key: cord-0022955-ua2rbc2l
authors: Cheng, Zai Ru; Tan, Yi Hua; Teoh, Oon Hoe; Lee, Jan Hau
title: Keeping Pace with Adolescent Asthma: A Practical Approach to Optimizing Care
date: 2021-11-06
journal: Pulm Ther
DOI: 10.1007/s41030-021-00177-2
sha: c5ea00b410a4fbdbe485aa0699a36d695d8afaf8
doc_id: 22955
cord_uid: ua2rbc2l

Known for their pre-occupation with body image, self-identity creation, peer acceptance, and risk-taking behaviors, adolescents with asthma face unique challenges. Asthma is a heterogeneous disease and accurate diagnosis requires assessment through detailed clinical history, examination, and objective tests. Diagnostic challenges exist as many adolescents can present with asthma-like symptoms but do not respond to asthma treatment and risk being mis-diagnosed. Under-recognition of asthma symptoms and denial of disease severity must also be addressed. The over-reliance on short-acting beta-agonists in the absence of anti-inflammatory therapy for asthma is now deemed unsafe. Adolescents with mild asthma benefit from symptom-driven treatment with combination inhaled corticosteroids (ICS) and long-acting beta-agonist (LABA) on an as-required basis. For those with moderate-to-persistent asthma requiring daily controller therapy, maintenance and reliever therapy using the same ICS-LABA controller simplifies treatment regimes, while serving to reduce exacerbation risk. A developmentally staged approach based on factors affecting asthma control in early, middle, and late adolescence enables better understanding of the individual’s therapeutic needs. Biological, psychological, and social factors help formulate a risk assessment profile in adolescents with difficult-to-treat and severe asthma. Smoking increases risks of developing asthma symptoms, lung function deterioration, and asthma exacerbations. Morbidity associated with e-cigarettes or vaping calls for robust efforts towards smoking and vaping cessation and abstinence. As adolescents progress from child-centered to adult-oriented care, coordination and planning are required to improve their self-efficacy to ready them for transition. Frequent flare-ups of asthma can delay academic attainment and adversely affect social and physical development. In tandem with healthcare providers, community and schools can link up to help shoulder this burden, optimizing care for adolescents with asthma.

The 'waters of adolescence' are navigated by individuals 10-19 years old [1] . Up to 12% of adolescents worldwide suffer from chronic disease [2] and asthma continues to afflict this age group. Widely considered a disease of childhood with reduction in symptom flare-ups with age [3] , adolescents still experience significant asthma morbidity [4] due to unique challenges posed whilst entering this phase and during transition to adult care [5] . Peer acceptance, selfidentity, and experimentation form a web of psychosocial factors that interlace with the biological changes of puberty to have a profound impact on adolescent health and wellbeing [6] . This necessitates the adoption of a developmentally staged management approach in adolescents with asthma [7] . This narrative review discusses diagnostic conundrums, pitfalls associated with over-and under-reporting of asthma symptoms, and the impact of developmental stages on adolescent asthma control. Factors associated with difficult-to-treat and severe asthma in adolescence and blind spots during transition to adult-oriented care are also highlighted. This article is based on reviews of current guidelines and literature and did not involve any new studies with human participants or animals performed by any of the authors. Table 1 lists common mimickers of asthma in an adolescent. Asthma is highly heterogeneous and symptoms and control vary with the passage of time [8] , on the back of a multitude of triggers [9] . Diagnostic uncertainty can arise when an asthmatic child does not demonstrate significant spirometry bronchodilator reversibility (increase in forced expiratory volume in 1 s (FEV1) by C 12%), especially if baseline pre-bronchodilator lung function test is normal [10] . The gathering of supportive evidence for asthma (e.g., response to previous inhaled corticosteroids (ICS) therapy, self-reported bronchodilator response and atopic status) over time may increase diagnostic confidence.

Of particular interest in adolescents, patients who report breathlessness and noisy breathing during rest or exercise may have inducible laryngeal obstruction (ILO) [11] . ILO that occurs during exercise can be due to exercise-induced laryngeal obstruction (EILO) [12] . This oft-under-recognized entity presents with inspiratory stridor, throat tightness, maximal breathlessness during exertion and resolution upon rest [13] , or changes in voice post-exercise [14] . EILO often affects elite athletes between 11 and 18 years old, especially those with underlying anxious personalities [15, 16] . Diagnosing EILO involves continuous fiber-optic laryngoscopy [17] . Few are accustomed or willing to tolerate this. EILO is often confused with exercise-induced bronchospasm (EIB), which requires a fall in FEV1 C 10% and [ 200 ml from baseline during an exercise challenge test [18] . These two conditions rarely co-exist [19] and have distinct clinical features [20] ( Table 2) .

Discrepancy can exist between perceived severity of symptoms and clinical assessments. Occasionally, reported ''severe'' symptoms are attributed to psycho-somatic manifestations in adolescents when objective assessments for asthma diagnosis are non-corroborative and response to treatment inconsistent [21] . The interplay between chronic disease and psychosocial functioning [22] must be discussed with the family and recognized as a potential contributor to erroneous symptom attribution or hyper-vigilance to asthma-related emotional cues of stress and anxiety [23] .

Conversely, under-recognition of asthma severity occurs more commonly in adolescents. Some adolescents normalize and accept their chronic asthma symptoms over time, while others adopt coping strategies (e.g., minimizing physical activity). Some under-report asthma symptoms or reliever medication use to avoid escalation of their controller therapy. As such, reversible airway obstruction and airway inflammation are often demonstrated on objective tests even when the patient reports no symptoms. The asthma control review should be done in a non-judgmental manner, involving a mix of open-ended questions and specific clarifications. Where available, the addition of regular lung function tests adds objectivity to the assessment of asthma control and severity (Table 3) .

Adolescents prescribed daily ICS are often non-concordant [24] . The need for different inhaler devices for both controller and reliever therapies adds to this problem. A major change in the Global Initiative for Asthma (GINA) [25] 2019 guidelines paved the way for adolescents with mild asthma to choose between daily low dose ICS or as-needed symptom-driven use of ICS combined with long-acting beta-agonist (LABA) in the form of budesonide-formoterol Symbicort Ò dry powder inhaler (DPI). This change was supported by the results of the 'SYmbicort Given as needed in Mild Asthma' (SYGMA-2) trial [26, 27] , which showed non-inferiority of budesonide-formoterol DPI as a reliever for the rate of annualized severe asthma exacerbations in patients C 12 years, compared to maintenance low-dose budesonide with asrequired short-acting beta-agonists (SABA). Asneeded treatment with budesonide-formoterol was shown to prevent exacerbations and significantly reduced median daily ICS dose. The preceding SYGMA-1 [28] trial also showed that asneeded budesonide-formoterol combination was superior to as-needed terbutaline for asthma symptom control and prevention of exacerbations. This heralded a fundamental shift away from solely using as required SABA in mild asthma, a practice now deemed unsafe [29] .

Adolescents aged C 12 years with moderateto-severe persistent asthma require daily controller therapy. Following the evolution of guidelines up to GINA 2021, there are currently two treatment tracks to choose from: budesonide-formoterol prescribed in a single inhaler for use in both 'Maintenance And Reliever Therapy' (MART), or higher-dose ICS-LABA as controller and SABA for reliever [30] . An asthma action plan based on MART that escalates treatment using the same controller inhaler based on self-recognition of symptoms is welcomed from a patient perspective [31] . MART reduces exacerbation risk that continues to exist even in the mildest of asthma phenotypes, simplifying treatment regimens and reducing acute care visits [32] .

Asthma may seem ''difficult to treat'' due to modifiable factors of poor adherence, smoke exposure, co-morbidities, or incorrect diagnosis (Table 1) . Table 4 lists predisposing factors for poor asthma control, protective factors [33] and helpful strategies across the adolescent trajectory in the three developmental stages of early, middle, and late adolescence [34] [35] [36] [37] [38] [39] [40] [41] [42] [43] [44] [45] [46] [47] .

The advent of biologics over the past decade has provided an alternative treatment option to steroid-dependent uncontrolled asthmatics [48] . The first widely used agent, omalizumab, initially targeted at children C 12 years, is currently approved for use in children C 6 years old. It is indicated as add-on therapy in severe asthmatics with elevated immunoglobulin-E (IgE) levels, inadequately controlled on ICS, with aeroallergen sensitization [49] . Omalizumab is a humanized monoclonal antibody that binds selectively to IgE and involves 2-4 weekly subcutaneous administration. It has been demonstrated to improve asthma symptom control, reduce exacerbations, and minimize the need for systemic corticosteroids [50] . A course of omalizumab is long drawn and its efficacy on asthma control after cessation has been evidenced to span at least 4 years in 60% of adult patients who voluntarily discontinued omalizumab after 6 years of therapy [51] . However, this finding has yet to be substantiated in pediatric studies. In view of its substantial cost and sporadic adverse effects that include risks of anaphylaxis and malignancy, initiation of omalizumab for severe asthmatics requires careful consideration under specialist review. A review of such biologics therapy is recommended if the patient is deemed clinically unresponsive after 16 weeks [52] . Omalizumab has nevertheless been proven to be safe and well tolerated in children [53] , even with treatment duration beyond 2 years [54] . Mepolizumab (targets interleukin-5) and dupilumab (antibody to interleukin-4) were more recently approved for children with refractory eosinophilic asthma [55] .

Adolescents with asthma who remain uncontrolled despite treatment concordance and mitigation of risk factors or worsen upon reduction of high-dose treatment are termed ''severe'' [56] . Recognizing biological, psychological, and social risk factors can help formulate a risk assessment profile in the process of delivering individualized care (Table 5) . Night awakening with symptoms -?

Female disposition ? -EIB Exercise-induced bronchospasm, GERD Gastro-esophageal reflux disease

Biological factors associated with greater risk of cardio-respiratory morbidity and mortality include poor lung function with severely impaired airflow obstruction, commonly taken as FEV1 \ 60% predicted [57, 58] . Predisposition towards impaired lung function in adulthood includes past admissions to intensive care for asthma [59] , over-usage of reliever medications, increased airway variability, and low baseline FEV1 [60] . In a Swedish birth cohort study analyzing body mass index (BMI) development throughout childhood in relation to the timing of asthma onset and remission, the persistence of asthma from childhood up to 18 years of age was temporally associated with high BMI amongst females, whereas girls without asthma had the lowest BMI throughout most of their childhood. This indicates that there are overlapping risk factors for being overweight and asthmatic, starting even from infancy [61] . Weight loss interventions such as diet and exercise improve asthma-related quality of life and control in studies conducted across obese pediatric and adult groups [62] and such measures should be openly discussed from an early age. Other factors such as increased blood eosinophilia at asthma diagnosis favorably predicted resolution of severe asthma during adolescence [63] .

Psychological factors and mental health play a big role in asthma outcomes. The prevalence of psychiatric comorbidities (e.g., depression and anxiety) is higher in adolescents with asthma; and quality of life and asthma control tend to be poorer when psychiatric disorders and asthma co-exist [64] . Vulnerability of the immune system related to psychological disorders can also lead to greater exacerbation risks [65] . Psychosocial stressors (e.g., poverty, violence, racism, and discrimination) adversely impact an adolescent's asthma control. Stress exerts direct effects via a pro-inflammatory physiological state, while indirect mechanisms are attributed to risky behaviors involving sex, cigarette smoking, alcohol, substance use, and poor dietary choices [66] .

Social factors, such as disorganized home environments, worsen asthma control [67] . Initiating timely support during periods of family chaos or breakdown in peer relationships [68] can steer the maladjusted adolescent away from harm. Exposure to household tobacco smoke and peer smokers influence the initiation and maintenance of smoking in adolescents with asthma [69] , who model after their closest contacts.

Individuals who smoke have a higher risk of developing asthma symptoms [70] , have poorer lung function [71] , and asthma flare-ups [72] . In a Brazilian study involving over 66,000 adolescents, smoke exposure amongst adolescents remains high with rates of 12-28% [73] . E-cigarette use amongst high-school teens in the United States reached 19.7% in 2020, with the majority sourcing vaping products from friends [74] . Morbidity attributed to e-cigarette or Notably, despite the majority having no significant past medical history other than asthma, 53% of patients required intensive care for respiratory failure [76] . Worrisome data from this cluster outbreak called for abstinence from e-cigarette use and greater awareness of its harms to avoid a rising national epidemic, resulting in a decline of cases in the United States, after peaking in September 2019 [77] . Comparatively, smoking-cessation measures are not as well studied in adolescents compared to adults [78] . Adolescents are a notoriously challenging group to enroll into formal smoking-cessation programs and have high dropout rates [79] . In a systematic review conducted involving 41 studies that recruited young people under 20 years, investigators found that beyond group-based counselling programs, other behavioral-support measures or smoking-cessation pharmacotherapeutics in young people have yet to show longterm efficacy [80] . This calls for more well-designed and adequately powered studies to advance adolescent smoking-cessation treatment programs. Nevertheless, environmental smoke exposure in a home setting is a modifiable risk factor for asthma in adolescents [81] . Smoking-cessation techniques employing motivational interviewing and cognitive behavioral techniques [82] are potentially useful if adapted to an adolescent's level of understanding. Adolescents are likely more susceptible than chronically smoking adults to experience rapid onset of nicotine dependence, occurring within 1 month of initiation [83] . This makes the process of quitting even more challenging. Nicotine dependence is best quantified by time to first cigarette upon waking and number of cigarettes smoked per day as part of the Fagerström test [84] . The 5As (Ask, Advise, Assess, Assist, Arrange) of smoking-cessation counselling are effective in smoking prevention and abstinence when modified for adolescents [85] .

Financial incentives with free cessation aids were proven to be more efficacious than usage of cessation aids alone, in employees up to 1-year post enrolment into smoking-cessation programs [86] . Incentivizing smoking cessation with vouchers rides on the developing adolescent brain's heightened response to rewardseeking [87] , outweighing the thrills sought from smoking.

Transitioning from child-centric to adult-oriented care requires planning and coordination [88] . Successful established pathways such as 'Ready Steady Go' initiated within the National Health Service, United Kingdom [89] , begins this staged process from age 11 years old, with generic patient and parent questionnaires applicable across all specialties [90] . Caregivers' and patients' disease knowledge and attitudes must first be addressed, followed by empowering the young person with self-help skills, all of which requires multidisciplinary healthcare support [91] . Best practices for transitional health care include appropriate parental involvement and promotion of the adolescents' self-efficacy in managing their health [92] . Adopting a flexible approach in the culmination to adult-oriented care from 16 to 19 years old onwards takes into consideration their transition readiness, school-leaving plans, and varied levels of self-efficacy [93] . Reaching this milestone in care should not be reliant on chronological age alone or orchestrated out of physician frustration towards an adolescent with difficult to control asthma [94] . An oppositional adolescent allowed to ''drop out'' of the healthcare system faces missed opportunities in addressing risks for severe exacerbations [95] . Generally, asthmatic adolescents who do not require daily medications can be transited to primary healthcare whilst some may require a specialist referral for shared care [96] . Those requiring daily medications with greater disease burden and family vulnerabilities can be transited to the adult respiratory specialist equipped with multi-disciplinary resources such as a specialist nurse practitioner trained in adolescent care to facilitate the process [97] . During this challenging pandemic, telemedicine has become integral to asthma care to allow continued engagement and adherence to outpatient appointments [98] . Furthermore, joint video consultations [99] with pediatric and adult medical practitioners can help orientate the patient amidst movement restrictions across institutions. However, for families unfamiliar with telemedicine, the option to switch to faceto-face visits should always still be made available to them. Care should be taken to avoid loading already-burdened families of chronic disease patients with the stress of partaking in technology that may remain inaccessible to them [100] .

The management of adolescent asthma should be supported by population, community-and school-based strategies in tandem with the efforts of healthcare providers (Fig. 1) . Marketing efforts by tobacco-sponsored industry increase the youth's susceptibility to smoking [101] . Raising the minimum legal age for sale of tobacco and e-cigarette products from 18 to 21 years [102] and launching youth e-cigarette prevention campaigns [103] are helpful counter-marketing measures [104] . School-based [105] and peer-led programs [106] have provided beneficial support for adolescents with asthma. Self-perceived under-performance in school and lack of participation in physical activities are more likely in asthmatics than in others [107] . As the burden of chronic disease competes with academic attainment, schools and healthcare teams must link up [108] , aiming to minimize school absenteeism attributed to appointments and flare-ups. Whilst asthma health technology [109] is eagerly embraced by adolescents, more evidence is required in proving that applications [110] for medication adherence, disease monitoring, and health literacy are effective. Human-computer interactions for inhaler technique competency, peak flow monitoring, and medication reminders are promising and complement current practices [111, 112] but require further patient engagement to fulfil unmet needs [113] .

A rewarding experience awaits as we journey with adolescents from asthma diagnosis to adult transition. Continued engagement with schools and communities can provide a safer springboard for individuals leaving childhood into adolescence, as they transition towards better asthma outcomes in adulthood. Authorship. All named authors meet the International Committee of Medical Journal Editors (ICMJE) criteria for authorship for this article, take responsibility for the integrity of the work as a whole, and have given their approval for this version to be published.

Author Contributions. Zai Ru Cheng: conceptualization, writing-original draft, visualization, project administration. Yi Hua Tan: writing-review and editing, supervision. Oon Hoe Teoh: writing-review and editing, supervision. Jan Hau Lee: writing-review and editing, supervision, resources, project administration.

Disclosures. Zai Ru Cheng, Yi Hua Tan, Oon Hoe Teoh, and Jan Hau Lee have nothing to disclose.

Compliance with Ethics Guidelines. This article is based on reviews of current guidelines and literature and did not involve any new studies with human participants or animals performed by any of the authors.

Commons Attribution-Non-Commercial 4.0 International License, which permits any non-commercial use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the articleöûûs Creative Commons licence, unless indicated otherwise in a credit line to the material. If Fig. 1 Levels of care in holistic asthma management for adolescents. Levels of asthma care range from large-scale population-based strategies to smaller-scale school and healthcare providers' efforts, followed by specific familyand peer-support measures material is not included in the articleöûûs Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc/4. 0/. 23 

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