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 Table of Contents  
Year : 2023  |  Volume : 2  |  Issue : 2  |  Page : 60-67

Short-term effectiveness of metabolic surgery in nonobese diabetic patients: A systematic review and meta-analysis

1 Department of Surgery and Anatomy, Medical School of Ribeirão Preto, University of São Paulo, Ribeirão Preto, Brazil
2 Department of Gastrointestinal Surgery, Marília School of Medicine, Marília, Brazil
3 Bariatric and Metabolic Surgery Unit, University of São Paulo, São Paulo, Brazil
4 Department of Surgery, Federal University of Santa Catarina, Florianópolis, Brazil
5 Department of Bariatric and Metabolic Surgery, King's College Hospital NHS Foundation, London, United Kingdom
6 Bariatric and Metabolic Service, Santa Casa de Misericórdia de Itabuna, Bahia, Brazil
7 Department of Surgery, Nilton Lins University, Manaus, Brazil
8 Department of Evidence Based Medicine, Lusíada University Center, Santos, Brazil
9 University of São Paulo, São Paulo, Brazil

Date of Submission25-Mar-2023
Date of Acceptance12-May-2023
Date of Web Publication10-Jul-2023

Correspondence Address:
Eduardo Lemos de Souza Bastos
Department of Gastrointestinal Surgery, Marília School of Medicine, Marília
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jbs.jbs_6_23

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Aim: The aim of this study was to assess the safety and short-term effectiveness of metabolic surgery (MS) in nonobese diabetic patients. Methods: Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement was used in this systematic review. The search for evidence was performed in the Medline (PubMed), Embase, Cochrane (CENTRAL), LILACS, and ClinicalTrials.gov databases from the inception to February 2023. The main eligibility criteria were nonobese adults (body mass index [BMI] <30 kg/m2) with type 2 diabetes mellitus (T2DM) undergoing MS. T2DM remission rate, glycemic parameters, and weight loss were measured before and after surgery. Complication rate was also described. Outcomes were aggregated and the quality of evidence was sorted. Heterogeneity was assumed when I2 >50%. The random-effects model was used to perform a proportional meta-analysis. Results: Twenty-one studies were included (n = 835). The overall rate of diabetes remission was 50.1% (95% confidence interval [CI] = 43.8%–56.1%; P = 0.993; I2 = 92%). The mean reduction of glycated hemoglobin and fasting glucose was 2.42% (95% CI = 1.91%–2.93%; P < 0.00001; I2 = 89%) and 70.60 mg/dL, respectively. A drop of 3.34 points (95% CI = 1.59–5.09; P < 0.0002; I2 = 95%) was observed in the HOMA-IR, and the mean postprandial glycemia was 123.27 mg/dL. No marked weight loss was observed (−3.80 kg/m2 in BMI; 95% CI = 2.70–4.91; P < 0.00001; I2 = 95%). There was no postoperative mortality, and the overall postoperative complication rate was about 12%. The certainty of evidence was low or very low. Conclusion: MS could be effective in the surgical approach of nonobese diabetic patients, but further long-term, more robust studies are needed to strengthen the evidence.

Keywords: Bariatric surgery, diabetes mellitus type 2, metabolic syndrome, systematic review

How to cite this article:
Salgado W, Bastos EL, Dantas AC, Onzi TR, Silva LB, Albano A, Cortez MV, Tristão LS, dos Santos CL, Bernardo WM. Short-term effectiveness of metabolic surgery in nonobese diabetic patients: A systematic review and meta-analysis. J Bariatr Surg 2023;2:60-7

How to cite this URL:
Salgado W, Bastos EL, Dantas AC, Onzi TR, Silva LB, Albano A, Cortez MV, Tristão LS, dos Santos CL, Bernardo WM. Short-term effectiveness of metabolic surgery in nonobese diabetic patients: A systematic review and meta-analysis. J Bariatr Surg [serial online] 2023 [cited 2023 Sep 29];2:60-7. Available from: http://www.jbsonline.org/text.asp?2023/2/2/60/380822

  Introduction Top

Type 2 diabetes mellitus (T2DM) is a chronic, progressive disease with several complications significantly affecting the quality of life.[1] The incidence has increased over the years, parallel to the growth of obesity. Data from 2021 show that more than 500 million adults have diabetes, projecting a prevalence of almost 650 million people with this disease in 2030. Furthermore, T2DM could be directly or indirectly linked to over 6.7 million deaths in 2021, with an estimated health expenditure close to US$ 1 trillion.[2]

The standards of care for diabetic patients seek to establish therapeutic goals for preventing complications. The clinical treatment is supported by nutritional guidance, changes in lifestyle, and pharmacotherapy.[3]

Metabolic surgery (MS) is already a well-recognized treatment option for poorly controlled diabetic patients with obesity, i.e., with body mass index (BMI) over 30 kg/m2, with some evidence of sustained improvement of metabolic syndrome.[4] A randomized controlled trial showed that Roux-en-Y gastric bypass (RYGB) or sleeve gastrectomy was superior compared to drug therapy alone in the long-term T2DM control.[5]

Despite the reports on the safety and efficacy of MS in the management of nonobese diabetic patients, there is still not enough scientific evidence to support this therapeutic option.[6],[7] Therefore, the aim of this systematic review was to assess the safety and short-term efficacy of MS in individuals with T2DM in the absence of obesity.

  Methods Top

Search strategy

The search for evidence was performed through a systematic review using the Medline (PubMed), Embase, Cochrane (CENTRAL), LILACS, and ClinicalTrials.gov databases. The search period ranged from the inception of the databases to February 2023, without restrictions to languages.

The terms used were (Diabetes OR T2DM) AND (low BMI OR non-obese OR overweight OR body mass index <30 kg/m2 OR normal weight) AND (Bariatrics OR Bariatric Surgery OR Bariatric Surgical Procedures OR Bariatric Surgical Procedure OR Bariatric Surgeries OR Stomach Stapling OR Gastric Bypass OR Gastroplasty OR Jejunoileal Bypass OR Metabolic Surgery). The search strategy was adapted to each base to increase sensitivity.

As all analyses were performed based on previously published studies, no approval was required from the Ethics Council or patient consent. This review followed the concepts of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guideline for reporting systematic reviews and meta-analyses.[8] Protocol details were recorded in PROSPERO[9] under the record CRD42022311111.

Inclusion and exclusion criteria

Inclusion criteria were (I) patients with T2DM submitted to MS, (II) patients with BMI <30 kg/m2, (III) study designs with the highest available strength of evidence, and (IV) full text or abstracts.

Exclusions were (I) reviews, case reports, editorials, and letters; (II) articles with mean BMI <30 kg/m2 but with patients with BMI ≥30 kg/m2; and (III) full text or abstract unavailable.

Following the eligibility criteria, the articles were first evaluated by title, then by abstract, and finally by full text by two independent evaluators (LST and WMB).


Outcomes evaluated were T2DM remission rate, changes in glycated hemoglobin (HbA1c) values (%), insulin resistance index (HOMA-IR), 2-h postprandial blood glucose (mg/dL), blood glucose fasting (mg/dL), C-peptide (ng/mL), and BMI (kg/m2). Concerning the definition of T2DM remission, we complied with the criteria adopted in each study. Secondarily, the main adverse events were described.

Quality of evidence

The certainty of evidence was evaluated through the software GRADEpro Guideline Development Tool[10] (© 2021, McMaster University and Evidence Prime Inc.), and the risk of bias by ROBINS-I.[11] The quality of evidence was assessed and sorted by the GRADE (the Grading of Recommendations Assessment, Development, and Evaluation) terminology in very low, low, moderate, and high if meta-analysis was accomplished.

Extraction of results and statistical analysis

The data of selected studies were extracted manually. For the meta-analysis, the Software Review Manager Version 5.4 (the Cochrane Collaboration, 2014) and Comprehensive Meta-Analysis were used.[12],[13] The comparisons were demonstrated in risk difference, the difference between means (DM), and a 95% confidence interval (95% CI). The inconsistency of the intervention effects (proportion of the total variation in the studies due to heterogeneity) was measured using I2. To obtain adequate CIs, we used the random-effects model if I2 >50% and the fixed-effects model if I2 ≤50%. The funnel plot for asymmetry was analyzed to assess possible publication biases.

  Results Top

The search conducted in February 2023 recovered 11,701 articles after removing duplicates. Of which, 68 were selected by the abstract. Following the eligibility criteria, 21 articles (n = 835 patients) were included in this systematic review.[6],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33] Fourteen are prospective cohorts and seven are retrospective.

A flow diagram describing the selection process (inclusion and exclusion) and the reason for the 15 full-text exclusions is shown in [Figure 1]. The basic characteristics of the included studies are summarized in [Table 1].
Figure 1: PRISMA flow diagram of literature search and selection. PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-Analyses. From: Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. doi: 10.1136/bmj.n71

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Table 1: Basic description of the included studies

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With the purpose of standardizing to better compare the results of the studies, we analyzed the outcomes based on the most common follow-up time expressed in the included studies, that is, from 12 months. The data obtained after the surgical procedures were compared with the baseline (before x after).

Complete remission of type 2 diabetes mellitus

The T2DM remission rate reported in 8 studies[14],[15],[17],[19],[25],[26],[27],[32] was 50.1% (95% CI = 43.8%–56.1%; P = 0.993; I2 = 92%; certainty of evidence: very low) [Figure 2]. The meta-analysis was based on data from 357 operated patients. The time elapsed between the procedure and the evaluation of T2DM remission varied between studies, with the majority presenting data with 12 months postoperatively,[15],[25],[26],[27] but periods of 18 months,[14] 2 years,[32] 3 years,[15] and even 6 years[19] are also mentioned.
Figure 2: T2DM remission. Forest plot. Random effect: 50.1% (95% CI = 43.8%–56.1%; P = 0.993). CI: Confidence interval, T2DM: Type 2 diabetes mellitus

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Glycated hemoglobin reduction (%)

HbA1c was reported by 14 articles, totaling 723 patients.[14],[15],[17],[18],[21],[23],[25],[26],[27],[28],[30],[31],[32],[33] The meta-analysis showed a 2.42% reduction in the HbA1c value after the surgical procedure (95% CI = 1.91%–2.93%; P < 0.00001; I2 = 89%, random model; certainty of evidence: low) [Figure 3].
Figure 3: HbA1c reduction. Forest plot. Random effect: 2.42% (95% CI = 1.91%–2.93%; P < 0.00001). HbA1c: Glycated hemoglobin, CI: Confidence interval

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HOMA-IR reduction

The meta-analysis of 6 articles,[15],[17],[21],[23],[30],[31] totaling 369 patients, showed that HOMA-IR reduced 3.34 points (95% CI = 1.59–5.09; P < 0.0002; I2 = 95%, random model; certainty of evidence: low) [Figure 4].
Figure 4: HOMA-IR reduction. Forest plot. Random effect: 3.34 points (95% CI = 1.59–5.09; P < 0.0002). HOMA-IR: Insulin resistance index, CI: Confidence interval

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Two-hour postprandial glycemia reduction (mg/dL)

Six articles reported 2-h postprandial glycemia.[14],[15],[17],[23],[26],[31] The meta-analysis showed that the patients (n = 439) had a reduction of 123.27 mg/dL (95% CI = 92.65–153.88; P < 0.00001; I2 = 91%, random model; certainty of evidence: low) [Figure 5].
Figure 5: Two-hour postprandial glycemia reduction. Forest plot. Random effect: 123.27 mg/dL (95% CI = 92.65–153.88; P < 0.00001). CI: Confidence interval

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Fasting glycemia reduction (mg/dL)

Based on 11 studies[14],[15],[17],[23],[26],[27],[28],[30],[31],[32],[33] with 1016 patients, the comparison of fasting glucose before and after MS showed a reduction of 70.60 mg/dL (95% CI = 45.92–95.29; P < 0.00001; I2 = 94%, random model; certainty of evidence: low) [Figure 6].
Figure 6: Fasting glycemia reduction. Forest plot. Random effect: 70.60 mg/dL (95% CI = 45.92–95.29; P < 0.00001). CI: Confidence interval

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C-peptide reduction (ng/mL)

C-peptide analysis reported by 7 articles[14],[17],[23],[26],[31],[32],[33] (424 patients) demonstrated that patients had a reduction of 0.37 ng/mL (95% CI = 0.04–0.70; P = 0.03; I2 = 83%, random model; certainty of evidence: low) [Figure 7].
Figure 7: C-peptide reduction. Forest plot. Random effect: 0.37 ng/mL (95% CI = 0.04–0.70; P = 0.03). CI: Confidence interval

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Body mass index reduction (kg/m2)

Data analysis showed that the BMI of patients (12 studies;[14],[15],[17],[21],[23],[25],[26],[27],[28],[30],[32],[33] n = 580) reduced 3.80 kg/m2 postoperatively (95% CI = 2.70–4.91; P < 0.00001; I2 = 95%, random model; certainty of evidence: low) [Figure 8].
Figure 8: BMI reduction. Forest plot. Random effect: 3.80 kg/m2 (95% CI = 2.70–4.91; P < 0.00001). BMI: Body mass index, CI: Confidence interval

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Adverse events

There was no postoperative mortality. Acute adverse events were reported by 13 articles (n = 630 patients exposed). Osman Abouzeid et al. reported moderate infection in the surgical wound and moderate bleeding in three patients.[14] DePaula et al. described one case of fistula, one of gastrointestinal bleeding, one of urinary tract infection, and two cases of pneumonia.[16] In the series of Dixon et al., three patients had gastrointestinal bleeding and one had a surgical site infection.[18] Kim and Hur reported 22 patients with marginal ulcers, 2 with gastrointestinal bleeding, and 2 reoperations (abscess and fistula).[23] Ferraz et al. reported one gastric fistula and one surgical site infection.[19] In the study by Lee et al., two patients had leakage and bleeding.[25] Liang et al. reported two patients with gastrointestinal bleeding and seven with anemia.[26] One patient from Navarrete et al. had intra-abdominal bleeding.[27] Scopinaro et al. reported one patient with intra-abdominal bleeding that needed reoperation.[30] Wang et al. reported three patients with gastric bleeding, one with posterior cerebral artery insufficiency, and one case of pneumonia.[32] Finally, three articles reported no serious acute adverse events.[29],[31],[33]

Late complications are mentioned in five studies, the most serious being two intestinal obstructions and one with ileal perforation all requiring reoperations.[16] Two studies mention that patients had anemia in the postoperative period but in values similar to those found in studies that operated on patients with obesity.[18],[25] Two authors report diarrhea and malnutrition, five in the study by Cui et al.[15] and one patient in the casuistic of Scopinaro et al.[30] In the latter, surgical reversal was necessary.

We categorized all the complications according to the Clavien–Dindo (CD) classification, where 2.40% were CD class I, 7.86% class II, 0.22% class IIIA, and 0.83% class IIIB.

  Discussion Top

Despite the low and very low certainty of evidence, our meta-analysis showed no marked weight loss, acceptable complication rates, and approximately 50% T2DM remission in the short-term follow-up of nonobese patients undergoing MS.

Previous systematic reviews have found similar outcomes. In 2018, a systematic review retrieved 21 studies encompassing 935 nonobese individuals who underwent MS with at least 1 year of follow-up. No meta-analysis was carried out. The T2DM remission rate was highly variable between studies, ranging from 13.3% to 90.2%. In addition, marked improvements in the parameters of glycemic metabolism and lipid profiles were observed across the studies, and no threatening weight loss was found (BMI at follow-up ranging from 20 to 26.4 kg/m2). However, the authors drew attention to the low quality of the included studies, preventing more robust conclusions.[34] A year later, another systematic review was published, this time with meta-analysis. Twenty-six studies were retrieved, comprising 1105 nonobese patients with at least 6 months of postoperative follow-up. The T2DM remission rate was 43% of the patients, while the reduction in BMI was 3.57 kg/m2, HbA1c was 2.08%, and fasting glucose was 55.93 mg/dL. The inconsistency of the meta-analysis was very high (I2 = 97%).[35] Comparing these data with our systematic review and meta-analysis, we can infer that powerful studies that could provide more robust answers to this still open issue have not been carried out in recent years.

New statements of bariatric and MS (BMS) have aroused the interest of the bariatric scientific community, since decades have passed since the publication of the National Institute of Health Consensus on bariatric surgery.[36] Throughout all these years, the scientific knowledge has opened a new frontier for the surgical approach to obesity and its related diseases, making metabolic and bariatric surgery (MBS) to be considered an option in patients with uncontrolled hyperglycemia and BMI >30 kg/m2.[37] Recently, the International Federation for the Surgery of Obesity and Metabolic Disorders and the American Society of MBS published a joint statement recommending the MBS for individuals with metabolic disease and class I obesity (BMI of 30–34.9 kg/m2), and no longer just from class II obesity.[4] Indisputably, a remarkable step forward.

Nevertheless, few studies addressing MS in the absence of obesity have been published. Accordingly, no consensus has been reached by the bariatric scientific community regarding this indication to date. Our systematic review retrieved observational, retrospective, and prospective studies but no randomized clinical trials. The sample size of some publications is small, and the average follow-up time is quite short. Regarding the follow-up period, four studies with <1 year of follow-up were retrieved by our systematic review based on the inclusion criteria but were not enrolled in the quantitative meta-analysis. Therefore, the results expressed in [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8] refer to at least 1 year after surgery.

Furthermore, the outcomes of various surgical techniques could not be individualized, weakening the strength of evidence in this meta-analysis. Although most patients were submitted to RYGB or sleeve gastrectomy techniques, several procedures were used as MS, such as one anastomosis gastric bypass (162 patients), ileal interposition with sleeve gastrectomy (69 patients), duodenal-jejunal exclusion (44 patients), or biliopancreatic diversion (15 patients).

The loss of follow-up in some studies may have negatively influenced the T2DM remission rate. In addition, there was high heterogeneity in the concept of complete T2DM remission, ranging from withdrawal of antidiabetic medications, fasting and postprandial glycemia values, and most of the time, HbA1c value. In addition, the HbA1c value cutoff line has also been quite variable between studies. We faithfully complied with the definition of diabetes remission adopted in each study, regardless of which one it was.

The short-term results seemed reasonable to us. However, long-term follow-up studies are needed to reveal whether the effects are lasting. Patients with a shorter disease duration (<7 years), with a BMI closer to the highest values (BMI >27 kg/m2), and with higher C-peptide values (>2 ng/mL) seem to be more likely to have T2DM control after surgery.[18],[25]

No postoperative deaths were described, and the overall complication rate was around 12%. Acute and chronic complications such as fistulas, bleeding, surgical wound infection, and anemia have been reported, similarly to those already described in BMS for patients with BMI >30 kg/m2.[38] In addition, 3 out of 13 articles reported no serious acute adverse events.[29],[31],[33]

The most significant limitation of our study was certainly the low or very low certainty of evidence. The inconsistency of meta-analysis remained above 90% for all variables analyzed. The studies included in the meta-analysis were observational, nonrandomized with short-term follow-up. In addition, most were published more than 5 years ago and with a small number of patients. The sample size ranged from 6 to 107 patients. Another significant limitation of this meta-analysis was the high heterogeneity concerning the definition of diabetes remission across the retrieved studies.

However, even considering these caveats, our meta-analysis suggests that MS could be effective in reaching T2DM remission and improving glycemic parameters in patients with BMI <30 kg/m2 without causing excessive weight loss. The T2DM remission rate of around 50% was mainly supported by the reduction of approximately two percentage points in HbA1c values, of −3.3 points in HOMA-IR, −123 mg/dL in 2-h postprandial glycemia, and −70 mg/dL in fasting glycemia. These significant results were achieved despite the slight reduction in BMI after 1 year (−3.80 kg/m2), dispelling fears of excessive weight loss in nonobese patients undergoing bariatric procedures such as RYGB and sleeve gastrectomy.

  Conclusion Top

This meta-analysis presents encouraging results regarding the safety and short-term efficacy of MS in controlling T2DM in nonobese patients. Nevertheless, these results should be viewed with some caution, and higher quality studies with larger sample sizes and long-term follow-up should be carried out to strengthen this evidence. Furthermore, priority should be given to establishing a universal definition of surgical remission of diabetes so that study results can be assembled with greater reliability.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]

  [Table 1]


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