Availability, production, and consumption of crops biofortified by plant breeding: current evidence and future potential

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1 Ann. N.Y. Acad. Sci. ISSN ANNALS OF THE NEW YORK ACADEMY OF SCIENCES Issue: Staple Crops Biofortified with Vitamins and Minerals REVIEW ARTICLE Availability, production, and consumption of crops biofortified by plant breeding: current evidence and future potential Amy Saltzman, 1 Ekin Birol, 1 Adewale Oparinde, 1 Meike S. Andersson, 2 Dorene Asare-Marfo, 1 Michael T. Diressie, 1 Carolina Gonzalez, 2 Keith Lividini, 1 Mourad Moursi, 1 and Manfred Zeller 3 1 HarvestPlus, International Food Policy Research Institute, Washington, DC. 2 HarvestPlus, International Center for Tropical Agriculture (CIAT), Cali, Colombia. 3 University of Hohenheim, Stuttgart, Germany Address for correspondence: Amy Saltzman, HarvestPlus, International Food Policy Research Institute, 2033 K St NW, Washington, DC ajsaltzman.hp@gmail.com Biofortification is the process of increasing the density of vitamins and minerals in a crop through plant breeding using either conventional methods or genetic engineering or through agronomic practices. Over the past 15 years, conventional breeding efforts have resulted in the development of varieties of several staple food crops with significant levels of the three micronutrients most limiting in diets: zinc, iron, and vitamin A. More than 15 million people in developing countries now grow and consume biofortified crops. Evidence from nutrition research shows that biofortified varieties provide considerable amounts of bioavailable micronutrients, and consumption of these varieties can improve micronutrient deficiency status among target populations. Farmer adoption and consumer acceptance research shows that farmers and consumers like the various production and consumption characteristics of biofortified varieties, as much as (if not more than) popular conventional varieties, even in the absence of nutritional information. Further development and delivery of these micronutrient-rich varieties can potentially reduce hidden hunger, especially in rural populations whose diets rely on staple food crops. Future work includes strengthening the supply of and the demand for biofortified staple food crops and facilitating targeted investment to those crop country combinations that have the highest potential nutritional impact. Keywords: biofortification; micronutrient deficiency; biofortification priority index; farmer adoption; consumer acceptance; nutritional efficacy Introduction In the wake of the Green Revolution, hunger energy deficits in developing countries has seen continual improvement. According to the Food and Agriculture Organization of the United Nations (FAO), the prevalence of undernourishment in the global population has decreased from 18.6% in to 10.9% in , but one in nine people in the world still suffers from hunger. 1 Despite this progress, more than two billion people or one in three globally suffer from micronutrient deficiency, also known as hidden hunger. As reported in Table 1, almost 2.5 billion people are at risk of vitamin A, iron, and/or zinc deficiencies, which are recognized by the international nutrition community as most limiting in diets. 2 Common approaches to address micronutrient deficiency include supplementation, fortification (including both commercial and home fortification), and dietary diversification. Over the past 15 years, research has demonstrated that another strategy, called biofortification, is an effective complement to these approaches in addressing micronutrient deficiency and related health problems. Biofortification involves breeding staple food crops to increase their micronutrient content or bioavailability, targeting foods widely consumed by low-income families globally, including those in Africa, Asia, and Latin America. The focus is on providing sufficient levels of vitamin doi: /nyas Ann. N.Y. Acad. Sci (2017) C 2017 New York Academy of Sciences.

2 Amy Saltzman et al. Biofortification: evidence and potential Table 1. Total population at risk of major micronutrient deficiencies and top five staple crops, by region Asia Africa Latin America and the Caribbean Total cases of deficiency/ inadequate intake Total population at risk All 1,722,763, ,818, ,644,347 2,466,226,780 Iron 699,198, ,395,434 57,962, ,556,079 Zinc 901,336, ,801, ,567,293 1,273,705,384 Vitamin A 122,228,982 67,621,409 8,114, ,965,317 Total kilocalories per day (millions) Rice 3,146, , ,990 3,489,295 Wheat 2,017, , ,579 2,570,236 Maize 301, , , ,175 Potatoes 223,633 34,527 24, ,007 Cassava 71, ,542 31, ,359 Source: Authors calculations based on the following resources: UN Population Projections: 2011 Revision (population estimates); 3 FAOSTAT (daily energy availability); 4 WHO, World Bank (prevalence of anemia, vitamin A deficiency, and crude birth rates); 5,6 izincg, 2004 (risk of inadequate zinc intake). 7 For iron deficiency, we assumed a 1:1 relationship between anemia and iron deficiency. A, iron, and/or zinc through these crops, based on existing consumption patterns. Table 1 shows the total energy supplied by the top five staple crops contributing to dietary energy, revealing their importance in the diets across regions of the world and their potential for combating micronutrient deficiencies in different regions. For example, rice and wheat are likely to be good vehicles in Asia, while maize and wheat offer potential in Africa, Latin America, and the Caribbean. There are three common approaches to biofortification: agronomic, conventional plant breeding, and plant breeding using genetic engineering. Agronomic biofortification provides temporary micronutrient increases through fertilizers. This approach is useful to increase micronutrients that can be directly absorbed by the plant, such as zinc, but less so for micronutrients that are synthesized in the plant and cannot be absorbed directly. 8 Agronomic biofortification is particularly useful for realizing the maximum expression of biofortified traits for crops produced in micronutrient-deficient soils. Conventional plant breeding involves identifying and developing parent lines with high vitamin or mineral levels and crossing and selecting the segregants over generations to produce plants with the desired nutrient and agronomic traits. 9,10 Biofortification by genetic engineering seeks to do the same and has been used primarily in crops where the target nutrient does not naturally exist at the required levels. This review focuses exclusively on the evidence developed for the conventional plant breeding approach to biofortification. For biofortification using the conventional plant breeding approach to be considered as a feasible and effective approach to alleviating hidden hunger, three conditions should be met. These are (1) conventional breeding can add extra nutrients in the crops without reducing yields; (2) when consumed, theincreaseinnutrientlevelscanmakeameasurable and significant impact on human nutrition; and (3) farmers are willing to grow biofortified crops and consumers to eat them. The first aim of this review is to present the most up-to-date breeding, nutrition, and monitoring and evaluation evidence supporting these three conditions. The second aim is to present the biofortification priority index (BPI) and the concept of mainstreaming, so as to stimulate the discussion on the future potential of biofortification. Current evidence for biofortified crops developed through conventional plant breeding Breeding evidence Today, biofortified crops developed using the conventional plant breeding approach, including provitamin A rich orange sweet potato (OSP), orange maize, and yellow cassava; iron bean and iron pearl millet; and zinc rice and zinc wheat, have been officially released for production in more than 30 countries and are being tested and grown in more Ann. N.Y. Acad. Sci (2017) C 2017 New York Academy of Sciences. 105

3 Biofortification: evidence and potential Amy Saltzman et al. Table 2. Testing and release status of biofortified varieties developed under HarvestPlus using the conventional plant breeding approach (December 2016) Status of biofortified varieties Region OSP a Maize Cassava Beans Pearl millet Rice Wheat Provitamin A Iron Zinc Tested in # countries Africa > Asia LAC Total Released in # countries Africa > Asia LAC Total Number of varieties released Africa > Asia LAC ` Total >90 >30 12 > LAC, Latin America and the Caribbean; OSP, orange sweet potato. a OSP variety development and dissemination is led by CIP. than 50 (Table 2). These releases, approved by the official national release committees of these countries, demonstrate that it is possible to increase the micronutrient content of (i.e., to biofortify) these crops using conventional breeding without sacrificing other production and consumption attributes that farmers and consumers prefer. Crop improvement continues, developing varieties with everhigher levels of vitamins and minerals that are adapted to a wide range of agroecological conditions and ensuring that the best germplasm for climateadaptive as well as food-quality traits continues to be used in breeding biofortified crops. Biofortified germplasm and nutrient-rich breeding lines, like most research produced by the Consultative Group for International Agricultural Research (CGIAR), are being made available as public goods to national governments, which can test and further improve these materials for subsequent official release as new crop varieties. 11 Nutrition evidence There is a considerable and ever-growing number of efficacy studies for biofortified crops developed using the conventional plant breeding approach. Efficacy trials for vitamin A rich OSP, 12,13 provitamina fortifiedorangemaize, 14,15 provitamin A fortified yellow cassava, 16,18 iron pearl millet, and iron beans 18,20 all provide promising evidence that biofortification improves micronutrient intake and deficiency status among target populations. Limited effectiveness evidence to date also reveals positive results. Evidence from rural Uganda shows that delivery of vitamin A rich OSP resulted in significantly increased vitamin A intakes among childrenandwomenandmeasurablyimprovedvitamin A status among some children. 21 In Mozambique, delivery of vitamin A rich OSP resulted in doubling of vitamin A intakes, with vitamin A rich OSP providing almost all of the total vitamin A intakes for children. 22 Consumption of vitamin A rich OSP was also found to reduce the prevalence and duration of diarrhea among children, revealing that child health could be improved through biofortification. 23 Adoption and consumption evidence Monitoring data to date reveal that, in HarvestPlus target countries, more than four million farming households have been reached by HarvestPlus or its partners with biofortified planting material since This figure can be considered as a lower bound, as it does not include (1) the delivery conducted by other organizations (such as the International Potato Center, which delivers vitamin A enriched OSP) and by the national governments or (2) the households who receive biofortified planting material through diffusion channels (such as through their social networks or through purchases of grains in local markets to be used as planting material). However, over the 4 years, there might also be a number of farmers who were counted 106 Ann. N.Y. Acad. Sci (2017) C 2017 New York Academy of Sciences.

4 Amy Saltzman et al. Biofortification: evidence and potential Table 3. Number of households reached in target countries ( 1000) Country crop Iron bean Rwanda Iron bean DR Congo Iron bean Uganda Iron pearl millet India Provitamin A maize Zambia Provitamin A cassava Nigeria Provitamin A cassava DR Congo Provitamin A orange sweet potato Uganda Zinc wheat India Zinc wheat Pakistan Zinc rice Bangladesh Total more than once, as they have repeatedly received biofortified seed over multiple seasons. Hence, the cumulative total figure of about four million households reached is to be seen as an estimate. Table 3 presents the numbers of households reached annually since 2012 in each of the HarvestPlus target countries. In several target countries, studies have been conducted to understand farmers evaluation of these biofortified crops vis-à-vis conventional ones and to assess future adoption and diffusion patterns. These studies suggest that farmers like the various production and consumption attributes of biofortified varieties, as measured with Likert scales, and they are planning to plant these in the forthcoming seasons, often allocating larger areas, as well as to give the planting material or information about these varieties to others in their social networks. A participatory farmer field day evaluation study was conducted among 242 randomly selected field day participants in 2012 in Zambia. This study confirmed a strong preference by farmers for both production and consumption attributes of orange maize varieties compared with conventional white maize varieties. 24 Farmers appreciated the yield, cob size, and cob-filling characteristics of the new varieties, as well as the taste and aroma of the orange maize preparations. Participants also indicated a high willingness to pay (as a proxy for demand) for the seed of the orange maize varieties, with an average premium of 40% over conventional white maize varieties. A farmer feedback study was conducted in Rwanda in 2012 among a representative sample of 305 first adopters/growers of the iron bean varieties. 25 The results revealed that iron bean adopters liked the various consumption and production attributes of these varieties at least as much as (if not more than) their most popular varieties. The primary reason for adopting iron bean varieties was the yield potential promised by the improved seed. About 80% of farmers said that they wanted to plant these varieties in the following season, of which 85% stated that they wanted to allocate a larger area to iron bean varieties in the following season. With regard to diffusion, over half said that they recommended the variety to an average of four other farmers in their social networks (e.g., neighbors, relatives, and friends), and a quarter of them gave some iron bean grain to an average of three others in their social networks. A similar farmer feedback study was conducted in Maharashtra, India, in 2012, among a representative sample of 1600 iron pearl millet growers, following the first wave of delivery of iron pearl millet varieties. 26 This study revealed that majority (83%) of pearl millet farmers who planted the iron pearl millet variety had replaced the old, lower-iron pearl variety with its iron counterpart. One third of these tried the iron variety because of its nutritional benefits, whereas over half (56%) because it replaced the old variety. Adopting farming households revealed that 84% of the grain output was consumed at home, indicating the potential nutrition impact of the higher-iron variety in rural areas. This study also revealed that farmers liked the various production, processing, and marketing and consumption attributes of the iron variety more than its conventional counterpart. Almost three-fourths (73%) stated an intention to plant next season and also to plant more seed, while 25% were not sure if they wanted to plant pearl millet the following season. There is a large potential for diffusion; 25% of the sample recommended this variety to an average of four farmers in their social networks. An impact-assessment study was conducted in Rwanda in 2015 to assess the adoption rates of iron bean varieties after eight seasons of intensive delivery efforts. Preliminary analysis of the nationally representative data on 19,575 rural households revealed that 29% of rural households almost half a million households have planted an iron bean Ann. N.Y. Acad. Sci (2017) C 2017 New York Academy of Sciences. 107

5 Biofortification: evidence and potential Amy Saltzman et al. variety since their release up to the first beangrowing season of This study further found that, in the first bean growing season of 2015, an estimated 21% of all bean growers in the country (i.e., about 350,000 rural households) grew iron beans. These results align with the monitoring evidence from this country, as reported in Table 3. Further analysis is currently being conducted to understand adoption, diffusion, and disadoptionrates/causes,aswellasfarmerevaluationof iron beans vis-à-vis conventional varieties, and final results are expected by mid Early analysis from a detailed survey conducted with a representative sample of 1397 households showed several very promising results: (1) farmers increase area planted to iron beans over time among farmers who grew iron beans for six consecutive seasons, bean area allocated to iron beans increase from 48% in season one to 70% in season six; (2) 54% of farmers who had grown at least one iron bean variety in the past eight seasons were either continuous or intermittent adopters suggesting that farmers continued to grow these varieties season after season; (3) farmers liked the various production and consumption attributes of iron beans as much as (if not more than) the various local and other improved varieties they produce; (4) seed-to-grain ratio (proxy for yield) for iron beans was significantly higher than those for local varieties (22.5% higher for bush varieties and 18% higher for climbing varieties); (5) 12% of total bean output in Rwanda 2015 season B was iron beans; and (6) social networks play a major role in diffusion of iron bean varieties 41% of iron bean growers received first planting material from a friend or neighbor. Consumers acceptance of the biofortified varieties has also been very promising. Birol et al. presented a review of the evidence on consumer acceptance of provitamin A and iron crops from both the economics and food sciences literatures. 28 According to that review, biofortified crops are liked by target consumers, as expressed either in terms of consumer valuation (captured as willingness to pay) or in terms of their sensory evaluation (captured through hedonic (i.e., liking) rating with 5- or 7-point Likert scales used to measure the consumers level of liking), in some cases even in the absence of information about their nutritional benefits, though information and awareness campaigns often have important roles to play. This finding is important for proving the acceptability of both vitamin A biofortified crops which change color and some other organoleptic characteristics owing to their -carotene content and mineral-fortified crops, which do not have any visible changes and hence may not be considered as more nutritious than their conventional counterparts. Consumer-acceptance studies provide more evidence about how preferences differ by crop, as well as between and sometimes within countries. Sensory evaluation studies were conducted in Uganda, 29 Mozambique, 30,31 and South Africa, 32 with sample sizes ranging from 201 and 212 in Mozambique and South Africa, respectively, to 467 in Uganda. These studies showed that consumers liked the sensory attributes of OSP, as well as those of various processed products (e.g., bread, chips, and doughnuts) made with OSP. The sensory attributes evaluated varied across studies but included those key attributes, such as taste, appearance, aroma, texture, and overall acceptability. Studies conducted in both rural and urban areas of Uganda revealed that, when nutrition information on the benefits of OSP was provided, consumers valued orange varieties more than white ones. Another study conducted in Mozambique, with 308 rural and urban consumers, found that consumers valued OSP and that the value was influenced by information on nutritional benefits. 33 These studies highlight the importance of information campaigns in driving demand for OSP. 33 In rural Zambia, a consumer-acceptance study conducted with 478 rural consumers found that consumers preferred the sensory attributes of nshima made with orange maize compared with nshima from white and yellow maize varieties, even in the absence of nutritional information. 34 Sensory attributes evaluated in this study included appearance, taste, aroma, texture, and overall acceptability. Providing nutritional information, however, also translated into consumers giving additional value to orange maize. Two media channels (simulated radio messaging and community leaders) were used to convey the nutrition message. The study found that consumers valued orange maize similarly regardless of the media source, implying that radio messaging, which is significantly less costly than face-to-face message delivery, can be used to convey nutritional information. Another study, conducted with 545 rural consumers in Ghana, evaluated 108 Ann. N.Y. Acad. Sci (2017) C 2017 New York Academy of Sciences.

6 Amy Saltzman et al. Biofortification: evidence and potential similar sensory attributes to the study in Zambia, and found that consumers valued kenkey made with orange maize less than kenkey made with either white or yellow maize, but the provision of nutrition information reversed this preference. An information campaign will therefore be key to driving consumer acceptance of orange maize in Ghana. 35 In Nigeria, a consumer-acceptance study conducted in the Imo and Oyo States tested yellow cassava gari (a popular dried, slightly fermented, granulated form of cassava) against local gari. The local gari tested against was white in Oyo, where 343 consumers participated in the study, but yellow (mixed with red palm oil) in Imo, where the study sample size was 328 consumers, in accordance with regional preferences. 36 The sensory attributes evaluated included the color, feel, and taste of gari,inboth states. In Oyo, consumers often drink gari, therefore drinking quality was also evaluated in that state. In Imo State, local (i.e., yellow) gari was preferred to the gari made with either light- or deeper-colored yellow cassava varieties. Once consumers were told about the nutritional benefits of yellow cassava, however, gari made with the deeper-colored yellow cassava was preferred. Nutrition campaigns are very important in this state. In Oyo State, consumers preferred the gari made with light yellow cassava over local (i.e., white) gari, even in the absence of nutritional information. Once consumers received information about the nutritional benefits of yellow cassava varieties, light-colored yellow cassava remained the most popular variety, but gari made with deeper-colored yellow cassava was preferred over the local variety. In Oyo, the light-colored yellow cassava could become a popular variety even without nutrition campaigns. These results also allude to the diverse preferences that are evident in large countries, such as Nigeria, and highlight that no single approach or variety could be universally applied in such settings. Another study on yellow cassava, this time in Kenya, was conducted with 30 caregivers (18 45 year olds) and 30 children (7 12 year olds). The study showed that both groups preferred yellow cassava over white cassava because of its soft texture, sweet taste, and attractive color. 37 More recently, a yellow cassava acceptance study was conducted in the western provinces of the Democratic Republic of Congo. 38 This study tested consumer acceptability and preference of traditional products (fufu and chikwangue)made with white cassava and biofortified yellow cassava among 947 respondents in urban Kinshasa and Bas Congo provinces. Results revealed that biofortified chikwangue has the greatest potential among biofortified products evaluated. The study also found that, to improve acceptability and preference of biofortified products, in particular fufu made with yellow cassava, the nutritional and socioeconomic benefits of yellow cassava should be strongly promoted. Consumers similarly like iron-biofortified crops, though the nutrition trait is invisible. Studies have been conducted for iron pearl millet in India and iron beans in Rwanda and Guatemala. In rural Maharashtra, India, bakhri made with iron pearl millet and market-purchased pearl millet was evaluated by 452 consumers. 39 The results revealed that, even in the absence of information about the nutritional benefits of iron pearl millet, consumers liked the sensory attributes of the grain and bakhri of the iron pearl millet variety as much as (if not more than) those of the conventional variety. The sensory attributes tested in this study included color and size of the pearl millet grain and the color, taste, layers, and ease of breaking of the bakhri. Nutritional information, however, significantly increased consumer preferences for iron pearl millet varieties. Consumer-acceptance studies conducted on 1150 consumers in rural Rwanda showed that, even in the absence of nutritional information, consumers in the western and northern provinces liked the sensory attributes of two of the iron bean varieties tested more than the local variety. 40 In urban retail markets, 659 consumers were interviewed, and it was found that these consumers preferred one of the iron bean varieties more than the local and other iron bean variety tested. The sensory attributes tested in this study included raw bean dryness, color and size; cooked bean size, taste, and ease of breaking in both rural and urban areas; and cooking time and overnight keeping quality in rural areas. In both rural and urban markets, information on the nutritional benefits of iron bean varieties had a positive effect on consumers premium for each of the iron bean varieties tested. Similar research in Guatemala, conducted on 360 rural consumers, found that consumers equally preferred the sensory attributes of iron bean to the local bean varieties tested. 41 Sensory attributes tested in that study included raw bean color and size, cooked bean taste and size, and overall acceptability. Ann. N.Y. Acad. Sci (2017) C 2017 New York Academy of Sciences. 109

7 Biofortification: evidence and potential Amy Saltzman et al. Future potential Mainstreaming Full proof of concept that biofortification using the conventional plant breeding approach works will pave the way for mainstreaming and long-term sustainability. In the coming years, biofortification is expected to be increasingly integrated into international and national crop-development programs, crop and food value chains, and national policies and standards. Crop development has already been initiated to develop biofortified varieties of several secondary staple crops, such as zinc and iron sorghum, lentil, cowpea, and Irish potato and vitamin A banana. HarvestPlus investments have filled breeding pipelines with varieties that are agronomically competitive or disease resistant, have preferred end-use qualities, and have full target levels of micronutrients. To sustain this investment, international research centers that are members of the CGIAR consortium and national agricultural research system (NARS) partners must mainstream biofortification, using micronutrient-dense materials throughout their breeding programs. This will ensure that biofortification is sustainable and that new, climateadaptive varieties also contain the micronutrient traits. Director generals of CGIAR centers have committed to mainstreaming biofortification in their conventional food crop development programs. 42 Demand for biofortified seeds continues to grow from a wide variety of partners, including governments, private seed companies, international nongovernmental organizations, and multilateral agencies. In countries with robust formal seed systems that reach smallholder farmers, private seed companies are a natural partner. This approach is particularly advantageous in the case of crops where hybrid seeds predominate (e.g., Seed Co. in Zambia (hybrid maize) and Nirmal Seeds in India (hybrid pearl millet)) and where seed companies operate regionally. In these partnerships, private seed companies participate in crop-development activities and multiply, market, and sell certified seed. HarvestPlus provides training, technical assistance, marketing support, and some limited purchase guarantees to help mitigate risk in the initial stages of delivery. Additionally, a partnership has been developed with World Vision to introduce biofortified crops into its agricultural programs, which are then linked to its health/nutrition programs, whereby World Vision takes the lead and HarvestPlus offers technical assistance, as needed. The World Food Programme s Purchase for Progress program is very interested in local purchasing of biofortified crops, and partnerships are being developed in several countries to link farmers to these markets. Significant progress has already been made in integrating biofortification into regional and national policies. At the Second International Conference on Nutrition in 2014, representatives from Bangladesh, Malawi, Nigeria, Pakistan, and Uganda highlighted the role of biofortification in their national strategies to end malnutrition by Panama and Colombia were among the first countries to include biofortification in their national food security plans. Since the Second Global Conference on Biofortification in 2014, biofortification has been included in national nutrition strategies in Rwanda, Zambia, and Nigeria. HarvestPlus and its partners are engaged with regional and global processes, like the African Union s Comprehensive Africa Agriculture Development Programme and the Scaling Up Nutrition movement, to ensure an enabling environment for biofortification. Efforts to include biofortification in global standards and guidelines for food products and labeling, such as the Codex Alimentarius, are well underway. A tool for informing future investments As evidence in favor of biofortification using the conventional plant breeding approach builds, and following the success of the Second Global Conference on Biofortification and the resultant Kigali Declaration on biofortified nutritious foods, various stakeholders are increasingly interested in investing in this intervention as a cost-effective means for reducing hidden hunger. 40,43 These stakeholders include donor agencies and international and national nongovernmental and government organizations from both agricultural and health sectors, as well as private seed and food companies. These stakeholders need evidence-based information on where to target specific biofortified crops to most cost-effectively achieve the highest nutrition, and hence health, impacts. To assist these stakeholders with their biofortification investments, HarvestPlus has developed a country crop micronutrient specific BPI. 44 The global BPI is a tool that ranks each of the seven 110 Ann. N.Y. Acad. Sci (2017) C 2017 New York Academy of Sciences.

8 Amy Saltzman et al. Biofortification: evidence and potential Figure 1. Biofortification priority index for vitamin A maize. aforementioned staple crops according to its suitability for investment in biofortification in 127 countries in Africa, Asia, and Latin America and the Caribbean. The BPI is calculated using secondary country-level data compiled from various sources, including the FAO, the World Health Organization (WHO), and the United States Department of Agriculture. Similar to the Human Development Index and Global Hunger Index, the BPI also comprises three subindices. The production subindex calculates the extent to which a country is a producer of the staple crop, while factoring in the amount of output retained for domestic consumption (production subindex = (1/2 per capita area harvested + 1/2 agricultural land allocated to the crop) (1 export share)). The consumption subindex captures the proportion of the crop under domestic production that is consumed by the country s population (consumption subindex = consumption per capita per year (1 import share)). The micronutrient deficiency subindex calculates the extent to which a country s population suffers from the respective micronutrient deficiency (i.e., vitamin A (micronutrient deficiency subindex (vitamin A) = 1/2 proportion of preschool-age children with serum retinol less than 0.7 mol/l +1/2 agestandardized disability-adjusted life years (DALYs) per 100,000 inhabitants lost to vitamin A deficiency), zinc (micronutrient deficiency subindex (zinc) = 1/2 percentage of population at risk of inadequate zinc intake +1/2 prevalence of stunting among children 6 59 months), or iron (micronutrient deficiency subindex (iron) = 1/2 proportion of preschool-age children with Hb < 110 g/dl +1/2 age-standardized DALYs per 100,000 inhabitants by iron-deficiency anemia)). The BPI allows stakeholders to identify top, high, medium, low, and little/no priority countries for investment in each biofortified crop. HarvestPlus recently developed an online and interactive BPI tool, which is a global map that illustrates countries that are most suitable for biofortification investment for the aforementioned seven crops, based on their BPI rankings (this tool can be accessed at A sample global BPI map for vitamin A fortified maize is presented in Figure 1. Overall, the BPI figures show that African countries rank highest for vitamin A rich crops and Asian countries rank highest for zinc-rich cereals. For iron-biofortified beans, several countries in Africa and some in Latin America and the Caribbean surface as high return-on-investment potentials, and, for iron-biofortified pearl millet, both Africa (especially West Africa) and South Asia are suitable candidate sites for investment. Both the BPI rankings and the tool have been extensively used by both HarvestPlus and its partners, as well as by various stakeholders/ Ann. N.Y. Acad. Sci (2017) C 2017 New York Academy of Sciences. 111

9 Biofortification: evidence and potential Amy Saltzman et al. organizations interested in investing in biofortification. For example, breeders in several CGIAR centers collaborating with HarvestPlus have used the BPI to see for which countries/agroecologies they should breed biofortified varieties and/or adapt the already existing biofortified varieties; USAID has used this tool to identify which biofortified crops could be introduced into Feed the Future (FTF) mission countries, and similarly World Vision International has used this tool to select the countries in which they will be including biofortified crops as part of their aid portfolio. Concluding remarks Over the past 15 years, conventional breeding efforts have resulted in the development of varieties of several staple food crops with significant levels of the three micronutrients that are most limiting in diets: zinc, iron, and vitamin A. Evidence from nutrition research has revealed that these varieties provide considerable amounts of bioavailable micronutrients, and consumption of these varieties can improve the micronutrient-deficiency status among target populations. Development and delivery of these micronutrient-rich biofortified varieties, developed using the conventional plant breeding approach, can potentially reduce hidden hunger, especially among rural populations whose diets rely on staple food crops. By 2016, more than 30 countries have officially released biofortified varieties developed using the conventional plant breeding approach, and at least an additional 20 countries have commenced the testing of these varieties. The CGIAR and its centers have included biofortification in many plant breeding programs and increasingly provide biofortified varieties as a public good to NARSs. While biofortification is being increasingly mainstreamed on the supply side, there is also a growing interest in biofortification on the demand side. In the eight HarvestPlus target countries, more than four million farmers have been reached with biofortified seeds. In Rwanda, for example, by 2015, about 29% of bean farmers had planted iron beans in at least one season over the past eight seasons, and about one fifth of bean-growing farmers allocated some of their bean area to iron beans in the first season of Farmer feedback and participatory evaluation research reveal that farmers like the various production and consumption characteristics of biofortified varieties, as much as (if not more than) their most popular conventional varieties. Similarly, consumer-acceptance research shows that consumers like the various organoleptic characteristics of biofortified varieties as much as conventional ones, often even in the absence of nutritional information, while informing consumers about the benefits of biofortified staple food crops improves demand for these varieties. Moreover, consumer-acceptance research also reveals that the different (yellow or orange) color of provitamin A biofortified crops (i.e., yellow cassava, OSP, and orange maize) is not a hindrance to consumer acceptance. Demand for biofortified crops and food will be further enhanced when major players in the food-value chain, such as international food processors and supermarket chains, become interested in aggregating and processing biofortified products to serve more urban clientele. However, the prime potential of biofortification is and will be to address hidden hunger among the farming and rural populations. In the future, it will be important not only to focus on strengthening domestic supply and demand of biofortified staple food crops, targeted to those crop country combinations identified by the BPI, but also to facilitate and strengthen international trade. On the supply side, regional agreements for the testing and release of varieties could reduce nontariff trade barriers in international trade of seed and allow spillover of technology from pioneer countries in biofortification to neighboring countries. For international trade in biofortified raw material as well as processed food to take off, standards will need to be developed (e.g., under the Codex Alimentarius). However, voluntary standards developed by the multinational food companies will certainly also contribute to the spread of biofortification over time. Using biofortified raw products may potentially complement fortification efforts by the food industry and can also lead to synergetic outcomes for markets and target clientele, which are part of the formal food chain. Acknowledgments We are grateful to Howarth (Howdy) E. Bouis for conceptualizing the idea of biofortification and for his tenacious efforts to bring it to life. The evidence summarized in this paper shows that perseverance pays off, and interdisciplinary efforts 112 Ann. N.Y. Acad. Sci (2017) C 2017 New York Academy of Sciences.

10 Amy Saltzman et al. Biofortification: evidence and potential can be powerful if not always harmonious game changers. A.S. and E.B. wrote the initial draft of the manuscript and had primary responsibility for the final content. D.A.M. and C.G. contributed to the section entitled A tool for informing future investments, M.T.D. and A.O. contributed to the sectionon Adoptionandconsumptionevidence, M.M. contributed to the section on Nutrition evidence, M.S.A. contributed to the section entitled Breeding evidence, K.L. contributed to the introduction, and M.Z. contributed to the conceptualization of the paper and drafting of the concluding remarks. All authors contributed to the development of this manuscript and read and approved the final manuscript. We are also grateful to Caitlin Herrington, Salomon Perez, and Jose Funes for their contributions to various studies summarized in this paper. This publication was made possible with support from HarvestPlus. HarvestPlus s principal donors are the U.K. Government, the Bill & Melinda Gates Foundation, the U.S. government s FTF initiative, the European Commission, and donors to the CGIAR Research Program on Agriculture for Nutrition and Health. This manuscript was presented at the WHO/FAO technical consultation Staple crops biofortified with vitamins and minerals: considerations for a public health strategy, convened on April 6 8, 2016 at the Sackler Institute for Nutrition Science, New York Academy of Sciences in New York, New York. This paper is being published individually but will be consolidated with other manuscripts as a special issue of Annals of the New York Academy of Sciences, the coordinators of which were Drs. Maria Nieves Garcia-Casal and Juan Pablo Peña-Rosas. The special issue is the responsibility of the editorial staff of Annals of the New York Academy of Sciences,who delegated to the coordinators preliminary supervision of both technical conformity to the publishing requirements of Annals of the New York Academy of Sciences and general oversight of the scientific merit of each article. The workshop was supported by the WHO, the FAO, and the Sackler Institute for Nutrition Science at the New York Academy of Sciences. The authors alone are responsible for the views expressed in this paper; they do not necessarily represent the views, decisions, or policies of the institutions with which they are affiliated or the decisions, policies, or views of the WHO. The opinions expressed in this publication are those of the authors and are not attributable to the sponsors, publisher, or editorial staff of Annals of the New York Academy of Sciences. Conflicts of interest The authors declare no conflicts of interest. References 1. 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