Advertisement

Diabetes Secondary to Pancreatic Diseases

  • Teresa Mezza
  • Francesca Cinti
  • Andrea Giaccari
Reference work entry
Part of the Endocrinology book series (ENDOCR)

Abstract

Diabetes secondary to pancreatic diseases is a well-known form of diabetes mellitus, classified as “diseases of the exocrine pancreas – other specific type of diabetes,” or Type 3c diabetes mellitus (T3cDM) Exocrine pancreatic diseases underlying T3cDM include benign and malign conditions, of any etiology, that diffusely injure the pancreas. Due to the heterogeneity of its underlying causes, it is rarely considered in everyday clinical practice, but it could be more common than generally thought. An early diagnosis of a pancreatic disease may substantially change the patient’s prognosis. Finally, endocrinologists should become more acquainted with pancreatic diseases, while all other specialists should attribute the deserved importance to diabetes and hyperglycemia, even in the apparently mild forms. A schematic revision of causes, clinical diagnoses and management will be discussed in the chapter.

Keywords

Pancreatic diseases Diabetes secondary Personalized Medicine Type 3c Diabetes Mellitus 

References

  1. Abraham D, Rogers J, Gault P, Kushner JP, McClain DA. Increased insulin secretory capacity but decreased insulin sensitivity after correction of iron overload by phlebotomy in hereditary haemochromatosis. Diabetologia. 2006;49:2546–51.PubMedCrossRefGoogle Scholar
  2. Alberti KGMM. Diabetes secondary to pancreatopathy: an example of brittle diabetes. In: Tiengo AAK, Del Prato S, Vranic M, editors. Diabetes secondary to pancreatopathy. Proceedings of the post EASD international symposium on diabetes secondary to pancreatopathy, Padova, 21–22 September 1987. International congress series 762. Amsterdam: Excerpta Medica; 1988. p. 211–4.Google Scholar
  3. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2011;34(Suppl 1):S62–9.PubMedCentralCrossRefPubMedGoogle Scholar
  4. Anderson MF, Davison SH, Dick AP, Hales CN, Owens J. Plasma insulin in pancreatic disease. Gut. 1970;11:524–31.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Angelopoulos N, Dervenis C, Goula A, Rombopoulos G, Livadas S, Kaltsas D, Kaltzidou V, Tolis G. Endocrine pancreatic insufficiency in chronic pancreatitis. Pancreatology. 2005;5:122–31.PubMedCrossRefGoogle Scholar
  6. Apte MV, Park S, Phillips PA, Santucci N, Goldstein D, Kumar RK, Ramm GA, Buchler M, Friess H, McCarroll JA, Keogh G, Merrett N, Pirola R, Wilson JS. Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas. 2004;29:179–87.PubMedCrossRefGoogle Scholar
  7. Bank S, Marks IN, Vinik AI. Clinical and hormonal aspects of pancreatic diabetes. Am J Gastroenterol. 1975;64:13–22.PubMedGoogle Scholar
  8. Bartosch-Harlid A, Andersson R. Diabetes mellitus in pancreatic cancer and the need for diagnosis of asymptomatic disease. Pancreatology. 2010;10:423–8.PubMedCrossRefGoogle Scholar
  9. Basso D, Greco E, Fogar P, Pucci P, Flagiello A, Baldo G, Giunco S, Valerio A, Navaglia F, Zambon CF, Pedrazzoli S, Plebani M. Pancreatic cancer-associated diabetes mellitus: an open field for proteomic applications. Clin Chim Acta. 2005;357:184–9.PubMedCrossRefGoogle Scholar
  10. Basso D, Greco E, Fogar P, Pucci P, Flagiello A, Baldo G, Giunco S, Valerio A, Navaglia F, Zambon CF, Falda A, Pedrazzoli S, Plebani M. Pancreatic cancer-derived S-100A8 N-terminal peptide: a diabetes cause? Clin Chim Acta. 2006;372:120–8.PubMedCrossRefGoogle Scholar
  11. Beglinger S, Drewe J, Schirra J, Goke B, D’Amato M, Beglinger C. Role of fat hydrolysis in regulating glucagon-like peptide-1 secretion. J Clin Endocrinol Metab. 2010;95:879–86.PubMedCrossRefGoogle Scholar
  12. Ben Q, Xu M, Ning X, Liu J, Hong S, Huang W, Zhang H, Li Z. Diabetes mellitus and risk of pancreatic cancer: a meta-analysis of cohort studies. Eur J Cancer. 2011;47:1928–37.PubMedCrossRefGoogle Scholar
  13. Bhanot UK, Moller P. Mechanisms of parenchymal injury and signaling pathways in ectatic ducts of chronic pancreatitis: implications for pancreatic carcinogenesis. Lab Invest. 2009;89:489–97.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bonner-Weir S, Trent DF, Weir GC. Partial pancreatectomy in the rat and subsequent defect in glucose-induced insulin release. J Clin Invest. 1983;71:1544–53.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Borgna-Pignatti C, Rugolotto S, De Stefano P, Zhao H, Cappellini MD, Del Vecchio GC, Romeo MA, Forni GL, Gamberini MR, Ghilardi R, Piga A, Cnaan A. Survival and complications in patients with thalassemia major treated with transfusion and deferoxamine. Haematologica. 2004;89:1187–93.PubMedGoogle Scholar
  16. Boucher BJ. Vitamin D insufficiency and diabetes risks. Curr Drug Targets. 2011;12:61–87.PubMedCrossRefPubMedCentralGoogle Scholar
  17. Buysschaert M, Paris I, Selvais P, Hermans MP. Clinical aspects of diabetes secondary to idiopathic haemochromatosis in French-speaking Belgium. Diabetes Metab. 1997;23:308–13.PubMedGoogle Scholar
  18. Chari ST, Leibson CL, Rabe KG, Timmons LJ, Ransom J, de Andrade M, Petersen GM. Pancreatic cancer-associated diabetes mellitus: prevalence and temporal association with diagnosis of cancer. Gastroenterology. 2008;134:95–101.PubMedCrossRefGoogle Scholar
  19. Cooke A, Phillips JM, Parish NM. Tolerogenic strategies to halt or prevent type 1 diabetes. Nat Immunol. 2001;2:810–5.PubMedCrossRefGoogle Scholar
  20. Cooksey RC, Jouihan HA, Ajioka RS, Hazel MW, Jones DL, Kushner JP, McClain DA. Oxidative stress, beta-cell apoptosis, and decreased insulin secretory capacity in mouse models of hemochromatosis. Endocrinology. 2004;145:5305–12.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Cui Y, Andersen DK. Pancreatogenic diabetes: special considerations for management. Pancreatology. 2011;11:279–94.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Dalgard C, Petersen MS, Weihe P, Grandjean P. Vitamin D status in relation to glucose metabolism and type 2 diabetes in septuagenarians. Diabetes Care. 2011;34:1284–8.PubMedPubMedCentralCrossRefGoogle Scholar
  23. Deckert T, Kolendorf K, Persson I, Worning H. Insulin secretion after tolbutamide and after secretin in patients with pancreatic diseases. Acta Med Scand. 1972;192:465–70.PubMedCrossRefPubMedCentralGoogle Scholar
  24. Dmochowski K, Finegood DT, Francombe W, Tyler B, Zinman B. Factors determining glucose tolerance in patients with thalassemia major. J Clin Endocrinol Metab. 1993;77:478–83.PubMedGoogle Scholar
  25. Donowitz M, Hendler R, Spiro HM, Binder HJ, Felig P. Glucagon secretion in acute and chronic pancreatitis. Ann Intern Med. 1975;83:778–81.PubMedCrossRefGoogle Scholar
  26. Ebert R, Creutzfeldt W. Reversal of impaired GIP and insulin secretion in patients with pancreatogenic steatorrhea following enzyme substitution. Diabetologia. 1980;19:198–204.PubMedCrossRefPubMedCentralGoogle Scholar
  27. Everhart J, Wright D. Diabetes mellitus as a risk factor for pancreatic cancer. A meta-analysis. JAMA. 1995;273:1605–9.PubMedCrossRefPubMedCentralGoogle Scholar
  28. Ewald N, Bretzel RG. Diabetes mellitus secondary to pancreatic diseases (type 3c) – are we neglecting an important disease? Eur J Intern Med. 2013;24:203–6.PubMedCrossRefPubMedCentralGoogle Scholar
  29. Ewald N, Kaufmann C, Raspe A, Kloer HU, Bretzel RG, Hardt PD. Prevalence of diabetes mellitus secondary to pancreatic diseases (type 3c). Diabetes Metab Res Rev. 2012;28:338–42.PubMedCrossRefPubMedCentralGoogle Scholar
  30. Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 2003;26(Suppl 1):S5–20.Google Scholar
  31. Farrow B, Evers BM. Inflammation and the development of pancreatic cancer. Surg Oncol. 2002;10:153–69.PubMedCrossRefPubMedCentralGoogle Scholar
  32. Ford ES, Zhao G, Tsai J, Li C. Associations between concentrations of vitamin D and concentrations of insulin, glucose, and HbA1c among adolescents in the United States. Diabetes Care. 2011;34:646–8.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Fox JN, Frier BM, Armitage M, Ashby JP. Abnormal insulin secretion in carcinoma of the pancreas: response to glucagon stimulation. Diabet Med. 1985;2:113–6.PubMedCrossRefGoogle Scholar
  34. Frye JN, Inder WJ, Dobbs BR, Frizelle FA. Pancreatic cancer and diabetes: is there a relationship? A case-controlled study. Aust N Z J Surg. 2000;70:722–4.PubMedCrossRefGoogle Scholar
  35. Ganda O. Secondary forms of diabetes. In: Kahn CR, Weir GC, editors. Joslin’s diabetes mellitus. New York: Lea & Febiger; 1994.Google Scholar
  36. Gaskin KJ, Durie PR, Corey M, Wei P, Forstner GG. Evidence for a primary defect of pancreatic HCO3-secretion in cystic fibrosis. Pediatr Res. 1982;16:554–7.PubMedCrossRefGoogle Scholar
  37. Guerra C, Schuhmacher AJ, Canamero M, Grippo PJ, Verdaguer L, Perez-Gallego L, Dubus P, Sandgren EP, Barbacid M. Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell. 2007;11:291–302.PubMedCrossRefGoogle Scholar
  38. Gullo L. Diabetes and the risk of pancreatic cancer. Ann Oncol. 1999;10(Suppl 4):79–81.PubMedCrossRefPubMedCentralGoogle Scholar
  39. Gullo L, Pezzilli R, Morselli-Labate AM, Italian Pancreatic Cancer Study Group. Diabetes and the risk of pancreatic cancer. N Engl J Med. 1994;331:81–4.PubMedCrossRefGoogle Scholar
  40. Hardt PD, Krauss A, Bretz L, Porsch-Ozcurumez M, Schnell-Kretschmer H, Maser E, Bretzel RG, Zekhorn T, Klor HU. Pancreatic exocrine function in patients with type 1 and type 2 diabetes mellitus. Acta Diabetol. 2000;37:105–10.PubMedCrossRefPubMedCentralGoogle Scholar
  41. Hardt PD, Brendel MD, Kloer HU, Bretzel RG. Is pancreatic diabetes (type 3c diabetes) underdiagnosed and misdiagnosed? Diabetes Care. 2008;31(Suppl 2):S165–9.PubMedCrossRefPubMedCentralGoogle Scholar
  42. Hatunic M, Finucane FM, Brennan AM, Norris S, Pacini G, Nolan JJ. Effect of iron overload on glucose metabolism in patients with hereditary hemochromatosis. Metabolism. 2010a;59:380–4.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Hatunic M, Finucane FM, Norris S, Pacini G, Nolan JJ. Glucose metabolism after normalization of markers of iron overload by venesection in subjects with hereditary hemochromatosis. Metabolism. 2010b;59:1811–5.PubMedCrossRefPubMedCentralGoogle Scholar
  44. Hjalgrim H, Frisch M, Ekbom A, Kyvik KO, Melbye M, Green A. Cancer and diabetes – a follow-up study of two population-based cohorts of diabetic patients. J Intern Med. 1997;241:471–5.PubMedCrossRefPubMedCentralGoogle Scholar
  45. Hramiak IM, Finegood DT, Adams PC. Factors affecting glucose tolerance in hereditary hemochromatosis. Clin Invest Med. 1997;20:110–8.PubMedPubMedCentralGoogle Scholar
  46. Hutchins RR, Hart RS, Pacifico M, Bradley NJ, Williamson RC. Long-term results of distal pancreatectomy for chronic pancreatitis in 90 patients. Ann Surg. 2002;236:612–8.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Huxley R, Ansary-Moghaddam A, Berrington de Gonzalez A, Barzi F, Woodward M. Type-II diabetes and pancreatic cancer: a meta-analysis of 36 studies. Br J Cancer. 2005;92:2076–83.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Ibars EP, Sanchez de Rojas EA, Quereda LA, Ramis RF, Sanjuan VM, Peris RT. Pancreatic function after acute biliary pancreatitis: does it change? World J Surg. 2002;26:479–86.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Isaksson B, Strommer L, Friess H, Buchler MW, Herrington MK, Wang F, Zierath JR, Wallberg-Henriksson H, Larsson J, Permert J. Impaired insulin action on phosphatidylinositol 3-kinase activity and glucose transport in skeletal muscle of pancreatic cancer patients. Pancreas. 2003;26:173–7.PubMedCrossRefPubMedCentralGoogle Scholar
  50. Jaster R. Molecular regulation of pancreatic stellate cell function. Mol Cancer. 2004;3:26.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Joffe BI, Bank S, Jackson WP, Keller P, O’Reilly IG, Vinik AI. Insulin reserve in patients with chronic pancreatitis. Lancet. 1968;2:890–2.PubMedCrossRefPubMedCentralGoogle Scholar
  52. Jouihan HA, Cobine PA, Cooksey RC, Hoagland EA, Boudina S, Abel ED, Winge DR, McClain DA. Iron-mediated inhibition of mitochondrial manganese uptake mediates mitochondrial dysfunction in a mouse model of hemochromatosis. Mol Med. 2008;14:98–108.PubMedCrossRefGoogle Scholar
  53. Kalk WJ, Vinik AI, Bank S, Keller P, Jackson WP. Selective loss of beta cell response to glucose in chronic pancreatitis. Horm Metab Res. 1974;6:95–8.PubMedCrossRefGoogle Scholar
  54. Kannan V, Nabarro JD, Cotton PB. Glucagon secretion in chronic pancreatitis. Horm Res. 1979;11:203–12.PubMedCrossRefGoogle Scholar
  55. Katsumichi I, Pour PM. Diabetes mellitus in pancreatic cancer: is it a causal relationship? Am J Surg. 2007;194:S71–5.PubMedCrossRefGoogle Scholar
  56. Kendall DM, Sutherland DE, Najarian JS, Goetz FC, Robertson RP. Effects of hemipancreatectomy on insulin secretion and glucose tolerance in healthy humans. N Engl J Med. 1990;322:898–903.PubMedCrossRefGoogle Scholar
  57. King J, Kazanjian K, Matsumoto J, Reber HA, Yeh MW, Hines OJ, Eibl G. Distal pancreatectomy: incidence of postoperative diabetes. J Gastrointest Surg. 2008;12:1548–53.PubMedCrossRefGoogle Scholar
  58. Koch C, Cuppens H, Rainisio M, Madessani U, Harms H, Hodson M, Mastella G, Navarro J, Strandvik B, McKenzie S, Investigators of the ERCF. European Epidemiologic Registry of Cystic Fibrosis (ERCF): comparison of major disease manifestations between patients with different classes of mutations. Pediatr Pulmonol. 2001;31:1–12.PubMedCrossRefPubMedCentralGoogle Scholar
  59. Koizumi M, Yoshida Y, Abe N, Shimosegawa T, Toyota T. Pancreatic diabetes in Japan. Pancreas. 1998;16:385–91.PubMedCrossRefPubMedCentralGoogle Scholar
  60. Kopelman H, Corey M, Gaskin K, Durie P, Weizman Z, Forstner G. Impaired chloride secretion, as well as bicarbonate secretion, underlies the fluid secretory defect in the cystic fibrosis pancreas. Gastroenterology. 1988;95:349–55.PubMedCrossRefPubMedCentralGoogle Scholar
  61. Kuo P, Stevens JE, Russo A, Maddox A, Wishart JM, Jones KL, Greville H, Hetzel D, Chapman I, Horowitz M, Rayner CK. Gastric emptying, incretin hormone secretion, and postprandial glycemia in cystic fibrosis – effects of pancreatic enzyme supplementation. J Clin Endocrinol Metab. 2011;96:E851–5.PubMedCrossRefPubMedCentralGoogle Scholar
  62. Larsen S, Hilsted J, Tronier B, Worning H. Metabolic control and B cell function in patients with insulin-dependent diabetes mellitus secondary to chronic pancreatitis. Metabolism. 1987;36:964–7.PubMedCrossRefPubMedCentralGoogle Scholar
  63. Larsen S, Hilsted J, Tronier B, Worning H. Pancreatic hormone secretion in chronic pancreatitis without residual beta-cell function. Acta Endocrinol. 1988;118:357–64.PubMedCrossRefPubMedCentralGoogle Scholar
  64. Leahy JL, Bumbalo LM, Chen C. Diazoxide causes recovery of beta-cell glucose responsiveness in 90% pancreatectomized diabetic rats. Diabetes. 1994;43:173–9.PubMedCrossRefPubMedCentralGoogle Scholar
  65. Li D. Diabetes and pancreatic cancer. Mol Carcinog. 2012;51:64–74.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Linde J, Nilsson LH, Barany FR. Diabetes and hypoglycemia in chronic pancreatitis. Scand J Gastroenterol. 1977;12:369–73.PubMedCrossRefPubMedCentralGoogle Scholar
  67. Liu J, Kazakoff K, Pour PM, Adrian TE. The intracellular mechanism of insulin resistance in the hamster pancreatic ductal adenocarcinoma model. Pancreas. 1998;17:359–66.PubMedCrossRefPubMedCentralGoogle Scholar
  68. Liu YQ, Nevin PW, Leahy JL. Beta-cell adaptation in 60% pancreatectomy rats that preserves normoinsulinemia and normoglycemia. Am J Physiol Endocrinol Metab. 2000;279:E68–73.PubMedCrossRefGoogle Scholar
  69. Massucco P, Calgaro M, Bertolino F, Bima C, Galatola G, Capussotti L. Outcome of surgical treatment for chronic calcifying pancreatitis. Pancreas. 2001;22:378–82.PubMedCrossRefGoogle Scholar
  70. Matveyenko AV, Veldhuis JD, Butler PC. Mechanisms of impaired fasting glucose and glucose intolerance induced by an approximate 50% pancreatectomy. Diabetes. 2006;55:2347–56.PubMedCrossRefGoogle Scholar
  71. McClain DA, Abraham D, Rogers J, Brady R, Gault P, Ajioka R, Kushner JP. High prevalence of abnormal glucose homeostasis secondary to decreased insulin secretion in individuals with hereditary haemochromatosis. Diabetologia. 2006;49:1661–9.PubMedCrossRefGoogle Scholar
  72. McCulloch DK, Koerker DJ, Kahn SE, Bonner-Weir S, Palmer JP. Correlations of in vivo beta-cell function tests with beta-cell mass and pancreatic insulin content in streptozocin-administered baboons. Diabetes. 1991;40:673–9.PubMedCrossRefGoogle Scholar
  73. Mendler MH, Turlin B, Moirand R, Jouanolle AM, Sapey T, Guyader D, Le Gall JY, Brissot P, David V, Deugnier Y. Insulin resistance-associated hepatic iron overload. Gastroenterology. 1999;117:1155–63.PubMedCrossRefGoogle Scholar
  74. Merkel PA, Simonson DC, Amiel SA, Plewe G, Sherwin RS, Pearson HA, Tamborlane WV. Insulin resistance and hyperinsulinemia in patients with thalassemia major treated by hypertransfusion. N Engl J Med. 1988;318:809–14.PubMedCrossRefGoogle Scholar
  75. Messina MF, Lombardo F, Meo A, Miceli M, Wasniewska M, Valenzise M, Ruggeri C, Arrigo T, De Luca F. Three-year prospective evaluation of glucose tolerance, beta-cell function and peripheral insulin sensitivity in non-diabetic patients with thalassemia major. J Endocrinol Invest. 2002;25:497–501.PubMedCrossRefGoogle Scholar
  76. Mezza T, Clemente G, Sorice GP, Conte C, De Rose AM, Sun VA, Cefalo CM, Pontecorvi A, Nuzzo G, Giaccari A. Metabolic consequences of the occlusion of the main pancreatic duct with acrylic glue after pancreaticoduodenectomy. Am J Surg. 2015;210:783–9.PubMedCrossRefGoogle Scholar
  77. Mohan K, Israel KL, Miller H, Grainger R, Ledson MJ, Walshaw MJ. Long-term effect of insulin treatment in cystic fibrosis-related diabetes. Respiration. 2008;76:181–6.PubMedCrossRefGoogle Scholar
  78. Moirand R, Adams PC, Bicheler V, Brissot P, Deugnier Y. Clinical features of genetic hemochromatosis in women compared with men. Ann Intern Med. 1997;127:105–10.PubMedCrossRefPubMedCentralGoogle Scholar
  79. Moran A, Hardin D, Rodman D, Allen HF, Beall RJ, Borowitz D, Brunzell C, Campbell PW 3rd, Chesrown SE, Duchow C, Fink RJ, Fitzsimmons SC, Hamilton N, Hirsch I, Howenstine MS, Klein DJ, Madhun Z, Pencharz PB, Quittner AL, Robbins MK, Schindler T, Schissel K, Schwarzenberg SJ, Stallings VA, Zipf WB, et al. Diagnosis, screening and management of cystic fibrosis related diabetes mellitus: a consensus conference report. Diabetes Res Clin Pract. 1999;45:61–73.PubMedCrossRefGoogle Scholar
  80. Moriai T, Morita Y, Matsui T, Okada M. Type 1 diabetes mellitus associated with clinical acute pancreatitis in an adult. Pancreas. 2000;20:415–6.PubMedCrossRefGoogle Scholar
  81. Nakamori S, Ishikawa O, Ohigashi H, Sasakuma F, Shimizu T, Nakaizumi A, Furukawa H, Sasaki Y, Imaoka S. Increased blood proinsulin and decreased C-peptide levels in patients with pancreatic cancer. Hepatogastroenterology. 1999;46:16–24.PubMedGoogle Scholar
  82. Nathan DM, Buse JB, Davidson MB, Ferrannini E, Holman RR, Sherwin R, Zinman B, American Diabetes Association, European Association for Study of Diabetes. Medical management of hyperglycemia in type 2 diabetes: a consensus algorithm for the initiation and adjustment of therapy: a consensus statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care. 2009;32:193–203.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Noel RA, Braun DK, Patterson RE, Bloomgren GL. Increased risk of acute pancreatitis and biliary disease observed in patients with type 2 diabetes: a retrospective cohort study. Diabetes Care. 2009;32:834–8.PubMedPubMedCentralCrossRefGoogle Scholar
  84. Nosadini R, del Prato S, Tiengo A, Duner E, Toffolo G, Cobelli C, Faronato PP, Moghetti P, Muggeo M. Insulin sensitivity, binding, and kinetics in pancreatogenic and type I diabetes. Diabetes. 1982;31:346–55.PubMedCrossRefGoogle Scholar
  85. Nyboe Andersen B, Krarup T, Thorsgaard Pedersen NT, Faber OK, Hagen C, Worning H. B cell function in patients with chronic pancreatitis and its relation to exocrine pancreatic function. Diabetologia. 1982;23:86–9.PubMedCrossRefGoogle Scholar
  86. Ogunleye AA, Ogston SA, Morris AD, Evans JM. A cohort study of the risk of cancer associated with type 2 diabetes. Br J Cancer. 2009;101:1199–201.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Ohneda A, Kai Y, Ishii S, Matsuda K, Horigome K. Insulin and glucagon response in patients with chronic pancreatitis. Tohoku J Exp Med. 1976;120:287–98.PubMedCrossRefGoogle Scholar
  88. Omary MB, Lugea A, Lowe AW, Pandol SJ. The pancreatic stellate cell: a star on the rise in pancreatic diseases. J Clin Invest. 2007;117:50–9.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Paye F. The pancreatic stump after pancreatoduodenectomy: the “Achille’s heel” revisited. J Visc Surg. 2010;147:e13–20.PubMedCrossRefGoogle Scholar
  90. Permert J, Ihse I, Jorfeldt L, von Schenck H, Arnqvist HJ, Larsson J. Pancreatic cancer is associated with impaired glucose metabolism. Eur J Surg. 1993a;159:101–7.PubMedPubMedCentralGoogle Scholar
  91. Permert J, Adrian TE, Jacobsson P, Jorfelt L, Fruin AB, Larsson J. Is profound peripheral insulin resistance in patients with pancreatic cancer caused by a tumor-associated factor? Am J Surg. 1993b;165:61–6; discussion 66–7PubMedCrossRefPubMedCentralGoogle Scholar
  92. Permert J, Larsson J, Westermark GT, Herrington MK, Christmanson L, Pour PM, Westermark P, Adrian TE. Islet amyloid polypeptide in patients with pancreatic cancer and diabetes. N Engl J Med. 1994;330:313–8.PubMedCrossRefPubMedCentralGoogle Scholar
  93. Permert J, Larsson J, Fruin AB, Tatemoto K, Herrington MK, von Schenck H, Adrian TE. Islet hormone secretion in pancreatic cancer patients with diabetes. Pancreas. 1997;15:60–8.PubMedCrossRefPubMedCentralGoogle Scholar
  94. Phillips JM, O’Reilly L, Bland C, Foulis AK, Cooke A. Patients with chronic pancreatitis have islet progenitor cells in their ducts, but reversal of overt diabetes in NOD mice by anti-CD3 shows no evidence for islet regeneration. Diabetes. 2007;56:634–40.PubMedCrossRefPubMedCentralGoogle Scholar
  95. Pietrangelo A. Hereditary hemochromatosis: pathogenesis, diagnosis, and treatment. Gastroenterology. 2010;139:393–408, 408.e391–2PubMedCrossRefPubMedCentralGoogle Scholar
  96. Pour PM, Permert J, Mogaki M, Fujii H, Kazakoff K. Endocrine aspects of exocrine cancer of the pancreas. Their patterns and suggested biologic significance. Am J Clin Pathol. 1993;100:223–30.PubMedCrossRefPubMedCentralGoogle Scholar
  97. Rickels MR, Bellin M, Toledo FG, Robertson RP, Andersen DK, Chari ST, Brand R, Frulloni L, Anderson MA, Whitcomb DC, PancreasFest Recommendation Conference Participants. Detection, evaluation and treatment of diabetes mellitus in chronic pancreatitis: recommendations from PancreasFest 2012. Pancreatology. 2013;13:336–42.PubMedCrossRefPubMedCentralGoogle Scholar
  98. Sadeghi N, Abbruzzese JL, Yeung SC, Hassan M, Li D. Metformin use is associated with better survival of diabetic patients with pancreatic cancer. Clin Cancer Res. 2012;18:2905–12.PubMedPubMedCentralCrossRefGoogle Scholar
  99. Saruc M, Pour PM. Diabetes and its relationship to pancreatic carcinoma. Pancreas. 2003;26:381–7.PubMedCrossRefGoogle Scholar
  100. Schneider MU, Knoll-Ruzicka ML, Domschke S, Heptner G, Domschke W. Pancreatic enzyme replacement therapy: comparative effects of conventional and enteric-coated microspheric pancreatin and acid-stable fungal enzyme preparations on steatorrhoea in chronic pancreatitis. Hepatogastroenterology. 1985;32:97–102.PubMedPubMedCentralGoogle Scholar
  101. Schneider L, Hartwig W, Flemming T, Hackert T, Fortunato F, Heck M, Gebhard MM, Nawroth PP, Bierhaus A, Buchler MW, Werner J. Protective effects and anti-inflammatory pathways of exogenous calcitonin gene-related peptide in severe necrotizing pancreatitis. Pancreatology. 2009;9:662–9.PubMedCrossRefPubMedCentralGoogle Scholar
  102. Schwarts SS, Zeidler A, Moossa AR, Kuku SF, Rubenstein AH. A prospective study of glucose tolerance, insulin, C-peptide, and glucagon responses in patients with pancreatic carcinoma. Am J Dig Dis. 1978;23:1107–14.PubMedCrossRefPubMedCentralGoogle Scholar
  103. Sikkens EC, Cahen DL, Koch AD, Braat H, Poley JW, Kuipers EJ, Bruno MJ. The prevalence of fat-soluble vitamin deficiencies and a decreased bone mass in patients with chronic pancreatitis. Pancreatology. 2013;13:238–42.PubMedCrossRefPubMedCentralGoogle Scholar
  104. Simcox JA, McClain DA. Iron and diabetes risk. Cell Metab. 2013;17:329–41.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Slezak LA, Andersen DK. Pancreatic resection: effects on glucose metabolism. World J Surg. 2001;25:452–60.PubMedCrossRefPubMedCentralGoogle Scholar
  106. Sparmann G, Hohenadl C, Tornoe J, Jaster R, Fitzner B, Koczan D, Thiesen HJ, Glass A, Winder D, Liebe S, Emmrich J. Generation and characterization of immortalized rat pancreatic stellate cells. Am J Physiol Gastrointest Liver Physiol. 2004;287:G211–9.PubMedCrossRefPubMedCentralGoogle Scholar
  107. Suc B, Msika S, Fingerhut A, Fourtanier G, Hay JM, Holmieres F, Sastre B, Fagniez PL, French Associations for Surgical Research. Temporary fibrin glue occlusion of the main pancreatic duct in the prevention of intra-abdominal complications after pancreatic resection: prospective randomized trial. Ann Surg. 2003;237:57–65.PubMedPubMedCentralCrossRefGoogle Scholar
  108. van den Berg JM, Morton AM, Kok SW, Pijl H, Conway SP, Heijerman HG. Microvascular complications in patients with cystic fibrosis-related diabetes (CFRD). J Cyst Fibros. 2008;7:515–9.PubMedCrossRefPubMedCentralGoogle Scholar
  109. Vogiatzi MG, Macklin EA, Trachtenberg FL, Fung EB, Cheung AM, Vichinsky E, Olivieri N, Kirby M, Kwiatkowski JL, Cunningham M, Holm IA, Fleisher M, Grady RW, Peterson CM, Giardina PJ, Thalassemia Clinical Research Network. Differences in the prevalence of growth, endocrine and vitamin D abnormalities among the various thalassaemia syndromes in North America. Br J Haematol. 2009;146:546–56.PubMedPubMedCentralCrossRefGoogle Scholar
  110. Wang F, Larsson J, Abdiu A, Gasslander T, Westermark P, Adrian TE, Permert J. Dissociated secretion of islet amyloid polypeptide and insulin in serum-free culture media conditioned by human pancreatic adenocarcinoma cell lines. Int J Pancreatol. 1997;21:157–64.PubMedGoogle Scholar
  111. Wang F, Adrian TE, Westermark G, Gasslander T, Permert J. Dissociated insulin and islet amyloid polypeptide secretion from isolated rat pancreatic islets cocultured with human pancreatic adenocarcinoma cells. Pancreas. 1999;18:403–9.PubMedCrossRefGoogle Scholar
  112. Wang F, Herrington M, Larsson J, Permert J. The relationship between diabetes and pancreatic cancer. Mol Cancer. 2003;2:4.PubMedPubMedCentralCrossRefGoogle Scholar
  113. Wang X, Misawa R, Zielinski MC, Cowen P, Jo J, Periwal V, Ricordi C, Khan A, Szust J, Shen J, Millis JM, Witkowski P, Hara M. Regional differences in islet distribution in the human pancreas – preferential beta-cell loss in the head region in patients with type 2 diabetes. PLoS One. 2013;8:e67454.PubMedPubMedCentralCrossRefGoogle Scholar
  114. Weatherall DJ. Pathophysiology of thalassaemia. Baillieres Clin Haematol. 1998;11:127–46.PubMedCrossRefGoogle Scholar
  115. Yki-Jarvinen H, Kiviluoto T, Taskinen MR. Insulin resistance is a prominent feature of patients with pancreatogenic diabetes. Metabolism. 1986;35:718–27.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Teresa Mezza
    • 1
  • Francesca Cinti
    • 1
  • Andrea Giaccari
    • 1
  1. 1.Center for Endocrine and Metabolic DiseasesFondazione Policlinico Universitario A. Gemelli, Università Cattolica del Sacro CuoreRomeItaly

Personalised recommendations