Improvement in Non-alcoholic Fatty Liver Disease Score Correlates with Weight Loss in Obese Patients Undergoing Laparoscopic Sleeve Gastrectomy: a Two-Centre Study from an Asian Cohort

  • Zong Jie Koh
  • Hrishikesh Pandurang Salgaonkar
  • Wei Jie Jonathan Lee
  • Guo Wei Kim
  • Chun Hai Tan
  • Anton Cheng
  • Davide Lomanto
  • Jimmy Bok Yan So
  • Yock Young Dan
  • Asim Shabbir
Original Contributions



Incidence of non-alcoholic fatty liver disease (NAFLD) is on the rise and is one of the most common causes of chronic liver disease worldwide. Obesity and metabolic syndrome are considered the most significant risk factors. Bariatric surgery is the only treatment modality in morbid obesity which allows long-term weight loss with improvement in associated co-morbid conditions. However, the effects of bariatric surgery on NAFLD are not well established. NAFLD fibrosis score (NFS) is a validated non-invasive scoring system used to assess advanced fibrosis. We used the NFS to analyse the impact of weight loss on NAFLD following sleeve gastrectomy.

Materials and Methods

174 patients who underwent bariatric surgery between 2010 and 2016 were retrospectively reviewed. Multivariate analysis was performed using pre-operative patient characteristics, biochemical markers and TANITA body analysis measurements to determine significant risk factors for NFS > 0.675. Additionally, the NFS was calculated at 6 months, 1 year and 2 years post-operatively to determine correlation with weight loss.


Pre-operatively, 13.8% of our patients had significant fibrosis by NFS. Mean change in NFS was − 0.46 ± 1.02, − 0.55 ± 0.98 and − 0.55 ± 1.12 at 6 months, 1 year and 2 years respectively. This was significantly correlated with percent of total weight loss with R coefficients of 0.253, 0.292 and 0.274 respectively (P < 0.05). 79.2% of patients with NFS > 0.675 achieved resolution by 2 years post-operatively.


Based on our study, we conclude that sleeve gastrectomy may be a viable treatment option for management of NAFLD in the obese.


Bariatric surgery Non-alcoholic fatty liver disease Non-alcoholic steatohepatitis Obesity Sleeve gastrectomy 


Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethics Statements

This study has been approved by the institutional research ethics committee. No formal consent was required as this was a retrospective study.


  1. 1.
    Browning JD, Szczepaniak LS, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004;40:1387–95.CrossRefPubMedGoogle Scholar
  2. 2.
    Bedogni G, Miglioli L, Masutti F, et al. Prevalence of and risk factors for nonalcoholic fatty liver disease: the Dionysos nutrition and liver study. Hepatology. 2005;42:44–52.CrossRefPubMedGoogle Scholar
  3. 3.
    Fan JG, Zhu J, Li XJ, et al. Prevalence of and risk factors for fatty liver in a general population of Shanghai, China. J Hepatol. 2005;43:508–14.CrossRefPubMedGoogle Scholar
  4. 4.
    Nomura H, Kashiwagi S, Hayashi J, et al. Prevalence of fatty liver in a general population of Okinawa, Japan. Jpn J Med. 1988;27:142–9.CrossRefPubMedGoogle Scholar
  5. 5.
    The World at Six Billion. UN Population Division.Google Scholar
  6. 6.
    Chitturi S, Farrell GC, Hashimoto E, et al. Nonalcoholic fatty liver disease in the Asia-Pacific region: definitions and overview of proposed guidelines. J Gastroenterol Hepatol. 2007;22(6):778–87.CrossRefPubMedGoogle Scholar
  7. 7.
    Jafar TH, Hatcher J, Poulter N, et al. Community-based interventions to promote blood pressure control in a developing country: a cluster randomized trial. Ann Intern Med. 2009;151(9):593–601.CrossRefPubMedGoogle Scholar
  8. 8.
    Lear SA, Toma M, Birmingham CL, et al. Modification of the relationship between simple anthropometric indices and risk factors by ethnic background. Metabolism. 2003;52(10):1295–301.CrossRefPubMedGoogle Scholar
  9. 9.
    Hamaguchi M, Kojima T, Takeda N, et al. The metabolic syndrome as a predictor of nonalcoholic fatty liver disease. Ann Intern Med. 2005;143(10):722–8.CrossRefPubMedGoogle Scholar
  10. 10.
    Brunt EM. Nonalcoholic steatohepatitis. Semin Liver Dis. 2004;24(1):3–20.CrossRefPubMedGoogle Scholar
  11. 11.
    Cusi K. Role of obesity and lipotoxicity in the development of non-alcoholic steatohepatitis: pathophysiology and clinical implications. Gastroenterology. 2012;142(4):711–25.CrossRefPubMedGoogle Scholar
  12. 12.
    Fabbrini E, Sullivan S, Klein S. Obesity and nonalcoholic fatty liver disease: biochemical, metabolic and clinical implications. Hepatology. 2010;51(2):679–89.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    McCullough AJ. Pathophysiology of nonalcoholic steatohepatitis. J Clin Gastroenterol. 2006;40(suppl 1):S17–29.PubMedGoogle Scholar
  14. 14.
    Duvnjak M, Lerotić I, Barsić N, et al. Pathogenesis and management issues for non-alcoholic fatty liver disease. World J Gastroenterol. 2007;13(34):4539–50.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Siebler J, Galle PR, Weber MM. The gut-liver-axis: endotoxemia, inflammation, insulin resistance and NASH. J Hepatol. 2008;48(6):1032–4.CrossRefPubMedGoogle Scholar
  16. 16.
    Wong VW, Wong GL, Choi PC, et al. Disease progression of non-alcoholic fatty liver disease: a prospective study with paired liver biopsies at 3 years. Gut. 2010;59(7):969–74.CrossRefPubMedGoogle Scholar
  17. 17.
    Pais R, Pascale A, Fedchuck L, et al. Progression from isolated steatosis to steatohepatitis and fibrosis in nonalcoholic fatty liver disease. Clin Res Hepatol Gastroenterol. 2011;35(1):23–8.CrossRefPubMedGoogle Scholar
  18. 18.
    Pais R, Charlotte F, Fedchuk L, et al. A systematic review of followup biopsies reveals disease progression in patients with non-alcoholic fatty liver. J Hepatol. 2013;59(3):550–6.CrossRefPubMedGoogle Scholar
  19. 17.
    Angulo P, Hui JM, Marchesini G, et al. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology. 2007;45(4):846–54.CrossRefPubMedGoogle Scholar
  20. 18.
    McPherson S, Stewart SF, Henderson E, et al. Simple non-invasive fibrosis scoring systems can reliably exclude advanced fibrosis in patients with non-alcoholic fatty liver disease. Gut. 2010;59(9):1265–9.CrossRefPubMedGoogle Scholar
  21. 19.
    Angulo P. Nonalcoholic fatty liver disease. N Engl J Med. 2002;346(16):1221–31.CrossRefPubMedGoogle Scholar
  22. 20.
    Qureshi K, Clements RH, Abrams GA. The utility of the “NAFLD fibrosis score” in morbidly obese subjects with NAFLD. Obes Surg. 2008;18(3):264–70.CrossRefPubMedGoogle Scholar
  23. 21.
    Pimentel SK, Strobel R, Gonçalves CG, et al. Evaluation of the nonalcoholic fat liver disease fibrosis score for patients undergoing bariatric surgery. Arq Gastroenterol. 2010;47(2):170–3.CrossRefPubMedGoogle Scholar
  24. 22.
    Attar BM, Van Thiel DH. Current concepts and management approaches in nonalcoholic fatty liver disease. ScientificWorldJournal. 2013;2013:481893.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 23.
    Marra F, Lotersztajin S. Pathophysiology of NASH: perspectives for a targeted treatment. Curr Pharm Des. 2013;19(29):5250–69.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 24.
    Mi X-X, Wang L, Xun Y-H, et al. Assessment nonalcoholic fatty liver disease fibrosis score for staging and predicting outcome. Int J Clin Exp Med. 2016;9(8):16146–56.Google Scholar
  27. 25.
    Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and managements 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. Scholar
  28. 26.
    Tai CM, Huang CK, Hwang JC, et al. Improvement of nonalcoholic fatty liver disease after bariatric surgery in morbidly obese Chinese patients. Obes Surg. 2012;22:1016–21.CrossRefPubMedGoogle Scholar
  29. 27.
    Kakizaki S, Takizawa D, Yamazaki Y, et al. Nonalcoholic fatty liver disease in Japanese patients with severe obesity who received laparoscopic Roux-en-Y gastric bypass surgery (LRYGB) in comparison to non-Japanese patients. J Gastroenterol. 2008;43(1):86–92.CrossRefPubMedGoogle Scholar
  30. 28.
    Praveen RP, Gomes RM, Kumar S, et al. The effect of surgically induced weight loss on nonalcoholic fatty liver disease in morbidly obese Indians: NASHOST prospective observational trial. Surg Obes Relat Dis. 2015;11(6):1315–22.CrossRefGoogle Scholar
  31. 29.
    Froylich D, Corcelles R, Daigle C, et al. Effect of Roux-en-Y gastric bypass and sleeve gastrectomy on nonalcoholic fatty liver disease: a comparative study. Surg Obes Relat Dis. 2016;12(1):127–31.CrossRefPubMedGoogle Scholar
  32. 30.
    Vargas V, Allende H, Lecube A, et al. Surgically induced weight loss by gastric bypass improves non alcoholic fatty liver disease in morbid obese patients. World J Hepatol. 2012;4(12):382–8.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 31.
    Cazzo E, Jimenez LS, Pareja JC, et al. Effect of roux-en-y gastric bypass on Nonalcoholic Fatty Liver Disease evaluated through NAFLD fibrosis score: a prospective study. Obes Surg. 2015;25:982–5.CrossRefPubMedGoogle Scholar
  34. 32.
    Karcz WK, Krawczykowski D, Kuesters S, et al. Influence of sleeve gastrectomy on NASH and type 2 diabetes mellitus. J Obes. 2011;2011:765473.CrossRefPubMedGoogle Scholar
  35. 33.
    Myronovych A et al. Vertical sleeve gastrectomy reduces hepatic steatosis while increasing serum bile acids in a weight-loss-independent manner. Obesity. 2014;22:390–400.CrossRefPubMedGoogle Scholar
  36. 34.
    Myronovych A, Salazar-Gonzalez R-M, Ryan KK, et al. The role of small heterodimer partner in nonalcoholic fatty liver disease improvement after sleeve gastrectomy in mice. Obesity. 2014;22:2301–11.CrossRefPubMedGoogle Scholar
  37. 35.
    Du J, Tian J, Ding L, et al. Vertical sleeve gastrectomy reverses diet-induced gene-regulatory changes impacting lipid metabolism. Sci Rep. 2017;7:5274.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 36.
    European Association for Study of Liver. Asociacion Latinoamericana para el Estudio del Higado EASL-ALEH Clinical Practice Guidelines: non-invasive tests for evaluation of liver disease severity and prognosis. J Hepatol. 2015;63:237–64. Scholar
  39. 37.
    McPherson S, Stewart SF, Henderson E, et al. Simple non-invasive fibrosis scoring systems can reliably exclude advanced fibrosis in patients with non-alcoholic fatty liver disease. Gut. 2010;59:1265–9. Scholar
  40. 38.
    Kim D, Kim WR, Kim HJ, et al. Association between noninvasive fibrosis markers and mortality among adults with nonalcoholic fatty liver disease in the United States. Hepatology. 2013;57:1357–65. Scholar
  41. 39.
    Treeprasertsuk S, Björnsson E, Enders F, et al. NAFLD fibrosis score: a prognostic predictor for mortality and liver complications among NAFLD patients. World J Gastroenterol. 2013;19:1219–29. Scholar
  42. 40.
    Wong VW, Wong GL, Chim AM, et al. Validation of the NAFLD fibrosis score in a Chinese population with low prevalence of advanced fibrosis. Am J Gastroenterol. 2008;103:1682–8. Scholar
  43. 41.
    Mummadi RR, Kasturi KS, Chennareddygari S, et al. Effects of bariatric surgery on nonalcoholic fatty liver disease: systematic review and meta- analysis. Clin Gastroenterol Hepatol. 2008;6(12):1396–402.CrossRefPubMedGoogle Scholar
  44. 42.
    Chavez-Tapia NC, Tellez-Avila FI, Barrientos-Gutierrez T, et al. Bariatric surgery for non-alcoholic steatohepatitis in obese patients. Cochrane Database Syst Rev. 2010;20(1):CD007340.Google Scholar
  45. 43.
    Ministry of Health. National health survey 2010. Singapore: Epidemiology and Disease Control Division, Ministry of Health; 2011.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Zong Jie Koh
    • 1
  • Hrishikesh Pandurang Salgaonkar
    • 1
  • Wei Jie Jonathan Lee
    • 2
  • Guo Wei Kim
    • 1
  • Chun Hai Tan
    • 3
  • Anton Cheng
    • 3
  • Davide Lomanto
    • 1
  • Jimmy Bok Yan So
    • 1
  • Yock Young Dan
    • 2
  • Asim Shabbir
    • 1
  1. 1.Department of General SurgeryNational University Health SystemSingaporeSingapore
  2. 2.Department of GastroenterologyNational University Health SystemSingaporeSingapore
  3. 3.Department of General SurgeryKhoo Teck Puat HospitalSingaporeSingapore

Personalised recommendations