Knowledge and opinions of asymptomatic adolescents and their caregivers on celiac disease screening

Abstract

Objectives

Celiac disease (CD) is an immune enteropathy caused by sensitivity to gluten affecting one per cent of the general population. Most people with CD are asymptomatic and some may be affected from childhood. Despite the latest recommendations of paediatric gastroenterology societies, targeted screening is still uncommon in clinical paediatric settings. A poor understanding of the asymptomatic population’s opinions creates obstacles for broader implementation of CD screening. This study aims to fill this gap by reporting on the knowledge and opinions of adolescents and caregivers of children on CD screening.

Methods

Adolescents with absence of classical symptoms of CD and caregivers of presumably asymptomatic children were asked about their knowledge and opinions of CD through a self-administered questionnaire.

Results

There were 227 respondents including 76 adolescents and 151 caregivers. A minority of respondents (8% of caregivers and 23% of adolescents) were identified as having a CD-associated condition (such as hypothyroidism, type 1 diabetes, Down syndrome, etc.). A majority of caregivers (84%) and half of adolescents (49%) already knew about CD. Half of the respondents (46%) were in favour of screening asymptomatic paediatric populations and this agreement increased to 81.7% when they were confronted with hypothetical risks of 10%.

Conclusion

This study reveals an increased willingness to screen when participants were faced with increasing hypothetical risks. This suggests that screening recommendations targeting high-risk populations, such as those of paediatric and non-paediatric gastroenterology societies, may be more widely accepted.

Celiac disease (CD) is an inflammatory reaction caused by a permanent immune sensitivity to gluten resulting in villous atrophy of the small intestine (1). People affected by CD are at increased risk of short stature, delayed puberty, vitamin deficiency, osteoporosis, and gastrointestinal cancer (2,3). However, most people with CD are asymptomatic and remain undiagnosed. In the paediatric population with CD, it is observed that the ratio between symptomatic and asymptomatic children is 1:7 (9,10–12).

Systematic screening of CD in populations with increased risk (such as type 1 diabetes mellitus, Turner syndrome, Down syndrome, Immunoglobulin A [IgA] deficiency, hypothyroidism, etc.) was recommended by paediatric and non-paediatric gastroenterology societies to help reverse these adverse health outcomes (13–18). Screening involves a simple serologic test (anti-tissue transglutaminase IgA) with validation of positive results by intestinal biopsy (19). The current effective treatment is the adoption of a strict gluten-free diet. However, the natural history of CD in asymptomatic populations is not well documented and the few studies exploring the long-term benefits of detecting and treating asymptomatic patients reported contradictory results (20,21). Moreover, the treatment is expensive and shows poor compliance among asymptomatic patients. In connection with these barriers, clinicians may be ambivalent about screening asymptomatic high-risk groups. Investigations of patient perception and satisfaction relating to CD diagnoses are rare but obtaining their views may influence clinicians in their decision to screen. Our study aims to evaluate the knowledge and opinions of presumably asymptomatic adolescents and of caregivers of presumably asymptomatic children on CD screening.

PATIENTS AND METHODS

Design, population, and recruitment

This is a cross-sectional descriptive study using a convenience sample of caregivers with children under 18 years of age and of adolescents between 14 and 17 years of age presenting in a paediatric outpatient clinic at the Centre Hospitalier Universitaire de Sherbrooke (CHUS). The targeted age range of 14 to 17 years old for adolescents was selected because under our legislation, they can freely participate in a research study without the permission of a parent or guardian. Participants were approached either directly by a research assistant or indirectly through an information brochure given at the front desk and freely accessible in the waiting room. Adolescents or caregivers of children with classic symptoms of CD (such as diarrhea, abdominal pain, unexplained loss of weight/growth impairment or anemia) or with a diagnosis of CD were excluded from this study. In this context, we consider them as presumably asymptomatic for CD as we were not able to exclude atypical presentation of CD. For the purpose of this survey, we did not distinguish nor exclude different types of caregivers (such as biological parents, adoptive parents, legal authority).

Recruitment was conducted over a 4-week period between November and December 2015. Participants’ knowledge and opinions were collected through a structured questionnaire that was self-administered. Implied consent of the participant was confirmed by completion and returning of the questionnaire. This study was approved by the hospital’s Research Ethics Board (2016-1084). Collected data were kept confidential and anonymous.

Measures

The questionnaire was created using expert advice and a literature review on the subject of CD. The questionnaire was created in French as the population in our city is francophone. The structured questionnaire consisted of three parts for a total of 18 main questions (eight knowledge questions, seven arguments in favour of or against screening, and three questions about willingness to screen). In the first section, evaluating the participants’ knowledge of CD, we referred to two studies that surveyed caregivers of children with CD to identify important elements to include in this section of the questionnaire (23,24). We started by asking the respondents if they had already heard of CD or gluten intolerance. Then, their knowledge was assessed by asking eight multiple-choice questions on CD-related subjects. In the second part, evaluating the opinion of the participant on screening for CD in an asymptomatic paediatric population, the pro and con arguments were based on various reports and expert advice (22,25–28). These seven questions were preceded by an explanatory text about CD that was sufficiently detailed so that participants could give clear consent about a screening test. Respondents were then asked to describe to what extent they agreed, on a six-point Likert scale, with seven arguments. The first three were arguments in favour of CD screening; the next four were arguments against CD screening. At the end of this section, respondents were asked, through three different questions, whether they were in favour of or against screening. First, we asked their opinion about screening without any reference to prevalence or risk of the disease. Those who were reluctant to undergo screening were asked again with the perspective of a hypothetical risk being 1% and 10%, which is close to the prevalence of CD in the general population and in a high-risk population, respectively (4). We did not ask the opinion of high-risk groups directly because we did not want them to feel directly involved and possibly create feelings of insecurity if they had never received information from their treating physician. This could have harmed the professional relationship and put the treating physician in a position where he or she felt pressure to screen for CD. This is why we asked presumably asymptomatic outpatients with no increased risk but put them in a hypothetical situation reflecting an increased risk to get their opinions. In the last part, respondents were asked to answer complementary questions, such as demographic and medical data. The questionnaire was pretested by five caregivers and five adolescents to ensure readability and adequate comprehension for future users.

Analyses

All analyses were conducted using SPSS 24.0. Continuous variables were described with mean and standard deviation when normality was confirmed visually. Categorical variables were described with frequencies and percentages. Chi-squared tests were used to compare categorical variables sex and opinion toward screening, between adolescents and caregivers. Chi-square tests were also used to compare knowledge questions between adolescents and caregivers. Univariable and multivariable logistic regressions were used to predict opinion on CD screening with 1) knowledge questions as predictor and with 2) argument Likert scales as predictors. McNemar’s test was used to assess the variation in time of a categorical variable (attitude toward screening depending on relative risk of the disease). Finally, Wilcoxon paired tests were used to compare argument Likert scales among each other while Mann–Whitney tests were used to compare argument Likert scales between two groups (adolescents versus caregivers or in favour of screening versus against screening). Significance level was determined at 0.05.

RESULTS

Population

Unfortunately, we do not have the specific information regarding response rate or the number of excluded participants as the majority of participants were approached indirectly through an information brochure given by the secretary at the front desk or freely accessible in the waiting room. We recruited them over a 4-week period and we have estimated a mean of 260 adolescents and 1,400 caregivers at the outpatient clinic during that period of time. Based on this, we can estimate a response rate of approximately 29% for adolescents and 11% for caregivers. Out of a total of 227 collected questionnaires (76 adolescents and 151 caregivers), 26 (11%) had at least one question missing (9 adolescents and 17 caregivers) from the 18 main questions. Missing data were considered as missing by chance and analyses were carried out on available data. Female gender was predominant in the caregiver group but not in the adolescent group (76% [109/144] and 55% [38/69] respectively, Chi-squared test P=0.002). Also, 82% (117/142) of the respondents in the caregiver group had a postsecondary education. In the caregiver group (n=144), mean age was 38.92 with a standard deviation of 8.27 and age ranges from 23 to 69 years old. In the adolescent group (n=69), mean age of participants was 15.43 with a standard deviation of 1.06 and age ranges from 14 to 17 years old.

About half of the caregivers (51% [73/144]) and a minority of adolescents (29% [20/69]) knew someone with CD. Of the 93 participants who knew people suffering from CD, 8 caregivers said it was themselves (11%), 30 respondents (32%) said they knew a member of their family suffering from CD, and 65 (70%) said they knew someone suffering from CD in their social circle. A minority of the caregivers’ children (8% [12/144]) and of adolescents (23% [16/70]) were known for a CD-associated condition (Down syndrome, IgA deficiency, hypothyroidism, type 1 diabetes, and/or Turner syndrome). Among this high-risk group, only 14% (4/28) reported having undergone a previous CD screening compared to 10% (18/185) of total respondents.

Knowledge of CD

A majority of caregivers (84% [124/148]) and half of the adolescents (49% [37/75]) had already heard of CD. Caregivers had a better knowledge of CD than adolescents (Table 1). Treatment of CD was known by a vast majority of respondents (89% [197/221]). In contrast, symptoms and complications of CD were only known by a minority of respondents (42% [94/224] and 8% [18/222], respectively).

Table 1.

Percentage of respondents with the right answer for each knowledge question about CD for adolescents and for caregivers

Knowledge questions	Number of respondents with the right answer (%)		Significance
	Adolescents (n=75)	Caregivers (n=149)
Food with gluten	50 (67%)	127 (85%)	**
Prevalence	60 (80%)	112 (75%)
Duration of disease	41 (55%)	102 (68%)	*
Symptoms	32 (43%)	62(42%)
Onset of CD	46 (61%)	117 (79%)	**
Complications	4/74 (5%)	14/148 (9%)
Diagnostic	47/73 (64%)	96/148 (64%)
Treatment	57/72 (79%)	140 (94%)	**

*0.01≤P<0.05; **P<0.01.

Opinion toward screening an asymptomatic paediatric population

Without specifying the risk of a presumably asymptomatic child having CD, 46% (101/219) of all respondents were in favour of screening a paediatric population (Figure 1); no difference was found between the adolescent and the caregiver groups (Chi-squared test P=0.80). When a hypothetical 1% risk of CD was presented to the respondents who were previously against screening, 21 (10%) respondents answered that they would be in favour of screening (6 adolescents and 15 caregivers). Furthermore, when subsequently confronted with the higher hypothetical risk of 10%, 78 respondents (36%) who were previously against screening became in favour of CD screening (27 adolescents and 51 caregivers). After multivariable analysis, we were able to identify one factor that influences opinions toward screening among the adolescent group. Having a right answer in the onset CD knowledge question increases the odds of having a positive opinion about screening (odds ratio [OR]=2.94; 95% confidence interval [CI]: 1.04 to 8.31, logistic regression P=0.043). In the caregiver group, a previous test for CD in their children was a factor that positively influenced their opinions (OR = 8.65; 95% CI: 1.86 to 40.29, logistic regression P=0.006).

Figure 1.

Respondents in favour of screening depending on the hypothetical risk of celiac disease. *McNemar’s test P<0.001 compared to undisclosed hypothetical risk.

Arguments influencing opinions

Regardless of their group and of their opinion toward screening, the majority of respondents agreed more with arguments in favour of screening (first three arguments) than with arguments against screening (last four arguments) (Figure 2). ‘Unnecessary gastroscopy’ was the argument against screening that gained the highest approval (Paired Wilcoxon test, comparison argument Q5 versus Q4, Q5 versus Q6, and Q5 versus Q7, all P<0.001; no other pairwise comparison between arguments was significant) (Figure 2A). There was no difference for level of agreement between adolescents and caregivers except for the ‘lifelong gluten-free diet’ argument which was a more important argument against screening for adolescents than for caregivers (Mann–Whitney test P<0.001; Figure 2B). For each argument, there was a significant difference between the group in favour of and the group against screening regarding the mean scores of agreement (Mann–Whitney test, all P<0.03). Considering a multivariable model to predict the position in favour of the screening, two arguments, the ‘right to know’ and the ‘resolution of health problems’ were significant predictors (Table 2).

Figure 2.

Likert scale responses to arguments concerning CD screening (a) comparing adolescents and caregivers responses (b) comparing respondents in favour or against screening.

Table 2.

Results from logistic regressions predicting the position of being in favour of screening (when no risk is presented) according to the arguments and the type of respondents

Arguments	Univariable models		Multivariable model
	OR [95% CI]	P-value	OR [95% CI]	P-value
Right to know	2.35 [1.85–2.99]	<0.001	1.66 [1.18–2.35]	0.004
Resolution of health problem	2.72 [2.02–3.67]	<0.001	1.75 [1.18–2.60]	0.006
Long-term benefits	2.40 [1.77–3.27]	<0.001	1.09 [0.69–1.73]	0.71
Pain associated	0.57 [0.42–0.76]	<0.001	0.88 [0.61–1.29]	0.53
Unnecessary gastroscopy	0.73 [0.61–0.88]	0.001	0.91 [0.71–1.17]	0.47
Lack of long-term benefits	0.74 [0.58–0.95]	0.02	0.97 [0.66–1.42]	0.86
Lifelong gluten-free diet	0.78 [0.61–0.99]	0.04	1.09 [0.77–1.55]	0.63
Being in the parents’ group	0.93 [0.53–1.63]	0.80	---	---

CI Confidence interval; OR Odds ratio.

DISCUSSION

This is the first study assessing the knowledge and opinion of a presumably asymptomatic paediatric population followed in an ambulatory clinic and their caregivers regarding CD and its systematic screening.

The analysis showed that caregivers had better knowledge of CD than adolescents. Despite this difference, both groups shared similar opinions toward CD screening. This finding correlates with a similar previous report where caregivers and adolescents both agree with an early and systematic screening of CD (22).

To our knowledge, only one study has also investigated the attitude of caregivers and adolescents toward paediatric mass screening (22). Rosen’s study showed that 92% of caregivers wanted CD screening to be implemented and that adolescents generally had positive opinions of screening. This finding contrasts with our observation of 46% of respondents that agree with systematic screening for CD among a presumably asymptomatic, low-risk population. While Rosen’s study consisted of adolescents with screening-detected CD and their caregivers, our study concerned a presumably asymptomatic and undiagnosed population. Comparing our results to theirs, we can postulate that an increase in the level of pretest probability of having CD among respondents can influence their opinion toward screening. In our study, when confronted with an increased hypothetical risk of having CD, more respondents reported that they would support CD screening.

A majority of respondents agreed more with arguments in favour of screening than with arguments against screening regardless of their final opinion. Literature reveals that adherence to treatment is one of the main issues reported by the diagnosed patients that comply with the strict gluten-free diet in 36 to 80% of the cases (29–31). However, the argument related to the gluten-free diet was not considered as a major barrier to screening in our study. Among the arguments against screening, the ‘unnecessary gastroscopy’ was the one with the highest score of agreement, though only 24% of adolescents and 32% of caregivers agreed with this argument. Interestingly, the respondents’ opinions remained consistent throughout the questionnaire. Those in favour of CD screening had a higher score of agreement with arguments in favour of screening and vice versa. However, for those against CD screening, the use of the six-point Likert scale revealed nuanced opinions compared to the question using dichotomous answers. Although these respondents affirmed that they were against systematic CD screening, they were mostly in agreement with arguments in favour of screening. This may reflect that arguments against screening have more influence in their final decision making.

Our study has some limitations. First, participants self-enrolled and self-administered the questionnaires. This may have generated missing data and introduced some bias such as selection of a high percentage of postsecondary education level for caregivers. It is possible that family members without a postsecondary education were not as aware of the added value of participating in a research project or may have anticipated some level of difficulty in filling in the questionnaire and did not choose to participate.

Even though the questionnaires were pretested for readability with 10 people before the study, the questionnaire was not formally validated. Focus group discussions would have been more appropriate than the questionnaire to highlight respondents’ arguments and deeper reasoning behind their opinions. By questioning different hypothetical risks, we may have measured the impact of rising prevalence for willingness to screen. Further research must be done to measure whether the absolute prevalence rates impact on thinking regarding screening.

One of the strengths of the study is the high number of respondents. As well, this is the first time that the presumably asymptomatic paediatric population is questioned about their knowledge of and opinions toward CD.

CONCLUSION

Mass screening was not acceptable to the majority of participants. However, we saw increased willingness to screen when participants were faced with increasing hypothetical risks. This suggests that screening recommendations targeting high-risk populations, such as those of paediatric and non-paediatric gastroenterology societies, may be more widely accepted, although this remains to be specifically studied.

Institution: Centre Intégré Universitaire de Santé et Services Sociaux de l’Estrie – Centre Hospitalier Universitaire de Sherbrooke (CIUSSSE-CHUS)

Ethics board: Research Ethics Board (REB) of Centre Intégré Universitaire de Santé et Services Sociaux de l’Estrie – Centre Hospitalier Universitaire de Sherbrooke (CIUSSSE-CHUS)