The triglycerides and glucose index is strongly associated with hepatic steatosis in children with overweight or obesity

Abstract

Given the worldwide increase prevalence of overweight, obesity, and nonalcoholic fatty liver disease (NAFLD), the objective of this study was to evaluate whether the triglycerides and glucose (TyG) index is associated with hepatic steatosis in children with overweight or obesity. Apparently healthy children aged 5‑17 years were included and allocated into the groups with and without hepatic steatosis. The TyG index was calculated as Ln [fasting triglycerides (mg/dL) × fasting glucose (mg/dL)]/2. Hepatic steatosis was diagnosed by ultrasonography. A total of 177 children, 66 (37.3%) girls and 111 (62.7%) boys, were included in the study. According to the hepatic ultrasonography, they were allocated into the groups with (n = 100) and without (n = 77) hepatic steatosis. The adjusted analysis by gender, body mass index, and waist circumference revealed that HDL-C (OR 0.96; 95% CI: 0.93–0.99), triglycerides (OR 1.005; 95% CI: 1.001–1.009), AST (OR 1.03; 95% CI: 1.008–1.07), ALT (OR 1.03; 95% CI: 1.01–1.05), and TyG index (OR 4.07; 95% CI: 1.26–13.15) remained associated with hepatic steatosis.

Conclusion: Compared to other biochemical markers, the TyG index is highly associated with the presence of fatty liver in children with overweight and obesity.

What is known:
• The triglycerides and glucose (TyG) index is effective in predicting high risk for incident nonalcoholic fatty liver disease (NAFLD) in adults.
What is new:
• Compared to other biochemical markers, the TyG index is highly associated with the presence of fatty liver in children with overweight or obesity.
• The triglycerides and glucose index may be a useful tool to detect children at high risk of fatty liver.
 

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Data availability

The database will not be shown because the participants did not authorize to this.

Abbreviations

NAFLD:

Nonalcoholic fatty liver disease

TyG:

Triglycerides and glucose

BMI:

Body mass index

AST:

Aspartate aminotransferase

ALT:

Alanine aminotransferase

References

  1. 1.

    Loomba R, Sirlin CB, Schwimmer JB, Lavine JE (2009) Advances in pediatric nonalcoholic fatty liver disease. Hepatology. 50(4):1282–1293. https://doi.org/10.1002/hep.23119

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Nobili V, Reale A, Alisi A, Morino G, Trenta I, Pisani M, Marcellini M, Raucci U (2009) Elevated serum ALT in children presenting to the emergency unit: relationship with NAFLD. Dig Liver Dis 41(10):749–752. https://doi.org/10.1016/j.dld.2009.02.048

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Anderson EL, Howe LD, Jones HE, Higgins JP, Lawlor DA (2015) Fraser A (2015) The prevalence of non-alcoholic fatty liver disease in children and adolescents: a systematic review and meta-analysis. PLoS One 10(10):e0140908. https://doi.org/10.1371/journal.pone.0140908

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M (2016) Global epidemiology of nonalcoholic fatty liver disease-meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 64(1):73–84. https://doi.org/10.1002/hep.28431

    Article  PubMed  Google Scholar 

  5. 5.

    Ozhan B, Ersoy B, Kiremitci S, Ozkol M, Taneli F (2015) Insulin sensitivity indices: fasting versus glucose-stimulated ındices in pediatric non-alcoholic fatty liver disease. Eur Rev Med Pharmacol Sci 19(18):3450–3458

    CAS  PubMed  Google Scholar 

  6. 6.

    Qayyum A, Nystrom M, Noworolski SM, Chu P, Mohanty A, Merriman R (2012) MRI steatosis grading: development and initial validation of a color mapping system. AJR Am J Roentgenol 198(3):582–588. https://doi.org/10.2214/AJR.11.6729

    Article  PubMed  Google Scholar 

  7. 7.

    Holterman A, Gurria J, Tanpure S, DiSomma N (2014) Nonalcoholic fatty liver disease and bariatric surgery in adolescents. Semin Pediatr Surg 23(1):49–57. https://doi.org/10.1053/j.sempedsurg.2013.10.016

    Article  PubMed  Google Scholar 

  8. 8.

    Alterio A, Alisi A, Liccardo D, Nobili V (2014) Non-alcoholic fatty liver and metabolic syndrome in children: a vicious circle. Horm Res Paediatr 82(5):283–289. https://doi.org/10.1159/000365192

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Simental-Mendía LE, Rodríguez-Morán M, Guerrero-Romero F (2008) The product of fasting glucose and triglycerides as surrogate for identifying insulin resistance in apparently healthy subjects. Metab Syndr Relat Disord 6(4):299–304. https://doi.org/10.1089/met.2008.0034

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Guerrero-Romero F, Simental-Mendía LE, González-Ortiz M et al (2010) The product of triglycerides and glucose, a simple measure of insulin sensitivity. Comparison with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab 95(7):3347–3351. https://doi.org/10.1210/jc.2010-0288

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Zhang S, Du T, Zhang J et al (2017) The triglyceride and glucose index (TyG) is an effective biomarker to identify nonalcoholic fatty liver disease. Lipids Health Dis 16(1):15. https://doi.org/10.1186/s12944-017-0409-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Zheng R, Du Z, Wang M, Mao Y, Mao W (2018) A longitudinal epidemiological study on the triglyceride and glucose index and the incident nonalcoholic fatty liver disease. Lipids Health Dis 17(1):262. https://doi.org/10.1186/s12944-018-0913-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Lee SB, Kim MK, Kang S, Park K, Kim JH, Baik SJ, Nam JS, Ahn CW, Park JS (2019) Triglyceride glucose index is superior to the homeostasis model assessment of insulin resistance for predicting nonalcoholic fatty liver disease in Korean adults. Endocrinol Metab (Seoul) 34(2):179–186. https://doi.org/10.3803/EnM.2019.34.2.179

    Article  Google Scholar 

  14. 14.

    Nakao K, Nakata K, Ohtsubo N, Maeda M, Moriuchi T, Ichikawa T, Hamasaki K, Kato Y, Eguchi K, Yukawa K, Ishii N (2002) Association between nonalcoholic fatty liver, markers of obesity, and serum leptin level in young adults. Am J Gastroenterol 97(7):1796–1801. https://doi.org/10.1111/j.1572-0241.2002.05846.x

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Hamaguchi M, Kojima T, Itoh Y, Harano Y, Fujii K, Nakajima T, Kato T, Takeda N, Okuda J, Ida K, Kawahito Y, Yoshikawa T, Okanoue T (2007) The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol 102(12):2708–2715. https://doi.org/10.1111/j.1572-0241.2007.01526.x

    Article  PubMed  Google Scholar 

  16. 16.

    Ogden CL, Kuczmarski RJ, Flegal KM, Mei Z, Guo S, Wei R, Grummer-Strawn LM, Curtin LR, Roche AF, Johnson CL (2002) Centers for Disease Control and Prevention 2000 growth charts for the United States: improvements to the 1977 National Center for Health Statistics version. Pediatrics. 109(1):45–60. https://doi.org/10.1542/peds.109.1.45

    Article  PubMed  Google Scholar 

  17. 17.

    Simental-Mendía LE, Hernández-Ronquillo G, Gómez-Díaz R, Rodríguez-Morán M, Guerrero-Romero F (2017) The triglycerides and glucose index is associated with cardiovascular risk factors in normal-weight children and adolescents. Pediatr Res 82(6):920–925. https://doi.org/10.1038/pr.2017.187

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr, Jones DW, Materson BJ, Oparil S, Wright JT Jr, Roccella EJ, Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. National Heart, Lung, and Blood Institute, National High Blood Pressure Education Program Coordinating Committee (2003) Seventh report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Hypertension. 42(6):1206–1252. https://doi.org/10.1161/01.HYP.0000107251.49515.c2

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Petta S, Di Marco V, Di Stefano R et al (2011) TyG index, HOMA score and viral load in patients with chronic hepatitis C due to genotype 1. J Viral Hepat 18(7):e372–e380. https://doi.org/10.1111/j.1365-2893.2011.01439.x

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Unger G, Benozzi SF, Perruzza F, Pennacchiotti GL (2014) Triglycerides and glucose index: a useful indicator of insulin resistance. Endocrinol Nutr 61(10):533–540. https://doi.org/10.1016/j.endonu.2014.06.009

    Article  PubMed  Google Scholar 

  21. 21.

    Brahimaj A, Rivadeneira F, Muka T, Sijbrands EJG, Franco OH, Dehghan A, Kavousi M (2019) Novel metabolic indices and incident type 2 diabetes among women and men: the Rotterdam Study. Diabetologia. 62(9):1581–1590. https://doi.org/10.1007/s00125-019-4921-2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Du T, Yuan G, Zhang M, Zhou X, Sun X, Yu X (2014) Clinical usefulness of lipid ratios, visceral adiposity indicators, and the triglycerides and glucose index as risk markers of insulin resistance. Cardiovasc Diabetol 13:146. https://doi.org/10.1186/s12933-014-0146-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Khan SH, Sobia F, Niazi NK, Manzoor SM, Fazal N, Ahmad F (2018) Metabolic clustering of risk factors: evaluation of triglyceride-glucose index (TyG index) for evaluation of insulin resistance. Diabetol Metab Syndr 10:74. https://doi.org/10.1186/s13098-018-0376-8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Buzzetti E, Pinzani M, Tsochatzis EA (2016) The multiple-hit pathogenesis of non-alcoholic fatty liver disease (NAFLD). Metabolism. 65(8):1038–1048. https://doi.org/10.1016/j.metabol.2015.12.012

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Gastaldelli A, Folli F, DeFronzo RA (2010) The product of triglycerides and glucose as index of insulin resistance. Validation in the SAM study. J Clin Endocrinol Metab 95:3351

    Google Scholar 

  26. 26.

    Bugianesi E, Moscatiello S, Ciaravella MF, Marchesini G (2010) Insulin resistance in nonalcoholic fatty liver disease. Curr Pharm Des 16(17):1941–1951. https://doi.org/10.2174/138161210791208875

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Guilherme A, Virbasius JV, Puri V, Czech MP (2008) Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 9(5):367–377. https://doi.org/10.1038/nrm2391

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Hotamisligil GS (2005) Role of endoplasmic reticulum stress and c-Jun NH2-terminal kinase pathways in inflammation and origin of obesity and diabetes. Diabetes. 54(Suppl 2):S73–S78. https://doi.org/10.2337/diabetes.54.suppl_2.s73

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Shoelson SE, Lee J, Goldfine AB (2006) Inflammation and insulin resistance published correction appears in. J Clin Invest 116(7):1793–1801. https://doi.org/10.1172/JCI29069

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Cusi K (2009) Role of insulin resistance and lipotoxicity in non-alcoholic steatohepatitis. Clin Liver Dis 13(4):545–563. https://doi.org/10.1016/j.cld.2009.07.009

    Article  PubMed  Google Scholar 

  31. 31.

    Manco M, Alisi A, Nobili V (2008) Risk of severe liver disease in NAFLD with normal ALT levels: a pediatric report. Hepatology. 48(6):2087–2088. https://doi.org/10.1002/hep.22631

    Article  PubMed  Google Scholar 

  32. 32.

    Schwimmer JB, Pardee PE, Lavine JE, Blumkin AK, Cook S (2008) Cardiovascular risk factors and the metabolic syndrome in pediatric nonalcoholic fatty liver disease. Circulation. 118(3):277–283. https://doi.org/10.1161/CIRCULATIONAHA.107.739920

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Kim JY, Cho J, Yang HR (2018) Biochemical predictors of early onset non-alcoholic fatty liver disease in young children with obesity. J Korean Med Sci 33(16):e122. https://doi.org/10.3346/jkms.2018.33.e122

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Peña-Espinoza BI, Granados-Silvestre MLÁ, Sánchez-Pozos K, Ortiz-López MG, Menjivar M (2017) Metabolic syndrome in Mexican children: low effectiveness of diagnostic definitions. Endocrinol Diabetes Nutr 64(7):369–376. https://doi.org/10.1016/j.endinu.2017.04.004

    Article  PubMed  Google Scholar 

  35. 35.

    Angulo P (2002) Nonalcoholic fatty liver disease. N Engl J Med 346(16):1221–1231. https://doi.org/10.1056/NEJMra011775

    CAS  Article  Google Scholar 

  36. 36.

    Rodríguez-Morán M, Simental-Mendía LE, Guerrero-Romero F (2017) The triglyceride and glucose index is useful for recognising insulin resistance in children. Acta Paediatr 106(6):979–983. https://doi.org/10.1111/apa.13789

    CAS  Article  PubMed  Google Scholar 

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Funding

This work was supported by the Consejo de Ciencia y Tecnología del Estado de Durango (grant number: FIS/IMSS/PROT/1761 and FIS/IMSS/PROT/1762) and Instituto Mexicano del Seguro Social (grant number: FIS/IMSS/PROT/G17-21727).

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Luis E. Simental-Mendía conceptualized and designed the study, drafted the initial manuscript, and approved the final version as submitted. César Javier Ortega-Pacheco contributed to conception, critically reviewed the manuscript, and approved the final version as submitted. Elvira García-Guerrero contributed to conception, critically reviewed the manuscript, and approved the final version as submitted. María Alejandra Sicsik-Aragón contributed to conception, critically reviewed the manuscript, and approved the final version as submitted. Fernando Guerrero-Romero contributed to conception, critically reviewed the manuscript, and approved the final version as submitted. Gerardo Martínez-Aguilar contributed to conception and study design, drafted the manuscript, critically revised the manuscript, and gave final approval.

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Correspondence to Gerardo Martínez-Aguilar.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments. Written informed consent was obtained from the parents.

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Simental-Mendía, L.E., Ortega-Pacheco, C.J., García-Guerrero, E. et al. The triglycerides and glucose index is strongly associated with hepatic steatosis in children with overweight or obesity. Eur J Pediatr (2021). https://doi.org/10.1007/s00431-021-03951-1

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Keywords

  • TyG index
  • Triglycerides
  • Glucose
  • Hepatic steatosis
  • Children