Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-06-10T16:03:46.784Z Has data issue: false hasContentIssue false

Green Tea Infusion Ameliorates Histological Damages in Testis and Epididymis of Diabetic Rats

Published online by Cambridge University Press:  29 June 2021

Luiz Otávio Guimarães-Ervilha
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais36570-900, Brazil
Luiz Carlos Maia Ladeira
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais36570-900, Brazil
Renner Philipe Rodrigues Carvalho
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais36570-900, Brazil
Isabela Pereira da Silva Bento
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais36570-900, Brazil
Daniel Silva Sena Bastos
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais36570-900, Brazil
Ana Cláudia Ferreira Souza
Affiliation:
Department of Animal Biology, Universidade Federal Rural do Rio de Janeiro, Rio de Janeiro23897-000, Brazil
Eliziária Cardoso Santos
Affiliation:
Medicine School, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina, Minas Gerais39100-000, Brazil
Leandro Licursi de Oliveira
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais36570-900, Brazil
Izabel Regina dos Santos Costa Maldonado
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais36570-900, Brazil
Mariana Machado-Neves*
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais36570-900, Brazil
*
*Author for correspondence: Mariana Machado-Neves, E-mail: mariana.mneves@ufv.br
Get access

Abstract

Green tea is a popular drink used for therapeutic purposes to mitigate the consequences of diabetes. In this study, we aimed at evaluating the potential of green tea infusion to ameliorate structural and enzymatic damages caused by hyperglycemia in the testis and epididymis of Wistar rats. For that, nondiabetic and streptozotocin-induced diabetic rats (negative control and diabetes control, respectively) received 0.6 mL of water by gavage. Another set of diabetic animals received 100 mg/kg of green tea infusion diluted in 0.6 mL of water/gavage (diabetes + green tea) daily. After 42 days of treatment, the testes and epididymides were removed and processed for histopathological analysis, micromineral determination, and enzymatic assays. The results showed that treatment with green tea infusion preserved the testicular and epididymal histoarchitecture, improving the seminiferous epithelium and the sperm production previously affected by diabetes. Treatment with green tea reduced tissue damages caused by this metabolic condition. Given the severity of hyperglycemia, there was no efficacy of the green tea infusion in maintaining the testosterone levels, antioxidant enzyme activity, and microminerals content. Thus, our findings indicate a protective effect of this infusion on histological parameters, with possible use as a complementary therapy for diabetes.

Type
Biological Applications
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdelrazek, HMA, Helmy, SA, Elsayed, DH, Ebaid, HM & Mohamed, RM (2016). Ameliorating effects of green tea extract on cadmium induced reproductive injury in male Wistar rats with respect to androgen receptors and caspase-3. Reprod Biol 16, 300308.CrossRefGoogle ScholarPubMed
Adewole, SO, Caxton-Martins, EA & Ojewole, AO (2007). Protective effect of quercetin on the morphology of pancreatic beta-cells of streptozotocin-treated diabetic rats. Afr J Trad 4(1), 6474.Google Scholar
Aebi, H (1984). [13] catalase in vitro. Methods Enzymol 105, 121126.CrossRefGoogle Scholar
Alves, MG, Martins, AD, Cavaco, JE, Socorro, S & Oliveira, PF (2013). Diabetes, insulin-mediated glucose metabolism and Sertoli/blood-testis barrier function. Tissue Barriers 1, e23992.CrossRefGoogle ScholarPubMed
Amann, RP (1961). Reproductive capacity of dairy bulls. IV. Spermatogenesis and testicular germ cell degeneration. Am J Anat 110, 4967.CrossRefGoogle Scholar
Amann, RP & Almquist, JO (1962). Reproductive capacity of dairy bulls. VIII. Direct and indirect measurement of testicular sperm production. J Dairy Sci 45, 774781.CrossRefGoogle Scholar
Amann, RP & Schanbacher, BD (1983). Physiology of male reproduction. J Anim Sci 57, 380403.Google ScholarPubMed
Anderson, JE & Thliveris, JA (1986). Testicular histology in streptozotocin-induced diabetes. Anat Rec 214, 378382.CrossRefGoogle ScholarPubMed
Azizi, P & Mehranjani, MS (2019). The effect of green tea extract on the sperm parameters and histological changes of testis in rats exposed to para-nonylphenol. Int J Reprod BioMed 17, 717726.Google Scholar
Bal, R, Türk, G, Tuzcu, M, Yilmaz, O, Ozercan, I, Kuloglu, T, Gür, S, Nedzvetsky, VS, Tykhomyrov, AA, Andrievsky, GV, Baydas, G & Naziroglu, M (2011). Protective effects of nanostructures of hydrated C60 fullerene on reproductive function in streptozotocin-diabetic male rats. Toxicology 282, 6981.CrossRefGoogle ScholarPubMed
Boyer, S, Sharp, PA, Debnam, ES, Baldwin, SA & Srai, SKS (1996). Streptozotocin diabetes and the expression of GLUT1 at the brush border and basolateral membranes of intestinal enterocytes. FEBS Lett 396, 218222.CrossRefGoogle Scholar
Chandra, AK, Choudhury, SR, De, N & Sarkar, M (2011). Effect of green tea (Camellia sinensis L.) extract on morphological and functional changes in adult male gonads of albino rats. Indian J Exp Biol 49(9), 689697.Google ScholarPubMed
Corrêa, LBNS, da Costa, CAS, Ribas, JAS, Boaventura, GT & Chagas, MA (2019). Antioxidant action of alpha lipoic acid on the testis and epididymis of diabetic rats: Morphological, sperm and immunohistochemical evaluation. Int Braz J Urol 45, 815824.CrossRefGoogle ScholarPubMed
Das, B, Biswas, B, Ghosh, A, Pakhira, BP & Ghosh, D (2017). Ameliorative role of ethyl-acetate fraction of methanolic leaf extract of Camellia sinensis (green tea) on streptozotocin-induced diabetes linked testicular hypofunction in albino rat: A dose-dependent biochemical and genomic transection study. J Complement Integr Med 14, 113.CrossRefGoogle ScholarPubMed
Das, SK & Karmakar, SN (2015). Effect of green tea (Camellia sinensis l.) leaf extract on reproductive system of adult male albino rats. Int J Physiol, Pathophysiol Pharmacol 7, 178184.Google ScholarPubMed
Dias, FCR, Gomes, MDLM, de Melo, FCSA, Menezes, TP, Martins, AL, do Carmo Cupertino, M, Otoni, WC & da Matta, SLP (2020). Pfaffia glomerata hydroalcoholic extract stimulates penile tissue in adult Swiss mice. J Ethnopharmacol 261, 113182.CrossRefGoogle ScholarPubMed
Dias, FCR, Martins, ALP, de Melo, FCSA, do Carmo Cupertino, M, Gomes, MDLM, de Oliveira, JM, Damasceno, EM, Silva, J, Otoni, WC & da Matta, SLP (2019). Hydroalcoholic extract of Pfaffia glomerata alters the organization of the seminiferous tubules by modulating the oxidative state and the microstructural reorganization of the mice testes. J Ethnopharmacol 233, 179189.CrossRefGoogle ScholarPubMed
Dias, TR, Alves, MG, Silva, J, Barros, A, Sousa, M, Casal, S, Silva, BM & Oliveira, PF (2017). Implications of epigallocatechin-3-gallate in cultured human Sertoli cells glycolytic and oxidative profile. Toxicol in Vitro 41, 214222.CrossRefGoogle ScholarPubMed
Dieterich, S, Bieligk, U, Beulich, K, Hasenfuss, G & Prestle, J (2000). Gene expression of antioxidative enzymes in the human heart: Increased expression of catalase in the end-stage failing heart. Circulation 101(1), 3339.CrossRefGoogle ScholarPubMed
Ding, GL, Liu, Y, Liu, ME, Pan, JX, Guo, MX, Sheng, JZ & Huang, HF (2015). The effects of diabetes on male fertility and epigenetic regulation during spermatogenesis. Asian J Androl 17, 948953.Google ScholarPubMed
Figueroa, MS, Vieira, JSBC, Leite, DS, Filho, RCOA, Ferreira, F, Gouveia, PS, Udrisar, DP & Wanderley, MI (2009). Green tea polyphenols inhibit testosterone production in rat Leydig cells. Asian J Androl 11(3), 362370.CrossRefGoogle Scholar
França, LR & Russell, LD (1998). The testis of domestic mammals. In Male Reproduction: A Multidisciplinary Overview, Martinez-Garcia, F & Regadera, J (Eds.), pp. 198219. Madrid: Churchill Communications.Google Scholar
Fu, QY, Li, QS, Lin, XM, Qiao, RY, Yang, R, Li, XM, Dong, ZB, Xiang, LP, Zheng, XQ, Lu, JL, Yuan, CB, Ye, JH & Liang, YR (2017). Antidiabetic effects of tea. Molecules 22, 119.CrossRefGoogle Scholar
Gennaro, G, Claudino, M, Cestari, TM, Ceolin, D, Germino, P, Garlet, GP, De Assis, GF & Gronthos, S (2015). Green tea modulates cytokine expression in the periodontium and attenuates alveolar bone resorption in type 1 diabetic rats. PLoS One 10, 116.CrossRefGoogle ScholarPubMed
Habig, WH, Pabst, MJ & Jakoby, WB (1974). Glutathione S-transferases: The first enzymatic step in mercapturic acid formation. J Biol Chem 249, 71307139.CrossRefGoogle ScholarPubMed
Hassan, E, Kahilo, K, Kamal, T, Hassan, M & Saleh Elgawish, M (2019). The protective effect of epigallocatechin-3-gallate on testicular oxidative stress in lead-induced toxicity mediated by Cyp19 gene/estradiol level. Toxicology 422, 7683.CrossRefGoogle ScholarPubMed
Hermo, L & Robaire, B (2002). Epididymal cell types and their functions. In The Epididymis: From Molecules to Clinical Practice, Robaire, B & Hinton, BT (Eds.), pp. 81102. New York: Springer.CrossRefGoogle Scholar
Hininger-Favier, I, Benaraba, R, Coves, S, Anderson, RA & Roussel, AM (2009). Green tea extract decreases oxidative stress and improves insulin sensitivity in an animal model of insulin resistance, the fructose-fed rat. J Am Coll Nutr 28, 355361.CrossRefGoogle Scholar
Hirai, S, Naito, M, Terayama, H, Qu, N, Kuerban, M, Musha, M, Ikeda, A, Miura, M & Itoh, M (2012). The origin of lymphatic capillaries in murine testes. J Androl 33, 745751.CrossRefGoogle ScholarPubMed
Johnson, L & Neaves, WB (1981). Age-related changes in the Leydig cell population, seminiferous tubules, and sperm production in stallions. Biol Reprod 24, 703712.CrossRefGoogle ScholarPubMed
Kaplanoglu, GT, Bahcelioglu, M, Gozil, R, Helvacioglu, F, Buru, E, Tekindal, MA, Erdogan, D & Calguner, E (2013). Effects of green tea and vitamin E in the testicular tissue of streptozotocin-induced diabetic rats. Saudi Med J 34, 734743.Google ScholarPubMed
Karnovsky, MJ (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 15, 127137.Google Scholar
Kempinas, WG & Klinefelter, GR (2014). Interpreting histopathology in the epididymis. Spermatogenesis 4, e979114.CrossRefGoogle Scholar
Kianifard, D, Sadrkhanlou, RA & Hasanzedh, S (2012). The ultrastructural changes of the Sertoli and Leydig cells following streptozotocin induced diabetes. Iran J Basic Med Sci 15(1), 623635.Google ScholarPubMed
Korejo, NA, Wei, QW, Shah, AH & Shi, FX (2016). Effects of concomitant diabetes mellitus and hyperthyroidism on testicular and epididymal histoarchitecture and steroidogenesis in male animals. J Zhejiang Univ Sci B 17, 850863.CrossRefGoogle ScholarPubMed
Ladeira, LCM, dos Santos, EC, Santos, TA, Da Silva, J, Lima, GDA, Machado-Neves, M, Silva, RC, Freitas, MB & Maldonado, IRSC (2021). Green tea infusion prevents diabetic nephropathy aggravation in recent-onset type 1 diabetes regardless of glycemic control. J Ethnopharmacol 274, 114032.CrossRefGoogle ScholarPubMed
Ladeira, LCM, dos Santos, EC, Valente, GE, da Silva, J, Santos, TA & Maldonado, IRSC (2020). Could biological tissue preservation methods change chemical elements proportion measured by energy dispersive X-ray spectroscopy? Biol Trace Elem Res 196, 168172.CrossRefGoogle ScholarPubMed
Lanning, LL, Creasy, DM, Chapin, RE, Mann, PC, Barlow, NJ, Regan, KS & Goodman, DG (2002). Recommended approaches for the evaluation of testicular and epididymal toxicity. Toxicol Pathol 30, 507520.CrossRefGoogle ScholarPubMed
La Vignera, S, Condorelli, R, Vicari, E, D'agata, R & Calogero, AE (2012). Diabetes mellitus and minireview sperm parameters. J Androl 33, 145153.CrossRefGoogle Scholar
Leite, GAA, Figueiredo, TM, Sanabria, M, Dias, AFMG, Silva, PVE, Martins Junior, ADC, Barbosa Junior, F & Kempinas, WDG (2017). Ascorbic acid supplementation partially prevents the delayed reproductive development in juvenile male rats exposed to rosuvastatin since prepuberty. Reprod Toxicol 73, 328338.CrossRefGoogle ScholarPubMed
Mahmoudi, R, Azizi, A, Abedini, S, Hemayatkhah Jahromi, V, Abidi, H & Jafari Barmak, M (2018). Green tea improves rat sperm quality and reduced cadmium chloride damage effect in spermatogenesis cycle. J Med Life 11, 371380.Google ScholarPubMed
Mäkelä, JA, Koskenniemi, JJ, Virtanen, HE & Toppari, J (2019). Testis development. Endocr Rev 40, 857905.CrossRefGoogle ScholarPubMed
Maresch, CC, Stute, DC, Alves, MG, Oliveira, PF, de Kretser, DM & Linn, T (2018). Diabetes-induced hyperglycemia impairs male reproductive function: A systematic review. Hum Reprod Update 24, 86105.CrossRefGoogle ScholarPubMed
Martins, AD, Alves, MG, Bernardino, RL, Dias, TR, Silva, BM & Oliveira, PF (2014). Effect of white tea (Camellia sinensis (L.)) extract in the glycolytic profile of Sertoli cell. Eur J Nutr 53, 13831391.CrossRefGoogle ScholarPubMed
Meneses, M, Silva, B, Sousa, M, , R, Oliveira, P & Alves, M (2015). Antidiabetic drugs: Mechanisms of action and potential outcomes on cellular metabolism. Curr Pharm Des 21, 36063620.CrossRefGoogle ScholarPubMed
Mineharu, Y, Koizumi, A, Wada, Y, Iso, H, Watanabe, Y, Date, C, Yamamoto, A, Kikuchi, S, Inaba, Y, Toyoshima, H, Kondo, T & Tamakoshi, A (2011). Coffee, Green tea, black tea and oolong tea consumption and risk of mortality from cardiovascular disease in Japanese men and women. J Epidemiol Community Health 65, 230240.CrossRefGoogle ScholarPubMed
Mohamed, NA, Ahmed, OM, Hozayen, WG & Ahmed, MA (2018). Ameliorative effects of bee pollen and date palm pollen on the glycemic state and male sexual dysfunctions in streptozotocin-induced diabetic wistar rats. Biomed Pharmacother 97, 918.CrossRefGoogle ScholarPubMed
Murray, FT, Cameron, DF, Orth, JM & Katovich, MJ (1985). Gonadal dysfunction in the spontaneously diabetic BB rat: Alterations of testes morphology, serum testosterone and LH. Horm Metab Res 17, 495501.CrossRefGoogle ScholarPubMed
Navarro-Casado, L, Juncos-Tobarra, MA, Cháfer-Rudilla, M, De Onzoño, , Blázquez-Cabrera, JA & Miralles-García, JM (2010). Effect of experimental diabetes and STZ on male fertility capacity. Study in rats. J Androl 31, 584592.CrossRefGoogle ScholarPubMed
Nazem, F, Farhangi, N & Neshat-Gharamaleki, M (2015). Beneficial effects of endurance exercise with Rosmarinus officinalis labiatae leaves extract on blood antioxidant enzyme activities and lipid peroxidation in streptozotocin-induced diabetic rats. Can J Diabetes 39, 229234.CrossRefGoogle ScholarPubMed
Opuwari, C & Monsees, T (2020). Green tea consumption increases sperm concentration and viability in male rats and is safe for reproductive, liver and kidney health. Sci Rep 10(1), 15269.CrossRefGoogle ScholarPubMed
Perva-Uzunalić, A, Škerget, M, Knez, Ž, Weinreich, B, Otto, F & Grüner, S (2006). Extraction of active ingredients from Green tea (Camellia sinensis): Extraction efficiency of major catechins and caffeine. Food Chem 96, 597605.CrossRefGoogle Scholar
Picut, CA & Remick, AK (2017). Impact of age on the male reproductive system from the pathologist's perspective. Toxicol Pathol 45, 195205.CrossRefGoogle ScholarPubMed
Rashidi, B, Malekzadeh, M, Goodarzi, M, Masoudifar, A & Mirzaei, H (2017). Green tea and its anti-angiogenesis effects. Biomed Pharmacother 89, 949956.CrossRefGoogle ScholarPubMed
Robaire, B & Viger, RS (1995). Regulation of epididymal epithelial cell functions. Biol Reprod 52, 226236.CrossRefGoogle ScholarPubMed
Rotruck, JT, Pope, AL, Ganther, HE, Swanson, AB, Hafeman, DG & Hoekstra, WG (1973). Selenium: Biochemical role as a component of glutathione peroxidase. Science 179, 588590.CrossRefGoogle ScholarPubMed
Roychoudhury, S, Agarwal, A, Virk, G & Cho, CL (2017). Potential role of green tea catechins in the management of oxidative stress-associated infertility. Reprod BioMed Online 34, 487498.CrossRefGoogle ScholarPubMed
Russell, L, Ettlin, R, Sinhahikim, A & Clegg, E (1990). Mammalian spermatogenesis. In Histological and Histopathological Evaluation of the Testis, Russel, L, Ettlin, R, Sinha Hikim, A & Clegg, E (Eds.), pp. 140a. Florida: Cache River Press.Google Scholar
Seethalakshmi, L, Menon, M & Diamond, D (1987). The effect of streptozotocin-induced diabetes on the neuroendocrine-male reproductive tract axis of the adult rat. J Urol 138, 190194.CrossRefGoogle ScholarPubMed
Sexton, WJ & Jarow, JP (1997). Effect of diabetes mellitus upon male reproductive function. Urology 49, 508513.CrossRefGoogle ScholarPubMed
Shrilatha, B & Muralidhara, (2007). Occurrence of oxidative impairments, response of antioxidant defences and associated biochemical perturbations in male reproductive milieu in the streptozotocin-diabetic rat. Int J Androl 30, 508518.CrossRefGoogle ScholarPubMed
Souza, ACF, Bastos, DSS, Sertorio, MN, Santos, FC, Ervilha, LOG, de Oliveira, LL & Machado-Neves, M (2019). Combined effects of arsenic exposure and diabetes on male reproductive functions. Andrology 7, 730740.CrossRefGoogle ScholarPubMed
Souza, ACF, Marchesi, SC, Ferraz, RP, De Almeida Lima, GD, De Oliveira, JA & Machado-Neves, M (2016). Effects of sodium arsenate and arsenite on male reproductive functions in Wistar rats. J Toxicol Environ Health A 79, 274286.CrossRefGoogle ScholarPubMed
Sullivan, R & Mieusset, R (2016). The human epididymis: Its function in sperm maturation. Hum Reprod Update 22, 574587.CrossRefGoogle ScholarPubMed
Tae, HJ, Jang, BG, Ahn, DC, Choi, EY, Kang, HS, Kim, NS, Lee, JH, Park, SY, Yang, HH & Kim, IS (2005). Morphometric studies on the testis of Korean ring-necked pheasant (Phasianus colchicus karpowi) during the breeding and non-breeding seasons. Vet Res Commun 29, 629643.CrossRefGoogle ScholarPubMed
Turner, TT, Jones, CE, Howards, SS, Ewing, LL, Zegeye, B & Gunsalus, GL (1984). On the androgen microenvironment of maturing spermatozoa. Endocrinology 115, 19251932.CrossRefGoogle ScholarPubMed
Ueda-Wakagi, M, Nagayasu, H, Yamashita, Y & Ashida, H (2019). Green tea ameliorates hyperglycemia by promoting the translocation of glucose transporter 4 in the skeletal muscle of diabetic rodents. Int J Mol Sci 20, 2436.CrossRefGoogle ScholarPubMed
Wagner, IV, Klöting, N, Savchuk, I, Eifler, L, Kulle, A, Kralisch-Jäcklein, S, Dötsch, J, Hiort, O, Svechnikov, K & Söder, O (2021). Diabetes type 1 negatively influences Leydig cell function in rats, which is partially reversible by insulin treatment. Endocrinology 162, 4.CrossRefGoogle ScholarPubMed
Wong, TP, Debnam, ES & Leung, PS (2009). Diabetes mellitus and expression of the enterocyte renin-angiotensin system: Implications for control of glucose transport across the brush border membrane. Am J Physiol Cell Physiol 297, 601610.CrossRefGoogle ScholarPubMed
Zirkin, BR & Papadopoulos, V (2018). Leydig cells: Formation, function and regulation. Biol Reprod 99(1), 101111.CrossRefGoogle ScholarPubMed
Supplementary material: File

Guimarães-Ervilha et al. supplementary material

Table S1

Download Guimarães-Ervilha et al. supplementary material(File)
File 15.8 KB