MRI-PDFF Assessment of Intrahepatic Fat Changes Post-Bariatric Surgery: A Systematic Literature Review
Abstract
1. Introduction
2. Materials and Methods
2.1. Eligibility Criteria
2.2. Search Strategy
2.3. Selection Process and Study Registration
2.4. Data Collection Process
2.5. Risk of Bias and Quality Assessment
3. Results
Study Selection and Study Characteristics
4. Discussion
4.1. Summary of Evidence
4.2. Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Pouwels, S.; Sakran, N.; Graham, Y.; Leal, A.; Pintar, T.; Yang, W.; Kassir, R.; Singhal, R.; Mahawar, K.; Ramnarain, D. Non-alcoholic fatty liver disease (NAFLD): A review of pathophysiology, clinical management and effects of weight loss. BMC Endocr. Disord. 2022, 22, 63. [Google Scholar] [CrossRef] [PubMed]
- Teng, M.L.; Ng, C.H.; Huang, D.Q.; Chan, K.E.; Tan, D.J.; Lim, W.H.; Yang, J.D.; Tan, E.; Muthiah, M.D. Global incidence and prevalence of nonalcoholic fatty liver disease. Clin. Mol. Hepatol. 2023, 29, S32–S42. [Google Scholar] [CrossRef] [PubMed]
- Maurice, J.; Manousou, P. Non-alcoholic fatty liver disease. Clin. Med. 2018, 18, 245–250. [Google Scholar] [CrossRef] [PubMed]
- Pierantonelli, I.; Svegliati-Baroni, G. Nonalcoholic Fatty Liver Disease: Basic Pathogenetic Mechanisms in the Progression From NAFLD to NASH. Transplantation 2019, 103, e1–e13. [Google Scholar] [CrossRef]
- Kasper, P.; Martin, A.; Lang, S.; Kütting, F.; Goeser, T.; Demir, M.; Steffen, H.M. NAFLD and cardiovascular diseases: A clinical review. Clin. Res. Cardiol. 2021, 110, 921–937. [Google Scholar] [CrossRef]
- Mantovani, A.; Scorletti, E.; Mosca, A.; Alisi, A.; Byrne, C.D.; Targher, G. Complications, morbidity and mortality of nonalcoholic fatty liver disease. Metabolism 2020, 111, 154170. [Google Scholar] [CrossRef]
- Ezzat, W.M. Impact of lifestyle interventions on pathogenesis of nonalcoholic fatty liver disease. World J. Gastroenterol. 2024, 30, 2633–2637. [Google Scholar] [CrossRef]
- Wolfe, B.M.; Kvach, E.; Eckel, R.H. Treatment of Obesity: Weight Loss and Bariatric Surgery. Circ. Res. 2016, 118, 1844–1855. [Google Scholar] [CrossRef]
- Ji, Y.; Lee, H.; Kaura, S.; Yip, J.; Sun, H.; Guan, L.; Han, W.; Ding, Y. Effect of Bariatric Surgery on Metabolic Diseases and Underlying Mechanisms. Biomolecules 2021, 11, 1582. [Google Scholar] [CrossRef]
- Murphy, R.; Plank, L.D.; Clarke, M.G.; Evennett, N.J.; Tan, J.; Kim, D.D.W.; Cutfield, R.; Booth, M.W.C. Effect of Banded Roux-en-Y Gastric Bypass Versus Sleeve Gastrectomy on Diabetes Remission at 5 Years Among Patients With Obesity and Type 2 Diabetes: A Blinded Randomized Clinical Trial. Diabetes Care 2022, 45, 1503–1511. [Google Scholar] [CrossRef]
- Głuszyńska, P.; Lemancewicz, D.; Dzięcioł, J.B.; Razak Hady, H. Non-Alcoholic Fatty Liver Disease (NAFLD) and Bariatric/Metabolic Surgery as Its Treatment Option: A Review. J. Clin. Med. 2021, 10, 5721. [Google Scholar] [CrossRef] [PubMed]
- Aminian, A.; Al-Kurd, A.; Wilson, R.; Bena, J.; Fayazzadeh, H.; Singh, T.; Albaugh, V.L.; Shariff, F.U.; Rodriguez, N.A.; Jin, J.; et al. Association of Bariatric Surgery With Major Adverse Liver and Cardiovascular Outcomes in Patients With Biopsy-Proven Nonalcoholic Steatohepatitis. JAMA 2021, 326, 2031–2042. [Google Scholar] [CrossRef] [PubMed]
- Ajmera, V.; Park, C.C.; Caussy, C.; Singh, S.; Hernandez, C.; Bettencourt, R.; Hooker, J.; Sy, E.; Behling, C.; Xu, R.; et al. Magnetic Resonance Imaging Proton Density Fat Fraction Associates with Progression of Fibrosis in Patients With Nonalcoholic Fatty Liver Disease. Gastroenterology 2018, 155, 307–310.e2. [Google Scholar] [CrossRef] [PubMed]
- Stine, J.G.; Munaganuru, N.; Barnard, A.; Wang, J.L.; Kaulback, K.; Argo, C.K.; Singh, S.; Fowler, K.J.; Sirlin, C.B.; Loomba, R. Change in MRI-PDFF and Histologic Response in Patients with Nonalcoholic Steatohepatitis: A Systematic Review and Meta-Analysis. Clin. Gastroenterol. Hepatol. 2021, 19, 2274–2283.e5. [Google Scholar] [CrossRef]
- Caussy, C.; Reeder, S.B.; Sirlin, C.B.; Loomba, R. Noninvasive, Quantitative Assessment of Liver Fat by MRI-PDFF as an Endpoint in NASH Trials. Hepatology 2018, 68, 763–772. [Google Scholar] [CrossRef]
- Rodge, G.A.; Goenka, M.K.; Goenka, U.; Afzalpurkar, S.; Shah, B.B. Quantification of Liver Fat by MRI-PDFF Imaging in Patients with Suspected Non-alcoholic Fatty Liver Disease and Its Correlation with Metabolic Syndrome, Liver Function Test and Ultrasonography. J. Clin. Exp. Hepatol. 2021, 11, 586–591. [Google Scholar] [CrossRef]
- Wu, F.Z.; Huang, Y.L.; Wu, C.C.; Wang, Y.C.; Pan, H.J.; Huang, C.K.; Yeh, L.R.; Wu, M.T. Differential Effects of Bariatric Surgery Versus Exercise on Excessive Visceral Fat Deposits. Medicine 2016, 95, e2616. [Google Scholar] [CrossRef]
- Xiang, A.H.; Martinez, M.P.; Trigo, E.; Utzschneider, K.M.; Cree-Green, M.; Arslanian, S.A.; Ehrmann, D.A.; Caprio, S.; Mohamed, P.H.I.H.; Hwang, D.H.; et al. Liver Fat Reduction After Gastric Banding and Associations with Changes in Insulin Sensitivity and β-Cell Function. Obesity 2021, 29, 1155–1163. [Google Scholar] [CrossRef]
- Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. Syst. Rev. 2021, 10, 89. [Google Scholar] [CrossRef]
- Stang, A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur. J. Epidemiol. 2010, 25, 603–605. [Google Scholar] [CrossRef]
- Folini, L.; Veronelli, A.; Benetti, A.; Pozzato, C.; Cappelletti, M.; Masci, E.; Micheletto, G.; Pontiroli, A.E. Liver steatosis (LS) evaluated through chemical-shift magnetic resonance imaging liver enzymes in morbid obesity; effect of weight loss obtained with intragastric balloon gastric banding. Acta Diabetol. 2014, 51, 361–368. [Google Scholar] [CrossRef] [PubMed]
- Hedderich, D.M.; Hasenberg, T.; Haneder, S.; Schoenberg, S.O.; Kücükoglu, Ö.; Canbay, A.; Otto, M. 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, 1755–1762. [Google Scholar] [CrossRef] [PubMed]
- Luo, R.B.; Suzuki, T.; Hooker, J.C.; Covarrubias, Y.; Schlein, A.; Liu, S.; Schwimmer, J.B.; Reeder, S.B.; Funk, L.M.; Greenberg, J.A.; et al. How bariatric surgery affects liver volume and fat density in NAFLD patients. Surg. Endosc. 2018, 32, 1675–1682. [Google Scholar] [CrossRef] [PubMed]
- Mamidipalli, A.; Fowler, K.J.; Hamilton, G.; Wolfson, T.; Covarrubias, Y.; Tran, C.; Fazeli, S.; Wiens, C.N.; McMillan, A.; Artz, N.S.; et al. Prospective comparison of longitudinal change in hepatic proton density fat fraction (PDFF) estimated by magnitude-based MRI (MRI-M) and complex-based MRI (MRI-C). Eur. Radiol. 2020, 30, 5120–5129. [Google Scholar] [CrossRef]
- Pooler, B.D.; Wiens, C.N.; McMillan, A.; Artz, N.S.; Schlein, A.; Covarrubias, Y.; Hooker, J.; Schwimmer, J.B.; Funk, L.M.; Campos, G.M.; et al. Monitoring Fatty Liver Disease with MRI Following Bariatric Surgery: A Prospective, Dual-Center Study. Radiology 2019, 290, 682–690. [Google Scholar] [CrossRef]
- Tan, H.C.; Shumbayawonda, E.; Beyer, C.; Cheng, L.T.; Low, A.; Lim, C.H.; Eng, A.; Chan, W.H.; Lee, P.C.; Tay, M.F.; et al. Multiparametric Magnetic Resonance Imaging and Magnetic Resonance Elastography to Evaluate the Early Effects of Bariatric Surgery on Nonalcoholic Fatty Liver Disease. Int. J. Biomed. Imaging 2023, 2023, 4228321. [Google Scholar] [CrossRef]
- Li, M.; Cao, D.; Liu, Y.; Jin, L.; Zeng, N.; Wang, L.; Zhao, K.; Lv, H.; Zhang, M.; Zhang, P.; et al. Alterations in the Liver Fat Fraction Features Examined by Magnetic Resonance Imaging Following Bariatric Surgery: A Self-Controlled Observational Study. Obes. Surg. 2020, 30, 1917–1928. [Google Scholar] [CrossRef]
- Syväri, J.; Junker, D.; Patzelt, L.; Kappo, K.; Al Sadat, L.; Erfanian, S.; Makowski, M.R.; Hauner, H.; Karampinos, D.C. Longitudinal changes on liver proton density fat fraction differ between liver segments. Quant. Imaging Med. Surg. 2021, 11, 1701–1709. [Google Scholar] [CrossRef]
- Fazeli Dehkordy, S.; Fowler, K.J.; Mamidipalli, A.; Wolfson, T.; Hong, C.W.; Covarrubias, Y.; Hooker, J.C.; Sy, E.Z.; Schlein, A.N.; Cui, J.Y.; et al. Hepatic steatosis and reduction in steatosis following bariatric weight loss surgery differs between segments and lobes. Eur. Radiol. 2019, 29, 2474–2480. [Google Scholar] [CrossRef]
- Bai, J.; Wang, S.; Pan, H.; Shi, Z.; Zhao, M.; Yue, X.; Yang, K.; Zhang, X.; Wang, W.; Liu, C.; et al. Correlation analysis of dynamic changes of abdominal fat during rapid weight loss after bariatric surgery: A prospective magnetic resonance imaging study. Eur. J. Radiol. 2024, 178, 111630. [Google Scholar] [CrossRef]
- Allen, A.M.; Shah, V.H.; Therneau, T.M.; Venkatesh, S.K.; Mounajjed, T.; Larson, J.J.; Mara, K.C.; Kellogg, T.A.; Kendrick, M.L.; McKenzie, T.J.; et al. Multiparametric Magnetic Resonance Elastography Improves the Detection of NASH Regression Following Bariatric Surgery. Hepatol. Commun. 2019, 4, 185–192. [Google Scholar] [CrossRef] [PubMed]
- Sun, J.; Lv, H.; Li, M.; Zhao, L.; Liu, Y.; Zeng, N.; Wei, X.; Chen, Q.; Ren, P.; Liu, Y.; et al. How much abdominal fat do obese patients lose short term after laparoscopic sleeve gastrectomy? A quantitative study evaluated with MRI. Quant. Imaging Med. Surg. 2021, 11, 4569–4582. [Google Scholar] [CrossRef] [PubMed]
- Loy, J.J.; Youn, H.A.; Schwack, B.; Kurian, M.; Ren Fielding, C.; Fielding, G.A. Improvement in nonalcoholic fatty liver disease and metabolic syndrome in adolescents undergoing bariatric surgery. Surg. Obes. Relat. Dis. 2015, 11, 442–449. [Google Scholar] [CrossRef]
- Nixdorf, L.; Hartl, L.; Ströhl, S.; Felsenreich, D.M.; Mairinger, M.; Jedamzik, J.; Richwien, P.; Mozayani, B.; Semmler, G.; Balcar, L.; et al. Rapid improvement of hepatic steatosis and liver stiffness after metabolic/bariatric surgery: A prospective study. Sci. Rep. 2024, 14, 17558. [Google Scholar] [CrossRef]
- Fakhry, T.K.; Mhaskar, R.; Schwitalla, T.; Muradova, E.; Gonzalvo, J.P.; Murr, M.M. Bariatric surgery improves nonalcoholic fatty liver disease: A contemporary systematic review and meta-analysis. Surg. Obes. Relat. Dis. 2019, 15, 502–511. [Google Scholar] [CrossRef]
- Kim, K.H.; Kim, Y.; Seo, K.I.; Seo, K.W. Short-term outcome of bariatric surgery on nonalcoholic fatty liver disease: A Korean perspective. Ann. Surg. Treat. Res. 2022, 102, 353–359. [Google Scholar] [CrossRef]
- Ruiz-Tovar, J.; Llavero, C.; Rodriguez-Ortega, M.; De Castro, N.M.; Martín-Crespo, M.C.; Escobar-Aguilar, G.; Martin-Nieto, A.; Gonzalez, G. Improvement of Metabolic-Associated Fatty Liver Disease by Magnetic Resonance Spectroscopy in Morbidly Obese Women Undergoing Roux-en-Y Gastric Bypass, following a Postoperative Mediterranean-like Diet. Nutrients 2024, 16, 2280. [Google Scholar] [CrossRef]
- Kirkpatrick, K.; Paull-Forney, B.; Okut, H.; Schwasinger-Schmidt, T. Bariatric Metabolic Surgery Reduced Liver Enzyme Levels in Patients with Non-Alcohol Fatty Liver Disease. Kans. J. Med. 2021, 14, 209–214. [Google Scholar] [CrossRef]
- Głuszyńska, P.; Łukaszewicz, A.; Diemieszczyk, I.; Chilmończyk, J.; Reszeć, J.; Citko, A.; Szczerbiński, Ł.; Krętowski, A.; Razak Hady, H. The Effect of Laparoscopic Sleeve Gastrectomy on the Course of Non-Alcoholic Fatty Liver Disease in Morbidly Obese Patients during One Year of Follow Up. J. Clin. Med. 2023, 12, 4122. [Google Scholar] [CrossRef]
- Verrastro, O.; Panunzi, S.; Castagneto-Gissey, L.; De Gaetano, A.; Lembo, E.; Capristo, E.; Guidone, C.; Angelini, G.; Pennestrì, F.; Sessa, L.; et al. Bariatric-metabolic surgery versus lifestyle intervention plus best medical care in non-alcoholic steatohepatitis (BRAVES): A multicentre, open-label, randomised trial. Lancet 2023, 401, 1786–1797. [Google Scholar] [CrossRef]
Study No. | Author(s) | Country | Year | Sample Size (n) | Types of Bariatric Surgery | Follow-Up Duration | Quality Score (NOS) |
---|---|---|---|---|---|---|---|
1 | Folini et al. [21] | Italy | 2013 | 40 | LAGB/BIB/Diet | 6 months | 7 |
2 | Hedderich et al. [22] | Germany | 2017 | 19 | LSG/LRYGB | 6 months | 8 |
3 | Luo et al. [23] | USA | 2018 | 49 | LSG/LRYGB/LAGB | 6 months | 8 |
4 | Mamidipalli et al. [24] | USA | 2020 | 54 | LSG/LRYGB | 6 months | 8 |
5 | Pooler et al. [25] | USA | 2019 | 50 | LSG/LRYGB/LAGB | 6 months | 8 |
6 | Tan et al. [26] | Singapore | 2023 | 9 | LSG | 6 months | 6 |
7 | Li et al. [27] | China | 2020 | 69 | LSG/LRYGB | 3 months | 7 |
8 | Syväri et al. [28] | Germany | 2021 | 32 | Lifestyle Intervention | 1 year | 7 |
9 | Fazeli Dehkordy et al. [29] | USA | 2018 | 118 | VLCD + WLS | Up to 6 months | 9 |
10 | Bai et al. [30] | China | 2023 | 44 | LSG | 6 months | 7 |
11 | Allen et al. [31] | USA | 2019 | 38 | Bariatric Surgery | 1 year | 8 |
12 | Sun et al. [32] | China | 2021 | 91 | LSG | ~100 days | 7 |
Study | Mean Age (Years) | Gender (M/F) | Baseline BMI (kg/m²) | Delta BMI (kg/m²) |
---|---|---|---|---|
Folini et al. [21] | 43.6 ± 12.2 | 2/16 | 43.8 ± 6.62 | −5.6 |
Hedderich et al. [22] | 41.4 ± 12.5 | 4/15 | 44.1 ± 5.2 | −10.3 |
Luo et al. [23] | 50.9 ± 10.8 | 7/42 | 45.3 ± 5.9 | −10.9 |
Mamidipalli et al. [24] | 52 ± 12 | 10/44 | 42.3 ± 5.0 | −8 |
Pooler et al. [25] | 51.0 ± 11.2 | 7/43 | 44.9 ± 6.5 | −10.4 |
Tan et al. [26] | 45.1 ± 9.0 | 5/4 | 39.7 ± 5.3 | −7.3 |
Li et al. [27] | 32 ± 8.67 | 14/55 | 37.92 ± 6.58 | −8.05 |
Syväri et al. [28] | 54.3 | 14/18 | Not specified | Variable |
Fazeli Dehkordy et al. [29] | 48.0 ± 13.0 | 16/102 | 43.4 ± 6.2 | Not specified |
Bai et al. [30] | Not specified | Not specified | 38.91 ± 5.29 | −11.02 |
Allen et al. [31] | 50 (Median) | 5/33 | 44.6 | −12.2 |
Sun et al. [32] | Not specified | 18/73 | 38.4 | −8.1 |
Study | Weight Loss (%) | Excess Weight Loss (%) | Delta Weight (kg) |
---|---|---|---|
Folini et al. [21] | Significant (p = 0.001) | Not reported | −14.1 |
Hedderich et al. [22] | 24.5 ± 6.3% | 58.7 ± 19.7% | −32.5 |
Luo et al. [23] | Significant (p < 0.001) | 55.6 ± 19.0% | −31.7 |
Mamidipalli et al. [24] | Not reported | Not reported | −24.3 |
Pooler et al. [25] | 24.6% weight loss | Not reported | −34.6 |
Tan et al. [26] | 18.2% weight loss | Not reported | −19.4 |
Li et al. [27] | 21.3% weight loss | Not reported | −22.7 |
Syväri et al. [28] | Variable weight change | Not applicable | −1.2 to +1.4 |
Fazeli Dehkordy et al. [29] | Not specified | Not specified | Not specified |
Bai et al. [30] | Significant decrease | Not specified | −26.67 |
Allen et al. [31] | Not specified | Not specified | Not specified |
Sun et al. [32] | Median weight loss of 23.1 kg | EWL: 58.7% | −23.1 |
Study | Baseline MRI-PDFF (%) | Follow-Up MRI-PDFF (%) | Delta MRI-PDFF (%) |
---|---|---|---|
Folini et al. [21] | 16.7 ± 10.91 | 7.6 ± 9.76 | −9.1 |
Hedderich et al. [22] | 10.1 ± 9.7 | 3.2 ± 2.2 | −6.9 |
Luo et al. [23] | 16.6 ± 7.8 | 4.4 ± 3.4 | −12.2 |
Mamidipalli et al. [24] | 16.6 ± 7.2 | 5.6 ± 3.7 | −11 |
Pooler et al. [25] | 18.1 ± 8.6 | 4.9 ± 3.4 | −13.2 |
Tan et al. [26] | 14.1 ± 7.4 | 4.9 ± 2.2 | −9.2 |
Li et al. [27] | 14.64 ± 9.02 | 5.74 ± 5.04 | −8.9 |
Syväri et al. [28] | 9.8 ± 9.7 | 10.2 ± 9.5 | 0.4 |
Fazeli Dehkordy et al. [29] | 13.6% (right lobe) | 4.20% | −9.4 |
Bai et al. [30] | 16.90 ± 9.45 | 2.91 ± 2.57 | −14 |
Allen et al. [31] | 10.0 (median) | 2.7 (median) | −7.3 |
Sun et al. [32] | 13.60 (median) | 3.44 (median) | −10.16 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Published by MDPI on behalf of the Lithuanian University of Health Sciences. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Dejeu, D.; Dejeu, P.; Muresan, A.; Bradea, P.; Dejeu, V. MRI-PDFF Assessment of Intrahepatic Fat Changes Post-Bariatric Surgery: A Systematic Literature Review. Medicina 2024, 60, 2003. https://doi.org/10.3390/medicina60122003
Dejeu D, Dejeu P, Muresan A, Bradea P, Dejeu V. MRI-PDFF Assessment of Intrahepatic Fat Changes Post-Bariatric Surgery: A Systematic Literature Review. Medicina. 2024; 60(12):2003. https://doi.org/10.3390/medicina60122003
Chicago/Turabian StyleDejeu, Danut, Paula Dejeu, Anita Muresan, Paula Bradea, and Viorel Dejeu. 2024. "MRI-PDFF Assessment of Intrahepatic Fat Changes Post-Bariatric Surgery: A Systematic Literature Review" Medicina 60, no. 12: 2003. https://doi.org/10.3390/medicina60122003
APA StyleDejeu, D., Dejeu, P., Muresan, A., Bradea, P., & Dejeu, V. (2024). MRI-PDFF Assessment of Intrahepatic Fat Changes Post-Bariatric Surgery: A Systematic Literature Review. Medicina, 60(12), 2003. https://doi.org/10.3390/medicina60122003