Beliefs about food allergies in adolescents aged 11–19 years: A systematic review

Abstract Aims Research suggests of people with food allergy (FA), adolescents have the highest risk of fatal allergic reactions to food, yet understanding of this population and how they manage their condition is limited. Understanding beliefs and how they affect behaviour could inform ways to reduce risk taking behaviour and fatal reactions in adolescents. This systematic review aimed to explore beliefs adolescents hold about their FA, and how these may be associated with FA management. Demographics Adolescents aged 11–19 years with FA. Methodology A systematic search of seven databases was conducted. Papers of any design were included that reported on the beliefs about FA in adolescents aged 11–19 years. Data was systemised by narrative thematic analysis. Findings 20 studies were included. Themes included navigating FA in different environments, carriage and use of adrenaline auto‐injectors, management of the risk of anaphylaxis, behaviour and understanding of others, and food‐allergic identity. Implications Adolescents with FA hold a variety of condition beliefs; some beliefs were related to behaviour that could lead to an allergic reaction, while other beliefs were related to protective behaviours. Further research into understanding adolescent beliefs in order to inform clinical management and reduce the risk of potential fatal reactions is essential.

carry their adrenaline auto injector (AAI) the only medication for anaphylaxis, a life-threatening severe allergic reaction. Adolescence is therefore a critical period to examine in those with FA, to attempt to reduce the likelihood of these reactions.
The impact of FA and how it is managed is thought to change as children develop, with adolescence as a time of transition where their beliefs about themselves, their world and their condition may change. Up to the age of 8 years, children tend to rely on parents to manage their FA, and after this age as they progress into adolescence, they become more aware of the difficulties of managing FA and believe it is more dangerous, leading to anxiety. 5 Over the age of 12 years, children have been reported to experience greater conflict with their parents regarding their FA 5 as beliefs begin to misalign (e.g., that parents know best and can always keep them safe) which may lead to risky behaviour as adolescents try to assert their independence.
Condition beliefs, how the adolescents feel about their FA, may provide insight into why they engage in these behaviours, but research of this topic is very limited. Beliefs are important as they may directly inform protective behaviours such as AAI carriage and label-checking, which may reduce reactions. 6,7 Qualitative research has highlighted adolescents hold strong beliefs about their AAIs, expressing the belief that AAIs are inconvenient due to their bulk 8,9 and some adolescents are afraid to use them due to the needle injection. 10,11 Beliefs of peers are also important for adolescents as these may influence the way in which children with FA manage their condition. 12,13 A review on adolescent experiences of food-induced anaphylaxis found beliefs around the adolescents' identity with FA, balance and controlling the uncontrollable to be themes considered to directly influence the adolescents' experiences. 14 There are currently no systematic reviews on adolescent beliefs about their FA. This systematic review, therefore, aimed to explore adolescent beliefs about their FA and how these may be associated with FA management behaviours.

| METHODS
This review is reported using the updated 2020 Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines 15 and the protocol was registered on PROSPERO (registration number: CRD42019133576).

| Eligibility criteria
The eligibility criteria and search terms were developed using the SPIDER (Sample, Phenomenon of Interest, Design, Evaluation, Research type) tool. 16 To be eligible, peer-reviewed articles were required to have sampled participants within the age range of 11-19 years with FA, explicitly discuss or contain significant analysis relevant to beliefs about FA, and be written in English. If papers also included participants outside of this age range but were explicit via quotes or written clarification as to what age the results referred to, these were included. Data from participants outside the age range was not included in analysis. Papers were considered if published between the years 2000 and 2022, as according to the UK's National Health Service, FA has 'risen sharply' during this time. 17 The Mixed Methods Appraisal Tool (MMAT) 18 was used to assess the quality of studies to be included, and studies were excluded if they were assessed as poor quality. Eligibility criteria are outlined in Table 1.

| Study selection
Records were assessed for eligibility by KN and RK and duplicates were removed by KN. Article titles and abstracts were read and removed by KN and RK if they did not meet eligibility criteria.
Following analysis of abstracts, relevant papers were read in full. Full papers were reviewed by KN and RK and excluded if they did not meet the eligibility criteria.

| Synthesis of results
Adolescent FA beliefs were extracted from the study results and reported. As both qualitative and quantitative data was analysed, and a variety of designs and outcomes emerged, a narrative synthesis incorporating thematic analysis 19 was used to communicate the results. Subgroup analysis was also conducted to assess differences between study samples, settings, and methods.

| RESULTS
A total of 526 research papers were identified during the database search, with 4 additional papers found through reference chaining, 81 duplicates were removed to leave 449 papers. Following abstract review, 32 papers were read in full, and 12 papers were excluded as they did not meet inclusion criteria. A total of 20 studies met eligibility criteria and were included in data extraction ( Figure 1).

| Study characteristics
A total of 16 studies used qualitative methods and four used quantitative methods. Papers reported data on approximately 956 participants aged 6-21 years; however, results reported for participants outside the age range for this review were excluded from analysis.  Table 2 provides details for each included study.

| Quality appraisal of studies
The MMAT 18 was used to assess the quality of the studies included in the systematic review. Included studies were assessed by KN and reviewed by RK and no studies were deemed unsuitable for analysis due to poor quality. Multiple papers had arguably small sample sizes; however, these were included due to the limited studies on this topic and following recommendations by Braun and Clarke 20 regarding sample sizes for qualitative studies. Multiple studies with the same author also included similar numbers of participants and inclusion criteria, however, as it is not clearly stated whether the samples were the same or different, and there were some different findings BIPQ was used as a measure, while data analysis included non-parametric analysis and Mann-Whitney analysis.
'Time-line' (illness duration) followed by 'concern', had highest overall scores on the BIPQ suggesting patients are most concerned about the chronic duration of their condition. Females had higher emotional representation and older participants (14-18 years) had stronger beliefs their condition will be long-lived.
Jones et al. reported, all were included for analysis. Full quality appraisal can be found in Table 3.

| Thematic analysis
Five themes were identified in the data: (1) navigating FA in different environments; (2) carriage and use of adrenaline auto-injectors; (3) managing the risk of anaphylaxis; (4) beliefs and understanding of others; (5) food-allergic identity.

| Navigating food allergy in different environments
Beliefs about differences in management in spaces such as friends' houses, school, restaurants and abroad on holidays were discussed by adolescents in N = 12 studies and were affected by perceived risk, predictability, familiarity and distance from external help 11,21-23 such as hospitals. The family home or where a parent was present was considered safest 21,23-25 as the adolescent could relax and leave responsibility of their safety to someone else.   Concerns of missing out were apparent in places difficult to manage FA. Restaurants and school trips were described as annoying as adolescents could not eat 'the same as everyone else'. 26 Scepticism of expertise of catering staff was an important factor in the eating out experience with concerns about food prepared in unknown places. 8,25 Asking staff about an allergen was embarrassing, 27,28 and difficult, 24 especially where staff were believed to be indifferent. 10,25 These beliefs were also expressed on holidays abroad, dealing with new foods and a different culture. Adolescents preferred to eat foods they knew were safe or rely on parental judgment, especially if there was a language barrier. 23 Schools were believed to be risky depending on perceived support and perceived efficiency of school policies. Secondary school was viewed as more dangerous than junior school, 28 due to less organisation and control from teachers. Adolescents believed secondary school to be exclusionary, isolating them by making them sit alone at lunch or excluding them from school trips. 28,29 However, it is not clear whether this was due to teacher choice or school policy.
Adolescents believed they must be cautious managing FA at school due to difficulty determining risk and lack of trust in teachers. Some did not feel safe due to concern of contamination or previous experience of bullying, including threats to contaminate food or having their allergen thrown at them. 24,26 Adolescents described instances where they left the classroom against teacher wishes because they did not feel safe. 29 Teachers were seen as unable to help due to the adolescent with FA being a minority in the classroom. 28 Adolescents believed there was greater potential risk of encountering allergens or a reaction due to a high volume of students, unsupervised lunch areas, common eating areas and untrained staff. 24,28 Where schools had attempted to be accommodating, such as using allergen-free ingredients in food technology classes, adolescents felt safer and included. 21 Others believed special treatment because of their FA highlighted them as different to their peers. 29 Some adolescents believed avoidance was the best way to cope with this, finding safe spaces where food was not allowed 23 and managing their stress by reducing their risk of having a reaction.

| Carriage and use of adrenaline auto-injectors
Beliefs about AAIs were discussed in N = 10 studies and were associated with likelihood of the adolescent carrying their AAI at all times and considered situational factors such as location, distance from home or parents, possibility of the allergen being present and whether they had visited a place before. [8][9][10][11] Barriers to AAI carriage were believed to be inconvenience of the size and difficulty of use. 8,9 Some adolescents were also afraid to administer 26 due to fear of the needle, even in the event of a reaction. 10,11 Those who strongly identified with their FA and had stronger feelings such as anger or anxiety were more likely to carry their AAI. 6 Also, adolescents with higher perceived severity and susceptibility to Findings from Gallagher et al. 9 in a qualitative study suggested that barriers such as fear and uncertainty of how to use the AAI and failure to recognise anaphylaxis may reduce AAI use.
When the perceived risk of reaction was low, such as going to play football, adolescents were less likely to carry their AAIs. 10,22 More boys reported being inconvenienced than girls by the size of AAIs, stating they were too large for a pocket 9-11 and believed they would be more likely to carry the AAI if they were smaller. 10 Some were embarrassed of their AAIs and less likely to carry them because of shame, fear of being seen as different or irritation at having to explain themselves. However, some adolescents acknowledged that the benefits outweighed the inconvenience. 9 Participants reduced discomfort of AAI carriage by leaving it with a friend, teacher or in their bag nearby. 11 Beliefs about how to use AAIs were also salient and discussed in six studies. Jones et al. 7 found the majority of their sample believed they could correctly use their AAI with 40% feeling 'sure' and 37% feeling 'absolutely sure'. This contrasts with the findings of qualitative papers with a similar age range (13-17 years) from Scotland, Europe, and the Netherlands, as well as another quantitative study in the Netherlands where adolescents did not believe they could use their AAIs properly and feared they would use it wrong. 9,27,30 Saleh-Langenberg et al. 30 suggested that lack of confidence using AAIs can result in a higher perceived burden. As some adolescents with FA were unsure of how to use AAIs, this could lead to misfires or reluctance to use the device. 11 Adolescents and their siblings were afraid of using the AAI and of contacting emergency services, preferring to use antihistamines due to their familiarity. 26 Anxious beliefs around the needles resulted in preferring someone else to administer the AAI 9,10 or for the AAI not to be used at all. 11

| Managing the risk of anaphylaxis
Adolescents believed it was difficult to manage the risk of an allergic reaction 25 and these beliefs were discussed in N = 11 of the studies.
Adolescents were either dismissive towards high-risk behaviours that may potentially result in anaphylaxis or expressed a great fear of allergic reactions, which they associated with severe danger. 5,8,21,25,28 Some adolescents presented both beliefs, being very aware of their FA yet simultaneously viewing it as 'no big deal'. 22 Where peers were all eating a food which potentially contained an allergen, this increased likelihood of consumption. 10 Eating a potential allergen despite the risk was undertaken to 'fit in' and gain the trust of others, and to increase independence, control and empowerment. 24 Some also believed that certain foods, such as chocolate, were worth the risk of having a reaction. 21,25 Some adolescents were more likely to eat food with a warning label if a parent was present compared to just friends, as they felt safer. 10 However the majority of adolescents were dismissive of 'may contain nut' warnings unless the product was made in a factory that made peanut products specifically. 10 Adolescents were also sceptical towards the legitimacy of the presence of allergens in foods with 'may contain' labels and the process of constant checking was believed to be annoying 8 and restrict their food choices. They believed less use of these 'defensive' warnings where risk was low as well as simpler and more consistent allergy warnings could improve allergen avoidance 10 as labels may be taken more seriously.

| Behaviour and understanding of others
Beliefs towards FA from others such as friends, classmates, school staff, parents and the wider community were discussed in N = 14 of the studies. Adolescents in N = 8 of the studies said that once their FA was disclosed to their classmates, they experienced discrimination and classmates being mean-spirited. 29 Some expressed frustration that peers tended to focus on the limitations of their FA, identifying them as different and making the situation difficult to cope with. 21 To avoid being excluded, some adolescents purposely did not disclose their FA, only confiding in close friends, 5,27 believing others would not understand. Classmates were highlighted as needing education and information to increase understanding. 10 Jones, Sommereux and Smith 31 emphasised the importance of social support groups. Being able to speak with others of a similar age and similar experiences with FA was believed to be helpful as they felt understood, which increased confidence.
A lack of education and awareness of others was the greatest barrier to adolescents with FA being understood, accepted and becoming independent. 28 Adolescents also believed they could not necessarily trust adults due to a lack of understanding of FA and felt they needed to take control themselves to prevent a reaction. This lack of awareness around FA, for example, thinking an allergic reaction could just cause a rash rather than be life-threatening, 5,21 led to adolescents feeling uncertain about how to manage different situations such as ordering food. 8 Adolescents felt frustrated and believed their FA was not taken seriously by others and often ignored in schools by teachers and peers 21,25 and even in situations where allergen information is important such as restaurants.
Parental beliefs and behaviour may also affect adolescent beliefs and were discussed in N = 8 studies. Some parents highlighted the risks, encouraging hypervigilance and reminding of possible consequences, which sometimes led to conflict. 5 at home. Further conflict may result in a breakdown of routine when with grandparents, who were described as more lenient. 24 When there was a family member or friend who also had a FA, adolescents felt more accepted 11,21 as otherwise some family members struggled to empathise.

| Food-allergic identity
A total of N = 17 studies discussed beliefs related to identity and FA.
Some adolescents believed FA was difficult as it was believed to be a big part of their identity, that they were powerless, and their FA was unmanageable. In response, maladaptive coping strategies including isolating themselves or excessive hand washing were reported. 28 High illness concern and emotional representation, especially in females may lead to emotional difficulties due to their FA and would require further support. 33 Believing it was necessary to depend on others and feeling a lack of control in relation to their own bodies was difficult for some adolescents, 21  Considering the future, gaining choice and control led to empowerment and gaining trust in themselves and their environment, resulting in a more positive outlook. 28 When reflecting on a future away from parental safety, adolescents believed although they would never be completely safe, they would get increasingly better at FA management 21 and in their own safe space would have control over what food they were exposed to. 25

| Subgroup analysis
Subgroup analysis was explored through results based on age, gender, geographical location, method and allergen to determine whether this may influence results. Gender differences between participants were limited, however frustration with AAI carriage was reported as more substantial in male participants. [9][10][11]32 Studies did not explicitly discuss differences in beliefs dependent on allergen.
Methodologically, there appeared to be minimal contrasting findings apart from where Jones et al. 7  Schools were believed to be risky places depending on how supported adolescents felt, and secondary school was viewed as more dangerous. 27 Stigma and bullying are issues in need of attention as not understanding the severity of FA can lead to fatalities, as in the case of West London student Karanbir Cheema who died of a severe allergic reaction aged 13 years. 33 Concerns around exclusion in schools from studies in this review have also been reported in other research looking into FA policies in schools. 35 Educating those with FA about risk rather than allowing fear to be a barrier may improve beliefs towards safety of places. Teaching adolescents how to manage risky situations such as navigating restaurant menu ingredients or eating with friends may also increase independence.
AAIs were highlighted as a big concern in this review, with subgroup analysis identifying more frustration with AAIs in male participants. Carrying their AAI despite its perceived inconvenience could be attributed to increased perceived severity of FA. Leach, Smith, Brown, Davies and Jones 36 suggest that adolescents aged 13-18 years were conscious about safety, speed of administration, accessibility and carriage, comprehensive instructions, indication of correct administration, visibility and precise drug delivery. AAI size and needle concern were also important, a re-evaluation of design to make the AAI smaller may increase likelihood of carriage. 10 Reassurance about the needle with frequent training and provision of trainer pens from allergy clinics may also increase confidence on administration and reduce apprehension, reducing mistakes such as not holding the device in place long enough. 37 Good administration was seen more in those who had a history of anaphylaxis, were over 18 years of age, prescribed an AAI more than 30 months, membership of a support group and AAI administration training by an allergist, highlighting a need for support in those under 18 years of age.
When managing the risk of anaphylaxis, adolescents found it difficult to balance increasing independence and accepting more responsibility for their FA, which is experienced uniquely in adolescence. Beliefs seen in this review were also seen in an older sample in A common risky behaviour was dismissal of 'may contain' food warnings and consuming foods that may not be safe, in line with findings from Greenhawt et al. and Sampson et al. 4,38 This is a concern as intentional exposure to allergens in children leading to an allergic reaction were cited as due to not yet having a serious reaction. 39 A study of food choices in nut-allergic consumers, 40 highlighted three strategies: past experiences of food consumption; sensory factors to determine risk; and quality of the product or the place the food originated from. Adolescents in this review also discussed using past experiences, supporting this technique. However, they also were influenced by parents or friends.
The visual aspect of the allergen labels such as where they were located on the packaging was is seen as important 41  Educating the wider community, beyond immediate peers, is also important for decreasing risk of reactions and reducing the negative impact of diagnosis and FA management. 49 Clinicians should also be aware that socioeconomic and racial factors may affect FA knowledge and should offer further support accordingly. 50 In family relationships, parental support and conflicts with independence were common in adolescents with FA and despite most participants having a good relationship with their parents, some felt their parents wanted to 'control their lives'. 25  in addition to more supportive peers and healthcare professionals listening to them without judgement. which may reduce bullying and stigma. 24,28,29 Adolescents feel peers could be more supportive with their allergic conditions, 12,13 and with increased peer acceptance and understanding, beliefs may change and shape attitudes towards FA, its impact and management. Ages of transition such as the move from primary to secondary school, and 12 of 15then the move to college or University would benefit from further research. These age groups as a focus are important as it is the age adolescents seek further independence and responsibility and increase control of managing their FA.

| CONCLUSION
Greater understanding from healthcare professionals about the importance of beliefs and how they relate to behaviour and the necessity for increased information in all areas, from schools, restaurants, and the wider community, is essential. In clinics, psychological support for families, FA management in adolescents seeking independence, and addressing misinformed or maladaptive beliefs is essential. Anxiety around FA must be addressed in children, adoles-