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Background:
Systematic Review

Effectiveness of Bariatric Surgeries for Metabolic Dysfunction-Associated Steatotic Liver Disease: A Systematic Review and Meta-Analysis

by
Abdullah Sulaiman AlRumaih
*,
Lama Abdullah Alzelfawi
,
Ghadah Khalid Alotaibi
,
Osamah AbdulAziz Aldayel
,
Abdulrahman Khazzam AlMutairi
,
Rosana Tariq Alnowaimi
,
Mubarak Mohammed Alshahrani
,
Rifal Sami Alsharif
and
Sarah Nabil Almadani
Adiriyah Hospital, Riyadh 11461, Saudi Arabia
*
Author to whom correspondence should be addressed.
Surgeries 2024, 5(3), 486-498; https://doi.org/10.3390/surgeries5030040
Submission received: 23 April 2024 / Revised: 1 June 2024 / Accepted: 12 June 2024 / Published: 27 June 2024
(This article belongs to the Special Issue Laparoscopic Surgery)
Browse Figures
Review Reports Versions Notes

Abstract

:
Metabolic dysfunction-associated steatotic liver disease (MASLD) is the most common liver disease worldwide and simultaneously the most common indication for liver transplants in Western countries This study aims to evaluate the effectiveness of laparoscopic sleeve gastrectomy (LSG) or Roux-en-Y gastric bypass (RYGB) on MDASLD histologically and biochemically. 14 studies met our criteria with a total population of 1942 who underwent LSG or RYGB 1–14. The Newcastle-Ottawa Scale (NOS) was used for quality evaluation of the included studies. Results: Both surgeries were effective in decreasing laboratory biomarkers like ALP, GGT, AST, and ALT with non-significant superiority of LSG over RYGB which did not significantly improve the AST level after one year. LSG showed more decrease in ALT levels (MD = −17.56, 95% CI = (−23.04, −12.089), p 0.001) and LSG was associated with increased change in NAS score with slight superiority. Both LSG and RYBG improve NAD and NASH outcomes after one and 10 years of surgery. However, randomized clinical trials with large samples are needed to confirm these results.

1. Introduction

Metabolic dysfunction-associated steatotic liver disease (MASLD) is the most common liver disease worldwide and the most common indication for liver transplants in Western countries [1]. The main risk factor for NAFLD is obesity, which affects more than 80% of patients at the time of diagnosis [2].
Bariatric surgery has proven to be effective in improving metabolic dysfunction and related steatohepatitis and fibrosis. Guidelines currently consider bariatric surgery a treatment option in non-cirrhotic MASLD/MASH patients who meet the criteria for metabolic weight loss surgery [3]. Many systematic reviews demonstrate that performing bariatric surgery in severely obese patients with compensated cirrhosis is safe and effective [4,5]. Therefore, this study aims to evaluate the effectiveness of bariatric surgeries against MASLD histologically and biochemically.

2. Materials and Methods

2.1. Literature Search Strategy

This systematic review and meta-analysis was conducted in adherence to the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) [6] guidelines and registered under the International Prospective Register of Systematic Reviews (PROSPERO) with the registration number CRD42024505841. An electronic search through diffirent databases PubMed, ScienceDirect, Google Scholar, and Web of Science only for studies published in the ten years from January 2013 to December 2023.
The general search string used in all searches was as follows: (non-alcoholic fatty liver disease) OR (nonalcoholic fatty liver disease) OR (NAFLD) OR (steatosis) OR (steatohepatitis) OR (liver cirrhosis) AND (bariatric surgery) OR (metabolic surgery) OR (weight loss surgery) OR (gastric bypass) OR (sleeve gastrectomy). The search terms were identified in the title, abstract, or medical subject heading.

2.2. Inclusion and Exclusion Criteria

This systematic review included case–control studies, cross-sectional studies, retrospective cohort studies, and prospective cohort studies that were published in the English language from January 2013 to December 2023 and included both males and females, over 14 years old, who underwent any bariatric surgery such as gastric bypass or sleeve gastrectomy. The outcome to measure in this study were the histologic improvement of MASLD as reflected by the NAFLD activity score (NAS), presence of steatohepatitis, presence of fibrosis, and fibrosis stage and the biochemical response as measured by laboratory values of aspartate aminotransferase (AST), alanine transaminase (ALT), alkaline phosphatase (ALP), and gamma-glutamyl transferase (GGT). Exclusion criteria included animal studies, studies not available in English, case reports, editorials, systemic reviews, letters, and meta-analyses. Pediatrics, geriatrics populations, and interventions other than bariatric surgeries were excluded.

2.3. Selection of Articles and Data Extraction

Four independent authors (R.A., M.A., O.A., and R.A.) screened the articles using Rayyan based on the titles and abstracts [7]. Rayyan also was used to eliminate duplicate articles. The full-text screening of all the included studies was carried out by two independent authors (G.A. and A.A.). Disagreements that arose during the screening process were resolved by L.A. All authors manually and independently extracted the data, which included study information (author, country, year of publication, study design, number of patients), demographic data (age, mean ± SD/median [range], gender), and outcomes (NAS score, presence of steatohepatitis, presence of fibrosis, fibrosis stage, biochemical response).

2.4. Quality Assessment

The Newcastle–Ottawa Scale (NOS) for non-randomized studies was used for the quality evaluation of the included studies [8]. Most of the included primary observational studies in the current review were considered to be of good quality except Elyasinia et al., 2021 which was considered to be of fair quality because they used an ultrasonographic assessment for non-alcoholic steatohepatitis without mentioning the validity assessment of the adopted grading system. In contrast, the other included studies used either a histopathology-based grading system or a validated ultrasonographic evaluation. The quality of the studies was scored using the Newcastle–Ottawa Scale as shown in Table 1.

2.5. Data Analysis

Data were analyzed with the OpenMetaAnalyst for Windows 8 (64-bit) (built 4 June 2015) [23]. We calculated the changes in laboratory and clinical parameters following the formula presented in the Cochrane Handbook for Systematic Reviews and Meta-analysis [24]. We used mean difference and 95% confidence interval in the analysis and the results were considered significant when p values were less than 0.05. The heterogeneity was assessed using the Cochrane Q test and the I2 statistical test, and the results were considered heterogeneous when the p value was less than 0.1 and I2 was greater than 50%. We used the random-effects model in conducting the meta-analyses because of the presence of a heterogenous population in the included studies, as most of them included both NAFLD and NASH patients without performing subgroup analysis. We tried to resolve the heterogeneity using sensitivity analysis or subgroup analysis; however, we could not perform subgroup analysis because of the limited number of included studies and the fact that the included studies did not present separate data for NAFLD and NASH patients.

3. Results

3.1. Literature Search Results

The database literature search resulted in 318 records; from them, 28 were removed as duplicates. We performed title and abstract screening on 289 records, and only 14 articles were eligible for the full-text screening phase, which resulted in 14 articles that were eligible for qualitative reporting and meta-analysis. Figure 1 shows the full details.

3.2. Baseline and Demographic Characteristics

We included 14 studies with a total population of 1942 individuals who underwent laparoscopic sleeve gastrectomy (LSG) or Roux-en-Y gastric bypass (RYGB). Nine studies were prospective cohort studies, while the rest were retrospective. The full details of age, sample size, country, intervention, gender, and baseline data of studies’ outcomes are described in Table 2 and Table 3.

3.3. Laboratory Outcomes

We assessed four biomarkers: alkaline phosphatase (ALP), aspartate aminotransferase (AST), alanine aminotransferase (ALT), and gamma-glutamyl transferase (GGT).
ALP has only been assessed pre- and postoperatively in Esquivel et al., 2018 [19] and they found that its level was significantly decreased after laparoscopic SG from 36 ± 18 (U/L) at baseline to 19 ± 9 after one year, p < 0.0001.
Regarding gamma-glutamyl transferase, it was assessed in LSG in only four studies; therefore, we could not perform a comparison with RYGB [12,16,21,22]. The pooled analysis showed that LSG significantly decreased the GGT after one year (MD = −13.064, 95% CI = (−14.677, −11.45), p < 0.001).
Figure 2 shows the full details of the pooled analysis of GGT change one year after LSG.
Regarding ALT changes, both surgeries were effective in decreasing its level after one year (p < 0.001), and LSG showed a greater decrease in ALT levels (MD = −17.56, 95% CI = (−23.04, −12.089), p < 0.001) than RYGB (MD = −10.621, 95% CI = (−19.99, −1.24), p < 0.001); however, this superiority of LSG over RYGB was not statistically significant (p = 0.249), Figure 3 shows the full details.
Meanwhile, regarding AST changes, LSG significantly decreased its level after one year (MD = −9.368, 95% CI = (−13.86, −4.86), p < 0.001), while RYGB did not significantly decrease its level (MD = −5.763, 95% CI = (−18.125, 6.59), p = 0.361); however, this superiority was also not statistically significant (p = 0.732). Figure 4 shows the full details.
The meta-analyses of both AST and ALT changes were heterogeneous; however, we could not resolve the heterogeneity by the leave-one-out method or subgroup analysis.

3.4. Clinical Outcomes

3.4.1. BMI Change

Both surgical procedures were effective in reducing BMI after one year (LSG MD = −11.578, 95% CI = (−12.982, −10.173), p < 0.001; RYGB MD = −10.509, 95% CI = (−15.516, −5.502), p < 0.001); therefore, the p value for subgroup difference was 0.807. The outcome was heterogeneous, and we could not resolve it by the leave-one-out method or by performing subgroup analysis. Figure 5 shows the full details.

3.4.2. NAS Score Change

Only two studies reported the NAS score one year after surgery, and by comparing both surgeries [13,17], we found that LSG was associated with increased change in NAS score (MD = −2.558, 95% CI = (−3.065, −2.051), p < 0.001) compared to RYGB (MD = 1.14, 95% CI = (−6.7, 8.98)). The analysis was homogeneous (I2 = 0%, p = 0.45). Figure 6 shows the full details.

3.4.3. Fibrosis

The analysis on NAFLD fibrosis score which was reported pre- and postoperatively in only three studies after one year [9,20,21] and both surgeries significantly decreased it with slight superiority of LSG (MD = −1.236, 95% CI = (−1.66, −0.801), p < 0.001) compared to RYGB (MD = −0.881, 95% CI = (−1.178, −0.585), p < 0.001); however, the difference between both options was not significant (p = 0.165). Additionally, Agrawal et al. [17] found no significant difference between LSG and RYGB in patients who experience worsening in their fibrosis degrees 17.1% and 11.1%, respectively, p = 0.75.
Additionally, Yeo et al., 2019 [18] found no significant difference between (LSG + Laparoscopic adjustable gastric banding) and RYGB in NAFLD fibrosis scores after six months and one year p = 0.205 and 0.119, respectively. Pedersen et al., 2021 [13] found that both surgeries did not significantly improve the Kleiner Fibrosis score and no significant differences were observed between both procedures. Additionally, Netanel et al., 2020 [15] found that LSG did not improve Fibro Test scores after one year (p = 0.061).

4. Discussion

Our systematic review and meta-analysis revealed that both surgeries effectively decreased laboratory biomarkers such as ALP, GGT, AST, and ALT, with nonsignificant superiority of LSG over RYGB, which did not significantly improve the AST level after one year. Additionally, this review found no significant difference between BMI and fibrosis between both procedures; however, LSG significantly improved the NAS score while RYGB did not.
This systematic review has compared the levels of laboratory biomarkers such as ALT, AST, GGT, and ALP in both groups as an improvement of MASLD after surgeries, as another study has proven that bariatric surgeries are effective in decreasing ALT and AST levels after two and ten years of surgery compared to only medical treatment [25]. Despite these laboratory tests having low specificity and sensitivity, they can be used beside imaging and scoring systems in evaluating NAFLD activity instead of biopsy, which is considered an invasive and expensive procedure with a risk of bleeding or bile leaking [26].
By comparing both procedures, LSG showed nonsignificant superiority in improving liver enzymes compared to RYGB [9,19]. Additionally, the ALP enzyme was reported only in Esquivel et al., 2018 [19], who found a significant reduction in its level one year of LSG, p < 0.001. In AST, there was a significant reduction one year after LSG in comparison to RYGB. Furthermore, in ALT, LSG showed more decrease than RYGB, which was also nonsignificant, which was supported by another systematic review that compared both procedures and found that LSG significantly decreased ALT and ALP compared to RYGB; however, no significant differences were observed between both procedures regarding GGT and AST [27]. These results were also supported by another systematic review that found nonsignificant improvement of ALT and AST favoring LSG over RYGB [28].
Improvement in NAS score was reported in only two studies [18,21]. Pedersen et al., 2021 [13] found that both procedures had the same effect on the NAS score without worsening fibrosis 10. In addition, Salman et al. [17] found that LSG significantly decreased the NAS score after one year of follow-up. Our net analysis result showed that LSG significantly improved the NAS score while RYGB did not; however, the analysis included only two studies with a small number of patients; therefore, other studies are needed to confirm the findings. On the contrary, another systematic review and meta-analysis showed nonsignificant differences between both procedures favoring RYGB, which did not align with our findings [28].
The MASLD fibrosis score was reported in only two studies, [11,14] and the net result was a slight nonsignificant superiority of LSG over RYGB. On the other hand, Baldwin et al., 2019 [28] found that both surgeries decreased MASLD fibrosis scores without significant differences between them. Despite many studies reporting improvement in fibrosis [12,14,21,23]. Pedersen et al., 2021 and Netanel et al., 2020 found that bariatric surgeries were ineffective in improving fibrosis [13,15]. In future studies, we recommend further comparing LSG and RYGB and its effectiveness in evaluating all liver enzymes.
The mechanism behind improving NAFLD parameters after LSG and RYGB is not clearly studied in the literature. After these surgeries, nutrient entry through the digestive tract decreases. Additionally, the absorption of fat is decreased, especially after RYBG in comparison to LSG, which results in improving NAFLD clinical outcomes and laboratory markers [29]; however, we found no difference between the two procedures.
The preference for a specific type of bariatric surgery is still unclear, as previous systematic reviews and meta-analyses showed controversial results; however, most of them corroborated our findings. Fakhry et al., 2018 showed that RYGB had greater improvement in the histological outcomes compared to other procedures [30], while other systematic reviews showed no difference between both procedures in improving clinical outcomes in MASLD patients [27,28]. These findings could help in choosing the most appropriate type of surgery with the mildest side effects given the similar efficacy results of both procedures. However, the side effects were also comparable in both procedures, except that LSG was associated with shorter operative time than RYGB [31,32]; other side effects were comparable between the two procedures [31,33,34].

5. Conclusions

Both LSG and RYGB improve MASLDoutcomes one year after surgery, with a slight superiority of LSG over RYGB; however, randomized clinical trials with large samples are needed to confirm these results.

Strength and Limitations

Limited studies are comparing both surgical procedures in NAFLD or NASH patients after one year, which is considered the main strength of the study. However, there are some limitations: all of the included studies are observational studies, which increases the risk of selection bias; there were high levels of heterogeneity in many outcomes that could not be resolved, which also may be due to the presence of both NAFLD and NASH patients in the same population in the included studies. Additionally, some outcomes were reported in only a small number of studies; further studies are required to confirm our findings. Finally, advanced evaluation methods such as MRI fat fraction, biopsy, and elastography were not commonly used in the assessment of NAFLD patients to accurately compare disease activity after follow-up; therefore, we recommend further studies using these methods to monitor the improvement of disease.

Author Contributions

Conception and design: L.A.A., Administrative support: L.A.A., Provision of study materials or patients: L.A.A., G.K.A., A.K.A. and O.A.A., Collection and assembly of data: L.A.A., M.M.A. and R.S.A., Data analysis and interpretation: L.A.A. and O.A.A., Manuscript writing: All authors; (VII) Final ap-proval of manuscript: All authors. All authors have read and agreed to the published version of the manuscript.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Conflicts of Interest

None declared. The authors have no financial, consultative, institutional, or other relationships that might lead to bias or conflict of interest.

References

  1. Lekakis, V.; Papatheodoridis, G.V. Natural history of metabolic dysfunction-associated steatotic liver disease. Eur. J. Intern. Med. 2024, 122, 3–10. [Google Scholar] [CrossRef] [PubMed]
  2. Younossi, Z.M.; Koenig, A.B.; Abdelatif, D.; Fazel, Y.; Henry, L.; Wymer, M. Global epidemiology of nonalcoholic fatty liver disease—Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology 2016, 64, 73–84. [Google Scholar] [CrossRef] [PubMed]
  3. Cusi, K.; Isaacs, S.; Barb, D.; Basu, R.; Caprio, S.; Garvey, W.T.; Kashyap, S.; Mechanick, J.I.; Mouzaki, M.; Nadolsky, K.; et al. American association of clinical Endocrinology clinical practice guideline for the diagnosis and management of nonalcoholic fatty liver disease in primary care and Endocrinology clinical settings: Co-sponsored by the American association for the study of liver dis- eases (AASLD). Endocr. Pract. 2022, 28, 528–562. [Google Scholar] [CrossRef] [PubMed]
  4. Manzano-Nunez, R.; Rivera-Esteban, J.; Comas, M.; Angel, M.; Flores, V.; Bañares, J.; Ciudin, A.; Vilallonga, R.; Pericas, J.M. Outcomes of patients with severe obesity and cirrhosis with portal hypertension undergoing bariatric surgery: A systematic review. Obes. Surg. 2023, 33, 224–233. [Google Scholar] [CrossRef] [PubMed]
  5. Wang, G.; Huang, Y.; Yang, H.; Lin, H.; Zhou, S.; Qian, J. Impacts of bariatric surgery on adverse liver outcomes: A systematic review and meta- analysis. Surg. Obes. Relat. Dis. 2023, 19, 717–726. [Google Scholar] [CrossRef] [PubMed]
  6. 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. BMJ 2021, 372, n71. [Google Scholar] [CrossRef] [PubMed]
  7. Ouzzani, M.; Hammady, H.; Fedorowicz, Z.; Elmagarmid, A. Rayyan—A web and mobile app for systematic reviews. Syst. Rev. 2016, 5, 210. [Google Scholar] [CrossRef]
  8. Lo, C.K.-L.; Mertz, D.; Loeb, M. Newcastle-Ottawa Scale: Comparing reviewers’ to authors’ assessments. BMC Med. Res. Methodol. 2014, 14, 45. [Google Scholar] [CrossRef]
  9. Głuszyńska, P.; Łukaszewicz, A.; Diemieszczyk, I.; Chilmończyk, J.; Reszeć, J.; Citko, A.; Szczerbiński, Ł.; Krętowski, A.; Hady, H.R. 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]
  10. Abbassi, Z.; Orci, L.; Meyer, J.; Sgardello, S.D.; Goossens, N.; Rubbia-Brandt, L.; Spahr, L.; Buchs, N.C.; Mönig, S.P.; Toso, C.; et al. Impact of nonalcoholic steatohepatitis on the outcome of patients undergoing Roux-en-Y gastric bypass surgery: A propensity score–matched analysis. Obes. Surg. 2021, 32, 74–81. [Google Scholar] [CrossRef]
  11. Agarwal, L.; Aggarwal, S.; Shalimar; Yadav, R.; Dattagupta, S.; Garg, H.; Agarwal, S. Bariatric surgery in nonalcoholic fatty liver disease (NAFLD): Impact assessment using paired liver biopsy and fibroscan. Obes. Surg. 2021, 31, 617–626. [Google Scholar] [CrossRef]
  12. Elyasinia, F.; Jalali, S.M.; Zarini, S.; Sadeghian, E.; Sorush, A.; Pirouz, A. The effect of laparoscopic sleeve gastrectomy and gastric bypass surgery on Non-alcoholic steatohepatitis in Iranian patients with obesity. Middle East J. Dig. Dis. 2021, 13, 200–207. [Google Scholar] [CrossRef]
  13. Pedersen, J.S.; Rygg, M.O.; Serizawa, R.R.; Kristiansen, V.B.; Albrechtsen, N.J.W.; Gluud, L.L.; Madsbad, S.; Bendtsen, F. Effects of roux-en-Y gastric bypass and sleeve gastrectomy on non-alcoholic fatty liver disease: A 12-month follow-up study with paired liver biopsies. J. Clin. Med. 2021, 10, 3783. [Google Scholar] [CrossRef]
  14. Cherla, D.V.; Rodriguez, N.A.; Vangoitsenhoven, R.; Singh, T.; Mehta, N.; McCullough, A.J.; Brethauer, S.A.; Schauer, P.R.; Aminian, A. Impact of sleeve gastrectomy and Roux-en-Y gastric bypass on biopsy-proven non-alcoholic fatty liver disease. Surg. Endosc. 2019, 34, 2266–2272. [Google Scholar] [CrossRef]
  15. Netanel, C.; Goitein, D.; Rubin, M.; Kleinbaum, Y.; Katsherginsky, S.; Hermon, H.; Tsaraf, K.; Tachlytski, I.; Herman, A.; Safran, M.; et al. The impact of bariatric surgery on nonalcoholic fatty liver disease as measured using non-invasive tests. Am. J. Surg. 2021, 222, 214–219. [Google Scholar] [CrossRef]
  16. Nikai, H.; Ishida, K.; Umemura, A.; Baba, S.; Nitta, H.; Sugai, T.; Sasaki, A. Effects of laparoscopic sleeve gastrectomy on non-alcoholic steatohepatitis and liver fibrosis in Japanese patients with severe obesity. Obes. Surg. 2020, 30, 2579–2587. [Google Scholar] [CrossRef]
  17. Salman, M.A.; Salman, A.A.; Abdelsalam, A.; Atallah, M.; Shaaban, H.E.-D.; El-Mikkawy, A.; Omar, M.G.; Elshenoufy, M. Laparoscopic sleeve gastrectomy on the horizon as a promising treatment modality for NAFLD. Obes. Surg. 2020, 30, 87–95. [Google Scholar] [CrossRef]
  18. Yeo, S.C.; Ong, W.M.; Cheng, K.S.A.; Tan, C.H. Weight loss after bariatric surgery predicts an improvement in the non-alcoholic fatty liver disease (NAFLD) fibrosis score. Obes. Surg. 2019, 29, 1295–1300. [Google Scholar] [CrossRef]
  19. Esquivel, C.M.; Garcia, M.; Armando, L.; Ortiz, G.; Lascano, F.M.; Foscarini, J.M. Laparoscopic sleeve gastrectomy resolves NAFLD: Another formal indication for bariatric surgery? Obes. Surg. 2018, 28, 4022–4033. [Google Scholar] [CrossRef]
  20. Jimenez, L.S.; Chaim, F.H.M.; Chaim, F.D.M.; Utrini, M.P.; Gestic, M.A.; Chaim, E.A.; Cazzo, E. 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, 3131–3135. [Google Scholar] [CrossRef] [PubMed]
  21. Nickel, F.; Tapking, C.; Benner, L.; Sollors, J.; Billeter, A.T.; Kenngott, H.G.; Bokhary, L.; Schmid, M.; von Frankenberg, M.; Fischer, 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, 1342–1350. [Google Scholar] [CrossRef] [PubMed]
  22. Lassailly, G.; Caiazzo, R.; Buob, D.; Pigeyre, M.; Verkindt, H.; Labreuche, J.; Raverdy, V.; Leteurtre, E.; Dharancy, S.; Louvet, A.; et al. Bariatric surgery reduces features of nonalcoholic steatohepatitis in morbidly obese patients. Gastroenterology 2015, 149, 379–388. [Google Scholar] [CrossRef] [PubMed]
  23. OpenMeta [Analyst]. Brown.edu. Available online: http://www.cebm.brown.edu/openmeta/ (accessed on 23 April 2024).
  24. Higgins, J.P.T.; Thomas, J.; Chandler, J.; Cumpston, M.; Li, T.; Page, M.J.; Welch, V.A. (Eds.) Cochrane Handbook for Systematic Reviews of Interventions, 2nd ed.; John Wiley & Sons: Chichester, UK, 2019. [Google Scholar]
  25. Burza, M.A.; Romeo, S.; Kotronen, A.; Svensson, P.-A.; Sjöholm, K.; Torgerson, J.S.; Lindroos, A.-K.; Sjöström, L.; Carlsson, L.M.S.; Peltonen, M. Long-term effect of bariatric surgery on liver enzymes in the Swedish obese subjects (SOS) study. PLoS ONE 2004, 8, e60495. [Google Scholar] [CrossRef] [PubMed]
  26. Spengler, E.K.; Loomba, R. Recommendations for diagnosis, referral for liver biopsy, and treatment of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Mayo Clin. Proc. 2015, 90, 1233–1246. [Google Scholar] [CrossRef] [PubMed]
  27. Silva, M.B.d.B.e.; Tustumi, F.; Neto, A.A.d.M.; Dantas, A.C.B.; Santo, M.A.; Cecconello, I. Gastric bypass compared with sleeve gastrectomy for nonalcoholic fatty liver disease: A systematic review and meta-analysis. Obes. Surg. 2021, 31, 2762–2772. [Google Scholar] [CrossRef] [PubMed]
  28. Baldwin, D.; Chennakesavalu, M.; Gangemi, A. Systematic review and meta-analysis of Roux-en-Y gastric bypass against laparoscopic sleeve gastrectomy for amelioration of NAFLD using four criteria. Surg. Obes. Relat. Dis. 2019, 15, 2123–2130. [Google Scholar] [CrossRef]
  29. Svane, M.S.; Bojsen-Møller, K.N.; Martinussen, C.; Dirksen, C.; Madsen, J.L.; Reitelseder, S.; Holm, L.; Rehfeld, J.F.; Kristiansen, V.B.; van Hall, G.; et al. Postprandial Nutrient Handling and Gastrointestinal Hormone Secretion After Roux-en-Y Gastric Bypass vs Sleeve Gastrectomy. Gastroenterology 2019, 156, 1627–1641.e1. [Google Scholar] [CrossRef] [PubMed]
  30. 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] [PubMed]
  31. Hedberg, S.; Thorell, A.; Österberg, J.; Peltonen, M.; Andersson, E.; Näslund, E.; Hertel, J.K.; Svanevik, M.; Stenberg, E.; Neovius, M.; et al. Comparison of Sleeve Gastrectomy vs Roux-en-Y Gastric Bypass. JAMA Netw. Open 2024, 7, e2353141. [Google Scholar] [CrossRef]
  32. Abdelkader, A.M.; Ali, H.; Mitwally, R.; Yousef, M.S. Laparoscopic sleeve gastrectomy compared with Roux-en-Y gastric bypass surgery: 2-year outcome of body weight, obesity-associated comorbidities, and quality of life. Egypt. J. Surg. 2017, 36, 432. [Google Scholar] [CrossRef]
  33. Peterli, R.; Wölnerhanssen, B.K.; Peters, T.; Vetter, D.; Kröll, D.; Borbély, Y.; Schultes, B.; Beglinger, C.; Drewe, J.; Schiesser, M.; et al. Effect of laparoscopic sleeve gastrectomy vs laparoscopic roux-en-y gastric bypass onweight loss in patients with morbid obesity the sm-boss randomized clinical trial. JAMA J. Am. Med. Assoc. 2018, 319, 255–265. [Google Scholar] [CrossRef]
  34. Salminen, P.; Helmiö, M.; Ovaska, J.; Juuti, A.; Leivonen, M.; Peromaa-Haavisto, P.; Hurme, S.; Soinio, M.; Nuutila, P.; Victorzon, M. Effect of laparoscopic sleeve gastrectomy vs laparoscopic roux-en-y gastric bypass on weight loss at 5 years among patients with morbid obesity the SLEEVEPASS randomized clinical trial. JAMA J. Am. Med. Assoc. 2018, 319, 241–254. [Google Scholar] [CrossRef]
Surgeries 05 00040 g001
Figure 1. PRISMA flow chart of the included studies [6].
Figure 1. PRISMA flow chart of the included studies [6].
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Figure 2. Gamma-glutamyl transferase (GGT) levels [9,15,17,19].
Figure 2. Gamma-glutamyl transferase (GGT) levels [9,15,17,19].
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Figure 3. Alanine transaminase (ALT) [9,10,12,13,14,15,16,17,19,20].
Figure 3. Alanine transaminase (ALT) [9,10,12,13,14,15,16,17,19,20].
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Figure 4. Alanine aminotransferase levels [9,10,12,13,14,16,17,19,20].
Figure 4. Alanine aminotransferase levels [9,10,12,13,14,16,17,19,20].
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Figure 5. BMI change after one year [9,10,12,13,15,16,17,19,20,22].
Figure 5. BMI change after one year [9,10,12,13,15,16,17,19,20,22].
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Figure 6. NAS score change [13,17].
Figure 6. NAS score change [13,17].
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Table 1. Newcastle–Ottawa Scale (NOS) quality assessment summary for included studies [8].
Table 1. Newcastle–Ottawa Scale (NOS) quality assessment summary for included studies [8].
StudyYearSelectionComparabilityOutcomeQuality
Representativeness of the ExposedNon-Exposed Ascertainment of ExposureBegin without Outcome PresentOutcome AssessmentFollow-Up
Length		Adequacy of Outcome
Głuszyńska [9]2023* ** **-Good
Abbassi
[10]		2022-********Good
Agarwal
[11]		2021- ** **-Good
Elyasinia
[12]		2021-**-*-**Fair
Pedersen [13]2021********-Good
Cherla [14]2020-********Good
Netanel [15]2020- ** ***Good
Nikai [16]2020-******-Good
Salman [17]2020- ** **-Good
Yeo [18]2019- ** ***Good
Esquivel [19]2018- ** **-Good
Jimenez [20]2018- ** **-Good
Nickel [21]2018-*******Good
Lassailly [22]2015- ** ***Good
*: is the star given to each study if it has a good quality in the corresponding quality domain. The stars are then collected in a score to calculate the overall quality of each study (according to NOS guideline). A maximum of two stars ** can be awarded for Control for important factor or additional factor.
Table 2. Baseline characteristics of the included studies.
Table 2. Baseline characteristics of the included studies.
AuthorYearStudy DesignCountryInterventionAgeSample SizeSample SizeSex
Mean (SD)MaleFemale
Nickel et al., 2017 [21]2017Prospective observational cohort studyGermanylaparoscopic sleeve gastrectomy (LSG)42.9 ± 11.6616123 (41.0)36 (59.0)
Roux-en-Y gastric bypass (RYGB)45.1 ± 9.5393915 (33.3)26 (66.7)
Głuszynska et al., 2023 [9] 2023Retrospective CohortPolandLaparoscopic sleeve gastrectomy39.83 ± 24.36555532 (58)23 (42)
Elyasinia et al., 2021 [12] 2021Prospective observational cohort studyIranLaparoscopic sleeve gastrectomy40.45 ± 12.0122224 (18.18)18 (81.81)
Laparoscopic gastric bypass22225 (22.7%)17 (77.3%)
Jimenez et al., 2018 [20] 2018Prospective observational cohort studyBrazilRoux-en-Y gastric bypass (RYGB)38.3 ± 10.3909082 (91.1)8 (8.9)
Abbassi et al., 2021 [10] 2021Retrospective observational cohort studySwitzerlandRoux-en-Y gastric bypass (RYGB)40.67 (11.9)516421 patients with NAFLD, 95 patients with NASH71 (17)350 (83)
Netanel et al., 2020 [15] 2020Prospective observational cohort studyIsraelSleeve gastrectomy44.1 ± 4.8262618 (69.2)8 (30.8)
Agarwal et al., 2020 [11] 2020Prospective observational cohort studyIndiaLaparoscopic sleeve gastrectomy, Roux-en-Y gastric bypass (RYGB), and anastomosis gastric bypass (OAGB)39.9 ± 11.2585817 (29.3)41 (70.7)
Pederson, 2021 [13] 2021Prospective observational cohort studyDenmarkLaparoscopic sleeve gastrectomy44 ± 9242410 (42)14 (58)
Roux-en-Y gastric bypass (RYGB)44 ± 216167 (44)9 (56)
Nikai et al., 2020 [16] 2020Prospective observational cohort studyJapanLaparoscopic sleeve gastrectomy44.7 ± 12.4686837 (54.5)31 (45.5)
Cherla et al., 2019 [14] 2019Retrospective observational cohort studyUSASleeve gastrectomy49 ± 10.6666622 (33)44 (67)
Roux-en-Y gastric bypass (RYGB)48 ± 11.7421421132 (31)289 (69)
Esquivel et al., 2018 [19] 2018Prospective observational cohort studySouth AmericaLaparoscopic sleeve gastrectomy40 ± 10636322 (35)41 (65)
Salman et al., 2019 [17] 2019Prospective studyEgyptLaparoscopic sleeve gastrectomy41.39 + 7.64949457 (61)37 (39)
Yeo et al., 2019 [18] 2019Retrospective observational cohort studySingaporeLSG (n = 99, 52%), followed by Roux-en-Y gastric bypass (n = 87, 45%), then gastric banding (n = 6, 3%)42.7 ± 10.219219272 (38)120 (62)
Lassailly et al., 2015 [22] 2015Retrospective observational cohort studyFranceBariatric surgery: gastric bypass (70), gastric banding (32), sleeve gastrectomy (6), and biliointestinal bypass (1)46.2 ± 10.510910940 (37)69 (63)
SummaryFourteen studies were included with a total population of 1942 individual who underwent laparoscopic sleeve gastrectomy (LSG) or Roux-en-Y gastric bypass (RYGB). Most of the studies were prospective cohort studies (nine), while the rest were retrospective.
Table 3. Baseline characteristics of study outcomes.
Table 3. Baseline characteristics of study outcomes.
Study NameNumberALP (Pre)AST (Pre)ALT (Pre)GGT (Pre)BMI (Pre)
LSGRYGBLSGRYGBLSGRYGBLSGRYGBLSGRYGB
LSGRYBGMean (SD)Mean (SD)Mean (SD)Mean (SD)Mean (SD)Mean (SD)Mean (SD)Mean (SD)Mean (SD)Mean (SD)
Nickel et al., 2017 [21]100100NRNR31.5 (17.3) n = 10043.3 (28.9) n = 10056.1 (66.5) n = 10049.9 (7.6)46.6 (6.6)
Głuszynska et al., 2023 [9]55NRNRNR27.166 (13.7)NR (NR)38.667 (25.04)NR35.53 (26.56)NR46.1 (5.861)NR
Elyasinia et al., 2021 [12]2222NRNR31.6 (14.3)28.7 (13.6)26.5 (10.2)22.4 (9.7)NRNR43.7 (4)43 (4.6)
Jimenez et al., 2018 [20]NR90NRNRNR25.5 (14)NR33.1 (37.8)NRNRNR35.7 (2.8)
Abbassi et al., 2021 [10]Non-NashNR418NRNRNR19.67 (7.43)NR26.33 (14.87)NRNRNR43.76 (4.46)
NashNR69NRNRNRNRNRNRNRNRNRNR
TotalNR487NRNRNRNRNRNRNRNRNRNR
Netanel et al., 2020 [15]26NRNRNRNRNR (NR)32.2 (17.6)NR41.4 (22.6)NR41.7 (4.8)NR
Agarwal et al., 2020 [11]All patients 141NRNR36.1 (22.8) n = 14132 (18.6) n = 141NRNR45.9 (6.9)
Pederson, 2021 [13]2416NRNR25 (8)25 (9)32 (11)33 (14)NRNR41 (4.5)43 (7.2)
Nikai et al., 2020 [16]NASH43NRNRNR50.7 (34.3)NR73.3 (52.6)NRNRNR41.9 (5.2)NR
Non-Nash25NRNRNR26.6 (15.9)NR37 (34.4)NRNRNR45 (7.3)NR
Total68NRNRNR41.83 (31.06)NR59.95 (49.69)NRNRNR43.03 (6.18)NR
Cherla et al., 2019 [14]6642177.1 (21.7)79.5 (23.6)49.1 (21.5)49.3 (22)61.7 (30)59.4 (24.9)NRNR48.6 (10.1)45.3 (6.9)
Esquivel et al., 2018 [19]63NR195 (55)NR26 (13)NR34 (18)NR36 (18)NR41.9 (5.4)NR
Salman et al., 2019 [17]93NRNRNR31.32 (5.58)NR38.19 (6.66)NR40.27 (6.99)NR44.54 (5.45)NR
Yeo et al., 2019 [18]9987NRNR26.7 ± 13.935.5 ± 26.2NRNR41.6 ± 7.98
Lassailly et al., 2015 [22]All patients 109NRNRNRNRNRNRNRNRNR50 (8.8)
NR: not reported.
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MDPI and ACS Style

AlRumaih, A.S.; Alzelfawi, L.A.; Alotaibi, G.K.; Aldayel, O.A.; AlMutairi, A.K.; Alnowaimi, R.T.; Alshahrani, M.M.; Alsharif, R.S.; Almadani, S.N. Effectiveness of Bariatric Surgeries for Metabolic Dysfunction-Associated Steatotic Liver Disease: A Systematic Review and Meta-Analysis. Surgeries 2024, 5, 486-498. https://doi.org/10.3390/surgeries5030040

AMA Style

AlRumaih AS, Alzelfawi LA, Alotaibi GK, Aldayel OA, AlMutairi AK, Alnowaimi RT, Alshahrani MM, Alsharif RS, Almadani SN. Effectiveness of Bariatric Surgeries for Metabolic Dysfunction-Associated Steatotic Liver Disease: A Systematic Review and Meta-Analysis. Surgeries. 2024; 5(3):486-498. https://doi.org/10.3390/surgeries5030040

Chicago/Turabian Style

AlRumaih, Abdullah Sulaiman, Lama Abdullah Alzelfawi, Ghadah Khalid Alotaibi, Osamah AbdulAziz Aldayel, Abdulrahman Khazzam AlMutairi, Rosana Tariq Alnowaimi, Mubarak Mohammed Alshahrani, Rifal Sami Alsharif, and Sarah Nabil Almadani. 2024. "Effectiveness of Bariatric Surgeries for Metabolic Dysfunction-Associated Steatotic Liver Disease: A Systematic Review and Meta-Analysis" Surgeries 5, no. 3: 486-498. https://doi.org/10.3390/surgeries5030040

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