Introduction

The prevalence of non-communicable chronic disorders including asthma and chronic obstructive pulmonary disease (COPD) is progressively increasing at all ages, with a significant impact on morbidity and mortality [1]. Approximately 10% of school-age children have asthma and some continue to have symptoms also later in the teenage years or adulthood [2]. Therefore, thanks to the improvement in asthma care and the availability of new effective medications, a relatively novel population of adolescents and young adults (AYA) with asthma, even those with the uncontrolled symptoms of severe asthma (SA), is growing significantly [3].

Transition is an active process that incorporates several changes from one stage of life, or physical or mental conditions, which can significantly affect the normal life of an individual [4]. In chronic diseases, transition involves an adjustment period to the new needs of the patients, which include the development of self-management skills and an increasing responsibility for their medical care [5]. Currently, both pediatric and adult pulmonologists and allergists are called upon to address the issues associated with a difficult moment in the lives of patients moving from child- to adult-centered asthma care, and this can largely influence the future course of the disease [6].

In this manuscript, we have critically examined retrospectively a small series of patients with SA who transitioned from our pediatric to adult asthma care. Our aims were to highlight the difficulties encountered in the transition process and to optimize the care for patients with high morbidity as occurs in SA.

At the Azienda Ospedaliera Universitaria Federico II, Naples, Italy, two specialized services providing separately care to children (Department of Mother and Child, Pediatric Pulmonology and Asthma center) and adults (Department of Medicine and Clinical Complexities, Allergy and Clinical Immunology) with asthma, respectively, have been instituted since 1993. In both units, the follow-up with visits scheduled at intervals of 3 to 6 months (based on the patients’ needs) includes spirometry, airways inflammation measurement by fractional exhaled nitric oxide (FeNO), laboratory analysis (for evaluating atopy), and hospital admission for drug administration and/or treatment of medical/surgical complications. Local treatment protocols generally derive from major updated pediatric and adult asthma guidelines or published documents [7]. In the last 5 years, pediatric and adult specialists have jointly organized the transition from the Pediatric to the Adult Asthma Centers. First, the transition program includes an outpatient visit a few months before the patient’s 18th birthday in the presence of both pediatric and adult specialists, as well as both parents or just one.

We herein report retrospectively about 4 transitioned patients with SA. For each patient, we described the clinical manifestations of SA, treatment at referral to the Pediatric Asthma unit and the course of the disease, which included the main laboratory findings at referral and one year after the addition of biologics. Similarly, we reported the characteristics of the same patients at transition to the Adult Asthma (division of internal medicine and clinical immunology) Center and during the follow-up. All patients provided written informed consent for the publication of their anonymized clinical and laboratory data.

Case report

The charts of 4 adolescents (2 males, 2 females) with SA, followed first at the Pediatric and then at the Adult Asthma Center were reviewed. They were all living in Campania (Southern Italy). We herein briefly describe the individual clinical course of the patients.

Discussion

It is well known that while most asthmatic children achieve optimal control with low-to-medium ICS, some have persistent difficult-to-treat asthma symptoms despite higher doses of ICS plus a second controller drug and/or OCS [8]. Once ruled out or modified some factors such as poor pulmonadherence, incorrect inhaler technique or comorbidities, children unable to achieve symptom control despite high doses of medications have likely developed SA [9]. A recent systematic review and meta-analysis of 9 studies from Europe indicated a 3% prevalence of SA in children and adolescents with asthma [10], yet the condition has an unacceptably high personal and economic burden because of frequent asthma attacks, continuous need for reliever and additional maintenance asthma medications, impaired lung function and poor quality of life (QoL) [11]. Pediatric SA prevalence has been most evaluated in studies investigating a mixed population of children and adolescents, while studies conducted exclusively in adolescents are lacking. Adolescents affected by chronic diseases are indeed under-studied, probably also because at this age there is a risk of misperception of one’s own health status, with over- or under-reporting symptoms. Teenagers with asthma, especially those with SA, face unique challenges. Due to their concerns about self-image, self-identity creation, and peer acceptance, they are at risk of behaviors resulting in poor adherence to relievers and maintenance treatment and/or refusal of scheduled visits, and this eventually compromises asthma control [12].

In the life of a teenager with SA, transition from the pediatric patients to adult-oriented care is a critical moment that can add further elements of complexity to the management of their asthma, especially SA [5]. The transition of SA teenagers requires specialized care tailored to their age-specific needs not only to guarantee the continuity of their care but also to face and address patients’ troubles [13]. On the other hand, developing a transition program including pediatric and adult asthma specialists can uncover the challenges of managing AYA with SA, which, once identified and addressed, help improve patients care and outcome.

Starting from these considerations, we retrospectively evaluated a small series of patients followed for a long time at a Pediatric Asthma Center, who transitioned to an Adult Asthma Center. The description of the cases highlights the most relevant aspects of transition of patients with a chronic disruptive disorder such as SA. Cases 1 and 4 from the series had asthma exacerbations during the transition follow-up period, likely due to patient-driven interruption of the biologic treatment. The lack of adherence to treatment during transition may be attributed to the complex psychological mechanisms occurring in adolescents [14, 15]. Probably, a prolonged period of absence of asthma exacerbations during the transition period and a long-lasting SA history from childhood to adolescence led patients to consider the possibility of clinical remission. The choice of interruption of the biologic was not shared by the adult specialist as criteria of complete clinical remission (need for OCS, symptoms, exacerbations or attacks, and pulmonary function stability) were not completely met [16, 17]. In fact, the disease inflammatory process was still present, and asthma exacerbations re-occurred. Thus, a phenotype-based reintroduction of biologic treatment took place. As both patients showed a Type 2 phenotype with elevated T2 biomarkers (IgE, FeNO and blood eosinophil count), dupilumab, which blocks signaling by interleukin-4 and interleukin-13, key and central drivers of Type 2 inflammation, was prescribed [18]. This choice led to better compliance due to self-administration with a pre-filled pen rather than the prefilled omalizumab syringe that requires monitoring by healthcare personnel during administration.

Similar to the pediatric setting, also in the adult outpatient clinic it is extremely important to guarantee to the young patients a careful follow-up, with tempestive and closely spaced schedule that offers the possibility of immediate therapeutic adjustments to reestablish clinical well-being. Notably, both female patients (cases 2 and 3) did not undergo significant changes of their therapeutic program, nor had asthma attacks or experienced significant clinical deterioration. All patients, despite of age, were accompanied by one or both parents. Case 2 was indeed fully independent from parental help and control, while case 3 still relied on her mother although she was convinced of the need to take care of her health on her own. Cases 1 and 4 reported being completely independent about treatment and have expressed willingness to implement future encounters independently. Our considerations were based on clinical observation, ability to discuss with the patient about pathology and treatment. Both male patients (cases 1 and 4) experienced exacerbations following an interruption of their biological therapy and appear still dependent on their parents for any needs related to the illness. Children typically attend pediatric clinics with their parents until they are teenagers or young adults, and parents take on the responsibility of managing the illness also to reduce the burden on their children. This can result, at least in some individuals, in less understanding of the illness and its management even once followed in the adult clinic [19]. Our observations are indeed based on a small case series report and a much larger number of transitioned patients with SA should be observed and monitored at our center to achieve definitive conclusion remarks. However, we observed a different gender approach of transition with males being less compliant and probably less independent than females. This needs more confirmation on larger study population.

In various personal interviews, all our patients have repeatedly requested the intervention of a psychologist addressing the critical aspects of the transition from the Pediatric to the Adult care. By providing support, the psychologist could also promote more effective communication among patients, families and specialists and prepare the patients for the new journey.

Although limited by small sample, this case series leads us to confirm that transitioning from child-centric to adult-oriented care is crucial for young adolescents with chronic inflammatory diseases such as SA [20]. It appears mandatory to schedule and program the transition from early adolescence (13–14 years) in accordance with the patient’s developmental stage, in consideration of the individual’s changes that can complicate the process if not adequately managed. In this context, risk factors such as smoking, drug abuse and emerging mental health problems should not be neglected. On the other hand, poor compliance related to adult independence status and therapy self-management may lead to uncontrolled disease and further reduced QoL. On the basis of what has just been said, it appears necessary for multidisciplinary approaches, integrating pulmonologists, allergists, psychologists, and social workers, to support both clinical and psychosocial transition challenges.

Pediatricians should inform the adolescent and the family about the upcoming transition in advance. The first scheduled visit would take place in the pediatric setting with both pediatric and adult specialists being present. During the first transition visit, the adult specialist will be introduced to the young patient and a detailed letter of the patient’s medical records including current diagnosis and treatment will be delivered. In this context, all our patients had the opportunity to meet the adult specialists in the pediatric clinic. They reported to be satisfied with the relationship established with their “new” doctors and the adult clinical setting.

Our study, which is a retrospective case series, is subject to several limitations, the main ones being the small sample size, which limits the generalizability of the findings, potential selection bias, the absence of a control group, and reliance on retrospective records, which may vary in accuracy and detail. Furthermore, we didn’t use standardized tests for assessing caregiver independence and self-management capacity. What is described is the result of our clinical evaluation and direct communication with the patient. However, this study may be useful for planning a national study that complements international research efforts on the transition of SA patients from pediatric to adult care as longitudinal studies that evaluate transition outcomes in larger populations of SA over extended periods of time.