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Review

Cystic fibrosis-related diabetes: links, challenges, and future directions

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Pages 157-167 | Published online: 05 Nov 2015

References

  • Moran A, Becker D, Casella SJ, et al. Epidemiology, pathophysiology, and prognostic implications of cystic fibrosis-related diabetes: a technical review. Diabetes Care. 2010;33(12):2677–2683.
  • Moran A, Dunitz J, Nathan B, Saeed A, Holme B, Thomas W. Cystic fibrosis-related diabetes: current trends in prevalence, incidence, and mortality. Diabetes Care. 2009;32(9):1626–1631.
  • Finkelstein SM, Wielinski CL, Elliott GR, et al. Diabetes mellitus associated with cystic fibrosis. J Pediatr. 1988;112(3):373–377.
  • Lewis C, Blackman SM, Nelson A, et al. Diabetes-related mortality in adults with cystic fibrosis. Role of genotype and sex. Am J Respir Crit Care Med. 2015;191(2):194–200.
  • Sheikh S, Zemel BS, Stallings VA, Rubenstein RC, Kelly A. Body composition and pulmonary function in cystic fibrosis. Front Pediatr. 2014;2:33.
  • Kerem E, Viviani L, Zolin A, et al. Factors associated with FEV1 decline in cystic fibrosis: analysis of the ECFS patient registry. Eur Respir J. 2014;43(1):125–133.
  • Koch C, Rainisio M, Madessani U, et al. Presence of cystic fibrosis-related diabetes mellitus is tightly linked to poor lung function in patients with cystic fibrosis: data from the European Epidemiologic Registry of Cystic Fibrosis. Pediatr Pulmonol. 2001;32(5):343–350.
  • Milla CE, Warwick WJ, Moran A. Trends in pulmonary function in patients with cystic fibrosis correlate with the degree of glucose intolerance at baseline. Am J Respir Crit Care Med. 2000;162(3 Pt 1):891–895.
  • Lanng S, Thorsteinsson B, Nerup J, Koch C. Influence of the development of diabetes mellitus on clinical status in patients with cystic fibrosis. Eur J Pediatr. 1992;151(9):684–687.
  • Sequeiros IM, Jarad N. Factors associated with a shorter time until the next pulmonary exacerbation in adult patients with cystic fibrosis. Chron Respir Dis. 2012;9(1):9–16.
  • Bismuth E, Laborde K, Taupin P, et al. Glucose tolerance and insulin secretion, morbidity, and death in patients with cystic fibrosis. J Pediatr. 2008;152(4):540–545, 545.e1.
  • Bradbury RA, Shirkhedkar D, Glanville AR, Campbell LV. Prior diabetes mellitus is associated with increased morbidity in cystic fibrosis patients undergoing bilateral lung transplantation: an ‘orphan’ area? A retrospective case-control study. Intern Med J. 2009;39(6):384–388.
  • Brennan AL, Gyi KM, Wood DM, et al. Airway glucose concentrations and effect on growth of respiratory pathogens in cystic fibrosis. J Cyst Fibros. 2007;6(2):101–109.
  • Garnett JP, Gray MA, Tarran R, et al. Elevated paracellular glucose flux across cystic fibrosis airway epithelial monolayers is an important factor for Pseudomonas aeruginosa growth. PLoS One. 2013;8(10):e76283.
  • Van Sambeek L, Cowley ES, Newman DK, Kato R. Sputum glucose and glycemic control in cystic fibrosis-related diabetes: a cross-sectional study. PLoS One. 2015;10(3):e0119938.
  • Rolon MA, Benali K, Munck A, et al. Cystic fibrosis-related diabetes mellitus: clinical impact of prediabetes and effects of insulin therapy. Acta Paediatr. 2001;90(8):860–867.
  • Nousia-Arvanitakis S, Galli-Tsinopoulou A, Karamouzis M. Insulin improves clinical status of patients with cystic-fibrosis-related diabetes mellitus. Acta Paediatr. 2001;90(5):515–519.
  • Dobson L, Hattersley AT, Tiley S, Elworthy S, Oades PJ, Sheldon CD. Clinical improvement in cystic fibrosis with early insulin treatment. Arch Dis Child. 2002;87(5):430–431.
  • Ripa P, Robertson I, Cowley D, Harris M, Masters IB, Cotterill AM. The relationship between insulin secretion, the insulin-like growth factor axis and growth in children with cystic fibrosis. Clin Endocrinol (Oxf). 2002;56(3):383–389.
  • Bizzarri C, Montemitro E, Pedicelli S, et al. Glucose tolerance affects pubertal growth and final height of children with cystic fibrosis. Pediatr Pulmonol. 2015;50(2):144–149.
  • Hameed S, Morton JR, Jaffe A, et al. Early glucose abnormalities in cystic fibrosis are preceded by poor weight gain. Diabetes Care. 2010;33(2):221–226.
  • Bizzarri C, Lucidi V, Ciampalini P, Bella S, Russo B, Cappa M. Clinical effects of early treatment with insulin glargine in patients with cystic fibrosis and impaired glucose tolerance. J Endocrinol Invest. 2006;29(3):RC1–RC4.
  • Hameed S, Morton JR, Field PI, et al. Once daily insulin detemir in cystic fibrosis with insulin deficiency. Arch Dis Child. 2012;97(5):464–467.
  • Mozzillo E, Franzese A, Valerio G, et al. One-year glargine treatment can improve the course of lung disease in children and adolescents with cystic fibrosis and early glucose derangements. Pediatr Diabetes. 2009;10(3):162–167.
  • Schwarzenberg SJ, Thomas W, Olsen TW, et al. Microvascular complications in cystic fibrosis-related diabetes. Diabetes Care. 2007;30(5):1056–1061.
  • 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(6):515–519.
  • Quon BS, Mayer-Hamblett N, Aitken ML, Smyth AR, Goss CH. Risk factors for chronic kidney disease in adults with cystic fibrosis. Am J Respir Crit Care Med. 2011;184(10):1147–1152.
  • American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2013;36 Suppl 1:S67–S74.
  • Iannucci A, Mukai K, Johnson D, Burke B. Endocrine pancreas in cystic fibrosis: an immunohistochemical study. Hum Pathol. 1984;15(3):278–284.
  • Abdul-Karim FW, Dahms BB, Velasco ME, Rodman HM. Islets of Langerhans in adolescents and adults with cystic fibrosis. A quantitative study. Arch Pathol Lab Med. 1986;110(7):602–606.
  • Soejima K, Landing BH. Pancreatic islets in older patients with cystic fibrosis with and without diabetes mellitus: morphometric and immunocytologic studies. Pediatr Pathol. 1986;6(1):25–46.
  • Adler AI, Shine BS, Chamnan P, Haworth CS, Bilton D. Genetic determinants and epidemiology of cystic fibrosis-related diabetes: results from a British cohort of children and adults. Diabetes Care. 2008;31(9):1789–1794.
  • Mohan K, Miller H, Dyce P, et al. Mechanisms of glucose intolerance in cystic fibrosis. Diabet Med. 2009;26(6):582–588.
  • No authors listed. Abstracts of the 27th Annual North American Cystic Fibrosis Conference. October 17–19, 2013. Salt Lake City, Utah, USA. Pediatr Pulmonol. 2013;48 Suppl 36:103–472.
  • Cucinotta D, Conti Nibali S, Arrigo T, et al. Beta cell function, peripheral sensitivity to insulin and islet cell autoimmunity in cystic fibrosis patients with normal glucose tolerance. Horm Res. 1990;34(1):33–38.
  • Moran A, Diem P, Klein DJ, Levitt MD, Robertson RP. Pancreatic endocrine function in cystic fibrosis. J Pediatr. 1991;118(5):715–723.
  • Cano Megias M, Gonzalez Albarran O, Guisado Vasco P, Lamas Ferreiro A, Maiz Carro L. Insulin resistance, beta-cell dysfunction and differences in curves of plasma glucose and insulin in the intermediate points of the standard glucose tolerance test in adults with cystic fibrosis. Endocrinol Nutr. 2015;62(2):91–99.
  • Rakotoambinina B, Delaisi B, Laborde K, et al. Insulin responses to intravenous glucose and the hyperglycemic clamp in cystic fibrosis patients with different degrees of glucose tolerance. Pediatr Res. 1994;36(5):667–671.
  • Lombardo F, De Luca F, Rosano M, et al. Natural history of glucose tolerance, beta-cell function and peripheral insulin sensitivity in cystic fibrosis patients with fasting euglycemia. Eur J Endocrinol. 2003;149(1):53–59.
  • Cucinotta D, De Luca F, Gigante A, et al. No changes of insulin sensitivity in cystic fibrosis patients with different degrees of glucose tolerance: an epidemiological and longitudinal study. Eur J Endocrinol. 1994;130(3):253–258.
  • Knop FK, Vilsboll T, Larsen S, et al. Increased postprandial responses of GLP-1 and GIP in patients with chronic pancreatitis and steatorrhea following pancreatic enzyme substitution. Am J Physiol Endocrinol Metab. 2007;292(1):E324–E330.
  • Kelly A, Moran A. Update on cystic fibrosis-related diabetes. J Cyst Fibros. 2013;12(4):318–331.
  • Perano SJ, Couper JJ, Horowitz M, et al. Pancreatic enzyme supplementation improves the incretin hormone response and attenuates postprandial glycemia in adolescents with cystic fibrosis: a randomized crossover trial. J Clin Endocrinol Metab. 2014;99(7):2486–2493.
  • O’Riordan SM, Robinson PD, Donaghue KC, Moran A; ISPAD Clinical Practice Consensus. Management of cystic fibrosis-related diabetes. Pediatr Diabetes. 2008;9(4 Pt 1):338–344.
  • Yung B, Noormohamed FH, Kemp M, Hooper J, Lant AF, Hodson ME. Cystic fibrosis-related diabetes: the role of peripheral insulin resistance and beta-cell dysfunction. Diabet Med. 2002;19(3):221–226.
  • Smerieri A, Montanini L, Maiuri L, Bernasconi S, Street ME. FOXO1 content is reduced in cystic fibrosis and increases with IGF-I treatment. Int J Mol Sci. 2014;15(10):18000–18022.
  • Moran A, Basu R, Milla C, Jensen MD. Insulin regulation of free fatty acid kinetics in adult cystic fibrosis patients with impaired glucose tolerance. Metabolism. 2004;53(11):1467–1472.
  • Hardin DS, LeBlanc A, Lukenbaugh S, Para L, Seilheimer DK. Proteolysis associated with insulin resistance in cystic fibrosis. Pediatrics. 1998;101(3 Pt 1):433–437.
  • Hanna RM, Weiner DJ. Overweight and obesity in patients with cystic fibrosis: a center-based analysis. Pediatr Pulmonol. 2015;50(1):35–41.
  • Donath MY, Halban PA. Decreased beta-cell mass in diabetes: significance, mechanisms and therapeutic implications. Diabetologia. 2004;47(3):581–589.
  • Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003;52(1):102–110.
  • Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444(7121):860–867.
  • Luciani A, Villella VR, Esposito S, et al. Cystic fibrosis: a disorder with defective autophagy. Autophagy. 2011;7(1):104–106.
  • Maiese K. New Insights for Oxidative Stress and Diabetes Mellitus. Oxid Med Cell Longev. 2015;2015:875961.
  • Blackman SM, Hsu S, Ritter SE, et al. A susceptibility gene for type 2 diabetes confers substantial risk for diabetes complicating cystic fibrosis. Diabetologia. 2009;52(9):1858–1865.
  • Blackman SM, Commander CW, Watson C, et al. Genetic modifiers of cystic fibrosis-related diabetes. Diabetes. 2013;62(10):3627–3635.
  • Park JH, Stoffers DA, Nicholls RD, Simmons RA. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest. 2008;118(6):2316–2324.
  • Sandovici I, Smith NH, Nitert MD, et al. Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets. Proc Natl Acad Sci U S A. 2011;108(13):5449–5454.
  • Dayeh T, Volkov P, Salo S, et al. Genome-wide DNA methylation analysis of human pancreatic islets from type 2 diabetic and non-diabetic donors identifies candidate genes that influence insulin secretion. PLoS Genet. 2014;10(3):e1004160.
  • Boom A, Lybaert P, Pollet JF, et al. Expression and localization of cystic fibrosis transmembrane conductance regulator in the rat endocrine pancreas. Endocrine. 2007;32(2):197–205.
  • Olivier AK, Yi Y, Sun X, et al. Abnormal endocrine pancreas function at birth in cystic fibrosis ferrets. J Clin Invest. 2012;122(10):3755–3768.
  • Guo JH, Chen H, Ruan YC, et al. Glucose-induced electrical activities and insulin secretion in pancreatic islet beta-cells are modulated by CFTR. Nat Commun. 2014;5:4420.
  • Uc A, Olivier AK, Griffin MA, et al. Glycaemic regulation and insulin secretion are abnormal in cystic fibrosis pigs despite sparing of islet cell mass. Clin Sci (Lond). 2015;128(2):131–142.
  • Bellin MD, Laguna T, Leschyshyn J, et al. Insulin secretion improves in cystic fibrosis following ivacaftor correction of CFTR: a small pilot study. Pediatr Diabetes. 2013;14(6):417–421.
  • Hayes D Jr, McCoy KS, Sheikh SI. Resolution of cystic fibrosis-related diabetes with ivacaftor therapy. Am J Respir Crit Care Med. 2014;190(5):590–591.
  • Moran A, Brunzell C, Cohen RC, et al. Clinical care guidelines for cystic fibrosis-related diabetes: a position statement of the American Diabetes Association and a clinical practice guideline of the Cystic Fibrosis Foundation, endorsed by the Pediatric Endocrine Society. Diabetes Care. 2010;33(12):2697–2708.
  • Moran A, Pekow P, Grover P, et al. Insulin therapy to improve BMI in cystic fibrosis-related diabetes without fasting hyperglycemia: results of the cystic fibrosis related diabetes therapy trial. Diabetes Care. 2009;32(10):1783–1788.
  • Scheuing N, Holl RW, Dockter G, et al. High variability in oral glucose tolerance among 1,128 patients with cystic fibrosis: a multicenter screening study. PLoS One. 2014;9(11):e112578.
  • Sterescu AE, Rhodes B, Jackson R, et al. Natural history of glucose intolerance in patients with cystic fibrosis: ten-year prospective observation program. J Pediatr. 2010;156(4):613–617.
  • Lanng S, Hansen A, Thorsteinsson B, Nerup J, Koch C. Glucose tolerance in patients with cystic fibrosis: five year prospective study. BMJ. 1995;311(7006):655–659.
  • Dobson L, Sheldon CD, Hattersley AT. Conventional measures underestimate glycaemia in cystic fibrosis patients. Diabet Med. 2004;21(7):691–696.
  • Street ME, Spaggiari C, Ziveri MA, et al. Insulin production and resistance in cystic fibrosis: effect of age, disease activity, and genotype. J Endocrinol Invest. 2012;35(3):246–253.
  • Cucinotta D, De Luca F, Scoglio R, et al. Factors affecting diabetes mellitus onset in cystic fibrosis: evidence from a 10-year follow-up study. Acta Paediatr. 1999;88(4):389–393.
  • Marshall BC, Butler SM, Stoddard M, Moran AM, Liou TG, Morgan WJ. Epidemiology of cystic fibrosis-related diabetes. J Pediatr. 2005;146(5):681–687.
  • Garagorri JM, Rodriguez G, Ros L, Sanchez A. Early detection of impaired glucose tolerance in patients with cystic fibrosis and predisposition factors. J Pediatr Endocrinol Metab. 2001;14(1):53–60.
  • Patient Registry. Annual data report to the Center directors. 2013. Cystic Fibrosis Foundation. Available from: https://www.cff.org/2013_CFF_Annual_Data_Report_to_the_Center_Directors.pdf. Accessed May 14, 2015.
  • Lee KM, Miller RJ, Rosenberg FM, Kreisman SH. Evaluation of glucose tolerance in cystic fibrosis: comparison of 50-g and 75-g tests. J Cyst Fibros. 2007;6(4):274–276.
  • Dobson L, Sheldon CD, Hattersley AT. Validation of interstitial fluid continuous glucose monitoring in cystic fibrosis. Diabetes Care. 2003;26(6):1940–1941.
  • Franzese A, Valerio G, Buono P, et al. Continuous glucose monitoring system in the screening of early glucose derangements in children and adolescents with cystic fibrosis. J Pediatr Endocrinol Metab. 2008;21(2):109–116.
  • Moreau F, Weiller MA, Rosner V, et al. Continuous glucose monitoring in cystic fibrosis patients according to the glucose tolerance. Horm Metab Res. 2008;40(7):502–506.
  • Schiaffini R, Brufani C, Russo B, et al. Abnormal glucose tolerance in children with cystic fibrosis: the predictive role of continuous glucose monitoring system. Eur J Endocrinol. 2010;162(4):705–710.
  • O’Riordan SM, Hindmarsh P, Hill NR, et al. Validation of continuous glucose monitoring in children and adolescents with cystic fibrosis: a prospective cohort study. Diabetes Care. 2009;32(6):1020–1022.
  • Godbout A, Hammana I, Potvin S, et al. No relationship between mean plasma glucose and glycated haemoglobin in patients with cystic fibrosis-related diabetes. Diabetes Metab. 2008;34(6 Pt 1):568–573.
  • Solomon MP, Wilson DC, Corey M, et al. Glucose intolerance in children with cystic fibrosis. J Pediatr. 2003;142(2):128–132.
  • Burgess JC, Bridges N, Banya W, et al. HbA1c as a screening tool for cystic fibrosis related diabetes. J Cyst Fibros. Epub April 10, 2015.
  • Moran A. Diagnosis, screening, and management of cystic fibrosis-related diabetes. Curr Diab Rep. 2002;2(2):111–115.
  • Tofe S, Moreno JC, Maiz L, Alonso M, Escobar H, Barrio R. Insulin-secretion abnormalities and clinical deterioration related to impaired glucose tolerance in cystic fibrosis. Eur J Endocrinol. 2005;152(2):241–247.
  • Minicucci L, Haupt M, Casciaro R, et al. Slow-release insulin in cystic fibrosis patients with glucose intolerance: a randomized clinical trial. Pediatr Diabetes. 2012;13(2):197–202.
  • 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(2):181–186.
  • Lanng S, Thorsteinsson B, Nerup J, Koch C. Diabetes mellitus in cystic fibrosis: effect of insulin therapy on lung function and infections. Acta Paediatr. 1994;83(8):849–853.
  • Onady GM, Stolfi A. Insulin and oral agents for managing cystic fibrosis-related diabetes. Cochrane Database Syst Rev. 2013;7:CD004730.
  • Spijker HS, Wolffenbuttel BH, van der Bij W, Engelse MA, Rabelink TJ, de Koning EJ. Islet-after-lung transplantation in a patient with cystic fibrosis-related diabetes. Diabetes Care. 2014;37(7):e159–e160.
  • Trujillo JM, Nuffer W, Ellis SL. GLP-1 receptor agonists: a review of head-to-head clinical studies. Ther Adv Endocrinol Metab. 2015;6(1):19–28.
  • Horton ES, Silberman C, Davis KL, Berria R. Weight loss, glycemic control, and changes in cardiovascular biomarkers in patients with type 2 diabetes receiving incretin therapies or insulin in a large cohort database. Diabetes Care. 2010;33(8):1759–1765.
  • Rickels MR, Bellin M, Toledo FG, et al. Detection, evaluation and treatment of diabetes mellitus in chronic pancreatitis: recommendations from PancreasFest 2012. Pancreatology. 2013;13(4):336–342.
  • Kawalec P, Mikrut A, Lopuch S. The safety of dipeptidyl peptidase-4 (DPP-4) inhibitors or sodium-glucose cotransporter 2 (SGLT-2) inhibitors added to metformin background therapy in patients with type 2 diabetes mellitus: a systematic review and meta-analysis. Diabetes Metab Res Rev. 2014;30(4):269–283.
  • Clemmons DR. Metabolic actions of insulin-like growth factor-I in normal physiology and diabetes. Endocrinol Metab Clin North Am. 2012;41(2):425–443.
  • Ramsey BW, Davies J, McElvaney NG, et al. A CFTR potentiator in patients with cystic fibrosis and the G551D mutation. N Engl J Med. 2011;365(18):1663–1672.
  • Millington K, Miller V, Rubenstein RC, Kelly A. Patient and parent perceptions of the diagnosis and management of cystic fibrosis-related diabetes. Journal of Clinical and Translational Endocrinology. 2014;1(3):100–107.