Skip to main content

Advertisement

Log in

Advances in the Etiology and Management of Hyperinsulinemic Hypoglycemia After Roux-en-Y Gastric Bypass

  • Review Article
  • Published:
Journal of Gastrointestinal Surgery Aims and scope

Abstract

Introduction

Hyperinsulinemic hypoglycemia with severe neuroglycopenia has been identified as a late complication of Roux-en-Y gastric bypass (RYGB) in a small number of patients.

Discussion

The rapid resolution of type 2 diabetes mellitus after RYGB is probably related to increased secretion of the incretin hormones glucose-dependent insulinotropic polypeptide (GIP) and glucagon-like peptide-1 (GLP-1), and patients with post-RYGB hypoglycemia demonstrate prolonged elevations of GIP and GLP-1 compared to non-hypoglycemic post-RYGB patients. Nesidioblastosis has been identified in some patients with post-RYGB hypoglycemia and is likely due to the trophic effects of GIP and GLP-1 on pancreatic islets.

Conclusions

Treatment of hypoglycemia after RYGB should begin with strict dietary (low carbohydrate) alteration and may require a trial of diazoxide, octreotide, or calcium-channel antagonists, among other drugs. Surgical therapy should include consideration of a restrictive form of bariatric procedure, with or without reconstitution of gastrointestinal continuity. Partial or total pancreatic resection should be avoided.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Chambliss HO, Finley CE, Blair SN. Attitudes toward obese individuals among exercise science students. Med Sci Sports Exerc. 2004;36(3):468–74.

    PubMed  Google Scholar 

  2. Pi-Sunyer FX. Comorbidities of overweight and obesity: current evidence and research issues. Med Sci Sports Exerc. 1999;31 Suppl 11:S602–8.

    PubMed  CAS  Google Scholar 

  3. Calle EE, Thun MJ, Petrelli JM, Rodriguez C, Heath CW Jr. Body-mass index and mortality in a prospective cohort of U.S. adults. N Engl J Med. 1999;341(15):1097–105.

    PubMed  CAS  Google Scholar 

  4. Safer DJ. Diet, behavior modification, and exercise: a review of obesity treatments from a long-term perspective. South Med J. 1991;84(12):1470–4.

    PubMed  CAS  Google Scholar 

  5. Astrup A, Finer N. Redefining type 2 diabetes: diabesity or obesity dependent diabetes mellitus? Obes Rev 2000; 1: 57–59.

    PubMed  CAS  Google Scholar 

  6. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM. Prevalence of overweight and obesity in the United States, 1999–2004. JAMA. 2006; 295(13):1549–55.

    PubMed  CAS  Google Scholar 

  7. CDC. State-specific prevalence of obesity among adults—United States, 2005. MMWR Morb Mortal Wkly Rep. 2006; 55(36): 985–8

    Google Scholar 

  8. Sjostrom L, Lindroos AK, Peltonen M, Torgerson J, BouchardC, Carlsson B, Dahlgren S, Larsson B, Narbro K, Sjostrom CD,Sullivan M, Wedel H. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med 2004; 351:2683–2693

    PubMed  Google Scholar 

  9. Sjostrom L, Narbro K, Sjostrom CD, Karason K, Larsson B,Wedel H, Lystig T, Sullivan M, Bouchard C, Carlsson B, BengtssonC, Dahlgren S, Gummesson A, Jacobson P, Karlsson J, LindroosAK, Lonroth H, Naslund I, Olbers T, Stenlof K, Torgerson J,Agren G, Carlsson LM. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med 2007; 357: 741–752

    PubMed  Google Scholar 

  10. Hafner RJ, Watts JM, Rogers J. Quality of life after gastric bypass for morbid obesity. Int J Obes. 1991; 15(8): 555–60.

    PubMed  CAS  Google Scholar 

  11. McTigue KM, Harris R, Hemphill B, Lux L, Sutton S, Bunton AJ, et al. Screening and interventions for obesity in adults: summary of the evidence for the U.S. Preventive Services Task Force. Ann Intern Med. 2003;139(11):933–49.

    PubMed  Google Scholar 

  12. Herpertz S, Kielmann R, Wolf AM, Langkafel M, Senf W, Hebebrand J. Does obesity surgery improve psychosocial functioning? A systematic review. Int J Obes Relat Metab Disord. 2003; 27(11):1300–14.

    PubMed  CAS  Google Scholar 

  13. Ashrafian H, le Roux CW. Metabolic surgery and guthormones – a review of bariatric entero-humoral modulation. Physiol Behav 2009; 97: 620–631.

    PubMed  CAS  Google Scholar 

  14. Ashrafian H, Darzi A, Athanasiou T. Autobionics: a newparadigm in regenerative medicine and surgery. Regen Med 2010; 5: 279–288.

    PubMed  Google Scholar 

  15. Buchwald H, Oien DM. Metabolic/bariatric surgery Worldwide 2008. Obes Surg 2009; 19: 1605–1611.

    PubMed  Google Scholar 

  16. Service GJ, Thompson GB, Service FJ, Andrews JC, Collazo- Clavell ML, Lloyd RV. Hyperinsulinemic hypoglycemia with nesidioblastosis after gastric-bypass surgery. N Engl J Med 2005; 353(3): 249–54

    PubMed  CAS  Google Scholar 

  17. Patti ME, McMahon G, Mun EC, Bitton A, Holst JJ, Goldsmith J, Hanto DW, Callery M, Arky R, Nose V, Bonner-Weir S, Goldfine AB. Severe hypoglycaemia post-gastric bypass requiring partial pancreatectomy: evidence for inappropriate insulin secretion and pancreatic islet hyperplasia. Diabetologia. 2005; 48(11): 2236–40.

    PubMed  CAS  Google Scholar 

  18. Clancy TE, Moore FD Jr, 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.

    PubMed  Google Scholar 

  19. Alvarez GC, Faria EN, Beck M, Girardon DT, Machado AC. Laparoscopic spleen-preserving distal pancreatectomy as treatment for nesidioblastosis after gastric bypass surgery. Obes Surg 2007; 17(4): 550–2.

    PubMed  Google Scholar 

  20. Kellogg TA, Bantle JP, Leslie DB, Redmond JB, Slusarek B, Swan T, Buchwald H, Ikramuddin S. Postgastric bypass hyperinsulinemic hypoglycemia syndrome: characterization and response to a modified diet. Surg Obes Relat Dis 2008; 4: 492–499.

    PubMed  Google Scholar 

  21. Marsk R, Jonas E, Rasmussen F, Näslund E. Nationwide cohort study of post-gastric bypass hypoglycemia including 5,040 patients undergoing surgery for obesity in 1986–2006 in Sweden. Diabetologia 2010; 53: 2307–2311.

    PubMed  CAS  Google Scholar 

  22. Evensen OK. Alimentary hypoglycemia after stomach operations and influence of gastric emptying on glucose tolerance curve. Acta Med Scand 1942; Suppl 126: 99–114

    Google Scholar 

  23. Barnes CG. Hypoglycaemia following partial gastrectomy. Lancet 1947; 2: 536–539.

    PubMed  CAS  Google Scholar 

  24. Gilbert JAL, Dunlop DM. Hypoglycaemia following partial gastrectomy. Br Med J 1947; 2: 330–332.

    PubMed  CAS  Google Scholar 

  25. Bacon PA, Myles AB. Hypoglycaemic coma after partial gastrectomy. Postgrad Med 1971; 47: 134–136.

    CAS  Google Scholar 

  26. Marks V, Rose FC. Reactive (rebound) hypoglycaemia. In: Marks V, Rose FC. Hypoglycaemia. 2nd Ed. Blackwell Scientific Publ. Oxford. 1981. pp 179–215

    Google Scholar 

  27. Goligher JC, Pulvertaft CN, deDombal FT, Conyers JH, Duthie HL, Feather DB, Latchmore AJC, Harrop Shoesmith J, Smiddy FG, Willson-Pepper J. Five- to eight-year results of Leeds/York controlled trial of elective surgery for duodenal ulcer. Br Med J 1968; 2: 781–787

    PubMed  CAS  Google Scholar 

  28. Yalow RS, Berson S. Immunoassay of endogenous plasma insulin. J Clin Invest 1960; 39: 1157–1161.

    PubMed  CAS  Google Scholar 

  29. McIntyre N, Holdsworth CD, Turner DS. New interpretation of oral glucose tolerance. Lancet 1964; 2: 20–25.

    PubMed  CAS  Google Scholar 

  30. LaBarre J. Sur les possibilities d’un traitement du diabete par l’incretine. Bull Acad R Med Belg 1932; 12: 620–634.

    Google Scholar 

  31. Roth DA, Meade RC. Hyperinsulinism-hypoglycemia in the post-gastrectomy patient. Diabetes 1965; 14: 526–528.

    PubMed  CAS  Google Scholar 

  32. Holdsworth CD, Turner D, McIntyre N. Pathophysiology of post-gastrectomy hypoglycaemia. Br Med J 1969; 4: 257–259.

    PubMed  CAS  Google Scholar 

  33. Schultz KT, Neelon FA, Nilson LB, Lebovitz HE. Mechanism of postgastrectomy hypoglycemia. Arch Int Med 1971; 128: 240–246.

    Google Scholar 

  34. Brown JC, Dryburgh JR. A gastric inhibitory polypeptide. II. The complete amino acid sequence. Can J Biochem 1971; 49: 867–872.

    PubMed  CAS  Google Scholar 

  35. Dupre J, Ross SA, Watson D, Brown JC. Stimulation of insulin secretion by gastric inhibitory polypeptide in man. J Clin Endocrinol Metab 1973; 37: 826–828.

    PubMed  CAS  Google Scholar 

  36. Andersen DK, Elahi D, Tobin JD, Andres R. Oral glucose augmentation of insulin secretion: Interactions of gastric inhibitory polypeptide with ambient glucose and insulin levels. J Clin Invest 1978; 62: 152–161.

    PubMed  CAS  Google Scholar 

  37. Elahi D, Andersen DK, Brown JC, Debas HT, Hershcopf RJ, Raizes GS, Tobin JD, Andres R. Pancreatic alpha- and beta-cell responses to gastric inhibitory polypeptide infusion in normal man. Am J Physiol 1979; 237(2): E185-E191.

    PubMed  CAS  Google Scholar 

  38. Bell GI, Santerre RF, Mullenbach GT. Hamster preproglucagon contains the sequence of glucagon and two related peptides. Nature 1983; 302: 716–718.

    PubMed  CAS  Google Scholar 

  39. Schmidt WE, Siegel EG, Creutzfeldt W. Glucagon-like peptide-1 but not glucagon-like peptide-2 stimulates insulin release from isolated rat pancreatic islets. Diabetologia 1985; 28: 704–707.

    PubMed  CAS  Google Scholar 

  40. Elahi D, McAloon-Dyke M, Fukagawa NK, Meneilly GS, Sclater AL, Minaker KL, Habener JF, Andersen DK. The insulinotropic actions of glucose-dependent insulinotropic polypeptide (GIP) and glucagon-like peptide-1 (7–37) in normal and diabetic subjects. Reg Peptides 1994; 51: 63–74.

    CAS  Google Scholar 

  41. Creutzfeldt W, Ebert R. Release of gastric inhibitory polypeptide (GIP) to a test meal under normal and pathological conditions in man. In: Bajaj JS (Ed). Diabetes. Exerpta Medica Intern Congr Series, Amsterdam. 1977; pp 413–419.

    Google Scholar 

  42. Mason EE, Ito C. Gastric bypass in obesity. Surg Clin North Am 1967; 47: 1345–1351.

    PubMed  CAS  Google Scholar 

  43. Suter M, Calmes JM, Paroz A, Romy S, Giusti V. Results of Roux-en-Y gastric bypass in morbidly obese vs superobese patients: similar body weight loss, correction of comorbidities, and improvement of quality of life. Arch Surg 2009; 144: 312– 318.

    PubMed  Google Scholar 

  44. Flum DR, Belle SH, King WC, Wahed AS, Berk P, Chapman W, Pories W, Courcoulas A, McCloskey C, Mitchell J, Patterson E, Pomp A, Staten MA, Yanovski SZ, Thirlby R, Wolfe B. Perioperative safety in the longitudinal assessment of bariatric surgery. N Engl J Med 2009; 361: 445–454.

    PubMed  Google Scholar 

  45. Robinson MK. Surgical treatment of obesity – weighing the facts. N Engl J Med 2009; 361: 520–521.

    PubMed  CAS  Google Scholar 

  46. Gracia JA, Martinez M, Elia M, Aguilella V, Royo P, Jimenez A, Bielsa MA, Arribas D. Obesity surgery results depending on technique performed: long-term outcome. Obes Surg 2009; 19: 432–438.

    PubMed  CAS  Google Scholar 

  47. Van Hee RH. Biliopancreatic diversion in the surgical treatment of morbid obesity. World J Surg 2004; 28: 435–444.

    PubMed  Google Scholar 

  48. Tice JA, Karliner L, Walsh J, Petersen AJ, Feldman MD. Gastric banding or bypass? A systematic review comparing the two most popular bariatric procedures. Am J Med 2008; 121: 885– 893.

    PubMed  Google Scholar 

  49. Patriti A, Facchiano E, Sanna A, Gulla N, Donini A. The enteroinsular axis and the recovery from type 2 diabetes after bariatric surgery. Obes Surg 2004; 14: 840–848.

    PubMed  Google Scholar 

  50. Bueter M, Ahmed A, Ashrafian H, le Roux CW. Bariatric surgery and hypertension. Surg Obes Relat Dis 2009; 5: 615–620.

    PubMed  Google Scholar 

  51. Polyzogopoulou EV, Kalfarentzos F, Vagenakis AG, et al. Restoration of euglycemia and normal acute insulin response to glucose in obese subjects with type 2 diabetes following bariatric surgery. Diabetes 2003; 52: 1098–1103.

    PubMed  CAS  Google Scholar 

  52. Wickremesekera K, Miller G, Naotunne TD, et al. Loss of insulin resistance after Roux-enY gastric bypass surgery: A timecourse study. Obes Surg 2005; 15: 474–481.

    PubMed  Google Scholar 

  53. Clements RH, Gonzalez QH, Long CI, et al. Hormonal changes after Roux-en-Y gastric bypass for morbid obesity and the control of Type-II diabetes mellitus. Am Surg 2004; 70: 1–4.

    PubMed  Google Scholar 

  54. Pontiroli AE, Pizzocri P, Librenti MC, et al. Laparoscopic adjustable banding for the treatment of morbid (grade 3) obesity and its metabolic complications: A three-year study. J Clin Endocrinol Metab 2002; 87: 3555–3561.

    PubMed  Google Scholar 

  55. Geloneze B, Tambascia MA, Pareja JC, et al. The insulin tolerance test in morbidly obese patients undergoing bariatric surgery. Obes Res 2001; 9: 763–769.

    PubMed  CAS  Google Scholar 

  56. Campos GM, Rabl C, Peeva S, Ciovica R, Rao M, Schwarz JM, Havel P, Schambelan M, Mulligan K. 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 lost. J Gastrointest Surg 2010; 14: 15–23.

    PubMed  Google Scholar 

  57. Friedman MN, Sancetta AJ, Magovern GJ. The amelioration of diabetes mellitus following subtotal gastrectomy, Surg Gynecol Obstet 1955; 100: 201–204.

    PubMed  CAS  Google Scholar 

  58. Angervall L, Dotevall G, Tillander H. Amelioration of diabetes mellitus following gastric resection. Acta Med Scand 1961; 169: 743–748.

    PubMed  CAS  Google Scholar 

  59. Bose M, Oliván B, Teixeira J, Pi-Sunyer FX, Laferrère B. Do incretins play a role in the remission of type 2 diabetes after gastric bypass surgery: What are the evidence? Obes Surg 2009; 19: 217–229.

    PubMed  Google Scholar 

  60. Goldfine AB, Mun EC, Devine E, Bernier R, Baz-Hecht M, Jones DB, Schneider BE, Holst JJ, Patti ME. Patients with neuroglycopenia after gastric bypass surgery have exaggerated incretin and insulin secretory responses to a mixed meal. J Clin Endocrinol Metab 2007; 92: 4678–4685.

    PubMed  CAS  Google Scholar 

  61. Laferrère 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: 2479–2485.

    PubMed  Google Scholar 

  62. Valverde I, Puente J, Martin-Duce A, et al. Changes in glucagon-like peptide-1 (GLP-1) secretion after biliopancreatic diversion or vertical banded gastroplasty in obese subjects. Obes Surg 2005; 15: 387–397.

    PubMed  Google Scholar 

  63. Guidone C, Manco M, Valera-Mora E, et al. Mechanism of recovery from type 2 diabetes after malabsorptive bariatric surgery. Diabetes 2006; 55: 2025–2031.

    PubMed  CAS  Google Scholar 

  64. Borg CM, le Roux CW, Ghatei MA, et al. Progressive rise in gut hormone levels after Roux-en-Y gastric bypass suggests gut adaptation and explains altered satiety. Br J Surg 2006; 93: 210–215.

    PubMed  CAS  Google Scholar 

  65. Morinigo R, Moize V, Musri M, et al. Glucagon-like peptide-1, peptide YY, hunger and satiety after gastric bypass surgery in morbidly obese subjects. J Clin Endocrinol Metab 2006; 91: 1735–1740.

    PubMed  CAS  Google Scholar 

  66. Reinehr T, Roth CL, Schernthaner GH, et al. Peptide YY and glucagon-like peptide-1 in morbidly obese patients before and after surgically induced weight loss. Obes Surg 2007; 17: 1571–1577.

    PubMed  Google Scholar 

  67. Laferrère B, Heshka S, Wang K, et al. Incretin levels and effect are markedly enhanced 1 month after Roux-en-Y gastric bypass surgery in obese patients with type 2 diabetes. Diabetes Care 2007; 30: 1709–1716.

    PubMed  Google Scholar 

  68. le Roux CW, Welbourn R, Werling M, et al. Gut hormones as mediators of appetite and weight loss after Roux-en-Y gastric bypass. Ann Surg 2007; 246: 780–785.

    PubMed  Google Scholar 

  69. Pournaras DJ, Osborne A, Hawkins SC, Mahon D, Ghatei MA, Bloom SR, Welbourn R, le Roux CW. The gut hormone response following Roux-en-Y gastric bypass: Cross-sectional and prospective study. Obes Surg 2010; 20:56–60.

    PubMed  Google Scholar 

  70. Morinigo R, Lacy AM, Casamitjana R, et al. GLP-1 and changes in glucose tolerance following gastric bypass surgery in morbidly obese subjects. Obes Surg 2006; 16: 1594–1601.

    PubMed  Google Scholar 

  71. Rabiee A, Magruder JT, Salas-Carrillo R, Carlson O, Egan JM, Askin FB, Elahi D, Andersen DK. Hyperinsulinemic hypoglycemia after Roux-en-Y gastric bypass: Unraveling the roles of gut hormonal and pancreatic endocrine dysfunction, J Surg Res 2011; 167: 199–205.

    PubMed  CAS  Google Scholar 

  72. Kim SH, Liu TC, Abbasi F, Lamendola C, Morton JM, Reaven GM, McLaughlin TL. Plasma glucose and insulin regulation is abnormal following gastric bypass surgery with or without neuroglycopenia. Obes Surg 2009; 19: 1550–1556.

    PubMed  Google Scholar 

  73. Reubi JC, Perren A, Rehmann R, Waser B, Christ E, Callery M, Goldfine AB, Patti ME. Glucagon-like peptide-1 (GLP-1) receptors are not overexpressed in pancreatic islets from patients with severe hyperinsulinaemic hypoglycaemia following gastric bypass. Diabetologia 2010; 53: 2641–2645.

    PubMed  CAS  Google Scholar 

  74. 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: 1582–1589.

    PubMed  CAS  Google Scholar 

  75. Anlauf M, Wieben D, Perren A, et al. Peristent hyperinsulinemic hypoglycemia in 15 adults with diffuse nesideoblastosis: Diagnostic criteria, incidence, and characterization of β-cell changes. Am J Surg Path 2005; 29: 524–529.

    PubMed  Google Scholar 

  76. Hong R, Choy DY, Lim SC. Hyperinsulinemic hypoglycemia due to diffuse nesideoblastosis in adults: A case report. World J Gastroenterol 2008; 14: 140–144.

    PubMed  Google Scholar 

  77. Kloppel G, Anlauf M, Raffel A, Perren A, Knoefel WT. Adult diffuse nesideoblastosis: Genetically or environmentally induced? Human Pathol 2008; 39: 3–8.

    Google Scholar 

  78. McElroy MK, Lowy A,Weidner M. Case report: Focal nesideoblastosis (“nesideoblastoma”) in an adult. Human Pathol 2010; 41: 447–451.

    Google Scholar 

  79. Raffel A, Krausch MM, Anlauf M, et al. Diffuse nesideoblastosis as a cause of hyperinsulinemic hypoglycemia in adults: A diagnostic and therapeutic challenge. Surgery 2007; 141: 179–183.

    PubMed  Google Scholar 

  80. Rumilla KM, Erickson LA, Service FJ, Vella A, Thompson GB, Grant CS, Lloyd RV. Hyperinsulinemic hypoglycemia with nesideoblastosis: Histologic features and growth factor expression. Mod Pathol 2009; 22: 239–245.

    PubMed  CAS  Google Scholar 

  81. Kaczirek K, Niederle B. Nesidioblastosis: an old term and a new understanding.World J Surg 2004; 28: 1227–1230.

    PubMed  Google Scholar 

  82. Thaler JP, Cummings DE. Minireview: hormonal and metabolic mechanisms of diabetes remission after gastrointestinal surgery. Endocrinology 2009; 150: 2518–2525.

    PubMed  CAS  Google Scholar 

  83. 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: 1554–1559.

    PubMed  Google Scholar 

  84. Meier JJ, Nauck MA, Butler PC. Comment to: Patti ME, McMahon G, Mun EC et al. (2005) Severe hypoglycaemia postgastric bypass requiring partial pancreatectomy: evidence for inappropriate insulin secretion and pancreatic islet hyperplasia. Diabetologia 2005; 48: 2236. Diabetologia 2006; 49: 607–608. author reply 609–610.

  85. Zagury L, Moreira RO, Guedes EP, Coutinho WF, Appolinario JC. Insulinoma misdiagnosed as dumping syndrome after bariatric surgery. Obes Surg 2004; 14: 120–123.

    PubMed  Google Scholar 

  86. Abellan P, Camara R, Merino-Torres JF, Perez-Lazaro A, del Olmo MI, Ponce JL, Rayon JM, Pinon F. Severe hypoglycemia after gastric bypass surgery for morbid obesity. Diabetes Res Clin Pract 2008; 79: e7-e9.

    PubMed  Google Scholar 

  87. Goldfine AB, Mun E, Patti ME. Hyperinsulinemic hypoglycemia following gastric bypass surgery for obesity. Curr Opin Endocrinol Diabetes 2006; 13: 419–424.

    Google Scholar 

  88. Z’Graggen K, Guweidhi A, Steffen R, Potoczna N, Biral R, Walther F, Komminoth P, Horber F. Severe recurrent hypoglycemia after gastric bypass surgery. Obes Surg 2008; 18: 981–988.

    PubMed  Google Scholar 

  89. Drucker DJ. Glucagon-like peptides: regulators of cell proliferation, differentiation, and apoptosis. Mol Endocrinol 2003; 17: 161–171.

    PubMed  CAS  Google Scholar 

  90. Hadjiyanni I, Baggio LL, Poussier P, Drucker DJ. Exendin-4 modulates diabetes onset in nonobese diabetic mice. Endocrinology 2008; 149: 1338–1349.

    PubMed  CAS  Google Scholar 

  91. Perfetti R, Zhou J, Doyle ME, Egan JM. Glucagon-like peptide-1 induces cell proliferation and pancreatic-duodenum homeobox-1 expression and increases endocrine cell mass in the pancreas of old, glucose-intolerant rats. Endocrinology 2000; 141: 4600–4605.

    PubMed  CAS  Google Scholar 

  92. Habener J, Stoffer D, Elahi D, et al. Role of homeodomain transcription factor IPF-1 in the pathogenesis of diabetes mellitus. In: Matschinsky FM (Ed). Frontiers in Diabetes Karger, Basel. 2000, pp 197–205

    Google Scholar 

  93. Duxbury MS, Waseem T, Ito H, Robinson MK, Zinner MJ, Ashley SW, Whang EE. Ghrelin promotes pancreatic adenocarcinoma cellular proliferation and invasiveness. Biochem Biophys Res Commun 2003; 309: 464–468.

    PubMed  CAS  Google Scholar 

  94. Nikolopoulos D, Theocharis S, Kouraklis G. Ghrelin’s role on gastrointestinal tract cancer. Surg Oncol 2010 Mar; 19(1): e2–e10. Epub 2009 Mar 28. PubMed PMID: 19328680

    PubMed  Google Scholar 

  95. Volante M, Allia E, Gugliotta P, Funaro A, Broglio F, Deghenghi R, Muccioli G, Chigo E, Papotti M. Expression of ghrelin and of the GH secretagogue receptor by pancreatic islet cells and related endocrine tumors. J Clin Endocrinol Metab 2002; 87: 1300–1308.

    PubMed  CAS  Google Scholar 

  96. Scavini M, Pontiroli AE, Folli F. Asymptomatic hyperinsulinemic hypoglycemia after gastric banding. N Engl J Med 2005; 353: 2822–2823.

    PubMed  CAS  Google Scholar 

  97. Catton JA, Zaitoun AM, Aithal GP, Sturrock ND, Lobo DN. Diffuse nesidioblastosis causing hyperinsulinemic hypoglycemia: the importance of pancreatic sampling on EUS. Gastrointest Endosc 2008; 68: 571–572. discussion 572

    PubMed  Google Scholar 

  98. Bendix F, Westphal S, Patschke R, Granowski D, Luley C, Lippert H, Wolff S. Weight loss and changes in salivary ghrelin and adiponectin: Comparison between sleeve gastrectomy and Roux-en-Y gastric bypass and gastric banding. Obes Surg 2011; doi:10-1007/sl1695-011-0374-5

  99. Beckman LM, Beckman TR, Sibley SD, Thomas W, Ikramuddin S, Kellogg TA, Ghatei MA, Bloom SR, le Roux CW, Earthman CP. Changes in gastrointestinal hormones and leptin after Roux-en-Y gastric bypass surgery. J Parenter Enteral Nutr 2011; 35: 169–180.

    CAS  Google Scholar 

  100. Bantle JP, Ikramuddin S, Kellogg TA, Buchwald H. Hyperinsulinemic hypoglycemia developing late after gastric bypass. Obes Surg 2007; 17: 592–594.

    PubMed  Google Scholar 

  101. Kellogg TA, Bantle JP, Leslie DB, Redmond JB, Slusarek B, Swan T, Buchwald H, Ikramuddin S. Postgastric bypass hyperinsulinemic hypoglycemia syndrome: Characterization and response to a modified diet. Surg Obes Relat Dis 2008; 4: 492–499.

    PubMed  Google Scholar 

  102. Hussain K, Aynsley-Green A, Stanley CA. Medications used in the treatment of hypoglycemia due to congenital hyperinsulinism of infancy (HI). Pediatr Endocrinol Rev 2004; 2(suppl 1): 163–167.

    PubMed  Google Scholar 

  103. Arao T, Okada Y, Hirose A, Tanaka Y. A rare case of adult-onset nesideoblastosis treated successfully with diazoxide. Endocr J 2006; 53: 95–100.

    PubMed  Google Scholar 

  104. Moreira RO, Moreira RB, Machado NA, Goncalves TB, Coutinho WF. Post-prandial hypoglycemia after bariatric surgery: pharmacological treatment with verapamil and acarbose. Obes Surg 2008; 18: 1618–1621.

    PubMed  Google Scholar 

  105. McLaughlin T, Peck M, Holst J, Deacon C. Reversible hyperinsulinemic hypoglycemia after gastric bypass: a consequence of altered nutrient delivery. J Clin Endocrinol Metab 2010; 95: 1851–1855.

    PubMed  CAS  Google Scholar 

  106. Kaczirek K, Niederle B. Nesideoblastosis: An old term and a new understanding. World J Surg 2004; 28: 1227–1230.

    PubMed  Google Scholar 

  107. Slezak LA, Andersen DK. Pancreatic resection: Effects on glucose metabolism. World J Surg 2001; 25: 452–460.

    PubMed  CAS  Google Scholar 

  108. Couet C, Genton P, Pointel JP, et al. The prevalence of retinopathy is similar in diabetes mellitus secondary to chronic pancreatitis with or without pancreatectomy and in idiopathic diabetes mellitus. Diabetes Care 1985; 8: 323–328.

    PubMed  CAS  Google Scholar 

  109. Dapri G, Cadière GB, Himpens J. Laproscopic reconversion of Roux-en-Y gastric bypass to original anatomy: Technique and preliminary outcomes. Obes Surg 2010: doi:10.1007/sl1695-010-0252-6

  110. Dapri G, Cadière GB, Himpens J. Laparoscopic conversion of Roux-en-Y gastric bypass to sleeve gastrectomy as first step of duodenal switch: Technique and preliminary outcomes. Obes Surg 2010; doi:10.1007/sl1695-010-0249-1

  111. Z’graggen K, Guweidhi A, Steffen R, Potoczna N, Biral R, Walther F, Komminoth P, Horber F. Severe recurrent hypoglycemia after gastric bypass surgery. Obes Surg 2008; 18: 981–988.

    PubMed  Google Scholar 

  112. Valderas JP, Irribarra V, Rubio L, Boza C, Escalona M, Liberona Y, Matamala A, Maiz A. Effects of sleeve gastrectomy and medical treatment for obesity on glucagon-like peptide-1 levels and glucose homeostasis in non-diabetic subjects. Obes Surg 2011; doi:10.1007/sl1695-011-0375-4

Download references

Conflict of Interest Statement

No conflicts of interest are declared.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dana K. Andersen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cui, Y., Elahi, D. & Andersen, D.K. Advances in the Etiology and Management of Hyperinsulinemic Hypoglycemia After Roux-en-Y Gastric Bypass. J Gastrointest Surg 15, 1879–1888 (2011). https://doi.org/10.1007/s11605-011-1585-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11605-011-1585-8

Keywords

Navigation