Abstract
The mechanisms of transmission of influenza A virus (IAV) and porcine reproductive and respiratory syndrome virus (PRRSV) in pigs during the pre-weaning period are not fully elucidated. Since viable IAV and PRRSV can be found on the udder skin of lactating sows and the use of nurse sows is a common management practice, we developed a novel nurse sow model to evaluate the transmission of IAV and PRRSV from lactating sows to their adopted piglets. In two studies, we infected pigs with either IAV or PRRSV who then contaminated the udder skin of lactating dams with their nasal and oral secretions while suckling. Once the skin was confirmed virus positive for IAV and PRRSV, the sows were moved to separate empty clean rooms to adopt IAV and PRRSV negative suckling piglets. After adoption, 1 out of eight (12.5%) piglets tested IAV positive 1-day post-adoption (dpa) and the entire litter (8 out of 8) became positive by 4 dpa. In the case of PRRSV, 3 out of 11 (27.3%) pigs tested rRT-PCR positive 2 dpa and there were 7 out of 11 (63.6%) pigs positive at the termination of the study at 7 dpa. This study documented the transmission of IAV and PRRSV between litters of piglets by nurse sows and highlights the importance of the nurse sow-piglet as a unit that contributes to the maintenance of endemic infections in breeding herds. The use of nurse sows in pig farms, though beneficial for minimizing pre-weaning mortality and maximizing farm productivity, is seemingly detrimental as this practice may facilitate the transmission of IAV and PRRSV to piglets prior to weaning.

Introduction
Influenza A virus (IAV) and porcine reproductive and respiratory syndrome virus (PRRSV) are two of the most important viruses affecting pigs. IAV causes respiratory disease characterized by high morbidity and low mortality with clinical signs of coughing, fever, and sneezing that result in decreased production performance [1]. PRRSV causes reproductive failure leading to abortions, premature farrowings, stillbirths and mummified fetuses, and respiratory disease with interstitial pneumonia in pigs [2]. PRRSV and IAV are commonly found co-circulating in swine herds and together can cause economic losses of up to $10 USD per pig [3].

In recent years, there have been significant efforts to control and eliminate PRRSV from swine breeding herds [4]. Control of IAV has also become a priority as novel viruses of human, avian and swine-origin have become widespread and endemic in U.S. swine herds [5]. The IAV and PRRSV control programs have the common goal of weaning piglets that are virus-free. Piglets prior to weaning are known to be a reservoir for PRRSV and IAV in endemically infected herds [6, 7]. Piglets are born IAV-free but commonly become infected during the suckling period prior to weaning [8]. IAV transmission in pigs occurs mainly by direct contact with virus-laden secretions and exposure to infectious aerosols, although other indirect routes of transmission also exist [8, 9]. In the case of PRRSV, pigs may be born viremic due to in utero infections, or transmission may occur due to contact with infected pigs [10], contaminated materials [11] or aerosols [12]. However, not all sources or the importance of the various transmission routes of IAV or PRRSV infection have been elucidated for piglets prior to weaning, particularly in endemically infected herds and herds undergoing virus control and elimination efforts with enhanced biosecurity practices. Indeed, having PRRSV positive piglets prior to weaning is one of the main challenges for herds attempting to achieve PRRSV-stability, i.e. no detectable PRRSV viremia for 90 days [7]. In addition, there is significant variability in the time it takes for a herd to reach stability and variations in management practices are suspected to contribute to those differences [13]. However, the management practices and on-farm procedures that contribute to or reduce PRRSV infections have not been fully elucidated.

To minimize pre-weaning mortality, it is not uncommon in animals to transfer progeny between dams in order to improve the progeny survivability. The dam that adopts the new progeny is often referred to as a nurse dam. The reasons for transferring the progenies vary and may include the dam’s lack of milking ability, too many animals nursing from a single dam, progenies losing body condition as a result of within litter competition or disease, or farm management protocols that limit the number of animals nursing from a single dam. Similarly, the mixing of animals between litters which is referred to as cross-fostering [14] is also a common practice in the US swine farms for some of the same reasons.

One of the most common practices during the lactation period is to identify a sow with good mothering ability and milk production, wean her biological piglets off of her and have this lactating sow adopt other piglets. We have identified the use of nurse sows as a potential management practice that may facilitate the transmission of IAV and PRRSV between lactating sows and adopted suckling piglets. The use of nurse sows is a standard farm management practice in U.S., in particular in farms with high productivity where approximately 10% of lactating sows will become nurse sows (Allerson, personal communication). Nurse sows are used to adopt piglets at risk of emaciation or mortality. Allowing these piglets to become adopted by and suckle a nurse sow is a way to improve pig livability and maximize pig weight gain through increased milk consumption. The nurse sow may be moved to a room housing the younger pigs or may stay in the same room and younger piglets be brought to her which may depend on the farm management protocols or farm lay-out design. Also, in pigs the practice of cross-fostering (i.e. moving pigs between litters) is common and has been associated with disease transmission between suckling piglets [15].

Our group identified and recently reported the presence of viable IAV and PRRSV on the udder skin of lactating sows [16]. Seventy-eight percent (31 out of 40) of samples collected from the surface of the udder skin of lactating sows from four IAV positive and endemic Midwestern US breeding herds yielded viable IAV [16] indicating that the skin may serve as a source of virus and facilitate IAV transmission between pigs. In humans, IAVs have been detected and isolated from the skin of infected people and direct contact with contaminated hands has been implicated in IAV transmission [17]. Thus, we hypothesize that nurse sows can transmit PRRSV and IAV between litters and effectively perpetuate these infections in piglets prior to weaning. In this study, we evaluated a nurse sow model to test this hypothesis and also evaluated the transmission of these viruses by cross-fostering.