Adrenal suppression by inhaled corticosteroids in patients with asthma: A systematic review and quantitative analysis

Allergy and Asthma Proceedings

Volumn 37, Issue 1, 2016, Pages 9-17

  Kowalski, Marek L ^a   Wojciechowski, Piotr ^b   Dziewonska, Marta ^b   Rys, Przemyslaw ^b  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

^b HTA CONSULTING   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

BECLOMETASONE DIPROPIONATE; BUDESONIDE; CICLESONIDE; CORTICOSTEROID; FLUTICASONE PROPIONATE; HYDROCORTISONE; ANTIASTHMATIC AGENT;

ADRENAL SUPPRESSION; AGE; ARTICLE; ASTHMA; DOSE RESPONSE; DRUG EFFECT; DRUG FORMULATION; DRUG SYNTHESIS; HUMAN; HYDROCORTISONE URINE LEVEL; QUANTITATIVE ANALYSIS; SYSTEMATIC REVIEW; ADRENAL GLAND; BLOOD; DRUG EFFECTS; FEMALE; INHALATIONAL DRUG ADMINISTRATION; MALE; META ANALYSIS; METABOLISM; URINE;

ADMINISTRATION, INHALATION; ADRENAL CORTEX HORMONES; ADRENAL GLANDS; ANTI-ASTHMATIC AGENTS; ASTHMA; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HUMANS; HYDROCORTISONE; MALE;

EID: 85010934113     PISSN: 10885412     EISSN: 15396304     Source Type: Journal    
DOI: 10.2500/aap.2016.37.3912     Document Type: Article

References (83)

1. Global strategy for asthma management and prevention. Updated 2012. http://www.ginasthma.org/local/uploads/files/GINA-Report-March13.pdf. Date last accessed: June 1, 2004.
2. British Guideline on the management of asthma. http://www.sign.ac.uk/pdf/sign101.pdf. (Superseded by SIGN 141. Updated January 2012). Date last accessed: June 1, 2004.
3. Gulliver T, Morton R, and Eid N. Inhaled corticosteroids in children with asthma: Pharmacologic determinants of safety and efficacy and other clinical considerations. Paediatr Drugs 9: 185-194, 2007.
4. Derendorf H, and Hochhaus G. What is the best marker for inhaled corticosteroid safety? Allergy Asthma Proc 26: 89-93, 2005.
5. Harrison LI Local versus total systemic bioavailability of beclomethasone dipropionate CFC and HFA metered dose inhaler formulations. J Aerosol Med 15: 401-406, 2002.
6. Singh SB, Weinberger MM, Zimmerman MB, and Starner TDI. Growth of preschool age children receiving daily inhaled corticosteroids. Allergy Asthma Proc 34: 511-518, 2013.
7. Bartholow AK, Deshaies DM, Skoner JM, and Skoner DP. A critical review of the effects of inhaled corticosteroids on growth. Allergy Asthma Proc 34: 391-407, 2013.
8. Suissa S, Kezouh A, and Ernst P. Inhaled corticosteroids and the risks of diabetes onset and progression. Am J Med 123: 1001-1006, 2010.
9. Ernst P, and Suissa S. Systemic effects of inhaled corticosteroids. Curr Opin Pulm Med 18: 85-89, 2012.
10. Haughney J, Price D, Barnes NC, et al. Choosing inhaler devices for people with asthma: Current knowledge and outstanding research needs. Respir Med 104: 1237-1245, 2010.
11. Berger WE, and Tashkin DP Flunisolide hydrofluoroalkane with integrated spacer for treating asthma: An updated review. Allergy Asthma Proc 36: 105-115, 2015.
12. Daley-Yates PT, Price AC, Sisson JR, et al. Beclomethasone dipropionate: Absolute bioavailability, pharmacokinetics and metabolism following intravenous, oral, intranasal and inhaled administration in man. Br J Clin Pharmacol 51: 400-409, 2001.
13. Zöllner EW. Hypothalamic-pituitary-adrenal axis suppression in asthmatic children on inhaled corticosteroids: Part 1. Which test should be used? Pediatr Allergy Immunol 18: 401-409, 2007.
14. Lipworth BJ Systemic adverse effects of inhaled corticosteroid therapy: A systematic review and meta-analysis. Arch Intern Med 159: 941-955, 1999.
15. Wlodarczyk JH, Gibson PG, and Caeser M. Impact of inhaled corticosteroids on cortisol suppression in adults with asthma: A quantitative review. Ann Allergy Asthma Immunol 100: 23-30, 2008.
16. http://www.r-project.org.
17. Postma DS, Sevette C, Martinat Y, et al. Treatment of asthma by the inhaled corticosteroid ciclesonide given either in the morning or evening. Eur Respir J 17: 1083-1088, 2001.
18. Farmer IS, Middle M, Savic J, et al. Therapeutic equivalence of inhaled beclomethasone dipropionate with CFC and non-CFC (HFA 134a) propellants both delivered via the Easibreathe inhaler for the treatment of paediatric asthma. Respir Med 94: 57-63, 2000.
19. Carlsen KC, Stick S, Kamin W, et al. The efficacy and safety of fluticasone propionate in very young children with persistent asthma symptoms. Respir Med 99: 1393-1402, 2005.
20. Kim KT, Milgrom H, Yoon YK, et al. Systemic exposure and urinary cortisol effects of fluticasone propionate formulated with hydrofluoroalkane in 4- to 11-year-olds with asthma. J Clin Pharmacol 48: 108-116, 2008.
21. Derom E, Van Schoor J, Verhaeghe W, et al. Systemic effects of inhaled fluticasone propionate and budesonide in adult patients with asthma. Am J Respir Crit Care Med 160: 157-161, 1999.
22. Martin RJ, Szefler SJ, Chinchilli VM, et al. Systemic effect comparisons of six inhaled corticosteroid preparations. Am J Respir Crit Care Med 165: 1377-1383, 2002.
23. Wolthers OD Systemic activity of inhaled hydrofluoroalkane134a metered dose inhaler with beclomethasone dipropionate in children with asthma. Pediatr Asthma Allergy Immunol 19: 172-179, 2006.
24. Kaur C, Bansal SK, and Chhabra SK Study on serum and urinary cortisol levels of asthmatic patients after treatment with high dose inhaled beclomethasone dipropionate or budesonide. Indian J Chest Dis Allied Sci 47: 89-95, 2005.
25. Agertoft L, and Pedersen S. Short-term lower-leg growth rate and urine cortisol excretion in children treated with ciclesonide. J Allergy Clin Immunol 115: 940-945, 2005.
26. Agertoft L, and Pedersen S. Short-term knemometry and urine cortisol excretion in children treated with fluticasone propionate and budesonide: A dose response study. Eur Respir J 10: 1507-1512, 1997.
27. Wolthers OD Short-term growth and adrenal function in children with asthma treated with inhaled beclomethasone dipropionate hydrofluoroalkane-134a. Pediatr Allergy Immunol 17: 613-619, 2006.
28. Kannisto S, Korppi M, Remes K, and Voutilainen R. Serum dehydroepiandrosterone sulfate concentration as an indicator of adrenocortical suppression in asthmatic children treated with inhaled steroids. J Clin Endocrinol Metab 86: 4908-4912, 2001.
29. Kannisto S, Laatikainen A, Taivainen A, et al. Serum dehydroepiandrosterone sulfate concentration as an indicator of adrenocortical suppression during inhaled steroid therapy in adult asthmatic patients. Eur J Endocrinol 150: 687-690, 2004.
30. Boulet LP, Lemière C, Gauvreau G, et al. Safety, pharmacodynamics and pharmacokinetics of TPI 1020 in smokers with asthma. Respir Med 103: 1159-1166, 2009.
31. Turktas I, Ozkaya O, Bostanci I, et al. Safety of inhaled corticosteroid therapy in young children with asthma. Ann Allergy Asthma Immunol 86: 649-654, 2001.
32. Kemp J, Wanderer AA, Ramsdell J, et al. Rapid onset of control with budesonide Turbuhaler in patients with mild-to-moderate asthma. Ann Allergy Asthma Immunol 82: 463-471, 1999.
33. Langdon CG, Adler M, Mehra S, et al. Once-daily ciclesonide 80 or 320 microg for 12 weeks is safe and effective in patients with persistent asthma. Respir Med 99: 1275-1285, 2005.
34. Scott MB, Ellis MH, Cruz-Rivera M, et al. Once-daily budesonide inhalation suspension in infants and children < 4 and > or = 4 years of age with persistent asthma. Ann Allergy Asthma Immunol 87: 488-495, 2001.
35. De Benedictis FM, Del Giudice MM, Vetrella M, et al. Flic12 Study Group. Nebulized fluticasone propionate vs. budesonide as adjunctive treatment in children with asthma exacerbation. J Asthma 42: 331-336, 2005.
36. Chapman KR, Patel P, D'Urzo AD, et al. Maintenance of asthma control by once-daily inhaled ciclesonide in adults with persistent asthma. Allergy 60: 330-337, 2005.
37. Agertoft L, and Pedersen S. Lower-leg growth rates in children with asthma during treatment with ciclesonide and fluticasone propionate. Pediatr Allergy Immunol 21: e199-e205, 2010.
38. Peden DB, Berger WE, Noonan MJ, et al. Inhaled fluticasone propionate delivered by means of two different multidose powder inhalers is effective and safe in a large pediatric population with persistent asthma. J Allergy Clin Immunol 102: 32-38, 1998.
39. Andersson O, Cassel TN, Grönneberg R, et al. In vivo modulation of glucocorticoid receptor mRNA by inhaled fluticasone propionate in bronchial mucosa and blood lymphocytes in subjects with mild asthma. J Allergy Clin Immunol 103: 595-600, 1999.
40. Doull IJ, Freezer NJ, Holgate ST. Growth of prepubertal children with mild asthma treated with inhaled beclomethasone dipropionate. Am J Respir Crit Care Med 151: 1715-1719, 1995.
41. Hoekstra MO, Grol MH, Bouman K, et al. Fluticasone propionate in children with moderate asthma. Am J Respir Crit Care Med 154: 1039-1044, 1996.
42. Ozbek OY, Turktas I, Bakirtas A, and Bideci A. Evaluation of hypothalamic-pituitary-adrenal axis suppression by low-dose (0.5 microg) and standard-dose (250 microg) adrenocorticotropic hormone (ACTH) tests in asthmatic children treated with inhaled corticosteroid. J Pediatr Endocrinol Metab 19: 1015-1023, 2006.
43. Nicolaizik WH, Marchant JL, Preece MA, and Warner JO. Endocrine and lung function in asthmatic children on inhaled corticosteroids. Am J Respir Crit Care Med 150: 624-628, 1994.
44. Lawrence M, Wolfe J, Webb DR, et al. Efficacy of inhaled fluticasone propionate in asthma results from topical and not from systemic activity. Am J Respir Crit Care Med 156: 744-751, 1997.
45. LaForce CF, Pearlman DS, Ruff ME, et al. Efficacy and safety of dry powder fluticasone propionate in children with persistent asthma. Ann Allergy Asthma Immunol 85: 407-415, 2000.
46. Shapiro G, Mendelson L, Kraemer MJ, et al. Efficacy and safety of budesonide inhalation suspension (Pulmicort Respules) in young children with inhaled steroid-dependent, persistent asthma. J Allergy Clin Immunol 102: 789-796, 1998.
47. Nayak A, Lanier R, Weinstein S, et al. Efficacy and safety of beclomethasone dipropionate extrafine aerosol in childhood asthma: A 12-week, randomized, double-blind, placebo-controlled study. Chest 122: 1956-1965, 2002.
48. Derom E, Van De Velde V, Marissens S, et al. Effects of inhaled ciclesonide and fluticasone propionate on cortisol secretion and airway responsiveness to adenosine 5'monophosphate in asthmatic patients. Pulm Pharmacol Ther 18: 328-336, 2005.
49. Lee DK, Bates CE, Currie GP, et al. Effects of high-dose inhaled fluticasone propionate on the hypothalamic-pituitary-adrenal axis in asthmatic patients with severely impaired lung function. Ann Allergy Asthma Immunol 93: 253-258, 2004.
50. Aaronson D, Kaiser H, Dockhorn R, et al. Effects of budesonide by means of the Turbuhaler on the hypothalamic-pituitaryadrenal axis in asthmatic subjects: A dose-response study. J Allergy Clin Immunol 101: 312-319, 1998.
51. Dal Negro R, Micheletto C, Tognella S, et al. Effect of inhaled beclomethasone dipropionate and budesonide dry powder on pulmonary function and serum eosinophil cationic protein in adult asthmatics. J Investig Allergol Clin Immunol 9: 241-247, 1999.
52. Lipworth BJ, Kaliner MA, LaForce CF, et al. Effect of ciclesonide and fluticasone on hypothalamic-pituitary-adrenal axis function in adults with mild-to-moderate persistent asthma. Ann Allergy Asthma Immunol 94: 465-472, 2005.
53. Wilson AM, and Lipworth BJ Dose-response evaluation of the therapeutic index for inhaled budesonide in patients with mild-to-moderate asthma. Am J Med 108: 269-275, 2000.
54. Shapiro G, Bronsky EA, LaForce CF, et al. Dose-related efficacy of budesonide administered via a dry powder inhaler in the treatment of children with moderate to severe persistent asthma. J Pediatr 132: 976-982, 1998.
55. Wilson AM, Sims EJ, and Lipworth BJ Dose response with fluticasone propionate on adrenocortical activity and recovery of basal and stimulated responses after stopping treatment. Clin Endocrinol (Oxf) 50: 329-335, 1999.
56. Toogood JH, White FA, Baskerville JC, et al. Comparison of the antiasthmatic, oropharyngeal, and systemic glucocorticoid effects of budesonide administered through a pressurized aerosol plus spacer or the Turbuhaler dry powder inhaler. J Allergy Clin Immunol 99: 186-193, 1997.
57. Clark DJ, Grove A, Cargill RI, and Lipworth BJ. Comparative adrenal suppression with inhaled budesonide and fluticasone propionate in adult asthmatic patients. Thorax 51: 262-266, 1996.
58. Perruchoud AP, Lundback B, Yigla M, and Sykes AP. Clinical efficacy and safety of fluticasone propionate 1 mg per day administered via a HFA 134a pressurized metered dose inhaler to patients with moderate to severe asthma. International study group. Respir Med 94(suppl. B): S35-S41, 2000.
59. Szefler S, Rohatagi S, Williams J, et al. Ciclesonide, a novel inhaled steroid, does not affect hypothalamic-pituitary-adrenal axis function in patients with moderate-to-severe persistent asthma. Chest 128: 1104-1114, 2005.
60. Pedersen S, Garcia Garcia ML, Manjra A, et al. A comparative study of inhaled ciclesonide 160 microg/day and fluticasone propionate 176 microg/day in children with asthma. Pediatr Pulmonol 41: 954-961, 2006.
61. Doull IJ, Donovan SJ, Wood PJ, and Holgate ST. Bloodspot cortisol in mild asthma: The effect of inhaled corticosteroids. Arch Dis Child 72: 321-324, 1995.
62. Skoner DP, Maspero J, and Banerji D. Ciclesonide Pediatric Growth Study Group. Assessment of the long-term safety of inhaled ciclesonide on growth in children with asthma. Pediatrics 121: e1-e14, 2008.
63. Lee DK, Fardon TC, Bates CE, et al. Airway and systemic effects of hydrofluoroalkane formulations of high-dose ciclesonide and fluticasone in moderate persistent asthma. Chest 127: 851-860, 2005.
64. Kannisto S, Korppi M, Remes K, and Voutilainen R. Adrenal suppression, evaluated by a low dose adrenocorticotropin test, and growth in asthmatic children treated with inhaled steroids. J Clin Endocrinol Metab 85: 652-657, 2000.
65. Clark DJ, and Lipworth BJ Adrenal suppression with chronic dosing of fluticasone propionate compared with budesonide in adult asthmatic patients. Thorax 52: 55-58, 1997.
66. Goldberg S, Einot T, Algur N, et al. Adrenal suppression in asthmatic children receiving low-dose inhaled budesonide: Comparison between dry powder inhaler and pressurized metered-dose inhaler attached to a spacer. Ann Allergy Asthma Immunol 89: 566-571, 2002.
67. Priftis KN, and Papadimitriou A, Anthracopoulos MB, et al. Adrenal function improves in asthmatic children on inhaled steroids: A longitudinal study. Neuroimmunomodulation 13: 56-62, 2006.
68. MacKenzie CA, Weinberg EG, Tabachnik E, et al. A placebo controlled trial of fluticasone propionate in asthmatic children. Eur J Pediatr 152: 856-860, 1993.
69. Hansel TT, Benezet O, Kafé H, et al. A multinational, 12-week, randomized study comparing the efficacy and tolerability of ciclesonide and budesonide in patients with asthma. Clin Ther 28: 906-920, 2006.
70. Nathan RA, Li JT, Finn A, et al. A dose-ranging study of fluticasone propionate administered once daily via multidose powder inhaler to patients with moderate asthma. Chest 118: 296-302, 2000.
71. Caffey LF, Raissy HH, Marshik P, et al. A crossover comparison of fluticasone propionate and montelukast on inflammatory indices in children with asthma. Pediatr Asthma Allergy Immunol 18: 123-130, 2005.
72. Nelson HS, Stricker W, Casale TB, et al. A comparison of methods for assessing hypothalamic-pituitary-adrenal (HPA) axis activity in asthma patients treated with inhaled corticosteroids. J Clin Pharmacol 42: 319-326, 2002.
73. Li JT, Ford LB, Chervinsky P, et al. Fluticasone propionate powder and lack of clinically significant effects on hypothalamic-pituitary-adrenal axis and bone mineral density over 2 years in adults with mild asthma. J Allergy Clin Immunol 103: 1062-1068, 1999.
74. Wolthers OD, and Walters EG Short-term lower leg growth in 5- to 11-year-old asthmatic children using beclomethasone dipropionate inhalers with chlorofluorocarbon or hydrofluoroalkane propellants: A 9-week, open-label, randomized, crossover, noninferiority study. Clin Ther 33: 1069-1076, 2011.
75. Woodcock A, Bleecker ER, Busse WW, et al. Fluticasone furoate: Once-daily evening treatment versus twice-daily treatment in moderate asthma. Respir Res 12: 160, 2011.
76. Harrison LI, Colice GL, Donnell D, et al. Adrenal effects and pharmacokinetics of CFC-free beclomethasone dipropionate: A 14-day dose-response study. J Pharm Pharmacol 51: 263-269, 1999.
77. Sorkness CA, LaForce C, Storms W, et al. Effects of the inhaled corticosteroids fluticasone propionate, triamcinolone acetonide, and flunisolide and oral prednisone on the hypothalamic-pituitary-adrenal axis in adult patients with asthma. Clin Ther 21: 353-367, 1999.
78. Weiner P, Berar-Yanay N, Davidovich A, and Magadle R. Nocturnal cortisol secretion in asthmatic patients after inhalation of fluticasone propionate. Chest 116: 931-934, 1999.
79. Tonnel AB, Bons J, Legendre M, et al. Clinical efficacy and safety of fluticasone propionate 250 microg twice daily administered via a HFA 134a pressurized metered dose inhaler to patients with mild to moderate asthma. French study group. Respir Med 94(suppl. B): S29-S34, 2000.
80. Derom E, Louis R, Tiesler C, et al. Effects of ciclesonide and fluticasone on cortisol secretion in patients with persistent asthma. Eur Respir J 33: 1277-1286, 2009.
81. Derendorf H. Pharmacokinetic and pharmacodynamic properties of inhaled ciclesonide. J Clin Pharmacol 47: 782-789, 2007.
82. Hübner M, Hochhaus G, and Derendorf H. Comparative pharmacology, bioavailability, pharmacokinetics, and pharmacodynamics of inhaled glucocorticosteroids. Immunol Allergy Clin North Am 25: 469-488, 2005.
83. Bodzenta-Łukaszyk A, and Kokot M. Pharmacological consequences of inhaled drug delivery to small airways in the treatment of asthma. Adv Ther 31: 803-816, 2014.