Holtkamp DJ, Polson DD, Torremorell M, et al. Terminology for classifying swine herds by porcine reproductive and respiratory syndrome virus status. J Swine Health Prod. 2011;19(1):44–56

Cite as: Holtkamp DJ, Polson DD, Torremorell M, et al. Terminology for classifying swine herds by porcine reproductive and respiratory syndrome virus status. J Swine Health Prod. 2011;19(1):44–56.
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Keywords: swine, porcine reproductive and respiratory syndrome virus, herd classification, definitions, disease status
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Received: March 19, 2010
Accepted: September 17, 2010

Veterinarians and researchers spend much time thinking about and communicating about porcine reproductive and respiratory syndrome (PRRS) virus (PRRSV). However, the swine industry has yet to specify any standardized and clearly defined nomenclature for describing the PRRSV status of herds. Standardized terminology related to PRRSV and the PRRSV status of herds is necessary to facilitate communications between veterinarians, swine producers, genetic companies, and other industry participants. Likewise, a standardized system for herd classification based upon a set of related definitions is required for implementation of regional and national efforts towards PRRSV control, elimination, or both.

The purpose of this paper is to provide a herd classification system for describing the PRRSV status of herds based upon a set of definitions that reflect the biology and ecology of PRRSV as it is understood today.

This system was developed by a definitions committee formed jointly by the American Association of Swine Veterinarians (AASV) and the United States Department of Agriculture (USDA) PRRS-Coordinated Agricultural Project (PRRS-CAP) and was approved by the AASV Board of Directors on March 9, 2010. The committee included veterinarians from private practice and industry, researchers, and representatives from AASV and the National Pork Board.

Classification of herds

For breeding herds, with or without growing pigs on the same premises (herd and premises defined in Table 1), there are four categories: Positive Unstable (Category I), Positive Stable (Category II), Provisional Negative (Category III), and Negative (Category IV) (Figure 1 and Table 2). Category II is further divided into two subcategories: Positive Stable (II-A) and Positive Stable Undergoing Elimination (II-B). Premises with only growing pigs are categorized simply as Positive or Negative (Tables 3 and 4).

Herd classification for PRRSV is based on determining both shedding and exposure status of the herd (Figure 1). Testing methods to determine shedding include direct detection of the virus by polymerase chain reaction (PCR) or virus isolation. Polymerase chain reaction is the preferred testing method. Exposure is determined by antibody testing: enzyme-linked immunosorbent assay (ELISA), immunofluorescent antibody (IFA), or immunoperoxidase monolayer assay (IPMA). ELISA is the preferred testing method. Classification is determined by monitoring the PRRSV status of specific subpopulations in a herd. For the purpose of classifying herds, the relevant subpopulations are adult breeding animals, weaning-age pigs, breeding replacement animals, and growing pigs (post weaning). Testing is based upon representative sampling of the population.

PRRS virus shedding status is classified as negative, uncertain, or positive. A negative shedding status means that the available evidence supports the absence of viral shedding in the herd. A positive shedding status is supported by diagnostic and clinical evidence of viral shedding and transmission in the herd. A positive shedding status is also assumed for all herds and situations when information on the actual herd status is lacking. On the other hand, an uncertain shedding status is used when diagnostic data in tested herds is available to suggest a negative shedding status, but without sufficient confidence to support a negative shedding status, usually because of lack of power in the sampling and testing strategy. An uncertain shedding status is considered transitory in the progress towards eliminating PRRSV from an infected herd.

Exposure status is classified as negative or positive. A negative exposure status means there is evidence to support the absence of prior exposure to the PRRSV in the population, assessed by the absence of antibodies to the virus in the samples tested.

Classification of breeding herds

Positive Unstable (Category I) breeding herds have positive shedding and exposure statuses. It is also the default category when herd shedding and exposure statuses have not been confirmed and when herds have not been tested. Herds going through a clinical PRRS outbreak and those with chronically recurring shedding of virus will fall into Category I.

Positive Stable (Category II) breeding herds have an uncertain shedding status and positive exposure status. Absence of clinical signs of PRRS in the breeding-herd population and confirmation of a sustained lack of detectable viremia in sampled weaning-age pigs (and growing pigs if present) for a minimum of 90 days is required. This classification requires a minimum of four consecutive negative PCR herd tests in weaning-age pigs sampled every 30 days or more frequently. “Weaning age” is defined as 7 days before and 3 days after weaning, regardless of the age of the pigs (Table 1). The exposure status of the breeding herd remains positive. The possibility that animals may still be infected and later shed the virus cannot be ruled out. A distinction is made between Category II breeding herds that are not undergoing PRRSV elimination (Category II-A) and those that are (Category II-B) (Table 2). A breeding herd is undergoing elimination if it has initiated an elimination procedure, as defined in Table 1. An elimination procedure begins when the last seropositive breeding replacements are introduced or when the last intentional exposure to any live PRRSV, wild-type or any vaccine (live or killed or both), occurs in the herd, whichever is later.

Confidence that the weaning-age pigs and growing pigs moving from Category II breeding herds are not shedding PRRSV increases over time if the breeding herd is undergoing PRRSV elimination, since steps are being taken to eliminate viral shedding in the herd undergoing elimination. These steps will include closure of the herd to introductions of breeding replacements and may also include restrictions on cross-fostering and initiation of whole-herd exposure to live virus or vaccination. All herds that are undergoing PRRSV elimination by herd rollover will meet the criteria to be classified as Category II-B at some point during the elimination process. Category II-A is the goal for herds that are trying to control, rather than eliminate, the virus.

Category II is meaningful for managing PRRSV both in a production setting and in regional or national elimination programs. In the context of managing PRRSV in a production setting, the absence of viremia is significant for management of pig flow and expectations about improved reproductive and growing-pig performance. In the context of a regional or national elimination program, the distinction between Positive Unstable and Positive Stable breeding herds and those undergoing elimination versus those that are not may have value for deciding where and when to move pigs.

Provisional Negative (Category III) breeding herds have a negative shedding status. For a herd to be classified as Category III, sustained introduction of negative breeding replacements (“negative breeding replacement” defined in Table 1) without their seroconversion to the PRRSV is required. Lack of seroconversion in introduced animals is considered sufficient evidence to confirm that PRRSV is no longer being transmitted in the herd. The negative breeding replacements must have been in contact with previously positive animals and remain seronegative by ELISA for a minimum of 60 days after entry into the breeding herd (Table 5). Some adult breeding animals in the herd may still have antibodies to the PRRSV due to prior infections. If growing pigs are present at the same premises, confirmation of a negative exposure status in that subpopulation is also required. The recommended diagnostic protocol to confirm that the negative breeding replacements are negative for antibodies and negative for viremia prior to entry into the breeding herd is presented in Table 6. Category III herds include those intentionally pursuing elimination via herd rollover by entering negative breeding replacements.

Negative (Category IV) breeding herds have a negative shedding and exposure status. Confirmation of the negative exposure status of Category IV breeding herds varies depending on how the herd is established negative. For herds established negative by herd rollover, diagnostic information is required to confirm the negative exposure status of adult breeding animals, but information from production records may also be used in conjunction with diagnostic information to confirm negative status. The recommended protocol is presented in Table 7. Production records may be used to identify the breeding animals on the inventory list just before the first negative breeding replacements are introduced: this is the population of animals that must have been removed. When the current inventory contains no adult breeding animals that were on that list, the herd has been completely “rolled over” once and may be classified as Category IV. Alternatively, a negative exposure status may be confirmed with a negative herd test based upon sampling adult breeding animals to confirm that they are seronegative (Table 8) after a minimum of 1 year from the start of Category III status. Individual animal records are not required for the alternative criterion. If growing pigs are present at the same premises, confirmation of a negative exposure status in that subpopulation is also required.

Category IV also encompasses new premises startups populated with negative breeding replacements or premises that were completely depopulated and repopulated with negative breeding replacements that have remained seronegative. For these herds, a negative ELISA herd test in adult breeding animals is required at least 30 days after the premises are populated to define the negative exposure status of the herd (Table 9).

Classification of growing-pig herds

Premises with growing pigs only are classified as either positive or negative (Table 10). Positive herds have a positive shedding status or a positive exposure status or both. It is also the default category when diagnostic information is inadequate to classify a herd as negative. Negative herds have a negative shedding status and a negative exposure status (Table 11).

Supporting material to define shedding and exposure status

The criteria for defining negative or uncertain shedding status or negative exposure status are based upon observable, objective, and quantifiable measures. The objective evidence includes diagnostic results and information from production records, both of which should be routinely collected. Absence of clinical signs consistent with PRRS can also be used to support the herd-status classification, but clinical signs alone are not sufficient.

Diagnostic evidence is based upon periodic herd tests. The definition for herd tests (Table 1) is adapted from the definition proposed by Christensen and Gardner.1 When possible, pooling of samples to increase sample size, frequency of testing, or both, and targeted sampling of subpopulations to improve herd-level sensitivity, are recommended. For the purpose of establishing positive versus negative herd status using currently available ELISAs, and until a differential diagnostic assay and related differentiable vaccine becomes available, no clear distinction is possible between diagnostic results that are positive due to live or killed vaccine usage versus those that are positive due to wild-type virus exposure; thus, no distinction is made.

Shedding status can be measured by direct detection of the virus by PCR and virus isolation. Polymerase chain reaction is the most commonly used agent-based detection technique, and therefore recommendations in this document are based on PCR testing, although other agent-detection methods could also be appropriate. The PCR test on serum detects viral genetic material and is relied upon to define shedding status. A negative result indicates the absence of viremia, but negative PCR results do not necessarily rule out the possibility that the animal is infected2 or shedding.3 However, monitoring serum from weaning-age pigs by PCR can be used as an indirect measure to monitor vertical transmission as well as horizontal sow-to-piglet and piglet-to-piglet transmission in breeding herds.4 Negative PCR tests on weaning-age pigs alone are not sufficient to establish a negative shedding status for a breeding herd. The ideal method for detecting shedding and transmission of virus in the breeding herd involves use of sentinel animals.

Prior exposure to the PRRSV is indicated by the presence of antibodies to the virus and is measured by tests such as ELISA, IFA, and IPMA. Commercial ELISA tests are the preferred methods to detect antibodies, and this document focuses on their use. Antibody levels are detectable in serum within 14 days5 after infection and may wane over time to a level that is no longer detectable in individual animals. A positive ELISA test indicates previous exposure. Because serological tests are rarely 100% specific, some false-positives are to be expected. To rule out false-positives, serial testing using another antibody-based test of greater specificity, such as the IFA, can be used.6,7 ELISA testing of serum is used to define exposure status as well as to confirm the seronegative status of negative breeding replacements. This is necessary for them to serve as sentinels to confirm the negative shedding status in Category III breeding herds.

For all herd tests that involve sampling, the sample size should be based on the target prevalence and desired confidence in detecting a positive.8 Confirmation of a negative or uncertain shedding status and negative exposure status of a previously positive herd will typically be sought when a herd is transitioning from positive to negative and the expected prevalence of positive animals is low. Furthermore, individual test sensitivity is potentially lowest in the transition from positive to negative when the concentrations of analytes (ie, PRRSV antibodies or viral RNA) are likely lowest in the course of infection. Therefore, a conservative sampling approach should be used to define the shedding and exposure status of a herd.9

Testing strategies should be modified as new methodologies are developed. For example the use of oral fluids offers great potential to test populations and should be considered in the future.10 New technologies in antibody and antigen detection should also be evaluated as they are developed.

Discussion

An accepted set of terms and herd classifications is required to facilitate regional and national efforts to eliminate PRRSV. Furthermore, the availability of standardized nomenclature should facilitate communications among researchers, veterinarians, producers, genetic companies, and other industry participants. Standardized nomenclature will facilitate better contractual and business arrangements, especially those between genetic and commercial production companies and agreements between producers that offer premiums for weaned pigs from breeding-herd sources with a specific PRRSV status. Researchers writing proposals and papers and making presentations may save time otherwise spent defining terms related to PRRSV, and standardized definitions will facilitate comparison of field-based research results by making clearer the conditions under which research trials are conducted.

Among the committee, definition of the Positive Stable category (II) was a contentious issue. The value of including this category, accounting for differences between herds pursuing elimination versus those pursuing control, the criteria for defining the status, and the meaning of the category were all fiercely debated. The literature does not support the proposal that negative PCR tests on weaning-age pigs constitutes sufficient evidence that a breeding herd is not infected with PRRSV. Without the benefit of monitoring a population of sentinel animals, it is not possible to establish the shedding status of breeding herds with sufficient certainty. However, anecdotal evidence from the field supports the notion that herds classified as Positive Stable (II) have better reproductive and growing-pig performance than herds that are Positive Unstable (I). Being Positive Stable (II) is the goal for breeding herds that are trying to control the virus. In the context of area or national elimination efforts, subdivision of category II into II-A and II-B is important to convey the likely differences in the risk of current or future shedding of virus by animals in these herds.

The standard herd classification scheme for the PRRSV status of herds and related definitions proposed here are consistent with the biology and ecology of PRRSV as it is understood currently. As new information becomes available, these definitions may need to be reviewed.

Acknowledgements

The authors wish to acknowledge Drs Jim McKean and Butch Baker for their insightful comments and suggestions. Their contributions substantially influenced the final classification scheme. This work was supported by the AASV and the PRRS-CAP USDA NIFA Award 2008-55620-19132.

References

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