Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Open Access

Peer-reviewed

Research Article

Effects of Bariatric Surgery on Renal Function in Obese Patients: A Systematic Review and Meta Analysis

  • Kun Li ,

    Contributed equally to this work with: Kun Li, Jianan Zou

    leeq8110@163.com

    Affiliation Department of General Surgery, Huadong Hospital Affiliated to Fudan University, Shanghai, China

    ⨯
  • Jianan Zou ,

    Contributed equally to this work with: Kun Li, Jianan Zou

    Affiliation Department of Nephrology, Huadong Hospital Affiliated to Fudan University, Shanghai, China

    ⨯
  • Zhibin Ye,

    Affiliation Department of Nephrology, Huadong Hospital Affiliated to Fudan University, Shanghai, China

    ⨯
  • Jianzhong Di,

    Affiliation Department of General Surgery, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai, China

    ⨯
  • Xiaodong Han,

    Affiliation Department of General Surgery, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai, China

    ⨯
  • Hongwei Zhang,

    Affiliation Department of General Surgery, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai, China

    ⨯
  • Weijie Liu,

    Affiliation Department of General Surgery, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai, China

    ⨯
  • Qinggui Ren,

    Affiliation Department of General Surgery, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai, China

    ⨯
  • Pin Zhang

    Affiliation Department of General Surgery, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai, China

    ⨯

Abstract

Background

Obesity is an independent risk factor of development and progression of chronic kidney disease (CKD). Data on the benefits of bariatric surgery in obese patients with impaired kidney function have been conflicting.

Objective

To explore whether there is improvement in glomerular filtration rate (GFR), proteinuria or albuminuria after bariatric surgery.

Methods

We comprehensively searched the databases of MEDLINE, Embase, web of science and Cochrane for randomized, controlled trials and observational studies that examined bariatric surgery in obese subjects with impaired kidney function. Outcomes included the pre- and post-bariatric surgery GFR, proteinuria and albuminuria. In obese patients with hyperfiltration, we draw conclusions from studies using measured GFR (inulin or iothalamate clearance) unadjusted for BSA only. Study quality was evaluated using the Newcastle-Ottawa Scale.

Results

32 observational studies met our inclusion criteria, and 30 studies were included in the meta-analysis. No matter in dichotomous data or in dichotomous data, there were statistically significant reduction in hyperfiltration, albuminuria and proteinuria after bariatric surgery.

Limitations

The main limitation of this meta-analysis is the lack of randomized controlled trials (RCTs). Another limitation is the lack of long-term follow-up.

Conclusions

Bariatric surgery could prevent further decline in renal function by reducing proteinuria, albuminuria and improving glomerular hyperfiltration in obese patients with impaired renal function. However, whether bariatric surgery reverses CKD or delays ESRD progression is still in question, large, randomized prospective studies with a longer follow-up are needed.

Citation: Li K, Zou J, Ye Z, Di J, Han X, Zhang H, et al. (2016) Effects of Bariatric Surgery on Renal Function in Obese Patients: A Systematic Review and Meta Analysis. PLoS ONE 11(10): e0163907. https://doi.org/10.1371/journal.pone.0163907

Editor: Jaap A. Joles, University Medical Center Utrecht, NETHERLANDS

Received: June 20, 2016; Accepted: September 18, 2016; Published: October 4, 2016

Copyright: © 2016 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and its Supporting Information files.

Funding: The authors received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Obesity is a growing problem in the world and is associated with highly elevated risks of adverse health outcomes. The Non-Communicable Diseases Risk Factor Collaboration revealed that between 1975 and 2014 the prevalence of obesity increased from 3.2% to 10.8% in men and from 6.4% to 14.9% in women in their pooled analysis of 1698 population-based studies including more than 19 million participants [1]. Also, obesity is a strong trigger of diabetes mellitus (DM), dyslipidemia, hypertension and metabolic syndrome which are strong risk factors for the development and progression of chronic kidney disease (CKD)[2, 3].

Bariatric surgery has been approved as an effective treatment that achieves dramatic and durable weight loss in obese patients [4]. Several studies have shown impressive improvements in hypertension, dyslipidemia as well as diabetic complications following bariatric surgery [5, 6]. However, the effects of weight loss and improved metabolic disorder on renal diseases after bariatric surgery have been poorly evaluated.

Extreme obesity is responsible for glomerulosclerosis [7]. Renal diseases in the setting of obesity often manifest albuminuria, proteinuria, glomerular hyperfiltration and decreased glomerular filtration rate (GFR)[8, 9]. Although many retrospective studies have shown improvement in proteinuria and impaired GFR, results vary in effect size, type of outcome, and precision. Several systematic reviews explored the effects of dietary restriction, weight-loss drug or exercise on renal function in obese subjects with or without CKD [10–12], and some meta-analysis researched the effects of bariatric surgery on albuminuria, proteinuria included cohorts with either normal range, nephrotic range or both [13, 14]. Also, some reviews only reported descriptive outcomes from each study without calculating a pooled effect size of proteinuria and impaired GFR. Thus, to quantitatively summarize existing evidences regarding the effects of bariatric surgery on nephrotic range albuminuria, proteinuria and impaired GFR, we performed a systematic review and meta-analysis of observational studies to find whether bariatric surgery could ameliorate nephrotic range albuminuria or proteinuria and reverse hyperfiltration or hypofiltration in obese individuals with impaired renal function.

Materials and Methods

Study Design

A systematic review and meta-analysis was conducted according to predefined guidelines provided by the Cochrane Collaboration (2008)[15]. All data were reported according to Meta-analysis Of Observational Studies in Epidemiology statement [16].

Search Strategy

Two authors (Kun Li, Jianan Zou) independently searched published studies indexed in the MEDLINE, EMBASE, web of science and the Cochrane Central Register of Controlled Trials (CENTRAL) in The Cochrane Library. References of all selected studies were also examined. The following main search terms were used: bariatric surgery, gastric bypass, sleeve gastrectomy, gastroplasty, biliopancreatic diversion, weight loss, kidney disease, obese, albuminuria, proteinuria, microalbuminuria, macroalbuminuria, renal function, glomerular filtration rate and creatinine. The latest date for this search was March, 2016.

Inclusion and exclusion criteria

This review included all published randomized controlled trials or observational studies including cohort, cross-sectional, and case-control studies that assessed the effects of bariatric surgery on impaired renal function in obese patients. Reviews, case reports, abstracts, and unpublished studies were excluded.

Two reviewers (Kun Li, Jianan Zou) independently screened all abstracts and selected studies in the meta-analysis if they met all of the following criteria: (1) randomized, controlled trial (RCT) or observational study; (2) minimum intervention period of 4 weeks; (3) studies aimed to analyze the impact of bariatric surgery in obese patients with hypofiltration; (4) studies that analyzed the effects of bariatric surgery in obese patients with micro- or macroalbuminuria or proteinuria and (5) studies that analyzed the impact of bariatric surgery on GFR in obese patients with glomerular hyperfiltration; (6) reports of pre- and post-surgery mean values (if not available, change from baseline values were used) with standard deviation (or basic data to calculate these parameters: standard error, 95% confidence interval, p-values). If data of ongoing studies were published as updates, results of only the longest duration periods were included. For studies without the outcomes we needed, author(s) would be contacted via e-mail for more relevant information, if necessary. In studies that analyzed multiple interventions, only data conducted by bariatric surgery were considered for inclusion.

All studies analyzing glomerular hyperfiltration were divided into four subgroups: mGFR, CrCl, eGFR with and without BSA, and they were analysed separately. Serum creatinine varies with both GFR and muscle mass, so eGFR and CrCl are influenced by both true GFR and muscle mass. The use of serum creatinine-based equations is problematic following bariatric surgery. In addition, eGFR and mGFR values adjusted for BSA lead to a systematic underestimation of GFR in patients with severe obesity [17]. Thus CrCl, eGFR with and without BSA are all clearly unreliable. In our review, we draw conclusions from studies using measured GFR (inulin or iothalamate clearance) without adjusted for BSA only.

Renal function impairment was considered as the stable presence of one or more of the following conditions: (i) GFR <90 mL/min (hypofiltration) (ii) GFR >125 mL/min (hyperfiltration), (iii) pathological proteinuria or albuminuria. As long as the population in the studies fulfilled the above criteria, they were included in this review. Obesity was defined as BMI >30 kg/m2 and hyperfiltration was defined as GFR>125 mL/min. GFR between 60 and 90 mL/min was considered as slightly impaired glomerular function [18]. Albuminuria was classified as microalbuminuria and macroalbuminuria. Microalbuminuria is defined as urinary albumin-to-creatinine ratio (UACR) between 30 and 300 mg/g of creatinine or 24-h albuminuria between 30 and 300 mg. Macroalbuminuria is defined as UACR>300 mg/g of creatinine or 24-h albuminuria>300 mg/g. 24-h proteinuria>0.15 g and 24-h albuminuria>30 mg were considered pathologic range.

Exclusion criteria were (1) reviews, comments, case reports and case series, (2) studies that analyzed the effects of bariatric surgery in dialysis patients, and (3) studies that assessed the impacts of bariatric surgery on albumin excretion in obese subjects with normal albuminuria. In studies that enrolled both patients with normal GFR and impaired GFR, only data relating to impaired GFR were included in the analysis. Similarly, in studies that enrolled both patients with normal albuminuria and microalbuminuria, only data pertaining to patients with microalbuminuria (when available) were extracted.

Data extraction

Two investigators (Kun Li, Jianan Zou) independently reviewed abstracts of all citations. Data verifications between the two authors were performed to ensure reliability and completeness after all abstracts were reviewed. The inclusion criteria were applied to all identified studies independently. Different decisions were resolved by consensus.

Full texts of potentially relevant articles identified through other sources were retrieved. If multiple articles from the same study were searched, only the article with the longest follow-up period was included. Data with respect to research design, type of surgery, participant characteristics, duration of study, and outcome were independently extracted. We contacted the authors for the primary reports of the unpublished data. If the authors did not reply, the available data were used for our analyses.

Methodological Quality Assessment

We used the nine-point Newcastle-Ottawa Scale to assess the study quality for all included observational studies. This scale evaluated a quality score calculated on three fundamental methodological criteria: study participants (0–4), adjustment for confounding (0–2) or ascertainment of the exposure or outcome of interest (0–3). We arbitrarily classified quality as high (score: 7–9) versus low (score: 0–3). We excluded studies from our meta-analysis if they had poor quality. Discrepant opinions between authors were resolved to reach a consensus.

Statistical Analysis

The data were pooled using REVMAN 5.0 software (The Nordic Cochrane Centre, Copenhagen, Denmark). For each study, we calculated Relative Risk (RR) with 95% Confidence Intervals (CIs) for dichotomous data and Standardised Mean Difference (SMD) with 95% CIs for continuous data. A Random-effect model (DerSimonian-Laird method) was used when significant heterogeneity was detected between studies (P<0.10; I2>50%). Otherwise, a Fixed-effect model (Mantel-Haenszel test) was used. To assess the stability of the results of the meta-analysis, sensitivity analysis was performed. Publication bias was assessed by the Egger’s test and represented graphically by funnel plots.

Results

Description of included studies

After excluding duplicate results, the initial search included 681 articles, 661 articles were excluded because 336 were off the topic after scanning the title and/or the abstract, 147 were not RCT or observational studies, 93 did not include obese patients with impaired renal function, and 73 did not measure hyperfiltration, hypofiltration, albuminuria or proteinuria as an outcome. 32 observational studies met our inclusion criteria, and 30 studies were included in the meta-analysis (Fig 1) and the characteristics are outlined in Table 1.

thumbnail
Download:
Table 1. Study details and patient demographics.

https://doi.org/10.1371/journal.pone.0163907.t001

thumbnail
Download:
Fig 1. Flow diagram of the selection process.

RCT: randomized, controlled trial.

https://doi.org/10.1371/journal.pone.0163907.g001

Quality assessment of included studies

NOS evaluated the quality of the included studies. Total score ranged from 4 to 8. None of the studies had low quality (total score below 3) and excluded from the meta-analysis.

Meta-analysis results

Due to their outcomes could not be combined with other studies, 2 studies [41, 48] were excluded from meta-analysis. 14 studies of 1186 patients with dichotomous data [21, 23, 24, 26, 27, 29, 32–34, 38, 42, 43, 45, 51] and 10 studies of 930 patients with continuous data [24, 25, 29, 33, 36, 37, 46, 47, 49, 50] were included in the meta-analysis of albuminuria and proteinuria. There were only 5 studies of 184 patients [25, 26, 28, 40, 44] in the review of CKD II. Due to 3 studies [26, 39, 43] using CrCl, eGFR with and without adjustment for BSA, the continuous data could not be combined in the meta-analysis of CKD III. Furthermore, 9 studies of 631 patients with continuous data [19, 20, 23, 26, 31, 32, 35, 44, 52] and 6 studies of 514 patients with dichotomous data [23, 29, 32, 33, 35, 53] were included in the meta-analysis of hyperfiltration.

The dichotomous data presented in Fig 2 show there was a statistically significant reduction in hyperfiltration after bariatric surgery (RR: 0.46, 95% CI 0.26–0.82, P = 0.008; I2 = 76%; Pheterogeneity = 0.001) (Fig 2). The continuous data presented in Fig 3 were divided into four subgroups. Meta-analysis showed statistically significant decrease in mGFR, CrCl, eGFR with and without adjustment for BSA after bariatric surgery (SMD: -1.62, 95% CI: -2.63 –-0.60, P = 0.002; I2 = 57%; Pheterogeneity = 0.1; SMD: -0.54, 95% CI: -1.03 –-0.04, P = 0.03; I2 = 82%; Pheterogeneity = 0.0007; SMD: -0.55, 95% CI: -0.84 –-0.27, P = 0.0001; I2 = 0%; Pheterogeneity = 0.89; SMD: -0.44, 95% CI: -0.62 –-0.27, P< 0.0001; I2 = 0%; Pheterogeneity = 0.83; respectively) (Fig 3).

thumbnail
Download:
Fig 2. Forest plot comparing glomerular hyperfiltration (dichotomous data) between presurgery and postsurgery.

unadj/BSA: unadjusted for BSA; adj/BSA: adjusted for BSA.

https://doi.org/10.1371/journal.pone.0163907.g002

thumbnail
Download:
Fig 3. Forest plot comparing glomerular hyperfiltration (continuous data) between presurgery and postsurgery.

mGFR: measured glomerular filtration rate; eGFR: estimated glomerular filtration rate; Crcl: creatinine clearance; BSA: body surface area; unadj/BSA: unadjusted for BSA; adj/BSA: adjusted for BSA.

https://doi.org/10.1371/journal.pone.0163907.g003

Likewise, we found statistically significant increase in eGFR with and without adjustment for BSA after bariatric surgery (SMD: 1.04, 95% CI: 0.71–1.37, P< 0.0001; I2 = 0%; Pheterogeneity = 0.32; SMD: 3.84, 95% CI: 0.81–6.87, P = 0.01; I2 = 98%; Pheterogeneity< 0.0001) (Fig 4).

thumbnail
Download:
Fig 4. Forest plot comparing CKD II (continuous data) between presurgery and postsurgery.

eGFR: estimated glomerular filtration rate; BSA: body surface area.

https://doi.org/10.1371/journal.pone.0163907.g004

There was a statistically significant reduction in the incidence of albuminuria and proteinuria after bariatric surgery (RR: 0.42, 95% CI: 0.36–0.50, P< 0.0001; I2 = 34%; Pheterogeneity = 0.10; RR: 0.31, 95% CI: 0.22–0.43, P< 0.0001; I2 = 0%; Pheterogeneity = 0.45; respectively) (Fig 5). In addition, the continuous data were presented in Fig 6. Meta-analysis showed statistically significant decrease in ACR and 24-h albuminuria after bariatric surgery (SMD: -2.33, 95% CI: -3.68 –-0.99, P = 0.0007; I2 = 99%; Pheterogeneity< 0.0001; SMD: -1.22, 95% CI: -1.93 –-0.51, P = 0.0007; I2 = 83%; Pheterogeneity< 0.0001; respectively) (Fig 5). Furthermore, there is statistically significant decrease in proteinuria after bariatric surgery (SMD: -1.39, 95% CI: -2.73 –-0.04, P = 0.04; I2 = 93%; Pheterogeneity< 0.0001) (Fig 6).

thumbnail
Download:
Fig 5. Forest plot comparing albuminuria and proteinuria (dichotomous data) between presurgery and postsurgery.

https://doi.org/10.1371/journal.pone.0163907.g005

thumbnail
Download:
Fig 6. Forest plot comparing albuminuria and proteinuria (continuous data) between presurgery and postsurgery.

DN3: Diabetic Nephropathy stages III; DN4: Diabetic Nephropathy stages IV; ACR: albumin-to-creatinine ratio.

https://doi.org/10.1371/journal.pone.0163907.g006

Sensitivity analysis

To assess the stability of the results of the meta-analysis of hyperfiltration, albuminuria and proteinuria, sensitivity analyses were conducted by excluding 1 study at a time. None of the results was significantly altered, indicating that our results were robust (Figs 7 and 8).

thumbnail
Download:
Fig 7. The sensitivity analysis of the results of the meta-analysis of the effect of bariatric surgery on glomerular hyperfiltration.

https://doi.org/10.1371/journal.pone.0163907.g007

thumbnail
Download:
Fig 8. The sensitivity analysis of the results of the meta-analysis of the effect of bariatric surgery on albuminuria and proteinuria.

https://doi.org/10.1371/journal.pone.0163907.g008

Publication bias

Because publication bias could affect the results of meta-analyses, we attempted to evaluate this potential publication bias by using funnel plots analysis and Egger’s test. Visualizing funnel plots for studies evaluating hyperfiltration, proteinuria and albuminuria, suggested a symmetric distribution of studies around the effect size and the Egger’s test confirmed the lack of publication bias in proteinuria and albuminuria (P = 0.562).

Discussion

The earliest study about the effect of bariatric surgery on renal function was published in 1980. Over the last 3 decades, the outcomes of bariatric surgery in obese patients with regard to mediating sustained weight reduction have been extensively evaluated. It is necessary to conduct a systematic review and meta-analysis assessing the effects of bariatric surgery on improvement of renal parameters in obese patients with impaired renal function. All studies included in our article investigated either the change of glomerular filtration capacity or the reduction in amount of urinary albumin or protein excretion in obese patients after bariatric surgery. Although several studies had relatively small sample size or loss of follow-up, there was statistically significant improvement of all parameters in obese patients with impaired renal function after bariatric surgery. There is a lack of long-term studies that analyzed the impact of bariatric surgery on the progressive of ESRD and mortality.

Obesity has been regarded as an independent risk factor for chronic kidney disease [54–56]. Several studies showed that glomerular hyperfiltration caused by obesity reflected loss of renal functional reserve and contributed to the development and progressive of CKD [57, 58]. Firstly, glomerulomegaly and focal glomerulosclerosis have been closely associated with obesity in order to meet increased metabolic demands in morbidly obese patients. These disorders are characterized by hyperfiltration, which leads to segmental scarring and worsen renal function. Secondly, abnormalities in vascular control associated with afferent renal vasodilation and increased renal blood flow might lead to the development of glomerular hyperfiltration in obese patients with diabetes. In the subgroup analysis of obese patients with glomerular hyperfiltration, using CrCl, eGFR with or without adjusted for BSA, a significant decrease in CrCl and eGFR (adjusted and unadjusted for BSA) was seen after bariatric surgery. However, firm conclusions cannot be drawn due to likely confounding effects of changes in muscle mass and protein intake on serum creatinine. In addition, eGFR and mGFR values adjusted for BSA lead to a systematic underestimation of GFR in patients with severe obesity [17], thus they are clearly unreliable with adjusted for BSA. In our review, we draw conclusions from studies using measured GFR (inulin or iothalamate clearance) unadjusted for BSA only. We found a statistically significant decrease in mGFR, indicating that glomerular hyperfiltration was significantly improved in obese patients after bariatric surgery. However, whether this normalization in hyperfiltration could translate into long-term renal benefits remains to be seen.

The association between obesity and CKD may be mediated through multiple biologic mechanisms. Excess adipose tissue can lead to the activation of the sympathetic nervous and renin-angiotensin systems, as well as lipid deposition, hyperfiltration, and increased sodium absorption in the kidneys, resulting in a feedback loop where obesity-induced declines in kidney function lead to the development of hypertension, which results in further damage to the kidneys [59, 60]. Pathways leading from obesity to diabetes have also been identified, including the development of insulin resistance through the disruption of insulin signaling pathways due to lipolysis, the release of adipokines [61] and inflammation [62]. In the morbidly obese population, weight loss that is attained through bariatric surgery results in an improvement in insulin resistance, oxidative stress, and inflammation [63, 64]. These improvements may contribute to the observed better outcomes after bariatric surgery in obese patients with CKD [25, 28]. As for CKD patients, the perioperative period is a time of considerable increase stress originating from fluid and hemodynamic shifts that can lead to acute kidney failure, and cardiac risk factors including angina, myocardial infarction, congestive heart failure, and DM have an intermediate probability of increased perioperative risk [65]. This may be the main reason why few patients have been included with advanced CKD in observational studies so far published. Several studies suggested that obese patients with CKD II and III could benefit from the improvement of GFR after bariatric surgery [25, 26, 28, 40, 44] and we found statistically significant increase in eGFR postoperatively. Because they used eGFR with or without adjusted for BSA to estimate glomerular filtration capacity, the results were still worth discussing. Inulin clearances have been regarded as the gold standard of GFR. So to assess whether there is a beneficial effect of bariatric surgery on kidney function of CKD patients requires further studies with larger sample size and longer duration of follow-up and GFR must be measured with exogenous glomerular filtration tracers.

Although GFR is the backbone of the current CKD classification and a low GFR is an important risk factor for end-stage renal disease (ESRD) [18], the impact of albuminuria for cardiovascular disease and CKD is significantly remarkable [66]. It is suggested that microalbuminuria was a sign of vascular damage and macroalbuminuria is evidence of a diseased glomerulus, so albuminuria has been considered as an independent risk factor of cardiovascular events and ESRD [67]. Several studies have consistently shown that GFR and ACR complement each other very well and both a higher albuminuria and a lower GFR provide synergistic, complementary risk-stratification for both CKD and cardiovascular disease [66, 68, 69]. Albuminuria comes from diabetes mellitus (DM), thus, remission of diabetes may affect the improvement of renal function after bariatric surgery. Our review revealed that the bariatric surgery could remarkably reduce urinary albumin and protein excretion in obese patients.

The heterogeneity between studies analyzing glomerular hyperfiltration, proteinuria and albuminuria were statistically significant. This heterogeneity was further explored in the sensitivity analysis, which suggested our results were robust. We believed that the observed heterogeneity in our meta-analysis was mainly attributed to differences in population, duration of obesity, study design, follow-up, sample size or co-morbidities.

Our review has some strengths and limitations. Strengths included the comprehensive search method, data extraction and study quality assessment made by two independent reviewers. There are also some limitations in our study. First, although comprehensive search strategies focused on bariatric surgery and a specific population (obese patients with impaired renal function) was implemented, this review is subject to publication bias inevitably. Second, most of the included studies are observational reports, which are of suboptimal quality and subject to selection bias. Third, randomized controlled studies of bariatric surgery compared with non-surgical weight loss or medical intervention are needed. Finally, the effect of bariatric surgery on kidney function of CKD patients requires further studies and GFR must be measured with inulin clearance. Further prospective studies are also needed to measure long-term effects of bariatric surgery in obese patients with impaired renal function.

Conclusions

In conclusion, bariatric surgery could prevent further decline in renal function by reducing proteinuria, albuminuria and improving glomerular hyperfiltration in obese patients with impaired renal function. However, whether bariatric surgery reverses CKD or delays ESRD progression is still in question, large, randomized prospective studies with a longer follow-up are needed.

Supporting Information

S1 Fig. Funnel plot to assess publication.

Funnel plot to assess publication for the most frequently reported outcome glomerular hyperfiltration. mGFR: measured glomerular filtration rate; eGFR: estimated glomerular filtration rate; Crcl: creatinine clearance; BSA: body surface area.

https://doi.org/10.1371/journal.pone.0163907.s001

(TIF)

S2 Fig. Funnel plot to assess publication.

Funnel plot to assess publication for the most frequently reported outcome albuminuria and proteinuria.

https://doi.org/10.1371/journal.pone.0163907.s002

(TIF)

S1 PRISMA Checklist. PRISMA Checklist.

https://doi.org/10.1371/journal.pone.0163907.s003

(DOC)

Author Contributions

  1. Conceptualization: KL.
  2. Data curation: KL JZ.
  3. Formal analysis: KL JZ.
  4. Investigation: KL JZ.
  5. Methodology: KL JZ ZY.
  6. Project administration: KL PZ.
  7. Software: JD XH HZ WL QR.
  8. Supervision: PZ.
  9. Writing – original draft: KL JZ.
  10. Writing – review & editing: PZ.

References

  1. 1. Collaboration NCDRF. 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. The Lancet. 2016;387:1377–96. pmid:27115820
  2. 2. Wahba IM, Mak RH. Obesity and obesity-initiated metabolic syndrome: mechanistic links to chronic kidney disease. Clinical Journal of the American Society of Nephrology. 2007;2:550–62. pmid:17699463
  3. 3. Tanner RM, Brown TM, Muntner P. Epidemiology of obesity, the metabolic syndrome, and chronic kidney disease. Current hypertension reports. 2012;14:152–9. pmid:22318504
  4. 4. Brolin RE. Bariatric surgery and long-term control of morbid obesity. Jama. 2002;288:2793–6. pmid:12472304
  5. 5. Schauer PR, Kashyap SR, Wolski K, Brethauer SA, Kirwan JP, Pothier CE, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. New England Journal of Medicine. 2012;366:1567–76. pmid:22449319
  6. 6. Mingrone G, Panunzi S, De Gaetano A, Guidone C, Iaconelli A, Leccesi L, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. New England Journal of Medicine. 2012;366:1577–85. pmid:22449317
  7. 7. Kambham N, Markowitz GS, Valeri AM, Lin J, D'Agati VD. Obesity-related glomerulopathy: an emerging epidemic. Kidney international. 2001;59:1498–509. pmid:11260414
  8. 8. Serra A, Romero R, Lopez D, Navarro M, Esteve A, Perez N, et al. Renal injury in the extremely obese patients with normal renal function. Kidney international. 2008;73:947–55. pmid:18216780
  9. 9. Verani RR. Obesity-associated focal segmental glomerulosclerosis: pathological features of the lesion and relationship with cardiomegaly and hyperlipidemia. American journal of kidney diseases. 1992;20:629–34. pmid:1462993
  10. 10. Schwingshackl L, Hoffmann G. Comparison of high vs. normal/low protein diets on renal function in subjects without chronic kidney disease: a systematic review and meta-analysis. PloS one. 2014;9:e97656. pmid:24852037
  11. 11. Van Huffel L, Tomson CR, Ruige J, Nistor I, Van Biesen W, Bolignano D. Dietary restriction and exercise for diabetic patients with chronic kidney disease: a systematic review. PloS one. 2014;9:e113667. pmid:25423489
  12. 12. Bolignano D, Zoccali C. Effects of weight loss on renal function in obese CKD patients: a systematic review. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association—European Renal Association. 2013;28 Suppl 4:iv82–98. pmid:24092846
  13. 13. Afshinnia F, Wilt TJ, Duval S, Esmaeili A, Ibrahim HN. Weight loss and proteinuria: systematic review of clinical trials and comparative cohorts. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association—European Renal Association. 2010;25:1173–83. pmid:19945950
  14. 14. Navaneethan SD, Yehnert H, Moustarah F, Schreiber MJ, Schauer PR, Beddhu S. Weight loss interventions in chronic kidney disease: a systematic review and meta-analysis. Clinical journal of the American Society of Nephrology: CJASN. 2009;4:1565–74. pmid:19808241
  15. 15. Higgins J, Altman DG. Assessing risk of bias in included studies. Cochrane handbook for systematic reviews of interventions: Cochrane book series. 2008:187–241.
  16. 16. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Jama. 2000;283:2008–12. pmid:10789670
  17. 17. Wuerzner G, Pruijm M, Maillard M, Bovet P, Renaud C, Burnier M, et al. Marked association between obesity and glomerular hyperfiltration: a cross-sectional study in an African population. American Journal of Kidney Diseases. 2010;56:303–12. pmid:20538392
  18. 18. Levey AS, Eckardt K-U, Tsukamoto Y, Levin A, Coresh J, Rossert J, et al. Definition and classification of chronic kidney disease: a position statement from Kidney Disease: Improving Global Outcomes (KDIGO). Kidney international. 2005;67:2089–100. pmid:15882252
  19. 19. Brochner-Mortensen J, Rickers H, Balslev I. Renal function and body composition before and after intestinal bypass operation in obese patients. Scandinavian journal of clinical and laboratory investigation. 1980;40:695–702. pmid:7280549
  20. 20. Chagnac A, Weinstein T, Herman M, Hirsh J, Gafter U, Ori Y. The effects of weight loss on renal function in patients with severe obesity. Journal of the American Society of Nephrology: JASN. 2003;14:1480–6. pmid:12761248
  21. 21. Agrawal V, Khan I, Rai B, Krause KR, Chengelis DL, Zalesin KC, et al. The effect of weight loss after bariatric surgery on albuminuria. Clinical nephrology. 2008;70:194–202. pmid:18793560
  22. 22. Navaneethan SD, Yehnert H. Bariatric surgery and progression of chronic kidney disease. Surgery for obesity and related diseases: official journal of the American Society for Bariatric Surgery. 2009;5:662–5. pmid:19359221
  23. 23. Serpa Neto A, Bianco Rossi FM, Dal Moro Amarante R, Alves Buriti N, Cunha Barbosa Saheb G, Rossi M. Effect of weight loss after Roux-en-Y gastric bypass, on renal function and blood pressure in morbidly obese patients. Journal of nephrology. 2009;22:637–46. pmid:19809997
  24. 24. Amor A, Jimenez A, Moize V, Ibarzabal A, Flores L, Lacy AM, et al. Weight loss independently predicts urinary albumin excretion normalization in morbidly obese type 2 diabetic patients undergoing bariatric surgery. Surgical endoscopy. 2013;27:2046–51. pmid:23292561
  25. 25. Fenske WK, Dubb S, Bueter M, Seyfried F, Patel K, Tam FWK, et al. Effect of bariatric surgery-induced weight loss on renal and systemic inflammation and blood pressure: A 12-month prospective study. Surgery for Obesity and Related Diseases. 2013;9:559–68. pmid:22608055
  26. 26. Hou CC, Shyu RS, Lee WJ, Ser KH, Lee YC, Chen SC. Improved renal function 12 months after bariatric surgery. Surgery for obesity and related diseases: official journal of the American Society for Bariatric Surgery. 2013;9:202–6. pmid:23246320
  27. 27. Stephenson DT, Jandeleit-Dahm K, Balkau B, Cohen N. Improvement in albuminuria in patients with type 2 diabetes after laparoscopic adjustable gastric banding. Diabetes & vascular disease research. 2013;10:514–9. pmid:23975723
  28. 28. Ruiz-Tovar J, Giner L, Sarro-Sobrin F, Alsina ME, Marco MP, Craver L. Laparoscopic Sleeve Gastrectomy Prevents the Deterioration of Renal Function in Morbidly Obese Patients Over 40 Years. Obesity surgery. 2014. pmid:25385417
  29. 29. Kim EY, Kim YJ. Does bariatric surgery really prevent deterioration of renal function? Surgery for obesity and related diseases: official journal of the American Society for Bariatric Surgery. 2015. pmid:26823090
  30. 30. Liu J, Wu Y, Hu ZB, Liu L, Liu BC, Miras AD, et al. Type 2 diabetes mellitus and microvascular complications 1 year after Roux-en-Y gastric bypass: a case-control study. American journal of physiology Endocrinology and metabolism. 2015;58:1443–7. pmid:25893730
  31. 31. Ngoh CL, So JB, Tiong HY, Shabbir A, Teo BW. Effect of weight loss after bariatric surgery on kidney function in a multiethnic Asian population. Surgery for obesity and related diseases: official journal of the American Society for Bariatric Surgery. 2015. pmid:26522229
  32. 32. Navarro-Diaz M, Serra A, Romero R, Bonet J, Bayes B, Homs M, et al. Effect of drastic weight loss after bariatric surgery on renal parameters in extremely obese patients: long-term follow-up. Journal of the American Society of Nephrology: JASN. 2006;17:S213–7. pmid:17130264
  33. 33. Reid TJ, Saeed S, McCoy S, Osewa AA, Persaud A, Ahmed L. The effect of bariatric surgery on renal function. Surgery for obesity and related diseases: official journal of the American Society for Bariatric Surgery. 2014;10:808–13. pmid:25304831
  34. 34. Palomar R, Fernandez-Fresnedo G, Dominguez-Diez A, Lopez-Deogracias M, Olmedo F, Martin de Francisco AL, et al. Effects of weight loss after biliopancreatic diversion on metabolism and cardiovascular profile. Obesity surgery. 2005;15:794–8. pmid:15978149
  35. 35. Lieske JC, Collazo-Clavell ML, Sarr MG, Rule AD, Bergstralh EJ, Kumar R. Gastric bypass surgery and measured and estimated GFR in women. American Journal of Kidney Diseases. 2014;64:663–5. pmid:25085645
  36. 36. Zhang H, Di J, Yu H, Han X, Li K, Zhang P. The Short-Term Remission of Diabetic Nephropathy After Roux-en-Y Gastric Bypass in Chinese Patients of T2DM with Obesity. Obesity surgery. 2015;25:1263–70. pmid:25925612
  37. 37. Mohan S, Tan J, Gorantla S, Ahmed L, Park CM. Early improvement in albuminuria in non-diabetic patients after Roux-en-Y bariatric surgery. Obesity surgery. 2012;22:375–80. pmid:21590347
  38. 38. Celik F, Ahdi M, Meesters EW, van de Laar A, Brandjes DP, Gerdes VE. The longer-term effects of Roux-en-Y gastric bypass surgery on sodium excretion. Obesity surgery. 2013;23:358–64. pmid:22983770
  39. 39. Gonzalez-Heredia R, Patel N, Masrur M, Murphey M, Patton K, Elli EF. Does bariatric surgery improve renal function? Bariatric Surgical Practice and Patient Care. 2016;11:6–10.
  40. 40. Zakaria AS, Rossetti L, Cristina M, Veronelli A, Lombardi F, Saibene A, et al. Effects of gastric banding on glucose tolerance, cardiovascular and renal function, and diabetic complications: a 13-year study of the morbidly obese. Surgery for obesity and related diseases: official journal of the American Society for Bariatric Surgery. 2015. pmid:26826918
  41. 41. Friedman AN, Moe S, Fadel WF, Inman M, Mattar SG, Shihabi Z, et al. Predicting the glomerular filtration rate in bariatric surgery patients. American journal of nephrology. 2014;39:8–15. pmid:24356416
  42. 42. Heneghan HM, Cetin D, Navaneethan SD, Orzech N, Brethauer SA, Schauer PR. Effects of bariatric surgery on diabetic nephropathy after 5 years of follow-up. Surgery for obesity and related diseases: official journal of the American Society for Bariatric Surgery. 2013;9:7–14. pmid:23211651
  43. 43. Navaneethan SD, Kelly KR, Sabbagh F, Schauer PR, Kirwan JP, Kashyap SR. Urinary albumin excretion, HMW adiponectin, and insulin sensitivity in type 2 diabetic patients undergoing bariatric surgery. Obesity surgery. 2010;20:308–15. pmid:20217955
  44. 44. Abouchacra S, Chaaban A, Gebran N, Hussein Q, Ahmed M, Bernieh B, et al. GFR estimation in the morbidly obese pre- and postbariatric surgery: one size does not fit all. International urology and nephrology. 2013;45:157–62. pmid:22388750
  45. 45. Iaconelli A, Panunzi S, De Gaetano A, Manco M, Guidone C, Leccesi L, et al. Effects of bilio-pancreatic diversion on diabetic complications: a 10-year follow-up. Diabetes care. 2011;34:561–7. pmid:21282343
  46. 46. Kumar KV, Ugale S, Gupta N, Naik V, Kumar P, Bhaskar P, et al. Ileal interposition with sleeve gastrectomy for control of type 2 diabetes. Diabetes technology & therapeutics. 2009;11:785–9. pmid:20001679
  47. 47. SunilKumar K, Surendra U, Neeraj G, Vishwas N, SivaKrishna K, Kvshari K, et al. Remission of type 2 diabetes mellitus by ileal interposition with sleeve gastrectomy. International Journal of Endocrinology and Metabolism. 2011;2011:374–81.
  48. 48. Miras AD, Chuah LL, Lascaratos G, Faruq S, Mohite AA, Shah PR, et al. Bariatric surgery does not exacerbate and may be beneficial for the microvascular complications of type 2 diabetes. Diabetes care. 2012;35:e81. pmid:23173142
  49. 49. Zeve JL, Tomaz CA, Nassif PA, Lima JH, Sansana LR, Zeve CH. Obese patients with diabetes mellitus type 2 undergoing gastric bypass in Roux-en-Y: analysis of results and its influence in complications. Arquivos brasileiros de cirurgia digestiva: ABCD = Brazilian archives of digestive surgery. 2013;26 Suppl 1:47–52. pmid:24463899
  50. 50. Saliba J, Kasim NR, Tamboli RA, Isbell JM, Marks P, Feurer ID, et al. Roux-en-Y gastric bypass reverses renal glomerular but not tubular abnormalities in excessively obese diabetics. Surgery. 2010;147:282–7. pmid:20004430
  51. 51. Miras AD, Chuah LL, Khalil N, Nicotra A, Vusirikala A, Baqai N, et al. Type 2 diabetes mellitus and microvascular complications 1 year after Roux-en-Y gastric bypass: a case-control study. Diabetologia. 2015;58:1443–7. pmid:25893730
  52. 52. Getty JL, Hamdallah IN, Shamseddeen HN, Wu J, Low RK, Craig J, et al. Changes in renal function following Roux-en-Y gastric bypass: a prospective study. Obesity surgery. 2012;22:1055–9. pmid:22318447
  53. 53. Friedman AN, Quinney SK, Inman M, Mattar SG, Shihabi Z, Moe S. Influence of dietary protein on glomerular filtration before and after bariatric surgery: A cohort study. American Journal of Kidney Diseases. 2014;63:598–603. pmid:24387796
  54. 54. Declèves A-E, Sharma K. Obesity and kidney disease: differential effects of obesity on adipose tissue and kidney inflammation and fibrosis. Current opinion in nephrology and hypertension. 2015;24:28–36. pmid:25470014
  55. 55. Wickman C, Kramer H. Obesity and kidney disease: potential mechanisms. Seminars in nephrology: Elsevier; 2013. p. 14–22. pmid:23374890
  56. 56. Hall ME, do Carmo JM, da Silva AA, Juncos LA, Wang Z, Hall JE. Obesity, hypertension, and chronic kidney disease. International journal of nephrology and renovascular disease. 2014;7:75–88. pmid:24600241
  57. 57. Helal I, Fick-Brosnahan GM, Reed-Gitomer B, Schrier RW. Glomerular hyperfiltration: definitions, mechanisms and clinical implications. Nature Reviews Nephrology. 2012;8:293–300. pmid:22349487
  58. 58. Chagnac A, Herman M, Zingerman B, Erman A, Rozen-Zvi B, Hirsh J, et al. Obesity-induced glomerular hyperfiltration: its involvement in the pathogenesis of tubular sodium reabsorption. Nephrology Dialysis Transplantation. 2008;23:3946–52. pmid:18622024
  59. 59. Aneja A, El-Atat F, McFarlane SI, Sowers JR. Hypertension and obesity. Recent progress in hormone research. 2004;59:169–206. pmid:14749502
  60. 60. Zalesin KC, McCullough PA. Bariatric surgery for morbid obesity: risks and benefits in chronic kidney disease patients. Advances in chronic kidney disease. 2006;13:403–17. pmid:17045226
  61. 61. Rosenberg DE, Jabbour SA, Goldstein BJ. Insulin resistance, diabetes and cardiovascular risk: approaches to treatment. Diabetes, Obesity and Metabolism. 2005;7:642–53. pmid:16219008
  62. 62. Fantuzzi G. Adipose tissue, adipokines, and inflammation. Journal of Allergy and Clinical Immunology. 2005;115:911–9. pmid:15867843
  63. 63. Neff KJ, O’Donohoe PK, le Roux CW. Anti-inflammatory effects of gastric bypass surgery and their association with improvement in metabolic profile. Expert Review of Endocrinology & Metabolism. 2015;10:435–46.
  64. 64. Neff KJ, le Roux CW. Metabolic Effects of Bariatric Surgery: A Focus on Inflammation and Diabetic Kidney Disease. Current Obesity Reports. 2013;2:120–7.
  65. 65. Jones DR, Lee HT. Surgery in the patient with renal dysfunction. Medical Clinics of North America. 2009;93:1083–93. pmid:19665621
  66. 66. Hallan SI, Ritz E, Lydersen S, Romundstad S, Kvenild K, Orth SR. Combining GFR and albuminuria to classify CKD improves prediction of ESRD. Journal of the American Society of Nephrology. 2009;20:1069–77. pmid:19357254
  67. 67. Gansevoort RT, de Jong PE. The case for using albuminuria in staging chronic kidney disease. Journal of the American Society of Nephrology. 2009;20:465–8. pmid:19255126
  68. 68. Johnson DW, Jones GR, Mathew TH, Ludlow MJ, Chadban SJ, Usherwood T, et al. Chronic kidney disease and measurement of albuminuria or proteinuria: a position statement. The Medical journal of Australia. 2012;197:224–5. pmid:22900872
  69. 69. Chronic Kidney Disease Prognosis C. Association of estimated glomerular filtration rate and albuminuria with all-cause and cardiovascular mortality in general population cohorts: a collaborative meta-analysis. The Lancet. 2010;375:2073–81. pmid:20483451