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Management of difficult-to-treat asthma in adolescence and young adults

Adel H. Mansur, Nagakumar Prasad
Breathe 2023 19: 220025; DOI: 10.1183/20734735.0025-2022
Adel H. Mansur
1Department of Respiratory Medicine, Heartlands Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK
3Institute of Inflammation and Ageing, University of Birmingham, Birmingham, UK
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  • For correspondence: Adel.Mansur@uhb.nhs.uk
Nagakumar Prasad
2Department of Respiratory medicine, Birmingham Women and Children's Hospital NHS Trust, , Birmingham, UK
3Institute of Inflammation and Ageing, University of Birmingham, Birmingham, UK
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Abstract

The period of adolescence and young adulthood (AYA) has been proposed to extend from 11 to 25 years of age as patients in this age group face similar challenges. AYA is a time of fast and great physiological and psychological growth, in which an individual transitions from a young dependent child to a mature independent adult. Behaviour patterns during adolescence, such as risk taking and desire for privacy, can challenge parents or healthcare professionals' (HCPs') ability to help adolescents to manage their asthma.

Asthma itself tends to remit, become milder or worsen into a severe variant during adolescence. The pre-pubertal male predominance of asthma switches to a female predominance in late teen years. ∼10% of AYA with asthma have “difficult-to-treat asthma (DTA)”, characterised by poor asthma control despite treatment with inhaled corticosteroids (ICS) and other controller medications. DTA management in AYA requires a multidisciplinary team approach and systematic assessment that can address the key questions of objective confirmation of diagnosis, severity assessment, phenotyping, comorbidities, asthma mimickers or other drivers of poor control such as non-adherence to treatment.

A key task for HCPs is to establish the magnitude of the severe asthma component versus other non-asthma drivers of symptoms (e.g. inducible laryngeal obstruction or breathing pattern disorder). Severe asthma is a subset of DTA and is determined once asthma diagnosis and its severity have been confirmed and adherence to controller (ICS) treatment has been assured. Severe asthma is a heterogeneous disease and appropriate phenotyping is necessary for the management of treatable traits and consideration for biologic therapies.

Finally, an important part of successful management of DTA in the AYA group is the provision of an effective transition of asthma care from paediatric to adult asthma services through setting up a well-designed asthma transition pathway tailored to the individual patient needs.

Abstract

Managing a heterogeneous and chronic disease like asthma in young people can be challenging. Early multidisciplinary management and effective transition of young people with difficult-to-treat asthma from paediatric to adult services is important. https://bit.ly/3h67VgS

Educational aims

  • To understand the challenges and complexity of managing young people with difficult-to-treat asthma.

  • To outline the systematic approach for management of young people with difficult-to-treat asthma.

  • To discuss the importance of a robust transition programme for safe and effective care of young people in adult asthma services.

Definitions

The Global Initiative for Asthma (GINA) [1] defines uncontrolled asthma as the presence of poor symptom control and/or asthma exacerbations leading to use of oral corticosteroids (OCS) twice or more per year or one or more hospital admissions per year for severe asthma attacks. Difficult-to-treat asthma (DTA) represents ∼17% of all asthmatic patients [2], who have uncontrolled asthma despite treatment with medium-to-high dose inhaled corticosteroids (ICS) in combination with a second controller (in keeping with treatment at steps 4–5 of the GINA guidelines). Multiple modifiable factors often drive poor control in DTA patients, which include wrong diagnosis (treating the wrong disease), presence of asthma mimickers, comorbidities, and suboptimal treatment or non-adherence to ICS treatment. Severe asthma, which affects <5% of all asthmatic patients [3, 4], is a subset of uncontrolled asthma in which asthma remains poorly controlled despite management of modifiable factors or becomes uncontrolled after a step down of treatment to below step 4 of the GINA guidelines (figure 1) [1].

FIGURE 1
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FIGURE 1

Asthma severity model. Uncontrolled asthma is often due to a lack of baseline treatment, but a minority will continue to have poor control despite treatment at steps 4–5 of the GINA guidelines and are labelled as difficult-to-treat asthma (DTA). A subset of DTA have severe asthma.

Natural history of asthma in adolescence and young adulthood

During adolescence, a child goes through significant physiological and psychological changes that impact on asthma prevalence, control and severity. The adolescence and young adulthood (AYA) age group (age 11–25 years) share similar challenges and require a similar health approach to manage chronic diseases such as bronchial asthma.

Asthma in adolescence is common and has been reported to afflict up to one in 7–12 people [5]. Risk of asthma morbidity including mortality in AYA is high. A review of asthma deaths in Australia demonstrated an increase in deaths in children up to the age of 17 years. Low socioeconomic status, poor follow-up care, poor adherence, lack of a personalised asthma action plan and tobacco smoking were identified to increase the risk of asthma deaths in this population [6]. However, in Finland the implementation of an integrated asthma programme improved asthma outcomes and reduced morbidity and mortality across all age groups including AYA [7], demonstrating that asthma outcomes can be improved if the correct approach is used.

Asthma can remit, or change to a mild or severe form during adolescence. Causes of remission or worsening of asthma in adolescence are not fully established. Reported predictors of asthma remission in adolescence include pre-pubertal mild disease, minor airway inflammation, absence of allergic sensitisation and male gender. Conversely, heredity, expression of high type 2 inflammation such as blood eosinophils, atopy, low lung function, smoking and pre-pubertal presence of severe asthma were all reported to predict asthma persistence and severity [8, 9]. Causes of the post-pubertal switch of asthma from male to female predominance are not known. Females are also more susceptible to develop severe asthma in their later teens. Genetics, sex hormones, pregnancy, immune responses and mechanical factors, such as airway size and lung growth, were all proposed to relate to the gender disparity of asthma prevalence in AYA [10]. In addition, obesity, environmental pollution and tobacco smoke exposure were reported to reduce responsiveness to ICS and accelerate loss of lung function and asthma severity [11].

Severe asthma is probably less common in children than adults, with a reported prevalence of 5% of all asthma at the age of 10 years [5, 12]. Despite this it disproportionately accounts for 60% of all asthma-related health cost, which is attributed to the disease and costs related to side-effects from excessive corticosteroids exposure [13].

Psychological factors and asthma in AYA

During adolescence, the growing child will be seeking independence and builds relationship with their friends and peers whilst aiming to keep harmony with their family. Adolescents prefer learning from direct experience, respond to rewards, and are probably more tolerant to ambiguity and to adopting risk-taking behaviour [14]. Key life drivers during the adolescence include academic and sporting performance and forming relationships, which all can increase risk of stress, anxiety, depression, or other mental health issues [15]. Marijuana, alcohol and other illicit drug use can also confound mental health during AYA. Teenagers may deny illness leading to under diagnosis and treatment, or overexpress symptoms leading to over diagnosis and treatment. In the latter group, patient symptoms will be discordant to objective measures of asthma such as lung function. The potential detrimental impact of social media on young people's mental health has been well described [16].

Diagnostic algorithm for DTA in AYA

Asthma in adolescence is both under- and over-diagnosed and is associated with erratic adherence and poor self-management [17, 18]. The complexity of factors driving DTA in AYA warrants the adoption of a systematic approach for its assessment and management. This will be comprised of obtaining a focused and detailed history, physical examination and conduction of investigations for objective asthma diagnosis confirmation, as well as identification of triggers and co-morbidities and establishing drivers of poor control such as treatment non-adherence.

Systematic assessment of DTA in AYA

Structured history and examination

A focused and structured history followed by physical examination is vital for the assessment of DTA. The use of a purposely designed proforma can improve the efficiency of clinic review. Predesigned assessment proforma (table 1) could be completed electronically or on paper by the patient/parent prior to a clinic visit and made available to the healthcare professional (HCP) to form the basis of the clinic consultation.

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TABLE 1

Focused history and examination of a young person with difficult asthma

Investigations

A stepwise investigations algorithm is needed to conduct the series of tests required to objectively assess asthma diagnosis, determine phenotype, severity, control and quality of life (table 2).

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TABLE 2

Investigations to be considered in a young person with difficult-to-treat asthma

The high prevalence of non-adherence to treatment in DTA (∼40–50%) mandates objective measurement of adherence [19, 20]. Reliance on patient accounts or HCPs impression were shown to be inaccurate [21], thus prompting the need for objective measures of adherence. Available tools to measure adherence include counting of prescription pick-up rate or prescription possession ratio, and use of dose counting chips attached to inhaler devices [22]. The presence of a high fraction of exhaled nitric oxide (FENO) despite treatment with high-dose ICS is often seen as a marker of non-adherence, which prompted the development of the FENO suppression test that measures the magnitude of FENO suppression following direct or virtual observation of ICS dosing (figure 2) [23]. Adherence to maintenance oral prednisolone/prednisone can be measured using a validated liquid chromatography–tandem mass spectrometry assay that can simultaneously measure prednisolone and cortisol. Adherent patients are expected to have detectable prednisolone and suppressed cortisol levels using spot testing [24]. AYA attitudes towards treatment adherence can also be evaluated using validated questionnaires which could facilitate initiation of a discussion to improve adherence [25].

FIGURE 2
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FIGURE 2

Methods of assessing adherence to asthma therapies in routine clinical practice. ICS: inhaled corticosteroids; MPR: medication possession ratio; FENO: fraction exhaled nitric oxide; ACQ: asthma control questionnaire.

Diagnostic outcomes and design of a management plan

The systematic assessment will lead to a series of outcomes related to asthma diagnosis confirmation, asthma control, severity, phenotyping, comorbidities and asthma mimickers. Particular consideration should be made to conditions that tend to be common in the AYA age group, such as anxiety, depression, exercise-induced dyspnoea (EID), breathing pattern disorders and hyperventilation syndromes, inducible laryngeal obstruction (ILO), underlying cardiac disease, congenital malformation and psychogenic cough [26]. Often talking to young people on their own may help the team in understanding their overall health needs. Multidisciplinary team discussion and an action plan will then need to be formulated to prioritise required steps of management and produce short- and long-term goals. Most AYA asthma patients should lead a normal life including fulfilling their academic and vocational aspirations whilst achieving good asthma control, which often means getting the basics right rather than reliance on expensive treatments. Unsuccessful DTA treatment in AYA is often due to failed medical care rather than due to patient-related factors.

Asthma treatment

Treatment of asthma in AYA would follow local, national and global guidelines, such as GINA [1]. Asthma guidelines are based on a step-wise treatment approach commencing from use of low-dose ICS and stepping up as guided by asthma control and exacerbation risk to add other controller treatments of leukotriene receptor antagonists, long-acting β2-agonists (LABA), long-acting antimuscarinic agonists (LAMA) or theophylline. AYA asthma patients are prone to excessive reliance on short-acting β2-agonist (SABA) relievers with consequent increased risk of poor control, exacerbation and mortality [27].

Patients with severe asthma require treatment at steps 4–5 of the GINA guidelines comprised of a moderate-to-high dose of ICS and other controllers and intermittent or regular use of OCS. Several effective biologic treatment options have become available for severe asthma. Frequent or regular OCS use should therefore become a treatment of last resort that should only be initiated under the guidance and monitoring of specialist centres. Prior to treatment step up, inhaler technique and adherence should be assessed and managed as described above. Table 3 presents potential barriers to adherence that are frequently encountered in AYA and proposed facilitators that can enhance and improve adherence.

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TABLE 3

Potential barriers to and proposed facilitators of adherence in adolescence and young adulthood

Self-management

Self-management comprises gaining the knowledge and skills that allow AYA patients with asthma to develop into autonomous experts who can manage their asthma throughout their adult life to reach better health outcomes [28]. Self-management reduces dependency on HCPs, parents and carers.

Enabling AYA patients to self-manage their asthma should start in the early phase of the transition period. Adolescents vary markedly during their teens in their ability and maturation, including literacy skills [29]. These factors need to be considered during the development of a self-management plan. Core items of self-management plans should include asthma education, asthma natural history, triggers, exacerbation risk, how treatment works, what good control looks like, and how to achieve and maintain it. A well-constructed self-management plan should enable AYA patients to assess their asthma control, reduce reliance on SABA use, measure peak expiratory flow rate and design treatment step up/down as required. A self-management plan should include attaining specific development goals and focus on areas where the AYA patient is not confident (e.g. a goal to reduce severe exacerbations to zero, or reduce use of SABA to <3 times per week, improve adherence to ICS to >80% of the time, develop an understanding of why preventer treatment is necessary).

Virtual mobile/web-based self-management has been increasingly used and is likely to become the main way of applying self-management in this era of smartphone applications [29]. Peer-led interventions may prove useful in assisting AYA patients to self-manage. The developed personalised asthma management plan should include input from family, school, teachers, co-workers and managers, and facilitate shared decision making. Motivational interviewing skills of active listening, empathy, a non- judgmental approach, gaining the AYA patient's confidence and maintaining medical privacy can all aid the HCP to assist AYA patients to set their goals, change behaviour and enable self-management [30, 31].

Severe asthma treatable traits

Effective self-management and adherence leads to significant improvement in asthma and reduces the need to escalate treatment to OCS or biologics. However, a minority of patients will continue to have uncontrolled asthma despite treatment optimisation at GINA steps 4–5 (severe asthma) [4]. Severe asthma is a heterogeneous disease that requires systematic phenotyping to allow identification of treatable traits where treatment can be tailored. The treatable trait concept describes a clinical entity that responds well to specific treatment (figure 3).

FIGURE 3
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FIGURE 3

Treatable traits of severe asthma. Treatable traits relate to all asthma and are not necessarily specific to the AYA group of asthma patients. #: one or more phenotypes can exist in the same individual, concept of “the dominant phenotype”. T2: type 2; IL-5: interleukin 5; anti-IL-5R: anti-interleukin 5 receptor; anti-IL-4R: anti-interleukin 4 receptor; anti-TSLP: anti-thymic stromal lymphopoietin; SAFS: severe asthma with fungal sensitisation; ABPA: allergic bronchopulmonary aspergillosis.

In the clinic, these phenotypes are not mutually exclusive, with patients often presenting with multiple traits (e.g. allergic, eosinophilic and infective traits presenting in the same patient). Therefore, the clinician's task is to apply a tailored treatment approached prioritising the strongest or most dominant phenotype likely to drive the disease, but also would consider treating factors that can undermine treatment response such as the co-presence of an infective phenotype prior to commencing biologic treatment. A management strategy should therefore be formulated to include staged treatment trials, review and assessment of response, and continuation of treatment long-term in the event of a satisfactory response or discontinuation and consideration for treatment switch in the event of a negative treatment trial outcome.

Organisation and delivery care transition from children to adult services

Transition of asthma care from children's to adult services is a process of empowering the growing child to become an independent, competent and expert adult patient (figure 4). Starting from 11 to 13 years of age, transition should be individualised depending on mental and physical development, disease activity and health literacy. Questionnaire-based tools have been developed to aid in assessing and preparing the adolescent for transition (e.g. transition readiness assessment tool; Ready Steady GO [40, 41].

FIGURE 4
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FIGURE 4

Example of a model of transition for adolescents and young adults with asthma from paediatric to adult services that specifies the key measures to activate transition, the overlap period and the ultimate transition goals to be achieved during adulthood. AYA: adolescent and young adult; MDT: multidisciplinary team.

Transition should be AYA patient-centred and include progress tracking, identification of key areas of knowledge that need development and should culminate in production of a transition report for the adult asthma service which should also link with the AYA primary care team. A transition report should cover areas of past medical history, concurrent treatment, comorbidities, emergency management plans and other AYA-related factors such as schooling and work and psychological wellbeing (figure 4).

A well-designed transition service requires the close working of paediatric and adult severe asthma team members through regular, joint multidisciplinary team (MDT) meetings, use of shared protocols and assessment tools, effective communication to ensure that all involved in AYA care say the same thing, and include family to support AYA independence and self-management. The example of a transition model we follow in Birmingham, UK is described in figure 5.

FIGURE 5
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FIGURE 5

Severe asthma transition from paediatric to adult services pathway followed in Birmingham, UK. Using key transition triggers, patients are identified and assessed by the paediatric difficult asthma MDT and discussed at the adult MDT of the Birmingham Regional Severe Asthma Service (BRSAS). Patients with specific needs, such as biologic treatment, and those requiring specialised MDT input transition to the hub site in BRSAS, while others with no specific concerns transition to local spokes within the network. BCH: Birmingham Children's Hospital; MDT: multidisciplinary team; BHH: Birmingham Heartlands Hospital “hub”; DGH: district general hospital.

The transition programme was developed following discussions between the paediatric and the adult MDT teams. The key elements of the pathway are the involvement of the respiratory nurses and a youth worker in preparing the young person for asthma care in the adult centre in line with their wishes. The pathway also provides equal emphasis on safe and effective transition of young people with significant comorbidities for continued MDT input and not just those on biologics.

The young person undergoes a transition-focused annual asthma assessment at 15 years of age. The asthma control, medications, comorbidities and investigations, like bone density scan or chest computed tomography, are reviewed. The paediatric severe asthma team attend the first appointment at the adult centre with the young person and the family following which the young person is formally discharged from paediatric services.

The process is reviewed regularly based on the feedback from the young person and the family. The establishment of a paediatric severe asthma MDT for effective management of comorbidities and the availability of new biologics have improved the care of young people. The unpublished data from our centre shows that of the 13 young people transitioned between 2019 and 2021, at a median age of 16.5 years, 11 (85%) were on biologics compared with eight out of 17 (47%) transitioned between 2016 and 2018. Moreover, the joint adult and paediatric work has resulted in a significant reduction in young people transitioned on maintenance OCS: 11 out of 17 (65%) to two out of 13 (15%) during the same time periods.

Conclusions

The management of DTA in adolescents and young adults is challenging but rewarding at the same time. Setting-up the correct service structure equipped with trained HCPs is essential to achieving successful outcomes for DTA management in AYA. Services should be patient centred with the ethos of forming healthy empowering and empathic relationships with the AYA patient to allow her/him to develop into a mature independent adult possessing lifelong knowledge and skills to self-manage their asthma and reduce dependency on family, carers and HCPs. Given the correct approach most AYA asthma patients should expect to lead a normal life, achieve best asthma outcomes, and reduce reliance on excessive use of SABA and OCS with its consequent serious side-effects. This article presents what would be considered an optimised model of care delivery that can be adapted for local use. Good asthma control is not necessarily the result of using the newest medicine, but about getting the best outcome with appropriate management.

Key points

  • Assessment and management of asthma severity and comorbidities in young people is key to improve disease control and quality of life.

  • A robust transition programme is required for supporting young people's asthma management.

Self-assessment questions

  1. What is the difference between difficult asthma and severe asthma?

  2. List any four treatable traits in severe asthma.

  3. What are the known predictors of asthma remission in young adults?

  4. Only children with severe asthma should be transitioned to the specialist adult severe asthma services. Is this statement true or false?

Suggested answers

  1. Difficult asthma is an umbrella term referring to patients with uncontrolled asthma despite being prescribed appropriate medications. Correction of modifiable factors usually improves asthma control. Severe asthma is a subset of difficult asthma where the disease remains uncontrolled despite optimisation of care.

  2. Infection, fungal sensitisation, type 2 (T2) high inflammation, allergic and eosinophilic asthma.

  3. Pre-pubertal mild disease, minor airway inflammation, absence of allergic sensitisation and male gender.

  4. False. Any young person with uncontrolled asthma should be transitioned to a specialist centre for multidisciplinary assessment of disease severity, management of comorbidities and access to specialist services like physiotherapy.

Footnotes

  • Conflict of interest: A.H. Mansur has nothing to disclose. P. Nagakumar has nothing to disclose.

  • Received February 27, 2022.
  • Accepted November 29, 2022.
  • Copyright ©ERS 2023
http://creativecommons.org/licenses/by-nc/4.0/

Breathe articles are open access and distributed under the terms of the Creative Commons Attribution Non-Commercial Licence 4.0.

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Management of difficult-to-treat asthma in adolescence and young adults
Adel H. Mansur, Nagakumar Prasad
Breathe Mar 2023, 19 (1) 220025; DOI: 10.1183/20734735.0025-2022

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Management of difficult-to-treat asthma in adolescence and young adults
Adel H. Mansur, Nagakumar Prasad
Breathe Mar 2023, 19 (1) 220025; DOI: 10.1183/20734735.0025-2022
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  • Article
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