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International ERS/ATS guidelines on definition, evaluation and treatment of severe asthma

Kian Fan Chung, Sally E. Wenzel, Jan L. Brozek, Andrew Bush, Mario Castro, Peter J. Sterk, Ian M. Adcock, Eric D. Bateman, Elisabeth H. Bel, Eugene R. Bleecker, Louis-Philippe Boulet, Christopher Brightling, Pascal Chanez, Sven-Erik Dahlen, Ratko Djukanovic, Urs Frey, Mina Gaga, Peter Gibson, Qutayba Hamid, Nizar N. Jajour, Thais Mauad, Ronald L. Sorkness, W. Gerald Teague
European Respiratory Journal 2014 43: 343-373; DOI: 10.1183/09031936.00202013
Kian Fan Chung
1National Heart and Lung Institute, Imperial College, London
2Biomedical Research Unit, Royal Brompton Hospital, London
21Both authors contributed equally
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  • For correspondence: f.chung@imperial.ac.uk
Sally E. Wenzel
3Dept of Medicine, University of Pittsburgh, Pittsburgh, PA
21Both authors contributed equally
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Jan L. Brozek
4Dept of Clinical Epidemiology and Biostatistics and Medicine, McMaster University, Hamilton, Ontario
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Andrew Bush
1National Heart and Lung Institute, Imperial College, London
2Biomedical Research Unit, Royal Brompton Hospital, London
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Mario Castro
5Dept of Medicine, Washington University, St Louis, MO
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Peter J. Sterk
6Dept of Respiratory Medicine, Academic Medical Centre, Amsterdam, The Netherlands
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Ian M. Adcock
1National Heart and Lung Institute, Imperial College, London
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Eric D. Bateman
7Lung Institute, University of Cape Town, Cape Town, South Africa
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Elisabeth H. Bel
6Dept of Respiratory Medicine, Academic Medical Centre, Amsterdam, The Netherlands
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Eugene R. Bleecker
8Dept of Medicine, Wake Forest University, Winston Salem, NC
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Louis-Philippe Boulet
9Centre de Recherche de l’Institut Universitaire de Cardiologie et de Pneumologie de Quebec, Quebec, Quebec
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Christopher Brightling
10Institute for Lung Health, Leicester University, Leicester
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Pascal Chanez
11Departement des Maladies Respiratoires, Marseille Universite, Marseille, France
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Sven-Erik Dahlen
12Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden
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Ratko Djukanovic
13Southampton NIHR Respiratory Biomedical Research Unit, University of Southampton School of Medicine and Southampton General Hospital, Southampton UK
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Urs Frey
14University Children’s Hospital (UKBB), University of Basel, Basel, Switzerland
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Mina Gaga
15th, Athens, Greece
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Peter Gibson
16Hunter Medical Research Institute, John Hunter Hospital, Newcastle, Australia
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Qutayba Hamid
17Meakins-Christie Laboratories, McGill University, Montreal, Quebec, Canada
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Nizar N. Jajour
18Dept of Medicine, University of Wisconsin, Madison, WI
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Thais Mauad
19Dept of Pathology, University Medical School, Sao Paulo, Brazil
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Ronald L. Sorkness
18Dept of Medicine, University of Wisconsin, Madison, WI
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W. Gerald Teague
20Division of Respiratory Medicine, Allergy, and Immunology, Dept of Paediatrics, University of Virginia School of Medicine, VA, USA
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    Figure 1–

    Integration of factors, beginning with genetics, which may contribute to the ultimate phenotype of the severe asthma patient.

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    Figure 2–

    Potential immune-inflammatory and cellular interactions contributing to the pathogenesis of phenotypes of asthma. CXCL: CXC chemokine ligand; CCL24/26: CC chemokine ligand 24/26; DUOX: dual oxidase; EPO: eosinophil peroxidase; IFNγ: interferon-γ; IgE: immunoglobulin E; IL: interleukin; iNOS: inducible nitric oxide synthase; MUC5AC: mucin 5AC; NO: nitric oxide; OX40/L: CD134 ligand; PGD2: prostaglandin D2; Tc1: cytotoxic T-cell type 1; TGFβ: transforming growth factor-β; Th1: T-helper cell type 1; Th2: T-helper cell type 2; TSLP: thymic stromal lymphopoietin.

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  • Table 1– Recommendations
    ContextRecommendationStrengthQuality of evidenceValues and preferencesRemarks
    Computed tomography of chest1In children and adults with severe asthma without specific indications for chest HRCT based on history, symptoms and/or results of prior investigations we suggest that a chest HRCT only be done when the presentation is atypicalConditionalVery lowThis recommendation places a relatively high value on identification of alternative diagnosis and comorbidities and a relatively low value on avoiding potential complications and cost of chest HRCTAn atypical presentation of severe asthma includes such factors as, for example, excessive mucus production, rapid decline in lung function, reduced carbon monoxide transfer factor coefficient and the absence of atopy in a child with difficult asthma
    Sputum eosinophil counts2AIn adults with severe asthma: we suggest treatment guided by clinical criteria and sputum eosinophil counts performed in centres experienced in using this technique rather than by clinical criteria aloneConditionalVery lowThe recommendation to use sputum eosinophil counts to guide therapy in adults places a higher value on possible clinical benefits from adjusting the treatment in selected patients and on avoidance of inappropriate escalation of treatment and a lower value on increased use of resourcesBecause, at the present time, measurement of sputum eosinophils has not yet been sufficiently standardised and is not widely available we suggest such an approach be used only in specialised centres experienced in this technique. Patients who are likely to benefit from this approach are those who can produce sputum, demonstrate persistent or at least intermittent eosinophilia and have severe asthma with frequent exacerbations Clinicians should recognise that different choices will be appropriate for different patients
    2BIn children with severe asthma: we suggest treatment guided by clinical criteria alone rather than by clinical criteria and sputum eosinophil countsConditionalVery lowThe recommendation not to use sputum eosinophil counts to guide therapy in children places higher value on avoiding an intervention that is not standardised and not widely available and lower value on the uncertain and possibly limited clinical benefit
    Exhaled nitric oxide3We suggest that clinicians do not use FeNO to guide therapy in adults or children with severe asthmaConditionalVery lowThis recommendation places a higher value on avoiding additional resource expenditure and a lower value on uncertain benefit from monitoring FeNO
    Anti-IgE antibody
    (omalizumab)
    4In patients with severe allergic asthma we suggest a therapeutic trial of omalizumab both in adults and in childrenConditionalLow (adults)
    Very low (children)
    This recommendation places higher value on the clinical benefits from omalizumab in some patients with severe allergic asthma and lower value on increased resource useThose adults and children aged ≥6 years with severe asthma who are considered for a trial of omalizumab, should have confirmed IgE-dependent allergic asthma uncontrolled despite optimal pharmacological and non-pharmacological management and appropriate allergen avoidance if their total serum IgE level is 30–700 IU·mL−1 (in three studies the range was wider: 30–1300 IU·mL−1) Treatment response should be globally assessed by the treating physician taking into consideration any improvement in asthma control, reduction in exacerbations and unscheduled healthcare utilisation, and improvement in quality of life If a patient does not respond within 4 months of initiating treatment, it is unlikely that further administration of omalizumab will be beneficial
    Methotrexate5We suggest that clinicians do not use methotrexate in adults or children with severe asthmaConditionalLowThis recommendation places a relatively higher value on avoiding adverse effects of methotrexate and a relatively lower value on possible benefits from reducing the dose of systemic corticosteroidsEvidence from randomised trials is only available for adults Because of the probable adverse effects of methotrexate and need for monitoring therapy we suggest that any use of methotrexate is limited to specialised centres and only in patients who require daily OCS If a decision to use methotrexate is made chest radiography, complete blood count with differential and platelets, liver function tests, serum creatinine and DLCO are recommended prior to and after commencing therapy
    Macrolide antibiotics6We suggest that clinicians do not use macrolide antibiotics in adults and children with severe asthma for the treatment of asthmaConditionalVery lowThis recommendation places a relatively higher value on prevention of development of resistance to macrolide antibiotics, and relatively lower value on uncertain clinical benefitsThis recommendation applies only to the treatment of asthma; it does not apply to the use of macrolide antibiotics for other indications, e.g. treatment of bronchitis, sinusitis or other bacterial infections as indicated
    Antifungal agents7AWe suggest antifungal agents in adults with severe asthma and recurrent exacerbations of ABPAConditionalVery lowThe recommendation to use antifungal agents in patients with severe asthma and ABPA places a higher value on possible reduction of the risk of exacerbations and improved symptoms, and a lower value on avoiding possible adverse effects, drug interactions and increased use of resourcesIn children, the evidence is limited to isolated case reports Children should be treated with antifungals only after the most detailed evaluation in a specialist severe asthma referral centre As antifungal therapies are associated with significant and sometimes severe side-effects, including hepatotoxicity, clinicians should be familiar with these drugs and follow relevant precautions in monitoring for these side-effects, observing the limits to the duration of treatment recommended for each
    7BWe suggest that clinicians do not use antifungal agents for the treatment of asthma in adults and children with severe asthma without ABPA irrespective of sensitisation to fungi (i.e. positive skin prick test or fungus-specific IgE in serum)ConditionalVery lowThe recommendation not to use antifungal agents in patients with severe asthma without confirmed ABPA (irrespective of sensitisation) places a higher value on avoiding possible adverse effects, interactions of antifungal agents with other medications and increased use of resources, and a lower value on uncertain possible benefitsThe recommendation not to use antifungal agents in patients with severe asthma without confirmed ABPA applies only to the treatment of asthma; it does not apply to the use of antifungal agents for other indications, e.g. treatment of invasive fungal infections
    Bronchial thermoplasty8We recommend that bronchial thermoplasty is performed in adults with severe asthma only in the context of an Institutional Review Board approved independent systematic registry or a clinical study (recommendation, quality evidence)StrongVery lowThis recommendation places a higher value on avoiding adverse effects, on an increased use of resources, and on a lack of understanding of which patients may benefit, and a lower value on the uncertain improvement in symptoms and quality of lifeThis is a strong recommendation, because of the very low confidence in the currently available estimates of effects of bronchial thermoplasty in patients with severe asthma Both potential benefits and harms may be large and the long-term consequences of this new approach to asthma therapy utilising an invasive physical intervention are unknown Specifically designed studies are needed to define its effects on relevant objective primary outcomes, such as exacerbation rates, and on long-term effects on lung function Studies are also needed to better understand the phenotypes of responding patients, its effects in patients with severe obstructive asthma (FEV1 <60% of predicted value) or in whom systemic corticosteroids are used, and its long-term benefits and safety Further research is likely to have an important impact on this recommendation
    • HRCT: high-resolution computed tomography; FeNO: exhaled nitric oxide fraction; OCS: oral corticosteroids; DLCO: transfer factor of the lung for carbon monoxide; ABPA: allergic bronchopulmonary aspergillosis; FEV1: forced expiratory volume in 1 s.

  • Table 2– Interpretation of strong and conditional recommendations
    Implications forStrong recommendationConditional recommendation
    PatientsMost individuals in this situation would want the recommended course of action, and only a small proportion would notThe majority of individuals in this situation would want the suggested course of action, but many would not
    CliniciansMost individuals should receive the intervention Adherence to this recommendation according to the guideline could be used as a quality criterion or performance indicator Formal decision aids are not likely to be needed to help individuals make decisions consistent with their values and preferencesRecognise that different choices will be appropriate for individual patients and that you must help each patient arrive at a management decision consistent with his or her values and preferences Decision aids may be useful in helping individuals to make decisions consistent with their values and preferences
    Policy makersThe recommendation can be adopted as policy in most situationsPolicy making will require substantial debate and involvement of various stakeholders
  • Table 3– Definition of severe asthma for patients aged ≥6 years
    Asthma which requires treatment with guidelines suggested medications for GINA steps 4–5 asthma (high dose ICS# and LABA or leukotriene modifier/theophylline) for the previous year or systemic CS for ≥50% of the previous year to prevent it from becoming “uncontrolled” or which remains “uncontrolled“ despite this therapy
     Uncontrolled asthma defined as at least one of the following:
      1) Poor symptom control: ACQ consistently ≥1.5, ACT <20 (or “not well controlled” by NAEPP/GINA guidelines)
      2) Frequent severe exacerbations: two or more bursts of systemic CS (≥3 days each) in the previous year
      3) Serious exacerbations: at least one hospitalisation, ICU stay or mechanical ventilation in the previous year
      4) Airflow limitation: after appropriate bronchodilator withhold FEV1 <80% predicted (in the face of reduced FEV1/FVC defined as less than  the lower limit of normal)
     Controlled asthma that worsens on tapering of these high doses of ICS or systemic CS (or additional biologics)
    • #: the definition of high dose inhaled corticosteroids (ICS) is age-specific (table 4). GINA: Global Initiative for Asthma; LABA: long-acting β2-agonists; CS: corticosteroids; ACQ: Asthma Control Questionnaire; ACT: Asthma Control Test; NAEPP National Asthma Education and Prevention Program.

  • Table 4– Definition of high daily dose of various inhaled corticosteroids in relation to patient age
    Inhaled corticosteroidThreshold daily dose in μg considered as high
    Age 6–12 yearsAge >12 years
    Beclomethasone dipropionate≥800 (DPI or CFC MDI)
    ≥320 (HFA MDI)
    ≥2000 (DPI or CFC MDI)
    ≥1000 (HFA MDI)
    Budesonide≥800 (MDI or DPI)≥1600 (MDI or DPI)
    Ciclesonide≥160 (HFA MDI)≥320 (HFA MDI)
    Fluticasone propionate≥500 (HFA MDI or DPI)≥1000 (HFA MDI or DPI)
    Mometasone furoate≥500 (DPI)≥800 (DPI)
    Triamcinolone acetonide≥1200≥2000
    • Notes: 1) Designation of high doses is provided from manufacturers' recommendations where possible. 2) As chlorofluorocarbon (CFC) preparations are being taken from the market, medication inserts for hydrofluoroalkane (HFA) preparations should be carefully reviewed by the clinician for the equivalent correct dosage. DPI: dry powder inhaler; MDI: metered-dose inhaler.

  • Table 5– Priority questions on phenotypes
    1) The validation of the eosinophilic versus non-eosinophilic, and of the Th2 predominant versus non-Th2 asthma phenotype, are they persistent over time and do they predict distinct natural histories?
    2) Are risk factors, comorbid factors and natural history also governed by specific immune-inflammatory phenotypes?
    3) Are there genetic, epigenetic and inflammatory biomarkers of specific phenotypes or characteristics of severe asthma?
    4) Is the innate immune response abnormal in severe asthma, and do these contribute to inflammation and remodelling of the airways?
    5) What is the relationship between structural determinants, inflammation and airway function in severe asthma, and can imaging be used to noninvasively address these issues?
    6) Is there an altered microbiome and virobiome in the airways of severe asthma?
    • Th: T-helper cell.

  • Table 6– Diseases which can masquerade as severe asthma
    Children
     Dysfunctional breathing/vocal cord dysfunction
     Bronchiolitis
     Recurrent (micro)aspiration, reflux, swallowing dysfunction
     Prematurity and related lung disease
     Cystic fibrosis
     Congenital or acquired immune deficiency
     Primary ciliary dyskinesia
     Central airways obstruction/compression
     Foreign body
     Congenital malformations including vascular ring
     Tracheobronchomalacia
     Carcinoid or other tumour
     Mediastinal mass/enlarged lymph node
     Congenital heart disease
     Interstitial lung disease
     Connective tissue disease
    Adults
     Dysfunctional breathlessness/vocal cord dysfunction
     Chronic obstructive pulmonary disease
     Hyperventilation with panic attacks
     Bronchiolitis obliterans
     Congestive heart failure
     Adverse drug reaction (e.g. angiotensin-converting enzyme inhibitors)
     Bronchiectasis/cystic fibrosis
     Hypersensitivity pneumonitis
     Hypereosinophilic syndromes
     Pulmonary embolus
     Herpetic tracheobronchitis
     Endobronchial lesion/foreign body (e.g. amyloid, carcinoid, tracheal stricture)
     Allergic bronchopulmonary aspergillosis
     Acquired tracheobronchomalacia
     Churg–Strauss syndrome
  • Table 7– Comorbidities and contributory factors
    1) Rhinosinusitis/(adults) nasal polyps
    2) Psychological factors: personality trait, symptom perception, anxiety, depression
    3) Vocal cord dysfunction
    4) Obesity
    5) Smoking/smoking related disease
    6) Obstructive sleep apnoea
    7) Hyperventilation syndrome
    8) Hormonal influences: premenstrual, menarche, menopause, thyroid disorders
    9) Gastro-oesophageal reflux disease (symptomatic)
    10) Drugs: aspirin, non-steroidal anti-inflammatory drugs (NSAIDs), β-adrenergic blockers, angiotensin-converting enzyme inhibitors
  • Table 8– Placebo-controlled studies of potential new treatments in severe asthma
    First author [ref.]SeveritySubjects nDesignTreatmentOutcomesSummary results
    Wenzel [99]Severe309R, db, pc, pGolimumab, anti TNF-α, 24 weeksFEV1, exacerbations AQLQ, PEFRFEV1 unchanged, no reduction in exacerbations, AQLQ, PEFR Adverse profile side-effects
    Pavord [56]Severe, with ≥2 exacerbations in past year621R, db, pc, pMepolizumab (75, 250 or 750 mg infusions at 4 weeks), anti-IL-5, 52 weeksRate of exacerbationsAll doses reduced exacerbations by 39–52% No effect on ACQ, AQLQ or FEV1
    Haldar [157]Severe61R, db, pc, pMepolizumab, anti-IL5, 50 weeksExacerbations, symptoms, FEV1, AQLQ, AHR, sputum and blood eosinophilsReduced exacerbations Improved AQLQ Reduced eosinophils
    Nair [58]Severe20R, db, pc, pMepolizumab, anti-IL5, 50 weeksExacerbations, oral steroid reductionReduced exacerbations, eosinophils and OCS dose
    Kips [159]Severe26R, db, pc, pSCH55700, anti-IL-5, 12 weeksSputum and blood eosinophils, symptoms, FEV1Reduced blood sputum eosinophils No other significant outcomes
    Castro [57]Poorly controlled on high-dose inhaled CS53R, db, pc, pReslimuzab, anti-IL-5, 12 weeksACQ, FEV1, Sputum eosinophilsImproved ACQ score Reduction in sputum eosinophils Improved FEV1
    Corren [160]Moderate-severe294R, db, pc, pAMG317, anti-IL-4Rα antibody, blocks IL-4 and IL-13, 12 weeksACQ scores, exacerbationsNo effect on ACQ or exacerbations
    Corren [59]Moderate-severe219R, db, pc, pLebrikizumab, anti-IL13 antibody, 24 weeksChange in pre-bronchodilator FEV1Improved FEV1, compared with placebo, with greatest changes in high levels of periostin or FeNO group (post hoc analyses) No effect on ACQ-5 or diary measures Exacerbations were 60% lower in treated group with high Th2
    Piper [60]Moderate-to-severe194R, db, pc, pTralokinumab (150, 300, or 600 mg), IL-13 neutralising monoclonal antibody, 3 monthsChange from baseline in ACQ-6 at week 13No change in ACQ-6 at 13 weeks FEV1 increase of 0.21 L versus 0.06 L with placebo (p=0.072) β2-agonist use decrease of -0.68 versus -0.10 with placebo (p=0.020) Better response in those with higher IL-13 levels in sputum
    Humbert [161]Severe, CS-dependent44R, db, pc, pMasitinib (3, 4.5 and 6 mg·kg−1·day−1), c-kit and PDGFR tyrosine kinase inhibitor, 16 weeksOCS dose ACQ, FEV1No difference in OCS dose
    ACQ improved, no difference in FEV1
    Busse [162]Moderate-to-severeR, db, pc, pDaclizumab, IL-2Rα chain antibody, 20 weeksChange in FEV1 (%)
    Asthma exacerbations
    Improved FEV1 Reduction in day-time asthma scores, use of SABA Prolonged time to severe exacerbations Reduction in blood eosinophils
    Nair [163]Severe asthma34R, db, pc, pSCH527123, CXCR2 receptor antagonist, 4 weeksChanges in sputum and neutrophil activation markersReduction in blood and sputum neutrophil Reduction in mild exacerbations No reduction in ACQ score (p=0.053)
    • R: Randomised; db: double-blind; pc: placebo-controlled; p: parallel; TNF-α: tumour necrosis factor-α; FEV1: forced expiratory volume in 1 s; AQLQ: Asthma Quality of Life Questionnaire; PEFR: peak expiratory flow rate; IL: interleukin; ACQ: Asthma Control Questionnaire; AHR: airway hyperresponsiveness; OCS: oral corticosteroids; CS: corticosteroids; FeNO: exhaled nitric oxide fraction; Th2: T-helper cell type 2; c-kit: stem cell factor receptor; PDGFR: platelet-derived growth factor receptor; IL-2Rα: IL-2 receptor-α; SABA: short-acting β-agonist.

  • Table 9– Potential phenotype-targeted therapies in severe asthma#
    CharacteristicAssociationsSpecifically targeted treatments
    Severe allergic asthmaBlood and sputum eosinophilsAnti-IgE (adults and children)
    High serum IgEAnti-IL-4/IL-13
    High FeNOAnti-IL-4 receptor
    Eosinophilic asthmaBlood and sputum eosinophilsAnti-IL-5
    Recurrent exacerbationsAnti-IL-4/IL-13
    High FeNOAnti-IL-4 receptor
    Neutrophilic asthma¶Corticosteroid insensitivityAnti-IL-8
    Bacterial infectionsCXCR2 antagonists
    Anti-LTB4 (adults and children)
    Macrolides (adults and children)
    Chronic airflow obstructionAirway wall remodelling as increased airway wall thicknessAnti-IL-13
    Bronchial thermoplasty
    Recurrent exacerbationsSputum eosinophils in sputumAnti-IL5
    Reduced response to ICS and/or OCSAnti-IgE (adults and children)
    Corticosteroid insensitivityIncreased neutrophils in sputum¶p38 MAPK inhibitors
    Theophylline (adults and children)
    Macrolides (adults and children)
    • FeNO: exhaled nitric oxide fraction; IL: interleukin; LTB4: leukotriene B4; ICS: inhaled corticosteroid; OCS: oral corticosteroid; MAPK: mitogen-activated protein kinase. #: Unless otherwise stated, these potential treatments apply to adults; ¶: neutrophilic asthma is rare in children.

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    • E.D. Bateman
    • N.N. Jajour
    • R.L. Sorkness
    • P.J. Sterk
    • W.G. Teague
    • S.E. Wenzel
    • E.H. Bel
    • E.R. Bleecker
    • L-P. Boulet
    • C. Brightling
    • M. Castro
    • K.F. Chung
    • M. Gaga
    • P. Gibson
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    • New guidelines for severe asthma provide an updated definition of the disease and a new plan to tackle it - A new guideline has provided an updated definition of severe asthma along with new recommendations for treating the condition.
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International ERS/ATS guidelines on definition, evaluation and treatment of severe asthma
Kian Fan Chung, Sally E. Wenzel, Jan L. Brozek, Andrew Bush, Mario Castro, Peter J. Sterk, Ian M. Adcock, Eric D. Bateman, Elisabeth H. Bel, Eugene R. Bleecker, Louis-Philippe Boulet, Christopher Brightling, Pascal Chanez, Sven-Erik Dahlen, Ratko Djukanovic, Urs Frey, Mina Gaga, Peter Gibson, Qutayba Hamid, Nizar N. Jajour, Thais Mauad, Ronald L. Sorkness, W. Gerald Teague
European Respiratory Journal Feb 2014, 43 (2) 343-373; DOI: 10.1183/09031936.00202013

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International ERS/ATS guidelines on definition, evaluation and treatment of severe asthma
Kian Fan Chung, Sally E. Wenzel, Jan L. Brozek, Andrew Bush, Mario Castro, Peter J. Sterk, Ian M. Adcock, Eric D. Bateman, Elisabeth H. Bel, Eugene R. Bleecker, Louis-Philippe Boulet, Christopher Brightling, Pascal Chanez, Sven-Erik Dahlen, Ratko Djukanovic, Urs Frey, Mina Gaga, Peter Gibson, Qutayba Hamid, Nizar N. Jajour, Thais Mauad, Ronald L. Sorkness, W. Gerald Teague
European Respiratory Journal Feb 2014, 43 (2) 343-373; DOI: 10.1183/09031936.00202013
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    • 1. Task Force definition of severe asthma
    • 2. Phenotyping: epidemiology, pathogenesis, pathobiology, structure and physiology
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