Review Article

The Epidemiology of Celiac Disease in the General Population and High-Risk Groups in Arab Countries: A Systematic Review

Table 1

The prevalence of celiac disease among high-risk groups.

S. no.Authors (year)CountryAimsStudy design/populationDiagnostic criteriaResultsNOS score

1.Boudraa et al. (1996) [16]West AlgeriaTo assess the prevalence of celiac disease in insulin-dependent diabetes mellitus (IDDM) and explore its presence in their first-degree relativesProspective study from 1 January 1993 to 31 December 1994
116 IDDM patients
381 first-degree relatives of IDDM patients
Serological markers, IgA and IgG antigliadin antibodies (AGA), and IgA antiendomysium antibodies (EMA)
Jejunal biopsy of symptomatic patients
Prevalence of CD in IDDM patients was 16% to 20% (since not all patients with positive serological markers experienced jejunal biopsy, the prevalence can be considerably higher up to 20%)
In 1st-degree relatives, 6.8% positive for one serological marker, while 3.4% had villous atrophy.
6
2.Al Attas (2002) [17]Eastern Saudi ArabiaTo estimate CD prevalence in clinically suspicious celiac disease patients and in patients with disorders considered to have an association with CD, such as autoimmune diseasesHospital-based study
Group 1 =145 patients (clinically suspected)
Group 2 = 80 with autoimmune diseases
Group 3 = 20 patients with IBD
Group 4 = 100 heathy blood donors
IgA-EMA and intestinal biopsy of confirmed cases,
(all have autoimmune thyroid disease (AITD)), and .
7
3.Ashabani et al. (2003) [18]LibyaTo investigate the CD-related marker occurrence in Libyan children patients with DMCohort study conducted on 234 Libyan children with DM (age range 2 to 25 years) and 50 healthy childrenIgA and IgG, AGA, anti-tTG, anticalreticulin antibodies, and EMA50 (21.3%) positive for IgA and/or IgG-AGA, tTG, and anticalreticulin antibodies
19 of these were EMA positive
24 had biopsy-proven CD including EMA-negative patient with IgA deficiency
Overall, CD prevalence found 10.3%
6
4.Al-Ashwal et al. (2003) [19]Saudi ArabiaTo examine celiac disease prevalence in young Saudi patients suffering from type I diabetes mellitus at “King Faisal Specialist Hospital and Research Centre, Riyadh”Hospital-based research; 123 type 1 diabetic patientsSerum gliadin immunoglobulin (Ig) A and reticulin IgA antibodySerology positive 10 (8.1%)
6 had jejunal biopsy and showed villus atrophy; thus, prevalence was 4.9%, based on biopsy results and antibodies.
7
5.Nowier et al. (2009) [20]EgyptCeliac disease prevalence among Egyptians with type 1 diabetes and the association with autoimmune thyroid diseaseCase-control study design where case and control groups were compared
73 type 1 DM patients
Enzyme-linked immunosorbent assay (ELISA) antibodies to tTGPrevalence of CD among type 1 DM patients was 5.48% positive anti-tTG antibodies
Anti-tTG antibody testing was negative for patients with autoimmune thyroid disease.
8
6.Al-Hussaini et al. (2012) [21]Middle EastTo identify the epidemiology of celiac diseases among type 1 diabetes in Middle Eastern childrenCross-sectional study; 106 children with type 1 diabetesIgA anti-tTG and EMA19 (18%) children showed positive results of anti-tTG and/or EMA
12 (11.3%) children were found to be CD positive by biopsy.
6
7.Saadah et al. (2012) [22]Saudi ArabiaCD prevalence in adolescent and children patients with type 1 DMRetrospective hospital record-based study
430 diabetic children
Anti-tTG antibodies91 (21.2%) positive for anti-tTG antibody
48 (11.2%) patients’ biopsy confirmed CD (42 asymptomatic).
3
8.Al-Sinani et al. (2013) [23]OmanCeliac disease prevalence in Omani children (type 1 diabetics)A prospective cross-sectional study
103 children with type 1 diabetes
Anti-tTG IgA, EMA IgA, and total IgA
Endoscopy and biopsy
17% () positive anti-tTG
5.5% () biopsy proven CD. Among these all 5 were also positive for EMA.
5
9.Farahid et al. (2014) [11]JordanTo estimate celiac disease prevalence in AIH patients in Jordan and to determine patients at higher disease riskCross-sectional record-based review; 914 AIH patients (108 males and 806 females) aged 20–82 yearsEMA IgA and IgG
Duodenal biopsy
117 (12.8%) seropositive for CD.
39 (44.8%) out of 87 biopsy proven
CD prevalence among patients with AIH was estimated to be 5.7% in comparison to seroprevalence of 12.8%
Higher association was found between CD and years, vitamin B12 deficiency, anemia, and other autoimmune diseases for example, Addison disease, diabetes mellitus, and vitiligo.
6
10.Al-Hakami (2016) [24]Saudi ArabiaTo determine the seroprevalence of coexisting autoantibodies among patients with type 1 diabetes and to look for possible association with glycemic control, diabetes duration, and diagnosis at Aseer Central Hospital, AbhaCross-sectional study
202 T1DM patients were included in this study
Anti-tTG, EMA21 (10.4%) positive for both anti-tTG and EMA
No significant association between the age at T1DM glycemic control, duration, and diagnosis and the autoantibody presence was observed.
5
11.Al-Ajlan (2016) [25]Saudi ArabiaTo examine the implications and prevalence of celiac disease among Saudi adults and comparing it with diagnosed with irritable bowel syndrome at Al-Iman General Hospital and Prince Salman Hospital, RiyadhProspective case-control study
Subjects aged 20-60
980 adult patients
Among them, 482 subjects were controls and 498 with IBS
Anti-tTG and EMA and biopsy1.9% CD in control group
9.6% in IBS group
55 out of 980 patients were found to be positive for celiac disease.
8
12.Al-Hakami (2016) [26]Saudi ArabiaTo estimate the prevalence of CD in high-risk groups in Aseer (southwest region) and to determine its associationsLaboratory records (retrospective case-finding)
315 patients
Anti-tTG and EMA and biopsy58 (18.4%) got a positive test for at least one antibody marker
17.5% positive for anti-tTG
15.6% positive for EMA
22 out of 40 biopsies were confirmed for CD
Type 1 DM was the most common clinical illness related to these markers with the percentage 47%
However, gastrointestinal presentations were observed to be only 11.5%.
4
13.Mansour and Najeeb (2011) [27]IraqTo evaluate silent CD frequency in Iraqi patients’ sample with type 1 diabetes mellitusProspective cross-sectional from November 2008 to December 2009; 62 patients with type 1 diabetes mellitus from age 8 to 42IgA, anti-tTG-IgA, anti-tTG-IgG, EMA-IgG, and duodenal biopsy11.2% in Iraqi patients with type 1 DM.
43.55% had Marsh 0
16.1% had Marsh I
0% had Marsh II
3.2% had Marsh IIIA
4.83% Marsh IIIB
3.2% Marsh IIIC
For diagnostic purposes, EMA and tTG tests were found to be useful.
6
14.Fraser et al. (2003) [28]OmanTo study the association between occult celiac disease and iron deficiency anemia in Omani adults in Sultan Qaboos University Hospital, MuscatHospital-based study
51 patients
IgA, anti-tTG-IgA, anti-tTG-IgG, EMA-IgG, and duodenal biopsyMean Hb 9 with confirmed low ferritin.
2 patients positive IgA-tTG and IgA EMA and IgG tTG
One patient biopsy done and showed villous atrophy.
Prevalence considered being approximately 1 : 30 in iron deficiency patients and 1 in 200-300 affected in the general population.
4
15.Oujamaa et al. (2019) [29]MoroccoTo examine the prevalence of specific autoantibodies to CD in adult and pediatric population with type 1 diabetesMulticenter, cross-sectional study
Study population consists of 276 adults and pediatric diabetic patients
Anti-tTG-IgA, anti-tTG-IgG, EMA, HLA-DQ2/DQ8 typing, and duodenal biopsySeroprevalence of CD in T1D patients was 9.1% ()
2 cases had biopsy-proven CD.
5
16Alyafei et al. (2018) [30]QatarTo determine the prevalence of autoantibodies in diabetic patients in QatarRetrospective cross-sectional study, 490 pediatric patients aged 0.5-16 yearsAnti-tTG IgA and anti-tTG IgG
Biopsy
In 365 T1DM, 18 (5%) patients have positive anti-tTG IgA and 16 (4.3%) anti-tTG IgG antibodies.
In 46 T2DM, anti-tTG IgA antibodies were found in 4 patients (8.7%), whereas no anti-tTG IgG antibodies detected in any patient.
Mucosal biopsy proved celiac disease in 9 out of 12 patients (75%) with positive ATT IgA and IgG antibodies.
4
17Odeh et al. (2019) [31]JordanTo determine the prevalence of biopsy-proven CD among T1DM pediatric patientsMixed prospective and retrospective study
538 children with T1DM
Data collected from 2012 to 2017
IgA-tTG and IgG-tTG antibodies Duodenal biopsyPrevalence of serology positive CD was 16.6% while biopsy-proven CD was 9.1%.5
18AlRuwaily et al. (2017) [32]Saudi ArabiaTo determine the prevalence of CD in Down syndrome Saudi patientsRetrospective study, files of 91 pediatric patients for serological markers and biopsy resultsAntigliadin antibody (AGA) IgA and IgG, EMA, IgA-tTG, and IgG-tTG antibodies(i) AGA-IgA found in 32.14%
(ii) AGA IgG in 52.38%
(iii) EMA tested positive in 14.28% and negative in 69.04%
(iv) Anti-tTG IgA was high in 15.5%
(v) Serum IgA normal level found in 43% patients while low in 1.2%.
Biopsy-confirmed cases of CD was 10.7%.
5
19Alghamdi et al. (2018) [33]Saudi ArabiaTo determine the prevalence of CD in T1DM patient living in Al-Baha region, Saudi ArabiaRetrospective record-based study
268 T1DM patients of age 2-23 years
IgA-tTG and IgG-tTG antibodiesPrevalence of serology positive cases of CD was 7.1%..3
20Alshareef et al. (2016) [34]Saudi ArabiaTo determine the prevalence of CD in T1DM patient of Saudi ArabiaCross-sectional study
218 T1DM patients with
Anti-tTG antibodies and duodenal biopsyRaised anti-TTG levels found in 7.3% patients.
Duodenal biopsies were done in 12 patients which showed
(i) total villous atrophy 3.7%
(ii) subtotal villous atrophy 0.8%
Chronic duodenitis 0.8%
4
21Al-Agha et al. (2015) [35]Saudi ArabiaTo investigate the coexistence of autoimmune diseases in T1DM patientsCross-sectional study
228 patients with age 1-18 years
Anti-tTG antibodies and jejunal biopsyCeliac disease was found in 19.7%.
CD was also significantly associated with a high level of HbA1C level (; 95% CI: 0.884-1.166).
5
22Abdulrazzaq et al. (2018) [36]UAETo investigate the presence of autoimmune diseases in Emirati children with Down’s syndromeCross-sectional study conducted on 92 Down’s syndrome patientsAnti-tTG antibodiesPrevalence of CD in study population was 1.1%.3

Abbreviation: IgA-tTG: antitissue transglutaminase IgA; IgG-tTG: antitissue transglutaminase IgG; EMA: antiendomysium antibodies; AGA: antigliadin antibodies; NOS: Newcastle-Ottawa Scale.