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(Journal of Nutrition. 2001;131:758-764.)
© 2001 The American Society for Nutritional Sciences


Articles

Dietary Intakes and Socioeconomic Factors Are Associated with the Hemoglobin Concentration of Bangladeshi Women1

Alok Bhargava*2, Howarth E. Bouis{dagger} and Nevin S. Scrimshaw**

* From the Department of Economics, University of Houston, Houston, Texas 77204-5882; {dagger} International Food Policy Research Institute, 2033 K Street NW, Washington, D.C. 20006 and ** International Nutrition Foundation, Box 500, Charles Street Station, Boston, Massachusetts 02114

2To whom correspondence should be addressed.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Iron deficiency anemia affects a large number of women in developing countries, especially during child-bearing years. The hemoglobin concentration is useful for identifying iron deficiency anemia. The main objectives of this study were, first, to extend algorithms for calculating bioavailable iron from mixed diets, taking into account the enhancers and inhibitors of iron absorption under alternative assumptions on body iron stores. Second, a comprehensive longitudinal model was developed for the proximate determinants of hemoglobin concentration that included the subjects’ dietary intakes, nutritional status, morbidity and socioeconomic factors and the unobserved between-subject differences. The model for hemoglobin concentration was estimated using three repeated observations on 514 free living women in Bangladesh. Socioeconomic factors affecting the iron intake from meat, fish and poultry and from all animal sources were also modeled. The main results were that bioavailable iron, women’s height and mid upper arm circumference and intake of iron tablets were significant predictors of hemoglobin concentration. Increases in household incomes were associated with higher intake of iron from meat, fish and poultry and from all animal sources. The algorithms for estimating bioavailable iron showed the importance of assumptions regarding body iron stores and underscored the need to develop suitable algorithms for subjects in developing countries.


KEY WORDS: • bioavailable iron • iron deficiency anemia • socioeconomic factors • longitudinal data • random effects models


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Iron deficiency anemia (IDA)3 is widely prevalent in low and middle income countries. It is estimated that 3.5 billion persons have IDA (UNICEF/WHO 1999Citation ). IDA hinders normal human functions in all age groups. For example, IDA lowered labor productivity of Indonesian rubber tappers (Basta et al. 1979Citation ) and Sri Lankan tea pickers (Gardner et al. 1977Citation ), adversely affected birth outcomes (Bhargava 2000Citation ) and impaired the cognitive development of children (Lozoff 1988Citation , Pollitt 1993Citation ). The productivity loss and human costs associated with IDA are enormous (UNICEF/UNU/WHO/MI 1999Citation ).

Poor diet quality and low bioavailability of dietary iron are important factors that contribute to IDA (Tatala et al. 1998Citation ); iron loss due to parasitic infection and menstrual bleeding and pregnancy can exacerbate IDA in women. For the design of effective policies, it is essential to adopt a multifactorial approach to analyzing the proximate determinants of IDA under actual living conditions. Thus, for example, the success of iron fortification programs is likely to vary with the intakes of meat, fish, poultry (MFP) and vitamins A and C, which enhance nonheme iron absorption, and of phytates and tannins, which inhibit it (Garcia-Casal et al. 1998Citation , Hallberg et al. 1989 and 1997Citation Citation , Monsen et al. 1978Citation ).

The algorithms developed for calculating iron bioavailability in the presence of enhancers such as meat and vitamin C were recently extended to incorporate the inhibitory effects of phytates, which chelate iron, thereby reducing its absorption (Tseng et al. 1997Citation ). Although iron intake by the poor in Bangladesh comes from staple foods such as rice, contamination iron from pots, small quantities from green and yellow vegetables and animal products, the phytate content of the meal is typically high. Thus, algorithms for calculating iron bioavailability and taking into account the enhancers and inhibitors of iron absorption at each meal are specially useful for subjects in developing countries. However, the inhibitory effects of phytate intakes have been customarily calculated from data on healthy subjects with ~500 mg of iron stores (Brune et al. 1992Citation , Hallberg et al. 1989Citation ). By contrast, iron absorption rates in the presence of enhancers were tabulated for body stores 0, 250 and 500 mg by Monsen et al. (1978Citation ); alternative assumptions on body iron stores lead to different estimates of absorbable iron.

Hemoglobin concentration (Hb) is a widely used measure for assessing IDA (Khusun et al. 1999Citation , UNICEF/WHO 1999Citation ). Although measures such as serum ferritin and erythrocyte protoporphyrin provide additional insights into iron status, there are logistics and other difficulties in transporting venous blood samples from a large number of subjects living in remote areas of developing countries. Thus, modeling the proximate determinants of Hb measured in the field through a fingerprick can be valuable for deciding on the allocation of resources among instruments such as government policies that encourage MFP production, the provision of elemental iron tablets, and so on.

Thus far, only a few studies in the nutrition literature have attempted to quantify the effects of dietary intakes on serum iron measures (Doyle et al. 1999Citation , Du et al. 2000Citation ). Also, most previous analyses did not incorporate other confounding factors and did not address in detail the methodological issues surrounding the bioavailability of iron. Dietary intakes and supplements, morbidity from infectious disease and genetic factors are likely to affect Hb status. Therefore, we developed and estimated comprehensive longitudinal models for the proximate determinants of the Hb status of Bangladeshi women. Because the success of interventions will be influenced by the way in which dietary intakes change with incomes, we also estimated a model for assessing the impact of increases in household incomes on iron intake from MFP (FeMFP) and for iron intake from all animal sources.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Subjects.

The study was conducted in 16 villages in Jessore, 10 in Saturia and 18 in Mymensingh, Bangladesh (Bouis et al. 1998Citation ). One of the purposes of the research was to investigate the nutritional impact of the adoption of agronomically improved vegetables in Saturia and fish pond management strategies in Jessore and Mymensingh. At each site, the new technologies were introduced through nongovernment organization programs that provided credit and training to women. The selection of households was done in a complex manner to ensure that the selected households were representative of the three sites. Initially, there were 990 households, of which 33 did not participate in all four survey rounds. The sample size was further reduced because some women were not available for Hb measurements during one or more survey rounds. A comparison of the households in the census sample with nationally representative surveys for Bangladesh (Rahman et al. 1996Citation ) indicated that households in our sample were representative of households in the threes sites and not atypical of rural Bangladesh.

The study design was approved in 1996 by a human subjects committee of the Bangladesh Medical Research Council in Dhaka. The surveys began in June 1996, and the fourth survey round was completed by September 1997. Because Hb was measured in survey rounds 2, 3 and 4, we analyzed the data from these rounds. Overall, there were 664 women in the age group 15–49 y (one from each household) for whom three observations separated by 4-mo intervals were available. Because observations on nutritional, anthropometric and other variables were missing for some women in the three survey rounds, models for Hb were estimated using the complete data on 514 women. The models for women’s intake of FeMFP and for iron intake from all animal sources were estimated using the data on 514 women. For the simple autoregressive models estimating between- and within-subject variations in Hb, data on 664 women in three survey rounds were used; Hb data on a subset of 71 women on 4 consecutive d in the fourth survey round were also analyzed.

Economic, demographic and morbidity variables.

Background information was compiled on household members’ age, relationship with the head of the household, occupation, education and other items. Detailed information was gathered in the four survey rounds on economic variables such as household assets, incomes, food and nonfood expenditures, wages and so on; a variable was constructed for the average per capita monthly expenditures for each round. In poor countries, expenditure data are more reliable measures of economic well-being than are incomes. The reproductive history of each woman was investigated, and the current pregnancy and lactation status was recorded. In each survey round, the women were questioned about symptoms such as fever, cough, diarrhea and any diseases in the past 2 wk; women with mucus and blood in the diarrhea were questioned. Work loss due to chronic illness during the year was also assessed.

Anthropometry and hematology.

Weight and arm circumferences of the women were measured in each survey round; height was measured at the start of the study. Spring scales accurate to 0.25 kg were used to measure the subjects’ weight in light clothing. An adjustable wooden measuring board was used to measure height to the nearest 0.1 cm with the woman standing in upright position. A paper tape was used to measure the mid upper arm circumference (MUAC). Hb status was measured in the three survey rounds with a fingerprick sample of capillary blood obtained by a physician and analyzed immediately using a portable photometer (HemoCue; HemoCue Inc., Mission Viejo, CA).

Nutritional intakes and bioavailable iron.

In each of the three survey rounds, food intakes were measured using the 24-h recall method for the four meals consumed (i.e., breakfast, lunch, dinner and snacks). The person primarily responsible for preparing the meals was questioned about the recipes, ingredients and amounts of dishes consumed by household members and guests. The women’s intakes of 40 nutrients at each meal were estimated using the food composition database of Calloway et al. (1994Citation ) for six countries.

For estimating the bioavailable iron, taking into account nutrient interactions at each meal, we focused on the intakes of dietary iron, iron from animal sources, ascorbic acid, phytates and tannins from tea. Because most women did not consume any snacks, the data on snacks were aggregated with nutrient intakes at lunch. Moreover, because tea consumption was negligible in this population, the inhibitory effects of phytates were the prime concern. To calculate the bioavailable iron, algorithms (Monsen et al. 1978Citation , Monsen and Balintfy 1982Citation , Tseng et al. 1997Citation ) were suitably extended. The enhancing effects of MFP and ascorbic acid were programmed to calculate bioavailable iron at each meal under the assumptions that the women’s iron body stores were 0, 250 and 500 mg. In comparison with normal subjects with iron stores of 500 mg, the absorption rates for heme and nonheme iron were 25 and 50% higher for subjects with iron stores of 250 and 0 mg, respectively (Monsen et al. 1978Citation , Table 1Citation ). The mathematical formulas for body stores of 0 and 250 mg have not been used in previous studies and may be more realistic for undernourished populations.


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Table 1. Selected variables in three survey rounds of Bangladeshi women from Saturia, Mymensingh and Jessore sites1

 
Further, the algorithm of Tseng et al. (1997Citation ) for calculating the inhibitory effects of phytate intakes assuming an iron store of 500 mg contained a mathematical error. The correct formulas for the 0-, 250- and 500-mg iron stores in the presence of enhancers and inhibitors of iron absorption in the meal are presented as eqs. 3–5 . A Fortran program for meal-by-meal calculations is available from the first author; the program also sums the bioavailable iron (and other nutrients) at three or more meals to produce figures for the 24-h period. Computer programs for statistical packages, such as those developed by Tseng et al. (1997)Citation for SAS (1996), can be easily modified on the basis of these mathematical formulas.

In the following equations, FeTOT indicates the total iron intake, and FeBIO indicates the bioavailable iron. Heme iron was assumed to constitute 40% of FeMFP (Monsen et al. 1978Citation ). Using the notation of Monsen and Balintfy (1982Citation ), let the enhancing factor (EF) for a meal be given by

(1)

where M, F and P are the edible quantities of MFP (in g), respectively, and AA is the intake of ascorbic acid (in mg). If EF is >75, then EF was assumed to be 75.

To take account of the inhibitory effects of phytates, using the data of Hallberg et al. (1989Citation ), Tseng et al. (1987) calculated the "correction term" (CT) (0 <= CT <= 1) that gives the proportion of FeBIO. However, Tseng et al. (1997Citation ) defined CT incorrectly when phytate intake was <=2.88 mg, because in the data of Hallberg et al. (1989Citation ), phytate intakes were either 0 or >2.88 mg. Let PHY be the total phytate intake (in mg) during the meal. Then, for PHY of <= 2.88 mg, we defined CT as 1 (i.e., we assumed that there were no inhibitory effects of phytate intake for such small values). By contrast, the algorithm of Tseng et al. (1997Citation ) would inadvertently imply that PHY intakes in the interval of 0–2.88 mg increase iron absorption. For other values of PHY, CT was defined by

(2)

where log10 is logarithm to the base 10. Thus, high values of PHY intake reduce FeBIO in a curvilinear fashion (Brune et al. 1992Citation , Tseng et al. 1997Citation ).

Assuming that body iron stores were 0, 250 and 500 mg, the FeBIO can be calculated, respectively, from the following three equations (Monsen et al. 1978Citation ; Table 1Citation ):

(3)


(4)


(5)

where logn is natural logarithm. Note that because the absorption of heme iron was assumed to be not affected by the presence of other nutrients in the meal, the formulas for calculating FeBIO simultaneously take into account the effects of enhancers and inhibitors on nonheme iron absorption (i.e., the order in which the adjustment is made for enhancers and inhibitors is immaterial). Also, the inhibitory effects of phytate intake in eqs. 3–5 assumed body iron stores of 500 mg; this issue is further discussed later.

A model for the proximate determinants of Hb concentration.

The Hb status of a woman is influenced by previous nutritional intakes, sicknesses, pregnancy and lactation status, dietary supplements and genetic factors. The intake of heme iron and interactions between nonheme iron and ascorbic acid, vitamin A, beta-carotene and phytates in the meal affect iron absorption and, ultimately, the Hb level. In developing countries, economic constraints on household food consumption adversely affect the quality of diet, thereby hindering iron absorption. Determination of within-subject variability in 24-h recall data at a given time requires two or three random repetitions within a limited time period. In our study, we obtained useful information on within-subject variability during the entire study by using the women’s dietary intakes in each of the three survey rounds.

Longitudinal studies that measure subjects’ dietary intakes over more extended periods of time would be prohibitively expensive. It is therefore important to introduce anthropometric variables such as the MUAC, height and weight in models that explain Hb status because they reflect the history of nutritional intakes and infections. Moreover, recent sicknesses, especially those involving blood loss, can reduce Hb (Scrimshaw et al. 1959Citation ). By contrast, iron supplements can raise Hb within a short time frame (Viteri 1999Citation ). The model for Hb should account for all of these factors.

The effects of dietary intakes and other factors on Hb status can be analyzed using longitudinal data by estimating autoregressive regression models that include previous measurement on Hb as an explanatory variable. Denoting the ith subject’s Hb in time period t by Hbit (i = 1, 2, ... , n; t = 2, 3), we postulated the autoregressive model for Bangladeshi women:




(6)

where a0, ... , a9 are the regression coefficients, uit is an error term (see eq. 7 ) and Hbit - 1 is the previous measurement of Hb status, with coefficient a9.

There were several attractive features of the model in eq. 6 for Bangladeshi women’s Hb status using three repeated observations in an 8-mo period. First, the short-run, or immediate, impact of a change in a variable such as the FeBIO on Hb was given by a6; the long-run impact was [a6/(1 - a9)]. Generally, one would expect 0 < a9 < 1, so the long-run effect would be greater than the short-run impact. Moreover, for small estimated values of a9, the 8-mo observation period was sufficiently long for much of the long-term effect to materialize.

Second, the error term uit in eq. 6 can be decomposed in a random effects fashion as:

(7)

where {delta}s are women-specific random effects, and v’s are independently distributed random variables. Because Hb is influenced by genetic factors (Garner et al. 2000Citation ) and other unobserved characteristics, one would expect the between-subject variance (of {delta}i) to be an important parameter in the model that explains differences in Hb status.

Third, Hb measurements using capillary blood often exhibit large within-subject variation that can obscure the effects of explanatory variables (Liu et al. 1976Citation , Morris et al. 1999Citation ). In contrast with a single observation on the subjects, however, maximum likelihood estimates computed using repeated observations in a random effects framework can alleviate some of these problems. Fourth, interesting hypotheses can be tested using the model given in eq. 6 . For example, economic factors are likely to affect diet quality of the Bangladeshi women; diet quality in turn would determine the quantity of FeBIO that would be expected to predict Hb status.

Autoregressive models for iron intake from MFP and iron from all animal sources.

To investigate the effects of economic variables on Hb status, we postulated an autoregressive model for the intake of FeMFP; such models are consistent with theories of "habit persistence" in diets that are important for analyzing dietary patterns, especially in traditional societies (Bhargava 1991Citation , Gorman 1967Citation ). The model can be written as:




(8)

Note that household size (and its square) were included in the model in eq. 8 because women in poor households with a large number of children were likely to consume inadequate quantities of FeMFP. The household per capita total expenditure, which changed with the survey rounds, was potentially important for explaining women’s intake of FeMFP. Women’s height and weight were introduced into the model because they reflected the energy requirements (James and Schofield 1990Citation ). In eq. 8 , height and weight were combined as the body mass index (BMI; in kg/m2) due to the results of a statistical test (Bhargava 1994Citation ). In rural populations subsisting in poverty, BMI can be a measure of chronic undernutrition and so associated with a variety of adverse outcomes (James and Ralph 1994Citation ).

Econometric procedure.

Because there were only three time observations available for the women, statistical estimation was based on the assumptions that the number of women was large but the number of survey rounds was fixed. Thus, initial observations on the dependent variables were treated as endogenous variables (correlated with the errors, Bhargava and Sargan 1983Citation ). The errors in eqs. 6 and 8 were assumed independent across women but correlated over time with a positive definite variance-covariance matrix. The random effects decomposition for the u values given in eq. 7 was a special case of this model.

The joint determination of the three observations on Hb (or FeMFP) implied that econometric techniques used for simultaneous equations were likely to be useful in this application. Details of the maximum likelihood estimation method are presented elsewhere (Bhargava and Sargan 1983Citation ). Here, we note that the profile log-likelihood functions of the models in eqs. 6 and 8 were optimized using numerical scheme E04 JBF from the Numerical Algorithm Group (1989Citation ); asymptotic standard errors of the parameters were obtained by approximating second derivatives of the function at the maximum. The maximized values of the logarithm of the likelihood function were used to test hypotheses regarding the coefficients of the variables included in the models for Hb and FeMFP.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Descriptive statistics.

The sample means of selected variables in three survey rounds for 514 Bangladeshi women are given in Table 1Citation . Striking features of the intake data were the low FeMFP intakes and the high phytate intakes. For example, in the first survey round, the average daily FeTOT intake was 6.93 ± 3.00 mg, of which only 0.33 ± 0.47 mg was FeMFP. Further, assuming 0-mg iron body stores and taking into account enhancers of iron absorption, the average daily FeBIO was 0.85 ± 0.54 mg. However, this was reduced to 0.20 ± 0.13 mg when the effect of phytate intake was incorporated; the suitability of the algorithm for incorporating inhibitory effects of phytate intakes in undernourished populations is addressed in Discussion. Similarly, assuming 250-mg iron stores, the average daily FeBIO fell from 0.56 ± 0.33 to 0.14 ± 0.09 mg when phytate intakes were taken into account. These intakes are well below the "safe" level of 2 mg recommended for a woman who weighs 50 kg (FAO/WHO 1988Citation ).

The average daily intake of FeMFP by 514 women at percentiles 1, 5, 10, 15, 25, 50, 75 and 90 was 0.009, 0.030, 0.058, 0.080, 0.111, 0.209, 0.338 and 0.513 mg, respectively. The corresponding values for Hb at these percentiles were 81.4, 97.0, 103.5, 106.1, 111.7, 118.0, 125.0 and 130.3 g/L, respectively. Using 120 g Hb/L as a cutoff point for IDA, >55% of the women would be classified as having IDA. For the 71 women who were pregnant during one or more of the three survey rounds, the respective Hb measurements were 76.7, 88.7, 99.3, 101.9, 104.0, 111.3, 116.0 and 122.8 g/L; hemodilution and iron cost of pregnancy are likely to diminish the Hb status of pregnant women.

Autocorrelations and between- and within-subject variations in Hb concentration.

Table 2Citation presents the results for a simple autoregressive model for the natural logarithm of Hb; the constant term was the only additional explanatory variable in eq. 6 . The point estimate of the coefficient of the lagged dependent variable using the data in three survey rounds was 0.18 (SE = 0.058). This was smaller than the corresponding estimate 0.248 (SE = 0.112) for the 4-d observations; both estimates were statistically significant. The difference in estimates seemed reasonable because nutritional and other factors such as women’s pregnancy status and anthropometric indicators changed over the three survey rounds.


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Table 2. Maximum likelihood estimates of a simple first-order autoregressive model with random effects for the natural logarithm of Bangladeshi women’s hemoglobin concentration measured in three survey rounds and hemoglobin concentration measured for a subset of the women on four consecutive days in the fourth survey round1

 
The ratio of between to within variance was 0.536 (SE = 0.133) for the three survey rounds and 0.417 (0.207) for 4 consecutive d observations. The between-subject variations in Hb were relatively large; individual characteristics such as the subjects’ height, MUAC and weight may account for some these differences. Underlying genetic factors (Garner et al. 2000Citation ) may also have contributed to the between-women differences. Last, the within-subject variance was large, especially in comparison with studies in which simple random effects models were estimated for venous blood samples (Morris et al. 1999Citation ). However, the autocorrelations were not estimated in previous studies.

Results from the autoregressive model explaining Bangladeshi women’s Hb concentration by demographic and nutritional variables.

The results from estimation of the autoregressive model given in eq. 6 for women’s Hb status are presented in Table 3Citation , where body iron stores were assumed to be 0 mg (similar results were obtained when iron stores were assumed to be 250 and 500 mg and hence are not reported). Table 3Citation presents results for the cases where, first, only the enhancers of iron absorption were taken into account and, second, the inhibitory effects of phytates in the meal were also incorporated in calculating FeBIO. The subjects’ age, height, MUAC, weight, FeBIO and the previous measurement of Hb were transformed into natural logarithms. The logarithmic transformation reduced internal variation in the data (Nelson et al. 1989Citation ). The estimated coefficients of the variables in logarithms were short-run "elasticities" (percentage change in the dependent variable resulting from a 1% change in an independent variable). The long-run elasticity with respect to an explanatory variable can be obtained by dividing the short-run elasticity by (1 - a9), where a9 was the coefficient of Hb in the previous time period.


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Table 3. Maximum likelihood estimates of a first order autoregressive model with random effects for Bangladeshi women’s hemoglobin concentration in 3 survey rounds explained by anthropometric and morbidity variables and by the intake of bioavailable Fe assuming 0 mg body Fe stores1

 
There was a significant decline in Hb with age in the model where only the enhancers of iron absorption were taken into account in calculating FeBIO; the coefficient was not statistically significant when the inhibitory effects of phytates were incorporated. Hb of pregnant women was significantly lower (P < 0.05). An additional indicator (0–1) variable was included for women who were lactating during the survey rounds. However, it was not statistically significant.

The women’s height and MUAC were positively associated with Hb status; these coefficients were statistically significant. Height is a good indicator of early nutrition, whereas MUAC can approximate lean body mass. It was not surprising that these two variables were positively associated with Hb. By contrast, weight was negatively associated, which may have been due to the presence of pregnant women in the sample; the indicator variable did not account for pregnancy trimesters.

In the first column, where only the enhancers of iron absorption were used for calculating the FeBIO, the coefficient of FeBIO was positive and significant at the 5% level. Moreover, this coefficient showed a 20% increase in the second column where the inhibitory effects of phytate intakes were also taken into account. The maximized value of the logarithm of the likelihood function was higher when the inhibitory effects of phytate intake were incorporated.

The indicator variable for woman with bloody diarrhea was negative but not significantly associated with Hb status; parity and the average birth interval were also insignificant. However, the indicator variable for women taking iron tablets during the survey round was positive and significant. In Bangladesh, iron tablets were often sold together with birth control pills. The results reported in Table 3Citation set the indicator variable for iron tablets to 1 only when the women answered the specific question regarding iron tablets intake. Last, maximized values of the logarithms of the likelihood functions were slightly higher when it was assumed that the women had 0-mg body iron stores than in the cases where the iron stores were assumed to be 250 or 500 mg. Although this was not direct evidence for the actual iron stores, the results suggested that the average woman probably had iron stores lower than 250 mg.

Results from autoregressive models explaining Bangladeshi women’s iron intake from MFP and from all animal sources by economic, demographic and nutritional variables.

The results from estimation of the model in eq. 8 for intake of FeMFP and iron from all animal sources are given in Table 4Citation . Because some women did not consume any MFP in one or more survey rounds but consumed some milk and animal products, the two sets of results give a better description of the food consumption patterns. The zero intakes of iron by some women were set to 0.01 mg before the logarithmic transformation; a sensitivity analysis was performed to investigate whether this assumption affected the results, but it did not. The interesting aspects of the results were that 1) age had a large negative coefficient that was statistically significant in both models; older women consumed lower quantities of animal products. This finding was also consistent with the slight decline in Hb with age in Table 3Citation . 2) There was a nonlinear effect of household size on intake of FeMFP and iron intake from all animal sources. This was an expected finding because larger households typically consist of a greater number of children growing up in poverty; the diet quality in such households is generally poor. 3) The coefficients of monthly average per capita expenditure were large and significant; a 1% increase in households’ monthly expenditure was associated with 0.65 and 0.71% increases in FeMFP intake and iron intake from all animal sources, respectively. The corresponding long-run income elasticities were 0.70 and 0.87. These results suggested that women’s iron intakes improved significantly with increases in household incomes.


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Table 4. Maximum likelihood estimates of a first order autoregressive model with random effects for Bangladeshi women’s iron intake from meat, fish and poultry (MFP) and iron intake from animal source in 3 survey rounds explained by anthropometric, demographic and economic variables1

 
4) The subjects’ BMI was a significant predictor of FeMFP and from all animal sources. In a long time frame, however, systematically higher intakes of FeBIO may contribute to a gain in lean body mass, thereby increasing the BMI. At the given data points, the possible reverse causality from higher intake of FeMFP to BMI was investigated by testing the null hypothesis that the correlation between the random effects ({delta}i) in eq. 8 and BMI was 0; the hypothesis was accepted for FeMFP (likelihood ratio statistic, 0.30, df, 3; P = 0.999). Similar results were obtained for iron intake from all animal sources.

5) The coefficients of lagged dependent variables were 0.077 and 0.130, respectively, in the models for intake of FeMFP and iron intake from all animal sources; both coefficients were statistically significant. The ratios of between to within variance were not statistically significant in either model. This was in part due to the large within-subject variation in iron intake from animal sources.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
IDA is widely prevalent in low and middle-income countries (UNICEF/WHO 1999Citation ). Using the recent longitudinal survey from Bangladesh, the intake of FeBIO were calculated under alternative assumptions of women’s iron stores. For example, the mean intake of FeBIO in survey round 2 was 0.20 mg/d, taking into account the meal-by-meal nutrient interactions and assuming negligible body iron stores; mean intakes of FeBIO were 0.14 and 0.10 mg/d, respectively, when the body stores were assumed to be 250 and 500 mg. Furthermore, high phytate content of the meals reduced FeBIO intake from 0.85 to 0.20 mg/d with the assumption of zero iron stores.

The inhibitory effects of phytates were calculated using algorithms based on data on healthy populations with iron stores of ~500 mg (Hallberg et al. 1989Citation , Tseng et al. 1997Citation ). It is plausible that inhibitory effects of phytates and tannins differ in populations with lower iron stores. For example, Murphy et al. (1992Citation ) adjusted nonheme iron intakes of toddlers in Egypt, Kenya and Mexico for the presence of tannins in the meal, although the data were not available by meals. The authors estimated that average FeMFP intakes of toddlers in Egypt, Kenya and Mexico were 0.64, 0.05 and 0.37 mg/d, respectively (Murphy et al. 1992Citation , Table 4Citation ). However, the corresponding FeBIO intakes incorporating the effects of tannins in the three populations were 0.49, 0.61 and 0.37 (mg/d), respectively. It is perhaps surprising that despite the lowest average intake (0.05 mg/d) of FeMFP in Kenya, these toddlers had the highest intake (0.61 mg/d) of FeBIO. It would seem critical to conduct studies in undernourished populations to derive suitable algorithms for iron absorption from mixed diets.

The second objective of the study was to develop comprehensive longitudinal models for the Hb status of Bangladeshi women and to model the socioeconomic determinants of the intake of FeMFP. From the results in Table 3Citation for Hb status, the short- and long-run elasticities of Hb with regard to FeBIO were 0.015 and 0.018, respectively. Using the sample means in round 2 in Table 1Citation , a doubling of FeBIO to 0.40 mg/d would result in a long-run increase of 3.6% in Hb. Because the sample mean of Hb was 117.3 ± 11.6 g/L, the average woman would then not be classified as having IDA. Moreover, a 10-fold increase of FeBIO from 0.20 mg to the "safe" level of 2.0 mg (FAO/WHO 1988Citation ) would be associated with a 18% increase in Hb, which would greatly reduce the prevalence of IDA. The magnitude of such increases is likely to be underestimated because within-subject variation in iron intakes results in measurement errors that bias the estimated coefficients downward (Liu et al. 1976Citation ). At any rate, there is evidence that even minor improvements in Hb have beneficial effects on child-bearing, time allocation, morbidity from infections, work productivity and cognition (UNICEF/UNU/WHO/MI 1999Citation ).

IDA among the poor in part results from high prices of animal products, which reduces the intake of heme iron. Also, prices of fresh vegetables and fruits show large seasonal fluctuations, making them less affordable outside the harvest season. Thus, the enhancing effects of vitamin C for iron absorption may be applicable primarily to the well-off groups and not to those most likely to have IDA. Cereal staples, such as rice, in Bangladesh have low iron and a high phytate content. Taken together, these factors suggest that to reduce IDA, one would need to evaluate the cost-effectiveness of instruments such as iron fortification of rice, increased consumption of MFP and easier access to iron tablets. Because women in our sample who took iron tablets had ~2.5% higher Hb levels and the costs of daily iron supplementation were ~$0.25 per woman per month (Levin et al. 1993Citation ), women, especially those of child-bearing age, would be good candidates for daily or weekly iron supplementation (Allen 2000Citation , Beard 1998Citation ).


    ACKNOWLEDGMENTS
 
The authors would like to thank the participants in the surveys and the staff of Data Analysis and Technical Assistance in Dhaka, Bangladesh, for making this study possible. We also thank K. Hallman, N. Hassan, N. Islam, E. Payongayong and A. Quisumbing for their help and P. Reeds for valuable suggestions.


    FOOTNOTES
 
1 Supported by grants from the Danish International Development Assistance and the U.S. Agency for International Development, Office of Women in Development, to the International Food Policy Research Institute. Back

3 Abbreviations used: FeBIO, bioavailable iron; FeMFP, iron from meat, fish and poultry; FeTOT, total iron; Hb, hemoglobin; IDA, iron deficiency anemia; MFP, meat, fish and poultry; MUAC, mid upper arm circumference. Back

Manuscript received February 28, 2000. Initial review completed May 12, 2000. Revision accepted November 28, 2000.


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