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Past asthma exacerbation in children predicting future exacerbation: a systematic review

Rachel Lowden, Steve Turner
ERJ Open Research 2022 8: 00174-2022; DOI: 10.1183/23120541.00174-2022
Rachel Lowden
1Child Health, University of Aberdeen, Aberdeen, UK
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Steve Turner
1Child Health, University of Aberdeen, Aberdeen, UK
2Paediatric Dept, NHS Grampian, Aberdeen, UK
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  • For correspondence: s.w.turner@abdn.ac.uk
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  • FIGURE 1
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    FIGURE 1

    Preferred Reporting Items for Systematic Reviews and Meta-Analyses flow diagram, showing details of the search and study inclusion process, including reasons for exclusion of full-text articles reviewed. CINAHL: Cumulative Index to Nursing and Allied Health.

  • FIGURE 2
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    FIGURE 2

    Summary of quality assessment using the Effective Public Health Practice Project quality assessment tool for quantitative studies. The domains blinding, intervention integrity and analyses were not applicable for any of the studies and were therefore removed. n/a: not applicable. #: retrospective case–control studies were given a n/a score in the withdrawals and dropouts domain in accordance with the tool recommendations.

  • FIGURE 3
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    FIGURE 3

    Exacerbation outcomes, showing the number of studies that relate different categories of exacerbations at baseline to risk of future exacerbations. ED: emergency department; ICU: intensive care unit.

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    FIGURE 4

    Forest plot of studies assessing past exacerbation (unspecified severity) predicting future exacerbation. Data presented separately for five of the databases used in Engelkes et al. [38]. AUH: Aarhus University prescription database; CPRD: Clinical Practice Research Datalink; IPCI: Integrated Primary Care Information; SIDIAP: Sistema d'Informació per al Desenvolupament de la Investigació en Atenció Primària.

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    FIGURE 5

    Forest plots based on exacerbation severity definition and location of study publication. In d), data are presented separately for five of the databases used in Engelkes et al. [38]. PICU: paediatric intensive care unit.

Tables

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  • TABLE 1

    Summary of key study characteristics of included studies

    First author, year [reference]Study designStudy settingData collection periodPopulation/inclusion criteriaSample size (n)Definition of acute exacerbationResults
    Emerman, 2001 [13]#Prospective cohort combining two studies with identical protocols44 EDs in USA and CanadaStudies performed 1997–1998
    Follow-up 2 weeks after index ED visit
    Children aged 2–17 years with ED visit for acute asthma
    Mean age 7.99 years
    59% male
    19% White, 55% Black, 24% Hispanic, 2% other
    1184 recruited; follow-up data available for 762ED visit with physician diagnosed acute asthmaFactors associated with acute asthma relapse:
    ED visits for asthma in past year (per 5 visits) OR 1.2 (1.0–1.5)
    Urgent clinic visits for asthma in past year (per 5 visits) OR 1.1 (0.9–1.3)
    Lafata, 2002 [14]Retrospective cohort study using routinely acquired dataMichigan, USA1992–1996
    2-year observation: 1 baseline year and 1 follow-up year
    Children aged 5–14 years, with 1 hospitalisation or 2 outpatient encounters for asthma and ≥1 paediatrician office visit for each year of inclusion
    Mean age 8.7 years
    63% male
    49% White, 44% African American, 7% other
    452ED visit or hospitalisation for asthmaFactors associated with ED use:
    ED visit for asthma in prior year OR 8.26 (4.79–14.25)
    Hospital admission for asthma in prior year OR 0.85 (0.32–2.22)
    Factors associated with ED or hospital admission for asthma:
    Prior ED visit for asthma OR 7.97 (4.64–13.71)
    Chen, 2003 [15]Prospective cohortChildren's Hospital, St Louis, MO, USAAdmissions between June and December 1999
    1 year follow-up
    Children aged 4–18 years, hospitalised for asthma
    Mean age 8.22 years
    65% male
    77% African American, 21% White, 2% other
    115Hospitalisation for asthmaLifetime history of hospitalisations as a predictor of future hospitalisation: OR 5.36 (1.90–15.14)
    Schatz, 2003 [16]Retrospective cohort study using routinely acquired dataCalifornia, USA1998–1999
    2-year observation: 1 baseline year and 1 follow-up year
    Individuals aged 3–64 years with asthma
    Children
    62.2% male
    11 101 in total; 6904 children aged 3–17 yearsHospitalisation or ED visit for asthmaIn children aged 3–17 years, 1998 hospitalisations as a predictor for asthma hospitalisation in 1999 OR 3.37 (1.61–7.04)
    McCoy, 2006 [17]Data from RCT used as an observational study19 American Lung Association clinical research centres, USARecruitment from 15 September to 30 November 2000
    Follow-up for 14 days after each injection (28 days total)
    Volunteers aged 3–64 years with physician-diagnosed asthma
    Of children originally enrolled,
    60% male
    60.5% White, 28.7% Black, 5.6% Hispanic, 4.4% other
    2032 enrolled, 1949 completed trial; 353 children aged 3–10 yearsNew or increased OCS or an unscheduled healthcare encounter for asthmaHistory of intubation for asthma, hospitalisation ≥2 times for asthma, ≥3 courses of OCS for asthma in past year, or ≥2 unscheduled health contacts for asthma in past year in children aged 3–10 years as a predictor of exacerbations OR 2.19 (1.18–4.06)
    Reznik, 2006 [18]Retrospective case–controlChildren's hospital, New York, USAAdmissions between January 1998–December 2004
    30-day follow-up
    Cases: children aged 0–21 years hospitalised for asthma and readmitted within 30 days of discharge for same reason
    Controls: children aged 0–21 years hospitalised for asthma, but not readmitted within 30 days of discharge
    Mean age 5.99 years
    61% male
    62.2% Hispanic, 34.2% African American, 3.6% other
    445
    Cases: 152
    Controls: 293
    Hospitalisation for asthmaPredictors of early asthma readmission:
    ED visit for asthma in past year OR 3.28 (1.55–6.94)
    Multivariate analysis of predictors of early asthma readmission:
    Hospital admission for asthma in past year OR 1.89 (1.10–3.25)
    Prior ICU admission for asthma OR 1.99 (0.93–4.27)
    Covar, 2008 [19]#Data from PACT RCT used as an observational studyUSARecruited between October 2002 and January 2004
    Trial period: 48 weeks
    Children aged 6–14 years with documented mild–moderate persistent asthma, screening FEV1 ≥80% predicted and methacholine reactivity
    61.4% male
    44.9% from a minority ethnic group
    285Systemic corticosteroids or emergency care (ED visit or hospitalisation) for acute asthmaLogistic regression analysis of factors at baseline predictive of exacerbation:
    History of exacerbation requiring corticosteroid course in past year OR 2.28 (1.59–3.26)
    Multivariable model of factors associated with exacerbations:
    Prednisone course in year prior to study OR 2.10 (1.42–3.09)
    Miller, 2008 [20]Prospective cohortMichigan, USAEnrolment over 1-year period
    Follow-up at 2 weeks and 6 months post-ED visit
    Children aged 2–17 years presenting to ED for acute asthma
    Mean age 8.1 years
    61.5% male
    71.7% White, 50% Black, 26% Hispanic, 7% American Indian or Alaska native, 2% Asian, 2% other
    197 enrolled; follow-up data available for 166Signs/symptoms compatible with asthma exacerbation (shortness of breath, coughing, wheezing, chest tightness) in a diagnosed asthmaticPrevious severe disease (e.g. systemic corticosteroids, ED visit or hospitalisation for asthma) as a predictor of 6-month morbidity (urgent care, ED or hospital admissions for asthma) Pearson correlation coefficient 0.17
    To, 2008 [21]Prospective cohortChildren's hospital, Toronto, CanadaED visit between January 2003 and June 2004
    Follow-up at 1 and 6 months post-ED visit
    Children aged 2–17 years visiting ED for acute asthma
    70% aged <7 years
    59% male
    269 enrolled;
    247 completed 1-month follow-up,
    220 completed 6-month follow-up
    Sudden worsening of symptoms resulting in difficulty breathing often requiring extra medicine to relieve symptoms, with/without unscheduled ED/doctor visitPredictors of acute asthma episode at 6-month follow-up:
    Acute asthma episode 6 months prior to baseline OR 4.73 (2.25–9.97)
    Predictors of ED visit at 6-month follow-up:
    ED visits in 12 months prior to baseline OR 6.27 (1.54–7.12)
    Haselkorn, 2009 [22]Prospective cohort
    Data from TENOR study
    USATENOR conducted from 2001 to 2004
    Follow-up with semi-annual visits for 3 years
    Children with severe asthma or mild/moderate asthma considered difficult to treat
    Had ≥2 OCS bursts in past year; ≥2 unscheduled clinic or hospital visits for asthma in past year; requirement for chronic, daily high doses of ICS; or ≥5 mg oral prednisone or current use of ≥3 medications to control asthma
    69% male
    62% White, 38% other
    4756
    637 children aged 6–11 years
    Data available for 563 children
    Use of a corticosteroid burstMultivariate model including 6- and 12-month events
    Recent exacerbation as a predictor of future exacerbation OR 1.99 (1.51–2.61)
    Multivariate model including only 6-month events:
    Recent exacerbation as a predictor of future exacerbation OR 3.08 (2.21–4.28)
    Tolomeo, 2009 [23]Retrospective cohort study using routinely acquired dataChildren's hospital, New England, USAHospitalisation between January and December 2006
    Data for 1 year before and after hospitalisation
    Children aged 2–15 years admitted to hospital for asthma
    Mean age 6.35 years
    66% male
    36% White, 35% Black, 24% Hispanic, 5% other
    298Hospital admission with primary diagnosis of asthmaPrevious asthma-related ED visit as a predictor of:
    Subsequent ED visit OR 3.3 (1.39–7.96)
    Subsequent hospitalisation for asthma OR 3.1 (1.17–8.33)
    Triasih, 2011 [24]#Retrospective cohortChildren's hospital, Melbourne, AustraliaICU admission between January 1990 and December 2004
    Mean follow-up 10.3 years
    Children aged 2–18 years with asthma admitted to ICU
    Median age at admission 7.0 years
    59% male
    410ICU admission for asthmaRisk factors for readmission to hospital:
    Previous hospital admission OR 3.3 (2.1–5.3)
    Admission in year prior to index admission aOR 4.5 (2.5–8.4)
    Multiple previous hospital admissions OR 2.4 (1.3–4.2)
    Risk factors for readmission to ICU:
    Previous hospital admission OR 16.9 (4.1–70.4)
    Admission in year prior to index admission aOR 4.7 (2.4–9.3)
    Multiple previous hospital admissions OR 3.2 (1.6–6.7)
    Previous ICU admission aOR 2.4 (0.8–6.7)
    Wu, 2011 [25]#Data from CAMP RCT used as an observational studyUSAEnrolment between December 1993 and September 1995
    Follow-up over 4 years
    Children aged 5–12 years with mild/moderate persistent asthma
    60% male
    68% White, 14% Black, 9% Hispanic, 9% other
    1041 enrolled
    1019 completed daily diary cards
    Episode requiring ≥3 days use of OCS, hospitalisation, or ED visit due to asthma (ATS/ERS statement)History of ED visits or hospitalisations in prior year as a predictor of having ≥1 severe exacerbations regression coefficient 0.73 (0.50–0.96)
    History of ≥3 days of treatment with OCS in prior 3 months as a predictor of having ≥1 severe exacerbations regression coefficient 0.40 (0.17–0.62)
    Li, 2012 [26]Retrospective cohort
    study using routinely acquired data
    Ontario, CanadaED visit between 14 April 2006 and 28 February 2009
    Follow-up for 1 year
    Children aged 2–17 years with prevalent asthma with unplanned visit to ED for asthma
    38.4% aged 2–5 years
    63.1% male
    29 391ED visit for asthmaAdjusted hazard ratios for ED re-visits:
    Asthma admission(s) in prior 2 years HR 1.45 (1.35–1.55)
    Asthma ED visit(s) in prior 2 years HR 2.03 (1.91–2.14)
    Adjusted hazard ratios for hospital admissions:
    Asthma admission(s) in prior 2 years HR 2.87 (2.43–3.39)
    Asthma ED visit(s) in prior 2 years HR 1.85 (1.57–2.19)
    van den Bosch, 2012 [27]#Retrospective case–control4 hospitals in the NetherlandsJanuary 1994–October 2006Cases: children with doctor-diagnosed asthma admitted to PICU for acute asthma
    Controls: patients with asthma who never needed PICU admission for any reason
    Median age at PICU admission 5.2 years
    77% White
    230
    Cases: 66
    Controls: 164
    PICU admission for acute asthmaEarlier hospitalisation for asthma (non-PICU) as a risk factor for PICU admission OR 5.4 (1.34–21.45)
    Visitsunthorn, 2013 [28]Retrospective case–controlChildren's hospital, Bangkok, ThailandJanuary 2006–December 2007
    1 year follow-up
    Children aged ≤14 years admitted to hospital for acute asthma
    50% aged >6 years
    64.5% male
    76
    1 admission: 56
    Readmission: 20
    Acute asthma that was severe or did not improve after 3 doses of bronchodilator nebulisationICU admission at first admission as a risk factor for readmission OR 29.62 (3.35–262.18)
    Kenyon, 2014 [29]Retrospective cohort study using routinely acquired dataUSADischarges between 1 July 2008 and 30 June 2010
    1 year follow-up
    Children aged ≥2 years discharged from hospital after admission for asthma
    61% aged 5–18 years
    61.1% male
    46.6% Black, 27.3% White, 16.8% Hispanic, 7.9% other
    36 601, contributing 44 203 hospitalisationsHospital admission for asthmaPrior-year admission as a risk factor for asthma rehospitalisation
    7 days OR 2.0 (1.4–2.7)
    15 days OR 2.7 (2.1–3.3)
    30 days OR 2.9 (2.5–3.4)
    60 days OR 3.5 (3.1–3.9)
    180 days OR 3.5 (3.3–3.8)
    365 days OR 3.6 (3.4–3.8)
    Zeiger, 2015 [30]Retrospective cohort study using routinely acquired dataCalifornia, USA2010–2011: 1 baseline year and 1 outcome yearChildren aged 5–11 years who met HEDIS criteria for persistent asthma
    Blood eosinophil level determined in 2010
    With eosinophil level:
    Mean age 7.7 years
    61.9% male
    45.3% Hispanic, 24.6% White, 17.4% Black
    2451
    With eosinophil count: 333
    Asthma outpatient visits requiring systemic corticosteroids within ±7 days or asthma ED visits or hospitalisationHistory of exacerbation as a risk factor for exacerbation:
    Adjusted rate ratio 2.35 (1.61–3.44)
    Adjusted risk ratio 1.94 (1.37–2.73)
    Engelkes, 2016 [31]#Retrospective cohort study using routinely acquired dataThe Netherlands1 January 2000 to 1 January 2012
    Mean follow-up 2.46 years
    Children with asthma aged 5–18 years
    Mean age: 10.5 years
    58.7% male
    14 303Hospitalisation, ED visit or prescription of systemic corticosteroids for ≥3 days for asthmaPrior exacerbations as a risk factor for exacerbation:
    Total cohort model 1: relative rate 1.99 (1.40–2.83), model 2: relative rate 2.17 (1.30–3.60)
    Children with ≥1 exacerbation ever model 1: relative rate 1.60 (1.37–1.88), model 2: relative rate 1.52 (1.19–1.94)
    Exacerbations as a risk factor for nonfrequent exacerbations compared to frequent exacerbations
    <2 versus ≥2 OR 2.11 (1.66–2.68) versus OR 1.93 (1.42–2.63)
    <3 versus ≥3 OR 2.43 (1.84–3.23) versus OR 1.99 (1.35–2.94)
    Quezada, 2016 [32]#Data from SARCA and SARA RCTs used for an observational studyUSA2007–2011
    24-week treatment period
    SARCA trial:
    children aged 6–17 years, with poor asthma control, being treated with inhaled glucocorticoids
    62% male
    39% White, 49% Black, 12% other
    718 enrolled
    Data for 295 from SARCA
    Requirement for OCS or urgent healthcare visit for asthma symptoms83% of children with an exacerbation had an unscheduled visit for asthma in the previous year and 80% had been treated with OCS
    69% of children without an exacerbation had an unscheduled visit for asthma in the previous year and 61% had been treated with OCS
    Costa, 2018 [33]#Retrospective case–controlGoiania, BrazilJune 2012–August 2013
    Data collected for 1 year prior to ED visit
    Cases: children aged 4–14 years, admitted to ED for asthma who had ≥3 previous episodes of bronchospasm
    Controls: asthmatic children without exacerbation recruited during outpatient appointment
    Cases:
    Median age 7 years
    56% male
    62% White
    Controls:
    Median age 8 years
    42% male
    28% White
    153
    Cases: 92
    Controls: 61
    Increased symptoms requiring change in medication, judged by physician according to ATS/ERS statement
    Severe exacerbation: hospital admission or course of OCS for asthma
    ≥3 ED visits in past year for asthma as a risk factor for asthma exacerbation incidence risk ratio 1.40 (1.01–1.95)
    Grunwell, 2018 [34]Retrospective case–control
    Data from outpatient asthma clinical research studies at Emory University
    Georgia, USAJanuary 2004–December 2015Cases: children aged 6–18 years with historical admission to PICU for acute asthma
    Controls: asthmatic children without prior PICU admission
    Cases:
    Median age 10 years
    56.7% male
    52.3% Black, 35.2% White, 12.5% other
    Controls:
    Median age 12 years
    61.8% male
    71.8% Black, 17.1% White, 11.2% other
    579
    Cases: 170
    Controls: 409
    PICU admission, hospitalisation or ED visit for asthmaHospitalisation for asthma in year prior to data collection was associated with increased odds of PICU admission OR 8.19 (4.83–13.89)
    To, 2018 [35]Retrospective cohort study using routinely acquired dataToronto, CanadaApril 2008–March 2014
    1 year follow-up
    Individuals aged 5–99 years with ED visit for asthma
    Aged 5–19 years
    Mean age 12.15 years
    57% male
    31% in most marginalised ethnic concentration quintile
    58 366
    18 352 aged 5–19 years
    ED visit for asthmaAdjusted relative risk of asthma ED return visit within 1 year of ED discharge in children aged 5–19 years 1.13 (1.03–1.25)
    Turner, 2018 [36]#Retrospective cohort study using routinely acquired dataUKJanuary 1999–December 2012
    1 baseline year and 1 outcome year
    Children aged 5–12 years diagnosed with asthma
    Mean age 9 years
    57% male
    3776Hospitalisation, ED admission or OCS for asthma (ATS/ERS)Previous asthma attack as a risk factor for ≥1 attack
    1 OR 3.74 (2.92–4.80)
    ≥2 OR 7.72 (5.55–10.74)
    Alsheri, 2020 [37]#Retrospective case–controlAbha Hospital, Saudi ArabiaJanuary 2014–December 2018Cases: children aged 2–14 years admitted to PICU for acute asthma
    Controls: children admitted to the ward for acute asthma
    Cases
    Mean age 6.3 years
    41.7% male
    Controls
    Mean age 4.6 years
    42.7% male
    320
    Cases: 72
    Controls: 248
    PICU or hospital admission for asthmaPrevious admission to PICU as a risk factor for PICU admission OR 7.83 (2.58–23.76)
    Engelkes, 2020 [38]#Retrospective cohort study using routinely acquired data from the Netherlands, Italy, UK, Denmark and SpainThe NetherlandsJanuary 2008–December 2013Patients aged 5–17 years with asthma
    Subcohort with severe asthma (requiring high dose ICS+second controller and/or systematic corticosteroids for ≥120 consecutive days)
    Mean age 10.4 years (7.2–14.8 years across databases)
    Male preponderance across all databases
    212 060
    Severe asthma 14 283
    Use of systemic corticosteroids, ED visit and/or hospitalisation, for worsening asthmaRelative rates of exacerbation in those with history of exacerbation
    CPRD 5.76 (5.25–6.33)
    SIDIAP 2.53 (2.27–2.81)
    IPCI 20.04 (12.91–31.10)
    AUH 45.71 (31.2–66.92)
    PEDIANET 29.36 (16.25–53.05)
    HSD 10.07 (4.56–22.20)

    Data are presented with 95% confidence intervals in brackets where provided. ED: emergency department; RCT: randomised controlled trial; OCS: oral corticosteroids; ICU: intensive care unit; PACT: Pediatric Asthma Controller Trial; FEV1: forced expiratory volume in 1 s; TENOR: The Epidemiology and Natural History of Asthma; ICS: inhaled corticosteroids; aOR: adjusted odds ratio; CAMP: Childhood Asthma Management Program; ATS: American Thoracic Society; ERS: European Respiratory Society; HR: hazard ratio; PICU: paediatric intensive care unit; HEDIS: Healthcare Effectiveness Data and Information Set; SARCA: Study of Acid Reflux in Children with Asthma; SARA: Study of Acid Reflux in Adults with Asthma; CPRD: Clinical Practice Research Datalink; SIDIAP: Sistema d'Informació per al Desenvolupament de la Investigació en Atenció Primària; IPCI: Integrated Primary Care Information; AUH: Aarhus University prescription database; HSD: Health Search Database. #: included in meta-analysis.

    • TABLE 2

      Key results shown by index and subsequent exacerbation type

      Category of subsequent exacerbation
      EDHospitalPICU
      Category of index exacerbation
       ED5 studies
      ORs 3.3 [23], 6.27 [21], 8.26 [14]
      HR 2.03 [26]
      Relative risk 1.13 [35]
      3 studies
      ORs 3.1 [23], 3.28 [18]
      HR 1.85 [26]
      No studies
       Hospital2 studies
      OR 0.85 [14]
      HR 1.45 [26]
      6 studies
      ORs 1.89 [18], 3.3 [24], 3.37 [16], 3.6 [29], 5.36 [15]
      HR 2.87 [26]
      3 studies
      ORs 5.4 [27], 8.19 [34], 16.9 [24]
       PICUNo studies2 studies
      ORs 2.18 [18], 29.62 [28]
      2 studies
      ORs 2.4 [24], 7.83 [37]

      ED: emergency department; PICU: paediatric intensive care unit; HR: hazard ratio.

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      Past asthma exacerbation in children predicting future exacerbation: a systematic review
      Rachel Lowden, Steve Turner
      ERJ Open Research Oct 2022, 8 (4) 00174-2022; DOI: 10.1183/23120541.00174-2022

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      Past asthma exacerbation in children predicting future exacerbation: a systematic review
      Rachel Lowden, Steve Turner
      ERJ Open Research Oct 2022, 8 (4) 00174-2022; DOI: 10.1183/23120541.00174-2022
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