1. Introduction
In recent decades, food allergies have become an increasing concern for families, clinicians, and policymakers worldwide. It is a key step of the “atopic march”, the natural history of allergic conditions that often progresses from atopic dermatitis in infancy, and later to food allergy, asthma, and allergic rhinitis [
1]. A recent systematic review reported the overall estimate for the prevalence of symptomatology plus confirmed allergic sensitivity with a positive serum-specific IgE or skin prick test (SPT) was 2.9% in Europe [
2].
Children with food allergies have a poorer emotional and social quality of life (QOL) compared to children with no food allergies or other chronic illnesses [
3]. Their primary caregivers also have a lower overall QoL than caregivers not looking after a child with food allergies, as it has a significant impact on parental emotions, parental time, and the QoL of the rest of the family. It is also related to high levels of stress and anxiety in parents [
3]. This impact on quality of life is attributed to the lack of a cure for food allergies, with treatment involving strict avoidance of the allergen and emergency treatment of symptoms caused by accidental exposure.
Anaphylaxis is defined by the World Allergy Organization as “typical skin symptoms AND significant symptoms from at least one other organ system; OR Exposure to a known or probable allergen for that patient, with respiratory and/or cardiovascular compromise” [
4]. While there is a global increase in the incidence of hospitalizations for anaphylaxis [
5], the highest incidence of fatal anaphylaxis due to a food allergy occurs in the second decade of life [
6].
The acute treatment of anaphylaxis involves self-management by the patient or caregiver using an adrenaline auto-injector (AAI) [
4]. Parents and children who have been prescribed an AAI should be given instruction and guidance on recognizing the signs and symptoms of anaphylaxis and how to administer an AAI [
4,
7]. However, the knowledge of anaphylaxis management and AAI administration among the parents of children with food allergies appears to be low [
8]. In a systematic review, knowledge of correct AAI administration technique was shown to be low, with only 32% of parents/caregivers successfully demonstrating a correct AAI technique [
9], while another review of the literature reported that the AAI administration success among parents ranged significantly, and the success rates varied from 5.6 to 84% [
10]. This may reflect several issues, including training effectiveness or lack of training, user stress during administration, or inherent differences consequent of the design of the individual auto-injector [
11].
Adrenaline can be administered using products from several different brands, three of which are available in Ireland: Epipen
® (Viatris, Canonsburg, PA, USA), Jext
® (ALK, Reading, UK), and Anapen
® (Bioprojet, Paris, France). Another brand, Emerade
® (Medeca Pharma AB, Uppsala, Sweden), has been recalled from the market in recent years [
12]. As the number of different AAI designs has increased, device switches could also become a significant clinical issue [
13].
There has been no previous research in Ireland assessing the anaphylaxis management knowledge of parents of children with food allergies. Similarly, possible factors that influence parents’ knowledge and the switching of brands of AAI have not been explored. Therefore, using a cross-sectional study method, the aim of this study was to assess the knowledge of anaphylaxis management and AAI administration of parents of children with food allergies attending a paediatric allergy clinic.
The primary objective is to assess the knowledge of anaphylaxis management and adrenaline auto-injector administration of parents of children with food allergies. The secondary objectives are to characterise the study population, to explore possible factors affecting the knowledge of parents, to document the switching between AAI devices, and to determine related factors.
2. Methodology
2.1. Study Design
This was a cross-sectional study that took place in the paediatric allergy clinic in Cork University Hospital, Cork, Ireland. This study was designed as part of a larger educational intervention project entitled Telemedicine as an Educational Tool Regarding Adrenaline Auto Injectors and Anaphylaxis Management (TEAAMs), for which ethical approval was received by the Clinical Research Ethics Committee of the Cork Teaching Hospitals (Reference code: ECM 4 (hh) 12 January 2021 and 3 (w) 9 March 2021).
2.2. Participants
Participants were caregivers of children with food allergies who had attended the paediatric allergy clinic. Inclusion criteria were parents or guardians of children under the age of 18 who had been diagnosed with an IgE-mediated food allergy, who had received previous training in anaphylaxis management and AAI administration, and who were currently prescribed an adrenaline auto-injector for their food allergy. Exclusion criteria were patients who were prescribed an AAI for drug or venom allergies.
Considering the COVID-19 pandemic, participants were identified from a retrospective chart review to minimize patient contact, and informed consent was obtained remotely.
2.3. Data Collection
Potential study participants were contacted initially by phone and asked if they were interested in taking part in the TEAAMs study, as well as the present study. Phone call attempts were made to each caregiver at least twice. During this telephone call, they were screened for eligibility, which may not have been apparent in their patient file. Eligible participants were sent an email containing detailed study information. They were given the opportunity to ask further questions by email or telephone. They then remotely completed the informed consent form and completed the online questions. Emails to remind interested caregivers to complete the questionnaire were sent three times if they had not completed the questionnaire. Google Forms was used to capture study responses.
2.4. Data Collection Methods
Participants were asked questions relating to socio-economic demographics (child’s age, parent’s age, child’s gender, relationship to child, household income, and level of education reached by caregiver), the child’s allergy history, and questions relating to AAI usage, such as whether participants have changed brands of AAI before and what influenced this change and what training they received from a healthcare professional. They then completed the anaphylaxis management knowledge questionnaire as described below. Once the online questionnaire was completed, they were then invited to take part in the online educational intervention, hosted on Microsoft Teams by a member of the research team, where their AAI administration is assessed remotely, with the caregiver demonstrating using a trainer pen or explaining the steps using their child’s AAI device, before continuing to take part in the education session.
2.4.1. Assessment of Knowledge of Anaphylaxis Management
An online questionnaire was designed to assess anaphylaxis management knowledge and allergy management behaviours. Questions were designed following a review of the literature, and validated amongst a pilot group of three parents, a consultant paediatric allergist, and an allergy nurse specialist. Small modifications were made based on the feedback from this pilot group before inclusion in the final questionnaire.
Anaphylaxis management was assessed through 9 knowledge questions (
Supplementary Materials Table S1), focusing on the meaning of anaphylaxis and the recognition and management of allergic symptoms. Of these, six questions are multiple-choice format, where the parent must choose the correct step in each situation. In the final question, parents are asked what behaviours are best to manage their child’s food allergy, and are able to choose from multiple options, with 5 options considered safe behaviours and are encouraged, one behaviour considered neither safe nor risky, but is not encouraged (‘Keep children at home from any parties where there may be foods the child is allergic to’) and two behaviours are considered unsafe behaviours and are discouraged (‘Keep adrenaline pens safe in a locked storage cabinet’ and ‘Wait until medical professionals arrive if you think your child might have anaphylaxis but are unsure’) (
Supplementary Materials Table S2).
The knowledge questions were stratified to obtain an overall anaphylaxis knowledge score of 12. For the nine anaphylaxis knowledge questions, one point each was awarded. For the allergy management behaviours, parents score one point for selecting the safe allergy behaviours, up to a maximum of three. The parent is not awarded any points for selecting ‘Keep children at home from any parties where there may be foods the child is allergic to’. For the two unsafe behaviours, two points are subtracted for each behaviour selected, to a minimum of 0. If a parent selects all 8 answers, it is assumed that the parent did not display critical thinking in answering the question, and thus is given a score of 0. Thus, the score between 0 and 3 for the allergy management behaviours question is added to the score out of 9 for the anaphylaxis management questions, for a maximum score of 12.
2.4.2. Assessment of AAI Administration Ability
The tool was designed using extensive literature research and adapted for an online assessment, specific for each brand of AAI. For the AAI assessment tool, the caregiver received a mark for each step they performed correctly for the specific brand of AAI, for a total score of 6. For Anapen, which is a two-cap device, one point was awarded for demonstrating the removal of both caps, while no points were awarded for demonstrating the removal of one or no caps. Parents were then scored on whether they performed the three ‘critical steps’ for AAI administration [
14]: (1) removing the cap(s); (2) pressing or pushing to hear a ‘click’; and (3) holding the device in place for the specified time, usually 10 s. If the parents performed only 2 or less of these steps, they were considered to have failed to deliver the adrenaline effectively.
2.5. Statistical Analysis
Descriptive statistical analysis was carried out for all collected variables. Continuous data were expressed as means and 95% Confidence Intervals (CIs), whereas categorical variables were reported as percentages e.g., age of child, age of parent, type of allergy, and mean household income. Comparisons of those who had optimal and suboptimal anaphylaxis knowledge and AAI administration were carried out using chi-square analysis and One Way Anova. The ability to administer the different AAI devices was compared using an Independent Samples Kruskal–Wallis Test. Data were considered statistically significant if p-value was ≤0.05. Univariate and multivariate logistic regression models were used to assess factors relating to anaphylaxis management knowledge, AAI administration, and switching AAI devices; odds ratios (ORs) were expressed with 95% CIs. Variables associated with an outcome in the univariate analysis (p-value < 0.05) were considered for the multivariate model, and the final model was selected using stepwise regression (p-value < 0.05). Data were analyzed with SPSS Version 28.
3. Results
3.1. Participants
A total of 701 parents were contacted between June 2021 and May 2022. Of these, 313 could not be reached by telephone or did not meet the eligibility criteria when screened. An invitation email was sent to 388 parents to take part in this study. A total of 185 responses were received through the Google Forms questionnaire. This equates to a response rate of 42.2%. Six responses were excluded from the analysis on further inspection, as they responded ‘No’ when asked if their child had been prescribed an AAI. Thus, 179 participants were eligible to take part in the online telemedicine assessment and intervention. Over the study period, 27 participants were lost to follow-up following completion of the initial questionnaire, leaving 152 participants to take part in the online telemedicine intervention, who were included in the analysis. A flow diagram depicting the recruitment of the participants to this study is shown in
Figure 1. A summary of the participant demographics is shown in
Table 1.
3.2. Anaphylaxis Knowledge
Regarding training in anaphylaxis management, 11.2% (n = 21) received training less than 6 months ago, 5.3% (n = 10) received training between 6 and 12 months ago, 18.1% (n = 34) received training 1–3 years ago, 16% (n = 30) received training 3–5 years ago, and 12.2% (n = 23) received training over 5 years ago, while 17.6% (n = 33) had never received training.
Out of a total score of 12, the mean anaphylaxis knowledge score was 9.76, SD 1.577, or 81.33%, with a maximum score of 12 (100%) and a minimum of 5 (41.66%). The topics that were answered correctly most frequently included the risk of anaphylaxis (94.7%) and the management of mild cutaneous allergic symptoms (94%). The topics that were answered correctly the least included the correct timing of administering a second adrenaline auto-injector when required (66.2%) and the recognition and management of cardiovascular signs of anaphylaxis (50.3%). The frequency with which the parents correctly answered each question is displayed in
Supplementary Materials Tables S1 and S2.
The factors relating to suboptimal anaphylaxis knowledge were identified by comparing those who had a below-average score in the anaphylaxis knowledge assessment (<9). The demographic factors included parents being older or younger than 40 years of age, children older or younger than 10 years of age, a household income less than EUR 40,000 per year, having a level 8 undergraduate education, a history of switching between AAI devices, and receiving anaphylaxis management training 3 years ago (
Table 2).
The frequency of correctly answered anaphylaxis knowledge questions is stratified by parent age and by household income in
Supplementary Materials Table S1. More parents with a household income EUR >40,000 per year correctly knew the definition of anaphylaxis (95.3% vs. 77.8%,
p = 0.004), while more parents who were >40 years of age chose the correct way to manage cutaneous allergic reaction symptoms (97.8% vs. 87.9%,
p = 0.029) and how to recognize and manage the respiratory symptoms of anaphylaxis (90.3% vs. 84.5%,
p = 0.037). In the final model, switching devices previously, the parent being aged under 40 years, the child being aged under 10 years, and a household income under EUR 40,000 per annum increased the risk of a suboptimal anaphylaxis management score, but these were not statistically significant (
Table 2).
3.3. AAI Administration Ability
When assessed for AAI administration ability, the median score among the 152 parents was 4 correctly performed steps out of 6 total steps (IQR 3–5). This included 5 parents (3.3%) who did not perform any of the steps correctly, 3 (2%) who performed one step correctly, 5 (3.3%) who performed two correctly, 33 (21.7%) performing three steps correctly, 53 (34.9%) performing four steps correctly, 38 (25%) performing five steps correctly, and 15 (9.9%) performing all six steps correctly. The steps that were incorrectly or not performed most frequently were pushing until hearing a ‘click’ (35%), holding in the device for the specified length of time (71%), and massaging the injection site following removal of the device (32%).
Of the 152 participants, 26.7% (n = 40) performed all three critical AAI administration steps correctly, while 49.3% (n = 75) performed two critical steps correctly, 17.8% (n = 27) performed one critical step correctly, and 6.6% (n = 10) performed none of the critical steps correctly.
The ability to administer the different AAI devices was compared using an Independent Samples Kruskal–Wallis Test. There was no statistical difference between the raw score of 6 among the three AAI brands, with a mean score for Epipen of 3.9 (95% CI 3.68–4.12), Jext of 4.21 (95% CI 3.43–4.99), and Anapen of 4.31 (95% CI 3.41–5.21) (
p = 0.159) (
Figure 2). The ability to carry out all three critical AAI administration steps also did not demonstrate a statistical difference, with 24.2% (n = 29) of those using Epipen performing all three steps, compared to 36.8% using Jext (n = 7) and 30.8% (n = 4) using Anapen (
p = 0.401).
There was no statistical difference between the ability to use the one-cap devices (Epipen and Jext) and the two-cap devices (Anapen) (25.9% vs. 30.8% respectively, p = 0.703).
The factors relating to successful AAI administration demonstration were identified in those who performed all three critical administration steps. A univariate analysis was conducted for demographic factors including parents being older or younger than 40 years of age, children older or younger than 10 years of age, a household income less than EUR 40,000 per year, having a level 8 undergraduate education, a history of switching between AAI devices, and receiving anaphylaxis management training 3 years ago (
Table 3).
The final model consisted of the factors considered statistically significant (≤0.05) in the univariate analysis, and other factors considered to be confounding factors (AAI device, parent age, switching AAI devices). The multivariate analysis demonstrates that a household income under EUR 40,000 per annum reduced the likelihood of successful AAI administration (OR 0.33 95% CI 0.125–0.87,
p = 0.025) (
Table 3).
3.4. Switching between AAI Devices
Of the three available AAI devices in Ireland, 78% participants (120) carried Epipen, 12.5% (n = 19) carried Jext, and 8.6% (n = 13) carried Anapen. When asked if they have switched between different AAI devices in the past, 46.4% claimed to have switched at least once before, with 19.4% switching once, 12.4% switching twice, 9.1% switching three times, and 5.4% having switched more than three times before.
The most common reason for switching was due to the unavailability of their usual device at their pharmacy (60%). Of those who changed brands, 65% (n = 46) did not receive training in the use of the new AAI.
An analysis of the factors relating to switching AAI devices was conducted for demographic factors including parents being older or younger than 40 years of age, children older or younger than 10 years of age, a household income less than EUR 40,000 per year, having a level 8 undergraduate education, and receiving AAI administration training less than one or more than three years ago (
Table 4).
In the final model, the parent being aged under 40 years (OR 0.342 95% CI 0.146–0.802,
p = 0.014) and receiving AAI administration training less than 3 years ago (OR 0.267 95% CI 0.125–0.571,
p < 0.001) reduced the incidence of switching AAI devices (
Table 3).
4. Discussion
This study assessed the knowledge of anaphylaxis management and AAI administration of parents of children with food allergies attending the paediatric allergy clinic in Cork University Hospital. This is the first study in Ireland to describe the knowledge of anaphylaxis management of parents of children with food allergies.
The knowledge areas explored in this study are reflected in other anaphylaxis knowledge assessments in studies focusing on assessing and improving parent knowledge [
15,
16,
17]. Sicherer et al. employed a true/false test approach, similarly testing the knowledge of the timing of allergic reactions, and the management of cutaneous and upper respiratory symptoms of anaphylaxis, while also testing the knowledge of food labelling laws [
17]. The parents scored highly in safe allergy management practices such as not storing their AAI in the fridge, while scoring poorly in the correct management of the symptoms of anaphylaxis [
17]. The Chicago Food Allergy Research Survey for Parents of Children with Food Allergy (CFARS-PRNT) was employed in studies in the USA and the Netherlands, similarly assessing parents’ understanding of the definition of anaphylaxis and common triggers of anaphylaxis, as well as the perceptions of susceptibility and prevalence [
15,
16]. The mean score among USA parents was 75.3% while in the Netherlands the mean score was 58.9%. The knowledge questionnaire employed in this study therefore assesses similar knowledge areas to other previously published questionnaires, with comparable levels of knowledge among parents.
One area which other published questionnaires fail to address in knowledge questionnaires are the gastrointestinal and cardiovascular signs and symptoms of anaphylaxis. The lack of recognition of cardiovascular and gastrointestinal symptoms of diagnosis is worrying, when it has been shown that in those who presented to the emergency department and were treated with adrenaline, 34.2% presented with nausea or vomiting, while 31.6% presented with hypotension [
18]. Future knowledge assessments should address the symptoms of anaphylaxis across the cutaneous, respiratory, gastrointestinal, and cardiovascular systems as described by the World Allergy Organization [
4].
While the majority of the parents correctly identified the five safe allergy management practices in the questionnaire, almost one quarter of the parents selected that they would keep the AAI devices stored in a locked cabinet. This is a concerning finding considering the emphasis that is placed on always carrying the child’s AAI device with them. Carrying one or more AAI devices is part of the European Academy of Allergy and Clinical Immunology (EAACI) anaphylaxis guidelines [
7]; however, the low carriage of AAI devices has been widely reported, particularly amongst adolescents and young adults [
19,
20], highlighting the urgent need for inclusive and thorough educational programs for children and young adults in transitioning from management dependent on their parent to independent self-management, while also empowering their parents with the knowledge and skills to support their child through this transition [
21].
Overall, the parents’ demonstration of correct AAI administration was suboptimal. A poor administration ability has been reported in studies across several countries [
9,
10]. The suboptimal AAI administration knowledge is reflective of the low confidence parents report for educating their children on correct AAI administration, resulting in their preference for a trained allergy professional to educate their children [
22]. While differences have been reported in the administration ability in different AAI devices, especially between one-cap devices such as Epipen and Jext and two-cap devices such as Anapen [
11,
13], this study demonstrated a similar administration ability across all available devices.
The combination of the poor recognition of anaphylaxis symptoms, the evidence of not carrying the AAI device, and the lack of confidence and knowledge of AAI administration are potential major contributing factors to the widespread underuse of adrenaline in the community, resulting in near fatal and fatal outcomes, with reports of an as low as 24% reported use of adrenaline when anaphylaxis symptoms are present [
23,
24,
25]. The delayed administration of adrenaline is associated with increased mortality, and thus the prompt recognition and immediate administration of adrenaline to a child by the parent is paramount in improving outcomes [
24].
Regarding patient demographics, the most common allergy for which an AAI was given was peanut allergy. While milk and egg allergies are the most common causes of anaphylaxis among infants [
6], it is expected that these allergies are underrepresented in this population as the mean age is 8, and with the majority of children being introduced to milk and egg using the milk ladder before the age of three, they are not normally prescribed an AAI [
26].
It was found that younger parents aged <40 years, a household income of EUR <40,000 per annum, and never switching between AAI devices increased the risk of scoring poorly in anaphylaxis knowledge. It is likely that younger parents have children of a younger age, and thus, may have had fewer interactions with paediatric allergy specialists where they would receive anaphylaxis training, and may not have had the opportunity to switch between different AAI devices. This is reflected in the multivariate analysis of whether parents had switched devices in the past, where older parents, most likely with older children who have had to manage their food allergy for longer, are more likely to have switched devices in the past.
Most notably, the factor which played a role in anaphylaxis management knowledge, AAI administration ability, and switching between devices was the annual household income. Earning EUR <42,000 is considered a low level of income in Ireland in other studies [
27], and it can be concluded from this study that parents with a low level of income score poorly in anaphylaxis knowledge and AAI administration ability, irrespective of education level or age. While the impact of low socioeconomic status on the health outcomes of neonates has been explored in Ireland [
27], similar studies have not been performed focusing on food allergies as well as other chronic conditions, despite the evidence of inequalities in access to specialized allergy care in other countries [
28]. Even in countries with universal access to healthcare [
29]. It can be hypothesized that those with a lower level of income are less likely to have access to specialized allergy clinics, and are less likely to receive formal training in anaphylaxis management, resulting in poorer health literacy for managing their child’s allergy. This is also reflected in the rate of switching between AAI devices, where those considered to have a high level of income in Ireland of EUR >100,000 per annum [
27] were more likely to have switched AAI devices in the past. While sufficient access to specialized allergy care is a known concern, there is the cost of clinic visits, transportation, medications, and special dietary products that manifest as disparities between those with a different socioeconomic status, and such disparities should be explored in greater detail in Ireland [
30].
This study has shown that switching AAI devices is a common occurrence among parents of children with food allergies, with almost half of parents reporting switching AAI devices at least once before. The reasons for switching brands is reported elsewhere, where it was found that 59.74% of caregivers said this was due to the lack of availability of their previous AAI at their pharmacy, 20.7% said the expiration date of the new AAI was longer than their previous AAI, 9.1% said the new AAI was recommended by their pharmacy, and 5.2% stated the new brand was easier to use [
31]. While parents are often required to switch brands due to pharmacy factors, almost two-thirds of parents do not receive training in the administration of the new AAI. This is supported by the literature, which explored AAI training practices among pharmacists in the Netherlands, where only half of all pharmacists demonstrated the use of the AAI when asked to fill out a prescription [
32], with none of the pharmacists in the study successfully demonstrating the correct use of the AAI [
32]. There is a need to explore the perspectives, beliefs, and attitudes of pharmacists in Ireland when prescribing adrenaline in order to develop practice guidelines for the adequate prescription of adrenaline in the community [
31].
4.1. Implications for Practice
As part of the long-term management of anaphylaxis, both EAACI and the WAO recommend the regular reinforcement of anaphylaxis management and AAI administration to parents, and that training should be received whenever switching to a new device takes place [
4,
7]. While this study did not find disparities in the administration ability between different devices, training should be provided regularly in all available devices regularly, and ideally once a year or at each clinical visit with the allergy team [
7].
Education and training interventions by expert healthcare professionals are known to improve parents’ knowledge of anaphylaxis management and AAI administration [
9,
10]. One recent randomized control trial employed an intervention comprising two 3 h sessions over a 2-week period and found significant improvements in knowledge and emergency management competence [
33]. A reduction in caregiver anxiety was also demonstrated following the intervention [
33]. Such educational interventions could be employed in allergy centres, involving specialist clinicians, nurses, dieticians, and psychologists [
4,
33], particularly aimed at parents of children recently diagnosed with a food allergy, as knowledge deficits were particularly noted in younger caregivers throughout this study.
Such interventions should also be adapted to create more accessible training opportunities for parents of a low socioeconomic or income level, such as telemedicine, which rapidly became a key feature of allergy clinics during the COVID-19 pandemic [
34]. However, its benefit for educational interventions for anaphylaxis management and AAI administration has not yet been explored.
4.2. Implications for Research
In order to improve the anaphylaxis knowledge of parents as described above, it is first essential to design and validate assessment tools for anaphylaxis knowledge and adrenaline auto-injector administration. While several questionnaires have been designed across multiple studies, only one tool has been cross-culturally employed in two countries [
15,
32]. The lack of consensus in assessment is more apparent for AAI administration, where no single study has provided a validated assessment tool [
10]. Such assessment tools could also be adapted for paediatric, adolescent, and adult patients, as well as specialist and non-specialist healthcare professionals [
35].
Furthermore, as it has been shown that switching between AAI devices is a common occurrence, and that training is often not provided when switching devices, it is imperative to improve pharmacist involvement in the community-based education of anaphylaxis [
32].
4.3. Strengths and Limitations
The strengths of this study include the design of assessment tools for anaphylaxis management which explore the parents’ knowledge using true/false questions while also assessing their situational judgement using multiple-choice questions, covering different systemic symptoms of anaphylaxis. In addition, a standardized tool to assess AAI administration for all available devices available in Ireland was employed. Furthermore, a large sample size, reflective of the population of parents attending the paediatric allergy clinic at Cork University Hospital, was utilized.
There are limitations to this study, which must be considered. Firstly, the relatively low response rate of parents to the online questionnaire and subsequent participation in the online educational intervention may potentially influence the results of this study due to participant bias. Secondly, most respondents to the questionnaire were mothers. Therefore, it was not possible to accurately compare the knowledge of anaphylaxis management between mothers and fathers, and whether the knowledge of the management of the child’s food allergies was shared among parents.