On the efficacy of current biosecurity measures at EU borders to prevent the transfer of zoonotic and livestock diseases by travellers

Abstract

Although many animal diseases have been eradicated from the European Union (EU), the animal production sectors in the EU are still under a major threat of disease pathogens introduced by travellers into a country through illegal importation of wildlife or production animals, and/or food products of animal origin. These may carry (exotic) pathogens or toxic metabolites that are hazardous for public health and have a zoonotic potential. According to experts, newly emerging diseases will most probably be zoonotic in nature. The control systems and inspection measures at the borders are, in general, sufficient to control the import of disease pathogens through commercial consignments, as regularly reported by the Food and Veterinary Office (FVO). The Schengen Agreement in the EU has pushed such inspections to the outer borders of the EU in the context of freedom of movement of ‘goods’ – including live animals and foods of animal origin – people and services within the EU (Treaty of Rome). However, it is questionable whether this policy and the inspection measures taken are effective in reducing public and animal health risks in the EU to an acceptable level. Risk assessment studies point to the potential dangers of illegal imports by travellers. This review article discusses the current status quo and more, in particular, the weaknesses of the current inspection procedures related to biosecurity and suggestions for improvement are made.

Keywords:

• EU border controls
• biosecurity
• food imports
• zoonotic diseases
• disease outbreaks
• foods of animal origin
• travellers

1. Introduction

In the EU, many classical animal diseases, such as rinderpest and foot-and-mouth disease, have, over the past decades, been largely eradicated in a long and costly way. Currently, in many European countries efforts are being made to eradicate other diseases, such as bovine virus diarrhoea (BVD), bovine Herpes virus-1 (infectious bovine rhino-tracheitis, IBR), and salmonellosis in dairy cows, and Aujeszky´s disease and Salmonellosis in pigs. Several EU member states are now officially free of some of these diseases. However, the various Member States’ cattle population remains susceptible to these agents. Hence, one has to remain vigilant. A single failure at border control may waste decades of huge financial efforts by the farming community and national authorities. Moreover, once pathogens have been introduced into the EU, in food animals or in wildlife, there is little that can be done by local farmers or veterinarians to sufficiently protect the herds. Also, in case of highly contagious diseases such as classical swine fever or foot-and-mouth disease, many animals have to be killed within a restriction zone, and this does not exclusively apply to affected animals. The latter will cause a huge economic loss, as well as represents socio-economic hardship for the farmers’ community and the society at large.

More than 1000 pathogens of humans are known, of which a majority are zoonotic. Currently, between 50% and 75% of all emerging pathogens are zoonotic in nature and most probably originate from wildlife (FLI 2010). It has been stated that the emergence of exotic epidemics and new serotypes of e.g. Bluetongue virus is to be expected and that the next exotic epidemics could very well be zoonotic ones (FLI 2010). This puts high demands on public health care, because, in addition to inter-animal transmission, there is the risk of diseases being transferred to humans via contaminated foods of animal origin, mostly as a result of illegal imports (FLI 2010).

Some 10 to 20 years ago, when travelling from Europe to e.g. the USA or Australia, one was obliged to fill out a questionnaire for European customs, on which boxes had to be checked off in case the traveller had recently visited a farm or had carried foods of animal origin. Upon entry into the USA or Australia this is still being applied, because these countries consider this an essential element of their overall biosecurity measures that aim at preventing the introduction of zoonotic diseases through live animals or goods of animal origin (CBP 2013). In the Treaty of Rome of 1957 and its revisions (EuroKnow 2012; Saravuth Pitiyasak 2013) the freedom of movement of goods, people and services within the EU (see Section 3 below) has been postulated. This not only has an economic rationale, but also a general public relevance. The European Union (EU) considers the borders of the outer member states as the borders of the EU. These member states have (a limited number of) border inspection posts (BIPs). Since the so-called Schengen Agreement was accepted in the EU in 1985 (further expanded in 1997), there is even more freedom of travelling for people and trading of goods including food products within the Schengen area (currently including 22 EU member and 4 non-EU member states). Hence, the EU BIPs deal mainly with travellers and commercial imports from third countries. BIPs can be found in airports, ports and major railway, road and post entry stations. Incidentally, one must confront the fact that other ‘entry-points’ exist, where border traffic takes place, and at these locations full-fledged inspection procedures are not necessarily in place. Although little recorded information on the latter is available, this contribution deals with EU entry points in general.

It would seem timely to raise the question: to what extent public and animal health is secured in the EU Schengen area as far as travellers are concerned, as compared to, for example, the USA and Australia? Answering this question is the main objective of this article. In addition, we present some field examples and recommendations for improvement.

2. Animal health and public health pathogens and the risk of their transmission

In the scientific literature various overviews on the (means of) transfer of zoonotic agents via various species of live animals or foods of animal origin are available (e.g. Merck 1973; Buncic et al. 2009; Poljak 2009; HPA 2012; Petdoc 2012). As an example, Table 1 presents the most important bacterial public health hazards related to dairy farming (EFSA 2008 in Smulders 2012). Obviously, there are also hazards related to the prevalence of parasites, viruses, prions and fungi. In Table 1 the modes of transfer of bacterial hazards have been indicated as ‘Category A’ (referring to disease pathogens transmissible to humans through animal contacts) and ‘Category B’ (referring to potentially harmful (contaminated) food products of animal origin or animals infected with zoonotic agents, entering a country illegally).

Table 1. The most important bacterial public health hazard related to dairy farming (¹ = A = through contact with animals; B = through animal products). Adapted from Smulders (2012).

Bacteria	Main on-farm sources	Main dairy–human link	Transfer^1
Bacillus anthracis	Soil; cows	Contact infection (e.g. during handling of skin or processing); rarely a food-borne disease.	A	(B)
Bacillus cereus	Cows; soil; vegetation	Via milk and beef		B
Brucella abortus	Cows	Contact infection (e.g. from handling infected animals/materials). Also via raw milk/milk products	A	(B)
VTEC	Cows; effluents; water; organic fertilisers	Mainly via meat and milk. Also via contact with cattle and associated environment	(A)	B
Campylobacter jejuni	Cows; effluents; water; organic fertilisers	Mainly via milk, and also via beef.		B
Clostridium perfringens	Cows; soil	Mainly via beef		B
Corynebacterium pseudotuberculosis	Cows	Contact infection. Also from raw milk	A	(B)
Erysipelothrix rhusiopathia	Cows	Mainly contact infection	A
Leptospira spp	Cows; rodents; contaminated water	Contact infection, from infected animal or rodent's urine or contaminated water	A
Listeria monocytogenes	Soil; effluents; water; silage; cows	Mainly via milk and beef. Also contact infection from handling infected animals/ materials	(A)	B
Salmonella spp	Cows; water; effluents; organic fertilisers	Mainly via milk and beef		B
Staphylococcus aureus	Cows; humans	Mainly via milk and beef		B
Mycobacterium bovis	Cows	Primarily via milk; very rarely via beef		B
Mycobacterium avium subsp. paratuberculosis	Cows	Possibly via milk and, less likely, beef (debatable)		B
Yersinia enterocolitica	Cows; water	Mainly via milk		B
Coxiella burnetii (Q fever)	Cows; ticks	Via contact, aerosol and milk. Possibly via tick bites	A	B

Given the pathogens and these two major ways of transmission, it should not be a surprise that the USA customs officers ask all passengers from outside the USA to mark the boxes on the entry form associated with category ‘A’ and/or ‘B’. Some of the pathogens listed in Table 1 cause disease in cattle (e.g. B. anthracis, B. abortus, Leptospira spp., and Listeria spp.) while others (e.g. VTEC) do not. This means that even when citizens are visiting a dairy farm and have direct contact with apparently healthy cattle, they can never be sure that those animals are indeed free of pathogens as illustrated by the findings of Elder et al. (2000). The same is true for foods of animal origin. For example, through the transport of milk or beef products from one country to another, pathogenic microorganisms or their toxic metabolites may be transferred. An example from the pig production sector, repeatedly occurring over time, is the case of pork sausages, manufactured in a country or on a farm where African swine fever is endemic and which may be transported by tourists to another country, where leftovers may be thrown away to ultimately end up in swine swill; the disease can hence be transmitted (ISID 2012). Simian viruses (simian immunodeficiency virus [SIV], simian T-lymphotropic virus [SLV], and simian foamy virus [SFV]), herpes viruses like cytomegalovirus [CMV] and lymphocryptovirus [LCV] all of which are associated with infected or contaminated bush meat, have also been identified as rare but serious public health risks, as has been reported by Switzer (2004).

A comprehensive list, including examples of biological food safety hazards associated with all major sectors of food producing animals, such as pigs, ruminants and poultry, can be found in Buncic et al. (2009). Obviously, there are many types of pathogens that are a potential hazard to the three major food animal production sectors, apart from those specifically threatening public health.

3. Policy of the EU regarding free movement and import of animals and food

3.1. EU legislation

The Treaty of Rome in 1957 and its revisions in 1986, 1992 and 1997, focuses on the internal EU market without internal borders. Products originating from a third country and entering the EU must be considered as ‘free to move’ within member states, provided that: (a) import formalities have been complied with; (b) any customs duties or charges have been levied in the importing member state; (c) those goods have not benefited from partial drawback of such duties/charges.

Free movement within the EU refers to goods, people, services and capital. Obstacles to such free movement must be accepted, as long as the general provision for free movement are considered necessary. The latter is to satisfy mandatory requirements relating in particular to the effectiveness of fiscal supervision, protection of public health, fairness of commercial transactions and defence of the consumer. Exceptions to the general provisions are the principle of equivalence and the principle of non-discrimination and proportionality. Judging by the law cases over the past years, there is frequently an interpretation problem related to the general provisions and their exemptions for the free movement of goods (EuroKnow 2012; Saravuth Pitiyasak 2013).

Furthermore, the objective of the EU's food safety policy is to protect consumer health and interests, while guaranteeing the smooth operation of the single EU market. To achieve this objective, the EU ensures that control standards are established and adhered to as regards food and food product hygiene, animal health and welfare, plant health and preventing the risk of contamination from external substances. Over the past decade this policy underwent a reform, in line with the ‘from farm to fork’ approach, thereby guaranteeing a high level of safety for foodstuffs and food products of animal origin marketed within the EU. This approach also involves commercial food products imported from third countries (EU 2012a). Moreover, the EU has issued several directives and regulations pertaining to the importation of animals and foods of animal origin and the veterinary controls of importation: EC 206/2009 (regarding the introduction of products of animal origin [POAO]), EC 97/78, 91/496/EC and EC 136/2004 (on the organisation and procedures for veterinary checks on animals and their products at border inspection points), and further EC 2007/275 (on animals and animal products subject to controls at border inspection points). Most of these texts only refer to the commercial trade of food and food products, including those of animal origin, and usually in large quantities (EU 2012b).

It has been stated that some food products are exempted from the control at outer EU borders. Among these products are those meant for personal consumption (potentially present in travellers’ luggage), those sent by post in small volumes to individuals and those sent as trade samples (EU 2012b; FVO 2013; see also directives 91/496/EC and 97/78/EC). Risk assessment studies associated with these exemptions have not been conducted, leaving uncertainty about the potential hazards related to these importations. If a serious threat to animal or public health is identified, the European Commission may suspend import or set special conditions for import. Given the highly infectious nature of the microorganisms mentioned above, it is justifiable to question, if the time interval between detection and implementation of such measures would not be far too long to prevent major infectious disease outbreaks in production animals and/or man.

Yet, the afore-mentioned pieces of legislation suggest that, in general, all is well in place and functioning properly.

3.2. The Food and Veterinary Office

The European Commission (EC) has an organisation called the Food and Veterinary Office (FVO), which conducts audits in EU member states to evaluate the extent to which they comply with the EU directives and regulations, and which makes inspection visits to third countries from where goods and/or animals are imported into the EU. The FVO adopts the responsibility of the EC for ensuring that community legislation on food safety, animal health, plant health and animal welfare is properly implemented and enforced. The mission of the FVO is to ‘improve the national control systems and the effective enforcement of requirements in the EU and third countries, all to ensure that consumers can be confident about food safety, that trade can take place under high safety levels, and that exporters can harness the advantages of a single EU market’. Such audits conducted by FVO include inspection visits focusing on illegal imports of food POAO and animals by travellers. On the website of the FVO (FVO 2013) one can observe that over the past decade FVO has conducted more than 200 inspection visits on border control and about 1500 inspection visits to third countries. In 2011, 185 audits were done concerning food safety (i.e. about 68% of the total number of visits), 22 on animal health (also including aquatic species), 19 on animal welfare (e.g. slaughter houses, transport) and 32 on other issues. The FVO reports are in the public domain and yield a lot of information about the functioning of border inspection points (BIPs), the control system in place, the staff competencies and the failures made. Between member states there are large differences in the proper functioning of controls. The following paragraphs summarise the major findings of FVO during some of their control visits in different member states.

3.2.1. The Netherlands

An FVO inspection visit to the Netherlands in 2004 for checking whether Dutch import control and risk communication conformed to EU rules (DG SANCO 2005), revealed that: (1) posters, if any, at airports had not been updated; (2) airport officials were not particularly cooperative in communicating risks to passengers; (3) customs were not always present at BIPs; (4) sniffer dogs were not available, and finally, (5) checks on luggage were routinely at a level of 5% and only increased up to 10% of the baggage in case of suspect flights.

Finally, as 40 kg of illegal imports were detected at non-BIPs per year, there is always the possibility that a portion of this 40 kg is contaminated. Unfortunately, these observations only partly reflect real life deficiencies. The 2011 inspection visit of FVO to the Netherlands showed that significant improvements had been achieved in terms of a well-developed control system, an effective verification system and effective internal audits to solve problems, proper training, knowledge and skills of staff and a significant progress in the use of TRACES (trade control and expert system). All deficiencies reported from the previous (2009) inspection visit had been corrected. Weak points that remained were identified as follows: the notification in advance of consignments of animals or POAO to be checked (all documents for all shipments were checked), and the (too) small sample size of containers to be checked in ports (10% of containers) increasing the risk of non-compliance. There was no information on illegal imports by travellers (DG SANCO 2011a).

3.2.2. United Kingdom (UK)

The FVO 2011 visit report regarding the UK pointed out that it has, overall, an effective control system on imports and transits in compliance with EU legislation. Moreover, their verification system was considered effective, as were staff training, review of procedures and instructions. However, the internal audit system was considered weak. Although the deficiencies detected during the earlier 2009 FVO visit had been addressed, there were still weak points, such as airline manifests and internal audits being inaccessible. At the BIPs, the level of non-compliance had remained at the same level due to a lack of proportionate and dissuasive sanctions. Selective risk-based checks are made on illegal consignments on the basis of risk analysis (animal disease risk assessment; other threat intelligence; country risk information). However, FVO stated that these checks would not necessarily detect the illegal imports of POAO. Problems apparently exist especially in airports like Heathrow and Gatwick, where sampling procedures are too selective and not representative. Hence, physical veterinary checks imply that non-compliance is not always detectable due to this too small sample size (DG SANCO 2012).

3.2.3. France

The report of FVO's visit to France in 2011 mentioned a good working control system, a properly operating network of authorities, good staff competencies and concluded that since the 2010 FVO visit significant improvements had been made. However, checks on imported pet animals did not necessarily lead to isolation of the animals, especially not when they were transported in baskets or on a leash; non-compliant animals could move freely due to imprecise instructions. Passenger information included posters, a website, leaflets and iPhone applications. Customs, however, did not state that passengers must present animals for checking. At one port entry point it was observed that passengers only presented their animal upon specific request from the customs authorities. Apparently, many travellers are not aware or do not want to live up to their obligations. For POAO, customs at international airports like Paris-Roissy-Charles de Gaulle use X-ray. Sniffer dogs were not available. The veterinary checks were much less variable than was noted in 2010. Customs information for travellers existed in the form of posters, website, leaflets and the iPhone. In 2011 there was a bush meat action to make the general public more aware of the potential problems associated with this product. Airport and port checks are done on the basis of personal risk analysis (origin of travellers; behaviour of travellers; type of luggage) and on selected flights or ships. The target for sampling luggage and travellers in 2009 was set at 3%; in 2010, 2.5% of POAO consignments were checked (1182 samples out of 47.175). Small parcels potentially containing POAO were not checked in post offices because it was assumed that small parcels would not contain POAO. The problem of non-notification before arrival in France was observed (DG SANCO 2010b, 2011b).

3.2.4. Portugal

In 2010, an FVO inspection visit was made to Portugal. During that visit many deficiencies were detected: not all consignments were submitted to a veterinary check; major personnel problems; digital networking and communication problems; incorrect procedures; no evaluation audits conducted; poor cooperation between authorities. Earlier detected shortcomings had not been taken care of. There was a major problem with passenger transport operators who neglected to alert passengers about prohibitions and limits regarding POAO in the luggage. It was unclear how requirements for personal consignments were applied and checked. Post offices were not included in the BIP network. Marinas fell completely out of the control scope. At the main airport, 10–15% of luggage was checked; in risk flights up to 50% was checked. Luggage scanning was done at a 10% level. In 2007, 207 POAO were seized (655 kg meat and 198 kg milk products); in 2008, 637 POAO were seized (1603 kg meat and 525 kg milk products); there were no statistics on origin or frequency. Customs seem to put high priority on CITES animals (Convention on International Trade in Endangered Species), drugs and weapons, and far less on POAO and animals transported by travellers. Regarding the check of pet animals, it could very well be that non-compliant pets were released from the entry point before health requirements were met. Passenger information (e.g. posters, leaflets, etc.) was not available (DG SANCO 2010a).

3.2.5. Australia and New Zealand

Australia and New Zealand, although not fully comparable to the EU situation, spend more money on control and prevention than the EU – possibly because their agro-products account for a larger proportion of their economy and export trade than in European countries – but also because they are determined to keep pathogens, hazardous for humans, food animals and crops, out of their country. In comparison, the USA still pertains to sticking to strict customs controls at their borders, while the interstate movements of goods and people in the USA are rather free, as is also the case within the EU.

4. Border inspection

4.1. Biosecurity

Biosecurity in this context covers all government management measures to identify potential public health and animal health hazards, their associated risks, as well as the risk management measures to prevent the introduction into and/or spread of infectious diseases within a certain country or continent. Biosecurity planning and execution is centred around four phases of Risk Analysis as shown in Table 2 (OIE 2004; CAC 2011). The list of hazards associated with imports into a country changes constantly, because in different countries there may be outbreaks of a classical disease or new (emerging) diseases may occur. Should this be the case, a (qualitative or quantitative) risk assessment or (quantitative) mathematical or epidemiological risk modelling based on available data has to be conducted to establish the most important risk factors and to determine priorities in biosecurity.

Table 2. The four phases in biosecurity planning and execution (adapted after CAC 2011).

Phases in biosecurity planning & execution		Key wording of a phase
1	Hazard identification	Hazards in the area of public health and animal health
2	Risk identification	Risk factors associated with each hazard identified
3	Risk management	Risk management measures to eliminate or reduce hazards
4	Risk communication	Preparing documents, TV-radio material, teaching material and all other material to inform and educate the general public and all stakeholders

EU commissioner Mrs Vassiliou (2008), elaborating on the EU biosecurity measures, stated the following: ‘The goal is to reduce the amount of illegal food or animals brought into the EU by travellers arriving from countries outside the EU, or sent through the post, and more widely to increase public interest in EU animal health and food safety matters. A series of actions will be organised in airports, ports and road-entry points in cooperation with the Directorate-General for Taxation and Customs Union of the European Commission, and the veterinary and customs authorities in the member states, with the aim of informing the public about the rules governing the introduction of personal consignments of products of animal origin and pets’.

The biosecurity measures addressed by Mrs Vassiliou appear to be correct on the surface. However, apparently, they are neither sufficient for properly protecting the food animal production sectors in Europe, nor for safeguarding public health. Illegal importation of animals or foods of animal origin still occur – sometimes to a large extent. This is particularly relevant as animal and/or human disease outbreaks occurring worldwide (see Table 3) represent a serious threat for the EU. Although the precise sources of these outbreaks are usually unknown (see Section 6 below) it is often assumed they could indeed be related to insufficient biosecurity measures during border control. Hence, it is relevant to consider two questions. Question 1: what is exactly done and how at those entry points and with what results? Question 2: to what extent are EU travellers indeed aware of potential hazards and these bio-security measures, and do they act accordingly?

Table 3. Major examples of recent disease outbreaks in various countries.

Years	Disease	Countries involved
1999–2012	West Nile virus disease	USA
2012	Foot and mouth disease	Bulgaria
2012	Schmallenberg virus	Various countries in Western Europe
2012	Brucellosis	Belgium/France
2012	Newcastle disease	Italy
2012	Anthrax	Germany
2012	African Swine Fever	Russia
2012	Hanta virus disease	USA
2012	African horse sickness	Russia
2012	Human Swine Influenza HPAI H7N3	USA
2013	Human Avian Influenza H7N9	China
2013	Human Avian Influenza H5N1	Vietnam, Bangladesh, South Africa

4.2. Border inspection points (BIPs) and customs

Customs demands concerning the control of introduction and spread of infectious diseases for humans and animals do not differ significantly between countries or unions, such as the USA, Australia and the EU (Table 4). For food imports in general, these are usually based on the guidelines of the FAO (2003a) and for animal imports on those of OIE (OIE 2012). The EU is comparable to the USA given their member states and states structure.

Table 4. Customs embargos on the import of animals or food of animal origin from third countries for the control of introduction and spread of infectious diseases of animals and/or humans (UKBA 2012; NAO 2005; CBP 2013).

Luggage not allowed in the USA and the European Union Note: Prior notice for food importation is required if food is sent by the shop where the traveller had bought it originally
Biologicals (animal tissue, bacterial culture, fungi, birds, etc.)
Prepared food products (e.g. bush meat). Note: bakery products are allowed
Fish and wildlife & their products (eggs, bones, feather, etc.)
Fruits and vegetables unless under strict conditions
Meat (fresh, dried, canned and food products containing meat), livestock and poultry
Pet dogs and cats (USDA–APHIS check needed); pet birds (avian influenza H5N1)
Plants, seeds and soil (unless a specific permit is obtained for import)
All dairy products (cheese, milk, dried milk included)

As confirmed by FVO visit records (see above), X-ray equipment is not used at all BIPs and sniffer dogs are not always available. In some cases, there are surrender bins, e.g. in airports, where passengers can dump the forbidden goods. In some BIPs, due to lack of personnel, the checks are conducted to a variable degree. Highly visible posters or video screens should indicate what is accepted and what is not, but these are not always present. If caught, a person may encounter a fine and in severe cases even imprisonment may follow. Most deficiencies identified by the FVO are related to problems in the area of infrastructure, administration, and technical and operational management. In addition, there may be economic constraints and human errors or negligence leading to failures. It should further be emphasised again that ‘entry points’ into the EU other than BIPs (e.g. smaller railway stations, tourist marinas and small airstrips) also represent a risk of introduction of infected/contaminated livestock or contaminated foods of animal origin. This risk is realistic, because the rather strict control measures stipulated for BIPs are generally not implemented.

5. Risk assessment studies

From a UK risk assessment study it has been reported that there is a continuous, albeit low, risk of livestock becoming infected as a result of illegal imports of POAO. This means that – when hazard magnitudes are indeed considerable, while the exposure may be low – the impact (the ultimate risk) can still be substantial. It was also established that passenger baggage is the most likely route by which illegal products enter the country (NAO 2005). Around 12,000 tons of illegal meat and meat products may enter the UK each year; a small portion of this is likely to be contaminated. Furthermore, bush meat from Africa is entering Europe in large quantities, e.g. 273,000 kg per year at Paris-Roissy-Charles de Gaulle airport, France. From here it is most often transported to the USA. At least a portion of this quantity might be contaminated.

The economic impact of the introduction of these items into the food chain could, on the other hand, be dramatic if it results in a major disease outbreak. The foot-and-mouth disease outbreak in the UK in 2001 (probably as a result of swill feeding), for example, cost the UK economy at least £8 billion (Jarvis 2001; personal communication). Similarly, a foot-and-mouth disease outbreak in California has been estimated to cost US$7 billion, provided it is detected within one week. If detected after two weeks, this figure amounts to twice as much (Jarvis 2001; personal communication). Many animals will have to be killed.

6. Why many biosecurity measures fail

Often, the general public does not understand what goes on in farming, what potential public health hazards prevail and how they should be dealt with in a proper manner. This gap in knowledge between civilians and the farming community is growing bigger and bigger over time (Noordhuizen et al. 2008). The perception of the consumer is based on information provided by the public media (which, unfortunately, is not always scientifically correct) and it is questionable if such information is fully understood. The latter is especially relevant, because perception is composed of a large proportion of emotion and non-rational behaviour. Therefore, authorities cannot expect that travellers would be fully aware of the hazards related to animal contacts or carrying foods of animal origin in their luggage. A Ministry of Agriculture, creating an Internet site communicating the risks of introducing food POAO into a country or of having been in contact with potentially infected animals, largely overestimates the efficacy and reach of this information. Asking people to change behaviour without providing them with a meaningful causal explanation of transmission of zoonoses is unlikely to be effective (Parveen et al. 2012).

7. Prevalence of zoonotic agents in illegally imported animals and foods of animal origin

The increased import of (exotic) foods in general – even when relying on regular import channels – bears the risk of transmission of zoonoses and an increased number of disease outbreaks may ensue. For example, the US Centers for Disease Control observed that, with increasing volumes of imported foods the number of disease outbreaks over the period 2005–2010 increased markedly (Gould et al. 2012).

The scientific and accurate attribution of food borne illnesses to specific foods (‘source attribution’) requires developing a comprehensive programme, combining various methods and can only be achieved through increased resources and optimal cooperation between food safety institutions (for details see: EFSA 2008). Such a systematic approach is currently hardly – if at all – implemented at the European level. Hence, not surprisingly, outbreak investigation data on cases attributable to illegally imported animals or foods of animal origin are scarce and fragmented and not readily retrievable, neither from the records of the European Centre for Disease Prevention and Control (ECDC, Dr Celine Gossner, personal communication), nor from those of the European Food Safety Authority (EFSA, Dr Pia Makela, personal communication). Hence, on the EU level, it cannot be reliably assessed how significant the contribution of illegally imported animals or foods to the total number of known disease outbreaks is. Yet, a limited number of well-documented cases exist that illustrate the relevance of the issue.

For instance, there was the recent case (Netherlands rabies case … 2012) of the illegal import into the Netherlands of an eight-week-old puppy from Morocco (note: a health certificate from a local Moroccan veterinarian had been issued, but the animal had not been vaccinated against rabies, as such is only applied from three weeks of age) . The puppy was transported by car to Spain where a health passport was obtained, before flying the animal to Amsterdam where it passed the customs without a health check and without the documentation being scrutinised, which should have led to an ordering of the appropriate quarantine procedures. When a Dutch practitioner was consulted as the animal fell ill shortly after arrival, authorities were alarmed and the animal was diagnosed with rabies, as a result of which 48 contact persons had to be treated.

A well-documented ‘case-control’ study of a human Salmonella typhimurium outbreak in which poultry meat illegally imported by travellers was incriminated has been described by Kapperud et al. (1998). Another, more recent report is that of a human trichinellosis outbreak in Bavaria caused by the consumption of illegally imported pork products manufactured from a pig slaughtered at a farm in Rumania (at that time not an EU member state). The cured paprika sausage confiscated at the patients’ household had a larval density (as assessed by artificial digestion) as high as 441 larvae/g (Nöckler et al. 2007). A similar case of a trichinellosis outbreak was reported from Austria in 2010, in which meat products illegally imported by immigrant workers from Bosnia-Herzegovina were confirmed as the causal factor (Lechner et al. 2012). The latter reports indicate that travellers’ unawareness of the risks associated with illegal food imports combined with failing border controls can easily lead to food-borne outbreaks. Unfortunately, until very recently, no attempts have been made to collect baseline data on the actual prevalence of zoonotic agents in foods of animal origin carried by travellers. In 2012, an EU-financed research project ‘PROMISE’ (Promise 2012) was started, its main objectives being the assessment of risks involved when foodborne pathogens are introduced by uncontrolled imports. Preliminary results of one of the project partners (Institute of Milk Hygiene, University of Veterinary Medicine, Vienna, Austria) have recently become available. With special permission of the Austrian health authorities, the luggage of randomly selected passengers of 200 flights from non-EU countries arriving at the Vienna International Airport was checked over a period of eight months (August through March 2012). When foods of animal origin (including canned products and honey) were detected, these were confiscated and subsequently microbiologically analysed for the prevalence of a range of food pathogens, including Salmonella spp., Campylobacter spp., verotoxigenic E. coli, coagulase + Staphylococcus aureus and Listeria spp. Although most presumptive isolates still have to be confirmed and subtyped in the final analyses, the preliminary results show that (disregarding canned products and honey) salmonellae prevailed in 11 samples (2.1%) and Listeria (confirmed as L. monocytogenes) in 13 samples (2.4%) (mainly meat and meat products, to a lesser extent milk and dairy products) (Prof Dr Martin Wagner, personal communication). Similar observations on the illegal import of bush meat from Africa or traditional Mexican cheeses have been reported from the USA (Bell et al. 2012; Sandoval et al. 2012) and the authors suggest that longstanding cultural practices and a lack of knowledge on what is and what is not legal make it difficult for travellers to acknowledge the associated risks.

These findings illustrate the potential public health risks associated with illegal imports of (generally ill-packaged and unrefrigerated) food items. In addition, and most relevant, such imports bear the risk that ‘exotic’ strains of traditional pathogens are introduced in the EU. The same is valid for the livestock sector.

8. Suggested improvements

Farming in the EU is, in general, still an economically highly important sector despite the fact that the number of farmers has dropped (only seven member states together produced 8.5 million tons of poultry meat in 2004 according to Eurostat 2004 data [Windhorst 2006]). The EU regions with the highest density of food animal populations are found in western Germany, southern Netherlands, eastern Belgium, Brittany in France and northern Italy (see Figures 84–86 in Smulders 2007). These regions are subject to a significant risk of epidemics, once pathogens have entered and farms have been affected. Other food animal production areas in the EU are more scattered but run a comparable risk, although the level of potential exposure per unit of time may be less. It would seem essential, therefore, to consider the border control strategies currently in place and identify areas for improvement.

We propose that authorities should always check all passengers and all luggage from international flights coming from countries outside the EU, where high-risk animal diseases and/or zoonoses have been detected or are suspected (see for further information: FAO 2013). The FAO receives daily and weekly reports on zoonotic diseases from all over the world. This information can be checked locally in order to update videos, posters, flyers and leaflet hand-outs, and alter passenger controls. Such an approach would conform to ‘risk oriented and precautionary border control’. To this end, all passengers should have to fill out a form with questions, not only regarding the country of first departure but also regarding all intermediate countries where a stop-over was made. Such a form can also be used in court cases of forgery.

Rather than merely rely on the provision of videos, posters, flyers, websites or Smartphone applications and expecting travellers to check those before entering the EU, a more proactive approach lays a substantial part of the responsibility with the traveller, in that the travel documents (including the filled out questionnaires) could lead to fines imposed in case of illegal imports and forgery. Air flight and port operators equally bear a part of the responsibility and liability as they should routinely provide, together with the flight tickets or E-tickets, each passenger with the most recent information regarding the (illegal) transport of animals and/or POAO. The same is valid for tour operators, who should provide such information to travellers at the booking of their journey.

Consequently, we suggest the following, specific measures at entry points to be (re-) considered by the EU authorities as soon as possible:

1. Introduction of mandatory customs questionnaire forms in which travellers must answer: (1) questions about contact with animals (food animals; pets; zoo) in all countries visited during the last 72 hrs before re-entering the EU as well as (2) questions about vegetables/fruits and food products of animal origin they are carrying;

2. Intensified luggage control and body search of individuals who answered one or more of the questions named under point 1 with a ‘yes’;

3. Passengers, arriving from countries where the animal disease profile is a ‘risky’ one, should all undergo a mandatory search of their luggage and, when justifiable, a body search for animals and food products of animal origin should be undertaken.

4. Linking the OIE and FAO animal disease reporting system to customs in the EU with TRACES and reassuring that each BIP will rapidly update the information they present to the general public.

5. Reformulation of a set of fines and prison sentences for those specific cases, where a person has been found to illegally import animals or food of animal origin from outside the EU, and to communicate this information to all travellers at entry points (leaflets; posters; large video screens; verbal messages). Such video-screens with updated information should be present in departure halls and at the gates of international flights from outside the EU.

6. Re-design and execute disease risk communication programmes throughout the EU at entry points like airports, ports, road entries, and also at non-BIP entry points. Such programmes are composed of brochures with up-to-date information, posters (e.g. Figure 1), short videos (all of these available on-site), airplane hand-outs, TV spots, airport/boat/train leaflets, large information screens, etc. Tour operators, airline agents and Internet-selling sites should provide information in a direct way to their clients: at booking and at the check-in.

   Figure 1. Example of a ‘not to be missed’ warning billboard. Upon arrival in one of the international airports of Australia, one is confronted with, among others, this billboard. The text indicates the products that are forbidden from being imported. The traveller can dispose of such products in special bins located under the billboard (photograph courtesy H. Surborg).

   

A final point of concern is the frequency and intensity of luggage control. One should bear in mind, that an estimated risk-based sample size of 5% of passengers or their luggage on a jumbo jet with 400 passengers comprises only 20 persons. Hence, the practice of routinely checking 5% of the luggage (observed during the EU inspection in the Netherlands in 2004, see above) is a purely cosmetic and non-rational activity. The probability that 380 passengers carry food products of animal origin is much higher than could possibly be assessed on the basis of a sample size of 20 (Frankena et al. 1990; Noordhuizen et al. 2001; see Figure 2). Moreover, the long distance flight crews are not frequently or not at all interviewed or checked for being a carrier of potential pathogens or food animal products.

Figure 2. A note on sampling procedures (after Noordhuizen et al. 2001).

Finally, non-BIP entry points should be checked from time to time to show that authorities are serious about the potential threats of introducing infections hazardous for man and livestock.

9. Discussion and conclusions

In the wake of having – in some parts of the world – largely eradicated some classical zoonotic diseases in production animals the farming world is now confronted with animal disease outbreaks caused by new emerging pathogens (e.g. Bluetongue in 2006–2007, the Schmallenberg virus in 2011, human swine influenza (HPAI) virus in the USA and Q Fever in Hungary both in 2012 and Human Avian Influenza H7N5 in China in 2013). The possible consequences of such outbreaks may be dramatic. The HPAI H7N3 virus is expected to occur more frequently (FLI 2010), and the Schmallenberg virus epidemic is expected to return in the UK in sheep with expected losses of 30% of the flock (Tarlinton 2012). These diseases represent a constant (sometimes increasing) threat to animal and possibly public health in the EU.

Even though not all these agents have a zoonotic potential for humans, it has been convincingly demonstrated that (1) the farmer can greatly reduce the potential public risks (both those at the farm and those associated with contamination of POAO originating from their livestock in general) by strictly adhering to Good Farming Practices, including on-farm biosecurity measures and risk management (FAO 2003b; FAO & IDF 2004; Buncic et al. 2009; Noordhuizen et al. 2008, 2012) and (2) the food processing industry can achieve such by implementing measures of Good Manufacturing and Good Hygiene Practices (Buncic et al. 2009). This remains the principal approach to the assurance of safety of foods of animal origin and is practised by responsible farmers and entrepreneurs. Unfortunately, not all geographical regions have such a track record and hence the influx of zoonotic agents from endemic areas through global trade and travel needs to be reckoned with.

It is unrealistic to expect an all-encompassing and fail-safe biosecurity system at all points of entry to the EU and primarily aimed at identifying travellers, knowingly or unknowingly introducing biological hazards, to be easily achieved. As argued earlier, there are many complicating factors and the (limited number of) case reports and source attribution data currently available suggest that increased global trade and travel activities will presumably remain a major cause of outbreaks of animal and human disease (Vågsholm and Smulders 2012), probably regardless of the measures taken: zero-risk does not exist in this context.

In August 2012, the Canadian federal food inspection agency launched a new set of biosecurity measures in the beef sector, aimed at further minimising the spread of endemic and foreign diseases (FAO 2012; Global Meat News 2012). It would appear that the Canadian authorities are more proactive than their European colleagues. Possibly based on considerations of minimising the costs that would be incurred [one of the so-called ‘legitimate factors’ to be considered in risk management (Smulders 2012)] the EU appears to have fewer reservations in accepting a high risk.

Unfortunately, a systematic, evidence-based risk assessment that would allow making cost-effective risk management decisions, is not yet available, and will not be available so long as the results of targeted baseline studies have not been published. Meanwhile, merely relying on economic or other mathematical simulation models would seem far from prudent, as these are rather non-specific for this purpose. Instead, we believe that adhering to basic preventive measures, as those discussed in earlier sections of this article, should be the starting point, after which other, more specific measures can be considered. It is rather likely that the latter risk management strategies would, at least to some extent, compromise the free movement principle. At the same time, travellers will understand why and learn to accept that such measures are taken, provided they are properly and proactively informed, as they have accepted the currently intensified personal control at customs. The fact that at one FVO inspection visit it was reported that customs put a higher priority on the control of drugs, weapons and CITES, rather than on POAO and live animals, emphasises the weaknesses of the current policy.

Obviously, effective control activities require considerable investments, both in terms of personnel and equipment, and in the absence of a thorough evidence-based analysis of the cost-effectiveness of certain measures it is difficult to convince risk managers at the EU level to adapt strategies. This having been said, one must nevertheless confront the fact that the current EU risk management and communication strategies for protecting livestock sectors and public health are suboptimal to say the least, and that much can be improved, relying on relatively simple and straightforward measures along the lines suggested in this article.