Eosinophilic esophagitis (EoE) is an increasingly common, chronic esophageal disease characterized by symptoms such as dysphagia, vomiting, and pain. Because of the unpleasant symptoms of EoE, its relation to food allergies, and its chronic nature, a number of studies and clinical reports have noted major effects on psychosocial aspects of life (1–5). Whereas presenting clinical and histological features of this population have been described extensively, measurements of the psychosocial features of patients with EoE, such as depression; anxiety; somatization; conduct problems; self-esteem; and emotional, behavioral and social adjustment have not been systematically addressed.
Qualitative studies have documented significant impact on quality of life in children with EoE, functional measures related to but distinct from psychosocial health (6,7). Limited aspects of psychological adjustment, including anxiety and depression (8) and emotional and behavioral difficulties (9), have been examined in pediatric patients with eosinophilic gastrointestinal diseases (EGIDs), a broad grouping of gastrointestinal diseases including EoE, eosinophilic gastroenteritis, and eosinophilic colitis. The spectrum and quantification of psychosocial problems of children with EoE have, however, not yet been fully described.
Children with chronic illness show increased levels of psychosocial problems in comparison with healthy children (10). A number of features contribute to the potential psychosocial effect of EoE (1). First, EoE is associated with symptoms involving chronic vomiting, dysphagia, or odynophagia that often lead to reluctance to eat or resistance to being fed, with resultant complications of inadequate weight gain and feeding dysfunction (2). To cope with EoE symptoms, children often develop compensatory behaviors such as prolonged chewing and avoidance of highly textured foods, behaviors, and symptoms that may contribute to psychosocial disturbances by limiting social contacts. Second, EoE management frequently involves significant dietary restrictions, repeat endoscopies, and, in some cases, gastrostomy tube (G-tube) feeding, each of which can affect psychosocial development. We hypothesized those children with EoE experience psychosocial dysfunction. The goals of this study were to identify and quantify psychosocial problems experienced by pediatric patients with EoE ranging in age from infancy through adolescence.
Study Design and Participants
A retrospective analysis was performed of the behavioral health assessments of children who underwent evaluation and treatment of EoE in the Gastrointestinal Eosinophilic Disease Program (GEDP) at Children's Hospital Colorado and National Jewish Health during an 18-month period (July 2008–December 2009). Medical records that included data on presentation, medical management, and psychosocial evaluations of patients cared for in the GEDP were reviewed and data were captured using a scoring system as defined below. Children with a confirmed diagnosis of EoE as defined by recently published guidelines (consistent symptoms, >15 eosinophils per high-power field, and other etiologies for esophagitis ruled out) were included (1). This study was approved by the Colorado multi-institutional review board and the National Jewish Health institutional review board (COMIRB 08–1208).
Behavioral Health Evaluation
Patients and their families evaluated in the GEDP were offered a 1-hour pediatric behavioral health assessment as a standard part of their clinical evaluation by either a psychologist (M.D.K., J.R.) or social worker (M.M.). All available family members participated in the assessment session, and parents’ concerns and the patient's self-reported concerns were elicited. Although self-report was naturally limited for the youngest patients, they were engaged to the extent possible and their behavior and interactions with family members were observed. All evaluations were performed in a similar fashion using open-ended clinical assessments that addressed patient and family members’ psychosocial functioning in 4 areas: EoE symptoms, including pain or physical discomfort, feeding, and eating or appetite difficulties; emotional coping and problem-solving skills regarding the practical demands of the medical and dietary management approaches; feelings of sadness or anxiety, social support, or social difficulties; and limitations on age-related activities imposed by the disease. As a part of the standard of care, any item noted above in these areas was documented in the behavioral health clinical note that was reviewed for this retrospective analysis.
Behavioral health clinicians’ reports were independently reviewed by extensively trained researchers (R.H., N.R.) and relevant information was recorded on standardized forms. Data were quantified using rating scales developed for quantifying psychosocial problems from medical record review (11). Ratings were made for the following behavioral domains: disease-related complaints, effect on activities of daily living, emotional symptoms, and global psychosocial adjustment. Interrater reliability was assessed for all scales. Ratings not in agreement were discussed (M.D.K., R.H., N.R.) and consensus scores were achieved.
- Pain/discomfort and feeding/appetite difficulties were rated on 3-point scales where ratings indicated no complaints, minimal/moderate and/or infrequent complaints, and severe and/or frequent complaints. Examples of symptoms and behaviors rated at each level for pain/discomfort or feeding/appetite difficulties described by the patient or parent as a present concern are presented in online supplemental Table A (http://links.lww.com/MPG/A232).
- Ability to function in 3 domains of daily living, sleep patterns, social functioning, and school functioning were rated on 3-point scales where ratings indicated no complaints, minimal/moderate and/or infrequent complaints, and severe and/or frequent complaints. Examples for each rating in each of these areas of functioning are described in online supplemental Table B (http://links.lww.com/MPG/A233). Sleep patterns and school functioning were rated specifically for EoE effect, whereas social functioning was rated for general manifestations. Social and school functioning were rated for children ages 5 years and older.
- Child depression and anxiety ratings were made using 5-point scales where ratings indicated no concerns; some concerns present but behavior in normal range; moderate concerns—behavior may indicate need for intervention; severe concerns, behavior in clinical range, and requires intervention; and preexisting mental health diagnoses or problems consistent with mental health diagnoses noted during behavioral health evaluation. Examples are provided for each rating in online supplemental Table C (http://links.lww.com/MPG/A234). Depression and anxiety were rated for children ages 5 and older.
- Global Psychosocial Adjustment (GPA) was rated from the behavioral health reports using a 10-point scale adapted from the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition Axis V 100-point Global Assessment of Functioning (GAF) scale used to describe individuals’ psychological, social, and occupational functioning on a hypothetical continuum of mental health (12). GAF, a hybrid of the Global Assessment Scale and the Children's Global Assessment Scale, is intended for clinical use in all ages (0–90 years) and has been useful in making assessments based on retrospective chart review (13). For our purposes, the original GAF scale anchor points were used; however, mental health impairments resulting from physical limitations were not excluded. Anchor points and guidelines for scoring GPA for different age groups were specified (M.D.K.), each assessment was reviewed independently by 2 researchers, and interrater reliability was calculated (14). Similar to the GAF, higher scores on this GPA scale indicated better functioning. Online supplemental Table D (http://links.lww.com/MPG/A235) presents the GPA scale anchor points and corresponding age-specific behavioral examples.
Data were examined for distributions and outliers. Data are presented as means with standard deviations (SD) where variables had continuous distributions, and as proportions for ordinal and categorical data. Intraclass correlations (ICC) were computed to assess interrater reliability for all rating scales. For descriptive purposes, continuous data were dichotomized (≥2 for 3-point scales and ≥3 for 5-point scales), and χ 2 analyses, with the Fisher exact test for small numbers, were performed. For continuous data, t tests were performed, and 1-way analysis of variance with Tukey post hoc testing was used to compare continuous data for age groups. All of the analyses were conducted using a significance level of P < 0.05. Given the exploratory nature of the study, no corrections were made for multiple tests. Statistical analyses were conducted using JMP version 8.0 (SAS Institute Inc, Cary, NC).
Clinical Characteristics of Study Participants
During the 18-month time period, 152 patients were evaluated in the GEDP who received a diagnosis of EoE; of these, 64 underwent psychosocial evaluation. Reasons for not undergoing psychosocial evaluation included scheduling conflicts, family refusal, or lack of insurance coverage for behavioral health assessments. Six children were excluded from feeding and appetite assessment because of lack of documentation in the medical record.
Subjects were predominately white and male (Table 1), closely reflecting presently published demographic data for patients with EoE (1). The mean age for all subjects was 7.1 years (SD 4.8). Ten subjects had feeding tubes (9 gastrostomy, 1 nasopharyngeal). Fifty-six subjects (88%) were being treated with dietary restrictions either for EoE or concomitant immunoglobulin E–mediated food allergy.
For the review of 64 evaluations, interrater reliability for ratings ranged from good to excellent: pain/discomfort and feeding/appetite issues (ICC = 0.91 and 0.96, respectively, P < 0.001), activities of daily living (ICC = 0.84–0.96, P < 0.001), child depression and anxiety (ICC = 0.89–0.95, P < 0.001), and GPA (ICC = 0.93, P < 0.001).
At the time of their evaluation, 56% of children reported EoE-related pain or discomfort (Table 2). Nine of these children (14%) experienced severe pain/discomfort (eg, severe abdominal pain, constant nausea; score of 3) and 27 (42%) experienced pain/discomfort to a lesser degree or less frequently (score of 2). No differences were observed in the pain/discomfort reports for subjects of different age groups.
Nearly half of the children (48%) reported feeding or appetite problems. Nine children (16%) had severe problems (eg, refusing all food; score of 3) and 19 (33%) had moderate problems (eg, slow eating, requiring a large amount of liquid to finish meals, decreased appetite; score of 2). Feeding problems occurred most frequently among the youngest children, ages 0 to 4 years. Six children, 5 of whom had feeding tubes, did not receive feeding/appetite ratings because of lack of documented detail for this variable (eg, reason for tube feeding, whether oral feeding permitted). For the 5 tube-fed children who received feeding/appetite ratings, 3 had severe eating disturbances and 2 had moderate problems.
Activities of Daily Living
Sleep was a common concern, with more than one-third of families reporting that children had sleep problems ranging from severe (rating of 3) in 12 subjects to moderate (rating of 2) in 9 (Table 2). Sleep problems were most commonly reported for the youngest children, but they occurred at all ages.
Social functioning problems occurred in the majority of children, with 9 children (23%) experiencing severe problems (rating of 3) such as having no age-appropriate friends, and 16 children (41%) reporting mild-to-moderate difficulties (rating of 2) such as problems making friends. School difficulties were reported in 26% of children older than 8 years, with severe problems in 5 children (13%).
Depression symptoms (ratings of 2–5 or more on a 5-point scale) in children 5 years and older (n = 39) were reported for 18 children (46%). For 7 of these patients (18%), depressive symptoms were mild or transient (ratings of 2) and described as episodes of sadness, for example, after being teased at school; however, for 11 (28%) of the patients, the depressed behavior was sufficiently concerning to merit clinical intervention (rated ≥3; Table 2). These included moderate symptoms (rating of 3), such as frequently appearing withdrawn or despondent, or severe symptoms (rating of 4 or 5), such as regular withdrawal, despondence, and expression of suicidal thoughts. Of those patients in the 8- to 12-year-old and 13- to 18-year-old groups who reported at least moderate depressive symptoms (n = 10), all experienced depression symptoms in the severe range. Among these patients, 3 had preexisting diagnoses of depression and already were receiving treatment.
Symptoms of anxiety (ratings of 2–5 or more on a 5-point scale) were reported for 20 of the 39 older children (51%). Four of the 20 children (10%) experienced mild anxiety symptoms (ratings of 2, eg, fears of medical procedures), whereas 16 children (41%) had symptoms meriting intervention (ratings ≥3 on a 5-point scale; Table 2). Nine children received ratings of 4 and 4 received ratings of 5, indicating that 13 children (33%) had severe anxiety that limited developmentally appropriate activities.
Global Psychosocial Adjustment
The mean score on the 10-point GPA scale was 6.9 ± 1.7. Older children and teenagers had significantly lower adjustment scores than younger subjects (Fig. 1). When taken as a whole, 44% of children experienced moderate-to-serious emotional or behavior problems (GPA ≤6), 16% had mild problems (GPA = 7), and the remaining 40% reported good psychosocial health (GPA ≥8). Supplemental Table D (http://links.lww.com/MPG/A235) provides examples of developmentally specific behavioral responses to having EoE, ranging on a continuum from well adjusted to problematic.
Disease Variables in Relation to Child Functioning
Reports of pain/discomfort were significantly associated with more sleep problems for children of all ages, and with more social and school functioning problems for children ages 5 and older (Table 3). Children with feeding/appetite problems were significantly more likely to have sleep problems and social difficulties. For the children with G-tubes, GPA scores were significantly lower than for children without G-tubes. Social functioning and school functioning were rated for children 5 years and older; social functioning was problematic for all children with G-tubes, and problems with school functioning were also significantly more common for these children than for those without G-tubes (P < 0.05). Of the 88% of children treated with diet restrictions, approximately one-third reported dysfunction in 4 of the domains (sleep, school, anxiety, and depression) and two-thirds reported social problems.
The goal of this study was to identify and measure previously unreported features of psychosocial dysfunction experienced by children affected by EoE in a tertiary care program. The majority of children had difficulties in at least one of the areas assessed (sleep, social, school, anxiety, and depression), with just less than half of children reporting these problems as moderate to severe in nature. Young children experienced more sleep disturbances, and children with G-tubes were more affected than those without in terms of global psychosocial adjustment.
Disease-related factors affecting children's adjustment to chronic illness include pain, impairments in physical functioning, and treatment burden (10,15–17). In our study, we found that symptoms of pain or discomfort were a concern for 56% of children with EoE, and concerns about children's food refusal or poor appetite were present for 48% of the sample. Considering the chronic nature of EoE, it is not surprising that we found a high rate of feeding problems in younger children and long-standing issues with decreased appetite in older children. Each of these domains forms a critical part of children's normal growth and development and impairment delays acquisition of age-appropriate eating skills, social functioning, and normal psychosocial health (2,4,18).
Children with EoE who experienced pain and eating problems had greater difficulties across multiple areas of psychological functioning. For instance, social interactions were especially affected, with 64% of children having difficulties in this area. Eating typically represents one of the most valued activities in a child's life because it occupies a significant amount of time and energy spent with family, friends, and schoolmates. Because EoE can lead to symptoms of vomiting, dysphagia, or food impactions or promote incapacitating coping behaviors such as long mealtimes or food limitations/avoidances, our findings are entirely reflective of how EoE can affect this domain of psychosocial functioning by interfering with children's motivation or comfort with peer interactions, family, and sporting activities.
Two studies have explored psychosocial aspects in children with EGID, a broad group of eosinophilic gastrointestinal disorders. Cortina et al evaluated health-related quality of life as well as anxiety and depressive symptoms in children and adolescents with EGID. Using teacher and parent reports and self-report in older children, patients were found to have increased internalizing and depressive symptoms compared with healthy controls. Patients did not have increased anxiety overall, but did have increased physical symptoms of anxiety (8). Taft et al recruited parents of children with EGID from an online interest group to assess caregiver stress in EGID. Parents reported increased emotional difficulty in their children with EGID compared with healthy controls (9). Consistent with these reports and findings for inflammatory bowel diseases and other chronic diseases (8,10,15,19–21), children with EoE in our study reported higher levels of emotional difficulties, including moderate levels of depressive feelings (28%) and anxiety (41%), findings often related to difficulties with the ingestion of food.
Besides the effect of symptoms on psychosocial health, chronically ill children can also experience problems related to prescribed treatments. Because of the social nature of eating, it was not surprising to find the high degree of problems reported in the sleep, school, anxiety, and depression domains in these children, almost all of whom were treated with diet restriction. This observation is consistent with studies examining psychosocial functioning in children with IgE-mediated food allergies who endure life-threatening consequences from dietary indiscretions (22). Consistent with this is the finding that children with G-tubes had significantly more psychosocial difficulties compared with those without a feeding device. In this small group of subjects, all experienced social difficulties, most had school problems, and as a group, they had poorer global psychosocial adjustment compared with others in the sample.
The effect of age and developmental level on psychological functioning among chronically ill children is essential to consider (23). By using a global psychosocial adjustment measure that was applicable for all ages, our study revealed differences in rates of overall adjustment and age-specific problems for each developmental stage. Psychosocial adjustment for children 0 to 4 years old focuses on somatic and emotional regulation, and indeed sleep disturbances and feeding problems predominated among the youngest group of children. Social difficulties became the predominant concern for children ages 5 years and older, whereas school difficulties and anxiety and depressive symptoms predominated among the older children and adolescents.
Although our study identified a number of psychosocial dysfunctions in children with EoE, results should be interpreted in light of several factors. Data were obtained only from children with EoE who underwent psychosocial evaluation; 88 other children with EoE underwent evaluation in the GEDP during this time but were excluded for reasons including insurance issues, lack of interest, and scheduling problems. Results from these excluded patients could have influenced the outcome of this study in a variety of ways. In addition, patients who were evaluated may have sought this because of self-identified psychosocial problems. Several patients in this study had other comorbid diseases including atopic dermatitis (41%) and asthma (48%), diseases that can affect psychosocial functioning; however, evaluation in this study focused on several areas targeted to EoE, such as feeding problems and pain, and the high rate of other atopic diseases in the study group is consistent with other observations in EoE. The retrospective nature of this study that recorded results from a clinical assessment record lacks the advantage of a standardized checklist; however, in this relatively new disease, this limitation is offset by the richness of the clinical information provided. Finally, this study emanates from a tertiary care program to which patients are often self-referred. These patients may have increased disease severity, a factor that could be associated with greater psychosocial dysfunction of children seen in a tertiary care program. Future prospective studies measuring similar features in children from a variety of different practice settings will be important to determine the overall breadth and depth of psychosocial dysfunction in children with EoE.
We have presented a qualitative and quantitative description of the large degree of psychosocial problems experienced by patients with EoE evaluated in a tertiary care program. We found that pediatric patients with EoE face disease- and treatment-related challenges that expose them to risk for psychosocial difficulties. Although not all children and adolescents with EoE develop psychosocial problems, our results suggest that children with EoE evaluated in a tertiary care program experience significant psychosocial dysfunction related to their disease and treatments. Some had serious issues requiring professional attention or moderate subclinical concerns. Our findings reinforce that behavioral health assessments of pediatric patients with EoE should occur across the entire age range, with consideration of developmentally specific concerns such as behavioral components of feeding disorders, the emotional effect for young children, and the nature of social limitations and emotional responses for older children. Investigations of how symptoms, treatment, and coping strategies affect the psychosocial health of patients, parents, and families will be critical to future care for pediatric patients with EoE.
We thank Jane Robinson, PhD, and Michael Miller, MEdS, LCSW, for their clinical work with pediatric patients with EoE; Nathan Riechers for reviewing and rating records; and Eleni Maria Weisnicht for assistance with manuscript preparation.
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