Research Article
Open Access Peer-reviewed

Araçá (Psidium cattleianum Sabine) Ameliorates Liver Damage and Reduces Hepatic Steatosis in Rats Fed with a High-fat Diet

Alice Helena S. PAULINO1, 2,, Ana Maria F. VIANA1, 2, Larissa F. BONOMO3, Joyce Ferreira C. GUERRA4, Juliana Márcia M. LOPES1, 2, Ana Carolina S. RABELO1, Miliane Martins A. FAGUNDES2, 5, Ana Lúcia Rissoni S. RÉGIS2, Wanderson G. LIMA1, 6, Maria Lúcia PEDROSA1, 6, Marcelo Eustáquio SILVA1, 2, 5

1Research Center in Biological Sciences (NUPEB), Federal University of Ouro Preto, Ouro Preto, MG, Brazil

2School of Nutrition, Federal University of Ouro Preto, Ouro Preto, MG, Brazil

3Department of Pharmacy. Federal University of Juiz de Fora, Governador Valadares Campus, Governador Valadares, MG, Brazil

4Institute of Genetics and Biochemistry, Federal University of Uberlândia, Patos de Minas, MG, Brazil

5Department of Foods (DEALI), Federal University of Ouro Preto, Ouro Preto, Minas Gerais, Brazil

6Department of Biological Sciences (DECBI), Federal University of Ouro Preto, Ouro Preto, Brazil

Journal of Food and Nutrition Research. 2019, 7(2), 132-140. DOI: 10.12691/jfnr-7-2-5
Received November 12, 2018; Revised January 03, 2019; Accepted February 14, 2019

Abstract

Bioactive compounds, present in some foods, act enhancing the endogenous antioxidant system and are proposed as an effective strategy in preventing the changes induced by free radicals in some diseases, such as nonalcoholic fatty liver disease (NAFLD). There has been an increase in the number of studies carried out with the aim of finding natural antioxidant compounds present in fruits, mainly the native fruits of Brazil, because they contain a high content of these compounds. Araçá (Psidium cattleianum Sabine) is a fruit that is rich in polyphenols and exhibits strong antioxidant, antiproliferative, and anti-inflammatory activities. Therefore, the present study investigated the effects of araçá flour on oxidative stress, liver injury, and antioxidant defenses in high-fat diet-induced hepatic steatosis in rats. In vitro experiments showed that araçá contains high concentrations of total polyphenols and exhibits strong antioxidant activity with no cytotoxicity. In vivo experiments indicated that the addition of araçá to a high-fat diet inhibited the activities of alanine aminotransferase and aspartate enzymes, reduced macrovesicular steatosis, increased the paraoxonase activity, and increased the concentration of the total and reduced forms of glutathione. Therefore, our findings suggested the hepatoprotective role of araçá against the progression of steatosis.

Keywords:

Psidium cattleianum Sabine, araçá, phenolic compounds, hepatic steatosis, antioxidants defenses
[1]  M. Vacca, M. Allison, J. L. Griffin, and A. Vidal-Puig, “Fatty Acid and Glucose Sensors in Hepatic Lipid Metabolism: Implications in NAFLD,” Semin Liver Dis, vol. 35, no. 3, pp. 250-261, 2015.View Article  PubMed
 
[2]  I. Nalbantoglu and E. M. Brunt, “Role of liver biopsy in nonalcoholic fatty liver disease,” World J. Gastroenterol., vol. 20, no. 27, pp. 9026-9037, 2014. PubMed  PubMed
 
[3]  C. E. Foulds, L. S. Treviño, B. York, and C. L. Walker, “Endocrine-disrupting chemicals and fatty liver disease,” Nat. Rev. Endocrinol., vol. 13, no. 8, pp. 445-457, 2017.View Article  PubMed  PubMed
 
[4]  R. Patell, “Non Alcoholic Fatty Liver Disease in Obesity,” J. Clin. Diagnostic Res., vol. 8, no. 1, pp. 62-66, 2014.View Article
 
[5]  G. Serviddio, F. Bellanti, and G. Vendemiale, “Free radical biology for medicine: Learning from nonalcoholic fatty liver disease,” Free Radic. Biol. Med., vol. 65, pp. 952-968, 2013.View Article  PubMed
 
[6]  Y. Y. Chang et al., “Preventive effects of taurine on development of hepatic steatosis induced by a high-fat/cholesterol dietary habit,” J. Agric. Food Chem., vol. 59, no. 1, pp. 450-457, 2011.View Article  PubMed
 
[7]  M. de L. P. Bianchi and L. M. G. Antunes, “Radicais livres e os principais antioxidantes da dieta,” Rev. Nutr., vol. 12, no. 2, pp. 123-130, 1999.View Article
 
[8]  M. Hariri et al., “Intakes of Vegetables and Fruits are Negatively Correlated with Risk of Stroke in Iran.,” Int. J. Prev. Med., vol. 4, no. Suppl 2, pp. S300-5, May 2013.
 
[9]  V. Lobo, A. Patil, A. Phatak, and N. Chandra, “Free radicals, antioxidants and functional foods: Impact on human health.,” Pharmacogn. Rev., vol. 4, no. 8, pp. 118-26, Jul. 2010.View Article  PubMed  PubMed
 
[10]  Y. Liu et al., “Inhibitory effect of blueberry polyphenolic compounds on oleic acid-induced hepatic steatosis in vitro,” J. Agric. Food Chem., vol. 59, no. 22, pp. 12254-12263, 2011.View Article  PubMed
 
[11]  S.-J. Cho, U. J. Jung, and M.-S. Choi, “Differential effects of low-dose resveratrol on adiposity and hepatic steatosis in diet-induced obese mice,” Br. J. Nutr., vol. 108, no. 12, pp. 2166-2175, 2012.View Article  PubMed
 
[12]  J. F. da C. Guerra et al., “Dietary açai attenuates hepatic steatosis via adiponectin-mediated effects on lipid metabolism in high-fat diet mice,” J. Funct. Foods, vol. 14, pp. 192-202, 2015.View Article
 
[13]  A. L. Medina et al., “Araçá (Psidium cattleianum Sabine) fruit extracts with antioxidant and antimicrobial activities and antiproliferative effect on human cancer cells,” Food Chem., vol. 128, no. 4, pp. 916-922, 2011.View Article
 
[14]  A. B. Ribeiro, R. C. Chisté, M. Freitas, A. F. Da Silva, J. V. Visentainer, and E. Fernandes, “Psidium cattleianum fruit extracts are efficient in vitro scavengers of physiologically relevant reactive oxygen and nitrogen species,” Food Chem., vol. 165, pp. 140-148, 2014.View Article  PubMed
 
[15]  W. Horwitz, P. Chichilo, and H. Reynolds, “Official methods of analysis of the Association of Official Analytical Chemists.,” Off. methods Anal. Assoc. Off. Anal. Chem., 1970.
 
[16]  P. J. Van Soest, R. H. Wine, A. Husbandry, and R. División, “Use of Detergents in the Analysis of Fibrous Feeds. IV. Determination of Plant Cell-Wall Constituents.”
 
[17]  S. Georgé, P. Brat, P. Alter, and M. J. Amiot, “Rapid determination of polyphenols and vitamin C in plant-derived products,” J. Agric. Food Chem., vol. 53, no. 5, pp. 1370-1373, 2005.View Article  PubMed
 
[18]  W. Brand-Williams, M. E. Cuvelier, and C. Berset, “Use of a free radical method to evaluate antioxidant activity,” LWT - Food Sci. Technol., vol. 28, no. 1, pp. 25-30, 1995.
 
[19]  T. Mosmann, “Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays,” J. Immunol. Methods, vol. 65, no. 1-2, pp. 55-63, Dec. 1983.View Article
 
[20]  P. G. Reeves, F. H. Nielsen, and G. C. Fahey, “AIN-93 Purified Diets for Laboratory Rodents: Final Report of the American Institute of Nutrition Ad Hoc Writing Committee on the Reformulation of the AIN-76A Rodent Diet,” J. Nutr., vol. 123, no. 11, pp. 1939-1951, 1993.View Article  PubMed
 
[21]  S. L. Matos et al., “Dietary models for inducing hypercholesterolemia in rats,” Brazilian Arch. Biol. Technol., vol. 48, no. 2, pp. 203-209, 2005.View Article
 
[22]  J. A. Buege and S. D. Aust, “Microsomal lipid peroxidation,” Methods Enzymol., vol. 52, pp. 302-310, Jan. 1978.View Article
 
[23]  R. L. Levine et al., “Determination of carbonyl content in oxidatively modified proteins,” Methods Enzymol., vol. 186, pp. 464-478, Jan. 1990.View Article
 
[24]  H. Aebi, “Catalase in vitro,” Methods Enzymol., vol. 105, pp. 121-126, Jan. 1984.View Article
 
[25]  R. J. Lowry, O. H.; Rosebrough, N. J.; Farr, A. L.; Randall, “The folin by oliver,” Anal. Biochem., vol. 217, no. 2, pp. 220-230, 1951.
 
[26]  S. Marklund and G. Marklund, “Involvement of the Superoxide Anion Radical in the Autoxidation of Pyrogallol and a Convenient Assay for Superoxide Dismutase,” 1974.
 
[27]  O. W. Griffith, “Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine,” Anal. Biochem., vol. 106, no. 1, pp. 207-212, Jul. 1980.View Article
 
[28]  J. Beltowski, G. Wojcicka, and A. Jamroz, “Differential effect of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors on plasma paraoxonase 1 activity in the rat 9,” Pol.J.Pharmacol., vol. 54, no. 1230-6002 (Print), pp. 661-671, 2002.
 
[29]  E. Albano et al., “Immune response towards lipid peroxidation products as a predictor of progression of non-alcoholic fatty liver disease to advanced fibrosis,” Gut, vol. 54, no. 7, pp. 987-993, 2005.View Article  PubMed  PubMed
 
[30]  A. de Lima, A. M. de O. e Silva, R. A. Trindade, R. P. Torres, and J. Mancini-Filho, “Composição química e compostos bioativos presentes na polpa e na amêndoa do pequi (Caryocar brasiliense, Camb.),” Rev. Bras. Frutic., vol. 29, no. 3, pp. 695-698, 2007.View Article
 
[31]  W. S. Rocha, R. M. Lopes, D. B. da Silva, R. F. Vieira, J. P. da Silva, and T. da S. Agostini-Costa, “Compostos fenólicos totais e taninos condensados em frutas nativas do cerrado,” Rev. Bras. Frutic., vol. 33, no. 4, pp. 1215-1221, 2011.View Article
 
[32]  E. M. Kuskoski, A. G. Asuero, A. M. Troncoso, J. Mancini-Filho, and R. Fett, “Aplicación de diversos métodos químicos para determinar actividad antioxidante en pulpa de frutos,” Ciência e Tecnol. Aliment., vol. 25, no. 4, pp. 726-732, 2005.View Article
 
[33]  A. Luísa, K. Faller, and E. Fialho, “Disponibilidade de polifenóis em frutas e hortaliças consumidas no Brasil Polyphenol availability in fruits and vegetables consumed in Brazil,” Rev Saúde Pública, vol. 43, no. 2, pp. 211-8, 2009.View Article
 
[34]  G. A. B. Canuto, A. A. O. Xavier, L. C. Neves, and M. de T. Benassi, “Caracterização físico-química de polpas de frutos da Amazônia e sua correlação com a atividade anti-radical livre,” Rev. Bras. Frutic., vol. 32, no. 4, pp. 1196-1205, 2010.View Article
 
[35]  H. Zhang and R. Tsao, “Dietary polyphenols, oxidative stress and antioxidant and anti-inflammatory effects,” Curr. Opin. Food Sci., vol. 8, pp. 33-42, 2016.View Article
 
[36]  M. Guasch-Ferré, J. Merino, Q. Sun, M. Fitó, and J. Salas-Salvadó, “Dietary Polyphenols, Mediterranean Diet, Prediabetes, and Type 2 Diabetes: A Narrative Review of the Evidence,” Oxid. Med. Cell. Longev., vol. 2017, 2017. PubMed  PubMed
 
[37]  K. S. Bhullar and H. P. V. Rupasinghe, “Polyphenols: Multipotent Therapeutic Agents in Neurodegenerative Diseases, Polyphenols: Multipotent Therapeutic Agents in Neurodegenerative Diseases,” Oxidative Med. Cell. Longevity, Oxidative Med. Cell. Longev., vol. 2013, 2013, p. e891748, 2013.
 
[38]  M. C. Pereira et al., “Characterization and antioxidant potential of Brazilian fruits from the Myrtaceae family,” J. Agric. Food Chem., vol. 60, no. 12, pp. 3061-3067, 2012.View Article  PubMed
 
[39]  O. A. Esmael, S. N. Sonbul, T. A. Kumosani, and S. . Moselhy, “Hypolipidemic effect of fruit fibers in rats fed with high dietary fat,” Toxicol. Ind. Health, vol. 31, no. 3, pp. 281-288, Mar. 2015.View Article  PubMed
 
[40]  Y. E. Pérez-Beltrán et al., “Nutritional characteristics and bioactive compound content of guava purees and their effect on biochemical markers of hyperglycemic and hypercholesterolemic rats,” J. Funct. Foods, vol. 35, pp. 447-457, Aug. 2017.View Article
 
[41]  T. Trasher and M. Abelmalek, “Non-alcoholic fatty liver disease Non-alcoholic fatty liver disease,” N C Med J, vol. 50, no. August, pp. 1-5, 2016.
 
[42]  H. Yoshitomi, X. Guo, T. Liu, and M. Gao, “Guava leaf extracts alleviate fatty liver via expression of adiponectin receptors in SHRSP.Z-Leprfa/Izm rats,” Nutr. Metab., vol. 9, no. 1, p. 13, 2012.View Article  PubMed  PubMed
 
[43]  M. Carmiel-Haggai, A. I. Cederbaum, and N. Nieto, “A high-fat diet leads to the progression of non-alcoholic fatty liver disease in obese rats.,” FASEB J., vol. 19, no. 1, pp. 136-138, 2005.View Article  PubMed
 
[44]  W. C. Chiu, H. H. Yang, S. C. Chiang, Y. X. Chou, and H. T. Yang, “Auricularia polytricha aqueous extract supplementation decreases hepatic lipid accumulation and improves antioxidative status in animal model of nonalcoholic fatty liver,” Biomed., vol. 4, no. 2, pp. 29-38, 2014.View Article  PubMed  PubMed
 
[45]  D. Dong et al., “Total saponins from Rosa laevigata Michx fruit attenuates hepatic steatosis induced by high-fat diet in rats,” Food Funct., vol. 5, no. 12, pp. 3065-3075, 2014.View Article  PubMed
 
[46]  A. M. Teixeira, F. C. Chaves, and C. V. Franzon, Rodrigo Cezar, Rombaldi, “Influence of Genotype and Harvest Season on the Phytochemical Composition of Araçá (Psidium Cattleianum Sabine) Fruit,” Int. J. Food Nutr. Sci., vol. 3, no. 4, pp. 1-7, 2016.
 
[47]  M. Aviram and M. Rosenblat, “Paraoxonases 1, 2, and 3, oxidative stress, and macrophage foam cell formation during atherosclerosis development,” Free Radic. Biol. Med., vol. 37, no. 9, pp. 1304-1316, 2004.View Article  PubMed
 
[48]  M. Aviram et al., “Pomegranate juice consumption reduces oxidative stress and low density lipoprotein atherogenic modifications: studies in the atherosclerotic apolipoprotein E deficient mice and in humans,” Am. J. Clin. Nutr., vol. 151, p. 111, 2000.
 
[49]  R. R. Pereira et al., “A�ai (Euterpe oleracea Mart.) Upregulates Paraoxonase 1 Gene Expression and Activity with Concomitant Reduction of Hepatic Steatosis in High-Fat Diet-Fed Rats,” Oxid. Med. Cell. Longev., vol. 2016, 2016.
 
[50]  P. C. Huber, W. P. Almeida, and Â. De Fátima, “Glutationa e enzimas relacionadas: Papel biologico e importancia em processos patologicos,” Quim. Nova, vol. 31, no. 5, pp. 1170-1179, 2008.View Article
 
[51]  L. Yuan and N. Kaplowitz, “Glutathione in liver diseases and hepatotoxicity,” Mol. Aspects Med., vol. 30, no. 1-2, pp. 29-41, Feb. 2009.View Article  PubMed