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The triglyceride-waist circumference index is a valid biomarker of metabolic syndrome in African Americans

Published:November 22, 2022DOI:https://doi.org/10.1016/j.amjms.2022.11.003

      Abstract

      Background

      The hypertriglyceridemia waist (HTGW) phenotype is associated with visceral adiposity, metabolic syndrome, type 2 diabetes mellitus (T2DM) and atherosclerotic cardiovascular disease (ASCVD). Since the cut points for abdominal obesity and hypertriglyceridemia, differ for different race groups, investigators have developed the product of triglycerides (TG) and waist circumference (WC) as the TG.WC index. We compared this TG.WC index to the TG:HDL-C ratio in the National Health and Nutrition Examination Survey (NHANES) study to predict metabolic syndrome (MetS) in African Americans (AAs).

      Methods

      Participants included 950 AAs and 2651 non-Hispanic Whites (NHWs) for comparison from the NHANES data set. Persons with diabetes, ASCVD and macro-inflammation were excluded. Fasting blood was obtained for lipids, insulin and CRP.

      Results

      In AAs and NHWs, both the TG.WC index and TG:HDL-C ratio were significantly increased in MetS patients. Also, both increased with increasing severity of MetS and correlated with all features of MetS, insulin resistance and inflammation. Receiver operating characteristic (ROC) curve analysis showed that discrimination with TG.WC for MetS was superior to the TG:HDL-C ratio especially in AAs.

      Conclusions

      TG.WC index is a superior biomarker to TG:HDL-C for predicting MetS in AAs despite their lower TG levels.

      Keywords

      Introduction

      Racial disparities in health care are pronounced in the US especially as it relates to minorities, such as African Americans (AAs).
      • Airhihenbuwa C.O.
      • Liburd L.
      Eliminating health disparities in the African American population: the interface of culture, gender, and power.
      The issue of differential health outcomes based on race clearly pertains to the area of cardio-metabolic disorders.
      It has been shown, using cut points for non-Hispanic whites (NHWs), that the hypertriglyceridemia waist (HTGW) phenotype, the simultaneous presence of increased waist circumference (WC) and hypertriglyceridemia, is strongly associated with cardio-metabolic risk, metabolic syndrome (MetS), type 2 diabetes mellitus (T2DM) and atherosclerotic cardiovascular disease (ASCVD).
      • Lemieux I.
      • Poirier P.
      • Bergeron J.
      • Alméras N.
      • Lamarche B.
      • Cantin B.
      • Dagenais G.R.
      • Deprés J.P.
      Hypertriglyceridemic waist: a useful screening phenotype in preventive cardiology?.
      • Després J.P.
      • Lemieux I.
      • Bergeron J.
      • Pibarot P.
      • Mathieu P.
      • Larose E.
      • Rodés-Cabau J.
      • Bertrand O.F.
      • Poirier P.
      Abdominal obesity and the metabolic syndrome: contribution to global cardio-metabolic risk.
      • Tchernof A.
      • Després J.P.
      Pathophysiology of human visceral obesity: an update.
      This was supported by many but not all studies in various parts of the world.
      • Sam S.
      • Haffner S.
      • Davidson M.H.
      • D'Agostino Sr., R.B.
      • Feinstein S.
      • Kondos G.
      • Perez A.
      • Mazzone T.
      Hypertriglyceridemic waist phenotype predicts increased visceral fat in subjects with type 2 diabetes.
      • Gasevic D.
      • Carlsson A.C.
      • Lesser I.A.
      • John Mancini G.B.
      • Lear S.A.
      The association between “hypertriglyceridemic waist” and sub-clinical atherosclerosis in a multiethnic population: a cross-sectional study.
      • Xu M.
      • Huang M.
      • Qiang D.
      • Gu J.
      • Li Y.
      • Pan Y.
      • Yao X.
      • Xu W.
      • Tao Y.
      • Zhou Y.
      • Ma H.
      Hypertriglyceridemic waist phenotype and lipid accumulation product: two comprehensive obese indicators of waist circumference and triglyceride to predict type 2 diabetes mellitus in Chinese population.
      • Lee B.J.
      • Kim J.Y.
      Identification of metabolic syndrome using phenotypes consisting of triglyceride levels with anthropometric indices in Korean adults.
      • Janghorbani M.
      • Amini M.
      Utility of hypertriglyceridemic waist phenotype for predicting incident type 2 diabetes prevention study.
      Based on a preliminary study of only 66 men, HTGW was not found to be a valid measure of the metabolic triad and ASCVD in AAs.
      • Yu S.S.K.
      • Castillo D.C.
      • Courville A.B.
      • Sumner AE.
      The triglyceride paradox in people of African descent.
      Due to the wide variation in waist circumference criteria in different races, investigators have instead quantitatively defined the TG.WC index as the product of WC and TG, using both as continuous variables. This new TG.WC index classified patients for their cardio-metabolic risk like the original definition of the HTGW phenotype.
      • Yang R.F.
      • Liu X.Y.
      • Lin Z.
      • Zhang G.
      Correlation study on waist circumference triglyceride (WT) index and coronary artery scores in patients with coronary heart disease.
      • Liu P.J.
      • Lou H.P.
      • Zhu YN.
      Screening for metabolic syndrome using an integrated continuous index consisting of waist circumference and triglyceride: a preliminary cross-sectional study.
      • Okosun I.S.
      • Okosun B.
      • Lyn R.
      • Airhihenbuwa C.
      Surrogate indexes of insulin resistance and risk of metabolic syndrome in non-Hispanic White, non-Hispanic Black and Mexican American.
      • de Cuevillas B.
      • Alvarez-Alvarez I.
      • Riezu-Boj J.I.
      • Navas-Carretero S.
      • Martinez J.A.
      The hypertriglyceridemic-waist phenotype as a valuable and integrative mirror of metabolic syndrome traits.
      • Jialal I.
      • Adams-Huet B.
      Comparison of the triglyceride-waist circumference and the C-reactive protein-waist circumference indices in nascent metabolic syndrome.
      MetS is a common global disorder comprising a cardio-metabolic cluster that predisposes to both type 2 diabetes mellitus (T2DM) and atherosclerotic cardiovascular disease (ASCVD).
      • Grundy S.M.
      • Cleeman J.I.
      • Daniels S.R.
      • Donato K.A.
      • Eckel R.H.
      • Franklin B.A.
      • Gordon D.J.
      • Krauss R.M.
      • Savage P.J.
      • Smith Jr, S.C.
      • Spertus J.A.
      • Costa F.
      Diagnosis and management of the metabolic syndrome: an American heart association/national heart, lung, and blood institute scientific statement.
      Recently it was shown, using this large National Health and Nutrition Examination Survey (NHANES) data set, that the ratio of triglycerides (TG) to high-density lipoprotein cholesterol (HDL-C) (TG:HDL-C) ratio is a better biomarker of MetS in AAs compared to the CRP:HDL-C ratio, despite their lower TG and higher CRP levels.
      • Jialal I.
      • Adams-Huet B.
      • Remaley AT.
      A comparison of the ratios of C-reactive protein and triglycerides to high-density lipoprotein-cholesterol as biomarkers of metabolic syndrome in African Americans and non-Hispanic Whites.
      In an attempt to improve the assessment of cardio-metabolic disease risk in AAs, in the present report, we compared, the TG.WC index to the TG:HDL-C ratio in AAs and NHWs in the large NHANES study to determine which is the superior biomarker for MetS.

      Methods

      Data from the US general population National Health and Nutrition Examination Survey (NHANES) cycles from 2005 to 2018) (https://www.cdc.gov/nchs/nhanes/index.htm) collected by the Centers of Disease Control and Prevention (CDC),
      • Jialal I.
      • Adams-Huet B.
      • Remaley AT.
      A comparison of the ratios of C-reactive protein and triglycerides to high-density lipoprotein-cholesterol as biomarkers of metabolic syndrome in African Americans and non-Hispanic Whites.
      • Li C.
      • Ford E.S.
      • Meng Y.X.
      • Mokdad A.H.
      • Reaven G.M.
      Does the association of the triglyceride to high-density lipoprotein cholesterol ratio with fasting serum insulin differ by race/ethnicity?.
      • Ford E.S.
      • Li C.
      • Zhao G.
      Prevalence and correlates of metabolic syndrome based on a harmonious definition among adults in the US.
      was used for analysis. NHANES was approved by the National Center for Health Statistics institutional review board and written consent was obtained from all participants. The work described has been carried out in accordance with the Code of Ethics of the World Medical Association for experiments involving human subjects. As described previously, the data set was restricted to NHW and non-Hispanic AA participants of either sex aged 20-80 years.
      • Jialal I.
      • Adams-Huet B.
      • Remaley AT.
      A comparison of the ratios of C-reactive protein and triglycerides to high-density lipoprotein-cholesterol as biomarkers of metabolic syndrome in African Americans and non-Hispanic Whites.
      Participants were defined as having MetS, if they had three or more cardio-metabolic features of MetS.
      • Grundy S.M.
      • Cleeman J.I.
      • Daniels S.R.
      • Donato K.A.
      • Eckel R.H.
      • Franklin B.A.
      • Gordon D.J.
      • Krauss R.M.
      • Savage P.J.
      • Smith Jr, S.C.
      • Spertus J.A.
      • Costa F.
      Diagnosis and management of the metabolic syndrome: an American heart association/national heart, lung, and blood institute scientific statement.
      WC was measured to the nearest 0.1 cm by trained personnel at the level of the ilium following normal respiratory expiration. Controls (non-MetS) needed to have 2 or fewer features of MetS and not be on blood pressure medications. To minimize confounding by other variables and to better focus on MetS in a nascent stage, exclusion criteria included diabetes, smoking and macro-inflammation (defined by a hsCRP >10mg/L and or an increased total white blood cell count).
      • Jialal I.
      • Devaraj S.
      • Adams-Huet B.
      • Chen X.
      • Kaur H.
      Increased cellular and circulating biomarkers of oxidative stress in nascent metabolic syndrome.
      A total of n = 3541 individuals (2635 controls and 906 MetS) were identified in this study. The TG.WC index was calculated as the product of triglycerides (mmol/L) x waist circumference (cm).
      • de Cuevillas B.
      • Alvarez-Alvarez I.
      • Riezu-Boj J.I.
      • Navas-Carretero S.
      • Martinez J.A.
      The hypertriglyceridemic-waist phenotype as a valuable and integrative mirror of metabolic syndrome traits.
      ,
      • Jialal I.
      • Adams-Huet B.
      Comparison of the triglyceride-waist circumference and the C-reactive protein-waist circumference indices in nascent metabolic syndrome.
      Laboratory tests were assayed by standardized techniques, as described previously.
      • Li C.
      • Ford E.S.
      • Meng Y.X.
      • Mokdad A.H.
      • Reaven G.M.
      Does the association of the triglyceride to high-density lipoprotein cholesterol ratio with fasting serum insulin differ by race/ethnicity?.
      ,
      • Ford E.S.
      • Li C.
      • Zhao G.
      Prevalence and correlates of metabolic syndrome based on a harmonious definition among adults in the US.
      Hepatic insulin resistance was calculated using the homeostasis model assessment of insulin resistance (HOMA-IR).
      • Jialal I.
      • Devaraj S.
      • Adams-Huet B.
      • Chen X.
      • Kaur H.
      Increased cellular and circulating biomarkers of oxidative stress in nascent metabolic syndrome.
      SAS version 9.4 (SAS Institute, Cary, NC) was used for statistical analysis. Stratified by race, TG.WC index and TG:HDL-C ratio were expressed as median and interquartile ranges. The MetS and control groups were compared with the Wilcoxon Rank Sum test. Trend analysis of the ratios associated with increasing number of characteristics of MetS in subjects was evaluated using the Jonckheere-Terpstra (J-T) test. After combining the control and MetS groups, Spearman rank correlation coefficients were determined to assess the association between TG.WC index and TG:HDL-C ratio and metabolic variables. Logistic regression models were used to compute receiver operating characteristic (ROC) curves. Comparison of areas under correlated ROC curves and 95% confidence intervals (CI) for the ROC area under curve (AUC) for biomarkers and biomarker differences were determined. The Youden Index was defined as the maximum value of sensitivity + specificity - 1. Significance was defined as a 2-sided p value <0.05.

      Results

      In this study, the same cohort from the NHANES population in which the TG:HDL-C ratio was recently shown to be a valid biomarker of MetS in AAs was used.
      • Jialal I.
      • Adams-Huet B.
      • Remaley AT.
      A comparison of the ratios of C-reactive protein and triglycerides to high-density lipoprotein-cholesterol as biomarkers of metabolic syndrome in African Americans and non-Hispanic Whites.
      Details on the demographic and metabolic characteristics of the cohort can be obtained from that publication.
      • Jialal I.
      • Adams-Huet B.
      • Remaley AT.
      A comparison of the ratios of C-reactive protein and triglycerides to high-density lipoprotein-cholesterol as biomarkers of metabolic syndrome in African Americans and non-Hispanic Whites.
      Briefly, the participants with MetS had significant differences in all cardio-metabolic features. In AAs the median WC, systolic BP, glucose, TG and HDL-C were significant different compared to controls, p < 0.0001: WC 109.5 cm vs 93.2 cm, systolic BP 136 mmHg vs 118 mmHg, glucose 112 mg/dl vs 95 mg/dl, TG 118 mg/dl vs 68 mg/dl and HDL-C 46 mg/dl vs 57 mg/dl. Also, HOMA-IR 1.83 vs 0.97 and hsCRP 2.9 mg/L vs 1.4 mg/L were significantly higher in AAs with MetS, p < 0.0001. As reported previously, AAs with MetS had lower TG levels (118 mg/dl vs 173 mg/dl, p < 0.001) and higher HDL-C levels (46 mg/dl vs 43 mg/dl, p = 0.0008) compared to NHWs.
      • Summer A.E.
      • Finley K.B.
      • Genovese D.J.
      • Criqui M.H.
      • Boston RC.
      Fasting triglyceride and the triglyceride-HDL cholesterol ratio are not markers of insulin resistance in African Americans.
      ,
      • Kim-Dorner S.J.
      • Deuster P.A.
      • Zeno S.A.
      • Remaley A.T.
      • Poth M.
      Should triglycerides and the triglycerides to high-density lipoprotein cholesterol ratio be used as surrogates for insulin resistance?.
      In both races, the TG:HDL-C
      • Jialal I.
      • Adams-Huet B.
      • Remaley AT.
      A comparison of the ratios of C-reactive protein and triglycerides to high-density lipoprotein-cholesterol as biomarkers of metabolic syndrome in African Americans and non-Hispanic Whites.
      ratio and TG.WC index were significantly increased in patients with MetS compared to controls, p < 0.0001 (Fig. 1). Both ratios increased significantly with increasing severity (number of cardio-metabolic features) of MetS, using the J-T test for trend; p < 0.0001 for both. In both AAs and NHWs patients, the TG.WC index was significantly correlated with all five features of MetS, as well as with hsCRP and HOMA-IR (Table 1). The TG.WC index was significantly higher in NHWs (median and inter-quartile range) 211 (160–280) compared to AAs 155 (99–233) with MetS, p < 0.0001. The TG:HDL-C ratio was also significantly higher in NHWs compared to the AAs in both the MetS and control groups, as previously reported.
      • Jialal I.
      • Adams-Huet B.
      • Remaley AT.
      A comparison of the ratios of C-reactive protein and triglycerides to high-density lipoprotein-cholesterol as biomarkers of metabolic syndrome in African Americans and non-Hispanic Whites.
      Fig 1
      Fig. 1A comparison of the TG.WC Index between MetS and controls in both races. Abbreviations: AAs, African Americans; MetS, metabolic syndrome; NHWs, non-Hispanic Whites; TG, triglycerides; WC, waist circumference.
      Table 1Spearman rank correlation between TG.WC and relevant cardio-metabolic variables in AA and NHW
      AANHW
      Rho coefficientP -valuesRho coefficientP -values
      Waist Circumference (cm)0.58<0.00010.61<0.0001
      BP-s (mmHg)0.31<0.00010.30<0.0001
      BP-d (mmHg)0.22<0.00010.18<0.0001
      Glucose (mg/dL)0.31<0.00010.32<0.0001
      Triglycerides (mg/dL)0.97<0.00010.97<0.0001
      HDL-C (mg/dL)-0.44<0.0001-0.54<0.0001
      hsCRP (mg/L)0.38<0.00010.40<0.0001
      HOMA-IR0.53<0.00010.57<0.0001
      Spearman rho correlation coefficient with p values
      ROC curve analyses for predicting MetS for the two indices is shown in Fig. 2. ROC-AUC (95% CI) for TG.WC for AAs and NHWs were excellent, according to the criteria of Hosmer and Lemeshow
      • Hosmer D.W.
      • Lemeshow S.
      Applied Logistic Regression.
      : 0.82 with 95% confidence intervals (CI) between 0.79–0.86 and 0.86 with 95% CI of 0.85-0.88. The ROC-AUC for NHWs compared to AAs was significantly higher, p = 0.04. As reported recently
      • Jialal I.
      • Adams-Huet B.
      • Remaley AT.
      A comparison of the ratios of C-reactive protein and triglycerides to high-density lipoprotein-cholesterol as biomarkers of metabolic syndrome in African Americans and non-Hispanic Whites.
      the ROC-AUC for TG:HDL-C was also significantly greater in NHWs compared to AAs, 0.85 (95% CI, 0.83-0.87) versus 0.79 (95% CI, 0.75-0.83) respectively, p = 0.004. In both the AA and NHW groups, the TG.WC index was a better predictor of MetS than the TG:HDL-C ratio, as shown in Fig. 2: in AAs 0.82 versus 0.79, AUC difference 0.03 (0.01, 0.05), p = 0.001; in NHWs 0.86 versus 0.85, AUC difference 0.01 (0.003, 0.02), p = 0.004. The improvement in the AUC by the TG.WC index for the NHWs group was smaller. The Youden index of TG. WC was computed to provide a practical cut point, it was 113 for AAs (sensitivity 0.78 and specificity 0.71) and 154 for NHWs (sensitivity 0.82 and specificity 0.77).
      Fig 2
      Fig. 2Comparison of receiver operating characteristic (ROC) area under the curves (AUC) between TG.WC index and TG:HDL-C ratio in AAs (p = 0.001) and NHWs (p = 0.004). Abbreviations: AAs, African Americans; HDL-C, high-density lipoprotein cholesterol; MetS, metabolic syndrome; NHWs, non-Hispanic Whites; TG, triglycerides; WC, waist circumference.

      Discussion

      Given the disparities in health care, particularly in AAs, we decided to focus on how well current and new biomarkers of cardio-metabolic risk work in this group. In the present report, we tested the TG.WC index as a biomarker of MetS since it uses both measures as continuous variables. The original criteria for the HTGW phenotype were based on NHWs data in Canadians and not AAs and was shown to severely underestimate risk in AAs.
      • Sumner A.E.
      • CC C.
      Ethnic differences in the ability of triglyceride levels to identify insulin resistance.
      Furthermore, only 41% of a well curated cohort of nascent MetS (predominantly NHWs) had a HTGW by Despres criteria.
      • Jialal I.
      • Adams-Huet B.
      Comparison of the triglyceride-waist circumference and the C-reactive protein-waist circumference indices in nascent metabolic syndrome.
      In the present report, we showed in both AAs and NHWs patients in this large cohort based on the US general population (NHANES) that the TG.WC index is superior to the well-known TG:HDL-C ratio in predicting MetS. In fact, the TG.WC index AUC compared to the TG:HDL-C AUC was significantly greater in AAs compared to the corresponding differences in NHWs. Furthermore, the TG.WC index correlated with all features of MetS, inflammation and insulin resistance and increased with increasing severity of MetS. Also, we provide the Youden index of 113 as a reasonable and practical decision point of increased cardio-metabolic risk in AAs. Despite the deficiencies in criteria to diagnose MetS in AAs based on their more favorable TG and HDL-C levels the most recent prevalence data (2011–2012) shows similar prevalence of MetS in NHWs and AAs of 37.4% and 35.5% respectively.
      • Aguilar M.
      • Bhuket T.
      • Torres S.
      • Liu B.
      • Wong R.J.
      Prevalence of metabolic syndrome in the United States, 2003–2012.
      We believe our simple TG.WC index will facilitate early and greater diagnosis of MetS in AAs resulting in better management to forestall the sequalae of T2DM and ASCVD.
      Some authors have used an index comprising 3 of the 5 features of MetS, glucose, TG and WC.
      • Okosun I.S.
      • Okosun B.
      • Lyn R.
      • Airhihenbuwa C.
      Surrogate indexes of insulin resistance and risk of metabolic syndrome in non-Hispanic White, non-Hispanic Black and Mexican American.
      ,
      • de Cuevillas B.
      • Alvarez-Alvarez I.
      • Riezu-Boj J.I.
      • Navas-Carretero S.
      • Martinez J.A.
      The hypertriglyceridemic-waist phenotype as a valuable and integrative mirror of metabolic syndrome traits.
      Since one needs 3 of the 5 features to sustain a diagnosis of MetS, we are unclear of the added value of this measure as a biomarker. Nonetheless in a Spanish population (n = 314), the TG.WC index was equivalent in predicting MetS compared to the TG.Glucose.WC index with similar ROC-AUC of 0.81 for both.
      • de Cuevillas B.
      • Alvarez-Alvarez I.
      • Riezu-Boj J.I.
      • Navas-Carretero S.
      • Martinez J.A.
      The hypertriglyceridemic-waist phenotype as a valuable and integrative mirror of metabolic syndrome traits.
      In the other report, they did not compare these 2 indices in predicting MetS but focused on the TG.Glucose.WC index.
      • Okosun I.S.
      • Okosun B.
      • Lyn R.
      • Airhihenbuwa C.
      Surrogate indexes of insulin resistance and risk of metabolic syndrome in non-Hispanic White, non-Hispanic Black and Mexican American.
      We strongly believe that biomarker research to define MetS should be confined to 2 or fewer features and metabolomics or proteomic biomarkers since 3 features define the syndrome and are cumbersome for clinical and research use.

      Conclusions

      In conclusion, in this study we show that the novel TG.WC index, using both as continuous variables instead of cut points defined for NHWs, is a superior measure of predicting MetS in African Americans than the more commonly used TG:HDL-C ratio. Furthermore, we provide a cut point using the Youden index of 113 to define cardio-metabolic risk in AAs. Thus, with a fasting lipid profile and tape measure one can assess cardio-metabolic risk at the bedside. In future studies, it will be instructive for investigators with other larger data sets comprising AAs to confirm our novel findings.

      Source of funding

      There was no funding for this research.

      Declaration of Competing Interest

      No conflicts of interest, financial or otherwise, are declared by any of the authors.

      Acknowledgments

      We thank the volunteers for participating in this study. We thank Maureen Samson from NIH for providing us access to the NHANES data.

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