Hostname: page-component-77c89778f8-sh8wx Total loading time: 0 Render date: 2024-07-17T11:19:12.379Z Has data issue: false hasContentIssue false
  • English
  • Français

The response of male and female rats to a high-fructose diet during adolescence following early administration of Hibiscus sabdariffa aqueous calyx extracts

Published online by Cambridge University Press:  19 June 2017

K. G. Ibrahim ,
E. Chivandi ,
F. B. O. Mojiminiyi  and
K. H. Erlwanger
K. G. Ibrahim*
Affiliation:
School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa Department of Physiology, College of Health Sciences, Usmanu Danfodiyo University, Sokoto, Nigeria
E. Chivandi
Affiliation:
School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
F. B. O. Mojiminiyi
Affiliation:
Department of Physiology, College of Health Sciences, Usmanu Danfodiyo University, Sokoto, Nigeria
K. H. Erlwanger
Affiliation:
School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
*
*Address for correspondence: K. G. Ibrahim, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, 7 York Road, Parktown, Johannesburg, 2193, South Africa. (Email ghandi.kasimu@udusok.edu.ng)
Get access Rights & Permissions [Opens in a new window]

Abstract

Metabolic syndrome is linked to the consumption of fructose-rich diets. Nutritional and pharmacological interventions perinatally can cause epigenetic changes that programme an individual to predispose or protect them from the development of metabolic diseases later. Hibiscus sabdariffa (HS) reportedly has anti-obesity and hypocholesterolaemic properties in adults. We investigated the impact of neonatal intake of HS on the programming of metabolism by fructose. A total of 85 4-day-old Sprague Dawley rats were divided randomly into three groups. The control group (n=27, 12 males, 15 females) received distilled water at 10 ml/kg body weight. The other groups received either 50 mg/kg (n=30, 13 males, 17 females) or 500 mg/kg (n=28, 11 males, 17 females) of an HS aqueous calyx extract orally till postnatal day (PND) 14. There was no intervention from PND 14 to PND 21 when the pups were weaned. The rats in each group were then divided into two groups; one continued on a normal diet and the other received fructose (20% w/v) in their drinking water for 30 days. The female rats that were administered with HS aqueous calyx extract as neonates were protected against fructose-induced hypertriglyceridaemia and increased liver lipid deposition. The early administration of HS resulted in a significant (P⩽0.05) increase in plasma cholesterol concentrations with or without a secondary fructose insult. In males, HS prevented the development of fructose-induced hypercholesterolaemia. The potential beneficial and detrimental effects of neonatal HS administration on the programming of metabolism in rats need to be considered in the long-term well-being of children.

Keywords

dyslipidaemiafructoseHibiscus sabdariffametabolic syndromeneonate
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 6 , December 2017 , pp. 628 - 637
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

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

1. Armitage, JA, Khan, IY, Taylor, PD, Nathanielsz, PW, Poston, L. Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J Physiol. 2004; 561, 355–377.CrossRefGoogle ScholarPubMed
2. Ebbeling, CB, Pawlak, DB, Ludwig, DS. Childhood obesity: public-health crisis, common sense cure. Lancet. 2002; 360, 473–482.Google Scholar
3. Gluckman, PD, Hanson, MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab. 2004; 15, 183–187.Google Scholar
4. Hales, CN, Barker, DJ. The thrifty phenotype hypothesis. Br Med Bull. 2001; 60, 5–20.CrossRefGoogle ScholarPubMed
5. Osmond, C, Barker, D, Winter, P, Fall, C, Simmonds, S. Early growth and death from cardiovascular disease in women. BMJ. 1993; 307, 1519–1524.Google Scholar
6. Hales, CN, Barker, DJP. Type 2 (noninsulin dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595–601.Google Scholar
7. Moura, EG, Passos, MC. Neonatal programming of body weight regulation and energetic metabolism. Biosci Rep. 2005; 25, 251–269.Google Scholar
8. Rooney, K, Ozanne, S. Maternal over-nutrition and offspring obesity predisposition: targets for preventative interventions. Int J Obes. 2011; 35, 883–890.Google Scholar
9. Alfaradhi, M, Ozanne, S. Developmental programming in response to maternal overnutrition. Front Genet. 2011; 2, 27.Google Scholar
10. Armitage, JA, Taylor, PD, Poston, L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol. 2005; 565, 3–8.CrossRefGoogle Scholar
11. Scarpellini, E, Campanale, M, Leone, D, et al. Gut microbiota and obesity. Intern Emerg Med. 2010; 5, 53–56.Google Scholar
12. Schmidt, I, Fritz, A, Schölch, C, et al. The effect of leptin treatment on the development of obesity in overfed suckling Wistar rats. Int J Obes Relat Metab Disord. 2001; 25, 1168–1174.Google Scholar
13. Khan, IY, Dekou, V, Douglas, G, et al. A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R127–R133.CrossRefGoogle ScholarPubMed
14. Pico, C, Oliver, P, Sanchez, J, et al. The intake of physiological doses of leptin during lactation in rats prevents obesity in later life. Int J Obes. 2007; 31, 1199–1209.Google Scholar
15. Kelishadi, R, Mansourian, M, Heidari-Beni, M. Association of fructose consumption and components of metabolic syndrome in human studies: a systematic review and meta-analysis. Nutrition. 2014; 30, 503–510.Google Scholar
16. Angelova, P, Boyadjiev, N. A review on the models of obesity and metabolic syndrome in rats. Trak J Sci. 2013; 11, 5–12.Google Scholar
17. Abdulla, MH, Sattar, MA, Johns, EJ. The relation between fructose-induced metabolic syndrome and altered renal haemodynamic and excretory function in the rat. Int J Nephrol. 2011; 2011, 1–17.Google Scholar
18. de Moura, RF, Ribeiro, C, de Oliveira, JA, Stevanato, E, de Mello, MAR. Metabolic syndrome signs in Wistar rats submitted to different high-fructose ingestion protocols. Br J Nutr. 2009; 101, 1178–1184.Google Scholar
19. Busserolles, J, Mazur, A, Gueux, E, Rock, E, Rayssiguier, Y. Metabolic syndrome in the rat: females are protected against the pro-oxidant effect of a high sucrose diet. Exp Biol Med. 2002; 227, 837–842.Google Scholar
20. Galipeau, D, Verma, S, McNeill, JH. Female rats are protected against fructose-induced changes in metabolism and blood pressure. Am J Physiol Heart Circ Physiol. 2002; 283, H2478–H2484.Google Scholar
21. Korićanac, G, Đorđević, A, Žakula, Z, et al. Gender modulates development of the metabolic syndrome phenotype in fructose-fed rats. Arch Bio Sci. 2013; 65, 455–464.CrossRefGoogle Scholar
22. Teff, KL, Elliott, SS, Tschöp, M, et al. Dietary fructose reduces circulating insulin and leptin, attenuates postprandial suppression of ghrelin, and increases triglycerides in women. J Clin Endocrinol Metab. 2004; 89, 2963–2972.Google Scholar
23. Mahadevan, N, Shivali, KP, Kamboj, P. Hibiscus sabdariffa Linn: an overview. Nat Prod Rad. 2009; 8, 77–83.Google Scholar
24. Mojiminiyi, FBO, Audu, Z, Etuk, EU, et al. Attenuation of salt-induced hypertension by aqueous calyx extract of Hibiscus Sabdariffa . Niger J Physiol Sci. 2012; 2, 195–200.Google Scholar
25. Alarcon-Aguilar, FJ, Zamilpa, A, Perez-Garcia, MD, et al. Effects of Hibiscus sabdariffa on obeisity in MSG mice. J Ethnopharmacol. 2007; 114, 66–71.Google Scholar
26. Da-Costa-Rocha, I, Bonnlaender, B, Sievers, H, et al. Hibiscus sabdariffa L. – a phytochemical and pharmacological review. Food Chem. 2014; 165, 424–443.Google Scholar
27. Patel, S. Hibiscus sabdariffa: an ideal yet under-exploited candidate for nutraceutical applications. Biomed Prev Nutr. 2014; 4, 23–27.Google Scholar
28. Kim, J-K, So, H, Youn, M-J, et al. Hibiscus sabdariffa L. water extract inhibits the adipocyte differentiation through the PI3-K and MAPK pathway. J Ethnopharmacol. 2007; 114, 260–267.Google Scholar
29. Carvajal-Zarrabal, O, Hayward-Jones, P, Orta-Flores, Z, et al. Effect of Hibiscus sabdariffa L. dried calyx ethanol extract on fat absorption-excretion, and body weight implication in rats. Biomed Res Int. 2009; 2009, 5.Google ScholarPubMed
30. Onyenekwe, PC, Ajani, EO, Ameh, DA, Gamaliel, KS. Antihypertensive effect of roselle (Hibiscus sabdariffa) calyx infusion in SHR and a comparism of its toxicity with that in Wistar rats. Cell Biochem Funct. 1999; 17, 199–206.3.0.CO;2-2>CrossRefGoogle Scholar
31. Mojiminiyi, FBO, Dikko, M, Muhammad, BY, et al. Antihypertensive effect of an aqueous extract of the calyx of Hibiscus sabdariffa . Fitoterapia. 2007; 78, 292–297.Google Scholar
32. Peng, C-H, Chyau, C-C, Chan, K-C, et al. Hibiscus sabdariffa polyphenolic extract inhibits hyperglycemia, hyperlipidemia, and glycation-oxidative stress while improving insulin resistance. J Agric Food Chem. 2011; 59, 9901–9909.CrossRefGoogle ScholarPubMed
33. Adisakwattana, S, Ruengsamran, T, Kampa, P, Sompong, W. In vitro inhibitory effects of plant-based foods and their combinations on intestinal alpha-glucosidase and pancreatic alpha-amylase. BMC Complement Altern Med. 2012; 12, 110.Google Scholar
34. Lin, T-L, Lin, H-H, Chen, C-C, et al. Hibiscus sabdariffa extract reduces serum cholesterol in men and women. Nutr Res. 2007; 27, 140–145.Google Scholar
35. Gurrola-Daiz, CM, Garcia-Lopez, PM, Sanchez Enriquez, S, et al. Effects of Hibiscus sabdariffa powder and preventive treatment (diet) on the lipid profiles of patients with metabolic syndrome. Phytomedicine. 2010; 17, 500–505.Google Scholar
36. Tseng, T-H, Hsu, J-D, Lo, M-H, et al. Inhibitory effects of Hibiscus protocatechuic acid on tumour promotion in mouse skin. Cancer Lett. 1998; 126, 199–207.Google Scholar
37. Gaya, I, Mohammad, O, Suleiman, A, Maje, M, Adekunle, A. Toxicological and lactogenic studies on the seeds of Hibiscus sabdariffa linn (Malvaceae) extract on serum prolactin levels of albino wistar rats. Internet J Endocrinol. 2009; 5, 6.Google Scholar
38. Ndu, OO, Nworu, CS, Ehiemere, CO, Ndukwe, NC, Ochiogu, IS. Herb–drug interaction between the extract of Hibiscus sabdariffa L. and hydrochlorothiazide in experimental animals. J Med Food. 2011; 14, 640–644.Google Scholar
39. Dangarembizi, R, Erlwanger, KH, Chivandi, E. Effects of Ficus thonningii extracts on the gastrointestinal tract and clinical biochemistry of suckling rats. Afr J Tradit Complement Altern Med. 2014; 11, 285–291.CrossRefGoogle ScholarPubMed
40. Ali, BH, Mousa, HM, El-Mougy, S. The effect of a water extract and anthocyanins of Hibiscus sabdariffa L. on paracetamol-induced hepatoxicity in rats. Phytother Res. 2003; 17, 56–59.Google Scholar
41. Chaturvedi, P, George, S, Milinganyo, M, Tripathi, YB. Effect of Momordica charantia on lipid profile and oral glucose tolerance in diabetic rats. Phytother Res. 2004; 18, 954–956.Google Scholar
42. Matthews, D, Hosker, J, Rudenski, A, et al. Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985; 28, 412–419.Google Scholar
43. Bligh, EG, Dyer, WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959; 37, 911–917.Google Scholar
44. Passonneau, JV, Lauderdale, VR. A comparison of three methods of glycogen measurement in tissues. Anal Biochem. 1974; 60, 405–412.CrossRefGoogle ScholarPubMed
45. Iyare, EE, Adegoke, OA. Postnatal weight gain and onset of puberty in rats exposed to aqueous extracts of Hibiscus sabdariffa in utero. Pak J Nutr. 2008; 7, 98–101.CrossRefGoogle Scholar
46. Iyare, EE, Nwagha, UI. Postweaning consumption of aqueous extract of Hibiscus sabdariffa may predispose rats to obesity. Pak J Nutr. 2009; 8, 1760–1765.Google Scholar
47. Miettinen, TA. Cholesterol production in obesity. Circulation. 1971; 44, 842–851.Google Scholar
48. Stanhope, KL, Havel, PJ. Fructose consumption: potential mechanisms for its effects to increase visceral adiposity and induce dyslipidemia and insulin resistance. Curr Opin Lipidol. 2008; 19, 16–24.Google Scholar
49. Conlee, R, Lawler, R, Ross, P. Effects of glucose or fructose feeding on glycogen repletion in muscle and liver after exercise or fasting. Ann Nutr Metab. 1987; 31, 126–132.Google Scholar
50. Koo, H-Y, Wallig, MA, Chung, BH, et al. Dietary fructose induces a wide range of genes with distinct shift in carbohydrate and lipid metabolism in fed and fasted rat liver. Biochim Biophys Acta. 2008; 1782, 341–348.Google Scholar
51. Eden, S. Age- and sex-related differences in episodic growth hormone secretion in the rat. Endocrinology. 1979; 105, 555–560.Google Scholar
52. Gabriel, S, Roncancio, J, Ruiz, N. Growth hormone pulsatility and the endocrine milieu during sexual maturation in male and female rats. Neuroendocrinology. 1992; 56, 619–628.Google Scholar
53. Ellis, J, Hollands, T, Allen, D. Effect of forage intake on bodyweight and performance. Equine Vet J. 2002; 34, 66–70.Google Scholar
54. MacCracken, JG, Stebbings, JL. Test of a body condition index with amphibians. J Herpetol. 2012; 46, 346–350.Google Scholar
55. Baum, HBA, Biller, BMK, Finkelstein, JS, et al. Effects of physiologic growth hormone therapy on bone density and body composition in patients with adult-onset growth hormone deficiency. A randomized, placebo-controlled trial. Ann Intern Med. 1996; 125, 883–890.Google Scholar
56. Eshet, R, Maor, G, Ari, TB, et al. The aromatase inhibitor letrozole increases epiphyseal growth plate height and tibial length in peripubertal male mice. J Endocrinol. 2004; 182, 165–172.Google Scholar
57. N.C.E.P. Third report of the National Cholesterol Education program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult treament panel III). Final report. 2002.Google Scholar
58. Tobey, T, Mondon, C, Zavaroni, I, Reaven, G. Mechanism of insulin resistance in fructose-fed rats. Metabolism. 1982; 31, 608–612.CrossRefGoogle ScholarPubMed
59. Nakagawa, T, Hu, H, Zharikov, S, et al. A causal role for uric acid in fructose-induced metabolic syndrome. Am J Physiol Renal Physiol. 2006; 290, F625–F631.Google Scholar
60. Motoyama, CS, Pinto, MJ, Lira, FS, et al. Gum Guar fiber associated with fructose reduces serum triacylglycerol but did not improve the glucose tolerance in rats. Diabetol Metab Syndr. 2010; 2, 1–17.CrossRefGoogle Scholar
61. Michalopoulos, GK. Liver regeneration. J Cell Physiol. 2007; 213, 286–300.Google Scholar
62. Sawchenko, P, Mark, I. Sensory functions of the liver: a review. Am J Physiol. 1979; 236, R5–R20.Google ScholarPubMed
63. Sallie, R, Michael Tredger, J, Williams, R. Drugs and the liver part 1: testing liver function. Biopharm Drug Dispos. 1991; 12, 251–259.Google Scholar
64. Seyama, Y, Kokudo, N. Assessment of liver function for safe hepatic resection. Hepatol Res. 2009; 39, 107–116.Google Scholar
65. Kelley, GL, Allan, G, Azhar, S. High dietary fructose induces a hepatic stress response resulting in cholesterol and lipid dysregulation. Endocrinology. 2004; 145, 548–555.Google Scholar
66. Thapa, B, Walia, A. Liver function tests and their interpretation. Indian J Pediatr. 2007; 74, 663–671.Google Scholar
67. Thulin, P, Rafter, I, Stockling, K, et al. PPARα regulates the hepatotoxic biomarker alanine aminotransferase (ALT1) gene expression in human hepatocytes. Toxicol Appl Pharmacol. 2008; 231, 1–9.Google Scholar
68. Rajesh, S, Rajkapoor, B, Kumar, RS, Raju, K. Effect of Clausena dentata (Willd.) M. Roem. against paracetamol induced hepatotoxicity in rats. Pak J Pharm Sci. 2009; 22, 90–93.Google Scholar
69. Pratt, DS, Kaplan, MM. Evaluation of abnormal liver-enzyme results in asymptomatic patients. N Engl J Med. 2000; 342, 1266–1271.Google Scholar
70. de Castro, U, Dos Santos, R, Silva, ME, et al. Age-dependent effect of high-fructose and high-fat diets on lipid metabolism and lipid accumulation in liver and kidney of rats. Lipids Health Dis. 2013; 12, 1–11.Google Scholar
71. West, JR. Foetal alcohol-induced brain damage and the problem of determining temporal vulnerability: a review. Alcohol Drug Res. 1987; 7, 423–441.Google Scholar