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Triglyceride glucose-waist to height ratio: a novel and effective marker for identifying hepatic steatosis in individuals with type 2 diabetes mellitus

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Abstract

Background

The triglyceride-glucose index (TyG), and TyG-driven parameters incorporating TyG and obesity indices have been proposed as reliable indicators of insulin resistance and its related comorbidities. This study evaluated the effectiveness of these indices in identifying hepatic steatosis in individuals with Type 2 diabetes (T2DM).

Methods

This was a cross-sectional study consisting of 175 patients with T2DM (122 with and 53 without NAFLD). TyG index, triglyceride glucose-body mass index (TyG-BMI), triglyceride glucose-waist circumference (TyG-WC), and triglyceride glucose-waist-to-height ratio (TyG-WHtR) were determined using standard formulas. Controlled attenuation parameter (CAP) was measured by transient elastography (FibroScan).

Results

Among obesity parameters, CAP showed the strongest correlation with WHtR, followed by BMI and WC (all P < 0.001). Regression analyses demonstrated TyG-WHtR as a significant predictor of NAFLD with the highest odds ratio, reaching 10.69 (95% CI: 1.68–68.22) for the top quartile (Q4) compared to the first quartile (P = 0.01), followed by TyG-BMI (Q4: 6.75; 95% CI: 1.49–30.67) and TyG-WC (Q4: 5.90; 95% CI: 0.99–35.18). Moreover, TyG-WHtR presented the largest AUC for detection of NAFLD (0.783, P < 0.001) in ROC analysis, followed by TyG-BMI (AUC: 0.751, P < 0.001), TyG-WC (AUC: 0.751, P < 0.001), and TyG (AUC: 0.647, P = 0.002). TyG-WHtR value of 5.58 (sensitivity: 79%, specificity: 68%, P < 0.001) was the best cut-off point to identify hepatic steatosis in this population.

Conclusions

This study confirmed that the TyG-related indices comprising TyG and obesity parameters can identify hepatic steatosis more successfully than TyG alone. Furthermore, our results highlighted TyG-WHtR as a simple and effective marker for screening fatty liver in patients with T2DM, which may be used practically in clinical setting.

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References

  1. N. Chalasani, Z. Younossi, J.E. Lavine, M. Charlton, K. Cusi, M. Rinella et al. The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American Association for the Study of Liver Diseases. Hepatology 67, 328–57 (2018)

    Article  Google Scholar 

  2. R. Kwok, K.C. Choi, G.L. Wong, Y. Zhang, H.L. Chan, A.O. Luk et al. Screening diabetic patients for non-alcoholic fatty liver disease with controlled attenuation parameter and liver stiffness measurements: a prospective cohort study. Gut 65, 1359–68 (2016)

    Article  CAS  PubMed  Google Scholar 

  3. Z. Younossi, Q.M. Anstee, M. Marietti, T. Hardy, L. Henry, M. Eslam et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat. Rev. Gastroenterol. Hepatol. 15, 11–20 (2018)

    Article  PubMed  Google Scholar 

  4. G. Targher, L. Bertolini, R. Padovani, S. Rodella, R. Tessari, L. Zenari et al. Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients. Diabetes Care 30, 1212–1218 (2007)

    Article  PubMed  Google Scholar 

  5. H. Tilg, A.R. Moschen, M. Roden, NAFLD and diabetes mellitus. Nat. Rev. Gastroenterol. Hepatol. 14, 32–42 (2017)

    Article  CAS  PubMed  Google Scholar 

  6. H. Poustchi, F. Alaei-Shahmiri, R. Aghili, S. Nobarani, M. Malek, M.E. Khamseh, Hepatic steatosis and fibrosis in type 2 diabetes: a risk-based approach to targeted screening. Arch. Iran. Med. 24, 177–186 (2021)

    Article  PubMed  Google Scholar 

  7. G. Targher, L. Bertolini, S. Rodella, R. Tessari, L. Zenari, G. Lippi et al. Nonalcoholic fatty liver disease is independently associated with an increased incidence of cardiovascular events in type 2 diabetic patients. Diabetes Care 30, 2119–21 (2007)

    Article  CAS  PubMed  Google Scholar 

  8. L.M. Alba, K. Lindor, Review article: non-alcoholic fatty liver disease. Aliment Pharm. Ther. 17, 977–86 (2003)

    Article  CAS  Google Scholar 

  9. L.E. Simental-Mendia, M. Rodriguez-Moran, F. Guerrero-Romero, The product of fasting glucose and triglycerides as surrogate for identifying insulin resistance in apparently healthy subjects. Metab. Syndr. Relat. Disord. 6, 299–304 (2008)

    Article  CAS  PubMed  Google Scholar 

  10. S. Zhang, T. Du, J. Zhang, H. Lu, X. Lin, J. Xie et al. The triglyceride and glucose index (TyG) is an effective biomarker to identify nonalcoholic fatty liver disease. Lipids Health Dis. 16, 15 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  11. M. Zhang, B. Wang, Y. Liu, X. Sun, X. Luo, C. Wang et al. Cumulative increased risk of incident type 2 diabetes mellitus with increasing triglyceride glucose index in normal-weight people: the Rural Chinese Cohort Study. Cardiovasc. Diabetol. 16, 30 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  12. L.K. Er, S. Wu, H.H. Chou, L.A. Hsu, M.S. Teng, Y.C. Sun et al. Triglyceride glucose-body mass index is a simple and clinically useful surrogate marker for insulin resistance in nondiabetic individuals. PLoS ONE 11, e0149731 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  13. S. Zheng, S. Shi, X. Ren, T. Han, Y. Li, Y. Chen et al. Triglyceride glucose-waist circumference, a novel and effective predictor of diabetes in first-degree relatives of type 2 diabetes patients: cross-sectional and prospective cohort study. J. Transl. Med. 14, 260 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  14. J. Lim, J. Kim, S.H. Koo, G.C. Kwon, Comparison of triglyceride glucose index, and related parameters to predict insulin resistance in Korean adults: an analysis of the 2007–2010 Korean National Health and Nutrition Examination Survey. PLoS ONE 14, e0212963 (2019)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. S.A. Parry, L. Hodson, Managing NAFLD in type 2 diabetes: the effect of lifestyle interventions, a narrative review. Adv. Ther. 37, 1381–406 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  16. C. Caussy, M.H. Alquiraish, P. Nguyen, C. Hernandez, S. Cepin, L.E. Fortney et al. Optimal threshold of controlled attenuation parameter with MRI-PDFF as the gold standard for the detection of hepatic steatosis. Hepatology 67, 1348–59 (2018)

    Article  CAS  PubMed  Google Scholar 

  17. W.T. Friedewald, R.I. Levy, D.S. Fredrickson, Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem. 18, 499–502 (1972)

    Article  CAS  PubMed  Google Scholar 

  18. E. Bonora, G. Targher, M. Alberiche, R.C. Bonadonna, F. Saggiani, M.B. Zenere et al. Homeostasis model assessment closely mirrors the glucose clamp technique in the assessment of insulin sensitivity: studies in subjects with various degrees of glucose tolerance and insulin sensitivity. Diabetes Care 23, 57–63 (2000)

    Article  CAS  PubMed  Google Scholar 

  19. J.H. Lee, D. Kim, H.J. Kim, C.H. Lee, J.I. Yang, W. Kim et al. Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Dig. Liver Dis. 42, 503–8 (2010)

    Article  CAS  PubMed  Google Scholar 

  20. H. Yang, G. Chen, C. Song, D. Li, Q. Ma, G. Chen et al. A novel index including SNPs for the screening of nonalcoholic fatty liver disease among elder Chinese: a population-based study. Medicine 97, e0272 (2018)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. A. Kotronen, M. Peltonen, A. Hakkarainen, K. Sevastianova, R. Bergholm, L.M. Johansson et al. Prediction of non-alcoholic fatty liver disease and liver fat using metabolic and genetic factors. Gastroenterology 137, 865–72 (2009)

    Article  CAS  PubMed  Google Scholar 

  22. F. Guerrero-Romero, L.E. Simental-Mendia, M. Gonzalez-Ortiz, E. Martinez-Abundis, M.G. Ramos-Zavala, S.O. Hernandez-Gonzalez et al. The product of triglycerides and glucose, a simple measure of insulin sensitivity. Comparison with the euglycemic-hyperinsulinemic clamp. J. Clin. Endocrinol. Metab. 95, 3347–51 (2010)

    Article  CAS  PubMed  Google Scholar 

  23. S.H. Lee, H.S. Kwon, Y.M. Park, H.S. Ha, S.H. Jeong, H.K. Yang et al. Predicting the development of diabetes using the product of triglycerides and glucose: the Chungju Metabolic Disease Cohort (CMC) study. PLoS ONE 9, e90430 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  24. C. Acierno, A. Caturano, P.C. Pafundi, R. Nevola, L.E. Adinolfi, F.C. Sasso, Nonalcoholic fatty liver disease and type 2 diabetes: pathophysiological mechanisms shared between the two faces of the same coin. Explor. Med. 1, 287–306 (2020).

    Article  Google Scholar 

  25. S.B. Lee, M.K. Kim, S. Kang, K. Park, J.H. Kim, S.J. Baik et al. Triglyceride glucose index is superior to the homeostasis model assessment of insulin resistance for predicting nonalcoholic fatty liver disease in korean adults. Endocrinol. Metab. 34, 179–86 (2019)

    Article  Google Scholar 

  26. L.E. Simental-Mendia, E. Simental-Mendia, H. Rodriguez-Hernandez, M. Rodriguez-Moran, F. Guerrero-Romero, The product of triglycerides and glucose as biomarker for screening simple steatosis and NASH in asymptomatic women. Ann. Hepatol. 15, 715–20 (2016)

    CAS  PubMed  Google Scholar 

  27. D.Y. Lee, E.S. Lee, J.H. Kim, S.E. Park, C.Y. Park, K.W. Oh et al. Predictive value of triglyceride glucose index for the risk of incident diabetes: a 4-year retrospective longitudinal study. PLoS ONE 11, e0163465 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  28. E. Tomas, Y.S. Lin, Z. Dagher, A. Saha, Z. Luo, Y. Ido et al. Hyperglycemia and insulin resistance: possible mechanisms. Ann. N. Y Acad. Sci. 967, 43–51 (2002)

    Article  CAS  PubMed  Google Scholar 

  29. J.M. Olefsky, J.W. Farquhar, G.M. Reaven, Reappraisal of the role of insulin in hypertriglyceridemia. Am. J. Med. 57, 551–60 (1974)

    Article  CAS  PubMed  Google Scholar 

  30. M. Mota, B.A. Banini, S.C. Cazanave, A.J. Sanyal, Molecular mechanisms of lipotoxicity and glucotoxicity in nonalcoholic fatty liver disease. Metabolism 65, 1049–61 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. M. Tomizawa, Y. Kawanabe, F. Shinozaki, S. Sato, Y. Motoyoshi, T. Sugiyama et al. Triglyceride is strongly associated with nonalcoholic fatty liver disease among markers of hyperlipidemia and diabetes. Biomed. Rep. 2, 633–6 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. K. Williams, N. Shackel, M. Gorrell, S. McLennan, S. Twigg, Diabetes and nonalcoholic fatty liver disease: a pathogenic duo. Endocr. Rev. 34, 84–129 (2013)

    Article  CAS  PubMed  Google Scholar 

  33. S. Zhang, T. Du, M. Li, J. Jia, H. Lu, X. Lin et al. Triglyceride glucose-body mass index is effective in identifying nonalcoholic fatty liver disease in nonobese subjects. Medicine 96, e7041 (2017)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. A. Kitae, Y. Hashimoto, M. Hamaguchi, A. Obora, T. Kojima, M. Fukui, The triglyceride and glucose index is a predictor of incident nonalcoholic fatty liver disease: a population-based cohort study. Can. J. Gastroenterol. Hepatol. 2019, 5121574 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  35. R. Zheng, Z. Du, M. Wang, Y. Mao, W. Mao, A longitudinal epidemiological study on the triglyceride and glucose index and the incident nonalcoholic fatty liver disease. Lipids Health Dis. 17, 262 (2018)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. M.E. Khamseh, M. Malek, R. Abbasi, H. Taheri, M. Lahouti, F. Alaei-Shahmiri, Triglyceride glucose index and related parameters (triglyceride glucose-body mass index and triglyceride glucose-waist circumference) identify nonalcoholic fatty liver and liver fibrosis in individuals with overweight/obesity. Metab. Syndr. Relat. Disord. 19(3), 167–173 (2021)

    Article  CAS  PubMed  Google Scholar 

  37. E.K. Hameed, TyG index a promising biomarker for glycemic control in type 2 diabetes mellitus. Diabetes Metab. Syndr. 13, 560–3 (2019)

    Article  PubMed  Google Scholar 

  38. E.Y. Lee, H.K. Yang, J. Lee, B. Kang, Y. Yang, S.H. Lee et al. Triglyceride glucose index, a marker of insulin resistance, is associated with coronary artery stenosis in asymptomatic subjects with type 2 diabetes. Lipids Health Dis. 15(1), 155 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  39. N. Li, H. Tan, A. Xie, C. Li, X. Fu, W. Xang et al. Value of the triglyceride glucose index combined with body mass index in predicting non-alcoholic fatty liver disease in patients with type 2 diabetes. Res. Squrare. (2020). https://www.researchsquare.com/article/rs-51148/v1

  40. Y. Chang, H.S. Jung, J. Cho, Y. Zhang, K.E. Yun, M. Lazo et al. Metabolically healthy obesity and the development of nonalcoholic fatty liver disease. Am. J. Gastroenterol. 111, 1133–40 (2016)

    Article  CAS  PubMed  Google Scholar 

  41. L. Li, D.W. Liu, H.Y. Yan, Z.Y. Wang, S.H. Zhao, B. Wang, Obesity is an independent risk factor for non-alcoholic fatty liver disease: evidence from a meta-analysis of 21 cohort studies. Obes. Rev. 17, 510–9 (2016)

    Article  CAS  PubMed  Google Scholar 

  42. R. Rocha, H.P. Cotrim, F.M. Carvalho, A.C. Siqueira, H. Braga, L.A. Freitas, Body mass index and waist circumference in non-alcoholic fatty liver disease. J. Hum. Nutr. Diet. 18, 365–70 (2005)

    Article  CAS  PubMed  Google Scholar 

  43. T. Bulum, K. Blaslov, L. Duvnjak, The use of anthropometric measurements of obesity in prediction of microvascular complications in obese type 2 diabetic patients. Acta Clin. Croat. 55, 217–23 (2016)

    Article  PubMed  Google Scholar 

  44. J.Y. Yim, D. Kim, S.H. Lim, M.J. Park, S.H. Choi, C.H. Lee, et al. Sagittal abdominal diameter is a strong anthropometric measure of visceral adipose tissue in the asian general population. Diabetes Care 33, 2665–2670 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  45. H.J. Schneider, J. Klotsche, S. Silber, G.K. Stalla, H.-U. Wittchen, Measuring abdominal obesity: effects of height on distribution of cardiometabolic risk factors risk using waist circumference and waist-to-height ratio. Diabetes Care 34, e7–e7 (2011)

    Article  PubMed  Google Scholar 

  46. H. Yang, Z. Xin, J.-P. Feng, J.-K. Yang, Waist-to-height ratio is better than body mass index and waist circumference as a screening criterion for metabolic syndrome in Han Chinese adults. Medicine 96, e8192 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  47. M. Ashwell, S.D. Hsieh, Six reasons why the waist-to-height ratio is a rapid and effective global indicator for health risks of obesity and how its use could simplify the international public health message on obesity. Int. J. Food Sci. Nutr. 56, 303–7 (2005)

    Article  PubMed  Google Scholar 

  48. R.-D. Zheng, Z.-R. Chen, J.-N. Chen, Y.-H. Lu, J. Chen, Role of body mass index, waist-to-height and waist-to-hip ratio in prediction of nonalcoholic fatty liver disease. Gastroenterol. Res. Pract. 2012, 362147 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  49. N. Motamed, B. Rabiee, G.R. Hemasi, H. Ajdarkosh, M.R. Khonsari, M. Maadi et al. Body roundness index and waist-to-height ratio are strongly associated with non-alcoholic fatty liver disease: a population-based study. Hepat. Mon. 16, e39575 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  50. R. Mansour-Ghanaei, F. Mansour-Ghanaei, M. Naghipour, F. Joukar, Z. Atrkar-Roushan, M. Tabatabaii et al. The role of anthropometric indices in the prediction of non-alcoholic fatty liver disease in the PERSIAN Guilan Cohort study (PGCS). J. Med. Life 11, 194–202 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  51. M.G. Swainson, A.M. Batterham, C. Tsakirides, Z.H. Rutherford, K. Hind, Prediction of whole-body fat percentage and visceral adipose tissue mass from five anthropometric variables. PLoS ONE 12, e0177175 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  52. N. Pimenta, H. Cortez-Pinto, X. Melo, J. Silva‐Nunes, L. Sardinha, H. Santa-Clara, Waist-to-height ratio is independently related to whole and central body fat, regardless of the waist circumference measurement protocol, in non‐alcoholic fatty liver disease patients. J. Hum. Nutr. Diet. 30, 185–92 (2017)

    Article  CAS  PubMed  Google Scholar 

  53. Q. Li, M. Dhyani, J.R. Grajo, C. Sirlin, A.E. Samir, Current status of imaging in nonalcoholic fatty liver disease. World J. Hepatol. 10, 530–42 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported by Iran University of Medical Sciences (IUMS) (Research project number: 98-4-24-16770).

Author contributions

M.E.K., M.M., and F.A.S. were involved in the conception and design of the study. S.N. and H.C. were involved in data collection. Data were analyzed and interpreted by F.A.S. who was also involved in drafting the manuscript. All authors have participated in reviewing the manuscript and approved the final version.

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Correspondence to Fariba Alaei-Shahmiri.

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The authors declare no competing interests.

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The current study was carried out under Helsinki Declaration and approved by ethics committee of Iran University of Medical Sciences (Approval number: IR.IUMS.REC.1398.1045).

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Malek, M., Khamseh, M.E., Chehrehgosha, H. et al. Triglyceride glucose-waist to height ratio: a novel and effective marker for identifying hepatic steatosis in individuals with type 2 diabetes mellitus. Endocrine 74, 538–545 (2021). https://doi.org/10.1007/s12020-021-02815-w

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