurowski, K., Szewczyk, B., Nowak, G., & Piekoszewski, W. (2014). Biological consequences of zinc deficiency in the pathomechanisms of selected diseases. JBIC Journal of Biological
Inorganic Chemistry, 19, 1069-1079.
Kazmi, A., Kazmi, A., Shams, S., Sajid, A., & Khan, K. (2019). Therapeutic role of bone marrow-derived stem cells and zinc sulfate for reduction of liver fibrosis. Progress in Stem Cell,6(2), 269-278.
Kumar, S. (2018). Occupational and environmental exposure to lead and reproductive health impairment: an overview. Indian journal of occupational and environmental medicine, 22(3), 128.
Lee, S., Min, J. Y., & Min, K. B. (2020). Female infertility associated with blood lead and cadmium levels. International journal of environmental research and public health, 17(5), 1794.
Leidens, D., Bianchini, A., Varela Junior, A. S., Barcarolli, I. F., Rosa, C. E., Bonnel, J., ... & Corcini, C. D. (2018). Effects of experimental lead exposure on testis of the Chestnut Capped Blackbird Chrysomus ruficapillus. Bulletin of environmental contamination and toxicology, 100, 324-330.
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Li, C., Zhao, K., Zhang, H., Liu, L., Xiong, F., Wang, K., & Chen, B. (2018). Lead exposure reduces sperm quality and DNA integrity in mice. Environmental Toxicology, 33(5), 594-602.
Madhavi, D., Devi, K. R., Rao, K. K., & Reddy, P. P. (2007). Modulating effect of Phyllanthus fruit extract against lead genotoxicity in germ cells of mice. Journal of Environmental Biology, 28(1), 115.
Maret, W. (2019). The redox biology of redox-inert zinc ions. Free Radical Biology and Medicine, 134, 311-326.
Marreiro, D. D. N., Cruz, K. J. C., Morais, J. B. S., Beserra, J. B., Severo, J. S., & De Oliveira, A. R. S. (2017). Zinc and oxidative stress: current mechanisms. Antioxidants, 6(2), 24.
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Mozaffari, Z., Parivar, K., Roodbari, N. H., & Irani, S. (2020). The impact of Zinc oxide nanoparticle on LH, FSH, and testosterone hormones in mature male NMRI rats. J Pharm Res Int, 32:30-37.
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Ogbuewu, I. P., Aladi, N. O., Etuk, I. F., Opara, M. N., Uchegbu, M. C., Okoli, I. C., & Iloeje, M. U. (2010). Relevance of oxygen free radicals and antioxidants in sperm. Res. J. Vet. Sci, 3, 138-164.
Prasad, A. S., & Bao, B. (2019). Molecular mechanisms of zinc as a pro-antioxidant mediator: clinical therapeutic implications. Antioxidants, 8(6), 164.
Prastiya, R. A., Munir, M. M., & Nugroho, A. P. (2021). The Protective Impacts of α-tocopherol Supplementation on the Semen Quality of Sapera Goat Preserved at 4⁰C. Tropical Animal Science Journal, 44(3), 261-266.
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Rajaraman, G., Wang, G. Q., Yan, J., Jiang, P., Gong, Y., & Burczynski, F. J. (2007). Role of cytosolic liver fatty acid binding protein in hepatocellular oxidative stress: effect of dexamethasone and clofibrate treatment. Molecular and cellular biochemistry, 295, 27-34.
Riana, E. N. & Yusuf, T. A. (2021). Heavy metal and vitamin E content in the testes of Wistar rats after exposure to water. Bioedusains, 4, 74-83.
Roshanravan, N., Alizadeh, M., Hedayati, M., Asghari-Jafarabadi, M., Alamdari, N. M., Anari, F., & Tarighat-Esfanjani, A. (2015). Effect of zinc supplementation on insulin resistance, energy and macronutrients intakes in pregnant women with impaired glucose tolerance. Iranian journal of public health, 44(2), 211.
Sakamoto, T., & Imai, H. (2017). Hydrogen peroxide produced by superoxide dismutase SOD-2 activates sperm in Caenorhabditis elegans. Journal of Biological Chemistry, 292(36), 14804-14813.
Silalahi, I. A., Turalaki, G. L., & Rumbajan, J. M. (2016). Difference in the effect of single administration of vitamin E with the combination of vitamin E and zinc against the quality of spermatozoa Wistar rat (Rattus norvegicus) given exposure to cigarette smoke. eBiomedik, 4.
Soler, C., Contell, J., Bori, L., Sancho, M., García-Molina, A., Valverde, A., & Segarvall, J. (2017). Sperm kinematic, head morphometric and kinetic-morphometric subpopulations in the blue fox (Alopex lagopus). Asian journal of andrology, 19(2), 154.
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Treuting, P. M., Dintzis, S., & Montine, K. S. (Eds.). (2017). Comparative anatomy and histology: a mouse, rat, and human atlas. Academic Press.
Valverde, A., Madrigal, M., Caldeira, C., Bompart, D., de Murga, J. N., Arnau, S., & Soler, C. (2019). Effect of frame rate capture frequency on sperm kinematic parameters and subpopulation structure definition in boars, analysed with a CASA‐Mot system. Reproduction in Domestic Animals, 54(2), 167-175.
Víquez, L., Barquero, V., Soler, C., Roldan, E. R., & Valverde, A. (2020). Kinematic sub-populations in bull spermatozoa: A comparison of classical and bayesian approaches. Biology, 9(6), 138.
Wang, L., Wang, L., Shi, X., & Xu, S. (2020). Chlorpyrifos induces the apoptosis and necroptosis of L8824 cells through the ROS/PTEN/PI3K/AKT axis. Journal of hazardous materials, 398, 122905.
Wiyasihati, S. I., & Wigati, K. W. (2016). Potensi Bayam Merah (Amaranthus tricolor L) sebagai Antioksidan pada Toksisitas Timbal yang Diinduksi pada Mencit. Majalah Kedokteran Bandung, 48(2), 63-67.
Zhu, C., Lv, H., Chen, Z., Wang, L., Wu, X., Chen, Z., ... & Jiang, Z. (2017). Dietary zinc oxide modulates antioxidant capacity, small intestine development, and jejunal gene expression in weaned piglets. Biological trace element research, 175, 331-338.
Al-Attar, A. M. (2011). Antioxidant effect of vitamin E treatment on some heavy metals-induced renal and testicular injuries in male mice. Saudi journal of biological sciences, 18(1), 63-72.
Alasia, D. D., Emem-Chioma, P. C., & Ojeka, S. O. (2020). An evaluation of the mitigating effects of α-tocopherol (vitamin E) and ascorbic acid (vitamin C) on the renal function and histology of adult male albino Wistar rats with sub-acute lead acetate exposure. Occupational Diseases and Environmental Medicine, 8(2), 35-49.
Asadi, N., Bahmani, M., Kheradmand, A., & Rafieian-Kopaei, M. (2017). The impact of oxidative stress on testicular function and the role of antioxidants in improving it: a review. Journal of clinical and diagnostic research: JCDR, 11(5), IE01.
Awadalla, N. J., El Helaly, M., Gouida, M., Mandour, R., & Mansour, M. (2011). Sperm chromatin structure, semen quality and lead in blood and seminal fluid of infertile men. Int J Occup Environ Med., 2, 27-36.
Ayinde, O. C., Ogunnowo, S., & Ogedegbe, R. A. (2012). Influence of Vitamin C and Vitamin E on testicular zinc content and testicular toxicity in lead exposed albino rats. BMC pharmacology and toxicology, 13(1), 1-8.
Bhardwaj, J. K., Paliwal, A., & Saraf, P. (2021). Effects of heavy metals on reproduction owing to infertility. Journal of Biochemical and Molecular Toxicology, 35(8), e22823.
Caldeira, C., García-Molina, A., Valverde, A., Bompart, D., Hassane, M., Martin, P., & Soler, C. (2018). Comparison of sperm motility subpopulation structure among wild anadromous and farmed male Atlantic salmon (Salmo salar) parr using a CASA system. Reproduction, Fertility and Development, 30(6), 897-906.
Chen, H., Kang, Z., Qiao, N., Liu, G., Huang, K., Wang, X., ... & Li, Y. (2020). Chronic copper exposure induces hypospermatogenesis in mice by increasing apoptosis without affecting testosterone secretion. Biological trace element research, 195, 472-480.
Daoud, N. M., Aly, M. S., Ezzo, O. H., & Ali, N. A. (2021). Zinc oxide nanoparticles improve testicular steroidogenesis machinery dysfunction in benzo [α] pyrene-challenged rats. Scientific reports, 11(1), 1-14.
Diana, A. N., I'tishom, R., & Sudjarwo, S. A. (2017). Nigella sativa extract improves seminiferous tubule epithelial thickness in lead acetate-exposed balb/c mice. Folia Medica Indonesiana, 53(3), 180-184.
Dorostghoal, M., Dezfoolian, A., & Sorooshnia, F. (2011). Effects of maternal lead acetate exposure during lactation on postnatal development of testis in offspring wistar rats. Iran J Basic Med Sci, 14, 122.e31.
Dutta, S., Henkel, R., Sengupta, P., & Agarwal, A. (2020). Physiological role of ROS in sperm function. Male infertility: Contemporary clinical approaches, Andrology, ART and antioxidants, 337-345.
Elsheikh, N. A. H., Omer, N. A., Yi‐Ru, W., Mei‐Qian, K., Ilyas, A., Abdurahim, Y., & Wang, G. L. (2020). Protective effect of betaine against lead‐induced testicular toxicity in male mice. Andrologia, 52(7), e13600.
Famurewa, A. C., & Ugwuja, E. I. (2017). Association of blood and seminal plasma cadmium and lead levels with semen quality in non-occupationally exposed infertile men in Abakaliki, South East Nigeria. Journal of family & reproductive health, 11(2), 97.
Fang, Y., Xiang, Y., Lu, X., Dong, X., Zhang, J., & Zhong, S. (2020). Epigenetic dysregulation of Mdr1b in the blood-testis barrier contributes to dyszoospermia in mice exposed to cadmium. Ecotoxicology and Environmental Safety, 190, 110142.
Flora, G., Gupta, D., & Tiwari, A. (2012). Toxicity of lead: a review with recent updates. Interdisciplinary toxicology, 5(2), 47-58.
Fu, Z., & Xi, S. (2020). The effects of heavy metals on human metabolism. Toxicology mechanisms and methods, 30(3), 167-176.
Gandhi, J., Hernandez, R. J., Chen, A., Smith, N. L., Sheynkin, Y. R., Joshi, G., & Khan, S. A. (2017). Impaired hypothalamic-pituitary-testicular axis activity, spermatogenesis, and sperm function promote infertility in males with lead poisoning. Zygote, 25(2), 103-110.
Güner, Ö., Güner, A., Yavaşoğlu, A., Karabay Yavaşoğlu, N. Ü., & Kavlak, O. (2020). Ameliorative effect of edible Halopteris scoparia against cadmium‐induced reproductive toxicity in male mice: A biochemical and histopathologic study. Andrologia, 52(6), e13591.
Hasanein, P., Fazeli, F., Parviz, M., & Roghani, M. (2018). Ferulic acid prevents lead‐induced testicular oxidative stress and suppressed spermatogenesis in rats. Andrologia, 50(1), e12798.
Huang, H., An, Y., Jiao, W., Wang, J., Li, S., & Teng, X. (2018). CHOP/caspase-3 signal pathway involves in mitigative effect of selenium on lead-induced apoptosis via endoplasmic reticulum pathway in chicken testes. Environmental Science and Pollution Research, 25, 18838-18845.
Ibanescu, I., Siuda, M., & Bollwein, H. (2020). Motile sperm subpopulations in bull semen using different clustering approaches–Associations with flow cytometric sperm characteristics and fertility. Animal Reproduction Science, 215, 106329.
Jegede, A. I., Offor, U., Azu, O. O., & Akinloye, O. (2015). Red Palm Oil attenuates lead acetate induced testicular damage in adult male Sprague-Dawley rats. Evidence-Based Complementary and Alternative Medicine, 2015.
Jungwirth, A., Diemer, T., Dohle, G. R., Giwercman, A., Kopa, Z., Tournaye, H., & Krausz, C. (2013). EAU guidelines on male infertility. Eur Urol, 7, 226-241.
Jurowski, K., Szewczyk, B., Nowak, G., & Piekoszewski, W. (2014). Biological consequences of zinc deficiency in the pathomechanisms of selected diseases. JBIC Journal of Biological
Inorganic Chemistry, 19, 1069-1079.
Kazmi, A., Kazmi, A., Shams, S., Sajid, A., & Khan, K. (2019). Therapeutic role of bone marrow-derived stem cells and zinc sulfate for reduction of liver fibrosis. Progress in Stem Cell,6(2), 269-278.
Kumar, S. (2018). Occupational and environmental exposure to lead and reproductive health impairment: an overview. Indian journal of occupational and environmental medicine, 22(3), 128.
Lee, S., Min, J. Y., & Min, K. B. (2020). Female infertility associated with blood lead and cadmium levels. International journal of environmental research and public health, 17(5), 1794.
Leidens, D., Bianchini, A., Varela Junior, A. S., Barcarolli, I. F., Rosa, C. E., Bonnel, J., ... & Corcini, C. D. (2018). Effects of experimental lead exposure on testis of the Chestnut Capped Blackbird Chrysomus ruficapillus. Bulletin of environmental contamination and toxicology, 100, 324-330.
Levin, R., Vieira, C. L. Z., Rosenbaum, M. H., Bischoff, K., Mordarski, D. C., & Brown, M. J. (2021). The urban lead (Pb) burden in humans, animals and the natural environment. Environmental research, 193, 110377.
Li, C., Zhao, K., Zhang, H., Liu, L., Xiong, F., Wang, K., & Chen, B. (2018). Lead exposure reduces sperm quality and DNA integrity in mice. Environmental Toxicology, 33(5), 594-602.
Madhavi, D., Devi, K. R., Rao, K. K., & Reddy, P. P. (2007). Modulating effect of Phyllanthus fruit extract against lead genotoxicity in germ cells of mice. Journal of Environmental Biology, 28(1), 115.
Maret, W. (2019). The redox biology of redox-inert zinc ions. Free Radical Biology and Medicine, 134, 311-326.
Marreiro, D. D. N., Cruz, K. J. C., Morais, J. B. S., Beserra, J. B., Severo, J. S., & De Oliveira, A. R. S. (2017). Zinc and oxidative stress: current mechanisms. Antioxidants, 6(2), 24.
Mirania, A. N. (2019). Pengaruh Pemberian Fraksi Daun Jambu Biji Merah (Psidium guajava L.) terhadap Tebal Epitel Epididimis Tikus Putih Jantan (Rattus norvegicus). Jurnal Kesehatan, 10(2), 215-223.
Mozaffari, Z., Parivar, K., Roodbari, N. H., & Irani, S. (2020). The impact of Zinc oxide nanoparticle on LH, FSH, and testosterone hormones in mature male NMRI rats. J Pharm Res Int, 32:30-37.
Murarka, S., Mishra, V., Joshi, P., & Kumar, P. (2015). Role of zinc in reproductive biology-an overview. Austin J Reprod Med Infertil, 2(2), 01-08.
Ogbuewu, I. P., Aladi, N. O., Etuk, I. F., Opara, M. N., Uchegbu, M. C., Okoli, I. C., & Iloeje, M. U. (2010). Relevance of oxygen free radicals and antioxidants in sperm. Res. J. Vet. Sci, 3, 138-164.
Prasad, A. S., & Bao, B. (2019). Molecular mechanisms of zinc as a pro-antioxidant mediator: clinical therapeutic implications. Antioxidants, 8(6), 164.
Prastiya, R. A., Munir, M. M., & Nugroho, A. P. (2021). The Protective Impacts of α-tocopherol Supplementation on the Semen Quality of Sapera Goat Preserved at 4⁰C. Tropical Animal Science Journal, 44(3), 261-266.
Prastiya, R. A., Prastika, Z., & Andriyani, A. (2021, May). Quality and morphometric characters of spermatozoa in two native bull (Pesisir and Rambon) in Indonesia. In AIP Conference Proceedings (Vol. 2353, No. 1, p. 030029). AIP Publishing LLC.
Rahman, M. T., & Karim, M. M. (2018). Metallothionein: a potential link in the regulation of zinc in nutritional immunity. Biological trace element research, 182, 1-13.
Rajaraman, G., Wang, G. Q., Yan, J., Jiang, P., Gong, Y., & Burczynski, F. J. (2007). Role of cytosolic liver fatty acid binding protein in hepatocellular oxidative stress: effect of dexamethasone and clofibrate treatment. Molecular and cellular biochemistry, 295, 27-34.
Riana, E. N. & Yusuf, T. A. (2021). Heavy metal and vitamin E content in the testes of Wistar rats after exposure to water. Bioedusains, 4, 74-83.
Roshanravan, N., Alizadeh, M., Hedayati, M., Asghari-Jafarabadi, M., Alamdari, N. M., Anari, F., & Tarighat-Esfanjani, A. (2015). Effect of zinc supplementation on insulin resistance, energy and macronutrients intakes in pregnant women with impaired glucose tolerance. Iranian journal of public health, 44(2), 211.
Sakamoto, T., & Imai, H. (2017). Hydrogen peroxide produced by superoxide dismutase SOD-2 activates sperm in Caenorhabditis elegans. Journal of Biological Chemistry, 292(36), 14804-14813.
Silalahi, I. A., Turalaki, G. L., & Rumbajan, J. M. (2016). Difference in the effect of single administration of vitamin E with the combination of vitamin E and zinc against the quality of spermatozoa Wistar rat (Rattus norvegicus) given exposure to cigarette smoke. eBiomedik, 4.
Soler, C., Contell, J., Bori, L., Sancho, M., García-Molina, A., Valverde, A., & Segarvall, J. (2017). Sperm kinematic, head morphometric and kinetic-morphometric subpopulations in the blue fox (Alopex lagopus). Asian journal of andrology, 19(2), 154.
Suvarna, K. S., Layton, C., & Bancroft, J. D. (Eds.). (2018). Bancroft's theory and practice of histological techniques E-Book. Elsevier health sciences.
Treuting, P. M., Dintzis, S., & Montine, K. S. (Eds.). (2017). Comparative anatomy and histology: a mouse, rat, and human atlas. Academic Press.
Valverde, A., Madrigal, M., Caldeira, C., Bompart, D., de Murga, J. N., Arnau, S., & Soler, C. (2019). Effect of frame rate capture frequency on sperm kinematic parameters and subpopulation structure definition in boars, analysed with a CASA‐Mot system. Reproduction in Domestic Animals, 54(2), 167-175.
Víquez, L., Barquero, V., Soler, C., Roldan, E. R., & Valverde, A. (2020). Kinematic sub-populations in bull spermatozoa: A comparison of classical and bayesian approaches. Biology, 9(6), 138.
Wang, L., Wang, L., Shi, X., & Xu, S. (2020). Chlorpyrifos induces the apoptosis and necroptosis of L8824 cells through the ROS/PTEN/PI3K/AKT axis. Journal of hazardous materials, 398, 122905.
Wiyasihati, S. I., & Wigati, K. W. (2016). Potensi Bayam Merah (Amaranthus tricolor L) sebagai Antioksidan pada Toksisitas Timbal yang Diinduksi pada Mencit. Majalah Kedokteran Bandung, 48(2), 63-67.
Zhu, C., Lv, H., Chen, Z., Wang, L., Wu, X., Chen, Z., ... & Jiang, Z. (2017). Dietary zinc oxide modulates antioxidant capacity, small intestine development, and jejunal gene expression in weaned piglets. Biological trace element research, 175, 331-338.
Published
2024-09-25
How to Cite
Prastiya, R. A., Sardjito, T., Agustono, B., Fikri, F., Saputro, A. L., Wurlina, W., Dewi, B. L., Pratiwi, S. M., Nugroho, A. P., & Moses, I. B. (2024). Zinc Sulfate and α-tocopherol Supplementation Enhance Reproductive Performance in Male Albino Rats (Rattus norvegicus) With Lead Acetate Toxicity. Indonesian Journal of Pharmacy, 35(3), 467–480. https://doi.org/10.22146/ijp.7445
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Research Article
