Global Food Security 12 (2017) 49–58

Contents lists available at ScienceDirect

Global Food Security

journal homepage: www.elsevier.com/locate/gfs

Improving nutrition through biofortification: A review of evidence from MARK

HarvestPlus, 2003 through 2016
⁎
Howarth E. Bouis , Amy Saltzman
International Food Policy Research Institute, Washington, DC, United States

A BS T RAC T

Biofortification is a feasible and cost-effective means of delivering micronutrients to populations that may have
limited access to diverse diets and other micronutrient interventions. Since 2003, HarvestPlus and its partners
have demonstrated that this agriculture-based method of addressing micronutrient deficiency through plant
breeding works. More than 20 million people in farm households in developing countries are now growing and
consuming biofortified crops. This review summarizes key evidence and discusses delivery experiences, as well
as farmer and consumer adoption. Given the strength of the evidence, attention should now shift to an action-
oriented agenda for scaling biofortification to improve nutrition globally. To reach one billion people by 2030,
there are three key challenges: 1) mainstreaming biofortified traits into public plant breeding programs; 2)
building consumer demand; and 3) integrating biofortification into public and private policies, programs, and
investments. While many building blocks are in place, institutional leadership is needed to continue to drive
towards this ambitious goal.

World Food Prize Winners 2016

The World Food Prize is the foremost international award that honours outstanding individuals who have made vital contributions to
improving the quality, quantity, or availability of food in the world (https://www.worldfoodprize.org/). This paper, authored by 2016 World
Food Prize winner, Howarth Bouis and his colleague Amy Saltzman, both of the International Food Policy Research Institute, describes work
under the HarvestPlus program on the global level on biofortification of staple foods to overcome micronutrient deficiencies. A companion paper
in this issue by fellow 2016 winners, Jan Low, Maria Andrade, and Robert Mwanga of the International Potato Center describes work on
biofortified orange-fleshed sweet potatoes in Africa.

1. Justification for biofortification and nutrition. This article extends the previously published theoretical
framework for biofortification (Bouis et al., 2011b) and supporting
1.1. Introduction evidence (Saltzman et al., 2013, 2015) to discuss delivery experiences
and an action-oriented agenda for scaling biofortification to improve
Biofortification is a process of increasing the density of vitamins nutrition globally. Delivery experiences are discussed from the per-
and minerals in a crop through plant breeding, transgenic techniques, spective of HarvestPlus, which leads a global interdisciplinary alliance
or agronomic practices. Biofortified staple crops, when consumed of research institutions and implementing agencies in the biofortifica-
regularly, will generate measureable improvements in human health tion effort.1 The evidence and building blocks for scale are in place;

⁎
Corresponding author.
E-mail address: h.bouis@cgiar.org (H.E. Bouis).
1
HarvestPlus is one component of the CGIAR Research Program on Agriculture for Nutrition and Health (A4NH). The CGIAR is a global agriculture research partnership for a food
secure future. Its science is carried out by its 15 research centers in collaboration with hundreds of partner organizations. The HarvestPlus program is administered under a joint venture
agreement by two of these centers, the International Center for Tropical Agriculture (CIAT) and the International Food Policy Research Institute (IFPRI). The primary role of
HarvestPlus is to catalyze, coordinate, and conduct oversight over a complex set of interdisciplinary activities by a large number of partner institutions, that lead to reductions in mineral
and vitamin deficiencies through biofortification. HarvestPlus has invested more than $300 million in biofortification activities during 2003–2016. Principal investors in HarvestPlus
currently include the UK Government, Bill & Melinda Gates Foundation, the US Government's Feed the Future initiative, the EU Commission, and donors to A4NH.

http://dx.doi.org/10.1016/j.gfs.2017.01.009
Received 18 January 2017; Received in revised form 25 January 2017; Accepted 27 January 2017
2211-9124/ © 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).
H.E. Bouis, A. Saltzman Global Food Security 12 (2017) 49–58

with sufficient institutional leadership, biofortification is poised to (Saltzman et al., 2013; Lividini and Fiedler, 2015; Asare-Marfo et al.,
reach one billion people by 2030. 2013; de Brauw et al., 2015).

1.2. Comparative advantages 2. Nutritional bioavailability and efficacy evidence

Micronutrient deficiencies afflict more than two billion individuals, Biofortified crops can improve human nutrition. To develop evi-
or one in three people, globally (FAO et al., 2015). Such deficiencies dence of nutritional efficacy, nutritionists first measure retention of
occur when intake and absorption of vitamins and minerals are too low micronutrients in crops under typical processing, storage, and cooking
to sustain good health and development. Over the last 50 years, practices to be sure that sufficient levels of vitamins and minerals will
agricultural research for developing countries has increased production remain in foods that target populations typically eat (for summary
and availability of calorically dense staple crops, but the production of results, see De Moura et al. (2015)). Genotypic differences in retention
micronutrient-rich non-staples, such as vegetables, pulses and animal and concentrations of compounds that inhibit or enhance micronu-
products, has not increased in equal measure. Non-staple food prices trient bioavailability are considered. Nutritionists also study the degree
have increased steadily and substantially, making it more and difficult to which nutrients bred into crops are absorbed, first by using models,
for the poor to afford dietary quality (Bouis et al., 2011a). In the long- then by direct study in humans in controlled experiments. Absorption
term, increasing the production of micronutrient-rich foods and is a prerequisite to demonstrating that biofortified crops can improve
improving dietary diversity will substantially reduce micronutrient micronutrient status, but the change in status with long-term intake of
deficiencies. In the near term, consuming biofortified crops can help biofortified foods must be measured directly. Therefore, randomized
address micronutrient deficiencies by increasing the daily adequacy of controlled efficacy trials are used to demonstrate the impact of
micronutrient intakes among individuals throughout the lifecycle biofortified crops on micronutrient status and functional indicators of
(Bouis et al., 2011b). micronutrient status (i.e. visual adaptation to darkness for vitamin A
No single intervention will alleviate micronutrient deficiencies, and crops, physical activity and cognition tests for iron crops, etc.).
biofortification complements existing interventions, such as supple- Highlights are discussed below, and further detail is summarized in
mentation and industrial food fortification. Biofortification, however, De Moura et al. (2014).
has two key comparative advantages: its long-term cost-effectiveness
and its ability to reach underserved, rural populations. Unlike the 2.1. Iron crops
continual financial outlays required for supplementation and commer-
cial fortification programs, an upfront investment in plant breeding Iron nutrition research has demonstrated the efficacy of biofortified
yields micronutrient-rich biofortified planting material for farmers to iron bean and iron pearl millet in improving the nutritional status of
grow at virtually zero marginal cost. Once developed, nutritionally target populations. In Rwanda, iron-depleted university women
improved crops can be evaluated and adapted to new environments showed a significant increase in hemoglobin and total body iron after
and geographies, multiplying the benefits of the initial investment. consuming biofortified beans for 4.5 months (Haas et al., 2017). The
Once the micronutrient trait has been mainstreamed into the core efficacy of iron pearl millet was evaluated in secondary school children
breeding objectives of national and international crop development from Maharashtra, India. A significant improvement in serum ferritin
programs, recurrent expenditures by agriculture research institutes for and total body iron was observed in iron-deficient adolescent boys and
monitoring and maintenance are minimal. girls after consuming biofortified pearl millet flat bread twice daily for
Biofortified crops are also a feasible means of reaching rural four months. The prevalence of iron deficiency was reduced signifi-
populations who may have limited access to diverse diets or other cantly in the high-iron biofortified pearl millet group. Those children
micronutrient interventions. Target micronutrient levels for bioforti- who were iron deficient at baseline were significantly (64%) more likely
fied crops are set to meet the specific dietary needs of women and to resolve their deficiency by six months (Finkelstein et al., 2015).
children, based on existing consumption patterns. Biofortification puts
a solution in the hands of farmers, combining the micronutrient trait 2.2. Vitamin A crops
with other agronomic and consumption traits that farmers prefer. After
fulfilling the household's food needs, surplus biofortified crops make Vitamin A bioavailability studies found efficient conversions from
their way into rural and urban retail outlets. provitamin A to retinol, the form of vitamin A used by the body.
Efficacy studies demonstrated that increasing provitamin A intake
1.3. Cost-effectiveness through consuming vitamin A-biofortified crops results in increased
circulating beta-carotene, and has a moderate effect on vitamin A
Ex-post cost-effectiveness data is currently available for orange status, as measured by serum retinol. Consumption of orange sweet
sweet potato in Uganda, where biofortification was demonstrated to potato (OSP) can result in a significant increase in vitamin A body
cost US$15–$20 per Disability Adjusted Life Year (DALY) saved, which stores across age groups (Haskell et al., 2004; Low et al., 2007; van
the World Bank considers highly cost effective (World Bank, 1993; Jaarsveld et al., 2005).
HarvestPlus, 2010). The primary evidence for the effectiveness of biofortification comes
Results of ex-ante cost-effectiveness studies have shown that for from OSP, assessed through a randomized controlled trial. The OSP
each of the country-crop-micronutrient combinations considered, intervention reached 24,000 households in Uganda and Mozambique
biofortification is a cost-effective intervention based on cost per from 2006 to 2009 with adoption rates of OSP greater than 60% above
DALY saved, using World Bank standards (Meenakshi et al., 2010). control communities (Hotz et al., 2012a, 2012b). Introduction of OSP
Furthermore, the Copenhagen Consensus ranked interventions for in rural Uganda resulted in increased vitamin A intakes among children
reducing micronutrient deficiencies, including biofortification, among and women, and improved vitamin A status among children – a
the highest value-for-money investments for economic development. decrease in the prevalence of low serum retinol by 9 percentage points.
For every dollar invested in biofortification, as much as US$17 of Women who got more vitamin A from OSP also had a lower likelihood
benefits may be gained (Hoddinott et al., 2012). The cost-effectiveness of having marginal vitamin A deficiency (Hotz et al., 2012a). Recent
of any given intervention is dependent on the crop, micronutrient, and research on the health benefits of biofortified OSP in Mozambique
delivery country. The methodology for determining cost-effectiveness showed that biofortification can improve child health; consumption of
and specific case studies are discussed in greater depth elsewhere biofortified orange sweet potato reduced the prevalence and duration of

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H.E. Bouis, A. Saltzman Global Food Security 12 (2017) 49–58

diarrhea in children under five (Jones and de Brauw, 2015). For yield or farmer-preferred agronomic traits. The crop development
additional information on the development and delivery of OSP, see process entails screening germsplasm for available genetic diversity,
Low et al. (2017, this issue). prebreeding parental genotypes, developing and testing micronutrient-
Biofortified provitamin A maize is an efficacious source of vitamin A dense germplasm, conducting genetic studies, and developing mole-
when consumed as a staple crop. An efficacy study conducted in cular markers to lower the costs and quicken the pace of breeding. After
Zambia with 5–7-year-old children showed that, after three months promising lines have been developed, they are tested in several
of consumption, the total body stores of vitamin A in the children who locations across target environments to determine the genotype x
were in the orange maize group increased significantly compared with environment interaction (GxE) – the influence of the growing environ-
those in the control group (Gannon et al., 2014). Consumption of ment on micronutrient expression. Robust regional testing enables
orange maize has been demonstrated to improve total body vitamin A reduced time-to-market for biofortified varieties.
stores as effectively as supplementation (Gannon et al., 2014), and Early in the conceptual development of biofortification, a working
significantly improve visual function in marginally vitamin A deficient group of nutritionists, food technologists, and plant breeders estab-
children (Palmer et al., 2016). lished nutritional breeding targets by crop, based on food consumption
To date, only a small provitamin A cassava efficacy study has been patterns of target populations, estimated nutrient losses during storage
completed in Eastern Kenya with 5–13-year-old children. This trial and processing, and nutrient bioavailability (Hotz and McClafferty,
demonstrated small but significant improvements in vitamin A status, 2007). Breeding targets (Table 1) for biofortified crops were designed
measured both by serum retinol and beta-carotene, in the yellow to meet the specific dietary needs and consumption patterns of women
cassava versus the control group (Talsma et al., 2016). A larger-scale and children. Taking into account baseline micronutrient content in
efficacy trial is underway in Nigeria. each crop, targets were set such that, for preschool children 4–6 years
old and for non-pregnant, non-lactating women of reproductive age:
2.3. Zinc crops the total amount of iron in iron beans and iron pearl millet will provide
approximately 60% of the Estimated Average Requirement (EAR) (30%
Zinc studies have demonstrated that zinc in biofortified wheat is of the EAR for iron at baseline before breeding for high iron); zinc in
bioavailable (Rosado et al., 2009). Because plasma zinc concentration, zinc wheat and zinc rice will provide 60–80% of the EAR (40% of the
the biomarker widely used to estimate zinc status, has limitations in EAR for zinc at baseline); and, provitamin A, the precursor of vitamin
measuring changes in dietary zinc, foundational research to identify A, will provide 50% of the vitamin A EAR in the case of yellow cassava
and test more sensitive biomarkers is underway. These biomarkers will and orange maize, and up to 100% in the case of orange sweet potato
be tested in the zinc rice and wheat efficacy trial scheduled for 2017. A (zero provitamin A at baseline). The breeding target is the sum of the
recent study showed that DNA strand breaks are a sensitive indicator of baseline micronutrient content and additional micronutrient content
modest increases in zinc intake, such as the amount of additional zinc required for each crop and micronutrient combination.
that might be delivered by a biofortified crop (King et al., 2016).
3.1. A conceptual framework for breeding biofortified germplasm
2.4. Future areas of investigation
Fig. 1 outlines the key activities in developing biofortified germ-
Areas for further research include robust new trials that test the plasm. The left column contains activities outside of crop development
efficacy of biofortified crops for a wider range of age and gender groups, to ensure nutritional impact and farmer and consumer acceptance. The
including infants, and over a longer time period (for example, prior to right columns reflect sequentially arranged stages and milestones in
conception through infancy). Other research will test the efficacy of crop development, and are superimposed upon a decision-tree that
consuming several different biofortified crops, each providing different allows monitoring progress and making strategic decisions if goals and
vitamins and/or minerals to the food basket. Nutritionists agree that targets cannot be achieved.
biofortified crops can improve nutritional status in micronutrient- Crop improvement activities for biofortification focus, first, on
deficient populations, but additional research is needed, using other, exploring the available genetic diversity for iron, zinc, and provitamin
more sensitive biochemical indicators, as well as functional indicators, A carotenoids (yellow boxes). At the same time or during subsequent
to more fully understand the health impact of consuming biofortified screening, agronomic and end-use features are characterized. The
foods. objectives when exploring the available genetic diversity are to identify:
(1) parental genotypes that can be used in crosses, genetic studies,
3. Crop development molecular-marker development, and parent-building, and (2) existing
varieties, pre-varieties in the release pipeline, or finished germplasm
Plant breeding can increase nutrient levels in staple crops to target products for “fast-tracking.” Fast-tracking refers to releasing, commer-
levels required for improving human nutrition, without compromising cializing, or introducing genotypes that combine the target micronu-

Table 1
Breeding targets (parts per million).
Source: HarvestPlus Breeding Program.

Provitamin A Sweet potato Maize Cassava

Baseline micronutrient content 2 0 0
Additional content required 30 15 15
Final target content 32 15 15
Iron Beans Pearl Millet
Baseline micronutrient content 50 47
Additional content required 44 30
Final target content 94 77
Zinc Rice Wheat
Baseline micronutrient content 16 25
Additional content required 12 12
Final target content 28 37

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H.E. Bouis, A. Saltzman Global Food Security 12 (2017) 49–58

Fig. 1. Crop development framework. Source: HarvestPlus.

trient density with the required agronomic and end-use traits so they banks, transgenic plant breeding is a promising approach to produce
can be delivered without delay. biofortified crops with the desired nutrient and agronomic traits. For
If variation is present in the strategic gene pool (only in unadapted example, transgenic iron and zinc rice has been developed and tested in
sources), pre-breeding is necessary prior to using the trait in final confined field trials that can provide 30% of the EAR for both nutrients
product development; if variation is present in the adapted gene pool, (Trijatmiko et al., 2016). Golden rice, which contains beta carotene,
the materials can be used directly to develop competitive varieties can provide more than 50% of the EAR for vitamin A. Despite being
(purple boxes). Most breeding programs simultaneously conduct pre- available as a prototype since early 2000, however, Golden Rice has not
breeding and product enhancement activities to develop germplasm been introduced in any country, in large part due to highly risk-averse
combining high levels of one or more micronutrients. regulatory approval processes (Wesseler and Zilberman, 2014). While
The next breeding steps involve developing and testing micronu- these transgenic varieties have tremendous nutritional potential,
trient-dense germplasm, conducting genetic studies, and developing release to farmers is several years in the future, and depends on
molecular markers to facilitate breeding. Genotype x environment approval through national biosafety and regulatory processes.
interaction (GxE) – the influence of the growing environment on Conventional breeding, rather than transgenic breeding, is used in
micronutrient expression – is then determined at experiment stations all of the crops released or in the near pipeline for HarvestPlus
and in farmers’ fields in the target countries (orange boxes). The most programs. Because conventional breeding does not face the same
promising varieties are selected for multi-locational testing over multi- regulatory hurdles and is widely accepted, HarvestPlus considers it to
ple seasons by national research partners, and then are submitted to be the fastest route to getting more nutritious crops into the hands of
national government agencies for testing for agronomic performance farmers and consumers. This article focuses on the evidence developed
and release, a process which typically takes two years, sometimes more. for conventionally-bred biofortified crops.

3.2. Transgenic approaches 3.3. International nurseries/global testing

In crops where the target nutrient does not naturally exist at the HarvestPlus has used two strategies to shorten time to market for
required levels in the tens of thousands of varieties in germplasm biofortified crops: 1) identifying adapted varieties with significant

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H.E. Bouis, A. Saltzman Global Food Security 12 (2017) 49–58

Fig. 2. Biofortified crop map (Jan 2017). Source: HarvestPlus.

micronutrient content for release and/or dissemination as “fast track” 4. Delivery experiences in target countries
varieties, while varieties with target micronutrient content are still
under development, and 2) deploying multi-location Regional Trials After biofortified varieties have been developed and released, they
across a wide range of countries and sites to accelerate release enter national farming and food systems. Research continues to
processes by increasing available performance data of elite breeding develop evidence that farmers are willing to grow biofortified crops
materials. Regional Trials also include already-released biofortified and that consumers are willing to eat them. The evidence base has been
varieties and generate data on their regional performance, in order to developed in eight target countries (Bangladesh, DR Congo, India,
take advantage of regional variety release systems such as under SADC Nigeria, Pakistan, Rwanda, Uganda, and Zambia) where HarvestPlus
(Southern African Development Community). Such regional agree- and national partners are taking the lead in delivery. As of the end of
ments harmonize seed regulations of member countries and allow any 2016, HarvestPlus estimates that approximately 20 million people in
variety that is tested, approved, and released in one member country to four million farming households in HarvestPlus target countries are
be released simultaneously in other member countries with similar now growing and consuming biofortified crops. This estimate is the
agro-ecologies. sum of 1.5 million farm households reached directly with biofortified
planting material by HarvestPlus and its partners in 2016, as well as
continued planting and diffusion from previous years to additional
farm households that regularly grow biofortified crops. Table 2 shows
3.4. Low-cost, high throughput methods numbers of households reached directly in each year, i.e. not a
cumulative total. Country-specific models have been estimated that
Biofortification breeding required developing or adapting cost- take into account assumed rates of adoption/non-adoption, informal
effective and rapid high throughout analytical techniques for micro- farmer-to-farmer diffusion, and disadoption. These assumptions are
nutrients, as thousands of samples need to be tested for mineral or tested through impact assessment surveys, with models updated
vitamin content each season. These trait diagnostics include near- accordingly.3
infrared spectroscopy (NIRS) and colorimetric methods for carotenoid Target countries represent a variety of market environments for
analysis. For mineral analysis, X-ray fluorescence spectroscopy (XRF) biofortified crops, from a primarily commercial private sector approach
emerged as the method of choice, as it requires minimal pre-analysis (India, Zambia), to various mixed public-private delivery systems
preparation and allows for non-destructive analysis (Paltridge et al., (Bangladesh, Nigeria, Rwanda, Uganda), to primarily public or infor-
2012a, 2012b). mal market systems (DR Congo). Progress in the integration of
biofortified crops into the seed and food value chains in target
countries is discussed below, using case studies to discuss how
3.5. Releases of biofortified crops HarvestPlus and its partners have strengthened seed systems, created
knowledge and demand, and expanded partnerships to ensure the
Cumulatively, more than 150 biofortified varieties of 10 crops have future sustainability of biofortification. Examples of delivery experi-
been released in 30 countries. Candidate biofortified varieties across 12 ences are presented for vegetatively propagated, self-pollinated, and
crops are being evaluated for release in an additional 25 countries. hybrid crops. Impact and effectiveness data are presented where
Fig. 2 depicts where biofortified varieties have been tested and released available; for countries where these studies are still underway, evidence
to date. Biofortified crops have been released in countries indicated in is primarily based on information captured through monitoring
dark purple, while crops are being tested in countries in light purple. systems.
This map includes countries where the International Potato Center
(CIP) has worked to release the orange sweet potato. More detailed
information about the varieties tested and released in each country is 3
A “household reached” received biofortified planting materials; not all households
available on the HarvestPlus website.2 reached are assumed to grow biofortified crops in the first year of having access to
biofortifed seeds (non-adoption), or to grow them over several years (disadoption). This
number of 20 million does not include orange sweet potato-growing households as
2
To view country- or crop-specific information about varietal testing and release, reported in Low et al. (2017, this issue) except in Uganda (a HarvestPlus target country),
please visit: http://harvestplus.org/sites/default/files/publications/HarvestPlus_ nor purchases of biofortified foods by non-growing (e.g. urban) households, nor
BiofortifiedCropMap_2016.pdf. estimates from all 22 non-target countries where biofortified crops have been released.

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H.E. Bouis, A. Saltzman Global Food Security 12 (2017) 49–58

Table 2
Number of households reached in target countries annually, 2012–2015 (x1000).
Source: HarvestPlus Monitoring Database.

Country-Crop 2012 2013 2014 2015

Iron Bean Rwanda 105 609 332 453

Iron Bean DR Congo 60 241 128 175
Iron Bean Uganda 29 69 43 39
Iron Pearl Millet India 30 40 62 125
Provitamin A Maize Zambia 0 11 104 126
Provitamin A Cassava Nigeria 0 106 360 528
Provitamin A Cassava DR Congo 0 25 75 127
Provitamin A Orange Sweet Potato Uganda 33 76 107 132
Zinc Wheat India 0 1 6 36
Zinc Wheat Pakistan 0 0 0 3
Zinc Rice Bangladesh 0 1 18 160
Total 257 1,179 1,235 1,865

4.1. Vegetatively propagated crops crops.4 In many countries, the public sector instead multiplies and
distributes self-pollinated seed, and further farmer-to-farmer dissemi-
Vegetatively propagated crops – those for which farmers plant nation is common. Self-pollinated biofortified crops include iron beans,
stems, tubers or vines rather than seeds – typically have seed delivered in Rwanda and Democratic Republic of Congo, zinc rice in
systems characterized by small, informal (rather than commercial) Bangladesh, and zinc wheat in India and Pakistan.
actors. Planting materials are perishable, expensive and bulky to Delivery has progressed most quickly in Rwanda, where initial public
transport over long distances, and must be replanted within several sector investments have now spurred private sector interest in meeting
days of harvesting. The lack of commercial private sector participa- growing demand for iron bean seed. Significant delivery has also taken
tion creates both a challenge and an opportunity for producing place in Bangladesh, where demand is driven by the zinc rice varieties that
planting materials of biofortified crops like orange sweet potato have attractive agronomic traits, including a short duration variety that
(distributed as vines) and provitamin A yellow cassava (distributed allows for production of a third crop between the wet and dry season rice
as stem cuttings). See Low et al. (2017, this issue) for additional crops. Delivery of zinc wheat in India and Pakistan is just beginning. In
evidence from OSP delivery. India, zinc wheat is predominantly marketed by the private sector as
truthfully labeled seed (TLS), and six private seed companies had
4.1.1. Cassava in Nigeria and DR Congo incorporated zinc wheat into their product lines. In Pakistan, the first
In parallel with strengthening the seed system through both zinc wheat variety was released in 2016, and delivery through public and
community-based and commercial stem production, awareness of private sector partners is now underway.
and demand for biofortified crops must be created simultaneously. In
the case of provitamin A yellow cassava, extension to farmers was at the 4.2.1. Beans in Rwanda and DR Congo
forefront of this effort. Initially, free bundles of stems were distributed In Rwanda, HarvestPlus worked closely with the Rwanda
to farmers, and accompanied by agronomic training and nutrition Agriculture Board (RAB) to facilitate production of bean seed through
information. In the following season, farmers who received free stems contracted farmers, cooperatives, and small seed companies. From
were required to distribute an equal amount of free stems to two 2011 to 2015, HarvestPlus procured about 80% of its certified seed
additional farmers, dramatically lowering delivery costs. This promo- through registered seed farmers under the supervision and certification
tional strategy was effective in reaching vulnerable populations who of RAB, with the remainder being produced through contracts with
typically do not have market access to improved varieties for planting. local seed companies. To increase available seed for the 2015 planting
It also piqued interest and allowed farmers in a low-risk way to test a season and beyond, HarvestPlus partnered with established local and
new product. Many of the farmers who received and planted free stems regional seed companies for seed multiplication, with RAB certifying
liked the yellow cassava and are now buying additional stems from the biofortified seed. HarvestPlus and its partners also proposed a new
commercial traders. seed class, “Declared Quality Seed” (DQS) or Certified II seed, first in
In 2015, HarvestPlus estimated that about 75% of all biofortified Rwanda and then in DRC. DQS is produced from certified seed and is
harvested roots were consumed on farm, as many households were not priced between certified seed and grain, bridging a price gap for
yet producing excess from the stem packs they received for trial. farmers who are inclined to plant recycled grain rather than purchase
Increased commercialization is expected going forward. As farmers certified seed.
began to produce yellow cassava in excess of their household food Farmers initially accessed iron bean seed either in small quantities
security needs, HarvestPlus and its partners have worked to increase through direct marketing (via established agrodealers or in local
awareness and demand from the food market for biofortified cassava. markets) or in larger quantities through a payback system that also
These efforts include consumer marketing via print, radio, and televi- included cooperatives. By the end of 2014, marketing data showed that
sion media (even feature-length movies), and market development an increasing number of farmers were purchasing seed, a trend that is
efforts by linking commercial food processing investors to supplies of expected to continue. Farmer-to-farmer dissemination is also an
yellow cassava roots. important delivery channel; an impact assessment conducted in 2015
found that nearly half of farmers growing iron bean had received their
4.2. Self-pollinated crops planting material from a person in their social network (Asare-Marfo
et al., 2016).
Self-pollinated crops – those which produce seed true to their
parent characteristics – can be replanted year after year. While farmers 4
For crops with a low seed rate, like pearl millet, farmers are more likely to purchase
do need to periodically replace their seed to maintain its desirable seed annually. An open-pollinated variety of biofortified iron pearl millet, which
agronomic traits, the possibility of self-production for seed typically combines the iron trait with 10% higher yield, has been successfully deployed through
limits private sector investment in producing seed for self-pollinated the private sector in India, where farmers generally purchase seed annually.

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H.E. Bouis, A. Saltzman Global Food Security 12 (2017) 49–58

Because the iron trait is invisible and iron beans are not easily between the first and second year of inclusion in the program.
distinguished from conventional varieties, the primary approach has A central element of the delivery strategy is to create awareness and
been to gain market share for biofortified beans due to their superior acceptance of orange maize through the use of social marketing
agronomic and consumption qualities. Over time, a high percentage of campaigns and advertisements placed in public media, including TV,
the total national supply of beans is expected to contain the biofortified radio, newspapers, and popular music. Educational and awareness-
trait, allowing access to additional iron for much of the population. creation activities stimulate consumer demand for orange maize
HarvestPlus and its partners have used a variety of delivery methods, products, while engagement with the private sector helps meet growing
including “swapping” biofortified seed for conventional seed, to ensure consumer demand.
a high rate of farmer trial and adoption. Only five years after the first To further stimulate cultivation of orange maize, creating markets
iron bean release, iron beans make up more than 10% of national bean for surplus production was essential, considering that 20–50% of rural
production in Rwanda (Asare-Marfo et al., 2016). households sell maize after satisfying their own food needs.
HarvestPlus therefore links major grain buyers to farmers and offers
4.2.2. Rice in Bangladesh grain samples to millers and food processors interested in incorporat-
At the core of the Bangladesh strategy are rice varieties with ing orange maize in their product lines. The multi-lateral AgResults
attractive agronomic properties and a robust farmer demonstration initiative also incentivizes millers to produce and market vitamin A
program. One released zinc rice for the wet season (BRRI dhan 64) is a maize products. Strong interest from farmers and food processors
short duration variety (100 days as compared with 140 days), which encourages increased private sector seed production.
allows production of a third crop of lentils or other food between wet
and dry season rice crops. Other biofortified zinc rice varieties carry 4.3.2. Pearl millet in India
different farmer-preferred agronomic traits, like high height at matur- Crop development and delivery in India is implemented through
ity, which is beneficial for flooded areas in Southern Bangladesh. A public and private sector partnerships. In crop development, the
robust demonstration program provides farmers a chance to observe International Crops Research Institute for the Semi-Arid Tropics
these new varieties, as well as training on growing the biofortified rice (ICRISAT) supplies parental materials/breeder seeds for next stage
and the health benefits of zinc. seed multiplication. Partners now testing and developing their iron
Seed is produced by both the private and the public sector. A private pearl millet varieties for seed sales include 15 private seed companies,
seed association called SeedNet produces truthfully labeled seed 2 public seed companies and 5 public organizations. HarvestPlus
alongside the foundation and certified seed produced by government supports ICRISAT to develop high iron hybrid parental lines and to
entities. HarvestPlus initially both guarantees a market for a portion of test hybrids with farmer-preferred traits, including of course high
the private sector production and subsidizes the price for any seed that yields. This unique crop development arrangement supports and
the private sector markets directly to consumers. Free seed is dis- encourages companies to develop their own biofortified varieties for
tributed by NGO and government partners in small seed packs, and all their target market segments. This approach is expected to more
free seed recipients agree to pass on the same amount of seed to three quickly increase the number and range of biofortified varieties available
neighboring farmers in the subsequent season. As an increasing in the years to come.
amount of zinc rice is available on the market, efforts to increase
consumer and miller awareness have increased, including outreach via 4.3.3. Lessons learned from delivery
SMS and programs on local television and community radio channels. While delivery experiences vary widely by country and seed system,
a few common themes have emerged from the delivery experience.
4.3. Hybrid crops First, multiplication of sufficient planting material is a crucial first step
– without planting material to “prime the pump”, there are no
Hybrid crops – those for which seed must be replaced each year to biofortified crops. HarvestPlus and its partners have focused on both
maintain the same yield and agronomic traits – offer the most potential strengthening capacity in the public and private sector to produce high
for private sector commercialization. While utilizing the private sector quality seed and reducing risk, to ensure that quality planting material
for delivery may lead to long-term sustainability, the speed of private is available for farmers. Second, demonstration trials have been key
sector uptake is dependent on their assessment of demand. Therefore, demand drivers at the farm level. Decentralized field demonstrations
the activities of biofortification proponents must focus on targeted and the availability of small promotional seed packs have allowed
demand creation for both farmers and consumers. interested farmers to view and try the new product without taking on a
great deal of risk in cultivating a crop for which the market has not yet
4.3.1. Maize in Zambia been tested. Third, nutrition messaging aimed at both men and women
Because private seed companies dominate the hybrid maize seed has also been key, and in general, involving women farmers has led to
market in Zambia, upon release, biofortified hybrid varieties were increasing demand for biofortified crops. While many biofortified crops
licensed to companies for commercialization of seed production and are acceptable to farmers and consumers without further information
distribution. As biofortified maize is scaled up to reach more house- about their nutrition traits, nutrition information helps ensure that the
holds in more provinces, the main challenge is to ensure extensive biofortified foods are integrated into child diets (Birol et al., 2015).
distribution through private networks to outlying areas. Because many Finally, multi-stakeholder platforms are crucial to scaling up the early
rural households purchasing from agrodealers cannot afford to buy uptake and success of biofortified crops. In target countries, there has
large quantities of seed, HarvestPlus is working with the private seed been rapid acceptance of biofortification by government entities, and
companies to ensure that large quantities of smaller, affordable pack national governments have proactively integrated it into their agricul-
sizes will be available. HarvestPlus also partners with the Zambia ture and nutrition policies. Integrating private and public sector actors
National Farmers Union and government extension services to dis- and interests around shared goals reduces barriers to scaling.
seminate information to farmers about the availability of vitamin A
maize seed in their local areas. The inclusion of orange maize seed in 5. Building blocks for global delivery
the Zambian government's Farmer Input Support Program (FISP) has
further facilitated access to orange maize, including for vulnerable For biofortification to reach scale and be truly sustainable, a
households. FISP provides at least a 50% subsidy for maize seed and number of institutions must become involved in establishing an
fertilizer to farmers considered economically disadvantaged. The enabling environment. This includes recognition of biofortification
quantity of orange maize seed distributed under FISP grew by 400% among global normative and regulatory agencies, integration into

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development policies and programs funded by multi-lateral institu- the food product value chain for biofortified crops. Small and medium-
tions, uptake by private sector entities, and incorporation into devel- size companies can play a role in creating demand for biofortified grain
opment programs being implemented on the ground, both in target and food even before supplies reach scale. For some crops and
countries and beyond. This enabling environment is essential to countries, like Nigeria cassava, the food value chain is dominated by
encourage the scaling up of biofortified crops and to support na- small and medium-size food processors. While the interest of multi-
tional-level actors in various spheres. national companies is slower to develop, several are now testing
biofortified crops in their food products. These companies also
5.1. Standards and regulatory contribute to the evidence base on vitamin and mineral retention by
assessing different processing methods for biofortified crops.
Efforts are underway to integrate biofortification into global
standards and guidelines, such as the Codex Alimentarius, the food 5.4. NGOs
standards-setting agency administered jointly by the World Health
Organization (WHO) and the Food and Agriculture Organization of the While private sector participation is essential in creating sustain-
United Nations (FAO) and recognized by the Sanitary and able markets for biofortified seed and foods, NGOs remain important in
Phytosanitary Agreement (SPS) of the World Trade Organization delivering this nutrition intervention to vulnerable households. The
(WTO) as its reference organization. Progress toward the development existing global partnership between World Vision and HarvestPlus is
of a definition and standards for biofortification within the Codex an example of how a leading development NGO can incorporate
Alimentarius continues. Once adopted, the internationally-recognized biofortified crops into its existing agricultural programs, linking them
Codex reference standard helps to facilitate cross-border marketing of to health and nutrition programs. While HarvestPlus provides techni-
biofortified crops and food, to standardize labeling and health claims, cal assistance, World Vision takes the lead in delivery, with activities
and to reduce the incidence of false claims. now in 15 countries. This type of partnership, whereby biofortified
crops are integrated into existing agriculture and nutrition projects or
5.2. Multi-lateral institutions included in collaboratively developed new projects, will continue to be
important to reach the most vulnerable households, which may also be
Beyond their individual investments and activities, multi-lateral the most likely to suffer from micronutrient deficiencies.
institutions, including the World Bank, the African Development Bank,
the World Food Programme, and the World Health Organization, 5.5. Moving beyond target countries to partnership country
collectively influence national government policymakers and opera- strategies
tional partners.
The World Bank is now implementing a number of projects Outside of target countries, HarvestPlus has invested in, advocated
supporting biofortification, including the Multisectoral Food Security for, and now works closely with government-sponsored biofortification
and Nutrition Project in Uganda, which is accelerating the scale-up of programs in Brazil, China, and India. Through the HarvestPlus Latin
orange sweet potato and iron beans. As a convener of development American and Caribbean (LAC) program, led by the Brazilian Ministry
partners, the Bank plays an important role in encouraging nutrition- of Agriculture's Research Corporation (EMBRAPA), HarvestPlus pro-
sensitive agricultural approaches, including biofortification, in arenas vides technical assistance and support to government-driven bioforti-
such as the Global Donor Platform for Rural Development. The African fication programs in Bolivia, Colombia, Guatemala, Haiti, Nicaragua,
Development Bank's new “Banking on Nutrition” technical partnership and Panama and is exploring efforts in several additional countries. As
is implementing a multi-sectoral and integrated approach to nutrition biofortification gains momentum, this type of partnership approach is
interventions, including the integration of biofortified crops. The World essential. While HarvestPlus will continue to provide technical assis-
Food Programme's (WFP) Purchase for Progress program is very tance and promote linkages between organizations, other organizations
interested in local purchase of biofortified crops, and partnerships and actors will increasingly take the lead in delivery on the ground.
are being developed in several countries. For example, in Rwanda, local
iron bean production is purchased and stored in WFP warehouses for 6. A future vision: institutional leadership to drive and guide
later emergencies. mainstreaming
In 2017 the WHO Nutrition Guidance Expert Advisory Group is
expected to issue a recommendation and guidelines on biofortification To reach its full potential, biofortification must be integrated as a
as a public health nutrition intervention. One step in the process will be core activity within a range of global institutions. This will require three
the publication of papers discussed in 2016 at an expert consultation critical elements.
held at the New York Academy of Sciences.
1. Supply: Agricultural research entities, both public and private, come
5.3. Private sector to recognize high mineral and vitamin content as core plant breeding
objectives; varietal release committees make minimum levels of
As crop development programs increase the number of released minerals and vitamins a requirement for approval for release (in
varieties of biofortified crops, seeds from these varieties must be made addition to the standard agronomic traits, such as high yield).
available to farmers. In countries with robust private seed systems that 2. Policy: A wide range of national and international public officials
reach smallholder farmers, private seed companies are a natural come to recognize the significant impact of biofortification for
partner. In some cases, HarvestPlus has brokered agreements between improving and sustaining public health, as well as the high economic
seed companies and interested NGOs or government entities to ensure return to investments in biofortification and the legitimacy conferred
that there will be a market for the seed produced by the private sector, by international recognition (especially by standards bodies).
reducing the risk associated with that private sector investment. While 3. Demand: Both rural and urban consumers come to see the value of,
the private sector has predominantly taken up hybrid crops, interest in and demand, high mineral and vitamin content in their staple foods.
a wider variety of crops has increased as the business case has been
developed. Involving private sector seed companies not only in 6.1. Supply
marketing, but also in developing and testing biofortified varieties,
shortens the time to market and lays the groundwork for sustainability. The key to continued supply of biofortified crops is to move beyond
Food processing companies play an important role in developing a biofortification-focused breeding program, with funding specifically

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for biofortified crops, to mainstream the nutrient traits into all relevant scientific contributions during 1993–2002 and in the early years of
crop pipelines and the best crop backgrounds being developed by HarvestPlus to conceptualizing and motivating a biofortification pro-
CGIAR centers and National Agricultural Research Systems (NARS). gram. This article describes the collective accomplishments of a large
Recent progress in developing molecular markers will help facilitate number of HarvestPlus staff and collaborating scientists and imple-
mainstreaming (Babu et al., 2013; Swamy et al., 2016). As new menters, too numerous to mention here.
varieties are developed and released, they should include the bioforti-
fied trait as a matter of standard practice. References

6.2. Policy Asare-Marfo, D., Birol, E., Gonzalez, C., et al., 2013. Prioritizing Countries for
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