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Original Communication

CD36 polymorphism, sugary drinks, and sedentarism are associated with hypertriglyceridemic waist phenotype

Published Online:https://doi.org/10.1024/0300-9831/a000771

Abstract:Background: The hypertriglyceridemic waist (HTGW) phenotype is characterized by concomitant increases in waist circumference (WC) and blood triglyceride levels (TG), which have been identified as a predictor of metabolic disorders. This study aimed to analyze associations between food consumption, exercise, and the CD36 gene rs1761667 G>A polymorphism with the HTGW phenotype in adult Mexicans. Methods: This cross-sectional study included a total of 255 participants (both genders, between 18–64 years of age). The HTGW phenotype was defined as WC >88 cm in women, WC >102 cm in men, and TG >150 mg/dL. Body composition was analyzed by electrical bioimpedance. Dietary intakes (macro and micronutrients) were evaluated through a validated 64-item food frequency questionnaire and a 24-h recall. Physical exercise was subjectively recorded asking the participants if they regularly performed some systematic exercise or sport of moderate intensity at least 150–300 minutes a week. Biochemical tests were determined by an automated system. A Taqman real-time assay was used to detect the rs1761667 (G>A) polymorphism of the CD36 gene. A multivariate logistic regression model was performed to analyze the variables potentially associated with the HTGW phenotype (adjusted for age, energy intake, and total fat mass). Results: Overall, 21.6% of the population presented the HTGW phenotype; compared to the HTGW−, also, they were older, had more body fat, higher glucose, cholesterol and insulin levels, and high blood pressure. Female sex (OR=2.92, 95% CI: 1.12–7.60, p=0.028), body mass index (OR=1.19, 95% CI: 1.07–1.32, p=0.001), total cholesterol (OR=1.01, 95% CI:1.00–1.02, p=0.039), daily consumption of sugary drinks (OR=6.94, 95% CI: 1.80–26.8, p=0.005), and the CD36 AG genotype (OR=3.81, 95% CI: 1.08–13.4, p=0.037) were positively associated with the HTGW phenotype, while performing exercise played a protective role (OR=0.23, 95% CI: 0.08–0.62, p=0.004). Overall, the model predicted the HTGW phenotype in 47% (R2=0.47, p≤0.001). Conclusion: The CD36 AG genotype, daily consumption of sugary drinks and sedentarism are risk factors for the HTGW phenotype in Mexicans.

References

  • 1 Després JP, Lemieux I. Abdominal obesity and metabolic syndrome. Nature. 2006;444(7121):881–7. https://doi.org/10.1038/nature05488 First citation in articleCrossref MedlineGoogle Scholar

  • 2 Rader DJ. Effect of insulin resistance, dyslipidemia, and intra-abdominal adiposity on the development of cardiovascular disease and diabetes mellitus. Am J Med. 2007;120(3 Suppl 1):S12–8. https://doi.org/10.1016/j.amjmed.2007.01.003 First citation in articleCrossref MedlineGoogle Scholar

  • 3 Braz MAD, Vieira JN, Gomes FO, da Silva PR, Santos OTM, da Rocha IMG, et al. Hypertriglyceridemic waist phenotype in primary health care: comparison of two cutoff points. Diabetes Metab Syndr Obes. 2017;10:385–91. https://doi.org/10.2147/DMSO.S143595 First citation in articleCrossref MedlineGoogle Scholar

  • 4 Tankó LB, Bagger YZ, Qin G, Alexandersen P, Larsen PJ, Christiansen C, Enlarged waist combined with elevated triglycerides is a strong predictor of accelerated atherogenesis and related cardiovascular mortality in postmenopausal women. Circulation. 2005;111:1883–90. https://doi.org/10.1161/01.CIR.0000161801.65408.8D First citation in articleCrossref MedlineGoogle Scholar

  • 5 Lemieux I, Poirier P, Bergeron J, Alméras N, Lamarche B, Cantin B, et al. Hypertriglyceridemic waist: a useful screening phenotype in preventive cardiology? Can J Cardiol. 2007;23(Suppl B):23B–31B. https://doi.org/10.1016/s0828-282x(07)71007-3 First citation in articleCrossref MedlineGoogle Scholar

  • 6 Amini M, Esmaillzadeh A, Sadeghi M, Mehvarifar N, Amini M, Zare M. The association of hypertriglyceridemic waist phenotype with type 2 diabetes mellitus among individuals with first relative history of diabetes. J Res Med Sci. 2011;16(2):156–64. First citation in articleMedlineGoogle Scholar

  • 7 Xuan Y, Shen Y, Wang S, Gao P, Gu X, Tang D, et al. The association of hypertriglyceridemic waist phenotype with hypertension: A cross-sectional study in a Chinese middle aged-old population. J Clin Hypertens (Greenwich). 2022;24(2):191–9. https://doi.org/10.1111/jch.14424 First citation in articleCrossref MedlineGoogle Scholar

  • 8 Zhou M, Li F, Tang H, Wu S, Meng L, Dong Y, et al. The hypertriglyceridemic waist phenotype is associated with fatty liver and glycometabolic profiles in overweight and obese adults: a cross-sectional study. Sci Rep. 2022;12(1):2410. https://doi.org/10.1038/s41598-021-00825-2 First citation in articleCrossref MedlineGoogle Scholar

  • 9 Tian YM, Ma N, Jia XJ, Lu Q. The, “hyper-triglyceridemic waist phenotype” is a reliable marker for prediction of accumulation of abdominal visceral fat in Chinese adults. Eat Weight Disord. 2020;25(3):719–26. https://doi.org/10.1007/s40519-019-00677-w First citation in articleCrossref MedlineGoogle Scholar

  • 10 Alavian SM, Motlagh ME, Ardalan G, Motaghian M, Davarpanah AH, Kelishadi R. Hypertriglyceridemic waist phenotype and associated lifestyle factors in a national population of youths: CASPIAN Study. J Trop Pediatr. 2008;54:169–177. https://doi.org/10.1093/tropej/fmm105 First citation in articleCrossref MedlineGoogle Scholar

  • 11 Liu S, Manson JE. Dietary carbohydrates, physical inactivity, obesity, and the “metabolic syndrome” as predictors of coronary heart disease. Curr Opin Lipidol. 2001;12:395–404. https://doi.org/10.1097/00041433-200108000-00005 First citation in articleCrossref MedlineGoogle Scholar

  • 12 Mamtani M, Kulkarni H, Dyer TD, Göring HH, Neary JL, Cole SA, et al. Genome- and epigenome-wide association study of hypertriglyceridemic waist in Mexican American families. Clin Epigenetics. 2016;8:6. https://doi.org/10.1186/s13148-016-0173-x First citation in articleCrossref MedlineGoogle Scholar

  • 13 Pepino MY, Kuda O, Samovski D, Abumrad NA, Structure-function of CD36 and importance of fatty acid signal transduction in fat metabolism. Annu Rev Nutr. 2014;34:281–303. https://doi.org/10.1146/annurev-nutr-071812-161220 First citation in articleCrossref MedlineGoogle Scholar

  • 14 Glatz JFC, Luiken JJFP. Dynamic role of the transmembrane glycoprotein CD36 (SR-B2) in cellular fatty acid uptake and utilization. J Lipid Res. 2018;59(7):1084–93. https://doi.org/10.1194/jlr.R082933 First citation in articleCrossref MedlineGoogle Scholar

  • 15 Chen Y, Zhang J, Cui W, Silverstein RL. CD36, a signaling receptor and fatty acid transporter that regulates immune cell metabolism and fate. J Exp Med. 2022;219(6):e20211314. https://doi.org/10.1084/jem.20211314 First citation in articleCrossrefGoogle Scholar

  • 16 Karunakaran U, Elumalai S, Moon JS, Won KC. CD36 signal transduction in metabolic diseases: novel insights and therapeutic targeting. Cells. 2021;10(7):1833. https://doi.org/10.3390/cells10071833 First citation in articleCrossref MedlineGoogle Scholar

  • 17 Shu H, Peng Y, Hang W, Nie J, Zhou N, Wang DW. The role of CD36 in cardiovascular disease. Cardiovasc Res. 2022;118(1):115–29. https://doi.org/10.1093/cvr/cvaa319 First citation in articleCrossref MedlineGoogle Scholar

  • 18 Love-Gregory L, Sherva R, Schappe T, Qi JS, McCrea J, Klein S, et al. Common CD36 SNPs reduce protein expression and may contribute to a protective atherogenic profile. Hum Mol Genet. 2011;20:193–201. https://doi.org/10.1093/hmg/ddq449 First citation in articleCrossref MedlineGoogle Scholar

  • 19 Rivas-Gomez B, Almeda-Valdés P, Tussié-Luna MT, Aguilar-Salinas CA. Dyslipidemia in Mexico: a call for action. Rev Invest Clin. 2018;70:211–6. https://doi.org/10.24875/RIC.18002573 First citation in articleCrossref MedlineGoogle Scholar

  • 20 Deprince A, Haas JT, Staels B. Dysregulated lipid metabolism links NAFLD to cardiovascular disease. Mol Metab. 2020;42: 101092. https://doi.org/10.1016/j.molmet.2020.101092 First citation in articleCrossref MedlineGoogle Scholar

  • 21 Ramos-Lopez O, Milton-Laskibar I, Martínez JA, Collaborators San-Cristobal RPortillo MP. Precision nutrition based on phenotypical traits and the (epi)genotype: nutrigenetic and nutrigenomic approaches for obesity care. Curr Opin Clin Nutr Metab Care. 2021;24(4):315–25. https://doi.org/10.1097/MCO.0000000000000754 First citation in articleCrossref MedlineGoogle Scholar

  • 22 Velázquez-López L, Díaz-García L. Anthropometric indicators and poor glycemic control in type 2 diabetes with kidney disease. Rev Med Inst Mex Seguro Soc. 2021;59:313–21. First citation in articleMedlineGoogle Scholar

  • 23 Navas-Carretero S, San-Cristobal R, Siig Vestentoft P, Brand-Miller JC, Jalo E, Westerterp-Plantenga M, et al. Appraisal of triglyceride-related markers as early predictors of metabolic outcomes in the PREVIEW lifestyle intervention: a controlled post-hoc trial. Front Nutr. 2021;8:733697. https://doi.org/10.3389/fnut.2021.733697 First citation in articleCrossref MedlineGoogle Scholar

  • 24 Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16(3):1215. https://doi.org/10.1093/nar/16.3.1215 First citation in articleCrossref MedlineGoogle Scholar

  • 25 Ramos-Lopez O, Panduro A, Rivera-Iñiguez I, Roman S. Dopamine D2 receptor polymorphism (C957T) is associated with sugar consumption and triglyceride levels in West Mexicans. Physiol Behav. 2018;1(194):532–7. https://doi.org/10.1016/j.physbeh.2018.07.004 First citation in articleCrossrefGoogle Scholar

  • 26 Norma Oficial Mexicana NOM-043-SSA2-2012. Servicios básicos de salud. Promoción y educación para la salud en materia alimentaria. Criterios para brindar orientación. Available from: https://www.cndh.org.mx/DocTR/2016/JUR/A70/01/JUR-20170331-NOR37.pdf First citation in articleGoogle Scholar

  • 27 Ramos-López O, Román S, Ojeda-Granados C, Sepúlveda-Villegas M, Martínez-López E, Torres-Valadez R, et al. Patrón de ingesta alimentaria y actividad física en pacientes hepatópatas en el Occidente de México. Rev Endocrinol Nutr. 2013;21(1):7–15. First citation in articleGoogle Scholar

  • 28 Ramos-Lopez O, Mejia-Godoy R, Frías-Delgadillo KJ, Torres-Valadez R, Flores-García A, Sánchez-Enríquez S, et al. Interactions between DRD2/ANKK1 TaqIA polymorphism and dietary factors influence plasma triglyceride concentrations in diabetic patients from Western Mexico: a cross-sectional study. Nutrients. 2019;11(12):2863. https://doi.org/10.3390/nu11122863 First citation in articleCrossref MedlineGoogle Scholar

  • 29 Pérez LAB, Marvan LL. Manual de dietas normales y terapéuticas: los alimentos en la salud y en la enfermedad, 5 ed. México, DF; La Prensa Médica Mexicana; 2005. First citation in articleGoogle Scholar

  • 30 Yang YJ. An overview of current physical activity recommendations in primary care. Korean J Fam Med. 2019;40(3):135–42. https://doi.org/10.4082/kjfm.19.0038 First citation in articleCrossref MedlineGoogle Scholar

  • 31 Ramos-Lopez O, Roman S, Martinez-Lopez E, Fierro NA, Gonzalez-Aldaco K, Jose-Abrego A, Panduro A. CD36 genetic variation, fat intake and liver fibrosis in chronic hepatitis C virus infection. World J Hepatol. 2016;8:1067–74. https://doi.org/10.4254/wjh.v8.i25.1067 First citation in articleCrossref MedlineGoogle Scholar

  • 32 Ramos-Lopez O, Panduro A, Martinez-Lopez E, Fierro NA, Ojeda-Granados C, Sepulveda-Villegas M, et al. Genetic variant in the CD36 gene (rs1761667) is associated with higher fat intake and high serum cholesterol among the population of West Mexico. J Nutr Food Sci. 2015;5:353. https://doi.org/10.4172/2155-9600.1000353 First citation in articleCrossrefGoogle Scholar

  • 33 de Cuevillas B, Alvarez-Alvarez I, Riezu-Boj JI, Navas-Carretero S, Martinez JA. The hypertriglyceridemic-waist phenotype as a valuable and integrative mirror of metabolic syndrome traits. Sci Rep. 2021;11:21859. https://doi.org/10.1038/s41598-021-01343-x First citation in articleCrossref MedlineGoogle Scholar

  • 34 Leprêtre F, Vasseur F, Vaxillaire M, Scherer PE, Ali S, Linton K, et al. A CD36 nonsense mutation associated with insulin resistance and familial type 2 diabetes. Hum Mutat. 2004;24:104. https://doi.org/10.1002/humu.9256 First citation in articleCrossref MedlineGoogle Scholar

  • 35 Solakivi T, Kunnas T, Nikkari ST. Contribution of fatty acid transporter (CD36) genetic variant rs1761667 to body mass index, the TAMRISK study. Scand J Clin Lab Invest. 2015;75(3):254–8. https://doi.org/10.3109/00365513.2014.1003596 First citation in articleCrossref MedlineGoogle Scholar

  • 36 Enciso-Ramírez M, Reyes-Castillo Z, Llamas-Covarrubias MA, Guerrero L, López-Espinoza A, Valdés-Miramontes EH. CD36 gene polymorphism -31118 G > A (rs1761667) is associated with overweight and obesity but not with fat preferences in Mexican children. Int J Vitam Nutr Res. 2021;91(5–6):513–21. https://doi.org/10.1024/0300-9831/a000656 First citation in articleLinkGoogle Scholar

  • 37 Gonzalez-Aldaco K, Roman S, Torres-Reyes LA, Panduro A. Association of Apolipoprotein e2 allele with insulin resistance and risk of type 2 diabetes mellitus among an admixed population of Mexico. Diabetes Metab Syndr Obes. 2020;13:3527–34. https://doi.org/10.2147/DMSO.S268329 First citation in articleCrossref MedlineGoogle Scholar

  • 38 Martinez-Lopez E, Curiel-Lopez F, Hernandez-Nazara A, Moreno-Luna LE, Ramos-Marquez ME, Roman S, et al. Influence of ApoE and FABP2 polymorphisms and environmental factors in the susceptibility to gallstone disease. Ann Hepatol. 2015;14:515–23. https://doi.org/10.1016/S1665-2681(19)31173-1 First citation in articleCrossref MedlineGoogle Scholar

  • 39 Fagundes LC, Fernandes MH, Brito TA, Coqueiro RDS, Carneiro JAO. Prevalence and factors associated with hypertriglyceridemic waist in the elderly: a population-based study. Cien Saude Colet. 2018;23:607–16. https://doi.org/10.1590/1413-81232018232.02862016 First citation in articleCrossref MedlineGoogle Scholar

  • 40 Lanzetta Haack R, Lessa Horta B, Petrucci Gigante D, Barros FC, Oliveira I, Silveira VM. Cintura hipertrigliceridêmica em adultos jovens no Sul do Brasil. Cad. Saúde Pública, Rio de Janeiro. 2013;29:999–1007. https://doi.org/10.1590/S0102-311X2013000500017 First citation in articleCrossref MedlineGoogle Scholar

  • 41 Esmaillzadeh A, Mirmiran P, Azadbakht L, Azizi F. Prevalence of the hypertriglyceridemic waist phenotype in Iranian adolescents. Am J Prev Med. 2006;30:52–58. https://doi.org/10.1016/j.amepre.2005.08.041 First citation in articleCrossref MedlineGoogle Scholar

  • 42 Cabral NA, Ribeiro VS, França AK, Salgado JV, Santos AM, Salgado Filho N, et al. Hypertriglyceridemic waist and cardiometabolic risk in hypertensive women. Rev Assoc Med Bras. 1992;2012(58):68–573. https://doi.org/10.1590/s0104-42302012000500014 First citation in articleCrossrefGoogle Scholar

  • 43 Weschenfelder C, Marcadenti A, Stein AT, Gottschall CB. Enlarged waist combined with elevated triglycerides (hypertriglyceridemic waist phenotype) and HDL-cholesterol in patients with heart failure. Sao Paulo Med J. 2017;135:50–6. https://doi.org/10.1590/1516-3180.2016.004519102016 First citation in articleCrossref MedlineGoogle Scholar

  • 44 Miñambres I, Sánchez-Hernandez J, Cuixart G, Sánchez-Pinto A, Sarroca J, Pérez A. Characterization of the hypertriglyceridemic waist phenotype in patients with type 2 diabetes mellitus in Spain: an epidemiological study. Rev Clin Esp (Barc). 2021;221:576–81. https://doi.org/10.1016/j.rceng.2020.06.010 First citation in articleCrossref MedlineGoogle Scholar

  • 45 Sheashea M, Xiao J, Farag MA. MUFA in metabolic syndrome and associated risk factors: is MUFA the opposite side of the PUFA coin? Food Funct. 2021;12(24):12221–34. https://doi.org/10.1039/d1fo00979f First citation in articleCrossref MedlineGoogle Scholar

  • 46 Roman S, Ojeda-Granados C, Ramos-Lopez O, Panduro A. Genome-based nutrition: an intervention strategy for the prevention and treatment of obesity and nonalcoholic steatohepatitis. World J Gastroenterol. 2015;21:3449–61. https://doi.org/10.3748/wjg.v21.i12.3449 First citation in articleCrossref MedlineGoogle Scholar

  • 47 Ramos-López O, Ojeda-Granados C, Román S, Panduro A. Influencia genética en las preferencias alimentarias. Rev Endocrinol Nutr. 2013;21:74–83. First citation in articleGoogle Scholar

  • 48 Malik VS, Popkin BM, Bray GA, Després JP, Willett WC, Hu FB. Sugar-sweetened beverages and risk of metabolic syndrome and type 2 diabetes: a meta-analysis. Diabetes Care. 2010;33(11):2477–83. https://doi.org/10.2337/dc10-1079 First citation in articleCrossref MedlineGoogle Scholar

  • 49 Dinu M, Pagliai G, Casini A, Sofi F. Mediterranean diet and multiple health outcomes: an umbrella review of meta-analyses of observational studies and randomised trials. Eur J Clin Nutr. 2018;72:30–43. https://doi.org/10.1038/ejcn.2017.58 First citation in articleCrossref MedlineGoogle Scholar

  • 50 Czernichow S, Bruckert E, Bertrais S, Galan P, Hercberg S, Oppert JM. Hypertriglyceridemic waist and 7.5-year prospective risk of cardiovascular disease in asymptomatic middle-aged men. Int J Obes (Lond). 2007;31:791–6. https://doi.org/10.1038/sj.ijo.0803477 First citation in articleCrossref MedlineGoogle Scholar

  • 51 Irving BA, Davis CK, Brock DW, Weltman JY, Swift D, Barrett EJ, et al. The metabolic syndrome, hypertriglyceridemic waist, and cardiometabolic risk factor profile in obese women. Obe Metab. 2007;3:50–7. First citation in articleMedlineGoogle Scholar

  • 52 Fernández-García JC, Muñoz-Garach A, Martínez-González MÁ, Salas-Salvado J, Corella D, Hernáez Á, et al. Association between lifestyle and hypertriglyceridemic waist phenotype in the PREDIMED-plus study. Obesity (Silver Spring). 2020;28:537–43. https://doi.org/10.1002/oby.22728 First citation in articleCrossref MedlineGoogle Scholar