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Semin Respir Crit Care Med 2009; 30(5): 514-530
DOI: 10.1055/s-0029-1238910
© Thieme Medical PublishersDOI: 10.1055/s-0029-1238910
Diabetes Mellitus and Bone Disease in Cystic Fibrosis
Further Information
Publication History
Publication Date:
16 September 2009 (online)
ABSTRACT
Patients with cystic fibrosis are frequently affected with pancreatic insufficiency and are predisposed to the development of diabetes mellitus (DM) and bone demineralization. Cystic fibrosis–related diabetes mellitus is a clinical entity distinct from type 1 and type 2 diabetes, with important implications for the nutritional and pulmonary health of cystic fibrosis patients. This form of diabetes owes largely to insulin deficiency, but alterations in insulin sensitivity and hepatic glucose production have also been described. Therapy for cystic fibrosis–related diabetes differs substantially from type 2 DM, with careful attention to prandial glycemic excursions crucial to controlling its metabolic effects. Bone disease, including osteopenia and osteoporosis, also occurs with increased frequency in cystic fibrosis, owing to defects in intestinal absorption, chronic inflammation, lung disease, low body weight, and gonadal dysfunction. The pathogenesis, implications, diagnosis, and therapy of cystic fibrosis–related bone demineralization are discussed, with attention to recommended approaches to prevention of and treatment of established bone disease.
KEYWORDS
Cystic fibrosis - cystic fibrosis–related diabetes mellitus - osteoporosis - osteopenia - vitamin D - cystic fibrosis–related bone disease
REFERENCES
- 1 Riordan J R, Rommens J M, Kerem B et al.. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science. 1989; 245 1066-1073
- 2 Moran A, Doherty L, Wang X, Thomas W. Abnormal glucose metabolism in cystic fibrosis. J Pediatr. 1998; 133 10-17
- 3 Cystic Fibrosis Patient Registry .2007 Annual Data Report. Bethesda, MD; CF Foundation 2008
- 4 Moran A, Hardin D, Rodman D et al.. Diagnosis, screening and management of cystic fibrosis related diabetes mellitus: a consensus conference report. Diabetes Res Clin Pract. 1999; 45 61-73
- 5 Lee K M, Miller R J, Rosenberg F M, Kreisman S H. Evaluation of glucose tolerance in cystic fibrosis: comparison of 50-g and 75-g tests. J Cyst Fibros. 2007; 6 274-276
- 6 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
- 7 Dobson L, Sheldon C D, Hattersley A T. Conventional measures underestimate glycaemia in cystic fibrosis patients. Diabet Med. 2004; 21 691-696
- 8 Bismuth E, Laborde K, Taupin P et al.. Glucose tolerance and insulin secretion, morbidity, and death in patients with cystic fibrosis. J Pediatr. 2008; 152 540-545
- 9 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 33-38
- 10 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
- 11 Rosenecker J, Eichler I, Kühn L, Harms H K, von der Hardt H. Multicenter Cystic Fibrosis Study Group . Genetic determination of diabetes mellitus in patients with cystic fibrosis. J Pediatr. 1995; 127 441-443
- 12 Lanng S, Hansen A, Thorsteinsson B, Nerup J, Koch C. Glucose tolerance in patients with cystic fibrosis: five year prospective study. BMJ. 1995; 311 655-659
- 13 Finkelstein S M, Wielinski C L, Elliott G R et al.. Diabetes mellitus associated with cystic fibrosis. J Pediatr. 1988; 112 373-377
- 14 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
- 15 Koch C, Rainisio M, Madessani U Investigators of the European Epidemiologic Registry of Cystic Fibrosis 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; 32 343-350
- 16 Milla C E, 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
- 17 Milla C E, Warwick W J, 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
- 18 van den Berg J M, Morton A M, Kok S W, Pijl H, Conway S P, Heijerman H G. Microvascular complications in patients with cystic fibrosis-related diabetes (CFRD). J Cyst Fibros. 2008; 7 515-519
- 19 Iannucci A, Mukai K, Johnson D, Burke B. Endocrine pancreas in cystic fibrosis: an immunohistochemical study. Hum Pathol. 1984; 15 278-284
- 20 Couce M, O’Brien T D, Moran A, Roche P C, Butler P C. Diabetes mellitus in cystic fibrosis is characterized by islet amyloidosis. J Clin Endocrinol Metab. 1996; 81 1267-1272
- 21 Lorenzo A, Razzaboni B, Weir G C, Yankner B A. Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature. 1994; 368 756-760
- 22 Lanng S, Thorsteinsson B, Røder M E 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 (Copenh). 1993; 128 207-214
- 23 Moran A, Diem P, Klein D J, Levitt M D, Robertson R P. Pancreatic endocrine function in cystic fibrosis. J Pediatr. 1991; 118 715-723
- 24 Hardin D S, LeBlanc A, Lukenbough S, Seilheimer D K. Insulin resistance is associated with decreased clinical status in cystic fibrosis. J Pediatr. 1997; 130 948-956
- 25 Lanng S, Thorsteinsson B, Røder M E, Nerup J, Koch C. Insulin sensitivity and insulin clearance in cystic fibrosis patients with normal and diabetic glucose tolerance. Clin Endocrinol (Oxf). 1994; 41 217-223
- 26 Hardin D S, Ahn C, Rice J, Rice M, Rosenblatt R. Elevated gluconeogenesis and lack of suppression by insulin contribute to cystic fibrosis-related diabetes. J Investig Med. 2008; 56 567-573
- 27 Austin A, Kalhan S C, Orenstein D, Nixon P, Arslanian S. Roles of insulin resistance and beta-cell dysfunction in the pathogenesis of glucose intolerance in cystic fibrosis. J Clin Endocrinol Metab. 1994; 79 80-85
- 28 Moran A, Pyzdrowski K L, Weinreb J et al.. Insulin sensitivity in cystic fibrosis. Diabetes. 1994; 43 1020-1026
- 29 O’Riordan S M, Robinson P D, Donaghue K C, Moran A. ISPAD Clinical Practice Consensus . Management of cystic fibrosis-related diabetes. Pediatr Diabetes. 2008; 9(4 Pt 1) 338-344
- 30 Wilson D C, Kalnins D, Stewart C et al.. Challenges in the dietary treatment of cystic fibrosis related diabetes mellitus. Clin Nutr. 2000; 19 87-93
- 31 Rosenecker J, Eichler I, Bärmeier H, von der Hardt H. Diabetes mellitus and cystic fibrosis: comparison of clinical parameters in patients treated with insulin versus oral glucose-lowering agents. Pediatr Pulmonol. 2001; 32 351-355
- 32 Moran A, Phillips J, Milla C. Insulin and glucose excursion following premeal insulin lispro or repaglinide in cystic fibrosis–related diabetes. Diabetes Care. 2001; 24 1706-1710
- 33 Freeland B S, Micallef J. Cystic-fibrosis-related diabetes mellitus. Diabetes Educ. 2002; 28 768-771, 774–775
- 34 Grover P, Thomas W, Moran A. Glargine versus NPH insulin in cystic fibrosis related diabetes. J Cyst Fibros. 2008; 7 134-136
- 35 Dobson L, Hattersley A T, Tiley S, Elworthy S, Oades P J, Sheldon C D. Clinical improvement in cystic fibrosis with early insulin treatment. Arch Dis Child. 2002; 87 430-431
- 36 Mohan K, Israel K L, Miller H, Grainger R, Ledson M J, Walshaw M J. Long-term effect of insulin treatment in cystic fibrosis-related diabetes. Respiration. 2008; 76 181-186
- 37 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
- 38 Hahn T J, Squires A E, Halstead L R, Strominger D B. Reduced serum 25-hydroxyvitamin D concentration and disordered mineral metabolism in patients with cystic fibrosis. J Pediatr. 1979; 94 38-42
- 39 Aris R M, Merkel P A, Bachrach L K et al.. Guide to bone health and disease in cystic fibrosis. J Clin Endocrinol Metab. 2005; 90 1888-1896
- 40 Louis O, Clerinx P, Gies I, De Wachter E, De Schepper J. Well-nourished cystic fibrosis patients have normal mineral density, but reduced cortical thickness at the forearm. Osteoporos Int. 2009; 20 309-314
- 41 Rossini M, Viapiana O, Del Marco A, de Terlizzi F, Gatti D, Adami S. Quantitative ultrasound in adults with cystic fibrosis: correlation with bone mineral density and risk of vertebral fractures. Calcif Tissue Int. 2007; 80 44-49
- 42 Bhudhikanok G S, Wang M C, Marcus R, Harkins A, Moss R B, Bachrach L K. Bone acquisition and loss in children and adults with cystic fibrosis: a longitudinal study. J Pediatr. 1998; 133 18-27
- 43 Buntain H M, Greer R M, Schluter P J et al.. Bone mineral density in Australian children, adolescents and adults with cystic fibrosis: a controlled cross sectional study. Thorax. 2004; 59 149-155
- 44 Douros K, Loukou I, Nicolaidou P, Tzonou A, Doudounakis S. Bone mass density and associated factors in cystic fibrosis patients of young age. J Paediatr Child Health. 2008; 44 681-685
- 45 Henderson R C, Madsen C D. Bone mineral content and body composition in children and young adults with cystic fibrosis. Pediatr Pulmonol. 1999; 27 80-84
- 46 Conway S P, Morton A M, Oldroyd B et al.. Osteoporosis and osteopenia in adults and adolescents with cystic fibrosis: prevalence and associated factors. Thorax. 2000; 55 798-804
- 47 Elkin S L, Fairney A, Burnett S et al.. Vertebral deformities and low bone mineral density in adults with cystic fibrosis: a cross-sectional study. Osteoporos Int. 2001; 12 366-372
- 48 Haworth C S, Selby P L, Webb A K et al.. Low bone mineral density in adults with cystic fibrosis. Thorax. 1999; 54 961-967
- 49 Aris R M, Neuringer I P, Weiner M A, Egan T M, Ontjes D. Severe osteoporosis before and after lung transplantation. Chest. 1996; 109 1176-1183
- 50 Aris R M, Renner J B, Winders A D et al.. Increased rate of fractures and severe kyphosis: sequelae of living into adulthood with cystic fibrosis. Ann Intern Med. 1998; 128 186-193
- 51 Shane E, Silverberg S J, Donovan D et al.. Osteoporosis in lung transplantation candidates with end-stage pulmonary disease. Am J Med. 1996; 101 262-269
- 52 Tschopp O, Boehler A, Speich R et al.. Osteoporosis before lung transplantation: association with low body mass index, but not with underlying disease. Am J Transplant. 2002; 2 167-172
- 53 Haworth C S, Webb A K, Egan J J et al.. Bone histomorphometry in adult patients with cystic fibrosis. Chest. 2000; 118 434-439
- 54 Boyle M P. Update on maintaining bone health in cystic fibrosis. Curr Opin Pulm Med. 2006; 12 453-458
- 55 Baim S, Binkley N, Bilezikian J P et al.. Official positions of the International Society for Clinical Densitometry and executive summary of the 2007 ISCD Position Development Conference. J Clin Densitom. 2008; 11 75-91
- 56 Donovan Jr D S, Papadopoulos A, Staron R B et al.. Bone mass and vitamin D deficiency in adults with advanced cystic fibrosis lung disease. Am J Respir Crit Care Med. 1998; 157(6 Pt 1) 1892-1899
- 57 Papaioannou A, Kennedy C C, Freitag A et al.. Longitudinal analysis of vertebral fracture and BMD in a Canadian cohort of adult cystic fibrosis patients. BMC Musculoskelet Disord. 2008; 9 125
- 58 Wolfenden L L, Judd S E, Shah R, Sanyal R, Ziegler T R, Tangpricha V. Vitamin D and bone health in adults with cystic fibrosis. Clin Endocrinol (Oxf). 2008; 69 374-381
- 59 Stephenson A, Jamal S, Dowdell T, Pearce D, Corey M, Tullis E. Prevalence of vertebral fractures in adults with cystic fibrosis and their relationship to bone mineral density. Chest. 2006; 130 539-544
- 60 Rovner A J, Zemel B S, Leonard M B, Schall J I, Stallings V A. Mild to moderate cystic fibrosis is not associated with increased fracture risk in children and adolescents. J Pediatr. 2005; 147 327-331
- 61 Haworth C S, Selby P L, Horrocks A W, Mawer E B, Adams J E, Webb A K. A prospective study of change in bone mineral density over one year in adults with cystic fibrosis. Thorax. 2002; 57 719-723
- 62 Henderson R C, Specter B B. Kyphosis and fractures in children and young adults with cystic fibrosis. J Pediatr. 1994; 125 208-212
- 63 Baroncelli G I, De Luca F, Magazzú G et al.. Bone demineralization in cystic fibrosis: evidence of imbalance between bone formation and degradation. Pediatr Res. 1997; 41 397-403
- 64 Grey V, Atkinson S, Drury D et al.. Prevalence of low bone mass and deficiencies of vitamins D and K in pediatric patients with cystic fibrosis from 3 Canadian centers. Pediatrics. 2008; 122 1014-1020
- 65 Haston C K, Li W, Li A, Lafleur M, Henderson J E. Persistent osteopenia in adult cystic fibrosis transmembrane conductance regulator-deficient mice. Am J Respir Crit Care Med. 2008; 177 309-315
- 66 Schulze K J, O’Brien K O, Germain-Lee E L, Booth S L, Leonard A, Rosenstein B J. Calcium kinetics are altered in clinically stable girls with cystic fibrosis. J Clin Endocrinol Metab. 2004; 89 3385-3391
- 67 Greer R M, Buntain H M, Potter J M et al.. Abnormalities of the PTH-vitamin D axis and bone turnover markers in children, adolescents and adults with cystic fibrosis: comparison with healthy controls. Osteoporos Int. 2003; 14 404-411
- 68 Aris R M, Guise T A. Cystic fibrosis and bone disease: are we missing a genetic link?. Eur Respir J. 2005; 25 9-11
- 69 King S J, Topliss D J, Kotsimbos T et al.. Reduced bone density in cystic fibrosis: DeltaF508 mutation is an independent risk factor. Eur Respir J. 2005; 25 54-61
- 70 Shead E F, Haworth C S, Gunn E, Bilton D, Scott M A, Compston J E. Osteoclastogenesis during infective exacerbations in patients with cystic fibrosis. Am J Respir Crit Care Med. 2006; 174 306-311
- 71 Aris R M, Ontjes D A, Buell H E et al.. Abnormal bone turnover in cystic fibrosis adults. Osteoporos Int. 2002; 13 151-157
- 72 Elkin S L, Vedi S, Bord S, Garrahan N J, Hodson M E, Compston J E. Histomorphometric analysis of bone biopsies from the iliac crest of adults with cystic fibrosis. Am J Respir Crit Care Med. 2002; 166 1470-1474
- 73 Holick M F. Vitamin D deficiency. N Engl J Med. 2007; 357 266-281
- 74 Aris R M, Lester G E, Dingman S, Ontjes D A. Altered calcium homeostasis in adults with cystic fibrosis. Osteoporos Int. 1999; 10 102-108
- 75 Kalnins D, Durie P R, Pencharz P. Nutritional management of cystic fibrosis patients. Curr Opin Clin Nutr Metab Care. 2007; 10 348-354
- 76 Aris R M, Ontjes D A, Brown S A, Chalermskulrat W, Neuringer I, Lester G E. Carboxylated osteocalcin levels in cystic fibrosis. Am J Respir Crit Care Med. 2003; 168 1129
- 77 Fewtrell M S, Benden C, Williams J E et al.. Undercarboxylated osteocalcin and bone mass in 8-12 year old children with cystic fibrosis. J Cyst Fibros. 2008; 7 307-312
- 78 Aris R M, Stephens A R, Ontjes D A et al.. Adverse alterations in bone metabolism are associated with lung infection in adults with cystic fibrosis. Am J Respir Crit Care Med. 2000; 162 1674-1678
- 79 Rossini M, Del Marco A, Dal Santo F et al.. Prevalence and correlates of vertebral fractures in adults with cystic fibrosis. Bone. 2004; 35 771-776
- 80 Nixon L S, Yung B, Bell S C, Elborn J S, Shale D J. Circulating immunoreactive interleukin-6 in cystic fibrosis. Am J Respir Crit Care Med. 1998; 157(6 Pt 1) 1764-1769
- 81 Manolagas S C, Jilka R L. Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med. 1995; 332 305-311
- 82 Manolagas S C, Weinstein R S. New developments in the pathogenesis and treatment of steroid-induced osteoporosis. J Bone Miner Res. 1999; 14 1061-1066
- 83 van Staa T P, Leufkens H G, Cooper C. The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporos Int. 2002; 13 777-787
- 84 van Staa T P, Leufkens H G, Cooper C. Use of inhaled corticosteroids and risk of fractures. J Bone Miner Res. 2001; 16 581-588
- 85 Thrailkill K M, Lumpkin Jr C K, Bunn R C, Kemp S F, Fowlkes J L. Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab. 2005; 289 E735-E745
- 86 Gordon C M, Binello E, LeBoff M S, Wohl M E, Rosen C J, Colin A A. Relationship between insulin-like growth factor I, dehydroepiandrosterone sulfate and proresorptive cytokines and bone density in cystic fibrosis. Osteoporos Int. 2006; 17 783-790
- 87 Frangolias D D, Paré P D, Kendler D L et al.. Role of exercise and nutrition status on bone mineral density in cystic fibrosis. J Cyst Fibros. 2003; 2 163-170
- 88 Raisz L G. Clinical practice. Screening for osteoporosis. N Engl J Med. 2005; 353 164-171
- 89 Ferrari S L, Nicod L P, Hamacher J et al.. Osteoporosis in patients undergoing lung transplantation. Eur Respir J. 1996; 9 2378-2382
- 90 Spira A, Gutierrez C, Chaparro C, Hutcheon M A, Chan C K. Osteoporosis and lung transplantation: a prospective study. Chest. 2000; 117 476-481
- 91 Gordon C M, Bachrach L K, Carpenter T O, Karsenty G, Rauch F. Bone health in children and adolescents: a symposium at the annual meeting of the Pediatric Academic Societies/Lawson Wilkins Pediatric Endocrine Society, May 2003. Curr Probl Pediatr Adolesc Health Care. 2004; 34 226-242
- 92 Hind K, Truscott J G, Conway S P. Exercise during childhood and adolescence: a prophylaxis against cystic fibrosis-related low bone mineral density? Exercise for bone health in children with cystic fibrosis. J Cyst Fibros. 2008; 7 270-276
- 93 Bradney M, Pearce G, Naughton G et al.. Moderate exercise during growth in prepubertal boys: changes in bone mass, size, volumetric density, and bone strength: a controlled prospective study. J Bone Miner Res. 1998; 13 1814-1821
- 94 Fuchs R K, Bauer J J, Snow C M. Jumping improves hip and lumbar spine bone mass in prepubescent children: a randomized controlled trial. J Bone Miner Res. 2001; 16 148-156
- 95 MacKelvie K J, Petit M A, Khan K M, Beck T J, McKay H A. Bone mass and structure are enhanced following a 2-year randomized controlled trial of exercise in prepubertal boys. Bone. 2004; 34 755-764
- 96 McKay H A, MacLean L, Petit M et al.. “Bounce at the Bell”: a novel program of short bouts of exercise improves proximal femur bone mass in early pubertal children. Br J Sports Med. 2005; 39 521-526
- 97 Petit M A, McKay H A, MacKelvie K J, Heinonen A, Khan K M, Beck T J. A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: a hip structural analysis study. J Bone Miner Res. 2002; 17 363-372
- 98 de Jong W, Grevink R G, Roorda R J, Kaptein A A, van der Schans C P. Effect of a home exercise training program in patients with cystic fibrosis. Chest. 1994; 105 463-468
- 99 Heijerman H G, Bakker W, Sterk P J, Dijkman J H. Long-term effects of exercise training and hyperalimentation in adult cystic fibrosis patients with severe pulmonary dysfunction. Int J Rehabil Res. 1992; 15 252-257
- 100 Klijn P H, Oudshoorn A, van der Ent C K, van der Net J, Kimpen J L, Helders P J. Effects of anaerobic training in children with cystic fibrosis: a randomized controlled study. Chest. 2004; 125 1299-1305
- 101 Orenstein D M, Hovell M F, Mulvihill M et al.. Strength vs aerobic training in children with cystic fibrosis: a randomized controlled trial. Chest. 2004; 126 1204-1214
- 102 Selvadurai H C, Blimkie C J, Meyers N, Mellis C M, Cooper P J, Van Asperen P P. Randomized controlled study of in-hospital exercise training programs in children with cystic fibrosis. Pediatr Pulmonol. 2002; 33 194-200
- 103 Chapuy M C, Preziosi P, Maamer M et al.. Prevalence of vitamin D insufficiency in an adult normal population. Osteoporos Int. 1997; 7 439-443
- 104 Holick M F, Siris E S, Binkley N et al.. Prevalence of Vitamin D inadequacy among postmenopausal North American women receiving osteoporosis therapy. J Clin Endocrinol Metab. 2005; 90 3215-3224
- 105 Hanly J G, McKenna M J, Quigley C, Freaney R, Muldowney F P, FitzGerald M X. Hypovitaminosis D and response to supplementation in older patients with cystic fibrosis. Q J Med. 1985; 56 377-385
- 106 Ott S M, Aitken M L. Osteoporosis in patients with cystic fibrosis. Clin Chest Med. 1998; 19 555-567
- 107 Rovner A J, Stallings V A, Schall J I, Leonard M B, Zemel B S. Vitamin D insufficiency in children, adolescents, and young adults with cystic fibrosis despite routine oral supplementation. Am J Clin Nutr. 2007; 86 1694-1699
- 108 Lark R K, Lester G E, Ontjes D A et al.. Diminished and erratic absorption of ergocalciferol in adult cystic fibrosis patients. Am J Clin Nutr. 2001; 73 602-606
- 109 Boyle M P, Noschese M L, Watts S L, Davis M E, Stenner S E, Lechtzin N. Failure of high-dose ergocalciferol to correct vitamin D deficiency in adults with cystic fibrosis. Am J Respir Crit Care Med. 2005; 172 212-217
- 110 Green D, Carson K, Leonard A et al.. Current treatment recommendations for correcting vitamin D deficiency in pediatric patients with cystic fibrosis are inadequate. J Pediatr. 2008; 153 554-559
- 111 Brown S A, Ontjes D A, Lester G E et al.. Short-term calcitriol administration improves calcium homeostasis in adults with cystic fibrosis. Osteoporos Int. 2003; 14 442-449
- 112 Khazai N B, Judd S, Jeng L et al.. Treatment and prevention of vitamin D insufficiency in cystic fibrosis patients: comparative efficacy of ergocalciferol, cholecalciferol and UV light. J Clin Endocrinol Metab. 2009; 94 2037-2043
- 113 Gronowitz E, Larkö O, Gilljam M et al.. Ultraviolet B radiation improves serum levels of vitamin D in patients with cystic fibrosis. Acta Paediatr. 2005; 94 547-552
- 114 Chandra P, Wolfenden L L, Ziegler T R et al.. Treatment of vitamin D deficiency with UV light in patients with malabsorption syndromes: a case series. Photodermatol Photoimmunol Photomed. 2007; 23 179-185
- 115 Bachrach L K. Acquisition of optimal bone mass in childhood and adolescence. Trends Endocrinol Metab. 2001; 12 22-28
- 116 Beker L T, Ahrens R A, Fink R J et al.. Effect of vitamin K1 supplementation on vitamin K status in cystic fibrosis patients. J Pediatr Gastroenterol Nutr. 1997; 24 512-517
- 117 Nicolaidou P, Stavrinadis I, Loukou I et al.. The effect of vitamin K supplementation on biochemical markers of bone formation in children and adolescents with cystic fibrosis. Eur J Pediatr. 2006; 165 540-545
- 118 Landon C, Rosenfeld R G. Short stature and pubertal delay in male adolescents with cystic fibrosis: androgen treatment. Am J Dis Child. 1984; 138 388-391
- 119 Rosen C J. Clinical practice: postmenopausal osteoporosis. N Engl J Med. 2005; 353 595-603
- 120 Haworth C S, Selby P L, Adams J E, Mawer E B, Horrocks A W, Webb A K. Effect of intravenous pamidronate on bone mineral density in adults with cystic fibrosis. Thorax. 2001; 56 314-316
- 121 Haworth C S, Selby P L, Webb A K, Mawer E B, Adams J E, Freemont T J. Severe bone pain after intravenous pamidronate in adult patients with cystic fibrosis. Lancet. 1998; 352 1753-1754
- 122 Aris R M, Lester G E, Renner J B et al.. Efficacy of pamidronate for osteoporosis in patients with cystic fibrosis following lung transplantation. Am J Respir Crit Care Med. 2000; 162(3 Pt 1) 941-946
- 123 Chapman I, Greville H, Ebeling P R et al.. Intravenous zoledronate improves bone density in adults with cystic fibrosis (CF). Clin Endocrinol (Oxf). 2009; 70 838-846
- 124 Boyle M P, Lechtzin N, Watt S. Zoledronate therapy for decreased bone density in adults with cystic fibrosis. Pediatr Pulmonol. 2005; (S28) 458
- 125 Aris R, Lester G, Ontjes D. Treatment of bone disease in cystic fibrosis. Curr Opin Pulm Med. 2004; 10 524-530
- 126 Aris R M, Lester G E, Caminiti M et al.. Efficacy of alendronate in adults with cystic fibrosis with low bone density. Am J Respir Crit Care Med. 2004; 169 77-82
- 127 Cawood T J, McKenna M J, Gallagher C G et al.. Oral bisphosphonates improve bone mineral density in adults with cystic fibrosis. Ir Med J. 2005; 98 270-273
- 128 Papaioannou A, Kennedy C C, Freitag A et al.. Alendronate once weekly for the prevention and treatment of bone loss in Canadian adult cystic fibrosis patients (CFOS trial). Chest. 2008; 134 794-800
- 129 Hardin D S, Ellis K J, Dyson M, Rice J, McConnell R, Seilheimer D K. Growth hormone improves clinical status in prepubertal children with cystic fibrosis: results of a randomized controlled trial. J Pediatr. 2001; 139 636-642
- 130 Hardin D S, Stratton R, Kramer J C, Reyes de la Rocha S, Govaerts K, Wilson D P. Growth hormone improves weight velocity and height velocity in prepubertal children with cystic fibrosis. Horm Metab Res. 1998; 30 636-641
- 131 Holmes S J, Shalet S M. Role of growth hormone and sex steroids in achieving and maintaining normal bone mass. Horm Res. 1996; 45 86-93
- 132 Saggese G, Baroncelli G I, Bertelloni S, Barsanti S. The effect of long-term growth hormone (GH) treatment on bone mineral density in children with GH deficiency: role of GH in the attainment of peak bone mass. J Clin Endocrinol Metab. 1996; 81 3077-3083
- 133 Hardin D S, Ahn C, Prestidge C, Seilheimer D K, Ellis K J. Growth hormone improves bone mineral content in children with cystic fibrosis. J Pediatr Endocrinol Metab. 2005; 18 589-595
- 134 Hardin D S, Adams-Huet B, Brown D et al.. Growth hormone treatment improves growth and clinical status in prepubertal children with cystic fibrosis: results of a multicenter randomized controlled trial. J Clin Endocrinol Metab. 2006; 91 4925-4929
- 135 Hardin D S, Ferkol T, Ahn C et al.. A retrospective study of growth hormone use in adolescents with cystic fibrosis. Clin Endocrinol (Oxf). 2005; 62 560-566
- 136 Cosman F. Parathyroid hormone treatment for osteoporosis. Curr Opin Endocrinol Diabetes Obes. 2008; 15 495-501
- 137 Body J J. Zoledronic acid: an advance in tumour bone disease therapy and a new hope for osteoporosis. Expert Opin Pharmacother. 2003; 4 567-580
- 138 Saag K G, Shane E, Boonen S et al.. Teriparatide or alendronate in glucocorticoid-induced osteoporosis. N Engl J Med. 2007; 357 2028-2039
- 139 Langdahl B L, Marin F, Shane E et al.. Teriparatide versus alendronate for treating glucocorticoid-induced osteoporosis: an analysis by gender and menopausal status. Osteoporos Int. 2009; , Apr 7. [Epub ahead of print]
John R McArdleM.D.
Section of Pulmonary and Critical Care Medicine, Yale University School of Medicine
333 Cedar St., P.O. Box 208057, New Haven, CT 06520-8057
Email: john.mcardle@yale.edu