SUDANESE JOURNAL OF PAEDIATRICS

2020; Vol 20, Issue No. 2

ORIGINAL ARTICLE

Clinical presentation of coeliac disease and the effect of sorghum-based diet on anthropometric measurements among Sudanese children

Ali Arabi (1), Zein A. Karrar (1), Fathia Hassan Mubarak (2), Jalal Ali Bilal (3)

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

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

(3) Pediatrics Department, College of Medicine, Shaqra University, Saudi Arabia

Correspondence to:

Ali Arabi

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

Email: draliarabi99 [at] gmail.com

Jalal Ali Bilal

Pediatrics Department, College of Medicine, Shaqra University, Shaqra, Saudi Arabia

Email: jalalbilal2000 [at] gmail.com

Received: 08 April 2020 | Accepted: 04 May 2020

How to cite this article:

Arabi A, Karrar ZA, Mubarak FH, Bilal JA. Clinical presentation of coeliac disease and the effect of sorghum-based diet on anthropometric measurements among Sudanese children. Sudan J Paediatr. 2020;20(2):144–151.

https://doi.org/10.24911/SJP.106-1586348889

ABSTRACT

Coeliac disease (CD) is a chronic enteropathy. Sorghum (Sorghum vulgaris) is a common staple in Sudan. The literature on the growth of children with CD following sorghum diet is scanty. The aim of this study was to identify the demographic and clinical characteristics of CD in children and to determine the anthropometric response to a diet based on sorghum. This prospective study included children with probable CD in Ibn Sina Hospital, Khartoum, Sudan, from January 2002 to February 2012. The demographic, anthropometric, clinical and laboratory data were recorded. The CD serology was done, and the diagnosis of CD was based on Marsh criteria. Children who consumed sorghum and their anthropometry were recorded at 3 and 6 months after diagnosis. Children enrolled were 218. The mean ± SD age was 8.2 ± 4.5, median was 7 years and female/male ratio was 1.12/1. CD was common among Nubians and Arabs. The majority (145, 66.5%) presented with gastrointestinal symptoms. Feeding on sorghum diet resulted in a significant increase in weight after 3 and 6 months (21.1 ± 9.8 and 25.1 ± 14.2 kg, respectively) of the initial visit (18.5 ± 9.4 kg), p < 0.001 and p = 0.001, respectively. The mean weight for height had significantly increased at the second compared to the initial visit (0.17 ± 0.05 vs. 0.15 ± 0.5), p < 0.001. There was no association between gaining weight and age, gender, or a family history of CD. In conclusion, Sudanese children with CD presented over 8 years of age. The common presentation was gastrointestinal symptoms. The initial weight and weight-for-height increment were significant on sorghum diet.

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KEYWORDS

Coeliac disease; Children; Dietary management; Sorghum; Sorghum vulgaris; Anthropometry; Sudan.

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INTRODUCTION

The European Society for Paediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN) defines coeliac disease (CD) as ‘an immune-mediated systemic disorder elicited by gluten and related prolamines in genetically susceptible individuals and characterised by the presence of a variable combination of gluten-dependent clinical manifestations, CD-specific antibodies, HLA-DQ2 or HLA-DQ8 haplotypes and enteropathy’ [1]. The first cases of CD in Sudan were reported in 1978 [2]. The prevalence of CD in Sudan is unknown, but it was confirmed in 22.5% of Sudanese children with clinical features suggestive of the disease [3]. Other studies reported a high seroprevalence range of 20.3%–27.3% though similarly among high-risk population [4,5]. These same studies reported mainly a classical presentation of CD among Sudanese children [3–5], the number of children included was small and the outcome on follow-up was not reported. The classical presentation of CD in young children is usually with gastrointestinal symptoms of diarrhoea, abdominal pain and weight loss. Sometimes, children present with the signs of malabsorption such as steatorrhoea and growth faltering and others may show the signs of iron-deficiency anaemia, short stature, liver disease, arthropathy, mouth ulcers, developmental regression and dermatitis herpetiformis [1]. The majority of children with CD presented with nonarboreal symptoms, such as growth failure, decelerated growth or short stature, abdominal pain and as a result of screening for type 1 diabetes mellitus, autoimmune thyroid disease or a first-degree relative with celiac disease [2]. In Sudan, on the other hand, a spectrum of the clinical presentation of CD in children was documented including chronic diarrhoea, abdominal distention, failure to thrive, rickets, iron-deficiency anaemia, short stature, oedema, clubbing and delayed bone age [2,3]. The clinical presentation of CD in Sudanese children was not extensively studied in Sudan, and whether the clinical presentation is different from those in other settings, needs further elucidation.

Since there are no commercialised gluten-free products in the Sudanese market, sorghum (Sorghum vulgaris) represents an affordable gluten-free grain, in which flour can be consumed by CD patients [6]. Although sorghum is inexpensive, available and well consumed as a staple in Sudan, the studies on sorghum consumption by celiac patients are scant. Sorghum was not studied in this country as an alternative to commercial gluten-free as well as its effect as a staple diet on the anthropometric measurements of CD children. Therefore, is sorghum a sufficient staple diet to improve the growth parameters in children with CD?

The aim of the present study was to identify the demographic and clinical presentation of CD in children in Sudan and to determine their response to a gluten free diet based on the cereal sorghum (Sorghum vulgaris).

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MATERIALS AND METHODS

This prospective cross-sectional hospital-based study included all children who were referred because of suspected CD to the Pediatrics Gastroenterology Department at Ibn Sina Hospital, Khartoum, Sudan, from January 2004 to February 2012. Ibn Sina Hospital is a specialised tertiary hospital receiving referrals from secondary hospitals all over Sudan.

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%) [1], 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%. The largest required sample size was found to be 305 children with 10% of non-respondents or have incomplete data.

This study included all children who were referred with one or any combination of the following: unexplained loss of weight, loss of appetite, unexplained or refractory anaemia, chronic diarrhoea, vomiting, failure to thrive, abdominal pain and/or distention and patients who were referred because of stunting. Children were excluded from the study if they presented with gastrointestinal bleeding, systemic disease not known to be associated with CD or nutritional history suggestive of primary protein–calorie malnutrition or if they were known to have a coagulopathy disorder other than Vitamin K deficiency.

A standardised questionnaire was used to collect information from all patients. This included demographic, anthropometric, clinical and laboratory data. All data were prospectively entered at the first and subsequent visits to the hospital for future analysis.

All patients were weighed with the minimal clothes on and barefooted using a mechanical weighing scale with a height rod (Seca® 700 Mechanical Medical Scale). The length was recorded for children whose age was up to 2 years and stature for children who were above 2 years of age using a measuring board and a stadiometer (Seca® 700 Mechanical Medical Scale), respectively. The measurements were recorded to the nearest decimal.

The serological tests for CD, which included serum immunoglobulin A (IgA) anti-tissue transglutaminase IgA antibody and/or endomysial IgA antibodies determinations [1], were included in the gastroenterology department protocol and were either requested by the referring doctor, or at least one was done at the department on receiving the patient. Children with at least one positive serological test underwent upper gastrointestinal endoscopy.

Biopsies were taken by upper endoscopy from the second or third portion of the duodenum. Four samples were taken, and at least one biopsy was taken from the duodenal bulb. ¨The diagnosis was based on gluten-dependent symptoms, CD-specific antibody levels and characteristic histological changes (villous atrophy and crypt hyperplasia) in the duodenal biopsy [4]. These diagnostic criteria were based on Marsh criteria and according to ESPGHAN guidelines together with positive CD antibodies as CD lesions Marsh 2 together with CD antibodies or above Marsh 3 [1,7].

Children who were diagnosed as having CD were then put on gluten-free diet based on sorghum (Sorghum vulgaris) in addition to the supplements for anaemia where present as well as appropriate vitamins and mineral supplementations if deficiencies were present. A specialised dietician affiliated to the department advised all families on the preparation of gluten-free diet both verbally and using a pamphlet, especially designed for patients with CD. The diet staple consisted of sorghum recipes mainly of ‘Kisra’, a local Sudanese bread sheets, ‘Asida’, a thick porridge or ‘Nasha’ prepared from sorghum flour [8]. Besides, the families were thoroughly counselled on gluten-containing products that they have strictly to avoid.

The follow-up visits were monthly scheduled, and the data at 3 and 6 months after diagnosis were used for analysis. In each visit, the same health worker recorded weight and height, and a compliance with the gluten-free diet and sorghum consumption were checked.

Data handling and analysis

All data were double-checked and entered using Statistical Package for the Social Sciences (SPSS) software version 22 (SPSS Inc., Chicago, IL). Frequencies and means were calculated. The paired t-test was used to determine whether there were significant differences between the means of children weights initially and at 3- and 6-month visits. Moreover, the repeated analysis of variance was used to analyse the difference between anthropometric values and ratios initially and after the administration of gluten-free diet at 3 and 6 months. The significance level was set as p < 0.05. A univariate logistic regression was performed to detect any association between the dependent variable weight gain (either a child with CD was gaining or not gaining weight) and the independent variables: age, gender and family history. The results were expressed as odds ratio within 95% confidence interval limit.

Ethical considerations

The Ethics Committee of the Faculty of Medicine, University of Khartoum, approved this study. All children and their families were informed about the study, and its purposes and all the parents/guardians of the participants signed an informed written consent.

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RESULTS

A total of 422 children fulfilled the inclusion criteria for enrollment in the study. Forty children were excluded for different reasons (Figure 1), and 382 children were included. Out of them, 300 children tested positive for transglutaminase antibody (TGA), and 218 underwent small bowel biopsies (Figure 1). However, only 218 (both TGA positive and biopsy Marsh 2 and above) children were diagnosed as having CD, and some were excluded because of incomplete data, they were ill at admission or their parents declined consent. Several children (n = 82) were excluded, who were seronegative among other causes (Figure 1). About 82 children who did not return for biopsy were all TGA positive; however, the parents were reluctant to biopsy and they did not return.

The demographics and clinical characteristics of the included 218 children with CD are shown in Table 1. The mean ± SD age was 8.2 ± 4.5 years. CD was more common in females than in males (1.12/1.0) but statistically insignificant (p = 0.716) and among children of Nubian and Arab origin than in those from other ethnicities. The different modalities of clinical presentation are shown in Table 1. Two children had diabetes type 1, and a child was clinically diagnosed as Down syndrome, but genetic tests were not done. All of them, after diagnosis and start of treatment, were referred to the appropriate departments for further management.

Feeding on sorghum resulted in a significant increase in the weight of children with CD after administration of sorghum-based diet at 3 and 6 months of the initial visit (p < 0.001 and p = 0.001, respectively). Similarly, the mean weight for height had significantly increased at the second visit compared to the initial after starting the gluten-free diet (p < 0.007). However, there was no significant increase in the mean weight-for-height ratio during the period of 3–6 months, and as well, there was no increase in height-for-age ratio in the two visits as shown in Table 2.

In a logistic regression, there was an insignificant association between gaining weight in children with CD after gluten-free diet and age, gender and a positive family history of CD.

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DISCUSSION

The sample in this study comprised the largest CD children population studied in Sudan. The major findings were that children with CD presented at a mean age of slightly more than 8 years, and the disease was a little more common among females and among Nubians and Arabs descendants more than other ethnicities. The major presentation of CD in this cohort was the gastrointestinal manifestations. The mean weight and weight-for-height ratio of children with CD increased initially on feeding sorghum-based diet.

The mean age at presentation, in this study, was lower than the reports in the same population but similar to another from entirely different high socioeconomic populations in developed countries [3,9]. A tendency towards relatively late presentation was reported in affluent countries [9–11]. Nevertheless, the relatively higher mean age at diagnosis in this cohort could be attributed to poor awareness of families and healthcare workers about the disease. Furthermore, usually local doctors have misconceptions that CD is mainly common among Caucasian populations. Poor diagnostic facilities and the probable masking of the disease by the more common conditions as diarrhoeal diseases, protein-energy malnutrition and intestinal parasites may be factors of late presentation [12]. In accordance with other reports, this study showed a preponderance of females over males as it is well known in CD and many other autoimmune diseases [3,9–11].

The classic presentation with gastrointestinal symptoms in this study was similar to Mohammad et al. [3], Ageep [4] and Hussien et al. [5] reports among Sudanese children. The trend of CD to present with gastrointestinal symptoms becomes less frequent in affluent countries besides it is commonly seen among older patients [10,11,13,14]. The disease obliviousness among health practitioners in Sudan might not warrant an early investigation/referral to a specialised centre, especially because of the pronounced mimicry to malnutrition and diarrhoeal diseases [12].

Figure 1. Flow chart of children with coeliac disease enrolled in the study.

Table 1. Demographic and clinical characteristic of children with CD (n = 218).

Variable
Demographic characteristics
Age in years: (mean±SD), mode, range	(8.2 ± 4.5), 6, 1–18
Gender frequency (%) female/male, ration	115 (52.8)/103 (47.2%), 1.12/1
Ethnic groups: frequency (%)
Nubians and Arabized-Nubians	147 (67.4)
Arabs	50 (22.9)
Beja	8 (3.7)
Other	10 (4.6)
Non-Sudanese	3 (1.4)
Clinical frequency (%)
Family history	54 (24.8)
Presentation on referral
Gastrointestinal symptomsa	145 (66.5)
Unexplained iron deficiency anemia	53 (24.3)
Other presentations Stunted growth Dermatitis herpetiformis	18 (8.2) 2 (1)	20 (9.2)

SD = Standard deviation.

^aChronic diarrhoea, abdominal distention, abdominal pain, constipation, dysphagia and loss of weight.

Table 2. Weights and weight-for-height of children with CD at initial and subsequent visits at 3, 6 and 9 months after diagnosis (n = 218).

Parameter	Schedule of visits			p value
	Initial	3 months	6 months
Weight (mean ± SD) kg	17.3 ± 11.4	19.6 ± 11.5	22.9 ± 19.5	<0.001
Weight for height ratio (mean ± SD)	0.15 ± 0.5	0.17 ± 0.05	0.41 ± 1.2	0.007
Height for age ratio (mean ± SD)	17.39 ± 9.4	17.41 ± 8.9	17.49 ± 10.4	0.742

SD = Standard deviation.

This, to the best of authors’ knowledge, is the first study of its type to report the response, based on weight and weight-for-height measurements of children with CD to sorghum-based diet. The significant increase in weight and weight-for-height after 3 months following the consumption of sorghum-based diet in this study could be attributed to feeding on sorghum since it is known for its safety for CD patients [15]. However, other factors such as socioeconomic status, consumption of other gluten-free foods and frequency of feeding were not confounded for, in this study, one of the limitations of the results. Furthermore, celiac antibodies were not measured to determine compliance because of the cost of the investigations and non-affordability for most families. Hopman et al. [16] though reported satisfactory nutritional responses based on weight and height. The subsequent static weight gain relative to the second visit may be attributed to noncompliance to the sorghum diet mostly by mistake or ignorance of food outside the home as was reported in other previous reports [16,17]. This might be because families were devoted to restriction to gluten-free diet at the beginning, but the tighten grip of restriction might become loose over time. More studies based on structured pre-validated questionnaires are required to elucidate this assertion. The literature on growth outcome in children with CD is scant. However, Reilly et al. [18] had reported a reduction of body mass index (BMI) even among patients with initial high BMI before diagnosis. The cause of failure to increase weight-for-height ratio among children with CD following sorghum diet in this study is unknown. An increase in height proportionate to weight might be a factor until now, which needs to be proved by further studies.

Age, gender and family history were not associated with gaining weight in children with CD. Many other factors can affect the outcome of dietary therapy in CD. The highly restricted diet has a negative social bearing, and the mandatory continuous attention to prevent gluten and the high frequency of unintentional exposure are proved to be the main factors of the large burden of the gluten-free diet and hence outcome [19]. More studies are needed to determine the predictors of growth parameters.

Further limitations were that HLA-DQ2 or HLA-DQ8 haplotypes and serum IgA measurements, for IgA deficiency, were not done, and besides, a healthy cohort was not used to control the anthropometric measurements in this study. The exclusion of IgA deficiency was not possible because of a lack of information on total serum IgA. The relatively short period of follow-up was also a major limitation of the present study, and a longer period would have yielded better results.

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CONCLUSIONS

Sudanese children with CD presented late, over 8 years of age. It is more common among females and among Nubian and Arab ethnicities. The common presentation was gastrointestinal symptoms. The initial weight and weight-for-height increment were significant on sorghum-based diet. It is a commonly used staple food, which is affordable and acceptable by children and their families.

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ACKNOWLEDGEMENTS

Kind regards and gratitude go to Dr. Mohammed A. Hameed for his effort in examining and reporting the histopathology and to the Department of Gastroenterology, Ibn Sina Hospital, who has been a welcoming host adopting the clinic. Much appreciation goes to the children and their families.

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FUNDING

None.

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CONFLICT OF INTEREST

None.

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ETHICAL APPROVAL

The Ethics Committee of the Faculty of Medicine, University of Khartoum, approved this study. All children and their families were informed about the study and its purposes, and all the parents/guardians of the participants signed an informed written consent. Confidentiality was ensured at all the stages.

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