Toxicology and Applied Pharmacology 207 (2005) S19 S27 www.elsevier.

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Review

What determines the acceptability of genetically modified food that can improve human nutrition?B
Iain F.H. Purchase*
University of Manchester, Oxford Road, Manchester M13 9PT, UK Received 15 July 2004; accepted 20 December 2004 Available online 27 June 2005

Abstract It has been predicted that by 2025 there will be an annual shortfall of cereals for feeding the human population of 68.5 million tonnes. One possible solution is the use of genetically modified (GM) crops, which are already grown extensively (59 million ha of GM crops were planted in 2002) in the USA, South America, Africa and China. Nevertheless, there is considerable disagreement about the advisability of using such crops, particularly in Europe. Obviously, the safety of the food derived from the GM crops is a primary consideration. Safety assessment relies on establishing that the food is substantially equivalent to its non-GM counterpart and specific testing for allergenicity of proteins and toxicity of metabolites and the whole food. There appears to be international agreement on the principles of safety assessment. Safety to the environment is equally important, but will not be covered in this presentation. The publics perception of the risk of new technology is critical to its acceptance. Perception of risk, in turn, depends on the credibility of the source of the information and trust in the regulatory process. In many countries, the public appears to have lost its trust in the scientists and government dealing with GM food, making the acceptability of GM crops uncertain. Of equal importance are the socio-economic factors that impinge on the viability of GM produce. These include intellectual property protection, trade liberalisation (through subsidy and tariff barriers in developed countries) and the intensity of bio safety regulations. The socio-economic interests of developed and developing countries may diverge and may even be contradictory in any one country. Acceptance of GM crops will thus depend on detailed issues surrounding particular crops and economies. D 2005 Elsevier Inc. All rights reserved.
Keywords: Genetically modified food; Safety; Public perception of risk; Socio-economic issues

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . Genetically modified foods . . . . . . . . . . . . . . . . . Is GM food safe? . . . . . . . . . . . . . . . . . . . . . . Assessment of substantial equivalence . . . . . . . . . Novel proteins. . . . . . . . . . . . . . . . . . . . . . Other constituents . . . . . . . . . . . . . . . . . . . . How do socio-economic factors influence the development, . . . . . . . . . . . . use . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . and control of . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . GM food? (Otsuka, 2003) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S20 S21 S21 S21 S21 S22 S22

i The International Union of Toxicology and the International Union of Nutritional Sciences initiated a project entitled FGenetically modified foods for human health and nutrition: the scientific basis for benefit/risk assessment_. It was supported financially by the International Council for Science and technically by the International Union of Biochemistry and Molecular Biology, International Union of Food Science and Technology, International Union of Pure and Applied Chemistry, International Union of Soil Science and the ICSU Advisory Committee on Genetic Experimentation and Biotechnology and the Committee on Sciences for Food Security. The final report was published in Trends in Food Science and Technology 14 (2003) 169 338. This article draws extensively on part of the report as is acknowledged in the references. * 79 Knutsford Road, Wilmslow, Cheshire SK9 6JH, UK. Fax: +44 1625 520325. E-mail address: ifhp@chadzombe.u-net.com.

0041-008X/$ - see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.taap.2004.12.025

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Sustainability . . . . . . . . . . . . . . . . . Development, use and control . . . . . . . . Development of GMOs . . . . . . . . . . Trade liberalisation . . . . . . . . . . . . Biosafety and labelling . . . . . . . . . . Public attitudes towards genetically modified Public attitudes . . . . . . . . . . . . . . Ethical concerns . . . . . . . . . . . . . Trust . . . . . . . . . . . . . . . . . . . Communicating uncertainty. . . . . . . . Emerging issues . . . . . . . . . . . . . Final thoughts . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . .

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Introduction Population growth is likely to increase the worlds population from 6 billion at the start of this century to 7.9 to 19.9 billion by 2025. The majority of this increase will occur in less economically developed countries (Garza and Stover, 2003). In spite of increases in crop production of about 3% per annum (The Pew Initiative, 2004), resulting from changes to agricultural practiceincluding plant breedingover the last few decades, food insecurity and the number of people suffering from undernutrition have increased. The situation is likely to become worse, with predictions that, by 2025, there will be a shortfall in worldwide cereal production of 68.5 million tonnes. This is made up from a shortfall of 307 million tonnes from Africa, Middle East, Asia and Latin America and a surplus of 461 million tonnes in Europe, North America and Oceania. Undernutrition is not limited to gross malnutrition. Micronutrient malnutrition has a considerable impact on the health and productivity of people in developing countries. For example, iron deficiency affects some 3 billion people, particularly women and children50% of pregnant women and 40% of non-pregnant women and children in poor countries are anaemic. This impairs physical growth and mental development in childhood and reduces the capacity for physical labour. Another example is vitamin A, where about 3 million children of pre-school age have visible eye damage resulting from its deficiency. An estimated 250,000 to 500,000 children go blind as a result of vitamin A deficiency and about two thirds of these children die within months of going blind (Bouis et al., 2003). One of the principal aims of producing GM crops for poorer countries is to address these issues of micronutrient malnutrition. In parallel, there is a need to reduce poverty and improve health, which in turn will assist long-term economic growth. In wealthy developed countries, consumers may spend, perhaps 10% of their income on food. They have good health care and access to a wide range of safe and healthy

food; nutrient deficiencies are infrequent. Thus, the impact of GM food on the cost of food is relatively unimportant. In contrast, in poor countries, malnutrition, nutrient deficiencies and ill health are more common. Poor consumers typically spend 70% of their income on food, and their diets consist primarily of staple foods, which lack the vitamins, minerals and possibly other nutrients necessary for good health. There exists, therefore, the opportunity to reduce costs and improve the nutritional quality of their food (Bouis et al., 2003). Implicit in the consideration of the role of GM foods in this arena is that science has a role to play in helping to tackle these issues. Specifically, transgenic modification has the potential to increase the speed and versatility of modification of crops and animals in comparison to traditional breeding methods. This is not to say that transgenic technology has all the answers, but that it has the potential to contribute to some of the solutions (Garza and Stover, 2003). GM technology has the potential to increase crop productivity, including the opportunity to grow crops in unfavourable growing environments, to reduce pesticide applications and to improve micronutrient content and availability in commonly consumed foods (Bouis et al., 2003). The traditional plant breeding methods of hybridization and cross breeding, resulting in enhancing desirable traits through genetic modification of plants, have resulted in documented improvements in productivity. The increases in food availability have had significant health benefits. However, there are no specific examples where intentional modification of plants has led to clear improvements in the health of human populations (Garza and Stover, 2003). The introduction of transgenic crops can be predicted to give rise to benefits and risks to health and the environment. The benefits to health include enhancement of food and nutritional security, more specific health benefits (such as immunization through food) and reduction in chronic diseases by manipulation of dietary composition. Health risks include toxicity, allergic reaction, nutrient imbalances and decreasing diversity of the diet. The specific risks and

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benefits to the environment are not considered here (Garza and Stover, 2003). Genetically modified foods The most widespread application of GM technology in food production arises from its application to crops. The first generation of transgenic crops provided agronomic benefits, such as insect or virus resistance, herbicide tolerance, delayed ripening and altered oil content. The total area planted to GM crops was 2 million ha in 1996, rising to 68 million ha in 2003. The main crop was soya, followed by maize, cotton and canola. It is estimated that 55 million farmers planted GM cotton in 2003. By far the largest producer of GM crops was the USA (66%) followed by Argentina (23%), Canada (6%), China (5.2%) and other countries producing 1% (South Africa, Australia, Mexico, Romania, Bulgaria, Spain, Germany, France, Uruguay, Indonesia, India, Colombia and Honduras) (The Pew Initiative, 2004). The application of genetic modification to farm animals (Sang, 2003) and fish for food production (Maclean, 2003) is currently at the research and development stage. The methods available in animals are too expensive currently for widespread use, although developments in fin fish are nearest to commercial exploitation. Microorganisms are used in various fermentation processes in food production and for the production of enzymes used as processing aids, food additives, flavours and amino acids (von Wright and Bruce, 2003). The use of GM microorganisms in food production has been slow to develop, because the final flavour and texture of food produced by fermentation depends on many genes; the modification of a single or a few genes will rarely have a predictable effect on the taste and texture of food. However, production of enzymes, food additives, flavours and amino acids by these techniques is easier. Some products are purified and have no residual genetic material from the producing microorganism, while others are more complex. In addressing the question of what makes GM food acceptable, there are three areas for review: Is the food safe? Does the public find it acceptable? and What socioeconomic impact will it have? Is GM food safe? Traditional breeding methods of altering the genetic make-up of plants have led to improvements in yield and other desirable characteristics. However, there are also examples of increased risks. Celery bred to be insect resistant was found to have increased levels of psoralens, and selective breeding of potatoes resulted in higher levels of solanines. In both cases, traditional methods of breeding resulted in potential toxicity of the new varieties (Garza and Stover, 2003). Similar unintended and unexpected hazards may follow GM methods of developing new varieties.

Genetic modification provides major advantages over traditional methods. First, the development of new varieties can be accelerated. Modification of genes can be more specific and controlled than is the case with conventional mutation and breeding methods, and genes from other varieties or species can be inserted to produce particular advantages (Kuiper and Kleter, 2003). Approaches for the hazard assessment of GM foods (derived from biotechnology) have been in preparation for many years through international collaboration of the FAO/ WHO and the OECD (Kuiper and Kleter, 2003). The toxicological methods developed for the hazard assessment of chemical entities, which rely on administration to animals of doses much higher than experienced in the environment, will not work for GM foods, where the whole food makes up much of the mass of the diet. Alternative methods have been developed, based on the premise that the use of DNA recombinant technology does not present any inherent risks because the structure of DNA is the same in all species and the transfer of genetic material between species has been a driving force in evolution (Konig et al., 2004). Hence, the methods are based on assessment of any changes of the functional and chemical characteristics that result from genetic modification. Foods generally accepted as safe, on the basis of their history of safe use (Kuiper and Kleter, 2003), are used for comparison. Assessment of substantial equivalence This describes the process where novel foods are compared with foods accepted as safe. Included in the comparison are the agronomic and morphological characteristics and the chemical composition of key nutrients and toxins or anti-nutrients present in the crop. There are several steps in this process: the characterisation of the organism (and the donor organism for transferred genes); description of the genetic modification (inserted gene, method of insertion and stability and expression of the resulting inserted gene); and the effects of the modification on the composition and morphology of the crop. On the basis of the assessment of substantial equivalence, the further toxicological assessment of the hazard from the novel food can be determined (Kuiper and Kleter, 2003). Novel proteins Following their identification, novel proteins should be characterised in terms of their structure and function. Included in this should be their similarity with other proteins and their fate after ingestion, processing and storage. Toxicological assessment will depend on the outcome of this characterisation. Usually, novel proteins will be tested in animal studies for at least 28 days. Where extraction of sufficient protein from the crop is difficult, the protein may be harvested from cell cultures. Toxicological assessment will normally include an assessment of allergenicity, based on sequence homology with known allergens, testing of stability in simulated gastric fluid and specific in

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vitro and in vivo testing for allergic potential (Kuiper and Kleter, 2003). Other constituents Any non-protein constituents will need to be assessed using traditional toxicological methods. The whole food will also need to be tested in in vivo studies, usually for at least 90 days. Recent guidance on the safety assessment of GM crops (Konig et al., 2004) builds on these concepts. A four-step process is proposed, beginning with the characterisation of the parent crop. The characterisation of the phenotype and chemical composition of the crop forms the first step. The OECD is compiling information considered to be of most relevance to the characterisation of the parent crop for this purpose. The second step is the provision of information on the transformation process, including the source of the transferred genes, the DNA sequence and the consequences of the DNA insertion. The third step is the safety assessment of the gene product to identify any toxic or allergenic potential. Finally, the safety of the GM crop is assessed by considering all the information about the identity, agronomic performance, compositional analysis, nutritional analysis and safety studies (including animal studies). This safety assessment provides information on the hazard, which together with an assessment of the exposure of the population, provides the basis of risk assessment. How do socio-economic factors influence the development, use and control of GM food? (Otsuka, 2003) It is likely that introduction of GM crops will have an impact on Sustainable Agriculture and Rural Development (SARDwhich aims to ensure the ecological, economic and social strength of future generations equally with those of the current generation). The concerns about the introduction of Genetically Modified Organisms (GMOs) focus on effects on the environment, economic viability and of social networks. Although the introduction of GMOs may improve the living standards of rural communities, it may worsen disparities between and within communities and strengthen corporate control over agriculture. There may be different impacts on agriculture between developed and developing countries. In developed countries, consumers may favour quality and variety over quantity of food. Nevertheless, farmers are confronted with increasing competition because of trade liberalisation, and efficiency may play an important role in sustainability. One reason for the controversy about the use of GMOs is the discrepancy of interests between overseas consumers of the final food and the producers. In contrast, in developing countries, where the quantity of food is more important, yield increase may be more important than cost efficiency. Many in the population obtain their food from local markets and thus the conflict between the interests of the producers and consumers may be smaller.

Sustainability Assessment of the sustainability of GMOs in agriculture can be made using the three indicators of SARD, namely, capital stocks, efficiency and equity. A wide variety of genes and parent organisms can be used in genetic manipulation, but in practice developments have concentrated on a few core crops (soybean, maize, canola, rice, wheat, cotton, tobacco and potato). Equally, the traits introduced are also concentrated (herbicide tolerance, insect and disease resistance, tolerance to stresses, quality improvement and productivity enhancement). There are two aspects to consideration of capital stocks, namely, natural resources and man-made capital. Beneficial effects of GM crops on natural resources can be expected, through reduction of ecological damage by reduction of the use of pesticides, avoidance of soil erosion and reduction of land use through productivity gains. Some of these benefits have been achieved, with reduction in pesticide use in cotton, soybeans and maize and the reduction of yield loss. Negative effects of GM crops on natural or environmental capital are more speculative. Nevertheless, reductions in biodiversity, selection of resistant pests and weeds and gene flow by cross-pollination may occur. As far as man-made capital (which includes financial and physical capitalsuch as machines, roads, energy and communicationsand human resources) is concerned, the current GMOs are focussed on achieving low farming costs in industrialised countries, as food security has already been achieved. There is very limited commercial appeal for the development of tropical Forphan_ crops, which are grown mainly for family consumption. Public sector research will have to be augmented in order to provide improved varieties through genetic manipulation for those who have insufficient food. Efficiency is the second indicator of SARD. Efficient transformation of capital stocks into human welfare can be evaluated by measuring productivity. The primary measure of economic productivity of GM crops is profitability, not only for the users but also for the rest of society. In the USA, there is evidence that farmers using GM crops tend to have higher profits, but this depends on region, crop and year. However, the resulting increase in production is likely to reduce the market price. For example, it is projected that complete adoption of Herbicide Tolerant (HT) soybean would result by 2010 in a 0.5% increase in production and a 0.6% decrease in price. The figures for HT corn are a 0.6% increase in production and a 1.7% reduction in price. Adoption of GM crops is expected to enhance the competitiveness of the agricultural and food sector in world markets. This is occurring in the USA because of a large domestic market and no segregation of GM and non-GM crops and food. However, the lack of agreement on the acceptability of GM products in importing countries, leading to market segmentation, may lead to uncertain conditions. Equity is the third factor. While the effects of GMOs on natural resources may be equally distributed among all

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stakeholders (agribiotech companies, farmers, food manufacturers and retailers, and consumers), the effects on manmade capital and efficiency may be distributed differently among the stakeholders. This can be assessed in at least three levels: between developed and developing countries, between various social sectors and between farms of different sizes and income structures. The current GMOs have been developed by the private sector and aimed primarily at farms and markets in the industrialised countries. Thus, small-scale farmers in developing countries may be Forphan_ groups left behind by these technical advances, accentuating the disparity between development levels. There are also disparities between the different stakeholders; the largest share of the profits from, for example, HT soybeans has been distributed to the agribiotech/seed companies due to the strong Intellectual Property Rights (IPR; e.g., patents and Plant Breeders Rights). Consumers in the rest of the world, followed by US farmers and consumers, received the next largest share. Farmers in the rest of the world who have not adopted GM crops may lose income. The third area, disparities among producers, is of concern because the patented technologies developed by the private sector are too expensive for poor farmers in developing countries. There is some evidence to suggest that, in the USA, the adoption rate is higher in larger farms. Studies in developing country conditions suggest that introduction of GM crops may lead to greater discrepancies between large-scale and small-scale producers. Subsidies, public research and local distribution and storage will be required to overcome such discrepancies.

focussed on temperate crops and cost-saving traits. In contrast, tropical orphan crops grown on small farms by poor farmers have difficulty in attracting R&D investment, and this is unlikely to be changed by stronger IPR. Nevertheless, as the development of a single GMO requires acquisition of 30 to 40 licences from patent holders, strong IPR protection can help non-profit research institutes owning patents to create Fbargaining chips_ that would allow access to these technologies. In addition to the need for significant investment in public sector research, there are several problems to be solved: the cost of access to the technology necessary for developing GMOs; risks associated with uncertainty in the technology; and the possibility that strong IPR provides an incentive for private companies to collect and preserve genetic resources. Trade liberalisation The major issues in international negotiations on trade liberalisation include market access, export subsidies and domestic support. Duties on imported agricultural products remain high and export subsidies and export credit are widely used by exporting developed countries. The majority (90%) of such domestic support is concentrated in the USA, the EU and Japan. The least developed countries and those that are net importers of food are sceptical about whether trade liberalisation, which aims to reduce domestic support, will have beneficial effects. Nevertheless economists believe that removal of trade distortions will boost economic welfare and in many cases improve the environment. The current GMOs have emerged in the global commodity market where large-scale farms with government support grow commodity crops that are substantially equivalent to non-GMO crops. Trade liberalisation is likely to create more differentiated opportunities for competition, creating a segmented market with opportunities for valueadded products. This may result in crop specialisation and loss of biodiversity. It is unlikely that complete market access will be achieved in the short term and thus commodity markets and segmented markets will co-exist. Developing countries may have options to pursue strategies other than those for the commodity or segmented value-added markets. If technology transfer and conditions for innovation were to be established and investment in public research were to increase, social institutions and market conditions specific for developing countries could lead to the development of GMOs suitable for local conditions. Biosafety and labelling The government of a developing country is confronted by issues of biosafety (both for domestic adoption of GMOs and imported GM products) in terms of both the environment and human health. Policy options range from a product-specific, equivalence principle to a process-specific, precautionary

Development, use and control The use of GMOs in agriculture can have both positive and negative effects on sustainability, as has been mentioned in the previous section. Governments can choose options in various policy areas relevant to socio-economic conditions that can influence the impact of GMOs and that may help to achieve sustainable development. These are IPR, Trade Liberalisation and Biosafety and Labelling. Development of GMOs Private firms have been the major innovators in the development of commercial GMOs, unlike the previous situation in the green revolution, where public research was the driving force. One reason for this has been the reduction in research expenditure in the public sector. IPR derives from patents or from Plant Breeders Rights, with or without farmers privilege. It seemed that stronger IPR would provide greater incentives for private firms to invest in the R&D necessary for producing improved varieties. However, empirical studies have failed to confirm this linkage. Other factors may also play an important role. R&D activities promoted by IPR are inherently market orientated and have

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principle for risk assessment, approval and labelling. The former favours no labelling or negative labelling, which indicates that a product is GM free, while the latter favours mandatory positive labelling. Many developing countries have a cautious approach to controlling GMOs but many have not yet established effective legislation. Most governments that have already approved GMOs have required some level of mandatory labelling, except for the USA, Canada, Argentina and some countries in Southeast Asia. In general, risks to human health and the environment are of less concern than are economic and agrarian problems to developing countries. Even though the logic for regulation differs from that in developed countries, which have based their regulation in terms of the precautionary principle, the consequences in terms of biosafety and labelling are similar. The outcome of similar regulation may differ depending on the self-sufficiency of the basic food supply, purchasing power and market conditions. Thus, in net food importing developed countries, biosafety and labelling may offer consumers choice and provide competitive opportunities for domestic farmers and retailers in value-added segmented markets. In contrast, in net food importing developing countries that have neither purchasing power nor a competitive food industry, these policies may undermine food security and the viability of the food manufacturing and retailing industry. In developing countries that are selfsufficient in basic food production, policies in food importing countries may present risks through uncertain market conditions and opportunities for entry into the newly segmented market for non-GM products. The impact of policy selection in the control of development, use and safety of GMOs appears very intricate. The options for policies in IPR protection, trade liberalisation and biosafety and labelling do not always produce consequences that coincide with each other. Strong IPR protection may lead to a monopolistic innovator and, as a consequence, restriction of competition. In the reverse direction, low supply elasticity in prices (where prices do not respond to changes in production volume, owing to, for example, subsidies) may allow farmers to expand production, which may increase demand for improved varieties with IPR protection, such as GMO varieties. Thus, the impacts of IPR protection and trade liberalisation may be in opposite directions. In general, in developed countries, the major inconsistency is between innovative incentive (IPR protection) and competitive efficiency (partly through trade liberalisation). In contrast, in developing countries, trade protectionism worsens agricultural productivity even with poor domestic R&D and weak IPR protection. A second contradiction is between trade liberalisation and strict biosafety regulations with mandatory labelling. Specialisation of niche agricultural products in deregulated market conditions entails differentiation from other products by labelling with identity-preserved distribution. On the other hand, commodity markets for mass-produced grains, which may be supported by protectionist farm support

policies, regard products derived from different regions and conditions as equivalent, not requiring labelling. Strict biosafety and labelling regulations may weaken the incentive for R&D firms to invest in that country. Strong IPR may result in collection of genetic resources outside the country, conflicting with preservation in situ of regionspecific crops. Thus, in some cases, biosafety and labelling regulations may conflict with IPR protection. The first generation of GMOs with input traits resulted from strong IPR protection and low supply elasticity in prices of farm products as a result of subsidised commodity agriculture. The commodity market for GM products may be inherently unstable because of the conflict between protectionist production policies and emerging biosafety policies that restrict commercialisation. Trade liberalisation may jeopardise the commodity market by cutting subsidies, which may reduce the profitability of farming with GMOs. These influences may pose greater uncertainty in the efficiency and equity of adopting GMOs. The second generation of GMOs, with value-added traits, will emerge under conditions of strong IPR protection, high supply elasticity in prices and strict biosafety regulation. The high supply elasticity and smaller markets for high value-added varieties may make innovating firms vulnerable to uncertain market and regulatory conditions. Thus, the segmented niche markets for GM and non-GM products seem unstable. Socio-economic conditions that shape the future of GMOs are in reality much more complicated than described above. It is not easy to forecast the impact of these influences on the future of GMOs, nor their effects on SARD. There is no single package of policy options that can establish appropriate development use and control of GMOs. It is likely that the trends of greater IPR protection, more trade liberalisation and greater biosafety regulation are inevitable, but the consequences on SARD and the success of GMOs remain uncertain.

Public attitudes towards genetically modified foods (Frewer, 2003) Public attitudes Public perceptions and attitudes about emerging biosciences and other new technologies are among the most important factors determining the likelihood of successful development and implementation of technology. An understanding of the determinants of perceptions and attitudes, and of trust in institutions must be considered to support successful exploitation of genetic technology. It is clearly important to develop the best method of communicating the risks and benefits of GM food. However, new ways of involving the public explicitly in the debate about new technology, in this case genetic modification of food, are also important.

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Peoples attitudes to particular activities help to explain why they support (or do not support) particular social policies, ideologies or technological advances. Attitudes are usually measured along a bipolar continuum that ranges from extremely positive to extremely negative and includes a neutral reference point. In general, people who have a positive attitude towards, say, GMF, are likely to associate it with positive attributes and are unlikely to associate it with negative attitudes (and vice versa). A change in attitude may occur when an individual receives some additional information about the issue. This may be, for example, through direct exposure to the GM food, where the experience may result in a more positive or a more negative attitude. Attitude changes following direct exposure may be difficult to detect, because other contextual factors mask the event. For example, with GM foods, such contextual factors may include the individuals interpretation of the information provided about the GM food or their beliefs about the motives of the source of the information (industry, regulators, etc.). The way a person perceives the risks associated with a particular hazard will have direct impact on their attitudes towards that hazard. Factors such as whether the risk is perceived as involuntary, potentially catastrophic or uncontrollable are more important determinants of public response to risks than are the more technical estimates of the risks. Some argue that the ways that technical experts and lay people think about risks are very different. There is some evidence that people will tolerate risk in the area of technology innovation if they perceive some direct benefit to themselves. There is some evidence that this occurs with GM foods and it has been argued that consumer rejection of the first generation of GM foods is because they have little direct benefit for the consumer. The two major areas of benefit, sustainability claims and health claims, are thought to have the greatest potential to improve consumer acceptance. However, neither type of benefit is persuasive when consumers are presented with particular examples of GM foods. Opinion polls provide information about peoples perceptions and attitudes to GM foods, but it is difficult to predict what their actual behaviour might be on the basis of the results of the polls. It is also difficult to compare the results of different opinion polls applied to different populations. The Eurobarometer survey has been applied to many countries and provides good comparative information. It has been implemented since 1973 in different European states and overseas. In general, Europeans have a positive view of science and technology, but their attitudes to GM foods are more negative. Of those sampled, 95% were concerned about the consumers lack of choice about consuming GM foods and 60% expressed the view that GM organisms had the potential to have negative effects on the environment. For some respondents, an increased scientific knowledge of genetic modification was linked with preference for greater regulatory control. Women perceived

greater risks than men and older people greater than younger respondents. In general, consumers in northern Europe tend to express more concern about the risk of genetic modification of food than those in southern Europe. Responses to the same survey indicated that New Zealanders were more positive about the use of agricultural applications of genetic modification in the context of specific applications than some European countries or Japanese populations. There is a view that people in the USA are less concerned about GM foods than in other countries, but this is not backed by empirical evidence. Survey data indicate that North American public opinion is equivocal about the acceptability of GM foods, with 53% believing that genetic engineering would improve their quality of life over the next 20 years and 30% believing it would make things worse. Many respondents did not appear to have confidence in US regulators concerning the safety of GM foods, although confidence in consumer groups and industry was generally high. It is important to emphasise that public opinion about technology implementation is dynamic and likely to change, as more information is made available about benefits, risks, societal impacts and other factors of relevance to the acceptance of GM foods. The results of surveys using structured questionnaires have been criticised because the questions may not reflect peoples actual concerns, and such methods do not provide information about the reasons underlying responses. Results from semi-structured qualitative methodology avoid these problems. Such research has shown that minor modifications to food products were associated with moderate concern. Risk and high levels of ethical concern were associated with modification involving humans or animals. Medical applications were perceived to be most important and necessary. A separate study revealed that peoples beliefs about GMFs fell into three groups. The largest group of concerns was linked to health. A second group of beliefs related to perceptions that genetic modification of food was not under the control of the consumer; in particular, that consumers had no choice about whether or not they ate GMFs. Finally, the third group related to perceived benefits, including reduced costs and wastage and increased shelf life. Knowledge of attitudes and concerns about GMFs, reviewed briefly here, has to be considered when providing information to the public. When introducing any new, potentially controversial technology, it is extremely important to provide information that addresses the concerns of the public directly, rather than information that focuses on technical risk estimates alone. Ethical concerns The publics concerns about the ethics of genetic modification are as important as their views on risk in the strategic development of the technology. Understanding how the public thinks about ethics helps to foster consensus

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building about the long-term application of GMOs. Differences in ethical views between cultures, religious groups and other interest groups are also important, particularly in the light of the global economy. What is considered ethically acceptable in one culture may be unacceptable in another. Public views on ethical matters might usefully be included in the regulatory framework surrounding biotechnology and thereby public trust in regulation and in biotechnology is likely to be increased. Trust Public perceptions of the risks and benefits of (new) technology have an important impact on the political decision making process. Trust in the companies and scientists conducting research into gene technologies has an important bearing on the perception of risks and benefits from the products derived from that research. The more the company and scientists are trusted to have the interests of society at the forefront of their activity, the less their work is perceived to be associated with risk and the more it is perceived to be associated with benefits. Social trust is defined as peoples willingness to rely on experts and institutions in the management of risks and technologies. Public trust of this sort in the particular scientific activity and in the regulators and regulatory institutions is likely to be crucial to technology acceptance. Unfortunately, public trust in scientific authority has lost much of its credibility, at least in the UK. There is evidence that differences exist between different countries in this area, with the Scandinavian public being more likely to trust government than is the case in southern Europe or the UK. Without public trust, long-term development of biotechnology, including GMFs, will be problematical. Source credibility refers to peoples perceptions of the motivations of institutions or individuals providing information to the public. It is usually assumed to be dependent on both the information source and the subject under consideration. FCompetence_ (the expertise and the extent to which the communicator are able to pass on information) and Fhonesty_ (the extent to which a communicator will be truthful) are two major factors that are important in determining trust. Expertise without honesty is unlikely to result in long-term changes in attitude. Trust in information sources has been examined in the context of GM foods. The results suggest that the extent to which people trusted information sources appeared to be driven by peoples attitudes to GM foods. Trust in information sources did not drive peoples reaction to the information. Thus, providing information about risks and benefits of GM foods is not sufficient to promote attitudinal change within the public. In the past, communication has often been technology driven or Ftop-down_. The communication has been driven by technical risk assessments rather than by issues salient to the wider public. This approach has failed to convince con-

sumers of the merits of such products. Information from a trusted source, which reassures people of safety, will reduce perceived risk. The same information from a distrusted source may increase perceived risk. Trust and perceived risk have independently influenced peoples attitudes to gene technology. Prior attitudes towards the hazard may also influence peoples interpretation of risk communication information. These processes create a positive feedback cycle that helps to explain the stability and resistance to change of peoples attitudes to particular hazards where these attitudes are strong and well established. Communicating uncertainty Scientific experts and the general public have different views about reaction to uncertainty. Scientific experts have believed that the public is unable to handle information about uncertainty and that providing such information would increase distrust in science and cause panic and confusion about the impact of a particular hazard. Interviews with members of the public showed that they are familiar with uncertainty, and their distrust in scientific and regulatory institutions increased with any tendency to deny that uncertainties exist when in fact uncertainty had been identified. Communication about GM foods should include discussion of uncertainty associated with risk management. Increased transparency in risk management and regulatory decision making will mean that information dissemination activities will focus as much on uncertainties as on what is known. Emerging issues The regulatory environment is changing its relationship with society. The Ftop-down_ risk communication model, where information is developed by experts who expect the public to attend to what they have communicated, is being replaced by more inclusive and transparent institutional processes. These changes reflect a decline in trust in science. Societal values are likely to contribute to consumer acceptance or otherwise of GM foods and need to be included in the debate about regulation and the associated communication strategies. In is now recognised that making decisions without public support is liable to lead to confrontation, dispute, disruption, boycott, unrest, distrust and public dissatisfaction in science and technology.

Final thoughts The factors that determine the acceptability of Genetically Modified Food are clearly very complex. Here, I have tried to summarise those issues that impact directly on human health, although many of them are intertwined with the issues that also affect the environment. The part of the process involving toxicologists, namely, safety evaluation

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and risk assessment, is only a part (albeit an important part) of the whole picture. GMFs must be safe for human consumption. But to be successful, GMFs must meet other criteria as well. They should not have a negative impact on Sustainable Agriculture and Rural Development. The impact of GMOs on economics and social structures is so complex as to defy simplification. Nevertheless, it is clear that their impact will vary, depending on the state of development of the country and its agriculture and the policies, adopted in intellectual property rights, international trade liberalisation and biosafety regulation. Equally, to be successful in the long term, they must be sustainable in this generation and for future generations. Ultimately, the acceptance of GM foods will depend on consumer attitudes. These in turn are influenced by technical assessments of risks and benefits and their communication to the consumer. Ethical considerations, uncertainties about the information provided, and trust in the regulatory system and information sources are also important determinants of consumer acceptance. Thus, the scientific, economic and other technical factors are insufficient to ensure acceptance of GM foods; social issues, such as trust and peoples values and attitudes, are equally important. References
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modified foods for human health and nutrition: the scientific basis for benefit/risk assessment. Trends Food Sci. Technol. 14, 119 209. Frewer, L., 2003. Societal issues and public attitudes towards genetically modified foods in: Genetically modified foods for human health and nutrition: the scientific basis for benefit/risk assessment. Trends Food Sci. Technol. 14, 319 332. Garza, C., Stover, P., 2003. General introduction: the role of science in identifying common ground in the debate on genetic modification of foods in: Genetically modified foods for human health and nutrition: the scientific basis for benefit/risk assessment. Trends Food Sci. Technol. 14, 182 190. Konig, A., et al., 2004. Food Chem. Toxicol. 42, 1047 1088. Kuiper, H.A., Kleter, G.A., 2003. The scientific basis for risk assessment and regulation of genetically modified foods in: Genetically modified foods for human health and nutrition: the scientific basis for benefit/risk assessment. Trends Food Sci. Technol. 14, 277 294. Maclean, N., 2003. Genetically modified fish and their effects on food quality and human health in: Genetically modified foods for human health and nutrition: the scientific basis for benefit/risk assessment. Trends Food Sci. Technol. 14, 242 252. Otsuka, Y., 2003. Socio-economic considerations relevant to the sustainable development, use and control of genetically modified foods in: Genetically modified foods for human health and nutrition: the scientific basis for benefit/risk assessment. Trends Food Sci. Technol. 14, 2294 2332. Sang, H., 2003. Genetically modified livestock and poultry and their potential effects on human health and nutrition in: Genetically modified foods for human health and nutrition: the scientific basis for benefit/risk assessment. Trends Food Sci. Technol. 14, 253 263. The Pew Initiative. Feeding the world. March 2004. www.pewinitiative.org accessed on 6 July 2004. von Wright, A., Bruce, A., 2003. Genetically modified microorganisms and their potential effect on human health and nutrition in: Genetically modified foods for human health and nutrition: the scientific basis for benefit/risk assessment. Trends Food Sci. Technol. 14, 264 276.