key: cord-1006341-cl3qt0qk
authors: Ferrante, Giuliana; Licari, Amelia; Marseglia, Gian Luigi; La Grutta, Stefania
title: Digital health interventions in children with asthma
date: 2020-12-06
journal: Clin Exp Allergy
DOI: 10.1111/cea.13793
sha: bdb7c5c2ee11337629064fdecb575920bf6c6779
doc_id: 1006341
cord_uid: cl3qt0qk

Although healthcare providers are actively involved in offering education, information and interventions for asthmatic patients, medication and therapeutic adherence remain low in the paediatric population, with estimates suggesting that adherence rates hover below 50%. A range of available digital health interventions has been explored in paediatric asthma with promising but variable results, limiting their widespread adoption in clinical practice. They include emerging technologies that yield the advantage of tracking asthma symptoms and medications, setting drug reminders, improving inhaler technique and delivering asthma education, such as serious games (video games designed for medical‐ or health‐related purposes), electronic monitoring devices, speech recognition calls, text messaging, mobile apps and interactive websites. Some of the proposed digital interventions have used multiple components, including educational and behavioural strategies and interactions with medical professionals. Overall, the implementation of such interventions may offer the opportunity to improve adherence and asthma control. In a state of emergency as the COVID‐19 pandemic, telemedicine can also play a central role in supporting physicians in managing children with asthma. This review evaluates the published literature examining digital health interventions for paediatric asthma and explores the most relevant issues affecting their implementation in practice and the associated evidence gaps, research limitations and future research perspectives.

Asthma is a common chronic disease in childhood, affecting approximately 10% of children worldwide. 1 The management of the disease is primarily aimed at maintaining symptoms control and reducing the risk of exacerbations. 2 Although most children achieve good control with standard therapies, such as inhaled corticosteroids (ICS) and/ or one or more controllers, asthma still imposes a high burden, especially in children with uncontrolled symptoms. 3, 4 A major cause of uncontrolled asthma is poor adherence to treatment, which has been described in 49%-71% of paediatric patients, resulting in an increased risk of missed days of school, decline in lung function, emergency department visits, hospitalizations and even death. [5] [6] [7] [8] [9] [10] Therefore, it is important to take into account treatment adherence, inhaler technique and self-management education in the management of children with asthma . However, asthma management can be hampered by several factors related to individual, family, community, healthcare system and patient-provider interaction domains. 11 Identifying interventions for promoting asthma treatment adherence and self-management is essential to obtain and maintain symptoms control and, finally, improve disease outcomes. These interventions may take many forms, including patient/caregiver education, simplified drug regimens, school nursing. Nonetheless, most of the studies performed to date have not shown significant self-management changes or better health outcomes due to improved adherence, mainly because these interventions are labour-intensive and not easily transferable to daily clinical practice. [12] [13] [14] [15] Over the last years, digital health emerged as a promising research area for achieving optimal and personalized asthma management.

The so-called electronic-Health (e-Health) solutions encompass various tools for self-monitoring of symptoms, self-management action plans, and patient education materials to improve treatment adherence and disease control. 16 They include emerging technologies that yield the advantage of tracking asthma symptoms and medications, setting drug reminders, improving inhaler technique and delivering asthma education, such as serious games (video games designed for medical or health-related purposes), electronic monitoring devices, speech recognition calls, text messaging, mobile-Health (m-Health) apps and interactive websites. 17 Of note, in the times of the pandemic, telemedicine would allow for quick contact and maintain continuity of care, especially for patients with chronic diseases.

A range of digital health interventions has been tested in paediatric asthma with variable results, which have currently limited their widespread adoption in real life, mainly due to heterogeneity of trials and lack of long-term effects. 18 This review evaluates the published literature examining digital health interventions for paediatric asthma and exploring the most relevant issues affecting their implementation in practice and the associated evidence gaps, research limitations and future research perspectives.

'Serious games', (SGs) that are games that do not have entertainment, enjoyment or fun as their primary purpose, have emerged as a new generation of videogames that offer the opportunity for constructive learning and training. 18, 19 Unlike traditional video games, SGs are built to convey meaningful information through interactive backgrounds similar to real-life situations.

One of the earliest SGs was an educational software program called 'Asthma Control': players could help Spacer, a superhero with asthma, manage his asthma by making decisions about taking rescue medication for acute symptoms and preventive medications regularly and consulting physicians for advice. Also, maintaining of normal activity, such as school attendance, was one of the proposed educational objectives. 20 This SG was tested in a randomized controlled trial (RCT) of 148 'inner-city' children, aged 7 to 12 years.

All children in the intervention group enjoyed playing the game and reached higher knowledge on asthma than the control group; however, no significant differences in parents' knowledge, children's behaviour related to asthma care and asthma severity were noted. 20 In a recent systematic review, Drummond et al reported the impact of 10 SGs focusing on asthma education targeting children and adolescents (Table 1) . 21 The role of SGs has also been investigated in teaching how to perform lung function tests, namely spirometry. Among others, 'SpiroGame' is an interactive respiratory game developed to teach spirometry. 33 Through a computer-animated program, children are facilitated to perform forced spirometry manoeuvers using multiple targets in a step-by-step manner. In the first step, the game teaches the child to differentiate between inhalation and exhalation by simulating a caterpillar crawling on a window to an apple for 30s of tidal breathing. In the second step, the game teaches performance of forced vital capacity by simulating a bee flying from flower to flower. 34 This approach has been evaluated both in healthy children and in children with asthma. Many children performed reliable forced expiratory flow-volume curves, with an overall success rate increasing with age. These were consistent with most of the established criteria by the American Thoracic Society/European Respiratory Society. 34 In comparison with verbal coaching techniques, 'SpiroGame' yielded comparable results and was also sensitive in detecting airway obstruction in children with moderate and severe symptoms.

Education delivered through SGs may facilitate healthcare professionals' specific tasks. Being child-centred and actively involving the child in his/her care, SGs may also enhance communication between children, their parents and clinicians by discussing progress achieved on a particular game. Also, including parents and caregivers in the learning process may positively impact family health behaviours.

Although SGs have shown good profile acceptability and feasibility and are effective in gaining knowledge, their use in paediatric asthma requires further studies on clinical outcomes. Electronic reminders: electronic tools allowing the patient to remember each medication dose through audio-visual devices.

Reminder systems are usually designed to ring only when an actuation/dose has been missed. 45 They can be connected to mobile devices and take advantage of the calendar of events/appointments with schedules configured based on the treatment plan. The

Smartinhaler technology platform has recently been combined with audio-visual alerts on the sensor device to remind patients if any medication is missed, and data on inhaler use can be uploaded using the Smartinhaler app or the Smartinhaler Connection Centre for sharing with clinicians via the software. 46 The effect of an EMD (SmartTrack; Nexus6, Auckland, New Zealand) recording time and number of actuations was investigated in a 6-month RCT on 220 schoolchildren with persistent asthma.

Children in the intervention group were also provided with an audio-visual reminder function and showed a median percentage adherence of 84% compared with 30% in the control group (P < .0001).

Moreover, they showed significantly higher symptoms control from baseline to 6 months than the control group (P = .008). However, it should be noted the lack of significant difference between groups for the primary outcome (number of days absent from school), likely because the study was underpowered to detect differences or because children with good adherence were using their devices incorrectly. 47 Larger and rigorous RCTs with post-intervention assessments are required to confirm the long-term efficacy of digital interventions in assessing adherence and other asthma-related outcomes, especially in managing children with persistent asthma.

Some of the proposed digital interventions have used multiple components, including educational and behavioural strategies and interactions with medical professionals.

Peer support group meetings and peer asthma messages delivered via mp3 players improved self-reported adherence to ICS in a 10-week RCT on 68 low-income adolescents with persistent asthma and poor adherence. No significant difference in objectively measured adherence was observed in comparison with controls. Of note, adherence declined in both groups over the study period, even though self-reported adherence resulted significantly higher than objectively measured adherence at the end of the study (P < .0001). 48 This finding suggests that healthcare professionals should be aware that there may be different priorities for adolescents and their caregivers for the management of asthma. About digital health, the use of electronic monitoring tools should be considered on a case-bycase basis, also taking into account patients' preferences in relation to asthma management within a context of shared decision-making.

Actively engaging patients and their caregivers in this process may reinforce the relationship with healthcare providers and ultimately improve self-management and disease outcomes. 49 An RCT testing the use of a website and text message reminders found a positive effect on medication adherence in adolescents with asthma. Forty-six subjects randomized to the intervention were asked to create a medication schedule and receive text message reminders at designated medication administration times for 3 weeks.

Controls received action lists as a part of their usual care. Although the authors did not perform an objective evaluation of treatment adherence, the intervention was associated with significant improvements in self-reported adherence (P = .011), QoL (P = .037) and

self-efficacy (P = .016). Interestingly, no significant improvement of asthma control was observed likely because most subjects in this study had good asthma control at baseline or because self-reported adherence was overestimated. 50 The use of a multidimensional web platform, including educa- 

The widespread use of smartphones contributed to the recent advancements in m-Health, an emerging healthcare model that is achievable through mobile devices. More than 500 asthma-related apps were reported in 2019, mainly providing health education, compliance to therapies, symptom tracking and environmental alerts. However, despite the significant number of available mobile apps for asthma, their use in clinical settings is not validated yet. 53 Its efficacy has not been evaluated; one pilot study in adults has shown its ability to predict asthmatic exacerbations. significant gains in asthma control (P = .03) and QoL (P = .05). This may be related to the high levels of self-reported adherence in both groups at baseline, probably due to children's awareness of taking part in a trial evaluating asthma outcomes, including adherence, which might have enhanced their motivation in following the medication prescription. 55 A summary of emerging e-Health solutions for asthma management is provided in Table 2 . 53, [56] [57] [58] [59] [60] [61] [62] Overall, both digital standalone and combined multicomponent interventions showed promising results on treatment adherence and clinical outcomes.

Nevertheless, inconsistencies between published results exist and might be mainly ascribed to different study populations and design.

Telemedicine involves the use of information and communication technologies to improve patient outcomes by increasing access to care and medical information. 63 Previous data on telemedicine in paediatric asthma management are available. Trials of telemedicine interventions were mainly applied in school settings, providing counselling services and managing exacerbations. The impact of telemedicine on asthma-related clinical outcomes, such as symptoms, pulmonary function, healthcare utilization and medication use, was also investigated, as well as patient/parent satisfaction and QoL ( Figure 1 ). 64, 65 As reported by recent systematic reviews, the available evidence supporting the introduction of telemedicine for asthma management showed conflicting data, but none of the included studies indicated adverse effects. 64, 65 In the context of the rapid worldwide spread of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), telemedicine might provide an additional and essential resource for managing children with asthma, replacing in-person visits. [66] [67] [68] [69] Telemedicine may also be helpful to patients with severe or uncontrolled asthma who might be at increased risk per se, due to lack of monitoring caused by social distancing and lockdowns. 70, 71 In order to prevent the risk of SARS-CoV-2 transmission, as well as gain and maintain asthma control, national and international guidelines were promptly published to provide new and essential recommendations for the management of paediatric asthma during the pandemic. 70, [72] [73] [74] [75] Firstly, telemedicine promotes social distancing. 70 Particularly, telemedicine may (a) limit the exposure of healthcare providers to potentially infected patients, (b) avoid the patient-to-patient viral transmission, protecting children with immunodeficiencies or other chronic comorbidities and (c) provide a rapid evaluation for potential viral infection. 76 Secondly, the availability of online communication platforms may easily allow virtual consultations for first and follow-up visits of asthmatic children and share F I G U R E 1 Telemedicine cycle in asthma management F I G U R E 2 Future goals of digital health interventions in paediatric asthma clinical data (investigations, imaging and laboratory results). In this context, the suspension of spirometry during the COVID-19 pandemic (as it is a possible aerosol-generating procedure) represents a barrier to proper asthma diagnosis and monitoring. 73 Thus, telemedicine should also be considered for remote lung function testing, as many innovative and emerging approaches are becoming available.

They include peak expiratory flow devices, portable electronic spirometers, portable exhaled nitric oxide measurement and novel digital health tools such as smartphone microphone spirometers. 77 Most of these devices that are commercially available are also designed to download results onto mobile devices or computers, facilitating transmission to and monitoring by healthcare professionals. While considering the limitations, including cost, lack of technique feedback and variable accuracy, some of these devices, such as portable spirometers, may be valuable in-home monitoring in some settings, integrating virtual care with critical physiological data. Finally, telemedicine may help paediatricians manage mild-moderate asthmatic exacerbations that do not show 'red flags', requiring urgent care or tests for COVID-19.

However, although telemedicine's potential, no studies have been realized to assess its real benefits and efficacy in managing asthma in children during this period of health emergency; thus, extensive and multicentric studies are truly indispensable.

The increased use of health digital devices will likely become a relevant aspect of a proactive asthma care model in the next few years ( Figure 2) . Extrapolated data will allow physicians to provide personalized tools, tailored solutions to improve child health, improve symptom reports and appropriate specialty referrals. Before such an approach can be widely integrated in routine clinical practice, the acceptability and feasibility should be ascertained among all patients, including those disproportionately affected by the disease. Indeed, most tools have not been designed to address barriers faced by racial/ethnic minority groups or those of low socioeconomic status and poor health literacy. 78 Overall, future research in this field should be based on larger and rigorous controlled trials with objective adherence assessment and post-intervention evaluation of long-term efficacy. 42 Finally, unique regulatory concerns need to be addressed with the increasing use of these new technologies. Not all devices require approval by regulatory bodies or need an evidence-based background to be marketed.

The increasing availability of technology-based solutions, only if combined with the clinician's equipment, will offer more successful opportunities in reaching the full benefit for patients and health systems alike.

The authors declare that they have no conflict of interest.

Data sharing not applicable to this article as no datasets were generated or analysed during the current study.

https://orcid.org/0000-0001-9917-2387

Amelia Licari https://orcid.org/0000-0002-1773-6482

Gian Luigi Marseglia https://orcid.org/0000-0003-3662-0159

Stefania La Grutta https://orcid.org/0000-0001-8026-0715

The burden of pediatric asthma

Pocket Guide for Asthma Management and Prevention. Global Initiative for Asthma

Difficult vs. severe asthma: definition and limits of asthma control in the pediatric population

The burden of severe asthma in childhood and adolescence: results from the paediatric U-BIOPRED cohorts

Adherence to asthma treatment in childhood and adolescence -a narrative literature review

National prevalence of poor asthma control and associated outcomes among school-aged children in the United States

Adherence rate to beclomethasone dipropionate and the level of asthma control

It's the adherence, stupid (that determines asthma control in preschool children)!

Anti-inflammatory medication adherence, healthcare utilization and expenditures among Medicaid and children's health insurance program enrollees with asthma

Low-dose inhaled corticosteroids and the prevention of death from asthma

Barriers to medication adherence in asthma: The importance of culture and context

Interventions to improve adherence to inhaled steroids for asthma

Behavioral interventions to improve asthma outcomes for adolescents: a systematic review

School-based supervised therapy programs to improve asthma outcomes: current perspectives

A pilot randomized trial of school-based administration of inhaled corticosteroids for at-risk children with asthma

Electronic health (e-Health): emerging role in asthma

Novel methods for device and adherence monitoring in asthma

What is the impact of innovative electronic health interventions in improving treatment adherence in asthma? The pediatric perspective

Serious games: games that educate, train, and inform. Muska & Lipman/Premier-Trade

An evaluation of an innovative multimedia educational software program for asthma management: report of a randomized, controlled trial

A systematic review of serious games in asthma education

The asthma files: evaluation of a multimedia package for children's asthma education

A randomized, controlled trial of an interactive educational computer package for children with asthma

Effectiveness of a multicomponent self-management program in at-risk, school-aged children with asthma

Backpack adventures in asthma': Interactive multimedia computer game piques childrens' interest in asthma

Inc 11830 Westline Industrial Dr

Educational intervention by computer in childhood asthma: a randomized clinical trial testing the use of a new teaching intervention in childhood asthma

Discover, Think, and Act: evaluation of computer-assisted instruction to improve asthma self-management in inner-city children

Impact of a computer-assisted education program on factors related to asthma self-management behavior

An in-school CD-ROM asthma education program

Quest for the Code': a study of a computer based education program for children with asthma

Enhancing learning through an online secondary school educational game

A randomized, controlled trial of LungtropolisTM: An internet asthma game for children and companion website for parents

The role of computer games in measuring spirometry in healthy and "asthmatic" preschool children

An interactive computer-animated system (SpiroGame) facilitates spirometry in preschool children

Adherence monitoring and e-health: how clinicians and researchers can use technology to promote inhaler adherence for asthma

Electronic monitoring of adherence to inhaled corticosteroids: an essential tool in identifying severe asthma in children

Validation of the Doser, a new device for monitoring metered-dose inhaler use

What we mean when we talk about adherence in respiratory medicine

Providing feedback on adherence increases use of preventive medication by asthmatic children

Adherence to medication in children and adolescents with asthma: methods for monitoring and intervention

Pragmatic trial of health care technologies to improve adherence to pediatric asthma treatment: a randomized clinical trial

Systematic review of digital interventions for pediatric asthma management

A randomized trial of user-controlled text messaging to improve asthma outcomes: a pilot study

e-Monitoring of Asthma Therapy to Improve Compliance in children (e-MATIC): a randomised controlled trial

Using electronic monitoring devices to measure inhaler adherence: a practical guide for clinicians

Smartinhaler for asthma

The effect of an electronic monitoring device with audiovisual reminder function on adherence to inhaled corticosteroids and school attendance in children with asthma: a randomised controlled trial

The Impact of Peer Support and mp3 Messaging on Adherence to Inhaled Corticosteroids in Minority Adolescents with Asthma: A Randomized, Controlled Trial

Adolescent and caregivers' experiences of electronic adherence assessment in paediatric problematic severe asthma

The feasibility of text reminders to improve medication adherence in adolescents with asthma

Evaluation of a web-based asthma self-management system: a randomised controlled pilot trial

Short-term effect of a smart nebulizing device on adherence to inhaled corticosteroid therapy in Asthma Predictive Index-positive wheezing children

Digital Phenotype and Actionable Insights for Pediatric Asthma

A tailored mobile health intervention to improve adherence and asthma control in minority adolescents

Targeting quality of life in asthmatic children: The MyTEP pilot randomized trial

A predictive model for clinical asthma exacerbations using albuterol eMDPI (ProAir Digihaler): a 12-week, open-label study

Effectiveness of population health management using the propeller health asthma platform: a randomized clinical trial

An audiovisual reminder function improves adherence with inhaled corticosteroid therapy in asthma

The reliability and patient acceptability of the SmartTrack device: a new electronic monitor and reminder device for metered dose inhalers

Mobile health applications for asthma

A systematic evaluation of asthma management apps examining behavior change techniques

Exploring the Association Between Self-Reported Asthma Impact and Fitbit-Derived Sleep Quality and Physical Activity Measures in Adolescents

School-based telemedicine interventions for asthma: a systematic review

Telemedical asthma education and health care outcomes for school-age children: a systematic review

Digital technologies and adherence in respiratory diseases: the road ahead

Impact of mHealth chronic disease management on treatment adherence and patient outcomes: a systematic review

Telemedicine in primary care for patients with chronic conditions: the ValCrònic Quasi-experimental study

Overview on the challenges and benefits of using telehealth tools in a pediatric population

COVID-19: Pandemic Contingency Planning for the Allergy and Immunology Clinic

Managing childhood allergies and immunodeficiencies during respiratory virus epidemics -The 2020 COVID-19 pandemic: A statement from the EAACI-section on pediatrics

Consensus statement of the Italian society of pediatric allergy and immunology for the pragmatic management of children and adolescents with allergic or immunological diseases during the COVID-19 pandemic

Italian pediatric respiratory society recommendations on pediatric pulmonary function testing during COVID-19 pandemic. Version 2

Impact of COVID-19 on Pediatric Asthma: Practice Adjustments and Disease Burden

Allergy and asthma in children and adolescents during the COVID outbreak: What we know and how we could prevent allergy and asthma flares

Use of telemedicine and virtual care for remote treatment in response to COVID-19 Pandemic

Addressing reduced laboratory-based pulmonary function testing during a pandemic

How to cite this article: Ferrante G, Licari A, Marseglia GL, La Grutta S. Digital health interventions in children with asthma