Current and Optimal Practices in Childhood Asthma Monitoring Among Multiple International Stakeholders

Key Points Question What are the actual and perceived optimal childhood asthma monitoring practices globally? Findings This international survey study of 1319 health care professionals and clinical academics from 88 countries found that children with mild to moderate asthma attended regular monitoring visits, whereas those with severe asthma required more frequent visits. Health care professionals reported monitoring pediatric asthma holistically, prioritizing symptoms, treatment adherence, pulmonary function, safety, and quality of life; airway inflammation, airway responsiveness, and biomarkers were evaluated on clinical indication. Meaning These findings suggest that pediatric asthma monitoring is performed generally homogeneously worldwide, in most cases following evidence-based standards.


Introduction
Asthma remains a major cause of morbidity, with socioeconomically challenged populations experiencing the most cases. 1,2Asthma outcomes largely depend on the quality and intensity of regular monitoring. 3,4Periodic or continuous assessment and review are key elements of asthma monitoring, according to the Global Initiative for Asthma. 5Nevertheless, monitoring procedures have attracted less attention than approaches to diagnosis or treatment choices, and monitoring pathways have been extensively revisited during the COVID-19 pandemic. 6,7These considerations are vital when it comes to children, in whom disease variability is higher in parallel to the child's growth. 8e literature offers substantial evidence on the efficacy of monitoring of particular domains, such as symptoms, 9 lung function, 10 airway inflammation, 11 airway responsiveness, 12 and adherence to treatment, 13 as well as on specific tools used within each domain.Additional aspects, such as the assessment of medication adverse effects, inhaler technique, psychological status, exercise, environmental factors, or diet, are also considered important.However, there is little formal assessment of prioritization among domains or on the value of care pathways that may result from different monitoring strategies.Innovative strategies, particularly on remote patient monitoring, are rapidly appearing. 14 important step toward optimal monitoring is understanding current practices.Although the literature on monitoring has been reviewed, 15 the characteristics of pediatric asthma monitoring in the clinical setting have never been assessed.Paediatric Asthma in Real Life (PeARL) is a think tank set up by the Respiratory Effectiveness Group that consists of international health care professionals (HCPs), clinical academics, and expert patient representatives with expertise in and professional exposure to pediatric asthma. 16,17Asthma monitoring techniques and frequency were prioritized in a previous PeARL report that explored unaddressed clinical needs in pediatric asthma. 16 this study, we surveyed monitoring practices worldwide, including in various health care settings.The aim of the study was to examine how monitoring practices diverge internationally and to what extent these practices fall short of an ideal monitoring care pathway, as perceived by HCPs.In addition, we extended our survey to crowdsource envisioned optimal approaches, providing the opportunity to compare and portray actual status and unmet needs.

Methods
This quantitative survey was developed, conducted, and reported following guidance on survey research by the American Association of Public Opinion Research. 18A list was prepared on the potential domains of monitoring and the tools that can be used to assess each domain (eTable 1 in Supplement 1).This list was based on literature searches (eAppendix in Supplement 1) followed by a saturation exercise among the PeARL Think Tank members, including expert patient representatives.
After deduplication, the list was used by the steering group to develop a survey designed to capture the frequency and priority of each of the monitoring domains, the frequency with which each of the tools is used in clinical practice, as well as the proportion of patients who require monitoring with each technique.The questions were repeated for optimal monitoring according to the perception of the respondent.Finally, information was captured on demographic and professional details of the respondents.Independent members of the group reviewed the survey to establish completeness

Statistical Analysis
Responses are presented descriptively.We tested for differences between the frequency that different techniques are actually used in practice vs optimal practice using cumulative link models for ordinal regression based on analysis of variance.The same test was used to explore between-group differences.We assessed differences across medical settings and country economies (World Bank classification).Because this was an extensive survey with optional responses, it was anticipated that some participants may discontinue before completing it.To explore potential attrition bias, we compared baseline characteristics and responses of those who completed at least 25%, 50%, 75%, and 100% of the responses compared with those who did not reach each of these thresholds, using 1-way, ordinal analysis of variance.In addition, we explored potential differences in the responses of European vs non-European respondents.
Analysis was performed in R software, version 3.6.3(R Foundation for Statistical Computing).All statistical tests were 2-sided, and the critical level of significance was set at P < .05.

Results
The

Tools and Techniques Used During Monitoring Visits
The tools and techniques used during monitoring visits are presented in Figure 3   comparing actual with optimal conditions; there were no differences between actual and optimal for spirometry and reversibility testing, whereas a large move from no use to occasional use was observed for oscillometry and plethysmography.referred to electronic patient and/or pharmacy records to assess adherence; both were suggested in an ideal setting by more than 90%.Quality of life was assessed by 685 of 1110 HCPs (61.7%).In the perceived optimal setting, this increased to more than 90%.Psychological, nutritional, and lifestyle aspects were variably monitored; in all instances, these parameters were perceived as improvable.

Between-Visit Monitoring
A more dynamic picture was drawn for monitoring between regular visits.The top priorities were similar as for regular visits: symptoms and control, adherence, comorbidities, and adverse events (90%-70%) (Figure 2B).However, lung function was considered a high or very high priority by only 449 of 960 respondents (46.8%).

Differentiation of Responses by Specialty, Level of Care, Geographic Region, and Affluence
Overall, we observed limited differences in the responses from different care settings or countries of different affluence per the World Health Organization (eFigures 12-17 in Supplement 1).The duration of visits for mild to moderate asthma was shorter in lower-income countries (median of 10-20 vs 20-30 minutes), whereas for severe asthma, visits were longer in upper-to middle-income Modest differences were observed when comparing professionals of different groups on use of monitoring instruments (eFigures 14-17 in Supplement 1).Although in low-and middle-income countries history and clinical examination were consistently used in every monitoring visit, in highincome countries, the use of standardized control questionnaires appeared to be prioritized for assessing symptoms and control.Spirometry was used more frequently in secondary and tertiary care and in more affluent countries, whereas an opposite trend was observed for peak expiratory flow rate.Our data suggest more widespread use of between-visit monitoring tools, predominantly symptom diaries but also spirometry and mHealth trackers in the less affluent countries.In addition, specialized care settings more frequently used body plethysmography, oscillometry, reversibility to bronchodilator, bronchial challenges, skin prick tests, and FeNO, whereas oxygen saturation was more often used in primary care.Finally, treatment adherence was more consistently assessed in secondary and tertiary care.

Discussion
To our knowledge, this survey study is the first description of actual pediatric asthma monitoring practices internationally.Combined with a prioritization exercise and a needs assessment, we point out priority areas of potential improvement.Different patterns of use of monitoring domains and tools emerged: (1) frequent use with expectations for further improvement (eg, control and adherence), (2) occasional use considered adequate (eg, spirometry and biomarkers), or (3) very low use with aspiration for availability (eg, technologically advanced tools available for research, oscillometry, and bronchoprovocations).Among several high-priority items, assessment of control, adherence, and growth were in the top tier, possibly reflecting empathetic monitoring directed at the needs of the patient (eBox in Supplement 1).In addition to clinical utility and efficacy, priorities may also reflect considerations such as time availability and access to technologies.Head-to-head studies comparing monitoring domains (eg, adherence vs adverse events) are not available or make little sense; therefore, consensus prioritization is important.
A surprising, but optimistic, finding was that differences not only in actual monitoring practices but also in aspirations across geography, economic status, or level of care were modest.Although actual practices may be influenced by international guidelines, it appears that, at least within the survey respondents, the core needs for pediatric asthma monitoring are universal.The area with the highest unmet need is that of new digital technologies for between-visit continuous monitoring, such as electronic patient diaries, smart devices for adherence monitoring, and health trackers.Validated symptom and control scores are considered the cornerstone of asthma monitoring. 5ey can identify and quantify poor asthma control, predict outcomes (such as exacerbations), and effectively guide further management. 19,20Not surprisingly, HCPs consistently use at least 1 score for monitoring asthma.Although the Asthma Control Test was more broadly used compared with the Asthma Control Questionnaire or the Composite Asthma Severity Index, our survey revealed a clear interest in expanding their use.
Spirometry is also used frequently, despite known limitations in childhood. 21The global lung initiative spirometry reference values and z scores for children and adolescents represent a significant step forward and need to be broadly adopted.Although PEFR is inferior to spirometry and its use has been questioned, it is a very simple and affordable measure of lung function.Because PEFR is an aerosol-generating procedure, its use was discouraged during the COVID-19 pandemic and its uptake may have been further reduced.In parallel, the use of novel tools, such as oscillometry, is limited, most likely because of limited availability and experience. 22rway inflammation monitoring, through FeNO, may guide asthma treatment. 23Some added value has been shown in predicting response to inhaled corticosteroids and preventing exacerbations, but there was no effect on symptoms or use of medications. 24Availability, cost, and variability due to unrelated exposures are probably reflected in the current infrequent use of FeNO monitoring, with moderate interest for intensification. 25rway hyperresponsiveness monitoring has been suggested as a strategy to improve outcomes in adult asthma, 26 but this has not been confirmed in children. 12Bronchial challenges are relatively invasive and time-consuming and thus not currently recommended for monitoring. 5Unsurprisingly, their actual use for this purpose is rare, although they are only moderately desired.Exercise challenge stands out because it is occasionally performed in children, however with no interest for additional use in an optimal scenario.
Levels of total and specific IgE and numbers of sputum or circulating eosinophils are critical for phenotyping and often for choosing treatment, particularly in severe asthma. 27The presence of atopy also has important predictive value for asthma persistence. 28Sputum eosinophils may guide management; however, the process is difficult, especially in younger children; time-consuming; and not significantly better in the long term compared with symptom-based management. 29In addition, the extent and clinical significance of biomarker fluctuations are not well established, and phenotypes are not stable in adults and even less in children, 30,31 which may explain their infrequent measurement and limited interest for expansion.Interestingly, the proposed optimal frequency of use of multiple allergen tests was less than the actual use (the only instance within the survey that such a reduction was suggested).
Besides growth monitoring, which was assessed by most respondents, other safety parameters were not considered a priority.Although extensive community studies do not support concerns about the potential long-term effect of inhaled corticosteroids on children's development, 32 inhaled corticosteroids, especially when used at excessive doses, as well as systemic corticosteroids and other asthma treatments, may have burdensome adverse events that require close monitoring. 33,34e structure of our survey, which only inquired about specific long-term safety parameters, possibly did not fully capture monitoring for adverse drug reactions.
Poor treatment adherence and inhalation technique are leading causes of treatment failure. 35,36r findings suggest that HCPs are aware of this, assessing adherence and providing education regularly.However, most often, adherence is not assessed in a standardized way.Adherence evaluation could be optimized using clinically validated tools, including questionnaires such as the Medication Adherence Rating Scale or Test of Adherence to Inhalers, electronic monitoring adherence tools, and electronic patient records with prescription pick-up linkage 37,38 ; however, this form of cooperation with patients may raise understandable ethical questions.
Although the importance of obesity, 39 psychological status, 40 and lifestyle 41 42 Importantly, quality of life is not being adequately addressed, despite being prioritized as an outcome by patients, their families, and clinicians. 43Environmental exposures are highly relevant to asthma activity in children, 44,45 but they also appear to be somehow neglected, possibly because of the challenge of identifying the environmental triggers and their fluctuations and the difficulty of modifying them.
In addition to visit-based intermittent monitoring, new technologies promise intensification and improvement of monitoring through regular or even continuous at-home evaluation. 37Although telemonitoring has not yet shown conclusive superiority, 46 its potential and use have rapidly increased during the COVID-19 pandemic, 6 whereas numerous approaches are being explored.
Although the usefulness and reliability of traditional tools for between-visit monitoring, such as diary cards and peak expiratory flow measurements, have been challenged, 47 there is much promise in mHealth and eHealth disease activity tracking, 48 as well as development of smart devices for medication adherence. 49According to our findings, this innovation scene has only reached a small proportion of patients; nevertheless, there is high expectation toward the inclusion of such tools in an ideal setting.Interestingly, the pattern of use and expectation is almost identical for all the novel approaches, probably because progress (and consequent offer) is faster than validation.
Nevertheless, highly promising and validated solutions, such as the MASK-air app, are rapidly being developed. 50

Strengths and Limitations
The study has several strengths.The sample size is large, with multistakeholders and international representation.The design allows direct comparisons between the actual and perceived ideal situation.Patient input was used in its design.A high proportion of the respondents were practicing physicians with direct clinical experience.The overrepresentation of tertiary care HCPs was addressed by subgroup analysis by treatment setting.
The study also has some limitations.As with any survey, this report is potentially biased by its sampling.Our study participants can be presumed to have had particular interest in pediatric asthma and therefore high clinical standards and expectations independent of their specialty.Nevertheless, these individuals would be the exact audience expected to study and appraise any further international harmonization efforts, as well as being the hubs for educating HCPs on a larger scale.
Although we aimed to cover all geographic areas and socioeconomic strata to the maximum possible extent, Europe is overrepresented, whereas low-income countries and Africa are less well represented in our sample.This limitation may reflect a lower asthma incidence but most probably represents reduced information access to and from these areas.In contrast to other studies 51,52 that specifically focused on underrepresented parts of the globe, we did not specifically aim to oversample underrepresented parts of the world, which might have remedied this limitation.
Because this was an extensive survey, a moderately high attrition rate was expected (range, 6.5%-29%); however, sensitivity analysis confirmed that this did not affect the outcomes.
Environmental factors were not adequately addressed in our survey and need to be addressed in future research.We only assessed whether environmental factors trigger a change in the frequency of asthma monitoring visits and not how often they are addressed in current or optimal practice.
Practice surveys are inherently limited by the subjectivity of responses and tendency of HCPs to overestimate their good care.Ideally, these findings will need to be validated in actual clinical data.
Furthermore, we recognize that monitoring choices should be personalized at a level of complexity beyond the capacity of a survey.

Conclusions
The results of this survey study suggest that asthma monitoring in children is performed rather homogeneously worldwide, with priorities consistent in most cases with the evidence.A core group

Figure 1 .
Figure 1.Actual and Perceived Optimal Monitoring Visit Frequency and Duration in Severe Asthma

Figure 2 .
Figure 2. Prioritization of Asthma Monitoring Domains

Figure 3 .
Figure 3. Use of Monitoring Tools During Asthma Monitoring Visits History and clinical examination A

Figure 4 .
Figure 4. Use of Monitoring Tools Between Asthma Monitoring Visits Asthma control questionnaires A Current and Optimal Practices in Childhood Asthma Monitoring Ethics review was not required for this survey of HCPs in line with the UK National Health Service Research Ethics Committee guidance.Participant consent was implied by voluntary completion of the survey.The study followed the American Association for Public Opinion Research (AAPOR) reporting guideline.The survey (eAppendix in Supplement 1) was launched via SurveyMonkey, version September 2021 (Momentive) between April 12 and September 3, 2021.It was disseminated globally to HCPs and clinical academics with a professional interest in and exposure to childhood asthma by email and through social media (Twitter and LinkedIn) by the Respiratory Effectiveness Group and European Academy of Allergy and Clinical Immunology.Responses were considered valid provided the participants answered at least 1 clinical question.

Table . Demographic
Characteristics of the Survey Respondents a Abbreviation: NA, not applicable.aDemographic characteristics are summarized as a percentage of all participants; missing data are not listed in this table.

JAMA Network Open | Pediatrics
of tools, including history, clinical examination, and treatment adherence assessment, are consistently implemented.Areas for improvement include standardized asthma control questionnaires, pulmonary function monitoring, delivery of patient education, and expansion of between-visit monitoring.Finally, a desire for access to advanced asthma phenotyping tools, such as airway inflammation and responsiveness assessment, emerged, especially among HCPs working in secondary or tertiary care and in more affluent health systems.There is an apparent need for additional standardization and increased availability of tools, although the promise of new technologies has already been translated into high expectations in continuous monitoring.The results of this survey, in conjunction with the available evidence base, can inform recommendations toward further optimization.Heatmap Summarising the Proportion of Respondents That Would Prefer to Use Each Monitoring Tool More Frequently eAppendix.Supplementary Methods eFigure 1. Participants by Country Income eFigure 2. Participants by Geographic Region eFigure 3. Participants by Country of Residence (Global Figures) eFigure 4. Participants by Country of Residence (Europe) eFigure 5. Participants by Country of Residence eFigure 6. Actual and Perceived Optimal Monitoring Visit Frequency (in Months) and Duration (in Minutes) for Children With Mild or Moderate Asthma eFigure 7. Actual (Light Blue, Left Side of the Violin Plots) and Perceived Optimal (Green, Right Side of the Violin Plots) Use of Monitoring Tools During Asthma Monitoring Visits eFigure 8. Prioritisation of Different Domains of Asthma Monitoring During Follow-up Visits, Stratified by Country Income eFigure 9. Prioritisation of Different Domains of Asthma Monitoring During Follow-up Visits, Stratified by Care Setting eFigure 10.Prioritisation of Different Domains of Asthma Monitoring Between Follow-up Visits, Stratified by Country Income eFigure 11.Prioritisation of Different Domains of Asthma Monitoring Between Follow-up Visits, Stratified by Care Setting eFigure 12. Actual (Left) and Perceived Optimal (Right) Monitoring Visit Frequency (in Months), for Children With Mild/Moderate and With Severe Asthma, Stratified by the Country Income and Health Care Setting of the Respondents JAMA Network Open | Pediatrics Current and Optimal Practices in Childhood Asthma Monitoring Actual (Left) and Perceived Optimal (Right) Monitoring Visit Duration (in Minutes), for Children With Mild/Moderate and With Severe Asthma, Stratified by the Country Income and Health Care Setting of the Respondents eFigure 14.Actual (Light Blue, Left Side of the Violin Plots) and Perceived Optimal (Green, Right Side of the Violin Plots) Use of Monitoring Tools During Asthma Monitoring Visits, Stratified by Country Income eFigure 15.Actual (Light Blue, Left Side of the Violin Plots) and Perceived Optimal (Green, Right Side of the Violin Plots) Use of Monitoring Tools During Asthma Monitoring Visits, Stratified by Care Setting eFigure 16.Actual (Light Blue, Left Side of the Violin Plots) and Perceived Optimal (Green, Right Side of the Violin Plots) Use of Monitoring Tools Between Asthma Visits, Stratified by Country Income eFigure 17.Actual (Light Blue, Left Side of the Violin Plots) and Perceived Optimal (Green, Right Side of the Violin Plots) Use of Monitoring Tools Between Asthma Visits, Stratified by Care Setting eBox.Identified Priorities for Monitoring During Visits JAMA Network Open.2023;6(5):e2313120.doi:10.1001/jamanetworkopen.2023.13120(Reprinted) May 12, 2023 10/15 Downloaded From: https://jamanetwork.com/ on 09/16/2023 JAMA Network Open.2023;6(5):e2313120.doi:10.1001/jamanetworkopen.2023.13120(Reprinted) May 12, 2023 14/15 Downloaded From: https://jamanetwork.com/ on 09/16/2023 eFigure 13.