Anaemia and iron de ciency among adolescent schoolgirls in peri-urban Bangladesh

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1 (2000) 54, 678±683 ß 2000 Macmillan Publishers Ltd All rights reserved 0954±3007/00 $ Anaemia and iron de ciency among adolescent schoolgirls in peri-urban Bangladesh F Ahmed 1 *, MR Khan 1, M Islam 1, I Kabir 2 and GJ Fuchs 2 1 Institute of Nutrition and Food Science, University of Dhaka, Dhaka-1000, Bangladesh; and 2 ICDDR, B: Centre for Health and Population Research, Dhaka, Bangladesh Objective: To investigate the prevalence of anaemia and iron de ciency among adolescent schoolgirls in periurban Bangladesh, and to identify various factors associated with anaemia in this population. Design: A cross-sectional design. Setting: Girls' high schools in ve sub-districts of Dhaka. Subjects: Adolescent girls (n ˆ 548) aged 11 ± 16 y from nine schools in Dhaka district participated in the study. Socio-economic, anthropometric and dietary information were collected. Blood haemoglobin (Hb), serum iron, total iron binding capacity (TIBC), transferrin saturation (TS), serum ferritin (SF) and serum retinol (vitamin A) were determined. Results: The prevalence of anaemia (Hb<120 g=l) among the participants was 27%. Seventeen percent had depleted iron stores (SF<12 mg=l). Of all anaemic girls, 32% had iron de ciency anaemia (Hb<120 g=l and SF<12 mg=l). When the girls were classi ed by serum vitamin A, the third with the lowest serum retinol levels had signi cantly lower Hb and SF levels. Signi cant positive correlations were observed between Hb and serum iron, TS, SF and retinol, while there was a negative correlation with serum TIBC. Occupancy, frequency of consumption of large sh, serum iron, TIBC, TS, SF and serum vitamin A were strongly related to Hb by multiple regression analysis. For 1 mg=l change in SF concentration, there was a g=l change in Hb, when adjusted for all other factors. Conclusion: Anaemia among these adolescent schoolgirls in peri-urban Bangladesh cannot be explained by iron de ciency alone, and other causes may also exist in this population. Descriptors: iron de ciency; anaemia; adolescent girls; serum ferritin; serum vitamin A (2000) 54, 678±683 Introduction Anaemia affects more than a billion people in the world (Viteri, 1994). It is generally believed that at least half of anaemia worldwide is due to nutritional iron de ciency (WHO, 1996). Other possibly important causes of nutritional anaemia in addition to iron de ciency include de ciencies of folic acid, vitamin B 12 and vitamin A (WHO, 1972; Mejia, 1992). Non-nutritional causes of anaemia, such as haemorrhage, infection and genetic disorders may also be extremely important (INACG=WHO, 1989; Linpisarn et al, 1996). Iron de ciency anaemia has serious health consequences, especially for young children and women. Anaemic pregnant women are at greater risk of death during the perinatal period (Viteri, 1994). A de cient intra-uterine blood supply to the foetus due to iron de ciency anaemia *Correspondence: F Ahmed, Institute of Nutrition and Food Science, University of Dhaka, Dhaka-1000, Bangladesh. farahmed@du.bangla.net Guarantor: F Ahmed. Contributors: F Ahmed took the lead in planning the study, coordinated the eld and laboratory work, analysed the data and writing the paper. MR Khan assisted in eld work, carried out biochemical analysis and contributed in writing the paper. M Islam assisted with data handling, analysis and writing the paper. I Kabir and GJ Fuchs were involved in designing the study and contributed in writing the paper. Received 14 October 1999; revised 12 April 2000; accepted 2 May 2000 during pregnancy may result in premature labour, still birth, abnormal labour (Goltner, 1975) and perhaps lower foetal weight (WHO, 1975). More insidious social costs of iron de ciency are limitation in intellectual development in children (Pollitt et al, 1989) and impaired work performance in adults (Edgerton et al, 1979), which together constrain social and economic development. The national vitamin A survey in 1997 ± 1998 revealed the prevalence of anaemia to be 43% in girls aged 11 ± 16 y and 45% in women of child bearing age in rural Bangladesh (HKI=IPHN, 1999a). However, data on the causes of anaemia and the proportion which can be directly attributed to iron de ciency among Bangladeshi population are scarce (Ahmed, 2000). In a study in urban school girls, we observed a negative correlation between serum total iron binding capacity and haemoglobin level, suggesting that a signi cant proportion of anaemia might be related to iron de ciency (Ahmed et al, 1996). Further, there was evidence of association between serum levels of vitamin A and iron indicators (Ahmed et al, 1996). Studies in other countries have also reported similar ndings (Bloem et al, 1989; Suharno et al, 1992; Wolde-Gebriel et al, 1993). There has been a suggestion that vitamin A exerts an in uence on the metabolic availability of iron, and hence haemoglobin formation (Mejia, 1992). The national vitamin A survey of Bangladesh in 1997 ± 1998 showed that nearly 47% of rural girls aged 11 ± 16 y had less than adequate levels of serum vitamin A (<1.05 mmol=l), with 11.6% having sub-

2 clinical de ciency (serum retinol <0.7 mmol=l, HKI=IPHN, 1999b). Adolescence is a critical stage of life for physical growth and sexual development (Dreizen et al, 1967). It is well documented that the growth velocity during adolescence is slower in undernourished populations (Eveleth and Tanner, 1990), giving rise to cephalopelvic disproportion which, in the adolescents who become pregnant, is related to increased maternal and foetal mortality (Harrison et al, 1985). It has also been suggested that iron is an essential nutrient for skeletal growth (Herbeth et al, 1991) and, thus, iron de ciency may be a limiting factor for growth during adolescence (Brabin and Brabin, 1992). In Bangladesh, almost a quarter of the total population are adolescents. In a society such as Bangladesh where the rst pregnancy is likely to occur before adolescence is completed, the physical growth of girls during adolescence may have critical effect on their capacity for successful pregnancies. The present study was designed to investigate the prevalence of anaemia and iron de ciency among adolescent schoolgirls in peri-urban Bangladesh, and to identify factors associated with anaemia in this population. Subjects and methods The study group consisted of 548 girls aged 11 ± 16 y, who were students of grades VI ± X in nine different high schools for girls in ve sub-districts of Dhaka district. Two schools were selected from all but one of the ve sub-districts. Twelve girls were selected from each class by random sampling. Thus, 60 girls from each school and 120 from each sub-district were selected. In one sub-district with only one girls' high school, all the 120 girls were selected from the same school by randomly selecting 24 students from each class. The purpose of the study was explained to the administration of each school and to subjects and their parents. Only girls who obtained written parental consent were included. The response rate varied from 80 to 95% in each school, and the study was conducted during September to November The ethical committee of the ICDDR, B: Centre for Health and Population Research approved the study. Questionnaire and sample collection A questionnaire was developed to obtain information on the socio-economic conditions, personal characteristics and current morbidity. Parents were asked about family size, income, their academic quali cations and occupation, housing conditions and cultivable land holdings. Personal characteristics and current morbidity of the subjects were collected by interviewing the subjects. Morbidity data were restricted to diarrhoea, respiratory tract infection and fever in the previous 2 weeks. A 7 day food frequency questionnaire on selected foods was used to obtain the dietary pattern of the participants. Fish intake was categorized as large and small sh. Anthropometric data and a sample of 5.0 ml venous blood were collected from each subject on the same day. An aliquot of the blood was placed immediately in a test tube containing Drabkin's solution for haemoglobin estimation. The rest of the blood specimen was taken in a deionized centrifuge tube and kept in an icebox, then transferred to the laboratory within 6 h, where serum was separated by centrifugation and kept frozen at 20 C until analysis. Anthropometric and biochemical measurements Body weight was taken to the nearest 100 g. The girls were weighed barefoot, with school uniform on. The school uniform was weighed later (average weight was 0.5 kg) and the value subtracted from the measured weight to provide the recorded weight. The height was measured barefoot to the nearest 0.1 cm. Weight and height were measured on a combined height ± weight scale (Detecto-Medic; Detecto Scales Inc., Webb City, MO). The percentage of median and Z-scores for weight-forage and height-for-age were calculated using the `Anthro' package based on United States National Center for Health Statistics (NCHS) reference data (CDC=WHO, 1990). Stunting was determined on the basis of height-for-age below the third percentile, using a 6 month age bracket (WHO, 1995), of the NCHS reference data (NCHS, 1976). Wasting, or thinness, was de ned by body mass index (BMI) for age using a cut-off value below the fth percentile, by a 12 month age bracket (WHO, 1995). Haemoglobin (Hb) concentration was quanti ed by the cyanomethaemoglobin method, and serum iron and total iron binding capacity (TIBC) were determined without deproteinization by the bathophenanthroline method using commercial kits (Boehringer Mannheim, Germany). Serum transferrin saturation (TS) was calculated from serum iron and TIBC values. Measurement of serum ferritin (SF) was performed by enzyme linked immunosorbant assay (Genzyme, California, USA). Serum vitamin A (retinol) was determined by the HPLC procedure as described elsewhere (Ahmed et al, 1997). Statistical analysis Univariate analysis consisted of simple frequency distribution of selected variables. Data are presented as mean + standard deviation. Anaemia was identi ed according to the WHO criterion, ie Hb level <120 g=l (WHO, 1972). The prevalence of various degrees of iron de ciency was determined by the following criteria: low iron stores were characterized as those having a normal Hb and SF 12 ± 20 mg=l; iron depletion was de ned as a normal Hb and SF<12 mg=l; and iron de ciency anaemia as Hb<120 g=l and SF<12 mg=l (Cook and Finch, 1979). It has been suggested that a higher cut-off value for SF (<20 mg=l) be used in populations where infections and=or in ammatory diseases are highly prevalent to assess risk of iron de ciency (Cook and Finch, 1979). To assess the relationship of serum vitamin A concentration with Hb and other iron indices, the girls were divided into three groups to produce approximately equal numbers in each group based upon the distribution of serum vitamin A. For each third, mean concentrations of Hb and other iron indices were calculated, and the statistical signi cance of the differences between groups assessed by one-way analysis of variance followed by Duncan's multiple range test. Pearson's correlation test was performed to examine the association of Hb concentration with various iron indices and serum vitamin A concentrations. Finally, backward stepwise multiple regression analysis was done to examine the independent relationship of Hb concentration with various social, dietary and biochemical factors. The data were analysed using SPSS=PC version

3 680 Results The mean age of the study participants was y. The girls came from families in which the parents had achieved at least moderate education level. Only 11% of the fathers and 22% of the mothers were illiterate. Seventyseven percent of the subjects' fathers had either jobs or businesses, and only 15% were farmers. Ninety-one percent of the mothers were housewives. Sixty percent of the girls came from medium size households consisting of ve to seven members, and 18% came from relatively low-income families, earning less than 2500 Taka (46 Taka ˆ 1 US$) per month. The majority (59%) of families owned no cultivable land. Eighty-six percent of the girls resided on homesteads owned by their families. Nearly sixty percent of the families lived in houses built of thatch, straw, clay etc, 69% had hygienic latrines and almost all (99%) families used tube well water in cooking and other household purposes. Mean ( + s.d.) body weight, height, weight-for-age, height-for-age and body mass index (BMI) of the girls are shown in Table 1. The prevalence of stunting increased from 11 to 15 y of age, with 28% of the girls being stunted on average (Figure 1). For the group as a whole, 13.5% of the girls were thin based on BMI for age, and 7% were overweight (weight-for-height >120%). The mean frequency of weekly consumption was for eggs 1.9, milk 3.1, meat 2.1, liver 0.2, large sh 3.8, small sh 5.5, dark green leafy vegetables (DGLV) 2.9, and fruits rich in vitamin C 3.5. A substantial proportion of the girls did not consume any eggs (36%), milk (36%), meat (39%) and vitamin C rich fruits (30%) in the week preceding the interview, while 60% of the girls consumed small sh, 44% consumed large sh and 31% of the girls consumed DGLV at least four times a week. Mean (+ s.d.) Hb concentration was (+ 11.6) g=l (Table 2). Twenty-seven percent were below the cut-off point for anaemia for girls in this age group, 120 g=l for Hb. Table 2 also shows the data on serum iron, TIBC, TS, SF and serum vitamin A. Thirty-one percent of the girls had low serum iron (<10.75 mmol=l). Using a cut-off point of 16% for serum TS, 21% of the girls had iron de cient erythropoiesis, and 17% of the girls had depleted iron stores judged by SF (<12 mg=l). Thirty-nine percent of the participants had serum vitamin A less than adequate level of 1.05 mmol=l, with only 3% having sub-clinical de ciency. Further analysis was done to examine the distribution of the participants by iron de ciency and iron de ciency anaemia. Of the anaemic girls, 32% were found to have iron de ciency anaemia (Hb<120 g=l and SF<12 mg=l). Although the girls in our study were apparently healthy, we did not have any information regarding concurrent subclinical infection. Using a more inclusive cut-off of SF of Figure 1 The degree of stunting and thinness of the girls at schools in peri-urban Bangladesh. <20 mg=l instead of <12 mg=l, a total of 44.2% were found to have iron de ciency anaemia. Among the girls with normal Hb ( 120 g=l) level, 11.7% were iron depleted (SF<12 mg=l) and 9.2% had low iron stores (SF 12 ± 20 mg=l). The relationships of serum vitamin A level with Hb and other iron indices of the girls are shown in Table 3. The girls were divided into three groups of approximately equal size based upon the distribution of serum vitamin A concentration. The mean concentrations of Hb and other iron indices were calculated for each third. As the serum retinol level increased, the mean levels of Hb, serum iron and SF increased. However, the differences between groups were statistically signi cant for Hb and SF only. There were signi cant positive correlations between the levels of Hb and serum iron (r ˆ 0.27; P ˆ 0.000), TS (r ˆ 0.26; P ˆ 0.000), SF (r ˆ 0.29; P ˆ 0.000) and serum vitamin A (r ˆ 0.32; P ˆ 0.000), but a negative correlation with serum TIBC (r ˆ 0.22; P ˆ 0.000). Factors in uencing Hb level of the girls were examined in more detail Table 1 Anthropometric indices of the adolescent girls at schools in periurban Bangladesh Variable Mean s.d. Body weight (kg) Height (cm) Weight-for-age (% median) Weight-for-age (Z-score) Height-for-age (% median) Height-for-age (Z-score) Body mass index (kg=m 2 ) Table 2 Haemoglobin, iron indices and serum vitamin A concentrations of the adolescent girls at schools in peri-urban Bangladesh Variable Mean s.d. Haemoglobin (g=l) Serum iron (mmol=l) Serum total iron binding capacity (mmol=l) Serum transferrin saturation (%) Serum Ferritin (mg=l) Serum vitamin A (mmol=l)

4 Table 3 Mean concentrations of haemoglobin and other iron indices by thirds of serum vitamin A (retinol) concentration 681 Low third, n ˆ 177 Middle third, n ˆ 169 High third, n ˆ 180 (upto mmol=l) (1.01 ± mmol=l) (above mmol=l) Variable Mean (95%Cl) Mean (95%Cl) Mean (95%Cl) P-value* Haemoglobin (g=l) (118.7 ± 122.3) a (124.8 ± 128.1) b (127.7 ± 130.6) c Serum iron (mmol=l) 12.4 (11.7 ± 13.2) a 12.9 (12.3 ± 13.6) ac 13.5 (12.8 ± 14.2) c 0.08 Serum total iron binding capacity (mmol=l) 58.0 (56.1 ± 59.9) 57.9 (56.3 ± 59.5) 57.6 (56.1 ± 59.2) 0.95 Serum Transferrin (%) 22.8 (21.2 ± 24.5) 22.9 (21.6 ± 24.3) 24.4 (23.0 ± 25.9) 0.24 Serum ferritin (mg=l) 41.0 (35.8 ± 46.2) a 45.3 (40.2 ± 50.5) a 53.7 (48.1 ± 59.4) b *Based on one-way analysis of variance. Values with different superscripts differ signi cantly from each other by Duncan's multiple range post hoc test. Table 4 Backward-stepwise multiple regression for haemoglobin concentration of adolescent school girls in the peri-urban Bangladesh Variable B s.e. B t Signi cance, t Serum iron (mmol=l) Serum total iron binding capacity (mmol=l) Serum transferrin saturation (%) Serum ferritin (mg=l) Serum vitamin A (mmol=l) Occupancy Consumption of large sh Multiple r, 0.505; R square, 0.255; adjusted R square, 0.244; F-ratio, 21.8 (d.f. 7); P ˆ using a backward stepwise multiple regression analysis (Table 4). In the analysis, age, BMI, per capita income, parent's education, cultivable land, occupancy, prevalence of morbidity, frequency of consumption of eggs, milk, meat, liver, small and large sh, DGLV and fruits, serum iron, TIBC, TS, SF and serum vitamin A were included. Using a P of >0.10 for exclusion, only occupancy, frequency of intake of large sh, serum iron, TIBC, TS, SF and serum vitamin A were found to be signi cantly related to Hb. The overall F-ratio was 21.8 (d.f. ˆ 7) and was highly signi cant (P ˆ ). The adjusted r square was (multiple r ˆ 0.505). For 1 mg=l change in SF level there was g=l change in Hb, taking into account all the other factors in the equation. Discussion This study reports on the extent of iron de ciency anaemia among adolescent schoolgirls in peri-urban Bangladesh. We are not aware of any other report that has characterized iron status of this population using the SF. Adolescent schoolgirls of Bangladesh were chosen as the subjects of this study because these girls are likely to become pregnant and their growth during adolescence will in part have an impact on their ability to carry a successful pregnancy, and thereby determine the well-being of the next generation. These girls mostly came from modestly educated families, but lived in a peri-urban setting with relatively low to modest socioeconomic background. The study did not include adolescents who were not attending schools and did not, therefore, include girls from the peri-urban poor. Girls who attend school are likely to come from backgrounds that represent better education as observed from the socioeconomic data and, therefore, the study subjects may not be representative of the wider population. If height is taken as the most representative characteristic for overall growth and development (Waterlow and Schurch, 1994), 28% of the girls showed evidence of stunting on the basis of height-for-age below the third percentile, indicating that a large proportion of the girls were suffering from chronic energy de ciency. Further, the prevalence of stunting was nearly three times that of adolescent school girls in Dhaka city (Ahmed et al, 1998). In the present study, about 13.5% of the girls were thin based on BMI for age and 7% overweight (weight for height >120%), which is very similar to 16% thin and 10% overweight in the earlier study in urban adolescent school girls (Ahmed et al, 1998). The data on dietary pattern of the girls revealed very low intakes of eggs, milk and meat, rich sources of protein and some important micronutrients. It appears that 25% of the girls did not eat large sh at all and another 36% ate them occasionally, indicating the possibility of inadequate protein intake. Quantitatively, the usual portion size of the small sh is very small and its contribution as a source of protein in the diet is negligible. On the other hand, the portion size of a large sh is usually considerable in amount and thus may contribute a substantial amount of protein in this population. To determine the prevalence of iron de ciency using a single criterion, the Hb concentration de nes anaemia, the TS de nes iron de cient erythropoiesis, and the SF de nes iron storage depletion (INACG, 1985). In the present study, 27% of the girls were anaemic (Hb<120 g=l), none with severe anaemia. For the group as a whole, 21% had iron de cient erythropoiesis (TS<16%) and 17% had depleted iron stores (SF<12 mg=l). The limitation in using the Hb level as a single criterion for iron de ciency is that it not only lacks speci city but is also relatively insensitive as there is a marked overlap in haemoglobin levels between normal and anaemic individuals (Garby et al, 1969). Further, the problem of overlapping values between normal and abnormal populations also applies to serum TS because of limited precision (Cook and Finch, 1979). Although SF is considered to be the most sensitive indicator of iron status, it should be mentioned that ferritin concentrations in serum can be in the normal range independent of iron de ciency in conditions of in ammation, concurrent infection, or liver disease (Siimes et al, 1974; Abshire and Reeves, 1983).

5 682 On the basis of combined cut-off points for Hb and SF concentrations (Hb<120 g=l and SF<12mg=l), the present study indicates that iron de ciency anaemia is a public health problem among adolescent schoolgirls of peri-urban Bangladesh, but unexpectedly constituted only about 32% of all anaemic girls. More recently, a study using the relative operating characteristics (ROC) curve testing, has investigated the sensitivity and speci city of SF as an indicator of iron de ciency, and showed that a cut-off value of 41 mg=l for SF could provide the optimal diagnostic ef ciency for iron de ciency among anaemic subjects (Punnonen et al, 1997). In the present study, using the cut-off limit of 41 mg=l for SF about 72% of the girls were found to have iron de ciency anaemia. However, it is noteworthy that still nearly a third of the anaemia in the girls could not be accounted for by iron de ciency. Recently, Kolsteren et al (1999) reported that 77% of the non-pregnant women from urban slum of the north-western part of Bangladesh had iron de ciency anaemia using the cut-off value of 41 mg=l. It may, however, be mentioned that now serum transferrin receptor is considered to be the more reliable indicator for the assessment of iron de ciency (Ferguson et al, 1992), thus the present study merits further investigation. A large number (39%) of our subjects had inadequate serum retinol concentration (<1.05 mmol=l), and we found a signi cant association between Hb and serum retinol levels. To further explore any relation between different levels of serum vitamin A and various iron indices, the subjects were divided into three groups on the basis of serum retinol concentrations. For each third, the mean Hb and other iron indices were calculated. The result of analysis of variance showed that the girls with lowest serum retinol level had lower Hb and SF levels, indicating that marginal vitamin A status might compromise iron metabolism and hence Hb formation. An association of lower serum retinol with lower iron indices, including Hb, has also been reported in children (Bloem et al, 1989), adolescent girls (Ahmed et al, 1996), and in pregnant women (Suharno et al, 1992). A depressed iron uptake by bone marrow and hence Hb formation has been suggested to be one of the mechanisms (Beyen et al, 1992; Mejia, 1992). A recent study suggests that vitamin A may also increase absorption of iron from forti ed food two-fold and that it prevents the inhibitory effects of dietary phytates on iron absorption in humans (Garcia-Casal et al, 1998). Finally, the ndings of the multiple regression analysis revealed that Hb concentration was independently signi cantly related to occupancy, frequency of consumption of large sh, various iron indices and serum vitamin A levels. The occupancy may be considered as a proxy of socioeconomic condition, and our data revealed that the girls who lived in rented houses (occupancy) had lower Hb level, suggesting that socioeconomic condition may be an important factor in maintaining normal Hb. A number of studies have also shown that children from lower socioeconomic group are more likely to have lower Hb level (Pollitt and Leibel, 1976; Ahmed et al, 1992). As has already been mentioned, large sh intake is considered to be an important source of dietary protein in this population, and protein status is closely related to Hb synthesis. Further, the results show that for a 1 mmol=l change in serum vitamin A there is a 10.1 g=l change in Hb level, taking other factors into account, a nding similar to that observed among adolescent schoolgirls in Dhaka city (Ahmed et al, 1996). Finally, the adjusted r square was found to be 0.244, suggesting that the variables in the equation accounted for 24.4% of the variance in Hb concentration. In conclusion, the results suggest that anaemia among peri-urban Bangladeshi adolescent schoolgirls cannot be solely explained by iron de ciency. Other causes may also exist in the population. The ndings of the present study have important implications on the iron supplementation programmes. Frequently the effectiveness of the programmes is found to be poor, which has become a major concern (UNACC=SCN, 1991; Schultink and Gross, 1996). Our data reinforce the suggestion that programmes designed to reduce anaemia should also aim to improve vitamin A status (Bloem, 1995). Acknowledgements ÐWe thank the PCC, ICDDR, B for the nancial support to conduct the study. The authors also express their sincere thanks to the participants of this study. References Abshire TC & Reeves JD (1983): Anaemia of acute in ammation in children. J. Pediatr. 103, 868 ± 871. Ahmed F (2000): Anaemia in Bangladesh: a review of prevalence and aetiology. Public Health. Nutr. (in press). Ahmed F, Mohiduzzaman M, Barua S, Shaheen N, Margetts BM & Jackson AA (1992): Effect of family size and income on the biochemical indices of urban school children of Bangladesh. Eur. J. Clin. Nutr. 46, 465 ± 473. Ahmed F Khan MR, Karim R, Taj S, Hyderi T, Faruque MO, Margetts BM & Jackson AA (1996): Serum retinol and biochemical measures of iron status in adolescent schoolgirls in urban Bangladesh. Eur. J. Clin. Nutr. 50, 346 ± 351. Ahmed F, Hasan N & Kabir Y (1997): Vitamin A de ciency among adolescent female garment factory workers in Bangladesh. Eur. J. Clin. Nutr. 51, 698 ± 702. Ahmed F, Zareen M, Khan MR, Banu CP, Haq N & Jackson AA (1998): Dietary pattern, nutrient intake and growth of adolescent school girls in urban Bangladesh. Public Health Nutr. 1, 83 ± 92. Beyen AC, Sijtsma KW, Van den Berg GJ, Lemmens AG, West CE (1992): Iron status in rats fed a puri ed diet without vitamin A. Biol. Trace Elem. Res. 35, 81 ± 84. Bloem M (1995): Interdependence of vitamin A and iron: an important association for programmes of anaemia control. Proc. Nutr. Soc. 54, 501 ± 508. Bloem MW, Wedel M, Egger RJ et al (1989): Iron metabolism and vitamin A de ciency in children in Northeast Thailand. Am. J. Clin. Nutr. 50, 332 ± 338. Brabin L & Brabin BJ (1992): The cost of successful adolescent growth and development in girls in relation to iron and vitamin A status. Am. J. Clin. Nutr. 55, 955 ± 958. CDC=WHO (1990): Anthro. Division of Nutrition, Center for Disease Control in collaboration with the Nutrition Unit, World Health Organization. Geneva: WHO. Cook JD & Finch CA (1979): Assessing iron status of a population. Am. J. Clin. Nutr. 32, 2115 ± Dreizen S, Spirakis CN & Stone RE (1967): A comparison of skeletal growth and maturation in undernourished and well-nourished girls before and after menarche. J. Pediatr. 70, 256 ± 263. Edgerton VR, Gardner GW, Ohira Y, Gunawardena KA & Senewiratne B (1979): Iron de ciency anaemia and its effect on work productivity and activity patterns. Br. Med. J. 2, 1546 ± Eveleth PB & Tanner JM (1990): Worldwide variation in Human Growth, 2nd edn. Cambridge: Cambridge University Press. Ferguson, BJ, Skikne BS, Simpson KM, Baynes RD & Cook JD (1992). Serum transferrin receptor distinguishes the anaemia of chronic disease from iron de ciency anaemia. J. Lab. Clin. Med. 19, 385 ± 390. Garby L, Irnell L & Werner I (1969). Iron de ciency in women of fertile age in Swedish community. III. Estimation of prevalence based on response to iron supplementation. Acta Med. Scand. 185, 113 ± 117. Garcia-Casal MN, Layrisse M, Solano L et al (1998): Vitamin A and betacarotene can improve non-heme iron absorption from rice, wheat and corn by humans. J Nutr. 128, 646 ± 650.

6 Goltner E (1975): Iron requirement and de ciency in menstruating and pregnant women. In: Iron Metabolism and its Disorders, ed. H. Keif. Proceedings of the Third Workshop Conference, Hoecnst. Schloss Reisnsburg, pp 159 ± 167. Amsterdam: Excerpta Medica. Harrison KA, Fleming AF, Briggs ND & Rossiter CE (1985): Growth during pregnancy in Nigerian primigravidae. Br. J. Obstet. Gynaccol. 5, (Suppl) 32 ± 39. Herbeth B, Spyckerella Y & Deschamps J-P (1991): Determinants of plasma retinol, beta carotene and tocopherol during adolescence. Am. J. Clin. Nutr. 54, 884 ± 889. HKI=IPHN (1999a): Iron de ciency anaemia throughout the lifecycle in rural Bangladesh: vitamin A survey 1997 ± Dhaka: HKI. HKI=IPHN (1999b): Vitamin A status throughout the lifecycle in rural Bangladesh: vitamin A survey 1997 ± 98. Dhaka: HKI. INACG (1985): Measurements of iron status: a report of the International Nutritional Anaemia Consultative Group. USA: INACG. INACG=WHO (1989): Iron de ciency in women. USA: INACG=Geneva: WHO. Kolsteren P, Rahman SR, Hilderbrand K & Diniz A (1999): Treatment for iron de ciency anaemia with a combined supplementation of iron, vitamin A and zinc in women of Dinajpur, Bangladesh. Eur. J. Clin. Nutr. 53, 102 ± 106. Linpisarn S, Tienboon P, Promtet N, Putsyaninunt P, Santawanpat S & Fuchs GJ (1996): Iron de ciency and anaemia in children with a high prevalence of haemoglobinopathies: implications for screening. Int. J. Epidemiol. 25: 1262 ± Mejia LA (1992): Role of vitamin A in iron de ciency anaemia. In: Nutritional Anaemias, eds SJ Fomon & S Zlotkin, Nestle Nutrition Workshop Series, Vol 30, pp 93 ± 101. Vevey: Nestle Ltd=New York: Raven Press. NCHS (1976): Growth curves for children 0 ± 18 y. Washington, DC: National Centre for Health Statistics. Pollitt E & Leibel RL (1976): Iron de ciency and behaviour. J. Paediatr. 88, 372 ± 381. Pollitt E, Hathirat P, Kotchabharkdi N, Missell L & Valyasevi A (1989): Iron de ciency and educational achievement in Thailand. Am. J. Clin. Nutr. 50(Suppl) 687 ± 696. Punnonen K, Irjala K & Rajamaki, A (1997): Serum transferrin and its ratio to serum ferritin in the diagnosis of iron de ciency. Blood 89, 1052 ± Schultink W & Gross R (1996): Iron de ciency alleviation in developing countries. Nutr. Res. Rev. 9, 281 ± 293. Siimes MA, Addiego JE & Dallman PR (1974): Ferritin in serum: the diagnosis of iron de ciency and iron overload in infants and children. Blood 43, 581 ± 590. Suharno D, West CE, Muhilal, Logman MHGM, de Waart FG, Karyadi D & Hautvast JGAJ (1992): Cross-sectional study on the iron and vitamin A of pregnant women in West Java, Indonesia. Am. J. Clin. Nutr. 56, 988 ± 993. UNACC=SCN (1991): Controlling iron de ciency. ACC=SCN state-ofthe-art series. Geneva: ACC=SCN. Viteri FE (1994): The consequences of iron de ciency and anaemia in pregnancy on maternal health, the foetus and the infants. SCN News. 11, 14 ± 17. Waterlow JC & Schurch B (1994): Causes and mechanism of linear growth retardation. Proceedings of the IDECG Workshop. Eur. J. Clin. Nutr. 48 (Suppl 1). Wolde-Gebriel Z, West C, Haile Gebru Tadesse A et al (1993): Interrelationship between vitamin A, iodine and iron status in school children in Shoa Region, Central Ethiopia. Br. J. Nutr. 70, 593 ± 607. WHO (1972): Nutritional anaemias. Technical Report Series 503. Geneva: WHO. WHO (1975): In control of nutritional anaemia with special reference to iron de ciency. Technical Report Series 580. Geneva: WHO. WHO (1995): Physical status: the use and interpretation of anthropometry. Technical Report Series no Geneva: WHO. WHO (1996): Guidelines for the control of iron de ciency in countries of the Eastern Mediterian, Middle East and North Africa. WHO- EM=NUT=177, E=G=11. Geneva: WHO. 683