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The social and economic impact of biofortification


through genetic modification
Hans De Steur1, Matty Demont2, Xavier Gellynck1 and
Alexander J Stein3

Genetic modification (GM) has been advocated as an application of mineral fertilizer. Given the existing liter-
alternative or complement to micronutrient interventions such ature [1,2,3], here we focus on GM biofortification.
as supplementation, fortification or dietary diversification.
While proof-of-concept of various GM biofortified crops looks Evidence of the value of biofortification through conven-
promising, the decision tree of policy makers is much more tional breeding (and related dissemination efforts) as a
complex, and requires insight on their socio-economic successful nutrition and public health intervention in
impacts: Will it actually work? Is it financially sound? Will people South-East Asia, Sub-Saharan Africa and Latin America,
accept it? Can it be implemented in a globalized world? is growing (for a progress report on conventional breeding
This review shows that GM biofortification could effectively efforts for biofortification, see Ref. [3]). This has been
reduce the burden of micronutrient deficiencies, in an clearly acknowledged at the WHO/FAO Technical con-
economically viable way, and is generally well received by sultation on biofortification in April 2016 [4]), and further
target beneficiaries, despite some resistance and uncertainty. exemplified when the pioneers of provitamin A-enriched
Practically, however, protectionist and/or unscientific orange-fleshed sweet potato (OFSP) were given the
regulations in some developed countries raise the (perceived) 2016 World Food Prize for their long-standing work to
bar for implementation in target countries. deploy this staple crop to nearly two million African
households. In the future, also the large-scale deployment
of other conventionally bred varieties could increase.
Addresses
1
Department of Agricultural Economics, Faculty of Bioscience When it comes to genetic engineering to increase the
Engineering, Ghent University, Coupure Links 653, B-9000 Ghent,
nutritional value of staple crops, while an increasing
Belgium
2
International Rice Research Institute (IRRI), DAPO Box 7777, number of successful efforts have been undertaken
Metro Manila, Philippines [5], no such crops have been introduced yet. Awaiting
3
DG MARE, European Commission, Brussels, Belgium the first approval and release of provitamin A-rich
‘Golden Rice’ and other genetically modified (GM) bio-
Corresponding author: Demont, Matty (m.demont@irri.org)
fortified crops, like multi-biofortified ‘BioCassava’ [6],
researchers have nevertheless attempted to examine their
Current Opinion in Biotechnology 2017, 44:161–168 economic value in various ways. This review focuses
This review comes from a themed issue on Plant biotechnology on evidence and key literature on health impacts and
Edited by Dominique Van Der Straeten, Hans De Steur and Teresa
cost-effectiveness, willingness-to-pay (WTP) and trade
B Fitzpatrick impacts of these crops. As such, this overview comple-
ments new/ongoing reviews focusing on nutritional
For a complete overview see the Issue and the Editorial
aspects [7].
Available online 21st February 2017
http://dx.doi.org/10.1016/j.copbio.2017.01.012
0958-1669/ã 2017 Elsevier Ltd. All rights reserved. Impact and cost-effectiveness
Biofortified crops are not ordinary consumer goods in that
they do not satisfy an obvious want but rather a hidden
health need. On the market place consumers may there-
fore not differentiate between non-biofortified and
biofortified crops, or they may not be prepared to pay a
Introduction higher price for biofortified crops. As such, biofortified
Building upon more than two decades of related research, crops (i) have an added nutrition dimension, which puts
the proof-of-concept and potential impact on public them into the realm of public health interventions; and
health of biofortification – that is, the enhancement of (ii) they target food insecure and poor population groups
the nutrient content of crops as opposed to the addition of in developing countries, which means their beneficiaries
nutrients to food during processing – has been established may not have sufficient purchasing power to create the
for a variety of crops and micronutrients; in particular demand needed for market actors to actually supply
this can be achieved through conventional breeding these crops, even if they are aware of their nutrition
(cross-breeding), genetic modification (GM), or the benefits.

www.sciencedirect.com Current Opinion in Biotechnology 2017, 44:161–168


Current Opinion in Biotechnology 2017, 44:161–168

162 Plant biotechnology


Table 1

Potential impact and cost-effectiveness of GM biofortified crops (and alternative interventions or benchmarks reported in different studies)

Biofortified crop (country) Impact Cost-effectiveness Profitability


Dawe et al. [16] Provitamin A ‘Golden’ Rice, 1st VA intake increases by 2–8% of current US$ 4–7 per million RAE provided (VA
generation (Philippines) intake supplementation = US$ 30–73 per
million RAE)
Zimmermann and Provitamin A ‘Golden’ Rice, 1st Burden of VAD decreases by 6–32%; 15 000–85 000 DALYs saved per year a 66–133% rate of return on R&D
Qaim [10] generation (Philippines) investments
Stein et al. [11] Provitamin A ‘Golden’ Rice, 2nd Burden of VAD decreases by 9–59%; US$ 3–19 per DALY saved (other VA 29–93% rate of return (international
Stein et al. [17] generation (India) 204 000–1 382 000 DALYs saved per year interventions = US$ 84–1860 per DALY agricultural R&D investments =
saved) 17–35%)
De Moura et al. [18] Provitamin A ‘Golden’ Rice, 2nd Impact: prevalence of VAD decreases by 71–78% in Bangladesh and by 30–60% in Indonesia and the Philippines
generation (Bangladesh,
Indonesia, Philippines)
Changat and Protein-rich potato (‘protato’) Impact: protein content increases by up to a third, and levels of essential amino acids increase significantly; protein intake should
Krishna [19] (India) increase and reduce the prevalence of PEM
Krishna and Qaim [20] Bt eggplant (India) b Impact: consumers benefit from a technology-induced decrease in eggplant prices; since eggplant is an important vegetable in low-
income households in India, this price decrease is pro-poor as positive nutritional effects can be expected from concomitant
increases in vegetable consumption
De Steur et al. [21] Folate-enriched rice (China) Impact: burden of folate deficiency decreases by 37–82%
De Steur et al. [22] Folate-enriched rice (China) Burden of folate deficiency decreases by US$ 21–64 per DALY saved
20–60%
Chow et al. [23] Provitamin A ‘Golden Mustard’ 905 000–1 685 000 DALYs saved per year US$ 92–171 per DALY savedc 21–42% rate of return
(India, rural areas of 16 (out of 29) (expanding supplementation = 635 000– (supplementation when fixed costs of (supplementation = 68–104%,
states and 8 urban areas) 1 380 000 DALYs saved) expanding services are ignored = US industrial fortification = 6–22%)
$23–50 per DALY saved)
Henley et al. [24] Transgenic biofortified sorghum Impact: PDCAAS doubles, while iron, zinc and provitamin A levels are expected to increase; young children should be able to meet
(Sub-Saharan Africa) most of their protein requirements from biofortified sorghum porridge
Nguema et al. [25] Multi-biofortified ‘BioCassava’ Burden of VAD and iron deficiency US$ 4–5 and US$ 56–87 per DALY saved in Nigeria and Kenya, respectively (other
(Nigeria, Kenya) decreases by 6% and 3% in Nigeria and VA interventions in Africa = US$ 41–52 per DALY)
Kenya, respectively
De Steur et al. [26] Multi-biofortified rice (China) Burden of VA, zinc, iron and folate US$ 2–10 per DALY saved
deficiency decreases by 11–46%
Fiedler et al. [12] High-provitamin A and high-iron Burden of VAD and IDA decreases by 3– US$ 50–77 per DALY saved (World 29–34% rate of return
banana (Uganda) 5%; 8600–12 900 DALYs saved per year Bank benchmark = US$260 per DALY,
WHO benchmark = US$1380 per DALY
saved)

Bt, Bacillus thuringiensis; VA, vitamin A (retinol); US$, United States dollar; RAE, retinol activity equivalents; VAD, VA deficiency; R&D, research and development; DALY, disability-adjusted life year;
PEM, protein-energy malnutrition; PDCAAS, protein digestibility corrected amino acid score; IDA, iron deficiency anemia; WHO, World Health Organization.
www.sciencedirect.com

a
DALYs is a common metric used in public health research to quantify the burden of a disease, illness or injury in terms of life years that are lost due to premature mortality as well as to morbidity (in
which case the severity of the condition is taken into account and the time spent with it is expressed as fractions of life years) [27,28,29].
b
Bt eggplant is a pest-resistant, first generation GM crop that is not a biofortified crop in the true sense, but it was included to show that other GM crops can have positive nutrition effects.
c
The authors only report incremental cost-effectiveness, but for better comparability across the studies, we calculated the stand-alone cost-effectiveness of Golden Mustard.
The social and economic impact of biofortification through genetic modification De Steur et al. 163

Therefore impact assessments are needed to capture the lower than in India (Table 2). In India there are more
nutrition benefit that may not be fully priced in a market individuals suffering from vitamin A deficiency than in
setting [8]. Cost-effectiveness analyses (CEAs) are the Philippines, and the Indian study assumed higher
required to compare the outcomes of biofortification with provitamin A-levels in the rice because by then a second
the costs for the development and dissemination of the generation of Golden Rice had been bred already. Con-
crops. By juxtaposing benefits and costs in a consistent sequently, the projected impact in terms of disability-
way, CEAs help policy-makers prioritize interventions adjusted life years (DALYs) saved in India is higher
for implementation while taking into account financial (DALYs are a metric for the burden of disease that takes
constraints. Cost-benefit analyses, which are less common into account the severity and duration of a condition to
in this context, express both benefits and costs in mone- express how many ‘healthy’ life years are lost—in this
tary terms and indicate the overall profitability of an case due to vitamin A deficiency). Additional differences
investment. can also arise because for cost-benefit analyses, the impact
of biofortification cannot be expressed in DALYs, which
Overall, CEAs indicate that GM biofortified crops are are the same across countries, but these have to be
interventions that offer good value for money and are converted into monetary terms. This can lead to biases,
often more cost-effective than alternative or complemen- for example, if different national per-capita incomes are
tary interventions (Table 1). These results are in line with used for this conversion [14,15].
conventional breeding efforts [9], and are also robust
when key assumptions are varied in sensitivity analyses Willingness-to-pay (WTP)
[10,11,12]. GM biofortified crops therefore represent Foods genetically engineered to provide nutritional ben-
sensible investments that increase public health and efits hold great promise for those seeking alternative
welfare. This can be explained with the rationale of strategies to tackle malnutrition. Consumer studies on
biofortified crops [1,2]: While other micronutrient foods with nutritional benefits [30] and/or GM foods
interventions incur recurrent costs (e.g., for supplements, [31,32] have shown a wide variety of concepts that can
fortificants or distribution), biofortification requires a big be measured to determine consumer reactions, for exam-
upfront investment into the breeding programs, but once ple, attitude, perceptions, beliefs, (sensory) acceptance,
the germplasm has been developed, benefits can be purchase intentions, willingness-to-accept (WTA) or
reaped year-on-year and across countries with only lim- WTP, of which the latter is commonly used in bioforti-
ited ancillary costs as biofortified seeds can ‘piggy-back’ fication studies. Regardless of the WTP method applied
on the normal seed distribution systems and be re-used by (such as experimental auctions), consumers’ WTP reflects
farmers (In the case of crops that are biofortified with the premium a consumer is prepared to pay for GM
provitamin A and therefore possibly change color, more biofortified crops. In other words, it measures the amount
intense education campaigns may be required. On the (%) consumers are willing-to-pay more for GM bioforti-
other hand, because of economies of scale, multi-biofor- fied crops as compared to non-biofortified crops.
tified crops will be more cost-effective).
Table 2 summarizes evidence from 10 WTP studies.
Moreover, other micronutrient interventions have their Overall, consumer studies indicate a high WTP for
own limitations – for example, supplementation requires GM biofortified foods. When information on vitamin
that beneficiaries are reached by public health services, levels or benefits is provided, consumers are prepared
and only commercial foodstuffs are fortified – this means to pay a premium of 20% or more in nearly all studies.
poor people in remote rural areas are hardly covered by While this corresponds with WTP studies on biofortifica-
common micronutrient interventions. Even buying tion through conventional breeding [33], as well as
enough fruit and vegetables to meet nutrition guidelines on other potential GM crops with health benefits, it gener-
requires a higher percentage of income in rural areas than ally contradicts research on GM crops with farmer benefits
in urban areas [13]. In contrast, biofortification is self- [34], for which consumers generally demand a discount of
targeting in that crops are grown in rural areas, and staples 29% (relative to non-GM crops) [35]. In other words,
are eaten in large quantities by poor people. It is therefore consumers reactions toward GM crops are much more
economies of scale as well as their wider coverage that set positive when direct consumer benefits are involved.
breeding approaches apart.
These positive findings, however, refer to cases where no
The impact of biofortified crops depends also on how specific information on the applied GM technology (i.e.,
much of a given micronutrient can be engineered into a positive, negative and/or objective statements) is pro-
crop, how much of the crop is eaten by the target vided. While WTP for GM biofortified foods is still
population, how bioavailable the micronutrients are, relatively high when consumers receive one-sided, posi-
and how many individuals suffer from the underlying tive information on GM technology, the provision of
deficiency. For instance, this can explain why the impact negative information results in lower premiums or nega-
of Golden Rice in the Philippines was projected to be tive values (i.e., discounts), even in the case of dual

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164 Plant biotechnology

Table 2

Consumers’ willingness-to-pay for GM biofortified crops according to provided information, in % premium for GM biofortified food

Biofortified crop (country)


Nutrition GM technology information g
information f
Vitamin Benefits Positive Negative Dual Dual + Objective
a
Transgenic biofortification
Lusk [37] b Provitamin A ‘Golden’ Rice (US) 20
Lusk and Rozan [38] b Provitamin A ‘Golden’ Rice (US) 38
Deodhar et al. [39] b Provitamin A ‘Golden’ Rice (India) 20 h
Kajale and Becker [40]b,d Provitamin A ‘Golden’ Rice (India) 4
Corrigan et al. [41]c,d Provitamin A ‘Golden’ Rice (Philippines) 33 53 7 20
Depositario et al. [42] b Provitamin A ‘Golden’ Rice (Philippines) 40 60
13 27
Gonzalez et al. [45] b Provitamin A Cassava (Brazil) 64/70
De Steur et al. [43] b B9 ‘Folate’ Rice (China) 34
De Steur et al. [44]c,e B9 ‘Folate’ Rice (China) 33 31 10 26(17h) 17 i
Colson et al. [49] c Vitamin C Potato (US) 62 14 0
22 20
Vitamin C Broccoli (US 33 38 12
12 6
Vitamin C Tomato (US) 25 28
21 3 15
Kassardjian et al. [46] c Vitamin C Apple (New Zealand) 48
Intragenic biofortification a
Colson et al. [49] c Vitamin C Potato (US) 61 50 13 2
12
Vitamin C Broccoli (US) 35 94 27 13
12
Vitamin C Tomato (US) 40 77 18 17
11

GM, genetic modification; US, United States.


Note: The values (in %) refers to the amount (i.e., premium) consumers are willing to pay more for a GM biofortified crop as compared to the non-
biofortified crop. Depending on the study, consumers received different types of information about the GM biofortified crop. When an information
treatment is not provided to consumers, an empty cell is shown.
a
Intragenic and transgenic biofortification refer to the use of GM techniques by which genes from, respectively, closely related species and species
not capable of sexual hybridization are transferred into the targeted crop.
b
Premium values are derived from a survey (i.e., open or closed-ended WTP questions) (see Supp. Table 3 in [5] for detailed information).
c
Premium values are derived from an experiment (auction or choice experiments) (see Supp. Table 3 in [5] for detailed information).
d
Based on a student sample.
e
Based on a sample of women of childbearing age; data also based on Ref. [50]).
f
Participants received information on the increased vitamin level, either alone (Vitamin) or together with its health benefits due to (Benefits).
g
Consumers received information about positive, negative and/or objective (science-based verifiable) statements related to GM technology (for detailed
information, see individual studies). Dual information refers to the provision of positive statements, followed by negative statements on GM technology.
h
Here, % premium levels are provided by consumers who first received negative information, followed by positive information about GM technology.
i
When only objective information is provided (not presented here), the premium consumers are willing to pay is higher (25% as compared to 17%,
i.e., when also dual information is given).

information, that is, when also positive information is is prevalent. This is particularly the case for already exist-
given. The power of negatively framed information, ing applications, like Golden Rice and folate (Vitamin B9)
which is inherent to the current reality of negative GM biofortified rice. Regarding the former, potential consumer
campaigning, is no surprise given the adverse effect of demand was assessed in the United States [37,38], India
risk communication on GMOs (genetically modified [39,40] and the Philippines [41,42], each by two different
organisms) [36], regardless of whether the information studies. Without giving specific information about GM
is scientifically underpinned. technology, consumers are prepared to pay between
20% and 40% more for Golden Rice than its regular
A comparison of GM biofortification studies targeting counterpart (except for the latest Indian study). Similar
different crops, vitamins and regions should be done with premium levels (34%) were reported for folate rice in a
scrutiny. Nevertheless, the positive findings that can be folate deficient region of China [43,44]. The large con-
drawn from studies looking at consumers in poor, devel- sumer interest in high-risk regions was further demon-
oping regions lend support for the introduction of GM strated for vitamin A cassava in North-East Brazil, where
biofortified crops where related micronutrient malnutrition WTP values up to 70% were reported [45].

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The social and economic impact of biofortification through genetic modification De Steur et al. 165

Furthermore, regarding the type of breeding approach, domestic gains from current GM crops with farmer ben-
one study shows that consumers are willing to pay more efits [52].
for GM biofortified crops when genes are transferred from
closely related species (intragenic breeding) rather than However, the trade argument has received limited atten-
from non-closely related species (transgenic breeding) tion in the literature on second-generation GM bioforti-
[46]. Given consumers’ different reactions toward the fied crops. On the one hand, while first-generation GM
applied breeding approach, future research should deter- crops mainly targeted non-food (feed and fiber) markets,
mine how novel, more precise genome-editing tools like second-generation GM biofortified crops mainly target
CRISPR/CAS9 [47], which most likely will influence the food markets for which approval, labeling, private-sector
GMO debate [48], will affect consumers reactions. standards, and market acceptance would matter even
more. On the other hand, second-generation GM biofor-
Even though a certain segment of the population may be tified crops are tailored to subsistence farmers and con-
still reluctant toward such GM crops, the high premiums sumers, and most of the currently developed crops are not
consumers are on average willing to pay for GM bioforti- major traded commodities in the targeted countries
fied crops provide an important indication of their market (Tables 1 and 2; [2]; Supp. Table 2 in [5]). This
potential. Therefore, it will be crucial for decision-makers means opposition to the approval of GM (biofortified)
to use these findings as a means to prioritize GM biofor- crops is mainly due to either external lobbying by inter-
tification as a health intervention, in order to ensure that national NGOs or due to the particular political economy
GM biofortified crops are consumed as widely as possible in the target country, where beneficiaries of biofortified
within the target populations. crops are poor and dispersed, whereas the potential losers
from trade problems that might arise from GMOs (e.g.,
Trade and regulations through adventitious presence and the rejection of ship-
First-generation GM technologies mainly targeted farm- ments by importing countries) are well-organized and
ers through increased production efficiency (increased politically influential, even if the overall loss of social
yields and reduced costs), and benefited consumers indi- welfare would be minor.
rectly through lower prices [51], while second-generation
GM technologies such as biofortified crops aim at benefit- Finally, GM biofortified crops are typically developed by
ing consumers more directly through nutrition and health public institutes in the context of humanitarian projects,
benefits [52]. Being developed by private companies for where the actual concern is to deliver the technology in
the biggest seed markets, first-generation GM crops were the hands of the targeted populations. The success of the
major, internationally traded commodities (e.g., soybean, latter crucially hinges on (i) the presence of well-devel-
maize, cotton, and canola) [53]. As a result, benefits were oped seed sectors and seed markets for dissemination,
shared internationally [54]. Trade studies are particularly and (ii) the development of value chains that are able to
relevant for these crops because impacts could be segregate, label and differentiate these crops from con-
affected by trade-related regulations specific to GM crops ventional crops, change consumer behavior (e.g., in the
and derived products [54], restrictions of trade due to case of visible traits such as Golden Rice and orange sweet
heterogeneity and asynchronicity in approval [55], and potato), and inform consumers about the benefits of GM
heterogeneity in food labeling policies [56], GM-free biofortified crops [2]. Since many of the current GM
private standards [57], and market acceptance [58]. biofortified crops are targeted to traditional food value
Potential trade restrictions are a major impediment to chains in developing countries, the success of GM bio-
the approval of GM technologies, although studies show fortified crops will crucially hinge on value chain upgrad-
that the economic argument is overstated in many cases. ing, development of standards and vertical coordination
Gruère et al. [53] reviewed the literature on global trade in order to efficiently govern quality and identity of GM
effects of first-generation GM crop adoption and came to biofortified crops from seed to plate.
three general conclusions. First, in the absence of GM
crop-specific trade regulations, countries that adopt GM Challenges and research needs
crops and countries that import these crops will typically The case of GM biofortification demonstrates the impor-
gain, while exporting countries that do not adopt GM tance of socio-economic analysis as a means to estimate
crops may lose. Secondly, the introduction of GM crop- future impacts and barriers of commercialization, while
specific trade regulations reduces welfare gains, espe- providing a basis for decision-making of key stakeholders
cially for non-adopters. Finally, importers’ regulations and health planners in particular. Researchers can and
can reduce gains for exporting adopters, but these losses should advance the aforementioned research domains in
are usually dwarfed by the large domestic gains from several ways, for example, by incorporating other micro-
adopting GM crops. This argument is even stronger in the nutrient strategies [59], evaluating combinations of
case of biofortified GM crops, as they target domestic farmer and consumer-oriented traits [60], assessing
consumers and are generally not intended for trade. For multi-biofortification [26] or food basket approaches
those crops, domestic welfare gains far exceed the (delivering a variety of biofortified crops together) [3],

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166 Plant biotechnology

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HDS conceived the overall manuscript and contributed the section on First detailed (household-level) cost-effectiveness analysis of a GM
willingness-to-pay and the general sections, MD contributed the section on biofortified crop, showing that such crops can have a significant impact
trade and revised the manuscript, XG reviewed the final manuscript, AJS on public health at a competitive price; including supplementary online
contributed the section on cost-effectiveness and the graphical abstract and information with further, more detailed discussion.
revised the manuscript.
12. Fiedler JL, Kikulwe EM, Birol E (Eds): An Ex Ante Analysis of the
Impact and Cost-effectiveness of Biofortified High-provitamin A
We did not receive any financial support for this work. and High-iron Banana in Uganda. IFPRI Discussion Paper 1277.
International Food Policy Research Institute (IFPRI); 2013.

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Current Opinion in Biotechnology 2017, 44:161–168 www.sciencedirect.com

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