Post-gastric bypass hypoglycemia: Diagnosis and management

Bariatric Surgery Complications and Emergencies

Volumn , Issue , 2016, Pages 253-268

  Fischer, Laura E ^a   Belt Davis, Dawn ^a   Khoraki, Jad ^a   Campos, Guilherme M ^b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Hyperinsulinemia; Hypoglycemia; Pancreatectomy; Reversal of gastric bypass; Roux en Y gastric bypass

Indexed keywords

EID: 84978296133     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-319-27114-9_21     Document Type: Chapter

References (95)

1. Ukleja A. Dumping syndrome: pathophysiology and treatment. Nutr Clin Pract. 2005;20(5): 517-25.
2. Ceppa EP, Ceppa DP, Omotosho PA, et al. Algorithm to diagnose etiology of hypoglycemia after Rouxen-Y gastric bypass for morbid obesity: case series and review of the literature. Surg Obes Relat Dis. 2012;8(5): 641-7.
3. Choudhary P, Teh MM, Amiel SA. Methods of assessment of counterregulation to hypoglycaemia. In: Roden M, editor. Clinical diabetes research: methods and techniques. Hoboken, NJ: John Wiley & Sons, Ltd.; 2007.
4. Kellogg TA, Bantle JP, Leslie DB, et al. Postgastric bypass hyperinsulinemic hypoglycemia syndrome: characterization and response to a modified diet. Surg Obes Relat Dis. 2008;4(4): 492-9.
5. Service FJ, Natt N, Thompson GB, et al. Noninsulinoma pancreatogenous hypoglycemia: a novel syndrome of hyperinsulinemic hypoglycemia in adults independent of mutations in Kir6.2 and SUR1 genes. J Clin Endocrinol Metab. 1999;84(5): 1582-9.
6. Roslin M, Damani T, Oren J, et al. Abnormal glucose tolerance testing following gastric bypass demonstrates reactive hypoglycemia. Surg Endosc. 2011;25(6): 1926-32.
7. Deitel M. The change in the dumping syndrome concept. Obes Surg. 2008;18(12): 1622-4.
8. Sawyers JL. Management of postgastrectomy syndromes. Am J Surg. 1990;159(1): 8-14.
9. Rodieux F, Giusti V, D’Alessio DA, et al. Effects of gastric bypass and gastric banding on glucose kinetics and gut hormone release. Obesity (Silver Spring). 2008;16(2): 298-305.
10. Mingrone G, Castagneto-Gissey L. Mechanisms of early improvement/resolution of type 2 diabetes after bariatric surgery. Diabetes Metab. 2009;35(6 Pt 2): 518-23.
11. Laferrere B. Do we really know why diabetes remits after gastric bypass surgery? Endocrine. 2011;40(2): 162-7.
12. Anderwald C-H, Tura A, Promintzer-Schifferl M, et al. Alterations in gastrointestinal, endocrine, and metabolic processes after bariatric Roux-en-Y gastric bypass surgery. Diabetes Care. 2012;35(12): 2580-7.
13. Caiazzo R, Zerrweck C, Verhaeghe R, et al. Gastric bypass and glucose metabolism. Diabetes Metab. 2009;35(6 Pt 2): 528-31.
14. Korner J, Inabnet W, Conwell IM, et al. Differential effects of gastric bypass and banding on circulating gut hormone and leptin levels. Obesity (Silver Spring). 2006;14(9): 1553-61.
15. Rubino F, Gagner M, Marescaux J. Surgical treatment of type 2 diabetes mellitus. Lancet. 2001;358(9282): 668-9.
16. Bikman BT, Zheng D, Pories WJ, et al. Mechanism for improved insulin sensitivity after gastric bypass surgery. J Clin Endocrinol Metab. 2008;93(12): 4656-63.
17. Cummings DE. Gastric bypass and nesidioblastosis-too much of a good thing for islets? N Engl J Med. 2005;353(3): 300-2.
18. Korner J, Inabnet W, Febres G, et al. Prospective study of gut hormone and metabolic changes after adjustable gastric banding and Roux-en-Y gastric bypass. Int J Obes (Lond). 2009;33(7): 786-95.
19. Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP. Gastroenterology. 2007;132(6): 2131-57.
20. Adams TD, Gress RE, Smith SC, et al. Long-term mortality after gastric bypass surgery. N Engl J Med. 2007;357(8): 753-61.
21. Buchwald H, Estok R, Fahrbach K, et al. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med. 2009;122(3): 248-56.
22. Adams TD, Pendleton RC, Strong MB, et al. Health outcomes of gastric bypass patients compared to nonsurgical, nonintervened severly obese. Obesity (Silver Spring). 2010;18(1): 121-30.
23. Service GJ, Thompson GB, Service FJ, et al. Hyperinsulinemic hypoglycemia with nesidioblastosis after gastric-bypass surgery. N Engl J Med. 2005;353(3): 249-54.
24. Clancy TE, Moore FD, Zinner MJ. Post-gastric bypass hyperinsulinism with nesidioblastosis: subtotal or total pancreatectomy may be needed to prevent recurrent hypoglycemia. J Gastrointest Surg. 2006;10(8): 1116-9.
25. Patti ME, McMahon G, Mun EC, et al. Severe hypoglycaemia post-gastric bypass requiring partial pancreatectomy: evidence for inappropriate insulin secretion and pancreatic islet hyperplasia. Diabetologia. 2005;48(11): 2236-40.
26. Alvarez GC, Faria EN, Beck M, et al. Laparoscopic spleen-preserving distal pancreatectomy as treatment for nesidioblastosis after gastric bypass surgery. Obes Surg. 2007;17(4): 550-2.
27. Meier JJ, Butler AE, Galasso R, et al. Hyperinsulinemic hypoglycemia after gastric bypass surgery is not accompanied by islet hyperplasia or increased betacell turnover. Diabetes Care. 2006;29(7): 1554-9.
28. Verhaeghe R, Zerrweck C, Hubert T, et al. Gastric bypass increases postprandial insulin and GLP-1 in nonobese minipigs. Eur Surg Res. 2014;52(1-2): 41-9.
29. Salehi M, Prigeon RL, D’Alessio DA. Gastric bypass surgery enhances glucagon-like peptide 1-stimulated postprandial insulin secretion in humans. Diabetes. 2011;60(9): 2308-14.
30. Korner J, Bessler M, Inabnet W, et al. Exaggerated glucagon-like peptide-1 and blunted glucosedependent insulinotropic peptide secretion are associated with Roux-en-Y gastric bypass but not adjustable gastric banding. Surg Obes Relat Dis. 2007;2007(3): 6.
31. Rabiee A, Magruder JT, Salas-Carrillo R, et al. Hyperinsulinemic hypoglycemia after Roux-en-Y gastric bypass: unraveling the role of gut hormonal and pancreatic endocrine dysfunction. J Surg Res. 2011;2011(167): 2.
32. Lee CJ, Brown T, Magnuson TH, et al. Hormonal response to a mixed-meal challenge after reversal of gastric bypass for hypoglycemia. J Clin Endocrinol Metab. 2013;98(7): E1208-12.
33. Laferrere B, Teixeira J, McGinty J, et al. Effect of weight loss by gastric bypass surgery versus hypocaloric diet on glucose and incretin levels in patients with type 2 diabetes. J Clin Endocrinol Metab. 2008;93(7): 2479-85.
34. Reubi JC, Perren A, Rehmann R, et al. Glucagon-like peptide (GLP-1) receptors are not overexpressed in pancreatic islets from patients with severe hyperinsulinaemic hypoglycaemia following gastric bypass. Diabetologia. 2010;53(12): 2641-5.
35. Salehi M, Gastaldelli A, D’Alessio DA. Blockage of glucagon-like peptide 1 receptor corrects postprandial hypoglycemia after gastric bypass. Gastroenterology. 2014;146(3): 669-80.
36. Goldfine AB, Mun EC, Devine E, et al. Patients with neuroglycopenia after gastric bypass surgery have exaggerated incretin and insulin secretory responses to a mixed meal. J Clin Endocrinol Metab. 2007;92(12): 4678-85.
37. Campos GM, Rabl C, Peeva S, et al. Improvement in peripheral glucose uptake after gastric bypass surgery is observed only after substantial weight loss has occurred and correlates with the magnitude of weight loss. J Gastrointest Surg. 2010;14(1): 15-23.
38. Patti ME, Goldfine AB. Hypoglycemia after gastric bypass: the dark side of GLP-1. Gastroenterology. 2014;146(3): 605-8.
39. Davis DB, Khoraki J, Campos GM. Recalcitrant hypoglycemia with neuroglycopenia after Roux-en-Y gastric bypass is caused by postprandial changes in glucose, gut and pancreatic hormone responses to altered feeding route, not nesidioblastosis. Scientific Papers Session. 31st Annual Meeting. American Society for Bariatric and Metabolic Surgery. Boston, MA; 2014.
40. Campos GM, Ziemelis M, Paparodis R, et al. Laparoscopic reversal of Roux-en-Y gastric bypass: technique and utility for treatment of endocrine complications. Surg Obes Relat Dis. 2014;10(1): 36-43.
41. Vilallonga R, van de Vrande S, Himpens J. Laparoscopic reversal of Roux-en-Y gastric bypass into normal anatomy with or without sleeve gastrectomy. Surg Endosc. 2013;27(12): 4640-8.
42. Cryer PE, Axelrod L, Grossman AB, et al. Evaluation and management of adult hypoglycemic disorders: an Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab. 2009;94(3): 709-28.
43. Lev-Ran A, Anderson RW. The diagnosis of postprandial hypoglycemia. Diabetes. 1981;30(12): 996-9.
44. Service FJ. Hypoglycemic disorders. N Engl J Med. 1995;332(17): 1144-52.
45. Mordes JP, Alonso LC. Evaluation, medical therapy, and course of adult persistent hyperinsulinemic hypoglycemia after Roux-en-Y gastric bypass surgery: a case series. Endocr Pract. 2014;1-34 (Epub ahead of print).
46. Scarpignato C. The place of octreotide in the medical management of the dumping syndrome. Digestion. 1996;57 Suppl 1: 114-8.
47. McLoughlin JC, Buchanan KD, Alam MJ. A glycoside-hydrolase inhibitor in treatment of dumping syndrome. Lancet. 1979;314(8143): 603-5.
48. Moreira RO, Moreira RB, Machado NAM, et al. Postprandial hypoglycemia after bariatric surgery: pharmacological treatment with verapamil and acarbose. Obes Surg. 2008;18(12): 1618-21.
49. Arao T, Okada Y, Hirose A, et al. A rare case of adultonset nesidioblastosis treated successfully with diazoxide. Endocr J. 2006;53(1): 95-100.
50. Ritz P, Vaurs C, Bertrand M, et al. 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.
51. Valderas JP, Ahuad J, Rubio L, et al. Acarbose improves hypoglycaemia following gastric bypass surgery without increasing glucagon-like peptide 1 levels. Obes Surg. 2012;22(4): 582-6.
52. Frankhouser SY, Ahmad AN, Perilli GA, et al. Postgastric-bypass hypoglycemia successfully treated with alpha-glucosidase inhibitor therapy. Endocr Pract. 2013;19(3): 511-4.
53. Geer RJ, Richards WO, O’Dorisio TM, et al. Efficacy of octreotide acetate in treatment of severe postgastrectomy dumping syndrome. Ann Surg. 1990;212(6): 678-87.
54. de Heide LJ, Laskewitz AJ, Apers JA. Treatment of severe postRYGB hyperinsulinemic hypoglycemia with pasireotide: a comparison with octreotide on insulin, glucagon, and GLP-1. Surg Obes Relat Dis. 2014;10(3): e31-3.
55. Myint KS, Greenfield JR, Farooqi IS, et al. Prolonged successful therapy for hyperinsulinaemic hypoglycaemia after gastric bypass: the pathophysiological role of GLP1 and its response to a somatostatin analogue. Eur J Endocrinol. 2012;166(5): 951-5.
56. Tabibian N. Successful treatment of refractory postvagotomy syndrome with verapamil (Calan SR). Am J Gastroenterol. 1990;85(3): 328-9.
57. Fernandez-Esparrach G, Lautz DB, Thompson CC. Peroral endoscopic anastomotic reduction improves intractable dumping syndrome in Rouxen-Y gastric bypass patients. Surg Obes Relat Dis. 2010;6(1): 36-40.
58. Leitman IM, Virk CS, Avgerinos DV, et al. Early results of trans-oral endoscopic plication and revision of the gastric pouch and stoma following Roux-en-Y gastric bypass surgery. JSLS. 2010;14(2): 217-20.
59. Vanderveen KA, Grant CS, Thompson GB, et al. Outcomes and quality of life after partial pancreatectomy for noninsulinoma pancreatogenous hypoglycemia from diffuse islet cell disease. Surgery. 2010;148(6): 1237-45.
60. Himpens J, Dapri G, Cadiere GB. Laparoscopic conversion of the gastric bypass into a normal anatomy. Obes Surg. 2006;16(7): 908-12.
61. Dapri G, Cadiere 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.
62. Campos GM, Jablons D, Brown LM, Ramirez RM, et al. A safe and reproducible anastomotic technique for minimally invasive Ivor Lewis oesophagectomy: the circular-stapled anastomosis with the trans-oral anvil. Eur J Cardiothorac Surg. 2010;37(6): 1421-6.
63. Mix CL. "Dumping stomach" following gastrojejunostomy. Surg Clin North Am. 1922;2: 617-22.
64. Banerjee A, Ding Y, Mikami DJ, et al. The role of dumping syndrome in weight loss after gastric bypass surgery. Surg Endosc. 2013;27(5): 1573-8.
65. Lips MA, de Groot GH, van Klinken JB, et al. Calorie restriction is a major determinant of the short-term metabolic effects of gastric bypass surgery in obese type 2 diabetic patients. Clin Endocrinol (Oxf). 2014;80(6): 834-42.
66. Isbell JM, Tamboli RA, Hansen EN, et al. The importance of caloric restriction in the early improvements in insulin sensitivity after Roux-en-Y gastric bypass surgery. Diabetes Care. 2010;33(7): 1438-42.
67. Lingvay I, Guth E, Islam A, et al. Rapid improvement in diabetes after gastric bypass surgery: is it the diet or surgery? Diabetes Care. 2013;36(9): 2741-7.
68. Swarbrick MM, Stanhope KL, Austrheim-Smith IT, et al. Longitudinal changes in pancreatic and adipocyte hormones following Roux-en-Y gastric bypass surgery. Diabetologia. 2008;51(10): 1901-11.
69. Olbers T, Bjorkman S, Lindroos A, et al. Body composition, dietary intake, and energy expenditure after laparoscopic Roux-en-Y gastric bypass and laparoscopic vertical banded gastroplasty: a randomized clinical trial. Ann Surg. 2006;244(5): 715-22.
70. Tamboli RA, Hossain HA, Marks PA, et al. Body composition and energy metabolism following Rouxen-Y gastric bypass surgery. Obesity (Silver Spring). 2010;18(9): 1718-24.
71. Miller GD, Carr JJ, Fernandez AZ. Regional fat changes following weight reduction from laparoscopic Roux-en-Y gastric bypass surgery. Diabetes Obes Metab. 2011;13(2): 189-92.
72. Immonen H, Hannukainen JC, Iozzo P, et al. Effect of bariatric surgery on liver glucose metabolism in morbidly obese diabetic and non-diabetic patients. J Hepatol. 2014;60(2): 377-83.
73. Lin E, Phillips LS, Ziegler TR, et al. Increases in adinopectin predict improved liver, but not peripheral, insulin sensitivity in severly obese women during weight loss. Diabetes. 2007;56(3): 735-42.
74. Malin SK, Bena J, Abood B, et al. Attenuated improvements in adinopectin and fat loss characterize type 2 diabetes non-remission status after bariatric surgery. Diabetes Obes Metab. 2014;16(12): 1230-8.
75. Geloneze B, Tambascia MA, Pareja JC, et al. Serum leptin levels after bariatric surgery across a range of glucose tolerance from normal to diabetes. Obes Surg. 2001;11(6): 693-8.
76. Camastra S, Gastaldelli A, Mari A, et al. Early and longer term effects of gastric bypass surgery on tissue-specific insulin sensitivity and beta cell function in morbidly obese patients with and without type 2 diabetes. Diabetologia. 2011;54(8): 2093-102.
77. Dunn JP, Abumrad NN, Breitman I, et al. Hepatic and peripheral insulin sensitivity and diabetes remission at 1 month after Roux-en-Y gastric bypass surgery in patients randomized to omentectomy. Diabetes Care. 2012;35(1): 137-42.
78. Bojsen-Moller KN, Dirksen C, Jorgensen NB, et al. Increased hepatic insulin clearance after Roux-en-Y gastric bypass. J Clin Endocrinol Metab. 2013;98(6): E1066-71.
79. Bojsen-Moller KN, Dirksen C, Jorgensen NB, et al. Early enhancements of hepatic and later of peripheral insulin sensitivity combined with increased postprandial insulin secretion contribute to improved glycemic control after Roux-en-Y gastric bypass. Diabetes. 2014;63(5): 1725-37.
80. Nannipieri M, Baldi S, Colligiani D, et al. Roux-en-Y gastric bypass and sleeve gastrectomy: mechanisms of diabetes remission and role of gut hormones. J Clin Endocrinol Metab. 2013;98(11): 4391-9.
81. Thaler JP, Cummings DE. Minireview: hormonal and metabolic mechanisms of diabetes remission after gastrointestinal surgery. Endocrinology. 2009;150(6): 2518-25.
82. Cummings DE, Weigle DS, Frayo RS, et al. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med. 2002;346(21): 1623-30.
83. Umeda LM, Silva EA, Carneiro G, et al. Early improvement in glycemic control after bariatric surgery and its relationships with insulin, GLP-1, and glucagon secretion in type 2 diabetic patients. Obes Surg. 2011;21(7): 896-901.
84. Kashyap SR, Daud S, Kelly KR, et al. Acute effects of gastric bypass versus gastric restrictive surgery on beta-cell function and insulinotropic hormones in severely obese patients with type 2 diabetes. Int J Obes (Lond). 2010;34(3): 462-71.
85. Weiss R. Effects of Roux-en-Y gastric bypass on β-cell function. Diabetes. 2014;63(4): 1171-3.
86. Ferrannini E, Mingrone G. Impact of different bariatric surgical procedures on insulin action and beta-cell function in type 2 diabetes. Diabetes Care. 2009;32(3): 514-20.
87. Rabl C, Rao MN, Schwarz JM, et al. Thermogenic changes after gastric bypass, adjustable gastric banding or diet alone. Surgery. 2014;156(4): 806-12.
88. Das SK, Roberts SB, McCrory MA, et al. Long-term changes in energy expenditure and body composition after massive weight loss induced by gastric bypass surgery. Am J Clin Nutr. 2003;78(1): 22-30.
89. Liou AP, Paziuk M, Luevano JM, Machineni S, et al. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med. 2013;5(178): 178ra41.
90. Vrieze A, Van Nood E, Holleman F, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143(4): 913-6.
91. Sweeney TE, Morton JM. Metabolic surgery: action via hormonal milieu changes, changes in bile acids or gut microbiota? A summary of the literature. Best Pract Res Clin Gastroenterol. 2014;28(4): 727-40.
92. Patti ME, Houten SM, Bianco AC, et al. Serum bile acids are higher in humans with prior gastric bypass: potential contribution to improved glucose and lipid metabolism. Obesity (Silver Spring). 2009;17(9): 1671-7.
93. Pournaras DJ, Glicksman C, Vincent RP, et al. The role of bile after Roux-en-Y gastric bypass in promoting weight loss and improving glycaemic control. Endocrinology. 2012;153(8): 3613-9.
94. Carswell KA, Vincent RP, Belgaumkar AP, et al. The effect of bariatric surgery on intestinal absorption and transit time. Obes Surg. 2014;24(5): 796-805.
95. Campos GM, Ziemelis M, Paparodis R, Ahmed M, Davis DB. Laparoscopic reversal of Roux-en-Y gastric bypass: technique and utility for treatment of endocrine complications. Surg Obes Relat Dis. 2014;10(1): 36-43. doi: 10.1016/j.soard.2013.05.012. Epub 2013 Jun 29.