Skip to main content
Top
Published in: Journal of Translational Medicine 1/2022

Open Access 01-12-2022 | Fatty Liver | Research

The triglyceride glucose-body mass index: a non-invasive index that identifies non-alcoholic fatty liver disease in the general Japanese population

Authors: Haofei Hu, Yong Han, Changchun Cao, Yongcheng He

Published in: Journal of Translational Medicine | Issue 1/2022

Login to get access

Abstract

Background

By identifying individuals at high risk for non-alcoholic fatty liver disease (NAFLD), interventional programs could be targeted more effectively. Some studies have demonstrated that triglyceride glucose-body mass index (TyG-BMI) showed an independent positive association with NAFLD. However, research on its diagnostic value in patients with suspected NAFLD is limited. In this study, we aimed to evaluate whether TyG-BMI was accurate in detecting NAFLD in the general Japanese population.

Methods

A cross-sectional study of 14,280 individuals who underwent a comprehensive health examination was conducted. Standard protocols were followed to collect anthropometric measurements, lab data, and ultrasonography features. All participants were randomly stratified into the development group (n = 7118) and validation group (n = 7162). The TyG-BMI was calculated. Following this, the diagnostic value of the TyG-BMI was evaluated based on the area under the receiver-operating characteristic curve (AUROC). Two cutoff points were selected and used to rule out or rule in the NALFD, and the specificity, sensitivity, negative predictive value, and positive predictive value were explored, respectively. In order to verify the stability of the results, external verification was performed.

Results

There were 1272 and 1243 NAFLD participants in the development and validation groups, respectively. The area under the ROC curve (AUC) of TyG-BMI was 0.888 (95% CI 0.876–0.896) and 0.884 (95% CI 0.875–0.894) for the training and validation group, respectively. Using the low TyG-BMI (182.2) cutoff, NAFLD could be excluded with high accuracy (negative predictive value: 96.9% in estimation and 96.9% in validation). The presence of NAFLD could effectively be determined by applying the high cutoff of TyG-BMI (224.0), as the positive predictive value of the estimation and validation groups is 70.7% and 70.1%, respectively. As a result of applying this model, 9996 (70%) of the 14,280 participants would not have undergone ultrasonography, with an accurate prediction of 9308 (93.1%). AUC was 0.874 for external validation using 183,730 Chinese non-obese participants. TyG-BMI was demonstrated to be an excellent diagnostic tool by both internal and external validation.

Conclusions

In conclusion, the present study developed and validated a simple, non-invasive, and cost-effective tool to accurately separate participants with and without NAFLD in the Japanese population, rendering ultrasonography for identifying NAFLD unnecessary in a substantial proportion of people.
Appendix
Available only for authorised users
Literature
1.
2.
go back to reference Raj H, Durgia H, Palui R, Kamalanathan S, Selvarajan S, Kar SS, Sahoo J. SGLT-2 inhibitors in non-alcoholic fatty liver disease patients with type 2 diabetes mellitus: a systematic review. World J Diabetes. 2019;10:114–32.PubMedPubMedCentralCrossRef Raj H, Durgia H, Palui R, Kamalanathan S, Selvarajan S, Kar SS, Sahoo J. SGLT-2 inhibitors in non-alcoholic fatty liver disease patients with type 2 diabetes mellitus: a systematic review. World J Diabetes. 2019;10:114–32.PubMedPubMedCentralCrossRef
3.
go back to reference Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther. 2011;34:274–85.PubMedCrossRef Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther. 2011;34:274–85.PubMedCrossRef
4.
go back to reference Calzadilla BL, Adams LA. The natural course of non-alcoholic fatty liver disease. Int J Mol Sci. 2016;17:774.CrossRef Calzadilla BL, Adams LA. The natural course of non-alcoholic fatty liver disease. Int J Mol Sci. 2016;17:774.CrossRef
5.
go back to reference Soon G, Wee A. Updates in the quantitative assessment of liver fibrosis for nonalcoholic fatty liver disease: histological perspective. Clin Mol Hepatol. 2021;27:44–57.PubMedCrossRef Soon G, Wee A. Updates in the quantitative assessment of liver fibrosis for nonalcoholic fatty liver disease: histological perspective. Clin Mol Hepatol. 2021;27:44–57.PubMedCrossRef
6.
go back to reference Söderberg C, Stål P, Askling J, Glaumann H, Lindberg G, Marmur J, Hultcrantz R. Decreased survival of subjects with elevated liver function tests during a 28-year follow-up. Hepatology. 2010;51:595–602.PubMedCrossRef Söderberg C, Stål P, Askling J, Glaumann H, Lindberg G, Marmur J, Hultcrantz R. Decreased survival of subjects with elevated liver function tests during a 28-year follow-up. Hepatology. 2010;51:595–602.PubMedCrossRef
7.
go back to reference Sanyal AJ, Harrison SA, Ratziu V, Abdelmalek MF, Diehl AM, Caldwell S, Shiffman ML, Aguilar SR, Jia C, McColgan B, et al. The Natural history of advanced fibrosis due to nonalcoholic steatohepatitis: data from the simtuzumab trials. Hepatology. 2019;70:1913–27.PubMedCrossRef Sanyal AJ, Harrison SA, Ratziu V, Abdelmalek MF, Diehl AM, Caldwell S, Shiffman ML, Aguilar SR, Jia C, McColgan B, et al. The Natural history of advanced fibrosis due to nonalcoholic steatohepatitis: data from the simtuzumab trials. Hepatology. 2019;70:1913–27.PubMedCrossRef
9.
go back to reference Adams LA, Anstee QM, Tilg H, Targher G. Non-alcoholic fatty liver disease and its relationship with cardiovascular disease and other extrahepatic diseases. Gut. 2017;66:1138–53.PubMedCrossRef Adams LA, Anstee QM, Tilg H, Targher G. Non-alcoholic fatty liver disease and its relationship with cardiovascular disease and other extrahepatic diseases. Gut. 2017;66:1138–53.PubMedCrossRef
10.
go back to reference Ballestri S, Mantovani A, Nascimbeni F, Lugari S, Lonardo A. Extra-hepatic manifestations and complications of nonalcoholic fatty liver disease. Future Med Chem. 2019;11:2171–92.PubMedCrossRef Ballestri S, Mantovani A, Nascimbeni F, Lugari S, Lonardo A. Extra-hepatic manifestations and complications of nonalcoholic fatty liver disease. Future Med Chem. 2019;11:2171–92.PubMedCrossRef
11.
go back to reference Wang XJ, Malhi H. Nonalcoholic fatty liver disease. Ann Intern Med. 2018;169:C65–80.CrossRef Wang XJ, Malhi H. Nonalcoholic fatty liver disease. Ann Intern Med. 2018;169:C65–80.CrossRef
12.
go back to reference Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M, Sanyal AJ. The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012;55:2005–23.PubMedCrossRef Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M, Sanyal AJ. The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012;55:2005–23.PubMedCrossRef
13.
go back to reference Davison BA, Harrison SA, Cotter G, Alkhouri N, Sanyal A, Edwards C, Colca JR, Iwashita J, Koch GG, Dittrich HC. Suboptimal reliability of liver biopsy evaluation has implications for randomized clinical trials. J Hepatol. 2020;73:1322–32.PubMedCrossRef Davison BA, Harrison SA, Cotter G, Alkhouri N, Sanyal A, Edwards C, Colca JR, Iwashita J, Koch GG, Dittrich HC. Suboptimal reliability of liver biopsy evaluation has implications for randomized clinical trials. J Hepatol. 2020;73:1322–32.PubMedCrossRef
14.
go back to reference Hernaez R, Lazo M, Bonekamp S, Kamel I, Brancati FL, Guallar E, Clark JM. Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: a meta-analysis. Hepatology. 2011;54:1082–90.PubMedCrossRef Hernaez R, Lazo M, Bonekamp S, Kamel I, Brancati FL, Guallar E, Clark JM. Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: a meta-analysis. Hepatology. 2011;54:1082–90.PubMedCrossRef
15.
go back to reference Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, Harrison SA, Brunt EM, Sanyal AJ. The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American Association for the Study of Liver Diseases. Hepatology. 2018;67:328–57.PubMedCrossRef Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, Harrison SA, Brunt EM, Sanyal AJ. The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American Association for the Study of Liver Diseases. Hepatology. 2018;67:328–57.PubMedCrossRef
16.
go back to reference Fedchuk L, Nascimbeni F, Pais R, Charlotte F, Housset C, Ratziu V. Performance and limitations of steatosis biomarkers in patients with nonalcoholic fatty liver disease. Aliment Pharmacol Ther. 2014;40:1209–22.PubMedCrossRef Fedchuk L, Nascimbeni F, Pais R, Charlotte F, Housset C, Ratziu V. Performance and limitations of steatosis biomarkers in patients with nonalcoholic fatty liver disease. Aliment Pharmacol Ther. 2014;40:1209–22.PubMedCrossRef
17.
go back to reference Zhang B, Ding F, Chen T, Xia LH, Qian J, Lv GY. Ultrasound hepatic/renal ratio and hepatic attenuation rate for quantifying liver fat content. World J Gastroenterol. 2014;20:17985–92.PubMedPubMedCentralCrossRef Zhang B, Ding F, Chen T, Xia LH, Qian J, Lv GY. Ultrasound hepatic/renal ratio and hepatic attenuation rate for quantifying liver fat content. World J Gastroenterol. 2014;20:17985–92.PubMedPubMedCentralCrossRef
18.
go back to reference Dasarathy S, Dasarathy J, Khiyami A, Joseph R, Lopez R, McCullough AJ. Validity of real time ultrasound in the diagnosis of hepatic steatosis: a prospective study. J Hepatol. 2009;51:1061–7.PubMedPubMedCentralCrossRef Dasarathy S, Dasarathy J, Khiyami A, Joseph R, Lopez R, McCullough AJ. Validity of real time ultrasound in the diagnosis of hepatic steatosis: a prospective study. J Hepatol. 2009;51:1061–7.PubMedPubMedCentralCrossRef
19.
go back to reference Zhou JH, Cai JJ, She ZG, Li HL. Noninvasive evaluation of nonalcoholic fatty liver disease: current evidence and practice. World J Gastroenterol. 2019;25:1307–26.PubMedPubMedCentralCrossRef Zhou JH, Cai JJ, She ZG, Li HL. Noninvasive evaluation of nonalcoholic fatty liver disease: current evidence and practice. World J Gastroenterol. 2019;25:1307–26.PubMedPubMedCentralCrossRef
20.
go back to reference Castera L, Friedrich-Rust M, Loomba R. Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology. 2019;156:1264–81.PubMedCrossRef Castera L, Friedrich-Rust M, Loomba R. Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology. 2019;156:1264–81.PubMedCrossRef
21.
go back to reference Cai J, Zhang XJ, Li H. Progress and challenges in the prevention and control of nonalcoholic fatty liver disease. Med Res Rev. 2019;39:328–48.PubMedCrossRef Cai J, Zhang XJ, Li H. Progress and challenges in the prevention and control of nonalcoholic fatty liver disease. Med Res Rev. 2019;39:328–48.PubMedCrossRef
23.
go back to reference Masarone M, Rosato V, Dallio M, Gravina AG, Aglitti A, Loguercio C, Federico A, Persico M. Role of oxidative stress in pathophysiology of nonalcoholic fatty liver disease. Oxid Med Cell Longev. 2018;2018:9547613.PubMedPubMedCentralCrossRef Masarone M, Rosato V, Dallio M, Gravina AG, Aglitti A, Loguercio C, Federico A, Persico M. Role of oxidative stress in pathophysiology of nonalcoholic fatty liver disease. Oxid Med Cell Longev. 2018;2018:9547613.PubMedPubMedCentralCrossRef
24.
go back to reference Alkhouri N, Dixon LJ, Feldstein AE. Lipotoxicity in nonalcoholic fatty liver disease: not all lipids are created equal. Expert Rev Gastroenterol Hepatol. 2009;3:445–51.PubMedPubMedCentralCrossRef Alkhouri N, Dixon LJ, Feldstein AE. Lipotoxicity in nonalcoholic fatty liver disease: not all lipids are created equal. Expert Rev Gastroenterol Hepatol. 2009;3:445–51.PubMedPubMedCentralCrossRef
25.
go back to reference Aronis A, Madar Z, Tirosh O. Mechanism underlying oxidative stress-mediated lipotoxicity: exposure of J774.2 macrophages to triacylglycerols facilitates mitochondrial reactive oxygen species production and cellular necrosis. Free Radic Biol Med. 2005;38:1221–30.PubMedCrossRef Aronis A, Madar Z, Tirosh O. Mechanism underlying oxidative stress-mediated lipotoxicity: exposure of J774.2 macrophages to triacylglycerols facilitates mitochondrial reactive oxygen species production and cellular necrosis. Free Radic Biol Med. 2005;38:1221–30.PubMedCrossRef
26.
go back to reference Geering B, Stoeckle C, Conus S, Simon HU. Living and dying for inflammation: neutrophils, eosinophils, basophils. Trends Immunol. 2013;34:398–409.PubMedCrossRef Geering B, Stoeckle C, Conus S, Simon HU. Living and dying for inflammation: neutrophils, eosinophils, basophils. Trends Immunol. 2013;34:398–409.PubMedCrossRef
27.
go back to reference de Freitas CM, Lage NN, de Souza PA, Pereira RR, de Almeida LT, Da ST, de Brito MC, de Lima WG, Silva ME, Pedrosa ML, Da CGJ. Effects of açai on oxidative stress, ER stress, and inflammation-related parameters in mice with high fat diet-fed induced NAFLD. Sci Rep. 2019;9:8107.CrossRef de Freitas CM, Lage NN, de Souza PA, Pereira RR, de Almeida LT, Da ST, de Brito MC, de Lima WG, Silva ME, Pedrosa ML, Da CGJ. Effects of açai on oxidative stress, ER stress, and inflammation-related parameters in mice with high fat diet-fed induced NAFLD. Sci Rep. 2019;9:8107.CrossRef
28.
go back to reference Khan RS, Bril F, Cusi K, Newsome PN. Modulation of insulin resistance in nonalcoholic fatty liver disease. Hepatology. 2019;70:711–24.PubMed Khan RS, Bril F, Cusi K, Newsome PN. Modulation of insulin resistance in nonalcoholic fatty liver disease. Hepatology. 2019;70:711–24.PubMed
29.
go back to reference Guerrero-Romero F, Simental-Mendía LE, González-Ortiz M, Martínez-Abundis E, Ramos-Zavala MG, Hernández-González SO, Jacques-Camarena O, Rodríguez-Morán M. The product of triglycerides and glucose, a simple measure of insulin sensitivity. Comparison with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab. 2010;95:3347–51.PubMedCrossRef Guerrero-Romero F, Simental-Mendía LE, González-Ortiz M, Martínez-Abundis E, Ramos-Zavala MG, Hernández-González SO, Jacques-Camarena O, Rodríguez-Morán M. The product of triglycerides and glucose, a simple measure of insulin sensitivity. Comparison with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab. 2010;95:3347–51.PubMedCrossRef
30.
go back to reference Sánchez-García A, Rodríguez-Gutiérrez R, Mancillas-Adame L, González-Nava V, Díaz GA, Solis RC, Álvarez-Villalobos NA, González-González JG. Diagnostic accuracy of the triglyceride and glucose index for insulin resistance: a systematic review. Int J Endocrinol. 2020;2020:4678526.PubMedPubMedCentralCrossRef Sánchez-García A, Rodríguez-Gutiérrez R, Mancillas-Adame L, González-Nava V, Díaz GA, Solis RC, Álvarez-Villalobos NA, González-González JG. Diagnostic accuracy of the triglyceride and glucose index for insulin resistance: a systematic review. Int J Endocrinol. 2020;2020:4678526.PubMedPubMedCentralCrossRef
31.
go back to reference Dikaiakou E, Vlachopapadopoulou EA, Paschou SA, Athanasouli F, Panagiotopoulos I, Kafetzi M, Fotinou A, Michalacos S. Τriglycerides-glucose (TyG) index is a sensitive marker of insulin resistance in Greek children and adolescents. Endocrine. 2020;70:58–64.PubMedCrossRef Dikaiakou E, Vlachopapadopoulou EA, Paschou SA, Athanasouli F, Panagiotopoulos I, Kafetzi M, Fotinou A, Michalacos S. Τriglycerides-glucose (TyG) index is a sensitive marker of insulin resistance in Greek children and adolescents. Endocrine. 2020;70:58–64.PubMedCrossRef
32.
go back to reference Er LK, Wu S, Chou HH, Hsu LA, Teng MS, Sun YC, Ko YL. Triglyceride glucose-body mass index is a simple and clinically useful surrogate marker for insulin resistance in nondiabetic individuals. PLoS One. 2016;11:e149731.CrossRef Er LK, Wu S, Chou HH, Hsu LA, Teng MS, Sun YC, Ko YL. Triglyceride glucose-body mass index is a simple and clinically useful surrogate marker for insulin resistance in nondiabetic individuals. PLoS One. 2016;11:e149731.CrossRef
33.
go back to reference Li Y, Zheng R, Li J, Feng S, Wang L, Huang Z. Association between triglyceride glucose-body mass index and non-alcoholic fatty liver disease in the non-obese Chinese population with normal blood lipid levels: a secondary analysis based on a prospective cohort study. Lipids Health Dis. 2020;19:229.PubMedPubMedCentralCrossRef Li Y, Zheng R, Li J, Feng S, Wang L, Huang Z. Association between triglyceride glucose-body mass index and non-alcoholic fatty liver disease in the non-obese Chinese population with normal blood lipid levels: a secondary analysis based on a prospective cohort study. Lipids Health Dis. 2020;19:229.PubMedPubMedCentralCrossRef
34.
go back to reference Wang R, Dai L, Zhong Y, Xie G. Usefulness of the triglyceride glucose-body mass index in evaluating nonalcoholic fatty liver disease: insights from a general population. Lipids Health Dis. 2021;20:77.PubMedPubMedCentralCrossRef Wang R, Dai L, Zhong Y, Xie G. Usefulness of the triglyceride glucose-body mass index in evaluating nonalcoholic fatty liver disease: insights from a general population. Lipids Health Dis. 2021;20:77.PubMedPubMedCentralCrossRef
35.
go back to reference Zhang S, Du T, Li M, Jia J, Lu H, Lin X, Yu X. Triglyceride glucose-body mass index is effective in identifying nonalcoholic fatty liver disease in nonobese subjects. Medicine. 2017;96:e7041.PubMedPubMedCentralCrossRef Zhang S, Du T, Li M, Jia J, Lu H, Lin X, Yu X. Triglyceride glucose-body mass index is effective in identifying nonalcoholic fatty liver disease in nonobese subjects. Medicine. 2017;96:e7041.PubMedPubMedCentralCrossRef
36.
go back to reference Khamseh ME, Malek M, Abbasi R, Taheri H, Lahouti M, Alaei-Shahmiri F. 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 D. 2021;19:167–73.CrossRef Khamseh ME, Malek M, Abbasi R, Taheri H, Lahouti M, Alaei-Shahmiri F. 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 D. 2021;19:167–73.CrossRef
37.
go back to reference Okamura T, Hashimoto Y, Hamaguchi M, Obora A, Kojima T, Fukui M. Ectopic fat obesity presents the greatest risk for incident type 2 diabetes: a population-based longitudinal study. Int J Obesity. 2019;43:139–48.CrossRef Okamura T, Hashimoto Y, Hamaguchi M, Obora A, Kojima T, Fukui M. Ectopic fat obesity presents the greatest risk for incident type 2 diabetes: a population-based longitudinal study. Int J Obesity. 2019;43:139–48.CrossRef
39.
go back to reference Lee J, Ha J, Jo K, Lim DJ, Lee JM, Chang SA, Kang MI, Kim MH. High normal range of free thyroxine is associated with decreased triglycerides and with increased high-density lipoprotein cholesterol based on population representative data. J Clin Med. 2019;8:758.PubMedCentralCrossRef Lee J, Ha J, Jo K, Lim DJ, Lee JM, Chang SA, Kang MI, Kim MH. High normal range of free thyroxine is associated with decreased triglycerides and with increased high-density lipoprotein cholesterol based on population representative data. J Clin Med. 2019;8:758.PubMedCentralCrossRef
40.
go back to reference Bull FC, Al-Ansari SS, Biddle S, Borodulin K, Buman MP, Cardon G, Carty C, Chaput JP, Chastin S, Chou R, et al. World Health Organization 2020 guidelines on physical activity and sedentary behaviour. Br J Sports Med. 2020;54:1451–62.PubMedCrossRef Bull FC, Al-Ansari SS, Biddle S, Borodulin K, Buman MP, Cardon G, Carty C, Chaput JP, Chastin S, Chou R, et al. World Health Organization 2020 guidelines on physical activity and sedentary behaviour. Br J Sports Med. 2020;54:1451–62.PubMedCrossRef
41.
go back to reference Hamaguchi M, Kojima T, Itoh Y, Harano Y, Fujii K, Nakajima T, Kato T, Takeda N, Okuda J, Ida K, et al. The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol. 2007;102:2708–15.PubMedCrossRef Hamaguchi M, Kojima T, Itoh Y, Harano Y, Fujii K, Nakajima T, Kato T, Takeda N, Okuda J, Ida K, et al. The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol. 2007;102:2708–15.PubMedCrossRef
42.
go back to reference Nalls MA, McLean CY, Rick J, Eberly S, Hutten SJ, Gwinn K, Sutherland M, Martinez M, Heutink P, Williams NM, et al. Diagnosis of Parkinson’s disease on the basis of clinical and genetic classification: a population-based modelling study. Lancet Neurol. 2015;14:1002–9.PubMedPubMedCentralCrossRef Nalls MA, McLean CY, Rick J, Eberly S, Hutten SJ, Gwinn K, Sutherland M, Martinez M, Heutink P, Williams NM, et al. Diagnosis of Parkinson’s disease on the basis of clinical and genetic classification: a population-based modelling study. Lancet Neurol. 2015;14:1002–9.PubMedPubMedCentralCrossRef
43.
go back to reference Sun DQ, Wu SJ, Liu WY, Wang LR, Chen YR, Zhang DC, Braddock M, Shi KQ, Song D, Zheng MH. Association of low-density lipoprotein cholesterol within the normal range and NAFLD in the non-obese Chinese population: a cross-sectional and longitudinal study. BMJ Open. 2016;6:e13781. Sun DQ, Wu SJ, Liu WY, Wang LR, Chen YR, Zhang DC, Braddock M, Shi KQ, Song D, Zheng MH. Association of low-density lipoprotein cholesterol within the normal range and NAFLD in the non-obese Chinese population: a cross-sectional and longitudinal study. BMJ Open. 2016;6:e13781.
45.
go back to reference Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig L, Lijmer JG, Moher D, Rennie D, de Vet HC, et al. STARD 2015: an updated list of essential items for reporting diagnostic accuracy studies. BMJ. 2015;351:h5527.PubMedPubMedCentralCrossRef Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig L, Lijmer JG, Moher D, Rennie D, de Vet HC, et al. STARD 2015: an updated list of essential items for reporting diagnostic accuracy studies. BMJ. 2015;351:h5527.PubMedPubMedCentralCrossRef
46.
go back to reference Machado MV, Cortez-Pinto H. Non-invasive diagnosis of non-alcoholic fatty liver disease. A critical appraisal. J Hepatol. 2013;58:1007–19.PubMedCrossRef Machado MV, Cortez-Pinto H. Non-invasive diagnosis of non-alcoholic fatty liver disease. A critical appraisal. J Hepatol. 2013;58:1007–19.PubMedCrossRef
47.
go back to reference Bedogni G, Bellentani S, Miglioli L, Masutti F, Passalacqua M, Castiglione A, Tiribelli C. The Fatty Liver Index: a simple and accurate predictor of hepatic steatosis in the general population. Bmc Gastroenterol. 2006;6:33.PubMedPubMedCentralCrossRef Bedogni G, Bellentani S, Miglioli L, Masutti F, Passalacqua M, Castiglione A, Tiribelli C. The Fatty Liver Index: a simple and accurate predictor of hepatic steatosis in the general population. Bmc Gastroenterol. 2006;6:33.PubMedPubMedCentralCrossRef
48.
go back to reference Motamed N, Faraji AH, Khonsari MR, Maadi M, Tameshkel FS, Keyvani H, Ajdarkosh H, Karbalaie Niya MH, Rezaie N, Zamani F. Fatty liver index (FLI) and prediction of new cases of non-alcoholic fatty liver disease: a population-based study of northern Iran. Clin Nutr. 2020;39:468–74.PubMedCrossRef Motamed N, Faraji AH, Khonsari MR, Maadi M, Tameshkel FS, Keyvani H, Ajdarkosh H, Karbalaie Niya MH, Rezaie N, Zamani F. Fatty liver index (FLI) and prediction of new cases of non-alcoholic fatty liver disease: a population-based study of northern Iran. Clin Nutr. 2020;39:468–74.PubMedCrossRef
49.
go back to reference Lee J, Kim D, Kim HJ, Lee C, Yang JI, Kim W, Kim YJ, Yoon J, Cho S, Sung M, Lee H. Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Digest Liver Dis. 2010;42:503–8.CrossRef Lee J, Kim D, Kim HJ, Lee C, Yang JI, Kim W, Kim YJ, Yoon J, Cho S, Sung M, Lee H. Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Digest Liver Dis. 2010;42:503–8.CrossRef
50.
go back to reference Kahn HS. The “lipid accumulation product” performs better than the body mass index for recognizing cardiovascular risk: a population-based comparison. BMC Cardiovasc Disord. 2005;5:26.PubMedPubMedCentralCrossRef Kahn HS. The “lipid accumulation product” performs better than the body mass index for recognizing cardiovascular risk: a population-based comparison. BMC Cardiovasc Disord. 2005;5:26.PubMedPubMedCentralCrossRef
51.
go back to reference Amato MC, Giordano C, Galia M, Criscimanna A, Vitabile S, Midiri M, Galluzzo A. Visceral adiposity index: a reliable indicator of visceral fat function associated with cardiometabolic risk. Diabetes Care. 2010;33:920–2.PubMedPubMedCentralCrossRef Amato MC, Giordano C, Galia M, Criscimanna A, Vitabile S, Midiri M, Galluzzo A. Visceral adiposity index: a reliable indicator of visceral fat function associated with cardiometabolic risk. Diabetes Care. 2010;33:920–2.PubMedPubMedCentralCrossRef
52.
go back to reference Oyarzún JE, Andia ME, Uribe S, Núñez PP, Núñez G, Montenegro G, Bridi R. Honeybee pollen extracts reduce oxidative stress and steatosis in hepatic cells. Molecules. 2020;26:6.PubMedCentralCrossRef Oyarzún JE, Andia ME, Uribe S, Núñez PP, Núñez G, Montenegro G, Bridi R. Honeybee pollen extracts reduce oxidative stress and steatosis in hepatic cells. Molecules. 2020;26:6.PubMedCentralCrossRef
53.
54.
go back to reference Lin Y, Gong X, Li X, Shao C, Wu T, Li M, Li F, Ma Q, Ye J, Zhong B. Distinct cause of death profiles of hospitalized non-alcoholic fatty liver disease: a 10 years’ cross-sectional multicenter study in China. Front Med. 2020;7:584396.CrossRef Lin Y, Gong X, Li X, Shao C, Wu T, Li M, Li F, Ma Q, Ye J, Zhong B. Distinct cause of death profiles of hospitalized non-alcoholic fatty liver disease: a 10 years’ cross-sectional multicenter study in China. Front Med. 2020;7:584396.CrossRef
55.
56.
go back to reference Zou Y, Sheng G, Yu M, Xie G. The association between triglycerides and ectopic fat obesity: an inverted U-shaped curve. PLoS One. 2020;15:e243068. Zou Y, Sheng G, Yu M, Xie G. The association between triglycerides and ectopic fat obesity: an inverted U-shaped curve. PLoS One. 2020;15:e243068.
57.
58.
go back to reference Swainson MG, Batterham AM, Hind K. Age- and sex-specific reference intervals for visceral fat mass in adults. Int J Obes. 2020;44:289–96.CrossRef Swainson MG, Batterham AM, Hind K. Age- and sex-specific reference intervals for visceral fat mass in adults. Int J Obes. 2020;44:289–96.CrossRef
59.
go back to reference Kwon YM, Oh SW, Hwang SS, Lee C, Kwon H, Chung GE. Association of nonalcoholic fatty liver disease with components of metabolic syndrome according to body mass index in Korean adults. Am J Gastroenterol. 2012;107:1852–8.PubMedCrossRef Kwon YM, Oh SW, Hwang SS, Lee C, Kwon H, Chung GE. Association of nonalcoholic fatty liver disease with components of metabolic syndrome according to body mass index in Korean adults. Am J Gastroenterol. 2012;107:1852–8.PubMedCrossRef
60.
go back to reference Liu L, Hu Q, Wu H, Wang X, Gao C, Chen G, Yao P, Gong Z. Dietary DHA/EPA ratio changes fatty acid composition and attenuates diet-induced accumulation of lipid in the liver of ApoE (−/−) mice. Oxid Med Cell Longev. 2018;2018:6256802.PubMedPubMedCentral Liu L, Hu Q, Wu H, Wang X, Gao C, Chen G, Yao P, Gong Z. Dietary DHA/EPA ratio changes fatty acid composition and attenuates diet-induced accumulation of lipid in the liver of ApoE (−/−) mice. Oxid Med Cell Longev. 2018;2018:6256802.PubMedPubMedCentral
61.
go back to reference European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD), European Association for the Study of Obesity (EASO). EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016;64:1388–402. European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD), European Association for the Study of Obesity (EASO). EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016;64:1388–402.
62.
go back to reference Xia MF, Yan HM, He WY, Li XM, Li CL, Yao XZ, Li RK, Zeng MS, Gao X. Standardized ultrasound hepatic/renal ratio and hepatic attenuation rate to quantify liver fat content: an improvement method. Obesity. 2012;20:444–52.PubMedCrossRef Xia MF, Yan HM, He WY, Li XM, Li CL, Yao XZ, Li RK, Zeng MS, Gao X. Standardized ultrasound hepatic/renal ratio and hepatic attenuation rate to quantify liver fat content: an improvement method. Obesity. 2012;20:444–52.PubMedCrossRef
63.
go back to reference Xiao G, Zhu S, Xiao X, Yan L, Yang J, Wu G. Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology. 2017;66:1486–501.PubMedCrossRef Xiao G, Zhu S, Xiao X, Yan L, Yang J, Wu G. Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology. 2017;66:1486–501.PubMedCrossRef
64.
go back to reference Zhu J, He M, Zhang Y, Li T, Liu Y, Xu Z, Chen W. Validation of simple indexes for nonalcoholic fatty liver disease in western China: a retrospective cross-sectional study. Endocr J. 2018;65:373–81.PubMedCrossRef Zhu J, He M, Zhang Y, Li T, Liu Y, Xu Z, Chen W. Validation of simple indexes for nonalcoholic fatty liver disease in western China: a retrospective cross-sectional study. Endocr J. 2018;65:373–81.PubMedCrossRef
65.
go back to reference Zhang X, Wong GL, Wong VW. Application of transient elastography in nonalcoholic fatty liver disease. Clin Mol Hepatol. 2020;26:128–41.PubMedCrossRef Zhang X, Wong GL, Wong VW. Application of transient elastography in nonalcoholic fatty liver disease. Clin Mol Hepatol. 2020;26:128–41.PubMedCrossRef
66.
go back to reference de Lédinghen V, Wong GL, Vergniol J, Chan HL, Hiriart JB, Chan AW, Chermak F, Choi PC, Foucher J, Chan CK, et al. Controlled attenuation parameter for the diagnosis of steatosis in non-alcoholic fatty liver disease. J Gastroenterol Hepatol. 2016;31:848–55.PubMedCrossRef de Lédinghen V, Wong GL, Vergniol J, Chan HL, Hiriart JB, Chan AW, Chermak F, Choi PC, Foucher J, Chan CK, et al. Controlled attenuation parameter for the diagnosis of steatosis in non-alcoholic fatty liver disease. J Gastroenterol Hepatol. 2016;31:848–55.PubMedCrossRef
67.
go back to reference Liu SY, Wong VW, Wong SK, Wong GL, Lai CM, Lam CC, Shu SS, Chan HL, Ng EK. A prospective 5-year study on the use of transient elastography to monitor the improvement of non-alcoholic fatty liver disease following bariatric surgery. Sci Rep. 2021;11:5416.PubMedPubMedCentralCrossRef Liu SY, Wong VW, Wong SK, Wong GL, Lai CM, Lam CC, Shu SS, Chan HL, Ng EK. A prospective 5-year study on the use of transient elastography to monitor the improvement of non-alcoholic fatty liver disease following bariatric surgery. Sci Rep. 2021;11:5416.PubMedPubMedCentralCrossRef
68.
go back to reference Kwok R, Tse YK, Wong GL, Ha Y, Lee AU, Ngu MC, Chan HL, Wong VW. Systematic review with meta-analysis: non-invasive assessment of non-alcoholic fatty liver disease–the role of transient elastography and plasma cytokeratin-18 fragments. Aliment Pharmacol Ther. 2014;39:254–69.PubMedCrossRef Kwok R, Tse YK, Wong GL, Ha Y, Lee AU, Ngu MC, Chan HL, Wong VW. Systematic review with meta-analysis: non-invasive assessment of non-alcoholic fatty liver disease–the role of transient elastography and plasma cytokeratin-18 fragments. Aliment Pharmacol Ther. 2014;39:254–69.PubMedCrossRef
69.
go back to reference Reccia I, Kumar J, Akladios C, Virdis F, Pai M, Habib N, Spalding D. Non-alcoholic fatty liver disease: a sign of systemic disease. Metabolism. 2017;72:94–108.PubMedCrossRef Reccia I, Kumar J, Akladios C, Virdis F, Pai M, Habib N, Spalding D. Non-alcoholic fatty liver disease: a sign of systemic disease. Metabolism. 2017;72:94–108.PubMedCrossRef
72.
go back to reference Eftekhari A, Hasanzadeh A, Khalilov R, Hosainzadegan H, Ahmadian E, Eghbal MA. Hepatoprotective role of berberine against paraquat-induced liver toxicity in rat. Environ Sci Pollut Res Int. 2020;27:4969–75.PubMedCrossRef Eftekhari A, Hasanzadeh A, Khalilov R, Hosainzadegan H, Ahmadian E, Eghbal MA. Hepatoprotective role of berberine against paraquat-induced liver toxicity in rat. Environ Sci Pollut Res Int. 2020;27:4969–75.PubMedCrossRef
73.
go back to reference Biccirè FG, Bucci T, Menichelli D, Cammisotto V, Pignatelli P, Carnevale R, Pastori D. Mediterranean diet: a tool to break the relationship of atrial fibrillation with the metabolic syndrome and non-alcoholic fatty liver disease. Nutrients. 2022;14:1260.PubMedPubMedCentralCrossRef Biccirè FG, Bucci T, Menichelli D, Cammisotto V, Pignatelli P, Carnevale R, Pastori D. Mediterranean diet: a tool to break the relationship of atrial fibrillation with the metabolic syndrome and non-alcoholic fatty liver disease. Nutrients. 2022;14:1260.PubMedPubMedCentralCrossRef
74.
go back to reference Mandegary A, Saeedi A, Eftekhari A, Montazeri V, Sharif E. Hepatoprotective effect of silyamarin in individuals chronically exposed to hydrogen sulfide; modulating influence of TNF-α cytokine genetic polymorphism. Daru. 2013;21:28.PubMedPubMedCentralCrossRef Mandegary A, Saeedi A, Eftekhari A, Montazeri V, Sharif E. Hepatoprotective effect of silyamarin in individuals chronically exposed to hydrogen sulfide; modulating influence of TNF-α cytokine genetic polymorphism. Daru. 2013;21:28.PubMedPubMedCentralCrossRef
75.
go back to reference Watal G, Watal A, Rai PK, Rai DK, Sharma G, Sharma B. Biomedical applications of nano-antioxidant. Methods Mol Biol. 2013;1028:147–51.PubMedCrossRef Watal G, Watal A, Rai PK, Rai DK, Sharma G, Sharma B. Biomedical applications of nano-antioxidant. Methods Mol Biol. 2013;1028:147–51.PubMedCrossRef
76.
go back to reference Kim JH, Kwon SY, Lee SW, Lee CH. Validation of fatty liver index and lipid accumulation product for predicting fatty liver in Korean population. Liver Int. 2011;31:1600–1.PubMedCrossRef Kim JH, Kwon SY, Lee SW, Lee CH. Validation of fatty liver index and lipid accumulation product for predicting fatty liver in Korean population. Liver Int. 2011;31:1600–1.PubMedCrossRef
77.
go back to reference Huang X, Xu M, Chen Y, Peng K, Huang Y, Wang P, Ding L, Lin L, Xu Y, Chen Y, et al. Validation of the fatty liver index for nonalcoholic fatty liver disease in middle-aged and elderly Chinese. Medicine. 2015;94:e1682.PubMedPubMedCentralCrossRef Huang X, Xu M, Chen Y, Peng K, Huang Y, Wang P, Ding L, Lin L, Xu Y, Chen Y, et al. Validation of the fatty liver index for nonalcoholic fatty liver disease in middle-aged and elderly Chinese. Medicine. 2015;94:e1682.PubMedPubMedCentralCrossRef
78.
go back to reference Chen LW, Huang PR, Chien CH, Lin CL, Chien RN. A community-based study on the application of fatty liver index in screening subjects with nonalcoholic fatty liver disease. J Formos Med Assoc. 2020;119:173–81.PubMedCrossRef Chen LW, Huang PR, Chien CH, Lin CL, Chien RN. A community-based study on the application of fatty liver index in screening subjects with nonalcoholic fatty liver disease. J Formos Med Assoc. 2020;119:173–81.PubMedCrossRef
79.
go back to reference Jung TY, Kim MS, Hong HP, Kang KA, Jun DW. Comparative assessment and external validation of hepatic steatosis formulae in a community-based setting. J Clin Med. 2020;9:2851.PubMedCentralCrossRef Jung TY, Kim MS, Hong HP, Kang KA, Jun DW. Comparative assessment and external validation of hepatic steatosis formulae in a community-based setting. J Clin Med. 2020;9:2851.PubMedCentralCrossRef
Metadata
Title
The triglyceride glucose-body mass index: a non-invasive index that identifies non-alcoholic fatty liver disease in the general Japanese population
Authors
Haofei Hu
Yong Han
Changchun Cao
Yongcheng He
Publication date
01-12-2022
Publisher
BioMed Central
Keyword
Fatty Liver
Published in
Journal of Translational Medicine / Issue 1/2022
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-022-03611-4

Other articles of this Issue 1/2022

Journal of Translational Medicine 1/2022 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.