Evaluation of adherence to gluten-free diets in Moroccan celiac patients and factors of adherence failure

. The prevalence of celiac disease (CD) is increasing in the world. In Morocco, its incidence is also increasing considerably. The gluten-free diet (GFD) remains the only effective treatment so far. Its effectiveness depends essentially on good adherence to this diet. However, several factors hinder adherence by contributing to diet failure. Within this framework, this study aims to evaluate adherence to this diet in celiac children and adolescents continuing in a tertiary health center. The article also looks to identify the different factors influencing adherence to GFD in Morocco. The results show from serological and/or biopsy tests on 238 celiac patients that half had good adherence and 13% had poor adherence. The questionnaire aimed at 127 parents or proxies of celiac children and adolescents shows that several factors are responsible for the failure to adhere to the diet such as the role of the mass media, cultural and psychological factors. The exorbitant price, nutritional quality, and low availability of gluten-free products play a major role in GFD failure. Low socio-economic factors have a negative influence on the adherence to the GFD.


INTRODUCTION
The ingestion of gluten found in wheat (gliadin), barley (ordein), and rye (secalin) causes immune reactions in some susceptible people [1]. This is celiac disease (CD), which destroys intestinal villi by causing poor absorption of nutrients [2]. It affects about 0.7 to 1.4% of the world's population [3]. It affects their quality of life [4]. The gluten-free diet (GFD) remains the only treatment to follow [5]. The patient is obliged to consume only naturally gluten-free foods and/or foods developed by industrialists and labelled "gluten-free". However, adapting to this change in eating habits is a great challenge for these patients. It is a question of having a good adherence to this diet [6]. According to Sevinc [7], Serological tests (anti-transglutaminase antibodies, antideamidated gliadin peptid antibodies, and anti-Endomysium antibodies) and/or duodenal biopsy can be used to confirm the disease and also to confirm level of adherence to GFD.
Good adherence to this diet corrects damage to the intestines and thus corrects the absorption of macros and micronutrients [8]. However, there are several factors that hinder good adhesion. These are the factors of failure to adhere to this regime. According to a review and metaanalysis conducted by MacCulloch et al. [9], cost, availability, labelling of gluten-free products (GFPs), are the factors of failure related to products used by celiac patients. In 2019, according to a joint review and metaanalysis by Xhakollari et al. [10], the review classifies the factors affecting GFD in eight groups: "Factors specific to the GFD"; "Socio-demographic factors"; "GF products' factors"; "Psychological Factors"; "Symptoms related to Celiac"; "Celiac Disease's factors"; "Quality of Life"; "Other Factors". However, no studies included in this review have been carried out in Africa. The overwhelming majority of the studies were carried out in Europe, North America, Australia, and South America by 47%, 29.7 and 15% respectively. Asia was represented only by 2% [10]. Highlighting the factors is essential for suggesting preventive and corrective actions to overcome factors and improve the level of adherence to this diet which is the only treatment for CD as well as any glutenrelated disease such as wheat allergy, gluten ataxia, dermatitis herpetiformis, sensitivity to non-coeliac gluten [11].
In Morocco, the prevalence of CD is unknown. However, the number of new cases is increasing considerably [12]. Hence, the need to have a good adherence to this GFD with the availability of all the factors of success to this adherence. It is within this framework that the objective of the present research is set. On the one hand, it is a question of highlighting the level of adherence to the GFD. On the other hand, the factors that contribute to the failure to adhere to the GFD should be determined.

Materials and methods
This study is divided into two parts. The first aims to assess adherence to the GFD. The second aims to determine the factors that contribute to the failure to adhere to the GFD.

Adherence to gluten-free diet
The study was carried out on 238 celiac children and adolescents between the ages of 2 and 15. The female sex is the most represented in this research with 154 girls (64.7%). However, the difference between the two sexes was non-significant (p=0.074).
The results of serological tests and intestinal biopsy showed that 52.94% of these patients represent good adherence to GFD. However, 13.87% of the patients showed poor adherence to the GFD. While 33.19% show an alternation between poor and good adherence. In the study conducted in Algeria in 2014, the prevalence of poor adherence was higher than in the present study (48% vs. 13%) [13]. However, the prevalence of good adherence after GFD in India was very high (92%) [14]. Table 1 presents the impact of the origin of residence of celiac children and adolescents on adherence to the GFD.

Fig. 1. prevalence of adherence to the gluten-free diet
The Chi-square test shows that celiac children and adolescents residing in rural areas adhered better to the GFD than those in urban areas. The latter had a worse adherence than those in urban areas. The impact was with a highly significant difference (p˂0.001) (Figure 1). Multiple Correspondent Analysis (MCA) has made it possible to show the correlation that exists between adherence and certain socio-economic and demographic factors whose variables are greater than 3. The MCA factor map shows that good adherence is correlated with children under 5 years of age. It is also correlated with people with average economic status. Failure to adhere is correlated mainly with illiterate parents with low economic status. It is also correlated with teenagers above the age of 12. Average adherence is rather correlated with children in the age group between 5 and 12 years old (Figure 2).

Factors that influence the adherence to gluten-free diet
The questionnaire is aimed at 127 parents or proxies of celiac children and adolescents. They were asked to confirm or not the contribution of these factors in the failure of GFD. 96% of the parents or proxies stated that media awareness is poor and in their opinion a factor in the failure to adhere to the GFD. The role of awarenessraising by the media (TV, radio, newspapers) is omniabsent. On the other hand, only 23% who see social networks as a factor of failure. The majority of parents or proxies saw that social networks (Facebook, what sup)  78% of the respondents also see that cooking at home is a factor in the failure to provide adequate single-use equipment for celiac patients. Cross-contamination at home is common during the preparation of gluten-free meals. Firstly, the blenders used to grind cereals or other foods by celiac patients are very expensive. This makes cross-contamination common if the washing is not done properly. So, it is advisable to rigorously apply methods for cleaning kitchen equipment and utensils [19].
Consultation with pediatricians and dieticians is not a major factor in failure. Almost half of the patients regularly visit them at home. These consultations improve the level of knowledge about gluten. Half of the parents or proxies see this last factor (knowledge about gluten) as a factor in failure.
Finally, in-food service meals are not a factor of failure. Only 39% see the opposite. This is mainly due to the fact that parents prevent their children from eating away from home. gluten-free foods are not enriched with nutrients such as iron and folic acid. These elements are necessary to reward the deficits noticed in celiac patients due to malabsorption secondary to the destruction of intestinal villi. This is confirmed by a study carried out in Morocco in 2020 which showed that the nutritional quality of PFG is unbalanced [24]. This impacts on the quality of life of Moroccan patients, which is poor in Moroccan children [25].

Fig.4. Factors related to gluten-free foods
The association between GFF-related factors and socioeconomic and demographic factors has shown that GFPs are more available in the urban environment. These people have a high economic situation considering that GFPs are cheap. While the availability of GFPs is mostly correlated with a very expensive price, especially in rural areas where the educational level of parents is dominated by illiterate parents, the availability of GFPs is also very high in rural areas ( Figure 5).

Conclusion
Half of Moroccan celiac children and adolescents have a good adherence to the GFD. However, 13% have poor adherence. Adherence is poorer among children and adolescents in rural areas than in urban areas. Poor adherence is also correlated with parents with low economic and educational levels. The factors are diverse, mainly citing the lack of awareness via the mass media (TV, radio, newspapers), cross-contamination during cooking at home, psychological factors and cultural factors. Factors related to GFPs contribute greatly to the failure of GFD. GFPs are scarcely available, expensive, and of poor nutritional quality. This situation is more serious in rural areas and among parents with low economic and educational levels.