Teaching children with food allergy to recognize anaphylaxis: The caregivers' perspectives

Anaphylaxis is rising in prevalence among children. The current recommendations on the effective transition of anaphylaxis management to adolescents and young adults suggest preparation for the transition may be considered at 11–13 years of age in accordance with the patient's developmental stage. However, there has been limited research conducted on the perspective of caregivers regarding the transition of anaphylaxis management to their children. This study aims to determine the age caregivers feel it is appropriate to begin to teach their child to recognize anaphylaxis and use their adrenaline auto‐injectors (AAI).


| INTRODUC TI ON
Anaphylaxis is a life-threatening, systemic allergic reaction associated with different mechanisms, triggers, clinical presentations, and severities. 1 Studies suggest increasing prevalence among children, with a higher likelihood of hospitalization among this cohort. 2 Optimal management of anaphylaxis involves avoiding known triggers, use of adrenaline auto-injectors (AAI) when necessary and devising a personalized anaphylaxis management plan. 3 In the case of pediatric patients, caregivers typically bear the responsibility of recognizing anaphylaxis symptoms, carrying, and administrating AAI to the child when required. 4 There are no published data on the optimal age to transfer responsibilities for recognition and treatment of anaphylaxis from caregiver to child. The European Academy of Allergy and Clinical Immunology (EAACI) recommends preparing children for the transition of anaphylaxis responsibility from early adolescence, that is 11-13 years. 5 General guidance in the education sector regarding students self-carrying and self-administrating prescribed medication does not provide precise age-based advice.
Children and adolescents are rarely included in studies that investigate the management of anaphylaxis. 6 There are concerns about the capability of children using the AAI correctly and safely such as applying the correct pressure when injecting or accidental self-harm due to unintentional injections from AAI devices. 7,8 As adolescents and young adults gain autonomy and their environment shifts from family to peer-based interactions, they may be at higher risk of anaphylaxis if they fail to take responsibility for selfmanagement of their condition. Fatal anaphylaxis is disproportionately more common among adolescents, possibly reflecting a failure to recognize symptoms and delayed use of AAI. 6,9,10 Two studies investigating caregiver and pediatric allergists' perspectives on this transition reported different findings. Caregivers of pediatric allergy patients expected their children to self-inject adrenaline by the age of 9-11, while pediatric allergists did not expect this autonomy until the age of 12-14. 11,12 This highlights the lack of consensus in this area by revealing that the expectations of clinicians do not correlate with the reality experienced by caregivers. Thus, with limited published data based on the standard age of transitioning these responsibilities onto the patient, this underpins the need for clear guidelines to address this critical knowledge gap. 13 The aim of this study was to determine the age caregivers begin to teach their children to recognize the symptoms of anaphylaxis and use an AAI. This study will also explore readiness factors that influence the caregivers' approach to transferring the responsibility of anaphylaxis management to their child, their confidence in training their children, and their views on who should support this transition.

| Study design and population
This was a quantitative descriptive cross-sectional study conducted between October 2020 and April 2022, conducted as part of a tele-

| Eligibility criteria
Caregivers were eligible to participate if they cared for patients who had been diagnosed with an IgE-mediated food allergy and were prescribed an AAI. A caregiver was excluded from participation if there were significant language barriers.
Caregivers attending the pediatric allergy clinic between October 2020 and April 2022 (n = 369) were contacted by phone where their eligibility was assessed and if inclusion criteria were met, were invited to participate in the interventional study. If permission was obtained, an invitation to complete an online questionnaire was sent by email.

Key Message
Caregivers in this sample believe it is appropriate to begin to transfer the responsibility of anaphylaxis recognition and AAI use to their children younger than the European Academy of Allergy and Clinical Immunology suggested age of 11-13 years. Most caregivers in this sample feel it is appropriate to begin to teach children to; recognize anaphylaxis symptoms under 6 years, and use an AAI at 9-11 years based on the child's readiness. Although most caregivers had received AAI training, only half felt confident in teaching their child its administration. Further evaluation is necessary to improve guidelines, enabling clinicians to train and support caregivers during this transition.
in Canada. 11 Questions related to demographics, readiness factors, parental AAI training, and caregiver confidence in training their children (Appendix S1). The questionnaire was piloted among a pediatric allergist, an allergy nurse, and general practitioners with special interest in allergy and a group of medical students from University College Cork (UCC).

| Data analyses
The survey data were extracted from Google Forms, downloaded into Microsoft Excel and imported into Stata 17 (StataCorp™, TX, USA) on an encrypted UCC computer.
Descriptive analysis was performed for each variable of interest.
Normally distributed data were expressed as mean and standard deviation (SD); non-normally distributed data were expressed as median and interquartile range (IQR); and categorical variables were reported as percentages. Normal distribution of data was evaluated by Shapiro-Wilk test. For non-normally distributed data, comparison was performed employing Mann-Whitney U test; comparison of normally distributed data was performed using independent sample ttest. For categorical data, the chi-squared test was used. Association between each independent variable and an ordinal variable was analyzed using a logistic regression with a cumulative odds model.

Confidence intervals of proportions were built by Wilson's method.
Parameters displaying p < .05 were considered statistically significant.

| Characteristics of sample
Of the 123 caregivers who completed the survey, 90.2% were mothers of the child and 8.94% were fathers. The majority of caregivers surveyed had children prescribed with an AAI in the <6 (25.2%) or 12-14 (27.64%) age groups. Most participants were in the 40-49 (51.22%) and 30-39 (32.52%) age groups and had completed postsecondary school education, with postgraduate college degrees as the most common level of schooling achieved (31.71%). The majority of households earned between €20,000 and €60,000. The characteristics of these caregivers are represented in Table 1.

| Age of transition
The most common ages selected for when caregivers feel it is appropriate to begin to transfer responsibilities were: <6 years for teaching recognition of anaphylaxis symptoms (65.9%); <6 years and 6-8 years for describing when adrenaline should be used (39%, 39%); 6-8 years for teaching how to self-inject adrenaline using an auto-injector trainer (35.8%); and 9-11 years for teaching how to use a real AAI on an orange or similar object (35.8%), carrying an AAI (35.8%), describe their anaphylaxis management plan (35.8%), and teaching to self-inject using an AAI (44.7%) ( Table 2).

| Readiness factors
Caregivers most frequently cited a history of more than one anaphylactic reaction (86.2%), history of severe anaphylaxis (94.3%), the child's ability to describe reasons to inject adrenaline (87.8%), and demonstrate AAI use (82.1%) as "very important" readiness factors influencing the age at which they feel it is appropriate to begin to teach their child to recognize anaphylaxis and use an AAI. The child's age (11.4%), school grade (30.9%), fear of needles (22%), and school policy regarding AAI carriage (22%) were the readiness factors

Not important
Somewhat important

Very important
Child has a history of more than one previous anaphylactic reaction 8 (

| DISCUSS ION
This is the first study in Ireland to examine caregivers' perspectives on when they believe it is the appropriate age to begin to transfer the responsibilities of anaphylaxis management to their child. Furthermore, readiness factors that influence the caregivers' approach to transferring the responsibility of anaphylaxis management to their child, their confidence in training their children and their views on who should support this transition were identified.
Caregivers in this sample believed it appropriate to begin to transfer the responsibility of anaphylaxis recognition and AAI use to their children younger than the EAACI suggested age of 11-13 years.
Most caregivers in this sample believed it appropriate to begin to teach children to recognize anaphylaxis symptoms from when a child is 6 years or younger and use an AAI at 9-11 years based on the child's readiness. The study of Canadian caregivers of allergy patients revealed similar trends, indicating shared experiences in transferring responsibilities to their children. 10 One study of 88 pediatric allergists found that very few expected the transfer of responsibilities to begin before the age of 9-11 years. 12 Most allergists considered 12-14 years of age to be appropriate for children to be able to recognize anaphylaxis symptoms, self-carry and use an AAI. These findings highlight the discrepancy between caregiver experience and clinician's expectations. 5

| Readiness factors
The readiness factors highlighted as "very important" by caregivers in this study were similar to those identified by allergists in Simon's study. 12 However, the leading factor for caregivers was "history of previous anaphylactic reaction" compared with the "ability to demonstrate AAI technique with trainer device," which was classed as the primary factor by allergists. 12 Even though the severity or number of past anaphylactic reactions cannot predict those of future episodes, parents were more motivated to start the teaching process after witnessing severe anaphylaxis. 14

| Caregiver training and confidence
In this study, pediatric allergy clinical staff were identified as the responsible party to teach children to use an AAI. It has been demonstrated that families were typically willing to take responsibility for their child's care; however, they require clear guidance, information, and support from medical professionals. 15 Although most caregivers had received AAI training, only around half felt confident in teaching their child to use an AAI. Evidently, the delivery of caregiver training requires improvement. One review of caregiver training in anaphylaxis management found that competence varied significantly between studies and further research is necessary to identify the most effective training strategies; however, clinician instruction on AAI administration correlates significantly with parental comfort with AAI use. 15,16 While the numbers in each subgroup analysis were small, this study suggests that caregivers with higher annual household incomes were more likely to believe they were responsible for training their child to recognize anaphylaxis and AAI use and exhibited higher confidence in doing so. This may reflect increased access to specialist health care in this group and therefore additional training in AAI use. [17][18][19] However, a 2021 study investigating factors contributing to the underuse of AAIs in pediatric patients found that despite caregivers reporting recent AAI training in clinic, they still feel nervous during anaphylactic episodes. 10 It is worth noting that the COVID-19 pandemic affected the delivery of all aspects of medical services, and this may have contributed to the lack of follow-up and training, particularly as outpatient appointments are typically where caregiver training occurs. 20 Telemedicine has come to the fore during the pandemic as a medium of healthcare delivery that can improve access to care, patientphysician interactions and limit costs. 21,22 In Ireland, telemedicine was used in epilepsy outpatient care and positive clinician and patient feedback was reported, thus indicating this may be beneficial in allergy management. 23

| Future research
Given the discrepancies between clinical and parental expectations, it would be pertinent for future research to study the factors that may indicate caregivers' desire to initiate an earlier transition of anaphylaxis management to their child among a larger cohort. Strategies to train and empower caregivers to teach their child anaphylaxis management should also be further investigated due to suboptimal caregiver confidence in training their children. Telemedicine can improve access to health care and outpatient management; therefore, it is important to investigate the potential role of telemedicine in providing caregiver training in AAI use.

ACK N OWLED G M ENTS
This research received support from Musgrave Group. The authors wish to thank Dr Elinor Simons, University of Manitoba, for kindly approving the use and adaptation of their questionnaire materials.
The authors wish to thank Ms. Jackie O 'Leary for her expertise and management of quality and regulatory affairs during this study. The authors are grateful to the parents who took the time to participate in the study. Open access funding provided by IReL.

PEER R E V I E W
The peer review history for this article is available at https://