Using Patient Characteristics to Individualize and Improve Asthma Care

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1 Using Patient Characteristics to Individualize and Improve Asthma Care Leonard B. Bacharier, M.D. Associate Professor of Pediatrics Clinical Director, Division of Allergy, Immunology, & Pulmonary Medicine

2 Outline Variability and heterogeneity of childhood asthma Asthma phenotypes Clinical features Inflammatory patterns Molecular phenotypes Phenotype-dependent therapeutic responses

3 Asthma - Definition Asthma is a complex (and heterogeneous) disorder (or collection of disorders) characterized by variable and recurring symptoms, airflow obstruction, airway hyperresponsiveness, and underlying inflammation. The interaction of these features determines the clinical manifestations, severity of asthma, and the response to treatment. Modified from NAEPP/EPR3

4 Asthma - Working Definition A chronic inflammatory disorder of the airways in which many cells and cellular elements play a role: in particular, mast cells, eosinophils, neutrophils, T lymphocytes, macrophages, and epithelial cells. In susceptible individuals, this inflammation causes recurrent episodes of coughing (particularly at night or early in the morning), wheezing, breathlessness and chest tightness. These episodes are usually associated with widespread but variable airflow obstruction that is often reversible either spontaneously or with treatment. Modified from NAEPP/EPR3

5 Phenotype Wilhelm Johannsen coined the term phenotype in 1910 Phenotype = a group of organisms, which in outward appearance seemed to belong to one type A set of observable characteristics that can be used to classify organisms into discrete groups

6 Asthma Phenotypes CLINICAL FEATURES Age of onset Triggers Allergen Infection Exercise Atopic vs non-atopic Natural history Severity Exacerbation-prone Response to therapy PATHOPHYSIOLOGY Pattern of inflammation Eosinophilic Neutrophilic Pauci-granulocytic Biomarkers eno, EBC, ULTE 4 Lung function Normal vs abnormal Reversible vs fixed obstruction (BD, steroids) AHR Asthma Is A Heterogeneous Disorder

7 FIXED OBSTRUCTION SEVERE EXACERBATION PRONE EXERCICE-INDUCED EOSINOPHILIC CORTICOSTEROID RESPONSIVE ALLERGIC Wenzel SE. Lancet 2006:368:804-13

8 Preschool Wheezing Phenotypes

9 Patterns of Early Childhood Wheezing Pattern of Wheeze During 1 st 6 Years 0-3 Years 4-6 Years % of Cohort Never Wheeze 51% Transient Early Wheeze Late-Onset Wheeze Persistent Wheeze 20% 15% 14% Tucson Children s Respiratory Study Martinez FD et al NEJM 1995;332:133

10 Early Life Wheezing Phenotypes Correlate with Wheezing at 16 Years Relative Risk for Wheeze at 16 years of age * 3.8 * Never Wheeze Transient Late Onset Persistent Wheeze Pattern Before 6 years of age * p<0.001 compared with never wheezers Tucson Children s Respiratory Study Morgan WJ et al AJRCCM 2005;172:1253

11 Asthma Predictive Index (API) Identify high risk children (ages 2 & 3 yrs) 4 wheezing episodes in the past year (at least one must be MD diagnosed) AND One major criterion Parent with MD asthma MD atopic dermatitis Aeroallergen sensitivity OR Two minor criteria Food sensitivity Peripheral eosinophilia (³4%) Wheezing not related to infection Modified from Castro-Rodriguez JA et al. Am J Respir Crit Care Med 2000;162:1403-6

12 Asthma Predictive Index (API) Active Asthma OR (95% CI) Positive Predictive Value (%) Negative Predictive Value (%) At Yr 6 At Yr ( ) 5.7 ( ) 47.5% 91.6% 51.5% 84.2% Castro-Rodriguez JA et al Am J Respir Crit Care Med 2000;162:1403-6

13 High Rate of Allergic Sensitization Among API+ Children Food 5% Neither 40% Food and Aeroallergen 26% Aeroallergen 29% Guilbert TW et al. J Allergy Clin Immunol 2004;114:1282-7

14 Distinguishing Phenotypes of Early Childhood Wheeze Using Latent Class Analysis 1650 white children recruited in 1990 at age 0-5 yrs Questionnaires in 1990, 1998, and 2003 Between , nested sample of 795 children invited for physiologic measures and interviews 222 w/parent reported wheeze and 367 asymptomatic Phenotypes identified based upon 1 st 2 surveys (1990 and ) Prognosis across phenotypes examined Spycher BD et al. ERJ 2008;31:

15 Distinguishing Phenotypes of Early Childhood Wheeze Using Latent Class Analysis 3 Phenotypes of Wheeze Identified Phenotype C Atopic persistent wheeze Attacks with and without colds. Nocturnal symptoms present. Lower lung function and greater BHR. Phenotype D Non-atopic persistent wheeze less frequent attacks than C. Attacks with and without colds. Normal lung function and BHR. Phenotype E - Transient viral wheeze attacks prior to 1 st survey & subsided by 2 nd survey. Only with colds. Normal lung function, but slightly greater BHR. Spycher BD et al. ERJ 2008;31:

16 Distinguishing Phenotypes of Early Childhood Wheeze Using Latent Class Analysis Current wheeze in past 12 months 4 or more wheeze attacks in past 12 months Bronchodilator use in past 12 months Cough without colds White = 8-13yrs; Grey = 13-18yrs Spycher BD et al. ERJ 2008;31:

17 Inflammation Related Phenotypes

18 Airway Inflammation Most data derived from adult studies Similar patterns demonstrated in children Many cells and cellular elements play a role: Mast cells Eosinophils Neutrophils T lymphocytes Macrophages Dendritic cells Epithelial cells

19 How to Measure Airway Inflammation Invasive Assessments Upper airway sampling Bronchoscopy-based techniques Bronchoalveolar lavage Biopsies

20 Noninvasive Measures Blood Non-Airway Derived Eosinophil counts Eosinophil cationic protein (ECP) Cytokines, sil-2r, sicam1, svcam Urine LTE 4 Eosinophil protein X (EPX) PGE2

21 Noninvasive Measures Airway Derived Exhaled air Exhaled nitric oxide Induced sputum Cellular composition Eosinophil cationic protein Cytokines and other mediators Exhaled breath condensate ph Markers of oxidative stress Leukotrienes Products of nitric oxide metabolism Airway hyperresponsiveness

22 Inflammation-Related Phenotypes NORMAL NEUTROPHILIC EOSINOPHILIC PAUCI-GRANULOCYTIC

23 Exhaled Nitric Oxide (NO) as a Phenotypic Biomarker Normal epithelial cells Minimal release of NO Activated epithelial cells during inflammation Increased production of NO NO is an endogenous regulatory molecule widely distributed throughout the body NO synthesis is mediated by a family of enzymes, the NO synthases (NOS) Inducible NOS-derived NO is predominantly produced in the bronchial epithelial cells NO increases when there is eosinophilic airway inflammation Yates DH. Immunol Cell Biol. 2001;79(2):

24 Association Between Exhaled NO and Eosinophilic Airway Inflammation Sputum eosinophil count (%) P<.001 R=0.52 Flow rate: 250 ml/s Exhaled NO concentration (ppb) Male Female Berry MA et al. Clin Exp Allergy. 2005;35(9):

25 How Do Clinicians Decide Which Medication Is Most Appropriate For A Given Patient?

26 Typical Patterns of Medical Decision Making Trial & Error & One Size Fits All 2 therapeutic approaches (A & B) compared in clinical trial(s) Heterogeneous populations studied 1 approach (A) demonstrated to be statistically superior to the comparator (B) Thus, approach A is adopted as the preferred approach, which then gets incorporated into treatment guidelines, managed care algorithms, etc. However, is this really the best strategy for determining therapy for the individual patient?

27 Stepwise Approach for Managing Asthma in Children 5-11 Years of Age Intermittent Asthma Persistent Asthma: Daily Medication Consult with asthma specialist if step 4 care or higher is required. Consider consultation at step 3. Step 1 Preferred: SABA PRN Step 2 Preferred: Low-dose ICS Alternative: LTRA, Cromolyn, Nedocromil, or Theophylline Step 3 Preferred: EITHER: Low-dose ICS + either LABA, LTRA, or Theophylline OR Medium-dose ICS Step 4 Preferred: Medium-dose ICS + LABA Alternative: Medium-dose ICS + either LTRA or Theophylline Step 5 Preferred: High-dose ICS + LABA Alternative: High-dose ICS + either LTRA or Theophylline Step 6 Preferred: High-dose ICS + LABA + Oral Systemic Corticosteroid Alternative: High-dose ICS + either LTRA or Theophylline + Oral Corticosteroid Each Step: Patient education, environmental control, and management of comorbidities Step 2-4: Consider subcutaneous allergen immunotherapy for patients who have allergic asthma Quick Relief Medications for All Patients SABA as needed for symptoms. Intensity of treatment depends on severity of symptoms. Up to 3 treatments at 20-minute intervals as needed. Short course of systemic corticosteroids may be needed. Caution: increasing use of beta-agonist, or use >2 times/week for symptom control (not prevention of EIB) indicates inadequate control and the need to step up treatment. Step up if needed (first, check adherence and environmental control) Assess control Step down if possible (and asthma is well controlled at least 3 months)

28 Using Phenotypes to Help Predict Response to Therapy

29 CLIC - Study Timeline Assessment/ Characterization Treatment Phase Randomization Mt FP Week Consent Asthma Hx Review diary Review diary eno eno eno Spirometry BD response Spirometry Spirometry Biomarkers Methacholine Genetics Skin testing Diary and PFM Szefler S et al. J Allergy Clin Immunol 2005;115: Mt FP FP Mt FP Visit Mt

30 Variability in Response to Therapy Mean Change in FEV 1 : FP 6.8% (0.96), Mt 1.9% (0.87) Participants, % <-30 <-30 to to < to <-15 No change -15 to < to <-5-5 to <0 0 to <5 5 to <10 10 to <15 15 to <20 20 to <25 25 to <30 Change in FEV 1 from Baseline, % FP (n=126) Mt (n=126) 30 to <35 35 to <40 >=40 Szefler S et al. J Allergy Clin Immunol 2005;115:233-42

31 Primary Outcome: FEV 1 Response FEV 1 % Change with Mt >7.5% Mt Response Concordance Correlation 0.54 (0.43, 0.65) Mt alone n=6 (5%) Neither n=69 (55%) Both n=22 (17%) FP alone n=29 (23%) >7.5% FP Response FEV 1 % Change with FP Szefler S et al. J Allergy Clin Immunol 2005;115:233-42

32 The efficacies of the various classes of medications are not equal among all patients and may be affected by asthma phenotypes, as well as environmental exposures and genetic differences. Can We Use Individual Patient Characteristics to Better Categorize Asthma? Potentially leading to more individualized treatment decisions

33 FEV 1 Response 7.5%: Median Baseline Characteristics Baseline Characteristic Both (n=22) FP only (n=29) Mt only (n=6) Neither (n=69) FEV 1 % predicted (pre-bd) FEV 1 /FVC (pre-bd) BD max (% increase) Methacholine PC 20 (mg/ml) eno (ppb) TEC (cells/mm 3 ) Serum ECP (mg/l) IgE (ku/l) Urinary LTE 4 (pg/mg) Asthma Free Days/Wk Szefler S et al. J Allergy Clin Immunol 2005;115:233-42

34 Is There Variation in Response to Therapy Within a Given Phenotype?

35 Phenotype: months of age Recurrent wheezing The PEAK Trial Positive asthma predictive index (API) Screening/ Eligibility Run-in Treatment FP 88mcg BID or Placebo Observation 1 month Years 1 & 2 Year 3 Randomize Interim Efficacy Tests Guilbert TW et al. NEJM 2006;354:

36 ICS Therapy Increases the Proportion of Episode-Free Days in API+ Children Treatment Observation Proportion of Episode-free Days ICS Placebo p<0.05 p< Months Guilbert TW et al. NEJM 2006;354:

37 Heterogeneity of ICS Response Within the API+ Population Stratifying Variable ICS Mean (95% CI) Percentage of EFDs Placebo Mean (95% CI) Difference (95% CI) P-value (ICS vs Placebo) Male 93 (92, 95) 86 (83, 89) 7.3 (3.9, 11.1) Female 92 (89, 94) 92 (89, 94) 0.1 (-3.4, 3.5) 0.9 Caucasian 93 (91, 95) 84 (80, 88) 9.1 (4.8, 13.9) Non-Caucasian 92 (89, 94) 93 (91, 94) -1.0 (-3.9, 1.7) 0.6 Run-In EFD <80% 92 (90, 94) 84 (79, 87) 8.6 (4.2, 13.2) Run-In EFD >=80% 93 (91, 95) 93 (91, 95) 0.0 (-2.5, 2.5) 0.9 ED/Hospitalization History 95 (93, 96) 87 (83, 90) 7.7 (3.9, No ED/Hospitalization History 90 (87, 92) 91 (89, 93) -1.1 (-4.4, 2.1) Positive Aeroallergen Skin Test 93 (91, 94) 86 (83, 89) 6.5 (3.2, 10.0) Negative Aeroallergen Skin Test 93 (90, 95) 92 (89, 94) 0.9 (-2.5, 4.4) 0.6 Bacharier LB et al. J Allergy Clin Immunol 2009:123:

38 Can the degree or pattern of airway inflammation influence response to therapy?

39 PACT: Study Overview 285 children 6-14 years of age with uncontrolled mild-moderate asthma FEV 1 80% predicted Methacholine PC mg/ml 2-week run-in Randomization 48-week treatment period 2 clinic visits 8 study encounters at 6-week intervals All participants receive: morning diskus evening diskus evening capsule albuterol prn ICS fluticasone fluticasone placebo LTRA placebo placebo montelukast Modified from Sorkness CA et al. J Allergy Clin Immunol 2007;119:64-72

40 PACT: Asthma Control Days p = Percent Asthma Control Days % 51% Effect Size: Asthma Control Days/year 0 Fluticasone Montelukast MORE ACDs 186 Sorkness CA et al. J Allergy Clin Immunol 2007;119:64-72

41 Therapeutic Response Varies by Baseline FeNO Level Percent Asthma Control Days Fluticasone 55 Montelukast Entire Cohort FeNO <25ppb FeNO 25ppb MORE ACDs

42 Phenotypic Predictors of Differential Predictor ACQ eno Eosinophils IgE Parental asthma PC 20 (mg/ml) Response to ICS and LTRA Subgroup Avg diff (FP-Mt) > <25ppb ppb 23.0 <5% % kU/L -2.3 >150kU/L 16.6 No 3.9 Yes < Percentage ACDs P values for interaction between treatment and predictor: univariate (multivariate) models Multivariate model also included ULTE4, Age at diagnosis, Age at entry, ICS use in past yr P-value 0.08 (0.3) (0.01) 0.05 (0.9) 0.03 (0.6) 0.07 (0.02) (0.2) Knuffman J et al. J Allergy Clin Immunol 2009; 123:411-6

43 Molecular Phenotyping Asthma is characterized by a Th2 type inflammation (IL-4, IL-5, IL-13) Is there heterogeneity in underlying mechanisms related to Th2 inflammation? 42 adults with mild-moderate asthma compared with 28 healthy controls Using gene expression approaches on airway epithelial brushings, 2 distinct subgroups identified Th2- high Th2- low Woodruff PG et al. Am J Respir Crit Care Med 2009;180:388-95

44 Molecular Phenotyping Normal Th2 Low Th2 High N P-value, Low vs. High Age (yrs) FEV 1 (% predicted) FEV 1 with albuterol (%) Methacholine PC 20 (mg/ml) <0.001 IgE (IU/mL) Blood Eos (x10 9 /L) BAL Eos (%) Woodruff PG et al. Am J Respir Crit Care Med 2009;180:388-95

45 Molecular Phenotyping 8 week randomized controlled trial of fluticasone 500mcg BID vs placebo Improvements in FEV 1 limited to the Th2 high group FEV1 (L) Placebo Th2 high Fluticasone Th2 low Fluticasone * * Weeks Woodruff PG et al. Am J Respir Crit Care Med 2009;180:388-95

46 Molecular Phenotyping Asthma can be divided into at least 2 distinct molecular phenotypes defined by degree of Th2 inflammation Suggest that Th2 cytokines are likely to be a relevant therapeutic target in only a subset of asthma patients Current paradigms do not adequately explain the non-th2 driven disease, which is quite common Woodruff PG et al. Am J Respir Crit Care Med 2009;180:388-95

47 The Phenotype Studied May Significantly Influence the Efficacy of Therapy

48 IL-5 and Asthma IL-5 is a key cytokine in eosinophil differentiation, recruitment, activation, and survival at sites of allergic inflammation. IL-5 levels elevated in BAL fluid and biopsies in patients with asthma and correlate with disease activity. Flood-Page P et al. Am J Respir Crit Care Med 2007;176:

49 Anti-IL5 and Asthma Randomized, double blind, placebo controlled trial in 55 centers 362 patients yrs with moderate persistent asthma, receiving ICS therapy (max dose BDP 1000mcd/d), FEV % predicted, 12% increase in FEV 1 after albuterol, and daily symptom score of 4 (max 12) during the 7 days preceding enrollment 4 week run in followed by 12 week treatment period with Mepolizumab 250mg IV q4wk, or Mepolizumab 750mg IV q4wk, or Placebo q4wk Primary outcome: change in home peak flow at weeks 12 and 20 Secondary outcomes: change in FEV 1, symptom scores, rescue albuterol use, QOL, exacerbations, and blood/sputum eosinophils Flood-Page P et al. Am J Respir Crit Care Med 2007;176:

50 Anti-IL5 and Asthma Marked and sustained reductions in blood and sputum eosinophils Blood Sputum 17 of 32 subjects had baseline eosinophils >3% (only 3 in mepolizumab 750mg) Flood-Page P et al. Am J Respir Crit Care Med 2007;176:

51 Anti-IL5 and Asthma Primary outcome statistically significant, but clinically small, increase in PEF between mepolizumab 250mg and placebo (13.5 LPM, p=0.03), but no difference between mepolizumab 750mg and placebo No differences between treatment groups for: FEV 1 Symptom scores (actually decreased more in placebo group than mepolizumab 750mg) Rescue albuterol use Quality of life Trend toward reduction in exacerbation rate among mepolizumab 750mg compared to placebo (p=0.065) Flood-Page P et al. Am J Respir Crit Care Med 2007;176:

52 Anti-IL5 and Asthma Was the lack of efficacy a result of studying the agent in the incorrect phenotype? Would the results have differed if a different phenotype of asthma (i.e. eosinophil predominant asthma) been studied?

53 Anti-IL5 and Exacerbations of Refractory Eosinophilic Asthma Randomized, double blind, placebo controlled trial 61 patients >18 yrs with refractory eosinophilic asthma and history of recurrent severe exacerbation Sputum eosinophils >3% despite high dose corticosteroids At least 2 exacerbations requiring oral corticosteroids in the past year 2 week run (including oral corticosteroid) in followed by 12 month treatment period with Mepolizumab 750mg IV q4wk or Placebo Primary outcome: number of severe exacerbations (oral corticosteroid) per subject Secondary outcomes: lung function, airway hyperresponsiveness, symptom scores, rescue albuterol use, sputum/blood eosinophils and airway pathology Haldar P et al. NEJM 2009;360:973-84

54 Anti-IL5 and Exacerbations of Refractory Eosinophilic Asthma Significant reductions in exacerbations (2.0 vs 3.4, RR 0.57) Haldar P et al. NEJM 2009;360:973-84

55 Anti-IL5 and Exacerbations of Refractory Eosinophilic Asthma Significant reductions in blood and sputum eosinophils No effect on symptoms, FEV 1 after bronchodilator, or AHR Haldar P et al. NEJM 2009;360:973-84

56 Summary Multiple phenotypes describe relevant elements of asthma in childhood These phenotypes are not just theoretical constructs, but have practical implications for asthma management The future of personalized medicine is dependent on accurate phenotyping

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