Abstract
Background
Bariatric surgery reduces incidence of albuminuria and end-stage renal disease in patients with obesity. Effects of bariatric surgery on long-term remission and progression of pre-existing obesity-related renal damage are mainly unexplored. Here we investigate the long-term effects of bariatric surgery compared with conventional obesity care on remission and progression of albuminuria.
Methods
4047 patients were included in the Swedish Obese Subjects study. Inclusion criteria were age 37–60 years, BMI ≥ 34 kg/m2 in men and BMI ≥ 38 kg/m2 in women. Our analysis comprised 803 patients (19.8% of total population, 357 control, 446 surgery) with pre-existing albuminuria including 693 patients (312 control, 381 surgery) with microalbuminuria, and 110 patients (45 control, 65 surgery) with macroalbuminuria. Surgery patients were treated with banding, vertical banded gastroplasty, or gastric bypass. Control patients received conventional obesity care.
Results
Total urinary albumin excretion was 36.5% lower in all patients with albuminuria after 15 years, 44.5% lower in patients with microalbuminuria after 15 years, and 27.8% lower in patients with macroalbuminuria after 2 years following bariatric surgery compared with conventional care. In surgery patients with microalbuminuria, remission to normoalbuminuria was higher (OR, 5.9, 2.2, 3.2, p < 0.001) and progression to macroalbuminuria was lower (OR, 0.28, 0.26, 0.25, p ≤ 0.02) at 2, 10, and 15 years, respectively, compared with control patients. In surgery patients with macroalbuminuria remission to normo- or microalbuminuria was higher (OR, 3.67, p = 0.003) after 2 years. No differences between surgery and control patients with macroalbuminuria were observed after 10 and 15 years. Surgery slowed progression of eGFR decline after 2 years in patients with microalbuminuria and macroalbuminuria (treatment effect: 1.0 ml/min/1.73 m2/year, p = 0.001 and 1.4 ml/min/1.73 m2/year, p = 0.047, respectively).
Conclusion
Bariatric surgery had better effects than conventional obesity care on remission of albuminuria and prevention of eGFR decline, indicating that patients with obesity-related renal damage benefit from bariatric surgery.
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References
Kazancioğlu R. Risk factors for chronic kidney disease: an update. Kidney Int Suppl (2011). 2013;3:368–71.
Hunley TE, Ma LJ, Kon V. Scope and mechanisms of obesity-related renal disease. Curr Opin Nephrol Hypertens. 2010;19:227–34.
Ejerblad E, Fored CM, Lindblad P, Fryzek J, McLaughlin JK, Nyrén O Obesity and risk for chronic renal failure. J Am Soc Nephrol. 2006;17:1695–702.
Bray GA Medical consequences of obesity. J Clin Endocrinol Metab. 2004;89:2583–9.
Mokdad AH, Ford ES, Bowman BA Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. JAMA. 2003;289:76–9.
Rhéaume C, Arsenault BJ, Bélanger S, Pérusse L, Tremblay A, Bouchard C Low cardiorespiratory fitness levels and elevated blood pressure: what is the contribution of visceral adiposity? Hypertension. 2009;54:91–8.
Docherty NG, le Roux CW Bariatric surgery for the treatment of chronic kidney disease in obesity and type 2 diabetes. Nat Rev Nephrol. 2020, published on-line.
Stefansson VT, Schei J, Jenssen TG, Melsom T, Eriksen BO. Central obesity associates with renal hyperfiltration in the non-diabetic general population: a cross-sectional study. BMC Nephrol. 2016;17:172.
Trevisan R, Dodesini AR. The hyperfiltering kidney in diabetes. Nephron. 2017;136:277–80.
Frederich RC, Kahn BB, Peach MJ, Flier JS. Tissue-specific nutritional regulation of angiotensinogen in adipose tissue. Hypertension. 1992;19:339–44.
Schorr U, Blaschke K, Turan S, Distler A, Sharma AM. Relationship between angiotensinogen, leptin and blood pressure levels in young normotensive men. J Hypertens. 1998;16:1475–80.
Goodfriend TL, Ball DL, Egan BM, Campbell WB, Nithipatikom K. Epoxy-keto derivative of linoleic acid stimulates aldosterone secretion. Hypertension. 2004;43:358–63.
Santini E, Lupi R, Baldi S, Madec S, Chimenti D, Ferrannini E, et al. Effects of different LDL particles on inflammatory molecules in human mesangial cells. Diabetologia. 2008;51:2117–25.
Bussolati B, Deregibus MC, Fonsato V, Doublier S, Spatola T, Procida S, et al. Statins prevent oxidized LDL-induced injury of glomerular podocytes by activating the phosphatidylinositol 3-kinase/AKT-signaling pathway. J Am Soc Nephrol. 2005;16:1936–47.
Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Investig. 2007;117:175–84.
Kato S, Nazneen A, Nakashima Y, Razzaque MS, Nishino T, Furusu A, et al. Pathological influence of obesity on renal structural changes in chronic kidney disease. Clin Exp Nephrol. 2009;13:332–40.
Praga M, Morales E. Obesity, proteinuria and progression of renal failure. Curr Opinion Nephrol Hypertens. 2006;15:481–6.
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 Int. 2008;73:947–55.
Grams ME, Sang Y, Ballew SH, Matsushita K, Astor BC, Carrero JJ, et al. Evaluating glomerular filtration rate slope as a surrogate end point for ESKD in clinical trials: an individual participant meta-analysis of observational data. J Am Soc Nephrol. 2019;30:1746.
Levey AS, Gansevoort RT, Coresh J, Inker LA, Heerspink HL, Grams ME, et al. Change in albuminuria and GFR as end points for clinical trials in early stages of CKD: A Scientific Workshop Sponsored by the National Kidney Foundation in Collaboration With the US Food and Drug Administration and European Medicines Agency. Am J Kidney Dis. 2020;75:84–104.
Sjöström L, Peltonen M, Jacobson P Bariatric surgery and long-term cardiovascular events. JAMA. 2012;307:56–65.
Carlsson LMS, Peltonen M, Ahlin S, Anveden A, Bouchard C, Carlsson B Bariatric surgery and prevention of type 2 diabetes in Swedish Obese Subjects. New Engl J Med. 2012;367:695–704.
Sjöström L, Peltonen M, Jacobson P, et al. Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascular and macrovascular complications. JAMA. 2014;311:2297–304.
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.
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. Surg Obesity Relat Dis. 2013;9:7–14.
Shulman A, Peltonen M, Sjöström CD, Andersson-Assarsson JC, Taube M, Sjöholm K, et al. Incidence of end-stage renal disease following bariatric surgery in the Swedish Obese Subjects Study. Int J Obesity. 2018;42:964–73.
Li K, Zou J, Ye Z, Di J, Han X, Zhang H, et al. Effects of bariatric surgery on renal function in obese patients: a systematic review and meta analysis. PLOS ONE. 2016;11:e0163907.
Bilha SC, Nistor I, Nedelcu A, Kanbay M, Scripcariu V, Timofte D, et al. The effects of bariatric surgery on renal outcomes: a systematic review and meta-analysis. Obesity Surg. 2018;28:3815–33.
Nehus EJ, Khoury JC, Inge TH, Xiao N, Jenkins TM, Moxey-Mims MM, et al. Kidney outcomes three years after bariatric surgery in severely obese adolescents. Kidney Int. 2017;91:451–8.
Chao ATL, Chee Fang S, Lam BCC, Cheng AKS, Low SKM, Su Chi L. Effect of bariatric surgery on diabetic nephropathy in obese type 2 diabetes patients in a retrospective 2-year study: a local pilot. Diabetes Vascular Dis Res. 2017;15:139–44.
Agrawal V, Khan I, Rai B, Krause KR, Chengelis DL, Zalesin KC, et al. The effect of weight loss after bariatric surgery on albuminuria. Clin Nephrol. 2008;70:194–202.
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 Dis Res. 2013;10:514–9.
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.
Miras AD, Chuah LL, Khalil N, Nicotra A, Vusirikala A, Baqai N Type 2 diabetes mellitus and microvascular complications 1 year after Roux-en-Y gastric bypass: a case–control study. Diabetologia. 2015;58:1443–7.
Iaconelli A, Panunzi S, De Gaetano A, Manco M, Guidone C, Leccesi L, et al. Effects of bilio-pancreatic diversion on diabetic complications. Diabetes Care. 2011;34:561.
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.
Cohen RV, Pereira TV, Aboud CM, Petry TBZ, Lopes Correa JL, Schiavon CA, et al. Effect of gastric bypass vs best medical treatment on early-stage chronic kidney disease in patients with type 2 diabetes and obesity: a randomized clinical trial. JAMA Surg. 2020:e200420-e.
Xu R, Sun S, Huo Y, Yun L, Huang S, Li G, et al. Effects of ACEIs versus ARBs on proteinuria or albuminuria in primary hypertension: a meta-analysis of randomized trials. Medicine. 2015;94:e1560–e.
Kanasaki K. The role of renal dipeptidyl peptidase-4 in kidney disease: renal effects of dipeptidyl peptidase-4 inhibitors with a focus on linagliptin. Clin Sci. 2018;132:489–507.
von Scholten BJ, Persson F, Rosenlund S, Hovind P, Faber J, Hansen TW, et al. The effect of liraglutide on renal function: a randomized clinical trial. Diabetes Obesity Metab. 2017;19:239–47.
van der Aart-van der Beek AB, van Raalte DH, Guja C, Hoogenberg K, Suchower LJ, Hardy E, et al. Exenatide once weekly decreases urinary albumin excretion in patients with type 2 diabetes and elevated albuminuria: Pooled analysis of randomized active controlled clinical trials. Diabetes Obesity Metab. 2020;22:1556–66.
Pollock C, Stefánsson B, Reyner D, Rossing P, Sjöström CD, Wheeler DC, et al. Albuminuria-lowering effect of dapagliflozin alone and in combination with saxagliptin and effect of dapagliflozin and saxagliptin on glycaemic control in patients with type 2 diabetes and chronic kidney disease (DELIGHT): a randomised, double-blind, placebo-controlled trial. Lancet Diabetes Endocrinol. 2019;7:429–41.
Carlsson LMS, Romeo S, Jacobson P, Burza MA, Maglio C, Sjoholm K The incidence of albuminuria after bariatric surgery and usual care in swedish obese subjects (SOS): a prospective controlled intervention trial. Int J Obes. 2015;39:169–75.
Sjöström L, Larsson B, Backman L, Bengtsson C, Bouchard C, Dahlgren S Swedish obese subjects (SOS). Recruitment for an intervention study and a selected description of the obese state. Int J Obes Relat Metab Disord. 1992;16:465–79.
Sjöström L, Narbro K, Sjöström CD, Karason K, Larsson B, Wedel H, et al. Effects of bariatric surgery on mortality in swedish obese subjects. N Engl J Med. 2007;357:741–52.
Zenténius E, Andersson-Assarsson JC, Carlsson LMS, Svensson P-A, Larsson I. Self-reported weight-loss methods and weight change: ten-year analysis in the swedish obese subjects study control group. Obesity. 2018;26:1137–43.
Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF III, Feldman HI, et al. A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009;150:604–12.
Heerspink HJL, Greene T, Tighiouart H, Gansevoort RT, Coresh J, Simon AL, et al. Change in albuminuria as a surrogate endpoint for progression of kidney disease: a meta-analysis of treatment effects in randomised clinical trials. The Lancet Diabetes Endocrinol. 2019;7:128–39.
Kröpelin TF, de Zeeuw D, Andress DL, Bijlsma MJ, Persson F, Parving H-H. et al. Number and frequency of albuminuria measurements in clinical trials in diabetic nephropathy. Clin J Am Soc Nephrol. 2015;10:410–6.
Acknowledgements
This study was supported by grants from the Swedish Research Council (2017-01707), the Swedish state under the agreement between the Swedish government and the county councils, the ALF agreement (ALFGBG-717881, ALFGBG-717891), The Swedish Heart-Lung Foundation (20180410), the Novo Nordisk Foundation (NNF19OC0057184), the Swedish Diabetes foundation (2019-417), and the National Institute of Diabetes and Digestive and Kidney Diseases of the National Institutes of Health (R01DK105948). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
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JCAA and MT provided data collection and linkage with the Swedish authorities. MP and JCAA had access to and were responsible for acquisition and integrity of the data. AS was responsible for the statistical data analysis. All authors were responsible for interpretation of the data. AS and PAS drafted the manuscript. All authors participated in critical revision of the manuscript and provided intellectual input. LMSC, PAS, JCAA, KS, and MT were involved in fundraising. All authors approved the final version and agreed to be accountable for all aspects of the work.
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CDS is employed by AstraZeneca. LMSC reports receiving consulting fees from Johnson&Johnson. CWlR serves on advisory boards for Novo Nordisk, GI Dynamics, Keyron, Herbalife, Boehringer Ingelheim, Johnson&Johnson, Sanofi, Consilient Health. Other authors report no conflicts of interest.
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Shulman, A., Andersson-Assarsson, J.C., Sjöström, C.D. et al. Remission and progression of pre-existing micro- and macroalbuminuria over 15 years after bariatric surgery in Swedish Obese Subjects study. Int J Obes 45, 535–546 (2021). https://doi.org/10.1038/s41366-020-00707-z
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DOI: https://doi.org/10.1038/s41366-020-00707-z
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