Foot and mouth disease (FMD) is a highly contagious viral disease that often manifests as vesicular lesions and erosions in the mouth and on the feet and teats of affected cloven-hoofed livestock species (1, 2). In addition to the adverse animal health and wellbeing impacts, international trade restrictions are also placed on countries where the disease is present. While the United States (U. S.) is currently free from FMD, the threat of re-introduction has necessitated the development of an array of preparedness and response resources intended to bolster response capabilities in the event of an incursion (3). If FMD were to enter the U. S., efforts to contain and eradicate the disease would likely involve animal movement controls and the required implementation of biosecurity plans (4–7).

Robust disease control efforts will be necessary to eradicate the disease; however, some degree of business continuity for the U. S. livestock industries and their associated marketing avenues must be protected to ensure the survival of the affected industries. In the U. S. auction markets are a primary marketing avenue for many classes of beef cattle, cull dairy cattle, and sheep (8–10), and are utilized to a lesser extent for marketing goats and swine (11, 12). Ideally during an outbreak, auction markets could implement practices to mitigate risk and be allowed to continue operating in a manner that does not amplify disease spread, which will in turn support maintenance of business continuity for several U. S. livestock industries. However, a current lack of biosecurity and risk mitigation guidance for auction markets increases the likelihood that they could serve as a source of a super spreader event through the congregation and dispersal of livestock. This risk makes regulatory officials reluctant to allow their continued operation during a disease outbreak (13).

Biosecurity guidance for foreign animal disease threats has been developed for other sectors of the U. S. livestock industry, including Secure Food Supply (SFS) plans for several livestock species and biosecurity guidance for packing plants (14, 15). The SFS plans recommend enhanced biosecurity practices for premises that maintain groups of livestock in order to keep the herds or flocks from becoming infected; whereas, the biosecurity guidance for packing plants focuses on structural and operational biosecurity measures for the packing plant facility. While some of the principles of existing SFS plans and packing plant guidance are applicable to auction markets, the unique nature of U. S. auction market operations and their business model requires a substantially different approach to biosecurity. Auction markets do not maintain a population of animals, but import new animals from numerous premises for each sale day, sort and recombine them into sale lots, and disperse them to multiple new premises. This uniquely positions auction markets where equal consideration for decreasing disease transmission risk needs to be placed on both the regularly imported animals and the potential for persistence of virus in the physical facility. Biosecurity and risk mitigation strategies specific to the business model of U. S. auction markets are needed to allow them to move livestock through their facilities in a manner that poses a low risk for the importation of infected animals, production of new infections, and the facility becoming contaminated. Allowing ongoing auction market activity without proper risk assessment and disease control efforts could substantially extend an outbreak and result in more harm to the affected livestock industries. However, evaluating the effectiveness of biosecurity and mitigation strategies of foreign animal diseases like FMD in field settings is challenging. Few opportunities exist to evaluate biosecurity or mitigation strategies in auction market settings that operate similarly to U. S. auction markets either in FMD-endemic areas or during FMD outbreaks. Still, reports from the scientific literature may provide information that can be used to inform the development of biosecurity and business continuity strategies for U. S. auction markets in the event of an FMD outbreak. Therefore, the objective of this scoping review is to identify peer-reviewed literature that describes biosecurity strategies which decrease the risk of FMD introduction into auction markets or mitigation strategies that prevent FMD transmission from auction markets. To accomplish this objective, the following questions were developed to guide the review.

This scoping review was conducted in accordance with the Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR) (16). The objective and review questions were developed a priori by group discussion. A protocol for this review was not registered.

During an FMD outbreak, the ideal situation for an auction market would be to never introduce infected animals into their facility while simultaneously preventing environmental contamination of the market site through all possible routes. Unfortunately, no reports describing FMD biosecurity risks to or strategies for auction markets were identified for inclusion in this review, leaving a gap in available resources to inform preparedness planning and the development of response strategies. The critical need for such resources is illustrated by the five reports included in this review which demonstrate the association between livestock movement through auction markets and FMD introduction risk to herds (18–22). These reports implicate both direct and indirect transmission as well as local spread as pathways which present a risk of FMD herd introduction. The Mansley et al. and Thursfield et al. outbreak investigations illustrate the potential for auction markets to contribute to widespread dissemination of FMD in the absence of biosecurity strategies, inspection requirements, or movement controls, further underscoring their necessity during an outbreak (21, 22). During these outbreak investigations, FMD was disseminated primarily through the movement of infected sheep (21, 22). While sheep do not shed FMD virus quantities as high as other livestock species, particularly swine, they also may not display clinical signs as noticeably as other livestock species (1, 2). The species of livestock infected during an outbreak will affect transmission dynamics of the outbreak, and will likely necessitate tailoring auction market biosecurity and mitigation strategies. For instance, livestock species, like sheep, that shed lower amounts of FMD virus may contribute to less environmental contamination of auction market sites due to less viral shedding; however, since they have less noticeable clinical signs, detection and subsequent outbreak response actions may be delayed. Whereas species that shed higher amounts of the virus and have more obvious clinical signs may contribute to more environmental contamination of premises and local spread via viral aerosolization, but overall time to detection of an outbreak may also be quicker, leading to a more timely response. Additionally, in the U. S., auction markets are utilized as the primary marketing channel for a far smaller volume of swine and sheep compared to other livestock species such as cattle, which will also impact outbreak transmission dynamics (8–12). Regardless of the species infected, practices to prevent entry and rapidly detect clinical animals are necessary. The findings of Wiratsudakul et al. provide further evidence supporting the impact of disease dissemination through markets on the magnitude of outbreaks by demonstrating the reduction in modeled outbreak size from closing highly connected markets (25). This finding was less notable for lowly connected markets, suggesting the need for individual rather than blanket interventions in an outbreak. Bronsvoort et al., ElAshmawy et al., and Lindholm et al. demonstrated the increased risk of FMD herd introduction through the direct movement of livestock purchased from auction markets (18–20). The extensive commingling of animals at auction markets and their subsequent dispersal presents a significant biosecurity risk to both the animals at the market as well as their destination farms. This aspect of the auction markets’ business model highlights the need for effective biosecurity protocols to decrease opportunities for disease transmission and subsequent dissemination.

Surveillance strategies which increase the likelihood of disease detection may also mitigate herd FMD introduction risk from direct movements of livestock purchased from auction markets, such as comprehensive inspections prior to or at the market to detect infected herds as modeled by Hernández-Jover et al. (24). However, these strategies may vary in effectiveness depending on the species infected and virus serotype (26). Moreover, if infected animals are detected at an auction market facility, that facility is likely to face significant challenges regarding best strategies for handling, holding, and potentially disposing of those infected animals. Currently available data identified in this review do not provide specific recommendations for auction markets to implement.

If an auction market facility were to become contaminated either directly by the movement of infected livestock or indirectly through human or vehicle traffic, Colenutt et al. provided evidence of that facility’s ability to serve as a source of viral exposure in both the report included in this review as well as in an additional recently published report (23, 27). However, since both studies were conducted in endemic areas, we cannot distinguish between repeated viral introduction into the auction market and persistence of FMD in the environment between market days. Mielke and Garabed report that FMD virus is capable of surviving in contaminated water sources for 11 to 30 days and in soil for 2 to greater than 30 days (28). Since these reported survival times can exceed the typical interval between sale days for U. S. auction markets, persistent viral load in the market environment is plausible and cleaning and disinfection steps would be necessary to reduce viral exposure and the potential for disease dissemination from auction markets during an outbreak. While cleaning and disinfection guidance is provided by the National Animal Health Emergency Management System (NAHEMS), these processes would be challenging and potentially infeasible for auction markets to repeat regularly (29). Additionally, Mielke and Garabed report a viral survival range of 1–5.5 days for aerosolized FMD virus with the potential for re-suspension of deposited virus particles due to environmental disturbances such as livestock or vehicular movement (28). This capability of the virus poses a risk to newly introduced animals and would necessitate further cleaning and disinfection procedures.

While not all susceptible livestock exposed to a contaminated market site become infected or propagate an outbreak, as illustrated by the Mansley et al. and Thursfield et al. outbreak investigations, the potential viral exposure of the animals, personnel, or other fomites and their subsequent movements do necessitate movement traces during an outbreak (21, 22). In the event of an FMD outbreak in the U. S., the volume of these types of movements originating from a contaminated market site has the potential to obligate personnel resources to a large number of tracing activities, thereby rendering them unavailable for other response activities and placing a strain on all response resources. If available, the implementation of effective biosecurity measures at auction markets could help to mitigate this sort of wastefulness and optimize resource utilization during an outbreak.

Reports included in this scoping review were limited to those published in English which may have eliminated some relevant reports from locations where FMD is endemic. Additionally, only reports from peer-reviewed sources were considered for inclusion in the review, which could have resulted in the exclusion of information relevant to the review questions. However, as there are few countries in which FMD is endemic that also have auction market settings similar to the U. S., the reviewers estimate these limitations to have minimal impact on the results of the review.

In order to reduce the risk of propagating FMD outbreaks due to livestock movement through auction markets while still maintaining some level of business continuity for the auction market sector of U. S. livestock industries, targeted guidance on implementing practical and feasible biosecurity practices and risk mitigation strategies specific to auction market facilities should be developed. Any proposed biosecurity strategies will need to consider and account for the unique business model of U. S. auction markets which result in a high volume of non-terminal livestock movements on a weekly basis. Addressing this current preparedness gap would substantially bolster the U. S. livestock industry’s resiliency in the event of an FMD incursion. Given the clear evidence of widespread dissemination of FMD through auction markets and the limited availability of biosecurity guidance for auction markets, robust implementation of procedures at the farm of origin to prevent movement of infected animals onto the auction market premises along with intensive active observational surveillance at the market is necessary. Farm of origin best practice recommendations for enhanced biosecurity and active observational surveillance are available to U. S producers in the Secure Beef Supply Plan (30).