Coeliac disease (CD) is an immune-mediated disorder with chronic inflammation of the small intestinal mucosa as a response to food-induced gluten. Prevalence rates range from 0.5% to 1% in the United States and in Europe (1). The only treatment of CD is the elimination of gluten-containing food, which means exclusion of wheat, rye, and barley. Compliance with a lifelong gluten-free diet (GFD) is essential to prevent long-term complications. Compliance with a strict GFD leads to disappearance of medical symptoms and full histological and serological remission can be attained (2,3).
The screening of asymptomatic individuals for CD is still controversial; arguments against a screen detection imply that it may even be harmful for the individual because lifelong GFD is not easy to maintain and as a result the subject's quality of life (QOL) may deteriorate (4,5). It has also been found that screen-detected patients with CD experience an improved QOL after adhering to GFD for 1 year, indicating that the concern about the burden of GFD may be unfounded (6).
Nevertheless, the dietary restrictions can be difficult to accept and follow, especially in adolescence, a period in which most dietary transgressions have been found (7,8). Compliance with GFD in adolescents has been reported to be between 52% and 81% (9). Female and younger adolescents have been found to be more compliant. Good school grades and high self-esteem also contribute to good compliance (10). The highest compliance rates have been found in patients who are diagnosed as young children, and the most transgressions in adolescents and those diagnosed via mass serological screening. The majority of children struggle to accept GFD, in particular adolescents between the ages of 12 and 17. Whereas the difficulties related to GFD are absent in the sufferers' family environment, they emerge significantly at times of meeting and socializing with friends (11). Socially perceived situations such as travelling and dining out have been found to be troublesome and may lead to transgressions, which are often associated with feelings of anger and envy (12,13). Thus, adhering to GFD has an impact on not only food consumption but also on the general lifestyle and QOL of individuals with CD (12,14–16). To examine QOL is important and especially recommended for future research of individuals with CD (1,4,17,18).
Hallert et al (19) found less well-being in patients with CD who have been on GFD compared with the general population. Female patients with CD perceived not only more somatic symptoms but also more distress in daily life, which was associated with different coping styles in men and women (20). A qualitative analysis revealed problems with food situations at work, with food selection in the supermarket, when travelling, and with meals at home or while out (21). Attendant emotions in problem situations included isolation, shame, fear of gluten contamination, and concerns about being a burden to others. A representative study in Germany came to the conclusion that although health-related QOL improves after starting GFD, overall QOL is still lower than in the general population (22).
Studies on the subpopulation of children and adolescents are scarce. Kolsteren et al (23) found a similar QOL in children and adolescents with CD as in a healthy reference sample. Rashid et al (3) found that better food labelling, more gluten-free foods in supermarkets and restaurants, and an earlier diagnosis of CD would improve QOL. Social impact and feelings of isolation, difference, and embarrassment, as well as anger and envy, were reported, and the need for improvement of social and emotional outcomes of young people with chronic diseases was outlined (3,11,24,25). Nevertheless, these studies have limitations. They either concentrate on somatic complaints and concrete limitations in daily life imposed by the treatment regimen or on limited aspects of QOL. Methodological problems as small sample sizes, no differentiation between children and adolescents, and no age-matched control groups limit the power of these studies.
Therefore, we aimed to assess the following in a case-control design:
- QOL differences in compliant and noncompliant adolescents with CD, and to compare them with a healthy control group without a chronic condition
- Differences in satisfaction with life and feelings of ill-being in compliant and noncompliant adolescents with CD, and to compare them with a healthy control group without a chronic condition
- QOL differences of adolescents with CD depending on the age at diagnosis
- Differences in satisfaction with life and feelings of ill-being dependent on age at CD diagnosis
MATERIALS AND METHODS
The Inventory of Life Quality in Children and Adolescents (ILC) (26) measures subjective well-being and subjective satisfaction with different areas of physical and psychological conditions as well as with social contexts in life. Subjective well-being or satisfaction is self-reported by the patients. Nine different areas are assessed: school, family, social peer contacts, interests and leisure activities, physical health, psychological health, overall QOL judgement, and disease and therapy-associated burden. The ILC is a 9-item self-rating questionnaire with answer categories that are 5-point Likert scaled. Internal consistencies (Cronbach α) range between .55 and .76, retest reliabilities for the total score range between .60 and .80. The ILC is known as an economically applicable screening instrument for the assessment of QOL in children and adolescents with chronic physical and mental illness. It is a widely used instrument in many European countries for evaluation and quality assurance of treatments of children and adolescents with chronic physical and mental conditions.
The Berner Subjective Well-being Inventory (BFW) (27) is based on the theoretical aspects of well-being as a cognitive and emotional experience, and has been constructed to measure “satisfaction” and “illness” as basic dimensions of subjective well-being. The components of satisfaction are “positive attitude towards life,” “self-esteem,” “depressive mood,” and “joy in life.” Ill-being comprises “problem perception” and “somatic complaints.” The BFW is a 39-item self-report questionnaire, with answer categories that are 4- and 6-point Likert scaled. Retest coefficients are .75 after 2 weeks and .50 after 2 years. Cronbach α for subscales of first order range from r = .60 to r = .87, for subscales of second order from r = .61 to r = .78.
Recruitment for this study was part of a larger project involving male and female adolescents with CD, assessing biopsychosocial factors affecting their eating behaviour (28). The study protocol was approved by the Medical University of Vienna and informed written consent was obtained from participants and a parent for minors. Participants were contacted via the Austrian and German coeliac societies, as well as 7 gastroenterology departments in Vienna, Klagenfurt, Villach, Graz, Wels, and Salzburg. Different contact approaches have been applied. In the case of the Austrian Coeliac Society, an announcement of the study was published in the quarterly nationwide newspaper “Zöliakie aktuell,” and interested participants with CD contacted us via telephone, the Internet, or letter. In the case of the gastroenterology clinics, all patients between 10 and 20 years old with CD were contacted by these clinics asking them to participate in our study, and those willing to participate contacted us via telephone, Internet, or mail. Participants fulfilling the inclusion criteria received a letter containing study information, consent letters, and all questionnaires. In Germany, a letter of announcement was sent to 250 adolescents with CD in the regions of Bavaria and Baden Württemberg before they received the letter with the questionnaires. From the German sample, 101 (40.4%) were interested in participating.
In Austria, 118 (49.6%) interested patients answered the advertisement in the Austrian newspaper for patients with CD. Through the Austrian clinics, 259 patients were approached and 120 displayed interest in participation. In summary, 339 patients with CD—238 (70.2%) in Austria and 101 (29.8%) in Germany—were sent questionnaires. Inclusion criteria were secured diagnosis of CD by biopsy and antibody tests; adhering for at least 1 year to GFD since diagnosis of CD; current age between 10 and 20 years; no other additional chronic condition such as diabetes, ulcerative colitis, or autism; and intellectual suitability.
Of the 339 initially interested patients, we received 310 complete questionnaires. Inclusion criteria were fulfilled by 283 (91.3%) participants; 5 (1.6%) did not have a secure diagnosis or held no diet at all, 3 (1%) did not fulfil the 1-year criterion since diagnosis, 1 (0.9%) did not fulfil the age criterion, 16 (5.2%) had a second chronic disease, and 2 (0.6%) were not intellectually suitable. A total of 283 participants with CD could be included for further analysis.
For control comparisons, we collected data from 82 controls without a chronic condition in high schools in Austria. A group matching has been performed, allocating to each age group an equal percentage of sex-matched controls, considering education and social status. For missing cases, we recruited new controls corresponding to the match.
Power analysis has revealed a power of 99.5%, assuming an average value of 1.5 (standard deviation [SD] 0.75) in QOL (measured by ILC) in healthy controls and 2.0 (SD 0.75) in a clinical sample, and an α error of 5% in a sample size of n = 80 per group.
For group comparisons, analysis of variance with post hoc Tukey has been used when criteria for normal distribution have been fulfilled, otherwise Kruskal-Wallis and exact tests were applied. To control for additional influencing variables that affected dependent variables, univariate general linear models were used.
From the total CD sample, 210 (74.2%) were females and 73 (25.8%) were males. Mean age in the female population was 14.83 (±3.00) years, in the male population 13.90 (±2.72) years. Of the patients with CD, 80.8% adhered strictly to GFD, 14.9% reported 2 to 3 dietary transgressions per month, and 4.3% more frequent dietary transgressions. Patients noncompliant with CD treatment were significantly older than compliant patients and healthy controls (χ2 = 21.284; df = 3; P = 0.000). Groups differed in current body mass index (BMI) (χ2 = 27.320; df = 3; P = 0.000), with the noncompliant groups having the highest current BMI, followed by healthy controls, and the compliant group showing the lowest BMI. No difference regarding duration of CD has been found within the CD group according to compliance status (χ2 = −4.228; df = 2; P = 0.121) Anti-gliadin antibodies class immunoglobulin (Ig)A were significantly more positive in the last blood checkup in noncompliant patients than in compliant patients (χ2 = 6.253; df = 2; P = 0.044). A nonsignificant higher percentage of IgG class anti-gliadin antibodies and endomysial antibodies in the last blood checkup was found in the noncompliant patient groups (Table 1).
Of the subjects, 168 (59.6%) were diagnosed as having CD before the age of 6 and assigned to the group “early CD diagnosed,” and 114 (40.4%) received their diagnosis after the age of 6 years and labelled as late CD diagnosed. Applying 1-way analysis of variance, both groups and the healthy control group did not differ in age but differed in current BMI (F = 4.024; df = 2; P = 0.019). Post hoc Tukey revealed that patients with CD and a late diagnosis had a significantly lower BMI (mean 18.79, SD 2.61) than healthy controls (mean 19.98, SD 3.09).
QOL Differences Between Compliant and Noncompliant Patients With CD and Healthy Controls Using ILC
Noncompliant patients with CD reported more family problems and problems in their leisure time than did compliant patients and healthy controls. Worse physical health and worse general QOL was found in noncompliant patients compared with compliant patients and healthy controls. Regarding “CD-associated burden” and “CD assessment and treatment-associated burden,” noncompliant patients perceived more subjective burden than compliant patients. Impairment of QOL tended to be more prominent in almost all dimensions in patients with CD and frequent dietary transgressions compared with patients with CD and 2 to 3 monthly dietary transgressions, reaching significance in the global QOL score. No differences in family problems, physical health, and global rating of QOL have been found between compliant patients with CD and healthy controls. Applying univariate general linear models, age was found to have an effect on the assessment of physical health (F = 3.213; df = 1; P = 0.022) and global rating of QOL (F = 6.067; df = 1; P = 0.014), but group differences still remain significant after accounting for age (Table 2).
Differences between early and late diagnosed CD patients and healthy controls using the ILC: Patients with a late CD diagnosis reported poorer QOL in the areas of school, physical health, and CD-associated burden than patients with an early diagnosis of CD, and they perceived more problems in social contact with peers than healthy controls (Table 3).
Well-being and Ill-being Differences Between Compliant and Noncompliant Patients With CD and Healthy Controls Using BFW
Noncompliant patients with CD showed a higher problem anticipation in the future and a generally higher feeling of ill-being than both compliant patients with CD and healthy controls; no differences in these aspects were found either between patients with frequent dietary transgressions and patients with 2 to 3 monthly dietary transgressions, nor between compliant patients with CD and healthy controls. Higher feelings of well-being have been reported in compliant patients with CD compared with noncompliant patients. No significant differences have been found between patients with frequent dietary transgressions and patients with 2 to 3 dietary transgressions. An influence of age has been assessed regarding ill-being (F = 13.895; df = 1; P = 0.000), but group differences remained significant after controlling for age effects (Table 4).
Differences Between Early- and Late-diagnosed Patients With CD and Healthy Controls Using BFW
No differences in well-being, ill-being, or the corresponding subscales could be found between patients with early or late CD diagnosis and healthy controls.
This is the first time that QOL, well-being, and ill-being have been assessed in a well-defined adolescent population with CD in a case-control design using a sufficiently large sample size. Differences according to compliance status and age of CD diagnosis have been analyzed.
We found that adolescents who were noncompliant with their GFD experienced a lower general QOL, especially lower physical health, with a higher feeling of ill-being, more family problems, and problems in their leisure time. CD-associated burden has been highest in patients with frequent dietary transgressions. They anticipated their future would be more difficult. In contrast, patients compliant with their GFD perceived an equally good QOL in all areas as healthy controls without a chronic disease. This indicates that strictly adhering to the diet does not affect QOL in adolescence and does not lead to deterioration in well-being. According to our results, even though GFD represents a challenge for both affected children and their parents, especially in the period of adolescence (9), if they are diagnosed early and are able to cope with CD and adhere to strict GFD, they do not have to experience an impairment in QOL.
In previous studies on QOL, an optimal QOL was assessed for children with CD defined by only physical health and in the absence of symptoms (23). Regarding QOL, social and psychological aspects also must be taken into consideration. Doing so, lower QOL in children with CD was found compared with a healthy reference group (9). Physical and psychosocial impairments have been found in adult women with CD who had been on GFD for 10 years, but not in men, which has been explained by different coping strategies (20,29). Besides the physical aspects of QOL, CD-associated burden and feelings of illness, our study shows that being noncompliant with GFD is associated with more problems within the family and in leisure time, and a higher anticipation of problems in the future. Further research is needed to find out whether this is an effect of noncompliance or a reason for noncompliance, and prospective studies are needed to answer this question. Self-esteem, general mood, and joy in life are not effected by compliance or illness status, and do not differ from those attitudes of a healthy reference group without a chronic disease.
Although Cinquetti et al (11) found difficulties in socializing with friends in adolescents with CD, but no problems within the family, Sverker et al (21) reported problems in both areas. Our results detail this further: Only noncompliant patients experience more family problems. Compliant patients do not perceive more problems with their families than healthy controls. Neither noncompliant nor compliant patients with CD perceive social contact with peers as difficult. Those who do have problems in social contact with peers are patients with a late CD diagnosis. No differences between patients with an early CD diagnosis and healthy controls in social contact with peers have been observed. Also, age at diagnosis does not affect family problems.
An important Canadian study comes to the conclusion that an early CD diagnosis led to an increased QOL (30). Our results affirm this conclusion, showing that late CD diagnosis is associated with not only more physical problems and CD-associated burden but also problems at school and with social contact in the peer group. Age at diagnosis, however, had no effect on life attitude, problem anticipation, self-esteem, non–CD-associated somatic complaints, mood, or joy in life—summarized as subjective well- and ill-being in life—and subjective judgments in these areas were comparable to those of healthy controls without a chronic disease.
Our study reveals that a better physical, psychological, and social QOL can be obtained by strict adherence to GFD. Educational and psychological support should be provided for those patients who show dietary transgression in adolescence. Diagnosis of CD at an early age (before 6 years) leads to better physical and social QOL and lower burden of disease. Therefore, it is important that patients with CD are diagnosed as early in life as possible.
We thank all of the patients, the cooperating centers (LKH Wels, LKH Klagenfurt, LKH Villach, Preyer'sches Kinderspital, LKH Graz, and LKH Salzburg), and the Austrian and German coeliac societies for their help in conducting the study. We also thank Astrid Eisenkölbl, Helga Hübner, and Martina Cislakova for their help in data collection and entry.
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