The ZJU index is a powerful surrogate marker for NAFLD in severely obese North American women

Autoři: Chia-Po Fu aff001;  Hira Ali aff004;  Vikrant P. Rachakonda aff005;  Elizabeth A. Oczypok aff004;  James P. DeLany aff006;  Erin E. Kershaw aff004
Působiště autorů: Division of Endocrinology and Metabolism, Department of Medicine, Taichung Veterans General Hospital, Taichung, Taiwan aff001;  Department of Medicine, Chung Shan Medical University, Taichung, Taiwan aff002;  Graduate Institute of Biomedical Electronics and Bioinformatics, College of Electrical Engineering and Computer Science, National Taiwan University, Taipei, Taiwan aff003;  Division of Endocrinology and Metabolism, Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America aff004;  Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America aff005;  Translational Research Institute for Metabolism and Diabetes, Florida Hospital, Orlando, Florida, United States of America aff006
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224942



Non-alcoholic fatty liver disease (NAFLD) is the most common chronic liver disease in the western world and is highly associated with multiple cardiometabolic complications. The Zhejiang University (ZJU) index was first developed to predict NAFLD in Chinese populations, where it was shown to have better predictive value than other currently used indices. The aims of the present study were to 1) determine the diagnostic accuracy of ZJU index in identifying NAFLD in a well-phenotyped cohort of obese middle-aged American women and 2) compare its performance with other non-invasive indices for NAFLD identification.


To achieve this goal, we performed a retrospective analysis of a prospectively-collected cohort of participants enrolled in a weight loss trial for severe obesity (RENEW, identifier: NCT00712127). One hundred and seven women between the age of 30 and 55 with obesity class II (BMI 35–39.9 kg/m2) or class III (BMI ≥ 40 kg/m2) were recruited for analyses. Hepatic steatosis was measured using liver/spleen attenuation ratio (L/S ratio) from unenhanced abdominal computed tomography. Beside ZJU index, hepatic steatosis index (HSI), lipid accumulation production index (LAPI), and visceral adiposity index (VAI) were also determined and to compare their performance in predicting NAFLD.


Of 107 obese women in the study, 40 (37.4%) met imaging criteria for NAFLD using cut-off value of L/S ratio < 1.1. The ZJU index was positively correlated with HIS, LAPI, but not VAI. The area under the curve was highest for the ZJU index (AUC = 0.742, 95% CI:0.647–0.837), followed by HSI (AUC = 0.728, 95% CI:0.631–0.825), LAPI (AUC = 0.682, CI:0.583–0.781), and VAI (AUC = 0.621, 95% CI:0.518–0.725), respectively, using the Youden method.


The ZJU index is a powerful surrogate marker for NAFLD in severely obese western females and its predictive value was better than that of other commonly used indices for predicting NAFLD. Our study is the first to suggest that the ZJU index could be a promising model for use in western as well as Chinese populations.

Klíčová slova:

Adipose tissue – Biopsy – Body Mass Index – Computed axial tomography – Fatty liver – Lipids – Obesity – Steatosis


1. McCullough AJ. The clinical features, diagnosis and natural history of nonalcoholic fatty liver disease. Clin Liver Dis. 2004;8(3):521–33, viii. doi: 10.1016/j.cld.2004.04.004 15331061

2. Rinella ME. Nonalcoholic fatty liver disease: a systematic review. JAMA. 2015;313(22):2263–73. doi: 10.1001/jama.2015.5370 26057287

3. Sattar N, Forrest E, Preiss D. Non-alcoholic fatty liver disease. BMJ. 2014;349:g4596. doi: 10.1136/bmj.g4596 25239614

4. 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(3):274–85. doi: 10.1111/j.1365-2036.2011.04724.x 21623852

5. Targher G, Byrne CD, Lonardo A, Zoppini G, Barbui C. Non-alcoholic fatty liver disease and risk of incident cardiovascular disease: A meta-analysis. J Hepatol. 2016;65(3):589–600. doi: 10.1016/j.jhep.2016.05.013 27212244

6. Ekstedt M, Hagstrom H, Nasr P, Fredrikson M, Stal P, Kechagias S, et al. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up. Hepatology. 2015;61(5):1547–54. doi: 10.1002/hep.27368 25125077

7. Targher G, Day CP, Bonora E. Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med. 2010;363(14):1341–50. doi: 10.1056/NEJMra0912063 20879883

8. Siddiqui MS, Fuchs M, Idowu MO, Luketic VA, Boyett S, Sargeant C, et al. Severity of nonalcoholic fatty liver disease and progression to cirrhosis are associated with atherogenic lipoprotein profile. Clin Gastroenterol Hepatol. 2015;13(5):1000–8 e3.

9. Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, et al. 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(6):2005–23. doi: 10.1002/hep.25762 22488764

10. Angulo P, Hui JM, Marchesini G, Bugianesi E, George J, Farrell GC, et al. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology. 2007;45(4):846–54. doi: 10.1002/hep.21496 17393509

11. Poynard T, Ratziu V, Naveau S, Thabut D, Charlotte F, Messous D, et al. The diagnostic value of biomarkers (SteatoTest) for the prediction of liver steatosis. Comp Hepatol. 2005;4:10. doi: 10.1186/1476-5926-4-10 16375767

12. Bedogni G, Bellentani S, Miglioli L, Masutti F, Passalacqua M, Castiglione A, et al. The Fatty Liver Index: a simple and accurate predictor of hepatic steatosis in the general population. BMC Gastroenterol. 2006;6:33. doi: 10.1186/1471-230X-6-33 17081293

13. Bedogni G, Kahn HS, Bellentani S, Tiribelli C. A simple index of lipid overaccumulation is a good marker of liver steatosis. BMC Gastroenterol. 2010;10:98. doi: 10.1186/1471-230X-10-98 20738844

14. Lee JH, Kim D, Kim HJ, Lee CH, Yang JI, Kim W, et al. Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Dig Liver Dis. 2010;42(7):503–8. doi: 10.1016/j.dld.2009.08.002 19766548

15. Amato MC, Giordano C, Galia M, Criscimanna A, Vitabile S, Midiri M, et al. Visceral Adiposity Index: a reliable indicator of visceral fat function associated with cardiometabolic risk. Diabetes Care. 2010;33(4):920–2. doi: 10.2337/dc09-1825 20067971

16. Wang J, Xu C, Xun Y, Lu Z, Shi J, Yu C, et al. ZJU index: a novel model for predicting nonalcoholic fatty liver disease in a Chinese population. Sci Rep. 2015;5:16494. doi: 10.1038/srep16494 26568423

17. Li L, You W, Ren W. The ZJU index is a powerful index for identifying NAFLD in the general Chinese population. Acta Diabetol. 2017;54(10):905–11. doi: 10.1007/s00592-017-1024-8 28698957

18. Goodpaster BH, Delany JP, Otto AD, Kuller L, Vockley J, South-Paul JE, et al. Effects of diet and physical activity interventions on weight loss and cardiometabolic risk factors in severely obese adults: a randomized trial. JAMA. 2010;304(16):1795–802. doi: 10.1001/jama.2010.1505 20935337

19. Rachakonda V, Wills R, DeLany JP, Kershaw EE, Behari J. Differential Impact of Weight Loss on Nonalcoholic Fatty Liver Resolution in a North American Cohort with Obesity. Obesity (Silver Spring). 2017;25(8):1360–8.

20. Rachakonda VP, Reeves VL, Aljammal J, Wills RC, Trybula JS, DeLany JP, et al. Serum autotaxin is independently associated with hepatic steatosis in women with severe obesity. Obesity (Silver Spring). 2015;23(5):965–72.

21. Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005;112(17):2735–52. doi: 10.1161/CIRCULATIONAHA.105.169404 16157765

22. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9. doi: 10.1007/bf00280883 3899825

23. Goodpaster BH, Kelley DE, Wing RR, Meier A, Thaete FL. Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes. 1999;48(4):839–47. doi: 10.2337/diabetes.48.4.839 10102702

24. Park SH, Kim PN, Kim KW, Lee SW, Yoon SE, Park SW, et al. Macrovesicular hepatic steatosis in living liver donors: use of CT for quantitative and qualitative assessment. Radiology. 2006;239(1):105–12. doi: 10.1148/radiol.2391050361 16484355

25. Machado MV, Cortez-Pinto H. Non-invasive diagnosis of non-alcoholic fatty liver disease. A critical appraisal. J Hepatol. 2013;58(5):1007–19. doi: 10.1016/j.jhep.2012.11.021 23183525

26. Kelley DE, McKolanis TM, Hegazi RA, Kuller LH, Kalhan SC. Fatty liver in type 2 diabetes mellitus: relation to regional adiposity, fatty acids, and insulin resistance. Am J Physiol Endocrinol Metab. 2003;285(4):E906–16. doi: 10.1152/ajpendo.00117.2003 12959938

27. Goodpaster BH, Thaete FL, Kelley DE. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr. 2000;71(4):885–92. doi: 10.1093/ajcn/71.4.885 10731493

28. Rocha PM, Barata JT, Minderico CS, Silva AM, Teixeira PJ, Sardinha LB. Visceral abdominal and subfascial femoral adipose tissue have opposite associations with liver fat in overweight and obese premenopausal caucasian women. J Lipids. 2011;2011:154672. doi: 10.1155/2011/154672 21961071

Článek vyšel v časopise


2019 Číslo 11