Current Controversies in Metabolic Surgery for Nonalcoholic Fatty Liver Disease

  • Iraklis Perysinakis
  • Harilaos C. Pappis
  • Elias Margaris
Review Article


Nonalcoholic fatty liver disease (NAFLD) represents the most common liver disease, and it is expected to become the leading cause of end-stage liver disease in the near future. Bariatric operations have beneficial effects on NAFLD, inducing histological resolution of liver damage through weight loss-dependent and weight loss-independent mechanisms. Due to lack of randomized controlled trials, no specific guidelines have been established so far. Yet there is growing evidence that NAFLD will eventually become a formal indication for metabolic surgery. Data regarding the choice of procedure are conflicting, although gastric bypass seems to be slightly superior to sleeve gastrectomy. The purpose of this review is to provide an update on the ongoing research regarding the role of metabolic surgery in NAFLD management.


Nonalcoholic fatty liver disease Liver steatosis Steatohepatitis Bariatric surgery Metabolic surgery Gastric bypass Sleeve gastrectomy 


Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Statement

This article does not contain any studies with human participants or animals performed by authors.

Consent Statement

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


  1. 1.
    Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American Association for the Study of Liver Diseases. Hepatology. 2018;67:328–57.CrossRefPubMedGoogle Scholar
  2. 2.
    European Association for the Study of the L, European Association for the Study of D and European Association for the Study of O. EASL-EASD-EASO clinical practice guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016;64:1388–402.Google Scholar
  3. 3.
    Younossi Z, Henry L. Contribution of alcoholic and nonalcoholic fatty liver disease to the burden of liver-related morbidity and mortality. Gastroenterology. 2016;150:1778–85.CrossRefPubMedGoogle Scholar
  4. 4.
    Esquivel CM, Garcia M, Armando L, et al. Laparoscopic sleeve gastrectomy resolves NAFLD: another formal indication for bariatric surgery? Obes Surg. 2018;28:4022–33.CrossRefPubMedGoogle Scholar
  5. 5.
    Clanton J, Subichin M. The effects of metabolic surgery on fatty liver disease and nonalcoholic steatohepatitis. Surg Clin North Am. 2016;96:703–15.CrossRefPubMedGoogle Scholar
  6. 6.
    Younossi Z, Stepanova M, Ong JP, et al. Nonalcoholic steatohepatitis is the fastest growing cause of hepatocellular carcinoma in liver transplant candidates. Clin Gastroenterol Hepatol. 2018;S1542–3565(18)30611–6.
  7. 7.
    Eslam M, Valenti L, Romeo S. Genetics and epigenetics of NAFLD and NASH: clinical impact. J Hepatol. 2018;68:268–79.CrossRefPubMedGoogle Scholar
  8. 8.
    Fried M, Yumuk V, Oppert JM, et al. Interdisciplinary European guidelines on metabolic and bariatric surgery. Obes Facts. 2013;6:449–68.CrossRefPubMedGoogle Scholar
  9. 9.
    Aguilar-Olivos NE, Almeda-Valdes P, Aguilar-Salinas CA, et al. The role of bariatric surgery in the management of nonalcoholic fatty liver disease and metabolic syndrome. Metabolism. 2016;65:1196–207.CrossRefPubMedGoogle Scholar
  10. 10.
    Chitturi S, Wong VW, Chan WK, et al. The Asia-Pacific working party on non-alcoholic fatty liver disease guidelines 2017-part 2: management and special groups. J Gastroenterol Hepatol. 2018;33:86–98.CrossRefPubMedGoogle Scholar
  11. 11.
    Neuschwander-Tetri BA, Clark JM, Bass NM, et al. Clinical, laboratory and histological associations in adults with nonalcoholic fatty liver disease. Hepatology. 2010;52:913–24.CrossRefPubMedGoogle Scholar
  12. 12.
    Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med. 2001;344:495–500.CrossRefPubMedGoogle Scholar
  13. 13.
    Boyum JH, Atwell TD, Schmit GD, et al. Incidence and risk factors for adverse events related to image-guided liver biopsy. Mayo Clin Proc. 2016;91:329–35.CrossRefPubMedGoogle Scholar
  14. 14.
    Hedderich DM, Hasenberg T, Haneder S, et al. Effects of bariatric surgery on non-alcoholic fatty liver disease: magnetic resonance imaging is an effective, non-invasive method to evaluate changes in the liver fat fraction. Obes Surg. 2017;27:1755–62.CrossRefPubMedGoogle Scholar
  15. 15.
    Schwenger KJP, Fischer SE, Jackson T, et al. In nonalcoholic fatty liver disease, Roux-en-Y gastric bypass improves liver histology while persistent disease is associated with lower improvements in waist circumference and glycemic control. Surg Obes Relat Dis. 2018;14(9):1233–1239.
  16. 16.
    Chou R, Wasson N. Blood tests to diagnose fibrosis or cirrhosis in patients with chronic hepatitis C virus infection: a systematic review. Ann Intern Med. 2013;158:807–20.CrossRefPubMedGoogle Scholar
  17. 17.
    Klebanoff MJ, Corey KE, Chhatwal J, et al. Bariatric surgery for nonalcoholic steatohepatitis: a clinical and cost-effectiveness analysis. Hepatology. 2017;65:1156–64.CrossRefPubMedGoogle Scholar
  18. 18.
    Rubino F, Nathan DM, Eckel RH, et al. Metabolic surgery in the treatment algorithm for type 2 diabetes: a joint statement by international diabetes organizations. Diabetes Care. 2016;39:861–77.CrossRefPubMedGoogle Scholar
  19. 19.
    Singh T, Kochhar GS, Goh GB, et al. Safety and efficacy of bariatric surgery in patients with advanced fibrosis. Int J Obes. 2017;41:443–9.CrossRefGoogle Scholar
  20. 20.
    Kalinowski P, Paluszkiewicz R, Ziarkiewicz-Wroblewska B, et al. Liver function in patients with nonalcoholic fatty liver disease randomized to Roux-en-Y gastric bypass versus sleeve gastrectomy: a secondary analysis of a randomized clinical trial. Ann Surg. 2017;266:738–45.CrossRefPubMedGoogle Scholar
  21. 21.
    Jan A, Narwaria M, Mahawar KK. A systematic review of bariatric surgery in patients with liver cirrhosis. Obes Surg. 2015;25:1518–26.CrossRefPubMedGoogle Scholar
  22. 22.
    Rebibo L, Gerin O, Verhaeghe P, et al. Laparoscopic sleeve gastrectomy in patients with NASH-related cirrhosis: a case-matched study. Surg Obes Relat Dis. 2014;10:405–10. quiz 565CrossRefPubMedGoogle Scholar
  23. 23.
    Alli V, Rogers AM. Gastric bypass and influence on improvement of NAFLD. Curr Gastroenterol Rep. 2017;19:25.CrossRefPubMedGoogle Scholar
  24. 24.
    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;137:532–40.CrossRefPubMedGoogle Scholar
  25. 25.
    Garg H, Aggarwal S, Shalimar YR, et al. Utility of transient elastography (fibroscan) and impact of bariatric surgery on nonalcoholic fatty liver disease (NAFLD) in morbidly obese patients. Surg Obes Relat Dis. 2018;14:81–91.CrossRefPubMedGoogle Scholar
  26. 26.
    Aldoheyan T, Hassanain M, Al-Mulhim A, et al. The effects of bariatric surgeries on nonalcoholic fatty liver disease. Surg Endosc. 2017;31:1142–7.CrossRefPubMedGoogle Scholar
  27. 27.
    Lassailly G, Caiazzo R, Buob D, et al. Bariatric surgery reduces features of nonalcoholic steatohepatitis in morbidly obese patients. Gastroenterology. 2015;149:379–88. quiz e315–376CrossRefPubMedGoogle Scholar
  28. 28.
    Parker BM, Wu J, You J, et al. Reversal of fibrosis in patients with nonalcoholic steatohepatosis after gastric bypass surgery. BMC Obes. 2017;4:32.CrossRefPubMedGoogle Scholar
  29. 29.
    Taitano AA, Markow M, Finan JE, et al. Bariatric surgery improves histological features of nonalcoholic fatty liver disease and liver fibrosis. J Gastrointest Surg. 2015;19:429–36. discussion 436-427CrossRefPubMedGoogle Scholar
  30. 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;4:382–8.CrossRefPubMedGoogle Scholar
  31. 31.
    Silverman EM, Sapala JA, Appelman HD. Regression of hepatic steatosis in morbidly obese persons after gastric bypass. Am J Clin Pathol. 1995;104:23–31.CrossRefPubMedGoogle Scholar
  32. 32.
    Kral JG, Thung SN, Biron S, et al. Effects of surgical treatment of the metabolic syndrome on liver fibrosis and cirrhosis. Surgery. 2004;135:48–58.CrossRefPubMedGoogle Scholar
  33. 33.
    Moretto M, Kupski C, da Silva VD, et al. Effect of bariatric surgery on liver fibrosis. Obes Surg. 2012;22:1044–9.CrossRefPubMedGoogle Scholar
  34. 34.
    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;15:1418–23.CrossRefPubMedGoogle Scholar
  35. 35.
    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;242:610–7. discussion 618-620PubMedGoogle Scholar
  36. 36.
    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;15:788–93.CrossRefPubMedGoogle Scholar
  37. 37.
    Stratopoulos C, Papakonstantinou A, Terzis I, et al. Changes in liver histology accompanying massive weight loss after gastroplasty for morbid obesity. Obes Surg. 2005;15:1154–60.CrossRefPubMedGoogle Scholar
  38. 38.
    Weiner RA. Surgical treatment of non-alcoholic steatohepatitis and non-alcoholic fatty liver disease. Dig Dis. 2010;28:274–9.CrossRefPubMedGoogle Scholar
  39. 39.
    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
  40. 40.
    Liu X, Lazenby AJ, Clements RH, et al. Resolution of nonalcoholic steatohepatits after gastric bypass surgery. Obes Surg. 2007;17:486–92.CrossRefPubMedGoogle Scholar
  41. 41.
    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;22:510–4.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;16:270–8.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;101:368–73.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;13:1180–6.CrossRefPubMedGoogle Scholar
  45. 45.
    Csendes A, Smok G, Burgos AM. Histological findings in the liver before and after gastric bypass. Obes Surg. 2006;16:607–11.CrossRefPubMedGoogle Scholar
  46. 46.
    Schneck AS, Anty R, Patouraux S, et al. Roux-en-Y gastric bypass results in long-term remission of hepatocyte apoptosis and hepatic histological features of non-alcoholic steatohepatitis. Front Physiol. 2016;7:344.CrossRefPubMedGoogle Scholar
  47. 47.
    Ooi GJ, Burton PR, Doyle L, et al. Effects of bariatric surgery on liver function tests in patients with nonalcoholic fatty liver disease. Obes Surg. 2017;27:1533–42.CrossRefPubMedGoogle Scholar
  48. 48.
    Ruiz-Tovar J, Alsina ME, Alpera MR, et al. Improvement of nonalcoholic fatty liver disease in morbidly obese patients after sleeve gastrectomy: association of ultrasonographic findings with lipid profile and liver enzymes. Acta Chir Belg. 2017;117:363–9.CrossRefPubMedGoogle Scholar
  49. 49.
    Jimenez LS, Mendonca Chaim FH, Mendonca Chaim FD, et al. Impact of weight regain on the evolution of non-alcoholic fatty liver disease after Roux-en-Y gastric bypass: a 3-year follow-up. Obes Surg. 2018;28:3131–5.CrossRefPubMedGoogle Scholar
  50. 50.
    Algooneh A, Almazeedi S, Al-Sabah S, et al. Non-alcoholic fatty liver disease resolution following sleeve gastrectomy. Surg Endosc. 2016;30:1983–7.CrossRefPubMedGoogle Scholar
  51. 51.
    Alizai PH, Wendl J, Roeth AA, et al. Functional liver recovery after bariatric surgery—a prospective cohort study with the LiMAx test. Obes Surg. 2015;25:2047–53.CrossRefPubMedGoogle Scholar
  52. 52.
    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
  53. 53.
    Burza MA, Romeo S, Kotronen A, et al. Long-term effect of bariatric surgery on liver enzymes in the Swedish obese subjects (SOS) study. PLoS One. 2013;8:e60495.CrossRefPubMedGoogle Scholar
  54. 54.
    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
  55. 55.
    Motamedi MAK, Khalaj A, Mahdavi M, et al. Longitudinal comparison of the effect of gastric bypass to sleeve gastrectomy on liver function in a bariatric cohort: Tehran obesity treatment study (TOTS). Obes Surg. 2018.
  56. 56.
    Luo RB, Suzuki T, Hooker JC, et al. How bariatric surgery affects liver volume and fat density in NAFLD patients. Surg Endosc. 2018;32:1675–82.CrossRefPubMedGoogle Scholar
  57. 57.
    Wang JZ, Cao HX, Chen JN, et al. PNPLA3 rs738409 underlies treatment response in nonalcoholic fatty liver disease. World J Clin Cases. 2018;6:167–75.CrossRefPubMedGoogle Scholar
  58. 58.
    Krawczyk M, Jimenez-Aguero R, Alustiza JM, et al. PNPLA3 p.I148M variant is associated with greater reduction of liver fat content after bariatric surgery. Surg Obes Relat Dis. 2016;12:1838–46.CrossRefPubMedGoogle Scholar
  59. 59.
    Ekstedt M, Franzen LE, Holmqvist M, et al. Alcohol consumption is associated with progression of hepatic fibrosis in non-alcoholic fatty liver disease. Scand J Gastroenterol. 2009;44:366–74.CrossRefPubMedGoogle Scholar
  60. 60.
    Musso G, Cassader M, Rosina F, et al. Impact of current treatments on liver disease, glucose metabolism and cardiovascular risk in non-alcoholic fatty liver disease (NAFLD): a systematic review and meta-analysis of randomised trials. Diabetologia. 2012;55:885–904.CrossRefPubMedGoogle Scholar
  61. 61.
    Tan CH, Al-Kalifah N, Lee WJ, et al. HSCRP as surrogate marker in predicting long term effect of bariatric surgery on resolution of non-alcoholic steatohepatitis. Asian J Surg. 2018;42(1):203–208.Google Scholar
  62. 62.
    von Schonfels W, Beckmann JH, Ahrens M, et al. Histologic improvement of NAFLD in patients with obesity after bariatric surgery based on standardized NAS (NAFLD activity score). Surg Obes Relat Dis. 2018;14(10):1607–1616.Google Scholar
  63. 63.
    Nickel F, Tapking C, Benner L, et al. Bariatric surgery as an efficient treatment for non-alcoholic fatty liver disease in a prospective study with 1-year follow-up : BariScan study. Obes Surg. 2018;28:1342–50.CrossRefPubMedGoogle Scholar
  64. 64.
    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;12:127–31.CrossRefPubMedGoogle Scholar
  65. 65.
    Billeter AT, Senft J, Gotthardt D, et al. Combined non-alcoholic fatty liver disease and type 2 diabetes mellitus: sleeve gastrectomy or gastric bypass?-a controlled matched pair study of 34 patients. Obes Surg. 2016;26:1867–74.CrossRefPubMedGoogle Scholar
  66. 66.
    Praveen Raj P, 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;11:1315–22.CrossRefPubMedGoogle Scholar
  67. 67.
    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;260:893–8. discussion 898-899CrossRefPubMedGoogle Scholar
  68. 68.
    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;16:1278–86.CrossRefPubMedGoogle Scholar
  69. 69.
    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;(1):CD007340.Google Scholar
  70. 70.
    Aminian A, Brethauer SA, Kirwan JP, et al. How safe is metabolic/diabetes surgery? Diabetes Obes Metab. 2015;17:198–201.CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Bariatric and Metabolic Surgery“HYGEIA” HospitalAthensGreece
  2. 2.Third Surgical Department“George Gennimatas” General HospitalAthensGreece

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