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. Author manuscript; available in PMC: 2025 Sep 4.
Published in final edited form as: Child Health Care. 2023 Sep 21;54(3):296–310. doi: 10.1080/02739615.2023.2259291

Associations between executive functioning and adherence in pediatric celiac disease

Maegan D Sady 1, Shayna S Coburn 2,3, Zachary Kramer 2, Randi Streisand 2,3, Ilana Kahn 2,3
PMCID: PMC12396579  NIHMSID: NIHMS1932371  PMID: 40893587

Abstract

A strict gluten-free diet is the only treatment for celiac disease (CD), yet dietary adherence can be challenging for youth and may be impacted by the youth’s executive functioning and attentional abilities. This study aimed to investigate whether attention and executive functioning (EF) were associated with dietary adherence in children with CD. Parents of 34 children (child age M(SD)=13.01(3.88), 56% female) from a multidisciplinary CD clinic completed ratings of attention and EF and dietary adherence. Parent-reported adherence was negatively correlated with behavioral regulation (r = −.52, p < .01, r2 = .27, 95% confidence interval (CI) [−.73, −.22]) and cognitive regulation (r = −.48, p < .01, r2 = .23, 95% CI [−.71, −.17]), with an interaction by age (p = .01, adjusted R2 = .35, B = −0.15, 95% CI [−0.29, −0.07]) for behavior regulation. Youth who were rated as less adherent by their parents were rated as having more problems with behavioral (e.g., inhibition and self-monitoring) and cognitive regulation (e.g., planning, organization), and adolescents with lower parent-rated adherence were rated as having more problems with behavioral regulation in particular. Executive functioning deficits are an important treatment consideration for CD, particularly during adolescence.

Keywords: celiac disease, adherence, executive functioning, attention, ADHD

Introduction

Recent research has identified high rates of extra-intestinal symptoms among children with celiac disease (CD) (Jericho & Guandalini, 2018), such as elevated rates of neurological (Jackson et al., 2012) and psychological comorbidities (Coburn et al., 2020; Coburn et al., 2019) compared to the general population. Comorbidity of CD with attention-deficit/hyperactivity disorder (ADHD) has received particular attention in CD research, with compelling evidence for a relatively high rate of co-occurrence reported in both ADHD (Niederhofer & Pittschieler, 2006) and CD clinic samples (Coburn et al., 2020; Coburn et al., 2019; Niederhofer & Pittschieler, 2006) though not universally. A recent meta-analysis indicated that the rate of ADHD diagnosis in CD patients is significantly higher than in the general population (odds ratio = 1.39; Clappison et al., 2020).

Recent research priorities for CD have emphasized the need to investigate cognitive and behavioral difficulties in relation to CD in children (Coburn et al., 2019), and this is particularly crucial for the possible role of ADHD-related symptoms in the ability to manage CD effectively. Cognitive and behavioral difficulties in ADHD are characterized by deficits in executive functioning (EF), a range of skills including working memory, inhibition, planning, and organization, that allow goal-oriented problem-solving (Gioia et al., 2002).

In CD, a strict gluten-free diet (GFD) is the only available treatment. Individuals with CD may experience intestinal injury from ingesting just 50mg (1/100th of a teaspoon) of gluten, and sometimes less, per day (Catassi et al., 2007). Short of repeat biopsies which are invasive, expensive, and time-consuming, there is no “gold standard” for tracking GFD adherence (Ludvigsson et al., 2018). Expert assessment has been reliable in detecting recent and potential risk for gluten exposure in individuals with CD and relies on a standardized rating scale incorporating available medical data, symptoms, dietary recall, and potential barriers and facilitators (Leffler et al., 2009). Research in adults has found some relation of better adherence with greater length of time since diagnosis, and the relationship of adherence to demographic factors (such as gender) have seen mixed results in adults (Hall et al., 2009); these relationships have not been studied extensively in children with CD.

GFD adherence is cognitively burdensome and may be vulnerable to symptoms of impulsivity, distractibility, and/or other impairments in executive functioning (EF) (Leffler et al., 2008, 2009). As seen in other illnesses, individuals with poor EF skills may be less able to manage their condition due to a “double deficit” of higher demands for self-care and lower executive functioning skills (Tarazi et al., 2007). This association has been studied preliminarily in children with diabetes, but the association between EF and disease management has been seen in other pediatric chronic illnesses, including cystic fibrosis and obesity (Borschuk et al., 2020; Lindblad et al., 2017; Macek et al., 2019; Vinker-Shuster et al., 2019; Yang et al., 2018). It follows that similar difficulties may arise in youth with co-occurring CD and ADHD/EF weaknesses with regard to GFD adherence. This risk may be particularly apparent during adolescence, a developmentally normative stage of transition from parental monitoring to more self-management. Adolescents with CD tend to have poorer GFD adherence and are more likely to engage in purposeful ingestion of gluten compared to younger children (Czaja-Bulsa & Bulsa, 2018).

Therefore, the primary objective of this study was to investigate the extent to which ADHD-related symptoms (including EF skills) were associated with poorer GFD adherence in children with CD. We hypothesized that (1) participants with greater ADHD-related symptoms would have poorer concurrent adherence to the GFD compared to children with lower ADHD-related symptoms, and (2) that this might be more apparent in adolescence given increased demands for self-management. Several variables of interest were also explored as predictors, including months since diagnosis and participant gender.

Materials and Methods

Participants

Participants were children with CD and their parents who attended a multidisciplinary CD clinic at a mid-Atlantic children’s hospital between January 2018 and August 2019. The multidisciplinary clinic was offered to all patients diagnosed with CD at this hospital as an enhanced standard of care, and attendees were recruited for research. Participants in this study were drawn from a larger prospective IRB-approved study of extra-intestinal symptoms and CD; psychological presentations in subsets of this sample have been reported previously (Coburn, Rose, Sady, et al., 2020; Coburn, Rose, Streisand et al., 2020). Criteria for inclusion in the current study were: (1) patient age 6–18, (2) patient diagnosed with CD by a physician (based on clinical history, positive tags IgA or IgG antibodies and/or intestinal enteropathy), (3) parent and/or clinician completed GFD adherence ratings, and (4) parent completed at least one of the structured questionnaires assessing ADHD-related symptoms and executive functioning during their clinic visit. Due to time constraints during clinic, a few participants were missing one rating or one questionnaire, with no participant missing more than one rating/measure.

Out of 138 consented participants in the larger study, the final sample for this investigation included 34 youth with CD, most of whom (82%) had been following a GFD for at least three months (see Table 1). All parents were mothers. The sample of CD participants was 6 to almost 18 years old (M = 13.01, SD = 3.88), equally distributed by gender (56% female), and primarily Caucasian (82%). Of note, gender as reported in this study was determined by parent and child report (in this sample, there were no cases where these reports were discordant from one another or from sex listed in the medical record). Consistent with previous research, a relatively large proportion of the sample had also been diagnosed with ADHD per parent report (18%); anxiety was also prominent (21%). Overall, the sample was demographically representative of both the patient population of the clinic and the consented participants (t-tests indicated no differences in age or months since diagnosis, and X2 tests indicated no differences in gender or race, between our substudy sample and those who attended the clinic but did not consent or consented but were not part of this substudy). The main factor limiting sample size was that, due to the lengthy nature of the clinic visit, many families did not want to stay after clinic to complete the structured questionnaires.

Table 1.

Sample Characteristics

M (SD) Minimum - Maximum
Age (years) 13.01(3.88) 6.04–17.77
Time since Celiac Disease Diagnosis (months) 23.27(23.28) 1.15–74.10
n %
Time since Celiac Disease Diagnosis (dichotomous)
 Recent (< 3 months) 6 18%
 Established (3+ months) 28 82%
Gender
 Female 19 56%
 Male 15 44%
Race/Ethnicity
 Black/African American 0 0%
 White/Caucasian, Non-Hispanic 28 82%
 Mixed/Multiracial 2 6%
 Hispanic/Latino 1 3%
 Other 3 9%
 Unknown/Did not report
Mental Health Diagnoses
 ADHD 6 18%
 Learning Disability 2 6%
 Anxiety 7 21%
 Depression 1 3%
 Developmental Delay 1 3%
Number of Mental Health Diagnoses 20 59%
 None 8 24%
 One 6  12%
 Two or more 6 18%
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N = 34; M = Mean, SD = Standard Deviation; ADHD = Attention Deficit/Hyperactivity Disorder

Time since diagnosis was collected from medical records; gender, race/ethnicity, and mental health diagnoses were reported by parents

Measures

Pre-Clinic Survey

Parents completed a survey (sent via REDCap to the parents’ preferred email address) within one week prior to their clinic visit about the patient’s CD symptoms, other medical and mental health diagnoses, treatment history and medications for these diagnoses, and ratings of their gluten-free experience. Parent-reported GFD adherence was assessed with the question, “How often do you think your child follows the gluten-free diet successfully?” using a visual analog scale format, using sliders with one-point intervals and anchors of 0 (never strictly gluten-free) to 100 (always strictly gluten-free). Visual analog scales have been used in some studies of adherence in adults with CD (Hall et al. 2009) and in preliminary investigations in pediatrics (Coburn, Rose, Streisand, et al., 2020). This rating was available for all 34 participants.

Interviews

During the multidisciplinary clinic visit, parents and patients met with gastroenterology, psychology, neuropsychology, neurology, and GFD education (a staff member with specialized expertise in GFD adherence). The following adherence questions were asked by the psychologist and recorded in a structured manner (Coburn, Rose, Sady, et al., 2020): (1) Interval since last gluten exposure; (2) Purposeful vs. accidental; (3) Confirmed vs. suspected; and (4) Frequency of exposures, with follow-up questions to assess details of additional exposures. Following the visit, the multidisciplinary team met and generated a clinician-rated adherence consensus score using a simplified version of the Standardized Dietitian Evaluation (Gładyś et al., 2020), with possible ratings consisting of poor (>1 recent exposures, risks, and/or symptoms in past 3 months), adequate (1 recent exposure, risk, or symptom in past 3 months), excellent (no recent known exposure, risk, or symptoms), or cannot rate (insufficient information). Reports from any member of the clinic team indicating known or suspected exposure to gluten were included in consideration for the consensus rating. An adherence rating was available for 33/34 participants; one participant did not receive an assessment due to time constraints in the interview and therefore was not given a rating.

Behavior Rating Inventory of Executive Functioning – second edition (BRIEF2)

The BRIEF2 is a widely used assessment of executive functioning for children aged 5–18 years, with strong reliability and validity (Gioia et al., 2015). Parent report consists of 63 items across three indices: Behavior Regulation, Emotion Regulation, and Cognitive Regulation. Items were developed to be ecologically valid behavioral correlates to executive functioning and are rated on a 3-point scale consisting of “never,” “sometimes,” and “often.” Age-adjusted T scores (mean = 50, SD = 10) were generated for each of the indices; higher scores indicate greater difficulties, with T > 65 indicating clinically significant problems. These scores were available for 33/34 participants.

Child Behavior Checklist (CBCL)

The CBCL is a caregiver-reported assessment of competencies and problems in children aged 6–18 years with strong reliability and validity (Achenbach, 1999). Caregivers indicate whether each of 112 items is “not true,” “somewhat or sometimes true,” or “very true or often true” of their child over the past 6 months. Items load onto eleven syndrome scales and six DSM-oriented scales. As with the BRIEF2, scores are reported as age-adjusted T scores, with higher scores indicate greater difficulties. For this study, the scales of interest were the Attention Problems syndrome scale and the DSM-oriented ADHD Problems scale. These scores were available for 32/34 participants.

Procedures

At or before the first visit to the multidisciplinary clinic, parents and patients were approached for participation in the larger study. All parents of patients who attended the multidisciplinary clinic completed the pre-clinic survey in the week prior to their clinic visit. Adherence ratings and interviews were completed during the visit as part of standard clinical care, and questionnaires were optional, for research only, and were completed on paper forms while in the waiting room or at the end of the clinic visit. Of note, self-report forms were also completed by patients ages 11 years and older, but sample sizes in this age range were too small to include self-report in this set of analyses.

Questionnaires were scored on each publisher’s website. Data from clinician adherence questions, interview, and questionnaires were entered by study staff and managed using REDCap electronic data capture tools (Harris et al., 2009).

Data Analysis

Convergence of Ratings

We first evaluated agreement within the two types of ratings. Within the adherence ratings, we calculated point-biserial correlations between clinician-rated adherence (dichotomized into poor/adequate vs excellent based on the distribution) and parent-reported adherence. Within the ADHD-related symptoms, we calculated correlations between T scores on the BRIEF2 and CBCL scales.

ADHD-Related Symptoms and Adherence

Associations between adherence (parent and clinician-rated) and ADHD-related symptoms (key scales on the BRIEF2 and CBCL) were evaluated using bivariate (parent-reported adherence) and point-biserial (clinician-rated adherence) correlations. Additional predictors (age, gender, ADHD diagnosis status, ADHD treatment status) of GFD adherence were assessed in regression models, using individual predictors and an interaction of ADHD-related symptoms with age. Across all analyses, relevant assumptions were evaluated and met; i.e., there were no outliers on continuous variables, equal variances were met or adjusted for, relationships between independent and dependent variables were linear, there was no multicollinearity of predictors, and residuals of regression models were roughly normally distributed.

Results

Mean Ratings

Parent-reported adherence ranged from 20 to 100, M = 87.9, SD = 20.4. Clinician-rated adherence was poor/adequate in 52% and rated as excellent in 48% of participants. T scores on the BRIEF2 and CBCL scales were as follows: Behavior Regulation Index M (SD) = 48.7 (10.9), Emotion Regulation Index M (SD) = 52.4 (13.2), Cognitive Regulation Index M (SD) = 48.5 (11.5), Attention Problems M (SD) = 55.7 (8.0), DSM-oriented ADHD Problems M (SD) = 54.8 (7.1).

Convergence of Ratings

There was no significant association between parent-reported adherence and clinician-rated adherence (rpb = .29, 95% CI [−.12, .61], p = .16, r2 = .08). As expected, however, ADHD-related symptom ratings were significantly correlated across the five BRIEF2 and CBCL scales, with an r range of .74 to .96, all p-values < .001, r2 range = .55 to .92.

ADHD-Related Symptoms and Adherence

There were significant negative correlations between parent-rated adherence and two of the BRIEF2 scales (Behavior Regulation r = −.52, 95% CI [−.73, −.22], p < .01, r2 = .27, Cognitive Regulation r = −.48, 95% CI [−.71, −.17], p < .01, r2 = .23), but not the BRIEF2 Emotion Regulation Index or either of the CBCL attention scales (r range −.32 to −.11, all p ≥ .10, all r2 < .10; see Table 2 for all coefficients and CIs). There were no significant correlations between clinician-rated adherence and any of the rating scales (rpb range −.14 to .03, all p > .49, all r2 < .02); see Table 2. When examining individual results, a relatively large proportion of individuals were rated as having elevated symptoms: 13–18% of the sample had CBCL and BRIEF2 ratings at the 95th percentile or above, where in a normative sample only 5% would have ratings this high.

Table 2.

Correlations of ADHD-related Symptoms and Demographic Variables with GFD Adherence

Parent-rated Adherence Clinician-rated Adherence
r [95% CI] p r [95% CI] p
BRIEF2
 Behavior Regulation Index −.52 [−.73, −.22] < .01 −.14 [−.55, .28] .49
 Emotion Regulation Index −.32 [−.59, −.03] .10 .03 [−.38, .44] .89
 Cognitive Regulation Index −.48 [−.71, −.17] .03 −.11 [−.51, .31] .58
CBCL
 Attention Problems −.11 [−.40, .25] .61 −.06 [−.47, .40] .79
 DSM AD/H Problems −.14 [−.45, .22] .49 −.11 [−.53, .35] .60
Age in years −.13 [−.43, .21] .46 −.36 [−.66, .04] .08
Gender .08 [−.26, .40] .66 .20 [−.21, .55] .34
Time since diagnosis in months .01 [−.33, .33] .99 −.19 [−.55, .22] .35
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ADHD = Attention Deficit/Hyperactivity Disorder

BRIEF2 = Behavior Rating Inventory of Executive Functioning, second edition

CBCL = Child Behavior Checklist

DSM = Diagnostic and Statistical Manual [of Mental Disorders]-Oriented scale

AD/H = Attention Deficit/Hyperactivity

For parent-reported adherence and the Behavior and Cognitive Regulation BRIEF2 indices, we built two linear regression models to better understand what might be driving those associations, and to account for other possible predictors of the outcomes. In each model, we included demographic predictors (age, gender, months since CD diagnosis, and ADHD diagnosis status), the BRIEF2 scale, plus an interaction between age and the BRIEF2 scale, with parent-reported adherence as the outcome. For BRIEF2 Cognitive Regulation, none of the demographic variables or interactions were significant predictors of parent-rated adherence (all p ≥ .10, overall adjusted R2 = .19). For the Behavior Regulation Index (BRI), the main effect of age and the interaction of BRI with age were significant (p = .03 and .01, respectively, overall adjusted R2 = .44). See Table 3 for full regression results, including estimates and confidence intervals.

Table 3.

Regression Model for BRIEF2 BRI Predicting Parent-rated Adherence

F df p Adjusted R2
Overall Model 4.69 6, 22 .003** .44
B SE 95% CI p
Beta LL UL
Constant 32.35 48.61 −68.47 133.16 .51
Age in years 1.51 8.17 3.41 1.09 15.25 .03 *
Gender (0 = female) 0.08 3.25 5.99 −9.16 15.66 .59
Time since diagnosis (months) −0.26 −0.23 0.13 −0.49 0.04 .09
Diagnosis of ADHD (0 = no) −0.09 −4.87 11.26 −28.21 18.48 .67
BRIEF2 BRI T-score 0.78 1.52 0.97 −0.49 3.52 .13
Age x BRI (interaction) −2.23 −0.19 0.07 −0.32 −0.05 .01 *
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**

p < 0.01,

*

p < 0.05

ADHD = Attention Deficit/Hyperactivity Disorder

BRIEF2 = Behavior Rating Inventory of Executive Functioning, second edition

BRI = Behavior Regulation Index

SE = standard error of regression B-weight

CI = confidence interval

LL, UL = lower limit and upper limit (95% CI) around B-weight

Figure 1 shows this interaction graphically, using the regression coefficients with sample individuals to calculate predicted parent-rated adherence, for children (using age 8 years to represent) and adolescents (using age 16) at both typical (T = 40) and elevated (T = 70) BRI ratings. Both children and adolescents with typical BRI ratings had high predicted parent-rated adherence. Children with elevated BRI ratings had slightly lower parent-rated adherence, whereas adolescents with elevated BRI ratings had significantly lower parent-rated adherence.

Figure 1.

Figure 1.

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Age by Behavior Regulation Index Interaction Predicting Parent-Rated Adherence

BRI = Behavior Regulation Index on the BRIEF2 (Behavior Rating Inventory of Executive Functioning, second edition). Child prediction was built using age 8 years as reference, Adolescent using age 16 years.

Regression models were not built for clinician-rated outcomes or the BRIEF2 Emotion Regulation or CBCL scales, given the absence of significant bivariate correlations.

Discussion

Celiac disease management involves careful adherence to a gluten-free diet, the successful execution of which requires one to examine food labels, ask questions at restaurants, and refrain from ingesting gluten-containing foods, among other behaviors. These tasks rely upon EF skills such as planning, organization, self-monitoring, impulse control, and flexibility. An additional concern in pediatric CD is that ADHD, which is associated with EF problems, may occur at higher rates in pediatric CD compared to the general population. In light of these concerns, we examined the potential links between EF and GFD adherence to identify potential risks in pediatric CD.

In our sample of youth with CD, there was a high rate of ADHD (18%) and of elevations on scales assessing attention and EF (13–18% of the sample were rated at the 95th percentile or above). Consistent with our first hypothesis, we found that weaknesses in certain aspects of EF (Behavior and Cognitive Regulation Indices) were associated with lower parent rated GFD adherence. Our findings did not differ by time since CD diagnosis, suggesting stability of these associations. The scales that comprise these indices are Inhibit and Self-Monitor (BRI) and Initiate, Working Memory, Plan/Organize, Task-Monitor, and Organization of Materials (CRI). When considered in the context of adhering to a GFD, individuals may impulsively eat food that is not gluten-free, have difficulty planning for situations in which safe food may be hard to find, and fail to recognize or consider the potential negative health effects of consuming gluten. This link has been observed in other pediatric chronic illnesses. In youth with type 1 diabetes, for example, EF problems were associated with higher hemoglobin A1C, with moderating effects from self- and parent responsibility over their condition management (Vloemans et al., 2019). In pediatric cystic fibrosis, another disorder with high burden for management, a moderate association was found between parent-rated EF and treatment adherence (Borschuk et al., 2020). In addition, a meta-analysis found evidence of impairments in EF such as inhibition and working memory among overweight individuals, with more extensive deficits (inhibition, cognitive flexibility, working memory, decision-making, verbal fluency, and planning) in obesity (Yang et al., 2018). Thus, EF weaknesses could have substantial clinical implications on self-management in conditions requiring the burdensome tasks associated with dietary self-management.

When considered with other demographic factors, we found support for our second hypothesis that the association between EF and adherence was strongest for adolescents who had elevated ratings in Behavior Regulation. Developmentally, EF during adolescence is by nature immature compared to adults, which could impede successful self-management of the GFD. This might occur due to the high demands for independent self-regulation paired with strong motivation among teens to fit in and engage in social activities with peers. As food is a major component of socialization across populations, the temptations and social complexities of avoiding gluten may be particularly challenging for teens (Ludvigsson et al., 2016, Chang et al., 2022). A similar association between adherence and behavioral regulation in particular was highlighted in a study of children and adolescents with HIV, with similar implications for transitioning responsibility for adherence to adolescents with less well-developed regulatory skills (Garvie et al., 2017).

We did not find associations between adherence and attention/ADHD scales. Although ADHD may be more prevalent in individuals with CD, the more nuanced skills specific to EF appear to be a better indicator of risk for nonadherence than diagnosis status or attention per se, especially in teens. This finding raises questions regarding the longitudinal effects of EF weaknesses on GFD adherence, and vice versa. In adults, individuals reported improved ADHD-related behavior and functioning after 6 months of treatment with a GFD (Niederhofer & Pittschieler, 2006); conversely, nonadherence may be a risk factor for increased ADHD-related symptoms. Therefore, future investigations of bidirectional effects of EF and GFD adherence should examine whether certain EF weaknesses could improve over time on the gluten-free diet, but also whether poor EF could lead to a negative feedback cycle of poor adherence.

In this study, EF weaknesses were linked to parent-reported adherence but not clinician-rated adherence. These differences may be due to differences in sample heterogeneity, rater judgment, measurement methodology, and other well-established challenges with quantifying GFD adherence (Wieser et al., 2021). Our sample was somewhat restricted in the range of adherence observed (many reported being highly adherent). In addition, the clinician interview and subsequent rating focused on recent exposure and risk-taking behavior; while methodical, these questions may have not been sufficiently sensitive or specific to long-term patterns of behavior. In contrast, the parent rating was more open-ended and less time-limited, capturing a global sense of adherence success rather than only adherence behaviors in the recent past. It is also possible that the clinician rating captured the overall adherence incorporating the child’s whole environment (self, parents, school, availability of options, etc.), while the parent rating focused more on the child’s role in adherence given the question wording of “how often do you think your child follows…”. Some studies of CD have relied on blood serum markers such as tissue transglutaminase IgA (tTg-Iga) as a measure of adherence, as it is used for screening and diagnosis. However, tTg-IgA is not a reliable or appropriate measure of adherence due to its inconsistent response to initiation of the GFD (Ludvigsson et al., 2018). Consistent with adherence research in other populations (Pruette et al., 2019), it is likely that a multi-rater method of adherence assessment is the optimal approach to reliably capturing and tracking different dimensions of adherence to the GFD in youth.

Limitations

While the general pattern of results is consistent with findings in other pediatric illness populations, a few limitations are notable. First, our sample comprised a small, cross-sectional portion of children with CD. Logistical limitations precluded some multidisciplinary clinic patients from completing the questionnaires during their visits, and while the sample was representative of the clinic population in demographic characteristics, the sample with complete data was smaller by comparison. Because self-report was only gathered from children 11 years and older, the very small sample size precluded analysis of their ratings. Particularly for adolescents, self-report of both EF skills and adherence is important to study, as they may have differing perspectives and unique knowledge of their behavior outside of the home. Additionally, we did not assess parent’s own EF skills, which especially for younger children, may play a significant role in adherence. Our sample was also somewhat homogenous in background (e.g., largely Caucasian) and reported adherence (mostly high), which may have limited our ability to examine the full range of behaviors and challenges in the greater pediatric CD population.

The use of parent-report measures for attention/EF and adherence raises the question of whether the association reflects shared method variance rather than a true link between EF and GFD adherence. However, the presence of the hypothesized age interaction and the absence of relation between attention scales (i.e., non-EF items) and adherence makes this less likely. A remaining limitation is the lack of availability of a well-validated approach to measure adherence in pediatric CD. Although there have been some efforts to adapt or develop structured rating scales, as well as advancements in technological approaches to measuring gluten intake (e.g., detection of gluten immunogenic peptides in stool), a feasible and validated “gold standard” for measuring GFD adherence is not yet available.

Future Directions

The results of this study provide a foundation for multiple future investigative pathways. To better understand the variability in parent-reported adherence we observed, qualitative interviews can glean the reasoning and specific concerns behind ratings. For example, parents who rate their child as less adherent may be fearful of poor adherence without necessarily having knowledge that they are not actually fully adherent. Given the prominent role of parents in GFD adherence in pediatric CD, future investigations of EF skills should also include assessment of parent EF. Further, investigation into the potential risks and challenges of the transition of GFD adherence in adolescents is needed to clarify the tasks and burdens associated with this sensitive developmental period and to develop appropriate supports and interventions to optimize adherence.

Implications for Practice

This study emphasizes the overlap between EF and self-management of CD in youth. A feasible and proactive step in the medical setting may be to incorporate screening for EF at the time of CD diagnosis to identify at-risk individuals, through use of short, validated questionnaires designed for medical professionals (e.g., the BRIEF2 Screening Form; Gioia et al, 2015). Teaching strategies for successful adherence should reference EF skills such as planning, impulse control, and flexibility. Adherence and EF skills should be re-assessed over time, particularly at times when the youth is changing (e.g., entering adolescence) or their environment is shifting (e.g., changing schools, going to restaurants without their parents). These approaches complement dietary/nutritional and medical assessment of GFD adherence in clinical settings in youth, particularly for teens and young adults.

Health care providers should also consider referring patients who are struggling with GFD adherence and/or are identified as having EF weaknesses to a behavioral specialist (i.e., pediatric psychologist, social worker). Comprehensive models of the factors that can influence adherence emphasize the role of EF, with proposed interventions drawing from cognitive-behavioral therapy techniques for changing behaviors (Brock et al., 2011). Behavioral health providers are well positioned to determine the potential influence of poor EF and its practical impact on barriers to adherence. For individuals (particularly adolescents) who are struggling, aspects of behavioral regulation, goal setting, and planning can be incorporated into exercises designed to improve GFD adherence. Along with targets such as improving education and knowledge, working on problematic EF skills may be of benefit.

Financial Support:

This work was supported by the Global Autoimmune Institute (PI: I. Kahn); the Lambert Family Foundation (Co-PIs: S. Coburn & M. Sady); and the National Institute of Diabetes and Digestive and Kidney Diseases of the National Institutes of Health under Grant K23DK129826 (PI: S. Coburn).

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