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Food Control 32 (2013) 190e197

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Food Control

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Food safety issues in fresh produce: Bacterial pathogens, viruses and pesticideresidues indicated as major concerns by stakeholders in the fresh produce chain

S. Van Boxstael a,*, I. Habib a,b,1, L. Jacxsens a,d, M. De Vocht a,c, L. Baert a, E. Van De Perre d, A. Rajkovic a,e,F. Lopez-Galvez a, I. Sampers a,f, P. Spanoghe g, B. De Meulenaer d, M. Uyttendaele a

a Laboratory of Food Microbiology and Food Preservation, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, BelgiumbDivision of Food Hygiene and Control, Department of Nutrition, High Institute of Public Health (HIPH), Alexandria University, 165 El-Horrya Avenue, Alexandria, EgyptcDepartment of Communication Science, Faculty Political and Social Sciences, Ghent University, Korte Meer 7-11, 9000 Ghent, BelgiumdResearch Group Food Chemistry and Human Nutrition, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, BelgiumeDepartment of Food Safety and Food Quality Management, Faculty of Agriculture, Belgrade University, Nemanjina 6, 11080 Zemun-Belgrade, SerbiafResearch Group EnBiChem, Department of Industrial Engineering and Technology, University College West-Flanders (Howest), Graaf Karel de Goedelaan 5, 8500 Kortrijk, Belgiumg Laboratory of Crop Protection Chemistry, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, Belgium

a r t i c l e i n f o

Article history:Received 21 June 2012Received in revised form11 November 2012Accepted 17 November 2012

Keywords:Discussion groupFresh produceFood safety issuesControl measuresContextual factorsInformation sources

* Corresponding author. Tel.: þ32 09 264 93 95; faE-mail address: sigrid.vanboxstael@ugent.be (S. V

1 Current address: Bioresources Unit, DepartmentAustrian Institute of Technology GmbH, Tulln, Austria

0956-7135/$ e see front matter � 2012 Elsevier Ltd.http://dx.doi.org/10.1016/j.foodcont.2012.11.038

a b s t r a c t

In January 2011, a workshop was organized by the EU FP7 Veg-i-Trade project to capture opinions ofstakeholders on food safety issues in the global fresh produce supply chain. Food safety experts fromvarious stakeholder types in the farm-to-fork chain were represented: farmer related organizations(n ¼ 6), fresh produce processing and trading companies (n ¼ 17), retail (n ¼ 3), consumer organizations(n ¼ 2), competent authorities (n ¼ 7) and lastly research institutes and universities (n ¼ 19). The expertswho originated mainly from European countries (92.6%) were grouped in nine discussion groups pertype of stakeholder and asked to rank food safety issues via a scoring approach according to perceivedimportance from their stakeholder type point of view. Also information sources for opinion making,appropriate food safety control measures and perceived contextual factors increasingly challenginggovernance of food safety in fresh produce were ranked according to perceived importance. Althoughsome differences were noted between opinions of the different stakeholders, there was in general anagreement on the main priorities in food safety of fresh produce. Bacterial pathogens were overallconsidered to be the most important food safety issue for fresh produce, followed by foodborne viruses,pesticide residues and mycotoxins. Alert systems such as the European Commission’s Rapid Alert Systemfor Food and Feed (RASFF) were considered as the most important source of information of food safetyissues, followed by reports of international organizations (e.g. WHO, EFSA), legislative documents (e.g. EUlegislation), national reports (e.g. on monitoring hazards, foodborne outbreaks) and exchange ofinformation between people (informal contacts). Concerning the control measures, the application ofgood agricultural practices (GAP) was identified to be the most important control measure to assure thesafety of fresh produce, followed by the application of good hygienic practices (GHP) and the certificationof food safety management systems (FSMS). Increasing international trade and globalization were overallexpected to have a large impact on food safety in fresh produce. Other contextual factors perceived to beimportant were the food safety policies by governments and the (lack of) food safety knowledge byconsumers and other stakeholders of the fresh produce supply chain. Although the various stakeholdergroups may conceive issues differently from their proper position in the fresh produce supply chain, nodeep disagreements emerged. This type of workshop enhances interaction and risk communicationbetween stakeholders and contributes to a better understanding of each other’s concerns, constraintsand interests to deal with the food safety of the increasingly complex and globalized fresh producesupply chain.

� 2012 Elsevier Ltd. All rights reserved.

x: þ32 09 225 55 10.an Boxstael).Health & Environment, AIT.

All rights reserved.

1. Introduction

Fresh produce is an important part of a healthy diet. Itsconsumption is known to have a protective health effect against

S. Van Boxstael et al. / Food Control 32 (2013) 190e197 191

a range of illnesses such as cancers and cardiovascular diseases(Block, Patterson, & Subar, 1992; Joshipura et al., 2001; Steinmetz &Potter, 1996). In more than twenty countries (e.g. the Netherlands,Spain, Norway, Belgium, the US and Brazil), fresh produceconsumption is encouraged by governmental health agencycampaigns. They recommend to consume at least five daily servingsof fruit and vegetables (Abadias, Usall, Anguera, Solson, & Vinas,2008). Despite the beneficial health effects of fresh produce, thereis a growing awareness concerning its microbial and chemical foodsafety (Lynch, Tauxe, & Hedberg, 2009; Strawn, Schneider, &Danyluk, 2011). Diseases linked to the sporadic presence of micro-bial hazards such as Salmonella spp., verotoxin producing Escher-ichia coli (VTEC) and norovirus (NoV) increasingly support thisallegation (Berger et al., 2010; FAO/WHO, 2008; Sivapalasingam,Friedman, Cohen, & Tauxe, 2004). In the EU in 2009 and 2010,respectively 4.4% and 10% of the foodborne verified outbreaks werelinked with the consumption of vegetables, fruits, berries, juices(and products thereof) (EFSA/ECDC, 2012). Such outbreaks havebesides very severe consequences for public health also a significanteconomic impact (Calvin, Avendano, & Schwentesius, 2004; WHO,2011a). Other food safety issues such as pesticide residues, anti-microbial resistance, wax coatings, nanomaterials and geneticallymodified organisms are increasingly becoming a concern for thefresh produce supply chain (Domingo & Gine Bordonaba, 2011;Magnuson, Jonaitis, & Card, 2011; Tait & Bruce, 2001). Hence,assuring the safety of fresh produce and alertness to maintainconsumer trust in fresh produce as a healthy food is of paramountimportance for stakeholders. This is a challenging task in anincreasingly globalized and more complex fresh produce foodsupply chain. It implies a shared responsibility of the stakeholderswithin the farm-to-fork continuum (producers, processors, tradingcompanies, retailers and consumers) and those closely involved insupporting food safety in the supply chain (competent authorities,industry associations, food scientists). Several studiesmeasured theperceptions of consumers on various aspects of food safety(Grunert, 2005; Nielsen et al., 2009; Soon-Mi et al., 2011; Sparks &Shepherd, 1994; Tonsor, Schroeder, & Pennings, 2009). A limitednumber of studies on opinions of key stakeholders (experts) on foodsafety policy are available (van Kleef et al., 2006; Sargeant et al.,2007). However, to the authors’ knowledge, a survey with farm-to-fork key stakeholders on priorities and challenges on the safetyof the fresh-produce chain is lacking. In the present study it was theobjective to capture opinions of fresh produce food safety expertswho are member of the EU FP7 Veg-i-Trade consortium (in theproject Veg-i-Trade the impact of climate change and globalizationon the safety of fresh produce is studied) and several other invitedEuropean stakeholders of the fresh produce supply chain. Theopinions of interest concerned the perceived importance for publichealth, economic impact, consumer trust, etc. according to theirstakeholder type point of view and their position as an actor withinor associated to the European oriented global fresh produce supplychainwith regard to four topics: i) food safety issues, ii) informationsources for stakeholders to get informed about food safety, iii)appropriate control measures to keep the fresh produce safe and iv)perceived contextual factors impacting on the food safety of freshproduce. Data collection for each of the topics was performed viadiscussion groups containing food safety experts grouped per typeof stakeholder: farmer related organizations, fresh produce pro-cessing and trading companies, food safety authorities, food scienceresearchers, retailers and consumer organizations. The obtainedinformation within our study gives insight into the current foodsafety priorities and challenges of the fresh produce chain andprovided an opportunity to exchange opinions between variousstakeholders of the fresh produce chain with a focus on the EUsituation.

2. Materials and methods

2.1. Participants and procedure

A total of 54 international experts participated (75 were initiallyinvited) to a workshop that was held on January 28th, 2011 at theFaculty of Bio-Science Engineering, Ghent University (Belgium) asa satellite to the EU FP7 Veg-i-Trade Consortium meeting in Ghent.The participants all have a professional function linked to foodsafety and quality of fresh produce and were recruited based ontheir involvement in the global fresh produce supply chain butwith a focus on EU production, intra community trade or import/export to or from EU, respectively. Fifty participants (92.6%) wererepresentatives from companies/organizations/institutions from 6European countries, namely Belgium (31), Spain (3), theNetherlands (9), France (1), Norway (4) and the UK (2). TheNetherlands, Spain, Belgium and France are important countries forfresh produce production and trade in EUwhile Norway and UK arenet importers. In addition some of the (mainly Belgian) participantswere representatives of fresh produce companies with variousproduction sites in EU, representatives of European fresh produceassociations, or from the European Commission. The other 4participants, all member of the Veg-i-Trade consortium originatedfrom research institutes and universities from India (1), Egypt (1)and South-Africa (2). Among the 54 participants, 27 (from Belgium,Netherlands, Norway, Spain, Egypt, South Africa and India) weremember of the EU FP7 Veg-i-Trade Consortium. The food safetyexperts were divided in nine groups of five to seven persons basedon their expertise: one group with experts from fresh producefarmer related organizations [primary production], three groupswith food safety experts of fresh produce processing and tradingcompanies [industry], three groups with food safety scientists fromuniversities and research institutes [scientists], one group withexperts from food safety authorities [authorities] and one groupcontaining food safety experts from retail and consumer organi-zations [retail/consumer organizations]. The number of participantswithin each group and the countries in which their affiliatedcompanies/institutions/organizations are located are presented inTable 1. Nine separate discussion tables were installed in a largemeeting room. Each table was attended by the members ofa specific discussion group and a moderator of the scientificresearch staff of the Association Ghent University (AUGent). Thegroup discussions were run according to a standardized procedure.To facilitate a common starting point, the concepts and a list ofchoices of i) fresh produce food safety issues and ii) informationsources were explained and subsequently two alphabeticallyordered short lists containing respectively 16 food safety issues (seeTable 2a) and 13 information sources (see Table 2b) were intro-duced by a AUGent researcher via a PowerPoint presentation. Afood safety issue was defined in a broad sense as ‘a concept that iswider than the definition of a food safety hazard by the CodexAlimentarius (biological, chemical or physical agent in a food, or thecondition of, with the potential to cause an adverse health effect(CAC, 2003))’ and included also health, quality and emerging issues.An information source was defined as ‘a source of information (e.g.observations, people, reports, organizations) used for food safetyopinion making’. The lists with topics were drawn up beforehandby the moderator team of AUGent researchers based on grey andscientific literature: food safety issues (Baert, Van Huffel et al., 2011;EC, 2010), control measures (Jacxsens, Devlieghere, & Uyttendaele,2009), information sources (EFSA, 2011a) and contextual factors(Baert et al., 2012; Noteborn & Ooms, 2005). After introduction ofthe short lists, the following questions were asked to each discus-sion group ‘Please rank the 5 most important food safety issuesaccording to your stakeholders group (1¼most important, 2¼ second

Table 1Number of experts in the discussion groups and the countries in which their affili-ated companies/institutions/organizations are located.

N�b BEc ESd FRe NLf UKg EGh INDi NOj SAk

Farmer relatedorganizations

6 (2) 3 2 1

Trade & processingindustry group 1

6 (3) 4 1 1

Trade & processingindustry group 2

5 (2) 2 1 1 1

Trade & processingindustry group 3

6 (2) 4 1 1

Retail/consumerorganizations

5 (1) 5

Food safetyauthoritiesa

7 (2) 4 1 1 1

Scientists group 1 7 (3) 3 1 1 1 1Scientists group 2a 6 (6) 2 1 1 1 1Scientists group 3 6 (6) 4 2

a Discussion group contains one expert affiliated to the European Commission.b Number of experts in the discussion groups (between brackets are the number

of experts in the group who are member of the Veg-i-Trade consortium).c Belgium.d Spain.e France.f Netherlands.g United Kingdom.h Egypt.i India.j Norway.k South-Africa.

S. Van Boxstael et al. / Food Control 32 (2013) 190e197192

most important,.)’ and ‘Please rank the 5 most important informa-tion sources for making up your opinion on the food safety issues byyour stakeholders group (1 ¼ most important, 2 ¼ second mostimportant,.)’. Thus each stakeholder type was deemed to discussand base their ranking upon perceived importance from theirposition and job experience point in relation to the fresh producesupply chain (e.g. as a scientist, manager running a business ordecision makers from competent authorities). The groups wereallocated 45 min for this group discussion. The moderators fromAUGent noted down the consensus Top 5 and also the opinions ofthe different members of each discussion group. This procedurewas repeated two times for the two remaining other topics i.e. i)control measures for assurance of the safety of fresh produce (15items, see Table 2c) and ii) contextual factors affecting the safety ofthe fresh produce chain (15 items, see Table 2d). A control measurewas defined as ‘a measure of managerial and/or technical naturetaken to control food safety hazards along the food chain’. Acontextual factor was defined as a technical, societal, economic,political or legislative factor inside or outside the supply food chainhaving a direct or indirect impact on the safety of the food. Each ofthe discussions for the latter two topics lasted approximately35 min.

2.2. Data analysis

The top 5 lists of the four topics (food safety issues, informationsources, control measures and contextual factors) by the ninegroups were collected. Subsequently an overall ranking of the itemsbased on equal weighting of the opinions of each type of discussiongroup was calculated (5 types: primary production, industry,authorities, scientists, retail/consumer organizations). In summary,aweighting factor (WF) equal to 5, 4, 3, 2,1was assigned to the itemsthatwere selected for the positions 1, 2, 3, 4, 5 respectively in the top5’s. Items that did not occur in any Top 5, received aWF¼ 0. Next, foreach item, a scorewas calculated as the total sum ofWFs andWFs/3depending on whether the item occurred in a top 5 of a single[primary production, authorities, retail/consumer organization] or

threefold [industry, scientists] represented stakeholder group type,respectively. The resulting sum for each item was divided by 5(5 types of discussion groups), which resulted in an averageimportance score between 0 (least important item) and 5 (mostimportant item). The approachof assigning aWForWF/3dependingon whether a group was single represented or threefold allowed toobtain an average importance score for each item reflecting equallythe ranking of each of the five stakeholder group types.

3. Results

3.1. Fresh produce food safety issues

Among the list of predefined food safety issues, the itemsbacterial pathogens (e.g. Salmonella, VTEC), foodborne viruses (e.g.norovirus, Hepatitis A) and pesticide residues (e.g. chlormequat)were identified as the three most important concerns (Table 2a).Next, mycotoxins (e.g. aflatoxins, patulin) and process contami-nants (e.g. disinfection by-products trihalomethanes) belongedalso to the overall top 5. A common criterion for all the stakeholdergroups for prioritization of the food safety issues concerned theestimated health risks of the issues/hazards for the consumer.However, also several other arguments were noted such as thepotential economic implications e.g. recall costs or overall decreasein sales in case of foodborne disease outbreaks reported in thebroad media [primary production, industry]. Also whether thespecific issues are well covered by EU/national legislation wasa motivation by some participants to attribute an important role toa hazard. For hazards for which specific EU criteria are in place suchas pesticide residues on fresh produce (EP and Council, 2005) andSalmonella in ready-to-eat pre-cut fruits and vegetables (EC, 2005),the attributed importance was deemed to be higher [industry].Other ranking argumentations were related to food safety concernsby consumers and various non-governmental organizations, play-ing an important role as a factor in competitiveness betweencompanies [industry, retail]. This argumentation was in particularcited by several participants [primary production, industry] for thehazard pesticides but remarkably, pesticide residues were notselected as a Top 5 item by the retail/consumer organization group.Other participants emphasized that ‘particular attention should go tocontrol of residues of non-authorized pesticides on vegetables andfruits that are imported into the EU’ [authorities]. Some participants[scientists] were of the opinion that ‘mycotoxins represent anemerging issue for fresh produce’. They argued that ‘although thecurrent knowledge on mycotoxins on fresh produce is limited, the foodsafety risk may be larger than is currently known’. It was alsomentioned that ‘due to the trend of using less fungicides, the amountof mold growth on fresh produce might increase and hereto linked thepotential mycotoxin production’ [scientists]. Related to processcontaminants (ranked as fifth important item), the example ofdisinfection by-products (e.g. trihalomethanes) that are formedduring treatment with chlorine based disinfectants of processwater to control microbial contamination of the water was noted.The motivation for not taking up genetically modified foods(GMO’s) in the top 5’s was that according to some participants[industry, scientists] ‘the majority of GMO’s should not be consideredas a food safety problem’. For nanomaterials and antimicrobialresistance, although the potential severity of it were deemed not tobe underestimated, participants found it ‘too early to take it up in thetop 50 [scientists]. It was emphasized that more scientific researchand risk assessments on these topics are required. The issue wasalso raised that ‘despite the chemical and microbiological food safetyrisks linked to the consumption of fresh produce, the main risk may bethe insufficient consumption of nutritional healthy fruits and vegeta-bles, leading to a higher risk of heart diseases and cancer’ [industry].

Table 2Top 5 by the nine groups and average weighted importance score for food safety issues, information sources, control measures and contextual factors.

Sa N�b Top 5 items

PrPrc Ind1d Ind2d Ind3d Re/Coe FSAf Sci1g Sci2g Sci3g

a) Food safety issuesBacterial pathogens 4.8 9 1 1 2 1 1 1 2 2 1Viruses 2.6 7 3 4 2 2 1 3 2Pesticide residues 2.4 7 2 2 1 5 4 4 3Mycotoxins 1.5 5 4 3 3 1 4Process contaminants 1.0 2 3 2Heavy metals 0.8 5 5 5 5 5 4Migrants from food contact materials 0.7 2 3 5Additives 0.4 1 4Allergens 0.3 3 5 4 5Physical hazards 0.2 1 3Quality and freshness of fresh produce 0.2 1 3Not a balanced and healthy diet 0.1 1 4Parasites 0.1 1 5Antimicrobial resistance 0 0Genetically modified food 0 0Nanomaterials 0 0b) Information sourcesAlert systems 3.1 8 1 4 3 3 1 3 5 2International reports 2.1 6 5 4 2 2 2 4Legislation on food safety and legislative documents 1.7 3 1 1 1National reports 1.4 3 3 3 3Information exchange via face-to-face contacts and informal networks 1.3 3 4 2 1Scientific literature 1.1 4 5 1 3 1Popular news media magazines 1.0 3 2 5 4Farmer/industry own information 1.0 4 3 3 5 1Food quality/safety conferences 0.7 4 5 4 4 4Quality assurance standards 0.5 2 2 2Professional journals 0.5 2 4 5Education by training 0.3 2 5 5Information by fresh produce stakeholder associations 0.3 1 2c) Control measuresGood agricultural practices 3.9 8 1 1 2 1 1 1 1 2Good hygienic practices 2.7 7 2 3 2 2 3 2 3Certification of food safety management systems 2.2 6 5 4 4 1 3 4Product control 1.5 4 3 5 3 5Setting criteria/limits 1.4 3 2 4 3Good handling practices 0.7 4 4 3 2 4Food safety/risk communication 0.4 1 4Tracking and tracing 0.4 1 4HACCP 0.4 2 1 5Training and capacity building 0.4 2 5 1Technical intervention 0.3 2 2 5Supplier selection 0.2 1 3Reflection and management 0.2 1 5Research & risk assessment 0.1 2 5 5Process control 0.1 1 4d) Contextual factorsGlobalisation and international trade 3.5 8 2 1 1 3 3 2 1 3Governmental policy 1.8 3 2 2 3Food safety knowledge 1.6 8 3 2 4 4 4 4 5 4Consumer demand 1.5 3 1 4 3Availability of alternative production techniques 1.4 3 1 5 1Legislation and enforcement by government 1.2 2 1 4Climate change 1.1 6 5 5 2 5 5 2Economical/financial climate 0.9 2 3 1Price of food material 0.7 3 4 5 3Eating habits 0.3 1 1Natural distasters 0.3 1 2Alternative detection methods 0.3 1 2Changes in biodiversity 0.2 1 3Demography 0.1 2 5 5Popular news media 0.1 1 4

a Average weighted importance score among the five stakeholder type groups (for calculation see materials and methods, score 0 ¼ least important; score 5 ¼ mostimportant).

b N� Number of groups that selected the particular item in their top 5.c Farmer related organizations.d Fresh produce processing & trading companies group 1, 2 and 3.e Retail and consumer organizations.f Food safety authorities.g Scientists from universities and research institutes group 1, 2 and 3.

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3.2. Information sources

Alert systems were overall identified as the most importantinformation source for food safety (Table 2b). Although severalrapid alert systems are frequently consulted such as the EuropeanCommission‘s (EC’s) Rapid Alert System for Food and Feed (RASFF),ProMED-Mail and INFOSAN, most participants considered the EC’sRASFF as the most important system to stay up-to-date with thelatest evolutions on food safety. International reports were alsofound to be a major information source by all groups except by thefresh produce processing groups. Most of the participants referredto documents of the European Food Safety Authority (EFSA) butalso to reports from the World Health Organization (WHO) andFood and Agriculture Organization (FAO). Besides the internationalreports, also national reports such as surveillance reports ofnational public health authorities or monitoring reports of foodsafety agencies are often consulted. However, it was argued that‘the accessibility of these reports is limited because they are generallyonly published in the national languages’ (in contrast to internationalreports that are mainly written in English) [authorities]. Legislationon food safety is considered to be an important information sourceby the industry and the retail/consumer organization groups. Thenational guides to good practices elaborated by industry associa-tions as an incentive to comply with the Hygiene Regulation (EC)852/2004 (EP and Council, 2004) were also considered as legislativedocuments because ‘they contain an up-to-date overview of thelegislation’ [industry]. Several differences between the selectionpreferences for the information sources among the differentstakeholders were observed. For example scientific literature wasselected as a top 5 information source by the three scientists groupsand the food safety authorities group but not by any of the othergroups while the item ‘industry-own-information’ and qualitystandards were only selected by the primary production and/orprocessing industry groups. Concerning scientific articles, it wasnoted that ‘because of the long time period between submission andacceptance, the availability of this information is late’ [scientists].Besides the paper media, spoken media such as informal face-to-face contacts and networks were also considered to be an impor-tant information source by several participants [scientists].

3.3. Control measures

The application of good agricultural practices (GAP) emerged asthe main control measure to control food safety hazards within thefresh produce supply chain (Table 2c). Next, the application of goodhygienic practices (GHP) was found to be the overall second mostimportant measure. GHP distinguishes itself from GAP beingapplicable to thewhole farm-to-fork continuum and not only to theproduction step by farmers. The application of certified food safetymanagement systems (FSMS) was overall ranked at the third place.Certification of food safety management systems is an additionalstep to the application of GAP and/or GHP implemented in thesesystems. Two main arguments were highlighted to select this item.The first was that ‘the verification and certification of food safetysystems by an outsider, a third party, results in better food safetymanagement systems and subsequently in a safer food chain’[authorities, industry]. The second argument was that ‘compliancewith certified food safety management systems is from a commercialpoint of view very important for gaining consumer trust and an aspectof brand or supplier image protection’. It is considered to be a licenseto trade/sell’ [retail]. The performance of microbiological andchemical analyses on fresh produce (product control) was selectedas a top 5 item by four discussion groups [primary production, retail/consumer, industry, authorities]. Some participants noted that‘product control will become more important when the proportion of

imported products compared to local products will increase’ [author-ities, primary production].

3.4. Contextual factors

In the farm-to-fork continuum, food safety is influenced byseveral contextual factors within and outside the food chain amongwhich globalization and the growing international trade wereattributed the highest impact (Table 2d). Arguments for thisselection were that ‘fresh produce production, processing and tradewithin a globalized context puts pressure on the stakeholders from thefresh produce chain in several ways, for example on the price setting(e.g. raw materials)’ [primary production] but also on ‘the demandsfor food safety of products sourced globally’ [industry, authorities].Several participants argued that ‘within a globalized world, theassurance of food safety will be a greater challenge’ [authorities]. Theimpact of public health policy, food safety policy and agriculturepolicy by governmental competent authorities (governmentalpolicy) was found to be the overall second most importantcontextual factor. The item knowledge on food safety was alsofound to be a major contextual factor and was interpreted ina broad sense by the participants: by some discussion groups[authorities, consumer organization/retail], it was mainly seen as theknowledge (or the lack of knowledge) by consumers but by otherdiscussion groups it was interpreted as the knowledge on foodsafety by the fresh produce processing industry and scientists. Thedemand of consumers as a pressure on food safety was identified asan important contextual factor by three groups [primary production,industry, scientists] among which primary production identified itas the most important factor while food safety reports in thepopular news media were selected as a top 5 item by only onediscussion group [industry]. It was noted that consumers can beinformed by a very broad range of channels (broad news media)and that ‘these channels are not always providing science-basedinformation, but may have a major influence on the consumer’sopinions and therefore impact on the economic activities of variousstakeholders’ (the example of yearly reports on pesticides by variousnon-governmental organizations was given) [primary production].Besides this, ‘these reports may also influence the food safety policy byprocessing and retail companies e.g. the frequency and type of hazardsthat are analyzed‘ [industry]. Availability of alternative processingand storage techniques was identified by two discussion groups asthe most important contextual factor [retail/consumer organization,industry]. The argumentation for this was that ‘as conventionalprocessing techniques like thermal heating can influence productquality of fruits and vegetables, there is an ongoing search for alter-native techniques’. In fact, it was the opinion of some participantsthat these new (non-thermal) processing techniques, for example highpressure or oscillating magnetic fields, can have a positive effect on thefood safety output, but also a negative effect when the obtained(estimated) reduction in microbial load is not very well assessed andvalidated‘ [industry]. The main argument for selecting the itemclimate change as a top 5 contextual factor by five discussiongroups concerned the relation between climate change and waterquality and availability. The example of increased microbiologicalhealth risk after water floods was given as floods can impactnegatively on the microbiological quality of the irrigation water[authorities].

4. Discussion and conclusion

This meeting organized by EU FP7 Veg-i-Trade provided anopportunity to capture the opinions from various key stakeholdersin the EU oriented fresh produce supply chain on four food safetyrelated topics: food safety issues, food safety information sources,

S. Van Boxstael et al. / Food Control 32 (2013) 190e197 195

control measures and contextual factors. The applied quantitativeapproach is different from the one used frequently during opensessions or working groups designed to capture the opinions ofexperts in a qualitative manner resulting in consensus reports(EFSA, 2011a; Havelaar et al., 2010).

It can be assumed that farmers, traders and processors woulduse criteria for ranking food safety items based on socio-economicimpact and client customer relationships whereas consumerorganizations and also retailers would primarily take into accountconsumer trust and potential negative effect for the business ascriteria. For competent authorities, it can be expected that they putthe focus on public health although economic impact is alsoa criterion to be taken into account. Scientists would be expected tofocus mainly on public health risk based on the currently availablescientific knowledge and risk assessments. During the discussionsit was observed that criteria for prioritization of food safety issuesweremultidimensional, consisting of a broad range of scientific andother arguments (see 3.1) who were inspired by several informa-tion sources (see 3.2). In general, limited disagreements emergedon the ranking of the food safety issues. A similar observation wasdone in a study by van Kleef et al. (2006) who found limiteddifferences in the way food safety experts from industry, govern-ment, consumer organizations, research institutes and universitiesperceive different aspects of food safety management. Theyobserved the experts more as a homogenous group, this in contrastto consumers who they considered as a heterogeneous group (vanKleef et al., 2006).

Rapid Alert Systems such as the Rapid Alert Systems for Foodand Feed of the European Commission (RASFF) or ProMED-mailwere overall identified as the most important information sour-ces for staying up-to-date with the most recent evolutions on foodsafety of fresh produce. After the workshop, the EC’s RASFF data-bank was consulted by the AUGent organization team. Subse-quently the shares of notifications by hazard type (e.g. bacterialpathogens, pesticide residues,.) for the category fruits and vege-tables and also for the category herbs and spices were calculated forthe period 2008e2010 and 2011 (Table 3). Bacterial pathogens wereidentified by the discussion groups as themost important challengefor fresh produce. However, Table 3 shows that for the categoryfruits and vegetables (period 2008e2010) only a moderate share ofnotifications (3.9%) is due to bacterial pathogens while the totalshare of notifications for pesticide residues is about tenfold larger(39.2%). In the category herbs and spices, bacterial hazards repre-sent a larger share of the notifications (24.9%) compared to the

Table 3Notifications to the European commission RASFF system for the categories ‘fruitsand vegetables’ and ‘herbs and spices’ during the period 2008e2010 and 2011.

Fruits and vegetables Herbs and spices

2008e2010(n ¼ 1338)

2011(n ¼ 669)

2008e2010(n ¼ 452)

2011(n ¼ 197)

Pesticide residues 39.2% 45.7% 12.1% 15.7%Mycotoxins 18.5% 13.6% 36.3% 31.5%Bacterial pathogens 3.9% 16.7%a 24.9% 32.0%Additives 9.0% 3.9% 0.6% 0.0%Hygiene/quality hazard 12.5% 7.8% 5.3% 8.6%Physical hazards 4.9% 2.1% 0.6% 0.5%Heavy metals 1.8% 1.3% 0.0% 1.0%Viruses 1.0% 1.2% 0.0% 0.0%Chemical hazard 4.9% 3.0% 0.8% 0.5%Parasites 0.0% 0.0% 0.0% 0.0%Unauthorized colour 0.0% 0.0% 15.4% 8.1%Other 4.4% 4.6% 4.0% 2.0%Total 100.0% 100.0% 100.0% 100.0%

a 11.8% is related to alerts on Salmonella in paan leaves; 4.9% is related to otheralerts such as VTEC in sprouted seeds, Salmonella in melons or Campylobacter inbaby corn.

share of pesticide residues (12.1%). An increase of the share ofRASFF notifications related to bacterial pathogens during the year2011 to 16.7% for fruits and vegetables (among which 11,8% of thealerts related to Salmonella in paan leaves imported fromBangladesh or India) and to 32% for herbs and spices was observed.This can be interpreted as an indication for the increasing impor-tance of bacterial pathogens for fresh produce. For viruses, identi-fied as the second most important concern by the discussiongroups, the share of alerts related to fruits and vegetables was 1.0%(2008e2010) and 1.2% (2011) while for herbs and spices no alertswere notified.

One of the plausible explanations why experts classified bacte-rial pathogens and viruses as the relatively most importantconcerns is that in case of a foodborne outbreak the consequencesare often severe both from public health point of view (highnumber of cases and high severity of disease) and from theeconomic point of view (loss of sales and trust). This was exem-plified in the year after the workshop by both the VTEC O104:H4outbreak in Germany in MayeJuly 2011 (EFSA, 2011b;WHO, 2011b)associated to consumption of sprouted seeds (4075 affectedpersons, including 908 hospitalizations and 50 deaths) and lateron a NoV outbreak in Germany in SeptembereOctober 2012(RKI, 2012) associated to consumption in school canteens ofa desert containing frozen strawberries (10950 cases, including 38hospitalizations).

For the established bacterial pathogens (e.g. Salmonella) stan-dardmethods are availablewhile for foodborne viruses such as NoVand Hepatitis A virus detection methods have only recently beendescribed and adopted and are not yet taken up in surveillanceprograms in many countries (Baert, Mattison et al., 2011). The sameholds for parasites for which capacity of detection is even morerestricted to a limited number of expert labs (Skotarczak, 2009).The latter may explain the absence of rapid alerts for parasites inTable 3 and the low ranking that this biological hazard achievedduring the workshop.

Mycotoxins were considered by the scientist groups as anemerging issue for fresh produce (e.g. alternariol on tomatoes)while their importance was estimated as low by the fresh produceprocessing experts. The scientific literature comprises severalstudies indicating the potential presence of mycotoxin producingfungi on fruits, fruit salads and vegetables (Ostry, 2008; Tournas,Heeres, & Burgess, 2006; Tournas & Katsoudas, 2005). However,scientific literature was not selected as an important informationsource by the experts from fresh produce processing and tradingcompanies who noted to consult other information sources such asrapid alert systems, legislation, industry own information andquality standards. Indeed the rapid alerts contain currently limitedinformation on mycotoxins on fresh produce. The notifications ofmycotoxins in fruits and vegetables and herbs and spices (Table 3)are entirely linked to dried products such as dried figs, raisins, chilipowder and paprika powder but are not linked to fresh vegetables,fruits and herbs. Also legislation, private collective and individualcompany standards do currently not cover “emerging mycotoxins”on fresh produce. This different use of information sources illus-trates the importance of exchange of information on hazards andrisks between food industry and scientists to disseminate theavailable information on emerging issues in a timely and efficientmanner (EFSA, 2009).

Among the discussed contextual factors during the workshop,the commonly acknowledged contextual factors such as global-ization and the growth of international trade were also identifiedto increase the risk of food safety (Havelaar et al., 2010;Lineback, Pirlet, Van Der Kamp, & Wood, 2009; Quested, Cook,Gorris, & Cole, 2010). The food safety authority experts wereconvinced that because of growing international trade, border

S. Van Boxstael et al. / Food Control 32 (2013) 190e197196

control of products will become increasingly important as anadditional measure to assure food safety. A regulatory frameworkto operationalize this concern is already in place in the EU:currently, the European Commission performs risk analysis, leadingto an increased border control of imports depending upon theirorigin. Examples are an increased analysis frequency for Salmonellaon basil imported from Thailand or for pesticide residues ontomatoes originating from Turkey (EC, 2009). Interestingly, themicrobiological and chemical analyses of food products were by thescientists not considered as an important control measure, sug-gesting that they are familiar with the limitations related tosampling and product analysis from a statistical point of view, inparticular for microbial hazards (Jongenburger, Reij, Boer, Gorris, &Zwietering, 2011; Pinto, Costafreda, & Bosch, 2009).

The lack of food safety knowledge was perceived to have animportant impact on food safety of fresh produce. Informationcampaigns on how to handle and wash vegetables and fruits (e.g.the UK FSA ‘vegetable best served washed’ campaign (FSA, 2011))are targeted to increase awareness and food safety knowledge byconsumers. However, the success of information campaigns dependon a whole range of elements such as consumer knowledge, socio-cultural factors and use of the appropriatemedia (Jacob, Mathiasen,& Powell, 2010).

The crucial role of “best practices” (whether GAP or GHP) toimprove food safety was identified as the most important controlmeasure strategy to prevent contamination. The relevance of GAP orGHP is generally recognized (Beuchat & Ryu, 1997; Brackett, 1999;da Cruz, Cenci, & Maia, 2006; De Roever, 1998) and is also the focusof the General Food Law as well as many voluntary collective orprivate standards and guidelines to the sector to guarantee safefresh produce. In addition, certification of food safety managementsystems by third-parties was also considered to be valuable forassuring food safety and quality as an independent audit team haveno stake in the outcome of the transaction andmay better recognizepotential failures or provide suggestions for improvement(Hatanaka, Bain, & Busch, 2005). Third party certification (e.g.Global GAP) is at present also a compulsory demand by retailers totheir suppliers and can be classified as a license to trade.

In conclusion, the workshop confirmed the acknowledgementof EU stakeholders of the fresh produce supply chain becomingincreasingly characterized by global sourcing and internationaltrade and thus resulting in a more complex food chain whichgreatly increases the challenges for food safety. The currently mostimportant fresh produce food safety issues for the European freshproduce market were identified to be bacterial pathogens, virusesand pesticide residues. An integrated farm-to-fork approach byimplementing preventive measures is of paramount importance toreduce food safety risks as low as reasonable achievable (ALARA).Alert systems such as the EC’s RASFF are the most often consultedinformation sources for forming food safety opinions by stake-holders whereas scientific papers are only addressed by particulargroups of stakeholders such as scientists and policy makers. Thistype of workshop facilitates interaction and risk communicationbetween stakeholders and contributes to a better understanding ofeach other’s concerns, constraints and interests to deal with thefood safety of the increasingly complex and globalized freshproduce supply chain.

Acknowledgements

This research is conducted within the framework of the EU FP7Veg-i-trade project ‘Impact of Climate Change and Globalization onSafety of Fresh Produce e Governing a Supply Chain of Uncom-promised Food Sovereignty’ (www.veg-i-trade.org, grant agree-ment no 244994).

Our special appreciation goes to all participants of theworkshopfor sharing their food safety experiences and opinions and also tothe personnel of the Laboratory of Food Preservation and FoodMicrobiology, Faculty of Bioscience Engineering, Ghent Universityfor assistance with the organization of the workshop.

References

Abadias, M., Usall, J., Anguera, M., Solson, C., & Vinas, I. (2008). Microbiologicalquality of fresh, minimally-processed fruit and vegetables, and sproutsfrom retail establishments. International Journal of Food Microbiology, 123,121e129.

Baert, L., Mattison, K., Loisy-Hamon, F., Harlow, J., Martyres, A., Lebeau, B., et al.(2011). Review: norovirus prevalence in Belgian, Canadian and French freshproduce: a threat to human health? International Journal of Food Microbiology,151, 261e269.

Baert, K., Van Huffel, X., Jacxsens, L., Berkvens, D., Diricks, H., Huyghebaert, A., et al.(2012). Measuring the perceived pressure and stakeholder’s response that mayimpact the status of the safety of the food chain in Belgium. Food ResearchInternational, 48, 257e264.

Baert, K., Van Huffel, X., Wilmart, O., Jacxsens, L., Berkvens, D., Diricks, H., et al.(2011). Measuring the safety of the food chain in Belgium: development ofa barometer. Food Research International, 44, 940e950.

Berger, C. N., Sodha, S. V., Shaw, R. K., Griffin, P. M., Pink, D., Hand, P., et al. (2010).Fresh fruit and vegetables as vehicles for the transmission of human pathogens.Environmental Microbiology, 12, 2385e2397.

Beuchat, L. R., & Ryu, J. H. (1997). Produce handling and processing practices.Emerging Infectious Diseases, 3, 459e465.

Block, G., Patterson, B., & Subar, A. (1992). Fruit, vegetables, and cancer prevention ea review of the epidemiologic evidence. Nutrition and Cancer-an InternationalJournal, 18, 1e29.

Brackett, R. E. (1999). Incidence, contributing factors, and control of bacterialpathogens in produce. Postharvest Biology and Technology, 15, 305e311.

CAC (CodexAlimentariusCommission). (2003).Generalpriniciples of foodhygieneeCAC/RCP1-1969. Rev. 4. http://www.codexalimentarius.org/standards/list-of-standards/en/?provide¼standards&orderField¼fullReference&sort¼asc&num1¼CAC/RCP.

Calvin, L., Avendano, B., & Schwentesius, R. (2004). The economics of food safety: Thecase of green onions and Hepatitis A outbreaks. USDA Economic Research Service,Report from the. http://www.ers.usda.gov/publications/vgs/nov04/VGS30501/VGS30501.pdf.

da Cruz, A. G., Cenci, S. A., & Maia, M. C. (2006). Quality assurance requirements inproduce processing. Trends in Food Science & Technology, 17, 406e411.

De Roever, C. (1998). Microbiological safety evaluations and recommendations onfresh produce. Food Control, 9, 321e347.

Domingo, J. L., & Gine Bordonaba, J. (2011). A literature review on the safetyassessment of genetically modified plants. Environment International, 37,734e742.

EC (European Commission). (2005). Commission Regulation (EC) N� 2073/2005 of15 November 2005 on microbiological criteria for foodstuffs. Official Journal ofthe European Union, L338, 1e26.

EC (European Commission). (2009). Commission Regulation (EC) N� 669/2009 of 24July 2009 implementing Regulation (EC) N� 882/2004 of the European Parlia-ment and of the Council as regards the increased level of official controls onimports of certain feed and food of non-animal origin. Official Journal of theEuropean Union, L194, 1e21.

EC (European Commission). (2010). Food related risks. Special Eurobarometer 354,(pp. 1e168). http://ec.europa.eu/public_opinion/archives/eb_special_359_340_en.htm.

EFSA (European food safety authority). (2009). Report advisory group on riskcommunication. Risk Communication Annual Review (pp. 1e48) http://www.efsa.europa.eu/en/agrc/documents/agrccommreview.pdf.

EFSA (European food safety authority). (2011a). Scientific colloquium on emergingrisks in food: from identification to communication. In EFSA ScientificColloquium Summary Report 15, 1e170. http://www.efsa.europa.eu/en/supporting/pub/114e.htm.

EFSA (European food safety authority). (2011b). Shiga toxin-producing E. coli (STEC)O104:H4 2011 outbreaks in Europe: taking stock. EFSA Journal, 9, 1e22.

EFSA/ECDC (European food safety authority/european centre for disease control).(2012). The European union summary report on trends and sources ofzoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA Journal, 10,2597e3039.

EP and Council (European Parliament and Council). (2004). Regulation (EC) 852/2004 of the European Parliament and of the Council of 29 April 2004 on thehygiene of foodstuffs. Official Journal of the European Union, L139, 1e23.

EP and Council (European Parliament and Council). (2005). Regulation (EC) 396/2005 of the European Parliament and of the Council of 23 February 2005 onmaximum residue levels of pesticides in or on food and feed of plant andanimal origin. Official Journal of the European Union, L70, 1e16.

FAO/WHO (Joint FAO/WHO (Food and Agricultural Organization/World HealthOrganization)). (2008). Microbiological hazards in fresh leafy vegetables andherbs. Microbiological Risk Assessment Series, 14, 1e163. http://www.who.int/foodsafety/publications/micro/mra_fruitveges/en/index.html.

S. Van Boxstael et al. / Food Control 32 (2013) 190e197 197

FSA (Food standards agency). (2011). Vegetable best served washed. http://www.food.gov.uk/news/newsarchive/2011/dec/vegcampaignni.

Grunert, K. G. (2005). Food quality and safety: consumer perception and demand.European Review of Agricultural Economics, 32, 369e391.

Hatanaka, M., Bain, C., & Busch, L. (2005). Third-party certification in the globalagrifood system. Food Policy, 30, 354e369.

Havelaar, A. H., Brul, S., de Jong, A., de Jonge, R., Zwietering, M. H., & ter Kuile, B. H.(2010). Future challenges to microbial food safety. International Journal of FoodMicrobiology, 139, S79eS94.

Jacob, C., Mathiasen, L., & Powell, D. (2010). Designing effective messages formicrobial food safety hazards. Food Control, 21, 1e6.

Jacxsens, L., Devlieghere, F., & Uyttendaele, M. (2009). Quality management systemsin the food industry. Sofia: St Kliment Ohridiski University Press.

Jongenburger, I., Reij, M., Boer, E., Gorris, L., & Zwietering, M. (2011). Random orsystematic sampling to detect a localised microbial contamination withina batch of food. Food Control, 22, 1448e1455.

Joshipura, K. J., Hu, F. B., Manson, J. E., Stampfer, M. J., Rimm, E. B., Speizer, F. E., et al.(2001). The effect of fruit and vegetable intake on risk for coronary heartdisease. Annals of Internal Medicine, 134, 1106e1114.

van Kleef, E., Frewer, L. J., Chryssochoidis, G. M., Houghton, J. R., Korzen-Bohr, S.,Krystallis, T., et al. (2006). Perceptions of food risk management among keystakeholders: results from a cross-European study. Appetite, 47, 46e63.

Lineback, D. R., Pirlet, A., Van Der Kamp, J.-W., & Wood, R. (2009). Globalization,food safety issues & role of international standards. Quality Assurance and Safetyof Crops & Foods, 1, 23e27.

Lynch, M., Tauxe, R.,V., & Hedberg, C. (2009). The growing burden of foodborneoutbreaks due to contaminated fresh produce: risks and opportunities.Epidemiology and Infection, 137, 307e315.

Magnuson, B. A., Jonaitis, T. S., & Card, J. W. (2011). A brief review of theoccurrence, use, and safety of food-related nanomaterials. Journal of FoodScience, 76, R126eR133.

Nielsen, H. B., Sonne, A. M., Grunert, K. G., Banati, D., Pollak-Toth, A., Lakner, Z., et al.(2009). Consumer perception of the use of high-pressure processing and pulsedelectric field technologies in food production. Appetite, 52, 115e126.

Noteborn, H., & Ooms, W. (2005). Pan-European pro-active identification of emergingrisks in the field of food production. Project ERA-NET SSA PERIAPT, financed by theEuropean Commission in the 6th FP. The Hague, The Netherlands: VWA.

Ostry, V. (2008). Alternaria mycotoxins: an overview of chemical characterization,producers, toxicity, analysis and occurrence in foodstuffs. World MycotoxinJournal, 1, 175e188.

Pinto, R. M., Costafreda, M.,I., & Bosch, A. (2009). Risk assessment in shellfish-borne outbreaks of hepatitis A. Applied and Environmental Microbiology, 75,7350e7355.

Quested, T., Cook, P., Gorris, L., & Cole, M. (2010). Trends in technology, trade andconsumption likely to impact on microbial food safety. International Journal ofFood Microbiology, 139, S29eS42.

RKI (Robert Koch Institut). (2012). Großer gastroenteritis-ausbruch durcheine charge mit noroviren kontaminierter tiefkühlerdbeeren in kinder-betreuungseinrichtungen und Schulen in Ostdeutschland. EpidemiologischesBulletin, 41, 415e417.

Sargeant, J., Ramsingh, B., Wilkins, A., Travis, R., Gavrus, D., & Snelgrove, J. (2007).Constraints to microbial food safety policy: opinions from stakeholder groupsalong the farm to fork continuum. Zoonoses and Public Health, 54, 177e184.

Sivapalasingam, S., Friedman, C. R., Cohen, L., & Tauxe, R. V. (2004). Fresh produce:a growing cause of outbreaks of foodborne illness in the United States, 1973through 1997. Journal of Food Protection, 67, 2342e2353.

Skotarczak, B. (2009). Methods for parasitic protozoans detection in theenvironmental samples. Parasite-Journal de la Societe Francaise de Parasitologie,16, 183e190.

Soon-Mi, S., Sun, H. S., Youngja, L., Gui-Im, M., Min-Shik, K., & Ju-Hee, P. (2011).Consumers’ knowledge and safety perceptions of food additives: evaluationon the effectiveness of transmitting information on preservatives. FoodControl, 22.

Sparks, P., & Shepherd, R. (1994). Public perceptions of the potential hazardsassociated with food-production and food-consumption e an empirical-study.Risk Analysis, 14, 799e806.

Steinmetz, K. A., & Potter, J. D. (1996). Vegetables, fruit, and cancer prevention:a review. Journal of the American Dietetic Association, 96, 1027e1039.

Strawn, L. K., Schneider, K. R., & Danyluk, M. D. (2011). Microbial safety of tropicalfruits. Critical Reviews in Food Science and Nutrition, 51, 132e145.

Tait, J., & Bruce, A. (2001). Globalization and transboundary risk regulation:pesticides and genetically modified crops. Health Risk & Society, 3, 99e112.

Tonsor, G. T., Schroeder, T. C., & Pennings, J. M. (2009). Factors impacting food safetyrisk perceptions. Journal of Agricultural Economics, 60, 625e644.

Tournas, V. H., Heeres, J., & Burgess, L. (2006). Moulds and yeasts in fruit salads andfruit juices. Food Microbiology, 23, 684e688.

Tournas, V. H., & Katsoudas, E. (2005). Mould and yeast flora in fresh berries,grapes and citrus fruits. International Journal of Food Microbiology, 105,11e17.

WHO (World Health Organization). (2011a). Foodborne outbreaks: managing therisks. Bulletin of the World Health Organization, 89, 554e555. http://www.who.int/bulletin/volumes/89/8/11-040811/en/index.html.

WHO (World Health Organization). (2011b). International health regulations.Outbreaks of E. coli O104:H4: update 30. http://www.euro.who.int/en/what-we-do/health-topics/emergencies/international-health-regulations/news/news/2011/07/outbreaks-of-e.-coli-o104h4-infection-update-30.