Beneficial effects of Hibiscus rosa-sinensis L. flower aqueous extract in pregnant rats with diabetes

PLoS ONE

Volumn 12, Issue 6, 2017, Pages

  Afiune, Luana Alves Freitas ^a   Leal Silva, Thaís ^a   Sinzato, Yuri Karen ^b   Moraes Souza, Rafaianne Queiroz ^a,b   Soares, Thaigra Sousa ^a,b   Campos, Kleber Eduardo ^a   Fujiwara, Ricardo Toshio ^c   Herrera, Emilio ^d   Damasceno, Débora Cristina ^b   Volpato, Gustavo Tadeu ^a,b  

^a FEDERAL UNIVERSITY OF MATO GROSSO   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^d UNIVERSIDAD SAN PABLO CEU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIDIABETIC AGENT; HIBISCUS ROSA SINENSIS EXTRACT; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; PLANT EXTRACT; UNCLASSIFIED DRUG; WATER;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDIABETIC ACTIVITY; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIABETES MELLITUS; DOSE RESPONSE; DRUG DOSE INCREASE; DRUG EFFECT; DRUG SCREENING; EMBRYO; FEMALE; FETUS WEIGHT; FLOWER; MOTHER FETUS RELATIONSHIP; NONHUMAN; PREGNANCY; PREIMPLANTATION EMBRYO; PROGENY; RAT; ANIMAL; BLOOD; CHEMISTRY; DIABETES MELLITUS, EXPERIMENTAL; DIABETES, GESTATIONAL; DRUG EFFECTS; HIBISCUS; ORAL DRUG ADMINISTRATION; OXIDATIVE STRESS; PHYSIOLOGY; PHYTOTHERAPY; PRECLINICAL STUDY; PREGNANCY OUTCOME; RANDOMIZATION; WISTAR RAT;

ADMINISTRATION, ORAL; ANIMALS; CHOLESTEROL, HDL; DIABETES MELLITUS, EXPERIMENTAL; DIABETES, GESTATIONAL; DRUG EVALUATION, PRECLINICAL; FEMALE; FLOWERS; HIBISCUS; HYPOGLYCEMIC AGENTS; OXIDATIVE STRESS; PHYTOTHERAPY; PLANT EXTRACTS; PREGNANCY; PREGNANCY OUTCOME; RANDOM ALLOCATION; RATS, WISTAR; WATER;

EID: 85021287173     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0179785     Document Type: Article

References (55)

1. Damasceno DC, Volpato GT Antidiabetic botanical extracts. In: Watson RR, Preedy VR editors. Botanical Medicine in Clinical Practice. CAB International, London; 2008. pp. 547-551.
2. Nayak D, Ashe S, Rauta PR, Nayak B. Biosynthesis, characterisation and antimicrobial activity of silver nanoparticles using Hibiscus rosa-sinensis petals extracts. IET Nanobiotechnol. 2015; 9: 288-293. https://doi.org/10.1049/iet-nbt.2014.0047 PMID: 26435282
3. Ruban P, Gajalakshmi K. In vitro antibacterial activity of Hibiscus rosa-sinensis flower extract against human pathogens. Asian Pac J Trop Biomed. 2012; 2: 399-403. https://doi.org/10.1016/S2221-1691(12)60064-1 PMID: 23569938
4. Bhaskar A, Nithya V. Evaluation of the wound-healing activity of Hibiscus rosa sinensis L (Malvaceae) in Wistar albino rats. Indian J Pharmacol. 2012; 44: 694-698. https://doi.org/10.4103/0253-7613.103252 PMID: 23248396
5. Shivananda Nayak B, Sivachandra Raju S, Orette FA, Chalapathi Rao AV. Effects of Hibiscus rosa sinensis L (Malvaceae) on wound healing activity: a preclinical study in a Sprague Dawley rat. Int J Low Extrem Wounds. 2007; 6: 76-81. https://doi.org/10.1177/1534734607302840 PMID: 17558005
6. Khalid L, Rizwani GH, Sultana V, Zahid H, Khursheed R, Shareef H. Antidepressant activity of ethanolic extract of Hibiscus rosa sinenesis Linn. Pak J Pharm Sci. 2014; 27: 1327-1331. PMID: 25176367
7. Shewale PB, Patil RA, Hiray YA. Antidepressant-like activity of anthocyanidins from Hibiscus rosasinensis flowers in tail suspension test and forced swim test. Indian J Pharmacol. 2012; 44: 454-457. https://doi.org/10.4103/0253-7613.99303 PMID: 23087504
8. Gauthaman KK, Saleem MT, Thanislas PT, Prabhu V, Krishnamoorthy KK, Devaraj NS. Cardioprotective effect of the Hibiscus rosa sinensis flowers in an oxidative stress model of myocardial ischemic reperfusion injury in rat. BMC Complement Altern Med. 2006; 6: 32-39. https://doi.org/10.1186/1472-6882-6-32 PMID: 16987414
9. Masaki HS, Sakaki S, Atsumi T, Sakurai H. Active oxygen scavenging activity of plant extracts. Biol Pharm Bull. 1995; 18: 162-166. https://doi.org/10.1248/bpb.18.162 PMID: 7735233
10. Damasceno DC, Sinzato YK, Lima PH, Souza MSS, Volpato GT, Campos KE, et al. Effects of exposure to cigarette smoke prior to pregnancy in diabetic rats. Diabetol Metab Syndr. 2011; 3: 20. https://doi.org/10.1186/1758-5996-3-20 PMID: 21851636
11. Sinzato YK, Volpato GT, Iessi IL, Bueno A, Calderon IM, Rudge MV, et al. Neonatally induced mild diabetes in rats and its effect on maternal, placental, and fetal parameters. Exp Diabetes Res. 2012; 2012: 108-163. https://doi.org/10.1155/2012/108163 PMID: 22778712
12. Volpato GT, Damasceno DC, Sinzato YK, Ribeiro VM, Rudge MV, Calderon IM. Oxidative stress status and placental implications in diabetic rats undergoing swimming exercise after embryonic implantation. Reprod Sci. 2015; 22: 602-608. https://doi.org/10.1177/1933719114556485 PMID: 25361551
13. Consonni M, Damasceno DC, Kempinas WG, Nassr ACC, Volpato GT, Dallaqua B, et al. Effect of oral supplementation of the linoleic and gammalinolenic acids on the diabetic pregnant rats. Braz Arch Biol Technol. 2012; 55: 695-703. https://doi.org/10.1590/S1516-89132012000500008
14. Volpato GT, Damasceno DC, Rudge MVC, Padovani CR, Calderon IMP. Effect of Bauhinia forficata aqueous extract on the maternal-fetal outcome and oxidative stress biomarkers of streptozotocin-induced diabetic rats. J Ethnopharmacol. 2008; 116: 131-137. https://doi.org/10.1016/j.jep.2007.11.013 PMID: 18155864
15. Bhaskar A, Nithya V, Vidhya VG. Phytochemical screening and in vitro antioxidant activities of the ethanolic extract of Hibiscus rosa-sinensis. Ann Biol Res. 2011; 2: 653-661.
16. Moqbel FS, Naik PR, Najma HM, Selvaraj S. Antidiabetic properties of Hibiscus rosa sinensis L. leaf extract fractions on nonobese diabetic (NOD) mouse. Indian J Exp Biol. 2011; 49: 24-29. PMID: 21365992
17. Pillai SS, Mini S. Hibiscus rosa sinensis Linn. petals modulates glycogen metabolism and glucose homeostasis signalling pathway in streptozotocin-induced experimental diabetes. Plant Foods Hum Nutr. 2016; 71: 42-48. https://doi.org/10.1007/s11130-015-0521-6 PMID: 26590603
18. Sachdewa A, Khemani LD. Effect of Hibiscus rosa sinensis Linn. ethanol flower extract on blood glucose and lipid profile in streptozotocin induced diabetes in rats. J Ethnopharmacol. 2003; 89: 61-66. https://doi.org/10.1016/S0378-8741(03)00230-7 PMID: 14522433
19. Sachdewa A, Nigam R, Khemani LD. Hypoglycemic effect of Hibiscus rosa sinensis L. leaf extract in glucose and streptozotocin induced hyperglycemic rats. Indian J Exp Biol. 2001; 39: 284-286. PMID: 11495291
20. Volpato GT, Moraes-Souza RQ, Soares TS, Leal-Silva T, Damasceno DC. Medicinal plants for diabetes treatment during pregnancy. Curr Med Chem. 2017; 24: 404-410. https://doi.org/10.2174/0929867323666161003122914 PMID: 27697077
21. Pinheiro MS, Rodrigues LS, Neto LS, Moraes-Souza RQ, Soares TS, et al. Effect of Bauhinia holophylla treatment in Streptozotocin-induced diabetic rats. An Acad Bras Cienc. 2017; 89: 263-272. https://doi.org/10.1590/0001-3765201720160050 PMID: 28225851
22. Salewski E. Farbemethode zum markroskopishen nachweis von implantatconsstellen an uterus der ratter naunyn schmuderbergs. Arch. Pharmacol. (Weinheim). 1964; 247: 367. https://doi.org/10.1007/BF02308461
23. Damasceno DC, Kempinas WG, Volpato GT, Consoni M, Rudge MVC, Paumgartten FJR. Anomalias Congênitas: Estudos Experimentais. Coopmed, Belo Horizonte; 2008.
24. Damasceno DC, Silva HP, Vaz GF, Vasques-Silva FA, Calderon IM, Rudge MV, et al. Diabetic rats exercised prior to and during pregnancy: maternal reproductive outcome, biochemical profile, and frequency of fetal anomalies. Reprod Sci. 2013; 20: 730-738. https://doi.org/10.1177/1933719112461186 PMID: 23171681
25. Wilson JG. Methods for administering agents and detecting malformations in experimental animal. In: Wilson JG, Warkany J editors. Teratology: Principles and Techniques. University of Chicago Press, Chicago; 1965. pp. 47-74.
26. Staples RE, Schnell VL. Refinements in rapid clearing technique in the KOH-alizarin red S method for fetal bone. Stain Technol. 1964; 39: 61-63. PMID: 14106473
27. Young D.S. Effects of drugs on clinical laboratory tests. AACC Press, London; 2000.
28. Knopfholz J, Disserol CC, Pierin AJ, Schirr FL, Streisky L, Takito LL, et al. Validation of the friedewald formula in patients with metabolic syndrome. Cholesterol. 2014; 2014: 261-878. https://doi.org/10.1155/2014/261878 PMID: 24672715
29. Liu CS, Lin CC, Li TC. The relation of white blood cell count and atherogenic index ratio of LDL-cholesterol to HDL-cholesterol in Taiwan school children. Acta Paediatr Taiwan. 1999; 40: 319-324. PMID: 10910541
30. Boers M, Nurmohamed MT, Doelman CJ, Lard LR, Verhoeven AC, Voskuyl AE, et al. Influence of glucocorticoids and disease activity on total and high density lipoprotein cholesterol in patients with rheumatoid arthritis. Ann Rheumatic Dis. 2003; 62: 842-845. https://doi.org/10.1136/ard.62.9.842 PMID: 12922956
31. Aebi H. Catalase in vitro. Meth Enzymol. 1984; 105: 121-126. https://doi.org/10.1016/S0076-6879(84)05016-3 PMID: 6727660
32. Jollow DJ, Mitchel JR, Zamppaglione Z, Gillette JR. Bromobenzene induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolites. Pharmacol. 1974; 11: 51-57. https://doi.org/10.1159/000136485
33. Venkatesh S, Thilagavathi J, Shyam Sundar D. Antidiabetic activity of flowers of Hibiscus rosa sinensis. Fitoterapia. 2008; 79: 79-81. https://doi.org/10.1016/j.fitote.2007.06.015 PMID: 17850989
34. Kahn CR, Weir GC, King GL, Jacobson AM, Moses AC, Smith RT. Joslin's Diabetes mellitus. Lippincott Williams & Wilkans, Philadelphia; 2004.
35. Luciani MF, Denizot F, Savary S, Mattei MG, Chimini G. Cloning of two novel ABC transporters mapping on human chromosome 9. Genomics. 1994; 21: 150-159. https://doi.org/10.1006/geno.1994.1237 PMID: 8088782
36. Rader DJ. Mechanisms of disease: HDL metabolism as a target for novel therapies. Nat Clin Pract Cardiovasc Med. 2007; 4:102-109. https://doi.org/10.1038/ncpcardio0768 PMID: 17245404
37. Tall AR. Cholesterol efflux pathways and other potential mechanisms involved in the athero-protective effect of high density lipoproteins. J Intern Med. 2008; 263: 256-273. https://doi.org/10.1111/j.1365-2796.2007.01898.x PMID: 18271871
38. Guérin M, Le Goff W, Lassel TS, Van Tol A, Steiner G, Chapman MJ. Proatherogenic role of elevated CE transfer from HDL to VLDL1 and dense LDL in type 2 diabetes. Arterioscler Thromb Vasc Biol. 2001; 21: 282-289. https://doi.org/10.1161/01.ATV.21.2.282 PMID: 11156866
39. Hokanson JE, Austin MA. Plasma triglyceride level is a risk factor to cardiovascular disease independent of high-density lipoprotein cholesterol level: a meta-analysis of population based prospective studies. J Cardiovasc Risk. 1996; 3: 213-219. https://doi.org/10.1177/174182679600300214 PMID: 8836866
40. Dobiásová M. Atherogenic index of plasma [log(triglycerides/HDL-cholesterol)]: theoretical and practical implications. Clin Chem. 2004; 50: 1113-1115. https://doi.org/10.1373/clinchem.2004.033175 PMID: 15229146
41. Murakami T, Michelagnoli S, Longhi R, Gianfranceschini G, Pazzucconi F, Calabresi L, et al. Triglycerides are major determinants of cholesterol esterification/transfer and HDL remodeling in human plasma. Arterioscler Thromb Vasc Biol. 1995; 15: 1819-1828. 0.1161/01.ATV.15.11.1819 PMID: 7583561
42. Mak YW, Chuah LO, Ahmad R, Bhat R. Antioxidant and antibacterial activities of hibiscus (Hibiscus rosa-sinensis L.) and Cassia (Senna bicapsualris L.) flower extracts. J King Saud Univ Sci. 2013; 25: 275-282. https://doi.org/10.1016/j.jksus.2012.003
43. Zhu Y, Huang X, Zhang Y, Wang Y, Liu Y, Sun R, et al. Anthocyanin supplementation improves HDL-associated paraoxonase 1 activity and enhances cholesterol efflux capacity in subjects with hypercholesterolemia. J Clin Endocrinol Metab. 2014; 99: 561-569. https://doi.org/10.1210/jc.2013-2845 PMID: 24285687
44. Qin Y, Xia M, Ma J, Hao YT, Liu J, Mou HY, et al. Anthocyanin supplementation improves serum LDL-and HDL-cholesterol concentrations associated with the inhibition of cholesteryl ester transfer protein in dyslipidemic subjects. Am J Clin Nutr. 2009; 90: 485-492. https://doi.org/10.3945/ajcn.2009.27814 PMID: 19640950
45. Volpato GT, Calderon IMP, Sinzato S, Campos KE, Rudge MVC, Damasceno DC. Effect of Morus nigra aqueous extracttreatment on the maternal-fetal outcome, oxidative stress status and lipid profile of streptozotocin-induced diabetic rats. J Ethnopharmacol. 2011; 138: 691-696. https://doi.org/10.1016/j.jep.2011.09.044 PMID: 21986227
46. Damasceno DC, Volpato GT, Calderon IMP, Rudge MVC. Oxidative stress and diabetes in pregnant rats. Anim Reprod Sci. 2002; 72: 235-244. https://doi.org/10.1016/S0378-4320(02)00094-5 PMID: 12137985
47. Eriksson UJ, Cederberg J, Wentzel P. Congenital malformations in offspring of diabetic mothers-animal and human studies. Rev Endocr Metab Disord. 2003; 4: 79-93. https://doi.org/10.1023/A:1021879504372 PMID: 12618562
48. Ajiboye TO, Salawu NA, Yakubu MT, Oladiji AT, Akanji MA, Okogun JI. Antioxidant and drug detoxification potentials of Hibiscus sabdariffa anthocyanin extract. Drug Chem Toxicol. 2011; 34: 109-115. https://doi.org/10.3109/01480545.2010.536767 PMID: 21314460
49. Da-Costa-Rocha I, Bonnlaender B, Sievers H, Pischel I, Heinrich M. Hibiscus sabdariffa L. - a phytochemical and pharmacological review. Food Chem. 2014; 165: 424-443. https://doi.org/10.1016/j.foodchem.2014.05.002 PMID: 25038696
50. Fernández-Arroyo S, Rodríguez-Medina IC, Beltrán-Debón R, Pasini F, Joven J, Micol V, et al. Quantification of the polyphenolic fraction and in vitro antioxidant and in vivo anti-hyperlipemic activities of Hibiscus sabdariffa aqueous extract. Foof Res Int. 2011; 44: 1490-1495. https://doi.org/10.2016/j.foodres.2011.03.040
51. Kholkute SD, Udupa KN. Effects of Hibiscus rosa sinensis on pregnancy of rats. Planta Med. 1976; 26: 321-329. https://doi.org/10.1055/s-0028-1097671 PMID: 959372
52. Pal AK, Bhattacharya K, Kabir SN, Pakrashi A. Flowers of Hibiscus rosa sinensis, a potential source of contragestive agent II. Possible mode of action with reference to antiimplantation effect of benzene extract. Contraception. 1985; 32: 517-529. https://doi.org/10.1016/0010-7824(85)90021-6 PMID: 4085250
53. Singh MP, Singh RH, Udupa KN. Antifertility activity of a benzene extract of Hibiscus rosa sinensis flowers in female albino rats. Planta Med. 1982; 44: 171-174. https://doi.org/10.1055/s-2007-971433 PMID: 7089096
54. Murthy DR, Reddy CM, Patil SB. Effect of benzene extract of Hibiscus rosa-sinensis on the estrous cycle and ovarian activity in albino mice. Biol Pharm Bull. 1997; 20: 756-758. https://doi.org/10.1248/bpb.20.756 PMID: 9255415
55. Vasudeva N, Sharma SK. Post-coital antifertility activity of Hibiscus rosa-sinensis Linn. roots. Evid Based Complement Alternat Med. 2008; 5: 91-94. https://doi.org/10.1093/ecam/nem003 PMID: 18317554