Introduction

Asthma and eczema are common childhood diseases, but little is known about how they affect children’s social and mental well-being in school. Studies which report increased levels of anxiety, depression, attention-deficit/hyperactivity disorder (ADHD), and behavioural problems in children with asthma [1–6] and eczema [7–10] have used mainly maternal reports of child mental well-being. Relatively little is known about the well-being of children with asthma or eczema in the school environment. Few studies have utilised teacher reports of child mental well-being; in a large UK study of children and adolescents, those with asthma had more teacher-reported emotional, peer, conduct and hyperactive problems than those without asthma [11]. However, in a Dutch case control study, children with asthma were rated by their teachers as being happier at school than children without asthma [12].

Both conditions have symptoms that can be noticeable to others, necessitate the use of medications, and result in school absence [13, 14]; thereby marking affected children as ‘different’ and potentially affecting their peer relationships. Bullying is common in childhood and has three key characteristics; repetition over time, harm, and unequal power. It can take many forms: physical (e.g. kicking); behavioural (e.g. being mean); verbal (e.g. derogatory remarks); or relational (e.g. disrupting social relationships between victim and peers) [15]. Children with chronic health conditions are known to be at increased risk of being a victim [15, 16], but there has been little research focused on asthma or eczema [17].

The few studies which have specifically considered whether asthma or eczema affect a child’s social well-being at school have had mixed results. In one Scandinavian study, parents reported that children with asthma, but not those with eczema, were more likely to be bullied [18]. However, in another Scandinavian study with child-reported measures, eczema was associated with being bullied in adolescent boys, but this association was not observed for girls, or for asthma for boys or girls [19]. In small studies from the UK and China, most children with eczema reported that their condition had a negative impact on their quality of life (due to itching, scratching and sleep disturbance), but only a minority reported that it made them feel embarrassed, affected their friendships, or caused them to be teased or bullied [20, 21]. In qualitative studies, bullying was frequently mentioned by 6–12 year old children with asthma [22], and patients with eczema reported being called names such as ‘leper’, peers thinking they were contagious, being made to feel like ‘a total freak’, and being socially excluded [23].

In this current study, we use data from a population-based birth cohort to examine the social and mental well-being at school of eight-year-old children with rash or wheeze. Our aims were to determine whether rash or wheeze were associated with (1) child reports of being bullied, left out, or unhappy at school and (2) teacher-reported child internalising (i.e. anxious and depressive) or externalising (i.e. oppositional and hyperactive) behaviours. We also considered whether child sleep or maternal mental health explained any of the association between child rash or wheeze and the teacher-reported mental well-being outcomes; it has previously been reported that adjustment for these factors attenuated associations between child rash and wheeze and maternally-reported child mental well-being [24].

Methods

Results

Sample characteristics

Rash and wheeze were common symptoms at school age, and were more likely to be persistent (i.e. symptoms started in infancy or preschool) than late onset (i.e. started for the first time at school-age) (Table 1). Almost 80% of the children reported being happy at school always or most of the time (Table 1). However, almost 10% reported frequently being left out or bullied.

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Table 1. Study population characteristics.

https://doi.org/10.1371/journal.pone.0135271.t001

Correlates of both high internalising and externalising scores were being male, being younger, family financial difficulties, living in a rented council home, and maternal anxiety and depression (S3 Table). Similarly, boys, children from lower SEP families, and those whose mothers reported more depressive or anxious feelings, tended to self-report less favourably on their well-being at school (S3 Table). The child-reported and teacher-reported measures of well-being were associated; children who reported being bullied, left out, or unhappy at school were more likely to have a high teacher-reported internalising and externalising score (S4 Table).

Association between rash, wheeze and child-reported outcomes

Children with persistent wheeze were more likely to report being left out at school than children who had never had wheeze [10.8% (95% CI 8.8%-12.8%) compared to 7.3% (6.5%-8.2%)], and more likely to report that they were never or only sometimes happy at school [23.4% (20.6% to 26.1%) compared to 19.4% (18.1% to 20.8%)]. Adjustment for measures of SEP attenuated these differences, but did not fully account for the greater likelihood of being left out (Table 2). Being bullied quite a lot or all the time was reported by 9.1% (7.9% to 10.3%) of children with persistent rash and 10.3% (7.4% to 13.2%) of children with late onset rash, compared to 7.4% (6.1% to 8.6%) of those with no rash at any age. These differences were not explained by SEP (Table 2).

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Table 2. Association between child rash and wheeze and child-reported outcomes.

https://doi.org/10.1371/journal.pone.0135271.t002

Association between rash, wheeze and teacher-reported outcomes

Child wheeze symptoms were not associated with teacher-reported internalising or externalising behaviours (Table 3). For rash, children with late onset symptoms were the most likely to have a high teacher-reported externalising (10.7%, 6.9% to 14.5%) and internalising (10.0%, 6.6% to 13.4%) score, and those who had never had symptoms were the least likely to have a high score [externalising (8.5%, 95% CI 6.9% to 10.1%); internalising (6.7%, 5.3% to 8.1%)]. After adjustment for SEP and wheeze status, late onset rash remained associated with a high internalising score (Table 3). For the externalising outcome, the odds of having a high score increased for the persistent rash group relative to the never rash group after adjustment for SEP and wheeze status (Table 3). Odds ratios were highest for the late onset group but confidence intervals were wide.

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Table 3. Association between child rash and wheeze and teacher-reported outcomes.

https://doi.org/10.1371/journal.pone.0135271.t003

The association between late onset rash and high internalising score was slightly attenuated by further adjustment for child sleep (OR1.56, 95% CI 0.99 to 2.48), or maternal anxiety and depression (1.56, 0.98 to 2.47), or both child sleep and maternal anxiety and depression (1.52, 0.96–2.42). The association between persistent rash and high externalising score was unaffected by adjustment for child sleep (1.36, 1.01–1.83) but was attenuated by adjustment for maternal anxiety and depression (1.32, 0.98–1.78).

Discussion

Children with rash were more likely to report being bullied, and those with wheeze to report being left out, at the age of 8 years in our population-based cohort. However, the vast majority of children with rash or wheeze reported positively on their school life. Children with rash, but not with wheeze, had more internalising and externalising teacher-reported behaviours.

Persistent wheeze was associated with feeling left out at school in our study. Being left out can be a type of relational bullying [15]. However, the children may have felt left out due to their condition preventing them from participating in activities, or causing school absence, rather than as a result of bullying. Either way, our results suggest children with persistent wheeze have more difficulties forming friendships at school. This is consistent with previous studies that have identified parent-reported [31, 32] and child-reported [22, 33, 34] friendship difficulties in children with asthma; not being able to play with friends, not having a group of friends to hang around with, feeling isolated and lonely, and being left out of social activities. There is a paucity of research on bullying in children with asthma, and results have been mixed. Bullying was frequently mentioned by 6–12 year old children with asthma in a qualitative study [22], however in a large cohort study there was no association between asthma and child-reported bullying at the age of 15 years [19]. Two cohort studies did report an increased risk of being bullied in children with asthma, but they used parent-reported measures of bullying and included a wide age range from infancy to 17 years [1, 18].

Children with rash at school age in our study reported an increased risk of being bullied. Although bullying is frequently appearance related, there has been little previous research on bullying in children or adolescents affected by skin disease [17]. In a large Norwegian school-based study of 15 year olds, boys who reported being bullied were more likely to have eczema than boys who were not bullied, but the prevalence of bullying was not reported and no association was observed for girls [19]. Three small studies which used the Children’s Dermatology Life Quality Index did report the prevalence of teasing, bullying and friendship problems due to eczema but had no controls with which to compare the prevalence rates: less than 10% of 43 children aged 5–10 years in Hong Kong said their eczema caused them to be bullied, or affected friendships, ‘very much or a lot’ [21]. Of 78 children aged 6–11 years in London and Wales, 17% reported being teased or bullied and 15% that it affected friendships [20]. Proportions were higher in a US study of 178 children aged 5–15 years, but this is likely due to ‘a little affected’ being combined with ‘very much or a lot’ in this study; 30% reported that their eczema affected friendships and 50% that it caused them to be teased or bullied [35].

Taken together, results from the previous studies are generally in concordance with ours; having eczema or asthma symptoms can increase the likelihood of a child being bullied or left out at school, but most of the children affected by these conditions are not bullied and do not have friendship problems at school. While this is a positive finding, the children in our sample were only eight years old, and it is known that most types of bullying increase with age [15].

We were able to investigate teacher-reported measures of child mental well-being. Child rash, particularly persistent rash, was associated with an increased likelihood of having a high externalising score. Late onset rash was associated with a high internalising score. In a previous study using ALSPAC data, children with rash were more likely to have a high maternal-reported internalising and externalising score [24]; this concordance suggests the behaviour of children with rash is affected in both their home and school life. We found no association between child wheeze and teacher-reported mental well-being, whereas the previous ALSPAC study found persistent wheeze to be associated with both maternal-reported internalising and externalising outcomes [24]. This could mean wheeze has a greater impact on a child’s behaviour at home than at school. However, in a large UK study, children aged 5–15 years with asthma, particularly those in poor health, had more teacher-reported internalising and externalising problems, than their healthy peers [11]. Our discordant findings could be due to maternal reporting bias, or to teachers not noticing or interpreting a child’s behaviour in the same way as the mothers.

Adjustment for maternal anxiety and depression attenuated associations between persistent rash and externalising problems, and late onset rash and internalising problems. This concurs with the previous ALSPAC study which found maternal anxiety and depression accounted for the association between child rash and maternal-reported internalising symptoms and partly for externalising symptoms [24] and previous studies which found children with eczema and asthma are more likely to have a mother with anxiety or depression compared with healthy children [36–39].

Despite sleep quality being considered a key factor in the association between eczema, asthma and behavioural problems in children [8, 9, 40, 41], it only explained some of the association between late onset rash and teacher-reported internalising problems, and did not alter the association between persistent rash and externalising problems. However, child sleep quality was measured at age 6 years 9 months and may not reflect sleep quality at the outcome time point, particularly if rash or wheeze symptoms changed after sleep quality was measured. Although rash and wheeze are likely to represent eczema and asthma in school-aged children, these symptoms are less specific in younger children and so not all reported rash and wheeze will have been due to eczema or asthma. We also had no measure of disease severity. Our child and teacher reported outcomes measured two different aspects of child well-being at school. As both were measured at the same point in time (child aged 8), it was not possible to examine how one influenced the other (i.e. did bullying result in a change in behaviour, or vice versa). Additionally, the children in our sample were at primary school in the late 1990s and early 2000s; school policies on bullying and child well-being may have changed over time. Further research on how the relationship between rash and wheeze and school well-being changes with age could help determine if there is a high-risk period, or identify the most appropriate age for interventions to prevent the initiation of chronic-disease related bullying.

Few previous studies on the well-being of children with asthma or eczema have included child or teacher reports. We have shown that having rash or wheeze can adversely affect a child’s social and mental well-being at primary school. The children in our sample were relatively young compared to many previous studies; our results thus signal the importance of recognising that these chronic conditions have social and behavioural comorbidities even at this young age. Furthermore, they suggest that any intervention, such as additional support at school or education of peers, should begin early.

Supporting Information

Acknowledgments

We are grateful to all the families who took part in this study, the midwives for their help in recruiting them, and the ALSPAC team, which includes interviewers, computer and laboratory technicians, clerical workers, research scientists, volunteers, managers, receptionists, and nurses.