Aqueous extract from Mangifera indica Linn. (Anacardiaceae) leaves exerts long-term hypoglycemic effect, increases insulin sensitivity and plasma insulin levels on diabetic Wistar rats

English version

Autoři: Gustavo Roberto Villas Boas ^aff001; João Marcos Rodrigues Lemos ^aff003; Matheus William de Oliveira ^aff003; Rafael Claudino dos Santos ^aff002; Ana Paula Stefanello da Silveira ^aff003; Flávia Barbieri Bacha ^aff003; Caren Naomi Aguero Ito ^aff003; Ediane Bortolotte Cornelius ^aff003; Fernanda Brioli Lima ^aff003; Andrea Marisa Sachilarid Rodrigues ^aff003; Nathália Belmal Costa ^aff003; Felipe Francisco Bittencourt ^aff003; Fernando Freitas de Lima ^aff002; Marina Meirelles Paes ^aff001; Priscila Gubert ^aff001; Silvia Aparecida Oesterreich ^aff002
Působiště autorů: Research Group on Development of Pharmaceutical Products (P&DProFar), Center for Biological and Health Sciences, Federal University of Western Bahia, Barreiras, Bahia, Brazil ^aff001; Faculty of Health Sciences, Federal University of Grande Dourados, Dourados, Mato Grosso do Sul, Brazil ^aff002; Faculty of Health Sciences, University Center of Grande Dourados, Dourados, Mato Grosso do Sul, Brazil ^aff003; Department of Biochemistry, Laboratory of Imunopathology Keizo Asami, Federal University of Pernambuco, Recife, Brazil ^aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0227105

Souhrn

Background

Diabetes mellitus is one of the most common todays public health problems. According to a survey by the World Health Organization, this metabolic disorder has reached global epidemic proportions, with a worldwide prevalence of 8.5% in the adult population.

Objectives

The present study aimed to investigate the hypoglycemic effect of aqueous extract of Mangifera indica (EAMI) leaves in streptozotocin-induced diabetic rats.

Methods

Sixty male rats were divided into 2 groups: Normoglycemic and Diabetic. Each group was subdivided into negative control, glibenclamide 3 or 10 mg/kg, EAMI 125, 250, 500, and 1000 mg/kg. Intraperitoneal injection of streptozotocin 100 mg/kg was used to DM induction. The hypoglycemic response was assessed acutely after two and four weeks of treatment. After a 6-hour fasting period, the fasting blood glucose of animals was verified, and 2.5 g/kg glucose solution was orally administered. The insulin tolerance test and plasma insulin levels assessment were performed in the morning after fasting of 12 to 14 hours.

Results and conclusion

The chemical analysis of EAMI showed high levels of phenolic compounds. There was no significant difference in fasting blood glucose between normoglycemic and diabetic groups, and that EAMI did not have an acute effect on diabetes. After two and four weeks of treatment, the extract significantly reduced blood glucose levels, exceeding glibenclamide effects. EAMI was effective in maintaining the long-term hypoglycemic effect, as well as, significantly increased the sensitivity of diabetic animals to insulin and the plasma insulin level.

Klíčová slova:

Insulin – Blood plasma – Leaves – Glucose – Blood sugar – Hypoglycemics – Phenols – diabetes mellitus

Zdroje

1. International Diabetes Federation. Diabetes Atlas. In: 8th Edition [Internet]. 2017 [cited 15 Oct 2019]. Available: www.diabetesatlas.org

2. De la Fuente Coria MC, Cruz-Cobo C, Santi-Cano MJ. Effectiveness of a Primary Care Nurse Delivered Educational Intervention for Patients With Type 2 Diabetes Mellitus in Promoting Metabolic Control and Compliance With Long-Term Therapeutic Targets: Randomised Controlled Trial. Int J Nurs Stud. 2019; 1–24. doi: 10.1016/j.ijnurstu.2019.103417 31683226

3. ADA. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2014;37: 81–90. doi: 10.2337/dc13-1041 23959568

4. Deepa P, Sowndhararajan K, Kim S, Park SJ. A role of Ficus species in the management of diabetes mellitus: A review. J Ethnopharmacol. 2018;215: 210–232. doi: 10.1016/j.jep.2017.12.045 29305899

5. WHO. Definition and Diagnosis of Diabetes Mellitus and Intermediate Hyperglycemia. Geneva; 2006. ISBN 92 4 159493 4

6. Thomas CC, Philipson LH. Update on Diabetes Classification. Med Clin North Am. 2015;99: 1–16. doi: 10.1016/j.mcna.2014.08.015 25456640

7. Beidokhti MN, Jäger AK. Review of antidiabetic fruits, vegetables, beverages, oils and spices commonly consumed in the diet. J Ethnopharmacol. 2017;201: 26–41. doi: 10.1016/j.jep.2017.02.031 28257977

8. Kannadasan K, Edla DR, Kuppili V. Type 2 diabetes data classification using stacked autoencoders in deep neural networks. Clin Epidemiol Glob Heal. 2018; 2–7. doi: 10.1016/j.cegh.2018.12.004

9. Tao Z, Shi A, Zhao J. Epidemiological Perspectives of Diabetes. Cell Biochem Biophys. 2015;73: 181–185. doi: 10.1007/s12013-015-0598-4 25711186

10. Campbell IW, Howlett HCS. Worldwide Experience of Metformin as an Effective Glucose‐lowering Agent: A Meta‐analysis. Diabetes Metab Rev. 1995;11: S57–S62. doi: 10.1002/dmr.5610110509 8529486

11. Murad MH, Coto-Yglesias F, Wang AT, Sheidaee N, Mullan RJ, Elamin MB, et al. Drug-induced hypoglycemia: A systematic review. J Clin Endocrinol Metab. 2009;94: 741–745. doi: 10.1210/jc.2008-1416 19088166

12. Dhawan M, Agrawal R, Ravi J, Gulati S, Silverman J, Nathan G, et al. Rosiglitazone-induced granulomatous hepatitis. J Clin Gastroenterol. 2002;34: 582–584. doi: 10.1097/00004836-200205000-00021 11960075

13. Idris I, Gray S, Donnelly R. Rosiglitazone and pulmonary oedema: An acute dose-dependent effect on human endothelial cell permeability. Diabetologia. 2003;46: 288–290. doi: 10.1007/s00125-002-1008-1 12627329

14. Lalau JD, Westeel PF, Debussche X, Dkissi H, Tolani M, Coevoet B, et al. Bicarbonate haemodialysis: an adequate treatment for lactic acidosis in diabetics treated by metformin. Intensive Care Med. 1987;13: 383–387. doi: 10.1007/bf00257680 2822788

15. Lalau JD, Lacroix C, Compagnon P, Cagny B De, Rigaud JP, Bleichner G, et al. Role of Metformin Accumulation in Metformin-Associated Lactic Acidosis. Diabetes Care. 1995;18: 779–784. doi: 10.2337/diacare.18.6.779 7555503

16. Noor HSM, Ismail NH, Kasim N, Zohdi RM, Ali AM. Hypoglycemic and glucose tolerance activity of standardized extracts Ficus deltoidea varieties in normal rats. J Med Plants Stud. 2016;4: 275–279.

17. Sahoo N, Manchikanti P, Dey S. Herbal drugs: Standards and regulation. Fitoterapia. 2010;81: 462–471. doi: 10.1016/j.fitote.2010.02.001 20156530

18. Villas Boas GR, Araújo FS de, Marcelino JM, Castro LHA, Silveira APS, Nacer RS, et al. Preclinical safety evaluation of the ethanolic extract from Campomanesia pubescens (Mart. ex DC.) O.BERG (guavira) fruits: analysis of genotoxicity and clastogenic effects. Food Funct. 2018;9: 3707–3717. doi: 10.1039/c8fo01017j 29978171

19. Ojewole J. Anti-inflammatory, analgesic and hypoglycaemic effects of Mangifera indica Linn. (Anacardiaceae) stem-bark aqueous extract. Methods Find Exp Clin Pharmacol. 2005;27: 547–554. doi: 10.1358/mf.2005.27.8.928308 16273134

20. Madunagu BE, Ebana RUB, Ekpe ED. Antibacterial and antifungal activity of some medicinal plants of Akwa Ibom state. West African J Biol Appl Chem. 1990;35: 25–30.

21. Gill LS. Ethnomedical Uses of Plants in Nigeria. 1th ed. Benin, Nigeria: University of Benin Press; 1992.

22. Perpétuo GF, Salgado JM. Effect of mango (Mangifera indica, L.) ingestion on blood glucose levels of normal and diabetic rats. Plant Foods Hum Nutr. 2003;58: 1–12. doi: 10.1023/a:1024063105507

23. Muruganandan S, Srinivasan K, Gupta S, Gupta PK, Lal J. Effect of mangiferin on hyperglycemia and atherogenicity in streptozotocin diabetic rats. J Ethnopharmacol. 2005;97: 497–501. doi: 10.1016/j.jep.2004.12.010 15740886

24. Canuto KM. Propriedades Químicas e Farmacológicas de Mangiferina: Um Composto Bioativo de Manga (Mangifera indica L.). Petrolina: Embrapa; 2009. p. 29.

25. Saleem M, Tanvir M, Akhtar MF, Iqbal M, Saleem A. Antidiabetic Potential of Mangifera indica L. cv. Anwar Ratol Leaves: Medicinal Application of Food Wastes. Medicina (B Aires). 2019;55: 353. doi: 10.3390/medicina55070353 31323919

26. Samanta S, Chanda R, Reddy AG. Anti-diabetic activity of mango (Mangifera indica): a review. MOJ Bioequiv Availab. 2019;6: 23–26. doi: 10.15406/mojbb.2019.06.00131

27. Toledo RCL, Brito LF, Caetano MMM, Nakajima VM, da Silva BP, Soares FE de F, et al. Acute treatment with Mangifera indica L. leaf extract attenuates liver inflammation in rats fed a cafeteria diet. Food Funct. 2019;10: 4861–4867. doi: 10.1039/c9fo00651f 31334539

28. Alkizim FO, Matheka D, Abdulrahman FK, Muriithi A. Inhibitory effect of Mangifera indica on gastrointestinal motility. Med Chem Drug Discov. 2012;2: 9–16.

29. Ngo DH, Ngo DN, Vo TTN, Vo TS. Mechanism of action of mangifera indica leaves for anti-diabetic activity. Sci Pharm. 2019;87: 1–15. doi: 10.3390/scipharm87020013

30. Correia SDJ, David JP, David JM. Metabólitos secundários de espécies de anacardiaceae. Quim Nova. 2006;29: 1287–1300. doi: 10.1590/S0100-40422006000600026

31. Nwinuka NM, Monanu MO, Nwiloh BI. Effects of Aqueous Extract of Mangifera indica L. (Mango) Stem Bark on Haematological Parameters of Normal Albino Rats. Pakistan Jounal of Nutrition. 2008. pp. 663–666.

32. Ross IA. Medicinal Plants of the World: Chemical Constituents, Traditional and Modern Medicinal Uses. 1th ed. Totowa, New Jersey: Humana Press Inc; 1999. doi: 10.1007/978-1-59259-887-8

33. Barreto JC, Trevisan MTS, Hull WE, Erben G, De ES, Pfundstein B, et al. Characterization and Quantitation of Polyphenolic Compounds in Bark, Kernel, Leaves, and Peel of Mango (Mangifera indica L.). J Agric Food Chem. 2008;56: 5599–5610. doi: 10.1021/jf800738r 18558692

34. Aderibigbe AO, Emudianughe TS, Lawal BAS. Evaluation of the antidiabetic action of Mangifera indica in mice. Phyther Res. 2001;15: 456–458. doi: 10.1002/ptr.859 11507745

35. Aderibigbe AO, Emudianughe TS, Lawal BAS. Antihyperglycaemic effect of Mangifera indica in rat. Phyther Res. 1999;13: 504–507. doi: 10.1002/(SICI)1099-1573(199909)13:6<504::AID-PTR533>3.0.CO;2–9

36. Simões CMO, Schenkel EP, Gosmann G, Mello DJCP, Mentz LA, Petrovick PR. Farmacognosia: da planta ao medicamento. 6th ed. Porto Alegre: Editora da UFSC; 2010.

37. Ateyyat MA, Al-mazra M, Abu-rjai T, Shatnawi MA. Aqueous extracts of some medicinal plants are as toxic as Imidacloprid to the sweet potato whitefly, Bemisia tabaci. J Insect Sci. 2009;9: 2–7. doi: 10.1673/031.009.0201

38. Lin JY, Tang CY. Determination of total phenolic and flavonoid contents in selected fruits and vegetables, as well as their stimulatory effects on mouse splenocyte proliferation. Food Chem. 2007;101: 140–147. doi: 10.1016/j.foodchem.2006.01.014

39. Broadhurst RB, Jones WT. Analysis of condensed tannins using acidified vanillin. J Sci Food Agric. 1978;29: 788–794. doi: 10.1002/jsfa.2740290908

40. Agostini-Costa TS, Garruti DS, Lima L, Freire S, Abreu FAP, Feitosa T. Avaliação de metodologias para determinação de taninos no suco de caju. Bol CEPPA. 1999;17: 167–176.

41. Villas Boas GR, Santos AC dos, Souza RIC, Araújo FHS, Traesel GK, Marcelino JM, et al. Preclinical safety evaluation of the ethanolic extract from guavira fruits (Campomanesia pubescens (D.C.) O. BERG) in experimental models of acute and short-term toxicity in rats. Food Chem Toxicol. 2018;118: 1–12. doi: 10.1016/j.fct.2018.04.063 29723584

42. Agrawal PK. Carbon-13 NMR of Flavonoids. 1th ed. Amsterdam: Elsevier Science; 1989.

43. Byrne LT, Cannon JR, Gawad DH, Joshi BS, Skelton BW, Toia RF, et al. The crystal structure of (S)-(−)-6-Bromo-5,7-dihydroxy8-methyl-2-phenyl-2,3-dihydro-4H-1 benzopyran-4-one [(−)-6-bromocryptostrobin] and a 13C N.M.R. Study of (±)-cryptostrobin and related substances. Revision of the structures of the natural products (±). Aust J Chem. 1982;35: 1851–1858.

44. Mustafa K, Perry N, Weavers R. Lipophilic C-methylflavonoids with no B-ring oxygenation in Metrosideros species (Myrtaceae). Biochem Syst Ecol. 2005;33: 1049–1059.

45. Solladié G, Gehrold N, Maignan J. Biomimetic Synthesis of the Flavanone Leridol, Revision of the Structure of the Natural Product. European J Org Chem. 1999; 2309–2314. doi: 10.1002/(SICI)1099-0690(199909)1999:

46. Srivastava R, Shaw AK, Kulshreshtha DK. Triterpenoids and chalcone from Syzygium samarangense. Phytochemistry. 1995;38: 687–689. doi: 10.1016/0031-9422(94)00739-G

47. Xu S, Jiang B, Maitland KA, Bayat H, Gu J, Nadler JL, et al. The thromboxane receptor antagonist S18886 attenuates renal oxidant stress and proteinuria in diabetic apolipoprotein E-deficient mice. Diabetes. 2006;55: 110–119. doi: 10.2337/diabetes.55.1.110 16380483

48. Mathews JNS, Altman DG, Campbell MJ, Royston P. Analysis of serial measurements in medical research. Br Med J. 1990;27: 230–235.

49. Rees DA, Alcolado JC. Animal models of diabetes mellitus. Diabet Med. 2005;22: 359–70. doi: 10.1111/j.1464-5491.2005.01499.x 15787657

50. Madhuri AS, Mohanvelu R. Evaluation of Antidiabetic Activity of Aqueous Extract of Mangifera Indica Leaves in Alloxan Induced Diabetic Rats. Biomed Pharmacol J. 2017;10: 1029–1035.

51. Gondi M, Prasada-Rao UJS. Ethanol extract of mango (Mangifera indica L.) peel inhibits α-amylase and α-glucosidase activities, and ameliorates diabetes related biochemical parameters in streptozotocin (STZ)-induced diabetic rats. Journal of Food Science and Technology. 2015. pp. 7883–7893. doi: 10.1007/s13197-015-1963-4 26604360

52. Sagbo IJ, Venter M Van De, Koekemoer T, Bradley G. In Vitro Antidiabetic Activity and Mechanism of Action of Brachylaena elliptica (Thunb.) DC. Evidence-Based Complement Altern Med. 2018;2018: 13. doi: 10.1155/2018/4170372 30108655

53. Hanhineva K, Törrönen R, Bondia-pons I, Pekkinen J. Impact of Dietary Polyphenols on Carbohydrate Metabolism. Int J Mol Sci. 2010;11: 1365–1402. doi: 10.3390/ijms11041365 20480025

54. Aryaeian N, Sedehi SK, Arablou T. Polyphenols and their effects on diabetes management: A review. Med J Islam Repub Iran. 2017;31: 1–14. doi: 10.18869/mjiri.31.1

55. Tan C, Wang Q, Luo C, Chen S, Li Q, Li P. Yeast α-Glucosidase Inhibitory Phenolic Compounds Isolated from Gynura medica Leaf.pdf. Int J Mol Sci. 2013;14: 2551–2558. doi: 10.3390/ijms14022551 23358246

56. Yao Y, Cheng X, Wang L, Wang S, Ren G. Determination of potential α-glucosidase inhibitors from azuki beans.pdf. Int J Mol Sci2. 2011;12: 6445–6451. doi: 10.3390/ijms12106445 22072898

57. Bhandari MR, Jong-Anurakkun N, Hong G, Kawabata J. α-Glucosidase and α-amylase inhibitory activities of Nepalese medicinal herb Pakhanbhed.pdf. Food Chem. 2008;106: 247–252. doi: 10.1016/j.foodchem.2007.05.077

58. Suh Y, Afaq F, Khan N, Johnson JJ, Khusro FH, Mukhtar H. Fisetin induces autophagic cell death through suppression of mTOR signaling pathway in prostate cancer cells. Carcinogenesis. 2010;31: 1424–1433. doi: 10.1093/carcin/bgq115 20530556

59. Fotsis T, Pepper MS, Montesano R, Aktas E, Breit S, Schweigerer L, et al. 7Phytoestrogens and inhibition of angiogenesis. Baillieres Clin Endocrinol Metab. 1998;12: 649–666. doi: 10.1016/s0950-351x(98)80009-8 10384818

60. Cheong H, Ryu SY, Oak MH, Cheon SH, Yoo GS, Kim KM. Studies of structure activity relationship of flavonoids for the anti-allergic actions. Arch Pharm Res. 1998;21: 478–480. doi: 10.1007/bf02974647 9875480

61. Divi RL, Doerge DR. Inhibition of thyroid peroxidase by dietary flavonoids. Chem Res Toxicol. 1996;9: 16–23. doi: 10.1021/tx950076m 8924586

62. Constantin RP, Constantin J, Pagadigorria CLS, Ishii-Iwamoto EL, Bracht A, De Kássia Cardoso Ono M, et al. The actions of fisetin on glucose metabolism in the rat liver. Cell Biochem Funct. 2010;28: 149–158. doi: 10.1002/cbf.1635 20084677

63. Prasath GS, Subramanian SP. Fisetin, A bioflavonoid ameliorates hyperglycemia in STZ-induced experimental diabetes in rats. Int J Pharm Sci Rev Res. 2011;6: 68–74.

64. Prasath GS, Subramanian SP. Modulatory effects of fisetin, a bioflavonoid, on hyperglycemia by attenuating the key enzymes of carbohydrate metabolism in hepatic and renal tissues in streptozotocin-induced diabetic rats. Eur J Pharmacol. 2011;668: 492–496. doi: 10.1016/j.ejphar.2011.07.021 21816145

65. Aloud AA, Chinnadurai V, Govindasamy C, Alsaif MA, Al-Numair KS. Galangin, a dietary flavonoid, ameliorates hyperglycaemia and lipid abnormalities in rats with streptozotocin-induced hyperglycaemia. Pharm Biol. 2018;56: 302–308. doi: 10.1080/13880209.2018.1474931 29952676

66. Aloud AA, Veeramani C, Govindasamy C, Alsaif MA, El Newehy AS, Al-Numair KS. Galangin, a dietary flavonoid, improves antioxidant status and reduces hyperglycemia-mediated oxidative stress in streptozotocin-induced diabetic rats. Redox Rep. 2017;22: 290–300. doi: 10.1080/13510002.2016.1273437 28030991

67. Ramírez-Espinosa JJ, Salda a-Ríos J, García-Jiménez S, Villalobos-Molina R, Ávila-Villarreal G, Rodríguez-Ocampo AN, et al. Chrysin induces antidiabetic, antidyslipidemic and anti-inflammatory effects in athymic nude diabetic mice. Molecules. 2018;23: 2–9. doi: 10.3390/molecules23010067 29283418

68. Zang Y, Igarashi K, Li Y. Anti-diabetic effects of luteolin and luteolin-7- O -glucoside on KK- A y mice. Biosci Biotechnol Biochem. 2016;80: 1580–1586. doi: 10.1080/09168451.2015.1116928 27170065

69. Luzi L, Pozza G. Glibenclamide: An old drug with a novel mechanism of action? Acta Diabetol. 1997;34: 239–244. doi: 10.1007/s005920050081 9451465

70. Reaven GM. Role of insulin resistance in human disease. Diabetes. 1988;37: 1595–1607. doi: 10.2337/diab.37.12.1595 3056758

71. DeFronzo RA. Pathogenesis of non-insulin-dependent diabetes mellitus. Diabetologia. 1992;35: 389––97. doi: 10.1007/bf00401208 1516769

72. Yki-Järvinen H, Koivisto VAV. Natural Course of Insulin Resistance in Type I Diabetes. N Engl J Med. 1986;315: 224–230. doi: 10.1056/NEJM198607243150404 3523247

73. Luzi L, Barrett EJ, Groop LC, Ferrannini E, Defronzo RA. Metabolic Effects of Low-Dose Insulin Therapy on Glucose Metabolism in Diabetic Ketoacidosis. Diabetes. 1988;37: 1470–7. doi: 10.2337/diab.37.11.1470 3141236

74. Bonadonna RC, Leif G, Kraemer N, Ferrannini E, Prato S Del, DeFronzo RA. Obesity and insulin resistance in humans: A dose-response study. Metabolism. 1990;39: 452–459. doi: 10.1016/0026-0495(90)90002-t 2186255

75. Kissebah AH. Insulin resistance in visceral obesity. Int J Obes. 1991;15: 109–15. 1794931

76. Geloneze BN, Tambascia MA. Avaliação laboratorial e diagnóstico da resistência insulínica. Atheros. 2002;13: 42–49.

77. Rizza R a., Cryer PE, Gerich JE. Role of Glucagon, Catecholamines, and Growth Hormone in Human Glucose Counterregulation. Effects of somatostatin and combined alfa and beta adrenergic blockade on plasma glucose recovery and glucose flux rates after insulin-induced hypoglycemia. J Clin Invest. 1979;64: 62–71. doi: 10.1172/JCI109464 36413

78. Bonora E, Moghetti P, Zancanaro C, Cigolini M, Querena M, Cacciatori V, et al. Estimates of Insulin action in Man: Comparison of insulin tolerance test with euglycaemic and hyperglycaemic clamp studies. J Clin Endocrinol Metab. 1989;68: 374–378. doi: 10.1210/jcem-68-2-374 2645308

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