To address the lack of information regarding IAV transmission in pigs with maternal immunity, an experimental transmission study was conducted to estimate the reproduction ratio (R) of IAV in pigs with varying levels of maternal immunity. In the experimental model, IAV was transmitted to all sentinel pigs that were seronegative to the challenge virus and sentinel pigs with heterologous maternal immunity, and the R values did not differ significantly between these groups. In contrast, transmission was a low probability event in the presence of homologous maternal immunity. While pigs were infected in all groups, clinical signs were mild in all infected pigs throughout the study (results not shown).
The reproduction ratio estimates obtained from the experimental model provide useful insights regarding IAV transmission in populations. As expected, all sentinel pigs became infected in the CTRL group with a basic reproduction ratio (Ro
) estimate of 10.4 (6.6–15.8). This is very similar to a previously determined Ro
of 10.7 in an older population of seronegative sentinel pigs [20
]. The stochastic models for the CTRL group demonstrate that major IAV outbreaks are likely to occur in small naïve populations following the introduction of an infected pig.
Similar to what was observed in the CTRL group, all sentinel pigs with heterologous maternal immunity were infected with IAV and the estimated value of R was 7.1 (4.2–11.3). While the transmission parameter (β) was numerically lower in the PASSV-HET group, the estimates were not statistically different between the CTRL and PASSV-HET groups. In contrast, the infectious period was slightly shorter in the PASSV-HET group compared to the CTRL group although the biological significance of this slightly shorter infectious period may be minimal. The resultant stochastic PASSV-HET group model showed this numerical difference with a slightly lower proportion of simulations with all pigs becoming infected and a slightly higher proportion of simulations with no new cases compared to the CTRL group. In contrast, the reproduction ratio estimate was significantly lower in the PASSV-HOM group at 0.8 (0.1–3.7) compared to the PASSV-HET and CTRL groups. Based on stochastic modeling, 57% of simulations resulted in no new cases in the PASSV-HOM group.
This study confirmed that IAV infection and transmission can take place in the presence of maternal immunity. The PASSV-HET group reinforced previous reports of IAV infection in the presence of maternal immunity and showed that the R estimate was similar to that of the CTRL group. This study also showed that infection was prevented in most pigs and transmission reduced in the presence of homologous maternal immunity. In addition, stochastic modeling showed that over half of the time an infected pig is introduced in the PASSV-HOM population described in our experimental setting, transmission was prevented. Optimization of passive or maternally derived immunity through sow vaccination is a widely practiced control measure for influenza transmission. The results from this experiment involving pigs in the PASSV-HOM group appear to justify that practice. The PASSV-HOM group demonstrates, in a “best case scenario,” that when pigs are challenged with IAV when maternal antibody titers to the challenge virus are high and with the same virus as contained in the sow vaccine preparation, then indeed transmission is decreased. Although transmission was decreased in the PASSV-HOM group one pig with a pre-contact homologous HI titer of 1:320 was infected, but secondary transmission from this pig was not observed.
While this study shows IAV transmission may be reduced given the specific settings of this study, field conditions may alter this impact. Pigs with homologous maternal immunity in this study had high and uniform titers, whereas pigs in a field setting may have more variable levels of maternally derived immunity as the concentration at weaning age depends on many factors including the initial IgG level in the colostrum, quantity of colostrum ingested, and gut closure timing [28
]. In addition, the main purpose of the PASSV-HET group in this study was to create a population of pigs with high levels of maternally derived immunity with limited cross-reactivity to the challenge virus. This situation may occur in field settings, but the level of cross-reactivity will differ. The terms homologous and heterologous were used in this study to describe immunity in neonatal pigs based on the vaccines and challenge strain used, but there is likely great variation within these descriptions in field settings. In this study, 4 mL of vaccine was administered as a booster dose 2–3 weeks pre-farrow to sows in the PASSV-HOM group (), while 2 mL was administered to sows in the PASSV-HET group. In addition to the factors mentioned above, this difference may have impacted the results observed in this study. However, the ultimate measure of interest regarding immunity in this study was HI antibody titer to the challenge virus (IA/04). In this study, a 4 mL vaccine dose was needed as a booster in order to achieve desirable HI titers in the PASSV-HOM group. The resultant HI titers in neonatal pigs to the challenge virus () need to be taken in account when interpreting results of this study. Animal housing types and the initial number of IAV infected pigs will also differ between farms, which could alter contact patterns between infected and susceptible pigs.
The level of specific passive antibody at the time of exposure has been regarded as an indicator of immune protection to IAV in young pigs [10
]. This study provides further evidence regarding this point in a transmission experiment. The majority of pigs that suckled colostrum from sows vaccinated with a homologous killed vaccine and then challenged via direct contact with an experimentally infected pig were completely protected. One pig did become infected even with a high HI titer to the challenge virus. However, the reproduction ratio was lower compared to pigs with high levels of heterologous maternal immunity and pigs seronegative to the challenge virus. These results suggest that while homologous immunity may not completely prevent transmission, it is still beneficial to decrease transmission and prevent disease.