SUDANESE JOURNAL OF PAEDIATRICS

2021; Vol 21, Issue No. 2

ORIGINAL ARTICLE

Evaluation of dietary compliance among Sudanese children with coeliac disease

Sakeena NourEldine Salih (1), Fathia Hassan Mubarak (2), Ali Elimam (3), Ali Arabi (4)

(1) Department of Pediatrics and Child Health, National University, Khartoum, Sudan

(2) Nutrition Department, Ibn Sina Hospital, Khartoum, Sudan

(3) Department of Obstetrics and Gynecology, Faculty of Medicine, Al Neelain University, Khartoum, Sudan

(4) Department of Paediatrics and Child Health, Faculty of Medicine, University of Khartoum, Khartoum, Sudan

Correspondence to:

Sakeena NourEldine Salih

Assistant professor of Pediatrics and Child Health, National University, Khartoum, Sudan

Email: skinasalih2018 [at] gmail.com

Received: 13 October 2020 | Accepted: 07 March 2021

How to cite this article:

Salih SN, Mubarak FH, Elimam A, Arabi A. Evaluation of dietary compliance among Sudanese children with coeliac disease. Sudan J Paediatr. 2021;21(2):137–143.

https://doi.org/10.24911/SJP.106-1602600969

ABSTRACT

The compliance to a gluten-free diet in Sudan is difficult because many Sudanese tribes depend on wheat product for their food with no access to gluten-free food. To evaluate dietary compliance among Sudanese children with coeliac disease (CD), a longitudinal, prospective and hospital-based study was carried out at Ibn Sina Hospital (Coeliac Clinic) and Gaafar Ibn Auf Children’s Hospital (Gastroenterology Clinic) from July 2011 to February 2012. Fifty children diagnosed with CD, followed for more than 6 months, were assessed for dietary compliance. Dietary good-compliant and poor-compliant groups were compared to assess factors affecting the dietary compliance. History, clinical examination and investigations were done initially and then 6 months later. Diagnosis of CD was based on serological tests and duodenal biopsy. The mean age of children with CD was 6.5 (± 2) years. More than three quarters of participants (38%-76%) had poor dietary compliance. Causes of poor compliance were as follows: in 7 (18.4%) was due to refusal of children, in 9 (23.7%) due to unpalatability of gluten free diet (GFD), in 12 (31.6%) due to difficulty in finding GFD and in 10 (26.3%) due to lack of awareness of parents about CD and GFD. The study showed significant correlation between the initial and after 6-month follow up, and the following measures: clinical assessment, nutrition status and difference in haemoglobin level (p < 0.05). To improve compliance, a team working among families is needed with specialised dietitian as well as follow-up at specialised CD clinics.

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KEYWORDS

Coeliac disease; Dietary compliance; Evaluation; Children; Sudan.

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INTRODUCTION

Coeliac disease (CD) (also known as gluten-sensitive enteropathy or non-tropical sprue) is an immune-mediated inflammation of the small intestine caused by sensitivity to dietary gluten and related proteins in genetically sensitive individuals. The disease was first reported in Sudan in 1978 when seven children were diagnosed with the disease [1]. In Sudan, the diagnosis of CD depends upon histological changes of the small bowel and improvement after withdrawal of gluten free diet (GFD). Serological test, although non-invasive and reliable, are not yet used routinely [2]. Many studies about CD were done but a few of them about clinical features suggestive of CD in children and infants were published [1,3]. CD presents between 6 and 24 months of age, after the introduction of gluten into the diet [4]. Patients present with chronic diarrhoea, which is bulky and foul-smelling, and may float because of steatorrhea, anorexia, vomiting, abdominal distension and pain. These symptoms are followed by malabsorption; failure to thrive or weight loss, severe anaemia and vitamins deficiency [5]. If the diagnosis is delayed, they may present with malnutrition and celiac crisis. Atypically CD may present with delay of growth and development [4,6], neurologic disease and behavioural symptoms [7-9], dermatitis herpetiformis [10,11], dental enamel defects [12], metabolic bone disease [13], arthritis [14], liver disease [15,16] and iron deficiency [4]; and a risk of malignancy is also reported [17]. Associated conditions are diabetes mellitus [18] and autoimmune thyroiditis [19]. The diagnosis typically requires both of the following: [4] the presence of characteristic histological changes on small intestinal biopsy in a symptomatic individual and complete symptom resolution on a GFD. The main elements in the management are [20]: consultation with a skilled dietitian, education about the disease, lifelong adherence to a GFD, identification and treatment of nutritional deficiencies, access to an advocacy group and continuous long-term follow-up by a multidisciplinary team. Also monitoring of dietary compliance is by clinical assessment [21], serology monitoring [4], duodenal biopsy and histopathology [4,22].

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MATERIALS AND METHODS

This is a longitudinal, prospective and hospital-based study carried out at Ibn Sina Hospital (Coeliac Disease Clinic) and Gaafar Ibnauf Children’s Hospital (Gastroenterology Clinic), Khartoum, Sudan from July 2011 to February 2012. The total follow-up in both clinics is about 200 patients. The clinic is run by a senior dietitian in Ibn Sina Hospital, since 2011, and has participated in conferences of gastroenterology inside and outside Sudan with a written handout and dietary recall. It also works with Food Research Centre, Shambat, Sudan, making several varieties of GFD; and provides consultations over the phone for any queries regarding GFD and use of sorghum with special precaution not to mix it with wheat. Patients at Gaafar Ibnauf Children’s Hospital Gastroenterology Clinic depend mainly on verbal advice from the doctors (consultant and registrars) rather than handout sheets, since there is currently no dietitian available there. Also, the clinic receives all gastroenterology diseased patients (i.e., not specialised for CD like Ibn Sina Coeliac Disease Clinic).

A total of 50 known cases of CD were studied. The Open Source Epidemiologic Statistics for Public Health (https://www.openepi.com/SampleSize/SSPropor.htm) was used to calculate the sample size. With reference to the seropositivity of CD among Sudanese children (27.3%) [4], a required sample size of children was calculated using single population proportion formula, with a hypothesised percentage frequency outcome factor (recovery) in the population of 80%, a 95% confidence interval and precision of 5.0% [13]. CD was confirmed using a serologic test, (antitissue transglutaminase [aTTG] antibody), with histopathology compatible with CD. Response to a GFD was according to the criteria of the European Society for Paediatric Gastroenterology, Hepatology and Nutrition.

Dietary compliance was assessed clinically using a questionnaire and by the evaluation of aTTG antibodies. After the dietary assessment, children and their parents were interviewed by the investigator. The interview consisted of a self-administered questionnaire which had 10 questions related to demographic profiles, questions related to the history of illness, questions related to parents’ knowledge and understanding of disease and others related to barriers to compliance. Compliance with the GFD was also defined, as subjects might have been unaware of eating any GFD. The compliance rate was evaluated, concerning age, sex, socioeconomic status and type of diet. Statistical analysis was performed via SPSS software (SPSS, Chicago, IL). Continuous variables were compared, using student’s t-test (for paired data) and Mann-Whitney U test for non-parametric data. For categorical data, the comparison was done using the Chi-square test (χ²) and Fisher’s exact test, when appropriate. p value of <0.05 was considered to be statistically significant.

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RESULTS

Fifty patients were included in the study, 27 (54%) were females and 23 (46%) were males (Table 1). Although non-significant, there were higher poor compliance rates among female patients than males (52.6% vs. 47%, p = 0.134). Forty two percent of them were aged between 5 and <10 years, 16 (32%) between 10 and 16 years and 13 (26%) under 5 years. Poor compliance rate was more common among age group 6-9 years with significant correlation (p = 0.001). Thirty (60%) were of low socioeconomic class, while 15 (30%) of middle socioeconomic status and only 5 (10%) were of high social class. Diagnoses with serology was done for all patients and were confirmed by duodenal biopsy that was consistent with partial villous atrophy in 22%, subtotal in 54 % and total villous atrophy in 24%. Regarding diet 62% of them were on strict GFD. All of them depended mainly on home preparation, while 13% of them got it from abroad beside the home preparation and 6.4% used to take it from supermarket beside home preparation. Seventy seven percent noticed health improvement after restriction of gluten free diet. Thirty eight (76%) had poor compliance (Table 1). Causes of poor compliance were as follows: in 7 (18.4%) was due to refusal of children, due to unpalatability of GFD in 9 (23.7%), while 12 (31.6%) children had difficulty in obtaining GFD, and in 10 (26.3%), it was due to lack of awareness of parents about disease and GFD. Regarding resource of health education, all patients belonged to special clinic, 20 (40%) depended on dietitian and hand out sheet; while those who belonged to Gaafar Ibnauf Children’s Hospital Gastroenterology Clinic depended mainly on verbal advice by doctors (20, 40%) and 10 (20%) received hand out sheets. In 25 patients, the tools used for follow up were haemoglobin (HB) and clinical assessment, in 20 (40%) it depended on clinical assessment, in three (6%) just by HB level and in two (4%) nothing was done.

Table 1. Nonparametric correlation between good and poor compliance regarding demographic data and clinical characteristics.

	Good compliance N = 12				Poor compliance N = 38				p value
	Count			%	Count			%
Age <2-5 6-9 10-16 Total	2 4 6 12			16.7% 33.3% 50.0% 100.0%	11 17 10 38			28.9% 44.8% 26.3% 100.0%	0.001*
Gender Male Female Total		5 7 12		41.7% 58.3% 100.0%		18 20 38		47.4% 52.6% 100.0%	0.134
Socioeconomic status High Middle Low Total			3 5 4 12	25.0% 41.7% 33.3% 100.0%			2 10 26 38	5.3% 26.3% 68.4% 100.0%	0.00*
Place of diet preparation Home Outside Total			10 2 12	83.3% 16.7% 100.0%			30 8 38	78.9% 21.1% 100.00%	0.01*
Type of diet Gluten free diet None gluten free diet Total			8 4 12	66.7% 33.3% 100.0%			23 15 38	60.5% 39.5% 100.00%	0.00*

*Statistically significant at 0.05 level.

Table 2 shows the clinical assessment that was done at the beginning in 38 (76%) patients with poor compliance and reveals the following clinical signs: 50% were pale, 13.1% were wasted, 15.8% had abdominal distention, 7.9% were edematous, 5.3% had skin rash, 2.6% had delayed puberty and 5.3% had ataxic and spastic cerebral palsy. After 6 months, clinical improvement was shown in 12 patients; only 23.7% had pallor, 5.3% were wasted, 10.5% had skin changes, 17.8% had abdominal distention, 5.3% had generalised body oedema and 7.9% had other signs (vitamin A deficiency, vitamin D deficiency and pre pubertal Tanner stage). The study showed significant correlation (p < 0.05) between before and after 6-month follow up and the following measures: clinical assessment, nutrition status and difference in haemoglobin level (Table 2). Serological assessment in patients with poor dietary compliance after six months of diagnosis revealed that 81.6% of them had positive IgA anti-tissue transglutaminase (Table 3).

Table 2. Nonparametric correlation regarding before and after six months follow up among 38 poor compliant children.

	Before		After			p value
	Count	%	Count		%
Clinical assessment Pallor Wasting Skin changes Abdominal distension Oedema Others Normal Total	19 05 02 06 03 03 00 38	50.0% 13.1% 05.3% 15.8% 07.9% 07.9% 00.0% 100.0%	09 02 04 06 02 03 12 38		23.6% 05.3% 10.5% 15.8% 05.3% 07.9% 31.6% 100.00%	0.01*
Nutritional status Severe malnutrition Moderate malnutrition Normal Total	6 18 14 38	15.8% 47.4% 36.8% 100.0%	1 23 14 38		2.6% 60.6% 36.8% 100.0%	0.01*
Difference in haemoglobin level <5 g/dl 5-9 g/dl 9-12 g/dl Total	2 31 5 38	05.3% 81.6% 13.1% 100.0%		0 21 17 38	00.0% 55.3% 44.7% 100.00%	0.00*

*Statistically significant at 0.05 level.

Table 3. Distribution of study population according to IgA anti-tissue transglutaminase among 38 poorly compliant patients.

IgA anti-tissue transglutaminase	Frequency	Percent
Positive	31	81.6
Negative	7	18.4
Total	38	100.0

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DISCUSSION

The present study is the first in Sudan about evaluation of dietary compliance among Sudanese children with CD. Recent guidelines on the screening, diagnosis and follow up of CD published by the North American Society of Pediatric, Gastroenterology, Hepatology, Nutrition and the National Institute of Health provide excellent resource about appropriate follow up strategies [4]. This is in addition to a large national survey conducted in Canada about evaluation of diagnosis and dietary compliance among children with CD in 2005 [22]. In Sudan, there was study conducted in 2006 [3] about clinical presentation in Sudanese children with CD.

Our study included 50 children with CD who were diagnosed serologically and confirmed by duodenal biopsy. Commonest age was between 5 and 10 years (42%, school age). The mean age of presentation was 3.5 years. This is not comparable with the Canadian study [22] where they had large sample size and they included all patients, even those who were clinically suspected. In our study, CD affected females more often than males in a ratio of 1.2:1, comparable to other studies where the ratio ranged from 1:3 to 3:1 [23,24].

Our study does not support the hypothesis that the disease affects people of middle and high socioeconomic status, because 30% of the patients lie in middle social class and two thirds are of low socioeconomic status, in agreement with a previous study from Sudan [3]. This may be due to fact that low socioeconomic class is more prevalent in developing countries [25]. The clinical evaluation of patients at the beginning of the study showed several signs in all patients with poor dietary compliance (76%), as shown in Table 2, including pallor, wasting, abdominal distention, and skin rash (urticaria, vetiligo and dermatitis herpetiform). Most of the children were screened IgA anti-tissue transglutaminase. It is warranted to investigate any patient with unexplained iron deficiency anaemia CD [4]. The study showed improvement after 6 months of follow-up since most of the patients had HB level between 9 and 12 g/dl that reflect dietary compliance to GFD. As shown in Table 1, only 24% had good compliance compared with higher rate of 95% in the Canadian study [23]. A lower result of 32%-81% was reported in several European studies [26-31]. The underlying cause may be due to unavailability of GFD, so all of them prepared diet at home. Also, another factor is the deficiency of resources of health education where just half of patients were seen by dietitian and given hand-out sheets. Those with high compliance are probably supported by the fact that their symptoms were distressing and affecting their life. Our study showed many difficulties affecting patient’s life style. Almost all patients (96%) shared the problem of unavailability of GFD in Sudan like different types of feeding (bread, biscuit…), and also the poor palatability [32].

Serological test was not done for all patients as a part of follow-up tool in both clinics. This reflects the importance of national protocol for follow-up, time and tools. After 6 months, our study showed some improvement clinically and haematologically (Table 2), observed mainly in those who were on regular follow-up and seen by both dietitian and doctors. Nevertheless, still 24 patients had clinical findings: 21 patients had anaemia, 19 patients were stunted and one had severe malnutrition. All of them had poor dietary compliance but the figures may not be accurate because of the short time of the study. Compliance to GFD alone should control the symptoms of CD, so other disorders should be excluded if the patients did not improve despite good compliance; a fact also highlighted by Fine et al [31].

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CONCLUSIONS

The study reflected that two thirds of patients are on GFD; however, a few (24%) have good compliance and this is mainly attributed to unavailability of GFD in Sudan. This makes difficulty in modifying life style. Also utilisation of care is much better for educated families since in 26% poor compliance was due to lack of awareness of parents about disease and GFD. Some children take free diet without consent of parents and refused GFD.

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RECOMMENDATIONS

Regular clinical assessment and HB level should be included in follow up, adding serological tests for those suspected to have poor compliance. It should be done after 6 months from diagnosis. Special CD clinics should be increased in number and improved in term of building, environment, resources and protocols to improve compliance of patients. Gluten free diet should be available and at affordable cost by building factories for Sudanese meals free of gluten. Further study in large number of patients is recommended.

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ACKNOWLEDGEMENTS

The authors acknowledge the cooperation of residents at Ibn Sina Hospital and Gaafar Ibn Auf Children’s Hospital who participated in arranging appointments for the patients and follow-up. The authors also appreciate the commitment and compliance of the patients and their families in providing the required data and for keeping with the regular follow-up appointments.

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CONFLICT OF INTEREST

None.

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FUNDING

This research project was self-sponsored.

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ETHICAL APPROVAL

Ethics approval was obtained from the Research and Ethics Committee of the hospitals (Ibn Sina Hospital and Gaafar Ibn Auf Children’s Hospital). Ethical clearance and approval for conducting this research was also obtained from the General Manager of the Ministry of health (Khartoum State). Ethical principles, as stipulated in the ethical guidelines of the Sudan Medical Specialisation board (SMSB), Medical Research Council, were upheld throughout the study. Informed consent was obtained from every respondent who agreed to participate in the study.

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