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Alterations in the Liver Fat Fraction Features Examined by Magnetic Resonance Imaging Following Bariatric Surgery: a Self-Controlled Observational Study

  • Mengyi Li
  • Di Cao
  • Yang Liu
  • Lan Jin
  • Na Zeng
  • Lixue Wang
  • Kaixin Zhao
  • Han Lv
  • Meng Zhang
  • Peng Zhang
  • Zhenghan YangEmail author
  • Zhongtao ZhangEmail author
Original Contributions
  • 10 Downloads

Abstract

Background

Obesity is a worldwide epidemic leading to non-alcoholic fatty liver disease. Alterations in the liver fat fraction (LFF) assessed by MRI following bariatric surgery is a promising feature; however, few studies have been fully elucidated.

Purpose

To determine the alterations in the LFF features following surgery using MRI, to determine the correlation with the clinical non-alcoholic steatohepatitis score (C-NASH score), and to identify the predictive factors for postoperative score changes.

Methods

Patients (n = 69) underwent MRI to measure the LFF at baseline and 3 months postoperatively. Paired sample t tests were applied to investigate the alterations in the major parameters. Univariate analyses were performed to evaluate the factors predicting C-NASH score changes after surgery.

Results

Compared with the baseline levels, the LFF significantly decreased 3 months postoperatively (P < 0.001). Significant positive correlations were detected between the C-NASH score and LFF levels (P < 0.001). Among the ROC curves for C-NASH score change, the AUC for the ROC curve of LFF was 0.812 (95% CI 0.707, 0.916) and the cut-off value was 6.16%. Weight at baseline was a significant predictive factor for postoperative changes when the C-NASH score was ≥ 3 (P < 0.001). The AUC for the ROC curve of weight was 0.897 (95% CI 0.782, 1.000) and 117 kg was the cut-off value.

Conclusions

LFF decreased following bariatric surgery, which predicted C-NASH score changes after surgery. For patients with a higher risk of NASH (score ≥ 3) at baseline and lower preoperative body weight, we noted significantly greater effects of surgery on score change value.

Keywords

Bariatric surgery Liver fat fraction Magnetic resonance imaging C-NASH score 

Notes

Acknowledgments

The authors would like to thank all of the involved study investigators, staffs, clinicians, nurses, and technicians for dedicating their time and skills to the completion of this study.

Funding Information

This study was supported by National Key Technologies R&D Program (Grant No. 2015BAI13B09), National Key Technologies R&D Program of China (No. 2017YFC0110904), Research Foundation of Beijing Friendship Hospital, Capital Medical University (Grant No. yyqdkt 2017-31), and Beijing Municipal Administration of Hospitals Incubating Program (Grant No. PX2018001).

Compliance with Ethical Standards

Conflict of Interests

The authors declare that they have no conflict of interest.

Statement of Informed Consent

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

Statement of Human and Animal Rights

This study was performed in accordance with the principles of the Declaration of Helsinki and was approved by the Ethics Committees of Beijing Friendship Hospital, Capital Medical University.

References

  1. 1.
    Collaboration, N.C.D.R.F. Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet. 2016;387(10026):1377–96.CrossRefGoogle Scholar
  2. 2.
    Younossi ZM, Koenig AB, Abdelatif D, et al. Global epidemiology of nonalcoholic fatty liver disease-meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016;64(1):73–84.PubMedCrossRefGoogle Scholar
  3. 3.
    Portillo-Sanchez P, Bril F, Maximos M, et al. High prevalence of nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus and normal plasma aminotransferase levels. J Clin Endocrinol Metab. 2015;100(6):2231–8.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Schwenzer NF, Springer F, Schraml C, et al. Non-invasive assessment and quantification of liver steatosis by ultrasound, computed tomography and magnetic resonance. J Hepatol. 2009;51(3):433–45.PubMedCrossRefGoogle Scholar
  5. 5.
    Reeder SB et al. Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging. 2011;34(4):spcone.CrossRefGoogle Scholar
  6. 6.
    Noworolski SM, Lam MM, Merriman RB, et al. Liver steatosis: concordance of MR imaging and MR spectroscopic data with histologic grade. Radiology. 2012;264(1):88–96.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Idilman IS, Aniktar H, Idilman R, et al. Hepatic steatosis: quantification by proton density fat fraction with MR imaging versus liver biopsy. Radiology. 2013;267(3):767–75.PubMedCrossRefGoogle Scholar
  8. 8.
    Tang A, Tan J, Sun M, et al. Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology. 2013;267(2):422–31.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Consultation WHOE. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363(9403):157–63.CrossRefGoogle Scholar
  10. 10.
    Tai CM et al. Derivation and validation of a scoring system for predicting nonalcoholic steatohepatitis in Taiwanese patients with severe obesity. Surg Obes Relat Dis. 2017;13(4):686–92.PubMedCrossRefGoogle Scholar
  11. 11.
    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(7):1755–62.PubMedCrossRefGoogle Scholar
  12. 12.
    Pooler BD, Wiens CN, McMillan A, et al. Monitoring fatty liver disease with MRI following bariatric surgery: a prospective, dual-center study. Radiology. 2019;290(3):682–90.PubMedCrossRefGoogle Scholar
  13. 13.
    Steven S, Hollingsworth KG, Small PK, et al. Calorie restriction and not glucagon-like peptide-1 explains the acute improvement in glucose control after gastric bypass in type 2 diabetes. Diabet Med. 2016;33(12):1723–31.PubMedCrossRefGoogle Scholar
  14. 14.
    Jorgensen NB et al. Exaggerated glucagon-like peptide 1 response is important for improved beta-cell function and glucose tolerance after Roux-en-Y gastric bypass in patients with type 2 diabetes. Diabetes. 2013;62(9):3044–52.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Romero F, Nicolau J, Flores L, et al. Comparable early changes in gastrointestinal hormones after sleeve gastrectomy and Roux-en-Y gastric bypass surgery for morbidly obese type 2 diabetic subjects. Surg Endosc. 2012;26(8):2231–9.PubMedCrossRefGoogle Scholar
  16. 16.
    Dirksen C, Bojsen-Møller KN, Jørgensen NB, et al. Exaggerated release and preserved insulinotropic action of glucagon-like peptide-1 underlie insulin hypersecretion in glucose-tolerant individuals after Roux-en-Y gastric bypass. Diabetologia. 2013;56(12):2679–87.PubMedCrossRefGoogle Scholar
  17. 17.
    Svegliati-Baroni G, Saccomanno S, Rychlicki C, et al. Glucagon-like peptide-1 receptor activation stimulates hepatic lipid oxidation and restores hepatic signalling alteration induced by a high-fat diet in nonalcoholic steatohepatitis. Liver Int. 2011;31(9):1285–97.PubMedCrossRefGoogle Scholar
  18. 18.
    Kim YO, Schuppan D. When GLP-1 hits the liver: a novel approach for insulin resistance and NASH. Am J Physiol Gastrointest Liver Physiol. 2012;302(8):G759–61.PubMedCrossRefGoogle Scholar
  19. 19.
    Sharma S, Mells JE, Fu PP, et al. GLP-1 analogs reduce hepatocyte steatosis and improve survival by enhancing the unfolded protein response and promoting macroautophagy. PLoS One. 2011;6(9):e25269.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Bojsen-Moller KN et al. Early enhancements of hepatic and later of peripheral insulin sensitivity combined with increased postprandial insulin secretion contribute to improved glycemic control after Roux-en-Y gastric bypass. Diabetes. 2014;63(5):1725–37.PubMedCrossRefGoogle Scholar
  21. 21.
    Jorgensen NB et al. Acute and long-term effects of Roux-en-Y gastric bypass on glucose metabolism in subjects with type 2 diabetes and normal glucose tolerance. Am J Physiol Endocrinol Metab. 2012;303(1):E122–31.PubMedCrossRefGoogle Scholar
  22. 22.
    Lassailly G, Caïazzo R, Pattou F, et al. Bariatric surgery for curing NASH in the morbidly obese? J Hepatol. 2013;58(6):1249–51.PubMedCrossRefGoogle Scholar
  23. 23.
    Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med. 2001;344(7):495–500.CrossRefGoogle Scholar
  24. 24.
    Ratziu V, Charlotte F, Heurtier A, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128(7):1898–906.PubMedCrossRefGoogle Scholar
  25. 25.
    Gholam PM, Flancbaum L, Machan JT, et al. Nonalcoholic fatty liver disease in severely obese subjects. Am J Gastroenterol. 2007;102(2):399–408.PubMedCrossRefGoogle Scholar
  26. 26.
    Campos GM, Bambha K, Vittinghoff E, et al. A clinical scoring system for predicting nonalcoholic steatohepatitis in morbidly obese patients. Hepatology. 2008;47(6):1916–23.PubMedCrossRefGoogle Scholar
  27. 27.
    Anty R, Iannelli A, Patouraux S, et al. A new composite model including metabolic syndrome, alanine aminotransferase and cytokeratin-18 for the diagnosis of non-alcoholic steatohepatitis in morbidly obese patients. Aliment Pharmacol Ther. 2010;32(11–12):1315–22.PubMedCrossRefGoogle Scholar
  28. 28.
    Ulitsky A, Ananthakrishnan AN, Komorowski R, et al. A noninvasive clinical scoring model predicts risk of nonalcoholic steatohepatitis in morbidly obese patients. Obes Surg. 2010;20(6):685–91.PubMedCrossRefGoogle Scholar
  29. 29.
    Pulzi FB, Cisternas R, Melo MR, et al. New clinical score to diagnose nonalcoholic steatohepatitis in obese patients. Diabetol Metab Syndr. 2011;3(1):3.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Tan CH, al-Kalifah N, Ser KH, et al. Long-term effect of bariatric surgery on resolution of nonalcoholic steatohepatitis (NASH): an external validation and application of a clinical NASH score. Surg Obes Relat Dis. 2018;14(10):1600–6.PubMedCrossRefGoogle Scholar
  31. 31.
    Tang A, Desai A, Hamilton G, et al. Accuracy of MR imaging-estimated proton density fat fraction for classification of dichotomized histologic steatosis grades in nonalcoholic fatty liver disease. Radiology. 2015;274(2):416–25.PubMedCrossRefGoogle Scholar
  32. 32.
    Permutt Z, le TA, Peterson MR, et al. Correlation between liver histology and novel magnetic resonance imaging in adult patients with non-alcoholic fatty liver disease - MRI accurately quantifies hepatic steatosis in NAFLD. Aliment Pharmacol Ther. 2012;36(1):22–9.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    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(1):328–57.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Garg H, Aggarwal S, Shalimar, 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(1):81–91.PubMedCrossRefGoogle Scholar
  35. 35.
    Caiazzo R 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 898-9PubMedCrossRefGoogle Scholar
  36. 36.
    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(6):1315–22.PubMedCrossRefGoogle Scholar
  37. 37.
    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.PubMedCrossRefGoogle Scholar
  38. 38.
    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.PubMedCrossRefGoogle Scholar
  39. 39.
    O’Kane M, Parretti HM, Hughes CA, et al. Guidelines for the follow-up of patients undergoing bariatric surgery. Clin Obes. 2016;6(3):210–24.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Department of General Surgery, Beijing Friendship HospitalCapital Medical University & National Clinical Research Center for Digestive DiseasesBeijingChina
  2. 2.Department of Radiology, Beijing Friendship HospitalCapital Medical UniversityBeijingChina
  3. 3.National Clinical Research Center for Digestive Diseases, Beijing Friendship HospitalCapital Medical UniversityBeijingChina

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