Management of cystic fibrosis-related diabetes in children and adolescents

Pediatric Diabetes

Volumn 15, Issue SUPPL.20, 2014, Pages 65-76

  Moran, Antoinette ^a   Pillay, Kubendran ^b   Becker, Dorothy J ^c   Acerini, Carlo L ^d  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Westville Hospital   (South Africa)

^c CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Consensus; Cystic fibrosis; Diabetes; Guidelines

Indexed keywords

ADOLESCENT; CHILD; COMPLICATION; CYSTIC FIBROSIS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; EVIDENCE BASED MEDICINE; FAMILY; HEALTH CARE ORGANIZATION; HUMAN; INFANT; INTERNATIONAL COOPERATION; MEDICINE; MULTIMODALITY CANCER THERAPY; PATHOPHYSIOLOGY; PATIENT EDUCATION; PEDIATRICS; PERSONALIZED MEDICINE; PRACTICE GUIDELINE; PRESCHOOL CHILD; PROGNOSIS; SELF CARE; TRENDS;

ADOLESCENT; ADOLESCENT MEDICINE; CHILD; CHILD, PRESCHOOL; COMBINED MODALITY THERAPY; CYSTIC FIBROSIS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; EVIDENCE-BASED MEDICINE; FAMILY; HUMANS; INDIVIDUALIZED MEDICINE; INFANT; INTERNATIONAL AGENCIES; PATIENT EDUCATION AS TOPIC; PEDIATRICS; PROGNOSIS; SELF CARE; SOCIETIES, SCIENTIFIC;

EID: 84906826756     PISSN: 1399543X     EISSN: 13995448     Source Type: Journal    
DOI: 10.1111/pedi.12178     Document Type: Article

References (90)

1. Moran A, Brunzell C, Cohen RC et al. Clinical care guidelines for CFRD: recommendations from the cystic fibrosis foundation, the American diabetes association and the pediatric endocrine society. Diabetes Care 2010: 33: 2697-2708.
2. 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: 1020-1022.
3. Moreau F, Weiller MA, Rosner V et al. Continuous glucose monitoring in CF patients according to the glucose tolerance. Horm Metab Res 2008: 40: 502-506.
4. Frohnert B, Ode KL, Moran A et al. Impaired fasting glucose in cystic fibrosis. Diabetes Care 2010: 33: 2660-2664.
5. Scheuing N, Holl RW, Dockter G et al. Diabetes in cystic fibrosis: Multicenter screening results based on current guidelines. PLoS One 2013: 8: e81545 doi:10.1371/journal.pone.0081545
6. Hardin DS, Rice J, Cohen RC, Ellis KJ, Nick JA. The metabolic effects of pregnancy in cystic fibrosis. Obstet Gynecol 2005: 106: 367-375.
7. Martin-Frias M, Lamas Ferreiro A, Enes Romero P, Cano Gutierrez B, Barrio Castellanos R. Abnormal glucose tolerance in prepubertal patients with cystic fibrosis. An Pediatr (Barc) 2012: 77: 339-343.
8. Lanng S, Hansen A, Thorsteinsson B, Nerup J, Koch C. Glucose tolerance in cystic fibrosis: a five year prospective study. BMJ 1995: 311: 655-659.
9. 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: 1626-1631.
10. Koch D, Rainisio M, Madessani U et al. Presence of cystic fibrosis-related diabetes mellitus is tightly liked to poor lung function in patients with cystic fibrosis: data from the European epidemiologic registry of cystic fibrosis. Pediatr Pulmonol 2001: 32: 343-350.
11. O'Riordan SM, Hoey H, Costigan C. Demographics and prevalence of glucose intolerance and cystic fibrosis related diabetes in 167 cystic fibrosis children. Diabetes 2006: 55: A224.
12. Lanng S. Glucose intolerance in cystic fibrosis patients. Paediatr Respir Rev 1991: 2: 253-259.
13. Iannucci A, Mukai K, Johnson D, Burke B. Endocrine pancreas in cystic fibrosis: an immunohistochemical study. Hum Pathol 1984: 15: 278-284.
14. Lohr M, Goertchem P, Nizze H et al. CF associated islet changes may provide a basis for diabetes. Virchows Arch A Pathol Anat 1989: 414: 179-185.
15. Couce M, O'Brien TD, Moran A, Roche PC, Butler PC. Diabetes mellitus in CF is characterized by islet amyloidosis. J Clin Endocrinol Metab 1996: 81: 1267-1272.
16. Gottlieb PA, Yu L, Babu S et al. No relation between cystic-fibrosis related diabetes and type 1 diabetes autoimmunity. Diabetes Care 2012: 35: e1.
17. Bismuth E, Laborde K, Taupin P et al. Glucose tolerance and insulin secretion, morbidity and death in patients with CF. J Pediatr 2008: 152: 540-545.
18. Holl RW, Wolf A, Thon A et al. Insulin resistance with altered secretory kinetics and reduced proinsulin in CF patients. J Pediatr Gastroenterol Nutr 1997: 25: 188-193.
19. Lanng S, Thorsteinsson B, Roder ME et al. Pancreas and gut hormone responses to oral glucose and intravenous glucagon in cystic fibrosis patients with normal, impaired, and diabetic glucose tolerance. Acta Endocrinol 1993: 128: 207-214.
20. DeSchepper J, Dab I, Derde MP, Loeb H. Oral glucose tolerance testing in cystic fibrosis: correlations with clinical parameters and glycosylated hemoglobin determinations. Eur J Pediatr 1991: 150: 403-406.
21. Hamdi I, Payne S, Barton D et al. Genotype analysis in CF in relation to the occurrence of diabetes mellitus. Clin Genet 1993: 43: 186-189.
22. Yung B, Noormohamed FH, Kemp M, Hooper J, Lant AF, Hodson ME. CFRD: the role of peripheral insulin resistance and beta-cell dysfunction. Diabet Med 2002: 19: 221-226.
23. Moran A, Diem P, Klein DJ, Levitt MD, Robertson RP. Pancreatic endocrine function in cystic fibrosis. J Pediatr 1991: 118: 715-723.
24. 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: 253-258.
25. Lanng S, Thorsteinsson B, Roder ME, Nerup J, Koch C. Insulin sensitivity and insulin clearance in CF patients with normal and diabetic glucose tolerance. Clin Endocrinol 1994: 41: 217-223.
26. Hardin DS, LeBlance A, Para L, Seilheimer DK. Hepatic insulin resistance and defects in substrate utilization in cystic fibrosis. Diabetes 1999: 48: 1082-1087.
27. Moran A, Pyzdrowski K, Weinreb MD et al. Insulin sensitivity in cystic fibrosis. Diabetes 1994: 43: 1020-1026.
28. Battezatti A, Mari A, Zazzerson L et al. Identification of insulin secretory defects and insulin resistance during oral glucose tolerance test in a cohort of cystic fibrosis patients. Eur J Endocrinol 2011: 165: 69-76.
29. Edlund A, Huhn M, Flodstrom-Tullberg M, Eliasson L. Active CFTR channels are important for insulin and glucagon secretion. Acta Physiologica 2010: 198 (Suppl. 677P-MON-66).
30. Boom A, Lybaert P, Pollet JF et al. Expression and localization of CFTR in the rat endocrine pancreas. Endocr Pract 2008: 32: 197-205.
31. Olivier AK, Yi Y, Sun X et al. Abnormal endocrine pancreas function at birth in cystic fibrosis ferrets. J Clin Invest 2012: 122: 3755-3768.
32. Bellin MD, Laguna T, Leschyshyn J et al. Proof-of-concept pilot: insulin secretion improves in cystic fibrosis following ivacaftor correction of CFTR. Pediatr Diabetes 2013: 14: 417-421.
33. Blackman SM, Hsu S, Vanscoy LL et al. Genetic modifiers play a substantial role in diabetes complicating cystic fibrosis. J Clin Endocrinol Metab 2009: 94: 1302-1309.
34. 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: 1858-1865.
35. Blackman SM, Commander CW, Watson C et al. Genetic modifiers of cystic fibrosis-related diabetes. Diabetes 2013: 62: 3627-3635.
36. Lanng S, Thorsteinsson B, Pociot F et al. Diabetes mellitus in cystic fibrosis: genetic and immunological markers. Acta Paediatr 1993: 82: 150-154.
37. Jensen P, Johansen HK, Carmi P, Hoiby N, Cohen IR. Autoantibodies to pancreatic hsp60 precede the development of gkucose intolerance in patients with CF. J Autoimmun 2001: 17: 165-172.
38. Derbel S, Doumaguet C, Hubert D et al. Calpain 10 and development of diabetes mellitus in cystic fibrosis. J Cyst Fibros 2006: 5: 47-51.
39. Braun AT, Merlo CA. Cystic fibrosis and lung transplantation. Curr Opin Pulm Med 2011: 17: 467-472.
40. Hadjiliadis D, Madill J, Chaparro C et al. Incidence and prevalence of diabetes mellitus in patients with cystic fibrosis undergoing lung transplantation before and after lung transplantation. Clin Transplant 2005: 19: 773-778.
41. Bradbury RA, Shirkhedkar D, Glanveill AR, Campbell LV. Prior diabetes mellitus is associated with increased morbidity in CF patients undergoing bilateral lung transplantation: an "orphan" area? A retrospective case-control study. Intern Med J 2009: 39: 384-388.
42. van Meerkerk G, van de Graff EA, Kwakkel-van Erp JM et al. Diabetes before and after lung transplantation in patients with cystic fibrosis and other lung diseases. Diabet Med 2012: 29: e159-e162.
43. Marshall BC, Butler SM, Stoddard M, Moran AM, Liou TG, Morgan WJ. Epidemiology of cystic fibrosis-related diabetes. J Pediatr 2005: 146: 681-687.
44. Finkelstein SM, Wielinski CL, Elliott GR et al. Diabetes mellitus associated with cystic fibrosis. J Pediatr 1988: 112: 373-377.
45. Rosenecker J, Hofler R, Steinkamp G et al. Diabetes mellitus in patients with cystic fibrosis: the impact of diabetes mellitus on pulmonary function and clinical outcome. Eur J Med Res 2001: 6: 345-350.
46. Milla CE, Billings J, Moran A. Diabetes is associated with dramatically decreased survival in female but not male subjects with cystic fibrosis. Diabetes Care 2005: 28: 2141-2144.
47. Sims EJ, Green MW, Mehta A. Decreased lung function in female but not male subjects with established cystic fibrosis-related diabetes. Diabetes Care 2005: 28: 1581-1587.
48. Chamnan P, Shine BSF, Haworth C, Bilton D, Adler AI. Diabetes as a determinant of mortality in cystic fibrosis. Diabetes Care 2010: 33: 311-316.
49. Kien CL, Zipf WB, Horswill CA, Denne SC, McCoy KS, O'Dorsio TM. Effects of feeding on protein turnover in healthy children and in children with cystic fibrosis. Am J Clin Nutr 1996: 64: 608-614.
50. Hardin DS, Leblanc A, Lukenbaugh S, Para L, Seilheimer DK. Proteolysis associated with insulin resistance in cystic fibrosis. Pediatrics 1998: 101: 433-437.
51. Moran A, Milla C, DuCret R, Nair KS. Protein metabolism in clinically stable adult CF patients with abnormal glucose tolerance. Diabetes 2001: 50: 1336-1343.
52. Moran A, Basu R, Milla C, Jensen M. Insulin regulation of free fatty acid kinetics in adult cystic fibrosis patients with impaired glucose tolerance. Metabolism 2004: 53: 1467-1472.
53. Brennan AL, Gyi KM, Wood DM et al. Airway glucose concentrations and effect on growth of respiratory pathogens in CF. J Cyst Fibros 2007: 6: 101-109.
54. Ntimbane T, Krishnamoorthy P, Huot C et al. Oxidative stress and cystic fibrosis-related diabetes: a pilot study in children. J Cyst Fibros 2008: 7: 373-384.
55. Suratwala D, Chan JSH, Kelly A et al. Nocturnal hypoxemia and glucose tolerance in children with cystic fibrosis. Thorax 2011: 66: 574-578.
56. Hunt WR, Zughaier SM, Guentert DE et al. Hyperglycemia impedes lung bacterial clearance in a murine model of cystic-fibrosis-related diabetes. Am J Physiol Lung Cell Mol Physiol 2014: 306: L43-L49.
57. Andersen HU, Lanng S, Tressler T, Laugesen CS, Mathiesen ER. Cystic fibrosis-related diabetes: the presence of microvascular diabetes complications. Diabetes Care 2006: 29: 2660-2663.
58. Schwarzenberg SJ, Thomas W, Olsen TW et al. Microvascular complications in cystic fibrosis-related diabetes. Diabetes Care 2007: 30: 1056-1061.
59. Figueroa V, Milla C, Parks EJ, Schwarzenberg SJ, Moran A. Abnormal lipid levels in cystic fibrosis. Am J Clin Nutr 2002: 75: 1005-1011.
60. Georgiopolou W, Denker A, Bishop KL et al. Metabolic abnormalities in adults with CF. Respirology 2010: 15: 823-829.
61. Ishimo MC, Belson L, Ziai S et al. Hypertriglyceridemia is associated with insulin levels in adult cystic fibrosis patients. J Cyst Fibros 2013: 12: 271-276.
62. Nash EF, Stephenson A, Helm EJ et al. Impact of lung transplantation on serum lipids in adults with cystic fibrosis. J Heart Lung Transplant 2011: 30: 188-193.
63. Rhodes B, Nash EF, Tullis E et al. Prevalence of dyslipidemia in adults with CF. J Cyst Fibros 2010: 9: 24-28.
64. Radike K, Molz K, Holl RW, Peoeter B, Hebestreit H, Ballmann M. Prognostic relevance of hypoglycemia following an oral glucose challenge for cystic fibrosis-related diabetes. Diabetes Care 2011: 34: e43.
65. 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: 684-687.
66. Milla CE, Warwick WJ, Moran A. Trends in pulmonary function in cystic fibrosis patients correlate with the degree of glucose intolerance at baseline. Am J Respir Crit Care Med 2001: 162: 891-895.
67. Nousia-Arvanitakis S, Galli-Tsinopoulou A, Karamouzis M. Insulin improves clinical status of patients with cystic fibrosis-related diabetes mellitus. Acta Paediatr 2001: 90: 515-519.
68. Rolon MA, Benali K, Munck A et al. CFRD: clinical impact of prediabetes and effects of insulin therapy. Acta Paediatr 2001: 90: 860-867.
69. White H, Morton AM, Peckham DG, Conway SP. Dietary intakes in adult patients with cystic fibrosis-do they achieve guidelines? J Cyst Fibros 2004: 3: 1-7.
70. Cheung MS, Bridges NA, Prasad SA et al. Growth in children with cystic fibrosis-related diabetes. Pediatr Pulmonol 2009: 44: 1223-1225.
71. Ripa P, Robertson I, Cowley D, Harris M, Master IB, Cotterill AM. The relationship between insulin secretion, the insulin-like growth factor axis and growth in children with cystic fibrosis. Clin Endocrinol 2002: 56: 383-389.
72. 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: 1783-1788.
73. Schmid K, Fink K, Holl RW, Hebestreit H, Ballmann M. Predictors for future cystic fibrosis-related diabetes by oral glucose tolerance test. J Cyst Fibros 2014: 13: 80-85.
74. Geocobbe LE, Nguyen RH, Aguilera MN et al. Effect of maternal cystic fibrosis genotype on diabetes in pregnancy. Obstet Gynecol 2012: 120: 1394-1399.
75. Hameed S, Morton J, Jaffe A et al. Early glucose abnormalities in cystic fibrosis are preceded by poor weight gain. Diabetes Care 2010: 33: 221-226.
76. Brodsky J, Dougherty S, Ramkrishna M, Rubenstein RC, Kelly A. Elevation of 1-hour plasma glucose during oral glucose tolerance testing is associated with worse pulmonary function in cystic fibrosis. Diabetes Care 2011: 34: 292-295.
77. Mozzillo E, Raia V, Raggorusso V et al. Glucose derangements in very young children with cystic fibrosis and pancreatic insufficiency. Diabetes Care 2012: 35: e78.
78. Ode KL, Frohnert B, Laguna T et al. Oral glucose tolerance testing in children with cystic fibrosis. Pediatr Diabetes 2010: 11: 487-492.
79. Dobson L, Sheldon CD, Hattersley AT. Conventional measures underestimate glycaemia in CF patients. Diabet Med 2004: 21: 691-696.
80. 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: 705-710.
81. Kolouskova S, Zemkova D, Bartosova J et al. Low-dose insulin therapy in patients with cystic fibrosis and early-stage insulinopenia prevents deterioration of lung function: a 30 year prospective study. J Pediatr Endocrinol Metab 2011: 24: 499-454.
82. Sunni M, Bellin MD, Moran A. Exogenous insulin requirements do not differ between youth and adults with cystic fibrosis related diabetes. Pediatr Diabetes 2013: 14: 295-298.
83. Konrad K, Thon A, Fritsch M et al. Comparison of CFRD with T1D based on a German/Austrian pediatric diabetes registry. Diabetes Care 2012: 35: 1-8.
84. Onady GM, Stolfi A. Insulin and oral agents for managing cystic fibrosis-related diabetes. Cochrane Database Syst Rev 2013: 7: CD004730. doi:10.1002/14651858.CD004730.pub3.
85. Nezer N, Shoseyov D, Kerem E, Zangen DH. Patients with cystic fibrosis and normoglycemia exhibit diabetic glucose tolerance during pulmonary exacerbation. J Cyst Fibros 2010: 9: 199-204.
86. Rasouli N, Seggelke S, Gibbs J et al. Cystic fibrosis-related diabetes in adults: impatient management of 121 patients druing 410 admissions. J Diabetes Sci Technol 2012: 6: 1038-1044.
87. 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: 162-167.
88. 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: RC1-RC4.
89. Hameed S, Morton JR, Field PI et al. Once daily insulin detemir in cystic fibrosis with insulin deficiency. ADC 2012: 97: 464-467.
90. HAPO Study Cooperative Research Group. Hyperglycemia and adverse pregnancy outcomes. N Engl J Med 2008: 358: 1991-2002.