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Original Article

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Insulin Sensitivity and Secretion in Obese Type 2 Diabetic Women after Various Bariatric Operations

Vrbikova J.a · Kunesova M.b, c · Kyrou I.d,e,f · Tura A.g · Hill M.h · Grimmichova T.a · Dvorakova K.a · Sramkova P.i · Dolezalova K.c, i · Lischkova O.j, k · Vcelak J.j · Hainer V.b · Bendlova B.j, k · Kumar S.d, f · Fried M.c, i

Author affiliations

aInstitute of Endocrinology, Clinical Department, Prague, Czech Republic; bInstitute of Endocrinology, Obesity Management Centre, Prague, Czech Republic; c1st Faculty of Medicine, Charles University, Prague, Czech Republic; dDivision of Translational and Experimental Medicine, Warwick Medical School, University of Warwick, Coventry, UK; eAston Medical Research Institute, Aston Medical School, Aston University, Birmingham, UK; fWarwickshire Institute for the Study of Diabetes, Endocrinology and Metabolism (WISDEM), University Hospitals of Coventry and Warwickshire (UHCW) NHS Trust, Coventry, UK; gISIB CNR Italy, Padua, Italy; hInstitute of Endocrinology, Steroid Hormone and Proteofactors Department, Prague, Czech Republic; iOB Klinika, Prague, Czech Republic; jInstitute of Endocrinology, Department of Molecular Endocrinology, Prague, Czech Republic; kFaculty of Science, Charles University, Prague, Czech Republic;

Corresponding Author

Prof. Dr. Martin Fried

OB Klinika

Pod Krejcárkem 975

130 00 Prague 3, Czech Republic

docfried@volny.cz

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Abstract

Objective: To compare the effects of biliopancreatic diversion (BPD) and laparoscopic gastric banding (LAGB) on insulin sensitivity and secretion with the effects of laparoscopic gastric plication (P). Methods: A total of 52 obese women (age 30-66 years) suffering from type 2 diabetes mellitus (T2DM) were prospectively recruited into three study groups: 16 BPD; 16 LAGB, and 20 P. Euglycemic clamps and mixed meal tolerance tests were performed before, at 1 month and at 6 months after bariatric surgery. Beta cell function derived from the meal test parameters was evaluated using mathematical modeling. Results: Glucose disposal per kilogram of fat free mass (a marker of peripheral insulin sensitivity) increased significantly in all groups, especially after 1 month. Basal insulin secretion decreased significantly after all three types of operations, with the most marked decrease after BPD compared with P and LAGB. Total insulin secretion decreased significantly only following the BPD. Beta cell glucose sensitivity did not change significantly post-surgery in any of the study groups. Conclusion: We documented similar improvement in insulin sensitivity in obese T2DM women after all three study operations during the 6-month postoperative follow-up. Notably, only BPD led to decreased demand on beta cells (decreased integrated insulin secretion), but without increasing the beta cell glucose sensitivity.

© 2016 The Author(s) Published by S. Karger GmbH, Freiburg


References

  1. Fried M: Bariatric and metabolic surgery. Minerva Endocrinol 2013;38:237-244.
    External Resources
  2. Tham JC, Howes N, le Roux CW: The role of bariatric surgery in the treatment of diabetes. Ther Adv Chronic Dis 2015;5:149-157.
  3. Buchwald H, Estok R, Fahrbach K, Banel D, Jensen MD, Pories WJ, Bantle JP, Sledge I: Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med 2009;122:248-256.e5.
  4. Knop FK, Taylor R: Mechanism of metabolic advantages after bariatric surgery: it's all gastrointestinal factors versus it's all food restriction. Diabetes Care 2013;36(suppl 2):S287-291.
  5. Lee WJ, Almulaifi A: Recent advances in bariatric/metabolic surgery: appraisal of clinical evidence. J Biomed Res 2015;29:98-104.
  6. Bradnova O, Kyrou I, Hainer V, Vcelak J, Halkova T, Sramkova P, Dolezalova K, Fried M, McTernan P, Kumar S, Hill M, Kunesova M, Bendlova B, Vrbikova J: Laparoscopic greater curvature plication in morbidly obese women with type 2 diabetes: effects on glucose homeostasis, postprandial triglyceridemia and selected gut hormones. Obes Surg 2014;24:718-726.
  7. Fried M, Dolezalova K, Sramkova P: Adjustable gastric banding outcomes with and without gastrogastric imbrication sutures: a randomized controlled trial. Surg Obes Relat Dis 2011;7:23-31.
  8. Talebpour M, Talebpour A, Barzin G, Shariat Moharari R, Khajavi MR:. Effects of laparoscopic gastric plication (LGP) in patients with type 2 diabetes, one year follow-up. J Diabetes Metab Disord 2015;14:60.
  9. Brethauer SA, Harris JL, Kroh M, Schauer PR: Laparoscopic gastric plication for treatment of severe obesity. Surg Obes Relat Dis 2011;7:15-22.
  10. Scopinaro N, Adami GF, Papadia FS, Camerini G, Carlini F, Fried M, Briatore L, D'Alessandro G, Andraghetti G, Cordera R: Effects of biliopanceratic diversion on type 2 diabetes in patients with BMI 25 to 35. Ann Surg 2014;253:699-703.
  11. Fried M, Yumuk V, Oppert JM, Scopinaro N, Torres AJ, Weiner R, Yashkov Y, Fruhbeck G: Interdisciplinary European guidelines on metabolic and bariatric surgery. Obes Facts 2013;6:449-468.
  12. DeFronzo RA, Tobin JD, Andres R: Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol 1979;237:e214-223.
    External Resources
  13. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC: Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28:412-429.
  14. Mari A, Camastra S, Toschi E, Giancaterini A, Gastaldelli A, Mingrone G, Ferrannini E: A model for glucose control of insulin secretion during 24 h of free living. Diabetes.2001;50(suppl 1):S164-168.
  15. Van Cauter E, Mestrez F, Sturis J, Polonsky KS: Estimation of insulin secretion rates from C-peptide levels. Comparison of individual and standard kinetic parameters for C-peptide clearance. Diabetes 1992;41:368-377.
  16. Meloun M, Hill M, Militky J, Kupka K: Transformation in the PC-aided biochemical data analysis. Clin Chem Lab Med 2000;38:553-559.
  17. Meloun M, Militky J, Hill M, Brereton RG: Crucial problems in regression modelling and their solutions. Analyst 2002;127:433-450.
  18. Panunzi S, De Gaetano A, Carnicelli A, Mingrone G: Predictors of remission of diabetes mellitus in severely obese individuals undergoing bariatric surgery: do BMI or procedure choice matter? A meta-analysis. Ann Surg 2015;261:459-467.
  19. Verdi D, Prevedello L, Albanese A, Lobba A, Foletto M: Laparoscopic gastric plication (LGCP) vs sleeve gastrectomy (LSG): a single institution experience. Obes Surg 2015;25:1653-1657.
  20. Robert M, Ferrand-Gaillard C, Disse E, Espalieu P, Simon C, Laville M, Gouillat C, Thivolet C: Predictive factors of type 2 diabetes remission 1 year after bariatric surgery: impact of surgical techniques. Obes Surg 2013;23:770-775.
  21. Kunešová M, Sedláčková B, Bradnová O, Tvrzická E, Staňková B, Šrámková P, DoleŽalová K, Kalousková P, Hlavatý P, Hill M, Bendlová B, Fried M, Hainer V, Vrbíková J: Fatty acid composition of adipose tissue triglycerides in obese diabetic women after bariatric surgery: a 2-year follow up. Physiol Res 2015;64(suppl 2):S155-166.
    External Resources
  22. Yska JP, van Roon EN, de Boer A, Leufkens HG, Wilffert B, de Heide LJ, de Vries F, Lalmohamed A: Remission of type 2 diabetes mellitus in patients after different types of bariatric surgery: a population-based cohort study in the United Kingdom. JAMA Surg 2015;150:1126-1133.
  23. Malkani S: An update on the role of bariatric surgery in diabetes management. Curr Opin Endocrinol Diabetes Obes 2015;22:98-105.
  24. Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Brethauer SA, Navaneethan SD, Aminian A, Pothier CE, Kim ES, Nissen SE, Kashyap SR: Bariatric surgery versus intensive medical therapy for diabetes - 3-year outcomes. N Engl J Med 2014;370:2002-2013.
  25. Mingrone G, Castagneto M: Bariatric surgery: unstressing or boosting the beta-cell? Diabetes Obes Metab 2009;11:130-142.
  26. Alam I, Stephens JW, Fielding A, Lewis KE, Lewis MJ, Baxter JN: Temporal changes in glucose and insulin homeostasis after biliopancreatic diversion and laparoscopic adjustable gastric banding. Surg Obes Relat Dis 2012;8:752-763.
  27. Tsoli M, Chronaiou A, Kehagias I, Kalfarentzos F, Alexandrides TK: Hormone changes and diabetes resolution after biliopancreatic diversion and laparoscopic sleeve gastrectomy: a comparative prospective study. Surg Obes Relat Dis 2013;9:667-677.
  28. Guidone C, Manco M, Valera-Mora E, Iaconelli A, Gniuli D, Mari A, Nanni G, Castagneto M, Calvani M, Mingrone G: Mechanisms of recovery from type 2 diabetes after malabsorptive bariatric surgery. Diabetes 2006;55:2025-2031.
  29. Astiarraga B, Gastaldelli A, Muscelli E, Baldi S, Camastra S, Mari A, Papadia F, Camerini G, Adami G, Scopinaro N, Ferrannini E: Biliopancreatic diversion in nonobese patients with type 2 diabetes: impact and mechanisms. J Clin Endocrinol Metab 2013;98:2765-2773.
  30. Dutia R, Brakoniecki K, Bunker P, Paultre F, Homel P, Carpentier AC, McGinty J, Laferrere B: Limited recovery of beta-cell function after gastric bypass despite clinical diabetes remission. Diabetes 2014;63:1214-1223.
  31. Pontiroli AE: Comment on Dutia et al. Limited recovery of beta-cell function after gastric bypass despite clinical diabetes remission. Diabetes 2014;63:1214-1223. Diabetes 2014;63:e3.
  32. World Medical Association Declaration of Helsinki: Recommendations guiding physicians in biomedical research involving human subjects. JAMA 1997;277:925-926.
    External Resources

Article / Publication Details

First-Page Preview
Abstract of Original Article

Received: April 14, 2016
Accepted: October 27, 2016
Published online: December 13, 2016
Issue release date: December 2016

Number of Print Pages: 14
Number of Figures: 2
Number of Tables: 2

ISSN: 1662-4025 (Print)
eISSN: 1662-4033 (Online)

For additional information: https://www.karger.com/OFA

References

  1. Fried M: Bariatric and metabolic surgery. Minerva Endocrinol 2013;38:237-244.
    External Resources
  2. Tham JC, Howes N, le Roux CW: The role of bariatric surgery in the treatment of diabetes. Ther Adv Chronic Dis 2015;5:149-157.
  3. Buchwald H, Estok R, Fahrbach K, Banel D, Jensen MD, Pories WJ, Bantle JP, Sledge I: Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med 2009;122:248-256.e5.
  4. Knop FK, Taylor R: Mechanism of metabolic advantages after bariatric surgery: it's all gastrointestinal factors versus it's all food restriction. Diabetes Care 2013;36(suppl 2):S287-291.
  5. Lee WJ, Almulaifi A: Recent advances in bariatric/metabolic surgery: appraisal of clinical evidence. J Biomed Res 2015;29:98-104.
  6. Bradnova O, Kyrou I, Hainer V, Vcelak J, Halkova T, Sramkova P, Dolezalova K, Fried M, McTernan P, Kumar S, Hill M, Kunesova M, Bendlova B, Vrbikova J: Laparoscopic greater curvature plication in morbidly obese women with type 2 diabetes: effects on glucose homeostasis, postprandial triglyceridemia and selected gut hormones. Obes Surg 2014;24:718-726.
  7. Fried M, Dolezalova K, Sramkova P: Adjustable gastric banding outcomes with and without gastrogastric imbrication sutures: a randomized controlled trial. Surg Obes Relat Dis 2011;7:23-31.
  8. Talebpour M, Talebpour A, Barzin G, Shariat Moharari R, Khajavi MR:. Effects of laparoscopic gastric plication (LGP) in patients with type 2 diabetes, one year follow-up. J Diabetes Metab Disord 2015;14:60.
  9. Brethauer SA, Harris JL, Kroh M, Schauer PR: Laparoscopic gastric plication for treatment of severe obesity. Surg Obes Relat Dis 2011;7:15-22.
  10. Scopinaro N, Adami GF, Papadia FS, Camerini G, Carlini F, Fried M, Briatore L, D'Alessandro G, Andraghetti G, Cordera R: Effects of biliopanceratic diversion on type 2 diabetes in patients with BMI 25 to 35. Ann Surg 2014;253:699-703.
  11. Fried M, Yumuk V, Oppert JM, Scopinaro N, Torres AJ, Weiner R, Yashkov Y, Fruhbeck G: Interdisciplinary European guidelines on metabolic and bariatric surgery. Obes Facts 2013;6:449-468.
  12. DeFronzo RA, Tobin JD, Andres R: Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol 1979;237:e214-223.
    External Resources
  13. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC: Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28:412-429.
  14. Mari A, Camastra S, Toschi E, Giancaterini A, Gastaldelli A, Mingrone G, Ferrannini E: A model for glucose control of insulin secretion during 24 h of free living. Diabetes.2001;50(suppl 1):S164-168.
  15. Van Cauter E, Mestrez F, Sturis J, Polonsky KS: Estimation of insulin secretion rates from C-peptide levels. Comparison of individual and standard kinetic parameters for C-peptide clearance. Diabetes 1992;41:368-377.
  16. Meloun M, Hill M, Militky J, Kupka K: Transformation in the PC-aided biochemical data analysis. Clin Chem Lab Med 2000;38:553-559.
  17. Meloun M, Militky J, Hill M, Brereton RG: Crucial problems in regression modelling and their solutions. Analyst 2002;127:433-450.
  18. Panunzi S, De Gaetano A, Carnicelli A, Mingrone G: Predictors of remission of diabetes mellitus in severely obese individuals undergoing bariatric surgery: do BMI or procedure choice matter? A meta-analysis. Ann Surg 2015;261:459-467.
  19. Verdi D, Prevedello L, Albanese A, Lobba A, Foletto M: Laparoscopic gastric plication (LGCP) vs sleeve gastrectomy (LSG): a single institution experience. Obes Surg 2015;25:1653-1657.
  20. Robert M, Ferrand-Gaillard C, Disse E, Espalieu P, Simon C, Laville M, Gouillat C, Thivolet C: Predictive factors of type 2 diabetes remission 1 year after bariatric surgery: impact of surgical techniques. Obes Surg 2013;23:770-775.
  21. Kunešová M, Sedláčková B, Bradnová O, Tvrzická E, Staňková B, Šrámková P, DoleŽalová K, Kalousková P, Hlavatý P, Hill M, Bendlová B, Fried M, Hainer V, Vrbíková J: Fatty acid composition of adipose tissue triglycerides in obese diabetic women after bariatric surgery: a 2-year follow up. Physiol Res 2015;64(suppl 2):S155-166.
    External Resources
  22. Yska JP, van Roon EN, de Boer A, Leufkens HG, Wilffert B, de Heide LJ, de Vries F, Lalmohamed A: Remission of type 2 diabetes mellitus in patients after different types of bariatric surgery: a population-based cohort study in the United Kingdom. JAMA Surg 2015;150:1126-1133.
  23. Malkani S: An update on the role of bariatric surgery in diabetes management. Curr Opin Endocrinol Diabetes Obes 2015;22:98-105.
  24. Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Brethauer SA, Navaneethan SD, Aminian A, Pothier CE, Kim ES, Nissen SE, Kashyap SR: Bariatric surgery versus intensive medical therapy for diabetes - 3-year outcomes. N Engl J Med 2014;370:2002-2013.
  25. Mingrone G, Castagneto M: Bariatric surgery: unstressing or boosting the beta-cell? Diabetes Obes Metab 2009;11:130-142.
  26. Alam I, Stephens JW, Fielding A, Lewis KE, Lewis MJ, Baxter JN: Temporal changes in glucose and insulin homeostasis after biliopancreatic diversion and laparoscopic adjustable gastric banding. Surg Obes Relat Dis 2012;8:752-763.
  27. Tsoli M, Chronaiou A, Kehagias I, Kalfarentzos F, Alexandrides TK: Hormone changes and diabetes resolution after biliopancreatic diversion and laparoscopic sleeve gastrectomy: a comparative prospective study. Surg Obes Relat Dis 2013;9:667-677.
  28. Guidone C, Manco M, Valera-Mora E, Iaconelli A, Gniuli D, Mari A, Nanni G, Castagneto M, Calvani M, Mingrone G: Mechanisms of recovery from type 2 diabetes after malabsorptive bariatric surgery. Diabetes 2006;55:2025-2031.
  29. Astiarraga B, Gastaldelli A, Muscelli E, Baldi S, Camastra S, Mari A, Papadia F, Camerini G, Adami G, Scopinaro N, Ferrannini E: Biliopancreatic diversion in nonobese patients with type 2 diabetes: impact and mechanisms. J Clin Endocrinol Metab 2013;98:2765-2773.
  30. Dutia R, Brakoniecki K, Bunker P, Paultre F, Homel P, Carpentier AC, McGinty J, Laferrere B: Limited recovery of beta-cell function after gastric bypass despite clinical diabetes remission. Diabetes 2014;63:1214-1223.
  31. Pontiroli AE: Comment on Dutia et al. Limited recovery of beta-cell function after gastric bypass despite clinical diabetes remission. Diabetes 2014;63:1214-1223. Diabetes 2014;63:e3.
  32. World Medical Association Declaration of Helsinki: Recommendations guiding physicians in biomedical research involving human subjects. JAMA 1997;277:925-926.
    External Resources
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