As globalization increases the interconnectedness between nations, economies, and industries, the introduction of diseases will continue to remain a prominent threat to the livestock sector and the trade of animals and animal products, as well as the livelihoods of farmers, food security and public health. The global pig sector, with its size and dichotomy between production type and biosecurity level, is particularly vulnerable to the transmission of transboundary animal diseases such as African and classical swine fever, foot and mouth disease, or porcine reproductive and respiratory syndrome. All of the above pose a constant threat to swine health, mainly as a result of both formal and informal international trade. Inspired in the risk assessment methodology, this paper classifies and provides an overview of the different pig disease introduction and exposure pathways, illustrated with abundant examples. Introduction pathways are classified as formal international trade (by product), informal international trade (by product), and spread through fomites. Formal trade of pigs and pork products is regulated by legislation and measures protecting animal populations from exotic diseases. Much more difficult to control is the transboundary swine disease transmission originating through informal trade, which entails illegal smuggling, but also the informal cross-border transfer of animals and products for personal use or within informal market chains. Meat products are most commonly mentioned, although fomites have also played a role in some cases, with live pigs, being more difficult to smuggle playing a role less frequently. The main exposure pathways are also described with the oral route playing a prominent role. Risk assessments can aid in the identification of pathways of pathogen introduction and exposure. However, quantitative information on informal disease introduction pathways remains very scarce and often incomplete, making it difficult to estimate the actual magnitudes of risks. Nevertheless, this knowledge is deemed essential to set up risk based awareness, prevention and surveillance programs that correspond to reality.

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Transboundary spread of pig diseases: the role of international trade and travel.

African swine fever causes substantial economic losses in the swine industry in affected countries. Traditionally confined to Africa with only occasional incursions into other regions, ASF began spreading into Caucasian countries and Eastern Europe in 2007, followed by Western Europe and Asia in 2018. Such a dramatic change in the global epidemiology of ASF has resulted in concerns that the disease may continue to spread into disease-free regions such as the US. In this study, we estimated the risk of introduction of ASF virus into the US through smuggling of pork in air passenger luggage. Results suggest that the mean risk of ASFV introduction into the US via this route has increased by 183.33% from the risk estimated before the disease had spread into Western Europe or Asia. Most of the risk (67.68%) was associated with flights originating from China and Hong Kong, followed by the Russian Federation (26.92%). Five US airports accounted for >90% of the risk. Results here will help to inform decisions related to the design of ASF virus surveillance strategies in the US.

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Risk of African swine fever virus introduction into the United States through smuggling of pork in air passenger luggage.

Globalisation, international trade and the ever-growing flow of goods and people enable animal diseases and zoonotic pathogens to travel worldwide. The risk of reintroducing previously eradicated animal diseases into the European Union is omnipresent as considerable amounts of food products of animal origin (POAO) from endemic countries are continuously imported legally and illegally into the EU. Additionally, these products may be potential vectors for emerging foodborne zoonoses, which are of public health concern due to their significant morbidity and mortality rates. This review summarises the legal background of veterinary public health measures and provides a critical overview on recent epidemiological studies, which analysed 1577 illegally imported POAO for major foodborne zoonotic pathogens and antimicrobial resistance in indicator bacteria. The samples rarely exceeded microbiological contamination levels of domestic products for Salmonella, Verotoxin-producing Escherichia coli and thermophilic Campylobacter spp. However, Listeria monocytogenes and Staphylococcus aureus were the most frequently detected pathogens in illegally imported meat and meat products (5% and 4.3%, respectively) and S. aureus in milk and milk products (7.4%). The most likely source of those zoonotic pathogens in illegally imported POAO are cross contamination and improper hygiene measures while handling, processing and storage. Moreover, uncommon and genetically distant variants including antimicrobial resistant foodborne pathogens such as methicillin-resistant S. aureus or extended-spectrum β-lactamase-producing Enterobacteriaceae were discovered. The introduction of POAO poses a largely underestimated threat, both to animal and public health.

Foodborne diseases do not respect borders: Zoonotic pathogens and antimicrobial resistant bacteria in food products of animal origin illegally imported into the European Union.

African swine fever (ASF), classical swine fever (CSF) and foot-and-mouth disease (FMD) are considered to be three of the most detrimental animal diseases and are currently foreign to the U.S. Emerging and re-emerging pathogens can have tremendous impacts in terms of livestock morbidity and mortality events, production losses, forced trade restrictions, and costs associated with treatment and control. The United States is the world's top producer of beef for domestic and export use and the world's third-largest producer and consumer of pork and pork products; it has also recently been either the world's largest or second largest exporter of pork and pork products. Understanding the routes of introduction into the United States and the potential economic impact of each pathogen are crucial to (a) allocate resources to prevent routes of introduction that are believed to be more probable, (b) evaluate cost and efficacy of control methods and (c) ensure that protections are enacted to minimize impact to the most vulnerable industries. With two scoping literature reviews, pulled from global data, this study assesses the risk posed by each disease in the event of a viral introduction into the United States and illustrates what is known about the economic costs and losses associated with an outbreak.

Risks of introduction and economic consequences associated with African swine fever, classical swine fever and foot-and-mouth disease: A review of the literature

On average 8,000 pork derived products are annually confiscated by Customs and Border Protection at the United States (US) ports of entry such as international airports, harbours or mail offices. These swine products with unknown sanitary status could pose a risk for foreign animal diseases introduction into the US. This study aimed at analysing the risk of African swine fever virus (ASFV) and classical swine fever virus (CSFV) being introduced into the US through prohibited swine products carried by air passengers (PSPAP) and identifying locations and time periods at higher risk where and when preventive and mitigation measures should be implemented. Our results estimated that the risk for CSFV entry was seven times higher and further spread between US airports than for ASFV. Specifically, the overall mean annual probability of ASFV entry was estimated as 0.061 at 95% confidence interval (CI) [0.007, 0.216] while the probability of CSFV entry was estimated as 0.414 (95% CI [0.074, 1]). For both diseases, July and May were the months at highest risk for entry. For ASFV, the origin countries of those PSPAP that represented the highest risk (above 70% of the total risk) were Ghana, Cape Verde, Ethiopia and the Russian Federation, while for CSFV above 90% of the risk at origin was concentrated in the Dominican Republic and Cuba, followed by India, Colombia, Peru, Ecuador and China. These results could be used to implement and feed real time surveillance systems, which could potentially help customs to increase the detection rate of smuggled products, indicating when and where to look for them. Similarly, these systems could be adapted and implemented to other diseases improving the cost-effectiveness of the resources invested in preventing entrance of diseases via air passengers' luggage.

Could African swine fever and classical swine fever viruses enter into the United States via swine products carried in air passengers’ luggage?

Protection against biological material entering a country or region through airports is important because, through them, infectious agents can quickly reach exotic destinations and be disseminated. Illegal products of animal origin may contain hazardous infectious agents that can compromise animal and public health. The aim of this study was to identify associations between possession of illegal animal products in baggage and demographic characteristics of the passengers, as well as characteristics of their travel plans in the two main Brazilian international airports. A total of 457 passengers were divided into two groups: passengers identified as carrying illegal animal products and control. Passengers identified as carrying illegal animal products not stated on the accompanied baggage declaration completed a questionnaire, to aid in profiling. Nationality, origin, age and residency of passengers were analyzed using chi square, logistic regression and odds ratios. Passengers from Eastern Europe were the most likely to enter with animal products as were those aged between 35 and 55 years. When evaluating the departure point, the highest frequency was seen in those coming from Portugal. Passenger group, reasons for travel, amount and type of baggage were available only for passengers identified as carrying illegal animal products, noting that they prefer traveling alone, for leisure, bringing few bags. Such information can contribute to the early identification of passengers that have illegal animal products in baggage at Brazilian airports.

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Christina Isoldi Seabra

Papers

Profile of international air passengers intercepted with illegal animal products in baggage at Guarulhos and Galeão airports in Brazil