Bariatric Surgery as an Efficient Treatment for Non-Alcoholic Fatty Liver Disease in a Prospective Study with 1-Year Follow-up

BariScan Study
  • Felix Nickel
  • Christian Tapking
  • Laura Benner
  • Janina Sollors
  • Adrian T. Billeter
  • Hannes G. Kenngott
  • Loay Bokhary
  • Mathias Schmid
  • Moritz von Frankenberg
  • Lars Fischer
  • Sebastian Mueller
  • Beat P. Müller-Stich
Original Contributions

Abstract

Background

Bariatric surgery gains attention as a potential treatment for non-alcoholic fatty liver disease (NAFLD). The present study aimed to evaluate improvement of NAFLD after the two most common bariatric procedures with validated non-invasive instruments.

Material and Methods

N = 100 patients scheduled for laparoscopic sleeve gastrectomy (LSG) or Roux-en-Y gastric bypass (RYGB) were included. NAFLD was evaluated preoperatively and postoperatively with liver stiffness measurement by transient elastography and laboratory-based fibrosis scores. Clinical data included body mass index (BMI), total weight loss (%TWL), excess weight loss (%EWL), age, gender, comorbidities, and the Edmonton obesity staging system (EOSS).

Results

There were significant improvements of BMI, %TWL, %EWL, and EOSS after bariatric surgery. Liver stiffness was significantly improved from pre- to postoperative (12.9 ± 10.4 vs. 7.1 ± 3.7 kPa, p < 0.001) at median follow-up of 12.5 months. Additionally, there were significant improvements of liver fibrosis scores (aspartate aminotransferase (AST)/alanine aminotransferase (ALT) ratio 0.8 ± 0.3 vs. 1.1 ± 0.4, p < 0.001; NAFLD fibrosis score − 1.0 ± 1.8 vs. − 1.7 ± 1.3, p < 0.001; APRI score 0.3 ± 0.2 vs. 0.3 ± 0.1, p = 0.009; BARD score 2.3 ± 1.2 vs. 2.8 ± 1.1, p = 0.008) and laboratory parameters (ALT, AST, and GGT). After adjustment for baseline liver stiffness, RYGB showed higher improvements than LSG, and there was no gender difference. Improvement of liver stiffness was not correlated to improvement of BMI, %TWL, %EWL, or EOSS.

Conclusions

NAFLD seems to be improved by bariatric surgery as measured by validated non-invasive instruments. Furthermore, it appears that RYGB is more effective than LSG. No correlation could be detected between NAFLD and weight loss. The present study highlights the potential of bariatric surgery for successful treatment of NAFLD. Further research is required to understand the exact mechanisms.

Keywords

Transient elastography Bariatric surgery Metabolic surgery Liver disease Liver fibrosis Gastric bypass Sleeve gastrectomy 

Notes

Acknowledgements

We would like to thank Carly R. Garrow for proofreading the manuscript.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Statement of Informed Consent

Informed consent was obtained from all individual participants included in the present study.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Ethical approval was obtained from the local ethics committee (S-181/2009, S-618/2011, S-500/2012 and S-629/2013).

References

  1. 1.
    Ng M. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;386(9945):766–81.CrossRefGoogle Scholar
  2. 2.
    WHO. Fact Sheet. 2015 [cited 2016 17.08.2016]; Available from: http://www.who.int/mediacentre/factsheets/fs311/en/.
  3. 3.
    Huang Z et al. Body weight, weight change, and risk for hypertension in women. Ann Intern Med. 1998;128(2):81–8.CrossRefPubMedGoogle Scholar
  4. 4.
    Sanyal AJ. A technical review on nonalcoholic fatty liver disease. Gastroenterology. 2002;123(5):1705–25.CrossRefPubMedGoogle Scholar
  5. 5.
    Day CP. Non-alcoholic fatty liver disease: current concepts and management strategies. Clin Med. 2006;6(1):19–25.CrossRefGoogle Scholar
  6. 6.
    Charlton MR et al. Frequency of outcomes of liver transplantation for nonalcoholic steatohepatitis in the United States. Gastroenterology. 2011;141(4):1249–53.CrossRefPubMedGoogle Scholar
  7. 7.
    Agopian VG et al. Liver transplantation for nonalcoholic steatohepatitis: the new epidemic. Ann Surg. 2012;256(4):624–33.CrossRefPubMedGoogle Scholar
  8. 8.
    Belli LS et al. Impact of direct anti-viral agents on inactivation/delisting of liver transplant candidates listed for decompensated C cirrhosis: a European study. In: International Liver Congress (ILC): abstract PS036; 2016.Google Scholar
  9. 9.
    Angulo P. Nonalcoholic fatty liver disease. N Engl J Med. 2002;346(16):1221–31.CrossRefPubMedGoogle Scholar
  10. 10.
    Palmer M, Schaffner F. Effect of weight reduction on hepatic abnormalities in overweight patients. Gastroenterology. 1990;99(5):1408–13.CrossRefPubMedGoogle Scholar
  11. 11.
    Park HS, Kim MW, Shin ES. Effect of weight control on hepatic abnormalities in obese patients with fatty liver. Kor Med Sci. 1995;10(6):414–21.CrossRefGoogle Scholar
  12. 12.
    Ueno T, Sugawara H, Sujaku K. Therapeutic effects of restricted diet and exercise in obese patients with fatty liver disease. J Hepatol. 1997;27(1):103–7.CrossRefPubMedGoogle Scholar
  13. 13.
    Sjöström L et al. Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascular and macrovascular complications. JAMA. 2014;311(22):2297–304.CrossRefPubMedGoogle Scholar
  14. 14.
    Nickel F et al. Gastrointestinal quality of life improves significantly after sleeve gastrectomy and Roux-en-Y gastric bypass-a prospective cross-sectional study within a 2-year follow-up. Obes Surg. 2017;27(5):1292–7.CrossRefPubMedGoogle Scholar
  15. 15.
    Nickel F et al. Influence of bariatric surgery on quality of life, body image, and general self-efficacy within 6 and 24 months-a prospective cohort study. Surg Obes Relat Dis. 2017;12(2):313–9.CrossRefGoogle Scholar
  16. 16.
    Echosens. FibroScan® user manual. Paris: Frankreich; 2015.Google Scholar
  17. 17.
    Sandrin L et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29(12):1705–13.CrossRefPubMedGoogle Scholar
  18. 18.
    Mueller S, Seitz HK, Rausch V. Non-invasive diagnosis of alcoholic liver disease. World J Gastroenterol. 2014;20(40):14626–41.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Boursier K, Konaté A, Gorea G. Reproducibility of liver stiffness measurement by ultrasonographic elastometry. Clin Gastroenterol Hepatol. 2008;6(11):1263–9.CrossRefPubMedGoogle Scholar
  20. 20.
    Castéra L et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology. 2005;128(2):343–50.CrossRefPubMedGoogle Scholar
  21. 21.
    Cichoz-Lach H. The BARD score and the NAFLD fibrosis score in the assessment of advanced liver fibrosis in nonalcoholic fatty liver disease. Med Sci Monit. 2012;18(12):735–40.CrossRefGoogle Scholar
  22. 22.
    Botros M, Sikaris KA. The De Ritis ratio: the test of time. Clin Biochem Rev. 2013;34(3):117–30.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Wai CT. A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology. 2003;38(2):518–26.CrossRefPubMedGoogle Scholar
  24. 24.
    R Core Team, A language and environment for statistical computing, R.C. Team, Editor 2015, R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  25. 25.
    Luger M et al. Prevalence of liver fibrosis and its association with non-invasive fibrosis and metabolic markers in morbidly obese patients with vitamin D deficiency. Obes Surg. 2016;Google Scholar
  26. 26.
    Hafeez S, Ahmed MH. Bariatric surgery as potential treatment for nonalcoholic fatty liver disease: a future treatment by choice or by chance? J Obes. 2013;Google Scholar
  27. 27.
    Mummadi RR 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
  28. 28.
    Fischer L et al. BariSurg trial: sleeve gastrectomy versus Roux-en-Y gastric bypass in obese patients with BMI 35–60 kg/m2—a multi-centre randomized patient and observer blind non-inferiority trial. BMC Surg. 2015;15(1):87.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Algooneh A et al. Non-alcoholic fatty liver disease resolution following sleeve gastrectomy. Surg Endosc. 2016;30(5):1983–7.CrossRefPubMedGoogle Scholar
  30. 30.
    Naveau S et al. The diagnostic accuracy of transient elastography for the diagnosis of liver fibrosis in bariatric surgery candidates with suspected NAFLD. Obes Surg. 2014;24(10):1693–701.CrossRefPubMedGoogle Scholar
  31. 31.
    Müller-Stich BP et al. Gastric bypass leads to improvement of diabetic neuropathy independent of glucose normalization—results of a prospective cohort study (DiaSurg 1 study). Ann Surg. 2013;258(5):760–5.CrossRefPubMedGoogle Scholar
  32. 32.
    Kenngott HG et al. DiaSurg 2 trial—surgical vs. medical treatment of insulin-dependent type 2 diabetes mellitus in patients with a body mass index between 26 and 35 kg/m2: study protocol of a randomized controlled multicenter trial—DRKS00004550. Trials. 2013;14(183)Google Scholar
  33. 33.
    Chalasani N et al. The diagnosis and management of nonalcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and American Gastroenterological Association. Hepatology. 2012;55(6):2005–23.CrossRefPubMedGoogle Scholar
  34. 34.
    Aguilar-Olivos NE et al. The role of bariatric surgery in the management of nonalcoholic fatty liver disease and metabolic syndrome. Metabolism. 2016;65(8):1196–207.CrossRefPubMedGoogle Scholar
  35. 35.
    Taitano A, Markow M, Finan J. Bariatric surgery improves histological features of nonalcoholic fatty liver disease and liver fibrosis. J Gastrointestinal Surg. 2015;19(3):429–37.CrossRefGoogle Scholar
  36. 36.
    Yoneda M et al. Transient elastography in patients with non-alcoholic fatty liver disease (NAFLD). Gut. 2007;56(9):1330–1.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Billeter AT 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(8):1867–74.CrossRefPubMedGoogle Scholar
  38. 38.
    Clark JM, Brancati FL, Diehl AM. The prevalence and etiology of elevated aminotransferase levels in the United States. Am J Gastroenterol. 2003;98(5):960–7.CrossRefPubMedGoogle Scholar
  39. 39.
    Torgerson JS et al. Are elevated aminotransferases and decreased bilirubin additional characteristics of the metabolic syndrome? Obes Res. 1997;5(2):105–14.CrossRefPubMedGoogle Scholar
  40. 40.
    Ekstedt M et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology. 2006;44(865–873)Google Scholar
  41. 41.
    Burza MA et al. Long-term effect of bariatric surgery on liver enzymes in the Swedish Obese Subjects (SOS) study. PLoS One. 2013;8(3)Google Scholar
  42. 42.
    Nascimento TM et al. Comparison of hepatic profile in pre and postoperative of bariatric surgery: private vs public network. Arg Bras Cir Dig. 2015;28(4):274–7.CrossRefGoogle Scholar
  43. 43.
    Giannini EG et al. A simple approach to noninvasively identifying significant fibrosis in chronic hepatitis C patients in clinical practice. J Clin Gastroenterol. 2006;40(6):521–7.CrossRefPubMedGoogle Scholar
  44. 44.
    Vallet-Pichard A et al. FIB-4: an inexpensive and accurate marker of fibrosis in HCV infection. Comparison with liver biopsy and fibrotest. Hepatology. 2007;46(1):32–6.CrossRefPubMedGoogle Scholar
  45. 45.
    Jeong WK et al. Principles and clinical application of ultrasound elastography for diffuse liver disease. Ultrasonography. 2014;33(3):149–60.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Foucher J et al. Prevalence of factors associated with failure liver stiffness measurement using Fibroscan in a prospective study of 2114 examinations. Eur J Gastroenterol Hepatol. 2006;18(4):411–2.CrossRefPubMedGoogle Scholar
  47. 47.
    Sandrin L, Fourquet B, Hasquenoph JM. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29(12):1705–13.CrossRefPubMedGoogle Scholar
  48. 48.
    Scott DR, Levy MT. Liver transient elastography (Fibroscan): a place in the management algorithms of chronic viral hepatitis. Antivir Ther. 2010;15(1):1–11.CrossRefPubMedGoogle Scholar
  49. 49.
    Wong GL et al. Assessment of fibrosis by transient elastography compared with liver biopsy and morphometry in chronic liver diseases. Clin Gastroenterol Hepatol. 2008;6(9):1027–35.CrossRefPubMedGoogle Scholar
  50. 50.
    Desai NK et al. Comparison of controlled attenuation parameter and liver biopsy to assess hepatic steatosis in pediatric patients. J Pediatr. 2016;173:160–3.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Pfeifer L et al. Prospective evaluation of acoustic radiation force impulse (ARFI) elastography and high-frequency B-mode ultrasound in compensated patients for the diagnosis of liver fibrosis/cirrhosis in comparison to mini-laparoscopic biopsy. Ultraschall Med. 2015;36(6):581–9.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Felix Nickel
    • 1
  • Christian Tapking
    • 1
  • Laura Benner
    • 3
  • Janina Sollors
    • 2
  • Adrian T. Billeter
    • 1
  • Hannes G. Kenngott
    • 1
  • Loay Bokhary
    • 1
  • Mathias Schmid
    • 1
  • Moritz von Frankenberg
    • 1
  • Lars Fischer
    • 1
  • Sebastian Mueller
    • 2
  • Beat P. Müller-Stich
    • 1
  1. 1.Department of General, Visceral and Transplant SurgeryUniversity of HeidelbergHeidelbergGermany
  2. 2.Department of Internal MedicineSalem HospitalHeidelbergGermany
  3. 3.Institute of Medical Biometry and InformaticsUniversity of HeidelbergHeidelbergGermany

Personalised recommendations