Indian Pediatrics 2003; 40:337-342 

Clinical and Nutritional Profile of Children with Celiac Disease

Key words: Celiac disease, Gluten enteropathy, Gluten free diet.

Celiac disease (CD), an enteropathy characterized by a permanent intolerance to gluten, has been well documented from northern parts of India(1-5). The disease manifests with variable severity of mal-absorption with an adverse effect on nutritional status. Even after a diagnosis of CD is established, exclusion of gluten containing foods from the diet modifies its composition exposing these children to nutritional imbalance. For developing countries like India, where wheat is the staple diet (especially in the northern parts) and not many nutritionally suitable options for a gluten free diet (GFD) are available, the nutritional imbalance due to exclusion of wheat from the diet is further compounded. Inspite of many reports of CD in India(1-5), few studies have demonstrated the follow up profile of these children on a gluten free diet. The present study details the clinical and nutritional profile of children with CD at the time of diagnosis and their follow up after they are put on a GFD.

Subjects and Methods

Sixty-five children of either sex diagnosed as celiac disease based on the modified ESPGAN criteria(6) i.e., demonstration of histological changes on intestinal biopsy while on gluten, and unequivocal clinical improvement on GFD, (gluten challenge and repeat biopsy is needed when there is a doubt on initial diagnosis, diagnosis in children <2 years, and teenagers who want to abandon GFD) were prospectively studied between March 1994 and December 2000. The diagnostic criteria for CD also included evaluation of antigliadin antibody IgG and IgA, antiendomysial antibody IgA and in some cases estimation of antireticulin anti-bodies. Children diagnosed as CD were put on a gluten free diet (GFD) and followed in the Pediatric Gastroenterology and Nutrition Clinic. In the follow up, these children were assessed for details of diet (to ascertain the compliance, quality of food intake) and their clinical profile. Nutritional assessment of the children included anthropometric measure-ments and hematological assessment at the time of diagnosis of CD (T0) and after institution of GFD (TGFD). The children with irregular follow up, on GFD for less than 6 months or a doubtful compliance were excluded from the final analysis. Equal number of age and sex matched children attending the Pediatric OPD for ambulatory checkup were included as controls. All cases were thoroughly evaluated for symptoms of diarrheal episodes, weight loss, pallor, vomiting, abdominal pain and skin changes. General behavior and scholastic examination was carried out for assessment of anemia and signs suggestive of any vitamin deficiency.

Anthropometry (weight, height, mid-arm circumference, skin-fold thickness) was recorded by standard techniques. Weight for height was calculated as the percentage of the reference median weight for height of the patient. Body mass index (BMI) was calculated as weight (kg)/height (m)2. Weight for age and height for age were expressed as Z scores relative to NCHS standards(7). Informed consent of all the subjects was obtained before collecting samples. Children who had been on a gluten free diet for at least one year were subjected to a repeat biopsy by a pediatric fiberoptic endoscope (GIF Type PQ 20 model Olympus) after informed consent and appropriate sedation. The biop-sies were graded according to a previously described score(8).

Results

Sixty-five children (30 males, 35 females) aged 2.5-12 years (mean 8.67 ± 3.37 years) with CD were put on a gluten free diet. The duration of symptoms prior to diagnosis ranged from 3 months to 10 years (mean 5.2 ± 3.0 years). Clinical profile of the cases at the time of admission is depicted in Table I.

Table I

Clinical Features of Children with Celiac Disease at Presentation.	

	Thapa(10) (n = 150)		Walker Smith(9) (n = 52)		Present study (n = 65)
	No.	%	No.	%	No.	%
Stunted growth	150	(100)	-		65	(100)
Pallor/anemia	150	(100)	7	(13.5)	65	(100)
Diarrhea	140	(93.3)	45	(86.5)	61	(93.8)
– malabsorption	110	(73.3)	-		48	(73.8)
– watery	30	(20)	-		13	(20)
Abdominal distension	110	(73.3)	23	(44.2)	46	(70.8)
Anorexia	70	(46.7)	25	(48.1)	38	(58.5)
Pain abdomen	30	(20)	23	(44.2)	33	(50.8)
Vomiting	30	(20)	32	(61.5)	6	(9.2)
Edema	15	(10)	7	(13.5)	5	(7.7)
Irritability	15	(10)	30	(57.7)	9	(13.8)
Rectal prolapse	2	(1.3)	2	(3.8)	2	(3.1)
Constipation	3	(2)	3	(5.8)	2	(3.1)

 

Of the 65 enrolled cases, only 41 children (15 males, 26 females) aged 4.5-11 years (mean 6.67 ± 2.37 years), who regularly attended the follow up and adhered to a strict dietary compliance, were included for nutritional and hematological assessment to ascertain the adequacy of GFD in comparison with the controls (Table II). The remaining 24 (36.9%) children with follow up period less than 6 months (n = 15), non-compliant/irregular compliance (n = 7) and lost to follow up (n = 2) were excluded from the follow up analysis. The mean duration of follow up on GFD was 22 months (range 6-48 ± 5.6 months). All the children with CD were malnourished at the time of diagnosis. Most of the anthropometric parameters improved significantly on GFD. On follow up, there was no significant difference in the weight for age Z score, weight for height Z score (calculated as percentage), mean triceps and biceps skin fold thickness, and mid arm circumference, when compared with controls. However, height for age Z score remained significantly lower while BMI was significantly higher after the introduction of GFD. There was no correlation between the duration of symptoms prior to diagnosis and any of the anthropo-metric parameters evaluated at the time of diagnosis of CD (p >0.05). All the hemato-logical para-meters improved significantly on GFD. Platelet count was high in 60% of cases at the time of diagnosis but after introduction of GFD only 1 child continued to have thrombocytosis. The intestinal biopsy of 21 children who had completed at least 1 year of treatment on GFD remained moderately affected (biopsy score 5-9) in 52.5% of the patients and minimally affected (biopsy score 0-5) in 9 patients (42.8%). Only in 1 case (4.7%) the intestinal biopsy had reverted to normal histological picture.

Table II

Anthropometric and Hematological Parameters in Cases vs. controls	

Parameter	T0 (n = 65)	P value	Controls (n = 65)	TGFD (n = 41)	P value*
Anthropometric parameters
Height for age (Z score)	–3.144	0.00	–1.029	–2.086	<0.0001
Weight for age (Z score)	–2.889	0.00	–1.029	–1.038	0.96 (NS)
Weight for Height	86.98	0.00	97.7	101.8	0.56 (NS)
(Z score in %)
BMI (Wt. in kg/Ht. in m2)	13.7	0.00	15.1	16.4	<0.0001
Triceps skinfold thickness (mm)	8.9	0.00	12.0	13.2	0.89 (NS)
Biceps skinfold thickness (mm)	8.1	0.00	11.2	11.8	0.74 (NS)
Mid arm circumference (cm)	12.9	0.00	16.2	16.9	0.51 (NS)
Hematological indices
Hemoglobin (g%)	7.7	0.00	10.9	10.7	0.12 (NS)
Platelet count (per cu mm)	450 × 103	0.00	285.07 × 103	299.96 × 103	0.42 (NS)
MCV (fl)	63.2	0.00	80.3	72.2	<0.0001
MCH (pg)	18.1	0.00	28.1	22.6	<0.0001
MCHC (% Hb/cell)	28.3	0.00	33.8	33.6	0.52 (NS)
Peripheral smear
– Normocytic normochromic (%)	-	-	100	81	-
– Microcytic hypochromic (%)	80	-	-	19	-
– Dimorphic (%)	20	-	-	-	-

T0 = Celiac children at diagnosis, TGFD = Celiac children on GFD.

P = between T0 and Controls, P* = between TGFD & Controls.

Discussion

Diarrhea, vomiting and failure to thrive are reported to be the most common presenting symptoms of children with CD(9). Main differences in the clinical features of CD as highlighted by the present study and other studies from northern India(10-12) as compared to the west(9) are the higher incidence of stunted growth and anemia (Table I). These two clinical manifestations are features of more severe disease and correlated with later mean age of diagnosis (8.7 ± 3.4 years) in our study population as compared to the classical age of presentation at 9-10 months(9). The higher mean age at the time of diagnosis in our patients reflects prolonged breastfeeding practices, late introduction of weaning and gluten and lack of awareness about CD. Of the 65 children diagnosed as CD, 7 cases (10.8%) were not included in the follow up evaluation because of non-compliance or a doubtful compliance. It is a matter of great concern that despite long duration of symptoms and poor general condition at the time of diagnosis, compliance on GFD could not be ensured in these children. Most of the non-compliant children admitted having consumed gluten occasion-ally at school or at parties and most of these dietary indiscretions were within the know-ledge of the parents. Apart from un-successful or partially successful counseling of these children and their families, poor availability of gluten free options seems to be a major reason for poor compliance.

Anthropometric and hematological evaluation clearly reveal malnutrition in our patients at the time of diagnosis of CD and a significant improvement in all the parameters after institution of GFD. However, after institution of GFD, these children tended to be stunted i.e., they had significantly lower height for age Z score while their weight for age Z score was comparable to the control group. These findings suggest height gain is slower than weight gain which may be related to late diagnosis in our patients (mean age 6.67 years), consistent with the observations of other workers(13,14). The slower and probably incomplete height gain but relatively faster weight gain could also explain the significantly higher mean BMI in these children in the follow up.

Anemia is a frequent feature of CD and may sometimes be the only presenting symptom(15). Iron deficiency and microcytic hypochromic anemia was the most common type of anemia recorded in our patients which is in conformity with the results of others(3,9). Megaloblastic anemia occurs rarely in children with CD but serum folate and red cell folate levels are usually reduced in celiac children(9). Thrombocytosis, postulated to be related to several mechanisms in adults with inflammatory bowel disease(16), was detected in 60% of our patients at diagnosis and in only 2.3% after institution of GFD. It is difficult to explain the cause of thrombocytosis in our cases since in the follow up almost all cases, in whom intestinal biopsy was repeated, continued to show some inflammatory changes but their platelet counts were normal.

The repeat biopsy of almost all the patients on GFD with mean duration of 2 years, except for 1 case, continued to have a minimally to moderately affected intestinal biopsy. Over a period of time appropriate treatment with GFD results in significant improvement in intestinal biopsy in CD patients. However, the mucosa of distal small intestine improves more rapidly than the severely injured proximal bowel. Therefore, months or even years of gluten withdrawal may be required in some patients before mucosal structure reverts maximally towards normal(17).

Our results suggest that CD is a common entity in countries like India especially in the northern parts where wheat is one of the staple food constituents. Celiac children are malnourished at diagnosis and institution of GFD leads to a rapid improvement in symptoms, and in nutritional and hemato-logical status. However, non compliance of GFD remains a critical issue in the manage-ment of these cases, particularly because not many nutritionally suitable options for GFD are available in our country. Regular follow up and counseling is recommended to ensure dietary compliance.

Acknowledgement

Authors are thankful to Drs. Deepak Bansal, Bharat Balani, Ashutosh Gangil and Amit Jain for their support during endoscopic procedures and in the Pediatric Gastro-enterology and Nutrition Follow Up Clinic.

Contributors: AKP designed the study and helped in the finalizing of the manuscript. He will act as the guarantor of this paper. VKA helped in the endoscopic procedures and follow up of the cases. GK conducted the study and drafted the manuscript. SN provided the histological and hematological support.

Funding: None.

Competing interests: None stated.

 References