Using fractional exhaled nitric oxide (FeNO) to diagnose steroid-responsive disease and guide asthma management in routine care

Clinical and Translational Allergy

Volumn 3, Issue 1, 2013, Pages 1-10

  Price, David ^a,b,c   Ryan, Dermot ^d   Burden, Annie ^a   Von Ziegenweidt, Julie ^a   Gould, Shuna ^a   Freeman, Daryl ^e   Gruffydd Jones, Kevin ^f   Copland, Anne ^g   Godley, Clifford ^h   Chisholm, Alison ^b   Thomas, Mike ⁱ  

^a Research in Real Life   (United Kingdom)

^b Respiratory Effectiveness Group   (United Kingdom)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e NORFOLK COMMUNITY HEALTH AND CARE NHS TRUST   (United Kingdom)

^f UNIVERSITY OF BATH   (United Kingdom)

^g Woodstock Medical Centre   (United Kingdom)

^h Avondale Medical Practice   (United Kingdom)

ⁱ UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Diagnosis; Fractional exhaled nitric oxide (FeNO); On going asthma management; Practical guidance; Steroid responsive disease

Indexed keywords

CORTICOSTEROID; FRACTIONAL EXHALED NITRIC OXIDE; NITRIC OXIDE; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AGED; ALGORITHM; ALLERGIC AIRWAY INFLAMMATION; ARTICLE; ASTHMA; ASTHMA MANAGEMENT; CHILD; COHORT ANALYSIS; CORTICOSTEROID THERAPY; DISEASE ASSESSMENT; DISEASE ASSOCIATION; DISEASE CONTROL; FEMALE; HUMAN; INCIDENCE; LUNG DISEASE; MAJOR CLINICAL STUDY; MALE; MEDICAL PRACTICE; NITRIC OXIDE ANALYZER; OBSERVATIONAL STUDY; OUTCOME ASSESSMENT; PATIENT ATTITUDE; PATIENT CARE; PATIENT COMPLIANCE; PATIENT MONITORING; PRIMARY MEDICAL CARE; PRIORITY JOURNAL; STEROID RESPONSIVE DISEASE; TREATMENT DURATION; TREATMENT RESPONSE; UNITED KINGDOM;

EID: 85006085633     PISSN: None     EISSN: 20457022     Source Type: Journal    
DOI: 10.1186/2045-7022-3-37     Document Type: Article

References (55)

1. Zacharasiewicz A, Wilson N, Lex C, Erin EM, Li AM, Hansel T, Khan M, Bush A: Clinical use of noninvasive measurements of airway inflammation in steroid reduction in children. Am J Respir Crit Care Med. 2005, 171: 1077-1082. 10.1164/rccm.200409-1242OC.
2. NHLBI/WHO Workshop Report: Global strategy for asthma management and prevention. 1995, Bethesda, MD: National Institutes of Health. National Heart, Lung, and Blood Institute, Publication No. 95-3659
3. Global Initiative for Asthma: Global strategy for asthma management and prevention. 2012,http://www.ginasthma.org,
4. Haldar P, Pavord ID, Shaw DE, Berry MA, Thomas M, Brightling CE, Wardlaw AJ, Green RH: Cluster analysis and clinical asthma phenotypes. Am J Respir Crit Care Med. 2008, 178: 218-224. 10.1164/rccm.200711-1754OC.
5. Bateman ED, Boushey HA, Bousquet J: Can guideline-defined asthma control Be achieved? the gaining optimal asthma controL study. Am J Respir Crit Care Med. 2004, 170: 36-844.
6. Pijnenburg MW, Bakker EM, Hop WC, De Jongste JC: Titrating steroids on exhaled nitric oxide in children with asthma: a randomized controlled trial. Am J Respir Crit Care Med. 2005, 172: 831-836. 10.1164/rccm.200503-458OC.
7. Grönke L, Kanniess F, Holz O, Jörres RA, Magnussen H: The relationship between airway hyper-responsiveness, markers of inflammation and lung function depends on the duration of the asthmatic disease. Clin Exp Allergy. 2002, 32: 57-63. 10.1046/j.0022-0477.2001.01297.x.
8. Langley SJ, Goldthorpe S, Custovic A, Woodcock A: Relationship among pulmonary function, bronchial reactivity, and exhaled nitric oxide in a large group of asthmatic patients. Ann Allergy Asthma Immunol. 2003, 91: 398-404. 10.1016/S1081-1206(10)61688-2.
9. Brightling CE, Monteiro W, Ward R, Parker D, Morgan MD, Wardlaw AJ, Pavord ID: Sputum eosinophilia and short-term response to Prednisolone in chronic obstructive pulmonary disease: a randomised controlled trial. Lancet. 2000, 356: 1480-1485. 10.1016/S0140-6736(00)02872-5.
10. Brightling CE, Ward R, Wardlaw AJ, Pavord ID: Airway inflammation, airway responsiveness and cough before and after inhaled budesonide in patients with eosinophilic bronchitis. Eur Respir J. 2000, 15: 682-686. 10.1034/j.1399-3003.2000.15d10.x.
11. Pavord ID, Brightling CE, Woltmann G, Wardlaw AJ: Non-eosinophilic corticosteroid unresponsive asthma. Lancet. 1999, 353: 2213-2214. 10.1016/S0140-6736(99)01813-9.
12. Green RH, Brightling CE, Woltmann G, Parker G, Wardlaw AJ, Pavord ID: Analysis of induced sputum in adults with asthma: identification of a sub group with isolated sputum neutrophilia and poor response to inhaled corticosteroids. Thorax. 2002, 57: 875-879. 10.1136/thorax.57.10.875.
13. Pizzichini E, Pizzichini MM, Gibson P, Parameswaran K, Gleich GJ, Berman L, Dolovich J, Hargreave FE: Sputum eosinophilia predicts benefit from prednisone in smokers with chronic obstructive bronchitis. Am J Respir Crit Care Med. 1998, 158 (5 Pt 1): 1511-
14. Berry M, Morgan A, Shaw DE, Parker D, Green R, Brightling C, Bradding P, Wardlaw AJ, Pavord ID: Pathological features and inhaled corticosteroid response of eosinophilic and non-eosinophilic asthma. Thorax. 2007, 62: 43-49. 10.1136/thx.2005.052191.
15. Rosi E, Ronchi MC, Grazzini M, Duranti R, Scano G: Sputum analysis, bronchial hyperresponsiveness, and airway function in asthma: results of a factor analysis. J Allergy Clin Immunol. 1993, 3 (2 Pt 1): 232-237.
16. Haldar P, Brightling CE, Hargadon B, Gupta S, Monteiro W, Sousa A, Marshall RP, Bradding P, Green RH, Wardlaw AJ, Pavord ID: Mepolizumab and exacerbations of refractory eosinophilic asthma. N Engl J Med. 2009, 360: 973-984. 10.1056/NEJMoa0808991.
17. Pearce N, Pekkanen J, Beasley R: How much asthma is really attributable to atopy?. Thorax. 1999, 54: 268-272. 10.1136/thx.54.3.268.
18. Douwes J, Gibson Pekkanen P, Pearce N: Non-eosinophilic asthma: importance and possible mechanisms. Thorax. 2002, 57: 643-648. 10.1136/thorax.57.7.643.
19. McGrath KW, Icitovic N, Boushey HA, Lazarus SC, Sutherland ER, Chinchilli VM, Fahy JV: Asthma clinical research network of the national heart, lung, and blood institute.: a large subgroup of mild-to-moderate asthma is persistently noneosinophilic. Am J Respir Crit Care Med. 2012, 185: 612-619. 10.1164/rccm.201109-1640OC.
20. Frank TL, Adisesh A, Pickering AC, Morrison JF, Wright T, Francis H, Fletcher A, Frank PI, Hannaford P: Relationship between exhaled nitric oxide and childhood asthma. Am J Respir Crit Care Med. 1998, 158: 1032-1036. 10.1164/ajrccm.158.4.9707143.
21. Shaw DE, Berry MA, Thomas M, Green RH, Brightling CE, Wardlaw AJ, Pavord ID: The use of exhaled nitric oxide concentration to identify eosinophilic airway inflammation: an observational study in adults with asthma. Clin Exp Allergy. 2005, 35: 1175-1179. 10.1111/j.1365-2222.2005.02314.x.
22. Piacentini GL, Bodini A, Costella S, Vicentini L, Mazzi P, Sperandio S, Boner AL: Exhaled nitric oxide and sputum eosinophil markers of inflammation in asthmatic children. Eur Respir J. 1999, 6: 1386-1390.
23. Payne DN, Adcock IM, Wilson NM, Oates T, Scallan M, Bush A: Relationship between exhaled nitric oxide and mucosal eosinophilic inflammation in children with difficult asthma, after treatment with oral Prednisolone. Am J Respir Crit Care Med. 2001, 64: 1376-1381.
24. Dweik RA, Boggs PB, Erzurum SC, Irvin CG, Leigh MW, Lundberg JO, Olin AC, Plummer AL, Taylor DR: American thoracic society committee on interpretation of exhaled nitric oxide levels (FENO) for clinical applications: an official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FeNO) for clinical application. Am J Respir Crit Care Med. 2011, 184: 602-615. 10.1164/rccm.9120-11ST.
25. Smith AD, Cowan JO, Brassett KP, Filsell S, McLachlan C, Monti-Sheehan G, Peter Herbison G, Robin Taylor D: Exhaled nitric oxide: a predictor of steroid response. Am J Respir Crit Care Med. 2005, 172: 453-459. 10.1164/rccm.200411-1498OC.
26. Smith AD, Cowan JO, Filsell S, McLachlan C, Monti-Sheehan G, Jackson P, Taylor DR: Diagnosing asthma: comparisons between exhaled nitric oxide measurements and conventional tests. Am J Respir Crit Care Med. 2004, 169: 473-10.1164/rccm.200310-1376OC.
27. Optimum patient care.http://www.optimumpatientcare.org,
28. Petsky HL, Cates CJ, Li A, Lynaston JA, Turner C, Chang AB: Tailored interventions based on exhaled nitric oxide versus clinical symptoms for asthma in children and adults. Cochrane Database Syst Rev. 2009, 2: CD006340
29. Petsky HL, Cates CJ, Lasserson TJ, Li AM, Turner C, Kynaston JA, Chang AB: A systematic review and meta-analysis: tailoring asthma treatment on eosinophilic markers (exhaled nitric oxide or sputum eosinophils). Thorax. 2012, 67: 199-208. 10.1136/thx.2010.135574.
30. Fuhlbrigge A, Peden D, Apter AJ, Boushey HA, Camargo CA, Gern J, Heymann PW, Martinez FD, Mauger D, Teague WG, Blaisdell C: Asthma outcomes: exacerbations. J Allergy Clin Immunol. 2012, 129: S34e48-
31. Powell H, Murphy VE, Taylor DR, Hensley MJ, McCaffery K, Giles W, Clifton VL, Gibson PG: Management of asthma in pregnancy guided by measurement of fraction of exhaled nitric oxide: a double-blind, randomized controlled trial. Lancet. 2011, 378: 983e90-
32. Smith AD, Cowan JO, Brassett KP, Herbison GP, Taylor DR: Use of exhaled nitric oxide measurements to guide treatment in chronic asthma. N Engl J Med. 2005, 352: 2163e73-
33. Shaw DE, Berry MA, Thomas M, Green RH, Brightling CE, Wardlaw AJ, Pavord ID: The use of exhaled nitric oxide to guide asthma management. Am J Respir Crit Care Med. 2007, 176: 231e7-
34. Donohue JF, Jain N: Exhaled nitric oxide to predict corticosteroid responsiveness and reduced asthma exacerbation rates. Respir Med. 2013, 107: 943-952. 10.1016/j.rmed.2013.02.018.
35. Mahr TA, Malka J, Spahn JD: Inflammometry in pediatric asthma: a review of factional exhaled nitric oxide in clinical practice. Allergy Asthma Proc. 2013, 34: 1-10. 10.2500/aap.2013.34.3629.
36. Green RH, Brightling CE, McKenna S, Hargadon B, Parker D, Bradding P, Wardlaw AJ, Pavord ID: Asthma exacerbations and sputum eosinophil counts: a randomised controlled trial. Lancet. 2002, 360: 1715-1721. 10.1016/S0140-6736(02)11679-5.
37. Zeiger RS, Schatz M, Zhang F, Crawford WW, Kaplan MS, Roth RM, Chen W: Elevated exhaled nitric oxide is a clinical indicator of future uncontrolled asthma in asthmatic patients on inhaled corticosteroids. J Allergy Clin Immunol. 2011, 128: 412-414. 10.1016/j.jaci.2011.06.008.
38. Gelb AF, Taylor CF, Shinar CM, Gutierrez C, Zamel N: Role of spirometry and exhaled nitric oxide to predict exacerbations in treated asthmatics. Chest. 2006, 129: 1492-1499. 10.1378/chest.129.6.1492.
39. Beck-Ripp JM, Griese S, Arenz C, Koring B, Pasqualoni B, Bufler P: Changes of exhaled nitric oxide during steroid treatment of childhood asthma. Eur Respir J. 2002, 19: 1015-1019. 10.1183/09031936.02.01582001.
40. Delgado-Corcoran C, Kissoon N, Murphy SP, Duckworth LJ: Exhaled nitric oxide reflects asthma severity and asthma control. Pediatr Crit Care Med. 2004, 5: 48-52. 10.1097/01.CCM.0000105310.00799.51.
41. Koster ES, Raaijmakers JA, Vijverberg SJ, Der Zee AH M-v: Inhaled corticosteroid adherence in paediatric patients: the PACMAN cohort study. Pharmacoepidemiol Drug Saf. 2011, 20: 1064-10772. 10.1002/pds.2228.
42. Cochrane MG, Bala MV, Downs KE, Mauskopf J, Ben-Joseph RH: Inhaled corticosteroids for asthma therapy: patient compliance, devices, and inhalation technique. Chest. 2000, 117: 542-550. 10.1378/chest.117.2.542.
43. Persson MG, Zetterstrom O, Agrenius V, Ihre E, Gustafsson LE: Singlebreath nitric oxide measurements in asthmatic patients and smokers. Lancet. 1994, 343: 146-147. 10.1016/S0140-6736(94)90935-0.
44. Robbins RA, Millatmal T, Lassi K, Rennard S, Daughton D: Smoking cessation is associated with an increase in exhaled nitric oxide. Chest. 1997, 112: 313-318. 10.1378/chest.112.2.313.
45. Kharitonov SA, Robbins RA, Yates D, Keatings V, Barnes PJ: Acute and chronic effects of cigarette smoking on exhaled nitric oxide. Am J Respir Crit Care Med. 1995, 152: 609-612. 10.1164/ajrccm.152.2.7543345.
46. Schilling J, Holzer P, Guggenbach M, Gyurech D, Marathia K, Geroulanos S: Reduced endogenous nitric oxide in the exhaled air of smokers and hypertensives. Eur Respir J. 1994, 7: 467-471. 10.1183/09031936.94.07030467.
47. Horvath I, Donnelly LE, Kiss A, Balint B, Kharitonov SA, Barnes PJ: Exhaled nitric oxide and hydrogen peroxide concentrations in asthmatic smokers. Respiration (Herrlisheim). 2004, 71: 463-468. 10.1159/000080630.
48. American Thoracic Society / European Respiratory Society: ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med. 2005, 171: 912-930.
49. Yavuz ST, Civelek E, Sahiner UM, Buyuktiryaki AB, Tuncer A, Karabulut E, Sekerel BE: Identifying uncontrolled asthma in children with the childhood asthma control test or exhaled nitric oxide measurement. Ann Allergy Asthma Immunol. 2012, 109: 36-40. 10.1016/j.anai.2012.05.011.
50. Green RJ, Klein M, Becker P, Halkas A, Lewis H, Kitchin O, Moodley T, Masekela R: Disagreement between common measures of asthma control in children. Chest. 2013, 143: 117-122. 10.1378/chest.12-1070.
51. Stern G, De Jongste J, van der Valk R, Baraldi E, Carraro S, Thamrin C, Frey U: Fluctuation phenotyping based on daily fraction of exhaled nitric oxide values in asthmatic children. J Allergy Clin Immunol. 2011, 128: 293-300. 10.1016/j.jaci.2011.03.010.
52. Lester D, Mohammad A, Hernandez PI, Leach EE, Walker EA: An investigation of asthma care best practices in a community health center. J Health Care Poor Underserv. 2012, 23 (3 Suppl): 255-264.
53. Wang L, Hollenbeak CS, Mauger DT, Zeiger RS, Paul IM, Sorkness CA, Lemanske RF, Martinez FD, Strunk RC, Szefler SJ, Taussig LM: Childhood asthma research and education network of the national heart, lung, and blood institute: cost-effectiveness of fluticasone versus Montelukast in children with mild-to-intermediate persistent asthma in the pediatric asthma controller trial. J Allergy Clin Immunol. 2011, 127: 161-166. 10.1016/j.jaci.2010.10.035.
54. Price D, Berg J, Lindgren P: An economic evaluation of NIOX MINO airway inflammation monitor in the United Kingdom. Allergy. 2009, 64: 431-438. 10.1111/j.1398-9995.2008.01855.x.
55. Calhoun WJ, Ameredes BT, King TS, Icitovic N, Bleecker ER, Castro M, Cherniack RM, Chinchilli VM, Craig T, Denlinger L, DiMango EA, Engle LL, Fahy JV, Grant JA, Israel E, Jarjour N, Kazani SD, Kraft M, Kunselman SJ, Lazarus SC, Lemanske RF, Lugogo N, Martin RJ, Meyers DA, Moore WC, Pascual R, Peters SP, Ramsdell J, Sorkness CA, Sutherland ER: Asthma clinical research network of the national heart, lung, and blood institute: comparison of physician-, biomarker-, and symptom-based strategies for adjustment of inhaled corticosteroid therapy in adults with asthma: the BASALT randomized controlled trial. JAMA. 2012, 308: 987-997. 10.1001/2012.jama.10893.