Porcine reproductive and respiratory syndrome virus infection in the boar: a review

Abstract

Porcine reproductive and respiratory syndrome (PRRS) is caused by PRRS virus, which, like other members of the Arterividae family, has the ability to infect macrophages and to persist in tissues for at least several months after the acute stage of infection subsides. As a consequence, PRRS has a complex epidemiologic profile and has been especially difficult to control under the usual conditions of commercial swine production. Although vaccines are commonly used, vaccination is only one of several approaches to be considered in designing a control strategy. At least equally important are procedures developed on the basis of a thorough understanding of the epidemiology of the disease. The objective of this review is to summarize current knowledge in relation to PRRS virus (PRRSV) infection in the boar. The information available related to this topic will be summarized and discussed, and the implications for the control of the condition highlighted. The main emphasis will be on questions about the pathogenesis of infection, including duration of viremia and the origin of PRRSV found in semen; the clinical signs associated with the disease, paying special attention to the effects on seminal quality; the epidemiology of the condition, with special emphasis on the duration of PRRSV shedding in semen and the implications that this may have on venereal transmission, as well as the role that other potential routes of shedding may have on the dissemination of PRRSV.

Introduction

Porcine reproductive and respiratory syndrome (PRRS) is one of the most economically devastating diseases affecting swine industry worldwide. The causative virus (PRRS virus, PRRSV) was first isolated in 1990 in The Netherlands [1] and shortly after in the USA [2]. Primarily, on the basis of similar morphology, genomic organization, replication and transcription strategy, and protein composition, PRRSV is classified, with equine arteritis virus (EAV), lactate-dehydrogenase elevating virus (LDV) and simian hemorrhagic fever virus (SHFV), in the family Arteriviridae [3]. Members of this family also share the ability to replicate in macrophages and induce persistent infections in their natural host.

Although, in general, PRRS is clinically similar in North America and Europe, the respective strains differ in virulence [4], and in antigenic [5], [6] and genetic [7] properties. These differences have led to the classification of strains into two subgroups: subgroup A, comprising most North American strains; and subgroup B, comprising most European strains [7].

The role of PRRSV in reproductive failure in the sow has been firmly established. Experimental infections have mirrored the clinical signs observed in natural outbreaks, including abortions, premature farrowings, mummified pigs, stillborn pigs, and elevated preweaning mortality [8], [9], [10], [11], [12]. Infection has also been associated with reduced conception rates, elevations in the percentage of regular, as well as irregular returns to estrus and sporadic early abortions [13]. Transplacental infection commonly follows exposure of gilts and sows during gestation [11], [14], [15], [16], especially when initial exposure is late in gestation [11]. As a consequence, maternal infection can give rise to the birth of congenitally infected pigs and to an elevated number of mummified fetuses, the latter as a result of a high mortality rate among infected fetuses [8], [9], [11], [14], [15], [16], [17], [18].

In the boar, clinical manifestations include anorexia, lethargy, and loss of libido [19], [20], and, on some occasions, alterations in semen quality, including a decrease in sperm motility, an increase in morphoanomalies and cytoplasmic droplets, and a decrease in the percentage of spermatozoa with a normal acrosome. These alterations have been described in both natural and experimental infections [19], [21], [22]. However, the consequences of infection in relation to semen are still controversial since some researchers have found that the quality of semen remains within normal limits after infection with PRRSV [23], [24].

The rapid spread and economic impact of PRRS have made it a frequent topic of research, especially in regard to its control. As with many other infectious diseases, the most effective means for control often depends on the use of vaccines as well as the implementation of improved management practices. Regarding the first option, there are currently several commercially available vaccines. These include live-modified-virus as well as inactivated-virus vaccines. However, the nature of the pig’s immune response to PRRSV makes the development of an unquestionably safe as well as highly effective vaccine a formidable challenge. Consequently, in many affected herds, the development of strategies for control and perhaps eventual eradication of PRRS depends on a thorough knowledge of the epidemiology of the disease.

We know today that one of the main characteristics of PRRSV is its high transmissibility, which almost certainly contributed markedly to its quick spread around the world. Pigs are susceptible to infection by a number of routes, including oral, intranasal, intramuscular, intraperitoneal, and vaginal. They can also shed the virus in a number of ways, including saliva [25], nasal secretions [26], urine [26], feces [27], mammary gland secretions [28], and semen [24], [29], [30]. Moreover, the interval of shedding can also be extensive [25], [29].

An important epidemiological feature of PRRSV, as well as other members of the Arteriviridae family, is their ability to induce persistent infections [31]. Notably, PRRSV has been isolated from experimentally infected pigs up to Day 157 post-infection (p.i.) [32]. However, the duration of persistence seems to vary among pigs and it is likely that the age of the pig at the time of its initial contact with PRRSV is also a factor; namely, experimentally induced infections of young pigs have persisted longer than those of adult pigs [11], [18], [33]. Despite the apparent age differences, numerous studies have indicated that many pigs, regardless of age, are infected for weeks, if not months, and that during most or all of that time, they are a potential source of infection for others.

The importance of persistent infection and contact transmission in the epidemiology of PRRS is emphasized by the fact that, despite extensive replication of PRRSV in the respiratory tract, it is not readily disseminated by aerosols [34], [35], [36], [37]. Additionally, although mechanical vectors of PRRSV transmission include contaminated needles [38], fomites, and unwashed hands of staff [39], mosquitoes [40], and houseflies [41], the significance of these vectors under field conditions, i.e. in commercial pigs farms, is still to be determined. Consequently, in most cases, transmission of PRRSV seems to be by direct contact among pigs – and persistent infection greatly extends the interval of potential transmission.

For the most effective control and possible eradication of PRRS, it is necessary to provide answers to a series of questions related to both persistence and dissemination of the virus within the adult swine population. These are especially important issues in regard to boars for which there is a need to evaluate not only the risk associated with their entrance into a stud or onto a farm, but also the epidemiological risk that transmission of PRRSV via artificial insemination poses for other farms. The objective of this review is to summarize the knowledge available today regarding PRRSV infection in the boar, trying to answer the main questions that the infection creates, especially those related to the epidemiological risk posed by the persistence and dissemination of the virus by different routes.