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

Abstract

Acute exacerbations are common in children and potentially preventable. Currently, a past exacerbation is the best predictor of a future exacerbation. We undertook a systematic review of the literature describing the relationship between past and future exacerbations. Our analysis considered whether the odds ratios for one exacerbation to predict a recurrence were different across different categories of exacerbation.

Four databases were searched systematically (MEDLINE, Embase, the Cumulative Index to Nursing and Allied Health and PsycInfo). Exacerbations were categorised by severity as: presentation to emergency department (ED); hospital admission; paediatric intensive care unit (PICU) admission; and “unspecified severity” (i.e. no distinction between severity categories was made). Meta-analysis was performed for studies where sufficient data were provided for inclusion.

There were 26 eligible articles from 9185 identified. There was significant heterogeneity in duration of follow-up, healthcare system and exacerbation definition between studies. For the unspecified severity definition, the odds ratio for an exacerbation after a previous exacerbation was 9.87 (95% CI 5.02–19.39; six studies, 162 583 individuals). PICU admission was also associated with increased risk of future admission (OR 5.87, 95% CI 2.96–11.64; two studies, 730 individuals). Meta-analysis was not possible for ED visits or hospitalisation. The median odds ratio (range) for past ED visit predicting future ED visit was 6.27 (3.3–8.26) and for past hospitalisation predicting future hospitalisation was 3.37 (1.89–5.36).

The odds for a second asthma exacerbation do not necessarily increase with increasing severity of an initial exacerbation.

Abstract

Asthma exacerbation in children is associated with increased odds for future exacerbation across all exacerbation severities. There is no evidence that severe exacerbations are associated with increased risk of future exacerbations. https://bit.ly/3n1O1Tv

Introduction

Asthma affects >1 million children in the United Kingdom (UK) [1] and >5 million in the United States of America [2], making it the most common long-term medical condition in young people. Patients with asthma can experience acute exacerbations, defined by the International Consensus on Pediatric Asthma as an acute or subacute episode of progressive increase in asthma symptoms, associated with airflow obstruction [3]. Exacerbations result in significant morbidity and socioeducational cost for the child through hospital admissions, interruption to education and social development, adverse effects from treatment and a decline in lung function [4, 5]. Moreover, there is economic impact on caregivers through working day and productivity loss [6].

A key goal of asthma treatment is to reduce risk of exacerbations. There has been limited systematic appraisal of the literature describing whether an exacerbation is followed by a subsequent exacerbation. The Global Initiative for Asthma, the British Thoracic Society/Scottish Intercollegiate Guidelines Network and the National Institute for Health and Care Excellence guidelines highlight the importance of identifying children who are at increased risk of exacerbations, and all cite a previous exacerbation as the major risk factor [7–9]. One systematic review which considered all risk factors for exacerbations in children with asthma identified 11 studies exploring previous exacerbation as a risk factor, and concluded that the odds ratio for an exacerbation being followed by a second exacerbation varied between 2.1 and 4.1 [10].

Here we describe a systematic review which was designed with a focus on exacerbation as a predictor of future exacerbation in children. Our hypothesis was the odds ratio (or a positive predictive value (PPV) for case-only populations) for an exacerbation would be greater following a more severe “index” exacerbation. Meta-analysis was carried out for studies where sufficient data were provided for inclusion.

Methods

Eligibility criteria and information sources

Full papers published in English from 2000 onwards describing asthma exacerbations in children where the mean age was between 5 and 18 years were eligible. Studies published before 2000 were ineligible, since they were considered less relevant to modern asthma care. Children aged <5 years were ineligible due to the potential to confuse an asthma exacerbation with lower respiratory tract infection in younger children. In articles where participants were of a wider age range than the desired population, if the mean age was between 5 and 18 years, or the desired age group of this review was reported separately, then the paper was included. Observational studies (including those using routinely acquired healthcare data and case–control and case-only studies), retrospective case–control studies and randomised controlled trials (RCT) were eligible. Data from RCTs were included regardless of the presentation of the results and whether the intervention may have influenced these. Letters and abstracts were ineligible. The outcome was exacerbation and was reported as odds ratio, since this is the best indicator of performance [11]. To make the best use of the data available (i.e. include data from case-only studies) and acknowledging odds ratio may have limitations [12], PPV was also reported for all studies with available data.

Literature was searched on 11 January 2021 using the databases MEDLINE, Embase, the Cumulative Index to Nursing and Allied Health and PsycInfo. Additional studies were identified from reviewing the references of the full papers assessed after the database search, including a previous review [10].

Search strategy

The search strategy was centred around the terms “asthma”, “asthma exacerbation/attack”, “child” and “risk factor” and appropriate derivatives and synonyms were included. These terms were decided upon after a review of terms used in another systematic review published in this research area [10] as well as discussion with an information assistant. The full search strategy can be found in the supplementary material.

Duplicate titles were removed. Papers were screened independently, initially by title and abstract and then by full paper by one researcher (R. Lowden). Decision making was reviewed at regular meetings with the second author.

Relevant data were extracted using a pre-designed template (table 1), and included publication date, study design, nation, study setting, data collection period, population/inclusion criteria, sample size, definition of acute exacerbation and results. For articles that did not report the required data for meta-analysis, authors were contacted and asked to provide additional data.

View this table:
TABLE 1

Summary of key study characteristics of included studies

Study risk-of-bias assessment

The Effective Public Health Practice Project (EPHPP) quality assessment tool for quantitative studies [39] was used to assess each individual study in terms of potential biases and global study quality. Studies are given a global rating of either strong, moderate or weak, based on their scoring in the first six domains. The tool was adapted to remove the domains blinding, intervention integrity and analyses, as these were not relevant to the design of studies evaluated in this review. This left the following domains: selection bias, study design, confounders, data collection methods and withdrawals and dropouts. This assessment was performed by one author (R. Lowden) with discussion undertaken with the second author. The supplementary material includes explanations of how the tool was applied.

Effect measures

The primary outcome was presence of an acute exacerbation, as measured by binary (yes/no) response.

Meta-analysis

When odds ratios were available, meta-analysis was performed using Review Manager v5.4 software (https://training.cochrane.org/online-learning/core-software/revman).

Other synthesis methods

Publication bias was explored using funnel plots. Exacerbations were categorised into three severity categories: presentation to emergency department (ED); admitted to hospital; admitted to paediatric intensive care unit (PICU). A fourth category of “unspecified severity” was used for remaining studies that did not distinguish between severity of exacerbation. The index exacerbation was defined as the first exacerbation in all studies. The subsequent exacerbation was defined as the exacerbation that occurred after the index exacerbation. PPVs were collectively described as a median and range. Subgroups based on study design and location of publication were created post hoc and analyses performed to explore potential reasons for heterogeneity between the study results. The review methodology was not registered. A protocol is available on request from the corresponding author.

Results

Study selection and study characteristics

The initial database search identified 9185 potential titles. Figure 1 summarises the full selection process. After deletion of duplicates and screening by title and abstract, 32 full papers were reviewed, of which 19 were eligible. An additional seven papers were identified after reading citations, including four in the previous review [10], meaning that 26 papers were finally included. Four of the 11 papers in the previous review [10] were excluded due to their cross-sectional nature (n=2), using the same dataset used in another included paper (n=1) and the full paper not being accessible (n=1).

FIGURE 1
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.

Key characteristics are presented in table 1. 11 studies were published between 2000 and 2010 [13–23] and 15 between 2011 and 2021 [24–38]. 18 studies were from North America [13–23, 25, 26 ,29, 30, 32, 34, 35], three were from the Netherlands [31, 38, 27], and one each were from the UK [36], Saudi Arabia [37], Brazil [33], Thailand [28] and Australia [24].

Five studies had a prospective cohort design [13, 15, 20–22], with follow-up of 2 weeks [13], 6 months [20, 21], 12 months [15] and 3 years [22]. 10 studies used routinely acquired data [14, 16, 23, 26, 29–31, 35, 36, 38]; six had a retrospective case–control design [18, 27, 28, 33, 34, 37]; and one other [24]. Data from four RCTs [17, 19, 25, 32] were used, with follow-up of 28 days [17], 24 weeks [32], 48 weeks [17, 19, 25, 32] and 4 years [25]. In two RCTs, the intervention had no effect on exacerbation outcomes and data from both arms of the trial were pooled [17, 32]. The intervention in two RCTs may have influenced exacerbation outcome [19, 25].

The age range for populations varied: four included children aged 2–17 years [13, 20, 21, 26]; two included children aged 5–12 years [25, 36]; 19 had different age ranges spanning from 0 to 21 years; and one did not specify the age of the paediatric participants [27]. Unpublished data were provided by authors of two studies [19, 38], with one of these providing data from six populations [38]. The sample size varied from 76 [28] to 212 060 participants [38].

Risk of bias in studies

A summary of the quality assessment undertaken using the EPHPP quality assessment tool is presented in figure 2. 23 studies received a strong [13, 14, 16–21, 23–31, 33–38], three received a moderate [15, 22, 32] and none received a weak global rating.

FIGURE 2
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.

Definition of exacerbation used

Nine studies had an unspecified severity for the index exacerbation [19, 21, 22, 25, 31, 31, 32, 26, 38], three used ED visit [26, 34, 39], four used hospital admission [15, 18, 23, 29], and two used PICU for the index exacerbation [24, 27]. Figure 3 shows the number of studies that relate these different categories of exacerbations at baseline to risk of future exacerbations. Additionally, two studies used either ED visit or hospital admission [14, 16], one used PICU or hospital admission [37] and one looked at PICU, hospital admission or ED visit [34]. Other studies used definitions of exacerbation as “appropriate signs and symptoms in a known asthmatic” [20], “sudden worsening of symptoms resulting in difficulty breathing often requiring extra medicine to relieve symptoms, with/without unscheduled ED/doctor visit” [21] and “acute asthma that was severe or did not improve after three doses of bronchodilator nebulisation” [28].

FIGURE 3
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.

Nine studies were included where the severity of the index exacerbation was not specified [19, 21, 22, 25, 30, 31, 32, 35, 38] and odds ratios for meta-analysis were reported in six (including 10 populations and 162 583 individuals). The pooled OR (95% CI) for an index exacerbation having a subsequent exacerbation was 9.87 (5.02–19.39) (figure 4). A funnel plot was asymmetric (supplementary figure S1).

FIGURE 4
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.

Eight studies were identified where the index exacerbation required an ED visit [13, 14, 18, 21, 23, 26, 33, 35]. Two studies identified an association between an ED visit for asthma and a future exacerbation, using an unspecified severity definition [13, 33] and three studies reported that children with an ED visit for asthma were at risk of a future hospitalisation for asthma [18, 23, 26]. Five studies assessed the link between a past ED visit for asthma and the risk of a future visit to the ED [14, 21, 23, 26, 35]. Raw data were not available to allow meta-analysis (e.g. only odds ratios were reported). The odds ratios for the three studies with available data (970 individuals) were 3.30, 6.27 and 8.26 [14, 21, 23] (table 2). The PPV for the two studies with available data were 0.12 and 0.22 [21, 35].

View this table:
TABLE 2

Key results shown by index and subsequent exacerbation type

Nine studies were identified where the index exacerbation was a hospital admission [14–16, 18, 24, 27, 29, 34, 36], including six that described the relationship between an index and subsequent hospital admission for asthma [15, 18, 16, 29, 26, 24]. The median (range) odds ratio was 3.60 (1.89–5.36) for the five studies with available data (41 475 individuals) [15, 16, 18, 24, 29] (table 2). The PPVs for the two case-only studies with available data were 0.17 and 0.69 [15, 29].

Table 2 shows the results of two studies that looked at prior hospitalisation for asthma predicting future ED use for asthma. Three studies found an association between hospitalisation for asthma and future PICU admission with data from two studies (639 individuals) available for meta-analysis with OR 8.68 (95% CI 4.42–17.07) (figure 5a).

FIGURE 5
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.

Four studies were identified where the index exacerbation was a PICU admission [18, 37, 24, 28]. Two studies assessed the link between index and subsequent PICU admissions and the odds ratio from meta-analysis was 5.87 (95% CI 2.96–11.64) [37, 24] (figure 5a). Two other studies reported a link between a history of PICU admission for asthma and subsequent hospitalisation with the reported odds ratios being 2.18 [18] and 29.62 [28] (table 2).

Factors associated with heterogeneity

Recognising the heterogeneity in results within different exacerbation definitions we explored post hoc whether heterogeneity was reduced when subgrouping by healthcare system (i.e. North American versus other). Of the 11 studies with available data for inclusion in a meta-analysis, the odds ratio for an index exacerbation to have a subsequent exacerbation was 2.69 (95% CI 2.19–3.30, I2 49%) in the four published from North America [13, 19, 32, 25] (figure 5c), and 12.36 (95% CI 7.33–20.84, I2 95%) for the seven published outside North America [24, 27, 31, 33, 36–38] (figure 5d). The asthma severity was not specified in three of the four studies [19, 32, 25] from North America and four of the seven studies from other regions [31, 33, 36, 38].

In addition, we explored whether results differed by study methodology (i.e. RCTs, prospective cohort, routinely acquired data and retrospective case–control). Where more than one exacerbation category was reported we deferred to the one with highest incidence. The median (range) of PPV differed by study design as follows: for three RCTs [19, 25, 32] 0.58 (0.42–0.77); for four prospective cohort studies [13, 15, 20, 21] 0.31 (0.14–0.54); for six studies analysing routinely acquired data [23, 29, 31, 35, 36, 38] 0.16 (0.06–0.43); and for four retrospective case–control studies [27, 28, 33, 37] 0.50 (0.25–0.78) (supplementary table S1). Across different study design there was an even distribution of exacerbation severity definitions.

Two papers reported how the risk of experiencing a future exacerbation increased over time after the index exacerbation; however, this increase plateaued after 3 months in a study of exacerbations requiring hospitalisation [29] and after 6 months in another study using the unspecified severity definition [31].

Discussion

Our main finding was that although as previously reported an asthma exacerbation is a risk factor for a further exacerbation, there was no evidence of a relationship between increasing severity of an index asthma exacerbation and increasing odds ratio for a subsequent exacerbation. Additional findings were that odds ratios for a second exacerbation differed by geography (i.e. North America compared to other continents), study methodology (i.e. RCT and retrospective case-only study compared to cohort and routinely acquired data) and duration since index exacerbation. These findings give insight into the complexity of the relationship between index and subsequent asthma exacerbations. When speaking to parents and patients, clinicians should be aware that “mild” and “severe” initial exacerbations may both have equal odds ratios for a subsequent exacerbation.

A previous review with a broader remit than ours has reported how an exacerbation is associated with increased odds ratio of a future exacerbation in children [10]. In our review we included a larger number of studies and in addition, to confirm the earlier report [10], we find a greater magnitude of association than the earlier review for an index exacerbation being followed by a subsequent exacerbation.

In adults, the best predictor of a future exacerbation is also a past exacerbation [40], but in adults (unlike our findings in children) the odds ratios of future exacerbations are highest in those with history of a severe exacerbation [40]. We were able to confirm in children the observation made in adults, that the risk of further exacerbation is highest in the period following the index exacerbation, although in adults this appears to remain over a period of years, whereas in children the risk may reach a plateau after a period of months. Differences between asthma in children and adults are well described [41], so discordant findings between exacerbation risk in children and adults is expected. These findings highlight the importance of inclusion of previous exacerbation in risk stratification models for future exacerbation.

There are some limitations to the literature, which should be considered. First, there was little standardisation of the definition of exacerbation between studies, e.g. criteria for ED presentation or hospital/PICU admission were not pre-specified, and this will have introduced variability into the relationship between past and future exacerbations. The odds ratios and PPVs for a second ED presentation or hospital admission were not different and this may be due to children with similar exacerbation severities entering different pathways of care in different healthcare systems, for example those in North America compared to other countries.

A second limitation was that data from 15 of the studies could not be included in the meta-analysis due to either raw data not being available or insufficient details given. An additional limitation was that the meta-analysis used raw data and could not adjust for factors that may have differed between groups with and without an exacerbation (e.g. gender, age, race, severity of asthma, month of exacerbation) and the magnitude of the actual odds ratio may differ from that reported herein. A further limitation is that none of the studies considered the cause of the exacerbation nor described different outcomes for different triggers. Therefore, we cannot comment whether different triggers are associated with different risk for future exacerbations and therefore risk assessment should consider whether causes of exacerbation could be avoided. Additionally, details of the treatment that children received, both for acute symptoms and asthma prevention, were not provided. Furthermore, adherence to preventer therapy was not considered. Lack of adequate asthma preventer treatment and/or lack of adherence to asthma preventer treatment are both important risk factors for future exacerbations and should be considered as part of comprehensive future risk assessment.

A further limitation is that 18 of the 26 studies identified in this review were from North American populations and we demonstrated that the odds ratio for an exacerbation following an index exacerbation were lower for these studies compared to others, possibly due to differences in healthcare systems in North America and other continents. The results from five different European countries [38] were heterogeneous, and this may highlight differences in how asthma exacerbations are managed between countries. The reason for these differences could come from variations in asthma management, including medications, follow-up and asthma action plans, as well as varying compliance with medications, environmental factors and cultural differences [38]. There was also evidence of publication bias in the included studies, although these had minimal effect on the overall odds ratio of the meta-analyses performed.

A limitation of the methodology used in this review is that the literature search, data extraction and quality assessment processes were performed by one individual, leading to potential bias. The effects of this were mitigated by detailed discussion and involvement of an experienced paediatric clinician at every stage of the review. A second limitation to our methodology is that our results cannot be generalised to children aged <5 years, whose results are not included in this review.

The odds ratios and PPVs of an index exacerbation being followed by a further exacerbation were higher in the unspecified severity category studies when compared with studies that applied any of the three specified exacerbation severities. This initially seems counterintuitive, as it would be expected that children requiring hospitalisation for asthma, especially requiring PICU admission, would have more severe disease and are therefore more likely to experience a future exacerbation. However, the experience of having symptoms which necessitate a visit to the ED or an admission to hospital may improve treatment compliance and avoidance of triggers for exacerbation and thus reduce the likelihood of further exacerbations.

In summary, an index asthma exacerbation in children aged 5–16 years is a predictor of future acute exacerbation, and this relationship is not necessarily affected by exacerbation severity but is related to the period of follow-up, healthcare system and study methodology.

Conclusion

Our review of the literature supports asthma guideline advice that a past exacerbation is predictive of a future exacerbation. Additionally, our study places an estimated magnitude on the odds ratio and PPV for an exacerbation predictive of further relapse. Finally, our work gives insight into the complexity of the relationship between successive asthma exacerbations in children.

Supplementary material

Supplementary Material

Please note: supplementary material is not edited by the Editorial Office, and is uploaded as it has been supplied by the author.

Supplementary material 00174-2022.SUPPLEMENT

Footnotes

  • Provenance: Submitted article, peer reviewed.

  • Author contributions: R. Lowden and S. Turner contributed to the conception, design, data collection, analysis of the results, and to the writing and reviewing of the manuscript. S. Turner is the guarantor of the paper.

  • This article has an editorial commentary: https://doi.org/10.1183/23120541.00322-2022

  • Conflict of interest: The authors declare that there are no conflicts of interest to disclose.

  • Received April 8, 2022.
  • Accepted June 10, 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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