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The burden of exacerbations in mild asthma: a systematic review

J. Mark FitzGerald, Peter J. Barnes, Bradley E. Chipps, Christine R. Jenkins, Paul M. O'Byrne, Ian D. Pavord, Helen K. Reddel
ERJ Open Research 2020 6: 00359-2019; DOI: 10.1183/23120541.00359-2019
J. Mark FitzGerald
1Institute for Heart and Lung Health, University of British Columbia, Vancouver, BC, Canada
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  • For correspondence: mark.fitzgerald@vch.ca7.Pleasecanwerequestasecondsetofproofstochecktheeditsthathavebeenmade?Thankyouinadvance
Peter J. Barnes
2Airway Disease Section, National Heart and Lung Institute, Imperial College, London, UK
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Bradley E. Chipps
3Capital Allergy and Respiratory Disease Center, Sacramento, CA, USA
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Christine R. Jenkins
4The George Institute for Global Health and Faculty of Medicine, UNSW, Sydney, Australia
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Paul M. O'Byrne
5Firestone Institute of Respiratory Health, St Joseph's Healthcare and Dept of Medicine, Michael G. DeGroote School of Medicine, McMaster University, Hamilton, ON, Canada
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Ian D. Pavord
6Oxford Respiratory NIHR BRC, Nuffield Dept of Medicine, University of Oxford, Oxford, UK
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Helen K. Reddel
7Woolcock Institute of Medical Research, University of Sydney, Sydney, Australia
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    Study selection process. RCT, randomised controlled trial.

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  • TABLE 1

    Definitions of mild asthma: classification used in this review

    Main criteria for mild asthmaRCTs (n=54)Observational/other studies (n=10)
    All n (%)Studies permitting past history of exacerbations n (%)All n (%)Studies permitting past history of exacerbations n (%)
    1) Treatment level3 (5.6)0 (0)52 (20.0)
    2) Symptom frequency criteria3 (5.6)3 (5.6)0–
    3) FEV1 ≥80% pred and symptoms<daily19 (35.2)15 (27.8)21 (10.0)
    4) FEV1 >60–80% pred and symptoms<daily15 (27.8)13 (24.1)11 (10.0)
    5) Miscellaneous definitions#9 (16.7)8 (14.8)0–
    6) Included patients aged <5 years5 (9.3)4 (7.4)22 (20.0)

    RCT: randomised controlled trial; FEV1: forced expiratory volume in 1 s. # Miscellaneous definitions not captured by the other five categories (e.g. “doctor-diagnosed mild asthma”, or “mild asthma based on airway hyper-responsiveness” alone), or, studies that did not state that patients had “mild asthma” but included patients with disease characteristics similar to those in the other five categories.

    • TABLE 2

      Mild asthma studies grouped by study type (RCT or observational/other) and by definition of mild asthma

      Study (year) [ref.]Age range or average age yearsTreatment durationPlaceboExacerbation definitionBaseline exacerbation dataPatients with history of exacerbation not excluded#
      Yes n, treatment allowedNo
      RCTs
      Category 1: RCTs that primarily defined mild asthma by treatment level
       Bateman  et al. (2018)  [26]12–8352 weeks✓✓✓
       Camargos  et al. (2018)  [31]10.6 (2.8)¶, 9.9 (2.7)¶6 weeks✓✓
       O’Byrne  et al. (2018)  [38]12–8552 weeks✓✓
      Category 2: RCTs that primarily defined mild asthma by symptom frequency
       Martinez  et al. (2011)  [36]5–1844 weeks74
      P bid + P/ALB rescue
      ✓✓✓
       Pauwels  et al. (2003)  [41]5–663 years3568
      P + usual asthma medication
      ✓✓✓
       Wongtim  et al. (1995)  [80]33.2 (7.46)¶, 32.8 (8.6)¶8 weeks10✓
      Category 3: RCTs that primarily defined mild asthma with a composite definition of FEV1 ≥80% pred and symptoms <daily
       Basyigit  et al. (2004)  [81]38 (8.2)¶, 42.4 (9.6)¶, 45.5 (10.9)¶8 weeks✓✓
       Bousquet  et al. (2005)  [29]15–8048 weeks (12 DB, 36 OL)✓✓✓
       Chrousos  et al. (2005)  [82]18–6514 days✓✓
       Chuang  et al. (2007)  [83]6–148 weeks✓✓
       Chuchalin  et al. (2005)  [33]6–8712 months✓✓✓
       Chuchalin  et al. (2008)  [32]12–7952 weeks315✓✓
       Currie et al.  (2003) [84]36 (4)+2×3 weeks✓✓
       Garcia Garcia  et al. (2005)  [35]6–1412 months✓✓✓
       Karaman  et al. (2004)  [85]8–1412 weeks✓✓
       Maiti et al.  (2011) [86]18–704 weeks✓✓
       Ng et al.  (2007) [37]6–142×8 weeks✓✓
       Reddel et al.  (2008) [42]18–8011 months21✓
       Renzi et al.  (2010) [43]≥1224 weeks✓✓✓
       Riccioni  et al. (2002)  [87]26.9 (12.3)¶, 26.7 (8.6)¶, 28.2 (10.1)¶16 weeks✓
       Shimoda  et al. (2005)  [88]36.2 (12.8)¶, 35.6 (14.4)¶6 months✓✓
       Tamaoki  et al. (2008)  [89]≥218 weeks✓✓
       Vatrella  et al. (2002)  [90]18–4816 weeks✓✓
       Zeiger et al.  (2005) [91]15–8548 weeks (12 DB, 36 OL)§✓✓
       Zietkowski  et al. (2006)  [92]45.2 (10.9)ƒ, 42 (14)ƒ, 51 (7.6)ƒ12 weeks✓✓
      Category 4: RCTs that primarily defined mild asthma with a composite definition of FEV1 approximately >60–80% and symptoms <daily
       Berger et al.  (2009) [48]≥1216 weeks177✓
       Boulet et al.  (2000) [93]≥1212 weeks✓✓
       Drazen et al.  (1996) [34]12–5520 weeks (16 weeks active treatment + 4 weeks withdrawal (OL ALB as needed))129
      P + ALB as needed##
      ✓✓
       Herjavecz  et al. (1999)  [55]17–6722 weeks (6 DB; 16 OL)✓✓✓
       O'Byrne  et al. (2001)  [39]≥121 yearGroup A: 239✓✓
       O'Sullivan  et al. (2003)  [94]19–502×8 weeks✓✓
       Papi et al.  (2007) [40]18–656 months118
      P bid + ALB 100 μg as needed
      ✓✓
       Peters et al.  (2007) [56]≥616 weeks✓✓✓
       Stone et al.  (2001) [95]≥164 weeks✓✓
       Tattersfield  et al. (2001)  [45]20–602 years✓✓
       Tomlinson  et al. (2005)  [46]20–6012 weeks✓✓✓
       van Grunsven  et al. (1996)  [47]≥302 years✓✓✓
       Verberne  et al. (1996)  [58]7–164 months✓✓✓
       Vermetten  et al. (1999)  [96]18–6612 weeks✓✓
       Woodcock  et al. (2002)  [59]18–656 weeks✓✓
      Category 5: RCTs that defined mild asthma by other/miscellaneous criteria
       Arets et al.  (2002) [23]5–1012 weeks33✓✓
       Boushey  et al. (2005)  [28]18–651 year✓✓✓
       Villaran  et al. (1999)  [97]14–458 weeks✓✓
      Category 5: RCTs that did not describe their patients as having “mild asthma” but included patients with disease characteristics similar to the categories described above
       Bailey et al.  (2008) [24]12–6552 weeks✓✓✓
       Barnes et al.  (2007) [98]≥1212 weeks✓✓
       Bateman  et al. (2012)  [25]≥128 weeks94✓✓✓
       Busse et al.  (2001) [30]>1524 weeks✓✓✓
       Busse et al.  (2001) [53]12–7512 weeks114
       van der  Molen et al.  (1998) [99]18–5012 weeks✓✓
      Category 6: RCTs that included patients <5 years old
       Bisgaard  et al. (2005)  [27]2–548 weeks271✓✓✓
       Shah et al.  (2014) [100]2–1812 weeks✓✓
       Szefler  et al. (2007)  [44]2–852 weeks✓✓✓
      Category 6: RCTs that included patients <5 years old that did not describe their patients as having “mild asthma” but included patients with disease characteristics similar to mild asthma
       Robertson  et al. (2007)  [21]2–1412 months113✓✓
       Skoner et al.  (2005) [57]2–53 weeks50✓
      Observational/other
      Category 1: Observational/other studies that primarily defined mild asthma by treatment level
       Ding and  Small  (2017) [49]≥12–NA✓✓
       Friedman  et al. (2010)  [50]12–25–NA✓
       Friedman  et al. (2010)  [51]12–65–NA✓
       McIvor et al.  (2009) [22]≥6Survey + 6-week treatmentNA✓✓
       Navaratnam  et al. (2009)  [52]12–65–NA✓
      Category 3: Observational/other studies that primarily defined mild asthma with a composite definition of FEV1 ≥80% and symptoms<daily
       Giraud et al.  (2006) [54]≥184–8 weeksNA✓✓
       Lai et al.  (2003) [61]Total (not just mild asthma) Children: 7.4 (3.8)¶Adults: 40.5 (18.5)¶–NA✓
      Category 4: Observational/other studies that primarily defined mild asthma with a composite definition of FEV1 approximately >60–80% and symptoms<daily
       Soyer et al.  (2009) [60]6–18–NA✓
      Category 6: Observational/other studies that included patients <5 years old
       König et al.  1996 [62]≤17–NA✓✓
       Robertson  et al. (1992)  [63]≤20–NA✓

      RCT: randomised controlled trial; bid: twice daily; P: placebo; ALB: albuterol; DB: double-blind; OL: open-label; FEV1: forced expiratory volume in 1 s; NA: not applicable. # History of exacerbations considered to be exacerbation, hospitalisation or emergency department visit or oral corticosteroid use that occurred prior to enrolment/screening (RCTs or prospective observational studies) or in the pre-index period (retrospective studies); ¶: mean (sd) age in years; +: mean (se) age. §: 10% of participants (determined at randomisation) switched therapies to preserve the masking in the preceding period; ƒ: median (range) age; ##: no dose given.

      • TABLE 3

        Retrospectively collected data on asthma exacerbations, hospitalisation and emergency department admissions/visits

        Study (year) [ref.]Age range yearsStudy groups nExacerbation parameter(s)Data for exacerbations by specified parameter, for each study group
        Exacerbations reported in ≤6 months prior to study entry
         Bateman et al.  (2012) [25]≥1297, 100, 110, 95, 102, 94Pts with ≥1 exacerbation in last 6 months18%, 19%, 16%, 25%, 17%, 21%
         McIvor et al.  (2009) [22]#≥6534Patients with any exacerbation in 6 weeks prior to study entry51.7%
         Skoner et al.  (2005) [57]2–558, 51, 52, 50No. of exacerbations in last 30 daysMean: 1.8, 1.3, 1.5, 1.2 Median: 0,1,0, 0
        Pts with ≥1 exacerbation in last 30 days48.3%, 52.9%, 48.1%, 36.7%
         Woodcock et al.  (2002) [59]18–6586, 86Mean no. daytime asthma attacks in 7-day run-in0.25, 0.18
        Mean no. night-time asthma attacks in 7-day run-in0.10, 0.10
        Exacerbations reported in 12 months/1 year prior to study entry
         Bateman et al.  (2018) [26]12–832089, 2087Pts with 1 severe exacerbation in last 12 months17.5%, 17.3%
        Pts with ≥1 severe exacerbations in last 12 months22%, 21.9%
        Pts with ≥2 severe exacerbations in last 12 months4.5%, 4.7%
         Ding and Small  (2017) [49]≥12524, 591Pts with 1 exacerbation in last 12 months9.0%, 13.1%
        Pts with ≥3 exacerbations in last 12 months3.4%, 1.9%
        Mean (sd) no. of moderate-to-severe exacerbations in last 12 months0.2 (0.6)¶
        Mean (sd) no. of exacerbations treated in ED or hospital in last 12 months0.1 (0.4), 0.1 (0.3)
        Mean (sd) no. of exacerbations treated with OCS, antibiotics, ED or hospital admission in last 12 months+0.1 (0.5), 0.2 (0.6)
        Pts with 1 exacerbation treated with OCS, antibiotics, ED or hospital admission in last 12 months+5.8%, 10.8%
        Pts with ≥3 exacerbations treated with OCS, antibiotics, ED or hospital admission in last 12 months+1.0%, 1.5%
         Giraud et al.  (2006) [54]≥1894Pts hospitalised for asthma in previous 12 months4.3%
         Herjavecz et al.  (1999) [55]17–6790, 91Time since last exacerbation12.5 months, 13.0 months
         Lai et al. (2003)  [61]Mean 7.4–40.51709, 633Pts with hospital admissions in last year7.3%, 15.4%
        Pts with any hospital ED/unscheduled emergency visit in the last year33.1%, 41.3%
         Martinez et al.  (2011) [36]5–1871, 72, 71,74Mean no. hospital visits for asthma in last 1 year0.3, 0.3, 0.2, 0.2
         O’Byrne et al.  (2018) [38]≥121277, 1277,1282Pts with ≥1 severe exacerbation in last 12 months20.0%, 20.1%, 18.8%
         Peters et al.  (2007) [56]≥6166, 165, 169Pts with ≥1 urgent visit for asthma in last 1 year30.7%, 35.8%, 35.5%
         Robertson et al.  (2007) [21]§2–1497, 105Median no. of ED attendances for asthma in last 1 year1, 1
        Median no. of hospital admissions for asthma in last 1 year1, 1
         Soyer et al.  (2009) [60]6–18522Mean (sd) no. of unscheduled visits per patient1.2 (0.2)
        Mean (sd) no. of ED visits per patient0.6 (0.05)
         Verbene et al.  (1996) [58]7–1630Pts hospitalised for asthma in last 1 year0%

        All studies were randomised controlled trials except Giraud et al. [54], McIvor et al. [22], Ding and Small [49], Lai et al. [61] and Soyer et al. [60]. pts: patients; ED: emergency department; OCS: oral corticosteroids; no.: number. # Study included patients with a history of exacerbations (time frame not specified); ¶ n=1076; + time frame not specified in Results section of [49] although Methods section suggests 12-month timeframe; §: Study included only patients with a history of 3–6 exacerbations (hospitalisation or ED visit or general practitioner visits) in the 12 months prior to enrolment/screening.

        • TABLE 4

          Prospective data on exacerbations and exacerbation-related outcomes in mild asthma from placebo arms of RCTs of ≥24 weeks' duration

          Study (year) [ref.]Age range yearsPlacebo nOther asthma medication in placebo armTreatment durationExacerbation parameterPlacebo arm
          Studies not excluding patients with exacerbation history+
           Bisgaard et al. (2005) [27]2–5271Rescue OCS or ICS or β2-agonist48 wksPts with exacerbation§56%
          Exacerbation rate/year (n=257)ƒ2.34
          Median time to first exacerbation147 days
          Pts with ≥1 unscheduled visit to physician for asthmaƒ42.4%
          Pts hospitalised for asthmaƒ5.8%
          Rate of OCS courses/yearƒ0.64
           Chuchalin et al. (2008) [32]12–79315Rescue ALB52 wksMean exacerbation rate per pt per year (mild, moderate, severe)2.88
          Moderate (OCS) or severe exacerbation (hospitalisation) rate/year0.33
          No. unscheduled asthma-related healthcare contacts7
          Pt withdrawal/discontinued due to exacerbation, n8
           Martinez et al. (2011) [36]5–1874Rescue ALB44 wksProbability (95% CI) of first exacerbation by end of trial requiring prednisone course49 (37–61)%
          Proportion with treatment failure (all defined by requirement for a second course of prednisone)23%
           O'Byrne et al. (2001) [39]≥12239Yes - only after first exacerbation (n=104)¶¶1 yrPts with severe exacerbation33.3%
          No. of pts with severe exacerbation, pts treated with OCSs70.9%
          Pts receiving systemic corticosteroids23.6%
          Severe exacerbation rate per pt per year0.77
           O’Byrne et al. (2018) [38]≥121277TERB 0.5 mg as needed1 yrPts with ≥1 moderate or severe exacerbation21.5%
          Pts with ≥1 severe exacerbation11.9%
          Annualised severe exacerbation rate0.20
           Papi et al. (2007) [40]18–65118ALB as-needed6 monthsPts with severe exacerbation3.4%
          Pts with ≥1 exacerbation17.80%
          Mean no. of exacerbations/pt/year1.63
           Pauwels et al. (2003) [41]5–663568Usual asthma treatment (SABA 64.6% of placebo pts) plus ICS or systemic corticosteroid if needed3 yrsPts with life-threatening exacerbation over 3 years, n24 (0.67%)
          Pts with ≥1 SARE over 3 years, n198
          Pts with ≥2 SAREs over 3 years, n49
          Mean no. of courses of systemic corticosteroids per year0.21
          Pts using systemic corticosteroids3 months: 4.1%
          12 months: 3.1%
          24 months: 3.3%
          36 months: 2.0%
          Pts with ≥1 systemic corticosteroid course23%
          Studies excluding patients with exacerbation history+
           Reddel et al. (2008) [42]18–8021ALB as-needed11 monthsPts with ≥1 mild exacerbation, n13
          Pts with severe exacerbation, n3
          Studies requiring patients to have a history of frequent exacerbations#
           Robertson et al. (2007) [21]2–14113Inhaled β2-agonist or OCS for acute asthma episode12 monthsProportion of children with ≥1 episode treated with short course of randomised therapy, n (%)105 (92.9%)
          Total number of treated episodes of asthma336
          Proportion of treated asthma episodes utilising ≥1 health resource, n (%)134 (39.9%)
          Proportion of treated asthma episodes requiring ED visit, n (%)46 (13.7%)
          Proportion of treated asthma episodes requiring hospitalisation, n (%)13 (3.9%)
          Proportion of treated asthma episodes with OCS use, n/N pts with diary data (%)78 of 321 (24.3%)

          RCT: randomised controlled trial; ED: emergency department; wks: weeks; pt: patient; OCS: oral corticosteroid; ICS: inhaled corticosteroid; CI: confidence interval; SABA: short-acting β2-agonist; SARE: severe asthma-related event; ALB: albuterol; TERB: terbutaline; GP: general practitioner; LABA: long-acting β2-agonist. # Study included only patients with a history of 3–6 exacerbations (hospitalisation or ED visit or GP visits) within 12 months prior to enrolment/screening); ¶ Unscheduled visits to GP, specialist paediatrician, ED or admission to hospital; +: Exacerbation history defined as an exacerbation, hospitalisation or ED visit or OCS use occurring ≥3 months prior to enrolment/screening; §: data appear to relate to 48-week double-blind period only (total study duration 1 year including screening and single-blind, placebo run-in period); ƒ: source publication refers to “yearly” data, but double-blind treatment period only 48 weeks (total study duration 1 year including screening and single-blind, placebo run-in period); ##: defined as the requirement for a second dose of prednisone within any 6-month period; ¶¶: most common extra medication in placebo group was systemic corticosteroids (n=56), ICS (n=15) and LABAs (n=11).

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          The burden of exacerbations in mild asthma: a systematic review
          J. Mark FitzGerald, Peter J. Barnes, Bradley E. Chipps, Christine R. Jenkins, Paul M. O'Byrne, Ian D. Pavord, Helen K. Reddel
          ERJ Open Research Jul 2020, 6 (3) 00359-2019; DOI: 10.1183/23120541.00359-2019

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          The burden of exacerbations in mild asthma: a systematic review
          J. Mark FitzGerald, Peter J. Barnes, Bradley E. Chipps, Christine R. Jenkins, Paul M. O'Byrne, Ian D. Pavord, Helen K. Reddel
          ERJ Open Research Jul 2020, 6 (3) 00359-2019; DOI: 10.1183/23120541.00359-2019
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