Download PDF
Semin Respir Crit Care Med 2019; 40(06): 810-824
DOI: 10.1055/s-0039-1697917
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Endocrine Complications of Cystic Fibrosis: A Multisystem Disease of the Endocrine Organs

Katie Larson Ode
1   Division of Pediatric Endocrinology and Diabetes, Department of Pediatrics, University of Iowa Stead Family Children's Hospital, Iowa City, Iowa
,
Christine L. Chan
2   Division of Pediatric Endocrinology, Department of Pediatrics, Colorado Children's Hospital, University of Colorado School of Medicine, Aurora, Colorado
,
Andrea Granandos
3   Division of Endocrinology and Metabolism, Department of Pediatrics, Children's Washington University School of Medicine in St. Louis, St. Louis, Missouri
,
Melissa Putman
4   Division of Endocrinology, Boston Children's Hospital, Boston, Massachusetts
5   Division of Endocrinology, Massachusetts General Hospital, Boston, Massachusetts
,
Amir Moheet
6   Department of Medicine, University of Minnesota, Minneapolis, Minnesota
› Author Affiliations
Further Information

Publication History

Publication Date:
03 November 2019 (online)

    Permissions and Reprints

Abstract

Cystic fibrosis (CF) is one of the most common life-limiting genetic disorders. Although CF is typically considered primarily as a pulmonary disease, the CF conductance transmembrane regulator is present throughout the body. From an endocrine perspective, this multisystem disease manifests primarily in the pancreas as a unique form of diabetes (CF-related diabetes mellitus), as bone disease, and as reproductive health issues in people with CF. These complications have become ever more concerning to people with CF as treatment for pulmonary disease improves and lifespans lengthen, increasing the impact of nonpulmonary complications. Our understanding of the management of these concerns continues to evolve, and, although there are some effective treatments, there is great opportunity for continued investigation into the pathophysiology of the endocrine complications of CF and their treatment.

Keywords

cystic fibrosis-related diabetes - cystic fibrosis - insulin - cystic fibrosis bone disease - hypogonadism - infertility - continuous glucose monitoring - bone mineral density
 

  • References

  • 1 Moheet A, Moran A. CF-related diabetes: containing the metabolic miscreant of cystic fibrosis. Pediatr Pulmonol 2017; 52 (S48): S37-S43
    CrossrefPubMedGoogle Scholar
  • 2 Aris RM, Merkel PA, Bachrach LK. , et al. Guide to bone health and disease in cystic fibrosis. J Clin Endocrinol Metab 2005; 90 (03) 1888-1896
    CrossrefPubMedGoogle Scholar
  • 3 Sueblinvong V, Whittaker LA. Fertility and pregnancy: common concerns of the aging cystic fibrosis population. Clin Chest Med 2007; 28 (02) 433-443
    CrossrefPubMedGoogle Scholar
  • 4 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 (09) 1626-1631
    CrossrefPubMedGoogle Scholar
  • 5 Marshall BC, Butler SM, Stoddard M, Moran AM, Liou TG, Morgan WJ. Epidemiology of cystic fibrosis-related diabetes. J Pediatr 2005; 146 (05) 681-687
    CrossrefPubMedGoogle Scholar
  • 6 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 (02) 194-200
    CrossrefPubMedGoogle Scholar
  • 7 Blackman SM, Commander CW, Watson C. , et al. Genetic modifiers of cystic fibrosis-related diabetes. Diabetes 2013; 62 (10) 3627-3635
    CrossrefPubMedGoogle Scholar
  • 8 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 (09) 1858-1865
    CrossrefPubMedGoogle Scholar
  • 9 Adler AI, Shine BSF, 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 (09) 1789-1794
    CrossrefPubMedGoogle Scholar
  • 10 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 (06) 384-388
    CrossrefPubMedGoogle Scholar
  • 11 Moran A, Becker D, Casella SJ. , et al; CFRD Consensus Conference Committee. Epidemiology, pathophysiology, and prognostic implications of cystic fibrosis-related diabetes: a technical review. Diabetes Care 2010; 33 (12) 2677-2683
    CrossrefPubMedGoogle Scholar
  • 12 Finkelstein SM, Wielinski CL, Elliott GR. , et al. Diabetes mellitus associated with cystic fibrosis. J Pediatr 1988; 112 (03) 373-377
    CrossrefPubMedGoogle Scholar
  • 13 Lanng S, Thorsteinsson B, Røder ME, Nerup J, Koch C. Insulin sensitivity and insulin clearance in cystic fibrosis patients with normal and diabetic glucose tolerance. Clin Endocrinol (Oxf) 1994; 41 (02) 217-223
    CrossrefPubMedGoogle Scholar
  • 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 (09) 684-687
    CrossrefPubMedGoogle Scholar
  • 15 Moran A, Pekow P, Grover P. , et al; Cystic Fibrosis Related Diabetes Therapy Study Group. 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
    CrossrefPubMedGoogle Scholar
  • 16 Yi Y, Norris AW, Wang K. , et al. Abnormal glucose tolerance in infants and young children with cystic fibrosis. Am J Respir Crit Care Med 2016; 194 (08) 974-980
    CrossrefPubMedGoogle Scholar
  • 17 Ode KL, Frohnert B, Laguna T. , et al. Oral glucose tolerance testing in children with cystic fibrosis. Pediatr Diabetes 2010; 11 (07) 487-492
    CrossrefPubMedGoogle Scholar
  • 18 Gottlieb PA, Yu L, Babu S. , et al. No relation between cystic fibrosis-related diabetes and type 1 diabetes autoimmunity. Diabetes Care 2012; 35 (08) e57
    CrossrefPubMedGoogle Scholar
  • 19 Konrad K, Scheuing N, Badenhoop K. , et al. Cystic fibrosis-related diabetes compared with type 1 and type 2 diabetes in adults. Diabetes Metab Res Rev 2013; 29 (07) 568-575
    PubMedGoogle Scholar
  • 20 Kelly A, Moran A. Update on cystic fibrosis-related diabetes. J Cyst Fibros 2013; 12 (04) 318-331
    CrossrefPubMedGoogle Scholar
  • 21 Arrigo T, Cucinotta D, Conti Nibali S. , et al. Longitudinal evaluation of glucose tolerance and insulin secretion in non-diabetic children and adolescents with cystic fibrosis: results of a two-year follow-up. Acta Paediatr 1993; 82 (03) 249-253
    CrossrefPubMedGoogle Scholar
  • 22 Couce M, O'Brien TD, Moran A, Roche PC, Butler PC. Diabetes mellitus in cystic fibrosis is characterized by islet amyloidosis. J Clin Endocrinol Metab 1996; 81 (03) 1267-1272
    PubMedGoogle Scholar
  • 23 Kelly A, De Leon DD, Sheikh S. , et al. Islet hormone and incretin secretion in cystic fibrosis after four months of ivacaftor therapy. Am J Respir Crit Care Med 2019; 199 (03) 342-351
    CrossrefPubMedGoogle Scholar
  • 24 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 (06) 417-421
    CrossrefPubMedGoogle Scholar
  • 25 Guo JH, Chen H, Ruan YC. , et al. Glucose-induced electrical activities and insulin secretion in pancreatic islet β-cells are modulated by CFTR. Nat Commun 2014; 5: 4420
    CrossrefPubMedGoogle Scholar
  • 26 Sun X, Yi Y, Xie W. , et al. CFTR influences beta cell function and insulin secretion through non-cell autonomous exocrine-derived factors. Endocrinology 2017; 158 (10) 3325-3338
    CrossrefPubMedGoogle Scholar
  • 27 Boom A, Lybaert P, Pollet J-F. , et al. Expression and localization of cystic fibrosis transmembrane conductance regulator in the rat endocrine pancreas. Endocrine 2007; 32 (02) 197-205
    CrossrefPubMedGoogle Scholar
  • 28 Rowe SM, Heltshe SL, Gonska T. , et al; GOAL Investigators of the Cystic Fibrosis Foundation Therapeutics Development Network. Clinical mechanism of the cystic fibrosis transmembrane conductance regulator potentiator ivacaftor in G551D-mediated cystic fibrosis. Am J Respir Crit Care Med 2014; 190 (02) 175-184
    CrossrefPubMedGoogle Scholar
  • 29 Hisert KB, Heltshe SL, Pope C. , et al. Restoring cystic fibrosis transmembrane conductance regulator function reduces airway bacteria and inflammation in people with cystic fibrosis and chronic lung infections. Am J Respir Crit Care Med 2017; 195 (12) 1617-1628
    CrossrefPubMedGoogle Scholar
  • 30 Edlund A, Pedersen MG, Lindqvist A, Wierup N, Flodström-Tullberg M, Eliasson L. CFTR is involved in the regulation of glucagon secretion in human and rodent alpha cells. Sci Rep 2017; 7 (01) 90
    CrossrefPubMedGoogle Scholar
  • 31 Moran A, Diem P, Klein DJ, Levitt MD, Robertson RP. Pancreatic endocrine function in cystic fibrosis. J Pediatr 1991; 118 (05) 715-723
    CrossrefPubMedGoogle Scholar
  • 32 Moran A, Milla C, Ducret R, Nair KS. Protein metabolism in clinically stable adult cystic fibrosis patients with abnormal glucose tolerance. Diabetes 2001; 50 (06) 1336-1343
    CrossrefPubMedGoogle Scholar
  • 33 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 (02) 131-142
    CrossrefPubMedGoogle Scholar
  • 34 Lanng S, Thorsteinsson B, Røder 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 (Copenh) 1993; 128 (03) 207-214
    PubMedGoogle Scholar
  • 35 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 (03) 253-258
    CrossrefPubMedGoogle Scholar
  • 36 Hardin DS, 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 (03) 567-573
    CrossrefPubMedGoogle Scholar
  • 37 Yki-Järvinen H, Sammalkorpi K, Koivisto VA, Nikkilä EA. Severity, duration, and mechanisms of insulin resistance during acute infections. J Clin Endocrinol Metab 1989; 69 (02) 317-323
    CrossrefPubMedGoogle Scholar
  • 38 Levy E, Gurbindo C, Lacaille F, Paradis K, Thibault L, Seidman E. Circulating tumor necrosis factor-α levels and lipid abnormalities in patients with cystic fibrosis. Pediatr Res 1993; 34 (02) 162-166
    CrossrefPubMedGoogle Scholar
  • 39 Colomba J, Boudreau V, Lehoux-Dubois C. , et al. The main mechanism associated with progression of glucose intolerance in older patients with cystic fibrosis is insulin resistance and not reduced insulin secretion capacity. J Cyst Fibros 2019; 18 (04) 551-556
    CrossrefPubMedGoogle Scholar
  • 40 Hull RL, Gibson RL, McNamara S. , et al. Islet interleukin-1β immunoreactivity is an early feature of cystic fibrosis that may contribute to β-cell failure. Diabetes Care 2018; 41 (04) 823-830
    CrossrefPubMedGoogle Scholar
  • 41 Hart NJ, Aramandla R, Poffenberger G. , et al. Cystic fibrosis-related diabetes is caused by islet loss and inflammation. JCI Insight 2018; 3 (08) 3
    PubMedGoogle Scholar
  • 42 Bogdani M, Blackman SM, Ridaura C, Bellocq J-P, Powers AC, Aguilar-Bryan L. Structural abnormalities in islets from very young children with cystic fibrosis may contribute to cystic fibrosis-related diabetes. Sci Rep 2017; 7 (01) 17231
    CrossrefPubMedGoogle Scholar
  • 43 Clark A, Wells CA, Buley ID. , et al. Islet amyloid, increased A-cells, reduced B-cells and exocrine fibrosis: quantitative changes in the pancreas in type 2 diabetes. Diabetes Res 1988; 9 (04) 151-159
    PubMedGoogle Scholar
  • 44 Westwell-Roper C, Dai DL, Soukhatcheva G. , et al. IL-1 blockade attenuates islet amyloid polypeptide-induced proinflammatory cytokine release and pancreatic islet graft dysfunction. J Immunol 2011; 187 (05) 2755-2765
    CrossrefPubMedGoogle Scholar
  • 45 Jin T. Current understanding on role of the Wnt signaling pathway effector TCF7L2 in glucose homeostasis. Endocr Rev 2016; 37 (03) 254-277
    CrossrefPubMedGoogle Scholar
  • 46 Derbel S, Doumaguet C, Hubert D. , et al. Calpain 10 and development of diabetes mellitus in cystic fibrosis. J Cyst Fibros 2006; 5 (01) 47-51
    CrossrefPubMedGoogle Scholar
  • 47 Horowitz M, Edelbroek MAL, Wishart JM, Straathof JW. Relationship between oral glucose tolerance and gastric emptying in normal healthy subjects. Diabetologia 1993; 36 (09) 857-862
    CrossrefPubMedGoogle Scholar
  • 48 Wu T, Rayner CK, Horowitz M. Incretins. Handb Exp Pharmacol 2016; 233: 137-171
    PubMedGoogle Scholar
  • 49 Kuo P, Stevens JE, Russo A. , et al. Gastric emptying, incretin hormone secretion, and postprandial glycemia in cystic fibrosis--effects of pancreatic enzyme supplementation. J Clin Endocrinol Metab 2011; 96 (05) E851-E855
    CrossrefPubMedGoogle Scholar
  • 50 Cucinotta D, De Luca F, Arrigo T. , et al. First-phase insulin response to intravenous glucose in cystic fibrosis patients with different degrees of glucose tolerance. J Pediatr Endocrinol Metab 1994; 7 (01) 13-17
    PubMedGoogle Scholar
  • 51 Geyer MC, Sullivan T, Tai A. , et al. Exenatide corrects postprandial hyperglycaemia in young people with cystic fibrosis and impaired glucose tolerance: a randomized crossover trial. Diabetes Obes Metab 2019; 21 (03) 700-704
    CrossrefPubMedGoogle Scholar
  • 52 Perano S, Rayner CK, Couper J, Martin J, Horowitz M. Cystic fibrosis related diabetes--a new perspective on the optimal management of postprandial glycemia. J Diabetes Complications 2014; 28 (06) 904-911
    CrossrefPubMedGoogle Scholar
  • 53 Moran A, Brunzell C, Cohen RC. , et al; CFRD Guidelines Committee. 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
    CrossrefPubMedGoogle Scholar
  • 54 Moran A, Pillay K, Becker DJ, Acerini CL. ; International Society for Pediatric and Adolescent Diabetes. ISPAD Clinical Practice Consensus guidelines 2014. Management of cystic fibrosis-related diabetes in children and adolescents. Pediatr Diabetes 2014; 15 (Suppl. 20) 65-76
    CrossrefPubMedGoogle Scholar
  • 55 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
    CrossrefPubMedGoogle Scholar
  • 56 Brodsky J, Dougherty S, Makani R, 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 (02) 292-295
    CrossrefPubMedGoogle Scholar
  • 57 Hameed S, Morton JR, Jaffé A. , et al. Early glucose abnormalities in cystic fibrosis are preceded by poor weight gain. Diabetes Care 2010; 33 (02) 221-226
    CrossrefPubMedGoogle Scholar
  • 58 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 (01) 53-59
    CrossrefPubMedGoogle Scholar
  • 59 Merjaneh L, He Q, Long Q, Phillips LS, Stecenko AA. Disposition index identifies defective beta-cell function in cystic fibrosis subjects with normal glucose tolerance. J Cyst Fibros 2015; 14 (01) 135-141
    CrossrefPubMedGoogle Scholar
  • 60 Chan CLPL, Vigers T, Zemanick ET, Zeitler PS, Sagel SD, Nadeau KJ. Continuous glucose monitoring reveals glucose abnormalities in CF youth despite normal OGTT. Paper presented at: North American Cystic Fibrosis Conference; 2015; Phoenix, AZ
    PubMedGoogle Scholar
  • 61 Ode KL, Moran A. New insights into cystic fibrosis-related diabetes in children. Lancet Diabetes Endocrinol 2013; 1 (01) 52-58
    CrossrefPubMedGoogle Scholar
  • 62 2014 Annual Data Report - Cystic Fibrosis Foundation Patient Registry. Bethesda, MD: Cystic Fibrosis Foundation; 2015
    PubMedGoogle Scholar
  • 63 Scheuing N, Berger G, Bergis D. , et al; German/Austrian Diabetes Prospective Documentation (DPV) Initiative. Adherence to clinical care guidelines for cystic fibrosis-related diabetes in 659 German/Austrian patients. J Cyst Fibros 2014; 13 (06) 730-736
    CrossrefPubMedGoogle Scholar
  • 64 Frohnert BI, Ode KL, Moran A. , et al. Impaired fasting glucose in cystic fibrosis. Diabetes Care 2010; 33 (12) 2660-2664
    CrossrefPubMedGoogle Scholar
  • 65 Holl RW, Buck C, Babka C, Wolf A, Thon A. HbA1c is not recommended as a screening test for diabetes in cystic fibrosis. Diabetes Care 2000; 23 (01) 126
    PubMedGoogle Scholar
  • 66 Chan CL, Hope E, Thurston J. , et al. Hemoglobin A1c accurately predicts continuous glucose monitoring-derived average glucose in youth and young adults with cystic fibrosis. Diabetes Care 2018; 41 (07) 1406-1413
    CrossrefPubMedGoogle Scholar
  • 67 Olson DE, Rhee MK, Herrick K, Ziemer DC, Twombly JG, Phillips LS. Screening for diabetes and pre-diabetes with proposed A1C-based diagnostic criteria. Diabetes Care 2010; 33 (10) 2184-2189
    CrossrefPubMedGoogle Scholar
  • 68 Burgess JC, Bridges N, Banya W. , et al. HbA1c as a screening tool for cystic fibrosis related diabetes. J Cyst Fibros 2016; 15 (02) 251-257
    CrossrefPubMedGoogle Scholar
  • 69 Boudreau V, Coriati A, Desjardins K, Rabasa-Lhoret R. Glycated hemoglobin cannot yet be proposed as a screening tool for cystic fibrosis related diabetes. J Cyst Fibros 2016; 15 (02) 258-260
    CrossrefPubMedGoogle Scholar
  • 70 Lam GY, Doll-Shankaruk M, Dayton J. , et al. The use of fructosamine in cystic fibrosis-related diabetes (CFRD) screening. J Cyst Fibros 2018; 17 (01) 121-124
    CrossrefPubMedGoogle Scholar
  • 71 Kinnaird KE, Sauerwein TJ. Lack of correlation between 1,5-anhydroglucitol assay and oral glucose tolerance test in patients with cystic fibrosis. Endocr Pract 2010; 16 (02) 167-170
    CrossrefPubMedGoogle Scholar
  • 72 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 (06) 1020-1022
    CrossrefPubMedGoogle Scholar
  • 73 Dobson L, Sheldon CD, Hattersley AT. Conventional measures underestimate glycaemia in cystic fibrosis patients. Diabet Med 2004; 21 (07) 691-696
    CrossrefPubMedGoogle Scholar
  • 74 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 (02) 109-116
    PubMedGoogle Scholar
  • 75 Chan CL, Vigers T, Pyle L, Zeitler PS, Sagel SD, Nadeau KJ. Continuous glucose monitoring abnormalities in cystic fibrosis youth correlate with pulmonary function decline. J Cyst Fibros 2018; 17 (06) 783-790
    CrossrefPubMedGoogle Scholar
  • 76 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 (07) 502-506
    Article in Thieme ConnectPubMedGoogle Scholar
  • 77 Beck RW, Riddlesworth T, Ruedy K. , et al; DIAMOND Study Group. Effect of continuous glucose monitoring on glycemic control in adults with type 1 diabetes using insulin injections: the DIAMOND randomized clinical trial. JAMA 2017; 317 (04) 371-378
    CrossrefPubMedGoogle Scholar
  • 78 Beck RW, Riddlesworth TD, Ruedy K. , et al; DIAMOND Study Group. Continuous glucose monitoring versus usual care in patients with type 2 diabetes receiving multiple daily insulin injections: a randomized trial. Ann Intern Med 2017; 167 (06) 365-374
    CrossrefPubMedGoogle Scholar
  • 79 Rachmiel M, Landau Z, Boaz M. , et al. The use of continuous glucose monitoring systems in a pediatric population with type 1 diabetes mellitus in real-life settings: the AWeSoMe Study Group experience. Acta Diabetol 2015; 52 (02) 323-329
    CrossrefPubMedGoogle Scholar
  • 80 Juvenile Diabetes Research Foundation Continuous Glucose Monitoring Study Group. Effectiveness of continuous glucose monitoring in a clinical care environment: evidence from the Juvenile Diabetes Research Foundation continuous glucose monitoring (JDRF-CGM) trial. Diabetes Care 2010; 33 (01) 17-22
    CrossrefPubMedGoogle Scholar
  • 81 Scheuing N, Badenhoop K, Borkenstein M. , et al; German/Austrian Diabetes Prospective Documentation Initiative. Why is insulin pump treatment rarely used in adolescents and young adults with cystic fibrosis-related diabetes?. Pediatr Diabetes 2015; 16 (01) 10-15
    CrossrefPubMedGoogle Scholar
  • 82 Frost F, Dyce P, Nazareth D, Malone V, Walshaw MJ. Continuous glucose monitoring guided insulin therapy is associated with improved clinical outcomes in cystic fibrosis-related diabetes. J Cyst Fibros 2018; 17 (06) 798-803
    CrossrefPubMedGoogle Scholar
  • 83 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 (02) 101-109
    CrossrefPubMedGoogle Scholar
  • 84 Wood DM, Brennan AL, Philips BJ, Baker EH. Effect of hyperglycaemia on glucose concentration of human nasal secretions. Clin Sci (Lond) 2004; 106 (05) 527-533
    CrossrefPubMedGoogle Scholar
  • 85 Adler AI, Shine B, Haworth C, Leelarathna L, Bilton D. Hyperglycemia and death in cystic fibrosis-related diabetes. Diabetes Care 2011; 34 (07) 1577-1578
    CrossrefPubMedGoogle Scholar
  • 86 Chamnan P, Shine BS, Haworth CS, Bilton D, Adler AI. Diabetes as a determinant of mortality in cystic fibrosis. Diabetes Care 2010; 33 (02) 311-316
    CrossrefPubMedGoogle Scholar
  • 87 Birch L, Lithander FE, Hewer SL, Harriman K, Hamilton-Shield J, Perry R. Dietary interventions for managing glucose abnormalities in cystic fibrosis: a systematic review protocol. Syst Rev 2018; 7 (01) 98
    CrossrefPubMedGoogle Scholar
  • 88 Solomon MP, Wilson DC, Corey M. , et al. Glucose intolerance in children with cystic fibrosis. J Pediatr 2003; 142 (02) 128-132
    CrossrefPubMedGoogle Scholar
  • 89 Soave D, Miller MR, Keenan K. , et al. Evidence for a causal relationship between early exocrine pancreatic disease and cystic fibrosis-related diabetes: a Mendelian randomization study. Diabetes 2014; 63 (06) 2114-2119
    CrossrefPubMedGoogle Scholar
  • 90 Konstan MW, Butler SM, Wohl ME. , et al; Investigators and Coordinators of the Epidemiologic Study of Cystic Fibrosis. Growth and nutritional indexes in early life predict pulmonary function in cystic fibrosis. J Pediatr 2003; 142 (06) 624-630
    CrossrefPubMedGoogle Scholar
  • 91 Yen EH, Quinton H, Borowitz D. Better nutritional status in early childhood is associated with improved clinical outcomes and survival in patients with cystic fibrosis. J Pediatr 2013; 162 (03) 530.e1-535.e1
    PubMedGoogle Scholar
  • 92 Corey M, McLaughlin FJ, Williams M, Levison H. A comparison of survival, growth, and pulmonary function in patients with cystic fibrosis in Boston and Toronto. J Clin Epidemiol 1988; 41 (06) 583-591
    CrossrefPubMedGoogle Scholar
  • 93 Zemel BS, Jawad AF, FitzSimmons S, Stallings VA. Longitudinal relationship among growth, nutritional status, and pulmonary function in children with cystic fibrosis: analysis of the Cystic Fibrosis Foundation National CF Patient Registry. J Pediatr 2000; 137 (03) 374-380
    CrossrefPubMedGoogle Scholar
  • 94 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 (03) 221-226
    CrossrefPubMedGoogle Scholar
  • 95 Battezzati A, Mari A, Zazzeron 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 (01) 69-76
    CrossrefPubMedGoogle Scholar
  • 96 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 (03) 246-253
    PubMedGoogle Scholar
  • 97 Hardin DS, LeBlanc A, Para L, Seilheimer DK. Hepatic insulin resistance and defects in substrate utilization in cystic fibrosis. Diabetes 1999; 48 (05) 1082-1087
    CrossrefPubMedGoogle Scholar
  • 98 Onady GM, Stolfi A. Insulin and oral agents for managing cystic fibrosis-related diabetes. Cochrane Database Syst Rev 2005; (03) CD004730
    PubMedGoogle Scholar
  • 99 Moheet A, Moran A. Pharmacological management of cystic fibrosis related diabetes. Expert Rev Clin Pharmacol 2018; 11 (02) 185-191
    CrossrefPubMedGoogle Scholar
  • 100 Alicandro G, Battezzati PM, Battezzati A. , et al. Insulin secretion, nutritional status and respiratory function in cystic fibrosis patients with normal glucose tolerance. Clin Nutr 2012; 31 (01) 118-123
    CrossrefPubMedGoogle Scholar
  • 101 Rasouli N, Seggelke S, Gibbs J. , et al. Cystic fibrosis-related diabetes in adults: inpatient management of 121 patients during 410 admissions. J Diabetes Sci Technol 2012; 6 (05) 1038-1044
    CrossrefPubMedGoogle Scholar
  • 102 Grover P, Thomas W, Moran A. Glargine versus NPH insulin in cystic fibrosis related diabetes. J Cyst Fibros 2008; 7 (02) 134-136
    CrossrefPubMedGoogle Scholar
  • 103 Hardin DS, Rice J, Rice M, Rosenblatt R. Use of the insulin pump in treat cystic fibrosis related diabetes. J Cyst Fibros 2009; 8 (03) 174-178
    CrossrefPubMedGoogle Scholar
  • 104 Moran A, Pillay K, Becker D, Granados A, Hameed S, Acerini CL. ISPAD Clinical Practice Consensus Guidelines 2018: management of cystic fibrosis-related diabetes in children and adolescents. Pediatr Diabetes 2018; 19 (Suppl. 27) 64-74
    CrossrefPubMedGoogle Scholar
  • 105 Scheuing N, Thon A, Konrad K. , et al; German/Austrian Diabetes Prospective Documentation Initiative and the BMBF Competence Network Diabetes Mellitus. Carbohydrate intake and insulin requirement in children, adolescents and young adults with cystic fibrosis-related diabetes: A multicenter comparison to type 1 diabetes. Clin Nutr 2015; 34 (04) 732-738
    CrossrefPubMedGoogle Scholar
  • 106 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 (04) 295-298
    CrossrefPubMedGoogle Scholar
  • 107 Widger J, Oliver MR, O'Connell M, Cameron FJ, Ranganathan S, Robinson PJ. Glucose tolerance during pulmonary exacerbations in children with cystic fibrosis. PLoS One 2012; 7 (09) e44844
    CrossrefPubMedGoogle Scholar
  • 108 Hollander FM, de Roos NM, Belle van Meerkerk G, Teding van Berkhout F, Heijerman HGM, van de Graaf EA. Body weight and body mass index in patients with end-stage cystic fibrosis stabilize after the start of enteral tube feeding. J Acad Nutr Diet 2017; 117 (11) 1808-1815
    CrossrefPubMedGoogle Scholar
  • 109 Koloušková S, Zemková D, Bartošová J. , et al. Low-dose insulin therapy in patients with cystic fibrosis and early-stage insulinopenia prevents deterioration of lung function: a 3-year prospective study. J Pediatr Endocrinol Metab 2011; 24 (7–8): 449-454
    PubMedGoogle Scholar
  • 110 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 (03) 162-167
    CrossrefPubMedGoogle Scholar
  • 111 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 (03) RC1-RC4
    CrossrefPubMedGoogle Scholar
  • 112 Hameed S, Morton JR, Field PI. , et al. Once daily insulin detemir in cystic fibrosis with insulin deficiency. Arch Dis Child 2012; 97 (05) 464-467
    CrossrefPubMedGoogle Scholar
  • 113 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 (05) 430-431
    CrossrefPubMedGoogle Scholar
  • 114 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 (02) 197-202
    CrossrefPubMedGoogle Scholar
  • 115 Ballmann M, Hubert D, Assael BM. , et al; CFRD Study Group. Repaglinide versus insulin for newly diagnosed diabetes in patients with cystic fibrosis: a multicentre, open-label, randomised trial. Lancet Diabetes Endocrinol 2018; 6 (02) 114-121
    CrossrefPubMedGoogle Scholar
  • 116 Hillman M, Eriksson L, Mared L, Helgesson K, Landin-Olsson M. Reduced levels of active GLP-1 in patients with cystic fibrosis with and without diabetes mellitus. J Cyst Fibros 2012; 11 (02) 144-149
    CrossrefPubMedGoogle Scholar
  • 117 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 (07) 2486-2493
    CrossrefPubMedGoogle Scholar
  • 118 Norris AW, Ode KL, Merjaneh L. , et al. Survival in a bad neighborhood: pancreatic islets in cystic fibrosis. J Endocrinol 2019; 241 (01) R35-R50
    CrossrefPubMedGoogle Scholar
  • 119 Hayes Jr D, McCoy KS, Sheikh SI. Resolution of cystic fibrosis-related diabetes with ivacaftor therapy. Am J Respir Crit Care Med 2014; 190 (05) 590-591
    CrossrefPubMedGoogle Scholar
  • 120 Aris RM, Renner JB, Winders AD. , et al. Increased rate of fractures and severe kyphosis: sequelae of living into adulthood with cystic fibrosis. Ann Intern Med 1998; 128 (03) 186-193
    CrossrefPubMedGoogle Scholar
  • 121 Henderson RC, Specter BB. Kyphosis and fractures in children and young adults with cystic fibrosis. J Pediatr 1994; 125 (02) 208-212
    CrossrefPubMedGoogle Scholar
  • 122 Bianchi ML, Romano G, Saraifoger S, Costantini D, Limonta C, Colombo C. BMD and body composition in children and young patients affected by cystic fibrosis. J Bone Miner Res 2006; 21 (03) 388-396
    CrossrefPubMedGoogle Scholar
  • 123 Conway SP, Morton AM, Oldroyd B. , et al. Osteoporosis and osteopenia in adults and adolescents with cystic fibrosis: prevalence and associated factors. Thorax 2000; 55 (09) 798-804
    CrossrefPubMedGoogle Scholar
  • 124 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 (05) 1014-1020
    CrossrefPubMedGoogle Scholar
  • 125 Henderson RC, Madsen CD. Bone density in children and adolescents with cystic fibrosis. J Pediatr 1996; 128 (01) 28-34
    CrossrefPubMedGoogle Scholar
  • 126 Kelly A, Schall J, Stallings VA, Zemel BS. Trabecular and cortical bone deficits are present in children and adolescents with cystic fibrosis. Bone 2016; 90: 7-14
    CrossrefPubMedGoogle Scholar
  • 127 Paccou J, Zeboulon N, Combescure C, Gossec L, Cortet B. The prevalence of osteoporosis, osteopenia, and fractures among adults with cystic fibrosis: a systematic literature review with meta-analysis. Calcif Tissue Int 2010; 86 (01) 1-7
    CrossrefPubMedGoogle Scholar
  • 128 Grey AB, Ames RW, Matthews RD, Reid IR. Bone mineral density and body composition in adult patients with cystic fibrosis. Thorax 1993; 48 (06) 589-593
    CrossrefPubMedGoogle Scholar
  • 129 Haworth CS, Selby PL, Webb AK. , et al. Low bone mineral density in adults with cystic fibrosis. Thorax 1999; 54 (11) 961-967
    CrossrefPubMedGoogle Scholar
  • 130 Legroux-Gérot I, Leroy S, Prudhomme C. , et al. Bone loss in adults with cystic fibrosis: prevalence, associated factors, and usefulness of biological markers. Joint Bone Spine 2012; 79 (01) 73-77
    CrossrefPubMedGoogle Scholar
  • 131 Sheikh S, Gemma S, Patel A. Factors associated with low bone mineral density in patients with cystic fibrosis. J Bone Miner Metab 2015; 33 (02) 180-185
    CrossrefPubMedGoogle Scholar
  • 132 Putman MS, Milliren CE, Derrico N. , et al. Compromised bone microarchitecture and estimated bone strength in young adults with cystic fibrosis. J Clin Endocrinol Metab 2014; 99 (09) 3399-3407
    CrossrefPubMedGoogle Scholar
  • 133 Putman MS, Greenblatt LB, Sicilian L. , et al. Young adults with cystic fibrosis have altered trabecular microstructure by ITS-based morphological analysis. Osteoporos Int 2016; 27 (08) 2497-2505
    CrossrefPubMedGoogle Scholar
  • 134 Nishiyama KK, Agarwal S, Kepley A. , et al. Adults with cystic fibrosis have deficits in bone structure and strength at the distal tibia despite similar size and measuring standard and relative sites. Bone 2018; 107: 181-187
    CrossrefPubMedGoogle Scholar
  • 135 Gensburger D, Boutroy S, Chapurlat R. , et al. Reduced bone volumetric density and weak correlation between infection and bone markers in cystic fibrosis adult patients. Osteoporos Int 2016; 27 (09) 2803-2813
    CrossrefPubMedGoogle Scholar
  • 136 Rossini M, Del Marco A, Dal Santo F. , et al. Prevalence and correlates of vertebral fractures in adults with cystic fibrosis. Bone 2004; 35 (03) 771-776
    CrossrefPubMedGoogle Scholar
  • 137 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 (02) 539-544
    CrossrefPubMedGoogle Scholar
  • 138 Putman MS, Baker JF, Uluer A. , et al. Trends in bone mineral density in young adults with cystic fibrosis over a 15 year period. J Cyst Fibros 2015; 14 (04) 526-532
    CrossrefPubMedGoogle Scholar
  • 139 Rana M, Munns CF, Selvadurai H, Briody J, Craig ME. The impact of dysglycaemia on bone mineral accrual in young people with cystic fibrosis. Clin Endocrinol (Oxf) 2013; 78 (01) 36-42
    CrossrefPubMedGoogle Scholar
  • 140 Shead EF, Haworth CS, Barker H, Bilton D, Compston JE. Osteoclast function, bone turnover and inflammatory cytokines during infective exacerbations of cystic fibrosis. J Cyst Fibros 2010; 9 (02) 93-98
    CrossrefPubMedGoogle Scholar
  • 141 Haworth CS, Webb AK, Egan JJ. , et al. Bone histomorphometry in adult patients with cystic fibrosis. Chest 2000; 118 (02) 434-439
    CrossrefPubMedGoogle Scholar
  • 142 Aris RM, Ontjes DA, Buell HE. , et al. Abnormal bone turnover in cystic fibrosis adults. Osteoporos Int 2002; 13 (02) 151-157
    CrossrefPubMedGoogle Scholar
  • 143 Baroncelli GI, De Luca F, Magazzú G. , et al. Bone demineralization in cystic fibrosis: evidence of imbalance between bone formation and degradation. Pediatr Res 1997; 41 (03) 397-403
    CrossrefPubMedGoogle Scholar
  • 144 Shead EF, Haworth CS, Condliffe AM, McKeon DJ, Scott MA, Compston JE. Cystic fibrosis transmembrane conductance regulator (CFTR) is expressed in human bone. Thorax 2007; 62 (07) 650-651
    CrossrefPubMedGoogle Scholar
  • 145 Dif F, Marty C, Baudoin C, de Vernejoul MC, Levi G. Severe osteopenia in CFTR-null mice. Bone 2004; 35 (03) 595-603
    CrossrefPubMedGoogle Scholar
  • 146 Haston CK, Li W, Li A, Lafleur M, Henderson JE. Persistent osteopenia in adult cystic fibrosis transmembrane conductance regulator-deficient mice. Am J Respir Crit Care Med 2008; 177 (03) 309-315
    CrossrefPubMedGoogle Scholar
  • 147 Pashuck TD, Franz SE, Altman MK. , et al. Murine model for cystic fibrosis bone disease demonstrates osteopenia and sex-related differences in bone formation. Pediatr Res 2009; 65 (03) 311-316
    CrossrefPubMedGoogle Scholar
  • 148 Le Henaff C, Gimenez A, Haÿ E, Marty C, Marie P, Jacquot J. The F508del mutation in cystic fibrosis transmembrane conductance regulator gene impacts bone formation. Am J Pathol 2012; 180 (05) 2068-2075
    CrossrefPubMedGoogle Scholar
  • 149 Paradis J, Wilke M, Haston CK. Osteopenia in Cftr-deltaF508 mice. J Cyst Fibros 2010; 9 (04) 239-245
    CrossrefPubMedGoogle Scholar
  • 150 Velard F, Delion M, Le Henaff C. , et al. Cystic fibrosis and bone disease: defective osteoblast maturation with the F508del mutation in cystic fibrosis transmembrane conductance regulator. Am J Respir Crit Care Med 2014; 189 (06) 746-748
    CrossrefPubMedGoogle Scholar
  • 151 Delion M, Braux J, Jourdain ML. , et al. Overexpression of RANKL in osteoblasts: a possible mechanism of susceptibility to bone disease in cystic fibrosis. J Pathol 2016; 240 (01) 50-60
    CrossrefPubMedGoogle Scholar
  • 152 Sermet-Gaudelus I, Bianchi ML, Garabédian M. , et al. European cystic fibrosis bone mineralisation guidelines. J Cyst Fibros 2011; 10 (Suppl. 02) S16-S23
    PubMedGoogle Scholar
  • 153 Tangpricha V, Kelly A, Stephenson A. , et al; Cystic Fibrosis Foundation Vitamin D Evidence-Based Review Committee. An update on the screening, diagnosis, management, and treatment of vitamin D deficiency in individuals with cystic fibrosis: evidence-based recommendations from the Cystic Fibrosis Foundation. J Clin Endocrinol Metab 2012; 97 (04) 1082-1093
    CrossrefPubMedGoogle Scholar
  • 154 Gordon CM, Leonard MB, Zemel BS. ; International Society for Clinical Densitometry. 2013 Pediatric Position Development Conference: executive summary and reflections. J Clin Densitom 2014; 17 (02) 219-224
    CrossrefPubMedGoogle Scholar
  • 155 Stallings VA, Stark LJ, Robinson KA, Feranchak AP, Quinton H. ; Clinical Practice Guidelines on Growth and Nutrition Subcommittee; Ad Hoc Working Group. Evidence-based practice recommendations for nutrition-related management of children and adults with cystic fibrosis and pancreatic insufficiency: results of a systematic review. J Am Diet Assoc 2008; 108 (05) 832-839
    CrossrefPubMedGoogle Scholar
  • 156 Curhan GC, Willett WC, Speizer FE, Spiegelman D, Stampfer MJ. Comparison of dietary calcium with supplemental calcium and other nutrients as factors affecting the risk for kidney stones in women. Ann Intern Med 1997; 126 (07) 497-504
    PubMedGoogle Scholar
  • 157 Putman MS, Haagensen A, Neuringer I, Sicilian L. Celiac disease in patients with cystic fibrosis-related bone disease. Case Rep Endocrinol 2017; 2017: 2652403
    PubMedGoogle Scholar
  • 158 Zanchetta MB, Longobardi V, Bai JC. Bone and celiac disease. Curr Osteoporos Rep 2016; 14 (02) 43-48
    CrossrefPubMedGoogle Scholar
  • 159 Behre HM, Kliesch S, Leifke E, Link TM, Nieschlag E. Long-term effect of testosterone therapy on bone mineral density in hypogonadal men. J Clin Endocrinol Metab 1997; 82 (08) 2386-2390
    CrossrefPubMedGoogle Scholar
  • 160 Katznelson L, Finkelstein JS, Schoenfeld DA, Rosenthal DI, Anderson EJ, Klibanski A. Increase in bone density and lean body mass during testosterone administration in men with acquired hypogonadism. J Clin Endocrinol Metab 1996; 81 (12) 4358-4365
    PubMedGoogle Scholar
  • 161 Finkelstein JS, Klibanski A, Neer RM. , et al. Increases in bone density during treatment of men with idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab 1989; 69 (04) 776-783
    CrossrefPubMedGoogle Scholar
  • 162 Warren MP, Brooks-Gunn J, Fox RP. , et al. Persistent osteopenia in ballet dancers with amenorrhea and delayed menarche despite hormone therapy: a longitudinal study. Fertil Steril 2003; 80 (02) 398-404
    CrossrefPubMedGoogle Scholar
  • 163 Klibanski A, Biller BM, Schoenfeld DA, Herzog DB, Saxe VC. The effects of estrogen administration on trabecular bone loss in young women with anorexia nervosa. J Clin Endocrinol Metab 1995; 80 (03) 898-904
    PubMedGoogle Scholar
  • 164 Strokosch GR, Friedman AJ, Wu SC, Kamin M. Effects of an oral contraceptive (norgestimate/ethinyl estradiol) on bone mineral density in adolescent females with anorexia nervosa: a double-blind, placebo-controlled study. J Adolesc Health 2006; 39 (06) 819-827
    CrossrefPubMedGoogle Scholar
  • 165 Misra M, Katzman D, Miller KK. , et al. Physiologic estrogen replacement increases bone density in adolescent girls with anorexia nervosa. J Bone Miner Res 2011; 26 (10) 2430-2438
    CrossrefPubMedGoogle Scholar
  • 166 Aris RM, Lester GE, Renner JB. , 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
    CrossrefPubMedGoogle Scholar
  • 167 Aris RM, Lester GE, Caminiti M. , et al. Efficacy of alendronate in adults with cystic fibrosis with low bone density. Am J Respir Crit Care Med 2004; 169 (01) 77-82
    CrossrefPubMedGoogle Scholar
  • 168 Boyle MP, Lechtzin N, Watts S. Zoledronate therapy for decreased bone density in adults with cystic fibrosis. . (abstract). Pediatr Pulmonol 2005; 40 (S28): 353
    PubMedGoogle Scholar
  • 169 Haworth CS, Selby PL, Adams JE, Mawer EB, Horrocks AW, Webb AK. Effect of intravenous pamidronate on bone mineral density in adults with cystic fibrosis. Thorax 2001; 56 (04) 314-316
    CrossrefPubMedGoogle Scholar
  • 170 Papaioannou A, Kennedy CC, 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 (04) 794-800
    CrossrefPubMedGoogle Scholar
  • 171 Chapman I, Greville H, Ebeling PR. , et al. Intravenous zoledronate improves bone density in adults with cystic fibrosis (CF). Clin Endocrinol (Oxf) 2009; 70 (06) 838-846
    CrossrefPubMedGoogle Scholar
  • 172 Haworth CS, Sharples L, Hughes V. , et al. Multicentre trial of weekly risedronate on bone density in adults with cystic fibrosis. J Cyst Fibros 2011; 10 (06) 470-476
    CrossrefPubMedGoogle Scholar
  • 173 Bianchi ML, Colombo C, Assael BM. , et al. Treatment of low bone density in young people with cystic fibrosis: a multicentre, prospective, open-label observational study of calcium and calcifediol followed by a randomised placebo-controlled trial of alendronate. Lancet Respir Med 2013; 1 (05) 377-385
    CrossrefPubMedGoogle Scholar
  • 174 Conwell LS, Chang AB. Bisphosphonates for osteoporosis in people with cystic fibrosis. Cochrane Database Syst Rev 2014; (03) CD002010
    PubMedGoogle Scholar
  • 175 Eastell R, Rosen CJ, Black DM, Cheung AM, Murad MH, Shoback D. Pharmacological management of osteoporosis in postmenopausal women: an endocrine society* clinical practice guideline. J Clin Endocrinol Metab 2019; 104 (05) 1595-1622
    CrossrefPubMedGoogle Scholar
  • 176 Le Henaff C, Haÿ E, Velard F. , et al. Enhanced F508del-CFTR channel activity ameliorates bone pathology in murine cystic fibrosis. Am J Pathol 2014; 184 (04) 1132-1141
    CrossrefPubMedGoogle Scholar
  • 177 Sermet-Gaudelus I, Delion M, Durieu I, Jacquot J, Hubert D. Bone demineralization is improved by ivacaftor in patients with cystic fibrosis carrying the p.Gly551Asp mutation. J Cyst Fibros 2016; 15 (06) e67-e69
    CrossrefPubMedGoogle Scholar
  • 178 Velard F, Delion M, Lemaire F. , et al. Cystic fibrosis bone disease: is the CFTR corrector C18 an option for therapy?. Eur Respir J 2015; 45 (03) 845-848
    CrossrefPubMedGoogle Scholar
  • 179 McCallum TJ, Milunsky JM, Cunningham DL, Harris DH, Maher TA, Oates RD. Fertility in men with cystic fibrosis: an update on current surgical practices and outcomes. Chest 2000; 118 (04) 1059-1062
    CrossrefPubMedGoogle Scholar
  • 180 Taussig LM, Lobeck CC, di Sant'Agnese PA, Ackerman DR, Kattwinkel J. Fertility in males with cystic fibrosis. N Engl J Med 1972; 287 (12) 586-589
    CrossrefPubMedGoogle Scholar
  • 181 Kaplan E, Shwachman H, Perlmutter AD, Rule A, Khaw KT, Holsclaw DS. Reproductive failure in males with cystic fibrosis. N Engl J Med 1968; 279 (02) 65-69
    CrossrefPubMedGoogle Scholar
  • 182 Chillón M, Casals T, Mercier B. , et al. Mutations in the cystic fibrosis gene in patients with congenital absence of the vas deferens. N Engl J Med 1995; 332 (22) 1475-1480
    CrossrefPubMedGoogle Scholar
  • 183 Chen H, Ruan YC, Xu WM, Chen J, Chan HC. Regulation of male fertility by CFTR and implications in male infertility. Hum Reprod Update 2012; 18 (06) 703-713
    CrossrefPubMedGoogle Scholar
  • 184 Sokol RZ. Infertility in men with cystic fibrosis. Curr Opin Pulm Med 2001; 7 (06) 421-426
    CrossrefPubMedGoogle Scholar
  • 185 Donovan Jr DS, Papadopoulos A, Staron RB. , 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
    CrossrefPubMedGoogle Scholar
  • 186 Leifke E, Friemert M, Heilmann M. , et al. Sex steroids and body composition in men with cystic fibrosis. Eur J Endocrinol 2003; 148 (05) 551-557
    PubMedGoogle Scholar
  • 187 Blackman SM, Tangpricha V. Endocrine disorders in cystic fibrosis. Pediatr Clin North Am 2016; 63 (04) 699-708
    CrossrefPubMedGoogle Scholar
  • 188 Stead RJ, Hodson ME, Batten JC, Adams J, Jacobs HS. Amenorrhoea in cystic fibrosis. Clin Endocrinol (Oxf) 1987; 26 (02) 187-195
    CrossrefPubMedGoogle Scholar
  • 189 Johannesson M, Landgren BM, Csemiczky G, Hjelte L, Gottlieb C. Female patients with cystic fibrosis suffer from reproductive endocrinological disorders despite good clinical status. Hum Reprod 1998; 13 (08) 2092-2097
    CrossrefPubMedGoogle Scholar
  • 190 Shteinberg M, Lulu AB, Downey DG. , et al. Failure to conceive in women with CF is associated with pancreatic insufficiency and advancing age. J Cyst Fibros 2019; 18 (04) 525-529
    CrossrefPubMedGoogle Scholar
  • 191 Kopito LE, Kosasky HJ, Shwachman H. Water and electrolytes in cervical mucus from patients with cystic fibrosis. Fertil Steril 1973; 24 (07) 512-516
    CrossrefPubMedGoogle Scholar
  • 192 Schram CA, Stephenson AL, Hannam TG, Tullis E. Cystic fibrosis (cf) and ovarian reserve: a cross-sectional study examining serum anti-mullerian hormone (amh) in young women. J Cyst Fibros 2015; 14 (03) 398-402
    CrossrefPubMedGoogle Scholar
  • 193 Edenborough FP, Borgo G, Knoop C. , et al; European Cystic Fibrosis Society. Guidelines for the management of pregnancy in women with cystic fibrosis. J Cyst Fibros 2008; 7 (Suppl. 01) S2-S32
    PubMedGoogle Scholar