POST-BARIATRIC HYPOGLYCAEMIA: FROM SCIENTIFIC EVIDENCE TO CLINICAL PRACTICE
Abstract
Approaching the patient presenting symptoms compatible with post-bariatric hypoglycaemia (PBH) is a major clinical challenge for surgeons, endocrinologists, nutritionists, and primary care physicians. Raising the hypothesis of PBH as differential diagnosis requires a high degree of suspicion, since patient clinical features at presentation are highly unspecific and overlap with those of dumping syndrome, which is highly prevalent in this population. The temporal relationship between food intake and hypoglycaemia poses an additional challenge for laboratorial documentation. PBH aetiology is poorly understood and appears to be multifactorial, which limits the possibility of targeting treatment interventions. By means of this review, we aim to summarize the best evidence available regarding PBH pathophysiology, diagnosis and treatment. A diagnosis and therapeutic algorithm for patient approach, easy to implement at both primary care and tertiary hospitalary centres settings is herein proposed.
Downloads
Download data is not yet available.
References
1. Frühbeck G, Busetto L, Dicker D, Yumuk V, Goossens GH, Hebebrand J, et al. The ABCD of Obesity: An EASO Position Statement on a Diagnostic Term with Clinical and Scientific Implications. Obesity Facts. 2019;12(2):131-6.
2. Cecchini M, Vuik S. The heavy burden of obesity. 2019.
3. Fried M, Yumuk V, Oppert JM, Scopinaro N, Torres A, Weiner R, et al. Interdisciplinary European guidelines on metabolic and bariatric surgery. Obes Surg. 2014;24(1):42-55.
4. Eisenberg D, Azagury DE, Ghiassi S, Grover BT, Kim JJ. ASMBS Position Statement on Postprandial Hyperinsulinemic Hypoglycemia after Bariatric Surgery. Surg Obes Relat Dis. 2017;13(3):371-8.
5. van Meijeren J, Timmer I, Brandts H, Janssen I, de Boer H. Evaluation of carbohydrate restriction as primary treatment for postgastric bypass hypoglycemia. Surg Obes Relat Dis. 2017;13(3):404-10.
6. Guimaraes M, Rodrigues P, Pereira SS, Nora M, Goncalves G, Albrechtsen NW, et al. GLP1 and glucagon co-secreting pancreatic neuroendocrine tumor presenting as hypoglycemia after gastric bypass. Endocrinol Diabetes Metab Case Rep. 2015;2015:150049.
7. Marsk R, Jonas E, Rasmussen F, Naslund E. Nationwide cohort study of post-gastric bypass hypoglycaemia including 5,040 patients undergoing surgery for obesity in 1986-2006 in Sweden. Diabetologia. 2010;53(11):2307-11.
8. American Diabetes A. 6. Glycemic Targets: Standards of Medical Care in Diabetes-2021. Diabetes Care. 2021;44(Suppl 1):S73-S84.
9. Battelino T, Danne T, Bergenstal RM, Amiel SA, Beck R, Biester T, et al. Clinical Targets for Continuous Glucose Monitoring Data Interpretation: Recommendations From the International Consensus on Time in Range. Diabetes Care. 2019;42(8):1593-603.
10. Lobato CB, Pereira SS, Guimarães M, Morais T, Oliveira P, de Carvalho JPM, et al. Use of flash glucose monitoring for post-bariatric hypoglycaemia diagnosis and management. Scientific Reports. 2020;10(1):11061.
11. Tharakan G, Behary P, Wewer Albrechtsen NJ, Chahal H, Kenkre J, Miras AD, et al. Roles of increased glycemic variability, GLP-1 and glucagon in hypoglycaemia after Roux-en-Y gastric bypass. Eur J Endocrinol. 2017.
12. Salehi M, Gastaldelli A, D’Alessio DA. Blockade of glucagon-like peptide 1 receptor corrects postprandial hypoglycemia after gastric bypass. Gastroenterology. 2014;146(3):669-80 e2.
13. Stano S, Alam F, Wu L, Dutia R, Ng SN, Sala M, et al. Effect of meal size and texture on gastric pouch emptying and glucagon-like peptide 1 after gastric bypass surgery. Surg Obes Relat Dis. 2017.
14. Murphy CF, Elliott JA, Docherty NG, Mohamed AA, Vincent RP, Ravi N, et al. Exaggerated postprandial GLP-1 secretion following esophagectomy is not associated with gastric emptying and intestinal transit. Dis Esophagus. 2020.
15. Kandel D, Bojsen-Moller KN, Svane MS, Samkani A, Astrup A, Holst JJ, et al. Mechanisms of action of a carbohydrate-reduced, high-protein diet in reducing the risk of postprandial hypoglycemia after Roux-en-Y gastric bypass surgery. Am J Clin Nutr. 2019.
16. Lobato CB, Pereira SS, Guimaraes M, Hartmann B, Wewer Albrechtsen NJ, Hilsted L, et al. A Potential Role for Endogenous Glucagon in Preventing Post-Bariatric Hypoglycemia. Front Endocrinol (Lausanne). 2020;11:608248.
17. Salinari S, Mingrone G, Bertuzzi A, Previti E, Capristo E, Rubino F. Down-regulation of Insulin Sensitivity After Oral Glucose Administration: Evidence for the “Anti-Incretin Effect”. Diabetes. 2017.
18. Meier JJ, Butler AE, Galasso R, Butler PC. Hyperinsulinemic hypoglycemia after gastric bypass surgery is not accompanied by islet hyperplasia or increased beta-cell turnover. Diabetes Care. 2006;29(7):1554-9.
19. Zaloga GP, Chernow B. Postprandial hypoglycemia after Nissen fundoplication for reflux esophagitis. Gastroenterology. 1983;84(4):840-2.
20. Mathur S, Boparai J, Mediwala SN, Garcia JM, Cunningham GR, Marcelli M, et al. Reversible Adrenal Insufficiency in Three Patients With Post-Roux-en-Y Gastric Bypass Noninsulinoma Pancreatogenous Hypoglycemia Syndrome. J Investig Med High Impact Case Rep. 2014;2(1):2324709614526992.
21. Scarpellini E, Arts J, Karamanolis G, Laurenius A, Siquini W, Suzuki H, et al. International consensus on the diagnosis and management of dumping syndrome. Nat Rev Endocrinol. 2020.
22. Yaqub A, Smith EP, Salehi M. Hyperinsulinemic hypoglycemia after gastric bypass surgery: what’s up and what’s down? Int J Obes (Lond). 2017.
23. Vilarrasa N, Goday A, Rubio MA, Caixas A, Pellitero S, Ciudin A, et al. Hyperinsulinemic Hypoglycemia after Bariatric Surgery: Diagnosis and Management Experience from a Spanish Multicenter Registry. Obes Facts. 2016;9(1):41-51.
24. Lee CJ, Clark JM, Schweitzer M, Magnuson T, Steele K, Koerner O, et al. Prevalence of and risk factors for hypoglycemic symptoms after gastric bypass and sleeve gastrectomy. Obesity (Silver Spring). 2015;23(5):1079-84.
25. Roslin M, Damani T, Oren J, Andrews R, Yatco E, Shah P. Abnormal glucose tolerance testing following gastric bypass demonstrates reactive hypoglycemia. Surg Endosc. 2011;25(6):1926-32.
26. Ilesanmi I, Tharakan G, Alexiadou K, Behary P, Alessimii H, Bovill-Taylor C, et al. Roux-en-Y Gastric Bypass Increases Glycemic Variability and Time in Hypoglycemia in Patients With Obesity and Prediabetes or Type 2 Diabetes: A Prospective Cohort Study. Diabetes Care. 2021;44(2):614-7.
27. Marques AR, Lobato CB, Pereira SS, Guimaraes M, Faria S, Nora M, et al. Insights from the Impact of Meal Composition on Glucose Profile Towards Post-bariatric Hypoglycemia Management. Obes Surg. 2019.
28. Suhl E, Anderson-Haynes SE, Mulla C, Patti ME. Medical nutrition therapy for post-bariatric hypoglycemia: practical insights. Surg Obes Relat Dis. 2017.
29. Valderas JP, Ahuad J, Rubio L, Escalona M, Pollak F, Maiz A. Acarbose improves hypoglycaemia following gastric bypass surgery without increasing glucagon-like peptide 1 levels. Obes Surg. 2012;22(4):582-6.
30. Ritz P, Vaurs C, Bertrand M, Anduze Y, Guillaume E, Hanaire H. Usefulness of acarbose and dietary modifications to limit glycemic variability following Roux-en-Y gastric bypass as assessed by continuous glucose monitoring. Diabetes Technol Ther. 2012;14(8):736-40.
31. Halperin F, Patti ME, Goldfine AB. Glucagon treatment for post-gastric bypass hypoglycemia. Obesity (Silver Spring). 2010;18(9):1858-60.
32. Mulla CM, Zavitsanou S, Laguna Sanz AJ, Pober D, Richardson L, Walcott P, et al. A Randomized, Placebo-Controlled Double-Blind Trial of a Closed-Loop Glucagon System for Post-Bariatric Hypoglycemia. J Clin Endocrinol Metab. 2019.
33. Craig CM, Liu LF, Deacon CF, Holst JJ, McLaughlin TL. Critical role for GLP-1 in symptomatic post-bariatric hypoglycaemia. Diabetologia. 2017;60(3):531-40.
34. Abrahamsson N, Engstrom BE, Sundbom M, Karlsson FA. GLP1 analogs as treatment of postprandial hypoglycemia following gastric bypass surgery: a potential new indication? Eur J Endocrinol. 2013;169(6):885-9.
35. Ohrstrom CC, Worm D, Hojager A, Andersen D, Holst JJ, Kielgast UL, et al. Postprandial hypoglycaemia after Roux-en-Y gastric bypass and the effects of acarbose, sitagliptin, verapamil, liraglutide and pasireotide. Diabetes Obes Metab. 2019.
36. Mathavan VK, Arregui M, Davis C, Singh K, Patel A, Meacham J. Management of postgastric bypass noninsulinoma pancreatogenous hypoglycemia. Surg Endosc. 2010;24(10):2547-55.
37. Svane MS, Toft-Nielsen MB, Kristiansen VB, Hartmann B, Holst JJ, Madsbad S, et al. Nutrient re-routing and altered gut-islet cell crosstalk may explain early relief of severe postprandial hypoglycaemia after reversal of Roux-en-Y gastric bypass. Diabet Med. 2017.
38. Dapri G, Cadière GB, Himpens J. Laparoscopic reconversion of Roux-en-Y gastric bypass to original anatomy: technique and preliminary outcomes. Obes Surg. 2011;21(8):1289-95.
39. Lee CJ, Brown T, Magnuson TH, Egan JM, Carlson O, Elahi D. Hormonal response to a mixed-meal challenge after reversal of gastric bypass for hypoglycemia. J Clin Endocrinol Metab. 2013;98(7):E1208-12.
2. Cecchini M, Vuik S. The heavy burden of obesity. 2019.
3. Fried M, Yumuk V, Oppert JM, Scopinaro N, Torres A, Weiner R, et al. Interdisciplinary European guidelines on metabolic and bariatric surgery. Obes Surg. 2014;24(1):42-55.
4. Eisenberg D, Azagury DE, Ghiassi S, Grover BT, Kim JJ. ASMBS Position Statement on Postprandial Hyperinsulinemic Hypoglycemia after Bariatric Surgery. Surg Obes Relat Dis. 2017;13(3):371-8.
5. van Meijeren J, Timmer I, Brandts H, Janssen I, de Boer H. Evaluation of carbohydrate restriction as primary treatment for postgastric bypass hypoglycemia. Surg Obes Relat Dis. 2017;13(3):404-10.
6. Guimaraes M, Rodrigues P, Pereira SS, Nora M, Goncalves G, Albrechtsen NW, et al. GLP1 and glucagon co-secreting pancreatic neuroendocrine tumor presenting as hypoglycemia after gastric bypass. Endocrinol Diabetes Metab Case Rep. 2015;2015:150049.
7. Marsk R, Jonas E, Rasmussen F, Naslund E. Nationwide cohort study of post-gastric bypass hypoglycaemia including 5,040 patients undergoing surgery for obesity in 1986-2006 in Sweden. Diabetologia. 2010;53(11):2307-11.
8. American Diabetes A. 6. Glycemic Targets: Standards of Medical Care in Diabetes-2021. Diabetes Care. 2021;44(Suppl 1):S73-S84.
9. Battelino T, Danne T, Bergenstal RM, Amiel SA, Beck R, Biester T, et al. Clinical Targets for Continuous Glucose Monitoring Data Interpretation: Recommendations From the International Consensus on Time in Range. Diabetes Care. 2019;42(8):1593-603.
10. Lobato CB, Pereira SS, Guimarães M, Morais T, Oliveira P, de Carvalho JPM, et al. Use of flash glucose monitoring for post-bariatric hypoglycaemia diagnosis and management. Scientific Reports. 2020;10(1):11061.
11. Tharakan G, Behary P, Wewer Albrechtsen NJ, Chahal H, Kenkre J, Miras AD, et al. Roles of increased glycemic variability, GLP-1 and glucagon in hypoglycaemia after Roux-en-Y gastric bypass. Eur J Endocrinol. 2017.
12. Salehi M, Gastaldelli A, D’Alessio DA. Blockade of glucagon-like peptide 1 receptor corrects postprandial hypoglycemia after gastric bypass. Gastroenterology. 2014;146(3):669-80 e2.
13. Stano S, Alam F, Wu L, Dutia R, Ng SN, Sala M, et al. Effect of meal size and texture on gastric pouch emptying and glucagon-like peptide 1 after gastric bypass surgery. Surg Obes Relat Dis. 2017.
14. Murphy CF, Elliott JA, Docherty NG, Mohamed AA, Vincent RP, Ravi N, et al. Exaggerated postprandial GLP-1 secretion following esophagectomy is not associated with gastric emptying and intestinal transit. Dis Esophagus. 2020.
15. Kandel D, Bojsen-Moller KN, Svane MS, Samkani A, Astrup A, Holst JJ, et al. Mechanisms of action of a carbohydrate-reduced, high-protein diet in reducing the risk of postprandial hypoglycemia after Roux-en-Y gastric bypass surgery. Am J Clin Nutr. 2019.
16. Lobato CB, Pereira SS, Guimaraes M, Hartmann B, Wewer Albrechtsen NJ, Hilsted L, et al. A Potential Role for Endogenous Glucagon in Preventing Post-Bariatric Hypoglycemia. Front Endocrinol (Lausanne). 2020;11:608248.
17. Salinari S, Mingrone G, Bertuzzi A, Previti E, Capristo E, Rubino F. Down-regulation of Insulin Sensitivity After Oral Glucose Administration: Evidence for the “Anti-Incretin Effect”. Diabetes. 2017.
18. Meier JJ, Butler AE, Galasso R, Butler PC. Hyperinsulinemic hypoglycemia after gastric bypass surgery is not accompanied by islet hyperplasia or increased beta-cell turnover. Diabetes Care. 2006;29(7):1554-9.
19. Zaloga GP, Chernow B. Postprandial hypoglycemia after Nissen fundoplication for reflux esophagitis. Gastroenterology. 1983;84(4):840-2.
20. Mathur S, Boparai J, Mediwala SN, Garcia JM, Cunningham GR, Marcelli M, et al. Reversible Adrenal Insufficiency in Three Patients With Post-Roux-en-Y Gastric Bypass Noninsulinoma Pancreatogenous Hypoglycemia Syndrome. J Investig Med High Impact Case Rep. 2014;2(1):2324709614526992.
21. Scarpellini E, Arts J, Karamanolis G, Laurenius A, Siquini W, Suzuki H, et al. International consensus on the diagnosis and management of dumping syndrome. Nat Rev Endocrinol. 2020.
22. Yaqub A, Smith EP, Salehi M. Hyperinsulinemic hypoglycemia after gastric bypass surgery: what’s up and what’s down? Int J Obes (Lond). 2017.
23. Vilarrasa N, Goday A, Rubio MA, Caixas A, Pellitero S, Ciudin A, et al. Hyperinsulinemic Hypoglycemia after Bariatric Surgery: Diagnosis and Management Experience from a Spanish Multicenter Registry. Obes Facts. 2016;9(1):41-51.
24. Lee CJ, Clark JM, Schweitzer M, Magnuson T, Steele K, Koerner O, et al. Prevalence of and risk factors for hypoglycemic symptoms after gastric bypass and sleeve gastrectomy. Obesity (Silver Spring). 2015;23(5):1079-84.
25. Roslin M, Damani T, Oren J, Andrews R, Yatco E, Shah P. Abnormal glucose tolerance testing following gastric bypass demonstrates reactive hypoglycemia. Surg Endosc. 2011;25(6):1926-32.
26. Ilesanmi I, Tharakan G, Alexiadou K, Behary P, Alessimii H, Bovill-Taylor C, et al. Roux-en-Y Gastric Bypass Increases Glycemic Variability and Time in Hypoglycemia in Patients With Obesity and Prediabetes or Type 2 Diabetes: A Prospective Cohort Study. Diabetes Care. 2021;44(2):614-7.
27. Marques AR, Lobato CB, Pereira SS, Guimaraes M, Faria S, Nora M, et al. Insights from the Impact of Meal Composition on Glucose Profile Towards Post-bariatric Hypoglycemia Management. Obes Surg. 2019.
28. Suhl E, Anderson-Haynes SE, Mulla C, Patti ME. Medical nutrition therapy for post-bariatric hypoglycemia: practical insights. Surg Obes Relat Dis. 2017.
29. Valderas JP, Ahuad J, Rubio L, Escalona M, Pollak F, Maiz A. Acarbose improves hypoglycaemia following gastric bypass surgery without increasing glucagon-like peptide 1 levels. Obes Surg. 2012;22(4):582-6.
30. Ritz P, Vaurs C, Bertrand M, Anduze Y, Guillaume E, Hanaire H. Usefulness of acarbose and dietary modifications to limit glycemic variability following Roux-en-Y gastric bypass as assessed by continuous glucose monitoring. Diabetes Technol Ther. 2012;14(8):736-40.
31. Halperin F, Patti ME, Goldfine AB. Glucagon treatment for post-gastric bypass hypoglycemia. Obesity (Silver Spring). 2010;18(9):1858-60.
32. Mulla CM, Zavitsanou S, Laguna Sanz AJ, Pober D, Richardson L, Walcott P, et al. A Randomized, Placebo-Controlled Double-Blind Trial of a Closed-Loop Glucagon System for Post-Bariatric Hypoglycemia. J Clin Endocrinol Metab. 2019.
33. Craig CM, Liu LF, Deacon CF, Holst JJ, McLaughlin TL. Critical role for GLP-1 in symptomatic post-bariatric hypoglycaemia. Diabetologia. 2017;60(3):531-40.
34. Abrahamsson N, Engstrom BE, Sundbom M, Karlsson FA. GLP1 analogs as treatment of postprandial hypoglycemia following gastric bypass surgery: a potential new indication? Eur J Endocrinol. 2013;169(6):885-9.
35. Ohrstrom CC, Worm D, Hojager A, Andersen D, Holst JJ, Kielgast UL, et al. Postprandial hypoglycaemia after Roux-en-Y gastric bypass and the effects of acarbose, sitagliptin, verapamil, liraglutide and pasireotide. Diabetes Obes Metab. 2019.
36. Mathavan VK, Arregui M, Davis C, Singh K, Patel A, Meacham J. Management of postgastric bypass noninsulinoma pancreatogenous hypoglycemia. Surg Endosc. 2010;24(10):2547-55.
37. Svane MS, Toft-Nielsen MB, Kristiansen VB, Hartmann B, Holst JJ, Madsbad S, et al. Nutrient re-routing and altered gut-islet cell crosstalk may explain early relief of severe postprandial hypoglycaemia after reversal of Roux-en-Y gastric bypass. Diabet Med. 2017.
38. Dapri G, Cadière GB, Himpens J. Laparoscopic reconversion of Roux-en-Y gastric bypass to original anatomy: technique and preliminary outcomes. Obes Surg. 2011;21(8):1289-95.
39. Lee CJ, Brown T, Magnuson TH, Egan JM, Carlson O, Elahi D. Hormonal response to a mixed-meal challenge after reversal of gastric bypass for hypoglycemia. J Clin Endocrinol Metab. 2013;98(7):E1208-12.
Published
2021-08-09
How to Cite
LOBATO, Carolina B.; MONTEIRO, Mariana P.; GUIMARÃES, Marta.
POST-BARIATRIC HYPOGLYCAEMIA: FROM SCIENTIFIC EVIDENCE TO CLINICAL PRACTICE.
Revista Portuguesa de Cirurgia, [S.l.], n. 50, p. 33-42, aug. 2021.
ISSN 2183-1165.
Available at: <https://revista.spcir.com/index.php/spcir/article/view/884>. Date accessed: 16 apr. 2024.
doi: https://doi.org/10.34635/rpc.884.
Section
Original Papers
