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Neonatal zingerone protects against the development of high-fructose diet-induced metabolic syndrome in adult Sprague-Dawley rats

Published online by Cambridge University Press:  05 June 2020

N. Muhammad Open the ORCID record for N. Muhammad [Opens in a new window] ,
B. W. Lembede  and
K. H Erlwanger Open the ORCID record for K. H Erlwanger [Opens in a new window]
N. Muhammad*
Affiliation:
School of Physiology, Faculty of Health Sciences, University of Witwatersrand, Johannesburg, South Africa Department of Physiology, College of Health Sciences, Federal University Birnin Kebbi, Birnin Kebbi, Nigeria
B. W. Lembede
Affiliation:
School of Physiology, Faculty of Health Sciences, University of Witwatersrand, Johannesburg, South Africa
K. H Erlwanger
Affiliation:
School of Physiology, Faculty of Health Sciences, University of Witwatersrand, Johannesburg, South Africa
*
Address for correspondence: N. Muhammad, School of Physiology, Faculty of Health Sciences, University of Witwatersrand, 7 York Road, Parktown, Johannesburg2193, South Africa. Email: nsmaaji@gmail.com
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Abstract

During the early postnatal period, dietary manipulations can alter the developmental trajectory of the growing offspring, causing beneficial or adverse health outcomes later in adult life. We investigated the potential preventive effects of neonatal zingerone intake on the development of fructose-induced metabolic derangements in rats.

Four-day old male and female Sprague-Dawley rat pups (n = 79) were randomly grouped and administered: 10 ml/kg body weight (bwt) of distilled water (W), 10 ml/kg bwt 20% fructose solution (FS), 10 ml/kg bwt fructose solution + 40 mg/kg bwt of zingerone in distilled water (ZF) or 40 mg/kg bwt of zingerone in distilled water (ZW) pre-weaning. After weaning, W and ZW continued on unlimited tap water, while FS and ZF continued on unlimited fructose solution for 10 weeks. Body mass and food and fluid intake were evaluated, plasma was collected for metabolic assays and visceral fat was quantified.

Food intake was decreased, fructose and overall caloric intake were increased due to fructose feeding in both sexes (P < 0.05). When compared with the controls, the high-fructose diet significantly raised the terminal body masses of females (P < 0.0001), concentrations of triglycerides, total cholesterol, LDL-c, TG:HDL-c ratio and visceral fat mass relative to bwt in both sexes (P < 0.05). Zingerone prevented (P < 0.05) the fructose-induced increase in body mass (females) and hypercholesterolemia (both sexes). Levels of HDL-c, glycaemic parameters and adiponectin were not affected by the interventions (P > 0.05). Sex-related differences were observed in food, fluid and caloric intake, terminal mass, cholesterol subtypes and visceral fat percentage (P < 0.05).

Zingerone could be used strategically in the neonatal phase as a prophylatic management of high-fructose diet-induced metabolic syndrome.

Keywords

Fructosemetabolic dysfunctionzingeroneneonataldyslipidaemiaobesity
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 4 , August 2021 , pp. 671 - 679
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

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References

Reichetzeder, C, Dwi Putra, SE, Li, J, Hocher, B. Developmental origins of disease – crisis precipitates change. Cell Physiol Biochem. 2016; 39, 919–938.CrossRefGoogle ScholarPubMed
Pandey, AK, Pandey, G. Epigenetics and systems physiology of nutrition: an overview. Adv Diabetes Metab. 2017; 5, 6–11.CrossRefGoogle Scholar
Dearden, L, Bouret, SG, Ozanne, SE. Sex and gender differences in developmental programming of metabolism. Mol Metab. 2018; 15, 8–19. Available from: https://doi.org/10.1016/j.molmet.2018.04.007 CrossRefGoogle Scholar
Alzamendi, A, Castrogiovanni, D, Gaillard, RC, Spinedi, E, Giovambattista, A. Increased male offspring’s risk of metabolic-neuroendocrine dysfunction and overweight after fructose-rich diet intake by the lactating mother. Endocrinology. 2010; 151, 4214–4223.CrossRefGoogle ScholarPubMed
Clayton, ZE, Vickers, MH, Bernal, A, Yap, C, Sloboda, DM. Early life exposure to fructose alters maternal, fetal and neonatal hepatic gene expression and leads to sex-dependent changes in lipid metabolism in rat offspring. PLoS One. 2015; 10, 1–28.CrossRefGoogle ScholarPubMed
Mai, BH, Yan, L. The negative and detrimental effects of high fructose on the liver, with special reference to metabolic disorders. Diabetes, Metab Syndr Obes Targets Ther. 2019; 12, 821–826.CrossRefGoogle ScholarPubMed
Buzzetti, E, Pinzani, M, Tsochatzis, EA. The multiple-hit pathogenesis of non-alcoholic fatty liver disease (NAFLD). Metabolism. 2016; 65, 1038–1048. Available from: http://dx.doi.org/10.1016/j.metabol.2015.12.012 CrossRefGoogle Scholar
Akbarzadeh, Z, Nourian, M, Hovsepian, S, Kelishadi, R. Dietary patterns and metabolic syndrome in children and adolescents: a systematic review. J Pediatr Rev. 2017; 6, 617–630. Available from: http://jpediatricsreview.com/en/articles/11656.html CrossRefGoogle Scholar
Saklayen, MG. The global epidemic of the metabolic syndrome. Curr Hypertens Rep. 2018; 20, 12. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29480368 CrossRefGoogle ScholarPubMed
Pai, SA, Munshi, RP, Panchal, FH, et al. Plumbagin reduces obesity and nonalcoholic fatty liver disease induced by fructose in rats through regulation of lipid metabolism, inflammation and oxidative stress. Biomed Pharmacother. 2019; 111, 686–694. Available from: https://doi.org/10.1016/j.biopha.2018.12.139 CrossRefGoogle ScholarPubMed
Mortera, RR, Bains, Y, Gugliucci, A. Fructose at the crossroads of the metabolic syndrome and obesity epidemics. Front Biosci – Landmark. 2019; 24, 186–211.Google Scholar
Hannou, SA, Haslam, DE, McKeown, NM, Herman, MA. Fructose metabolism and metabolic disease. J Clin Invest. 2018; 128, 545–555.CrossRefGoogle ScholarPubMed
Tappy, L. Fructose metabolism and noncommunicable diseases: recent findings and new research perspectives. Curr Opin Clin Nutr Metab Care. 2018; 21, 214–222.CrossRefGoogle ScholarPubMed
Reynolds, CM, Vickers, MH. The role of adipokines in developmental programming: evidence from animal models. J Endocrinol. 2019; 242, T81–T94.CrossRefGoogle Scholar
Fuchs, M. Managing the silent epidemic of nonalcoholic fatty liver disease. Fed Pract. 2019; 36, 12–13.Google ScholarPubMed
Lembede, BW, Erlwanger, KH, Nkomozepi, P, Chivandi, E. Effect of neonatal orally administered S-allyl cysteine in high-fructose diet fed Wistar rats. J Dev Orig Health Dis. 2017; 9, 160–171.CrossRefGoogle ScholarPubMed
Jamshidi-kia, F, Lorigooini, Z, Amini-khoei H. Medicinal plants: past history and future perspective. J Herbmed Pharmacol. 2018; 7, 1–7.CrossRefGoogle Scholar
Nyakudya, TT, Mukwevho, E, Nkomozepi, P, Erlwanger, KH. Neonatal intake of oleanolic acid attenuates the subsequent development of high fructose diet-induced non-alcoholic fatty liver disease in rats. J Dev Orig Health Dis. 2018; 9, 500–510.CrossRefGoogle ScholarPubMed
Mukonowenzou, NC. The Effects of Ursolic Acid on Neonatal Programming and Its Potential to Prevent the Development of Metabolic Dysfunction in Sprague Dawley Rats [Internet]. University of Witwatersrand; 2016. Available from: http://hdl.handle.net/10539/23339 Google Scholar
Kumar, L, Harjai, K, Chhibber, S. Recent update on multiple pharmacological benefits of zingerone: a quick review. Am J Phytomedicine Clin Ther. 2014; 2, 693–704.Google Scholar
Ahmad, B, Rehman, MU, Amin, I, et al. Zingerone (4-(4-hydroxy-3-methylphenyl) butan-2-one) protects against alloxan-induced diabetes via alleviation of oxidative stress and inflammation: probable role of NF-kB activation. Saudi Pharm J. 2018; 26, 1137–1145. Available from: https://doi.org/10.1016/j.jsps.2018.07.001 CrossRefGoogle ScholarPubMed
Ghareib, SA, El-bassossy, HM, Elberry, AA, Azhar, A, Malcolm, L. Protective effect of zingerone on increased vascular contractility in diabetic rat aorta. 2016; 780, 174–179.Google Scholar
Jothi, MA, Parameswari, C, Vincent, S. Antidiabetic, hypolipidemic and histopathological analysis of zingerone in streptozotocin induced diabetic rats. Int J Pharm Sci Res. 2016; 7, 2385–2393.Google Scholar
Jothi, MA, Parameswari, C, Vincent, S. Enhanced glycemic control, pancreas protective, modulated carbohydrate metabolic enzyme activities by zingerone in streptozotocin-induced diabetic rats. World J Pharm Res. 2018; 7, 416–435.Google Scholar
Narayanan, JM, Jesudoss, VAS. Disease in rats fed with fructose-enriched diet Hepatoprotective potential of zingerone against nonalcoholic fatty liver disease in rats fed with fructose-enriched diet. Gen Physiol Biophys. 2016; 35, 185–194.CrossRefGoogle Scholar
Mani, V, Siddique, AI, Arivalagan, S, Thomas, NS. Zingerone ameliorates hepatic and renal damage in alcohol induced toxicity in experimental rats. Int J Nutr Pharmacol Neurol Dis. 2016; 6, 125–132.Google Scholar
Julietpoornamathy, J, Parameswari, CS. Zingerone ameliorates hepatotoxicity. Int J Res Pharm Sci. 2020; 11, 280–284.CrossRefGoogle Scholar
Mamikutty, N, Thent, ZC, Suhaimi, FH. Fructose-drinking water induced nonalcoholic fatty liver disease and ultrastructural alteration of hepatocyte mitochondria in male Wistar rat. Biomed Res Int. 2015; 2015, 1–8.CrossRefGoogle Scholar
Mamikutty, N, Thent, ZC, Sapri, SR, et al. The establishment of metabolic syndrome model by induction of fructose drinking water in male Wistar rats. Biomed Res Int. 2014; 2014, 1–8.CrossRefGoogle ScholarPubMed
Charan, J, Kantharia, N. How to calculate sample size in animal studies? J Pharmacol Pharmacother. 2013; 4, 303–306.CrossRefGoogle ScholarPubMed
Zatroch, KK, Knight, CG, Reimer, JN, Pang, DSJ. Refinement of intraperitoneal injection of sodium pentobarbital for euthanasia in laboratory rats (Rattus norvegicus). BMC Vet Res. 2017; 13, 4–10.Google Scholar
Matthews, DR, Hosker, JR, Rudenski, AS, 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.CrossRefGoogle ScholarPubMed
Li, Z, Wang, Y, Sun, KK, et al. Sex-related difference in food-anticipatory activity of mice. Horm Behav. 2015; 70, 38–46. Available from: http://dx.doi.org/10.1016/j.yhbeh.2015.02.004 CrossRefGoogle ScholarPubMed
Ackroff, K, Sclafani, A. Fructose-conditioned flavor preferences in male and female rats: effects of sweet taste and sugar concentration. Appetite. 2004; 42, 287–297.CrossRefGoogle ScholarPubMed
Curtis, KS, Stratford, JM, Contreras, RJ. Estrogen increases the taste threshold for sucrose in rats. Physiol Behav. 2005; 86, 281–286.CrossRefGoogle ScholarPubMed
Briffa, JF, O’dowd, R, Romano, T, et al. Reducing pup litter size alters early postnatal calcium homeostasis and programs adverse adult cardiovascular and bone health in male rats. Nutrients. 2019; 11, 118.CrossRefGoogle ScholarPubMed
McGrath-Morrow, SA, Hayashi, M, Aherrera, A, et al. The effects of electronic cigarette emissions on systemic cotinine levels, weight and postnatal lung growth in neonatal mice. PLoS One. 2015; 10, 2–11.Google Scholar
Ahmad, B, Rehman, MU, Amin, I, et al. A review on pharmacological properties of zingerone (4-(4-Hydroxy-3-methoxyphenyl)-2-butanone). Sci World J. 2015; 2015, 816364.CrossRefGoogle Scholar
Stafford, DEJ. Sex steroids and growth hormone secretion. In Growth Hormone Deficiency, 2016; pp. 21–28. Springer International Publishing, Switzerland.CrossRefGoogle Scholar
Spritzer, MD, Roy, EA. Testosterone and adult neurogenesis. Biomolecules. 2020; 10, 1–24.Google Scholar
Hu, L, Huang, X, You, C, et al. Prevalence of overweight, obesity, abdominal obesity and obesity-related risk factors in southern China. PLoS One. 2017; 12, 1–14.CrossRefGoogle ScholarPubMed
Zemel, M, Lee, J. Call for special issue papers: obesity. J Med Food. 2019; 22, 1091.CrossRefGoogle ScholarPubMed
Chusyd, DE, Wang, D, Huffman, DM, Nagy, TR. Relationships between rodent white adipose fat pads and human white adipose fat depots. Front Nutr. 2016; 3, 1–12.CrossRefGoogle ScholarPubMed
da Luz, P, Favarato, D, Faria-Neto, J Jr, Lemos, P, Chagas, A. High ratio of triglycerides to HDL-cholesterol predicts extensive coronary disease. Clinics. 2008; 63, 427–432.Google ScholarPubMed
Chu, S. Risk assessment of metabolic syndrome in adolescents using the triglyceride/high-density lipoprotein cholesterol ratio and the total cholesterol/high-density lipoprotein cholesterol ratio. Ann Pediatr Endocrinol Metab. 2019; 1012, 41–48.CrossRefGoogle Scholar
Gupta, R, Singh, PK, Singh, R, Singh, RL. Pharmacological activities of Zingiber officinale (ginger) and its active ingredients: a review. Int J Innov Sci Res. 2016; 4, 1–18.Google Scholar
Ibrahim, KG, Chivandi, E, Mojiminiyi, FBO, Erlwanger, KH. The response of male and female rats to a high-fructose diet during adolescence following early administration of Hibiscus sabdariffa aqueous calyx extracts. J Dev Orig Health Dis. 2017; 8, 628–637.CrossRefGoogle ScholarPubMed
Ibitoye, OB, Ajiboye, TO. Dietary phenolic acids reverse insulin resistance, hyperglycaemia, dyslipidaemia, inflammation and oxidative stress in high-fructose diet-induced metabolic syndrome rats. Arch Physiol Biochem. 2018; 124, 410–417. Available from: https://doi.org/10.1080/13813455.2017.1415938 CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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