Skip to main content

Advertisement

SpringerLink
Log in

Long-term impact of bariatric surgery in diabetic nephropathy

  • 2018 SAGES Oral
  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Bariatric surgery has been shown to improve and resolve diabetes. However, limited literature about its impact on end-organ complications of diabetes is available. The aim of this study was to examine the long-term effect of bariatric surgery on albuminuria.

Methods

We studied 101 patients with pre-operative diabetes and albuminuria [defined as urine albumin:creatinine ratio (uACR) > 30 mg/g] who underwent bariatric surgery at an academic center from 2005 to 2014.

Results

Fifty-seven patients (56%) were female with a mean age of 53 (± 11) years. The mean pre-operative BMI and glycated hemoglobin (HbA1c) were 43.1 (± 7.6) kg/m2 and 8.4 (± 1.8)%, respectively. The median pre-operative uACR was 80.0 (45.0–231.0) mg/g. Bariatric procedures included Roux-en-Y gastric bypass (n = 75, 74%) and sleeve gastrectomy (n = 26, 26%). The mean follow-up period was 61 (± 29) months. At last follow-up, the mean BMI was 33.8 (± 8.3) kg/m2. The overall glycemic control improved after bariatric surgery. At last follow-up, 73% had good glycemic control (HbA1c < 7%) and 27% met diabetes remission criteria. The mean HbA1c at last follow-up was 6.7 (± 1.0)% and the median uACR was 30 (IQR 7–94) mg/g. Albuminuria improved in 77% and resolved in 51% of patients at long-term.

Conclusions

Bariatric surgery has a significantly positive impact on albuminuria in patients with obesity and type 2 diabetes. Our data showed almost an 80% improvement in albuminuria at the short- and long-term period after bariatric surgery.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Molitch ME, DeFronzo RA, Franz MJ, Keane WF, Mogensen CE, Parving H-H, Steffes MW, American Diabetes Association (2004) Nephropathy in diabetes. Diabetes Care 27(Suppl 1):S79–S83. https://doi.org/10.2337/DIACARE.27.2007.S79

    Article  PubMed  Google Scholar 

  2. Postma MJ, de Zeeuw D (2009) The economic benefits of preventing end-stage renal disease in patients with type 2 diabetes mellitus. Nephrol Dial Transplant 24:2975–2983. https://doi.org/10.1093/ndt/gfp352

    Article  PubMed  Google Scholar 

  3. Damien P, Lanham HJ, Parthasarathy M, Shah NL (2016) Assessing key cost drivers associated with caring for chronic kidney disease patients. BMC Health Serv Res 16:690. https://doi.org/10.1186/s12913-016-1922-4

    Article  PubMed  PubMed Central  Google Scholar 

  4. Romagnani P, Remuzzi G, Glassock R, Levin A, Jager KJ, Tonelli M, Massy Z, Wanner C, Anders H-J (2017) Chronic kidney disease. Nat Rev Dis Prim 3:17088. https://doi.org/10.1038/nrdp.2017.88

    Article  PubMed  Google Scholar 

  5. Burrows NR, Hora I, Geiss LS, Gregg EW, Albright A (2017) Incidence of end-stage renal disease attributed to diabetes among persons with diagnosed diabetes—United States and Puerto Rico, 2000–2014. MMWR Morb Mortal Wkly Rep 66:1165–1170. https://doi.org/10.15585/mmwr.mm6643a2

    Article  PubMed  PubMed Central  Google Scholar 

  6. González-Muniesa P, Mártinez-González M-A, Hu FB, Després J-P, Matsuzawa Y, Loos RJF, Moreno LA, Bray GA, Martinez JA (2017) Obesity. Nat Rev Dis Prim 3:17034. https://doi.org/10.1038/nrdp.2017.34

    Article  PubMed  Google Scholar 

  7. Wang Y, Chen X, Song Y, Caballero B, Cheskin LJ (2008) Association between obesity and kidney disease: a systematic review and meta-analysis. Kidney Int 73:19–33. https://doi.org/10.1038/sj.ki.5002586

    Article  CAS  PubMed  Google Scholar 

  8. Hsu C, McCulloch CE, Iribarren C, Darbinian J, Go AS (2006) Body mass index and risk for end-stage renal disease. Ann Intern Med 144:21. https://doi.org/10.7326/0003-4819-144-1-200601030-00006

    Article  PubMed  Google Scholar 

  9. Garofalo C, Borrelli S, Minutolo R, Chiodini P, De Nicola L, Conte G (2017) A systematic review and meta-analysis suggests obesity predicts onset of chronic kidney disease in the general population. Kidney Int 91:1224–1235. https://doi.org/10.1016/j.kint.2016.12.013

    Article  PubMed  Google Scholar 

  10. Bayliss G, Weinrauch LA, D’Elia JA (2012) Pathophysiology of obesity-related renal dysfunction contributes to diabetic nephropathy. Curr Diab Rep 12:440–446. https://doi.org/10.1007/s11892-012-0288-1

    Article  CAS  PubMed  Google Scholar 

  11. Rossi M, Nicolucci A, Pellegrini F, Comaschi M, Ceriello A, Cucinotta D, Giorda C, Pomili B, Valentini U, Vespasiani G, De Cosmo S (2010) Obesity and changes in urine albumin/creatinine ratio in patients with type 2 diabetes: the DEMAND study. Nutr Metab Cardiovasc Dis. https://doi.org/10.1016/j.numecd.2009.02.013

    Article  PubMed  Google Scholar 

  12. Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, Schoelles K (2004) Bariatric surgery. JAMA 292:1724. https://doi.org/10.1001/jama.292.14.1724

    Article  CAS  PubMed  Google Scholar 

  13. Carlsson LMS, Peltonen M, Ahlin S, Anveden Å, Bouchard C, Carlsson B, Jacobson P, Lönroth H, Maglio C, Näslund I, Pirazzi C, Romeo S, Sjöholm K, Sjöström E, Wedel H, Svensson P-A, Sjöström L (2012) Bariatric surgery and prevention of type 2 diabetes in Swedish obese subjects. N Engl J Med 367:695–704. https://doi.org/10.1056/NEJMoa1112082

    Article  CAS  PubMed  Google Scholar 

  14. Maciejewski ML, Arterburn DE, Van Scoyoc L, Smith VA, Yancy WS, Weidenbacher HJ, Livingston EH, Olsen MK, Olsen MK (2016) Bariatric surgery and long-term durability of weight loss. JAMA Surg 151:1046–1055. https://doi.org/10.1001/jamasurg.2016.2317

    Article  PubMed  PubMed Central  Google Scholar 

  15. Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Aminian A, Brethauer SA, Navaneethan SD, Singh RP, Pothier CE, Nissen SE, Kashyap SR (2017) Bariatric surgery versus intensive medical therapy for diabetes—5-year outcomes. N Engl J Med 376:641–651. https://doi.org/10.1056/NEJMoa1600869

    Article  PubMed  PubMed Central  Google Scholar 

  16. Aminian A (2018) Sleeve gastrectomy: metabolic surgical procedure of choice? Trends Endocrinol Metab 29:531–534

    Article  CAS  PubMed  Google Scholar 

  17. Aminian A, Brethauer SA, Andalib A, Nowacki AS, Jimenez A, Corcelles R, Hanipah ZN, Punchai S, Bhatt DL, Kashyap SR, Burguera B, Lacy AM, Vidal J, Schauer PR (2017) Individualized metabolic surgery score. Ann Surg 266:650–657. https://doi.org/10.1097/SLA.0000000000002407

    Article  PubMed  Google Scholar 

  18. Ardestani A, Rhoads D, Tavakkoli A (2015) Insulin cessation and diabetes remission after bariatric surgery in adults with insulin-treated type 2 diabetes. Diabetes Care 38:dc141751. https://doi.org/10.2337/dc14-1751

    Article  CAS  Google Scholar 

  19. Aminian A, Daigle CR, Romero-Talamás H, Kashyap SR, Kirwan JP, Brethauer SA, Schauer PR (2014) Risk prediction of complications of metabolic syndrome before and 6 years after gastric bypass. Surg Obes Relat Dis 10:576–582. https://doi.org/10.1016/j.soard.2014.01.025

    Article  PubMed  Google Scholar 

  20. Wong MG, Perkovic V, Chalmers J, Woodward M, Li Q, Cooper ME, Hamet P, Harrap S, Heller S, MacMahon S, Mancia G, Marre M, Matthews D, Neal B, Poulter N, Rodgers A, Williams B, Zoungas S, ADVANCE-ON Collaborative Group (2016) Long-term benefits of intensive glucose control for preventing end-stage kidney disease: ADVANCE-ON. Diabetes Care 39:694–700. https://doi.org/10.2337/dc15-2322

    Article  CAS  PubMed  Google Scholar 

  21. Resnick HE, Foster GL, Bardsley J, Ratner RE (2006) Achievement of American Diabetes Association clinical practice recommendations among U.S. adults with diabetes, 1999–2002: the National Health and Nutrition Examination Survey. Diabetes Care 29:531–537. https://doi.org/10.2337/DIACARE.29.03.06.DC05-1254

    Article  PubMed  Google Scholar 

  22. American Diabetes Association (2018) Standards of medical care in diabetes—2018. Diabetes Care 41:S3. https://doi.org/10.2337/dc18-Sppc01

    Article  Google Scholar 

  23. Rubino F, Nathan DM, Eckel RH, Schauer PR, Alberti KGMM, Zimmet PZ, Del Prato S, Ji L, Sadikot SM, Herman WH, Amiel SA, Kaplan LM, Taroncher-Oldenburg G, Cummings DE, Delegates of the 2nd Diabetes Surgery Summit (2016) Metabolic surgery in the treatment algorithm for type 2 diabetes: a joint statement by international diabetes organizations. Diabetes Care 39:861–877. https://doi.org/10.2337/dc16-0236

    Article  CAS  PubMed  Google Scholar 

  24. Morales E, Praga M (2012) The effect of weight loss in obesity and chronic kidney disease. Curr Hypertens Rep 14:170–176. https://doi.org/10.1007/s11906-012-0247-x

    Article  PubMed  Google Scholar 

  25. Heneghan HM, Cetin D, Navaneethan SD, Orzech N, Brethauer SA, Schauer PR (2013) Effects of bariatric surgery on diabetic nephropathy after 5 years of follow-up. Surg Obes Relat Dis 9:7–14. https://doi.org/10.1016/j.soard.2012.08.016

    Article  PubMed  Google Scholar 

  26. Upala S, Wijarnpreecha K, Congrete S, Rattanawong P, Sanguankeo A (2016) Bariatric surgery reduces urinary albumin excretion in diabetic nephropathy: a systematic review and meta-analysis. Surg Obes Relat Dis 12:1037–1044. https://doi.org/10.1016/j.soard.2015.11.019

    Article  PubMed  Google Scholar 

  27. de Jong PE, Curhan GC (2006) Screening, monitoring, and treatment of albuminuria: public health perspectives. J Am Soc Nephrol 17:2120–2126. https://doi.org/10.1681/ASN.2006010097

    Article  PubMed  Google Scholar 

  28. Buse JB, Caprio S, Cefalu WT, Ceriello A, Del Prato S, Inzucchi SE, McLaughlin S, Phillips GL, Robertson RP, Rubino F, Kahn R, Kirkman MS (2009) How do we define cure of diabetes? Diabetes Care 32:2133–2135. https://doi.org/10.2337/dc09-9036

    Article  PubMed  PubMed Central  Google Scholar 

  29. Brethauer SA, Kim J, el Chaar M, Papasavas P, Eisenberg D, Rogers A, Ballem N, Kligman M, Kothari S, ASMBS Clinical Issues Committee (2015) Standardized outcomes reporting in metabolic and bariatric surgery. Surg Obes Relat Dis 11:489–506. https://doi.org/10.1016/j.soard.2015.02.003

    Article  PubMed  Google Scholar 

  30. Aminian A, Brethauer SA, Andalib A, Punchai S, Mackey J, Rodriguez J, Rogula T, Kroh M, Schauer PR (2016) Can sleeve gastrectomy “cure” diabetes? Long-term metabolic effects of sleeve gastrectomy in patients with type 2 diabetes. Ann Surg 264:674–681. https://doi.org/10.1097/SLA.0000000000001857

    Article  PubMed  Google Scholar 

  31. Brethauer SA, Aminian A, Romero-Talamás H, Batayyah E, Mackey J, Kennedy L, Kashyap SR, Kirwan JP, Rogula T, Kroh M, Chand B, Schauer PR (2013) Can diabetes be surgically cured? Long-term metabolic effects of bariatric surgery in obese patients with type 2 diabetes mellitus. Ann Surg 258:628–636. https://doi.org/10.1097/SLA.0b013e3182a5034b

    Article  PubMed  Google Scholar 

  32. Chernecky C, Berger B (2013) Creatinine—serum. In: Chernecky C, Berger B (eds) Laboratory tests and diagnostic procedures, 6th edn. Elsevier, St Louis, MO, pp 266–432

    Google Scholar 

  33. Basi S, Fesler P, Mimran A, Lewis JB (2008) Microalbuminuria in type 2 diabetes and hypertension: a marker, treatment target, or innocent bystander? Diabetes Care 31(Suppl 2):S194–S201

    Article  CAS  PubMed  Google Scholar 

  34. Asselbergs FW, Diercks GF, Hillege HL, van Boven AJ, Janssen WM, Voors AA, de Zeeuw D, de Jong PE, van Veldhuisen DJ, van Gilst WH, Prevention of Renal and Vascular Endstage Disease Intervention Trial (PREVEND IT) Investigators (2004) Effects of fosinopril and pravastatin on cardiovascular events in subjects with microalbuminuria. Circulation 110:2809–2816

    Article  CAS  PubMed  Google Scholar 

  35. Ibsen H, Olsen MH, Wachtell K, Borch-Johnsen K, Lindholm LH, Mogensen CE, Dahlöf B, Devereux RB, de Faire U, Fyhrquist F, Julius S, Kjeldsen SE, Lederballe-Pedersen O, Nieminen MS, Omvik P, Oparil S, Wan Y (2005) Reduction in albuminuria translates to reduction in cardiovascular events in hypertensive patients: losartan intervention for endpoint reduction in hypertension study. Hypertension 45:198–202

    Article  CAS  PubMed  Google Scholar 

  36. Parving HH, Lehnert H, Bröchner-Mortensen J, Gomis R, Andersen S, Arner P, Irbesartan in Patients with Type 2 Diabetes and Microalbuminuria Study Group (2001) The effect of irbesartan on the development of diabetic nephropathy in patients with type 2 diabetes. N Engl J Med 345:870–878

    Article  CAS  PubMed  Google Scholar 

  37. Zeve JL, de M, Tomaz, Nassif CAB, Lima PAN, Sansana JH, Zeve LRZ CH (2013) Obese patients with diabetes mellitus type 2 undergoing gastric bypass in Roux-en-Y: analysis of results and its influence in complications. Arq Bras Cir Dig 26(Suppl 1):47–52

    Article  PubMed  Google Scholar 

  38. Kota SK, Ugale S, Gupta N, Modi KD (2012) Laparoscopic ileal interposition with diverted sleeve gastrectomy for treatment of type 2 diabetes. Diabetes Metab Syndr Clin Res Rev 6:125–131. https://doi.org/10.1016/j.dsx.2012.09.014

    Article  Google Scholar 

  39. Amor A, Jiménez A, Moizé V, Ibarzabal A, Flores L, Lacy AM, Vidal J (2013) Weight loss independently predicts urinary albumin excretion normalization in morbidly obese type 2 diabetic patients undergoing bariatric surgery. Surg Endosc 27:2046–2051. https://doi.org/10.1007/s00464-012-2708-3

    Article  PubMed  Google Scholar 

  40. Zhang H, Di J, Yu H, Han X, Li K, Zhang P (2015) The short-term remission of diabetic nephropathy after Roux-en-Y gastric bypass in Chinese patients of T2DM with obesity. Obes Surg 25:1263–1270. https://doi.org/10.1007/s11695-015-1666-y

    Article  PubMed  PubMed Central  Google Scholar 

  41. Saliba J, Kasim NR, Tamboli RA, Isbell JM, Marks P, Feurer ID, Ikizler A, Abumrad NN (2010) Roux-en-Y gastric bypass reverses renal glomerular but not tubular abnormalities in excessively obese diabetics. Surgery 147:282–287. https://doi.org/10.1016/j.surg.2009.09.017

    Article  PubMed  Google Scholar 

  42. Miras AD, Chuah LL, Khalil N, Nicotra A, Vusirikala A, Baqai N, Graham C, Ravindra S, Lascaratos G, Oliver N, le Roux CW (2015) Type 2 diabetes mellitus and microvascular complications 1 year after Roux-en-Y gastric bypass: a case–control study. Diabetologia 58:1443–1447. https://doi.org/10.1007/s00125-015-3595-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Carlsson LMS, Romeo S, Jacobson P, Burza MA, Maglio C, Sjöholm K, Svensson P-A, Haraldsson B, Peltonen M, Sjöström L (2015) The incidence of albuminuria after bariatric surgery and usual care in swedish obese subjects (SOS): a prospective controlled intervention trial. Int J Obes 39:169–175. https://doi.org/10.1038/ijo.2014.72

    Article  CAS  Google Scholar 

  44. Retnakaran R, Cull CA, Thorne KI, Adler AI, Holman RR, UKPDS Study Group (2006) Risk factors for renal dysfunction in type 2 diabetes: U.K. Prospective Diabetes Study 74. Diabetes 55:1832–1839. https://doi.org/10.2337/db05-1620

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cleveland Clinic Lerner of College of Medicine, Cleveland, OH, USA

    LeAnne Young, Stacy A. Brethauer, Philip R. Schauer & Ali Aminian

  2. Department of General Surgery, Bariatric and Metabolic Institute, Cleveland Clinic, Mail Code M61, 9500 Euclid Avenue, Cleveland, OH, 44195, USA

    Zubaidah Nor Hanipah, Stacy A. Brethauer, Philip R. Schauer & Ali Aminian

  3. Department of Surgery, Faculty of Medicine and Health Sciences, University Putra Malaysia, Serdang, Selangor, Malaysia

    Zubaidah Nor Hanipah

Authors
  1. LeAnne Young
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zubaidah Nor Hanipah
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stacy A. Brethauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philip R. Schauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ali Aminian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ali Aminian.

Ethics declarations

Disclosures

Authors Young, Nor Hanipah, Brethauer, Schauer, and Aminian have no conflicts of interest or financial ties to disclose.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Young, L., Nor Hanipah, Z., Brethauer, S.A. et al. Long-term impact of bariatric surgery in diabetic nephropathy. Surg Endosc 33, 1654–1660 (2019). https://doi.org/10.1007/s00464-018-6458-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-018-6458-8

Keywords

Search

Navigation