Skip to main content Accessibility help
×
Home
Hostname: page-component-5d6d958fb5-8cb25 Total loading time: 1.631 Render date: 2022-11-26T13:16:46.603Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "displayNetworkTab": true, "displayNetworkMapGraph": false, "useSa": true } hasContentIssue true

Anaemia prevalence may be reduced among countries that fortify flour

Published online by Cambridge University Press:  23 June 2015

Jonathan S. Barkley
Affiliation:
Food Fortification Initiative, 1599 Clifton Road, Atlanta, GA 30322, USA Hubert Department of Global Health, Rollins School of Public Health, Emory University, 1518 Clifton Road North East, Atlanta, GA30322, USA
Kathleen S. Wheeler
Affiliation:
Food Fortification Initiative, 1599 Clifton Road, Atlanta, GA 30322, USA Hubert Department of Global Health, Rollins School of Public Health, Emory University, 1518 Clifton Road North East, Atlanta, GA30322, USA
Helena Pachón*
Affiliation:
Food Fortification Initiative, 1599 Clifton Road, Atlanta, GA 30322, USA Hubert Department of Global Health, Rollins School of Public Health, Emory University, 1518 Clifton Road North East, Atlanta, GA30322, USA
*
*Corresponding author: H. Pachón, fax +1 404 727 9745, email helena.pachon@emory.edu
Rights & Permissions[Opens in a new window]

Abstract

The effectiveness of flour fortification in reducing anaemia prevalence is equivocal. The goal was to utilise the existing national-level data to assess whether anaemia in non-pregnant women was reduced after countries began fortifying wheat flour, alone or in combination with maize flour, with at least Fe, folic acid, vitamin A or vitamin B12. Nationally representative anaemia data were identified through Demographic and Health Survey reports, the WHO Vitamin and Mineral Nutrition Information System database and other national-level nutrition surveys. Countries with at least two anaemia surveys were considered for inclusion. Within countries, surveys were excluded if altitude was not consistently adjusted for, or if the blood-draw site (e.g. capillary or venous) or Hb quantification method (e.g. HemoCue or Cyanmethaemoglobin) differed. Anaemia prevalence was modelled for countries that had pre- and post-fortification data (n 12) and for countries that never fortified flour (n 20) using logistic regression models that controlled for time effects, human development index (HDI) and endemic malaria. After adjusting for HDI and malaria, each year of fortification was associated with a 2·4 % reduction in the odds of anaemia prevalence (PR 0·976, 95 % CI 0·975, 0·978). Among countries that never fortified, no reduction in the odds of anaemia prevalence over time was observed (PR 0·999, 95 % CI 0·997, 1·002). Among both fortification and non-fortification countries, HDI and malaria were significantly associated with anaemia (P< 0·001). Although this type of evidence precludes a definitive conclusion, results suggest that after controlling for time effects, HDI and endemic malaria, anaemia prevalence has decreased significantly in countries that fortify flour with micronutrients, while remaining unchanged in countries that do not.

Type
Full Papers
Copyright
Copyright © The Authors 2015 

Anaemia continues to be an important public health problem in many regions of the world, and there has been a little decrease in the global prevalence in recent years( Reference Stevens, Finucane and De-Regil 1 ). It is a major public health problem in many regions, particularly low- to middle-income countries with prevalence exceeding 40 %( Reference de Benoist, McLean and Egli 2 ) for pre-school children in Central and West Africa, East Africa and Southern Africa, South Asia, and Oceania, and for non-pregnant and pregnant women of reproductive age in Central and West Africa and South Asia( Reference Stevens, Finucane and De-Regil 1 ). Compared with 1995, 2011 estimates of the prevalence of anaemia declined by 5 % points or less, from 47 to 43 % in pre-school children, 33 to 29 % in non-pregnant women (NPW) and 43 to 38 % in pregnant women( Reference Stevens, Finucane and De-Regil 1 ). Nutritional causes of anaemia include Fe and other nutrient deficiencies, while non-nutritional causes include malaria, infections and haemoglobinopathies( Reference de Benoist, McLean and Egli 2 ).

Food fortification can address many of the nutritional causes of anaemia. That is, the risk for anaemia is lowered if foods are fortified( Reference Allen, de Benoist and Dary 3 ) with nutrients known to influence Hb synthesis such as the minerals Cu, Fe, Se and Zn, and the vitamins A, B2, B6, folic acid (B9), B12 and E( Reference Kraemer and Zimmermann 4 ). A meta-analysis of efficacy trials has indicated that fortifying food with Fe increases Hb levels and decreases the prevalence of anaemia( Reference Gera, Sachdev and Boy 5 ). Currently, eighty-one countries mandate fortification of wheat flour alone or in combination with maize flour( 6 ). Fe and folic acid, the synthetic form of folate (vitamin B9), are the combinations of fortificants most commonly used.

The evidence on the effectiveness of flour fortification for reducing anaemia is inconsistent. Ten publications were reviewed that summarise studies completed in twelve countries reporting Hb levels before and after initiation of flour fortification; inconsistent methodology across the studies precluded completing a meta-analyses of their results( 7 ). The nutrients added to wheat and maize flour in these studies included Fe, Zn and vitamins A, B1, B2, B3, B6, B12 and folic acid. Notably, in eight of the countries, the recommended Fe compounds( 8 ) were used. The post-fortification measurement was conducted as early as 6·5 months after fortification began in one Australian study( Reference Kamien, Woodhill and Nobile 9 ) and as late as 8 years after fortification began in Bushehr province in Iran( Reference Sadighi, Sheikholeslam and Mohammad 10 ). A total of twenty-three subgroup analyses were reported. Of them, eleven reported an increase in Hb levels after flour fortification began. The increase ranged from 1 g/l in Brazilian pregnant women( Reference Fujimori, Sato and Szarfarc 11 ) to 21 g/l in Tajik children( Reference Tazhibayev, Dolmatova and Ganiyeva 12 ). Of the total subgroups, twelve showed a decrease in Hb levels after fortification began, or no change in relation to a control group (nine analyses)( Reference Nestel, Nalubola and Sivakeneshan 13 ). In summary, the evidence from effectiveness trials is equivocal on whether fortification of flour with one or several nutrients improves Hb.

The objective of the present study was to use nationally representative anaemia surveys to assess whether anaemia prevalence was reduced in NPW after countries began fortifying wheat flour, alone or in combination with maize flour, with at least Fe, folic acid, vitamin A or vitamin B12.

Methods

No identifying information of human subjects was used; thus, the present study was exempt from Institutional Review Board review.

Survey collection and determining anaemia prevalence

Nationally representative anaemia surveys of NPW were identified through Demographic and Health Surveys (DHS)( 14 ), the WHO Vitamin and Mineral Nutrition Information System database( 15 ), Multiple Indicator Cluster Surveys( 16 ) and internet searches. The total number of NPW with measured Hb values and the proportion with anaemia were abstracted from each survey report. Anaemia proportions specific to NPW were not always reported in the final DHS reports; thus, data files were used to determine these values among countries with DHS (Table 1). To be consistent with DHS methodology, the anaemia variables were weighted as described by DHS( 17 ) and Hb values between 0 and 60 g/l were considered implausible values for calculation and excluded. Altitude-adjusted Hb is included as a variable in the DHS data files and was used to determine anaemia prevalence. Anaemia prevalence was calculated as the proportion of NPW with Hb < 120 g/l.

Table 1 Summary of country characteristics, survey results and covariate values for fortification (n 12) and non-fortification (n 20) countries that conducted nationally representative anaemia surveys on non-pregnant women (NPW)

HDI, human development index; DHS, Demographic and Health Surveys; FFI, Food Fortification Initiative; NA, not applicable.

* Information obtained from most recently available data in FFI's database( 6 ).

HDI closest to the year the survey was conducted was obtained from a UN Development Program report( 18 ). All values are between 0 and 1, where 1 represents higher social and economic development.

Endemic malaria was obtained from the WHO's 2011 global burden of malaria report( 19 ), where 0 represents not endemic and 1 represents endemic.

§ All anaemia prevalence from DHS were calculated using the data files and analysis guidelines provided through the DHS Website.

Inclusion/exclusion criteria

To ensure data consistency within a country, surveys were excluded if altitude was not consistently adjusted for (i.e. if one survey was adjusted for altitude and another was not), if different cut-offs were used to define anaemia, or if either the blood-draw site (i.e. venous or capillary) or the Hb-quantification method (i.e. HemoCue or Cyanmethaemoglobin) differed.

Countries were included in the analysis if at least two nationally representative anaemia surveys were conducted on NPW and met the inclusion criteria. Countries with flour-fortification programs were included if at least one anaemia survey was available before fortification was implemented, at least one survey was available at least 2 years after fortification was implemented, and the above criteria were met. A country was considered a ‘fortification country’ if wheat flour was fortified either alone, or in combination with maize flour, with at least Fe, folic acid, vitamin A or vitamin B12 (Table 1). Non-fortification countries were included if at least two surveys were available, they met the inclusion criteria, and no mandatory flour fortification was ongoing during the survey period.

Data collection of covariates

To control for factors associated with anaemia, data on the human development index (HDI) and malaria were collected. HDI data were obtained from the UN Development Program( 18 ). HDI is a single statistic that combines life expectancy, education and income indices into a composite value that represents a county's social and economic development. HDI values range between 0 and 1; higher values are indicative of greater social and economic development. If an index was not available from the same year of a nutrition survey, then the index value from the closest available year ( ± 4 years) was used (Table 1). A cross-sectional assessment of countries with endemic malaria was obtained from the WHO's 2011 global malaria report( 19 ) (Table 1).

Statistical analysis

Anaemia prevalence ratios were studied using logistic regression models separately for countries that fortified and for those that did not. A continuous exposure variable was used for countries that fortified and countries that never fortified. For countries with data during the pre- and post-fortification periods, exposure was coded as years since fortification was implemented ((before (negative values) or after (positive values)). For countries that never fortified, exposure was similarly coded as years since baseline (positive values), where baseline was defined as the year of the first available anaemia survey. Data were managed in Excel. In addition to the exposure variable, each model included HDI and endemic malaria (dummy coded 0/1). Modelling anaemia prevalence using the events/trials format of logistic regression allowed the sample sizes of each survey to be taken into account. All analyses were conducted using SAS 9.3 (SAS Institute, Inc.). Prevalence ratios were reported along with their corresponding 95 % CI, and an α level of 0·05 was used to determine statistical significance.

Results

Characteristics of data sets

Anaemia data from two countries with pre- and post-fortification data (El Salvador( Reference Stetler and Huong 20 23 ) and Guatemala( 24 26 )) and seven countries that never fortified (Azerbaijan( Reference Branca, Burkholder and Hamel 27 , Reference Serbanescu, Morris and Rahimova 28 ), Guinea( 14 , 29 ), Liberia( 14 , Reference Mulder-Sibanda, Dahn and Duworko 30 ), Mozambique( 14 , 31 ), Sri Lanka( Reference Mudalige and Nestel 32 , Reference Piyasena and Mahamithawa 33 ), Vanuatu( 16 , Reference Harvey, Carlot and Menere 34 ) and Vietnam( Reference Yip 35 , Reference Khoi, Khan and Tam 36 )) were excluded because they did not meet the inclusion criteria. Table 1 ( 6 , 14 , Reference Pena-Rosas and Sinclair 37 67 ), therefore, summarises data from fortification countries that met the inclusion criteria (n 12) and from countries that did not fortify and met the inclusion criteria (n 20).

Modelling

Adjusting for HDI and malaria, each year of flour fortification was associated with a 2·4 % decreased odds of anaemia (prevalence OR (PR) 0·976, 95 % CI 0·975, 0·978; Fig. 1). Among countries that never fortified, no reduction in anaemia over time was observed (PR 0·999, 95 % CI 0·997, 1·002). In both models, HDI and malaria were significantly associated with anaemia, but with differing directions of association (P< 0·001). HDI was inversely associated with anaemia among fortification countries such that a unit increase was associated with a large reduction in the odds of anaemia (PR 0·040, 95 % CI 0·036, 0·045); however, endemic malaria was also associated with reduced anaemia odds (PR 0·546, 95 % CI 0·522, 0·571). Among countries that never fortified, endemic malaria was positively associated with odds of anaemia (PR 2·805, 95 % CI 2·703, 2·911), and increasing HDI was also associated with increased anaemia odds (PR 3·890, 95 % CI 3·443, 4·394).

Fig. 1 Prevalence OR and 95 % CI for the effect of exposure on anaemia prevalence in non-pregnant women after controlling for human development index and endemic malaria. Exposure was coded as years since fortification was implemented for fortification countries (●, n 12) and year since baseline survey for non-fortification countries (, n 20).

Discussion

The purpose of the present study was to use existing data sources to examine anaemia trends in NPW among countries that fortified wheat flour, alone or in combination with maize flour, and among those that did not. We found that after controlling for endemic malaria and HDI, significant reductions in anaemia prevalence were only observed among countries that initiated fortification. Among countries that fortified, each year of fortification was associated with a 2·4 % reduction in the odds of anaemia compared with each previous year. Although this type of evidence precludes a definitive conclusion, overall, the results suggest that flour fortification may be able to significantly reduce anaemia burden at the population level.

The reduction in anaemia prevalence in NPW found in the present study is consistent with the small (4 % points) global reduction in anaemia observed between 1995 and 2011 in NPW( Reference Stevens, Finucane and De-Regil 1 ). This small reduction is also consistent with the fact that fortification can only address nutritional causes of anaemia, such as Fe deficiency( Reference Kassenbaum, Jasrasaria and Naghavi 68 ) or other nutrient deficiencies.

However, the conclusion that fortification can significantly lower the burden of anaemia at a population level contradicts findings from a desk review( Reference Hurrell, Ranum and de Pee 69 ). Hurrell et al. ( Reference Hurrell, Ranum and de Pee 69 ) reviewed the design of flour-fortification programs and concluded that most countries that fortify with Fe use non-recommended forms with low bioavailability that would not be sufficient to lower anaemia prevalence at the population level (n 50 of 78). Among the twelve fortification countries that were included in the analyses, seven currently use a higher-bioavailability Fe compound recommended by the WHO( 8 ). Since a greater proportion of countries that fortify using higher bioavailability Fe compounds were included in the present study, this may help explain why reductions in anaemia prevalence were observed. Fe levels and flour consumption among the included countries may have also influenced this result. In addition, Hurrell et al. ( Reference Hurrell, Ranum and de Pee 69 ) noted that compliance to fortification programs is often low and can play a contributing role to non-improvement over time. However, the present analysis did not assess the contributing effect of fortification compliance.

The present study attempted to address non-nutritional causes of anaemia by controlling for HDI and endemic malaria. HDI, composed from life expectancy, education and income indices, synthesises social and economic development – two underlying causes of anaemia( Reference Teta, Kuate-Defo and Receveur 70 ) – into a single statistic. As expected, increased social and economic development (HDI) was inversely associated with anaemia prevalence in countries that initiated flour fortification. However, surprisingly, increased HDI was positively associated with anaemia among non-fortification countries. This unexpected result may be explained in part by differences in regional representativeness between the two groups of countries. As presented in Table 1, the non-fortification countries were more representative of Africa and tended to have lower HDI than the fortification countries. Since HDI values tended to be low in non-fortification countries (mean 0·46) compared with fortification countries (mean 0·63), it is possible that these values were not able to adequately capture differences in economic and social development between countries. Thus, among the non-fortification countries included in this analysis, large improvements in a macro index such as HDI would be probably necessary to capture population shifts in living conditions that would relate to improved nutrition and concomitant reductions in anaemia. Although endemic malaria was positively associated with anaemia among non-fortification countries, it was unexpectedly associated with decreased anaemia prevalence among fortification countries. This inverse effect may be partially explained by the fact that in a country that fortifies, those with malaria are also likely to consume fortified foods and are therefore getting more nutrients in their diets. Thus, in these countries, malaria status may not be as strong of a predictor of anaemia prevalence. This result may be further explained by the geographic representativeness of the countries, in addition to limitations due to how malaria was coded. African countries tend to have larger anaemia burdens due to malaria, infections, inflammation and hook worms. In regions where these non-nutritional anaemia causes play a role, food fortification would be expected to have less effect. Countries that fortified were more representative of the Americas (Table 1), which has a much lower malaria burden than Africa. Specifically, 83 % of confirmed reported malaria cases occurred in Africa, while only 4 % occurred in the Americans( 19 ). The graduations in endemic malaria exposure cannot be captured by the current 0/1 dummy variable coding, and thus, this may explain why the expected association was not observed among the fortification countries. This dummy coding was employed since poor malaria surveillance systems exist for many countries( 19 ). Unlike HDI, endemic malaria was assessed at one point in time (based on a 2011 WHO global malaria report( 19 )), and thus was not able to account for temporal changes in disease risk. However, since no significant impact was made on reducing global malaria prevalence between 1992 and 2002( Reference Hay, Guerra and Tatem 71 ), and the malaria endemic countries as identified by WHO's malaria reports (only available since 2008) have remained largely unchanged, using a one-time assessment for malaria was likely acceptable. Nevertheless, in future investigations, employing more categories to represent graduations of malaria burden would be preferable. Other issues, such as the seasonality of malaria and differential participation rates, may have also influenced the malaria results among countries that fortified. Malaria has a lower disease burden during dry seasons( 19 ); thus, each survey's results could be biased depending on the season and the disease status (malaria or non-malaria) of those who agreed to provide blood samples.

There are both advantages and limitations to the present study that are important to recognise for future investigations that further explore these associations. This analysis was able to account for elapsed time through the use of continuous exposure variables (years since fortification implementation for fortification countries, and years since baseline survey for non-fortification countries). Countries that have been fortifying for a longer time are more likely to see reductions in anaemia simply because the intervention has had more time to take effect. Thus, considering exposure in this way can lead to more valid results than simply comparing countries that fortify to those that do not. The main advantage is that analyses were restricted to nationally representative surveys and an attempt was made to ensure data quality and consistency by excluding surveys that were not comparable within countries. In cases where raw data files were available for the countries, consistent adjustments for altitude were made so that data were not unnecessarily excluded.

However, the fact that exclusions were made may have influenced the results. As mentioned, two and seven countries were excluded from the fortification and non-fortification groups, respectively, because they did not meet the inclusion criteria. The most common reason for exclusion (n 7) was that both the blood-draw and Hb-quantification methods differed between surveys. It has been shown that each of these factors can influence reported anaemia prevalence( 72 ); thus, for future comparisons, it would be helpful if surveys followed consistent methodology over time. DHS were the most common source for anaemia data (Table 1) and consistently used capillary blood and the HemoCue method to measure Hb. Thus, if other investigations similarly followed consistent methodology, more accurate comparisons could be made between and within countries.

A main limitation of the present study was the small sample size. This limited the number of covariates that could be adjusted for in the analyses and may have led to biased associations. Residual confounding could still be present either from imprecision/measurement errors associated with covariates we adjusted for or from those that could not be considered in the present study. A final limitation worth noting is the generalisability of the results. Due to data availability, most non-fortification countries were from Africa (n 14 of 20), while most countries that initiated fortification were from Latin America (n 6 of 12). Due to these differences, a single model that matched a non-fortification country to a fortification country was not viable, and instead two separate logistic models were run. Using this approach still allows for conclusions to be made about each group of countries, and effects due to unmeasured or unknown confounders were likely similar within each group because the fortification and non-fortification countries were generally from the same region. Furthermore, despite small sample sizes, the CI obtained for the measures of effect between both groups of countries were narrow, suggesting good precision of the estimates.

In conclusion, after adjusting for important factors associated with anaemia, flour fortification was associated with decreased anaemia prevalence in NPW. Since efforts were made to control for other factors associated with anaemia, this observation is encouraging. Evidence that low bioavailable Fe compounds are typically used, as stated by Hurrell et al. ( Reference Hurrell, Ranum and de Pee 69 ), suggests there is room to improve Hb concentration through Fe fortification. Of the eighty-one countries that mandate fortification of wheat flour alone, or in combination with maize flour, only twelve had consistent, nationally representative anaemia data suggesting that increased surveillance efforts are important for most countries. As more anaemia surveys are conducted using consistent methodology, the association between flour fortification and anaemia prevalence will be better elucidated, and stronger support for the effectiveness of flour fortification may be achieved.

Acknowledgements

The authors thank Dr Yaw Addo of Emory University for his statistical help and assistance with SAS and R programs; Drs Aryeh Stein, David Kleinbaum and Eli Rosenberg of Emory University for their helpful statistical consults; Ms Katie Kendrick of Emory University for performing anaemia prevalence calculations for Indonesia; DHS Program support staff for responding to data-related inquiries; and Ms Sarah Zimmerman from the Food Fortification Initiative for editorial assistance.

J. S. B. and K. S. W.'s time was jointly funded by Emory University's Rollins Earn and Learn (REAL) program and the Food Fortification Initiative (FFI). H. P.'s time was supported by an appointment to the Research Participation Program at the US Centers for Disease Control and Prevention (CDC) administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the US Department of Energy and CDC.

None of the authors has any conflicts of interest to declare.

The authors' contributions are as follows: J. S. B., K. S. W. and H. P. designed the study; J. S. B. and K. S. W. conducted the study; J. S. B. analysed the data; J. S. B., K. S. W. and H. P. wrote the manuscript; J. S. B. had primary responsibility for the final content of the manuscript. All authors read and approved the final manuscript.

References

1 Stevens, GA, Finucane, MM, De-Regil, LM, et al. (2013) Global, regional, and national trends in haemaglobin concentration and prevalence of total and severe anaemia in children and pregnant and non-pregnant women for 1995–2011: a systematic analysis of population-representative data. Lancet Glob Health 1, e16e25.CrossRefGoogle Scholar
2 de Benoist, B, McLean, E, Egli, I, et al. (editors) (2008) Worldwide Prevalence of Anaemia 1993–2005: WHO Global Database on Anaemia. Geneva: WHO.Google Scholar
3 World Health Organization & Food and Agriculture Organization (2006) Guidelines on Food Fortification with Micronutrients. [Allen, L, de Benoist, B, Dary, O et al., editors]. Geneva: WHO.Google Scholar
4 Kraemer, K & Zimmermann, MB (2007) Nutritional Anaemia. Basel: Sight and Life Press.Google Scholar
5 Gera, T, Sachdev, HS & Boy, E (2012) Effect of iron-fortified foods on hematologic and biologic outcomes: systematic review of randomized controlled trials. Am J Clin Nutr 96, 309324.CrossRefGoogle Scholar
6 Food Fortification Initiative. Food Fortification Initiative database [Internet]. Atlanta, GA: Food Fortification Initiative (accessed January 2015).Google Scholar
7 Food Fortification Initiative (2013) Impact of wheat flour fortification on anemia. http://www.ffinetwork.org/why_fortify/documents/Brief_4_Anemia_2013.pdf (accessed January 2015).Google Scholar
8 World Health Organization (2009) Recommendations on Wheat and Maize Flour Fortification. Meeting Report: Interim Consensus Statement. Geneva: WHO. http://www.who.int/nutrition/publications/micronutrients/wheat_maize_fort.pdf?ua = 1/ (accessed accessed January 2014).Google ScholarPubMed
9 Kamien, M, Woodhill, JM, Nobile, S, et al. (1974) Nutrition in the Australian aborigines–effects of the fortification of wheat flour. Aust N Z J Med 5, 123133.CrossRefGoogle Scholar
10 Sadighi, J, Sheikholeslam, R, Mohammad, K, et al. (2008) Flour fortification with iron: a mid-term evaluation. Public Health 122, 313321.CrossRefGoogle ScholarPubMed
11 Fujimori, E, Sato, APS, Szarfarc, SC, et al. (2011) Anaemia in Brazilian pregnant women before and after flour fortification with iron. Rev Saúde Publica 45, 10271035.CrossRefGoogle ScholarPubMed
12 Tazhibayev, S, Dolmatova, O, Ganiyeva, G, et al. (2008) Evaluation of the potential effectiveness of wheat flour and salt fortification programs in five Central Asian countries and Mongolia, 2002–2007. Food Nutr Bull 29, 255265.CrossRefGoogle Scholar
13 Nestel, P, Nalubola, R, Sivakeneshan, R, et al. (2004) The use of iron-fortified wheat flour to reduce anaemia among the estate population in Sri Lanka. Int J Vitam Nutr Res 74, 3551.CrossRefGoogle Scholar
14 ICF International (2012) Demographic and Health Surveys (Various) [Datasets]. Calverton, MD: ICF International (distributor).Google Scholar
15 World Health Organization. Vitamin and Mineral Nutrition Information System. Micronutrients Database. Geneva: WHO. http://www.who.int/vmnis/database/en/ (accessed accessed January 2014).Google ScholarPubMed
16 United Nations Children's Fund. Multiple Indicator Cluster Surveys. New York: UNICEF. http://www.unicef.org/statistics/index_24302.html (accessed accessed January 2014).Google ScholarPubMed
17 United States Agency for International Development, Demographic and Health Survey Program. Using Datasets for Analysis. Rockville, MD: ICF International. http://www.measuredhs.com/data/Using-Datasets-for-Analysis.cfm (accessed accessed January 2014).Google Scholar
18 United Nations Development Program. Human Development Reports. New York: UNDP. http://hdr.undp.org/en/content/human-development-index-hdi-table (accessed accessed December 2013).Google Scholar
19 World Health Organization (2011) World Malaria Report. http://www.who.int/malaria/world_malaria_report_2011/en/ (accessed accessed December 2013).Google Scholar
20 Stetler, HC & Huong, AY (1981) Epidemiología de la anaemia en niños de edad preescolar y sus madres en El Salvador (Epidemiology of anaemia in preschool children and their mothers in El Salvador). Arch Latinoam Nutr 31, 4250.Google Scholar
21 Salvadoran Demographic Association & Interinstitutional Consultative Committee (2000) Encuesta nacional de salud familiar FESAL-98 (National Family Health Survey FESAL-98). San Salvador: Salvadoran Demographic Association.Google Scholar
22 Salvadoran Demographic Association, United States Agency for International Development & Centers for Disease Control and Prevention (2004) Encuesta nacional de salud familiar FESAL 2002–2003: Informe final (FESAL National Family Health Survey 2002–2003: Final Report). San Salvador: Salvadoran Demographic Association.Google Scholar
23 Salvadoran Demographic Association, United States Agency for International Development & Centers for Disease Control and Prevention (2009) Encuesta nacional de salud familiar FESAL 2008: Informe final (FESAL National Family Health Survey 2008: Final Report). San Salvador: Salvadoran Demographic Association.Google Scholar
24 Ministerio de Salud Pública y Asistencia Social (1996) Encuesta nacional de micronutrients (National Micronutrient Survey). Guatemala City: Ministerio de Salud Pública y Asistencia Social.Google Scholar
25 Ministerio de Salud Pública y Asistencia Social, Instituto Nacional de Estadística, Universidad del Valle de Guatemala, et al. (2003) Encuesta nacional de salud materno infantil 2002 (National Maternal and Infant Health Survey 2002). Guatemala City: Ministerio de Salud Pública y Asistencia Social.Google Scholar
26 Ministerio de Salud Pública y Asistencia Social, Instituto Nacional de Estadística, Universidad del Valle de Guatemala, et al. (2010) Encuesta nacional de salud materno infantil 2008–2009 (National Maternal and Infant Health Survey 2008–2009). Guatemala City: Ministerio de Salud Pública y Asistencia Social.Google Scholar
27 Branca, F, Burkholder, B, Hamel, M, et al. (1996) Health and Nutrition Survey of Internally Displaced and Resident Population of Azerbaijan. Atlanta, GA: CDC.Google Scholar
28 Serbanescu, F, Morris, L, Rahimova, S, et al. (editors) (2003) Reproductive Health Survey Azerbaijan, 2001 [Final Report]. Atlanta, GA: CDC.Google Scholar
29 Ministère de la Santé Publique [Guinée] (2001) Enquête nationale sur l'anémie ferriprive en Guinée (National Survey of Iron Deficiency Anaemia in Guinea). Conakry, Republic of Guinea: Ministry of Health and Public Hygiene.Google Scholar
30 Mulder-Sibanda, M, Dahn, B, Duworko, M, et al. (1999) National Micronutrient Survey. A National Prevalence Study on Vitamin A Deficiency, Iron Deficiency Anaemia, Iodine Deficiency. Monrovia: Ministry of Health and Social Welfare.Google Scholar
31 Ministério da Saúde & Direcção Nacional de Saúde (2003) Inquérito nacional seovre a deficiência de vitamina A, prevalência de anaemia e malária em crianças dos 6–59 meses e respectivas mães (National Survey of Vitamin A Deficiency, Prevalence of Anaemia and Malaria in Children Aged 6–59 Months and their Mothers). Maputo: Instituto Nacional de Saúde.Google Scholar
32 Mudalige, R & Nestel, P (2001) Prevalence of anaemia in Sri Lanka. Ceylon Med J 39, 916.Google Scholar
33 Piyasena, C & Mahamithawa, A (2003) Assessment of Anaemia Status in Sri Lanka 2001 [Survey Report]. Colombo: Ministry of Health, Nutrition and Welfare, Department of Health Services, Medical Research Institute.Google Scholar
34 Harvey, P, Carlot, M & Menere, R (1998) Report of the Second National Nutrition Survey 1996. Port Vila: Department of Health.Google Scholar
35 Yip, R (1996) Final Report of the 1995 Viet Nam National Nutrition Anaemia and Intestinal Helminth Survey: A Recommended Plan of Action for the Control of Iron Deficiency for Viet Nam. Jakarta: United Nations Children's Fund.Google Scholar
36 Khoi, HH, Khan, NC, Tam, NC, et al. (2001) Report on Viet Nam National Anaemia Survey, 2000. Hanoi: National Institute of Nutrition.Google Scholar
37 Pena-Rosas, JP & Sinclair, BM (2007) Wheat flour fortification for prevention and control of iron deficiency anaemia in Latin America: issues to consider in a systematic evaluation. Rev Med Minas Gerais 1/2 Suppl. 1, 17, S66S73.Google Scholar
38 Ministerio de Salud (1986) Encuesta nacional de nutrición: evaluación dietética 1982 (National Nutrition Survey: Dietary Assessment 1982). San José: Ministerio de Salud.Google Scholar
39 Rodriguez, S, Blanco, A, Cunningham, L, et al. (2001) Prevalencia de las anaemias nutricionales de mujeres en edad fértil, Costa Rica: encuesta nacional de nutrición, 1996 (Prevalence of nutritional anaemias of women of childbearing age, Costa Rica: National Nutrition Survey, 1996). Arch Latinoam Nutr 51, 1924.Google Scholar
40 Ministerio de Salud (2009) Encuesta nacional de nutrición 2008–2009 (National Nutrition Survey 2008–2009). San José: Ministerio de Salud.Google Scholar
41 National Food and Nutrition Centre (2007) Report on the Micronutrient Status of Women in Fiji. 2004 Report. Suva: National Food and Nutrition Centre.Google Scholar
42 National Food and Nutrition Centre (2012) Impact of Iron Fortified Flour in Childbearing Age Women in Fiji. 2010 Report. Suva: National Food and Nutrition Centre.Google Scholar
43 Ministerio de Salud Pública, Secretaría de Salud, Fundación Internacional de Ojos et al. (1997) Encuesta nacional de micronutrientes Honduras, 1996 (Honduras National Micronutrient Survey, 1996). Tegucigalpa: Secretaría de Salud, Ministerio de Salud Pública.Google Scholar
44 Frankenberg, E & Thomas, D (2000) The Indonesian Family Life Survey (IFLS): Study Design and Results from Waves 1 and 2. Santa Monica, CA: RAND.Google Scholar
45 Strauss, J, Beegle, K, Sikoki, B, et al. (2004) The Third Wave of the Indonesian Family Life Survey (IFLS): Overview and Field Report. Santa Monica, CA: RAND.Google Scholar
46 Strauss, J, Witoelar, F, Sikoki, B, et al. (2009) The Fourth Wave of the Indonesian Family Life Survey (IFLS4): Overview and Field Report. Santa Monica, CA: RAND.Google Scholar
47 Martínez, H, González, T, Flores, , et al. (1995) Anemia en mujeres de edad reproductiva. Resultados de una encuesta probabilística nacional (Anaemia in women of reproductive age. Results of a national probabilistic survey). Salud Pública de México 37, 108119.Google Scholar
48 Ministerio de Salud (2001) Encuesta Nacional de Nutrición 1999. Estado nutricio de niños y mujeres en México (National Nutrition Survey 1999. Nutritional Status of Children and Women in Mexico). Cuernavaca: Instituto Nacional de Salud Pública.Google Scholar
49 Ministerio de Salud (2007) Resultados de nutrición de la Encuesta nacional de salud y nutrición 2005–2006 (Nutrition Results from the National Survey of Health and Nutrition 2005–2006). Cuernavaca: Instituto Nacional de Salud Pública.Google Scholar
50 Ministerio de Salud (2012) Encuesta nacional de nutrición: resultados nacionales 2012 (National Nutrition Survey: National Results 2012). Cuernavaca: Instituto Nacional de Salud Pública.Google Scholar
51 Darnton-Hill, I, Mora, JO, Weinstein, H, et al. (1999) Iron and folate fortification in the Americas to prevent and control micronutrient malnutrition: an analysis. Nutr Rev 57, 2531.CrossRefGoogle ScholarPubMed
52 Ministerio de Salud (1994) Encuesta nacional sobre deficiencia de micronutrientes en Nicaragua 1993: resumen ejecutivo (National Survey on Micronutrient Deficiency in Nicaragua 1993: Executive Summary). Managua: Ministerio de Salud.Google Scholar
53 Ministerio de Salud (2002) Encuesta nacional de micronutrientes 2000 (National Micronutrient Survey 2000). Managua: Ministerio de Salud.Google Scholar
54 Ministerio de Salud (2006) Sistema integrado de vigilancia de intervenciones nutricionales 2003–2005 (Integrated System for Monitoring Nutritional Interventions 2003–2005). Managua: Ministerio de Salud.Google Scholar
55 Food and Nutrition Research Institute (1984) Second National Nutrition Survey, Philippines, 1982. Manila: Food and Nutrition Research Institute.Google Scholar
56 Food and Nutrition Research Institute (1987) Third National Nutrition Survey, Philippines, 1987. Manila: Food and Nutrition Research Institute, Department of Science and Technology.Google Scholar
57 Food and Nutrition Research Institute (1993) Fourth National Nutrition Survey. Manila: Food and Nutrition Research Institute.Google ScholarPubMed
58 Food and Nutrition Research Institute, Department of Science and Technology & United Nations Children's Fund (2001) Philippine Nutrition Facts & Figures. Manila: Food and Nutrition Research Institute.Google Scholar
59 Food and Nutrition Research Institute (2008) Seventh National Nutrition Survey, Philippines: 2008 Initial Results. Manila: Food and Nutrition Research Institute, Department of Science and Technology.Google Scholar
60 Northrop-Clewes, C, Hund, L, Valadez, J, et al. (2013) Global Alliance for Improved Nutrition LC-LQAS Survey Report. Uzbekistan: Ministry of Health.Google Scholar
61 Ministry of Health, Republic of Maldives (2001) Multiple Indicator Cluster Survey (MICS 2), Maldives. Malé: Ministry of Health.Google Scholar
62 Ministry of Health and Family [Maldives] & United Nations Children's Fund (2007) Project Report: National Micronutrient Survey 2007. Malé: Ministry of Health.Google Scholar
63 Ministry of Health Nepal, Child Health Division, New ERA, et al. (1999) Nepal Micronutrient Status Survey 1998. Kathmandu: Ministry of Health.Google Scholar
64 Branca, F, Ferrari, M & Rossi, L (2004) Micro-nutrient Status Survey in Tajikistan, 2003. Rome: National Institute for Research on Food and Nutrition, Kazakh Academy of Nutrition.Google Scholar
65 Ministry of Health Republic of Tajikistan & United Nations Children's Fund (2010) Micronutrient Status Survey in Tajikistan, 2009. Dushanbe: Ministry of Health Republic of Tajikistan.Google Scholar
66 Luo, C, Mwela, CM & Campbell, J (1999) National Baseline Survey on Prevalence and Aetiology of Anaemia in Zambia: A Random Cluster Community Survey Involving Children, Women and Men. Lusaka: National Food and Nutrition Commission.Google Scholar
67 Micronutrient Operational Strategies and Technologies (MOST), United Nations Children's Fund, Centers for Disease Control and Prevention, et al. (2003) Report of the National Survey to Evaluate the Impact of Vitamin A Interventions in Zambia, July and November 2003. Lusaka: MOST, United States Agency for International Development (USAID) Micronutrient Program.Google Scholar
68 Kassenbaum, NJ, Jasrasaria, R, Naghavi, M, et al. (2014) A systematic analysis of global anemia burden from 1990 to 2010. Blood 123, 615624.CrossRefGoogle Scholar
69 Hurrell, R, Ranum, R, 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, S7S21.CrossRefGoogle ScholarPubMed
70 Teta, N, Kuate-Defo, B & Receveur, O (2008) Multilevel modelling of sociodemographic predictors of various levels of anaemia among women in Mali. Public Health Nutr 12, 14621469.CrossRefGoogle Scholar
71 Hay, SI, Guerra, CA, Tatem, AJ, et al. (2004) The global distribution and population at risk of malaria: past, present, and future. Lancet Infect Dis 4, 327336.CrossRefGoogle ScholarPubMed
72 Masimo Corporation (2009) Total Haemoglobin Measurements: Accuracy of Laboratory Devices and Impact of Physiologic Variation. Irvine, CA: Masimo Corporation. http://www.masimo.com/pdf/sphb/lab5527a.pdf (accessed accessed January 2014).Google Scholar
Figure 0

Table 1 Summary of country characteristics, survey results and covariate values for fortification (n 12) and non-fortification (n 20) countries that conducted nationally representative anaemia surveys on non-pregnant women (NPW)

Figure 1

Fig. 1 Prevalence OR and 95 % CI for the effect of exposure on anaemia prevalence in non-pregnant women after controlling for human development index and endemic malaria. Exposure was coded as years since fortification was implemented for fortification countries (●, n 12) and year since baseline survey for non-fortification countries (, n 20).

You have Access
31
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Anaemia prevalence may be reduced among countries that fortify flour
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

Anaemia prevalence may be reduced among countries that fortify flour
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

Anaemia prevalence may be reduced among countries that fortify flour
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *