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Nutritional markers in patients with diabetes and pancreatic exocrine failure

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Abstract

Aims

Altered pancreatic exocrine function can be observed in patients with type 1 or type 2 diabetes. In the present study, we evaluated the potential nutritional consequences of this dysfunction.

Methods

Serum concentrations of nutritional markers, including albumin, cholesterol, triacylglycerol, vitamins A, D, and E, were assessed in a cohort of 468 patients (137 with type 1 diabetes and 331 with type 2 diabetes), after exclusion of the patients with a CRP > 10 mg/l. These patients were compared with 47 patients with diseases of the exocrine pancreas and diabetes (type 3c diabetes or pancreatogenic diabetes). Fecal elastase-1 and chymotrypsin concentrations were measured and patients with type 1 and type 2 diabetes were divided into three groups according to whether zero (group NN), one (group LN), or both (group LL) concentrations were decreased.

Results

Several markers differed significantly between the groups of patients, including BMI, albumin, phosphorus, and fat-soluble vitamins. Patients with pancreatogenic diabetes had markedly more profound alterations than patients with type 1 or type 2 diabetes and altered exocrine function. However, patients with type 1 or type 2 diabetes and decreased concentrations of both elastase-1 and chymotrypsin had lower albumin, phosphorus, and vitamin A than patients with normal pancreatic exocrine function.

Conclusions

Modest nutritional alterations were found in patients with type 1 or type 2 diabetes and altered exocrine function. Patients with type 1 or type 2 diabetes and altered exocrine function may thus deserve to be screened for nutritional deficiencies.

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References

  1. Larger E, Philippe MF, Barbot-Trystram L et al (2012) Pancreatic exocrine function in patients with diabetes: pancreatic function in patients with diabetes. Diabet Med 29:1047–1054. https://doi.org/10.1111/j.1464-5491.2012.03597.x

    Article  CAS  PubMed  Google Scholar 

  2. Shivaprasad C, Pulikkal AA, Kumar KMP (2015) Pancreatic exocrine insufficiency in type 1 and type 2 diabetics of Indian origin. Pancreatology 15:616–619. https://doi.org/10.1016/j.pan.2015.09.018

    Article  CAS  PubMed  Google Scholar 

  3. Pollard HM, Miller L, Brewer WA (1943) The external secretion of the pancreas and diabetes mellitus. Am J Dig Dis 10:20–23. https://doi.org/10.1007/BF02997405

    Article  CAS  Google Scholar 

  4. Chey WY, Shay H, Shuman CR (1963) External pancreatic secretion in diabetes mellitus. Ann Intern Med 59:812–821

    Article  CAS  PubMed  Google Scholar 

  5. Vacca JB (1964) The exocrine pancreas in diabetes mellitus. Ann Intern Med 61:242. https://doi.org/10.7326/0003-4819-61-2-242

    Article  CAS  PubMed  Google Scholar 

  6. Mohan V, Snehalatha C, Ahmed MR et al (1989) Exocrine pancreatic function in tropical fibrocalculous pancreatic diabetes. Diabetes Care 12:145–147

    Article  CAS  PubMed  Google Scholar 

  7. Goda K, Sasaki E, Nagata K et al (2001) Pancreatic volume in type 1 and type 2 diabetes mellitus. Acta Diabetol 38:145–149

    Article  CAS  PubMed  Google Scholar 

  8. Gaglia JL, Guimaraes AR, Harisinghani M et al (2011) Noninvasive imaging of pancreatic islet inflammation in type 1A diabetes patients. J Clin Invest 121:442–445. https://doi.org/10.1172/JCI44339

    Article  CAS  PubMed  Google Scholar 

  9. Virostko J, Hilmes M, Eitel K et al (2016) Use of the electronic medical record to assess pancreas size in type 1 diabetes. PLoS ONE 11:e0158825. https://doi.org/10.1371/journal.pone.0158825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Campbell-Thompson M, Rodriguez-Calvo T, Battaglia M (2015) Abnormalities of the exocrine pancreas in type 1 diabetes. Curr Diabetes Rep 15:79. https://doi.org/10.1007/s11892-015-0653-y

    Article  CAS  Google Scholar 

  11. Williams AJK, Thrower SL, Sequeiros IM et al (2012) Pancreatic volume is reduced in adult patients with recently diagnosed type 1 diabetes. J Clin Endocrinol Metab 97:E2109–E2113. https://doi.org/10.1210/jc.2012-1815

    Article  CAS  PubMed  Google Scholar 

  12. Sasamori H, Fukui T, Hayashi T et al (2018) Analysis of pancreatic volume in acute-onset, slowly-progressive and fulminant type 1 diabetes in a Japanese population. J Diabetes Investig. https://doi.org/10.1111/jdi.12816

    Article  PubMed  PubMed Central  Google Scholar 

  13. Philippe M-F, Benabadji S, Barbot-Trystram L et al (2011) Pancreatic volume and endocrine and exocrine functions in patients with diabetes. Pancreas 40:359–363. https://doi.org/10.1097/MPA.0b013e3182072032

    Article  CAS  PubMed  Google Scholar 

  14. Gepts W (1965) Pathologic anatomy of the pancreas in juvenile diabetes mellitus. Diabetes 14:619–633. https://doi.org/10.2337/diab.14.10.619

    Article  CAS  PubMed  Google Scholar 

  15. Coppieters KT, Dotta F, Amirian N et al (2012) Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J Exp Med 209:51–60. https://doi.org/10.1084/jem.20111187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Rodriguez-Calvo T, Ekwall O, Amirian N et al (2014) Increased immune cell infiltration of the exocrine pancreas: a possible contribution to the pathogenesis of type 1 diabetes. Diabetes 63:3880–3890. https://doi.org/10.2337/db14-0549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ehses JA, Perren A, Eppler E et al (2007) Increased number of islet-associated macrophages in type 2 diabetes. Diabetes 56:2356–2370. https://doi.org/10.2337/db06-1650

    Article  CAS  PubMed  Google Scholar 

  18. Cecil RL (1909) A study of the pathological anatomy of the pancreas in ninety cases of diabetes mellitus. J Exp Med 11:266–290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Icks A, Haastert B, Giani G, Rathmann W (2001) Low fecal elastase-1 in type I diabetes mellitus. Z Gastroenterol 39:823–830. https://doi.org/10.1055/s-2001-17867

    Article  CAS  PubMed  Google Scholar 

  20. Ewald N, Raspe A, Kaufmann C et al (2009) Determinants of exocrine pancreatic function as measured by fecal elastase-1 concentrations (FEC) in patients with diabetes mellitus. Eur J Med Res 14:118–122

    PubMed  PubMed Central  Google Scholar 

  21. Hardt PD, Hauenschild A, Nalop J et al (2003) High prevalence of exocrine pancreatic insufficiency in diabetes mellitus. A multicenter study screening fecal elastase 1 concentrations in 1,021 diabetic patients. Pancreatology 3:395–402. https://doi.org/10.1159/000073655

    Article  PubMed  Google Scholar 

  22. Ewald N, Bretzel RG, Fantus IG et al (2007) Pancreatin therapy in patients with insulin-treated diabetes mellitus and exocrine pancreatic insufficiency according to low fecal elastase 1 concentrations. Results of a prospective multi-centre trial. Diabetes Metab Res Rev 23:386–391. https://doi.org/10.1002/dmrr.708

    Article  CAS  PubMed  Google Scholar 

  23. Vujasinovic M, Zaletel J, Tepes B et al (2013) Low prevalence of exocrine pancreatic insufficiency in patients with diabetes mellitus. Pancreatology 13:343–346. https://doi.org/10.1016/j.pan.2013.05.010

    Article  PubMed  Google Scholar 

  24. Creutzfeldt W, Gleichmann D, Otto J et al (2005) Follow-up of exocrine pancreatic function in type-1 diabetes mellitus. Digestion 72:71–75. https://doi.org/10.1159/000087660

    Article  PubMed  Google Scholar 

  25. Hahn J-U, Kerner W, Maisonneuve P et al (2008) Low fecal elastase 1 levels do not indicate exocrine pancreatic insufficiency in type-1 diabetes mellitus. Pancreas 36:274–278. https://doi.org/10.1097/MPA.0b013e3181656f8

    Article  CAS  PubMed  Google Scholar 

  26. Canaway S, Phillips I, Betts P (2000) Pancreatic exocrine insufficiency and type 1 diabetes mellitus. Br J Nurs 9:2030–2032. https://doi.org/10.12968/bjon.2000.9.18.12461

    Article  CAS  PubMed  Google Scholar 

  27. Lindkvist B, Nilsson C, Kvarnström M, Oscarsson J (2018) Importance of pancreatic exocrine dysfunction in patients with type 2 diabetes: a randomized crossover study. Pancreatology. https://doi.org/10.1016/j.pan.2018.05.483

    Article  PubMed  Google Scholar 

  28. Duncan A, Talwar D, McMillan DC et al (2012) Quantitative data on the magnitude of the systemic inflammatory response and its effect on micronutrient status based on plasma measurements. Am J Clin Nutr 95:64–71. https://doi.org/10.3945/ajcn.111.023812

    Article  CAS  PubMed  Google Scholar 

  29. Kuhn M, Nakib S, De Bandt JP et al (2008) Simultaneous determination of retinol and alpha-tocopherol in polymeric diets for enteral nutrition. J Chromatogr A 1205:186–190. https://doi.org/10.1016/j.chroma.2008.07.076

    Article  CAS  PubMed  Google Scholar 

  30. Cashman KD, Dowling KG, Škrabáková Z et al (2016) Vitamin D deficiency in Europe: pandemic? Am J Clin Nutr 103:1033–1044. https://doi.org/10.3945/ajcn.115.120873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Navarro JF, Mora C, Jiménez A et al (1999) Relationship between serum magnesium and parathyroid hormone levels in hemodialysis patients. Am J Kidney Dis 34:43–48. https://doi.org/10.1053/AJKD03400043

    Article  CAS  PubMed  Google Scholar 

  32. Krempf M, Ranganathan S, Ritz P et al (1991) Plasma vitamin A and E in type 1 (insulin-dependent) and type 2 (non-insulin-dependent) adult diabetic patients. Int J Vitam Nutr Res 61:38–42

    CAS  PubMed  Google Scholar 

  33. Basu TK, Tze WJ, Leichter J (1989) Serum vitamin A and retinol-binding protein in patients with insulin-dependent diabetes mellitus. Am J Clin Nutr 50:329–331. https://doi.org/10.1093/ajcn/50.2.329

    Article  CAS  PubMed  Google Scholar 

  34. Tanumihardjo SA, Russell RM, Stephensen CB et al (2016) Biomarkers of nutrition for development (BOND)—vitamin a review 1, 2, 3, 4. J Nutr 146:1816S–1848S. https://doi.org/10.3945/jn.115.229708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. West KP (2003) Vitamin A deficiency disorders in children and women. Food Nutr Bull 24:S78–S90. https://doi.org/10.1177/15648265030244S204

    Article  PubMed  Google Scholar 

  36. Wako Y, Suzuki K, Goto Y, Kimura S (1986) Vitamin A transport in plasma of diabetic patients. Tohoku J Exp Med 149:133–143

    Article  CAS  PubMed  Google Scholar 

  37. Löser C, Möllgaard A, Fölsch UR (1996) Faecal elastase 1: a novel, highly sensitive, and specific tubeless pancreatic function test. Gut 39:580–586

    Article  PubMed  PubMed Central  Google Scholar 

  38. Leeds JS, Oppong K, Sanders DS (2011) The role of fecal elastase-1 in detecting exocrine pancreatic disease. Nat Rev Gastroenterol Hepatol 8:405–415. https://doi.org/10.1038/nrgastro.2011.91

    Article  CAS  PubMed  Google Scholar 

  39. Brydon WG, Kingstone K, Ghosh S (2004) Limitations of faecal elastase-1 and chymotrypsin as tests of exocrine pancreatic disease in adults. Ann Clin Biochem 41:78–81. https://doi.org/10.1258/000456304322664753

    Article  CAS  PubMed  Google Scholar 

  40. Siegmund E, Löhr JM, Schuff-Werner P (2004) The diagnostic validity of non-invasive pancreatic function tests—a meta-analysis. Z Gastroenterol 42:1117–1128. https://doi.org/10.1055/s-2004-813604

    Article  CAS  PubMed  Google Scholar 

  41. Vanga RR, Tansel A, Sidiq S et al (2018) Diagnostic performance of measurement of fecal elastase-1 in detection of exocrine pancreatic insufficiency: systematic review and meta-analysis. Clin Gastroenterol Hepatol 16:1220–1228.e4. https://doi.org/10.1016/j.cgh.2018.01.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Conwell DL, Lee LS, Yadav D et al (2014) American Pancreatic Association practice guidelines in chronic pancreatitis: evidence-based report on diagnostic guidelines. Pancreas 43:1143–1162. https://doi.org/10.1097/MPA.0000000000000237

    Article  PubMed  PubMed Central  Google Scholar 

  43. Lindkvist B (2013) Diagnosis and treatment of pancreatic exocrine insufficiency. World J Gastroenterol 19:7258–7266. https://doi.org/10.3748/wjg.v19.i42.7258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Etienne Larger.

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The authors declare that they have no conflict of interest. All investigations were performed in the context of routine patient’s care.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Alexandre-Heymann, L., Lemoine, A.Y., Nakib, S. et al. Nutritional markers in patients with diabetes and pancreatic exocrine failure. Acta Diabetol 56, 651–658 (2019). https://doi.org/10.1007/s00592-019-01294-w

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  • DOI: https://doi.org/10.1007/s00592-019-01294-w

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