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Revista chilena de pediatría

Print version ISSN 0370-4106

Rev. chil. pediatr. vol.89 no.2 Santiago Apr. 2018  Epub Apr 04, 2018 


Perception of following gluten-free diet and adherence to treatment in pediatric patients with celiac disease

Karin W. SchillingA 

Karla YohannessenA 

Magdalena ArayaB 

A Hospital Roberto del Río, Santiago, Chile.

B INTA, University of Chile, Santiago, Chile.



Celiac disease (CD) is a chronic immune-mediated enteropathy present in ~1% of population. Gluten-free diet (GFD) is the only treatment for this condition and the main limitation of its efficacy is the lack of adherence.


To assess factors influencing adherence to GFD in pediatric patients and measure the concordance between serological results and a nutritional adhe rence questionnaire.

Patients and Methods:

celiac patients younger than 18 years of age, diagnosed CD following ESPGHAN criteria, on GFD for at least 6 months and consulting at Hospital Roberto del Río, Santiago, in 2008-2016, were assessed. Clinical presentation, nutritional evaluation and fac tors related to adherence to treatment (diet) were registered. A subsample answered Biaggi's nutri tional questionnaire.


Of 65 evaluated patients, 44% and 30,1% adhered to GFD according to blood autoantibodies (TTG and EMA) and the adherence questionnaire, respectively. “Age at debut” (p = 0.049), “perception of following GFD correctly” (p = 0.002) and “behavior in social events” (p = 0.005) were significantly associated with adherence to GFD. There was concordance between serological test and Biagi’s questionnaire (p = 0.0001).


Adherence to GFD was lower than reported in literature. Intervention of some of the identified variables associated with adherence may help improving follow-up of celiac patients, especially those that due to diverse situations cannot measure their antibodies periodically.

Keywords: Celiac disease; gluten; adherence; perception; ESPGHAN


Celiac disease (CD) is an immune-mediated chro nic enteropathy, produced by the interaction of certain haplotypes (genes) of the host that provide the genetic susceptibility1 and the environment, which contributes the prolamins of gluten in the diet2. Other factors, such as epigenetics and host microbiota, would participate in the pathogenesis of CD through less-known mecha nisms3. It is currently recognized as a high-frequency autoimmune condition, which appears at any age4, re aching a global prevalence of 1-3% of the population5. It is diagnosed by serology (measurement of antibodies against tissue transglutaminase 2(TTG), anti-endomysial (EMA) antibodies or deamidated gliadin peptides (DGP) and histological confirmation in duodenal biopsies, which show various degrees of lymphocytic infiltration, crypt hyperplasia, and villous flattening4,6. By now, the only effective treatment for CD is the glu ten-free diet (GFD), strict, permanent and lifelong4. This diet eliminates wheat, rye, and barley from the diet, included in both natural and processed foods7. Oats are also usually eliminated because it has a high probability of being contaminated8. The main limita tion of this treatment is the lack of adherence of pa tients to GFD.

The treatment of CD includes patients follow-up, periodic and long-term, to evaluate the clinical course and adherence to GFD. This evaluation is difficult be cause there is no reliable and reproducible method to measure the actual gluten intake. The current strategy is based on the consensus of specialists4. They recom mend periodic check-ups that estimate the adheren ce based on what the patient reports and the measu rement of antibodies that reflect autoimmunity. The most used are TTG9,10. It is expected that, by not eating gluten, patients will show blood clearance and progres sive reduction of the intestinal mucosa damage and autoimmunity phenomena. However, the usefulness of these antibodies for follow-up has currently under discussion11-13, exposing again the problem of how to ensure that the information provided by the patient is accurate and reliable. Foreign data show that adhe rence to GFD in children is 80-95% and in adolescents and adults 36-52%14,15. Assessing adherence through interviews by specialized professionals and validated questionnaires is giving promising results, but not yet definitive ones12,16. In Chile, studies indicate that pediatric patients who adhere to GFD vary between 24- 34%17-19, without significant variations over time. The World Health Organization (WHO) has described five types of factors that influence the adherence to a chro nic treatment: related to the disease, the patient, the treatment, the health system or health team, and the socioeconomic characteristics. The information about how these factors affect the celiac patient and the GFD is insufficient. Considering that the available data in our country are scarce, show low degrees of adherence and that in the national public health system the fo llow-up is by serology (TTG and occasionally EMA), the objective of this study was to evaluate the factors that influence in adherence to GFD. Additionally, the concordance between the measured antibodies (TTG and EMA) and the nutritional adherence questionnai re was evaluated.

Patients and Methods

Study group

Cross-sectional, analytical study that assessed the universe of patients diagnosed with CD treated at the Gastroenterology Service of the Roberto del Río Hos pital (HRR), Santiago, 2008-2016. Patients under 18 years of age, diagnosed by serology and intestinal biopsy4 and following GFD for at least six months before the study were included. The protocol was accepted by the Ethics Committee of the Institute of Nutrition and Food Technology (INTA), University of Chile, by the HRR Management, and the Ethics Committee of the North Metropolitan Health Service (SSMN). The records of consultations during the period were reviewed (code K90.0, diagnosis of CE in the inter national statistical classification of diseases and rela ted health problems ICD10, WHO 2005). Out of 101 patients detected, 86 met inclusion criteria and were contacted by telephone to invite them to participate. However, 15 were not available and six did not show up for the interview (despite four telephone attempts). Although this represents a selection bias in the study group, the information on the clinical records showed that demographic and biological characteristics of the se 15 and six mentioned patients did not show signifi cant differences from patients included in the analysis. After explaining the protocol and obtaining informed consent, 65 patients entered the study. The partici pants (patients and/or parents or guardians) answered an ad hoc questionnaire that addressed the five groups of factors indicated by the WHO20.

The following were recorded: General data: socio demographic characteristics and socioeconomic level (according to Esomar survey, Adimark, October 2000). History: weight, height, and physical examination. The clinical characteristics were registered at the time of diagnosis and during the last three months, including date and age of diagnosis, gastrointestinal symptoms (diarrhea, abdominal distension, anorexia, constipa tion, steatorrhea, malnutrition, abdominal pain, vo miting, celiac crisis), extra gastrointestinal symptoms (anemia, short stature, pubertal delay, dental enamel hypoplasia); and the presence of associated autoim mune diseases (diabetes mellitus type I, autoimmune thyroiditis, autoimmune hepatitis, dermatitis herpeti formis). Patients were classified as typical, atypical or silent. The anthropometry followed the current Chi lean criteria (Ministry of Health of Chile)21, corrected by Tanner22 as needed. Disease Management: During the last three months, the diet was recorded, including the perception (of parents/guardians and the patient if adolescent) of following GFD correctly; knowledge of the allowed foods and the availability of those in the country, knowledge of the gluten-free symbols and if the patient does or does not read the food ingredients list before buying it. A knowledge score was made, gi ving a point to each correct answer (minimum 0 and maximum 4). In addition, we asked: i) if they knew support groups for celiac patients and if they attended their meetings or visited their websites; ii) if the school was aware of the patient’s condition, whether or not the patient had received support from the school and if the school allowed the patient to bring his/her own food or if he/she had to consume the food provided by the school; iii) if the patient does or does not break the regime when eating out of home, the behavior in birth days or social events out of home, if inthi¿ese occasion the patient chooses only gluten-free foods, consumes anything, brings food from home or does not parti cipate in this kind of events; iv) patient’s behavior in case of need for treatments with oral medications, and for the intake of food (wine, wafer, bread, matzo) in religious ceremonies; v) access to an evaluation and/or check-up with nutritionist, psychologist and/or social worker. A subgroup (patients entered to the study af ter 2009) also answered the adherence questionnaire to the gluten-free diet described by Biagi16.


EMA and TTG were measured within two weeks after the interview. The measurement of serum IgA ruled out IgA deficiency in all participants. It was not possible to measure TTG in four patients and EMA in nine. In both cases, patients did not attend sample co llection. The anthropometric evaluation (weight and height) was performed with a Seca digital scale. The Biagi questionnaire was applied following author’s instructions. It is based on four questions that inform about if the patient eats gluten voluntarily, the behavior they have when eating outside, reading the labeling of packaged foods looking for if they contain gluten and if only eats foods guaranteed by some Association of celiac patients16.

Analysis of results

Descriptive statistics were applied; the analysis was carried out in two ways: a) accepting that adherence is represented by the negative results of the serological markers (TTG antibodies and negative EMA) and b) by the data obtained by the nutritional questionnaire (Biagi). The concordance between the TTG and the nutritional adherence questionnaire was analyzed with Kappa index; the association between the evaluated factors and the results of EMA and TTG (both nega tive), with chi-square test; Odd Ratio was used as a measure of association (95% confidence interval). Lo gistic regression was applied to the factors associated with the results of EMA and TTG (positive-negative). “Good adherence to GFD” was defined when EMA and TTG were both negative.


The universe of patients (2008-2016) with diag nosis of CD was 101, which represents 0.04% of the new consultations made at the HRR during the period23. 86/101 patients met the inclusion criteria and 65 (75.6%) agreed to enter the study. 61.5% were girls, a percentage higher than in the general popula tion in that age group24. 69.2% of patients were eutrophic, 10.8% at risk or malnourished, and 20% were overweight or obese. In the assessed age group, the percentage of eutrophic/at nutritional risk was higher and the percentage of obesity was lower than in the general population25. 86% of the patients lived in the Metropolitan Region, 93.8% was using Fonasa (public health system) as health system and 86% was in middle socioeconomic level (SEL), according to Esomar 2000 classification. 50.8% of the patients were preschool children or had completed 4th grade or less. 66.1% of mothers and 55.4% of fathers had completed secon dary education or higher. Table 1 shows the variables related to the patient and his/her disease and table 2 the knowledge, disease management, and lifestyle. 52.3% of the interviewed patients (or guardians) stated that the GFD was handled correctly. There was 100% of concordance between the responses of adolescents and their parents or guardians. 43.1% (28 patients) received at least one medication permanently, mainly levothyroxine, insulin, zinc sulfate, polyvitamins, fe rrous sulfate, folic acid, and valproic acid. 6.2% repor ted receiving food in religious ceremonies, 10.8% did not commune due to fear of getting sick, and 43% had doubts about their first communion.

Table 1 Variables related to the child and his/her illness. 

Table 2 Variables related to knowledge on celiac disease and life style. 

Graph 1 shows the frequency of adherence/transgression to the GFD measured by the presence of antibodies EMA +/-, TTG +/-, EMA and TTG +/-, and EMA or TTG +/-. According to the adherence ques tionnaire to the GFD (scores 3 and 4 of Biagi), 30.8% adhered strictly to the GFD. There was concordance between the questionnaire and both tests performed and their combinations, being all P significant with modera te concordance force (table 3). In the analysis of adherence defined by serology (chi-square), only three variables were significant: “age of disease onset” (p = 0.049), “perception of doing well the GFD” (p = 0.002) and “behavior of the pa tient in front of food in social events”(p = 0.005). Assessed by serology at the time of the interview, those diagnosed be fore two years of age, between 2-10 years and after 10 years old, 60.7%, 28% and 33.3% were adherent to the GFD, res pectively. At the time of the interview, 63.3% of those who “think that they are correctly following GFD” had negative both antibodies. Among patients whose guardian thinks that they are making mistakes in the GFD, 75.9% had some positive serology, but 24.1% of the patients, although they stated to transgress the regimen, maintained both blood antibodies negative. The third significant variable was the “habits that patients have at birthdays and/or social events” (p = 0.005). Those who choose only gluten-free foods or those who take food from their homes had a significantly higher frequency of negative TTG and EMA (adherence) than those who do not follow the diet on social occasions. 63.2% of those who choose “only gluten-free” and 57.1% of those who take food from home, had negative serology. 8/9 (88.9%) patients who “eat everything” had some positive test (EMA or TTG). Meanwhile, 90% of patients who do not attend birthdays had positive serology (EMA or TTG). In relation to EMA, there were two significant variables: “read ingredients in the nutrition labeling” (p = 0.041) and “feel welcomed by the foundations supporting the ce liac patient” (p = 0.045), but these variables were not significant for the combination EMA-TTG. The self perception analysis of the GFD and the Biagi question naire showed 72% of concordance. 10/11 patients in whom there was no concordance thought they were doing well with the diet and the Biagi questionnaire classified them as transgressors.

Graph 1 Percentage of patients adhering or not adhering gluten free-diet (GFD), defined by negative serology (TTG* and EMA**). *antitransglutaminase 2 antibo dies. **anti endomysial antibodies. 

Table 3 Concordance serology/autoimmune antibodies EMA and TTG and Biagi's adherence questionnaire*. 

The logistic regression provided a predictive model that included three variables: “perception of following well the GFD” (p = 0.003), “patient’s behavior in front of foods in social events” (p = 0.003) and “age of disea se onset” (p = 0.049). In the logistic regression model only two out of the three variables reached statistical significance (table 4).

Table 4 Logistic Regression with EMA-TTG, OR, adjusted. 

The GFD Knowledge Score did not show signifi cant differences for adherence by serology. When divi ding patients into those with a score of < 3 and those with a score of 4 in the Biagi questionnaire, half of the patients were grouped in each group. Patients with Score < 3 had 1.5 times more risk of transgressing the diet. Although this variable was not significant in the chi-square analysis, due to the importance of patient education, it was included in the multivariable logistic regression analysis.


The adherence to GFD in this study is lower than the one published in the international literature for this age group14,19, but similar to the ones described in our country in previous studies17-19, both by measurement of TTG and EMA antibodies and the questionnaire de veloped by Biagi. This indicates that the adherence to GFD among our pediatric patients is not only low but has not changed significantly in the last two decades. It is interesting that both methodologies showed concor dance since other studies have not shown it11.

The variable “perception” of following the GFD correctly, was the one that showed the best associa tion with negative markers, being always statistically significant. The patient who believes that he/she is not doing a correct diet has 3.4 times higher risk of not adhering than the patient that believes that he/she fo llows GFD correctly The second t variable best asso ciated with adherence was age of diagnosis. Patients diagnosed before two years of age showed significantly higher adherence to GFD than those diagnosed at later ages. One can think that the earlier CD is diagnosed, the easier it is to incorporate and accept the limita tions imposed by GFD8. The “attitude in birthdays” was significant when making a univariate analysis, but it lost significance in the logistic regression of associa tion, except in the group that “does not attend birth days”, which showed a greater risk of “transgressing the GFD”. This implies that not taking celiac children to birthday parties does not protect them from trans gressions to diet. That 90% of patients who did not attend a birthday presented positive serology (EMA or TTG) is against the expected; it could be interpre ted as a behavioral option to avoid the opportunity to transgress26.

The guardian and/or the patient’s “perception” of “being doing GFD properly” shows that two out of three patients who believe that they are following the diet, are really achieving it. This contrasts with the variables referring to knowledge itself about diet and gluten-free foods, which did not achieve statistical sig nificance in any of the analyses. On the other hand, in patients whose guardian thinks that they make mis takes in GFD, 75.9% have some positive serology. It is interesting that 24.1% of patients (seven children), despite thinking that they are doing poorly, either be cause they eat gluten in an obvious way or because they do not have clear their indications of feeding, main tained negative both antibodies. This supports the idea that serology is not a good indicator for follow- up11,27-29; it also opens the possibility that some patients have certain tolerance to small amounts of gluten without arising a detectable autoimmune response30. Another possibility is that the time elapsed between the transgression of the diet and the measurement of mar kers was insufficient to produce a detectable change. Undoubtedly, it is necessary to improve the capacities to measure gluten intake in celiac patients along time. Measurements of gluten in stools and/or urine seem an interesting option, but the currently available results are not sufficient to propose them as marker of follow up in t CD31-35.

In this respect, it is relevant to remind that if the re are doubts about whether a patient has elevated antibodies because he/she does not adhere to GFD or because he/she does not respond to treatment, a new duodenal biopsy is useful, as well as a genetic study if it shows absence of risk haplotypes. Unfortunately, genetic studies are not usually practiced in our country. It is interesting that the patient or guardian that reads the nutritional labeling of packaged foods showed signifi cant association with negative EMA. This relation with adherence could reflect a behavior of greater com mitment to leading a good management of the disease.

Results show that for health professionals to pro vide effective counseling to celiac patients, in addition to know the biological aspects of the disease, it is ne cessary they manage the emotional and social aspects imposed by chronic diseases. It must be considered that treatments that involve restrictions in daily life are difficult to maintain in the long-term and can affect quality of life26,36,37. This is important to highlight sin ce we must recognize the enormous benefit that most patients who follow GFD have; they manage to stay asymptomatic and avoid the risks of long-term com plications. In this sense, the chronic or sporadic consumption of medications and the intake of foods re lated to religious ceremonies gain interest. In the first case, it is important to choose gluten-free medicines and in case of not having safe alternatives, put in the balance the risk/benefit of each treatment. In the case of foods consumed in religious ceremonies, alternati ves suitable for celiacs must be offered to maintain ad herence to GFD, such as communion wafer for celiacs, as is the case in our country, where wafers are certified by the Archbishopric of Santiago. These aspects favor the integral recovery of the patient (physical, emotio nal and spiritual).

Due to the importance of patient education in the treatment of CD38,39, the multivariable logistic re gression analysis was adjusted by the knowledge sco re, although this was not significant in the univariate analysis. The fact that the “perception” of being doing correctly the GFD maintain its significance, seems to us a very relevant finding since it can be used to modify/reinforce behaviors and improve the follow-up and adherence to the treatment of celiac patients4.

Ethical Responsibilities

Human Beings and animals protection: Disclosure the authors state that the procedures were followed according to the Declaration of Helsinki and the World Medical Association regarding human experimenta tion developed for the medical community.

Data confidentiality: The authors state that they have followed the protocols of their Center and Local regulations on the publication of patient data.

Rights to privacy and informed consent: The authors have obtained the informed consent of the patients and/or subjects referred to in the article. This docu ment is in the possession of the correspondence author.

Financial Disclosure: INTA, Universidad de Chile. This study had no exter nal funding.

Conflicts of Interest: Authors declare no conflict of interest regarding the present study.

Acknwoledgements: Authors thank all professionals of the Gastroenterolo gy Unit, Hospital Roberto del Río, Santiago Chile that helped us conducting this study.


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Received: June 15, 2017; Accepted: December 14, 2017

Correspondence: Prof. Magdalena Araya

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