Postprandial hypoglycemia after upper gastrointestinal tract surgery: diagnosis and treatment (part 2)

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Abstract

The causes of postprandial hyperinsulinemic hypoglycemia (PHH) in patients who have under-gone an upper gastrointestinal tract surgery are still a matter of debate in the scientific community. Low postoperative body mass index, high postprandial beta-cell activity before the surgery, and younger age are all have been associated with higher PHH risk. It is hypothesized that the insulin-like growth factor-1 increases the tissue sensitivity to insulin and indirectly promotes the development of hypoglycemia. An increase in postprandial secretion of enteropancreatic hormones is still considered to be the main reason for PHH manifestation; however, a particular contribution has been ascribed to glycentin, which could be used as a marker of PHH risk in the future. At present, there are no clinical guidelines for the diagnosis of PHH. Undoubtedly, the first step in this direction should be the collection of the disease history. The provocative tests have been proposed for the detection of PHH. Today, the 72-hour fast test is still the gold standard in the diagnosis of hypoglycemia. However, most post-bariatric patients do not have fasting hypoglycemia, and insulinoma is extremely rare in this patient category. The use of a prolonged oral glucose tolerance test as the main method is associated with a risk of a false diagnosis, because about 12% of healthy individuals may have their glycemic levels at below 2.8 mmol/l. The mixed meal test has not been validated yet. The best results in the assessment of glucose variability have been obtained with “real time” continuous glucose monitoring the interstitial fluid for several days. The goal of PHH treatment is to reduce the stimulated insulin secretion. First of all, patients are advised to eat small meals consisting of carbohydrates with a low glycemic index in combination with proteins and lipids, with high fiber content. Should the nutritional modification be ineffective, it is possible to prescribe medical treatment, such as acarbose or somatostatin analogs. Diazoxide and slow calcium channel blockers can be used as the third line of therapy. A recent study has suggested that exogenous agonists of glucagon-like peptide-1 (GLP-1) receptors by stronger bonds with receptors, compared to those with endogenous GLP-1, could enhance glucagon response to hypoglycemia, thereby stabilizing glucose levels. In severe refractory PHH, reconstructive surgery and gastric banding are to be considered. If the expected decrease in insulin hypersecretion by reconstructive surgery is not achieved, partial or complete pancreatectomy remains the only possible approach to prevent hypoglycemia. However, due to the small number and short duration of the studies, effectiveness and safety of these techniques for PHH treatment have not yet been proven.

About the authors

M. Yu. Yukina

National Medical Research Center for Endocrinology

Author for correspondence.
Email: endo-yukina@yandex.ru
ORCID iD: 0000-0002-8771-8300

Marina Yu. Yukina – MD, PhD, Leading Research Fellow, Department of Therapeutic Endocrinology

11 Dm. Ul'yanovа ul., Moscow, 117036

Россия

M. O. Chernova

National Medical Research Center for Endocrinology

Email: fake@neicon.ru
ORCID iD: 0000-0002-7250-4588

Maria O. Chernova – Resident

11 Dm. Ul'yanovа ul., Moscow, 117036

Россия

E. A. Troshina

National Medical Research Center for Endocrinology

Email: fake@neicon.ru
ORCID iD: 0000-0002-8520-8702

Ekaterina A. Troshina – MD, PhD, Professor, Corresponding Member of the Russian Academy of Sciences, Director of the Institute of Clinical Endocrinology

11 Dm. Ul'yanovа ul., Moscow, 117036

Россия

V. V. Evdoshenko

Institute of Plastic Surgery and Cosmetology;
N.I. Pirogov Russian National Research Medical University

Email: fake@neicon.ru
ORCID iD: 0000-0002-1339-4868

Vladimir V. Evdoshenko – MD, PhD, Head of the Clinical Center for Surgery of Overweight and Metabolic Disorders Institute of Plastic Surgery and Cosmetology; Professor, Chair of Experimental and Clinical Surgery, Biomedical Faculty N.I. Pirogov Russian National Research Medical University

27 Ol'khovskaya ul., Moscow, 105066;

1 Ostrovityanova ul., Moscow, 117997

Россия

N. M. Platonova

National Medical Research Center for Endocrinology

Email: fake@neicon.ru
ORCID iD: 0000-0001-6388-1544

Nadezhda M. Platonova – MD, PhD, Head of Department of Therapeutic Endocrinology

11 Dm. Ul'yanovа ul., Moscow, 117036

Россия

References

  1. Юкина МЮ, Чернова МО, Трошина ЕА, Евдошенко ВВ, Платонова НМ. Постпрандиальные гипогликемии после оперативных вмешательств на верхних отделах желудочно-кишечного тракта: распространенность и патогенез (часть 1). Альманах клинической медицины. 2021;49. doi: 10.18786/2072-0505-2021-49-029.
  2. Lee CJ, Clark JM, Schweitzer M, Magnuson T, Steele K, Koerner O, Brown TT. Prevalence of and risk factors for hypoglycemic symptoms after gastric bypass and sleeve gastrectomy. Obesity (Silver Spring). 2015;23(5): 1079–1084. doi: 10.1002/oby.21042.
  3. Sarwar H, Chapman WH 3 rd , Pender JR, Ivanescu A, Drake AJ 3 rd , Pories WJ, Dar MS. Hypoglycemia after Roux-en-Y gastric bypass: the BOLD experience. Obes Surg. 2014;24(7): 1120–1124. doi: 10.1007/s11695-014-1260-8.
  4. Pigeyre M, Vaurs C, Raverdy V, Hanaire H, Ritz P, Pattou F. Increased risk of OGTT-induced hypoglycemia after gastric bypass in severely obese patients with normal glucose tolerance. Surg Obes Relat Dis. 2015;11(3): 573–577. doi: 10.1016/j.soard.2014.12.004.
  5. Nielsen JB, Pedersen AM, Gribsholt SB, Svensson E, Richelsen B. Prevalence, severity, and predictors of symptoms of dumping and hypoglycemia after Roux-en-Y gastric bypass. Surg Obes Relat Dis. 2016;12(8): 1562–1568. doi: 10.1016/j.soard.2016.04.017.
  6. Karakelides H, Irving BA, Short KR, O'Brien P, Nair KS. Age, obesity, and sex effects on insulin sensitivity and skeletal muscle mitochondrial function. Diabetes. 2010;59(1): 89–97. doi: 10.2337/db09-0591.
  7. Basu R, Breda E, Oberg AL, Powell CC, Dalla Man C, Basu A, Vittone JL, Klee GG, Arora P, Jensen MD, Toffolo G, Cobelli C, Rizza RA. Mechanisms of the age-associated deterioration in glucose tolerance: contribution of alterations in insulin secretion, action, and clearance. Diabetes. 2003;52(7): 1738–1748. doi: 10.2337/diabetes.52.7.1738.
  8. Seltzer HS, Allen EW, Herron AL Jr, Brennan MT. Insulin secretion in response to glycemic stimulus: relation of delayed initial release to carbohydrate intolerance in mild diabetes mellitus. J Clin Invest. 1967;46(3): 323–335. doi: 10.1172/JCI105534.
  9. Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22(9): 1462–1470. doi: 10.2337/diacare.22.9.1462.
  10. Meier JJ, Menge BA, Breuer TG, Müller CA, Tannapfel A, Uhl W, Schmidt WE, Schrader H. Functional assessment of pancreatic beta-cell area in humans. Diabetes. 2009;58(7): 1595–1603. doi: 10.2337/db08-1611.
  11. Raverdy V, Baud G, Pigeyre M, Verkindt H, Torres F, Preda C, Thuillier D, Gélé P, Vantyghem MC, Caiazzo R, Pattou F. Incidence and Predictive Factors of Postprandial Hyperinsulinemic Hypoglycemia After Roux-en-Y Gastric Bypass: A Five year Longitudinal Study. Ann Surg. 2016;264(5): 878–885. doi: 10.1097/SLA.0000000000001915.
  12. Itariu BK, Zeyda M, Prager G, Stulnig TM. Insulin-like growth factor 1 predicts post-load hypoglycemia following bariatric surgery: a prospective cohort study. PLoS One. 2014;9(4):e94613. doi: 10.1371/journal.pone.0094613.
  13. Salehi M, Gastaldelli A, D'Alessio DA. Blockade of glucagon-like peptide 1 receptor corrects postprandial hypoglycemia after gastric bypass. Gastroenterology. 2014;146(3): 669–680. e2. doi: 10.1053/j.gastro.2013.11.044.
  14. Holst JJ. Enteroendocrine secretion of gut hormones in diabetes, obesity and after bariatric surgery. Curr Opin Pharmacol. 2013;13(6): 983–988. doi: 10.1016/j.coph.2013.09.014.
  15. Romero F, Nicolau J, Flores L, Casamitjana R, Ibarzabal A, Lacy A, Vidal J. Comparable early changes in gastrointestinal hormones after sleeve gastrectomy and Roux-En-Y gastric bypass surgery for morbidly obese type 2 diabetic subjects. Surg Endosc. 2012;26(8): 2231–2239. doi: 10.1007/s00464-012-2166-y.
  16. Sandoval DA, D'Alessio DA. Physiology of proglucagon peptides: role of glucagon and GLP-1 in health and disease. Physiol Rev. 2015;95(2): 513–548. doi: 10.1152/physrev.00013.2014.
  17. Cavin JB, Couvelard A, Lebtahi R, Ducroc R, Arapis K, Voitellier E, Cluzeaud F, Gillard L, Hourseau M, Mikail N, Ribeiro-Parenti L, Kapel N, Marmuse JP, Bado A, Le Gall M. Differences in Alimentary Glucose Absorption and Intestinal Disposal of Blood Glucose After Roux-en-Y Gastric Bypass vs Sleeve Gastrectomy. Gastroenterology. 2016;150(2): 454–464.e9. doi: 10.1053/j.gastro.2015.10.009.
  18. Meyer-Gerspach AC, Wölnerhanssen B, Beglinger B, Nessenius F, Napitupulu M, Schulte FH, Steinert RE, Beglinger C. Gastric and intestinal satiation in obese and normal weight healthy people. Physiol Behav. 2014;129:265–271. doi: 10.1016/j.physbeh.2014.02.043.
  19. Raffort J, Lareyre F, Massalou D, Fénichel P, Panaïa-Ferrari P, Chinetti G. Insights on glicentin, a promising peptide of the proglucagon family. Biochem Med (Zagreb). 2017;27(2): 308–324. doi: 10.11613/BM.2017.034.
  20. Poitou C, Bouaziz-Amar E, Genser L, Oppert JM, Lacorte JM, Le Beyec J. Fasting levels of glicentin are higher in Roux-en-Y gastric bypass patients exhibiting postprandial hypoglycemia during a meal test. Surg Obes Relat Dis. 2018;14(7): 929–935. doi: 10.1016/j.soard.2018.03.014.
  21. Cryer PE, Axelrod L, Grossman AB, Heller SR, Montori VM, Seaquist ER, Service FJ; Endocrine Society. Evaluation and management of adult hypoglycemic disorders: an Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab. 2009;94(3): 709–728. doi: 10.1210/jc.2008-1410.
  22. Øhrstrøm CC, Worm D, Hansen DL. Postprandial hyperinsulinemic hypoglycemia after Roux-en-Y gastric bypass: an update. Surg Obes Relat Dis. 2017;13(2): 345–351. doi: 10.1016/j.soard.2016.09.025.
  23. Vella A, Service FJ. Incretin hypersecretion in post-gastric bypass hypoglycemia – primary problem or red herring? J Clin Endocrinol Metab. 2007;92(12): 4563–4565. doi: 10.1210/jc.2007-2260.
  24. Melmed S, Williams RH. Williams textbook of endocrinology. 12 th ed. Philadelphia: Elsevier/ Saunders; 2011. 1897 p.
  25. Abrahamsson N, Edén Engström B, Sundbom M, Karlsson FA. Hypoglycemia in everyday life after gastric bypass and duodenal switch. Eur J Endocrinol. 2015;173(1): 91–100. doi: 10.1530/EJE-14-0821.
  26. Ritz P, Hanaire H. Post-bypass hypoglycaemia: a review of current findings. Diabetes Metab. 2011;37(4): 274–281. doi: 10.1016/j.diabet.2011.04.003.
  27. Halperin F, Patti ME, Skow M, Bajwa M, Goldfine AB. Continuous glucose monitoring for evaluation of glycemic excursions after gastric bypass. J Obes. 2011;2011:869536. doi: 10.1155/2011/869536.
  28. Nielsen JB, Abild CB, Pedersen AM, Pedersen SB, Richelsen B. Continuous Glucose Monitoring After Gastric Bypass to Evaluate the Glucose Variability After a Low-Carbohydrate Diet and to Determine Hypoglycemia. Obes Surg. 2016;26(9): 2111–2118. doi: 10.1007/s11695-016-2058-7.
  29. Rodríguez Flores M, Cruz Soto RC, Vázquez Velázquez V, Soriano Cortés RR, Aguilar Salinas C, García García E. Continuous glucose monitoring in the management of patients after gastric bypass. Endocrinol Diabetes Metab Case Rep. 2019;2019(1): 1–6. doi: 10.1530/EDM-18-0155.
  30. Kefurt R, Langer FB, Schindler K, Shakeri-Leidenmühler S, Ludvik B, Prager G. Hypoglycemia after Roux-En-Y gastric bypass: detection rates of continuous glucose monitoring (CGM) versus mixed meal test. Surg Obes Relat Dis. 2015;11(3): 564–569. doi: 10.1016/j.soard.2014.11.003.
  31. Vaurs C, Brun JF, Bertrand M, Burcelin R, du Rieu MC, Anduze Y, Hanaire H, Ritz P. Post-prandial hypoglycemia results from a non-glucose-dependent inappropriate insulin secretion in Roux-en-Y gastric bypassed patients. Metabolism. 2016;65(3): 18–26. doi: 10.1016/j.metabol.2015.10.020.
  32. Mulla CM, Storino A, Yee EU, Lautz D, Sawnhey MS, Moser AJ, Patti ME. Insulinoma After Bariatric Surgery: Diagnostic Dilemma and Therapeutic Approaches. Obes Surg. 2016;26(4): 874–881. doi: 10.1007/s11695-016-2092-5.
  33. 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. 2015;21(3): 237–246. doi: 10.4158/EP14118.OR.
  34. 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(4): 492–499. doi: 10.1016/j.soard.2008.05.005.
  35. Botros N, Rijnaarts I, Brandts H, Bleumink G, Janssen I, de Boer H. Effect of carbohydrate restriction in patients with hyperinsulinemic hypoglycemia after Roux-en-Y gastric bypass. Obes Surg. 2014;24(11): 1850–1855. doi: 10.1007/s11695-014-1319-6.
  36. 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): 736–740. doi: 10.1089/dia.2011.0302.
  37. 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): 582–586. doi: 10.1007/s11695-011-0581-0.
  38. Nadelson J, Epstein A. A rare case of non-insulinoma pancreatogenous hypoglycemia syndrome. Case Rep Gastrointest Med. 2012;2012:164305. doi: 10.1155/2012/164305.
  39. Myint KS, Greenfield JR, Farooqi IS, Henning E, Holst JJ, Finer N. 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): 951–955. doi: 10.1530/EJE-11-1065.
  40. 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–e33. doi: 10.1016/j.soard.2013.11.006.
  41. Tack J, Arts J, Caenepeel P, De Wulf D, Bisschops R. Pathophysiology, diagnosis and management of postoperative dumping syndrome. Nat Rev Gastroenterol Hepatol. 2009;6(10): 583–590. doi: 10.1038/nrgastro.2009.148.
  42. Malik S, Mitchell JE, Steffen K, Engel S, Wiisanen R, Garcia L, Malik SA. Recognition and management of hyperinsulinemic hypoglycemia after bariatric surgery. Obes Res Clin Pract. 2016;10(1): 1–14. doi: 10.1016/j.orcp.2015.07.003.
  43. Halperin F, Patti ME, Goldfine AB. Glucagon treatment for post-gastric bypass hypoglycemia. Obesity (Silver Spring). 2010;18(9): 1858–1860. doi: 10.1038/oby.2010.15.
  44. Bantle AE, Wang Q, Bantle JP. Post-Gastric Bypass Hyperinsulinemic Hypoglycemia: Fructose is a Carbohydrate Which Can Be Safely Consumed. J Clin Endocrinol Metab. 2015;100(8): 3097–3102. doi: 10.1210/jc.2015-1283.
  45. Abrahamsson N, Engström 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): 885–889. doi: 10.1530/EJE-13-0504.
  46. Ceppa EP, Ceppa DP, Omotosho PA, Dickerson JA 2 nd , Park CW, Portenier DD. Algorithm to diagnose etiology of hypoglycemia after Roux-en-Y gastric bypass for morbid obesity: case series and review of the literature. Surg Obes Relat Dis. 2012;8(5): 641–647. doi: 10.1016/j.soard.2011.08.008.
  47. 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.
  48. Svane MS, Toft-Nielsen MB, Kristiansen VB, Hartmann B, Holst JJ, Madsbad S, Bojsen-Møller KN. 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;34(12): 1783–1787. doi: 10.1111/dme.13443.
  49. Davis DB, Khoraki J, Ziemelis M, Sirinvaravong S, Han JY, Campos GM. Roux en Y gastric bypass hypoglycemia resolves with gastric feeding or reversal: Confirming a non-pancreatic etiology. Mol Metab. 2018;9:15–27. doi: 10.1016/j.molmet.2017.12.011.
  50. Qvigstad E, Gulseth HL, Risstad H, le Roux CW, Berg TJ, Mala T, Kristinsson JA. A novel technique of Roux-en-Y gastric bypass reversal for postprandial hyperinsulinemic hypoglycaemia: A case report. Int J Surg Case Rep. 2016;21:91–94. doi: 10.1016/j.ijscr.2016.02.033.
  51. Tong J, Prigeon RL, Davis HW, Bidlingmaier M, Kahn SE, Cummings DE, Tschöp MH, D'Alessio D. Ghrelin suppresses glucose-stimulated insulin secretion and deteriorates glucose tolerance in healthy humans. Diabetes. 2010;59(9): 2145–2151. doi: 10.2337/db10-0504.
  52. Cavin JB, Bado A, Le Gall M. Intestinal Adaptations after Bariatric Surgery: Consequences on Glucose Homeostasis. Trends Endocrinol Metab. 2017;28(5): 354–364. doi: 10.1016/j.tem.2017.01.002.
  53. Майоров АЮ, Урбанова КА, Галстян ГР. Методы количественной оценки инсулино-резистентности. Ожирение и метаболизм. 2009;6(2): 19–23. doi: 10.14341/2071-8713-5313.
  54. Svane MS, Toft-Nielsen MB, Kristiansen VB, Hartmann B, Holst JJ, Madsbad S, Bojsen-Møller KN. 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;34(12): 1783–1787. doi: 10.1111/dme.13443.
  55. Davis DB, Khoraki J, Ziemelis M, Sirinvaravong S, Han JY, Campos GM. Roux en Y gastric bypass hypoglycemia resolves with gastric feeding or reversal: Confirming a non-pancreatic etiology. Mol Metab. 2018;9:15–27. doi: 10.1016/j.molmet.2017.12.011.
  56. Lee CJ, Brown T, Magnuson TH, Egan JM, Carlson O, Elahi D. Hormonal response to a mixedmeal challenge after reversal of gastric bypass for hypoglycemia. J Clin Endocrinol Metab. 2013;98(7):E1208–E1212. doi: 10.1210/jc.2013-1151.
  57. Vilsbøll T, Krarup T, Madsbad S, Holst JJ. Both GLP-1 and GIP are insulinotropic at basal and postprandial glucose levels and contribute nearly equally to the incretin effect of a meal in healthy subjects. Regul Pept. 2003;114(2–3): 115–121. doi: 10.1016/s0167-0115(03)00111-3.
  58. 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(4): 1851–1855. doi: 10.1210/jc.2009-1628.
  59. Service GJ, Thompson GB, Service FJ, Andrews JC, Collazo-Clavell ML, Lloyd RV. Hyperinsulinemic hypoglycemia with nesidio-blastosis after gastric-bypass surgery. N Engl J Med. 2005;353(3): 249–254. doi: 10.1056/NEJMoa043690.
  60. 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): 2236–2240. doi: 10.1007/s00125-005-1933-x.
  61. 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): 1554–1559. doi: 10.2337/dc06-0392.
  62. Sendino O, Fernández-Esparrach G, Solé M, Colomo L, Pellisé M, Llach J, Navarro S, Bordas JM, Ginès A. Endoscopic ultrasonography-guided brushing increases cellular diagnosis of pancreatic cysts: A prospective study. Dig Liver Dis. 2010;42(12): 877–881. doi: 10.1016/j.dld.2010.07.009.
  63. Mala T. Postprandial hyperinsulinemic hypoglycemia after gastric bypass surgical treatment. Surg Obes Relat Dis. 2014;10(6): 1220–1225. doi: 10.1016/j.soard.2014.01.010.
  64. Macedo AL, Hidal JT, Marcondes W, Mauro FC. Robotic Near-Total Pancreatectomy for Nesidioblastosis after Bariatric Surgery. Obes Surg. 2016;26(12): 3082–3083. doi: 10.1007/s11695-016-2318-6.
  65. Hu M, Zhao G, Luo Y, Liu R. Laparoscopic versus open treatment for benign pancreatic insulinomas: an analysis of 89 cases. Surg Endosc. 2011;25(12): 3831–3837. doi: 10.1007/s00464-011-1800-4.
  66. Daouadi M, Zureikat AH, Zenati MS, Choudry H, Tsung A, Bartlett DL, Hughes SJ, Lee KK, Moser AJ, Zeh HJ. Robot-assisted minimally invasive distal pancreatectomy is superior to the laparoscopic technique. Ann Surg. 2013;257(1): 128–132. doi: 10.1097/SLA.0b013e31825fff08.
  67. Antonakis PT, Ashrafian H, Martinez-Isla A. Pancreatic insulinomas: Laparoscopic management. World J Gastrointest Endosc. 2015;7(16): 1197–1207. doi: 10.4253/wjge.v7.i16.1197.
  68. Chen OT, Dojki FK, Weber SM, Hinshaw JL. Percutaneous Microwave Ablation of an Insulinoma in a Patient with Refractory Symptomatic Hypoglycemia. J Gastrointest Surg. 2015;19(7): 1378–1381. doi: 10.1007/s11605-015-2831-2.

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