Journal of the American College of Nutrition

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Knowledge, Attitudes Toward, and Acceptability of Genetic Modification among Western Balkan University Students of Life Sciences (AGREE Study) Vladica Veličković MD, PhD(c), Marko Jović MD, Ena Nalić MSc, Aleksandar Višnjić MD, PhD, Olivera Radulović MD, PhD, Čedomir Šagrić MD, PhD(c) & Milan Ćirić MD, PhD To cite this article: Vladica Veličković MD, PhD(c), Marko Jović MD, Ena Nalić MSc, Aleksandar Višnjić MD, PhD, Olivera Radulović MD, PhD, Čedomir Šagrić MD, PhD(c) & Milan Ćirić MD, PhD (2015): Knowledge, Attitudes Toward, and Acceptability of Genetic Modification among Western Balkan University Students of Life Sciences (AGREE Study), Journal of the American College of Nutrition, DOI: 10.1080/07315724.2014.1003115 To link to this article: http://dx.doi.org/10.1080/07315724.2014.1003115

Published online: 01 Jun 2015.

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Knowledge, Attitudes Toward, and Acceptability of Genetic Modification among Western Balkan University Students of Life Sciences (AGREE Study) Vladica Velickovic, MD, PhD(c), Marko Jovic, MD, Ena Nalic, MSc, Aleksandar Visnjic, MD, PhD,    c, MD, PhD Olivera Radulovic, MD, PhD, Cedomir Sagri c, MD, PhD(c), Milan Ciri Department of Public Health (V.V., A.V., O.R., C.S., M.C.), Department of Histology and Embryology (M.J.), Faculty of Medicine, University of Ni s, Nis, SERBIA; Faculty of Agriculture and Food Sciences, University of Sarajevo, Sarajevo, BOSNIA AND HERZEGOVINA (E.N.) Key words: bioactive compounds, diets, general nutrition, government regulations, supplements and functional foods Background: There are still no data on the attitudes and acceptance of genetic modification (GM) food in European developing countries, such as the Western Balkan countries. The aim of the study was to assess the knowledge, attitudes, and acceptance of GM but also to shed light on the multifactorial process leading to acceptance of genetic modifications among Western Balkan students of life sciences. Methods: In this cross-sectional study, the final study population sample was composed of 1251 university students. The instrument for data collection was a questionnaire consisting of 49 items composed of 5 sections taken from the literature. Attitudes toward GM were analyzed by using Q-mode factor analysis and principal component analysis was run for the assessment of perception of personal health risks. The acceptability of GM was analyzed in binary probit models assessing the acceptability of GM products in different areas of application with Q models, sociodemographic variables, perception of personal health risks factors, respondents’ knowledge about biotechnology, gender, and age as explanatory variables. Results: This study demonstrated that students of life sciences supported the implementation of GM in industry and medicine production but not in food production. Their acceptance was most influenced by 3 out of 5 attitude models that were identified (p < 0.0001). Regarding the perception of personal health risks, the factor “credence risks” was seen as a negative predictor of acceptance of GM in industry and food production (p < 0.05). The main knowledge predictor of rejecting GM was misconception, whereas real knowledge had no impact (p < 0.0001). Conclusion: The AGREE study provided the first rough picture of the knowledge, attitudes, and acceptance of GM in this area. Given the target population, it could be expected that the general population’s acceptance of all observed elements, especially knowledge, would be lower.

INTRODUCTION

open question of acceptance of genetic modification by the general population. In the spirit of movement within public health that aims to make the public health field more accessible to the general public and more user-driven, so-called Public Health 2.0, it is very important to examine the attitudes, knowledge, and acceptance of genetic modification in different applications [1]. Using selective breeding, man has altered the genomes of species for millennia [2]. At first half of the 20th century, we have started to alter the genomes of species through

A high level of technological development of human society has resulted in exponential growth of the population, which has inevitably led to global changes due to increased demand. This increased demand leads to food and water shortages, deforestation, greenhouse effect, and extinction of some species. All of this has a tremendous impact on the global public health. Genetic modification in various fields of applications offers solutions to some of the problems, but it remains an

Address correspondence to: Vladica Velickovic, Department of Public Health, Faculty of Medicine, University of Nis, Bulevar Dr Zorana Đinđica 81, Nis 18000, SERBIA. E-mail: [email protected]

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Acceptance of Genetic Modification mutagenesis [3]. In the 1970s, genetic modification as the direct manipulation of DNA by humans appeared (more specifically, by creation of the first recombinant DNA by Paul Berg in 1972) [4]. A tremendous amount of research has led to major breakthroughs in the field and its rapid evolution from the first transgenic animal [5] and the first genetic engineering company (Genentech 1976) to today’s achievements of the creation of a bacterial cell controlled by a chemically synthesized genome [6] and approval of commercial release of a large number of products for use in medicine, food production, and industrial production. Concerns about potential risks caused by genetic engineering were discussed in depth at the Asilomar Conference in 1975 [7]. Rapidly evolving scientific disciplines using various types of genetic modification, characterized by a high degree of possibility of direct practical application in major industries, such as health care, agriculture, industry, and environment, raises many questions that are not solely and exclusively related to science but have political, economic, ethical, and educational consequences. However, no application of genetic modification causes more controversy than the use of genetically modified products in the food industry, which remains a controversial issue especially among politicians and consumers. Only the scientific community has reached a broad consensus that genetically modified (GM) food does not constitute a higher risk to human health than conventional food [8]. Consumers have divided attitudes about GM food, ranging from acceptance and optimism regarding GM food improvements to rejection and pessimism. Today it is more than evident that support of GM food is increasingly declining in most European countries [9]. Moreover, recent studies have shown slightly declining support of GM food in the United States as well [10,11]. Findings from several consumer surveys in Asia have pointed to mixed attitudes, which is especially pronounced in China [12], whereas in South Korea and Japan [13] support of GM food has started declining. However, surveys conducted in developing countries show increasing support of GM food [14,15]. Studies increasingly emphasize the need for examination of the real causes behind public controversy [16,17]. Though Eurobarometer surveys provide accurate information about EU countries, there are still no data on the attitudes and acceptance of GM food in European developing countries, such as the Western Balkan countries. These countries’ legal systems currently do not allow the import and distribution of GM food and seeds, so consumers in these markets do not come into contact with GM food and seeds. Nevertheless, strong public debates and media coverage of this topic are characteristic of these countries. Bearing in mind that the consumers have no practical experience regarding these products and have very limited knowledge of genetic modification, we decided to conduct a survey of university life sciences students. Life sciences students are some of the most important drivers of the future development of these countries, as well as the

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future leaders of the development of biotechnology. In the future, their publicly expressed opinions, especially in the media, can significantly influence the formation of attitudes toward GM products. Therefore, we decided to include this population as the target group in a survey entitled Knowledge, Attitudes towards, and Acceptability of Genetic Modification among Western Balkan Students of Life Sciences (te AGREE study). The aim of the AGREE study was to assess the knowledge, attitudes, and acceptance of genetic modification but also to shed light on the multifactorial process leading to acceptance of GM among Western Balkan students of life sciences.

METHODS Design The AGREE study is a cross-sectional study carried out with university students in the summer semester of 2013. The sampling goal of the study was to represent the population consisting of Western Balkan university students (Southeast European area, which includes countries that are not members of the European Union: Serbia, Bosnia and Herzegovina, and Montenegro) in all its diversity—men and women in all study years at nationally representative universities. These requirements dictated that the process of sample selection be performed in stages. The first stage involved the selection of universities and the second stage focused on the selection of students. The selection of universities for the sample was based on 3 sampling rules. The first rule in the process of selecting the universities per country paid attention to the country’s population size. The second rule required the selection of the largest universities in each country. The third rule governed the selection of universities having Faculties of Medical Sciences and Faculties of Sciences and Mathematics. These faculties were included in each country because their students were chosen to comprise the target population. Based on these 3 sampling rules, the following universities were selected: 4 state universities from Serbia (University of Belgrade, University of Nis, University of Novi Sad, and University of Kragujevac), one state university from Bosnia and Herzegovina (University of Sarajevo), and one state university from Montenegro (University of Montenegro). A total of 13 faculties of life sciences from all universities was selected. From each Serbian university 2 faculties were selected for the survey. Two faculties were surveyed from the University of Montenegro and 3 faculties from the Bosnian university were surveyed. The second stage involved the selection of students. Administration of the questionnaire was conducted on-site and not by mail because the latter may have produced a strong self-selectivity bias. On-site administration was considered to produce a more reliable representation of those asked to complete the

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Acceptance of Genetic Modification questionnaire. Through the regional biomedical portal MDexplorer, 29 interviewers were selected and recruited. The interviewers were exclusively from the ranks of employees and students (graduate and undergraduate). All interviewers attended a 2-week online training covering the survey sampling methodology. Then they all became familiar with the rules governing the survey sampling with detailed step-by-step instructions. Each faculty had to have at least 2 trained interviewers. Students were selected randomly and each particular questionnaire had to be completed in the presence of the interviewer on the faculty site. Two thousand six hundred questionnaires were printed and distributed by 29 trained interviewers. The final sample included only the questionnaires that were fully completed and approved by both interviewers from each faculty. The final study population sample was composed of 1251 university students, with a response rate of 48.11%. All respondents and faculties were assured of anonymity.

Measurement Instrument The instrument for data collection was a questionnaire consisting of 49 items with an estimated time for completion of no more than 20 minutes (see Appendix 1). The questionnaire consisted of 5 sections. The Introduction section involved general information questions; section A included items measuring the acceptability of genetic modification in different areas of application (medicine, food production, and industrial production), compiled from Christoph et al. [17]. Section B included 22 items on a 5-point Likert scale about risks and benefits of GM products, the production process, their confidence in governmental regulations and technological development, as well as overall questions about food and nature. These 22 items measuring the attitudes toward genetic modification were compiled from Noussair et al. [18]. In addition, the perception of personal health risks, in section C, was measured by using 12 items inquiring about the perceived exposure to different health risks. Items were taken from Oltersdorf [19]. Section D focused on the respondents’ knowledge about biotechnology, which was assessed by 6 true or false questions that were taken from Gaskell [9].

perception of personal health risks. To ensure that the sample was suitable for analysis, the KMO test and Bartlett’s test of sphericity were conducted. Principal component analysis was carried out with varimax rotation. Factors were extracted following the Kaiser and scree plot criteria. The acceptability of genetic modification was analyzed in binary probit models assessing the acceptability of GM products in different areas of application with Q models, sociodemographic variables, perception of personal health risk factors, respondents’ knowledge about biotechnology, gender, and age as explanatory variables. Summary and descriptive statistics were used as well. Statistical significance was taken at p < 0.05. All statistical analyses were carried out with STATA software (version 12.0 for Windows, StataCorp, SE, College Station, TX).

Theoretical Framework One of the major tasks of this study was to design a theoretical model aimed at explaining the multifactorial processes how the attitudes and other factors influence the acceptance of GM products. The model shown in Fig. 1 summarizes the conceptual steps of this analysis. The initial hypothesis was that a large number of factors influence acceptance of GM products. Therefore, the effects of the following important factors were tested: attitudes toward genetic modification, perception of personal health risks, knowledge about genetics and biotechnology, gender, and age.

RESULTS The methodological baseline of our study was Bredahl et al.’s [21] model about consumer attitudes and decision making with regard to GM food products, based on an adapted version of Fishbein’s multi-attribute attitude model and other main principles of cognitive psychology. The acceptance of genetic modification in a variety of areas is affected by a large number of factors. The AGREE study attempted to be

Statistical Analysis Attitudes toward genetic modification were analyzed by using Q-mode factor analysis. The Kaiser-Meyer-Olkin (KMO) measure of sampling adequacy test and Bartlett’s test of sphericity were used to determine whether factor analysis was suitable for the data sample. Q methodology is a more robust technique for the measurement of attitudes and subjective opiniosn in comparison to alternative methods [20]. The Q-mode factor analysis was carried out with promax rotation at level 3. Obtained Q factors were converted to Q models. Principal component analysis was run for the assessment of

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Fig. 1. Theoretical model explaining the multifactorial processes forming the basis of acceptance of GM products.

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Acceptance of Genetic Modification objective and determine the most important factors and their impact. Special attention was paid to the process of forming attitudes about genetic modification, the most important step toward acceptance. The study also investigated the impact of other factors on acceptance, primarily personal health risks and knowledge about biotechnology. Table 1 shows some characteristics of the sample. Universities usually have students from the regions and countries in which universities are located. However, Serbian universities also have students from Bosnia and Montenegro. The selected universities accepted students from various parts of countries based upon their university entrance exam results. These universities were nationally representative and the students came from various social and cultural backgrounds. However, this study did not insist upon a declaration of nationality in the questionnaire because the research was not planned to go in that direction and because of specific interethnic relationships. There were no adequate data from previous papers and literature with which it was possible to compare the AGREE study sample. A higher number of female students was expected, which adequately reflects the real-world situation in these faculties. Despite certain deviations, it could be assumed that the sample was a good representation of the Western Balkan university students of life sciences.

Acceptability of Genetic Modification in Different Application Areas Section A of the questionnaire included items measuring acceptability of genetic modification in different areas of application (medicine, food production, and industrial production). The section contained 5 questions with the possibility of choosing one of the 3answers: “yes,” “no,” and “do not know.” The objective was to determine the areas in which practical application of genetic modification was acceptable to the respondents. Each survey question referred to one area of use of genetic modification, presented as follows: “GM insulin instead of pig insulin” determined the respondents’ acceptability of genetic modification in medicine production and “paper made from GM starch (potato) preventing deforestation” determined the respondents’ acceptability of genetic modification in industrial production. Three questions determined acceptability of the

use of genetic modification in different areas of application related to food production: “vitamin-enriched rice for prevention of deficiency diseases in developing countries,” “fiberenriched potatoes that might prevent colon cancer,” and “plants that need less fertilizers and cause less environmental harm.” Descriptive analysis showed that the largest percentage of university students (76.8%) accepted the use of genetic modification in industrial production, whereas 54.2% supported its use in medicine production. On the other hand, most students did not accept the use of genetic modification in any area of food production: 48.83% of students accepted “vitamin-enriched rice for prevention of deficiency diseases in developing countries,” 47.53% accepted “fiber-enriched potatoes that might prevent colon cancer,” and 39.93% accepted “plants that need less fertilizers and cause less environmental harm.” All differences were deemed significant. In all further analyses concerning this item, answers “no” and “do not know” were treated as “no.” Acceptability in all areas of application was tested as the outcome variable in a series of probit analyses.

Attitudes Toward Genetic Modification In the next step, attitudes toward genetic modification were analyzed by using Q-mode factor analysis. The main objective of this part of the analysis was to reveal the underlying aspects leading to the formation of attitudes. The analysis focused on the respondents’ general attitudes, as well as attitudes toward nature, technology, food, government institutions, etc. Q-mode factor analysis is a type of factor analysis that produces a factor solution that identifies the ways in which individuals cluster on certain attitudinal dimensions. The subjects associated with each significant factor are assumed to share a common perspective, with each of the factors in the solution representing a different perspective. Data collected by 22 items measuring the attitudes toward genetic modification were tested using the KMO measure of sampling adequacy test and Bartlett’s test of sphericity to determine whether factor analysis was suitable for the data sample. Bartlett’s test of sphericity value was 0.000 and the KMO measure of sampling adequacy value was 0.885. These measures ensured suitability of data for factor analysis. In order to perform Q-mode factor analysis and identify

Table 1. Characteristics of the study sample Serbia

Bosnia

Montenegro

Total

University

University of Belgrade

University of Nis

University of Novi Sad

University of Kragujevac

Total Serbian Universities

University of Sarajevo

University of Montenegro

All Universities

Participants, n (%) Mean age (SD) Women, n (%) Median study year

215 (17.19) 22.18 (2.37) 105 (48.84) 3

216 (17.27) 22.56 (1.83) 91 (42.13) 3

208 (16.63) 23.40 (3.51) 139 (66.83) 3

203 (16.23) 24.19 (2.77) 129 (63.55) 4

842 (67.31) 23.07 (2.78) 464 (55.11) 3

310 (24.78) 22.86 (2.02) 229 (73.87) 3

99 (7.91) 22.65 (1.51) 79 (79.80) 4

1251 (100) 22.98 (2.53) 772 (61.71) 3

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appropriate clusters, the traditional data matrix was transposed. The Q-mode factor analysis was used with promax rotation at level 3. Several methods were used to determine an appropriate range of solutions to be investigated. The following methods were used: Kaiser criterion, variance explained criteria, Cattell’s scree plot, and Horn’s parallel analysis. Based on these methods, 5 factors were determined. Q-factors identified the clusters of persons sharing common subjectivities. Q-models were developed from the content of those shared subjectivities. Together, 5 Q-models accounted for 53.25% of the error variance. Table 2 presents the factor loadings of all 5 models.

The cutoff value was set to §1.0 in identifying the salient positive and salient negative statements within the Q-models. Those Q-models were as follows: 1. Strong opponents of GM food—This model represented the clusters of persons with very negative attitudes toward the use of GM, especially in food production. People who shared these viewpoints believed that GM food was not necessary and that it did not offer any benefits. Moreover, they believed that GM food was harmful to human health and that the potential risks to human health were

Table 2. Promax Rotated Q-Factor Loadings for Attitude toward Biotechnologya Item in the Attitude toward Biotechnology/Q Factor

Strongly Opponents of GM Food

GM foods can cause an immense benefit for a lot of people Using biotechnology, the products can be produced in a way that is friendlier to the environment GM foods might improve the standard of living of future generations The use of biotechnology in food production can solve environmental problems GM foods are of higher quality than those produced without biotechnology Risks related to biotechnology are acceptable GM foods are not necessary Environmental organizations tend to exaggerate and see dangers everywhere Even if nowadays a process is assumed to be safe, it is not known how it develops in 50 years GM foods might cause allergies Even if GM foods have benefits, it still is unnatural GM foods are a danger to human health GM products are always a risk The use of biotechnology in food production might cause environmental risks The food industry will not risk selling a harmful product, because of fear of causing a scandal If scientists declare a product as safe, I will believe that GM products are more strictly controlled than those produced without biotechnology The degree of civilization may be recognized by technical development Due to technical progress, we will be able to solve future problems I don’t trust newly introduced food products Changes in nature due to humans rarely cause any serious problems Biotechnology only serves the interest of big companies

Attitude toward Progress

Distrust of Institutions

Scepticism toward Biotechnology

Cautious Acceptance

¡1.323

0.209

0.593

¡0.827

0.372

¡0.592

0.919

1.044

¡0.936

¡0.058

¡1.389

0.021

0.548

¡1.406

0.349

¡0.824

0.544

0.971

¡1.025

¡0.039

¡1.843

¡1.354

¡0.853

¡0.457

¡1.431

¡1.122 1.041 ¡0.903

¡0.702 0.100 ¡1.557

¡0.146 ¡0.510 1.604

0.774 1.212 2.921

¡1.504 ¡2.169 1.472

0.699

0.739

0.670

0.472

¡0.288

0.741 1.431

¡0.180 0.637

0.621 0.801

0.048 0.793

1.005 1.288

1.090 0.850 0.663

¡1.146 ¡1.213 ¡0.719

¡0.766 ¡1.137 ¡0.538

¡0.235 ¡0.840 ¡0.594

0.605 0.565 0.468

¡0.303

¡0.257

¡1.562

¡0.646

0.953

¡0.727

1.058

¡2.355

1.253

0.886

¡0.664

0.452

¡0.902

0.348

¡0.120

0.076

1.485

¡0.120

0.627

0.342

0.034

1.611

0.099

0.212

0.021

0.780 1.211

¡1.691 1.287

¡0.054 1.368

¡0.784 ¡0.299

¡1.459 ¡1.386

1.073

¡0.244

0.621

¡0.614

0.128

GM D genetic modification. a Bold items are used in the interpretation of the respective factor.

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Acceptance of Genetic Modification

2.

3.

4.

5.

6

unacceptable. They considered that any human interference in fundamental biological processes, especially in food production, was unnatural and strongly rejected the possibility that GM food was of higher quality than that produced without biotechnology. Bearing in mind that they did not recognize any benefits of GM food, it could be concluded that they considered it to serve only to the interests of big companies. Their opposition to biotechnology was limited to food production and they could not be considered as general opponents of biotechnology and the overall technical progress. This model explained about 25.11% of the variance. Attitude toward progress—This model represented the cluster of people sharing a common viewpoint and being optimistic about overall technological progress of civilization. In contrast to the previous model, this model expressed a positive opinion about innovation and the overall technical progress. They believed in science and that due to technical progress we would be able to solve future problems. Although this model opposed the opinion on the basis of which GM food was deemed unnecessary, people representing it still did not believe that GM food was of higher quality than conventional food produced without biotechnology. This model explained about 12.98% of the variance. Distrust of institutions—This group expressed distrust in all official institutions, which is characteristic of many people from the Western Balkans whose lack of trust is caused by institutional corruption. However, they were ready to support GM, especially in resolving environmental problems, and did not believe that GM products were always risky. Moreover, they believed that using biotechnology products could be done in a way that was friendlier to the environment. Bearing in mind that the officials from these countries frequently expressed their attitudes against GM food, these views were expected. This model explained about 5.74% of the variance. Skepticism toward biotechnology—This model reflected a skeptical viewpoint about the benefits of biotechnology not only in food production but also in other areas of use. It is interesting that this cluster did not reflect opinions that were against scientific and technological development. The respondents belonging to this group believed in scientists but were skeptical about the use of biotechnology and the necessity of GM food. This model explained about 4.94% of the variance. Cautious acceptance—This model reflected the views held by people who believed that GM food was necessary and believed in new food industry products. However, they were still very cautious regarding the potential health risks of GM food. It could be concluded that this cluster accepted GM food and biotechnology but that they were also critical and cautious about the consequences to human health and

effects on nature. This model explained about 4.48% of the variance. It is evident that none of the models included attitudes in favor of an open and unconditional support of GM food. Students were either against or very skeptical and abstained with respect to GM food. Even those with the view that GM food was necessary were very careful about the possible side effects. Probit analysis tested the impact of each model on acceptance of genetic modification in different areas of application.

Perception of Personal Health Risks Perception of personal health risks was measured by using Oltersdorf items that contained 12 questions on a 5-point scale ranging from very high to very low. Principal component analysis was run using varimax rotation. To ensure that the sample was suitable for the analysis, Bartlett’s test of sphericity and the KMO test were conducted and the values were 0.000 for Bartlett’s test and 0.835 for the KMO test. Four factors were extracted following the Kaiser test and scree plot criteria. Taken together, these factors explained about 58.90% of the variance. Table 3 shows varimax-rotated factor loadings for the perception of personal health risks and items used in the interpretation of the respective factors:  Environmental health risks—combined the perception of environmental health risks that were mainly not associated with food.  Credence risks (taken from Nelson’s terminology [22])— combined risks that could not be influenced by consumers themselves and were related to the food risk.  Behavioral risks—combined risks that could be influenced by consumers themselves: alcohol, cigarettes, and unbalanced diet.  Risk of uncultivated food—combined risks of raw food diet, without the use of pest control in food production. In probit analyses, all respective factors were tested as independent predictors of acceptance of genetic modification in different areas of application.

Knowledge about Genetics and Biotechnology Knowledge about genetics and biotechnology was measured by the section containing 6 true and false questions. These questions offered no opportunity for “do not know” answers. Table 4 shows the results. The correct answers are indicated in bold. Based on the first 4 questions, it could be concluded that most students had good knowledge about genetics and biotechnology, which was expected. However, the last 2 questions pointed to misconceptions on the part of most students. The explanation of such differences in the last 2

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Acceptance of Genetic Modification Table 3. Varimax-Rotated Factor Loadings for Perception of Personal Health Risksa

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Item in the Perception of Personal Health Risks/Factor Food additives Veterinary residues in food Pesticides Genetically modified food Raw food Alcohol Cigarettes Unbalanced diet Food borne infections Climate change/ozone hole Radioactivity Road traffic

Nonfood Risks

Credence

Behavioral Risks

Risk of Uncultivated Food

¡0.153 0.036 0.118 0.071 0.134 ¡0.147 0.006 0.255 0.560 0.346 0.514 0.394

0.619 0.560 0.364 0.256 0.155 0.032 0.069 ¡0.154 ¡0.140 0.071 0.055 0.156

0.043 ¡0.071 0.027 0.015 0.055 0.698 0.575 0.388 0.062 0.066 ¡0.113 ¡0.004

0.027 ¡0.038 ¡0.334 0.056 0.805 0.116 ¡0.131 0.033 ¡0.093 ¡0.359 0.255 ¡0.032

a

Survey question: “Hazards to health are mentioned daily in the media. How high, do you think, is your personal risk posed by the following factors?” Responses ranged from 1 D very high to 5 D very low. Bold items are used in the interpretation of the respective factor.

questions was most likely because the questions were relating to the practical application of biotechnology, which these students did not experience in their countries and definitely did not have enough knowledge about; that is, they had poor factual knowledge. These results supported the assumption that in this region, students received good theoretical knowledge but lacked the possibility of its practical application due to lack of resources. Too much theoretical knowledge usually leads to students not knowing how to use it properly in real-world situations. In our case, women showed higher levels of knowledge in some areas, significantly in items 1 and 5.

Probit Analysis Acceptability of genetic modification in different areas of application was analyzed in probit models assessing the effect of attitudes, perception of personal health risks, knowledge, gender, and age on the process leading to acceptance. Results are shown in Table 5. More acceptance of GM in all areas of application is most influence by the people who share attitudes toward progress and distrust of institutions. These attitude models were the most important predictors found in this study. The opposite was found in an attitude model, strong opponents of GM food, in which respondents did not accept GM in any area of

application except for industrial purposes. Factors included in this model stood for the main negative predictors. Another interesting finding was that poor factual knowledge had a stronger negative impact on the acceptance of GM than good theoretical knowledge. Positive impacts of theoretical knowledge were not even significantly measurable. It should also be pointed out that gender was not a significant predictor. Its only significance was attached to the fact that female students were more likely to accept industrial application of GM. Study year was a very important positive predictor of accepting GM in medicine production. Regarding the impact of perception of personal health risks, only credence risk was regarded as a negative predictor of acceptance of GM in food and industrial production.

DISCUSSION In the last 2 decades, many studies were conducted with the aim of determining the knowledge, attitudes, and acceptance of genetic modification and biotechnology. In most countries, studies targeted the general population, but there were also several studies that targeted high school students and only a few that targeted university students. The AGREE study differed by being specific and targeting life sciences students.

Table 4. Knowledge of Biotechnology (%) Questions:

True

False

Yeast that is used for brewing beer contains living organisms Plants did not have genes in former times Men always take in genes with their food The father’s genes decide a child’s sex Genetically modified plants have always bigger and/or more fruits All products produced using biotechnology contain modified genes

71.62 19.74 58.03 68.03 70.50 66.51

28.38 80.26 41.97 31.97 29.50 33.49

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Acceptance of Genetic Modification Table 5. Coefficient Estimates of Probit Models Explaining Acceptability of Genetic Modification in Different Areas of Applicationa

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Accept GM in Food Production

Gender (1 D female) Age Study year Attitudes effect Strongly opponents of GM food Attitude toward progress Distrust of institutions Scepticism toward biotechnology Cautious acceptance Perception of personal health risks effect Environmental health risks Credence Behavioral risks Uncultivated food risk Knowledge effect Yeast that is used for brewing beer contains living organisms Plants did not have genes in former times Men always take in genes with their food The father’s genes decide a child’s sex Genetically modified plants have always bigger and/or more fruits All products produced using biotechnology contain modified genes Constant McFadden R2 Right predictions (%) x2

Accept GM in Medicine Production

Accept GM in Industrial Production

Vitamin¡ Enriched Rice

Health Impact

Environment Impact

0.030 (0.079) ¡0.027 (0.021) 0.217 (0.038)

0.180 (0.086) ¡0.004 (0.021) ¡0.011 (0.040)

0.084 (0.079) ¡0.028 (0.022) 0.061 (0.038)

0.124 (0.079) ¡0.009 (0.021) 0.023 (0.038)

0.090 (0.080) 0.032 (0.020) ¡0.037 (0.037)

¡0.400 (0.113) 1.002 (0.149) 1.019 (0.171) 0.177 (0.168) 0.362 (0.180)

0.317 (0.121) 1.367 (0.168) 1.079 (0.191) 0.043 (0.185) 0.245 (0.191)

¡0.860 (0.114) 1.135 (0.149) 0.704 (0.168) ¡0.035 (0.168) 0.396 (0.177)

¡0.836 (0.113) 1.123 (0.149) 0.656 (0.168) ¡0.096 (0.167) 0.297 (0.177)

¡1.112 (0.115) 0.550 (0.150) 0.619 (0.170) ¡0.371 (0.168) ¡0.152 (0.177)

¡0.013 (0.032) ¡0.057 (0.033) 0.025 (0.033) ¡0.017 (0.036)

¡0.035 (0.035) ¡0.070 (0.035) ¡0.001 (0.0365) 0.090 (0.040)

0.008 (0.031) ¡0.084 (0.033) 0.004 (0.032) 0.022 (0.036)

¡0.011 (0.031) ¡0.077 (0.032) ¡0.002 (0.032) ¡0.026 (0.036)

¡0.052 (0.031) ¡0.003 (0.033) ¡0.042 (0.033) ¡0.036 (0.037)

0.254 (0.086)

0.047 (0.094)

0.052 (0.086)

0.141 (0.085)

¡0.019 (0.087)

0.086 (0.097) 0.046 (0.079) 0.282 (0.082) ¡0.196 (0.086)

0.052 (0.107) 0.129 (0.087) 0.063 (0.089) ¡0.383 (0.092)

0.014 (0.098) ¡0.029 (0.079) 0.124 (0.083) ¡0.090 (0.087)

¡0.179 (0.098) ¡0.014 (0.079) 0.130 (0.083) ¡0.050 (0.086)

¡0.046 (0.099) ¡0.075 (0.080) 0.061 (0.084) ¡0.091 (0.087)

¡0.025 (0.083)

¡0.182 (0.090)

¡0.151 (0.084)

¡0.128 (0.083)

¡0.252 (0.085)

¡0.585 (0.433) 0.137 55.07 0.00001

0.364 (0.445) 0.1321 79.82 0.00001

0.280 (0.445) 0.1473 49.03 0.00001

¡0.045 (0.428) 0.1397 47.26 0.00001

¡0.673 (0.412) 0.1379 38.52 0.00001

GM D genetically modified. a Standard errors are reported in parentheses. Significant at *p < 0.05, **p < 0.01, ***p < 0.001, *****p < 0.0001.

Moreover, research conducted within this study was conducted in countries where legislation did not allow the import and distribution of GM food and seeds. Investigation of attitudes and acceptance of genetic modification in the Western Balkans was very specific, because consumers did not come into contact with GM products and had strong, mostly negative, attitudes toward GM. The topic also received widespread media coverage, which was usually accompanied by negative attitudes toward GM products and a prominent concern for potential health side effects. Official representatives of state institutions expressed distrust of GM products, especially in the food industry. No prior studies covering this topic had been conducted in the Western Balkans. Given the low level of knowledge on the part of average consumers in these countries as well as the specific conditions, the choice of life sciences student as the target population in the AGREE study was fully justified. Some limitations of the AGREE study were reflected in the fact that it did not include all countries of the Western Balkans. The sample included students from Serbia, Bosnia, and

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Montenegro but not from Macedonia and Albania. Bearing in mind that these are countries with small populations, a small number of universities and a small number of students, the fact that they were not included in the sample did not significantly change the overall picture provided by the AGREE study. This particularly referred to Macedonia, which has a very similar education system compared to other countries in the sample. In addition, attitudes more strongly predicted future behavior when participants had direct experience with the attitude object and when participants formed their attitudes on the basis of behavior-relevant information [22]. That was not the case with the AGREE study. In addition, respondents were strongly influenced by the media, which was not measured. Furthermore, university students frequently followed scientific publications, so that they might not have been suitable representatives of the general public. The AGREE study has response rate of 48.11%. We analyze the reasons for nonresponse and they included absence from faculty site, lack of motivation to fill out the questionnaire, incompletely filled questionnaire, lack of time, etc.

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Acceptance of Genetic Modification Bearing in mind that we were unable to identify any dominant cause for nonresponse, we assumed an absence of nonresponse bias. In addition, we want to emphasize that this study was conducted as a cross-sectional study and consequently all potential causalities established by the AGREE study need confirmation by a longitudinal study. The AGREE study findings about the students’ acceptance of GM in industry and medicine production and rejection of GM in food production was in line with other studies. Current findings showed that the life sciences students’ acceptance of GM food was increasing and that they were becoming less negative about it [23]. Of course, this could have been expected given that these students had more knowledge about biotechnology than the general population and students of other orientations. However, life sciences students included in the AGREE study were not familiar with practical application of biotechnology. Their knowledge was theoretical, which influenced their attitudes. The connection between being comfortable with practical application of science and technology and positive attitude toward GM had already been demonstrated in previous studies [24–26]. Therefore, we could assume that the situation would be similar in Western Balkan countries and that the attitudes determined in this study would fall under more optimistic and inclined to GM compared to the general population’s viewpoints. In general, attitudes of students in previous research had shown that students had a negative attitude toward GM in food production. This was confirmed in studies involving university students from the United States [10], Finland [26], Turkey [27], Slovakia [28], and South Korea [29]. The AGREE study confirmed that in all identified attitude models, including attitude toward progress, there were concerns about the health effects of genetically modified food. Although 2 attitude models (attitude toward progress and distrust of institutions) accepted GM application in all areas, there is still a great deal of restraint and thinking that GM food cannot be of better quality than the food produced without biotechnology. The other 3 attitude models were in direct opposition to any use of GM in food production. These negative attitudes were more pronounced than in the case of life sciences students from other countries. This could be explained by the extremely negative media campaign via all forms of media in the last few years. A study conducted in similar conditions as the AGREE study was carried out by Prokop et al. [28], which involved Slovakian university students and whose results regarding the attitudes of students were very similar to those in the AGREE study. Slovakia is another country whose legal system bans the distribution of genetically engineered products, which is why Slovakian university students have negative attitudes towards GM products and do not accept them. The AGREE study was the first study that used a Q methodology approach to analyze complex, interrelated, underlying aspects that are essential for the forming of attitudes toward

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genetic modification. The attitude models identified by this approach are the results of complex, previously more general attitudes and heuristic systems that each person has. One attitude or point of view is generated as a combination of unique (individual) and shared (social and cultural) experiences. These subjectivities are not subject to external validation or “objective” proof, and they are critically important for our understanding of human attitudes. The AGREE study showed that the models identified by this approach were the most important for the students’ acceptance of genetic modification. They were also higher predictors of their acceptance, much higher than the knowledge or perception of personal health risks. Five such attitude models were identified in the AGREE study, 3 of which were the main predictors: strong opponents of GM food, attitude toward progress, and distrust of institutions. The attitude model distrust of institutions is an interesting finding for further studies. The big question is whether the students’ acceptance of GM reflected only youthful whim typical of students and opposition to authorities in Serbia that did not allow GM and whether this would change if the government allowed distribution and import of GM food. Although direct comparison between these models and similar models from other studies is difficult due to the fact that Q-models have not been used in the studies of attitudes regarding GM food, it can be concluded that the characteristics of the attitude model distrust of institutions make it unprecedented, which means that it has not been used in similar studies relying on multifactorial explanatory approach [17]. With respect to the above-mentioned students’ knowledge of biotechnology, several studies found that many concepts related to genetically modified food were not well understood by the majority of students [30,31]. The AGREE study found average values of the students’ knowledge. Interestingly, the knowledge was very different, especially with respect to issues related to the practical application of biotechnology, for which knowledge was extremely low and far below the expectations of average students of life sciences. Among all knowledge items, factual knowledge was the most important predictor identified in the AGREE study. The AGREE study also confirmed the existence of poor factual knowledge, which created misconceptions leading toward significant rejection of GM among students. The study also resulted in significant findings on the basis of which these misconceptions stood for negative predictor of acceptance, whereas real knowledge was neither a positive nor negative predictor of acceptance of GM food. However, previous studies had shown that even when factual knowledge was at an acceptable level, mere familiarity with facts sometimes led to greater polarization of opinions. Psychological insights tell us that the views would be stronger if consumers had direct contact with products. Direct contact with the product creates a completely different kind of knowledge that is more important for respondents in the process of forming attitudes and acceptance of products. This is consistent

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Acceptance of Genetic Modification with recent findings from experimental studies. Future research of knowledge about biotechnology and its impact on the formation of attitudes and acceptance of GM has to go in that direction [32,33]. As for gender differences, the AGREE study has shown better knowledge on the part of female students and their greater acceptance of the use of GM in industry in relation to male students. A large number of studies have shown different findings regarding gender, both in terms of knowledge and in terms of acceptance. However, recent studies have concluded that these differences are quantitative rather than qualitative [26]. On the whole, the gender paradox hypothesis, which states that in the case of GM food, women are less accepting of novel products than men, has not been confirmed by the AGREE study. Recent studies are not consistent with this hypothesis [17]. Although larger and systematic studies on this subject have not been implemented in the Western Balkans countries, there was one study that was indirectly focused on GM products. This study examined the factors that affect consumers’ (from northwestern Bosnia and Herzegovina) decisions when they choose a trademark or product, as well as their attitudes concerning product origin, quality, and GM labels. Results showed that 45% of consumers were familiar with the meaning of the label GM although in Bosnia import of GM foods is not yet legalized [34]. Concerns and lack of consumer trust in this region were also confirmed with Vlahovic et al.’s study on consumer attitudes toward organic food consumption in Serbia. When it comes to organic food products, more than a third of respondents still do not trust institutions (i.e., do not believe that the food is produced organically) [35]. Based on this, we can speculate that the attitude model distrust of institutions identified by the AGREE study was not limited only to students. Regional laws and regulations generally conform to EU requirements relating to food safety [36], and specific consumer attitudes in this region should be better explored in future studies.

CONCLUSION Bearing in mind that this kind of study was conducted in the Western Balkans for the first time, the obtained results are of great importance. The AGREE study provided the first rough picture of the knowledge, attitudes, and acceptance of GM in this area. Given the target population, it could be expected that the general population’s acceptance of all observed elements, especially knowledge, would be lower. The AGREE study unambiguously demonstrated that students of life sciences supported the implementation of GM in industry and medicine production but not in food production. Their acceptance was most influenced by 3 out of 5 attitude models that were identified. Those attitude models were strong opponents of GM food, attitude toward progress, and distrust

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of institutions. It is evident that deep-seated heuristics systems, which are difficult to influence, are behind these attitudes. The AGREE study also demonstrated that knowledge had a partial and specific influence on acceptance of GM. Namely, the main knowledge predictor of rejecting GM was misconceptions, whereas real knowledge had no impact. This is important information, primarily for university systems, which points to the need for reevaluation of curricula and education approaches. Small but significant predictors were found in the following: gender (female) was seen as a positive predictor of acceptance of GM in industrial application; regarding the perception of personal health risks, the factor credence risks was seen as a negative predictor of acceptance of GM in industry and food production. It remains unclear which other factors influence the acceptance of GM products, and there is a reasonable assumption that further research should take into account the influence of the media. This assumption is based on similar studies that have helped in understanding of the differences in public perceptions of biotechnology in Europe and the United States [37].

REFERENCES 1. Wilson K, Keelan J: Coping with public health 2.0. Can Med Assoc J 180:1080, 2009. 2. Conner JK: Artificial selection: a powerful tool for ecologist. Ecology 84:1650–1660, 2003. 3. Beale G: The discovery of mustard gas mutagenesis by Auerbach and Robson in 1941. Genetics 134:393–399, 1993. 4. Jackson DA, Symons RH, Berg P: Biochemical method for inserting new genetic information into DNA of simian virus 40: circular SV40 DNA molecules containing lambda phage genes and the galactose operon of Escherichia coli. Proc Natl Acad Sci U S A 69:2904–2909, 1972. 5. Jaenisch R, Mintz B: Simian virus 40 DNA sequences in DNA of healthy adult mice derived from preimplantation blastocysts injected with viral DNA. Proc Natl Acad Sci U S A 71:1250– 1254, 1974. 6. Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang R-Y, Algire MA, Benders GA, Montague MG, Ma L, Moodie MM, Merryman C, Vashee S, Krishnakumar R, Assad-Garcia N, Andrews-Pfannkoch C, Denisova EA, Young L, Qi Z-Q, SegallShapiro TH, Calvey CH, Parmar PP, Hutchison CA, Smith HO, Venter JC: Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329:52–56, 2010. 7. Berg P, Baltimore D, Brenner S, Roblin RO, Singer MF: Summary statement of the Asilomar Conference on recombinant DNA molecules. Proc Natl Acad Sci U S A 72:1981–1984, 1975. 8. Directorate-General for Research and Innovation: “A Decade of EU-Funded GMO Research (2001–2010). Biotechnologies, Agriculture, Food.” European Union, Brussels. 9. Gaskell G: Europeans and biotechnology in 2005: patterns and trends. Eurobarometer 64:83–85, 2006.

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Acceptance of Genetic Modification 10. Hallman WK, Hebden WC, Cuite CL, Auino HL, Lang JT: “Americans and GM Food: Knowledge, Opinion & Interest in 2004.” New Brunswick, NJ: Food Policy Institute, Cook College, Rutgers, the State University of New Jersey. Accessed at: http:// www.foodpolicyinstitute.org 2004. 11. Hossain F, Onyango B: Product attributes and consumer acceptance of nutritionally enhanced genetically modified foods. Int J Consum Stud 28:255–267, 2004. 12. Huang J, Qiu H, Bai J, Pray C: Awareness, acceptance of and willingness to buy genetically modified foods in urban China. Appetite 46:144–151, 2006. 13. Macer D, Ng MAC: Changing attitudes to biotechnology in Japan. Nat Biotechnol 18:945–947, 2000. 14. Aerni P: “Public Attitudes towards Agricultural Biotechnology in Developing Countries: A Comparison between Mexico and the Philippines.” Cambridge, MA: Harvard University, 2001. STI/ CID Policy Discussion Paper No. 10. 15. Curtis KR, McCluskey JJ, Wahl TI: Consumer acceptance of genetically modified food products in the developing world. AgBioForum 7:70–75, 2004. 16. Frewer L: Societal aspects of genetically modified foods. Food Chem Toxicol 42:1181–1193, 2004. 17. Christoph IB, Bruhn M, Roosen J: Knowledge, attitudes towards and acceptability of genetic modification in Germany. Appetite 51:58–68, 2008. 18. Noussair C, Robin S, Ruffieux B: Do consumers not care about biotech food or do they just not read labels? Econ Lett 75:47–53, 2002. 19. Oltersdorf U: Ern€ahrungsabh€angige Gesundheitsrisiken-Einsch€atzung durch Verbraucher. Ern€ahrungsinformation “richtig essenges€ under leben”, 2002. 20. Cross RM: Exploring attitudes: the case for Q methodology. Health Educ Res 20:206–213, 2005. 21. Bredahl L, Grunert KG, Frewer L: Consumer attitudes and decision-making with regard to genetically engineered food products—a review of the literature and a presentation of models for future research. Journal of Consumer Policy 21:251–277, 1998. 22. Glasman LR, Albarracın D: Forming attitudes that predict future behavior: a meta-analysis of the attitude-behavior relation. Psychol Bull 132:778–822, 2006. 23. Priest SH: US public opinion divided over biotechnology? Nat Biotechnol 18:939–942, 2000. 24. Bredahl L: Determinants of consumer attitudes and purchase intentions with regard to genetically modified foods—results of a crossnational survey. Journal of Consumer Policy 24:23–61, 2001.

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25. Grunert KG, Bredahl L, Scholderer J: Four questions on European consumer’s attitudes toward the use of genetic modification in food production. Innov Food Sci Emerg Technol 4:435–445, 2003. 26. Saher M, Lindeman M, Hursti U: Attitudes towards genetically modified and organic foods. Appetite 46:324–331, 2006. 27. Usak M, Erdogan M, Prokop P, Ozelk M: High school and university students’ knowledge and attitudes regarding biotechnology. Biochem Mol Biol Educ 37:123–130, 2009. 28. Prokop P, Leskova A, Kubiatko M, Diran C: Slovakian students knowledge of and attitudes toward biotechnology. Int J Sci Educ 29:895–907, 2007. 29. Finke M, Kim H: Attitudes about genetically modified foods among Korean and American college students. AgBioForum 6:191–197, 2003. 30. Mohapatra AK, Priyadarshini D, Biswas A: Genetically modified food: knowledge and attitude of teachers and students. J Sci Educ Technol 19:489–497, 2010. 31. Hursti K, Magnusson MK: Consumer perceptions of genetically modified and organic foods. What kind of knowledge matters? Appetite 41:207–209, 2003. 32. Scholderer J, Frewer LJ: The biotechnology communication paradox: experimental evidence and the need for a new strategy. Journal of Consumer Policy 26:125–157, 2003.  33. Grunert KG, Bech Larsen T, Lahteenmaki L, Ueland Ø, Astr€om A: Attitudes towards the use of GMOs in food production and their impact on buying intention: the role of positive sensory experience. Agribusiness 20:95–107, 2004. 34. Alibabic V, Jokic S, Mujic I, Rudic D, Bajramovic M, Jukic H: Attitudes, behaviors, and perception of consumers’ from northwestern Bosnia and Herzegovina toward food products on the market. Procedia Soc Behav Sci 15:2932–2937, 2011. 35. Vlahovic B, Puskaric A, Jelocnik M: Consumer attitude to organic food consumption in Serbia. Petroleum Gas University of Ploiesti Bulletin 63:45–52, 2011. 36. Turubatovic L, Veskovic Moracanin S, Geric T: Harmonisation of Serbian and EU food safety regulations. Journal of Hygienic Engineering and Design 1:162–165, 2012. 37. Gaskell G, Bauer MW, Durant J, Allum NC: Worlds apart? The reception of genetically modified foods in Europe and the US. Science 5426 (285): 384–387, 2000. Received November 12, 2014; accepted December 23, 2014.

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APPENDIX Knowledge, attitudes towards and acceptability of genetic modification among students of life science

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Gender: M F University (faculty): Study year: Year of birth: A. Acceptability questions There are lots of discussions about genetic modification. Do you think it would be reasonable to use genetic modification in the following applications? (three options: agree, disagree, do not know) 1. Genetically modified insulin for diabetes treatment instead of pigs’ insulin? 2. Vitamin-enriched rice to prevent deficiency diseases in developing countries? 3. Fibre-enriched potatoes that might prevent colon cancer? 4. Plants which need less fertilizers so that they pollute the environment less than without that modification? 5. Paper made of genetically modified starch to prevent deforestation? B. Attitude towards biotechnology (five-point Likert scale) 1. GM foods can cause an immense benefit for a lot of people 2. Using biotechnology the products can be produced in a way that is friendlier to the environment 3. GM foods might improve the standard of living of future generations 4. The use of biotechnology in food production can solve environmental problems 5. GM foods are of higher quality than those produced without biotechnology 6. Risks related to biotechnology are acceptable 7. GM foods are not necessary 8. Environmental organisations tend to exaggerate and see dangers everywhere 9. Even if nowadays a process is assumed to be safe, it is not known how it develops in 50 years 10. GM foods might cause allergies 11. Even if GM foods have benefits, it still is unnatural 12. GM foods are a danger to human health 13. GM products are always a risk 14. The use of biotechnology in food production might cause environmental risks 15. The food industry will not risk selling a harmful product, because of fear of causing a scandal 16. If scientists declare a product as safe, I will believe that 17. GM products are more strictly controlled than those produced without biotechnology 18. The degree of civilization may be recognized by technical development 19. Due to technical progress, we will be able to solve future problems 20. I don’t trust newly introduced food products 21. Changes in nature due to humans rarely cause any serious problems 22. Biotechnology only serves the interest of big companies C. Perception of personal health risks (five-point scale ranging the personal exposure to different health risks from “very high” to “very low”) “Hazards to health are mentioned daily in the media. How high, do you think is your personal risk posed by the following factors?” Responses ranged from “1 = very high” to “5 = very low”. 1. Food additives 2. Veterinary residues in food 3. Pesticides 4. Genetically modified food 5. Raw food 6. Alcohol

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7. 8. 9. 10. 11. 12.

Cigarettes Unbalanced diet Food borne infections Climate change/ozone hole Radioactivity Road traffic

D. Knowledge of biotechnology (true or false) 1. Yeast that is used for brewing beer contains living organisms 2. Plants did not have genes in former times 3. Men always take in genes with their food 4. The father’s genes decide a child’s sex 5. Genetically modified plants have always bigger and/or more fruits 6. All products produced using biotechnology contain modified genes

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Knowledge, Attitudes Toward, and Acceptability of Genetic Modification among Western Balkan University Students of Life Sciences (AGREE Study).

There are still no data on the attitudes and acceptance of genetic modification (GM) food in European developing countries, such as the Western Balkan...
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