Abstract
Objective
To assess Fe intake, calculate the prevalence of inadequate Fe intake and identify food contributors to Fe intake during 2003 and 2008 in a population-based study, reflecting before and after the mandatory fortification of flour with Fe.
Design
Two cross-sectional population-based studies conducted in 2003 and 2008. Dietary intake was evaluated by 24 h recall and the Software for Intake Distribution Estimation (PC-SIDE) was used to estimate within-person variance and prevalence of inadequate Fe intake. The statistical analysis was conducted considering the complex survey design.
Setting
São Paulo, Brazil.
Subjects
Adolescents, adults and elderly adults of both sexes, interviewed in 2003 (n 2386) and 2008 (n 1661).
Results
The Fe intake mean increased in all populations in the post-fortification period. A reduction of over 90 % was observed in the prevalence of inadequate Fe intake among men for all age groups analysed. When evaluating women, despite the substantial reduction (over 63 %), prevalence of inadequate Fe intake remained high (34 %) in those aged 19–50 years. Major food contributors to Fe intake before fortification were beans, beef, vegetables and dairy. There was an alteration in the contributors in the post-fortification period, with bread, beef, beans and biscuits as main contributors.
Conclusions
The mandatory fortification with Fe significantly furthered the reduction in the prevalence of inadequacy, except among women of reproductive age, and changed the main contributors to this nutrient in the studied population. Therefore, monitoring of Fe addition in flour is essential to assess compliance to the fortified flour policy and to guarantee a safe Fe intake for all the population.
Keywords: Fortification, Programme assessment, Iron, Dietary intake, Prevalence of inadequacy
Worldwide, Fe deficiency is the most common and widespread micronutrient malnutrition, and is a public health problem in both industrialized and non-industrialized countries that affects over 24 % of the world’s population, but even more so in developing regions. Fe deficiency can reach all age groups, although young children and women tend to be among those most at risk of developing micronutrient deficiencies( 1 ).
Several studies have shown that the population of countries such as Denmark, Germany, Spain, the Netherlands, the UK, Poland, France, Ireland and Italy has an inadequate intake of Fe, especially among women of reproductive age( 2 , 3 ). Although micronutrient deficiency is highly prevalent in many regions of the world and has a high social impact( 4 ), there are low-cost and highly effective approaches to prevention. Such programmes comprise food diversification to promote the consumption of food sources of Fe, the distribution of supplements and food fortification( 5 ). Food fortification is a safe and cost-effective strategy used in several countries to reduce micronutrient deficiencies( 6 , 7 ). Although many countries combat Fe deficiency with a flour fortification strategy, it seems that only nine of the seventy-eight national fortification programmes can have the desired nutritional impact due to the use of Fe with low bioavailability( 8 ).
In Brazil, there are no past or current figures for Fe deficiency. Since 1999, with the intent being to increase the intake amount of this micronutrient to prevent low stores and Fe-deficiency anemia, the Brazilian Ministry of Health has undertaken some strategies that include the promotion of a healthy diet, the use of supplements in target groups and the fortification of foods. The mandatory fortification of foods with Fe was initiated in 2004; wheat and maize flour was selected as the major vehicle with 4·2 mg of Fe per 100 g of flour( 9 ).
The main objectives of the present study were to assess the Fe intake, calculate the prevalence of inadequate Fe intake and identify the food contributors to Fe intake during 2003 and 2008 in a population-based study, reflecting before and after the mandatory fortification of flour with Fe.
Methods
Study population
For the present analysis, we compared data from two population-based studies: Health Survey–São Paulo (ISA-Capital 2003 and ISA-Capital 2008). The Healthy Survey–São Paulo is a cross-sectional study of health and living conditions among a representative sample of individuals living in São Paulo city, south-eastern Brazil. The ISA-Capital 2003 was conducted during 2003, reflecting the time prior to Fe fortification, and ISA-Capital 2008 was conducted during 2008, reflecting the time after fortification.
The sampling process for ISA-Capital 2003 was carried out in two stages: census tracts and households. For the draw, sectors were gathered into three strata based on the percentage of family heads with university-level education: <5 %, 5–24·9 % and ≥25 %. In total 2386 individuals were interviewed, 183 adolescents (12–13 years), 523 adolescents (14–18 years), 747 adults (19–50 years) and 933 adults (≥51 years), of both sexes.
The sample at ISA-Capital 2008 was defined in eight age domains: <1 year old, 1–11 years old and three more age groups for each sex, namely 12–19 years (adolescents), 20–59 years (adults) and ≥60 years (elderly adults). Two-stage cluster sampling of census tracts and households was performed. In the first stage, by using probability proportional to size, ten census tracts were drawn from each of the strata, making a total of thirty census tracts for each region. In the second stage, households were drawn from each sector. A total of 3271 individuals (197 aged <1 year, 383 aged 1–11 years and 2691 aged ≥12 years) participated in ISA-Capital 2008. For the present study, we invited all individuals older than 12 years from the ISA-Capital 2008 sample to answer one 24 h recall (24HR). Of these, 1662 individuals completed the dietary measurement. One person was excluded owing to supplement use, leaving 1661 individuals: 151 adolescents (12–13 years), 357 adolescents (14–18 years), 529 adults (19–50 years) and 624 adults (≥51 years), of both sexes.
Data collection and processing
In both surveys (ISA-Capital 2003 and ISA-Capital 2008), information on food intake, demographics and socio-economic variables was obtained using structured questionnaires through household interviews. The 24HR was administered in the household by trained interviewers using the multiple-pass method. In this process the respondent is guided through five steps (quick listing, quick listing review, naming meals, detail cycle and general review) using a standardized process that keeps individuals interested and engaged in the interview, which helps them remember all items consumed( 10 ). The sampling days for participants covered all the days of the week.
Foods reported in each 24HR were critically reviewed to identify any failures in reporting related to the descriptions of the foods consumed or food preparation techniques, including their apportioning and quantification. Fe intake was analysed using the Nutrition Data System for Research software program version 2007 (Nutrition Coordinating Center, University of Minnesota, Minneapolis, MN, USA), which is based on data from tables published by the US Department of Agriculture. The amount of Fe added to fortified products was corrected to account for the quantity of fortification in maize and wheat flour that has been mandatory in Brazil since 2004. There is a difference between the quantities of Fe added to fortified foods in Brazil and the USA. In addition, the Brazilian food composition table was used to verify the adequacy of nutritional values of Fe from food.
Estimating usual iron intake in the pre- and post-fortification periods
Due to day-to-day variation (within-person random error), nutrient intake distributions based on one or a few collection-days of 24HR provide biased estimations of percentiles of intake and consequently biased estimations of the prevalence of inadequacy( 11 ). The use of methods to remove within-person variance and estimate usual nutrient intake is widely recommended and has been implemented in several studies worldwide. To do so, at least one replication of the 24HR is needed in a sub-sample of the study population( 12 ). In the post-fortification period we administered two non-consecutive 24HR, the first was in person and the second a telephone-based interview (in a sample of 50·06 %). Mean time interval between the first and second measurement was about 6 months. Nevertheless, in the pre-fortification period, there was only a single measurement for each participant. According to previous studies( 13 , 14 ), in cases of absence of the repetition of the 24HR, it is advised that the within-person variance component from a study with a similar population should be applied in order to correctly estimate the distribution of usual nutrient intake. Therefore, to correct the distribution of Fe intake in the pre-fortification period, we applied the variance components derived from the post-fortification period. To estimate within-person variance components by each age and sex group and the prevalence of inadequate Fe intake we used the Software for Intake Distribution Estimation (PC-SIDE) that implements the method proposed by Nusser et al. ( 12 ).
Prevalence of inadequacy
The US Institute of Medicine’s set of intake recommendations for Fe was used as the reference for intake adequacy, specifically the Estimated Average Requirement( 15 ). The prevalence of inadequate Fe intake was calculated as the proportion of individuals whose usual intake fell below the Estimated Average Requirement for a specific age and sex group. To provide valid estimates of prevalence of inadequate intake, the distribution of the intake requirement must be symmetric, which is not the case for women of reproductive age due to Fe loss in the menstrual cycle. In this case, a suitable method to estimate usual intake that accounts for menstrual losses was applied( 16 ). Confidence intervals for the prevalence of inadequate intake were derived from standard errors based on a jackknife replication technique considering the complex sample design. Specifically, for women of reproductive age (14–18 years and 19–50 years) it was not possible to estimate standard errors due to statistical constraints.
The contribution of foods to Fe intake was calculated by the methodology described in Block et al. ( 17 ), considering the study sampling design. This method estimates the major contributors to total Fe intake through a ratio of the daily total Fe provided by the specific food or food group to the daily total intake of Fe from all foods. Subsequently the foods were arranged in decreasing order according to the amount of Fe per food portion, calculated from the median food consumption in grams in the study population.
All analyses were conducted using the appropriate sample weights to account for the complex survey design. For all analyses, the Stata® statistical software package version 12 was used and P<0·05 was considered statistically significant.
Results
Mean Fe intake and the prevalence of inadequate Fe intake in the pre- and post-fortification periods are shown in Table 1. The Fe intake mean increased in all age and sex groups, ranging from 3·91–6·99 mg/d in the pre-fortification period to 7·81–15·20 mg/d in the post-fortification period. There was no identified risk of excessive Fe intake in this population.
Table 1.
Prevalence of inadequate intake of iron in the pre- and post-fortification periods according to life stage. São Paulo, Brazil, 2008
| EAR | Fe intake (mg/d) | Prevalence of inadequacy | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Sex/age | (mg/d) | Mean | 95 % CI | P5 | P10 | P25 | P50 | P75 | P90 | P95 | % | 95 % CI |
| Pre-fortification | ||||||||||||
| Males | ||||||||||||
| 12–13 years | 5·9 | 5·72 | 4·88, 6·56 | 3·10 | 3·60 | 4·50 | 5·60 | 6·80 | 8·00 | 8·80 | 57·00 | 37·40, 76·60 |
| 14–18 years | 7·7 | 6·68 | 6·21, 7·15 | 3·50 | 4·10 | 5·20 | 6·50 | 8·00 | 9·00 | 10·50 | 70·00 | 60·20, 79·80 |
| 19–50 years | 6·0 | 6·99 | 6·60, 7·38 | 3·90 | 4·50 | 5·40 | 6·80 | 8·20 | 9·80 | 10·80 | 34·00 | 28·12, 39·88 |
| ≥51 years | 6·0 | 5·69 | 5·12, 6·26 | 3·10 | 3·60 | 4·40 | 5·60 | 7·10 | 8·80 | 10·10 | 58·00 | 48·20, 67·80 |
| Females | ||||||||||||
| 12–13 years | 5·7 | 5·75 | 4·65, 6·85 | 3·20 | 3·50 | 4·30 | 5·40 | 6·80 | 8·40 | 9·60 | 56·00 | 36·40, 75·60 |
| 14–18 years | 7·9 | 5·78 | 5·21, 6·35 | 3·60 | 3·90 | 4·60 | 5·60 | 6·70 | 7·90 | 8·70 | 86·00 | – |
| 19–50 years | 8·1 | 4·83 | 4·48, 5·18 | 3·48 | 3·74 | 4·20 | 4·70 | 5·40 | 6·00 | 6·40 | 92·00 | – |
| ≥51 years | 5·0 | 3·91 | 3·64, 4·18 | 2·21 | 2·51 | 3·07 | 3·78 | 4·62 | 5·49 | 6·06 | 82·00 | 78·08, 85·92 |
| Post-fortification | ||||||||||||
| Males | ||||||||||||
| 12–13 years | 5·9 | 13·16 | 11·79, 14·53 | 8·30 | 9·30 | 10·90 | 12·90 | 15·20 | 17·40 | 18·70 | 0·00 | 0·00, 2·06 |
| 14–18 years | 7·7 | 15·20 | 14·00, 16·40 | 9·00 | 10·20 | 12·20 | 14·90 | 17·70 | 20·90 | 23·00 | 1·00 | 0·00, 2·96 |
| 19–50 years | 6·0 | 12·30 | 11·42, 13·18 | 7·20 | 8·10 | 9·80 | 12·00 | 14·50 | 17·10 | 18·80 | 1·00 | 0·00, 2·96 |
| ≥51 years | 6·0 | 9·87 | 9·05, 10·69 | 6·00 | 6·70 | 8·00 | 9·60 | 11·50 | 13·30 | 14·50 | 5·00 | 0·00, 10·88 |
| Females | ||||||||||||
| 12–13 years | 5·7 | 12·70 | 10·58, 14·82 | 7·60 | 8·50 | 10·20 | 12·40 | 14·90 | 17·40 | 19·10 | 1·00 | 0·00, 2·56 |
| 14–18 years | 7·9 | 11·27 | 10·29, 12·25 | 7·30 | 8·10 | 9·40 | 11·10 | 12·90 | 14·70 | 15·80 | 18·00 | – |
| 19–50 years | 8·1 | 9·27 | 8·64, 9·90 | 7·16 | 7·57 | 8·30 | 9·20 | 10·15 | 11·10 | 11·60 | 34·00 | – |
| ≥51 years | 5·0 | 7·81 | 7·32, 8·30 | 5·20 | 5·70 | 6·60 | 7·70 | 8·90 | 10·10 | 11·00 | 3·00 | 0·00, 8·88 |
EAR, Estimated Average Requirement; P, percentile.
There was a reduction of over 90 % in the prevalence of inadequacy among men in all age groups analysed. When evaluating women, it was noted that despite the substantial reduction (over 63 %), the prevalence of inadequate Fe intake remained high (34 %) in those aged 19–50 years.
The food groups that contributed most to the intake of Fe before fortification were beans, beef, vegetables and dairy, accounting for more than 58 % of the Fe intake in all age and sex groups studied (Table 2). In the post-fortification period, there was a change in the pattern of contributors: bread, beef, beans and biscuits were main contributors (Table 3).
Table 2.
Food contributors to total intake of iron in the pre-fortification period according to life stage. São Paulo, Brazil, 2003
| 9–13 years | 14–18 years | 19–50 years | ≥51 years | ||||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Median | Percentage (%) | Median | Percentage (%) | Median | Percentage (%) | Median | Percentage (%) | ||||||||||||
| Rank | Food | (g) | Relative | Cumulative | Rank | Food | (g) | Relative | Cumulative | Rank | Food | (g) | Relative | Cumulative | Rank | Food | (g) | Relative | Cumulative |
| Pre-fortification | |||||||||||||||||||
| 1 | Beans | 86·0 | 22·3 | 22·3 | 1 | Beef | 99·2 | 26·6 | 26·6 | 1 | Beef | 100·0 | 29·7 | 29·7 | 1 | Beef | 80·0 | 27·0 | 27·0 |
| 2 | Beef | 70·0 | 21·1 | 43·4 | 2 | Beans | 86·0 | 26·2 | 52·8 | 2 | Beans | 86·0 | 22·8 | 52·5 | 2 | Beans | 86·0 | 24·1 | 51·1 |
| 3 | Dairy | 25·0 | 9·7 | 53·1 | 3 | Vegetables | 18·0 | 6·2 | 59·0 | 3 | Vegetables | 20·0 | 7·8 | 60·3 | 3 | Vegetables | 20·0 | 10·6 | 61·7 |
| 4 | Vegetables | 10·0 | 5·3 | 58·4 | 4 | Dairy | 25·0 | 5·7 | 64·7 | 4 | Processed meat and sausages | 45·0 | 4·6 | 64·9 | 4 | Fruits and juices | 101·0 | 5·3 | 67·0 |
| 5 | Cereals | 1·8 | 4·8 | 63·3 | 5 | Processed meat and sausages | 39·1 | 3·8 | 68·5 | 5 | Fruits and juices | 91·3 | 3·6 | 68·5 | 5 | Poultry | 60·0 | 4·1 | 71·1 |
| 6 | Processed meat and sausages | 30·0 | 4·4 | 67·7 | 6 | Poultry | 51·0 | 3·7 | 72·1 | 6 | Poultry | 60·0 | 3·5 | 72·1 | 6 | Processed meat and sausages | 40·0 | 3·6 | 74·6 |
| 7 | Candies | 11·3 | 4·0 | 71·7 | 7 | Fruits and juices | 99·4 | 3·5 | 75·7 | 7 | Rice | 150·0 | 3·2 | 75·3 | 7 | Rice | 116·3 | 3·6 | 78·2 |
| 8 | Poultry | 44·3 | 3·8 | 75·5 | 8 | Rice | 150·0 | 3·3 | 79·0 | 8 | Dairy | 25·0 | 2·9 | 78·2 | 8 | Tubers | 62·2 | 2·6 | 80·8 |
| 9 | Sauces | 20·0 | 3·2 | 78·7 | 9 | Candies | 15·7 | 2·9 | 81·8 | 9 | Tubers | 77·3 | 2·6 | 80·8 | 9 | Legumes | 6·2 | 2·6 | 83·3 |
| 10 | Fruits and juices | 86·0 | 3·1 | 81·8 | 10 | Tubers | 78·1 | 2·6 | 84·4 | 10 | Candies | 16·8 | 2·2 | 83·0 | 10 | Cereals | 3·0 | 1·9 | 85·3 |
| 11 | Rice | 125·0 | 2·8 | 84·5 | 11 | Sauces | 15·0 | 2·3 | 86·7 | 11 | Sauces | 15·0 | 2·1 | 85·1 | 11 | Milk | 123·8 | 1·9 | 87·1 |
| 12 | Tubers | 78·1 | 2·7 | 87·3 | 12 | Cereals | 1·8 | 1·7 | 88·5 | 12 | Flavoured drink | 10·8 | 1·9 | 87·0 | 12 | Candies | 15·0 | 1·6 | 88·7 |
| 13 | Cheese | 22·1 | 1·6 | 88·9 | 13 | Cheese | 22·0 | 1·3 | 89·8 | 13 | Cheese | 30·0 | 1·8 | 88·8 | 13 | Sauces | 13·6 | 1·5 | 90·3 |
| 14 | Other flour | 8·0 | 1·6 | 90·4 | 14 | Snacks | 38·0 | 1·1 | 90·9 | 14 | Fish and seafood | 50·0 | 1·2 | 90·1 | 14 | Cheese | 30·0 | 1·4 | 91·6 |
| 15 | Flavoured drink | 10·8 | 1·3 | 91·7 | 15 | Flavoured drink | 10·8 | 1·1 | 92·0 | 15 | Cereals | 1·7 | 1·0 | 91·1 | 15 | Fish and seafood | 63·6 | 1·21 | 92·9 |
Table 3.
Food contributors to total intake of iron in the post-fortification period according to life stage. São Paulo, Brazil, 2008
| 9–13 years | 14–18 years | 19–50 years | ≥51 years | ||||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Median | Percentage (%) | Median | Percentage (%) | Median | Percentage (%) | Median | Percentage (%) | ||||||||||||
| Rank | Food | (g) | Relative | Cumulative | Rank | Food | (g) | Relative | Cumulative | Rank | Food | (g) | Relative | Cumulative | Rank | Food | (g) | Relative | Cumulative |
| Post-fortification | |||||||||||||||||||
| 1 | Bread | 50·0 | 26·6 | 26·6 | 1 | Bread | 50·0 | 24·9 | 24·9 | 1 | Bread | 50·0 | 27·0 | 27·0 | 1 | Bread | 50·0 | 26·4 | 26·4 |
| 2 | Biscuits | 40·0 | 13·4 | 40·0 | 2 | Beef | 80·0 | 16·2 | 41·1 | 2 | Beef | 82·5 | 15·6 | 42·5 | 2 | Beef | 75·0 | 15·5 | 41·9 |
| 3 | Beef | 99·2 | 13·1 | 53·0 | 3 | Beans | 107·6 | 11·4 | 52·5 | 3 | Beans | 86·0 | 12·9 | 55·4 | 3 | Beans | 86·0 | 14·5 | 56·3 |
| 4 | Beans | 86·0 | 11·3 | 64·3 | 4 | Biscuits | 63·0 | 8·6 | 61·0 | 4 | Wheat and maize flour | 17·5 | 6·0 | 61·4 | 4 | Vegetables | 20·0 | 5·7 | 62·1 |
| 5 | Wheat and maize flour | 18·8 | 5·8 | 70·1 | 5 | Wheat and maize flour | 19·7 | 6·8 | 67·8 | 5 | Biscuits | 30·0 | 5·0 | 66·4 | 5 | Wheat and maize flour | 14·5 | 5·2 | 67·3 |
| 6 | Pastas | 150·5 | 4·0 | 74·1 | 6 | Dairy | 32·0 | 4·0 | 71·9 | 6 | Vegetables | 20·0 | 4·8 | 71·3 | 6 | Fruits and juices | 86·0 | 3·7 | 71·0 |
| 7 | Dairy | 32·0 | 3·9 | 78·0 | 7 | Pastas | 100·4 | 3·9 | 75·8 | 7 | Pastas | 96·7 | 4·4 | 75·7 | 7 | Pastas | 81·0 | 3·5 | 74·4 |
| 8 | Vegetables | 14·4 | 2·9 | 80·9 | 8 | Vegetables | 16·7 | 3·1 | 78·9 | 8 | Poultry | 70·0 | 2·8 | 78·5 | 8 | Biscuits | 24·0 | 3·3 | 77·8 |
| 9 | Processed meat and sausages | 38·6 | 2·5 | 83·5 | 9 | Processed meat and sausages | 38·6 | 2·8 | 81·7 | 9 | Processed meat and sausages | 34·0 | 2·8 | 81·3 | 9 | Poultry | 65·0 | 2·6 | 80·3 |
| 10 | Candies | 20·0 | 2·0 | 85·4 | 10 | Candies | 15·0 | 2·0 | 83·6 | 10 | Dairy | 32·0 | 2·2 | 83·4 | 10 | Processed meat and sausages | 31·0 | 2·1 | 82·4 |
| 11 | Pork | 37·9 | 1·6 | 87·0 | 11 | Poultry | 75·0 | 1·9 | 85·5 | 11 | Fruits and juices | 80·4 | 2·1 | 85·5 | 11 | Rice | 119·3 | 1·9 | 84·4 |
| 12 | Fruits and juices | 54·0 | 1·5 | 88·6 | 12 | Fruits and juices | 55·8 | 1·6 | 87·1 | 12 | Rice | 124·0 | 1·7 | 87·2 | 12 | Tuber | 60·0 | 1·2 | 85·5 |
| 13 | Poultry | 55·0 | 1·4 | 90·0 | 13 | Rice | 150·0 | 1·3 | 88·4 | 13 | Candies | 14·7 | 1·4 | 88·6 | 13 | Pork | 32·0 | 1·6 | 87·1 |
| 14 | Rice | 125·0 | 1·4 | 91·4 | 14 | Tubers | 85·6 | 1·3 | 89·6 | 14 | Sauces | 11·9 | 1·4 | 90·0 | 14 | Candies | 14·7 | 1·3 | 88·4 |
| 15 | Other flour | 12·2 | 1·3 | 92·7 | 15 | Cereals | 2·0 | 1·2 | 90·8 | 15 | Tubers | 81·9 | 1·4 | 91·4 | 15 | Cereals | 3·8 | 1·2 | 89·6 |
Discussion
Our results show that fortified foods had an impact in reducing the prevalence of inadequate Fe intake and increasing the mean Fe intake in all life stages, regardless of sex.
The mean Fe intake in the post-fortification period in all age and sex groups was similar to that found by Santos et al. ( 18 ) in their evaluation of the flour fortification programme in a representative sample of Brazilians. Berner et al. ( 19 ) found that food fortification with Fe contributed to reducing the prevalence of inadequacy of this nutrient in adolescents, similar to the results of the present study. Martorell et al. ( 20 ) showed that the Fe fortification policy in Costa Rica reduced the prevalence of anaemia from 18·4 to 10·2 % in adult women. In South Africa, the fortification policy implemented in 2003 also led to an increase in Fe intake( 21 ). The average Fe intake in men and adult women was higher than that evidenced in the present study. Fulgoni et al. ( 22 ) assessed the contributions to various micronutrients from the usual diet according to different sources (natural, fortified or enriched and dietary supplement) among individuals over two years according to National Health and Nutrition Examination Survey 2003–2006 data, and found that the percentage of the population with usual intakes below the Estimated Average Requirement decreased from 21·8 to 6·5 %.
The prevalence of inadequate Fe intake in women of reproductive age was over 20 % in the present study, even after the mandatory fortification. This high prevalence in this age group suggests that the policy has limited effectiveness and it is necessary to consume a greater amount of fortified flour( 6 ). However, the incentive to increase consumption of flour should not stimulate the growing prevalence of weight excess( 23 ). Thus, other approaches to increase Fe intake (e.g. supplementation) should be considered in this population group in a region where anaemia is highly prevalent( 24 ).
Bioavailability is the other relevant issue regarding Fe fortification. In Brazil, reduced Fe is the main source used by the industry in the fortification policy( 25 ). However, this type of Fe provides a low bioavailability compared with ferrous sulfate and ferrous fumarate( 26 ). The extent of its use is due to the low cost and stability when added in flour. The low bioavailability of this source may explain the findings of Assunção and colleagues( 27 ) who showed that Fe fortification in Brazil had no impact on anaemia in children under 6 years old living in the urban area of the city of Pelotas, southern Brazil. Hurrell et al.( 8 ) reviewed the efficacy and effectiveness studies with various Fe-fortified foods and found strong evidence that reduced Fe and other forms of Fe with low bioavailability cannot be efficacious to a have satisfactory impact on Fe status. Thus, it is necessary that the government review the fortification policy in order to increase the effectiveness of the programme by use of an Fe form with better bioavailability.
Despite a significant increase in Fe intake after fortification, the population in the present study showed no intakes near the tolerable upper intake level of this micronutrient. The 95th percentile of intake (11–19 mg Fe/d) in the post-fortification period is lower than that observed in the adult female population of Europe, whose 95th percentile of Fe intake ranged from 13 mg/d (Ireland) to 20 mg/d (Germany). However, the 95th percentile of Fe intake observed in adult men in the current study population is similar to levels found in Denmark, the Netherlands and Spain( 3 ).
Although there is no evidence of risk of adverse effects related to higher intake of Fe from the fortification( 3 , 28 ), studies are needed to assess the impact of fortification in individuals with low nutritional risk. Abtahi and colleagues( 29 ) evaluated the effects of Fe-fortified bread consumption on oxidative stress in healthy individuals in Iran. They showed that there was an increase in the level of superoxide dismutase and a reduction in the value of the total antioxidant capacity in men. These results suggest that consumption of flour fortified with Fe in non-anaemic adults in the long term cannot be without adverse effects. Furthermore, monitoring of Fe addition to flour is essential to assess compliance to the fortified flour policy and to guarantee a safe Fe intake.
The panorama of foods that contributed to the Fe intake also changed after fortification. In 2003, the main contributors were food groups that were natural sources of this nutrient, such as beef and beans. However, there was an important change after fortification, in which bread, biscuits, wheat and maize flour were among the top five contributors. Therefore, flour was a good vehicle for Fe fortification, corroborating results observed in previous studies, in which higher intakes of Fe were associated with high consumption of fortified foods( 3 , 19 , 30 ).
Food fortification is a safe and cost-effective strategy used in several countries to reduce micronutrient deficiencies( 6 , 7 ). Baltussen and co-workers( 31 ) estimated the cost-effectiveness of Fe supplementation and Fe fortification programmes, at different coverage levels, in four subregions of the world. The cost-effectiveness of fortification was always lower than the cost-effectiveness of supplementation, regardless of the coverage level. Fiedler and Macdonald( 32 ) estimated that in Brazil the fortification of wheat and maize flour has a cost, over 10 years, of about $US 41 per disability-adjusted life year saved. If health interventions with a good cost-effectiveness are those with a cost lower than $US 200 per disability-adjusted life year saved, as suggested by the World Bank, then the fortification of flour with Fe appears to be a public health strategy with good cost-effectiveness( 33 ).
Few studies in Brazil have evaluated the effectiveness of the flour fortification policy in a representative sample and in different age groups. Thus, the present study is the first to provide representative estimates of the prevalence of inadequate Fe intake in the pre- and post-fortification periods in this country. The reduction in inadequacy may be associated with reducing Fe deficiency, but due to the methodological limitations inherent in the evaluation methods of dietary intake and the lack of knowledge of Fe bioavailability, this result may not have a significant impact on body stores of this nutrient. Another limitation of the study is the use of the food composition tables from the US Department of Agriculture. However, the Fe contents of fortified foods available in the Brazilian food composition table were corrected. Moreover, during the pre-fortification period there was no replication of the 24HR, so the variance components derived from the post-fortification period were used to estimate the within-person variance.
Conclusion
In conclusion, the mandatory fortification of wheat and maize flour with Fe significantly furthered the reduction in the prevalence of inadequate intake, except among women of reproductive age, and changed the main contributors to this nutrient in the studied population. Therefore, monitoring of Fe addition in flour is essential to assess compliance to the fortified flour policy and to guarantee a safe Fe intake for all the population.
Acknowledgements
Acknowledgements: The authors would like to thank the participants of the study and researchers of the Dietary Assessment Group (GAC; Grupo de Pesquisa de Avaliação do Consumo Alimentar). Financial support: This study was funded by the São Paulo Research Foundation (FAPESP; grant number 2012/22113-9); the National Council of Technological and Scientific Development (CNPq; grant number 472873/2012-1); and scholarships offered by FAPESP (grant number 2013/06979-9). FAPESP and CNPq had no role in the design, analysis or writing of this article. Conflict of interest: The authors confirm that there is no conflict of interest. Authorship: D.A.S.V. contributed with analysis, interpretation of data and wrote the manuscript. J.S. contributed with interpretation of data and wrote the manuscript. E.V.J. contributed with analysis of the manuscript. R.M.F. conceived the study, designed the study and revised the article critically. D.M.M. contributed with design of the study and revising the article critically. All authors read and approved the submitted version. Ethics of human subject participation: The study protocol in both surveys was reviewed and approved by the Ethics Committee at the School of Public Health, University of São Paulo. All participants enrolled in the study after providing free and written informed consent forms signed by themselves or by their guardians, when younger than 18 years.
References
- 1. World Health Organization (2008) Worldwide Prevalence of Anaemia 1993–2005: WHO Global Database on Anaemia. Geneva: WHO. [Google Scholar]
- 2. Mensink GBM, Fletcher R, Gurinovic M et al. (2013) Mapping low intake of micronutrients across Europe. Br J Nutr 110, 755–773. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. Flynn A, Hirvonen T, Mensink GBM et al. (2009) Intake of selected nutrients from foods, from fortification and from supplements in various European countries. Food Nutr Res 2009, 53. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. UNICEF & The Micronutrient Initiative (2004) Vitamin & Mineral Deficiency: A Global Progress Report. Ottawa: UNICEF and The Micronutrient Initiative. [Google Scholar]
- 5. World Health Organization (2001) Iron Deficiency Anaemia: Assessment, Prevention, and Control. A Guide for Programme Managers. Geneva: WHO. [Google Scholar]
- 6. World Health Organization & Food and Agriculture Organization of the United Nations (2006) Guidelines on Food Fortification with Micronutrients. Geneva: WHO. [Google Scholar]
- 7. Bailey RL, West KP Jr & Black RE (2015) The epidemiology of global micronutrient deficiencies. Ann Nutr Metab 66, Suppl. 2, S22–S33. [DOI] [PubMed] [Google Scholar]
- 8. Hurrell R, Ranum P, de Pee S et al. (2010) Revised recommendations for iron fortification of wheat flour and an evaluation of the expected impact of current national wheat flour fortification programs. Food Nutr Bull 31, Suppl. 1, S7–S21. [DOI] [PubMed] [Google Scholar]
- 9. Ministério da Saúde (2002) Resolução no 344, 13 de dezembro de 2002. Aprova o regulamento técnico para a fortificação das farinhas de trigo e das farinhas de milho com ferro ácido fólico, constante no anexo desta resolução. Diário Oficial da União; available at http://bvsms.saude.gov.br/bvs/saudelegis/anvisa/2002/rdc0344_13_12_2002.html
- 10. Guenther PM, DeMaio TJ, Ingwersen LA et al. (1995) The multiple-pass approach for the 24 hour recall in the Continuing Survey of Food Intakes by Individuals (CSFII) 1994–1996. Paper presented at the 2nd International Conference on Dietary Assessment Methods, Boston, MA, USA, 22–24 January 1995.
- 11. Dodd KW, Guenter PM, Freedman LS et al. (2006) Statistical methods for estimating usual intake of nutrients and foods: a review of the theory. J Am Diet Assoc 106, 1640–1650. [DOI] [PubMed] [Google Scholar]
- 12. Nusser SM, Carriquiry AL, Dodd KW et al. (1996) A semiparametric transformation approach to estimating usual daily intake distributions. J Am Stat Assoc 91, 1440–1449. [Google Scholar]
- 13. Verly-Jr E, Cesar CLG, Fisberg RM et al. (2013) Variância intrapessoal da ingestão de energia e nutrientes em adolescentes: correção de dados em estudos epidemiológicos. Rev Bras Epidemiol 16, 170–177. [PubMed] [Google Scholar]
- 14. Jahns L, Carriquiry A, Arab L et al. (2004) Within- and between-person variation in nutrient intakes of Russian and US children differs by sex and age. J Nutr 134, 3114–3120. [DOI] [PubMed] [Google Scholar]
- 15. Institute of Medicine, Food and Nutrition Board (2000) Using the estimated average requirement for nutrient assessment of groups. In Dietary Reference Intakes: Applications in Dietary Assessment, pp. 73–105. Washington, DC: National Academy Press. [Google Scholar]
- 16. National Research Council (1989) Recommended Dietary Allowances. Washington, DC: National Academy Press. [Google Scholar]
- 17. Block G, Dresser CM, Hartman AM et al. (1985) Nutrient sources in the American diet: quantitative data from the NHANES II survey. II. Macronutrients and fats. Am J Epidemiol 122, 27–40. [DOI] [PubMed] [Google Scholar]
- 18. Santos Q, Nilson EAF, Verly-Junior E et al. (2015) An evaluation of the effectiveness of the flour iron fortification programme in Brazil. Public Health Nutr 18, 1670–1674. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19. Berner LA, Keast DR, Bailey RL et al. (2014) Fortified foods are major contributors to nutrient intakes in diets of US children and adolescents. J Acad Nutr Diet 114, 1009–1022. [DOI] [PubMed] [Google Scholar]
- 20. Martorell R, Ascencio M, Tacsan L et al. (2015) Effectiveness evaluation of the food fortification program of Costa Rica: impact on anemia prevalence and hemoglobin concentrations in women and children. Am J Clin Nutr 101, 210–217. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Steyn NP, Wolmarans P, Nel JH et al. (2008) National fortification of staple foods can make a significant contribution to micronutrient intake of South African adults. Public Health Nutr 11, 307–313. [DOI] [PubMed] [Google Scholar]
- 22. Fulgoni VL, Keast DR, Bailey RL et al. (2011) Foods, fortificants, and supplements: where do Americans get their nutrients? J Nutr 141, 1847–1854. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Instituto Brasileiro de Geografia e Estatística (2011) Análise do Consumo Alimentar Pessoal no Brasil, 2008–2009 (Family Budget Survey, 2008–2009). Rio de Janeiro: IBGE. [Google Scholar]
- 24. World Health Organization (2011) Guideline. Intermittent Iron and Folic Acid Supplementation in Menstruating Women. Geneva: WHO. [PubMed] [Google Scholar]
- 25. Ministério da Saúde (2011) II Reunião Ordinária da Comissão Interinstitucional para Implementação, Acompanhamento e Monitoramento das Ações de Fortificação de Farinhas de Trigo, Milho e de seus subprodutos. http://189.28.128.100/dab/docs/portaldab/documentos/2_reuniao_ordinaria.pdf (accessed September 2015).
- 26. Germani R, Ascheri JLR, Silva FT et al. (2001) Manual de Fortificação de Farinha de Trigo com Ferro. Rio de Janeiro: Embrapa Agroindústria de Alimentos; available at http://189.28.128.100/dab/docs/portaldab/documentos/manual_fortificacao.pdf [Google Scholar]
- 27. Assunção MCF, Santos IS, Barros AJD et al. (2012) Flour fortification with iron has no impact on anaemia in urban Brazilian children. Public Health Nutr 15, 1796–1801. [DOI] [PubMed] [Google Scholar]
- 28. Hennessy A, Walton J & Flynn A (2013) The impact of voluntary food fortification on micronutrient intakes and status in European countries: a review. Proc Nutr Soc 72, 433–440. [DOI] [PubMed] [Google Scholar]
- 29. Abtahi M, Neyestani TR, Pouraram H et al. (2014) Iron-fortified flour: can it induce lipid peroxidation? Int J Food Sci Nutr 65, 649–654. [DOI] [PubMed] [Google Scholar]
- 30. Fulgoni VL & Buckley RB (2015) The contribution of fortified ready-to-eat cereal to vitamin and mineral intake in the US population, NHANES 2007–2010. Nutrients 7, 3949–3958. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31. Baltussen R, Knai C & Sharan M (2004) Iron fortification and iron supplementation are cost-effective interventions to reduce iron deficiency in four subregions of the world. J Nutr 134, 2678–2684. [DOI] [PubMed] [Google Scholar]
- 32. Fiedler JL & Macdonald B (2009) A strategic approach to the unfinished fortification agenda: feasibility, costs, and cost-effectiveness analysis of fortification programs in 48 countries. Food Nutr Bull 30, 238–316. [DOI] [PubMed] [Google Scholar]
- 33. World Bank (1993) World Development Report: Investing in Health. New York: Oxford University Press. [Google Scholar]