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Benefits of the consumption of Brazil nut (Bertholletia excelsa) extract in male reproductive parameters of streptozotocin-induced diabetic rats

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Abstract

Objective

The objective of this study was to evaluate the effects of intake of Brazil nut extract (BN) or sodium selenite solution on reproductive parameters of male diabetic animals.

Methods

A total of 48 Wistar rats were distributed into six groups: diabetes (n = 8); diabetes and Brazil nut extract (n = 8); diabetes and sodium selenite (Na2SeO3) (n = 8); Brazil nut extract (n = 8); sodium selenite (n = 8) and control (n = 8). A single dose of streptozotocin (65 mg/kg) was injected intravenously to the rats to induce diabetes. BN or Na2SeO3 were administered by gavage for 56 days.

Results

The diabetes caused critical alterations on body mass gain, reproductive parameters and antioxidant capacity. Treatments with both BN or Na2SeO3 were able to increase significantly the glutathione peroxidase and the daily sperm production, both in diabetic (p < 0.01 and p < 0.05) and in healthy animals (p < 0.01 and p < 0.05).

Conclusion

The Brazil nut extract and sodium selenite were able to improve some reproductive parameters of diabetic rats. Moreover, we could infer that this effect is probably due to the natural selenium content of the BN.

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References

  1. Chougala MB, Bhaskar JJ, Rajan MG, Salimath PV. Effect of curcumin and quercetin on lysosomal enzyme activities in streptozotocin-induced diabetic rats. Clin Nutr. 2012;31:749–55.

    Article  CAS  PubMed  Google Scholar 

  2. Vehik K, Dabelea D. The changing epidemiology of type 1 diabetes: why is it going through the roof? Diabetes Metab Res Rev. 2011;27:3–13.

    Article  PubMed  Google Scholar 

  3. World Health Organization.

  4. Maritim AC, Sanders RA, Watkins JB 3rd. Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol. 2003;17:24–38.

    Article  CAS  PubMed  Google Scholar 

  5. Vincent AM, Russell JW, Low P, Feldman EL. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev. 2004;25:612–28.

    Article  CAS  PubMed  Google Scholar 

  6. Sexton WJ, Jarow JP. Effect of diabetes mellitus upon male reproductive function. Urology. 1997;49:508–13.

    Article  CAS  PubMed  Google Scholar 

  7. La Vignera S, Condorelli R, Vicari E, D'Agata R, Calogero AE. Diabetes mellitus and sperm parameters. J Androl. 2012;33:145–53.

    Article  PubMed  CAS  Google Scholar 

  8. Fernandes GS, Fernandez CD, Campos KE, Damasceno DC, Anselmo-Franci JA, Kempinas WD. Vitamin C partially attenuates male reproductive deficits in hyperglycemic rats. Reprod Biol Endocrinol. 2011 27; 9:100.

  9. Agarwal A, Prabakaran SA, Said TM. Prevention of oxidative stress injury to sperm. J Androl. 2005;26:654–60.

    Article  CAS  PubMed  Google Scholar 

  10. Pires VC, Gollücke AP, Ribeiro DA, Lungato L, D'Almeida V, Aguiar O. Grape juice concentrate protects reproductive parameters of male rats against cadmium-induced damage: a chronic assay. Br J Nutr. 2013;9:1–10.

    Google Scholar 

  11. Meletis C, Barker J. Natural ways to enhance male fertility. Alternative and complementary therapies. 2004;10:73–7.

    Article  Google Scholar 

  12. Papp LV, Lu J, Holmgren A, Khanna KK. From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid Redox Signal. 2007;9:775–806.

    Article  CAS  PubMed  Google Scholar 

  13. Ognjanović BI, Marković SD, Pavlović SZ, Zikić RV, Stajn AS, Saicić ZS. Effect of chronic cadmium exposure on antioxidant defense system in some tissues of rats: protective effect of selenium. Physiol Res. 2008;57:403–11.

    PubMed  Google Scholar 

  14. Thomson CD, Chisholm A, McLachlan SK, Campbell JM. Brazil nuts: an effective way to improve selenium status. Am J Clin Nutr. 2008;87:379–84.

    Article  CAS  PubMed  Google Scholar 

  15. John JA, Shahidi F. Phenolic compounds and antioxidant activity of Brazil nut (Bertholletia excelsa). J Funct Foods. 2010:196–209.

  16. Stockler-Pinto MB, Mafra D, Farage NE, Boaventura GT, Cozzolino SM. Effect of Brazil nut supplementation on the blood levels of selenium and glutathione peroxidase in hemodialysis patients. Nutrition. 2010;26:1065–9.

    Article  CAS  PubMed  Google Scholar 

  17. Cominetti C, de Bortoli MC, Garrido AB Jr, Cozzolino SM. Brazilian nut consumption improves selenium status and glutathione peroxidase activity and reduces atherogenic risk in obese women. Nutr Res. 2012;32:403–7.

    Article  CAS  PubMed  Google Scholar 

  18. Cai L, Chen S, Evans T, Deng DX, Mukherjee K, Chakrabarti S. Apoptotic germ-cell death and testicular damage in experimental diabetes: prevention by endothelin antagonism. Urol Res. 2000;28:342–7.

    Article  CAS  PubMed  Google Scholar 

  19. Ferberg,I; Cabral, L. C.; Gonçalves, E. B.; Deliza, R. Efeito das condições de extração no rendimento e qualidade do leite de castanha-do-brasil despeliculada. Boletim do Centro de Pesquisa em Processamento de Alimentos: Curitiba, 2002. 20, p 75–88.

  20. Cardareli HR, Oliveira AJ. Conservação do Leite de Castanha-do-Pará. Scientia Agricola, Piracicaba. 2000;57:617–22.

    Article  Google Scholar 

  21. Lima LW, Stonehouse GC, Walters C, Mehdawi AFE, Fakra SC, Pilon-Smits EAH. Selenium Accumulation, Speciation and Localization in Brazil Nuts (Bertholletia excelsa H.B.K.). Plants (Basel). 2019 Aug 16;8(8).

  22. Robb GW, Amann RP, Killian GJ. Daily sperm production and epididymal sperm reserves of pubertal and adult rats. J Reprod Fertil. 1978;54:103–7.

    Article  CAS  PubMed  Google Scholar 

  23. 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. ILSI risk science institute expert working group on sperm evaluation. Reprod Toxicol. 1996;10:237–44.

    Article  CAS  PubMed  Google Scholar 

  24. Predes FS, Diamante MA, Dolder H. Testis response to low doses of cadmium in Wistar rats. Int J Exp Pathol. 2010;91:125–31.

    Article  CAS  Google Scholar 

  25. 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;1:2–25.

    CAS  PubMed  Google Scholar 

  26. Tsounapi P, Saito M, Dimitriadis F, Koukos S, Shimizu S, Satoh K, et al. Antioxidant treatment with edaravone or taurine ameliorates diabetes-induced testicular dysfunction in the rat. Mol Cell Biochem. 2012;369:195–204.

    Article  CAS  PubMed  Google Scholar 

  27. Lee JH, Sul D, Oh E, Jung WW, Hwang KW, Hwang TS, et al. Panax ginseng effects on DNA damage, CYP1A1 expression and histopathological changes in testes of rats exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Food Chem Toxicol. 2007;45:2237–44.

    Article  CAS  PubMed  Google Scholar 

  28. Neter, J; Kutnher, M. H.; Nachsteim, C. J. e Wasserman, W. Applied Linear Statistical Models. Irwin. (1996).

  29. Shrilatha B; Muralidhara. Occurrence of oxidative impairments, response of antioxidant defences and associated biochemical perturbations in male reproductive milieu in the Streptozotocin-diabetic rat. Int J Androl. 2007; 30: 508–518.

  30. Etuk EU. Animals models for studying diabetes mellitus. ABJNA. 2010;1:130–4.

    CAS  Google Scholar 

  31. Stapleton SR. Selenium: an insulin-mimetic. Cell Mol Life Sci. 2000;57:1874–9.

    Article  CAS  PubMed  Google Scholar 

  32. Hei YJ, Farahbakhshian S, Chen X, Battell ML, McNeill JH. Stimulation of MAP kinase and S6 kinase by vanadium and selenium in rat adipocytes. Mol Cell Biochem. 1998;178:367–75.

    Article  CAS  PubMed  Google Scholar 

  33. Pillai SS, Sugathan JK, Indira M. Selenium downregulates RAGE and NFκB expression in diabetic rats. Biol Trace Elem Res. 2012;149:71–7.

    Article  CAS  PubMed  Google Scholar 

  34. Güney M. Selenium-vitamin e combination modulates endometrial lipid peroxidation and antioxidant enzymes in streptozotocin-induced diabetic rat. Biol Trace Elem Res. 2012;149:234–40.

    Article  PubMed  CAS  Google Scholar 

  35. Erbayraktar Z, Yilmaz O, Artmann AT, Cehreli R, Coker C. Effects of selenium supplementation on antioxidant defense and glucose homeostasis in experimental diabetes mellitus. Biol Trace Elem Res. 2007;118:217–26.

    Article  CAS  PubMed  Google Scholar 

  36. Ayaz M, Can B, Ozdemir S, Turan B. Protective effect of selenium treatment on diabetes-induced myocardial structural alterations. Biol Trace Elem Res. 2002;89:215–26.

    Article  CAS  PubMed  Google Scholar 

  37. Barceloux DG. Selenium. J Toxicol Clin Toxicol. 1999;37:145–72.

    Article  CAS  PubMed  Google Scholar 

  38. Ricci G, Catizone A, Esposito R, Pisanti FA, Vietri MT, Galdieri M. Diabetic rat testes: morphological and functional alterations. Andrologia. 2009;41:361–8.

    Article  CAS  PubMed  Google Scholar 

  39. Mohasseb M, Ebied S, Yehia MA, Hussein N. Testicular oxidative damage and role of combined antioxidant supplementation in experimental diabetic rats. J Physiol Biochem. 2011;67:185–94.

    Article  CAS  PubMed  Google Scholar 

  40. Unlüçerçi Y, Bekpinar S, Koçak H. Testis glutathione peroxidase and phospholipid hydroperoxide glutathione peroxidase activities in aminoguanidine-treated diabetic rats. Arch Biochem Biophys. 2000;379:217–20.

    Article  PubMed  CAS  Google Scholar 

  41. Rauscher FM, Sanders RA, Watkins JB 3rd. Effects of coenzyme Q10 treatment on antioxidant pathways in normal and streptozotocin-induced diabetic rats. J Biochem Mol Toxicol. 2001;15:41–6.

    Article  CAS  PubMed  Google Scholar 

  42. Sözmen EY, Sözmen B, Delen Y, Onat T. Catalase/superoxide dismutase (SOD) and catalase/paraoxonase (PON) ratios may implicate poor glycemic control. Arch Med Res. 2001 Jul-Aug;32(4):283–7.

    Article  PubMed  Google Scholar 

  43. Brigelius-Flohé R, Maiorino M. Glutathione peroxidases. Biochim Biophys Acta. 2012;29.

  44. Chowdhury AK, Tcholakian RK. Effects of various doses of testosterone propionate on intratesticular and plasma testosterone levels and maintenance of spermatogenesis in adult hypophysectomized rats. Steroids. 1979;34:151–62.

    Article  CAS  PubMed  Google Scholar 

  45. Chernyshova ES, Zaikina YS, Tsvetovskaya GA, Strokotov DI, Yurkin MA, Serebrennikova ES, et al. Influence of magnesium sulfate on HCO3/cl transmembrane exchange rate in human erythrocytes. J Theor Biol. 2016 Mar 21;393:194–202.

    Article  CAS  PubMed  Google Scholar 

  46. Morabito R, Remigante A, Marino A. Protective role of magnesium against oxidative stress on SO(4)(=) uptake through band 3 protein in human erythrocytes. Cell Physiol Biochem. 2019;52(6):1292–308.

    Article  CAS  PubMed  Google Scholar 

  47. Wang C, Zhang Y, Liang J, Shan G, Wang Y, Shi Q. Impacts of ascorbic acid and thiamine supplementation at different concentrations on lead toxicity in testis. Clin Chim Acta. 2006 Aug;370(1–2):82–8.

    Article  CAS  PubMed  Google Scholar 

  48. Kolagal V, Karanam SA, Dharmavarapu PK, D'Souza R, Upadhya S, Kumar V, et al. Determination of oxidative stress markers and their importance in early diagnosis of uremia-related complications. Indian J Nephrol. 2009 Jan;19(1):8–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Pérez YG, Pérez LC, Netto Rde C, Lima DS, Lima ES. Malondialdehyde and sulfhydryl groups as biomarkers of oxidative stress in patients with systemic lupus erythematosus. Rev Bras Reumatol. 2012 Aug;52(4):658–60.

    Article  PubMed  Google Scholar 

  50. Hernández-Montiel HL, Vásquez López CM, González-Loyola JG, Vega-Anaya GC, Villagrán-Herrera ME, Gallegos-Corona MA, et al. Chronic administration of thiamine pyrophosphate decreases age-related histological atrophic testicular changes and improves sexual behavior in male Wistar rats. Histol Histopathol. 2014 Jun;29(6):785–95.

    PubMed  Google Scholar 

  51. Guneli E, Tugyan K, Ozturk H, Gumustekin M, Cilaker S, Uysal N. Effect of melatonin on testicular damage in streptozotocin-induced diabetes rats. Eur Surg Res. 2008;40:354–60.

    Article  CAS  PubMed  Google Scholar 

  52. Masaki H, Okano Y, Sakurai H. Differential role of catalase and glutathione peroxidase in cultured human fibroblasts under exposure of H2O2 or ultraviolet B light. Arch Dermatol Res. 1998;290:113–8.

    Article  CAS  PubMed  Google Scholar 

  53. Luo L, Chen H, Trush MA, Show MD, Anway MD, Zirkin BR. Aging and the brown Norway rat leydig cell antioxidant defense system. J Androl. 2006;27:240–7.

    Article  CAS  PubMed  Google Scholar 

  54. Miller WL. StAR search--what we know about how the steroidogenic acute regulatory protein mediates mitochondrial cholesterol import. Mol Endocrinol. 2007;21:589–601.

    Article  CAS  PubMed  Google Scholar 

  55. Ren XM, Wang GG, Xu DQ, Luo K, Liu YX, Zhong YH, et al. The protection of selenium on cadmium-induced inhibition of spermatogenesis via activating testosterone synthesis in mice. Food Chem Toxicol. 2012;50:3521–9.

    Article  CAS  PubMed  Google Scholar 

  56. Behne D, Höfer T, von Berswordt-Wallrabe R, Elger W. Selenium in the testis of the rat: studies on its regulation and its importance for the organism. J Nutr. 1982;112:1682–7.

    Article  CAS  PubMed  Google Scholar 

  57. Walker WH. Testosterone signaling and the regulation of spermatogenesis. Spermatogenesis. 2011;1(2):116–120. Ahmed OM, Gabar MA, Ali TM. Impacts of the coexistence of diabetes and hypothyroidism on body weight gain, leptin and various metabolic aspects in albino rats. J Diabetes Complications. 2012 Jul 4.

  58. Zirkin BR, Santulli R, Awoniyi CA, Ewing LL. Maintenance of advanced spermatogenic cells in the adult rat testis: quantitative relationship to testosterone concentration within the testis. Endocrinology. 1989 Jun;124(6):3043–9.

    Article  CAS  PubMed  Google Scholar 

  59. Coviello AD, Bremner WJ, Matsumoto AM, Herbst KL, Amory JK, Anawalt BD, et al. Intratesticular testosterone concentrations comparable with serum levels are not sufficient to maintain normal sperm production in men receiving a hormonal contraceptive regimen. J Androl. 2004 Nov-Dec;25(6):931–8.

    Article  CAS  PubMed  Google Scholar 

  60. Sharpe RM, Donachie K, Cooper I. Re-evaluation of the intratesticular level of testosterone required for quantitative maintenance of spermatogenesis in the rat. J Endocrinol. 1988 Apr;117(1):19–26.

    Article  CAS  PubMed  Google Scholar 

  61. Castro ACS, Berndtson WE, Cardoso FM. Plasma and testicular testosterone levels, volume density and number of Leydig cells and spermatogenic efficiency of rabbits. Braz J Med Biol Res [online]. 2002;35(4):493–8.

  62. Walker WH. Molecular mechanisms of testosterone action in spermatogenesis. Steroids. 2009;74:602–7.

    Article  CAS  PubMed  Google Scholar 

  63. Juan ME, González-Pons E, Munuera T, Ballester J, Rodríguez-Gil JE, Planas JM. Trans-resveratrol, a natural antioxidant from grapes, increases sperm output in healthy rats. J Nutr. 2005;135:757–60.

    Article  CAS  PubMed  Google Scholar 

  64. Behne D, Höfer T, von Berswordt-Wallrabe R, Elger W. Selenium in the testis of the rat: studies on its regulation and its importance for the organism. J Nutr. 1982;112:1682–7.

    Article  CAS  PubMed  Google Scholar 

  65. Saaranen M, Suistomaa U, Kantola M, Saarikoski S, Vanha-Perttula T. Lead, magnesium, selenium and zinc in human seminal fluid: comparison with semen parameters and fertility. Hum Reprod. 1987;2:475–9.

    Article  CAS  PubMed  Google Scholar 

  66. Hawkes WC, Alkan Z, Wong K. Selenium supplementation does not affect testicular selenium status or semen quality in north American men. J Androl. 2009;30:525–33.

    Article  CAS  PubMed  Google Scholar 

  67. Singh S, Malini T, Rengarajan S, Balasubramanian K. Impact of experimental diabetes and insulin replacement on epididymal secretory products and sperm maturation in albino rats. J Cell Biochem. 2009;108:1094–101.

    Article  CAS  PubMed  Google Scholar 

  68. Vigueras-Villaseñor RM, Rojas-Castañeda JC, Chávez-Saldaña M, Gutiérrez-Pérez O, García-Cruz ME, Cuevas-Alpuche O, et al. Alterations in the spermatic function generated by obesity in rats. Acta Histochem. 2011;113:214–20.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Nascimento, L.P.S. received fellowship from CAPES REUNI (Coordenação de Aperfoiçoamento de Pessoal de Nível Superior). All authors contributed significantly to the study development and manuscript preparation. The authors thank Marcia Regina Nagaoka and Edílson Dantas for sharing their knowledge during the induction of diabetes phase; Celina de Almeida Lamas for helping with animals’ gavage; Daniela Ortolani for assisting animals’ euthanasia and Vânia D’Almeida for the valuable discussion concerning the antioxidant parameters of this work.

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Authors and Affiliations

  1. Departamento de Biociências, Universidade Federal de São Paulo (UNIFESP), Campus Baixada Santista, Rua Silva Jardim, 136, Vila Mathias, Santos, SP, 11015-020, Brazil

    Leonardo Parreira Silva Nascimento, Vanessa Cardoso Pires, Daniel Araki Ribeiro, Andréa Pittelli Boiago Gollücke & Odair Aguiar Junior

  2. Departamento de Química e Hexalab, Universidade Católica de Santos, Avenida Conselheiro Nébias, 300, Santos, SP, 11015-002, Brazil

    Hirochi Yamamura

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  1. Leonardo Parreira Silva Nascimento
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Nascimento, L.P.S., Pires, V.C., Ribeiro, D.A. et al. Benefits of the consumption of Brazil nut (Bertholletia excelsa) extract in male reproductive parameters of streptozotocin-induced diabetic rats. J Diabetes Metab Disord 19, 187–196 (2020). https://doi.org/10.1007/s40200-020-00490-8

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