High Prevalence of Nonalcoholic Fatty Liver Disease in Patients With Type 2 Diabetes Mellitus and Normal Plasma Aminotransferase Levels - PubMed
High Prevalence of Nonalcoholic Fatty Liver Disease in Patients With Type 2 Diabetes Mellitus and Normal Plasma Aminotransferase Levels
Paola Portillo-Sanchez et al. J Clin Endocrinol Metab. 2015 Jun.
Abstract
Context and objective: Nonalcoholic fatty liver disease (NAFLD) and its more severe form with steatohepatitis (NASH) are common in patients with type 2 diabetes mellitus (T2DM). However, they are usually believed to largely affect those with elevated aminotransferases. The aim of this study was to determine the prevalence of NAFLD by the gold standard, liver magnetic resonance spectroscopy ((1)H-MRS) in patients with T2DM and normal aminotransferases, and to characterize their metabolic profile.
Participants and methods: We recruited 103 patients with T2DM and normal plasma aminotransferases (age, 60 ± 8 y; body mass index [BMI], 33 ± 5 kg/m(2); glycated hemoglobin [A1c], 7.6 ± 1.3%). We measured the following: 1) liver triglyceride content by (1)H-MRS; 2) systemic insulin sensitivity (homeostasis model assessment-insulin resistance); and 3) adipose tissue insulin resistance, both fasting (as the adipose tissue insulin resistance index: fasting plasma free fatty acids [FFA] × insulin) and during an oral glucose tolerance test (as the suppression of FFA).
Results: The prevalence of NAFLD and NASH were much higher than expected (50% and 56% of NAFLD patients, respectively). The prevalence of NAFLD was higher in obese compared with nonobese patients as well as with increasing BMI (P = .001 for trend). Higher plasma A1c was associated with a greater prevalence of NAFLD and worse liver triglyceride accumulation (P = .01). Compared with nonobese patients without NAFLD, patients with NAFLD had severe systemic (liver/muscle) and, particularly, adipose tissue (fasting/postprandial) insulin resistance (all P < .01).
Conclusions: The prevalence of NAFLD is much higher than previously believed in overweight/obese patients with T2DM and normal aminotransferases. Moreover, many are at increased risk of NASH. Physicians should have a lower threshold for screening patients with T2DM for NAFLD/NASH.
Figures

Relationship between BMI and liver triglyceride content measured by 1H-MRS. A, Correlation between BMI and liver triglyceride content. B, Prevalence of NAFLD according to different BMI groups (n = 31, 34, 29, and 9, respectively).

The role of obesity and NAFLD on adipose tissue insulin sensitivity. A, Adipo-IRindex (Adipo-IRindex = fasting plasma FFA × fasting plasma insulin concentration). B, Percentage suppression of plasma FFA concentration after an OGTT. Patients with NAFLD had worse adipose tissue insulin resistance when compared with those without NAFLD (No-NAFLD). Results are expressed as the mean ± SEM. P-value represents P for trend (n = 7, 10, 16, and 49, respectively).

Relationship between glycemic control on liver triglyceride content measured by 1H-MRS. A, Correlation between plasma A1c levels and liver triglyceride content. B, Prevalence of NAFLD among patients with a broad spectrum of plasma A1c levels (n = 15, 19, 54, and 15, respectively).
Similar articles
-
Portillo Sanchez P, Bril F, Maximos M, Lomonaco R, Biernacki D, Orsak B, Subbarayan S, Webb A, Hecht J, Cusi K. Portillo Sanchez P, et al. J Clin Endocrinol Metab. 2014 Oct 10;100(5). doi: 10.1210/jc.2014-2739. Epub 2014 Oct 10. J Clin Endocrinol Metab. 2014. PMID: 25303488 Retracted.
-
Metabolic Impact of Nonalcoholic Steatohepatitis in Obese Patients With Type 2 Diabetes.
Lomonaco R, Bril F, Portillo-Sanchez P, Ortiz-Lopez C, Orsak B, Biernacki D, Lo M, Suman A, Weber MH, Cusi K. Lomonaco R, et al. Diabetes Care. 2016 Apr;39(4):632-8. doi: 10.2337/dc15-1876. Epub 2016 Feb 9. Diabetes Care. 2016. PMID: 26861926 Free PMC article.
-
Ortiz-Lopez C, Lomonaco R, Orsak B, Finch J, Chang Z, Kochunov VG, Hardies J, Cusi K. Ortiz-Lopez C, et al. Diabetes Care. 2012 Apr;35(4):873-8. doi: 10.2337/dc11-1849. Epub 2012 Feb 28. Diabetes Care. 2012. PMID: 22374640 Free PMC article.
-
Nonalcoholic Fatty Liver Disease: The New Complication of Type 2 Diabetes Mellitus.
Bril F, Cusi K. Bril F, et al. Endocrinol Metab Clin North Am. 2016 Dec;45(4):765-781. doi: 10.1016/j.ecl.2016.06.005. Epub 2016 Oct 4. Endocrinol Metab Clin North Am. 2016. PMID: 27823604 Review.
-
Non-alcoholic fatty liver disease and type 2 diabetes mellitus: the liver disease of our age?
Firneisz G. Firneisz G. World J Gastroenterol. 2014 Jul 21;20(27):9072-89. doi: 10.3748/wjg.v20.i27.9072. World J Gastroenterol. 2014. PMID: 25083080 Free PMC article. Review.
Cited by
-
Taheri H, Malek M, Ismail-Beigi F, Zamani F, Sohrabi M, Reza Babaei M, Khamseh ME. Taheri H, et al. Adv Ther. 2020 Nov;37(11):4697-4708. doi: 10.1007/s12325-020-01498-5. Epub 2020 Sep 25. Adv Ther. 2020. PMID: 32975679 Free PMC article. Clinical Trial.
-
Deb R, Goswami S, Sengupta N, Baidya A, Khare VR, Datta J, Jhaveri K, Das M, Ray D. Deb R, et al. Indian J Endocrinol Metab. 2024 Jul-Aug;28(4):385-390. doi: 10.4103/ijem.ijem_203_23. Epub 2024 Jun 6. Indian J Endocrinol Metab. 2024. PMID: 39371654 Free PMC article.
-
Liu X, Xu H, Zhan M, Niu J. Liu X, et al. Med Sci Monit. 2019 Aug 17;25:6174-6180. doi: 10.12659/MSM.916107. Med Sci Monit. 2019. PMID: 31420961 Free PMC article.
-
Non-alcoholic Steatohepatitis: From Pathophysiology to Clinical Practice.
Schwartz S, Lucas J, DeLegge MH. Schwartz S, et al. touchREV Endocrinol. 2021 Nov;17(2):112-120. doi: 10.17925/EE.2021.17.2.112. Epub 2021 Sep 14. touchREV Endocrinol. 2021. PMID: 35118457 Free PMC article. Review.
-
Zhang M, Hu ML, Huang JJ, Xia SS, Yang Y, Dong K. Zhang M, et al. Chin Med J (Engl). 2019 Dec 20;132(24):2927-2933. doi: 10.1097/CM9.0000000000000559. Chin Med J (Engl). 2019. PMID: 31809318 Free PMC article.
References
-
- Loomba R, Sanyal AJ. The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol. 2013;10:686–690. - PubMed
-
- Mishra P, Younossi ZM. Abdominal ultrasound for diagnosis of nonalcoholic fatty liver disease (NAFLD). Am J Gastroenterol. 2007;102:2716–2717. - PubMed
-
- Williams CD, Stengel J, Asike MI, et al. . Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: A prospective study. Gastroenterology. 2011;140:124–131. - PubMed
-
- Szczepaniak LS, Nurenberg P, Leonard D, et al. . Magnetic resonance spectroscopy to measure hepatic triglyceride content: Prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab. 2005;288:E462–E468. - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical