Obesity Surgery

, Volume 25, Issue 12, pp 2280–2289 | Cite as

Bariatric Surgery and Non-Alcoholic Fatty Liver Disease: a Systematic Review of Liver Biochemistry and Histology

  • Guy Bower
  • Tania Toma
  • Leanne Harling
  • Long R Jiao
  • Evangelos Efthimiou
  • Ara Darzi
  • Thanos Athanasiou
  • Hutan AshrafianEmail author
Original Contributions



Non-alcoholic fatty liver disease (NAFLD) is becoming a leading cause of global liver disease that is associated with the rising prevalence of obesity worldwide. There is now increasing clinical and mechanistic evidence reporting on the metabolic and weight loss effects of bariatric surgery on improving NAFLD in obese patients.


The aim of this paper was to quantify the effects of bariatric surgery on NAFLD by appraising the modulation between pre- and post-operative liver enzyme levels (as markers of liver injury) and liver histology.


A systematic review of studies reporting pre-operative and post-operative liver enzymes or liver histology was done in obese patients with NAFLD undergoing bariatric surgery. Data were meta-analysed using random-effects modelling. Subgroup analysis, quality scoring and risk of bias were assessed.


Bariatric surgery is associated with a significant reduction in the weighted incidence of a number of histological features of NAFLD including steatosis (50.2 and 95 %CI of 35.5–65.0), fibrosis (11.9 and 95 %CI of 7.4–16.3 %), hepatocyte ballooning (67.7 and 95 %CI 56.9–78.5) and lobular inflammation (50.7 and 95 %CI 26.6–74.8 %). Surgery is also associated with a reduction in liver enzyme levels, with statistically significant reductions in ALT (11.36 u/l, 95 %CI 8.36–14.39), AST (3.91 u/l, 95 %CI 2.23–5.59), ALP (10.55 u/l, 95 %CI 4.40–16.70) and gamma-GT (18.39 u/l, 95 %CI 12.62–24.16). Heterogeneity in results was high.


Bariatric surgery is associated with a significant improvement in both histological and biochemical markers of NAFLD. Future studies must focus on higher levels of evidence to better identify the benefits of bariatric surgery on liver disease in order to enhance future treatment strategies in the management of NAFLD.


Non-alcoholic fatty liver disease NAFLD Bariatric surgery Metabolic surgery Body mass index Intervention Surgery Weight loss 


Ethical Approval

For this type of study, formal consent is not required.

Conflict of Interest

The authors declare that they have no conflict of interest.

Financial Disclosure



  1. 1.
    WGO. Nonalcoholic fatty liver disease and nonalcoholic steatohepatitis ( 2012.
  2. 2.
    Blachier M, Leleu H, Peck-Radosavljevic M, et al. The burden of liver disease in Europe: a review of available epidemiological data. J Hepatol. 2013;58(3):593–608.CrossRefPubMedGoogle Scholar
  3. 3.
    Angulo P, Lindor KD. Non-alcoholic fatty liver disease. J Gastroenterol Hepatol. 2002;17(Suppl):S186–90.CrossRefPubMedGoogle Scholar
  4. 4.
    Dixon JB, Bhathal PS, O'Brien PE. Nonalcoholic fatty liver disease: predictors of nonalcoholic steatohepatitis and liver fibrosis in the severely obese. Gastroenterology. 2001;121(1):91–100.CrossRefPubMedGoogle Scholar
  5. 5.
    Gupta R, Bhangoo A, Matthews NA, et al. The prevalence of non-alcoholic fatty liver disease and metabolic syndrome in obese children. J Pediatr Endocrinol Metab. 2011;24(11–12):907–11.PubMedGoogle Scholar
  6. 6.
    WHO. Obesity and overweight ( 2014.
  7. 7.
    Kelly T, Yang W, Chen CS, et al. Global burden of obesity in 2005 and projections to 2030. Int J Obes (Lond). 2008;32(9):1431–7.CrossRefGoogle Scholar
  8. 8.
    Harrison SA, Day CP. Benefits of lifestyle modification in NAFLD. Gut. 2007;56(12):1760–9.PubMedCentralCrossRefPubMedGoogle Scholar
  9. 9.
    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
  10. 10.
    Puterbaugh JS. The emperor’s tailors: the failure of the medical weight loss paradigm and its causal role in the obesity of America. Diabetes Obes Metab. 2009;11(6):557–70.CrossRefPubMedGoogle Scholar
  11. 11.
    Fassio E, Alvarez E, Dominguez N, et al. Natural history of nonalcoholic steatohepatitis: a longitudinal study of repeat liver biopsies. Hepatology. 2004;40(4):820–6.PubMedGoogle Scholar
  12. 12.
    Livingston EH. The incidence of bariatric surgery has plateaued in the U.S. Am J Surg. 2010;200(3):378–85.PubMedCentralCrossRefPubMedGoogle Scholar
  13. 13.
    Buchwald H, Avidor Y, Braunwald E, et al. Bariatric surgery: a systematic review and meta-analysis. JAMA. 2004;292(14):1724–37.CrossRefPubMedGoogle Scholar
  14. 14.
    Adams TD, Gress RE, Smith SC, et al. Long-term mortality after gastric bypass surgery. N Engl J Med. 2007;357(8):753–61.CrossRefPubMedGoogle Scholar
  15. 15.
    Pontiroli AE, Morabito A. Long-term prevention of mortality in morbid obesity through bariatric surgery. A systematic review and meta-analysis of trials performed with gastric banding and gastric bypass. Ann Surg. 2011;253(3):484–7.CrossRefPubMedGoogle Scholar
  16. 16.
    Reha JL, Lee S, Hofmann LJ. Prevalence and predictors of nonalcoholic steatohepatitis in obese patients undergoing bariatric surgery: a Department of Defense experience. Am Surg. 2014;80(6):595–9.PubMedGoogle Scholar
  17. 17.
    Weiner RA. Surgical treatment of non-alcoholic steatohepatitis and non-alcoholic fatty liver disease. Dig Dis. 2010;28(1):274–9.CrossRefPubMedGoogle Scholar
  18. 18.
    Caiazzo R, Lassailly G, Leteurtre E, et al. Roux-en-Y gastric bypass versus adjustable gastric banding to reduce nonalcoholic fatty liver disease: a 5-year controlled longitudinal study. Ann Surg. 2014;260(5):893–8. discussion 8-9.CrossRefPubMedGoogle Scholar
  19. 19.
    Abdennour M, Reggio S, Le Naour G, et al. Association of adipose tissue and liver fibrosis with tissue stiffness in morbid obesity: links with diabetes and BMI loss after gastric bypass. J Clin Endocrinol Metab. 2014;99(3):898–907.PubMedGoogle Scholar
  20. 20.
    Coupaye M, Riviere P, Breuil MC, et al. Comparison of nutritional status during the first year after sleeve gastrectomy and Roux-en-Y gastric bypass. Obes Surg. 2014;24(2):276–83.CrossRefPubMedGoogle Scholar
  21. 21.
    de Jonge C, Rensen SS, Koek GH, et al. Endoscopic duodenal-jejunal bypass liner rapidly improves plasma parameters of nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2013;11(11):1517–20.CrossRefPubMedGoogle Scholar
  22. 22.
    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.PubMedCentralPubMedGoogle Scholar
  23. 23.
    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(7):1016–21.CrossRefPubMedGoogle Scholar
  24. 24.
    Moretto M, Kupski C, da Silva VD, et al. Effect of bariatric surgery on liver fibrosis. Obes Surg. 2012;22(7):1044–9.CrossRefPubMedGoogle Scholar
  25. 25.
    Caiazzo R, Arnalsteen L, Pigeyre M, et al. Long-term metabolic outcome and quality of life after laparoscopic adjustable gastric banding in obese patients with type 2 diabetes mellitus or impaired fasting glucose. Br J Surg. 2010;97(6):884–91.CrossRefPubMedGoogle Scholar
  26. 26.
    Bell LN, Temm CJ, Saxena R, et al. Bariatric surgery-induced weight loss reduces hepatic lipid peroxidation levels and affects hepatic cytochrome P-450 protein content. Ann Surg. 2010;251(6):1041–8.PubMedCentralCrossRefPubMedGoogle Scholar
  27. 27.
    Mathurin P, Hollebecque A, Arnalsteen L, et al. Prospective study of the long-term effects of bariatric surgery on liver injury in patients without advanced disease. Gastroenterology. 2009;137(2):532–40.CrossRefPubMedGoogle Scholar
  28. 28.
    Swierczynski J, Sledzinski T, Slominska E, et al. Serum phenylalanine concentration as a marker of liver function in obese patients before and after bariatric surgery. Obes Surg. 2009;19(7):883–9.CrossRefPubMedGoogle Scholar
  29. 29.
    Frige F, Laneri M, Veronelli A, et al. Bariatric surgery in obesity: changes of glucose and lipid metabolism correlate with changes of fat mass. Nutr Metab Cardiovasc Dis. 2009;19(3):198–204.CrossRefPubMedGoogle Scholar
  30. 30.
    Moschen AR, Molnar C, Wolf AM, et al. Effects of weight loss induced by bariatric surgery on hepatic adipocytokine expression. J Hepatol. 2009;51(4):765–77.CrossRefPubMedGoogle Scholar
  31. 31.
    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
  32. 32.
    de Andrade AR, Cotrim HP, Alves E, et al. Nonalcoholic fatty liver disease in severely obese individuals: the influence of bariatric surgery. Ann Hepatol. 2008;7(4):364–8.PubMedGoogle Scholar
  33. 33.
    Alexandrides TK, Skroubis G, Kalfarentzos F. Resolution of diabetes mellitus and metabolic syndrome following Roux-en-Y gastric bypass and a variant of biliopancreatic diversion in patients with morbid obesity. Obes Surg. 2007;17(2):176–84.CrossRefPubMedGoogle Scholar
  34. 34.
    Furuya Jr CK, de Oliveira CP, de Mello ES, et al. Effects of bariatric surgery on nonalcoholic fatty liver disease: preliminary findings after 2 years. J Gastroenterol Hepatol. 2007;22(4):510–4.CrossRefPubMedGoogle Scholar
  35. 35.
    Phillips ML, Boase S, Wahlroos S, et al. Associates of change in liver fat content in the morbidly obese after laparoscopic gastric banding surgery. Diabetes Obes Metab. 2008;10(8):661–7.CrossRefPubMedGoogle Scholar
  36. 36.
    Liu X, Lazenby AJ, Clements RH, et al. Resolution of nonalcoholic steatohepatits after gastric bypass surgery. Obes Surg. 2007;17(4):486–92.CrossRefPubMedGoogle Scholar
  37. 37.
    Mathurin P, Gonzalez F, Kerdraon O, et al. The evolution of severe steatosis after bariatric surgery is related to insulin resistance. Gastroenterology. 2006;130(6):1617–24.CrossRefPubMedGoogle Scholar
  38. 38.
    Dixon JB, Bhathal PS, O'Brien PE. Weight loss and non-alcoholic fatty liver disease: falls in gamma-glutamyl transferase concentrations are associated with histologic improvement. Obes Surg. 2006;16(10):1278–86.CrossRefPubMedGoogle Scholar
  39. 39.
    Klein S, Mittendorfer B, Eagon JC, et al. Gastric bypass surgery improves metabolic and hepatic abnormalities associated with nonalcoholic fatty liver disease. Gastroenterology. 2006;130(6):1564–72.CrossRefPubMedGoogle Scholar
  40. 40.
    Meinhardt NG, Souto KE, Ulbrich-Kulczynski JM, et al. Hepatic outcomes after jejunoileal bypass: is there a publication bias? Obes Surg. 2006;16(9):1171–8.CrossRefPubMedGoogle Scholar
  41. 41.
    Csendes A, Smok G, Burgos AM. Histological findings in the liver before and after gastric bypass. Obes Surg. 2006;16(5):607–11.CrossRefPubMedGoogle Scholar
  42. 42.
    de Almeida SR, Rocha PR, Sanches MD, et al. Roux-en-Y gastric bypass improves the nonalcoholic steatohepatitis (NASH) of morbid obesity. Obes Surg. 2006;16(3):270–8.CrossRefPubMedGoogle Scholar
  43. 43.
    Barker KB, Palekar NA, Bowers SP, et al. Non-alcoholic steatohepatitis: effect of Roux-en-Y gastric bypass surgery. Am J Gastroenterol. 2006;101(2):368–73.CrossRefPubMedGoogle Scholar
  44. 44.
    Clark JM, Alkhuraishi AR, Solga SF, et al. Roux-en-Y gastric bypass improves liver histology in patients with non-alcoholic fatty liver disease. Obes Res. 2005;13(7):1180–6.CrossRefPubMedGoogle Scholar
  45. 45.
    Jaskiewicz K, Raczynska S, Rzepko R, et al. Nonalcoholic fatty liver disease treated by gastroplasty. Dig Dis Sci. 2006;51(1):21–6.CrossRefPubMedGoogle Scholar
  46. 46.
    Mottin CC, Moretto M, Padoin AV, et al. Histological behavior of hepatic steatosis in morbidly obese patients after weight loss induced by bariatric surgery. Obes Surg. 2005;15(6):788–93.CrossRefPubMedGoogle Scholar
  47. 47.
    Keshishian A, Zahriya K, Willes EB. Duodenal switch has no detrimental effects on hepatic function and improves hepatic steatohepatitis after 6 months. Obes Surg. 2005;15(10):1418–23.CrossRefPubMedGoogle Scholar
  48. 48.
    Mattar SG, Velcu LM, Rabinovitz M, et al. Surgically-induced weight loss significantly improves nonalcoholic fatty liver disease and the metabolic syndrome. Ann Surg. 2005;242(4):610–7. discussion 8-20.PubMedCentralPubMedGoogle Scholar
  49. 49.
    Stratopoulos C, Papakonstantinou A, Terzis I, et al. Changes in liver histology accompanying massive weight loss after gastroplasty for morbid obesity. Obes Surg. 2005;15(8):1154–60.CrossRefPubMedGoogle Scholar
  50. 50.
    Kral JG, Thung SN, Biron S, et al. Effects of surgical treatment of the metabolic syndrome on liver fibrosis and cirrhosis. Surgery. 2004;135(1):48–58.CrossRefPubMedGoogle Scholar
  51. 51.
    Dixon JB, Bhathal PS, Hughes NR, et al. Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss. Hepatology. 2004;39(6):1647–54.CrossRefPubMedGoogle Scholar
  52. 52.
    Luyckx FH, Desaive C, Thiry A, et al. Liver abnormalities in severely obese subjects: effect of drastic weight loss after gastroplasty. Int J Obes Relat Metab Disord. 1998;22(3):222–6.CrossRefPubMedGoogle Scholar
  53. 53.
    Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA. 2000;283(15):2008–12.CrossRefPubMedGoogle Scholar
  54. 54.
    Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535.PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    Farrell GC, van Rooyen D, Gan L, et al. NASH is an inflammatory disorder: pathogenic, prognostic and therapeutic implications. Gut Liver. 2012;6(2):149–71.PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Matteoni CA, Younossi ZM, Gramlich T, et al. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology. 1999;116(6):1413–9.CrossRefPubMedGoogle Scholar
  57. 57.
    Rakha EA, Adamson L, Bell E, et al. Portal inflammation is associated with advanced histological changes in alcoholic and non-alcoholic fatty liver disease. J Clin Pathol. 2010;63(9):790–5.CrossRefPubMedGoogle Scholar
  58. 58.
    Wu R, Ortiz J, Dallal R. Is bariatric surgery safe in cirrhotics? Hepat Mon. 2013;13(2):e8536.PubMedCentralCrossRefPubMedGoogle Scholar
  59. 59.
    Verna EC, Berk PD. Role of fatty acids in the pathogenesis of obesity and fatty liver: impact of bariatric surgery. Semin Liver Dis. 2008;28(4):407–26.CrossRefPubMedGoogle Scholar
  60. 60.
    Dallal RM, Mattar SG, Lord JL, et al. Results of laparoscopic gastric bypass in patients with cirrhosis. Obes Surg. 2004;14(1):47–53.CrossRefPubMedGoogle Scholar
  61. 61.
    Bi WR, Yang CQ, Shi Q, et al. Large-scale analysis of factors influencing nonalcoholic fatty liver disease and its relationship with liver enzymes. Genet Mol Res. 2014;13(3):5880–91.CrossRefPubMedGoogle Scholar
  62. 62.
    Prati D, Taioli E, Zanella A, et al. Updated definitions of healthy ranges for serum alanine aminotransferase levels. Ann Intern Med. 2002;137(1):1–10.CrossRefPubMedGoogle Scholar
  63. 63.
    Kim WR, Flamm SL, Di Bisceglie AM, et al. Serum activity of alanine aminotransferase (ALT) as an indicator of health and disease. Hepatology. 2008;47(4):1363–70.CrossRefPubMedGoogle Scholar
  64. 64.
    Ashrafian H, le Roux CW, Rowland SP, et al. Metabolic surgery and obstructive sleep apnoea: the protective effects of bariatric procedures. Thorax. 2012;67(5):442–9.CrossRefPubMedGoogle Scholar
  65. 65.
    Ashrafian H, Ahmed K, Rowland SP, et al. Metabolic surgery and cancer: protective effects of bariatric procedures. Cancer. 2011;117(9):1788–99.CrossRefPubMedGoogle Scholar
  66. 66.
    Polesel J, Zucchetto A, Montella M, et al. The impact of obesity and diabetes mellitus on the risk of hepatocellular carcinoma. Ann Oncol. 2009;20(2):353–7.CrossRefPubMedGoogle Scholar
  67. 67.
    Larsson SC, Wolk A. Overweight, obesity and risk of liver cancer: a meta-analysis of cohort studies. Br J Cancer. 2007;97(7):1005–8.PubMedCentralPubMedGoogle Scholar
  68. 68.
    Ashrafian H, Athanasiou T, Li JV, et al. Diabetes resolution and hyperinsulinaemia after metabolic Roux-en-Y gastric bypass. Obes Rev. 2011;12(5):e257–72.CrossRefPubMedGoogle Scholar
  69. 69.
    Ashrafian H, Darzi A, Athanasiou T. Autobionics: a new paradigm in regenerative medicine and surgery. Regen Med. 2010;5(2):279–88.PubMedCentralCrossRefPubMedGoogle Scholar
  70. 70.
    Guidone C, Manco M, Valera-Mora E, et al. Mechanisms of recovery from type 2 diabetes after malabsorptive bariatric surgery. Diabetes. 2006;55(7):2025–31.CrossRefPubMedGoogle Scholar
  71. 71.
    Trakhtenbroit MA, Leichman JG, Algahim MF, et al. Body weight, insulin resistance, and serum adipokine levels 2 years after 2 types of bariatric surgery. Am J Med. 2009;122(5):435–42.PubMedCentralCrossRefPubMedGoogle Scholar
  72. 72.
    Ashrafian H, le Roux CW. Metabolic surgery and gut hormones—a review of bariatric entero-humoral modulation. Physiol Behav. 2009;97(5):620–31.CrossRefPubMedGoogle Scholar
  73. 73.
    Patti ME, Houten SM, Bianco AC, et al. Serum bile acids are higher in humans with prior gastric bypass: potential contribution to improved glucose and lipid metabolism. Obesity (Silver Spring). 2009;17(9):1671–7.CrossRefGoogle Scholar
  74. 74.
    Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009;106(7):2365–70.PubMedCentralCrossRefPubMedGoogle Scholar
  75. 75.
    Li JV, Ashrafian H, Bueter M, et al. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut. 2011;60(9):1214–23.PubMedCentralCrossRefPubMedGoogle Scholar
  76. 76.
    Ashrafian H, le Roux CW, Darzi A, et al. Effects of bariatric surgery on cardiovascular function. Circulation. 2008;118(20):2091–102.CrossRefPubMedGoogle Scholar
  77. 77.
    Koca SS, Bahcecioglu IH, Poyrazoglu OK, et al. The treatment with antibody of TNF-alpha reduces the inflammation, necrosis and fibrosis in the non-alcoholic steatohepatitis induced by methionine- and choline-deficient diet. Inflammation. 2008;31(2):91–8.CrossRefPubMedGoogle Scholar
  78. 78.
    Zhang L, Yang M, Ren H, et al. GLP-1 analogue prevents NAFLD in ApoE KO mice with diet and Acrp30 knockdown by inhibiting c-JNK. Liver Int. 2013;33(5):794–804.CrossRefPubMedGoogle Scholar
  79. 79.
    Finelli C, Tarantino G. What is the role of adiponectin in obesity related non-alcoholic fatty liver disease? World J Gastroenterol. 2013;19(6):802–12.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Guy Bower
    • 1
  • Tania Toma
    • 1
  • Leanne Harling
    • 1
  • Long R Jiao
    • 1
    • 3
  • Evangelos Efthimiou
    • 1
    • 2
  • Ara Darzi
    • 1
  • Thanos Athanasiou
    • 1
  • Hutan Ashrafian
    • 1
    • 2
    • 3
    Email author
  1. 1.Department of Surgery and CancerImperial College LondonLondonUK
  2. 2.Department of Bariatric SurgeryChelsea and Westminster HospitalLondonUK
  3. 3.Department of Hepatobiliary and Pancreatic SurgeryImperial College Healthcare NHS TrustLondonUK

Personalised recommendations