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

Cordeiro, G. S.; Santos, L. S.; Vieira, G. P.; Espírito-Santo, D. A.; Teixeira, R. S.; Matos, R. J. B; Costa, C. A. S.; Deiró, T. C. B. J.; Barreto-Medeiros, J. M.

doi:10.1590/1519-6984.266108

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Original Article • Braz. J. Biol. 83 • 2023 • https://doi.org/10.1590/1519-6984.266108 linkcopy

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

Authorship SCIMAGO INSTITUTIONS RANKINGS

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

Criterion	Description
Population	Rat or mouse or mice
Intervention/exposure	Consumption of a high-fat diet and supplementation of the onion or its by-products
Comparison	The comparison groups were defined as follows: use of a diet rich in fat
Outcome	Any health-related outcome
Study design	Experimental studies in rats, mice, or mouse.

Main author / year	Animal species	Gender/ Age	Composition of the high fat diet	high fat diet exposure period	Onion characteristics and methodology used	Period of exposure to onion or its by-products	Quantity used of onion or its by-products	Main results	Final score of adequacy by ARRIVE
Chang et al. (2022)	Sprague Dawley	Male; 4 weeks	Fat: 43%	12 weeks	-Allium cepa L.	12 weeks	1% e 5% dried onion;	Onion powder Effects:	17/20
					- The onion pieces were lyophilized at 40°C for 24 hrs and gridded into fine poder. The quercetin was determined using high performance liquid chromatography.		180 mg/kg quercetin	- 1%, 5% and 180mg/kg quercetin:
								⁼ Energy intake;
								^↓ Epididymal, Perirenal and Mesenteric Mass;
								↓Total cholesterol, TG, LDL, Free fatty acid;
								↓TNF-α, IL-6, TBARS;
								↓Total cholesterol, TG, TNF-α, IL-6, TBARS in liver;
								- 1% or 5%:
								↓Subcutaneous adipose; adipocyte area epididymal;
								^↑SOD and Catalase;
								↓scores for damage of hepatic; protein expression of ACC-α and Ras;
								Feces: ↑Acetic and Butyric acid; Total cholesterol and TG;
								↓accumulation of lipids in the retina
Momoh et al. (2022)	Wistar	Male, Age not informed	Fat: 50%	12 weeks	-Allium cepa L.	28 days (4 weeks)	10% and 20%	Onion leaves Effects:	17/20
					- The onion leaves were sliced into tiny pieces and dried at temperature of 22 ± 2 ◦C, and blended into powder.			- 10% and 20%:
								= food intake;
								↓ Body Weight; Fat mass;
								↓ AST; Creatinine, Urea; glucose;
								=HDL; Uric acid;
								↓ Accumulation of lipids in liver;
								↓ Kidney inflammation;
								- 20%:
								↓Kidney weight; ALT;
								↓Total cholesterol, TG, LDL, and VLDL.
Yu et al. (2021)	C57BL/6J	Male, 6-8 weeks	Fat: 34.9% (Soybean Oil and Lard)	8 weeks	-Allium cepa L.	8 weeks	36 mg/kg; 90 mg/kg; 144 mg/kg;	Yellow onion peel extract Effects:	16/20
					- Yellow onion peel. The extraction with 5 L distilled water for 5 h at 80 ◦C.			- High and medium dose group (144mg/kg and 90mg/kg):
								↓ Body Weight;
								- Low, medium, and High dose group (36mg/kg, 90mg/kg and 144mg/kg):
								=Liver Mass; ↓Total cholesterol, TG and LDL; =HDL; ↓Total cholesterol, TG in liver;
								↓ Accumulation of lipids in liver;
								↓ Epididymal adipocytes;
								↓ PPARγ, C/EBPα, FAS, ACC, AP2, and SREBP1 expression;
								↓ PPARγ protein expression
Grzelak-Błaszczyk et al. (2020)	Wistar	Male; 4 weeks	Fat: 14% (Palm oil)	4 weeks	- No informed;	4 weeks	- HF+ Quercetin diglycosides = 0.44%;	HF+ Quercetin diglycosides Effects:	16/20
					- Yellow onion residues. The extraction with 50% water solution of ethanol, temperature was 35°C; time was 6 h.		- HF+ Quercetin monoglycosides = 0.34%;	↑ pH of digesta;
							- HF+ protocatechuic acid = 0.25%	↑ β-glucosidase day 7; ↓ β-galactosidase days 3,7,14 and 28; ↓ β-glucuronidase; ↓isovaleric and butyric; ↓ Total SCFA;
								↓ Liver Mass; ↓creatinine;
								HF+ Quercetin monoglycosides Effects:
								↓ Diet intake;
								↑ β-glucosidase day 3,7,14 and 28; ↑β-glucuronidase day 7,14 and 28; ↓ propionic and isobutyric; ↑Total SCFA;
								↓TG and atherogenic index II;
								HF+ protocatechuic acid Effects:
								↑β-glucuronidase day 7 and 28; ↓Total SCFA; ↓Liver Mass;
								↓Total cholesterol, TG and atherogenic index I and II; ↑HDL; ↓Uric acid.
Grzelak-Błaszczyk et al. (2018)	Wistar	Male; 4 weeks	Fat: 14% (Palm oil)	4 weeks	- No informed;	4 weeks	- HF+ Quercetin= 0.21%;	HF+ Quercetin Effects:	15/20
					- Yellow onion residues. The extraction with 50% water solution of ethanol, temperature was 35°C; time was 6 h.		- HF+ Quercetin monoglycosides = 0.36%;	= Body Weight;
								↓mass of colon tissue;
								↓Sucrase and Maltase; ↑lactose; ↑β-glucosidase, β-glucuronidase and β-galactosidase;↑SCFA (acetic, propionic and butyric);
								=TBARS;
								↑antioxidant capacity of lipid and of water fraction of serum;
								= glucose and AST; ↓ALT and atherogenic index II and urea.
								HF+ Quercetin monoglycosides Effects:
								= Body Weight;
								↓pH of digesta cecum and colon;
								↓ mass of colon tissue;
								↓Sucrase; ↑lactose; ↑β-glucosidase, β-glucuronidase and β-galactosidase;
								↑antioxidant capacity of water fraction of serum;
								↓ALT and atherogenic index II.
Emamat et al. (2018)	Sprague ‐ Dawley	Male;	Fat: 59%;	7 weeks	- No informed;	7 weeks	7%	↓ALT, AST, TG, glucose and insulin;	14/20
		Age not informed	Carbohydrate: 30%;		- Whole yellow onion powder. During powder processing, the leaves were heated to 200 ºC for 15 s and mechanically crushed into fragments of 500–2000µm.			= LDL-C e Total cholesterol;
			Protein: 11%					↓TNF-α gene expression in liver;
								↓ degree of hepatic steatosis in lobular and portal inflammation;
								= weight gain;
								#NOME?
Forney et al. (2018)	C57BL/6J	Gender not informed; 5 weeks	Fat: 45%;	9 weeks	- No informed;	9 weeks	17mg/kg	Red onion extract Effects:	15/20
					- Red onion extract in 80% ethanol, lyophilized to obtain the powder.			↓weight of inguinal and epididymal adipose tissue; ↓size of inguinal and epididymal adipocytes; ↑density of inguinal and epididymal adipocytes;
								↓Cd11b and Cd68, =Mcp-1 and F4/80 (inguinal);
								↑Cd11b, ↓Cd68 and Mcp-1 and =F4/80 (epididymal);
								= leptin and adiponectin; ↓ IL-6;
								↑ multilocular adipocytes (inguinal).
								Quercetin Effects:
								↓weight of inguinal and epididymal adipose tissue; ↓size of epididymal adipocytes; ↑ density of epididymal adipocytes;
								↓Cd11b and Cd68, =Mcp-1 and F4/80 (inguinal);
								=Cd11b, ↑Cd68, ↓Mcp-1 and =F4/80 (epididymal);
								↑ multilocular adipocytes (inguinal).
Yang et al. (2018)	Sprague ‐ Dawley	Male;	Casein: 20%; Sucrose: 25.3%; Fiber: 4%;	- No informed;	-Allium cepa L.;	60 days (8 weeks)	46.3 mg /kg/d and 92.6 mg/kg/ d	Onion Oil Effects:	15/20
		Age not informed	Lard: 10%;		- To obtain the oil, the onion bulbs were minced, soaked in distilled water 1.5 times at 35 °C for 2.5 h.			↓ weight gain; ↓ Lee index;
			Custard powder: 5%;					↓ weight of epididymal and perirenal adipose tissue;
			Cholesterol:1.5%					- High dose group (92.6mg/kg/d):↓TG, Total cholesterol and LDL-C;
								- High dose group (92.6mg/kg/d):↑HDL-C;
								↓ atherosclerosis index;
								↓ degree of hepatic steatosis;
								= food intake;
								↑ liver and kidney relative weight.
Devarshi et al. (2017)	C57BL / 6J	Male; 5 weeks	Fat: 45%	9 weeks	- No informed;	9 weeks	- 17mg/kg	↓ gene expression Pgc-1α-a;	out/20
					- Red onion peel extracts			↑ gene expression NT-Pgc-1α;
								↓ gene expression FL-Pgc-1α.
Lee et al. (2017)	C57BL / 6	Male; 4 weeks	Fat:60%	8 weeks	- No informed	8 weeks	0.50%	#NOME?	16/20
					- Onion peels were washed and air-dried overnight. Onion peel were pulverized for 3 min with 1 L of 60% aqueous ethanol as the extracting solvent.			= expression PPARγ and FAS (epididymal, retroperitoneal and subcutaneous adipose tissue); = TBX1 and CPT1α (epididymal, retroperitoneal and subcutaneous adipose tissue);
								↓ expression ACC (epididymal);
								↑ PRDM16, PGC1α and UCP1 (retroperitoneal);
								↑ CIDEA (retroperitoneal and subcutaneous)
Emamat et al. (2016)	Sprague ‐ Dawley	Male;	Fat:59%;	7 weeks	- No informed;	4 weeks	7%	↑ weight gain – control group + onion;	13/20
		Age not informed	Carbohydrate: 30%;		- Whole yellow onion powder. During powder processing, the leaves were heated to 200 ºC for 15 s and mechanically crushed into fragments of 500–2000µm.			↑ food intake – control group + onion;
			Protein: 11%					↓ ALT, TG, glucose and insulin;
								↓ TNFα gene expression in liver;
								#NOME?
Henagan et al. (2015)	C57BL / 6J	Gender not informed; 5 weeks	Fat:45%	9 weeks	- No informed;	9 weeks	17mg	Red onion extract and Quercetin Effects:	15/20
					- Red onion extract in 80% ethanol, lyophilized to obtain the powder.			= food intake;
								↓ body weight; ↓percent fat mass; ↑ muscle mass; ↓ insulin test;
								↑Energy expenditure; ↓ respiratory
								exchange ratio; ↑ Mitochondrial number;
								#NOME?
								determined by measuring acid
								soluble metabolites (ASM);
								↓ Nd3, Nd4, Cox1 and Atp8 (Only quercetin).
Matsunaga et al. (2014)	BALB/c	Male; 4 weeks	Fat: 32%	28 days (4 weeks)	- No informed;	28 days (4 weeks)	5%	Effects of onion peel tea:	11/20
					- lyophilized onion peel tea containing 1.15 mg / g quercetin			↓ body weight and weight of epididymal adipose tissue;
								↓ total cholesterol on day 14 and glucose and leptin on day 28. ↓ TG on day 14 and 28; ↑alkaline phosphatase on day 28;
								= ALT, AST, GGT or Alb on days 14 or 28.
Moon et al. (2013)	Sprague ‐ Dawley	Male;5 weeks	Fat: 40%	8 weeks	- No informed;	8 weeks	0.36% e 0.72%	Effects of onion extract (0.36% and 0.72%) on the high fat diet showed:	14/20
			Sucrose: 34%		- Onion peel extracts extracted with 60% aqueous ethanol solution (50 ° C, 3 hours).			↓final body weight and weight of mesenteric adipose tissue;
			Casein: 20%					= weight of perirenal and epididymal adipose tissuel; ↓feed efficiency ratio;
								↓ gene expression PPAR-γ, FAS e ACC;
								↑ CPT-1α;
								Effects of onion extract (0.72%):
								↓ retroperitoneal adipose tissue and visceral fat; ↓ C/EBP-α;
								Effects of onion extract (0.36%):
								↑ gene expression UCP-1.
Benítez et al. (2012)	Wistar	Female; 6 weeks	Glucose: 189g; Casein: 200g; butter: 370g; Cholesterol: 45g	4 weeks	- Allium cepa L.;	4 weeks	10%	Effects of onion bagasse on the high fat diet:	14/20
					- The onions were milled to obtain a “bagasse” added to the diet.			↓ body weight and food efficiency;
								↑food consumption;
								= weight of organs such as heart, kidney, intestine and spleen; all animals pallid colored liver and bigger livers;
								↓ total cholesterol and TG;
								↓ pH cecal content and fecal weight;
								↑ HDL-C.
Lee et al. (2012)	Sprague ‐ Dawley	Male; 3 weeks	Fat: 33%;	8 weeks	- No informed;	8 weeks	0.20%	↑ LDLR, SREBP-2, HMG-CoAR and staeroyl - coA desaturase 1 gene expression in liver; ↓ apolipoprotein A1;	out/20
			Sucrose: 10%		- Onion peel extracts extracted with 60% aqueous ethanol solution (50 ° C, 3 hours).			↑ gene expression PPARγ2 and ATP-binding cassette subfamily G member 1 (ABDG1);
			Casein: 20%					= body weight; = gene expression LXRα;
								↑ food efficiency; ↓ food consumption;
Hamauzu et al. (2011)	Wistar	Male; 9 weeks	Fat: 5.1%;	18 weeks	- Allium cepa L.;	18 weeks	5%	= body weight;	12/20
			Protein: 22.2%		- The powder was prepared from the external layer of the onion.			↓ modulus of elasticity of rat aorta;
								↓ atherogenic index;
								= TG, total cholesterol and HDL-C.
Kim et al. (2012)	Sprague ‐ Dawley	Male; 3 weeks	Sucrose: 10%;	8 weeks	- No informed;	8 weeks	0.20%	↓ food consumption; ↑ food efficiency index;	dez/20
			Casein: 20%; Cholesterol: 1%		- Onion peel extracts extracted with 60% aqueous ethanol solution.			= body weight; = weight of perirenal and epididymal adipose tissue;
			Corn oil: 6%					= liver enzymes, blood urea nitrogen and Creatinine; = IL-6 gene expression;
			Lard: 10%					↑ adiponectin and PPAR2γ gene expression in mesenteric fat; ↓ weight of mesenteric fat;

Study	Sequence Generation	Baseline Characteristics	Allocation Concealment	Random Housing	Performance Blinding	Random outcome assessment	Blinding of outcome assessment	Incomplete outcome data	Selective outcome reporting	Other sources of bias
Chang et al. (2022)	Y	Y	N	Y	N	U	U	Y	U	Y
Momoh et al. (2022)	Y	Y	N	Y	N	U	U	Y	U	Y
Yu et al. (2021)	Y	Y	N	Y	N	U	U	Y	U	Y
Grzelak-Błaszczyk et al. (2020)	Y	Y	N	Y	N	Y	Y	Y	U	Y
Grzelak-Błaszczyk et al. (2018)	Y	Y	N	U	N	U	U	Y	U	Y
Emamat et al. (2018)	Y	Y	N	Y	N	U	U	Y	U	Y
Forney et al. (2018)	Y	Y	N	Y	N	U	U	Y	U	Y
Yang et al. (2018)	Y	Y	N	Y	N	U	U	Y	U	Y
Devarshi et al. (2017)	Y	Y	N	Y	N	U	U	Y	U	Y
Lee et al. (2017)	Y	Y	N	Y	N	U	U	Y	U	Y
Emamat et al. (2016)	Y	Y	N	Y	N	U	U	Y	U	Y
Henagan et al. (2015)	Y	Y	N	Y	N	U	U	Y	U	Y
Matsunaga et al. (2014)	Y	Y	N	Y	N	U	U	Y	U	Y
Moon et al. (2013)	Y	Y	N	Y	N	U	U	Y	U	Y
Benítez et al. (2012)	Y	Y	N	Y	N	U	U	Y	U	Y
Lee et al. (2012)	Y	Y	N	Y	N	U	U	Y	U	Y
Hamauzu et al. (2011)	Y	Y	N	U	N	U	U	Y	U	Y
Kim et al. (2012)	Y	Y	N	Y	N	U	U	Y	U	Y

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[1] PICOS (Participants / Population, Interventions / Exposure, Comparison, Outcomes and Study design).