Effects of Rooibos (Aspalathus linearis) on the Testicular Parenchyma of Adult BALB/C Mice Submitted to a Hypercaloric Diet

Authors

  • Hilara Niemeyer Ruas Universidade Federal do Triângulo Mineiro
  • João Vitor Lopes-Ferreira Universidade Federal do Triângulo Mineiro
  • Fernanda Carolina Ribeiro Dias Universidade Federal do Triângulo Mineiro https://orcid.org/0000-0002-6530-4684
  • Maria Emília Soares Martins dos Santos Universidade Federal do Triângulo Mineiro https://orcid.org/0000-0001-8922-0867
  • Angelica de Oliveira Gomes Universidade Federal do Triângulo Mineiro
  • Mariella Bontempo Freitas Universidade Federal de Viçosa https://orcid.org/0000-0001-5132-242X
  • Marcos de Lucca Moreira Gomes Universidade Federal do Triângulo Mineiro https://orcid.org/0000-0003-4397-4609

DOI:

https://doi.org/10.14393/BJ-v39n0a2023-64537

Keywords:

High fat diet, Obesity, Oxidative stress, Reproduction, Testis.

Abstract

Oxidative stress due to obesity plays a detrimental role in the testicular microenvironment and sperm parameters. We explored the impact of a hypercaloric diet in male BALB/c mice as a condition to trigger damage to the spermatogenic process and the antioxidant effect of Aspalathus linearis as well. We used a hypercaloric diet in animals divided into 3 groups: Control, Hypercaloric diet control (HC) and Hypercaloric diet and Rooibos infusion (HCR). Morphometric parameters, enzyme dosages, cell viability, and tubular histopathology were evaluated. Body weight increased in HCR animals at weeks 3, 4, and 8. We found a reduction in seminiferous epithelium height, with an increase in the tubular diameter of the HCR group. Catalase levels were lower in HC and HCR, while carbonyl protein was decreased in HC. We estimate that it induces oxidative stress (OS) capable of affecting the seminiferous epithelium and that the infusion of A. linearis does not demonstrate a potential benefit in cell preservation.

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References

AGARWAl A, PAREKH N, SELVAM MKP, HENKEL R, SHAH R, HOMA ST, et al. Male oxidative stress infertility (MOSI): Proposed terminology and clinical practice guidelines for management of idiopathic male infertility. World Journal of Men?s Health. Korean Society for Sexual Medicine and Andrology; 2019. 37, 296–312. https://doi.org/10.5534/wjmh.190055

ASADI N, BAHMANI M, Kheradmand A, Rafieian-Kopaei M. The impact of oxidative stress on testicular function and the role of antioxidants in improving it: A review. J Clin Diagnostic Res. 2017. 11(5), 1-5. https://doi.org/10.7860/jcdr/2017/23927.9886

AWONIYI DO, Aboua YG, MARNEWICK J, BROOKS N. The effects of Rooibos (Aspalathus linearis), green te (Camelli sinensis) and commercial Rooibos and green tea supplements on epididymal sperm in oxidative stress-induced rats. Phyther Res. 2012. 26(8), 1231–1239. https://doi.org/10.1002/ptr.3717

BANSAL AK, BILASPURI GS. Impacts of Oxidative Stress and Antioxidants on Semen Functions. Vet Med Int [Internet]. 2011. 2011, 1–7. / https://doi.org/10.4061/2011/686137

BARBOSA KBF, COSTA NMB, DE CÁSSIA Gonçalves Alfenas R, DE PAULA SO, MINIM VPR, BRESSAN J. Estresse oxidativo: Conceito, implicações e fatores modulatórios. Rev Nutr. 2010. 23(4), 629–643. https://doi.org/10.1590/S1415-52732010000400013

CANDA BD, OGUNTIBEJU OO, Marnewick JL. Effects of consumption of Rooibos (Aspalathus linearis) and a Rooibos-derived commercial supplement on hepatic tissue injury by tert -butyl hydroperoxide in wistar rats. Oxid Med Cell Longev. 2014; 2014, 9. https://doi.org/10.1155/2014/716832

CARDOSO PC dos S. Avaliação in vitro dos possíveis efeitos citotóxicos, genotóxicos e mutagênicos das drogas antimaláricas artemisinina e artemeter em linfócitos humanos. 2012. 59. http://repositorio.ufpa.br/jspui/handle/2011/3288

CHU HF, PAN MH, Ho CT, TSENG YH, WANg WWL, CHAU CF. Variations in the efficacy of resistant maltodextrin on body fat reduction in rats fed different high-fat models. J Agric Food Chem. 2014. 62(1), 192–197. https://doi.org/10.1021/jf404809v

DE OLIVEIRA CFA, Lara N de L e. M, Cardoso BRL, de França LR, de Avelar GF. Comparative testis structure and function in three representative mice strains. Cell Tissue Res. 2020. 382(2), 391–404. https://doi.org/10.1007/s00441-020-03239-0

DIAS FCR, MARTINS ALP, DE MELO FCSA, CUPERTINO M do C, GOMES M de LM, DE OLIVEIRA JM, et al. 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 [Internet]. 2019. 233, 179–189. https://doi.org/10.1016/j.jep.2018.12.047

DIAS FCR, Machado-Neves M, Lima GDA, Martins ALP, Menezes TP, Melo FCSA, et al. How bad is brazilian ginseng extract for reproductive parameters in mice? Histol Histopathol. 2020. 35(10), 1135–1149. https://doi.org/10.14670/hh-18-244.

DUTTA S, MAJZOUB A, AGARWAL A. Oxidative stress and sperm function: A systematic review on evaluation and management. Arab J Urol [Internet]. 2019. 17(2), 87–97. https://doi.org/10.1080/2090598X.2019.1599624

AEBI, Hugo. [13] Catalase in vitro. Methods in enzymology. 1984. 105, 121-126.https://doi.org/10.1016/s0076-6879(84)05016-3

GREENWALD, Robert A. CRC Handbook of Methods for Oxygen Radical. by Thornalley PJ, Bannister JV, CRC Press, New York. 1985. 133-136. https://doi.org/10.1016/s0076-6879(84)05016-3

FAN Y, LIU Y, XUE K, GU G, FAN W, XU Y, et al. Diet-induced obesity in male C57BL/6 mice decreases fertility as a consequence of disrupted blood-testis barrier. PLoS One. 2015. 10(4), 1–15. https://doi.org/10.1371/journal.pone.0120775.

FUNES A, SAEZ Lancellotti TE, SANTILLAN LD, DELLA Vedova MC, MONCLUS MA, CABRILLANA ME, et al. A chronic high-fat diet causes sperm head alterations in C57BL/6J mice. Heliyon [Internet]. 2019. 5(11). https://doi.org/10.1016/j.heliyon.2019.e02868

GHOLAMI S, ANSARI-Lari M, KHALILI L. Histologic and histomorphometric changes of testis following oral exposure to methyl tertiary-butyl ether in adult rat. Iran J Vet Res. 2015. 16(3), 288–292. http://www.ncbi.nlm.nih.gov/pmc/articles/pmc4782700/

GIRI BR, ROY B. Cysticercus fasciolaris infection induced oxidative stress and apoptosis in rat liver: a strategy for host-parasite cross talk. Parasitol Res [Internet]. 2016. 115(7), 2617–2624. Available from: http://dx.doi.org/10.1007/s00436-016-5008-3

GÓMEZ-ELÍAS MD, RAINERO Cáceres TS, GIACCAGLi MM, GUAZZONE VA, DALTON GN, DE SIERVI A, et al. Association between high-fat diet feeding and male fertility in high reproductive performance mice. Sci Rep. 2019. 9(1), 1–9. https://doi.org/10.1038/s41598-019-54799-3

GONÇALVES R V., NOVAES RD, LEITE JPV, VILELA EF, CUPERTINO MC, NUNEs LG, et al. Hepatoprotective effect of Bathysa cuspidata in a murine model of severe toxic liver injury. Int J Exp Pathol. 2012. 93(5), 370–376. https://doi.org/10.1111/j.1365-2613.2012.00835.x.

HABIG WH, PABST MJ, JAKOBY WB. Glutathione S transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem [Internet]. 1974. 249(22), 7130–7139. http://dx.doi.org/10.1016/S0021-9258(19)42083-8.

HESS RA, DE FRANCA LR. Spermatogenesis and cycle of the seminiferous epithelium. Adv Exp Med Biol. 2008. 636, 1–15. https://doi.org/10.1007/978-0-387-09597-4_1

HOLSBERGER DR, BUCHOLD GM, Leal MC, KIESEWETTER SE, O’BRIEN DA, HESS RA, et al. Cell-cycle inhibitors p27Kip1 and p21cip1 regulate murine sertoli cell proliferation. Biol Reprod. 2005. 72(6), 1429–1436. https://doi.org/10.1080/15384101.2016.1207835

JOHNSEN SG. Testicular biopsy score count--a method for registration of spermatogenesis in human testes: normal values and results in 335 hypogonadal males. Hormones. 1970. 1(1), 2–25. https://doi.org/10.1159/000178170.

KARL J, CAPEL B. Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev Biol. 1998. 203(2), 323–333. https://doi.org/10.1006/dbio.1998.9068

KEFER JC, AGARWAL A, SABANEGH E. Role of antioxidants in the treatment of male infertility. Int J Urol. 2009. 16(5), 449–457. https://doi.org/10.1111/j.1442-2042.2009.02280.x

KENAGY GJ, TROMBULAK SC. Size and Function of Mammalian Testes in Relation to Body Size. Jounal Mammal [Internet]. 1986. 67(1), 1–22. https://doi.org/10.2307/1380997

LEISEGANG, Kristian; HENKEL, Ralf; AGARWAL, Ashok. Obesity and metabolic syndrome associated with systemic inflammation and the impact on the male reproductive system. American journal of reproductive immunology. 2019. 82(5), 13178, 2019. https://doi.org/10.1111/aji.13178

LIN B, HASEGAWA Y, TAKANE K, KOIBUCHI N, CAO C, KIM-Mitsuyama S. High-Fat-Diet Intake Enhances Cerebral Amyloid Angiopathy And Cognitive Impairment In A Mouse Model Of Alzheimer’s Disease, Independently Of Metabolic Disorders. J Am Heart Assoc. 2016. 5(6), 1–16. https://doi.org/10.1161/jaha.115.003154

LIU Y, DING Z. Obesity, A Serious Etiologic Factor For Male Subfertility In Modern Society. Reproduction. 2017. 154(4), 123–131. https://doi.org/10.1530/rep-17-0161

LOWRY Oh, Rosebrough Nj, Farr Al, Randall Rj. Protein Measurement With The Folin Phenol Reagent. J Biol Chem [Internet]. 1951. 193(1), 265–275. http://dx.doi.Org/10.1016/S0021-9258(19)52451-6

MÄKELÄ Ja, KOSKENNIEMi Jj, VIRTANEN He, TOPPARI J. Testis Development. Endocr Rev. 2019. 40(4), 857–905. https://doi.org/10.1210/er.2018-00140

MATHIJS I, DA CUNHA Da, HIMPE E, LADRIERE L, CHELLAN N, ROUX Cr, Et Al. Phenylpropenoic Acid Glucoside Augments Pancreatic Beta Cell Mass In High-Fat Diet-Fed Mice And Protects Beta Cells From Er Stress-Induced Apoptosis. Mol Nutr Food Res. 2014. 58(10), 1980–1990. https://doi.org/10.1371/journal.pone.0157604

MCPHERSON No, LANE M. Male Obesity And Subfertility, Is It Really About Increased Adiposity? Asian J Androl. 2015. 17(3), 450–458. https://doi.org/10.4103/1008-682x.148076

MELO Fcsa, MATTA Slp, PAULA Tar, GOMES Mlm, OLIVEIRA Lc. The Effects Of Tynnanthus Fasciculatus (Bignoniaceae) Infusion On Testicular Parenchyma Of Adult Wistar Rats. Biol Res. 2010. 43(4), 445–450. http://dx.doi.org/10.4067/S0716-97602010000400009

MORTON Jf. Rooibos Tea, Aspalathus Linearis, A Caffeineless, Low-Tannin Beverage 1. Econ Bot. 1983. 37(2), 164–173. https://doi.Org/10.1016/J.Sajb.2011.07.004

MU Y, YAN Wj, YIN Tl, YANG J. Curcumin Ameliorates High-Fat Diet-Induced Spermatogenesis Dysfunction. Mol Med Rep. 2016. 14(4), 3588–3594. https://doi.org/10.3892/mmr.2016.5712

NASCIMENTO Af, SUGIZAKI Mm, LEOPOLDO As, LIMA-LEOPOLDO Ap, LUVIZOTTO Ram, NOGUEIRA Cr, Et Al. A Hypercaloric Pellet-Diet Cycle Induces Obesity And Co-Morbidities In Wistar Rats. Arq Bras Endocrinol Metabol. 2008. 52(6), 968–974. Https://doi.Org/10.1590/S0004-27302008000600007

OAKBERG Ef. Duration Of Spermatogenesis In The Mouse And Timing Of Stages Of The Cycle Of The Seminiferous Epithelium. Am J Anat. 1956. 99(3). 507–516. https://doi.org/10.1002/aja.1000990307

OLIVEIRA Cf, LARA Nl, LACERDA Sm, RESENDE Rr, FRANÇA Lr, AVELAR Gf. Foxn1 And Prkdc Genes Are Important For Testis Function: Evidence From Nude And Scid Adult Mice. Cell Tissue Res. 2020. 380(3), 615–625. https://doi.org/10.1007/s00441-019-03165-w

OLIVEIRA Mc, MENEZES-GARCIA Z, Henriques Mcc, Soriani Fm, Pinho V, Faria Amc, Et Al. Acute And Sustained Inflammation And Metabolic Dysfunction Induced By High Refined Carbohydrate-Containing Diet In Mice. Obesity. 2013. 21(9). https://doi.org/10.1002/oby.20230

OPUWARI Cs, MONSEES Tk. In Vivo Effects Of Aspalathus Linearis (Rooibos) On Male Rat Reproductive Functions. Andrologia. 2014. 46(8), 867–77. https://doi.org/10.1111/and.12158

PEREIRA Jl, E SOUZA Pcs, SHINZATO Vi, SASSO S, SANTO Bls Do E, SANTANA Lf, Et Al. Ganho De Peso E Alterações Metabólicas Em Camundongos Submetidos À Dieta Hiperlipídica. Ciência & Saúde. 2018. 11(1), 51. https://doi.Org/10.15448/1983-652x.2018.1.27672

RIBEIRO S, SCARTON S, BARBOSA Retameiro Ac, TEREZA A, GUIMARÃES B, MEIRE R, Et Al. Sericin Exerts Antioxidation On Testis And Epididyms Of C57bl/6 Mice Fed High Fat Diet. Int J Dev Res. 2017. 7(10), 15813–15820. https://doi.org/10.1371/journal.pone.0120775

RICART-JANÉ D, LLOBERA M, LÓPEZ-TEJERO Md. Anticoagulants And Other Preanalytical Factors Interfere In Plasma Nitrate/Nitrite Quantification By The Griess Method. Nitric Oxide - Biol Chem. 2002. 6(2), 178–185. https://doi.org/10.1006/niox.2001.0392

Rosini Tc, Da Silva Asr, Moraes C De. Obesidade Induzida Por Consumo De Dieta: Modelo Em Roedores Para O Estudo Dos Distúrbios Relacionados Com A Obesidade. Rev Assoc Med Bras. 2012. 58(3), 383–387.https://doi.org/10.1590/S0104-42302012000300021

SALAS-HUETOS A, BULLÓ M, SALAS-SALVADÓ J. Dietary Patterns, Foods And Nutrients In Male Fertility Parameters And Fecundability: A Systematic Review Of Observational Studies. Hum Reprod Update. 2017. 23(4), 371–389. https://doi.org/10.1093/humupd/dmx006

SASAKI M, NISHIDA N, SHIMADA M. A Beneficial Role Of Rooibos In Diabetes Mellitus: A Systematic Review And Meta-Analysis. Molecules. 2018. 23(4), 1–15. https://doi.org/10.3390/molecules23040839.

SEED J, CHAPIN Re, CLEGG Ed, DOSTAL La, FOOTE Rh, HURTT Me, Et Al. Methods For Assessing Sperm Motility, Morphology, And Counts In The Rat, Rabbit, And Dog: A Consensus Report. Reprod Toxicol. 1996. 10(3), 237–244. https://doi.org/10.1016/0890-6238(96)00028-7

ULIČNÁ O, VANČOVÁ O, BOŽEK P, ČÁRSKY J, ŠEBEKOVÁ K, BOOR P, Et Al. Rooibos Tea (Aspalathus Linearis) Partially Prevents Oxidative Stress In Streptozotocin-Induced Diabetic Rats. Physiol Res. 2006. 55(2), 157–64. http://www.biomed.cas.cz/physiolres/pdf/55/55_157.pdf

VELLOSO La. The Brain Is The Conductor: Diet-Induced Inflammation Overlapping Physiological Control Of Body Mass And Metabolism. Arq Bras Endocrinol Metabol. 2009. 53(2), 151–158. https://doi.org/10.1590/S0004-27302009000200006

WAGNER H, CHENG Jw, KO Ey. Role Of Reactive Oxygen Species In Male Infertility: An Updated Review Of Literature. Arab J Urol [Internet]. 2018. 16(1), 35–43. https://doi.org/10.1016/J.Aju.2017.11.001

WALLIN B, ROSENGREN B, SHERTZER Hg, CAMEJO G. Lipoprotein Oxidation And Measurement Of Thiobarbituric Acid Reacting Substances Formation In A Single Microtiter Plate: Its Use For Evaluation Of Antioxidants. Analytical Biochemistry. 1993. 108, 10–5. https://doi.org/10.1006/abio.1993.1002

WHITE Pas, CERCATO Lm, ARAÚJO Jmd, SOUZA La, SOAREs Af, BARBOSa Apo, Et Al. Modelo De Obesidade Induzida Por Dieta Hiperlipídica E Associada À Resistência À Ação Da Insulina E Intolerância À Glicose. Arq Bras Endocrinol Metabol. 2013. 57(5), 339–345. https://doi.org/10.1590/S0004-27302013000500002

YUAN M, HUANG G, LI J, ZHANG J, LI F, LI K, Et Al. Hyperleptinemia Directly Affects Testicular Maturation At Different Sexual Stages In Mice, And Suppressor Of Cytokine Signaling 3 Is Involved In This Process. Reprod Biol Endocrinol [Internet]. 2014. 12(1), 1–13. https://doi.org/10.1186/1477-7827-12-15

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Published

2023-02-24

How to Cite

NIEMEYER RUAS, H., LOPES-FERREIRA, J.V., DIAS, F.C.R., SANTOS, M.E.S.M. dos, GOMES, A. de O., FREITAS, M.B. and GOMES, M. de L.M., 2023. Effects of Rooibos (Aspalathus linearis) on the Testicular Parenchyma of Adult BALB/C Mice Submitted to a Hypercaloric Diet. Bioscience Journal [online], vol. 39, pp. e39030. [Accessed15 November 2024]. DOI 10.14393/BJ-v39n0a2023-64537. Available from: https://seer.ufu.br/index.php/biosciencejournal/article/view/64537.

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Biological Sciences