Volume 1540, Issue 1 p. 235-250
ORIGINAL ARTICLE
Open Access

Bouillon fortification as a strategy to address inequities in micronutrient adequacy of diets in Nigeria

Katherine P. Adams

Corresponding Author

Katherine P. Adams

Institute for Global Nutrition, Department of Nutrition, University of California, Davis, Davis, California, USA

Correspondence

Katherine P. Adams, Institute for Global Nutrition, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA. Email: [email protected]

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Stephen A. Vosti

Stephen A. Vosti

Institute for Global Nutrition, Department of Nutrition, University of California, Davis, Davis, California, USA

Department of Agricultural and Resource Economics, University of California, Davis, Davis, California, USA

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Emily Becher

Emily Becher

Institute for Global Nutrition, Department of Nutrition, University of California, Davis, Davis, California, USA

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Faith Ishaya

Faith Ishaya

Helen Keller International, Abuja, Nigeria

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Reina Engle-Stone

Reina Engle-Stone

Institute for Global Nutrition, Department of Nutrition, University of California, Davis, Davis, California, USA

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First published: 10 September 2024
Citations: 2

Abstract

Bouillon is a widely consumed condiment in many West African countries, including Nigeria. Although Nigeria has mandatory fortification standards for multiple food vehicles, bouillon fortification could help address remaining gaps in micronutrient intake. Using household food consumption data, we used the nutrient density method to model the additional contribution of bouillon fortified with vitamin A (40–250 µg/g bouillon), folic acid (20–120 µg/g), vitamin B12 (0.2–2 µg/g), iron (0.6–5 mg/g), and zinc (0.6–5 mg/g) for meeting micronutrient requirements of women of reproductive age (WRA) and children aged 6–59 months. Accounting for existing fortification programs, our results showed that, except for iron, the prevalence of inadequacy was substantially higher among WRA and children living in poorer and rural households. Given the ubiquity of bouillon consumption, bouillon fortification has the potential to virtually eliminate vitamin A, folate, and vitamin B12 inadequacy, reduce the prevalence of zinc inadequacy by over 20 percentage points, and improve equity in the micronutrient adequacy of diets across socioeconomic strata and urban and rural residence. Our results also suggested that designing a bouillon fortification program would require careful planning to balance reductions in inadequacy with the risk of high intakes. This evidence provides important input into decisions around bouillon fortification in Nigeria.

INTRODUCTION

Large-scale food fortification (LSFF), the addition of one or more micronutrients to food or condiments during processing, has proven potential to reduce micronutrient deficiencies and improve population health in low- and middle-income countries.1 Given its strong evidence base, LSFF is supported by the World Health Organization,2 and it is a recommended intervention in the 2021 Lancet Series on Maternal and Child Undernutrition.3 Today, over 100 countries have legislation mandating the fortification of one or more food vehicles.4 Nigeria is among the countries that have adopted LSFF, with national standards mandating the fortification of multiple food vehicles, including salt, wheat flour, maize flour, refined oil, sugar, and margarine.5

Despite these existing LSFF programs, micronutrient deficiencies remain a public health concern in Nigeria. Based on the 2021 National Food Consumption and Micronutrient Survey (NFCMS) final report, among children 6–59 months of age nationally, 31.1% are vitamin A deficient (serum retinol <0.70 µmol/L, using BRINDA-adjusted serum retinol), 20.7% are iron deficient (ferritin <12.0 µg/L, adjusted for inflammation), and 35.2% are zinc deficient (zinc <65 µg/dL).6 Among women of reproductive age (15–49 years of age, WRA), 11.6% are vitamin A deficient (serum retinol <0.70 µmol/L, using BRINDA-adjusted serum retinol), 10% are iron deficient (ferritin <15.0 µg/L, adjusted for inflammation), 95.4% have red blood cell (RBC) folate deficiency (RBC folate concentration <748 nmol/L), and 35.1% are zinc deficient (zinc <66 µg/dL). Among both children and WRA, the prevalence of vitamin B12 deficiency (serum B12 concentration <148 pmol/L) was low (< 3%).

Bouillon, a condiment often added to dishes as a seasoning during cooking, is widely consumed in multiple countries in West Africa, including Nigeria.6, 7 While several companies supplying bouillon in Nigeria voluntarily fortify bouillon with iron,8 there are several reasons for why bouillon might be an ideal candidate for mandatory fortification to complement existing mandatory LSFF programs in Nigeria and help close remaining dietary micronutrient gaps. First, the 2021 NFCMS data showed that household consumption of branded refined oil (where consumption of branded, or commercially produced, oil is a proxy for consumption of fortifiable refined oil) is low (< 25%) in the North Central, North East, and North West geopolitical zones and among households in the lowest two wealth quintiles, consumption of branded wheat flour is <20% nationally, and less than 1% of households consume branded maize flour.6 The same survey also showed that bouillon is consumed by over 99% of households,6 indicating a potential to reach households not reached by other fortifiable food vehicles. Additionally, when food vehicles like oil, rice, or maize flour are processed or refined at the household or village level, fortification is challenging to implement and monitor at scale, thus limiting feasibility.2 Bouillon, on the other hand, is usually centrally processed, enhancing the feasibility of fortification and monitoring and enforcement of fortification standards.2, 9

Nigeria is currently considering the introduction of a bouillon fortification program, and this decision requires, among other evidence, evidence on the potential impacts of fortified bouillon on the micronutrient adequacy of diets. The objectives of this paper are, therefore, to present modeled estimates of the potential contribution of adding a multiple-micronutrient (vitamin A, folic acid, vitamin B12, iron, and/or zinc) bouillon fortification program to existing LSFF programs in Nigeria to meet the dietary micronutrient requirements of WRA and children 6–59 months of age—two population groups that are particularly vulnerable to micronutrient deficiencies given their high relative micronutrient requirements.2, 10 We present the modeling results at the national level, and, to assess how fortified bouillon might help close the micronutrient gap among segments of the population that tend to be less likely to consume fortifiable forms of other mandatorily fortified food vehicles, we also present results by household socioeconomic status (SES) and urban and rural residence.

This research is part of an initiative to generate evidence related to bouillon fortification, including technical feasibility, efficacy, costs, and cost effectiveness. The acceptability of bouillon fortified with vitamin A, folic acid, vitamin B12, iron, and zinc has been established in Northern Ghana,11 and a randomized controlled trial is currently underway in the same communities to assess the efficacy of fortified bouillon for improving micronutrient status.12 Alongside this evidence, the modeling evidence presented in this paper provides policymakers in Nigeria with evidence-based information to inform decisions around adding multiple micronutrient-fortified bouillon to the country's portfolio of LSFF programs.

METHODS

Estimating apparent food consumption, micronutrient intake, and the adequacy of household diets

We used data from the most recent household consumption and expenditure survey (HCES), the 2018–2019 Nigeria Living Standards Survey (NLSS),13 to estimate household-level apparent food consumption and nutrient intake. The NLSS was implemented by the National Bureau of Statistics with support from the World Bank. Data were collected over a 1-year period, from September, 2018 through September, 2019, and are representative at the national, zonal, and state levels.14 We received approval from the World Bank to use the 2018–2019 NLSS data. All data used in the analyses were deidentified and were used in compliance with the World Bank's data access policy.

The food consumption module of the NLSS asked the household respondent to recall the total quantity of each of the 99 prespecified foods consumed by household members in the 7 days preceding the survey. The respondent was also asked to recall the amount of total consumption that came from purchases, the amount that came from their own production, and the amount that came from gifts or other sources. Using conversion factors provided with the NLSS data, we converted the total quantity consumed to daily apparent consumption in grams. To manage outliers in the food consumption data, we used age and sex data from household rosters to calculate the number of adult male equivalents (AMEs) in each household.15 We then calculated the food item- and zone-specific 95th percentile of apparent consumption per day per AME and replaced values above the 95th percentile with the value at the 95th percentile.16

The nutrient composition of the household diet was estimated by matching each food item to an entry in a food composition table (FCT). We matched most food items to entries in the West African FCT,17 and where appropriate matches could not be made, we used entries from the Nutrition Coordinating Center Nutrient Database for Standard Reference18 and the Malawian FCT.19 Some food items were aggregate in nature, and in those cases, the nutrient composition was based on a weighted average of several FCT entries. For example, the nutrient composition for fresh milk was based on zone-specific weighted averages of raw and pasteurized cow milk, goat milk, and sheep milk. The food list also included the generic item palm oil without distinguishing between types of palm oil. Therefore, based on input from Nigerian collaborators and an expert group composed of Nigerians with expertise in nutrition and LSFF, we assumed all reported palm oil consumption was unrefined red palm oil (i.e., we assumed that when respondents were asked about consumption of palm oil, they referred to consumption of red palm oil rather than refined palm oil).

We then calculated total daily household apparent intake of vitamin A, folate, vitamin B12, and iron, and, combined with estimates of total daily apparent energy intake, calculated the nutrient density of the household diet for each micronutrient. Nutrient density, which is a measure of the micronutrient quality of the diet per 1000 kcal, is calculated as the ratio of daily micronutrient intake to daily energy intake, multiplied by 1000.20 We assessed the adequacy of the household diet for meeting the micronutrient requirements of target household members (WRA aged 15–49 years and children aged 6–59 months). Target household members were identified using the household roster. For households with more than one WRA or more than one child aged 6–59 months, we randomly selected one household member from that target group to include in the analyses. Households without a target household member were excluded from the analyses.

To assess dietary micronutrient adequacy, we calculated critical nutrient densities for each target household members as age- and sex-specific estimated average requirements (EARs) (or values along the distribution of requirements for iron) divided by age- and sex-specific energy requirements, multiplied by 1000. Vitamin A, folate, vitamin B12, and iron requirements were from the US Institute of Medicine.21, 22 Based on dietary patterns in Nigeria, we selected distributions of iron requirements corresponding to low (10%) iron bioavailability. Using published algorithms for children23 and adults24 to estimate absorbable zinc, we calculated fractional zinc absorption for each target household member as the ratio of absorbed zinc to total zinc. Then, we estimated dietary zinc requirements (and critical nutrient densities) by adjusting physiological zinc requirements for children25 and WRA26 by the estimated person-specific fractional zinc absorption. Assumed micronutrient and energy requirements are available in Table S1.

We used the EAR cut-point method to assess the adequacy of the household diet for meeting vitamin A, folate, vitamin B12, and zinc requirements and the full probability method for iron to account for non-normally distributed iron requirements among target household members.2, 27 We also estimated the risk of high intakes of vitamin A (in the form of preformed retinol), folic acid, iron, and zinc by comparing the nutrient density of the household diet to the critical upper density of the target household member, where critical upper densities were calculated as the age- and sex-specific tolerable upper intake level (UL) divided by the age- and sex-specific energy requirement, expressed per 1000 kcal (Table S2).

Note that because nutrient density is a measure of dietary quality assuming energy requirements are being met, classifications of micronutrient adequacy and high intakes were based on the assumption that target household members were also meeting their age- and sex-specific energy requirements.28 Also note that because the NLSS did not collect data on the pregnancy status of WRA, we estimated the adequacy of diets to meeting the needs of both pregnant and nonpregnant WRA by (1) first assessing adequacy as if all WRA were not pregnant and comparing the nutrient density of the household diet to the requirements of nonpregnant WRA; (2) assessing adequacy as if all WRA were pregnant and comparing the nutrient density of the household diet to the requirements of pregnant WRA; and (3) generating an overall prevalence of inadequacy among WRA as the weighted average prevalence of inadequacy for nonpregnant and pregnant WRA, where the weights were based on the most recent Demographic and Health Survey estimate of the percent of pregnant WRA in the population.29

Modeling the contribution of LSFF

For target household members, we estimated apparent consumption of potentially fortifiable (i.e., purchased) food vehicles that currently have national standards mandating their fortification with one or more of vitamin A, folic acid, vitamin B12, iron, or zinc. In Nigeria, these food vehicles are refined oil, sugar, margarine, wheat flour, and maize flour.30 We estimated the apparent consumption of these food vehicles by multiplying total household apparent daily consumption of each food vehicle by target household members’ AME ratios, calculated as his/her AME weight divided by the total number of AMEs in the household. Estimating individual apparent consumption using AME ratios implies that fortifiable foods were distributed within the household in proportion to age- and sex-specific energy requirements. Where relevant, total quantities consumed included consumption of both the food vehicle itself as well as fortifiable food equivalents of processed foods containing the food vehicle (e.g., wheat flour in bread).

The edible oils included in the NLSS food list were palm oil, groundnut oil, and “other oil and fat.” Based on information provided by Nigerian collaborators and the expert group that refined oils in Nigeria are generally considered vegetable oils without regard to the specific type of oil, we made zone-specific assumptions about the proportion of reported groundnut oil consumption that was actually groundnut oil (which was assumed to be refined at small scale and hence not fortifiable), while the remainder was assumed to be refined, fortifiable palm and soybean oils (Table S3). Because bouillon was not included in the NLSS food list, the proportion of households consuming bouillon in each geopolitical zone was assigned based on findings from the 2021 National Food Consumption and Micronutrient Survey,6 and we imputed daily household apparent bouillon consumption based on outlier-corrected, zone-specific median bouillon consumption per AME based on household-level bouillon consumption data collected on behalf of the Nigeria Bouillon Country Working Group in 2020. That is, the zone-specific median quantity of bouillon consumed per AME in the 2020 bouillon consumption dataset was assigned to all households in that zone, and total apparent quantity consumed by the household was calculated by multiplying that value by the total number of AMEs in the household.

We modeled the contribution of existing LSFF by adjusting the nutrient density of the household diet to account for additional micronutrients provided via LSFF, which, among the micronutrients being analyzed, included fortification of refined oil, sugar, margarine, wheat flour, and maize flour with vitamin A and wheat flour and maize flour additionally fortified with folic acid, vitamin B12, iron, and zinc (Table S4). We adjusted mandatory fortification levels to reflect the most recent information on the performance of the existing LSFF programs. Specifically, we adjusted fortification levels to account for the percent of each food vehicle that is fortifiable, the percent that is fortified to any extent, and the average fortification level at markets/households (Table 1, primary analysis). We multiplied the adjusted fortification levels by daily apparent household consumption of the food vehicle, recalculated household nutrient densities, and compared household nutrient densities with LSFF to critical nutrient densities.

TABLE 1. Fortification program modeling assumptions.
Vehicle Food vehicle that is industrially produced/fortifiable Fortifiable food vehicle fortified to any extent Average fortification level among fortified food as a percent of the standard after adjusting for expected losses from point of fortification to households
Value Source Value Source Value Source
Primary analysis Refined oil 80% Expert opinion1 31% Federal Government of Nigeria (FGN), & The International Institute of Tropical Agriculture (IITA), 2022 62% Federal Government of Nigeria (FGN), & The International Institute of Tropical Agriculture (IITA), 2022, adjusted for expected losses5
Sugar 100% Expert opinion2 74% Federal Government of Nigeria (FGN), & The International Institute of Tropical Agriculture (IITA), 2022 59% Federal Government of Nigeria (FGN), & The International Institute of Tropical Agriculture (IITA), 2022, adjusted for expected losses5
Margarine 100% Assumption 75% Assumption 100% Assumption
Wheat flour 96% Global Fortification Data Exchange, 2023 26% (vitamin A), 100% (folic acid, vitamin B12, iron, and zinc) Federal Government of Nigeria (FGN), & The International Institute of Tropical Agriculture (IITA), 2022 and expert opinion3 80% (vitamin A), 85% (iron), 74% (folic acid, vitamin B12, and zinc) Federal Government of Nigeria (FGN), & The International Institute of Tropical Agriculture (IITA), 2022 and expert opinion,3 adjusted for expected losses5
Maize flour 20% Global Fortification Data Exchange, 2023 26% (vitamin A), 100% (folic acid, vitamin B12, iron, and zinc) Expert opinion4 80% (vitamin A), 85% (iron), 74% (folic acid, vitamin B12, and zinc) Expert opinion,4 adjusted for expected losses5
Bouillon 100% Assumption 75% Modeling assumption 100% Modeling assumption
Sensitivity analysis Refined oil 80% Expert opinion1 75% Modeling assumption 100% Modeling assumption
Sugar 100% Expert opinion2 75% Modeling assumption 100% Modeling assumption
Margarine 100% Assumption 75% Assumption 100% Assumption
Wheat flour 96% Global Fortification Data Exchange, 2023 75% (vitamin A), 100% (folic acid, vitamin B12, iron, and zinc) Modeling assumption 100% Modeling assumption
Maize flour 20% Global Fortification Data Exchange, 2023 75% (vitamin A), 100% (folic acid, vitamin B12, iron, and zinc) Modeling assumption 100% Modeling assumption
Bouillon 100% Assumption 75% Modeling assumption 100% Modeling assumption
  • Note: Data come from Federal Government of Nigeria (FGN), & The International Institute of Tropical Agriculture (IITA). (2024). National food consumption and micronutrient survey 2021. Final report. Abuja and Ibadan, Nigeria: FGN and IITA; and Global Fortification Data Exchange. (2023). Dashboard: Country fortification. http://www.fortificationdata.org
  • aBased on the expert opinion of large-scale food fortification experts in Nigeria, as informed by data on refined oil in Nigeria collected by TechnoServe.
  • b Adjusted for expected micronutrient losses/degradation of 30% of vitamin A added to oil and sugar, 50% of vitamin A added to wheat flour or maize flour, and 20% of folic and vitamin B12 added to wheat flour or maize flour, based on expert opinion.
  • c Based on the expert opinion of large-scale food fortification experts in Nigeria.
  • d Parameter values for folic acid and vitamin B12 informed by the expert opinion of large-scale food fortification experts in Nigeria, as informed by testing of B vitamins in wheat flour conducted by TechnoServe.
  • e Parameter values for maize flour assumed to be the same as wheat flour, as informed by the expert opinion of large-scale food fortification experts in Nigeria.

We then modeled the potential additional contribution of adding bouillon fortification to existing LSFF. We evaluated the additional contributions over a range of possible fortification levels (40–250 µg vitamin A per gram bouillon, 20–120 µg folic acid per gram bouillon, 0.2–2 µg vitamin B12 per gram bouillon, 0.6–5 mg iron per gram bouillon, and 0.6–5 mg zinc per gram bouillon) that were selected to allow for consideration of alternative micronutrient concentrations in fortified bouillon that might be chosen to balance reductions in micronutrient inadequacy with risk of high intakes. For modeling purposes and to allow for the possibility of imperfect compliance, we assumed that 75% of bouillon would be fortified to the specified level (i.e., we multiplied each fortification level by 0.75 to arrive at an average fortification level if 75% of bouillon were fortified). Then, we multiplied daily apparent bouillon consumption by each adjusted fortification level and recalculated the nutrient density of the household diet, prevalence of inadequacy, and, where relevant, prevalence of high intakes with both existing LSFF and bouillon fortification. We assumed that, without the addition of compounds to enhance absorption, 2% of iron added to bouillon via fortification would be absorbed.31, 32

Apparent micronutrient adequacy and consumption of fortifiable food were estimated at the national level, by quintiles of household SES (constructed based on annual per capita household expenditures reported in the NLSS data), and by urban and rural residence. We did not model the contribution of micronutrient supplementation because data on consumption of supplements were not collected as part of the NLSS. Likewise, we did not account for voluntary fortification, as there are insufficient data on the extent of voluntary fortification and levels of micronutrients voluntarily added to some food products in Nigeria and insufficient specificity of potentially voluntarily fortified foods in the NLSS food list. Finally, we were unable to incorporate the contribution of breastmilk to meeting the micronutrient requirements of breastfed children since breastfeeding status was not collected in the NLS. As such, the modeling reflects the adequacy of diets without breastmilk. All estimates account for survey weights. Our comparisons of consumption of fortifiable food vehicles and the prevalence of inadequacy across food vehicles and population subgroups were qualitative.

Zonal estimates and sensitivity analyses

In addition to assessing the additional contribution of bouillon by household SES and urban and rural residence, we also modeled an additional scenario, assessed at the level of geopolitical zone, in which bouillon fortification levels were selected in order to meet 30% of the Codex nutrient reference values (NRVs), calculated assuming 2.5 g of bouillon consumption per day among adults (per gram bouillon: 96 µg vitamin A, 28.8 µg folic acid, 0.288 µg vitamin B12, 2.64 mg iron, and 1.68 mg zinc per gram of bouillon) (Table S4). These fortification levels were chosen because they represent levels that may be commercially feasible for voluntary fortification and, based on Codex requirements, could be labeled as “high in” these micronutrients because they provide at least 30% of Codex NRVs. In this scenario, modeled bouillon fortification levels were also adjusted to account for the assumption that 75% of bouillon would be fortified to these levels.

Given the potential for improvements in compliance with existing LSFF standards if Nigeria invested in enhanced monitoring and enforcement, we estimated the through a sensitivity analysis the potential additional contribution of fortified bouillon to meeting micronutrient requirements and, where relevant, risk of high intakes, if compliance with national standards improved. Specifically, for the improved compliance scenario, we assumed 75% of the fortifiable food vehicle was fortified to the standard (Table 1, sensitivity analysis). Note that in cases where greater than 75% of the food vehicle was fortified under the current compliance scenario, the value under current compliance was maintained.

As previously described, the NLSS did not collect data on bouillon consumption, so we relied on an alternative data source to model the potential impacts of bouillon fortification. As such, these estimates of bouillon consumption are a source of uncertainty in our modeling. The final report of Nigeria's NFCMS was recently released and includes summary information on bouillon consumption among WRA and children based on 24-hour dietary recall data.6 As a second sensitivity analysis, we replaced our primary estimates of apparent bouillon consumption with imputed estimates based on zone-specific median bouillon consumption per 1000 kcal as summarized in the NFCMS report (see Supporting Methods for further details). We then re-estimated the potential contributions of, and risk of high intakes associated with, multiply fortified bouillon and assessed the extent to which key policy messages emerging from this work might change relative to the results of the primary analysis.

RESULTS

Apparent consumption of fortifiable foods and condiments

For most foods with mandatory fortification standards in Nigeria, households in lower SES quintiles and households in rural areas were less likely to report consumption in the 7 days preceding the NLSS than wealthier and urban households (Table 2). Almost 80% of households reported consuming refined oil or food products containing refined oil, ranging from 68% of households in the lowest SES quintile up to 90% among households in the highest SES quintile. Reported consumption of refined oil was 12 percentage points higher among urban households compared to rural households. Median apparent quantities consumed were likewise higher among wealthier and urban households. Similarly, almost 80% of households reported consuming sugar purchased for use at home (note that sugar used in industrially processed food products and beverages is not covered under Nigeria's sugar fortification standard), with a higher proportion of households in higher SES quintiles and urban households reporting consuming sugar. However, among sugar consumers, median quantities apparently consumed were higher among households in lower SES quintiles and among rural, compared to urban, households. Nationally, only 4% of households reported consuming margarine, with almost all consumption concentrated among wealthy, urban households.

TABLE 2. Apparent consumption of refined oil, sugar, margarine, wheat flour, maize flour, and bouillon in the past 7 days.
National SES 1a SES 2 SES 3 SES 4 SES 5 Urban Rural
Refined oil Households consuming1 (%) 79% 68% 69% 73% 84% 90% 86% 74%
Median apparent consumption among consumers, grams/day WRA 7.1 5.5 5.9 5.9 7.2 9.7 8.9 6.1
Children2 3.4 2.7 2.9 3.0 3.5 4.9 4.2 3.0
Sugar Households consuming1 (%) 79% 72% 79% 80% 80% 82% 83% 77%
Median apparent consumption among consumers, grams/day WRA 6.1 8.2 7.7 6.3 5.2 5.1 5.8 6.3
Children 3.3 4.0 3.9 3.5 2.8 2.7 3.2 3.4
Margarine Households consuming1 (%) 4% 0% 1% 1% 4% 11% 8% 2%
Median apparent consumption among consumers, grams/day WRA 2.9 6.4 2.1 2.1 3.4 2.8 2.8 3.0
Children 1.6 2.8 1.0 0.9 1.7 1.5 1.5 1.7
Wheat flour Households consuming1 (%) 77% 48% 60% 76% 87% 95% 89% 69%
Median apparent consumption among consumers, grams/day WRA 31.2 23.4 25.0 25.7 30.9 39.7 38.3 26.7
Children 14.9 12.0 12.5 12.5 15.3 19.7 18.6 13.0
Maize flour Households consuming1 (%) 17% 9% 11% 14% 20% 24% 27% 11%
Median apparent consumption among consumers, grams/day WRA 50.9 74.6 74.0 56.8 52.5 43.8 49.6 54.7
Children 27.1 34.6 39.1 28.2 27.3 21.5 26.6 27.9
Bouillon4 Households consuming1 (%) 98% 98% 99% 99% 98% 98% 98% 98%
Median apparent consumption among consumers, grams/day WRA 3.7 3.8 3.8 3.8 3.7 3.6 3.6 3.8
Children 1.9 2.0 2.0 2.0 1.8 1.6 1.6 2.0
  • Abbreviations: SES, socioeconomic status; WRA, women of reproductive age.
  • a SES wealth quintiles based on annual per capita household expenditures. SES 1 is poorest/lowest SES; SES 5 is wealthiest/highest SES.
  • b Households with a WRA reporting any consumption of the food vehicle (or processed food containing the food vehicle), from household purchases, during the recall period categorized as consuming the food vehicle.
  • c Children 6−59 months of age.
  • d Because bouillon consumption was not collected in the Nigeria Living Standards Survey, bouillon consumption estimates are imputed based on outlier-corrected, zone-specific median bouillon consumption per AME based on household-level bouillon consumption data collected on behalf of the Nigeria Bouillon Country Working Group in 2020.

Wheat flour, and products containing wheat flour such as bread, were apparently consumed by 77% of households, with less than half of households in the lowest SES quintile reporting consumption and 95% of households in the highest quintile reporting consumption. Among consumers, median apparent quantities consumed were likewise higher among wealthier households. Consumption of purchased maize flour was more commonly reported among urban than rural households and households of higher SES, but unlike consumption of wheat flour, median apparent quantities consumed were larger among households of low SES and among rural households. Finally, based on imputed bouillon consumption estimates, essentially all (98%) of households apparently consumed bouillon, with similar median apparent consumption quantities across SES quintiles and in urban and rural areas (3.6–3.8 grams per WRA per day and 1.6–2.0 grams per child per day).

Prevalence of apparent inadequacy and modeled contribution of bouillon fortification

Accounting for existing LSFF programs at current levels of compliance (Table 1, primary analysis), household diets were inadequate to meet the vitamin A requirements of 20% of WRA and 21% of children 6–59 months of age (bouillon fortification level “0” in Figure 1 and Table S5). Note that from here forward, if not explicitly stated, inadequacy refers to apparent inadequacy. Vitamin A inadequacy was around eight times higher among WRA and children living in households in the lowest SES quintile compared to the highest SES quintile and was more than twice as high in rural areas compared to urban areas. The addition of vitamin A–fortified bouillon at 40 µg per gram of bouillon was predicted to reduce the national prevalence of inadequacy among WRA and children by approximately half (to 10% and 11%, respectively), with higher fortification levels reducing the national prevalence of inadequacy to 5% or less. Subnationally, vitamin A–fortified bouillon was predicted to have the largest impact (i.e., the highest percentage point reduction in inadequacy) among WRA and children in households in the lower SES quintiles and in rural households. However, at modeled fortification levels of 200 µg vitamin A per gram bouillon, ∼8% of children, nationally, were predicted to be at risk of high vitamin A intake, reaching up to 10% of children among some subgroups (Figure 1, Figure S1, and Table S6).

Details are in the caption following the image
Prevalence of apparent vitamin A inadequacy (top) or risk of high intakes (bottom), nationally and by socioeconomic status (SES), with bouillon fortification added to existing fortification at different bouillon fortification levels. Note that the modeled bouillon fortification levels (x-axis) are not always evenly spaced. SES quintiles based on annual per capita household expenditures. SES 1 is poorest/lowest quintile of SES; SES 5 is wealthiest/highest quintile of SES.

The prevalence of folate inadequacy, accounting for the existing wheat flour and maize flour fortification programs, was 14% among WRA (ranging from 8% to 19% across household SES and from 9% to 17% in urban and rural areas) and 4% among children (ranging from 3% to 6% across household SES and from 4% to 5% in urban and rural areas) (Figure 2, Figure S2, and Table S7). Fortifying bouillon with folic acid was predicted to virtually eliminate inadequacy among children at 20 µg folic acid per gram bouillon and among WRA at 40–60 µg per gram bouillon. Nationally at 60 µg per gram bouillon, 1% of WRA and children would be at risk of high folic acid intakes (Table S8). The risk of high folic acid intakes among children was predicted to exceed 10% nationally at 100 µg per gram bouillon.

Details are in the caption following the image
Prevalence of apparent folate inadequacy (top) or risk of high folic acid intakes (bottom), nationally and by socioeconomic status (SES), with bouillon fortification added to existing fortification at different bouillon fortification levels. SES quintiles based on annual per capita household expenditures. SES 1 is poorest/lowest quintile of SES; SES 5 is wealthiest/highest quintile of SES.

Accounting for existing wheat flour and maize flour fortification, household diets were inadequate to meet the vitamin B12 requirements of 42% of WRA and 39% of children (Figure 3 and Table S9). Subnationally, the prevalence of vitamin B12 inadequacy reached 75% among WRA and 68% among children in the lowest SES quintile and was more than 20 percentage points higher among WRA and children in rural households compared to urban households (Figure S3). Fortifying bouillon with 1.2 µg per gram bouillon was predicted to reduce the national prevalence of inadequacy to 1% among both WRA and children and would reduce inadequacy in the lowest SES quintile by 71 percentage points among WRA (bringing inadequacy down to 4%) and by 66 percentage points among children (bringing inadequacy to 2%). Reductions in vitamin B12 inadequacy were predicted to plateau at higher modeled fortification levels.

Details are in the caption following the image
Prevalence of apparent vitamin B12 inadequacy, nationally and by socioeconomic status (SES), with bouillon fortification added to existing fortification at different bouillon fortification levels. Note that the modeled bouillon fortification levels (x-axis) are not always evenly spaced. SES quintiles based on annual per capita household expenditures. SES 1 is poorest/lowest quintile of SES; SES 5 is wealthiest/highest quintile of SES.

The national prevalence of iron inadequacy, accounting for existing LSFF programs, was estimated to be 24% among WRA and 12% among children with little subnational variation (Figure 4, Figure S4, and Table S10). Predicted reductions in the prevalence of iron inadequacy did not exceed 7 percentage points nationally, even at the highest modeled fortification level (5 mg per gram bouillon). Meanwhile, with bouillon fortified at 3 mg per gram, over 5% of WRA would be at risk of high iron intakes, reaching up to 14% among women in households in the lowest SES quintile (Table S11). At 5 mg per gram, over 20% of WRA would be a risk of high iron intakes.

Details are in the caption following the image
Prevalence of apparent iron inadequacy (top) or risk of high intakes (bottom), nationally and by socioeconomic status (SES), with bouillon fortification added to existing fortification at different bouillon fortification levels. Note that the modeled bouillon fortification levels (x-axis) are not always evenly spaced. SES quintiles based on annual per capita household expenditures. SES 1 is poorest/lowest quintile of SES; SES 5 is wealthiest/highest quintile of SES.

With wheat flour and maize flour fortification, the national prevalence of zinc inadequacy was 31% among WRA and 38% among children (Figure 5 and Table S12). By household SES, inadequacy among WRA ranged from 20% in the highest SES to 46% in the lowest SES and from 36% to 42% among children. Inadequacy was also higher among WRA and children residing in rural areas compared to urban areas (Figure S5). Zinc-fortified bouillon was predicted to reduce the national prevalence of inadequacy by 7–20 percentage points among WRA and by 6–19 percentage points among children, depending on the modeled fortification level. Among WRA, predicted reductions were largest among poorer and rural populations, while among children, predicted reductions were similar across subpopulations. Without bouillon fortification, 13% of children were estimated to be at risk of high zinc intakes, climbing to between 32% and 96% depending on the modeled bouillon fortification level (Table S13). The risk of high zinc intakes among WRA also exceeded 10% at 5 mg zinc per gram of bouillon.

Details are in the caption following the image
Prevalence of apparent zinc inadequacy (top) or risk of high intakes (bottom), nationally and by socioeconomic status (SES), with bouillon fortification added to existing fortification at different bouillon fortification levels. Note that the modeled bouillon fortification levels (x-axis) are not always evenly spaced. SES quintiles based on annual per capita household expenditures. SES 1 is poorest/lowest quintile of SES; SES 5 is wealthiest/highest quintile of SES.

Modeled contribution of bouillon fortification at 30% of Codex by geopolitical zone

Estimates of the prevalence of micronutrient inadequacy by geopolitical zone in Nigeria without and with bouillon fortified at 30% of the Codex NRVs are presented in Figure 6 (WRA), Figure 7 (children), and Tables S14S18. Accounting for the contribution of existing LSFF at current levels of compliance, the prevalence of vitamin A inadequacy among WRA ranged from 5% in the South South and South West zones to 43% in the North West. Accounting for the added contribution of bouillon fortified with 96 µg vitamin A per gram of bouillon, vitamin A inadequacy was eliminated in the South South and South West zones and declined to 13% in the North West Zone. The subnational patterns of vitamin A inadequacy among children were very similar to those among WRA.

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Prevalence of vitamin A, folate, vitamin B12, iron, and zinc inadequacy among women of reproductive age without (left panels) and with (right panels) bouillon fortification modeled to meet 30% of the Codex nutrient reference values, calculated assuming 2.5 g of bouillon consumption per day among adults (per gram bouillon: 96 µg vitamin A, 28.8 µg folic acid, 0.288 µg vitamin B12, 2.64 mg iron, and 1.68 mg zinc). See Tables S14S18 for point estimates by geopolitical zone.
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Prevalence of vitamin A, folate, vitamin B12, iron, and zinc inadequacy among children 6–59 months of age without (left panels) and with (right panels) bouillon fortification modeled to meet 30% of the Codex nutrient reference values, calculated assuming 2.5 g of bouillon consumption per day among adults (per gram bouillon: 96 µg vitamin A, 28.8 µg folic acid, 0.288 µg vitamin B12, 2.64 mg iron, and 1.68 mg zinc). See Tables S14S18 for point estimates by geopolitical zone.

Accounting for existing LSFF, folate inadequacy among WRA ranged from 7% in the South West Zone to 20% in the South South. The addition of bouillon fortified with 28.8 µg folic acid per gram of bouillon was predicted to reduce the prevalence of inadequacy to 1% of WRA across all geopolitical zones. Among children, the prevalence of folate inadequacy was between 3% and 6% without bouillon fortification and was predicted to drop to 0% in all zones with bouillon fortification.

With existing LSFF, vitamin B12 inadequacy among WRA ranged from 17% in the South South Zone to 80% in the North West, and bouillon fortified with 0.288 µg vitamin B12 per gram of bouillon was predicted to reduce inadequacy to between 4% (South South) and 56% (North West). The subnational patterns were similar among children.

Iron inadequacy with existing LSFF was similar across geopolitical zones among WRA, ranging from 23% to 26%. The addition of bouillon fortified with 2.64 mg iron per gram of bouillon was predicted to reduce iron inadequacy among WRA to 18%–22%. Among children, iron inadequacy without bouillon fortification ranged from 8% (North West Zone) to 17% (South West Zone) and declined to between 6% (North West) and 14% (South West Zone) with bouillon fortification. Finally, accounting for existing fortification, zinc inadequacy among WRA was lowest in the South East Zone (11%) and highest in the North West Zone (52%). Adding bouillon fortified with 1.68 mg zinc per gram of bouillon was predicted to reduce inadequacy to between 6% and 34%. Similarly, zinc inadequacy among children ranged from 25% (South East) to 47% (North West) without bouillon fortification and was predicted to decline to between 11% and 35%, respectively, with bouillon fortification.

Sensitivity analyses

If compliance with Nigeria's national LSFF standards improved (Table 1, sensitivity analysis), the predicted prevalence of vitamin A inadequacy without bouillon fortification was 17% among both WRA and children, although the prevalence would still exceed 40% among WRA and children in households in the lowest SES quintile (bouillon fortification level “0” in Figure S6). Both the predicted reductions in vitamin A inadequacy and the risk of high vitamin A intakes across the range of modeled bouillon fortification levels were similar to the current compliance scenario (within several percentage points).

With improved compliance with the wheat flour and maize flour fortification standards, the national prevalence of folate inadequacy would be 11% among WRA and 3% among children (Figure S7). With the addition of bouillon fortification at 40 µg folic acid per gram bouillon, folate inadequacy was predicted to be virtually eliminated among both WRA and children, while corresponding risks of high intake would not exceed 1%. Because estimates of the current compliance with the wheat flour and maize flour standards for vitamin B12, iron, and zinc are high, the predicted potential additional contribution of bouillon fortification, as well as the risk of high intakes of iron and zinc, were very similar (within a few percentage points) to estimates at current compliance (Figures S8S10).

Results based on bouillon consumption estimates presented in the final report of the NFCMS are reported in Table S18 and Figures S16S20). In agreement with the usual bouillon consumption reported in the NFCMS data, median apparent bouillon consumption nationally, and especially among consumers in lower SES quintiles, was higher compared to our primary estimates (Table S19). As a result, predicted reductions in the prevalence of micronutrient inadequacies among WRA and children as a result of bouillon fortification, accounting for existing fortification at estimated current compliance with national standards, were generally larger at lower fortification levels compared to our primary estimates, especially among households in lower SES quintiles (the exception was iron for which predicted reductions were very similar to our primary estimates). At the same time, for vitamin A, folic acid, iron, and zinc, a higher proportion of children and/or WRA were predicted to exceed the UL threshold at a lower fortification level compared to our primary estimates.

DISCUSSION

Nigeria currently mandates the fortification of multiple food vehicles with multiple micronutrients. Accounting for the contribution of these existing programs at current levels of compliance, the national prevalence of apparent vitamin A, folate, and iron inadequacy among both WRA and children was estimated to be less than 25%, while the national prevalence of vitamin B12 (42% among WRA and 39% among children) and zinc inadequacy (31% among WRA and 38% among children) were higher. However, for all micronutrients except iron, there was substantial subnational variation in the prevalence of inadequacy with existing LSFF, with generally much higher prevalence of inadequacy among WRA and children living in poorer and rural households. Moreover, the 2021 NFCMS revealed high rates of micronutrient deficiencies, especially vitamin A and zinc among children and folate and zinc among WRA. Because bouillon in Nigeria is consumed by almost all households, based on two different sources of data on bouillon consumption and varying assumptions about the performance of existing LSFF, our modeling results consistently showed that bouillon fortification has the potential to bring about substantial reductions in the prevalence of vitamin A, folate, vitamin B12, and zinc inadequacy among poor and rural populations and, depending on the specific fortification level, create more equity in the micronutrient adequacy of diets in Nigeria.

However, given that there are already a number of LSFF programs in place in Nigeria, coupled with high quantities of bouillon consumption relative to some other countries in the region,33, 34 the design of a bouillon fortification program would require careful planning to identify a fortification standard that balances reductions in inadequacy with risk of high intakes.35 In our primary analysis, we found that for vitamin A and folic acid, there were bouillon fortification levels for which the added benefit of higher fortification levels plateaued, which roughly coincided with fortification levels at which risk of high intakes among children reached levels of 5% or higher. In the sensitivity analysis in which bouillon consumption was estimated based on the NFCMS report, these plateaus occurred at lower fortification levels, and the proportions of children or WRA at risk of high intakes were substantially larger at lower fortification levels, exceeding 10% above the UL among children nationally at 160 µg/g vitamin A, 80 µg/g folic acid, and 0.6 mg/g zinc and among WRA at 3 mg/g iron. Both sets of results suggest that a bouillon fortification program with these micronutrients could be designed to maximize benefits while also maintaining a low risk of high intakes, although for some micronutrients, identifying a single fortification level might require tradeoffs between meeting the requirements of some target populations and maintaining a low risk of high intakes among other population groups. A similar set of modeling exercises using the NFCMS 24-hour dietary recall data, when available, would be valuable to help identify these fortification levels.

For vitamin B12, although there is no tolerable upper intake level, our modeling results did suggest that based on both sources of bouillon consumption, there are bouillon fortification levels beyond which any additional benefits plateau because dietary adequacy is achieved for virtually everyone who consumes bouillon. For zinc, the prevalence of high intakes among children was estimated at 13% without bouillon fortification and jumped above 30% at the lowest modeled level of zinc-fortified bouillon (over 40% in the sensitivity analysis based on NFCMS bouillon consumption estimates), though at this fortification level, the prevalence of zinc inadequacy was still 32% among children and 25% among WRA (or 30% and 21% based on NFCMS bouillon consumption estimates). Tolerable upper zinc intake levels for children, which were established based on extrapolation from results of studies in adults, have recently been criticized as being set below levels of observed usual dietary zinc intake that show no adverse effects and at levels so near recommended intake levels that designing zinc intervention programs in contexts of high zinc deficiency is difficult.36 As such, including zinc in a bouillon fortification program in Nigeria would also require careful consideration of the potential nutrition benefits relative to the potential risk of high intakes. Finally, the predicted potential reductions in iron inadequacy were modest among both WRA and children, and based on both sets of bouillon consumption estimates, driven largely by low expected iron absorption in fortified bouillon.31 This, combined with the predicted risk of high iron intakes >5% among WRA at fortification levels of 3 mg iron per gram bouillon, suggests that unless iron absorption in fortified bouillon can be improved, other strategies might be required to help meet iron requirements among individuals with inadequate intake.

With regard to estimating the need for interventions, it is important to note that although our analysis of household food consumption data suggested a low risk of dietary folate inadequacy, the 2021 biomarker data showed extremely high rates (>95%) of RBC folate deficiency among WRA.6 The thresholds for dietary folate adequacy used in our study were established based on indicators of adequate folate status but not specifically on neural tube defect (NTD) prevention.21 Available information suggests that NTD birth prevalence is very high in the sub-Saharan African region.37, 38 This suggests that folic acid interventions could reduce the burden of NTDs in Nigeria; modeled estimates of NTD prevention are reported elsewhere.39

Analysis of HCES data is playing an increasingly common role in modeling the need for and impacts of LSFF and other micronutrient interventions.16, 40 While the use of HCES data does help fill a crucial gap in the evidence needed to inform the design or redesign of LSFF programs, its use comes with some limitations. First, estimates of the prevalence of dietary micronutrient inadequacy and the modeled contribution of LSFF to meeting micronutrient requirements are based on the assumption that food is distributed within the household in proportion to age- and sex-specific energy requirements. Evidence from previous studies assessing the validity of this assumption by comparing HCES-based to individual-level food consumption data has been mixed, although the accuracy of the AME method to estimate food consumption and/or micronutrient intake among young children seems to be particularly tenuous.41-44 Another limitation stems from the likelihood of error in reported household-level food consumption as a result of recall error and inadequate accounting for foods consumed away from home.16 In an effort to account for some of this error, we assessed the adequacy of diets using the energy-adjusted nutrient density metric. This methodological approach has been adopted in several other studies using HCES data,45-47 and in one study that compared this approach to estimates of dietary intake and/or adequacy based on 24-hour dietary recall data, the nutrient density method was generally found to generate similar estimates of nutrient densities and the prevalence of nutrient inadequacies,47 but more comparative work in a broader range of country contexts is needed. And while nutrient density can help correct for measurement error in food consumption that is similar to the reported household diet, it relies on the assumption that household members are meeting their energy requirements, and it cannot help account for error in reporting of foods that vary considerably in nutrient contents from the typical household diet, such as foods consumed away from home. Finally, although not common to all HCES data, another important limitation faced in this analysis was that the Nigeria Living Standard Survey did not collect data on household bouillon consumption, so our modeling of the potential contribution of fortified bouillon was based on imputed estimates of bouillon consumption. Although we conducted sensitivity analysis around this source of uncertainty using the recently released final report of the NFCMS, neither source of data reflect actual bouillon consumption at the household level. Once the 24-hour dietary recall data collected during the 2021 NFCMS are publicly available, replicating the HCES-based modeling with individual-level data could help overcome many of these limitations and add to the evidence base on the potential for bouillon fortification to help fill dietary gaps in Nigeria.

In addition to the modeling evidence presented here, discussions around adding bouillon fortification to Nigeria's existing LSFF programs should also consider consumer acceptance, technical feasibility, cost, affordability among all stakeholder groups, and cost-effectiveness. Considerations around cost, affordability, and cost-effectiveness are presented in Vosti et al. (under review) and Vosti et al. (in preparation). Consumer acceptance of nonproprietary bouillon formulation fortified with vitamin A, folic acid, vitamin B12, iron, and zinc at 45%–125% of Codex NRVs in 2.5 grams of bouillon has been established in Northern Ghana,11 and the bouillon cubes currently being used in the randomized trial in Northern Ghana contain 200 µg vitamin A, 80 µg folic acid, 1.2 µg vitamin B12, 4 mg iron, and 3 mg zinc per gram of bouillon.12, 48 However, to our knowledge, higher fortification levels have not been tested for technical feasibility and consumer acceptability. In addition, fortification levels that are technically feasible for research may be higher than what is feasible in a commercial context due to differences between specific bouillon formulations (e.g., specific spices and other ingredients) and especially the typical storage conditions and duration in research versus commercial settings (e.g., exposure to heat and humidity). Work to further understand the technical feasibility of commercial formulations is underway. And finally, discussions around bouillon fortification in Nigeria have raised some concerns about sodium intake and noncommunicable diseases. Studies elsewhere in West Africa have suggested that the contribution of bouillon to total sodium intake ranges from 14% to 25%49, 50 and is much lower than the amount consumed as discretionary salt at home. Research is currently underway to estimate sodium exposure and the proportion contributed by bouillon in Nigeria (Faith Ishaya, personal communication, 2024) to inform efforts to reduce sodium exposure and hypertension risk. While there is no evidence that bouillon fortification would increase bouillon (and thus salt) consumption, if sodium reduction efforts did reduce bouillon intake, it would be important to collect information on changes in consumption so that micronutrient fortification levels could be adjusted.

Nigeria is developing a Code of Practice for voluntary bouillon fortification. The evidence presented in the paper, alongside evidence on cost (Vosti et al., under review) and cost-effectiveness (Vosti et al., in preparation), provide important input into that decision-making process. Our modeling results suggest that bouillon fortification could virtually eliminate dietary inadequacies of vitamin A, folate, and vitamin B12 while also improving equity in the micronutrient adequacy of diets in the country. Zinc-fortified bouillon could also improve the zinc adequacy of diets, but establishing zinc fortification levels will require considering tradeoffs in potential nutrition benefits versus potential risk of high zinc intakes.

AUTHOR CONTRIBUTIONS

K.P.A., S.A.V., and R.E.-S. designed the study and developed the methods. K.P.A., E.B., and F.I. made the food composition table matches. K.P.A. analyzed and modeled the data and wrote the first draft of the manuscript. All authors contributed to the data interpretation and revisions of the manuscript, and read and approved the final manuscript.

ACKNOWLEDGMENTS

This work was supported, in part, by the Bill & Melinda Gates Foundation via a grant to Helen Keller International [INV-007916]. Under the grant conditions of the Foundation, a Creative Commons Attribution 4.0 Generic License has already been assigned to the Author Accepted Manuscript version that might arise from this submission. The authors gratefully acknowledge the National Bureau of Statistics (NBS) in Nigeria and the World Bank for the household survey data.

    COMPETING INTERESTS

    All authors have no competing interests to declare.

    PEER REVIEW

    The peer review history for this article is available at: https://publons.com/publon/10.1111/nyas.15207.