6,091
Views
36
CrossRef citations to date
0
Altmetric
Review

Improving the diagnosis of eosinophilic asthma

&
Pages 1093-1103 | Received 06 Jun 2016, Accepted 12 Sep 2016, Published online: 22 Sep 2016

References

  • Martinez FD, Vercelli D. Asthma. Lancet. 2013;382(9901):1360–1372.
  • Gauthier M, Ray A, Wenzel SE. Evolving concepts of asthma. Am J Respir Crit Care Med. 2015;192(6):660–668.
  • De Groot JC, Ten Brinke A, Bel EHD. Management of the patient with eosinophilic asthma: a new era begins. ERJ Open Res. 2015;1(1):00024–02015.
  • Hilvering B, Xue LZ, Pavord ID. Evidence for the efficacy and safety of anti-interleukin-5 treatment in the management of refractory eosinophilic asthma. Ther Adv Respir Dis. 2015;9(4):135–145.
  • Ortega HG, Liu MC, Pavord ID, et al. Mepolizumab treatment in patients with severe eosinophilic asthma. New Engl J Med. 2014;371(13):1198–1207.
  • Bel EH, Wenzel SE, Thompson PJ, et al. Oral glucocorticoid-sparing effect of mepolizumab in eosinophilic asthma. New Engl J Med. 2014;371(13):1189–1197.
  • Douwes J, Gibson P, Pekkanen J, et al. Non-eosinophilic asthma: importance and possible mechanisms. Thorax. 2002;57(7):643–648.
  • McGrath KW, Icitovic N, Boushey HA, et al. A large subgroup of mild-to-moderate asthma is persistently noneosinophilic. Am J Respir Crit Care Med. 2012;185(6):612–619.
  • Hargreave FE. Induced sputum and response to glucocorticoids. J Allergy Clin Immunol. 1998;102(5):S102–105.
  • Green RH, Brightling CE, McKenna S, et al. Asthma exacerbations and sputum eosinophil counts: a randomised controlled trial. Lancet. 2002;360(9347):1715–1721.
  • Jayaram L, Pizzichini MM, Cook RJ, et al. Determining asthma treatment by monitoring sputum cell counts: effect on exacerbations. Eur Respir J. 2006;27(3):483–494.
  • Cowan DC, Cowan JO, Palmay R, et al. Effects of steroid therapy on inflammatory cell subtypes in asthma. Thorax. 2010;65(5):384–390.
  • Kupczyk M, Dahlen B, Sterk PJ, et al. Stability of phenotypes defined by physiological variables and biomarkers in adults with asthma. Allergy. 2014;69(9):1198–1204.
  • Haldar P, Brightling CE, Hargadon B, et al. Mepolizumab and exacerbations of refractory eosinophilic asthma. New Engl J Med. 2009;360(10):973–984.
  • Wenzel SE, Schwartz LB, Langmack EL, et al. Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics. Am J Respir Crit Care Med. 1999;160(3):1001–1008.
  • Pavord ID, Korn S, Howarth P, et al. Mepolizumab for severe eosinophilic asthma (DREAM): a multicentre, double-blind, placebo-controlled trial. Lancet. 2012;380(9842):651–659.
  • Nair P, Pizzichini MM, Kjarsgaard M, et al. Mepolizumab for prednisone-dependent asthma with sputum eosinophilia. N Engl J Med. 2009;360(10):985–993.
  • Van Veen IH, Ten BA, Gauw SA, et al. Consistency of sputum eosinophilia in difficult-to-treat asthma: a 5-year follow-up study. J Allergy Clin Immunol. 2009;124(3):615–617.e2.
  • Klion AD, Bochner BS, Gleich GJ, et al. Approaches to the treatment of hypereosinophilic syndromes: a workshop summary report. J Allergy Clin Immunol. 2006;117(6):1292–1302.
  • Walford HH, Doherty TA. Diagnosis and management of eosinophilic asthma: a US perspective. J Asthma Allergy. 2014;7:53–65.
  • Groh M, Pagnoux C, Baldini C, et al. Eosinophilic granulomatosis with polyangiitis (Churg-Strauss) (EGPA) consensus task force recommendations for evaluation and management. Eur J Intern Med. 2015;26(7):545–553.
  • In ‘T Veen JCCM, De Gouw HWFM, Smits HH, et al. Repeatability of cellular and soluble markers of inflammation in induced sputum from patients with asthma. Eur Respir J. 1996;9(12):2441–2447.
  • Korevaar DA, Westerhof GA, Wang J, et al. Diagnostic accuracy of minimally invasive markers for detection of airway eosinophilia in asthma: a systematic review and meta-analysis. Lancet Respir Med. 2015;3(4):290–300.
  • Ten Brinke A, De Lange C, Zwinderman AH, et al. Sputum induction in severe asthma by a standardized protocol: predictors of excessive bronchoconstriction. Am J Respir Crit Care Med. 2001;164(5):749–753.
  • Berry A, Busse WW. Biomarkers in asthmatic patients: has their time come to direct treatment? J Allergy Clin Immunol. 2016;137(5):1317–1324.
  • Hastie AT, Moore WC, Li H, et al. Biomarker surrogates do not accurately predict sputum eosinophil and neutrophil percentages in asthmatic subjects. J Allergy Clin Immunol. 2013;132(1):72–80.
  • Spector SL, Tan RA. Is a single blood eosinophil count a reliable marker for “eosinophilic asthma? J Asthma. 2012;49(8):807–810.
  • Flood-Page PT, Menzies-Gow AN, Kay AB, et al. Eosinophil’s role remains uncertain as anti-interleukin-5 only partially depletes numbers in asthmatic airway. Am J Respir Crit Care Med. 2003;167(2):199–204.
  • Alving K, Weitzberg E, Lundberg JM. Increased amount of nitric oxide in exhaled air of asthmatics. Eur Respir J. 1993;6(9):1368–1370.
  • Mummadi SR, Hahn PY. Update on exhaled nitric oxide in clinical practice. Chest. 2016;149(5):1340–1344.
  • Dweik RA, Boggs PB, Erzurum SC, et al. An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med. 2011;184(5):602–615.
  • Berry MA, Shaw DE, Green RH, et al. The use of exhaled nitric oxide concentration to identify eosinophilic airway inflammation: an observational study in adults with asthma. Clin Exp Allergy. 2005;35(9):1175–1179.
  • Jatakanon A, Lim S, Kharitonov SA, et al. Correlation between exhaled nitric oxide, sputum eosinophils, and methacholine responsiveness in patients with mild asthma. Thorax. 1998;53(2):91–95.
  • Silkoff PE, Lent AM, Busacker AA, et al. Exhaled nitric oxide identifies the persistent eosinophilic phenotype in severe refractory asthma. J Allergy Clin Immunol. 2005;116(6):1249–1255.
  • Corren J, Lemanske RF, Hanania NA, et al. Lebrikizumab treatment in adults with asthma. N Engl J Med. 2011;365(12):1088–1098.
  • Brusselle GG, Maes T, Bracke KR. Eosinophils in the spotlight: eosinophilic airway inflammation in nonallergic asthma. Nat Med. 2013;19(8):977–979.
  • Crespo A, Giner J, Torrejon M, et al. Clinical and inflammatory features of asthma with dissociation between fractional exhaled nitric oxide and eosinophils in induced sputum. J Asthma. 2016;53(5):459–464.
  • Petsky HL, Cates CJ, Lasserson TJ, et al. A systematic review and meta-analysis: tailoring asthma treatment on eosinophilic markers (exhaled nitric oxide or sputum eosinophils). Thorax. 2012;67(3):199–208.
  • Khanduja KL, Kaushik G, Khanduja S, et al. Corticosteroids affect nitric oxide generation, total free radicals production, and nitric oxide synthase activity in monocytes of asthmatic patients. Mol Cell Biochem. 2011;346(1–2):31–37.
  • Agusti A, Bel E, Thomas M, et al. Treatable traits: toward precision medicine of chronic airway diseases. Eur Respir J. 2016;47(2):410–419.
  • McNicholl DM, Stevenson M, McGarvey LP, et al. The utility of fractional exhaled nitric oxide suppression in the identification of nonadherence in difficult asthma. Am J Respir Crit Care Med. 2012;186(11):1102–1108.
  • Jia G, Erickson RW, Choy DF, et al. Periostin is a systemic biomarker of eosinophilic airway inflammation in asthmatic patients. J Allergy Clin Immunol. 2012;130(3):647-654.e10.
  • Simpson JL, Yang IA, Upham JW, et al. Periostin levels and eosinophilic inflammation in poorly-controlled asthma. BMC Pulm Med. 2016;16(1):67.
  • Woodruff PG, Boushey HA, Dolganov GM, et al. Genome-wide profiling identifies epithelial cell genes associated with asthma and with treatment response to corticosteroids. Proc Natl Acad Sci U S A. 2007;104(40):15858–15863.
  • Mouthuy J, Viart S, Ladjemi MZ, et al. Mite allergen-specific IgE is detectable in bronchial secretions of patients with nonatopic asthma and correlates with mucosal expression of periostin. J Allergy Clin Immunol. 2015;136(6):1685-1688e1681-1682.
  • Wagener AH, De Nijs SB, Lutter R, et al. External validation of blood eosinophils, FE(NO) and serum periostin as surrogates for sputum eosinophils in asthma. Thorax. 2015;70(2):115–120.
  • Froidure A, Mouthuy J, Durham SR, et al. Asthma phenotypes and IgE responses. Eur Respir J. 2016;47(1):304–319.
  • Cieslewicz G, Tomkinson A, Adler A, et al. The late, but not early, asthmatic response is dependent on IL-5 and correlates with eosinophil infiltration. J Clin Invest. 1999;104(3):301–308.
  • Djukanovic R, Wilson SJ, Kraft M, et al. Effects of treatment with anti-immunoglobulin E antibody omalizumab on airway inflammation in allergic asthma. Am J Respir Crit Care Med. 2004;170(6):583–593.
  • Westerhof GA, Korevaar DA, Amelink M, et al. Biomarkers to identify sputum eosinophilia in different adult asthma phenotypes. Eur Respir J. 2015;46(3):688–696.
  • Massanari M, Holgate ST, Busse WW, et al. Effect of omalizumab on peripheral blood eosinophilia in allergic asthma. Respir Med. 2010;104(2):188–196.
  • Pavord ID, Bafadhel M. Exhaled nitric oxide and blood eosinophilia: independent markers of preventable risk. J Allergy Clin Immunol. 2013;132(4):828–829.
  • Castro M, Wenzel SE, Bleecker ER, et al. Benralizumab, an anti-interleukin 5 receptor α monoclonal antibody, versus placebo for uncontrolled eosinophilic asthma: a phase 2b randomised dose-ranging study. Lancet Respir Med. 2014;2(11):879–890.
  • Khatry DB, Gossage DL, Geba GP, et al. Discriminating sputum-eosinophilic asthma: accuracy of cutoffs in blood eosinophil measurements versus a composite index, ELEN. J Allergy Clin Immunol. 2015;136(3):812–814.e812.
  • Johansson MW, Evans MD, Crisafi GM, et al. Serum periostin is associated with type 2 immunity in severe asthma. J Allergy Clin Immunol. 2016;137:1904-1907.e2.
  • Heaney LG, Djukanovic R, Woodcock A, et al. Research in progress: medical research council united kingdom refractory asthma stratification programme (RASP-UK). Thorax. 2016;71(2):187–189.
  • Belda J, Leigh R, Parameswaran K, et al. Induced sputum cell counts in healthy adults. Am J Respir Crit Care Med. 2000;161(2 Pt 1):475–478.
  • Hanania NA, Noonan M, Corren J, et al. Lebrikizumab in moderate-to-severe asthma: pooled data from two randomised placebo-controlled studies. Thorax. 2015;70(8):748–756.
  • Fowler SJ, Tavernier G, Niven R. High blood eosinophil counts predict sputum eosinophilia in patients with severe asthma. J Allergy Clin Immunol. 2015;135(3):822–824.e822.
  • Bjermer L, Lemiere C, Maspero J, et al. Reslizumab for inadequately controlled asthma with elevated blood eosinophil levels: a randomized phase 3 study. Chest. 2016. doi: 10.1016/j.chest.2016.03.032.
  • Castro M, Zangrilli J, Wechsler ME, et al. Reslizumab for inadequately controlled asthma with elevated blood eosinophil counts: results from two multicentre, parallel, double-blind, randomised, placebo-controlled, phase 3 trials. Lancet Respir Med. 2015;3(5):355–366.
  • Corren J, Weinstein S, Janka L, et al. Phase 3 Study of Reslizumab in Patients with Poorly Controlled Asthma: Effects Across a Broad Range of Eosinophil Counts. Chest. 2016. doi: 10.1016/j.chest.2016.03.018.
  • Ortega H, Katz L, Gunsoy N, et al. Blood eosinophil counts predict treatment response in patients with severe eosinophilic asthma. J Allergy Clin Immunol. 2015;136(3):825–826.
  • Katz LE, Gleich GJ, Hartley BF, et al. Blood eosinophil count is a useful biomarker to identify patients with severe eosinophilic asthma. Ann Am Thorac Soc. 2014;11(4):531–536.
  • Wenzel S, Castro M, Corren J, et al. Dupilumab efficacy and safety in adults with uncontrolled persistent asthma despite use of medium-to-high-dose inhaled corticosteroids plus a long-acting beta agonist: a randomised double-blind placebo-controlled pivotal phase 2b dose-ranging trial. Lancet. 2016.;388(10039):31–44.
  • Hillas G, Kostikas K, Mantzouranis K, et al. Exhaled nitric oxide and exhaled breath condensate pH as predictors of sputum cell counts in optimally treated asthmatic smokers. Respirology. 2011;16(5):811–818.
  • Alvarez-Puebla MJ, Rivera JMO, Almudevar E, et al. Cutoff point for exhaled nitric oxide corresponding to 3% sputum eosinophils. J Invest Allerg Clin. 2015;25(2):107–111.
  • Schneider A, Schwarzbach J, Faderl B, et al. FENO measurement and sputum analysis for diagnosing asthma in clinical practice. Respir Med. 2013;107(2):209–216.
  • Green RH, Pavord I. Stability of inflammatory phenotypes in asthma. Thorax. 2012;67(8):665–667.
  • Ortega H, Gleich G, Mayer B, et al. Reproducibility of a single blood eosinophil measurement as a biomarker in severe eosinophilic asthma. Ann Am Thorac Soc. 2015;12(12):1896–1897.
  • Nanda CR, Singapuri A, Soares M, et al. Domiciliary exhaled nitric oxide and eosinophilic airway inflammation in adults with asthma. Eur Respir J. 2016;48:242–244.
  • De Groot JC, Storm H, Amelink M, et al. Clinical profile of patients with adult-onset eosinophilic asthma. ERJ Open Res. 2016;2(2):00100–02015.
  • Boots AW, Bos LD, Van Der Schee MP, et al. Exhaled molecular fingerprinting in diagnosis and monitoring: validating volatile promises. Trends Mol Med. 2015;21(10):633–644.
  • Van Der Schee MP, Paff T, Brinkman P, et al. Breathomics in lung disease. Chest. 2015;147(1):224–231.
  • Van De Kant KD, Van Der Sande LJ, Jobsis Q, et al. Clinical use of exhaled volatile organic compounds in pulmonary diseases: a systematic review. Respir Res. 2012;13:117.
  • Ibrahim B, Basanta M, Cadden P, et al. Non-invasive phenotyping using exhaled volatile organic compounds in asthma. Thorax. 2011;66(9):804–809.
  • Plaza V, Crespo A, Giner J, et al. Inflammatory asthma phenotype discrimination using an electronic nose breath analyzer. J Investig Allergol Clin Immunol. 2015;25(6):431–437.
  • van der Schee MP, Palmay R, Cowan JO, et al. Predicting steroid responsiveness in patients with asthma using exhaled breath profiling. Clin Exp Allergy. 2013;43(11):1217–1225.
  • Wheelock CE, Goss VM, Balgoma D, et al. Application of ‘omics technologies to biomarker discovery in inflammatory lung diseases. Eur Respir J. 2013;42(3):802–825.
  • Leckie MJ, Brinke A, Khan J, et al. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyper-responsìveness, and the late asthmatic response. Lancet. 2000;356(9248):2144–2148.
  • Lambrecht BN, Hammad H. The immunology of asthma. Nat Immunol. 2015;16(1):45–56.
  • Yu S, Kim HY, Chang YJ, et al. Innate lymphoid cells and asthma. J Allergy Clin Immunol. 2014;133:943–950.
  • Spits H, Artis D, Colonna M, et al. Innate lymphoid cells–a proposal for uniform nomenclature. Nat Rev Immunol. 2013;13(2):145–149.
  • Smith SG, Chen R, Kjarsgaard M, et al. Increased numbers of activated group 2 innate lymphoid cells in the airways of patients with severe asthma and persistent airway eosinophilia. J Allergy Clin Immunol. 2016;137(1):75-86.e8.
  • Liu T, Wu J, Zhao J, et al. Type 2 innate lymphoid cells: a novel biomarker of eosinophilic airway inflammation in patients with mild to moderate asthma. Respir Med. 2015;109(11):1391–1396.
  • Lambrecht BN, Hammad H. Allergens and the airway epithelium response: gateway to allergic sensitization. J Allergy Clin Immunol. 2014;134(3):499–507.
  • Gauvreau GM, O’Byrne PM, Boulet LP, et al. Effects of an anti-TSLP antibody on allergen-induced asthmatic responses. N Engl J Med. 2014;370(22):2102–2110.
  • Nagarkar DR, Poposki JA, Tan BK, et al. Thymic stromal lymphopoietin activity is increased in nasal polyps of patients with chronic rhinosinusitis. J Allergy Clin Immunol. 2013;132(3):593–600e512.
  • Buchheit KM, Cahill KN, Katz HR, et al. Thymic stromal lymphopoietin controls prostaglandin D2 generation in patients with aspirin-exacerbated respiratory disease. J Allergy Clin Immunol. 2016;137(5):1566–1576e1565.
  • Holgate ST. Innate and adaptive immune responses in asthma. Nat Med. 2012;18(5):673–683.
  • Na HJ, Hamilton RG, Klion AD, et al. Biomarkers of eosinophil involvement in allergic and eosinophilic diseases: review of phenotypic and serum markers including a novel assay to quantify levels of soluble Siglec-8. J Immunol Methods. 2012;383(1–2):39–46.
  • Kiwamoto T, Kawasaki N, Paulson JC, et al. Siglec-8 as a drugable target to treat eosinophil and mast cell-associated conditions. Pharmacol Ther. 2012;135(3):327–336.
  • Denner DR, Sangwan N, Becker JB, et al. Corticosteroid therapy and airflow obstruction influence the bronchial microbiome, which is distinct from that of bronchoalveolar lavage in asthmatic airways. J Allergy Clin Immunol. 2016;137(5):1398–1405e1393.
  • Zhang Q, Cox M, Liang Z, et al. Airway microbiota in severe asthma and relationship to asthma severity and phenotypes. PLoS One. 2016;11(4):e0152724.
  • Pavord ID, Wardlaw AJ. The A to E of airway disease. Clin Exp Allergy. 2010;40(1):62–67.
  • Orie NG, Slutter HJ, De V, et al. Chronic nonspecific respiratory diseases. Ned Tijdschr Geneeskd. 1961;105:2136–2139.
  • Collins FS, Varmus H. A new initiative on precision medicine. N Engl J Med. 2015;372(9):793–795.
  • Sterk PJ. Chronic diseases like asthma and COPD: do they truly exist? Eur Respir J. 2016;47(2):359–361.
  • Global Initiative for Asthma. Global strategy for asthma management and prevention; 2016. Cited 2016 May 31. Available from: www.ginasthma.org