Citrus Flavonoids as Regulators of Lipoprotein Metabolism and Atherosclerosis

Mulvihill, Erin E.; Burke, Amy C.; Huff, Murray W.

doi:10.1146/annurev-nutr-071715-050718

Cited by 228Bioactive Compounds in PlantsPhytochemicals and Antioxidant ActivitiesFlavonoids in Medical Research

Citrus Flavonoids as Regulators of Lipoprotein Metabolism and Atherosclerosis

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Mulvihill, Erin E., Burke, Amy C., Huff, Murray W.·2016·Annual Review of Nutrition

DOI 10.1146/annurev-nutr-071715-050718

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Abstract

Citrus flavonoids are polyphenolic compounds with significant biological properties. This review summarizes recent advances in understanding the ability of citrus flavonoids to modulate lipid metabolism, other metabolic parameters related to the metabolic syndrome, and atherosclerosis. Citrus flavonoids, including naringenin, hesperitin, nobiletin, and tangeretin, have emerged as potential therapeutics for the treatment of metabolic dysregulation. Epidemiological studies reveal an association between the intake of citrus flavonoid–containing foods and a decreased incidence of cardiovascular disease. Studies in cell culture and animal models, as well as a limited number of clinical studies, reveal the lipid-lowering, insulin-sensitizing, antihypertensive, and anti-inflammatory properties of citrus flavonoids. In animal models, supplementation of rodent diets with citrus flavonoids prevents hepatic steatosis, dyslipidemia, and insulin resistance primarily through inhibition of hepatic fatty acid synthesis and increased fatty acid oxidation. Citrus flavonoids blunt the inflammatory response in metabolically important tissues including liver, adipose, kidney, and the aorta. The mechanisms underlying flavonoid-induced metabolic regulation have not been completely established, although several potential targets have been identified. In mouse models, citrus flavonoids show marked suppression of atherogenesis through improved metabolic parameters as well as through direct impact on the vessel wall. Recent studies support a role for citrus flavonoids in the treatment of dyslipidemia, insulin resistance, hepatic steatosis, obesity, and atherosclerosis. Larger human studies examining dose, bioavailability, efficacy, and safety are required to promote the development of these promising therapeutic agents.

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In the same study, ginger increased gastric antral contractions without adverse symptoms.
“In a randomized, double-blind study with 24 healthy adults, 1.2 g of oral ginger accelerated gastric emptying (half-emptying time after a meal 13 min vs. 27 min with placebo), and increased gastric antral contractions without adverse symptoms [350].”
From Nutritional Approaches to Enhance GLP-1 Analogue Therapy in Obesity: A Narrative Review (2025) · cites this paper as [350]
In a randomized, double-blind study with 24 healthy adults, 1.2 g oral ginger accelerated gastric emptying (half-emptying time after a meal 13 min vs 27 min with placebo).
“In a randomized, double-blind study with 24 healthy adults, 1.2 g of oral ginger accelerated gastric emptying (half-emptying time after a meal 13 min vs. 27 min with placebo), and increased gastric antral contractions without adverse symptoms [350].”
From Nutritional Approaches to Enhance GLP-1 Analogue Therapy in Obesity: A Narrative Review (2025) · cites this paper as [350]

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Lee, E., Kim, D., Kim, W., & Moon, S. (2009) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200800210 · Cited by 91 · see citing works
Naringenin inhibits TNF-α induced VSMC proliferation and migration via induction of HO-1
Chen, S., Ding, Y., Tao, W., Zhang, W., Liang, T., & Liu, C. (2012) · Food and Chemical Toxicology · doi:10.1016/j.fct.2012.06.006 · Cited by 90 · see citing works
Clinical Study to Assess the Efficacy and Safety of a Citrus Polyphenolic Extract of Red Orange, Grapefruit, and Orange (Sinetrol‐XPur) on Weight Management and Metabolic Parameters in Healthy Overweight Individuals
Dallas, C., Gerbi, A., Elbez, Y., Caillard, P., Zamaria, N., & Cloarec, M. (2013) · Phytotherapy Research · doi:10.1002/ptr.4981 · Cited by 90 · see citing works
Lemon Polyphenols Suppress Diet-induced Obesity by Up-Regulation of mRNA Levels of the Enzymes Involved in β-Oxidation in Mouse White Adipose Tissue
Fukuchi, Y., Hiramitsu, M., Okada, M., Hayashi, S., Nabeno, Y., Osawa, T., & Naito, M. (2008) · Journal of Clinical Biochemistry and Nutrition · doi:10.3164/jcbn.2008066 · Cited by 88 · see citing works
The effects of daily consumption of grapefruit on body weight, lipids, and blood pressure in healthy, overweight adults
Dow, C. A., Going, S. B., Chow, H.-H. S., Patil, B. S., & Thomson, C. A. (2012) · Metabolism · doi:10.1016/j.metabol.2011.12.004 · Cited by 88 · see citing works
Long-term orange juice consumption is associated with low LDL-cholesterol and apolipoprotein B in normal and moderately hypercholesterolemic subjects
Aptekmann, N. P., & Cesar, T. B. (2013) · Lipids in Health and Disease · doi:10.1186/1476-511x-12-119 · Cited by 88 · see citing works
The Influence of Naringin on the Oxidative State of Rats with Streptozotocin- Induced Acute Hyperglycaemia
Mamdouh, M., & Monira, A. A. E. K. (2004) · Zeitschrift für Naturforschung C · doi:10.1515/znc-2004-9-1018 · Cited by 86 · see citing works
Naringenin 7-O-cetyl ether as inhibitor of HMG-CoA reductase and modulator of plasma and hepatic lipids in high cholesterol-fed rats
Lee, M., Moon, S., Lee, S., Bok, S., Jeong, T., Park, Y. B., & Choi, M. (2003) · Bioorganic & Medicinal Chemistry · doi:10.1016/s0968-0896(02)00441-8 · Cited by 84 · see citing works
Naringenin enhances insulin-stimulated tyrosine phosphorylation and improves the cellular actions of insulin in a dietary model of metabolic syndrome
Kannappan, S., & Anuradha, C. V. (2009) · European Journal of Nutrition · doi:10.1007/s00394-009-0054-6 · Cited by 81 · see citing works
Inhibition of hepatocyte apoB secretion by naringenin
Borradaile, N. M., de Dreu, L. E., Barrett, P. H. R., & Huff, M. W. (2002) · Journal of Lipid Research · doi:10.1194/jlr.m200115-jlr200 · Cited by 79 · see citing works
Self-citation
Glucosyl Hesperidin Lowers Serum Triglyceride Level in Hypertriglyceridemic Subjects through the Improvement of Very Low-Density Lipoprotein Metabolic Abnormality
Miwa, Y., Mitsuzumi, H., SUNAYAMA, T., Yamada, M., OKADA, K., Kubota, M., Chaen, H., Mishima, Y., & Kibata, M. (2005) · Journal of Nutritional Science and Vitaminology · doi:10.3177/jnsv.51.460 · Cited by 76 · see citing works
Citrus Fruit Extracts Reduce Advanced Glycation End Products (AGEs)- and H2O2-Induced Oxidative Stress in Human Adipocytes
Ramful‐Baboolall, D., Tarnus, E., Rondeau, P., Silva, C. R. D., Bahorun, T., & Bourdon, E. (2010) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf102762s · Cited by 74 · see citing works
Activity and mRNA levels of enzymes involved in hepatic fatty acid oxidation in mice fed citrus flavonoids
Huong, D. T. T., Takahashi, Y., & Ide, T. (2006) · Nutrition · doi:10.1016/j.nut.2005.11.006 · Cited by 68 · see citing works
Hypocholesterolemic Effect of Naringin Associated with Hepatic Cholesterol Regulating Enzyme Changes in Rats
Shin, Y. W., Bok, S. H., Jeong, T., Bae, K.-H., Jeoung, N. H., Choi, M., Lee, S. H., & Park, Y. B. (1999) · International Journal for Vitamin and Nutrition Research · doi:10.1024/0300-9831.69.5.341 · Cited by 66 · see citing works
Naringenin Inhibits Adipogenesis and Reduces Insulin Sensitivity and Adiponectin Expression in Adipocytes
Richard, A. J., Amini, Z., Ribnicky, D., & Stephens, J. M. (2013) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2013/549750 · Cited by 65 · see citing works
Tangeretin, a citrus flavonoid, inhibits PGDF-BB-induced proliferation and migration of aortic smooth muscle cells by blocking AKT activation
Seo, J., Lee, H. S., Ryoo, S., Seo, J. H., Min, B.-S., & Lee, J. (2011) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2011.10.011 · Cited by 61 · see citing works
Tangeretin Regulates Platelet Function Through Inhibition of Phosphoinositide 3-Kinase and Cyclic Nucleotide Signaling
Vaiyapuri, S., Ali, M. S., Moraes, L. A., Sage, T., Lewis, K. R., Jones, C. I., & Gibbins, J. M. (2013) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.113.301988 · Cited by 60 · see citing works
Is Insulin Resistance a Feature of or a Primary Risk Factor for Cardiovascular Disease?
Laakso, M. (2015) · Current Diabetes Reports · doi:10.1007/s11892-015-0684-4 · Cited by 56 · see citing works
Hesperetin Stimulates Cholecystokinin Secretion in Enteroendocrine STC-1 Cells
Kim, H. Y., Park, M. S., Kim, K., Lee, Y. M., & Rhyu, M. R. (2013) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2012.077 · Cited by 56 · see citing works
Inhibition of apoB secretion from HepG2 cells by insulin is amplified by naringenin, independent of the insulin receptor
Allister, E. M., Mulvihill, E. E., Barrett, P. H. R., Edwards, J. Y., Carter, L. P., & Huff, M. W. (2008) · Journal of Lipid Research · doi:10.1194/jlr.m800297-jlr200 · Cited by 50 · see citing works
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Citrus Flavonoids and the Prevention of Atherosclerosis
Mulvihill, E. E., & Huff, M. W. (2012) · Cardiovascular & Haematological Disorders - Drug Targets · doi:10.2174/1871529x11202020084 · Cited by 49 · see citing works
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Tissue distribution of naringenin conjugated metabolites following repeated dosing of naringin to rats
Lin, S.-P., Hou, Y., Tsai, S.-Y., Wang, M.-J., & Chao, P.-D. L. (2014) · Biomedicine · doi:10.7603/s40681-014-0016-z · Cited by 47 · see citing works
Citrus flavonoid, naringenin, increases locomotor activity and reduces diacylglycerol accumulation in skeletal muscle of obese ovariectomized mice
Ke, J., Cole, R. M., Hamad, E. M., Hsiao, Y., Cotten, B. M., Powell, K. A., & Belury, M. A. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500379 · Cited by 41 · see citing works
Naringenin derivatives as anti-atherogenic agents
Lee, S., Lee, C., Moon, S., Kim, E. S., Kim, C., Kim, B., Bok, S., & Jeong, T. (2003) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2003.09.009 · Cited by 39 · see citing works
The metabolic syndrome and diabetes mellitus as predictors of thoracic aortic calcification as detected by non‐contrast computed tomography in the Multi‐Ethnic Study of Atherosclerosis
Katz, R., Budoff, M. J., O’Brien, K. D., Wong, N. D., & Nasir, K. (2015) · Diabetic Medicine · doi:10.1111/dme.12958 · Cited by 36 · see citing works
Is Cholesteryl Ester Transfer Protein Inhibition an Effective Strategy to Reduce Cardiovascular Risk?: CETP as a Target to Lower CVD Risk: Suspension of Disbelief?
Hovingh, G. K., Ray, K. K., & Boekholdt, S. M. (2015) · Circulation · doi:10.1161/circulationaha.115.014026 · Cited by 31 · see citing works
(2S)-Naringenin from Typha angustata inhibits vascular smooth muscle cell proliferation via a G0/G1 arrest
Lee, J.-J., Yi, H., Kim, I., Kim, Y., Nhiệm, N. X., Kim, Y. H., & Myung, C. (2011) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2011.12.038 · Cited by 31 · see citing works
Effect of Chronic Administration of Fruit Extract (Citrus unshiuMarc.) on Glucose Tolerance in GK Rats, a Model of Type 2 Diabetes
Sugiura, M., OGAWA, K., & Yano, M. (2006) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.70.293 · Cited by 19 · see citing works
17β-Estradiol but not the phytoestrogen naringenin attenuates aortic cholesterol accumulation in WHHL rabbits
Mortensen, A., Breinholt, V. M., Dalsgaard, T., Frandsen, H. L., Lauridsen, S. T., Laigaard, J., Ottesen, B., & Larsen, J. (2001) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)31646-1 · Cited by 19 · see citing works
[Naringin inhibits monocyte adhesion to high glucose-induced human umbilical vein endothelial cells].
Xiong, Y., Wang, G., Zhang, J., Wu, S., Xu, W., Zhang, J., Wu, S., & Rao, J.-J. (2010) · PubMed · Cited by 8 · see citing works
Abstract 67: Intervention With Citrus Flavonoids Reverses Existing Metabolic Disorders and Attenuates the Progression of Advanced Atherosclerosis in High Fat--Fed LDLr-/- Mice
Burke, A. C., Sutherland, B. G., Sawyez, C. G., Telford, D. E., Umoh, J. U., Drangova, M., & Huff, M. W. (2014) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvb.34.suppl_1.67 · Cited by 3 · see citing works
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Abstract 686: Intervention with Naringenin Enhances Weight Loss, Potentiates Improvements in Metabolic Dysregulation and Halts Progression of Atherosclerosis Induced by a High-Fat Diet in LDLr-/- Mice.
Burke, A. C., Sutherland, B. G., Assini, J. M., & Huff, M. W. (2015) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvb.35.suppl_1.686 · Cited by 2 · see citing works
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How can nobiletin prevent obesity?
Mulvihill, E. E., & Huff, M. W. (2011) · Expert Review of Endocrinology & Metabolism · doi:10.1586/eem.11.46 · Cited by 1 · see citing works
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Flavonoids: Potential therapeutic agents for cardiovascular disease
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Nobiletin mitigates hepatocytes death, liver inflammation, and fibrosis in a murine model of NASH through modulating hepatic oxidative stress and mitochondrial dysfunction
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The citrus flavonoid nobiletin confers protection from metabolic dysregulation in high-fat-fed mice independent of AMPK
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Citrus flavonoids and lipid metabolism
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Mulvihill, E. E., & Huff, M. W. (2012)
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Protection from Metabolic Dysregulation, Obesity, and Atherosclerosis by Citrus Flavonoids: Activation of Hepatic PGC1α-Mediated Fatty Acid Oxidation
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Citrus Flavonoids and the Prevention of Atherosclerosis
Mulvihill, E. E., & Huff, M. W. (2012) · Cardiovascular & Haematological Disorders - Drug Targets · doi:10.2174/1871529x11202020084 · Cited by 49 · see citing works
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Beneficial Effects of Citrus Flavonoids on Cardiovascular and Metabolic Health
Mahmoud, A. M., Hernández-Bautista, R., Sandhu, M. A., & Hussein, O. E. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/5484138 · Cited by 303 · see citing works

Authors: Mulvihill, E. E., Burke, A. C., & Huff, M. W.
Affiliations: Western University (CA)
ORCID: Mulvihill, Erin E.
Huff, Murray W.
Venue: Annual Review of Nutrition
Publisher: Annual Reviews
Published: 2016-07-17
Volume: 36
Issue: 1
Pages: 275-299
ISSN: 0199-9885 (ISSN-L)
1545-4312
DOI: 10.1146/annurev-nutr-071715-050718
OpenAlex: W2211999579
Cited by: 228
References: 100
Citations by year: 2026: 20 · 2025: 15 · 2024: 24 · 2023: 19 · 2022: 26 · 2021: 31 · 2020: 38 · 2019: 25 · 2018: 17 · 2017: 9 · 2016: 4
FWCI: 1.78
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Annual Review of Nutrition (publishedVersion)
PubMed (publishedVersion)
Funders: Heart and Stroke Foundation of Canada (G-14-0006179)
Canadian Institutes of Health Research (T-7007)
Topics: Life Sciences › Agricultural and Biological Sciences › Plant Science › Bioactive Compounds in Plants
Health Sciences › Medicine › Biochemistry › Phytochemicals and Antioxidant Activities
Health Sciences › Medicine › Pharmacology › Flavonoids in Medical Research
Keywords: citrus flavonoids, naringenin, hesperidin, nobiletin, tangeretin, lipoprotein metabolism, atherosclerosis, metabolic syndrome, dyslipidemia, insulin resistance, hepatic steatosis, hepatic fatty acid synthesis, fatty acid oxidation, anti-inflammatory activity, antihypertensive effect, cardiovascular disease prevention, obesity
MeSH terms: Animals, Anti-Inflammatory Agents, Non-Steroidal, Hypolipidemic Agents, Antioxidants, Citrus, Diabetes Mellitus, Type 2, Flavonoids, Humans, Hyperlipidemias, Insulin Resistance, Lipoproteins, Risk Factors, Anti-Obesity Agents, Dietary Supplements, Overweight, Atherosclerosis, Non-alcoholic Fatty Liver Disease

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Citrus Flavonoids as Regulators of Lipoprotein Metabolism and Atherosclerosis

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