Celiac disease (CD) is an autoimmune enteropathy based on genetic susceptibility and triggered by the ingestion of gluten. It has a prevalence of 1% worldwide (1). In addition to both overt gastrointestinal and extra-intestinal manifestations, CD is known to present with growth failure, of particular concern in pediatric subjects (2,3).
For this reason, growth parameters are closely followed in pediatric CD as patients are initiated on a gluten-free diet (GFD). Although this consideration is important in disease management, growth failure is by no means expected in CD and, in fact, 40% of adults with CD are classified as either overweight or obese (4). Although few studies have focused on body mass index (BMI) in children with CD, some data suggests that BMI also increases in this population following introduction of a GFD (5). For children with CD, this finding may be related to food choices as has been seen in analysis of childhood obesity trends and interventions (6).
The recent embrace of the GFD in mainstream, especially by those without CD, has led to an emergence of processed gluten-free (GF) food options. One report details that GF products increased from 3.4% of the emerging food market in 2003 to 24.3% by 2013. Although often marketed as “healthy,” GF products may have higher fat and carbohydrate content than gluten-containing options (7). A recent study found that 80% of child-targeted GF foods have high sugar content (8). More research is needed to determine if this trend has affected the food choices of children with CD. Here, we aim to characterize the extent of processed food inclusion in the GFD and, secondarily, how best to home counseling in the context of developing dietary habits for children with CD and their families.
Pediatric subjects diagnosed with CD seen in specialty clinics at the University of Chicago Celiac Center from 2015 to 2018 were screened via use of the electronic medical record and then contacted through email to participate in an optional 20 question Likert survey available via RedCap (9,10). All survey items were required to be completed in order to successfully submit. Eligibility criteria for inclusion were subjects with CD 18 years or younger with an available email address for survey distribution. Exclusion criteria were subjects unable to consume a per oral diet. Minimal criteria were used in an attempt to capture a large range of CD patients that would minimize selection bias and allow results to remain externally valid. Children age 12 years and over were asked to complete the survey without assistance whereas children under age 12 years were assisted by their parents. Three unique appeals were made for subjects to participate, though, the survey could only be completed once per subject. A statistical analysis with pairwise comparison was then performed across 3 age groups roughly approximating middle school to high school age (13–18 years), elementary school age (7–12 years), and infancy to preschool (0–6 years). The Bonferroni method was used to adjust for multiple comparisons.
The survey was distributed to 177 unique subjects and completed by a total of 100 children with CD. As survey responses were anonymous, there was no means of ascertaining, which individuals had not completed the study or the reasons underlying their nonparticipation. Of the respondents, 63% were girls. The mean age of subjects in this study was 11.85 years (±4.32 years) with a range of 2 to 18 years. The mean age of diagnosis of CD was 7.86 years (±4.41 years).
All subjects in our cohort acknowledge eating processed GF foods, specifically classified as “ultra-processed” in a cross-sectional analysis of data from the National Health and Nutrition Examination Survey (11). These energy-dense foods, provided to respondents in list form and reinforced with photographs, include breads, salty snacks, breakfast cereals, ready-to-eat pizzas/hamburgers/sandwiches, frozen meals, sweet snacks, and desserts. Although processed foods were consumed on at least a weekly basis by all subjects, 77% consume processed GF foods multiple times per day and 20% eat exclusively processed GFDs. These patterns are seen across all age groups; however, a higher percentage of those who rarely consume processed GF options is registered in the older cohort (30.2%) compared with children under the age of 12 years (17.5%), though this does not reach statistical significance (Table 1).
In response to why children and their families choose processed GF foods, 76% of subjects identified convenience as their primary motivation. In comparison, 18% of subjects linked “better taste” to their preference for processed foods. Children ages 0 to 6 years reported a higher percentage of perceived improved taste at 45.5% compared with children 7 to 18 years where the percentage drops to 14.6%, and convenience becomes a more important factor.
Further analysis by age groups showed that older children are more likely to prepare their own meals (P < 0.0001). In children ages 0 to 6 years, 63.6% do not take part in their meal preparation. Of those participating at all, only the 6-year-old children “sometimes” assisted. The percentage of those not involved in meal preparation decreases in the 7- to 12-year-old group and 13- to 18-year-old group to 17.4% and 2.3%, respectively (Table 1).
Although overall 67% of subjects desire dietary counseling at regular checkups, 19.5% of total subjects would be interested in more frequent education. Interest in dietary counseling was found to be significantly varied as a function of age. In the younger cohort, 63.6% of subjects (or their parents) were interested in dietary guidance more frequently than just at regular celiac check-ups. This decreased to 26.1% in the 7- to 12-year-old group and further to 4.7% in the 13- to 18-year-old group (Fig. 1). Our survey additionally revealed that the desire for dietary counseling diminished with time from CD diagnosis. In children less than 1 year from diagnosis 34.6% would like dietary feedback more often. This interest incrementally decreased at 2 to 3 years from diagnosis (18.3%), 4 to 6 years from diagnosis (14.8%) and at greater than 7 years (11.1%), though these values do not reach statistical significance.
This study builds upon recently reported data from our institution, which showed that children with CD demonstrated a trend toward higher BMI in adolescents after 2011 (12). Although other studies have described obesity in pediatric CD (13,14), as far as we are aware, this is a first attempt to explore its association with the expansion of the processed GF market. Furthermore, although the effects of a processed foods-rich diet has been linked to habit formation and obesity in children without CD (15,16), the downstream consequences of the expanded GF market on pediatric CD has yet to be explored. For the first time, we report that all children with CD, regardless of age, consume processed GF items multiple times per week. For some, including younger children, these items are consumed exclusively.
Additionally, this study reveals that processed GF options have become a mainstay of the GFD for children with CD based, in part, on the convenience these options provide. Although this finding may not surprise clinicians caring for children with CD, it suggests that providing dietary guidance solely on the basis of gluten exclusion may not be sufficient. This is supported by a recent study, which found that children with CD consume a predominantly Western-style diet with low dietary quality and insufficient daily folate (17). These findings run parallel in the non-CD population, with cross-sectional data suggesting that processed foods constitute a majority of daily calories consumed by children of diverse backgrounds throughout the United States (18).
Another important finding is that children and their families are less interested in dietary counseling over time, both as a factor of time from diagnosis and in terms of chronological age. This may be a reflection of greater comfort with the GFD as subjects move further from diagnosis or an indication that dietary preferences become ingrained over time. In either case, this finding suggests that our greatest opportunity for helping children with CD to form healthy dietary habits occurs at the time of diagnosis. At the same time, children are increasingly taking responsibility for their own meal preparation as they age, presenting a challenge for CD providers and dietitians when it comes to on-going assessment and education.
In this vein, clinicians caring for children with CD should partner with dietitians to not only just clearly define the GFD at diagnosis but also to alert families to the potential dangers of relying too heavily on processed GF foods. Subsequently, a targeted effort to assess the quality of the GFD and make adjustments over time should be a routine facet of CD care. An on-going dialogue may aid clinicians in avoiding incorrect assumptions about dietary quality and allow patients and families the opportunity to re-evaluate food choices as the GF market continues to expand. Although our center strives to follow this model and to provide unrestricted access to a dietitian with expertise in CD, the results of this study highlight the need for a standardized approach and a prospective assessment of patient and parental perceptions about a healthy GFD and adherence to those recommendations.
This study is limited in size and does not directly correlate dietary preferences with individual BMI or trends over time. Though, we asked families to assist children less than 12 years with answering questions and to allow older children to answer for themselves, the answers given may be more reflective of parental understanding of dietary habits and desire for further dietary education as opposed to the opinions of the children themselves. Additionally, as a referral center for CD, this study may be subject to selection bias. As CD-trained dietitians are, however, available for all, or most, clinic visits in our center, we might expect that healthier dietary habits would be reinforced compared with clinics where this valuable resource is not always present. As no respondents were excluded based on eligibility criteria, we feel this cohort is representative of the general CD population, however, using a de-identified survey, this study does not control for volunteer or nonresponse bias.
A prospective analysis is needed in order to more directly explore the link between food habits and BMI trends in children with CD. Aside from higher caloric density of processed GF foods, there may also be concerns related to vitamin and micronutrient content, deficiencies for which children with CD are already at high risk (19,20). As the GFD is known to be restrictive, and difficulties with adherence remain a challenge for children with CD (21,22), efforts to limit processed GF consumption may place additional burden on children and families with CD. As such, it will be important to collaborate with dietitians to determine how best to deliver advice to families and children with respect to moderation of processed GF inclusion in the diet.
Despite these limitations, we feel these findings should serve as red flag for all clinicians providing dietary management in pediatric CD. Our analysis confirms that processed GF items are a staple of the diet in children with CD and for some patients, the primary form of caloric intake. Acknowledgement of this finding will allow clinicians and dietitians to best meet the needs of their patients with CD as the processed GF market continues to expand. Without upfront and on-going education around a healthy GF diet, CD providers are missing an opportunity to correct problematic dietary habits, which may ultimately be linked to complications, such as obesity and poor cardiovascular health.
1. Singh P, Arora A, Strand TA, et al. Global prevalence of celiac disease: systematic review and meta-analysis. Clin Gastroenterol Hepatol
2018; 16: 823–836 e2.
2. Khatib M, Baker RD, Ly EK, et al. Presenting pattern of pediatric celiac disease. J Pediatr Gastroenterol Nutr
3. Saari A, Harju S, Mäkitie O, et al. Systematic growth monitoring for the early detection of celiac disease in children. JAMA Pediatr
4. Dickey W, Kearney N. Overweight in celiac disease: prevalence, clinical characteristics, and effect of a gluten-free diet. Am J Gastroenterol
5. Valletta E, Fornaro M, Cipolli M, et al. Celiac disease and obesity: need for nutritional follow-up after diagnosis. Eur J Clin Nutr
6. Bleich SN, Vercammen KA, Zatz LY, et al. Interventions to prevent global childhood overweight and obesity: a systematic review. Lancet Diabetes Endocrinol
7. Kulai T, Rashid M. Assessment of nutritional adequacy of packaged gluten-free food products. Can J Diet Pract Res
8. Elliott C. The nutritional quality of gluten-free products for children. Pediatrics
9. Harris PA, Taylor R, Thielke R, et al. Research electronic data capture (REDCap)--a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform
10. Harris PA, Taylor R, Minor BL, et al. The REDCap consortium: building an international community of software platform partners. J Biomed Inform
11. Martinez Steele E, Baraldi LG, Louzada ML, et al. Ultra-processed foods and added sugars in the US diet: evidence from a nationally representative cross-sectional study. BMJ Open
12. Amirikian K, Sansotta N, Guandalini S, et al. Effects of the gluten-free diet on body mass indexes in pediatric celiac patients. J Pediatr Gastroenterol Nutr
13. Venkatasubramani N, Telega G, Werlin SL. Obesity in pediatric celiac disease. J Pediatr Gastroenterol Nutr
14. Reilly NR, Aguilar K, Hassid BG, et al. Celiac disease in normal-weight and overweight children: clinical features and growth outcomes following a gluten-free diet. J Pediatr Gastroenterol Nutr
15. Luque V, Escribano J, Closa-Monasterolo R, et al. Unhealthy dietary patterns established in infancy track to mid-childhood: the EU Childhood Obesity Project. J Nutr
16. Costa CS, Rauber F, Leffa PS, et al. Ultra-processed food consumption and its effects on anthropometric and glucose profile: a longitudinal study during childhood. Nutr Metab Cardiovasc Dis
17. Mager DR, Liu A, Marcon M, et al. Diet patterns in an ethnically diverse pediatric population with celiac disease and chronic gastrointestinal complaints. Clin Nutr ESPEN
18. Eicher-Miller HA, Fulgoni VL 3rd, Keast DR. Energy and nutrient intakes from processed foods differ by sex, income status, and race/ethnicity of US adults. J Acad Nutr Diet
19. Deora V, Aylward N, Sokoro A, et al. Serum vitamins and minerals at diagnosis and follow-up in children with celiac disease. J Pediatr Gastroenterol Nutr
20. Imam MH, Ghazzawi Y, Murray JA, et al. Is it necessary to assess for fat-soluble vitamin deficiencies in pediatric patients with newly diagnosed celiac disease? J Pediatr Gastroenterol Nutr
21. MacCulloch K, Rashid M. Factors affecting adherence to a gluten-free diet in children with celiac disease. Paediatr Child Health
22. Mehta P, Pan Z, Riley MD, et al. Adherence to a gluten-free diet: assessment by dietician interview and serology. J Pediatr Gastroenterol Nutr