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Comparison of Computed Tomography-based Abdominal Adiposity Indexes as Predictors of Non-alcoholic Fatty Liver Disease Among Middle-aged Korean Men and Women

  • Baek, Jongmin (Department of Preventive Medicine, Yonsei University College of Medicine) ;
  • Jung, Sun Jae (Department of Preventive Medicine, Yonsei University College of Medicine) ;
  • Shim, Jee-Seon (Department of Preventive Medicine, Yonsei University College of Medicine) ;
  • Jeon, Yong Woo (Department of Preventive Medicine, Yonsei University College of Medicine) ;
  • Seo, Eunsun (Department of Preventive Medicine, Yonsei University College of Medicine) ;
  • Kim, Hyeon Chang (Department of Preventive Medicine, Yonsei University College of Medicine)
  • Received : 2020.04.17
  • Accepted : 2020.05.14
  • Published : 2020.07.31

Abstract

Objectives: We compared the associations of 3 computed tomography (CT)-based abdominal adiposity indexes with non-alcoholic fatty liver disease (NAFLD) among middle-aged Korean men and women. Methods: The participants were 1366 men and 2480 women community-dwellers aged 30-64 years. Three abdominal adiposity indexes-visceral fat area (VFA), subcutaneous fat area (SFA), and visceral-to-subcutaneous fat ratio (VSR)-were calculated from abdominal CT scans. NAFLD was determined by calculating the Liver Fat Score from comorbidities and blood tests. An NAFLD prediction model that included waist circumference (WC) as a measure of abdominal adiposity was designated as the base model, to which VFA, SFA, and VSR were added in turn. The area under the receiver operating characteristic curve (AUC), integrated discrimination improvement (IDI), and net reclassification improvement (NRI) were calculated to quantify the additional predictive value of VFA, SFA, and VSR relative to WC. Results: VFA and VSR were positively associated with NAFLD in both genders. SFA was not significantly associated with NAFLD in men, but it was negatively associated in women. When VFA, SFA, and VSR were added to the WC-based NAFLD prediction model, the AUC improved by 0.013 (p<0.001), 0.001 (p=0.434), and 0.009 (p=0.007) in men and by 0.044 (p<0.001), 0.017 (p<0.001), and 0.046 (p<0.001) in women, respectively. The IDI and NRI were increased the most by VFA in men and VSR in women. Conclusions: Using CT-based abdominal adiposity indexes in addition to WC may improve the detection of NAFLD. The best predictive indicators were VFA in men and VSR in women.

Keywords

References

  1. Stepanova M, Rafiq N, Makhlouf H, Agrawal R, Kaur I, Younoszai Z, et al. Predictors of all-cause mortality and liver-related mortality in patients with non-alcoholic fatty liver disease (NAFLD). Dig Dis Sci 2013;58(10):3017-3023. https://doi.org/10.1007/s10620-013-2743-5
  2. Paik JM, Henry L, De Avila L, Younossi E, Racila A, Younossi ZM. Mortality related to nonalcoholic fatty liver disease is increasing in the United States. Hepatol Commun 2019;3(11):1459-1471. https://doi.org/10.1002/hep4.1419
  3. Jakobsen MU, Berentzen T, Sorensen TI, Overvad K. Abdominal obesity and fatty liver. Epidemiol Rev 2007;29(1):77-87. https://doi.org/10.1093/epirev/mxm002
  4. Kim D, Chung GE, Kwak MS, Seo HB, Kang JH, Kim W, et al. Body fat distribution and risk of incident and regressed nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2016;14(1):132-138. https://doi.org/10.1016/j.cgh.2015.07.024
  5. Radmard AR, Rahmanian MS, Abrishami A, Yoonessi A, Kooraki S, Dadgostar M, et al. Assessment of abdominal fat distribution in non-alcoholic fatty liver disease by magnetic resonance imaging: a population-based study. Arch Iran Med 2016;19(10): 693-699.
  6. Despres JP. Body fat distribution and risk of cardiovascular disease: an update. Circulation 2012;126(10):1301-1313. https://doi.org/10.1161/CIRCULATIONAHA.111.067264
  7. Fukuda T, Bouchi R, Takeuchi T, Nakano Y, Murakami M, Minami I, et al. Ratio of visceral-to-subcutaneous fat area predicts cardiovascular events in patients with type 2 diabetes. J Diabetes Investig 2018;9(2):396-402. https://doi.org/10.1111/jdi.12713
  8. Kaess BM, Pedley A, Massaro JM, Murabito J, Hoffmann U, Fox CS. The ratio of visceral to subcutaneous fat, a metric of body fat distribution, is a unique correlate of cardiometabolic risk. Diabetologia 2012;55(10):2622-2630. https://doi.org/10.1007/s00125-012-2639-5
  9. Piche ME, Poirier P, Lemieux I, Despres JP. Overview of epidemiology and contribution of obesity and body fat distribution to cardiovascular disease: an update. Prog Cardiovasc Dis 2018; 61(2):103-113. https://doi.org/10.1016/j.pcad.2018.06.004
  10. Eguchi Y, Eguchi T, Mizuta T, Ide Y, Yasutake T, Iwakiri R, et al. Visceral fat accumulation and insulin resistance are important factors in nonalcoholic fatty liver disease. J Gastroenterol 2006; 41(5):462-469. https://doi.org/10.1007/s00535-006-1790-5
  11. Holt HB, Wild SH, Wood PJ, Zhang J, Darekar AA, Dewbury K, et al. Non-esterified fatty acid concentrations are independently associated with hepatic steatosis in obese subjects. Diabetologia 2006;49(1):141-148. https://doi.org/10.1007/s00125-005-0070-x
  12. Thomas EL, Hamilton G, Patel N, O'Dwyer R, Dore CJ, Goldin RD, et al. Hepatic triglyceride content and its relation to body adiposity: a magnetic resonance imaging and proton magnetic resonance spectroscopy study. Gut 2005;54(1):122-127. https://doi.org/10.1136/gut.2003.036566
  13. Park BJ, Kim YJ, Kim DH, Kim W, Jung YJ, Yoon JH, et al. Visceral adipose tissue area is an independent risk factor for hepatic steatosis. J Gastroenterol Hepatol 2008;23(6):900-907. https://doi.org/10.1111/j.1440-1746.2007.05212.x
  14. van der Poorten D, Milner KL, Hui J, Hodge A, Trenell MI, Kench JG, et al. Visceral fat: a key mediator of steatohepatitis in metabolic liver disease. Hepatology 2008;48(2):449-457. https://doi.org/10.1002/hep.22350
  15. Oh YH, Moon JH, Kim HJ, Kong MH. Visceral-to-subcutaneous fat ratio as a predictor of the multiple metabolic risk factors for subjects with normal waist circumference in Korea. Diabetes Metab Syndr Obes 2017;10:505-511. https://doi.org/10.2147/DMSO.S150914
  16. Shim JS, Song BM, Lee JH, Lee SW, Park JH, Choi DP, et al. Cardiovascular and Metabolic Diseases Etiology Research Center (CMERC) cohort: study protocol and results of the first 3 years of enrollment. Epidemiol Health 2017;39:e2017016. https://doi.org/10.4178/epih.e2017016
  17. Zeb I, Li D, Nasir K, Katz R, Larijani VN, Budoff MJ. Computed tomography scans in the evaluation of fatty liver disease in a population based study: the multi-ethnic study of atherosclerosis. Acad Radiol 2012;19(7):811-818. https://doi.org/10.1016/j.acra.2012.02.022
  18. Korean Association for the Study of the Liver. Guidelines for diagnosis of non-alcoholic fatty liver disease; 2013 [cited 2020 Jul 20]. Available from: https://kasl.org/bbs/index.html?code=guide&category=&gubun=&idx=&page=1&number=51&mode=view&order=&sort=&keyfield=&key= (Korean).
  19. Loria P, Adinolfi LE, Bellentani S, Bugianesi E, Grieco A, Fargion S, et al. Practice guidelines for the diagnosis and management of nonalcoholic fatty liver disease. A decalogue from the Italian Association for the Study of the Liver (AISF) Expert Committee. Dig Liver Dis 2010;42(4):272-282. https://doi.org/10.1016/j.dld.2010.01.021
  20. Lee YH. Diagnosis of non-alcoholic fatty liver disease based on clinical and laboratory data. J Korean Diabetes 2017;18(2): 102-108 (Korean). https://doi.org/10.4093/jkd.2017.18.2.102
  21. Kotronen A, Peltonen M, Hakkarainen A, Sevastianova K, Bergholm R, Johansson LM, et al. Prediction of non-alcoholic fatty liver disease and liver fat using metabolic and genetic factors. Gastroenterology 2009;137(3):865-872. https://doi.org/10.1053/j.gastro.2009.06.005
  22. 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. https://doi.org/10.1186/1471-230X-6-33
  23. Long MT, Pedley A, Colantonio LD, Massaro JM, Hoffmann U, Muntner P, et al. Development and validation of the Framingham steatosis index to identify persons with hepatic steatosis. Clin Gastroenterol Hepatol 2016;14(8):1172-1180. https://doi.org/10.1016/j.cgh.2016.03.034
  24. GitHub. SAS_Macros/NRI and IDI index.sas [cited 2020 Apr 1]. Available from: https://github.com/drkrisrogers/SAS_Macros/blob/master/NRI%20and%20IDI%20index.sas.
  25. Jun DW, Han JH, Kim SH, Jang EC, Kim NI, Lee JS, et al. Association between low thigh fat and non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2008;23(6):888-893. https://doi.org/10.1111/j.1440-1746.2008.05330.x
  26. Tchernof A, Despres JP. Pathophysiology of human visceral obesity: an update. Physiol Rev 2013;93(1):359-404. https://doi.org/10.1152/physrev.00033.2011
  27. Wang T, Ma X, Peng D, Zhang R, Sun X, Chen M, et al. Effects of obesity related genetic variations on visceral and subcutaneous fat distribution in a Chinese population. Sci Rep 2016;6:20691. https://doi.org/10.1038/srep20691
  28. Malis C, Rasmussen EL, Poulsen P, Petersen I, Christensen K, Beck-Nielsen H, et al. Total and regional fat distribution is strongly influenced by genetic factors in young and elderly twins. Obes Res 2005;13(12):2139-2145. https://doi.org/10.1038/oby.2005.265
  29. Wells JC. Sexual dimorphism of body composition. Best Pract Res Clin Endocrinol Metab 2007;21(3):415-430. https://doi.org/10.1016/j.beem.2007.04.007
  30. Karpe F, Pinnick KE. Biology of upper-body and lower-body adipose tissue--link to whole-body phenotypes. Nat Rev Endocrinol 2015;11(2):90-100. https://doi.org/10.1038/nrendo.2014.185