We previously established that male Swiss mice (Mus musculus) receiving a high-fat diet (HFD) during 8 weeks exhibit similar caloric ingestion and body weight (grams) compared with mice fed a high-carbohydrate diet (HCD). HFD mice exhibit a lower inflammatory state than an HCD in the liver, skeletal muscle, and brain. In addition, we demonstrated that HFD and HCD modulated fatty acids (FA) composition in these tissues. In this study, our objective was to compare HFD mice and HCD mice in terms of systemic inflammation.
Methods:
Saturated FA (SFA), monounsaturated FA, omega-6 polyunsaturated FA (n-6 PUFA), and n-3 PUFA were evaluated at the time points 0, 1, 7, 14, 28, and 56 days after starting the administration of the diets. We investigated n-6 PUFA:n-3 PUFA, SFA:n-3 PUFA, palmitic acid:α-linolenic acid (ALA), and myristic acid:docosahexaenoic acid (DHA) ratios as potential serum biomarkers of systemic inflammation. We also measured the serum levels of basic fibroblast growth factor, granulocyte-macrophage colony-stimulating factor (GM-CSF), inducible protein 10 (IP-10), interferon gamma (IFN-γ), interleukin (IL)-1α, IL-1β, IL-2, IL-4, IL-5, IL-6, IL-10, IL-13, IL-17, macrophage inflammatory protein-1α (MIP-1-α), monocyte chemotactic protein 1 (MCP-1), monokine induced by IFN-γ (MIG), and tumor necrosis factor α (TNF-α).
Results:
The HFD group had lower (P < 0.05) n-6 PUFA:n-3 PUFA, palmitic acid:ALA, myristic acid:DHA ratios, and lower plasma levels of proinflammatory cytokines (IFN-γ, MIG, GM-CSF, and IL-6).
Conclusion:
The HFD mice showed lower systemic inflammation compared with a caloric ingestion–body weight-matched control HCD mice.
Get full access to this article
View all access options for this article.
References
1.
HaririN, ThibaultL. High-fat diet-induced obesity in animal models. Nutr Res Rev, 2010; 23:270–299.
2.
VargheseJ, JamesJV, AnandR, et al.Development of insulin resistance preceded major changes in iron homeostasis in mice fed a high-fat diet. J Nutr Biochem, 2020; 84:108441.
3.
AraújoEP, De SouzaCT, UenoM, et al.Infliximab restores glucose homeostasis in an animal model of diet-induced obesity and diabetes. Endocrinology, 2007; 148:5991–5997.
SaitoY, KuwaharaY, YamamotoY, et al.ddY Mice fed 10% fat diet exhibit high p27KIP expression and delayed hepatocyte DNA synthesis during liver regeneration. Metab Syndr Relat Disord, 2018; 16:305–313.
6.
SirjaniM, TalebanFA, HekmatdoostA, et al.The effects of high fat, low carbohydrate and low fat, high carbohydrate diets on tumor necrosis factor superfamily proteins and proinflammatory cytokines in C57BL/6 mice. Iran J Allergy Asthma Immunol, 2014; 13:247–255.
7.
GillmanMW, CupplesLA, MillenBE, et al.Inverse association of dietary fat with development of ischemic stroke in men. JAMA, 1997; 278:2145–2150.
8.
ParrySA, HodsonL. Influence of dietary macronutrients on liver fat accumulation and metabolism. J Investig Med, 2017; 65:1102–1115.
9.
de Almeida-SouzaCB, AntunesMM, GodoyG, et al.Interleukin-12 as a biomarker of the beneficial effects of food restriction in mice receiving high fat diet or high carbohydrate diet. Braz J Med Biol Res, 2018; 51:e7900.
10.
da Silva-SantiL, AntunesMM, Caparroz-AssefSM, et al.Liver fatty acid composition and inflammation in mice fed with high-carbohydrate diet or high-fat diet. Nutrients, 2016; 8:E682.
11.
AntunesMM, GodoyG, de Almeida-SouzaCB, et al.A high-carbohydrate diet induces greater inflammation than high-fat diet in mouse skeletal muscle. Braz J Med Biol Res, 2020; 53:e9039.
12.
da Silva-SantiLG, AntunesMM, Caparroz-AssefSM, et al.Brain fatty acid composition and inflammation in mice fed with high-carbohydrate diet or high-fat diet. Nutrients, 2018; 10:1277.
13.
BjermoH, IggmanD, KullbergJ, et al.Effects of n-6 PUFAs compared with SFAs on liver fat, lipoproteins, and inflammation in abdominal obesity: A randomized controlled trial. Am J Clin Nutr, 2012; 95:1003–1012.
14.
MasquioDC, de Piano-GanenA, OyamaLM, et al.The role of free fatty acids in the inflammatory and cardiometabolic profile in adolescents with metabolic syndrome engaged in interdisciplinary therapy. J Nutr Biochem, 2016; 33:136–144.
15.
Fernández-RealJM, BrochM, VendrellJ, et al.Insulin resistance, inflammation, and serum fatty acid composition. Diabetes Care, 2003; 26:1362–1368.
16.
Warensjö E, Risérus U, Vessby B.. Fatty acid composition of serum lipids predicts the development of the metabolic syndrome in men. Diabetologia, 2005; 48:1999–2005.
17.
SimonJA, HodgkinsML, BrownerWS, et al.Serum fatty acids and the risk of coronary heart disease. Am J Epidemiol, 1995; 142:469–476.
18.
KhalidA, SiddiquiAJ, HuangJH, et al.Alteration of serum free fatty acids are indicators for progression of pre-leukemia diseases to leukaemia. Sci Rep, 2018; 8:1488.
19.
ReevesPG, NielsenFH, FaheyGC. AIN-93 Purified diets for laboratory rodents: Final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76A rodent diet. J Nutr, 1993; 123:1939–1951.
20.
AbdelmagidSA, ClarkeSE, NielsenDE, et al.Comprehensive profiling of plasma fatty acid concentrations in young healthy Canadian adults. PLoS One, 2015; 10:e0116195.
21.
MartínezL, TorresS, BauliesA, et al.Myristic acid potentiates palmitic acid-induced lipotoxicity and steatohepatitis associated with lipodystrophy by sustaning de novo ceramide synthesis. Oncotarget, 2015; 6:41479–41496.
22.
TsoukalasD, FragoulakisV, SarandiE, et al.Targeted metabolomic analysis of serum fatty acids for the prediction of autoimmune diseases. Front Mol Biosci, 2019; 6:120.
23.
TomitaK, TerataniT, YokoyamaH, et al.Plasma free myristic acid proportion is a predictor of nonalcoholic steatohepatitis. Dig Dis Sci, 2011; 56:3045–3052.
24.
SandersFWB, AcharjeeA, WalkerC, et al.Hepatic steatosis risk is partly driven by increased de novo lipogenesis following carbohydrate consumption. Genome Biol, 2018; 19:79.
25.
AntunesMM, GodoyG, FernandesIL, et al.The dietary replacement of soybean oil by canola oil does not prevent liver fatty acid accumulation and liver inflammation in mice. Nutrients, 2020; 12:E3667.
26.
RochaDM, BressanJ, HermsdorffHH. The role of dietary fatty acid intake in inflammatory gene expression: A critical review. Sao Paulo Med J, 2017; 135:157–168.
27.
KaramJ, BibiloniMDM, PonsA, et al.Total fat and fatty acid intakes and food sources in Mediterranean older adults requires education to improve health. Nutr Res, 2019; 73:67–74.
28.
MartinSA, BrashAR, MurphyRC. The discovery and early structural studies of arachidonic acid. J Lipid Res, 2016; 57:1126–1132.
29.
RomanattoT, FiamonciniJ, WangB, et al.Elevated tissue omega-3 fatty acid status prevents age-related glucose intolerance in fat-1 transgenic mice. Biochim Biophys Acta, 2014; 1842:186–191.
30.
SimopoulosAP. An increase in the omega-6/omega-3 fatty acid ratio increases the risk for obesity. Nutrients, 2016; 8:128.
31.
ThomasSS, ChaYS, KimKA. Perilla oil alleviates high-fat diet-induced inflammation in the colon of mice by suppressing nuclear factor-kappa B activation. J Med Food, 2020; 23:818–826.
32.
KaurKK, AllanhbadiaG, SinghM. Synthesis and functional significance of polyunsaturated fatty acids (PUFA's) in the body. Acta Sci Nutr Health, 2018; 2:43–50.
33.
da SilvaCS, MonteiroCRA, da SilvaGHF, et al.Assessing the metabolic impact of ground chia seed in overweight and obese prepubescent children: Results of a double-blind randomized clinical trial. J Med Food, 2020; 23:224–232.
34.
DinarelloCA. Historical insights into cytokines. Eur J Immunol, 2007; 37:S34–S45.
35.
CândidoFG, ValenteFX, Grześkowiak ŁM, et al. Impact of dietary fat on gut microbiota and low-grade systemic inflammation: Mechanisms and clinical implications on obesity. Int J Food Sci Nutr, 2018; 69:125–143.
36.
CalderPC, AhluwaliaN, BrounsF, et al.Dietary factors and low-grade inflammation in relation to overweight and obesity. Br J Nutr, 2011; 106:S75–S78.
37.
GallandL. Diet and inflammation. Nutr Clinl Pract, 2010; 25:634–640.
38.
HamleyS. The effect of replacing saturated fat with mostly n-6 polyunsaturated fat on coronary heart disease: A meta-analysis of randomised controlled trials. Nutr J, 2017; 16:30.
39.
FritscheKL. The science of fatty acids and inflammation. Adv Nutr, 2015; 6:93S–301S.
40.
BarrenaHC, SchiavonFPM, CararraMA, et al.Effect of linseed oil and macadamia oil on metabolic changes induced by high-fat diet in mice. Cell Biochem Funct, 2014; 32:333–340.
41.
SchiavonFP, MarquesAC, CarraraMA, et al.Pivotal role of cAMP in the activation of liver glycogen breakdown in high-fat diet fed mice. Life Sci, 2014; 109:111–115.
42.
LicholaiJA, NguyenKP, FobbsWC, et al.Why do mice overeat high-fat diets? How high-fat diet alters the regulation of daily caloric intake in mice. Obesity, 2018; 26:1026–1033.
43.
ObiciS, TavoniTM, BarrenaHC, et al.Time sequence of the intensification of the liver glucose production induced by high-fat diet in mice. Cell Biochem Funct, 2012; 30:335–339.
44.
ChoiMS, ChoiJY, KwonEY. Fisetin alleviates hepatic and adipocyte fibrosis and insulin resistance in diet-induced obese mice. J Med Food, 2020; 23:1019–1032.
