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Antioxidant, anti-inflammatory and anti-obesity effects of onion and its by-products in high-fat fed rodents: a systematic review

Efeitos antioxidantes, anti-inflamatórios e anti-obesidade da cebola e seus subprodutos em roedores alimentados com alto teor de gordura: uma revisão sistemática

Abstract

The effects of onion and its by-products on metabolic changes induced by excessive consumption of a high fat diet have been the focus of many studies. The aim of this study was to systematically review the effects of onion and its by-products antioxidant, anti-inflammatory and anti-obesity in rats exposed to a high-fat diet. Five databases were used: Pubmed, EMBASE, Science Direct, Web of science and Scopus until June 2020 updated December 1, 2022. Research of the articles was carried out by two reviewers, searching and selecting studies after an initial reading of the titles and abstracts. In total, 2,448 papers were found and, after assessing against the inclusion and exclusion criteria, 18 papers were selected for this review. The findings of this review show the beneficial effects of onion and its by-products on inflammatory parameters, obesity, cardiovascular disease, thermogenesis and hepatic alterations generally associated with the consumption of a high-fat diet.

Keywords:
high fat diet; onion; onion by-products; Allium cepa L.; rats

Resumo

Os efeitos da cebola e seus subprodutos nas alterações metabólicas induzidas pelo consumo excessivo de uma dieta rica em gordura têm sido foco de muitos estudos. O objetivo deste estudo foi revisar sistematicamente os efeitos da cebola e seus subprodutos antioxidantes, anti-inflamatórios e anti-obesidade em ratos expostos a uma dieta hiperlipídica. Foram utilizadas cinco bases de dados: Pubmed, EMBASE, Science Direct, Web of science e Scopus até junho de 2020, atualizado em 01 de dezembro de 2022. A pesquisa dos artigos foi realizada por dois revisores, buscando e selecionando os estudos após leitura inicial dos títulos e resumos. No total, 2.448 artigos foram encontrados e, após avaliação de acordo com os critérios de inclusão e exclusão, 18 artigos foram selecionados para esta revisão. Os achados desta revisão mostram os efeitos benéficos da cebola e seus subprodutos sobre parâmetros inflamatórios, obesidade, doenças cardiovasculares, termogênese e alterações hepáticas geralmente associadas ao consumo de uma dieta hiperlipídica.

Palavras-chave:
dieta hiperlipídica; cebola; subprodutos da cebola; Allium cepa L.; ratos

1. Introduction

Obesity is a multifactorial disease that is growing in the world’s population (Popkin et al., 2012POPKIN, B.M., ADAIR, L.S. and NG, S.W., 2012. The global nutrition transition: the pandemic of obesity in developing countries. Nutrition Reviews, vol. 70, no. 1, pp. 3-21. http://dx.doi.org/10.1111/j.1753-4887.2011.00456.x. PMid:22221213.
http://dx.doi.org/10.1111/j.1753-4887.20...
; Popkin, 2015POPKIN, B.M., 2015. Nutrition transition and the global diabetes epidemic. Current Diabetes Reports, vol. 15, no. 9, pp. 64. http://dx.doi.org/10.1007/s11892-015-0631-4. PMid:26209940.
http://dx.doi.org/10.1007/s11892-015-063...
). Among the factors associated with this pathology, modern eating habits, characterized mainly by the excessive consumption of ultra-processed foods with a high saturated fat content, have been associated with the appearance of metabolic alterations resulting in the development of diseases (WHO, 2003World Health Organization – WHO, 2003. Diet, nutrition and the prevention of chronic diseases: expert consultation. Geneva: WHO.; Popkin et al., 2012POPKIN, B.M., ADAIR, L.S. and NG, S.W., 2012. The global nutrition transition: the pandemic of obesity in developing countries. Nutrition Reviews, vol. 70, no. 1, pp. 3-21. http://dx.doi.org/10.1111/j.1753-4887.2011.00456.x. PMid:22221213.
http://dx.doi.org/10.1111/j.1753-4887.20...
; Popkin, 2015POPKIN, B.M., 2015. Nutrition transition and the global diabetes epidemic. Current Diabetes Reports, vol. 15, no. 9, pp. 64. http://dx.doi.org/10.1007/s11892-015-0631-4. PMid:26209940.
http://dx.doi.org/10.1007/s11892-015-063...
). Obesity induced by the excessive dietary intake of fat is associated with abdominal fat accumulation, adipocyte size expansion, and the triggering of inflammatory processes, and may also predispose the individual to the development of insulin resistance, and non-alcoholic fatty liver disease (NAFLD), among other things (Lam et al., 2012LAM, Y.Y., HA, C.W.Y., CAMPBELL, C.R., MITCHELL, A.J., DINUDOM, A., OSCARSSON, A., COOK, D.I., HUNT, N.H., CATERSON, I.D., HOLMES, A.J. and STORLIEN, L.H., 2012. Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice. PLoS One, vol. 7, no. 3, pp. e34233. http://dx.doi.org/10.1371/journal.pone.0034233. PMid:22457829.
http://dx.doi.org/10.1371/journal.pone.0...
; Dinh et al., 2015DINH, C.H.L., SZABO, A., YU, Y., CAMER, D., WANG, H. and HUANG, X.F., 2015. Bardoxolone methyl prevents mesenteric fat deposition and inflammation in high-fat diet mice. TheScientificWorldJournal, vol. 2015, pp. 549352. http://dx.doi.org/10.1155/2015/549352. PMid:26618193.
http://dx.doi.org/10.1155/2015/549352...
; Umekawa et al., 2015UMEKAWA, T., SUGIYAMA, T., DU, Q., MURABAYASHI, N., ZHANG, L., KAMIMOTO, Y., YOSHIDA, T., SAGAWA, N. and IKEDA, T., 2015. A maternal mouse diet with moderately high-fat levels does not lead to maternal obesity but causes mesenteric adipose tissue dysfunction in male offspring. The Journal of Nutritional Biochemistry, vol. 26, no. 3, pp. 259-266. http://dx.doi.org/10.1016/j.jnutbio.2014.10.012. PMid:25533905.
http://dx.doi.org/10.1016/j.jnutbio.2014...
; Perez et al., 2015PEREZ, G.S., SANTOS, L.S., CORDEIRO, G.S., PARAGUASSÚ, G.M., ATHANAZIO, D.A., COUTO, R.D., DEIRÓ, T.C.B.J., CASTRO, R.M. and BARRETO-MEDEIROS, J.M., 2015. Maternal and post-weaning exposure to a high fat diet promotes visceral obesity and hepatic steatosis in adult rats. Nutrición Hospitalaria, vol. 32, no. 4, pp. 1653-1658. PMid:26545531.; Lima et al., 2018LIMA, M.S., PEREZ, G.S., MORAIS, G.L., SANTOS, L.S., CORDEIRO, G.S., COUTO, R.D., DEIRÓ, T.C.B.J., LEANDRO, C.G. and BARRETO-MEDEIROS, J.M., 2018. Effects of maternal high fat intake during pregnancy and lactation on total cholesterol and adipose tissue in neonatal rats. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 78, no. 4, pp. 615-618. http://dx.doi.org/10.1590/1519-6984.166788. PMid:29319751.
http://dx.doi.org/10.1590/1519-6984.1667...
; Santos, et al., 2022SANTOS, L.S., MATOS, R.J.B., CORDEIRO, G.S., SANTOS, J.N., PEREZ, G.S., GONÇALVES, M.S., RIBEIRO, I.O. and BARRETO-MEDEIROS, J.M., 2022. Perinatal and post-weaning exposure to an obesogenic diet promotes greater expression of nuclear factor-Kb and tumor necrosis factor-α in white adipose tissue and hypothalamus of adult rats. Nutritional Neuroscience, vol. 25, no. 3, pp. 502-510. http://dx.doi.org/10.1080/1028415X.2020.1764291. PMid:32496945.
http://dx.doi.org/10.1080/1028415X.2020....
; Macêdo et al., 2021MACÊDO, A.P.A., CORDEIRO, G.S., SANTOS, L.S., SANTO, D.A.E., PEREZ, G.S., COUTO, R.D., MACHADO, M.E.P.C. and BARRETO-MEDEIROS, J.M., 2021. Murinometric measurements and retroperitoneal adipose tissue in young rats exposed to the high-fat diet: is there correlation? Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 81, no. 2, pp. 246-250. http://dx.doi.org/10.1590/1519-6984.221405. PMid:32428096.
http://dx.doi.org/10.1590/1519-6984.2214...
; Cordeiro et al., 2022CORDEIRO, G.S., GÓIS, M.B., SANTOS, L.S., ESPÍRITO-SANTO, D.A., SILVA, R.T., PEREIRA, M.U., SANTOS, J.N., CONCEIÇÃO-MACHADO, M.E.P., DEIRÓ, T.C.B.J. and BARRETO-MEDEIROS, J.M., 2022. Perinatal and postweaning exposure to a high-fat diet causes histomorphometric, neuroplastic, and histopathological changes in the rat ileum. Journal of Developmental Origins of Health and Disease. Ahead of print. http://dx.doi.org/10.1017/S2040174422000514. PMid:36073012.
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).

In order to mitigate the effects caused by the excessive consumption of a high-fat diet, studies have investigated the benefits of polyphenols in the health process (Pimentel et al., 2013PIMENTEL, G.D., LIRA, F.S., ROSA, J.C., CARIS, A.V., PINHEIRO, F., RIBEIRO, E.B., NASCIMENTO, C.M.O. and OYAMA, L.M., 2013. Yerba mate extract (Ilex paraguariensis) attenuates both central and peripheral inflammatory effects of diet-induced obesity in rats. The Journal of Nutritional Biochemistry, vol. 24, no. 5, pp. 809-818. http://dx.doi.org/10.1016/j.jnutbio.2012.04.016. PMid:22841395.
http://dx.doi.org/10.1016/j.jnutbio.2012...
; Zou et al., 2017ZOU, T., CHEN, D., YANG, Q., WANG, B., ZHU, M.J., NATHANIELSZ, P.W. and DU, M., 2017. Resveratrol supplementation of high-fat diet-fed pregnant mice promotes brown and beige adipocyte development and prevents obesity in male offspring. The Journal of Physiology, vol. 595, no. 5, pp. 1547-1562. http://dx.doi.org/10.1113/JP273478. PMid:27891610.
http://dx.doi.org/10.1113/JP273478...
; Porras et al., 2017PORRAS, D., NISTAL, E., MARTÍNEZ-FLÓREZ, S., PISONERO-VAQUERO, S., OLCOZ, J.L., JOVER, R., GONZÁLEZ-GALLEGO, J., GARCÍA-MEDIAVILLA, M.V. and SÁNCHEZ-CAMPOS, S., 2017. Protective effect of quercetin on high-fat diet-induced non-alcoholic fatty liver disease in mice is mediated by modulating intestinal microbiota imbalance and related gut-liver axis activation. Free Radical Biology & Medicine, vol. 102, pp. 188-202. http://dx.doi.org/10.1016/j.freeradbiomed.2016.11.037. PMid:27890642.
http://dx.doi.org/10.1016/j.freeradbiome...
; Barroso et al., 2019BARROSO, M.V., GRAÇA-REIS, A., CATTANI-CAVALIERI, I., GITIRANA, L.B., VALENÇA, S.S. and LANZETTI, M., 2019. Mate tea reduces high fat diet-induced liver and metabolic disorders in mice. Biomedicine and Pharmacotherapy, vol. 109, pp. 1547-1555. http://dx.doi.org/10.1016/j.biopha.2018.11.007. PMid:30551407.
http://dx.doi.org/10.1016/j.biopha.2018....
). These substances, present in vegetables and fruits, are part of a large group of bioactive compounds that are divided into subclasses, flavonoids being the most studied, especially quercetin (Slimestad et al., 2007SLIMESTAD, R., FOSSEN, T. and VAGEN, I.M., 2007. Onions: a source of unique dietary flavonoids. Journal of Agricultural and Food Chemistry, vol. 55, no. 25, pp. 10067-10080. http://dx.doi.org/10.1021/jf0712503. PMid:17997520.
http://dx.doi.org/10.1021/jf0712503...
; Hamauzu et al., 2011HAMAUZU, Y., NOSAKA, T., ITO, F., SUZUKI, T., TORISU, S., HASHIDA, M., FUKUZAWA, A., OHGUCHI, M. and YAMANAKA, S., 2011. Physicochemical characteristics of rapidly dried onion powder and its anti-atherogenic effect on rats fed high-fat diet. Food Chemistry, vol. 129, no. 3, pp. 810-815. http://dx.doi.org/10.1016/j.foodchem.2011.05.027. PMid:25212303.
http://dx.doi.org/10.1016/j.foodchem.201...
; Lee et al., 2012LEE, S.-M., MOON, J., DO, H.J., CHUNG, J.H., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Onion peel extract increases hepatic low-density lipoprotein receptor and ATP-binding cassette transporter A1 messenger RNA expressions in Sprague-Dawley rats fed a high-fat diet. Nutrition Research (New York, N.Y.), vol. 32, no. 3, pp. 210-217. http://dx.doi.org/10.1016/j.nutres.2012.01.004. PMid:22464808.
http://dx.doi.org/10.1016/j.nutres.2012....
; Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Nabavi et al., 2015NABAVI, S.F., RUSSO, G.L., DAGLIA, M. and NABAVI, S.M., 2015. Role of quercetin as an alternative for obesity treatment: you are what you eat. Food Chemistry, vol. 179, pp. 305-310. http://dx.doi.org/10.1016/j.foodchem.2015.02.006. PMid:25722169.
http://dx.doi.org/10.1016/j.foodchem.201...
; Forney et al., 2018FORNEY, L.A., LENARD, N.R., STEWART, L.K. and HENAGAN, T.M., 2018. Dietary quercetin attenuates adipose tissue expansion and inflammation and alters adipocyte morphology in a tissue-specific manner. International Journal of Molecular Sciences, vol. 19, no. 3, pp. 895. http://dx.doi.org/10.3390/ijms19030895. PMid:29562620.
http://dx.doi.org/10.3390/ijms19030895...
; Fraga et al., 2019FRAGA, C.G., CROFT, K.D., KENNEDY, D.O. and TOMÁS-BARBERÁN, F.A., 2019. The effects of polyphenols and other bioactives on human health. Food & Function, vol. 10, no. 2, pp. 514-528. http://dx.doi.org/10.1039/C8FO01997E. PMid:30746536.
http://dx.doi.org/10.1039/C8FO01997E...
; Grzelak-Błaszczyk et al., 2020GRZELAK-BŁASZCZYK, K., MILALA, J., KOLODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KOSMALA, M., KLEWICKI, R., FOTSCHKI, B., JURGOŃSKI, A. and JUŚKIEWICZ, J., 2020. Onion protocatechuic acid and quercetin glucosides attenuate changes induced by high fat diet in rats. Food & Function, vol. 4, no. 4, pp. 3585-3597. http://dx.doi.org/10.1039/C9FO02633A.
http://dx.doi.org/10.1039/C9FO02633A...
). Among vegetables, the onion (Allium cepa L.), a popular consumer product that is rich in quercetin and also in other phenolic compounds such as kampferol, protocatechuic acid, anthocyanin and dietary fiber, has been the focus of some studies due to its effects antioxidant, anti-inflammatory and anti-obesity characteristics (Slimestad et al., 2007SLIMESTAD, R., FOSSEN, T. and VAGEN, I.M., 2007. Onions: a source of unique dietary flavonoids. Journal of Agricultural and Food Chemistry, vol. 55, no. 25, pp. 10067-10080. http://dx.doi.org/10.1021/jf0712503. PMid:17997520.
http://dx.doi.org/10.1021/jf0712503...
; Hamauzu et al., 2011HAMAUZU, Y., NOSAKA, T., ITO, F., SUZUKI, T., TORISU, S., HASHIDA, M., FUKUZAWA, A., OHGUCHI, M. and YAMANAKA, S., 2011. Physicochemical characteristics of rapidly dried onion powder and its anti-atherogenic effect on rats fed high-fat diet. Food Chemistry, vol. 129, no. 3, pp. 810-815. http://dx.doi.org/10.1016/j.foodchem.2011.05.027. PMid:25212303.
http://dx.doi.org/10.1016/j.foodchem.201...
; Lee et al., 2012LEE, S.-M., MOON, J., DO, H.J., CHUNG, J.H., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Onion peel extract increases hepatic low-density lipoprotein receptor and ATP-binding cassette transporter A1 messenger RNA expressions in Sprague-Dawley rats fed a high-fat diet. Nutrition Research (New York, N.Y.), vol. 32, no. 3, pp. 210-217. http://dx.doi.org/10.1016/j.nutres.2012.01.004. PMid:22464808.
http://dx.doi.org/10.1016/j.nutres.2012....
; Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Nabavi et al., 2015NABAVI, S.F., RUSSO, G.L., DAGLIA, M. and NABAVI, S.M., 2015. Role of quercetin as an alternative for obesity treatment: you are what you eat. Food Chemistry, vol. 179, pp. 305-310. http://dx.doi.org/10.1016/j.foodchem.2015.02.006. PMid:25722169.
http://dx.doi.org/10.1016/j.foodchem.201...
; Forney et al., 2018FORNEY, L.A., LENARD, N.R., STEWART, L.K. and HENAGAN, T.M., 2018. Dietary quercetin attenuates adipose tissue expansion and inflammation and alters adipocyte morphology in a tissue-specific manner. International Journal of Molecular Sciences, vol. 19, no. 3, pp. 895. http://dx.doi.org/10.3390/ijms19030895. PMid:29562620.
http://dx.doi.org/10.3390/ijms19030895...
; Fraga et al., 2019FRAGA, C.G., CROFT, K.D., KENNEDY, D.O. and TOMÁS-BARBERÁN, F.A., 2019. The effects of polyphenols and other bioactives on human health. Food & Function, vol. 10, no. 2, pp. 514-528. http://dx.doi.org/10.1039/C8FO01997E. PMid:30746536.
http://dx.doi.org/10.1039/C8FO01997E...
; Grzelak-Błaszczyk et al., 2020GRZELAK-BŁASZCZYK, K., MILALA, J., KOLODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KOSMALA, M., KLEWICKI, R., FOTSCHKI, B., JURGOŃSKI, A. and JUŚKIEWICZ, J., 2020. Onion protocatechuic acid and quercetin glucosides attenuate changes induced by high fat diet in rats. Food & Function, vol. 4, no. 4, pp. 3585-3597. http://dx.doi.org/10.1039/C9FO02633A.
http://dx.doi.org/10.1039/C9FO02633A...
). Experimental studies have shown the beneficial effects of the consumption of onion peel powder, bulb, or even tea, on NAFLD, inflammation, cardiovascular disease, body weight, and insulin resistance induced by the consumption of an excessive high-fat diet (Hamauzu et al., 2011HAMAUZU, Y., NOSAKA, T., ITO, F., SUZUKI, T., TORISU, S., HASHIDA, M., FUKUZAWA, A., OHGUCHI, M. and YAMANAKA, S., 2011. Physicochemical characteristics of rapidly dried onion powder and its anti-atherogenic effect on rats fed high-fat diet. Food Chemistry, vol. 129, no. 3, pp. 810-815. http://dx.doi.org/10.1016/j.foodchem.2011.05.027. PMid:25212303.
http://dx.doi.org/10.1016/j.foodchem.201...
; Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Emamat et al., 2016EMAMAT, H., FOROUGHI, F., EINI–ZINAB, H., TAGHIZADEH, M., RISMANCHI, M. and HEKMATDOOST, A., 2016. The effects of onion consumption on treatment of metabolic, histologic, and inflammatory features of nonalcoholic fatty liver disease. Journal of Diabetes and Metabolic Disorders, vol. 15, no. 1, pp. 25. http://dx.doi.org/10.1186/s40200-016-0248-4. PMid:27453880.
http://dx.doi.org/10.1186/s40200-016-024...
, 2018EMAMAT, H., FOROUGHI, F., EINI-ZINAB, H. and HEKMATDOOST, A., 2018. The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry, vol. 33, no. 1, pp. 75-80. http://dx.doi.org/10.1007/s12291-017-0636-7. PMid:29371773.
http://dx.doi.org/10.1007/s12291-017-063...
).

However, despite the evidence already established with regard to the benefits of using and dose onion or its by-products to reduce the consequences of a high-fat diet intake, no systematic review has been performed to date. Thus, the aim of this study was to systematically review the effects of onion and its by-products antioxidant, anti-inflammatory and anti-obesity in rats subjected to a high-fat diet.

2. Methods

The systematic review was carried out following the recommendations of the Preferred reporting items for Systematic reviews and MetaAnalysis (PRISMA) (Moher et al., 2009MOHER, D., LIBERATI, A., TETZLAFF, J. and ALTMAN, D.G., 2009. Reprint-preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Physical Therapy, vol. 89, no. 9, pp. 873-880. http://dx.doi.org/10.1093/ptj/89.9.873. PMid:19723669.
http://dx.doi.org/10.1093/ptj/89.9.873...
). Registered the protocol in PROSPERO having as registration number is CDR42020188172. The record can be accessed at https://www.crd.york.ac.uk/PROSPERO.

2.1. Eligibility criteria

The research question was defined according to the PICOS approach (Participants / Population, Interventions / Exposure, Comparison, Outcomes and Study design) Table 1.

Table 1
PICOS criteria for inclusion and exclusion of studies.

Studies that investigated the effect of the high-fat diet and supplementation of the onion or its by-products on any result related to the health of rats or mice were included. The comparison groups were defined as follows: use of a diet rich in fat versus supplemented with onion and its by-products (in any dose or quantity and any duration of consumption / exposure). In addition, to be included, studies needed to report any health-related results. No restrictions for language were applied. Reviews, human studies, and studies with drugs or other substances unrelated to the use of onion or its by-products were excluded. The identified studies were evaluated according to the inclusion criteria: studies with rats or mice that were exposed to a high-fat diet in the early stages or during adulthood.

2.2. Search strategy and study selection

The evaluation of titles, abstracts, and complete articles was performed between May and June 2020 updated December 1, 2022, following the steps of identification, screening, and eligibility with respect to the inclusion criteria, with no limitation of the year of publication.

The paper research was performed in the electronic databases Pubmed, EMBASE, ScienceDirect, Web of Science and Scopus, using a combination of the terms MeSH (Medical Subject Headings): high fat diet, high-fat diet, occidental diet, western diet, onion, Allium cepa, rat, mouse, mice. The boolean operators “AND” and “OR” were used to cross terms: (high fat diet OR high-fat diet OR occidental diet OR western diet) AND (onion OR Allium cepa) AND (rat OR mouse OR mice).

Research of the articles was carried out by two reviewers, searching and selecting studies after an initial reading of the titles and abstracts. In cases of disagreement, a third reviewer was used to verify whether the study was eligible.

2.3. Quality and risk-of-bias assessment

The quality of the articles used in this review was evaluated according to the guidelines of ARRIVE - Animals in Research: Reporting In Vivo Experiments (Percie Du Sert et al., 2020PERCIE DU SERT, N., HURST, V., AHLUWALIA, A., ALAM, S., AVEY, M.T., BAKER, M., BROWNE, W.J., CLARK, A., CUTHILL, I.C. and DIRNAGL, U., 2020. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biology, vol. 18, no. 7, pp. e3000410. http://dx.doi.org/10.1371/journal.pbio.3000410. PMid:32663219.
http://dx.doi.org/10.1371/journal.pbio.3...
). To evaluate the adequacy of the papers according to the guidelines, a scoring system (0 - no; 1 - yes) was used for the 20 items listed in the ARRIVE guidelines. Information about each study analyzed is summarized in Table 2.

Table 2
Described variables of the selected articles regarding the analysis of the effects of onion and its by-products in animals submitted to a high-fat diet.

To assess the risk of bias, the Systematic Review Center for Laboratory animal Research (SYRCLE) (Hooijmans et al., 2014HOOIJMANS, C.R., ROVERS, M.M., DE VRIES, R.B.M., LEENAARS, M., RITSKES-HOITINGA, M. and LANGENDAM, M.W., 2014. SYRCLE’s risk of bias tool for animal studies. BMC Medical Research Methodology, vol. 14, no. 1, pp. 43. http://dx.doi.org/10.1186/1471-2288-14-43. PMid:24667063.
http://dx.doi.org/10.1186/1471-2288-14-4...
), risk of bias tool was used for the 18 studies selected for this review. The “yes” judgment indicates that the risk of bias is low and the “no” judgment indicates a high degree of risk of bias. If the details of the report are insufficient to assess the appropriate risk of bias, the judgment will be “unclear” Table 3.

Table 3
Risk of bias of the included animal studies, assessed according to the SYRCLE guideline.

3. Results

A total of 2,448 papers were selected from the five databases searched. Of these, 347 were excluded due to duplicated titles and 2,064 after reading the abstracts, as they did not fit the defined inclusion criteria. After the full-text reading, of the 37 remaining articles, 18 studies were considered eligible and were included in the review (Figure 1).

Figure 1
Flowchart of the search result in the information sources, the selection and inclusion of the original articles in the systematic review (Moher et al., 2009MOHER, D., LIBERATI, A., TETZLAFF, J. and ALTMAN, D.G., 2009. Reprint-preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Physical Therapy, vol. 89, no. 9, pp. 873-880. http://dx.doi.org/10.1093/ptj/89.9.873. PMid:19723669.
http://dx.doi.org/10.1093/ptj/89.9.873...
).

The results tabulated in the present study were: identification of the work (main author and year); species of animal that served as the study model; age and gender; high-fat diet composition; period of exposure to the diet; onion type and experimental methodology used; exposure period of onion, bulb, oil or tea or peel powder; dosage used of onion, bulb, oil or tea or peel powder; and main results (Table 2).

In 83% of the articles, male animals were used, 1 study used female animals and 2 studies did not report the gender of the animal. In 66.6% of the studies Wistar or Sprague-Dawley rats were used and in 33.3% C57BL/6 and Balb/c mice, aged three to nine weeks, were considered young animals. The percentage of fat in the high-fat diets varied between 5.1% and 60% and the period of exposure to this diet varied between 4 and 18 weeks. The period of exposure to onion or its by-products varied between 4 and 12 weeks.

The main benefits of onion and its by-products, found in this review, lipid profile and cardiovascular risk with decreased total cholesterol, low-density lipoprotein cholesterol (LDL-C), triglycerides (TG), atherosclerosis index and aorta elastic modulus, and increased high-density lipoprotein cholesterol (HDL-C) (Hamauzu et al., 2011HAMAUZU, Y., NOSAKA, T., ITO, F., SUZUKI, T., TORISU, S., HASHIDA, M., FUKUZAWA, A., OHGUCHI, M. and YAMANAKA, S., 2011. Physicochemical characteristics of rapidly dried onion powder and its anti-atherogenic effect on rats fed high-fat diet. Food Chemistry, vol. 129, no. 3, pp. 810-815. http://dx.doi.org/10.1016/j.foodchem.2011.05.027. PMid:25212303.
http://dx.doi.org/10.1016/j.foodchem.201...
; Benítez et al., 2012BENÍTEZ, V., MOLLÁ, E., MARTÍN-CABREJAS, M.A., AGUILERA, Y., LÓPEZ-ANDRÉU, F.J. and ESTEBAN, R.M., 2012. Onion (Allium cepa L.) by-products as source of dietary Wber: physicochemical properties and effect on serum lipid levels in high-fat fed rats. European Food Research and Technology, vol. 234, no. 4, pp. 617-625. http://dx.doi.org/10.1007/s00217-012-1674-2.
http://dx.doi.org/10.1007/s00217-012-167...
; Matsunaga et al., 2014MATSUNAGA, S., AZUMA, K., WATANABE, M., TSUKA, T., IMAGAWA, T., OSAKI, T. and OKAMOTO, Y., 2014. Onion peel tea ameliorates obesity and affects blood parameters in a mouse model of high-fat-diet-induced obesity. Experimental and Therapeutic Medicine, vol. 7, no. 2, pp. 379-382. http://dx.doi.org/10.3892/etm.2013.1433. PMid:24396409.
http://dx.doi.org/10.3892/etm.2013.1433...
; Emamat et al., 2018EMAMAT, H., FOROUGHI, F., EINI-ZINAB, H. and HEKMATDOOST, A., 2018. The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry, vol. 33, no. 1, pp. 75-80. http://dx.doi.org/10.1007/s12291-017-0636-7. PMid:29371773.
http://dx.doi.org/10.1007/s12291-017-063...
; Yang et al., 2018YANG, C., LI, L., YANG, L., LǙ, H., WANG, S. and SUN, G., 2018. Anti-obesity and Hypolipidemic effects of garlic oil and onion oil in rats fed a high-fat diet. Nutrition & Metabolism, vol. 15, no. 1, pp. 43. http://dx.doi.org/10.1186/s12986-018-0275-x. PMid:29951108.
http://dx.doi.org/10.1186/s12986-018-027...
; Grzelak-Błaszczyk et al., 2020GRZELAK-BŁASZCZYK, K., MILALA, J., KOLODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KOSMALA, M., KLEWICKI, R., FOTSCHKI, B., JURGOŃSKI, A. and JUŚKIEWICZ, J., 2020. Onion protocatechuic acid and quercetin glucosides attenuate changes induced by high fat diet in rats. Food & Function, vol. 4, no. 4, pp. 3585-3597. http://dx.doi.org/10.1039/C9FO02633A.
http://dx.doi.org/10.1039/C9FO02633A...
; Yu et al., 2021YU, S., LI, H., CUI, T., CUI, M., PIAO, C., WANG, S., JU, M., LIU, X., ZHOU, G., XU, H. and LI, G., 2021. Onion (Allium cepa L.) peel extract effects on 3T3-L1 adipocytes and high-fat diet-induced obese mice. Food Bioscience, vol. 41, pp. 101019. http://dx.doi.org/10.1016/j.fbio.2021.101019.
http://dx.doi.org/10.1016/j.fbio.2021.10...
; Momoh et al., 2022MOMOH, B.J., OKERE, S.O. and ANYANWU, G.O., 2022. The anti-obesity effect of Allium cepa L. leaves on high fat diet induced obesity in male wistar rats. Clinical Complementary Medicine and Pharmacology., vol. 2, no. 3, pp. 100035. http://dx.doi.org/10.1016/j.ccmp.2022.100035.
http://dx.doi.org/10.1016/j.ccmp.2022.10...
; Chang et al., 2022CHANG, W., LIU, P.-Y., YEH, S. and LEE, H., 2022. Effects of dried onion powder and quercetin on obesity-associated hepatic menifestation and retinopathy. International Journal of Molecular Sciences, vol. 23, no. 19, pp. 11091. http://dx.doi.org/10.3390/ijms231911091.
http://dx.doi.org/10.3390/ijms231911091...
).

Decreased or non-altered mesenteric, epididymal, perirenal, retroperitoneal, inguinal, and weight gain adiposity were also observed (Lee et al., 2012LEE, S.-M., MOON, J., DO, H.J., CHUNG, J.H., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Onion peel extract increases hepatic low-density lipoprotein receptor and ATP-binding cassette transporter A1 messenger RNA expressions in Sprague-Dawley rats fed a high-fat diet. Nutrition Research (New York, N.Y.), vol. 32, no. 3, pp. 210-217. http://dx.doi.org/10.1016/j.nutres.2012.01.004. PMid:22464808.
http://dx.doi.org/10.1016/j.nutres.2012....
; Benítez et al., 2012BENÍTEZ, V., MOLLÁ, E., MARTÍN-CABREJAS, M.A., AGUILERA, Y., LÓPEZ-ANDRÉU, F.J. and ESTEBAN, R.M., 2012. Onion (Allium cepa L.) by-products as source of dietary Wber: physicochemical properties and effect on serum lipid levels in high-fat fed rats. European Food Research and Technology, vol. 234, no. 4, pp. 617-625. http://dx.doi.org/10.1007/s00217-012-1674-2.
http://dx.doi.org/10.1007/s00217-012-167...
; Kim et al., 2012KIM, O.Y., LEE, S.-M., DO, H., MOON, J.W., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Influence of quercetin-rich onion peel extracts on adipokine expression in the visceral adipose tissue of rats. Phytotherapy Research, vol. 26, no. 3, pp. 432-437. http://dx.doi.org/10.1002/ptr.3570. PMid:21833991.
http://dx.doi.org/10.1002/ptr.3570...
; Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Matsunaga et al., 2014MATSUNAGA, S., AZUMA, K., WATANABE, M., TSUKA, T., IMAGAWA, T., OSAKI, T. and OKAMOTO, Y., 2014. Onion peel tea ameliorates obesity and affects blood parameters in a mouse model of high-fat-diet-induced obesity. Experimental and Therapeutic Medicine, vol. 7, no. 2, pp. 379-382. http://dx.doi.org/10.3892/etm.2013.1433. PMid:24396409.
http://dx.doi.org/10.3892/etm.2013.1433...
; Henagan et al., 2015HENAGAN, T.M., CEFALU, W.T., RIBNICKY, D.M., NOLAND, R.C., DUNVILLE, K., CAMPBELL, W.W., STEWART, L.K., FORNEY, L.A., GETTYS, T.W., CHANG, J.S. and MORRISON, C.D., 2015. In vivo effects of dietary quercetin and quercetin-rich red onion extract on skeletal muscle mitochondria, metabolism, and insulin sensitivity. Genes & Nutrition, vol. 10, no. 1, pp. 451. http://dx.doi.org/10.1007/s12263-014-0451-1. PMid:25542303.
http://dx.doi.org/10.1007/s12263-014-045...
; Emamat et al., 2016EMAMAT, H., FOROUGHI, F., EINI–ZINAB, H., TAGHIZADEH, M., RISMANCHI, M. and HEKMATDOOST, A., 2016. The effects of onion consumption on treatment of metabolic, histologic, and inflammatory features of nonalcoholic fatty liver disease. Journal of Diabetes and Metabolic Disorders, vol. 15, no. 1, pp. 25. http://dx.doi.org/10.1186/s40200-016-0248-4. PMid:27453880.
http://dx.doi.org/10.1186/s40200-016-024...
, 2018EMAMAT, H., FOROUGHI, F., EINI-ZINAB, H. and HEKMATDOOST, A., 2018. The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry, vol. 33, no. 1, pp. 75-80. http://dx.doi.org/10.1007/s12291-017-0636-7. PMid:29371773.
http://dx.doi.org/10.1007/s12291-017-063...
; Lee et al., 2017LEE, S.G., PARKS, J.S. and KANG, H.W., 2017. Quercetin, a functional compound of onion peel, remodels white adipocytes to brown-like adipocytes. The Journal of Nutritional Biochemistry, vol. 42, pp. 62-71. http://dx.doi.org/10.1016/j.jnutbio.2016.12.018. PMid:28131896.
http://dx.doi.org/10.1016/j.jnutbio.2016...
; Forney et al., 2018FORNEY, L.A., LENARD, N.R., STEWART, L.K. and HENAGAN, T.M., 2018. Dietary quercetin attenuates adipose tissue expansion and inflammation and alters adipocyte morphology in a tissue-specific manner. International Journal of Molecular Sciences, vol. 19, no. 3, pp. 895. http://dx.doi.org/10.3390/ijms19030895. PMid:29562620.
http://dx.doi.org/10.3390/ijms19030895...
; Yang et al., 2018YANG, C., LI, L., YANG, L., LǙ, H., WANG, S. and SUN, G., 2018. Anti-obesity and Hypolipidemic effects of garlic oil and onion oil in rats fed a high-fat diet. Nutrition & Metabolism, vol. 15, no. 1, pp. 43. http://dx.doi.org/10.1186/s12986-018-0275-x. PMid:29951108.
http://dx.doi.org/10.1186/s12986-018-027...
; Grzelak-Błaszczyk et al., 2018GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
; Yu et al., 2021YU, S., LI, H., CUI, T., CUI, M., PIAO, C., WANG, S., JU, M., LIU, X., ZHOU, G., XU, H. and LI, G., 2021. Onion (Allium cepa L.) peel extract effects on 3T3-L1 adipocytes and high-fat diet-induced obese mice. Food Bioscience, vol. 41, pp. 101019. http://dx.doi.org/10.1016/j.fbio.2021.101019.
http://dx.doi.org/10.1016/j.fbio.2021.10...
; Chang et al., 2022CHANG, W., LIU, P.-Y., YEH, S. and LEE, H., 2022. Effects of dried onion powder and quercetin on obesity-associated hepatic menifestation and retinopathy. International Journal of Molecular Sciences, vol. 23, no. 19, pp. 11091. http://dx.doi.org/10.3390/ijms231911091.
http://dx.doi.org/10.3390/ijms231911091...
).

Liver abnormalities were also attenuated, with decreases observed in liver enzymes alanine aminotransferase (ALT) and aspartate aminotransferase (AST), the degree of steatosis and lobular and portal inflammation (Emamat et al., 2016EMAMAT, H., FOROUGHI, F., EINI–ZINAB, H., TAGHIZADEH, M., RISMANCHI, M. and HEKMATDOOST, A., 2016. The effects of onion consumption on treatment of metabolic, histologic, and inflammatory features of nonalcoholic fatty liver disease. Journal of Diabetes and Metabolic Disorders, vol. 15, no. 1, pp. 25. http://dx.doi.org/10.1186/s40200-016-0248-4. PMid:27453880.
http://dx.doi.org/10.1186/s40200-016-024...
, 2018EMAMAT, H., FOROUGHI, F., EINI-ZINAB, H. and HEKMATDOOST, A., 2018. The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry, vol. 33, no. 1, pp. 75-80. http://dx.doi.org/10.1007/s12291-017-0636-7. PMid:29371773.
http://dx.doi.org/10.1007/s12291-017-063...
; Yang et al., 2018YANG, C., LI, L., YANG, L., LǙ, H., WANG, S. and SUN, G., 2018. Anti-obesity and Hypolipidemic effects of garlic oil and onion oil in rats fed a high-fat diet. Nutrition & Metabolism, vol. 15, no. 1, pp. 43. http://dx.doi.org/10.1186/s12986-018-0275-x. PMid:29951108.
http://dx.doi.org/10.1186/s12986-018-027...
; Grzelak-Błaszczyk et al., 2018GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
; Momoh et al., 2022MOMOH, B.J., OKERE, S.O. and ANYANWU, G.O., 2022. The anti-obesity effect of Allium cepa L. leaves on high fat diet induced obesity in male wistar rats. Clinical Complementary Medicine and Pharmacology., vol. 2, no. 3, pp. 100035. http://dx.doi.org/10.1016/j.ccmp.2022.100035.
http://dx.doi.org/10.1016/j.ccmp.2022.10...
; Chang et al., 2022CHANG, W., LIU, P.-Y., YEH, S. and LEE, H., 2022. Effects of dried onion powder and quercetin on obesity-associated hepatic menifestation and retinopathy. International Journal of Molecular Sciences, vol. 23, no. 19, pp. 11091. http://dx.doi.org/10.3390/ijms231911091.
http://dx.doi.org/10.3390/ijms231911091...
).

Inflammatory and metabolic parameters were reduced by the addition of onion or its by-products, as seen in the expression of pro-inflammatory cytokine Tumor Necrosis Factor alpha (TNFα), Interleukin 6 (IL-6), Cluster of differentiation 11b (Cd11b), Cluster of differentiation 68 (Cd68), respectively, Monocyte chemoattractant protein 1 (Mcp-1), and factors such as peroxisome proliferator-activated receptor-gamma (PPARγ), fatty acid synthase (FAS), and acetyl CoA carboxylase (ACC), as well as a decrease in leptin, insulin, and glucose, with increased expression of the uncoupling protein (UCP-1), PR domain containing 16 (PRDM16), and cell death-inducing DNA fragmentation factor-alpha-like effector A (CIDEA), followed by an increase in mitochondria, and multilocular adipocytes in white adipose tissue (Lee et al., 2012LEE, S.-M., MOON, J., DO, H.J., CHUNG, J.H., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Onion peel extract increases hepatic low-density lipoprotein receptor and ATP-binding cassette transporter A1 messenger RNA expressions in Sprague-Dawley rats fed a high-fat diet. Nutrition Research (New York, N.Y.), vol. 32, no. 3, pp. 210-217. http://dx.doi.org/10.1016/j.nutres.2012.01.004. PMid:22464808.
http://dx.doi.org/10.1016/j.nutres.2012....
; Kim et al., 2012KIM, O.Y., LEE, S.-M., DO, H., MOON, J.W., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Influence of quercetin-rich onion peel extracts on adipokine expression in the visceral adipose tissue of rats. Phytotherapy Research, vol. 26, no. 3, pp. 432-437. http://dx.doi.org/10.1002/ptr.3570. PMid:21833991.
http://dx.doi.org/10.1002/ptr.3570...
; Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Matsunaga et al., 2014MATSUNAGA, S., AZUMA, K., WATANABE, M., TSUKA, T., IMAGAWA, T., OSAKI, T. and OKAMOTO, Y., 2014. Onion peel tea ameliorates obesity and affects blood parameters in a mouse model of high-fat-diet-induced obesity. Experimental and Therapeutic Medicine, vol. 7, no. 2, pp. 379-382. http://dx.doi.org/10.3892/etm.2013.1433. PMid:24396409.
http://dx.doi.org/10.3892/etm.2013.1433...
; Henagan et al., 2015HENAGAN, T.M., CEFALU, W.T., RIBNICKY, D.M., NOLAND, R.C., DUNVILLE, K., CAMPBELL, W.W., STEWART, L.K., FORNEY, L.A., GETTYS, T.W., CHANG, J.S. and MORRISON, C.D., 2015. In vivo effects of dietary quercetin and quercetin-rich red onion extract on skeletal muscle mitochondria, metabolism, and insulin sensitivity. Genes & Nutrition, vol. 10, no. 1, pp. 451. http://dx.doi.org/10.1007/s12263-014-0451-1. PMid:25542303.
http://dx.doi.org/10.1007/s12263-014-045...
; Emamat et al., 2016EMAMAT, H., FOROUGHI, F., EINI–ZINAB, H., TAGHIZADEH, M., RISMANCHI, M. and HEKMATDOOST, A., 2016. The effects of onion consumption on treatment of metabolic, histologic, and inflammatory features of nonalcoholic fatty liver disease. Journal of Diabetes and Metabolic Disorders, vol. 15, no. 1, pp. 25. http://dx.doi.org/10.1186/s40200-016-0248-4. PMid:27453880.
http://dx.doi.org/10.1186/s40200-016-024...
, 2018EMAMAT, H., FOROUGHI, F., EINI-ZINAB, H. and HEKMATDOOST, A., 2018. The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry, vol. 33, no. 1, pp. 75-80. http://dx.doi.org/10.1007/s12291-017-0636-7. PMid:29371773.
http://dx.doi.org/10.1007/s12291-017-063...
; Forney et al., 2018FORNEY, L.A., LENARD, N.R., STEWART, L.K. and HENAGAN, T.M., 2018. Dietary quercetin attenuates adipose tissue expansion and inflammation and alters adipocyte morphology in a tissue-specific manner. International Journal of Molecular Sciences, vol. 19, no. 3, pp. 895. http://dx.doi.org/10.3390/ijms19030895. PMid:29562620.
http://dx.doi.org/10.3390/ijms19030895...
).

Of the studies selected for this review, 13% showed an increase in the total concentration of short chain fatty acids (SCFA), of intestinal enzymes such as β-glucosidase and β-glucuronidase and of propionic and butyric acid in groups supplemented with onion or its by-products (Grzelak-Błaszczyk et al., 2018GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
, 2020GRZELAK-BŁASZCZYK, K., MILALA, J., KOLODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KOSMALA, M., KLEWICKI, R., FOTSCHKI, B., JURGOŃSKI, A. and JUŚKIEWICZ, J., 2020. Onion protocatechuic acid and quercetin glucosides attenuate changes induced by high fat diet in rats. Food & Function, vol. 4, no. 4, pp. 3585-3597. http://dx.doi.org/10.1039/C9FO02633A.
http://dx.doi.org/10.1039/C9FO02633A...
).

In addition, it should be noted that the papers that composed this review reached 50% to 85% of the items recommended by the ARRIVE protocol (Table 2). In assessing the risk of bias, it was observed that 50% of the questions in the SYRCLE protocol, were positively filled by all selected articles, considering a low risk of bias. However, all studies showed inadequacies in 20% of the questions related to Allocation Concealment and Performance Blinding, presenting a high risk of bias. It was also observed that 30% of the questions related to Random outcome assessment, Blinding of outcome assessment and Selective outcome reporting, were unclear in all studies in this review (Table 3).

4. Discussion

Excessive consumption of high saturated fat diets is associated with obesity, predisposing the individual to the appearance of metabolic and inflammatory changes. One way to mitigate the negative effects caused by the consumption of a high-fat diet is the addition of onion or its by-products in the diet, as onion contains elements such as quercetin, a well-studied flavonoid that may contribute to the prevention or treatment of diseases. The most studied forms of quercetin are aglycone (free form), quercetin monoglycosides, and quercetin diglycosides. The onion peel has a higher concentration of quercetin aglycone compared to the whole onion, which may be related to the hydrolysis of quercetin glycosides during the formation of the peel (Grzelak-Błaszczyk et al., 2018GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
; Xu et al., 2019XU, D., HU, M.-J., WANG, Y.-Q. and CUI, Y.-L., 2019. Antioxidant activities of quercetin and its complexes for medicinal application. Molecules (Basel, Switzerland), vol. 24, no. 6, pp. 1123. http://dx.doi.org/10.3390/molecules24061123. PMid:30901869.
http://dx.doi.org/10.3390/molecules24061...
). This vegetable and its by-products are rich in fiber and also contain other flavonoids, such as kampferol and protocatechuic acid, both of which exert their own health benefits (Slimestad et al., 2007SLIMESTAD, R., FOSSEN, T. and VAGEN, I.M., 2007. Onions: a source of unique dietary flavonoids. Journal of Agricultural and Food Chemistry, vol. 55, no. 25, pp. 10067-10080. http://dx.doi.org/10.1021/jf0712503. PMid:17997520.
http://dx.doi.org/10.1021/jf0712503...
; Hamauzu et al., 2011HAMAUZU, Y., NOSAKA, T., ITO, F., SUZUKI, T., TORISU, S., HASHIDA, M., FUKUZAWA, A., OHGUCHI, M. and YAMANAKA, S., 2011. Physicochemical characteristics of rapidly dried onion powder and its anti-atherogenic effect on rats fed high-fat diet. Food Chemistry, vol. 129, no. 3, pp. 810-815. http://dx.doi.org/10.1016/j.foodchem.2011.05.027. PMid:25212303.
http://dx.doi.org/10.1016/j.foodchem.201...
; Benítez et al., 2012BENÍTEZ, V., MOLLÁ, E., MARTÍN-CABREJAS, M.A., AGUILERA, Y., LÓPEZ-ANDRÉU, F.J. and ESTEBAN, R.M., 2012. Onion (Allium cepa L.) by-products as source of dietary Wber: physicochemical properties and effect on serum lipid levels in high-fat fed rats. European Food Research and Technology, vol. 234, no. 4, pp. 617-625. http://dx.doi.org/10.1007/s00217-012-1674-2.
http://dx.doi.org/10.1007/s00217-012-167...
; Lee et al., 2012LEE, S.-M., MOON, J., DO, H.J., CHUNG, J.H., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Onion peel extract increases hepatic low-density lipoprotein receptor and ATP-binding cassette transporter A1 messenger RNA expressions in Sprague-Dawley rats fed a high-fat diet. Nutrition Research (New York, N.Y.), vol. 32, no. 3, pp. 210-217. http://dx.doi.org/10.1016/j.nutres.2012.01.004. PMid:22464808.
http://dx.doi.org/10.1016/j.nutres.2012....
; Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Matsunaga et al., 2014MATSUNAGA, S., AZUMA, K., WATANABE, M., TSUKA, T., IMAGAWA, T., OSAKI, T. and OKAMOTO, Y., 2014. Onion peel tea ameliorates obesity and affects blood parameters in a mouse model of high-fat-diet-induced obesity. Experimental and Therapeutic Medicine, vol. 7, no. 2, pp. 379-382. http://dx.doi.org/10.3892/etm.2013.1433. PMid:24396409.
http://dx.doi.org/10.3892/etm.2013.1433...
; Emamat et al., 2016EMAMAT, H., FOROUGHI, F., EINI–ZINAB, H., TAGHIZADEH, M., RISMANCHI, M. and HEKMATDOOST, A., 2016. The effects of onion consumption on treatment of metabolic, histologic, and inflammatory features of nonalcoholic fatty liver disease. Journal of Diabetes and Metabolic Disorders, vol. 15, no. 1, pp. 25. http://dx.doi.org/10.1186/s40200-016-0248-4. PMid:27453880.
http://dx.doi.org/10.1186/s40200-016-024...
, 2018EMAMAT, H., FOROUGHI, F., EINI-ZINAB, H. and HEKMATDOOST, A., 2018. The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry, vol. 33, no. 1, pp. 75-80. http://dx.doi.org/10.1007/s12291-017-0636-7. PMid:29371773.
http://dx.doi.org/10.1007/s12291-017-063...
; Grzelak-Błaszczyk et al., 2018GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
; Yang et al., 2018YANG, C., LI, L., YANG, L., LǙ, H., WANG, S. and SUN, G., 2018. Anti-obesity and Hypolipidemic effects of garlic oil and onion oil in rats fed a high-fat diet. Nutrition & Metabolism, vol. 15, no. 1, pp. 43. http://dx.doi.org/10.1186/s12986-018-0275-x. PMid:29951108.
http://dx.doi.org/10.1186/s12986-018-027...
). This systematic review evaluated a number of studies that investigated the effects of onion or its by-products singly or in combination with garlic oil, either at different doses or exposure periods, but always added to a high-fat diet. Studies have also shown that onion or its by-products, reduced the deleterious health effects of high-fat diet (Figure 2).

Figure 2
Graphical Abstract. Onions and their by-products mitigated the effects of consuming a high-fat diet in different organs, tissues, and cells. In the intestine, there was an increase in intestinal enzymes, short-chain fatty acids, and a decrease in digestive pH. In the liver, the degree of steatosis was reduced, as well as liver enzymes and the expression of TNF-α, a pro-inflammatory cytokine. In the heart, there was a reduction in the rates of atherosclerosis I and II, in the modulation and elasticity of the aorta, and an improvement in the lipid profile. At the mitochondrial level, there was an increase in Pgc-1 and a decrease in mitochondrial genes with quercetin supplementation but not with onion extract. There was an increase in genes specific for brown adipose tissue in white adipose tissues, genes such as UCP-1, PRDM16, and CIDEA. Thus, the use of these products may have additional implications for the prevention of pathologies related to obesity.

All selected papers in this review used male or female rats or mice, aged three to nine weeks, being considered young animals. These animals were exposed to a high-fat diet with onion peel powder, bulb, oil, leaves or tea added at different periods, ranging from 4 to 18 weeks. The amount of onion peel and leaves powder also varied between the authors studied, from 0.2% to 20%, onion extract varying in mg (17mg) and percentage (0.21% to 0.44%) and the onion peel tea varied from 46.3 mg/kg to 92 mg/kg animal weight. Independent of the amount of onion or its by-products used, the introduction of this vegetable brought benefits to the supplemented animals.

To analyze the quality of the papers, we used the ARRIVE protocol, specific for experimental studies (Percie Du Sert et al., 2020PERCIE DU SERT, N., HURST, V., AHLUWALIA, A., ALAM, S., AVEY, M.T., BAKER, M., BROWNE, W.J., CLARK, A., CUTHILL, I.C. and DIRNAGL, U., 2020. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biology, vol. 18, no. 7, pp. e3000410. http://dx.doi.org/10.1371/journal.pbio.3000410. PMid:32663219.
http://dx.doi.org/10.1371/journal.pbio.3...
). Most articles in this review were found to meet more than 50% of the ARRIVE checklist with most of the criteria not met being related to the absence of facilities description, animal veterinary conditions, and the description of scientific implications such as study limitations.

There was a risk of bias in the selected studies when related to Allocation Concealment and Performance Blinding. Some studies were evaluated with unclear risk for evaluation Random outcome assessment, Blinding of outcome assessment and Selective outcome reporting. However, most articles had a low risk of bias in 50% of the questions in the SYRCLE assessment.

Onion is known for its antioxidant, anti-obesity, anti-inflammatory, and prebiotic powers. These attributes are mainly due to the presence of quercetin, a highly studied flavonoid with important functional characteristics (Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Nabavi et al., 2015NABAVI, S.F., RUSSO, G.L., DAGLIA, M. and NABAVI, S.M., 2015. Role of quercetin as an alternative for obesity treatment: you are what you eat. Food Chemistry, vol. 179, pp. 305-310. http://dx.doi.org/10.1016/j.foodchem.2015.02.006. PMid:25722169.
http://dx.doi.org/10.1016/j.foodchem.201...
; Forney et al., 2018FORNEY, L.A., LENARD, N.R., STEWART, L.K. and HENAGAN, T.M., 2018. Dietary quercetin attenuates adipose tissue expansion and inflammation and alters adipocyte morphology in a tissue-specific manner. International Journal of Molecular Sciences, vol. 19, no. 3, pp. 895. http://dx.doi.org/10.3390/ijms19030895. PMid:29562620.
http://dx.doi.org/10.3390/ijms19030895...
; Fraga et al., 2019FRAGA, C.G., CROFT, K.D., KENNEDY, D.O. and TOMÁS-BARBERÁN, F.A., 2019. The effects of polyphenols and other bioactives on human health. Food & Function, vol. 10, no. 2, pp. 514-528. http://dx.doi.org/10.1039/C8FO01997E. PMid:30746536.
http://dx.doi.org/10.1039/C8FO01997E...
). This flavonoid is capable of eliminating free radicals due to its effect on the potentiation of antioxidant enzymes such as glutathione (GSH) and superoxide dismutase (SOD) (Hayek et al., 1997HAYEK, T., FUHRMAN, B., VAYA, J., ROSENBLAT, M., BELINKY, P., COLEMAN, R., ELIS, A. and AVIRAM, M., 1997. Reduced progression of atherosclerosis in apolipoprotein e-deficient mice following consumption of red wine, or its polyphenols Quercetin or Catechin, is associated with reduced susceptibility of LDL to oxidation and aggregation. Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 17, no. 11, pp. 2744-2752. http://dx.doi.org/10.1161/01.ATV.17.11.2744. PMid:9409251.
http://dx.doi.org/10.1161/01.ATV.17.11.2...
; Erden Inal and Kahraman, 2000ERDEN INAL, M. and KAHRAMAN, A., 2000. The protective effect of flavonol quercetin against ultraviolet a induced oxidative stress in rats. Toxicology, vol. 154, no. 1-3, pp. 21-29. http://dx.doi.org/10.1016/S0300-483X(00)00268-7. PMid:11118667.
http://dx.doi.org/10.1016/S0300-483X(00)...
; Kobori et al., 2015KOBORI, M., TAKAHASHI, Y., AKIMOTO, Y., SAKURAI, M., MATSUNAGA, I., NISHIMURO, H., IPPOUSHI, K., OIKE, H. and OHNISHI-KAMEYAMA, M., 2015. Chronic high intake of quercetin reduces oxidative stress and induces expression of the antioxidant enzymes in the liver and visceral adipose tissues in mice. Journal of Functional Foods, vol. 15, pp. 551-560. http://dx.doi.org/10.1016/j.jff.2015.04.006.
http://dx.doi.org/10.1016/j.jff.2015.04....
). In this process, the donation of electrons contributes to stabilizing these free radicals, thus reducing the oxidative stress and consequent associated diseases (Hayek et al., 1997HAYEK, T., FUHRMAN, B., VAYA, J., ROSENBLAT, M., BELINKY, P., COLEMAN, R., ELIS, A. and AVIRAM, M., 1997. Reduced progression of atherosclerosis in apolipoprotein e-deficient mice following consumption of red wine, or its polyphenols Quercetin or Catechin, is associated with reduced susceptibility of LDL to oxidation and aggregation. Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 17, no. 11, pp. 2744-2752. http://dx.doi.org/10.1161/01.ATV.17.11.2744. PMid:9409251.
http://dx.doi.org/10.1161/01.ATV.17.11.2...
; Erden Inal and Kahraman, 2000ERDEN INAL, M. and KAHRAMAN, A., 2000. The protective effect of flavonol quercetin against ultraviolet a induced oxidative stress in rats. Toxicology, vol. 154, no. 1-3, pp. 21-29. http://dx.doi.org/10.1016/S0300-483X(00)00268-7. PMid:11118667.
http://dx.doi.org/10.1016/S0300-483X(00)...
; Kobori et al., 2015KOBORI, M., TAKAHASHI, Y., AKIMOTO, Y., SAKURAI, M., MATSUNAGA, I., NISHIMURO, H., IPPOUSHI, K., OIKE, H. and OHNISHI-KAMEYAMA, M., 2015. Chronic high intake of quercetin reduces oxidative stress and induces expression of the antioxidant enzymes in the liver and visceral adipose tissues in mice. Journal of Functional Foods, vol. 15, pp. 551-560. http://dx.doi.org/10.1016/j.jff.2015.04.006.
http://dx.doi.org/10.1016/j.jff.2015.04....
). Quercetin, for example, can reduce the oxidation of LDL molecules due to the elimination of free radicals, thus preventing diseases such as atherosclerosis (Ji et al., 2019JI, Y., YIN, Y., LI, Z. and ZHANG, W., 2019. Gut microbiota-derived components and metabolites in the progression of Non-Alcoholic Fatty Liver Disease (NAFLD). Nutrients, vol. 11, no. 8, pp. 1712. http://dx.doi.org/10.3390/nu11081712. PMid:31349604.
http://dx.doi.org/10.3390/nu11081712...
).

In this review, 22% of the selected articles showed an improvement in the lipid profile, especially in LDL levels, of animals supplemented with onion oil compared to the group that was submitted only to a high-fat diet, confirming the protective effect of onion (Yang et al., 2018YANG, C., LI, L., YANG, L., LǙ, H., WANG, S. and SUN, G., 2018. Anti-obesity and Hypolipidemic effects of garlic oil and onion oil in rats fed a high-fat diet. Nutrition & Metabolism, vol. 15, no. 1, pp. 43. http://dx.doi.org/10.1186/s12986-018-0275-x. PMid:29951108.
http://dx.doi.org/10.1186/s12986-018-027...
). Also, studies have demonstrated improvements in all lipid profiles, with a decreased serum determination of total cholesterol and TG, and an increase in HDL-C, confirming that animals benefited from the powder, tea, oil or extracts of onion concentrated of protocatechuic acid (Benítez et al., 2012BENÍTEZ, V., MOLLÁ, E., MARTÍN-CABREJAS, M.A., AGUILERA, Y., LÓPEZ-ANDRÉU, F.J. and ESTEBAN, R.M., 2012. Onion (Allium cepa L.) by-products as source of dietary Wber: physicochemical properties and effect on serum lipid levels in high-fat fed rats. European Food Research and Technology, vol. 234, no. 4, pp. 617-625. http://dx.doi.org/10.1007/s00217-012-1674-2.
http://dx.doi.org/10.1007/s00217-012-167...
; Matsunaga et al., 2014MATSUNAGA, S., AZUMA, K., WATANABE, M., TSUKA, T., IMAGAWA, T., OSAKI, T. and OKAMOTO, Y., 2014. Onion peel tea ameliorates obesity and affects blood parameters in a mouse model of high-fat-diet-induced obesity. Experimental and Therapeutic Medicine, vol. 7, no. 2, pp. 379-382. http://dx.doi.org/10.3892/etm.2013.1433. PMid:24396409.
http://dx.doi.org/10.3892/etm.2013.1433...
; Emamat et al., 2018EMAMAT, H., FOROUGHI, F., EINI-ZINAB, H. and HEKMATDOOST, A., 2018. The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry, vol. 33, no. 1, pp. 75-80. http://dx.doi.org/10.1007/s12291-017-0636-7. PMid:29371773.
http://dx.doi.org/10.1007/s12291-017-063...
; Yang et al., 2018YANG, C., LI, L., YANG, L., LǙ, H., WANG, S. and SUN, G., 2018. Anti-obesity and Hypolipidemic effects of garlic oil and onion oil in rats fed a high-fat diet. Nutrition & Metabolism, vol. 15, no. 1, pp. 43. http://dx.doi.org/10.1186/s12986-018-0275-x. PMid:29951108.
http://dx.doi.org/10.1186/s12986-018-027...
; Grzelak-Błaszczyk et al., 2020GRZELAK-BŁASZCZYK, K., MILALA, J., KOLODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KOSMALA, M., KLEWICKI, R., FOTSCHKI, B., JURGOŃSKI, A. and JUŚKIEWICZ, J., 2020. Onion protocatechuic acid and quercetin glucosides attenuate changes induced by high fat diet in rats. Food & Function, vol. 4, no. 4, pp. 3585-3597. http://dx.doi.org/10.1039/C9FO02633A.
http://dx.doi.org/10.1039/C9FO02633A...
; Yu et al., 2021YU, S., LI, H., CUI, T., CUI, M., PIAO, C., WANG, S., JU, M., LIU, X., ZHOU, G., XU, H. and LI, G., 2021. Onion (Allium cepa L.) peel extract effects on 3T3-L1 adipocytes and high-fat diet-induced obese mice. Food Bioscience, vol. 41, pp. 101019. http://dx.doi.org/10.1016/j.fbio.2021.101019.
http://dx.doi.org/10.1016/j.fbio.2021.10...
; Chang et al., 2022CHANG, W., LIU, P.-Y., YEH, S. and LEE, H., 2022. Effects of dried onion powder and quercetin on obesity-associated hepatic menifestation and retinopathy. International Journal of Molecular Sciences, vol. 23, no. 19, pp. 11091. http://dx.doi.org/10.3390/ijms231911091.
http://dx.doi.org/10.3390/ijms231911091...
; Momoh et al.,2022MOMOH, B.J., OKERE, S.O. and ANYANWU, G.O., 2022. The anti-obesity effect of Allium cepa L. leaves on high fat diet induced obesity in male wistar rats. Clinical Complementary Medicine and Pharmacology., vol. 2, no. 3, pp. 100035. http://dx.doi.org/10.1016/j.ccmp.2022.100035.
http://dx.doi.org/10.1016/j.ccmp.2022.10...
).

Cardiovascular protection associated with the consumption of powder, oil or extracts of onion concentrated with protocatechuic acid and quercetin monoglycosides was also observed in the heart structure of rats, which showed benefits in the atherosclerosis index, as well as decreasing the elasticity of the aorta of these animals, even when combined with a high-fat diet (Hamauzu et al., 2011HAMAUZU, Y., NOSAKA, T., ITO, F., SUZUKI, T., TORISU, S., HASHIDA, M., FUKUZAWA, A., OHGUCHI, M. and YAMANAKA, S., 2011. Physicochemical characteristics of rapidly dried onion powder and its anti-atherogenic effect on rats fed high-fat diet. Food Chemistry, vol. 129, no. 3, pp. 810-815. http://dx.doi.org/10.1016/j.foodchem.2011.05.027. PMid:25212303.
http://dx.doi.org/10.1016/j.foodchem.201...
; Yang et al., 2018YANG, C., LI, L., YANG, L., LǙ, H., WANG, S. and SUN, G., 2018. Anti-obesity and Hypolipidemic effects of garlic oil and onion oil in rats fed a high-fat diet. Nutrition & Metabolism, vol. 15, no. 1, pp. 43. http://dx.doi.org/10.1186/s12986-018-0275-x. PMid:29951108.
http://dx.doi.org/10.1186/s12986-018-027...
; Grzelak-Błaszczyk et al., 2018GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
, 2020GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
).

Another important characteristic of onion is its anti-inflammatory effect. Inflammation may occur due to various stimuli, one of which may be the excessive consumption of a high saturated fat diet. This eating habit may predispose the individual to intestinal dysbiosis, with an increase in gram-negative bacteria, which has in its outermost layer the endotoxin called lipopolysaccharide (LPS). LPS binds to toll-like 4 membrane receptors (TLR4), increasing intestinal permeability, triggering inflammatory processes, and releasing pro-inflammatory cytokines such as TNFα and IL-6, as well as elevating nuclear factor kappa B (NF-Kb) levels (Poggi et al., 2007POGGI, M., BASTELICA, D., GUAL, P., IGLESIAS, M.A., GREMEAUX, T., KNAUF, C., PEIRETTI, F., VERDIER, M., JUHAN-VAGUE, I., TANTI, J.F., BURCELIN, R. and ALESSI, M.C., 2007. C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia, vol. 50, no. 6, pp. 1267-1276. http://dx.doi.org/10.1007/s00125-007-0654-8. PMid:17426960.
http://dx.doi.org/10.1007/s00125-007-065...
; Manco et al., 2010MANCO, M., PUTIGNANI, L. and BOTTAZZO, G.F., 2010. Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocrine Reviews, vol. 31, no. 6, pp. 817-844. http://dx.doi.org/10.1210/er.2009-0030. PMid:20592272.
http://dx.doi.org/10.1210/er.2009-0030...
; Guo et al., 2013GUO, S., AL-SADI, R., SAID, H.M. and MA, T.Y., 2013. Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. American Journal of Pathology, vol. 182, no. 2, pp. 375-387. http://dx.doi.org/10.1016/j.ajpath.2012.10.014. PMid:23201091.
http://dx.doi.org/10.1016/j.ajpath.2012....
; Ma et al., 2017MA, J., ZHOU, Q. and LI, H., 2017. Gut microbiota and nonalcoholic fatty liver disease: insights on mechanisms and therapy. Nutrients, vol. 9, no. 10, pp. 1124. http://dx.doi.org/10.3390/nu9101124. PMid:29035308.
http://dx.doi.org/10.3390/nu9101124...
). Quercetin, present in onion, significantly inhibits these inflammatory effects. This was confirmed in this review, with 20% of the studies showing that the onion, rich in this flavonoid, reduces the excretion of inflammatory cytokines, mainly TNFα and IL-6 (Emamat et al., 2016EMAMAT, H., FOROUGHI, F., EINI–ZINAB, H., TAGHIZADEH, M., RISMANCHI, M. and HEKMATDOOST, A., 2016. The effects of onion consumption on treatment of metabolic, histologic, and inflammatory features of nonalcoholic fatty liver disease. Journal of Diabetes and Metabolic Disorders, vol. 15, no. 1, pp. 25. http://dx.doi.org/10.1186/s40200-016-0248-4. PMid:27453880.
http://dx.doi.org/10.1186/s40200-016-024...
, 2018EMAMAT, H., FOROUGHI, F., EINI-ZINAB, H. and HEKMATDOOST, A., 2018. The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry, vol. 33, no. 1, pp. 75-80. http://dx.doi.org/10.1007/s12291-017-0636-7. PMid:29371773.
http://dx.doi.org/10.1007/s12291-017-063...
; Forney et al., 2018FORNEY, L.A., LENARD, N.R., STEWART, L.K. and HENAGAN, T.M., 2018. Dietary quercetin attenuates adipose tissue expansion and inflammation and alters adipocyte morphology in a tissue-specific manner. International Journal of Molecular Sciences, vol. 19, no. 3, pp. 895. http://dx.doi.org/10.3390/ijms19030895. PMid:29562620.
http://dx.doi.org/10.3390/ijms19030895...
).

Increased intestinal permeability, induced by the consumption of a high fat-diet, may be associated with the development of NAFLD, due to the increase of gram-negative bacteria that release lipopolysaccharides LPS (Poggi et al., 2007POGGI, M., BASTELICA, D., GUAL, P., IGLESIAS, M.A., GREMEAUX, T., KNAUF, C., PEIRETTI, F., VERDIER, M., JUHAN-VAGUE, I., TANTI, J.F., BURCELIN, R. and ALESSI, M.C., 2007. C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia, vol. 50, no. 6, pp. 1267-1276. http://dx.doi.org/10.1007/s00125-007-0654-8. PMid:17426960.
http://dx.doi.org/10.1007/s00125-007-065...
; Manco et al., 2010MANCO, M., PUTIGNANI, L. and BOTTAZZO, G.F., 2010. Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocrine Reviews, vol. 31, no. 6, pp. 817-844. http://dx.doi.org/10.1210/er.2009-0030. PMid:20592272.
http://dx.doi.org/10.1210/er.2009-0030...
; Guo et al., 2013GUO, S., AL-SADI, R., SAID, H.M. and MA, T.Y., 2013. Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. American Journal of Pathology, vol. 182, no. 2, pp. 375-387. http://dx.doi.org/10.1016/j.ajpath.2012.10.014. PMid:23201091.
http://dx.doi.org/10.1016/j.ajpath.2012....
). Increased LPS levels in the liver inhibit the fasting-induced adipose factor (Fiaf) that regulates lipoprotein lipase, whose function is to store fat in organs such as the liver and adipose tissue (Poggi et al., 2007POGGI, M., BASTELICA, D., GUAL, P., IGLESIAS, M.A., GREMEAUX, T., KNAUF, C., PEIRETTI, F., VERDIER, M., JUHAN-VAGUE, I., TANTI, J.F., BURCELIN, R. and ALESSI, M.C., 2007. C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia, vol. 50, no. 6, pp. 1267-1276. http://dx.doi.org/10.1007/s00125-007-0654-8. PMid:17426960.
http://dx.doi.org/10.1007/s00125-007-065...
; Aguirre and Venema, 2015AGUIRRE, M. and VENEMA, K., 2015. Does the gut microbiota contribute to obesity? Going beyond the gut feeling. Microorganisms, vol. 3, no. 2, pp. 213-235. http://dx.doi.org/10.3390/microorganisms3020213. PMid:27682087.
http://dx.doi.org/10.3390/microorganisms...
; Larsen et al., 2019LARSEN, N., SOUZA, C.B., KRYCH, L., CAHÚ, T.B., WIESE, M., KOT, W., HANSEN, K.M., BLENNOW, A., VENEMA, K. and JESPERSEN, L., 2019. Potential of pectins to beneficially modulate the gut microbiota depends on their structural properties. Frontiers in Microbiology, vol. 10, pp. 223. http://dx.doi.org/10.3389/fmicb.2019.00223. PMid:30828323.
http://dx.doi.org/10.3389/fmicb.2019.002...
). Studies using powder, oil or extracts of onion concentrated with quercetin monoglycosides showed an improvement in the activity scores of NAFLD, improving the degree of steatosis, decreasing hepatic ALT and AST enzymes and lobular and portal inflammation (Emamat et al., 2016EMAMAT, H., FOROUGHI, F., EINI–ZINAB, H., TAGHIZADEH, M., RISMANCHI, M. and HEKMATDOOST, A., 2016. The effects of onion consumption on treatment of metabolic, histologic, and inflammatory features of nonalcoholic fatty liver disease. Journal of Diabetes and Metabolic Disorders, vol. 15, no. 1, pp. 25. http://dx.doi.org/10.1186/s40200-016-0248-4. PMid:27453880.
http://dx.doi.org/10.1186/s40200-016-024...
, 2018EMAMAT, H., FOROUGHI, F., EINI-ZINAB, H. and HEKMATDOOST, A., 2018. The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry, vol. 33, no. 1, pp. 75-80. http://dx.doi.org/10.1007/s12291-017-0636-7. PMid:29371773.
http://dx.doi.org/10.1007/s12291-017-063...
; Yang et al., 2018YANG, C., LI, L., YANG, L., LǙ, H., WANG, S. and SUN, G., 2018. Anti-obesity and Hypolipidemic effects of garlic oil and onion oil in rats fed a high-fat diet. Nutrition & Metabolism, vol. 15, no. 1, pp. 43. http://dx.doi.org/10.1186/s12986-018-0275-x. PMid:29951108.
http://dx.doi.org/10.1186/s12986-018-027...
; Grzelak-Błaszczyk et al., 2018GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
; Yu et al., 2021YU, S., LI, H., CUI, T., CUI, M., PIAO, C., WANG, S., JU, M., LIU, X., ZHOU, G., XU, H. and LI, G., 2021. Onion (Allium cepa L.) peel extract effects on 3T3-L1 adipocytes and high-fat diet-induced obese mice. Food Bioscience, vol. 41, pp. 101019. http://dx.doi.org/10.1016/j.fbio.2021.101019.
http://dx.doi.org/10.1016/j.fbio.2021.10...
; Chang et al., 2022CHANG, W., LIU, P.-Y., YEH, S. and LEE, H., 2022. Effects of dried onion powder and quercetin on obesity-associated hepatic menifestation and retinopathy. International Journal of Molecular Sciences, vol. 23, no. 19, pp. 11091. http://dx.doi.org/10.3390/ijms231911091.
http://dx.doi.org/10.3390/ijms231911091...
; Momoh et al.,2022MOMOH, B.J., OKERE, S.O. and ANYANWU, G.O., 2022. The anti-obesity effect of Allium cepa L. leaves on high fat diet induced obesity in male wistar rats. Clinical Complementary Medicine and Pharmacology., vol. 2, no. 3, pp. 100035. http://dx.doi.org/10.1016/j.ccmp.2022.100035.
http://dx.doi.org/10.1016/j.ccmp.2022.10...
).

In addition to the benefits of quercetin, pectin, a soluble dietary fiber, is another important component present in onions, which may contribute to the balance of intestinal microbiota and the reduction of cardiovascular risks (Hamauzu et al., 2011HAMAUZU, Y., NOSAKA, T., ITO, F., SUZUKI, T., TORISU, S., HASHIDA, M., FUKUZAWA, A., OHGUCHI, M. and YAMANAKA, S., 2011. Physicochemical characteristics of rapidly dried onion powder and its anti-atherogenic effect on rats fed high-fat diet. Food Chemistry, vol. 129, no. 3, pp. 810-815. http://dx.doi.org/10.1016/j.foodchem.2011.05.027. PMid:25212303.
http://dx.doi.org/10.1016/j.foodchem.201...
; Benítez et al., 2012BENÍTEZ, V., MOLLÁ, E., MARTÍN-CABREJAS, M.A., AGUILERA, Y., LÓPEZ-ANDRÉU, F.J. and ESTEBAN, R.M., 2012. Onion (Allium cepa L.) by-products as source of dietary Wber: physicochemical properties and effect on serum lipid levels in high-fat fed rats. European Food Research and Technology, vol. 234, no. 4, pp. 617-625. http://dx.doi.org/10.1007/s00217-012-1674-2.
http://dx.doi.org/10.1007/s00217-012-167...
). This is because pectin is easily degraded by commensal bacteria in the gut, generating energy from the fermentation process and producing SCFA, primarily butyrate, which serve as an energy source for epithelial cells (Habinowski and Witters, 2001HABINOWSKI, S.A. and WITTERS, L.A., 2001. The effects of AICAR on adipocyte differentiation of 3T3-L1 cells. Biochemical and Biophysical Research Communications, vol. 286, no. 5, pp. 852-856. http://dx.doi.org/10.1006/bbrc.2001.5484. PMid:11527376.
http://dx.doi.org/10.1006/bbrc.2001.5484...
; Hamauzu et al., 2011HAMAUZU, Y., NOSAKA, T., ITO, F., SUZUKI, T., TORISU, S., HASHIDA, M., FUKUZAWA, A., OHGUCHI, M. and YAMANAKA, S., 2011. Physicochemical characteristics of rapidly dried onion powder and its anti-atherogenic effect on rats fed high-fat diet. Food Chemistry, vol. 129, no. 3, pp. 810-815. http://dx.doi.org/10.1016/j.foodchem.2011.05.027. PMid:25212303.
http://dx.doi.org/10.1016/j.foodchem.201...
; Guo et al., 2013GUO, S., AL-SADI, R., SAID, H.M. and MA, T.Y., 2013. Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. American Journal of Pathology, vol. 182, no. 2, pp. 375-387. http://dx.doi.org/10.1016/j.ajpath.2012.10.014. PMid:23201091.
http://dx.doi.org/10.1016/j.ajpath.2012....
). The formation of SCFA can inhibit the development of pathogenic bacteria and assist in intestinal immunity, improving their integrity and favoring adhesion of probiotic strains in the intestinal epithelium (Habinowski and Witters, 2001HABINOWSKI, S.A. and WITTERS, L.A., 2001. The effects of AICAR on adipocyte differentiation of 3T3-L1 cells. Biochemical and Biophysical Research Communications, vol. 286, no. 5, pp. 852-856. http://dx.doi.org/10.1006/bbrc.2001.5484. PMid:11527376.
http://dx.doi.org/10.1006/bbrc.2001.5484...
).

Fiber intake can provide benefits, such as reduced energy intake, increased satiety due to its viscosity, and gel formation, which may favor decreased intestinal absorption of food components such as fat, thereby reducing serum lipids and total cholesterol (Habinowski and Witters, 2001HABINOWSKI, S.A. and WITTERS, L.A., 2001. The effects of AICAR on adipocyte differentiation of 3T3-L1 cells. Biochemical and Biophysical Research Communications, vol. 286, no. 5, pp. 852-856. http://dx.doi.org/10.1006/bbrc.2001.5484. PMid:11527376.
http://dx.doi.org/10.1006/bbrc.2001.5484...
; Hamauzu et al., 2011HAMAUZU, Y., NOSAKA, T., ITO, F., SUZUKI, T., TORISU, S., HASHIDA, M., FUKUZAWA, A., OHGUCHI, M. and YAMANAKA, S., 2011. Physicochemical characteristics of rapidly dried onion powder and its anti-atherogenic effect on rats fed high-fat diet. Food Chemistry, vol. 129, no. 3, pp. 810-815. http://dx.doi.org/10.1016/j.foodchem.2011.05.027. PMid:25212303.
http://dx.doi.org/10.1016/j.foodchem.201...
; Benítez et al., 2012BENÍTEZ, V., MOLLÁ, E., MARTÍN-CABREJAS, M.A., AGUILERA, Y., LÓPEZ-ANDRÉU, F.J. and ESTEBAN, R.M., 2012. Onion (Allium cepa L.) by-products as source of dietary Wber: physicochemical properties and effect on serum lipid levels in high-fat fed rats. European Food Research and Technology, vol. 234, no. 4, pp. 617-625. http://dx.doi.org/10.1007/s00217-012-1674-2.
http://dx.doi.org/10.1007/s00217-012-167...
). In addition, the consumption of fiber-rich foods may benefit intestinal transit time with a decreased caecal pH due to fermentation by commensal bacteria producing SCFA, and thus improving constipation (Benítez et al., 2012BENÍTEZ, V., MOLLÁ, E., MARTÍN-CABREJAS, M.A., AGUILERA, Y., LÓPEZ-ANDRÉU, F.J. and ESTEBAN, R.M., 2012. Onion (Allium cepa L.) by-products as source of dietary Wber: physicochemical properties and effect on serum lipid levels in high-fat fed rats. European Food Research and Technology, vol. 234, no. 4, pp. 617-625. http://dx.doi.org/10.1007/s00217-012-1674-2.
http://dx.doi.org/10.1007/s00217-012-167...
; Grzelak-Błaszczyk et al., 2018GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
). In this review, an increase in SCFA was observed in animals supplemented with onion extract concentrated in quercetin and quercetin monoglycosides, with an increase in the concentrations of propionic and butyric acid (Grzelak-Błaszczyk et al., 2018GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
, 2020GRZELAK-BŁASZCZYK, K., MILALA, J., KOLODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KOSMALA, M., KLEWICKI, R., FOTSCHKI, B., JURGOŃSKI, A. and JUŚKIEWICZ, J., 2020. Onion protocatechuic acid and quercetin glucosides attenuate changes induced by high fat diet in rats. Food & Function, vol. 4, no. 4, pp. 3585-3597. http://dx.doi.org/10.1039/C9FO02633A.
http://dx.doi.org/10.1039/C9FO02633A...
). There was also an increase in intestinal enzymes such as β-glucosidase and β-glucuronidase, which can be associated with bacterial adaptation to higher levels of quercetin glycosides present in the diet (Grzelak-Błaszczyk et al., 2018GRZELAK-BŁASZCZYK, K., MILALA, J., KOSMALA, M., KOŁODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KLEWICKI, R., JUŚKIEWICZ, J., FOTSCHKI, B. and JURGOŃSKI, A., 2018. Onion quercetin monoglycosides alter microbial activity and increase antioxidant capacity. The Journal of Nutritional Biochemistry, vol. 56, pp. 81-88. http://dx.doi.org/10.1016/j.jnutbio.2018.02.002. PMid:29518727.
http://dx.doi.org/10.1016/j.jnutbio.2018...
, 2020GRZELAK-BŁASZCZYK, K., MILALA, J., KOLODZIEJCZYK, K., SÓJKA, M., CZARNECKI, A., KOSMALA, M., KLEWICKI, R., FOTSCHKI, B., JURGOŃSKI, A. and JUŚKIEWICZ, J., 2020. Onion protocatechuic acid and quercetin glucosides attenuate changes induced by high fat diet in rats. Food & Function, vol. 4, no. 4, pp. 3585-3597. http://dx.doi.org/10.1039/C9FO02633A.
http://dx.doi.org/10.1039/C9FO02633A...
).

The anti-obesity effect is another functional characteristic of quercetin, present in onion, and some authors claim that this flavonoid has an antiadipogenic effect due to the activation of adenosine monophosphate-activated protein kinase (AMPK) (Berg et al., 2001BERG, A.H., COMBS, T.P., DU, X., BROWNLEE, M. and SCHERER, P.E., 2001. The adipocyte secreted protein Acrp30 enhances hepatic insulin action. Nature Medicine, vol. 7, no. 8, pp. 947-953. http://dx.doi.org/10.1038/90992. PMid:11479628.
http://dx.doi.org/10.1038/90992...
; Devarshi et al., 2017DEVARSHI, P.P., JONES, A.D., TAYLOR, E., STEFANSKA, B. and HENAGAN, T.M., 2017. Quercetin and quercetin-rich red onion extract alter Pgc-1𝛼 promoter methylation and splice variant expression. PPAR Research, vol. 2017, pp. 3235693. PMid:28191013.). Quercetin can reduce adipocyte hyperplasia which is an important process for the development of metabolic syndrome (Berg et al., 2001BERG, A.H., COMBS, T.P., DU, X., BROWNLEE, M. and SCHERER, P.E., 2001. The adipocyte secreted protein Acrp30 enhances hepatic insulin action. Nature Medicine, vol. 7, no. 8, pp. 947-953. http://dx.doi.org/10.1038/90992. PMid:11479628.
http://dx.doi.org/10.1038/90992...
; Devarshi et al., 2017DEVARSHI, P.P., JONES, A.D., TAYLOR, E., STEFANSKA, B. and HENAGAN, T.M., 2017. Quercetin and quercetin-rich red onion extract alter Pgc-1𝛼 promoter methylation and splice variant expression. PPAR Research, vol. 2017, pp. 3235693. PMid:28191013.).

In this review, than 38.8% of the studies found benefits from the addition of onion powder, tea, oil, or extract concentrated in quercetin and monoglycoside quercetin to the diet, including reduced body weight and weight of epididymal, perirenal, mesenteric, inguinal, and retroperitoneal adipose tissues (Lee et al., 2012LEE, S.-M., MOON, J., DO, H.J., CHUNG, J.H., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Onion peel extract increases hepatic low-density lipoprotein receptor and ATP-binding cassette transporter A1 messenger RNA expressions in Sprague-Dawley rats fed a high-fat diet. Nutrition Research (New York, N.Y.), vol. 32, no. 3, pp. 210-217. http://dx.doi.org/10.1016/j.nutres.2012.01.004. PMid:22464808.
http://dx.doi.org/10.1016/j.nutres.2012....
; Benítez et al., 2012BENÍTEZ, V., MOLLÁ, E., MARTÍN-CABREJAS, M.A., AGUILERA, Y., LÓPEZ-ANDRÉU, F.J. and ESTEBAN, R.M., 2012. Onion (Allium cepa L.) by-products as source of dietary Wber: physicochemical properties and effect on serum lipid levels in high-fat fed rats. European Food Research and Technology, vol. 234, no. 4, pp. 617-625. http://dx.doi.org/10.1007/s00217-012-1674-2.
http://dx.doi.org/10.1007/s00217-012-167...
; Kim et al., 2012KIM, O.Y., LEE, S.-M., DO, H., MOON, J.W., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Influence of quercetin-rich onion peel extracts on adipokine expression in the visceral adipose tissue of rats. Phytotherapy Research, vol. 26, no. 3, pp. 432-437. http://dx.doi.org/10.1002/ptr.3570. PMid:21833991.
http://dx.doi.org/10.1002/ptr.3570...
; Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Matsunaga et al., 2014MATSUNAGA, S., AZUMA, K., WATANABE, M., TSUKA, T., IMAGAWA, T., OSAKI, T. and OKAMOTO, Y., 2014. Onion peel tea ameliorates obesity and affects blood parameters in a mouse model of high-fat-diet-induced obesity. Experimental and Therapeutic Medicine, vol. 7, no. 2, pp. 379-382. http://dx.doi.org/10.3892/etm.2013.1433. PMid:24396409.
http://dx.doi.org/10.3892/etm.2013.1433...
; Henagan et al., 2015HENAGAN, T.M., CEFALU, W.T., RIBNICKY, D.M., NOLAND, R.C., DUNVILLE, K., CAMPBELL, W.W., STEWART, L.K., FORNEY, L.A., GETTYS, T.W., CHANG, J.S. and MORRISON, C.D., 2015. In vivo effects of dietary quercetin and quercetin-rich red onion extract on skeletal muscle mitochondria, metabolism, and insulin sensitivity. Genes & Nutrition, vol. 10, no. 1, pp. 451. http://dx.doi.org/10.1007/s12263-014-0451-1. PMid:25542303.
http://dx.doi.org/10.1007/s12263-014-045...
; Forney et al., 2018FORNEY, L.A., LENARD, N.R., STEWART, L.K. and HENAGAN, T.M., 2018. Dietary quercetin attenuates adipose tissue expansion and inflammation and alters adipocyte morphology in a tissue-specific manner. International Journal of Molecular Sciences, vol. 19, no. 3, pp. 895. http://dx.doi.org/10.3390/ijms19030895. PMid:29562620.
http://dx.doi.org/10.3390/ijms19030895...
; Yang et al., 2018YANG, C., LI, L., YANG, L., LǙ, H., WANG, S. and SUN, G., 2018. Anti-obesity and Hypolipidemic effects of garlic oil and onion oil in rats fed a high-fat diet. Nutrition & Metabolism, vol. 15, no. 1, pp. 43. http://dx.doi.org/10.1186/s12986-018-0275-x. PMid:29951108.
http://dx.doi.org/10.1186/s12986-018-027...
; Yu et al., 2021YU, S., LI, H., CUI, T., CUI, M., PIAO, C., WANG, S., JU, M., LIU, X., ZHOU, G., XU, H. and LI, G., 2021. Onion (Allium cepa L.) peel extract effects on 3T3-L1 adipocytes and high-fat diet-induced obese mice. Food Bioscience, vol. 41, pp. 101019. http://dx.doi.org/10.1016/j.fbio.2021.101019.
http://dx.doi.org/10.1016/j.fbio.2021.10...
; Chang et al., 2022CHANG, W., LIU, P.-Y., YEH, S. and LEE, H., 2022. Effects of dried onion powder and quercetin on obesity-associated hepatic menifestation and retinopathy. International Journal of Molecular Sciences, vol. 23, no. 19, pp. 11091. http://dx.doi.org/10.3390/ijms231911091.
http://dx.doi.org/10.3390/ijms231911091...
). With regard to food intake, the animals that were exposed to onion presented an increased food efficiency index and decreased consumption, possibly related to the satiety provided by the dietary fiber intake, which may contribute to a reduction in weight (Benítez et al., 2012BENÍTEZ, V., MOLLÁ, E., MARTÍN-CABREJAS, M.A., AGUILERA, Y., LÓPEZ-ANDRÉU, F.J. and ESTEBAN, R.M., 2012. Onion (Allium cepa L.) by-products as source of dietary Wber: physicochemical properties and effect on serum lipid levels in high-fat fed rats. European Food Research and Technology, vol. 234, no. 4, pp. 617-625. http://dx.doi.org/10.1007/s00217-012-1674-2.
http://dx.doi.org/10.1007/s00217-012-167...
; Kim et al., 2012KIM, O.Y., LEE, S.-M., DO, H., MOON, J.W., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Influence of quercetin-rich onion peel extracts on adipokine expression in the visceral adipose tissue of rats. Phytotherapy Research, vol. 26, no. 3, pp. 432-437. http://dx.doi.org/10.1002/ptr.3570. PMid:21833991.
http://dx.doi.org/10.1002/ptr.3570...
). Also observed was an increased expression of adiponectin (in mesenteric adipose tissue), an adipokine secreted by adipocytes that exerts some protective effects which are anti-atherogenic and anti-inflammatory (Berg et al., 2001BERG, A.H., COMBS, T.P., DU, X., BROWNLEE, M. and SCHERER, P.E., 2001. The adipocyte secreted protein Acrp30 enhances hepatic insulin action. Nature Medicine, vol. 7, no. 8, pp. 947-953. http://dx.doi.org/10.1038/90992. PMid:11479628.
http://dx.doi.org/10.1038/90992...
; Kim et al., 2012KIM, O.Y., LEE, S.-M., DO, H., MOON, J.W., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Influence of quercetin-rich onion peel extracts on adipokine expression in the visceral adipose tissue of rats. Phytotherapy Research, vol. 26, no. 3, pp. 432-437. http://dx.doi.org/10.1002/ptr.3570. PMid:21833991.
http://dx.doi.org/10.1002/ptr.3570...
). The decreased expression of inflammatory genes such as Cd11b and Cd68 in inguinal adipose tissue and of McP-1 and IL-6 genes in epididymal adipose tissue in groups supplemented with onion extract attenuated the inflammatory effect of the high-fat diet (Forney et al., 2018FORNEY, L.A., LENARD, N.R., STEWART, L.K. and HENAGAN, T.M., 2018. Dietary quercetin attenuates adipose tissue expansion and inflammation and alters adipocyte morphology in a tissue-specific manner. International Journal of Molecular Sciences, vol. 19, no. 3, pp. 895. http://dx.doi.org/10.3390/ijms19030895. PMid:29562620.
http://dx.doi.org/10.3390/ijms19030895...
).

The positive effects of onion can also be observed with the increased expression of the uncoupling protein 1 (UCP-1), important in the thermogenesis process, suggesting that this vegetable can stimulate lipid catabolism, promoting fat burning (Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Lee et al., 2017LEE, S.G., PARKS, J.S. and KANG, H.W., 2017. Quercetin, a functional compound of onion peel, remodels white adipocytes to brown-like adipocytes. The Journal of Nutritional Biochemistry, vol. 42, pp. 62-71. http://dx.doi.org/10.1016/j.jnutbio.2016.12.018. PMid:28131896.
http://dx.doi.org/10.1016/j.jnutbio.2016...
). This process can occur by the action of quercetin on white and brown adipose tissue, in which this flavonoid activates AMPK which in turn activates PPARγ (Lee et al., 2012LEE, S.-M., MOON, J., DO, H.J., CHUNG, J.H., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Onion peel extract increases hepatic low-density lipoprotein receptor and ATP-binding cassette transporter A1 messenger RNA expressions in Sprague-Dawley rats fed a high-fat diet. Nutrition Research (New York, N.Y.), vol. 32, no. 3, pp. 210-217. http://dx.doi.org/10.1016/j.nutres.2012.01.004. PMid:22464808.
http://dx.doi.org/10.1016/j.nutres.2012....
; Kim et al., 2012KIM, O.Y., LEE, S.-M., DO, H., MOON, J.W., LEE, K.H., CHA, Y.J. and SHIN, M.J., 2012. Influence of quercetin-rich onion peel extracts on adipokine expression in the visceral adipose tissue of rats. Phytotherapy Research, vol. 26, no. 3, pp. 432-437. http://dx.doi.org/10.1002/ptr.3570. PMid:21833991.
http://dx.doi.org/10.1002/ptr.3570...
; Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
). This subsequently interacts with the gamma 1 peroxisome proliferator-activated receptor (Pgc-1α), its coactivator increases UCP-1 transcription, contributing to the browning of white adipose tissue and the activation of brown adipose tissue (Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Devarshi et al., 2017DEVARSHI, P.P., JONES, A.D., TAYLOR, E., STEFANSKA, B. and HENAGAN, T.M., 2017. Quercetin and quercetin-rich red onion extract alter Pgc-1𝛼 promoter methylation and splice variant expression. PPAR Research, vol. 2017, pp. 3235693. PMid:28191013.; Lee et al., 2017LEE, S.G., PARKS, J.S. and KANG, H.W., 2017. Quercetin, a functional compound of onion peel, remodels white adipocytes to brown-like adipocytes. The Journal of Nutritional Biochemistry, vol. 42, pp. 62-71. http://dx.doi.org/10.1016/j.jnutbio.2016.12.018. PMid:28131896.
http://dx.doi.org/10.1016/j.jnutbio.2016...
; Choi et al., 2018CHOI, H., KIM, C.-S. and YU, R., 2018. Quercetin upregulates uncoupling protein 1 in white/brown adipose tissues through sympathetic stimulation. Journal of Obesity & Metabolic Syndrome, vol. 27, no. 2, pp. 102-109. http://dx.doi.org/10.7570/jomes.2018.27.2.102. PMid:31089549.
http://dx.doi.org/10.7570/jomes.2018.27....
). This browning can be observed by the presence of multilocular adipocytes in white adipose tissue presenting morphology and functions similar to those found in brown adipose tissue (Forney et al., 2018FORNEY, L.A., LENARD, N.R., STEWART, L.K. and HENAGAN, T.M., 2018. Dietary quercetin attenuates adipose tissue expansion and inflammation and alters adipocyte morphology in a tissue-specific manner. International Journal of Molecular Sciences, vol. 19, no. 3, pp. 895. http://dx.doi.org/10.3390/ijms19030895. PMid:29562620.
http://dx.doi.org/10.3390/ijms19030895...
).

Other genes specific to brown adipose tissue showed greater expression in retroperitoneal and epididymal white adipose tissue, genes such as PRDM16 transcriptional co-regulator necessary for the development of brown and beige adipocytes, and CIDEA an important protein in the formation of lipid droplets brown and beige adipose tissue (Harms et al., 2014HARMS, M.J., ISHIBASHI, J., WANG, W., LIM, H.W., GOYAMA, S., SATO, T., KUROKAWA, M., WON, K.J. and SEALE, P., 2014. Prdm16 is required for the maintenance of brown adipocyte identity and function in adult mice. Cell Metabolism, vol. 19, no. 4, pp. 593-604. http://dx.doi.org/10.1016/j.cmet.2014.03.007. PMid:24703692.
http://dx.doi.org/10.1016/j.cmet.2014.03...
; Barneda et al., 2015BARNEDA, D., PLANAS-IGLESIAS, J., GASPAR, M.L., MOHAMMADYANI, D., PRASANNAN, S., DORMANN, D., HAN, G.S., JESCH, S.A., CARMAN, G.M., KAGAN, V., PARKER, M.G., KTISTAKIS, N.T., KLEIN-SEETHARAMAN, J., DIXON, A.M., HENRY, S.A. and CHRISTIAN, M., 2015. The brown adipocyte protein CIDEA promotes lipid droplet fusion via a phosphatidic acid-binding amphipathic helix. eLife, vol. 4, pp. e07485. http://dx.doi.org/10.7554/eLife.07485. PMid:26609809.
http://dx.doi.org/10.7554/eLife.07485...
; Lee et al., 2017LEE, S.G., PARKS, J.S. and KANG, H.W., 2017. Quercetin, a functional compound of onion peel, remodels white adipocytes to brown-like adipocytes. The Journal of Nutritional Biochemistry, vol. 42, pp. 62-71. http://dx.doi.org/10.1016/j.jnutbio.2016.12.018. PMid:28131896.
http://dx.doi.org/10.1016/j.jnutbio.2016...
).

The onion extract was also able to increase the number of mitochondria in skeletal muscle, improving fat metabolism, insulin sensitivity, and increasing energy expenditure (Henagan et al., 2015HENAGAN, T.M., CEFALU, W.T., RIBNICKY, D.M., NOLAND, R.C., DUNVILLE, K., CAMPBELL, W.W., STEWART, L.K., FORNEY, L.A., GETTYS, T.W., CHANG, J.S. and MORRISON, C.D., 2015. In vivo effects of dietary quercetin and quercetin-rich red onion extract on skeletal muscle mitochondria, metabolism, and insulin sensitivity. Genes & Nutrition, vol. 10, no. 1, pp. 451. http://dx.doi.org/10.1007/s12263-014-0451-1. PMid:25542303.
http://dx.doi.org/10.1007/s12263-014-045...
; Emamat et al., 2016EMAMAT, H., FOROUGHI, F., EINI–ZINAB, H., TAGHIZADEH, M., RISMANCHI, M. and HEKMATDOOST, A., 2016. The effects of onion consumption on treatment of metabolic, histologic, and inflammatory features of nonalcoholic fatty liver disease. Journal of Diabetes and Metabolic Disorders, vol. 15, no. 1, pp. 25. http://dx.doi.org/10.1186/s40200-016-0248-4. PMid:27453880.
http://dx.doi.org/10.1186/s40200-016-024...
, 2018EMAMAT, H., FOROUGHI, F., EINI-ZINAB, H. and HEKMATDOOST, A., 2018. The effects of onion consumption on prevention of nonalcoholic fatty liver disease. Indian Journal of Clinical Biochemistry, vol. 33, no. 1, pp. 75-80. http://dx.doi.org/10.1007/s12291-017-0636-7. PMid:29371773.
http://dx.doi.org/10.1007/s12291-017-063...
). There was also a reduction in mitochondrial genes Nd3, Nd4 (subunits of complex I), Cox1 (a subunit of complex IV) and Atp8 (a subunit of ATPsintase) in groups supplemented with quercetin, but not in those supplemented with onion extract, than can indicate changes in the oxidative phosphorylation system (OXPHOS) which is located in the inner mitochondrial membrane (Henagan et al., 2015HENAGAN, T.M., CEFALU, W.T., RIBNICKY, D.M., NOLAND, R.C., DUNVILLE, K., CAMPBELL, W.W., STEWART, L.K., FORNEY, L.A., GETTYS, T.W., CHANG, J.S. and MORRISON, C.D., 2015. In vivo effects of dietary quercetin and quercetin-rich red onion extract on skeletal muscle mitochondria, metabolism, and insulin sensitivity. Genes & Nutrition, vol. 10, no. 1, pp. 451. http://dx.doi.org/10.1007/s12263-014-0451-1. PMid:25542303.
http://dx.doi.org/10.1007/s12263-014-045...
; Bouchez and Devin, 2019BOUCHEZ, C. and DEVIN, A., 2019. Mitochondrial biogenesis and mitochondrial Reactive Oxygen Species (ROS): a complex relationship regulated by the cAMP/PKA signaling pathway. Cells, vol. 8, no. 4, pp. 287. http://dx.doi.org/10.3390/cells8040287. PMid:30934711.
http://dx.doi.org/10.3390/cells8040287...
).

The anti-obesity effect of onion and its by-products may be justified by the reduction of adipogenesis through pathways involved in lipid metabolism (Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
). Authors have shown in their experimental studies that the addition of onion peel extract reduced PPARγ expression as an adipogenesis transcription factor, thus contributing to decreased adipocyte proliferation (Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
). Also, PPARγ regulates the enzymes fatty acid synthase (FAS) and acetyl CoA carboxylase (ACC), consequently reducing the expression of these genes (Moon et al., 2013MOON, J., DO, H.-J., KIM, O.Y. and SHIN, M.J., 2013. Antiobesity effects of quercetin-rich onion peel extract on the differentiation of 3T3-L1 preadipocytes and the adipogenesis in high fat-fed rats. Food and Chemical Toxicology, vol. 58, pp. 347-354. http://dx.doi.org/10.1016/j.fct.2013.05.006. PMid:23684756.
http://dx.doi.org/10.1016/j.fct.2013.05....
; Lee et al., 2017LEE, S.G., PARKS, J.S. and KANG, H.W., 2017. Quercetin, a functional compound of onion peel, remodels white adipocytes to brown-like adipocytes. The Journal of Nutritional Biochemistry, vol. 42, pp. 62-71. http://dx.doi.org/10.1016/j.jnutbio.2016.12.018. PMid:28131896.
http://dx.doi.org/10.1016/j.jnutbio.2016...
).

The studies that make up this review show methodological differences, such as the use of different by-products, dosages, and administration periods, which made it impossible to carry out a meta-analysis due to the heterogeneity of the data. This review, demonstrated the importance of consuming onion and its by-products. Benefits related to the inflammatory parameters, obesity, cardiovascular disease, thermogenesis, and liver disorders were observed, associated with the consumption of a high-fat diet.

In conclusion, was observed the beneficial effects of onion or its by-products on inflammatory parameters, obesity, cardiovascular diseases, thermogenesis and hepatic alterations associated with the consumption of a high-fat diet. Thus, the use of these products may have further implications in preventing obesity-related pathologies. Despite these beneficial effects, the minimum amount sufficient to bring benefits or the limit amount /excessive that were able of causing damage to health were not shown in the studies. Therefore, further studies are needed to determine these issues.

Acknowledgements

The present study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant no. 425425/2018-5) and Coordenação de Aperfeiçoamento Pessoal de Nível Superior-Brazil (CAPES)- Finance code 001. Gabriele dos Santos Cordeiro was the recipient of a doctoral fellowship from FAPESB (Fundação de Amparo à Pesquisa do Estado da Bahia), Brazil.

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Publication Dates

  • Publication in this collection
    13 Feb 2023
  • Date of issue
    2023

History

  • Received
    18 July 2022
  • Accepted
    17 Jan 2023
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