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Original Article: Gastroenterology: Celiac Disease

Health-related Quality of Life in Newly Diagnosed Pediatric Patients With Celiac Disease

Shull, Mary H.∗,‡; Ediger, Tracy R.; Hill, Ivor D.; Schroedl, Rose L.

Author Information
Journal of Pediatric Gastroenterology and Nutrition: December 2019 - Volume 69 - Issue 6 - p 690-695
doi: 10.1097/MPG.0000000000002465

Abstract

What Is Known/What Is New

What Is Known

  • Celiac disease is a common chronic condition associated with a broad range of physical and psychosocial problems.
  • Health-related quality of life describes a patient's perception of the way that his or her illness affects all domains of functioning, and the PedsQL is one of the most widely used, well-validated pediatric measures of health-related quality of life.

What Is New

  • Pediatric patients with newly diagnosed celiac disease reported lower health-related quality of life compared to healthy children and similar health-related quality of life as children with nonceliac gastrointestinal complaints.
  • School functioning is especially impaired at diagnosis of celiac disease, and many patients may benefit from early interventions such as a Section 504 plan.

There is increasing focus on patient-reported outcomes and health-related quality of life (HRQOL) in children with chronic illnesses. Celiac disease (CD) affects approximately 1% of children worldwide (1–3) and is a chronic gastrointestinal (GI) condition with many extraintestinal manifestations, including poorly understood neuropsychiatric symptoms such as irritability, behavioral problems, anxiety, depression, and fatigue (1,4). There is limited research on HRQOL in pediatric patients with newly diagnosed CD, when these symptoms may be most predominant.

The World Health Organization defines quality of life as a person's perception of his or her position in life within the context of societal culture and in relation to his or her own goals and expectations (5). HRQOL more specifically describes one's perception of the influence that illness has on one's physical and emotional health, as well as psychological and social functioning; HRQOL also incorporates one's perceived ability to participate in activities, and satisfaction with that level of involvement (6). More than just absence of disease, it is complex to quantitatively measure, as it is affected by many different factors and each patient's perceived disease burden is highly variable.

The PedsQL 4.0 Generic Core Module has been used to study HRQOL in both healthy children and those with a variety of chronic pediatric GI diseases (7–17). Reported use of PedsQL in pediatric patients with CD is, however, rare, and no study has used PedsQL at diagnosis. This study seeks to employ this widely used and well-validated measure of HRQOL in a large, more homogeneous sample of children newly diagnosed with CD to characterize their HRQOL and compare it to that of healthy youth and those with nonceliac GI conditions.

METHODS

Procedure

This study combined data collected from 2 studies in which the PedsQL 4.0 Generic Core Scales was administered. The PedsQL parent report was given to all caregivers, and children aged 8 to 18 years also completed the self-report. Depending on the study, PedsQL was administered at either the time of diagnostic esophagogastroduodenoscopy (sample 1, N = 60) or before their initial clinic visit with a registered dietitian to learn about the gluten-free diet (GFD), usually within a few weeks of diagnosis (sample 2, N = 99). The total sample consists of 159 patients between the ages of 21 months and 18 years. Patients were included when newly diagnosed with CD based on elevated serological markers and confirmatory duodenal biopsies showing modified Marsh 3 or 4 changes (see Supplemental Digital Content, https://links.lww.com/MPG/B703). All were eating a regular diet or had been restricting gluten for <6 weeks at time of study recruitment. Some patients from sample 2 had attempted to reduce gluten from their diet before their dietitian visit and were excluded if they had done so for >6 weeks to minimize recall bias. Families were asked to fill out questionnaires as they would on the last day the child ate a gluten-containing diet. Demographic and relevant medical variables were obtained from chart review, including symptoms before diagnosis, family history of CD, most common comorbidities, and Marsh scores at diagnosis (see Supplemental Digital Content, https://links.lww.com/MPG/B703).

Data for sample 1 were collected from January 2015 to September 2016, as part of a study evaluating the role of serological tests in the diagnosis of CD. Data for sample 2 were collected from June 2016 to November 2017 as part of a study focusing on the psychosocial and cognitive functioning of pediatric patients with newly diagnosed CD.

The study was approved by the Institutional Review Board at Nationwide Children's Hospital. Informed consent and assent (when aged 8 years and older) from subjects was obtained.

Measures

The Pediatric Quality of Life Inventory 4.0, Generic Core Scales is a brief 23-item measure, which assesses 4 core domains of HRQOL: physical, emotional, social, and school functioning. It is available as a self-reported measure and as a parent report version. Both generally take fewer than 5 minutes to complete. Different age-appropriate self-report versions are available for the 5 to 7, 8 to 12, and 13 to 18 year age groups; parent proxy reports are similarly different for each age group (2–4, 5–7, 8–12, and 13–18 years). Responses are based on a Likert-type scale and assess the level of impairment in each domain over the past month. Higher scores indicate higher HRQOL. Total score is calculated by summing all 4 domains of functioning, and the measure provides 2 summary scores: the Physical Health Summary Score (based on the physical functioning subscale) and the Psychosocial Health Summary Score (calculated using the Emotional, Social, and School Functioning Subscales) (18). The PedsQL has strong psychometric properties, including reliability, factor structure (19), and construct validity across disease populations, including GI disorders.

Comparison Samples

Means and standard deviations for both healthy and nonceliac GI samples were obtained from Varni et al's (7) large-scale study comparing self- and parent-reported scores on the PedsQL across a variety of disease populations, and 9566 healthy children recruited either from well-child checks in their physicians’ offices or through a State Children's Health Insurance Program evaluation. The nonceliac GI conditions sample from this study included 287 total children with irritable bowel syndrome (42.9%), functional abdominal pain (28.6%), and organic GI disorders (28.6%) recruited from gastroenterology clinics (7).

Statistical Analysis

Comparison of Celiac Disease Sample With Nonceliac Gastrointestinal Sample and Healthy Sample

Mean parent-report and self-report PedsQL summary and subscale scores were calculated for the CD sample and compared to means from the sample with other nonceliac GI conditions, as well as to a healthy sample (7) using one-sample t-tests. To account for multiple comparisons a Bonferroni-corrected P value was applied for the 1-sample t tests, such that statistical significance for these comparisons was set at P < 0.008.

Respondent and Gender Differences in CD Sample

Multivariate analysis of variance was conducted to investigate differences between parent- and self-report mean summary and subscale scores. The role of sex on parent-reported and self-reported summary and subscale scores was also evaluated using multivariate analysis of variance.

RESULTS

Sample

The total sample included 159 patients between the ages of 21 months and 18 years. The demographic variables for the 2 samples which comprise the final data set are included in supplemental digital content (https://links.lww.com/MPG/B703). Independent sample t tests and Chi-square analyses were conducted comparing the 2 samples on demographic variables. No significant difference was found between samples 1 and 2 on any demographic variables or PedsQL summary or subscale scores (P < 0.008).

Comparisons Within the Celiac Disease Sample

No differences were found between parent and patient responses for total and all subscale scores on the PedsQL for the patients with CD (Table 1).

T1
TABLE 1:
Means and standard deviations (in parentheses), medians, and ranges of parent- and self-report PedsQL summary and subscales scores for the celiac disease sample

Significant differences were found on mean subscale scores for parent-reported Social Functioning (F[1, 142] = 6.16, P < 0.01), with parents rating male patients as having lower social functioning (M[standard deviation (SD)] = 77.4[19.21]) compared to female patients (M[SD] = 86.10[16.5]). No differences were found between boys and girls on self-reported PedsQL summary and subscale scores (Table 2).

T2
TABLE 2:
Means and standard deviations (in parentheses), medians, and ranges of self-report PedsQL summary and subscales scores by sex and comparison sample

Rates of Clinically Significant PedsQL Scores in Celiac Disease Patients

Parent-reported PedsQL mean subscale scores were coded as clinically significant based on cut-off scores derived by Huang et al (20). Within the CD sample, 62.7% had scores in the clinically significant range for Physical Health, whereas 54.4% reported significant scores for Emotional Functioning, 43.7% had significant Social Functioning scores, 55.9% reported significant School Functioning scores, and 49% of subjects had scores in the significant range for Total Scores.

Comparison of Celiac Disease Sample With a Healthy Sample

Parent-reported summary and subscale PedsQL scores for the CD sample were significantly lower for Total Score (t[156] = −4.73, P < 0.008), Physical Health (t[156] = −3.82, P < 0.008), Psychosocial Health (t[142] = −4.19, P < 0.008), Emotional Functioning (t[156] = −4.67, P < 0.008), and School Functioning (t[141] = −4.83, P < 0.008) when compared to a healthy sample. No difference was found between the CD and healthy groups on parent-reported Social Functioning (t[156] = −0.42, P > 0.05, Table 3).

T3
TABLE 3:
Means and standard deviations (in parentheses), medians, and ranges of parent-report PedsQL summary and subscales scores by sex and comparison samples

A similar pattern of results was found when comparing self-reported PedQL summary and subscales scores between the CD sample and the healthy sample. The CD sample had significantly lower self-reported Total Score (t[103] = −5.69, P < 0.008), Physical Health (t[103] = −5.22, P < 0.008), Psychosocial Health (t[103] = −4.96, P < 0.008), Emotional Functioning (t[103] = −3.98, P < 0.008), and School Functioning (t[101] = −7.43, P < 0.008) scores. No difference was found between the CD and healthy samples on self-reported Social Functioning (t[103] = −0.65, P > 0.05, Table 2).

Comparison of Celiac Disease Sample With a Nonceliac Gastrointestinal Sample

Comparison of parent-reported PedsQL scores for the CD and nonceliac GI samples revealed differences on parent-reported Psychosocial Health (t[141] = 3.02, P < 0.008) and Emotional Functioning (t[156] = 4.59, P < 0.008), with the CD sample reporting higher scores than the nonceliac GI sample. No differences were found between the CD and nonceliac GI groups on parent-reported Total Score (t[156] = 2.63, P > 0.01), Physical Health (t[157] = 1.10, P > 0.05), Social Functioning (t[156] = 1.81, P > 0.05), and School Functioning (t[141] = 0.89, P > 0.05).

No differences were found between the CD and nonceliac GI groups on self-reported Total Score (t[103] = −1.42, P > 0.05), Physical Health (t[103] = −0.90, P > 0.05), Psychosocial functioning (t[103] = −1.81, P > 0.05), Emotional Functioning (t[103] = −1.41, P > 0.05), Social Functioning (t[103] = −0.21, P > 0.05), and School Functioning (t[101] = −1.89, P > 0.05, Table 2).

DISCUSSION

Children with newly diagnosed CD had lower HRQOL scores on the PedsQL compared to healthy children on both self- and parent report. On self-report, children with newly diagnosed CD had similar HRQOL as that of a nonceliac GI sample. Lower reported HRQOL in the domain of physical health would be expected, given that the patients with CD were newly diagnosed and usually symptomatic, as they had not yet started treatment. In fact, 62.7% of our sample reported significant impairment in physical functioning, more than half of patients had significantly lower emotional functioning, and approximately half had significant impairment in social functioning. Many parents and patients report difficulty concentrating, irritability, and feelings of sadness, worry, or anger in youth with untreated CD, and although the current literature is inconsistent there does appear to be an association between anxiety, depression, and fatigue with CD (4). This study shows that school functioning is also affected by untreated CD, with more than half of the patients experiencing significant impairment in school performance, such as missing school or being unable to concentrate or keep up with schoolwork.

To our knowledge, no previous pediatric studies have assessed HRQOL with the PedsQL in children with newly diagnosed CD. However, our results are consistent with previous studies using other measures of HRQOL in such children which also found decreased HRQOL at diagnosis when compared to healthy children (21,22). The existing studies of HRQOL in pediatric CD mainly focus on patients years after diagnosis and do not adequately control for time since diagnosis or other variables, such as adherence, which may affect HRQOL. Few address a more homogenous sample of newly diagnosed patients who have not yet started the GFD, and few use as well-validated measures as the PedsQL, which is frequently used in other chronic illnesses. Of the studies reporting use of the PedsQL in CD, children with previously diagnosed CD had lower total and subscale scores on the PedsQL compared to healthy controls (23). A larger Canadian study included PedsQL with other measures of HRQOL (Celiac Disease DUX and CD Quality of Life Scale-KINDL) in children who had been diagnosed with CD an average of 2.3 years (24). This indicated that children with CD on the GFD had HRQOL that was similar to a healthy reference population and significantly higher than patients with mild GI complaints and negative celiac serology and biopsies. Few studies follow HRQOL over time after diagnosis and initiation of treatment with GFD, but 2 pediatric studies (22,25) and several adult studies (26–28) suggest that HRQOL improves with time on the GFD and resolution of symptoms. Although the current study only addresses the decrease in HRQOL found at diagnosis, it seems likely, based on the literature, that HRQOL will improve with initiation of the GFD. The GFD is, however, burdensome, costly, and can be socially isolating, which may decrease HRQOL. This study establishes an important baseline for HRQOL in newly diagnosed pediatric patients with CD, which can be further studied with repeated PedsQL administration after initiating treatment.

Overall, the patients with CD in this study had similar social functioning subscale scores as healthy children and children with nonceliac GI conditions for both parent- and self-report. There was, however, a sex difference in parental perceptions of social functioning, with parents of newly diagnosed male patients with CD reporting significantly lower social functioning compared to females. There was no significant difference between boys and girls on weight, height, and body mass index percentile and z scores in this study, but both groups had small stature and low weight with boys having mean height z score −0.34(SD 1.2), weight z score −0.12(SD 1.3), and body mass index z score −0.1(SD 1.3). One study examining the effect of short stature on children found that girls with short-stature have more adaptive psychosocial functioning than boys (29). Perhaps boys with CD are more bothered by their smaller stature leading to peer rejection and neglect, with inability to keep up with peers in physical activity, or perhaps it is only parental perception. In a large study examining the effect of growth hormone use on HRQOL in children with chronic kidney disease using PedsQL, there was a significant association between catch up growth on parent-proxy reports of both child physical and social functioning (30). The lower social functioning in male patients with CD may be temporal and improve with initiation of the GFD, resolution of symptoms, and catch-up growth, but other sex differences may develop with time. This emphasizes the potential importance of assessing HRQOL in all patients at diagnosis and following HRQOL longitudinally, preferably using both parent- and self-report when possible.

There was no self-reported sex difference in social functioning in the patients with CD. Although this study found no difference in parent- and self-report for the patients with CD on any other subscales or total score, this degree of concordance is unusual. This may be because most children with CD included in this study are symptomatic and frequently discussing their symptoms and functioning with their parents around the time of diagnosis. It is well-known in the HRQOL literature that parents often report lower HRQOL in their children than the children themselves report, referred to as the “proxy problem” (31–33). A Swedish study of HRQOL of pediatric patients with previously diagnosed CD noted that parents reported lower HRQOL for the children than the children themselves did (25). Another large study using the PedsQL in diabetic youth found that parents frequently underestimate their children's HRQOL except in the youngest children (34). In our study, on parent report the patients with CD had lower total score, psychosocial health, and emotional functioning when compared to the historic patient with nonceliac GI conditions; these changes were not noted on self-report and this is likely an example of the parent-proxy effect. Parents’ answers may be influenced by their varying degrees of involvement in their children's lives and the parents’ own quality of life; in very young children or children with significant cognitive impairment; however, the parental report is all that is available. Children may be the best reporters of their own emotions and social interactions or may lack insight into areas of difficulty. Ultimately, both parents and children are assessing the HRQOL of the child assimilating different information; thus, both perspectives are valuable and should be obtained when possible.

Given the high rates of decreased school, emotional, and physical functioning found in newly diagnosed patients with CD, we recommend assessing HRQOL in patients at diagnosis to establish a baseline and intervene early when necessary. Meeting with a psychologist or social worker may help promote coping and adjustment. Establishing a Section 504 plan ensures appropriate accommodations at school for children in the United States, and The Celiac Disease Foundation has a sample 504 plan for patients with CD which can be downloaded at www.celiac.org(35); similar accommodations should be made for children with CD in other countries. Providing thorough education about the GFD and access to CD support groups in person or online may help make patients feel less overwhelmed and streamline initiation of the GFD. It is important to consider the far-reaching implications of CD at diagnosis, as further interventions may help those patients who do have clinically significant abnormal scores in different domains of HRQOL.

Limitations of this study include the use of published means for the healthy and nonceliac GI populations instead of a concurrently collected control group. Therefore, the cohorts cannot be matched on demographic variables, and thus increasing the risk of systematic error in the statistical analysis. In addition, we do not have information about when the historic patients with nonceliac GI diagnoses filled out the questionnaires in relation to diagnosis. Given the large size and heterogeneity of the healthy and nonceliac GI comparison populations, this comparison, however, provides valuable initial information on HRQOL of newly diagnosed pediatric CD patients. Several previous studies have used similar methods in comparing published means for healthy patients on the PedsQL in patients with inflammatory bowel disease (12) and cyclic vomiting syndrome (8). Finally, we chose to use the PedQL 4.0 Generic Core Scales as it is a frequently used, reliable, and well-validated tool for studying HRQOL, but use of a more disease-specific measure such as the Celiac Disease DUX (36) for newly diagnosed patients may provide additional information.

In conclusion, this study is, to our knowledge, the first to assess HRQOL with the PedsQL in a large pediatric population with newly diagnosed CD. Similar to the few previous studies using other measures of HRQOL, compared to healthy children the children with CD had lower total HRQOL, and physical, emotional, and school scores on both the parent- and self-report versions. On self-report the children with newly diagnosed CD had similar HRQOL compared to children with other, nonceliac GI conditions, with higher emotional functioning scores in the patients with CD as reported by their parents. A novel finding was that parents reported boys with newly diagnosed CD had lower social functioning than the girls, whereas this difference was not seen on self-report. It may be helpful to routinely assess HRQOL using the PedsQL in every patient at CD diagnosis, optimally with both self-report and parent-proxy. Some patients may benefit from additional support at diagnosis, and screening all newly diagnosed patients may identify those at highest risk for targeting interventions. It is important to continue further research regarding HRQOL to improve patient outcomes.

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Keywords:

gluten-free diet; health-related quality of life; pediatric celiac disease; PedsQL

Supplemental Digital Content

Copyright © 2019 by European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition