Indian Pediatrics 2002; 39:136-144  

Iron Status of Children Aged 9-36 Months in an Urban Slum Integrated Child Development Services Project in Delhi

Deeksha Kapur, Kailash N. Agarwal, Sushma Sharma, Kusum Kela and Iqbal Kaur

From the Department of Women Education, School of Continuing Education, Indira Gandhi National Open University, New Delhi, India.

Correspondence to: Prof. K.N. Agarwal, Department of Pediatrics, University College of Medical Sciences and Guru Teg Bahadur Hospital, Delhi 110 095, India. E-mail: [email protected]

Manuscript received: July 25, 2001, 
Initial review completed: August 18, 2001,
Revision accepted: October 22, 2001.

Objective: To assess the magnitude/severity and possible etiology of anemia and iron deficiency among children 9-36 months of age. Methods: A population-based study on the prevalence, etiology of anemia and iron status in 545 children, 9-36 months of age, was conducted in an urban slum ICDS (Integrated Child Development Services) project in North-East Delhi. Hemoglobin and serum ferritin was estimated and information on socio-economic, demographic, parasitic infection/infestation and dietary intake was collected. Results: Prevalence of anemia (using WHO cut-off values of Hb <11.0 g/dl) among children, 9-36 months of age, was 64%, of these 7.8% had severe anemia (Hb <7.0 g/dl). Using 10.0 g/dl as the Hb cut-off point 44% children less than 18 months of age in the present study population were anemic. On a sub-sample study, 88% children were estimated to be iron deficient, with serum ferrtin concentration less than 12 µg/L. The peripheral smear red cell morphology showed 33.9% as microcytic-hypochromic and 37.1% as dimorphic. Dimorphic anemia was 55% in moderate anemia group. The energy and iron intakes were 56% and 45%, respectively of the Recommended Dietary Allowances (RDA). The parasitic infestation/infection was not related to the prevalence or severity of anemia. Conclusions: In Delhi, high prevalence of moderate to severe anemia and iron deficiency with vitamins folate and/or B12 among children under 3 years of age in an ICDS block in operation for 20 years is of concern. Dietary origin was the main cause of anemia in this age group.

Key words: Anemia, Dietary iron, Dimorphic anemia, Iron deficiency.

NATIONAL Family Health Survey (NFHS-2) (1998-99) data(1), reveal that 74% children, 6-35 months of age, are anemic. Iron deficiency in young age can impair physical growth and cognitive function(2,3). Evidence from animal model studies investi-gating behavioral and functional consequen-ces of early iron deficiency, reveal that iron deficiency occurring in intrauterine life or during the early weaning period results in adepletion of brain iron and irreversible changes in neurotransmitters(4). In spite of these known debilitating ill effects of iron deficiency in the very young, children less than 3 years of age, have not been particularly targeted for intervention in the Integrated Child Development Services (ICDS) program. ICDS program launched initially in 33 blocks, in 1975, today spreads across 4348 blocks(5). The program is specially designed to reach disadvantaged and low-income groups, for effective disparity reduction. The national prophylaxis program for control of nutritional anemia is one direct intervention integrated in ICDS. The aim of the present study was to assess the iron status and dietary iron intake of children, 9-36 months of age, in an urban slum ICDS project in Delhi operational since last two decades.

The study was conducted from July to November 1997 in the 41 Anganwadis (AWs) of Nand Nagri ICDS project, located in North-East Delhi. Nand Nagri has a total population of 65,000 with approximately 2629 children in the age group 9-36 months.

It was calculated according to the standard statistical formula indicated herewith:

n = 4 s2 / L2

where s is the standard deviation (SD) and L is the limit of error. Based on a pilot study for prevalence of anemia, the SD (Hb) was taken as 1.9. The limit of error was set at 0.2, since this was considered adequate for the purpose of this study. The sample size was calculated to be 361 children. A 30% safety margin was added to allow for a maximum estimated non-response, giving a sample size of ³510 subjects.

A complete record of 2629 children, 9-36 months of age, registered in the 41 AWs was obtained from the respective anganwadi workers. Based on these data, using the random number tables, 545 children aged 9-36 months of age and their caretakers (mother’s) were invited to participate in the study. No child was receiving iron/hematinic supplement in the ICDS program.

Ethical approval for the study was obtained from the institutional ethics committee. Following their advise, informed consent was obtained from the parents participating in the study and the ICDS functionaries.

At the time of enrolment, socio-demographic details were derived from the subjects (mother’s) using a questionnaire specially designed for the study. Information regarding social class, family income, maternal occupation, education, birth order, birth interval and number of siblings was collected.

Twenty µl blood by finger prick in 5ml Drabkin’s solution was transported (protected from light) within 2 hours to the laboratory where hemoglobin (Hb) measurements were undertaken immediately. The hemoglobin was measured using the Cyanmethemoglobin method(6) (using Drabkin’s solution and a hemoglobin standard from M/s. Ranbaxy, India, New Delhi). The variation in hemoglobin estimation on two consecutive (separate, finger prick) determinations was 2.9%, on every 10th child. To evaluate body iron stores, the level of serum ferritin (SF) was tested in a sub-sample of children (every fifth child). The blood for serum ferritin was taken by venepuncture. Serum ferritin was determined with a commercially available enzyme - immunoassay kit (Spectro Ferritin kit, Ramco Lab, Inc., Houston, TX, USA). For all the subjects included for the serum ferritin estimation, the detection of C-reactive Protein (CRP) was undertaking using AVITEX-CRP Latex Test (Omega Diagnostic Limited, Scotland, UK).

Anemia was classified based both on the cut off point at 12 and 18 months of age of hemoglobin >10.0 g/dl(7) and also WHO(8) cut-off value of <11.0 g/dl for children 5 months to 5 years of age. Hb concentrations less than 7.0 g/dl were considered severe anemia, 7.0 to 9.9 g/dl as moderate anemia and 10.0 to 10.9 g/dl as mild anemia. A cut-off value of 12 µg/L for serum ferritin was chosen based on the recommendations of WHO(8) for diagnosis of iron deficiency.

Peripheral blood films prepared in the field were stained (in the laboratory) using Leishman’s stain (Merck India Ltd., Worli, Mumbai) and the RBC morphology was studied. The slides were also examined for malarial parasite.

Stool samples were collected (from every alternate child) and examined on the same day for the presence of ova/cyst of the following parasites: Ascaris lumbricoides, Ankylostoma duodenale, Hymenolepis nana, Giardia lamblia and Entamoeba histolytica.

The food and nutrient intake of children was assessed using a ten-item food frequency and amount questionnaire (FAQ). The FAQ was designed with the intention to estimate the usual frequency and/or amount of consumption of specific items of food and drinks, including dietary supplements such as minerals, vitamin drops, etc. by children. The reliability of the dietary intake data was assessed by correlating the mean intake of the major nutrients derived from the FAQ record with the mean nutrient intake derived from the 2-3 day diet record method for approximately one-fifth of the total sample. Overall, the results for the 2-3 day dietary record method appeared to be lower than the food frequency and amount method, the difference was only significant for vitamin C (p <0.001). Except for vitamin C, high correlation was obtained for all nutrients.

Food models and series of photographs were used to help mother’s quantify the amount of food consumed. The weight of the food portions consumed was derived from the known weights of the portions portrayed in the photographs and/or from weighing duplicate portions of the items consumed.

The mean food intake was assessed for adequacy by comparing with the Balanced Diet for children as per the Dietary Guidelines for Indians(9). Nutrient intake of children was computed using the nutritional database consisting of the Indian Council of Medical Research’s (ICMR) "Food Composition Tables". For few specific local foods/items, e.g., Rusk, ‘phan’ (puffed patty) (for which data were not available in the Food Composition Table) nutritive value estimation was undertaken in the Food Analysis and Research Center (FARC), New Delhi. For breast-fed infants, the quantity of breast milk consumed was estimated based on data specific to Indian children(10).

All data were analyzed using the SPSS statistical software package. Means and standard deviations were calculated. Chi-square and ‘t’ test was used to evaluate the statistical significance. All the observations on serum ferritin and nutrient intake were taken on usual logarithm scales and then compared. Mean ± SD, geometric mean was also computed using the log transformed serum ferritin and nutrient intake observations. The significance tests were done on log values. Multiple regression analysis was performed. Statistical significance was defined as p <0.05.

A total of 545 children aged 9-36 months and their caretakers (mothers) were invited to participate in the study. These subjects (children) corresponded to about 20% of the children (in the age group 9-36 months) enrolled in the 41 AWs of Nand Nagri. The distribution of these children according to sex in different age groups was similar. Majority (50.4%) of the children belonged to schedule caste families, with an average family income of Rs. 1000-1200/month. The mother’s were predominantly housewives, majority (54%) of them illiterate.

Blood samples for Hb estimation could be obtained from 523 subjects. Parents of 22 children did not cooperate for hematological measurement. Using 10.0 g/dl as the Hb cut-off point 44% children, less than 18 months of age, in the present study population were anemic. The prevalence was comparatively higher in 13-30 months age group, with an overall prevalence of 64% among children, 9-36 month of age, based on WHO (Hb <11.0 g/dl) criteria. There were no male-female differences in any age group for hemoglobin.

Data with respect to the distribution of Hb concentration (Table I) suggest that majority (36.1%) of the children were suffering from moderate anemia, and prevalence of severe anemia among children was 7.8%. The prevalence of severe anemia was highest among children (both boys and girls) in the age category 13-18 months.

With respect to estimating the magnitude/severity of iron deficiency, 106 children were assessed for serum ferritin along with C-reactive protein (CRP). Sub-clinical infection as evident by positive CRP was found in 16 (15%) children. The log mean ± SD serum ferritin was 1.2 ± 0.5 µg/1 (geometric mean = 16.98 µg/L, 95% CI of 10.01-29.62) in CRP positive cases and 0.8 ± 0.3 µg/L (geometric mean = 6.1 µg/L, 95% CI of 5.25-7.01) in case of 90 CRP negative children, the difference being significant (p <0.001).

The serum ferritin log mean ± SD in the 46 anemic (Hb <11.0 g/dl) CRP negative cases was 0.7 ± 0.2 µg/L, with geometric mean of 4.8 µg/L (95% CI of 4.26-5.57) and mean ± SD for serum ferritin in the 44 non-anemic group was 0.9 ± 0.4 µg/L with geometric mean being 7.8 µg/L (95% CI of 5.93-9.93), the difference being highly significant (p <0.001).

The distribution of serum ferritin values among the study group with respect to age suggest that the serum ferritin values were low in most children (90 CRP negative cases). Twenty eight (31.1%) children had serum ferritin levels between 0-4.99 µg/L, 50 (55.6%) children between 5-9.99 µg/L and 1 (1.1%) child had serum ferritin between 10-11.99 µg/L, thus indicating approximately 87% prevalence (79 out of 90 children) of iron deficiency in the study population. When serum ferritin level <12 µg/L was taken as the criteria for iron deficiency, 88% prevalence of iron deficiency was recorded.

Peripheral blood smear red cell morpho-logy findings were obtained from 448 children. Normocytic normochromic peripheral smear was present in 27.5%, microcytic hypo-chromic type in 33.9%, dimorphic type (combined deficiency of iron/folate and/or vitamin B12) in 37.1%, and macrocytic normochromic type in 1.6% children (Table II). The association of the peripheral smear findings with the Hb levels (Table II) indicated that the moderate-severe anemia group had 55% dimorphic and 40.4% microcytic-hypo-chromic (95.4% iron deficient). In contrast in mild anemia group, 27%, 43.2% and 27% had normocytic-normochromic, microcytic-hypo-chromic and dimorphic anemia, respectively (70% iron-deficient). The prevalence of macrocytic anemia was least common (1.6%). No significant difference was found in the morphology of anemia between boys and girls and between the different age categories.

No peripheral smear was positive for malarial parasite.

A total of 270 stool samples were analyzed. The overall prevalence rate of intestinal parasitic infestation in the study population was 45.2%, with Giardia lamblia in 17.6%, Entamoeba histolytica cyst in 11.7% and Ascaris lumbricoides in 8.8%; others had mixed infestations. Hookworm infestation demonstrated that those children who had giardiasis and Entamoeba histolytica infection had greater prevalence of anemia. However, no significant difference was found in the distribution of Hb in the infested/non-infested children. The mean Hb among parasitic infested and non-infested children was 10.1 ± 2.2 g/dl and 10.3 ± 2.0 g/dl, respectively which was also not significantly different.

The mean food intake was calculated for 242 children (every alternate child except those not available in the second visit) based on the data obtained from the Food Frequency and Amount Questionnaire. The portion sizes for different food items consumed were taken as per the Dietary Guidelines for Indians(9). The total cereal intake was calculated to be 52 g/day. This amount was equivalent to a little more than one and a half portion of total cereals per day. The mean pulse intake was 10 g and intake of flesh foods (including meat, poultry, fish and eggs) was 4 g/day. The mean milk consumption was 410 g, amounting to approximately 4 portions of milk per day. The daily intake of green leafy vegetables (GLVs) and other vegetables was 5 g and 15 g, respectively which amounted to an intake of less than one-sixth of a portion of GLVs and other vegetables per day. Fruits were consumed in larger amounts, as compared to GLVs and vegetables, the intake being 27 g per day. Nuts and oilseeds were consumed in negligible amounts, i.e., 3 g/day. Tea intake ranged from one to six times a day, with majority of the children drinking tea 1-3 times a day.

The mean values of food when assessed for adequacy by comparing with the balanced diet for children, as per the Dietary Guidelines for Indians(9) indicated that the intake of cereals, pulses, roots, GLVs, other vegetables, fruits, sugar and fats and oils was grossly inadequate, meeting only 43%, 33%, 48%, 13%, 39%, 28%, 56% and 40%, respectively of the recommendations of balanced diet for children. The deficit in the case of GLVs was as high as 87%.

The daily nutrient intake was calculated for 242 subjects based on the data obtained from the food frequency intake questionnaire. The geometric mean daily nutrient intake of children is presented in Table III. Based on the ICMR recommended allowances(9), nutrient intake ranged from 45% (for iron) to 84% (for vitamin C) and 56% (for energy) of the RDA.

Multiple regression analysis with Hb as dependent variable (unweighted least square linear regression analysis) and socio-demographic characteristics, child’s nutrition, dietary intake, etc. as dependent variables (Table IV) showed that the birth order, number of siblings and milk intake had a significant association (p <0.05). However, these vari-ables accounted for only 14% variation, seen in the hemoglobin.

Based on the epidemiological criteria defined by the WHO(11) the severity and magnitude of anemia among children, 9-36 months of age, in the present study sample was found to be moderate to severe.

* p<0.05

There is a growing awareness that iron deficiency anemia is very common among young children primarily because of the high iron requirements for rapid growth and a low content of bioavailable iron in the child’s diet. Growth process in early childhood is important determinant of ferritin concentra-tion in the blood and it changes rapidly in the first 18 months of life(12). Investigators(12,13) have suggested alternative cut-off for infants and young children to assess the iron status. Recently, data from UK(7) suggest that a cut off of 10.0 g/dl of Hb might be more appropriate for children 12-18 months than the threshold of 11.0 g/dl recommended by WHO(8) and for serum ferritin 16 µg/L at 12 months and 12 µg/L at 18 months. Using 10.0 g/dl as the Hb cut-off point, 44% children less than 18 months of age, in the present study population were anemic. Sixty four per cent children were found to be anemic using WHO cut-off value (Hb <11.0 g/dl). Further, 88% were iron deficient using 12 µg/L as the serum ferritin cut-off value. The high incidence of anemia and iron deficiency recorded in an urban slum ICDS block in Delhi is of concern. Further, 90.4% of the study children had acute malnutrition taking weight for age as the criteria and 45% children were stunted (under preparation). Such findings provide strong basis for targeting preventive strategies for children 0-3 years of age.

Iron deficiency of dietary origin seems to be the main cause of anemia in this population, as indicated by dietary intake data, with iron being the single nutrient deficient in the diet along with energy (88% children having serum ferritin <12 µg/L). The red cell morphology also showed higher prevalence of iron defi-ciency more common in moderately anemic alongwith vitamins folate/B12 deficiency. Therefore anemic children <3 years of age (dimorphic >45%) should receive these vitamins alongwith iron. Similar findings were reported in earlier studies (14,15).

Iron intake on an average was approximately one-third of the RDA and approximately 98% children had an intake below the RDA. The iron density of the diet was found to be .008 mg/unit calories, almost 20% less than the recommended(9). The main source of iron in the diet was cereals. Consumption of green leafy vegetables and pulses was limited. Access to meat and flesh foods (sources of haem iron) was limited (with mean daily intake of 4 g). Diluted milk boiled in aluminium pans, serving, as main diet is the important cause of anemia. Such diet reduced appetite for other dietary items. Intake of tea (an iron inhibitor) ranged from 1-6 times a day. The availability of iron from such a diet would have been low. Though the bioavailability of iron in the diet was not estimated, but based on evidence(16), it would not be very wrong to presume that the bioavailability of iron from such a diet (consisting primarily of cereals, pulses, vegetable and tea) would not be more than 1.8-4.5%. Inadequate intake (with adequacy ranging from 13% to 56% as compared to RDA for children) coupled with possible low bioavailability of dietary iron would have been a major contributor to the high prevalence of anemia recorded in the study. Seasonal green leafy vegetables and fruits are becoming affordable, these will provide iron, enhancers for absorption and vitamins. In addition cooking in cast iron utensils will improve dietary iron intake(17). Failure of birth control has much to contribute, too as found by multiple regression analysis, babies of anemic mothers start life with low iron stores, further aggravated by low dietary intakes, which may affect brain functions(4). Parasitic infestations had limited or no role in the causation of anemia in the present study. No peripheral blood smear demonstrated malarial parasite. In spite of ICDS coverage in the Nand Nagri block for over two decades, the findings of the present study indicate a poor iron status of children, with prevalence of anemia in 64% and hypoferritinemia in 88% (most marked in 13-18 month old children). Forty five per cent are dimorphic suggesting vitamin folate and or B12 deficiency. Anemia was associated with poor dietary intakes. These findings in an ICDS project in the National capital, located at a distance of 2 km from the medical college hospital, shows general apathy in recognizing and controlling the most common nutritional anemia, which is manageable. Within the ICDS, therefore, such interventions need to be planned so that children under 3 years of age be specially targeted and prevented from retardation in their cognitive functions.

To conclude, world over the WHO recommended cut-off of less than 11.0 g/dl for hemoglobin and less than 12 µg/L for serum ferritin are widely used for the detection of iron deficiency anemia, among young children. A wide prevalence of anemia (63.5%, i.e., Hb <11.0 g/dl) and iron deficiency (88%, i.e., serum ferritin < 12 µg/L) was documented by us in an ICDS urban slum in 9-36 months old children and 45% of the anemic children had folate and or B12 deficiency.

The authors are indebted to Dr. Bharat Singh, Chief, Blood Transfusion Services, University College of Medical Sciences and Guru Teg Bahadur Hospital, Delhi for valuable support and assistance. Valuable suggestion from Dr. Sheila Vir are gratefully acknowledged.

Contributors: DK, KNA and LS planned and conducted the study and drafted the manuscript. KK and IK helped in hematological and microbiological studies, respectively. KNA will act as guarantor for the study.

Funding: United Nations Childrens Fund.

Competing interests: None declared.

1. National Family Health Survey-2 (NFHS-2) - India 1998-99. Key findings: Anemia among women and children. Mumbai, International Institute for Population Sciences, 2000; p 19.

2. Bhatia D, Seshadri S. Growth performance in anemia and following iron supplementation. Indian Pediatr 1993; 30: 195-200.

3. Lozoff B, Jemenez E, Wolf AW. Long-term development outcome of infants with iron deficiency. New Engl J Med 1991; 325: 687-694.

4. Agarwal KN. Iron and the brain: Neurotransmitter receptors and magnetic resonance spectroscopy. Brit J Nutr 2001; 85 (Suppl 2): 147-150.

5. Integrated Child Development Services: A Compendium of Guidelines-2000. Department of Women and Child Development, Ministry of Human Resource Development, New Delhi, Government of India, September 2000; pp vii-viii.

6. Crosby WH, Munn JG, Furth ED. Cyanmethemoglobin method for estimation of hemoglobin. US Armed Forces Med J 1964; 5: 693-697.

7. Sherriff A, Emond A, Hawkins N, Golding J and ALSPAC Children in Focus Study Team. Hemoglobin and ferritin concentration in children aged 12 and 18 months. Arch Dis Child 1999; 80: 153-157.

8. DeMaeyer EM, Dallman P, Gurney JM, Hallberg L, Sood SK, Srikantia SG. Preventing and Controlling Iron Deficiency Anemia Through Primary Health Care. Geneva. World Health Organization, 1989; pp 8-9.

9. Dietary Guidelines for Indians - A Manual. National Institute of Nutrition, India Council of Medical Research. Hyderabad, India, 1998; pp 65-73.

10. World Health Organization. The Quantity and Quality of Breast Milk. Report on the WHO Collaboration Study on Breast Feeding. Geneva, World Health Organization, 1985; pp 3-11.

11. World Health Organization. Guidelines for the Control of Iron Deficiency Anemia in Countries of the Eastern Mediterranean, Middle East and North Africa. World Health Organization, Regional Office for the Eastern Mediterranean, Alexandria, Egypt, 1996; pp 8-9.

12. Freeman VE, Hoey HMV, Gibney MJ. Iron deficiency anemia in apparently healthy free-living infants: A longitudinal study. In: Iron Nutrition in Health and Disease. International Symposikum Arranged by the Swedish Nutrition Foundation and the Swedish Society of Medicine, August 24-27, 1995.

13. Milman N. Serum ferritin in Danes: Studies of iron status from infancy to old age, during blood donation and pregnancy. Int J Hematol 1996; 63: 103-135.

14. Das BK, Bal MS, Tripathi AM, Singla PN, Agarwal DK, Agarwal KN. Evaluation of frequency and dose of iron and other hematinics: An alternative strategy for anemia prophylaxis in rural preschoolers. Indian Pediatr 1984; 21: 933-938.

15. Gomber S, Kumar S, Rusia U, Gupta P, Agarwal KN, Sharma S. Prevalence and etiology of nutritional anemias in early childhood in an urban slum. Indian J Med Res 1998; 107: 269-273.

16. Narasinga Rao BS. Bioavailability of dietary iron. Proc Nutr Soc India 1983; 28: 1-6.

17. Lal H, Agarwal KN, Gupta M, Agarwal DK. Protein and iron supplementations by altering cooking practices in community. Indian J Med Res 1973; 61: 918-925.