Discussion
Swine slaughtered in a large central abattoir in Hong Kong were sourced from farms in multiple provinces of China. We utilized paired virological and serological surveillance data, together with data on farm of origin and date of sampling to assess the transmission risk in the swine transport and marketing system in China. Our results showed that pigs experienced a higher FOI (229%-414%) during transport per-unit time, compared to that within the farms. This suggested that the industrial scale swine production, transportation and marketing of live pigs provide settings favorable to influenza transmission, though the much longer stay in farms allow more infections over swine’s lifetime. The phylogenetic tree topology of the concatenated genomes also provided clear molecular epidemiological evidence of cross-transmission along the transport chain, between swine originating from different parts of mainland China. Interestingly, the isolation of similar though not identical viruses from the same farm over a two-year period suggested that swine influenza virus lineages may be maintained within a single source farm for over a year. We did not have detailed farm management data to ascertain herd sizes or management practices, in particular whether these large farms are ever completely emptied of pigs, which was unlikely. The likelihood that sequential batches of swine of different age groups are raised on the same farm increases the possibility of a virus to maintain itself within farms with large herd sizes.
We found that pigs were more likely to be infected with H3 virus during transportation, if originating farms had a high seroprevalence over 30%. The high farm-level seroprevalence implied a high circulation of H3 SIV in farms. Hence, some pigs from the herd were more likely to be infectious at the beginning of the transport chain and more likely to transmit to others along the route (e.g. inspection or holding at the transfer house and holding within the abattoir). However, the infection risk during transportation for pigs with HAI titer of ≥1:40 reduced substantially by 67%, which is compatible with the protective effect of humoral immune response for humans (Hobson, 1972).
Distance of transportation was not found to be associated with the risk of transmission. We observed a lower transmission risk for swine from farms further away from Hong Kong, though the difference was not statistically significant (Table 2). There could be other economic factors which may affect biosecurity measures during transport for these farms. The extent of mixing with other swine during inspection, waiting or holding at the transfer house, quarantine station and abattoir may pose greater transmission risks than that during transportation, with only about 40 pigs in a truck. Hence, the relative contribution of transmission risk during transportation may be less, even with a long trip from source farms to abattoir, than that associated with the mixing taking place at the quarantine stations and other common transport hubs. The isolation rate did not increase significantly for pigs staying longer times in the abattoir in Hong Kong which may imply that transmission within the abattoir was not a major driver of cross-infection. This is possibly related to the short time pigs were held in the abattoir prior to slaughter which may not provide adequate time for transmission and incubation period for there to be detectable virus at slaughter. The emergence of African swine fever in China since 2018 has led to a further shortening of the period of pigs being held in the abattoir in Hong Kong prior to slaughter, likely further reducing risk of cross-infection within the abattoir. The increased FOI during transportation may be facilitated by the high-density and high-stress environment at the transfer houses at the Shenzhen-Hong Kong border. Limiting the number of pigs and time of travel may reduce cross-infection.
There were several limitations in our study. First, the actual duration and distance of transportation duration and distance for the live pigs were not available. We used province as a proxy for duration of transport. We could not rule out impacts arising from other activities related to swine trading. Secondly, while pigs from farms not previously infected with H3N2 virus got infected during the transport to the abattoir, we did not have unequivocal evidence that new viruses were introduced back to farms, although this could occur through contaminated trucks. Third, our estimates focused on H3-subtype SIV only, giving us a smaller sample size. The serological cross-reactivity between multiple co-circulating H1 viruses make such an analysis difficult to interpret with H1 swine viruses. Finally, our study deduced the infection history of individual pigs based on surveillance in the slaughterhouse only. The actual prevalence of infectious virus in individual farms or transfer house were not available, which prevented us from estimating the transmission risk at different points of transportation.
In conclusion, we used paired serological and virologic samples collected from a swine slaughterhouse to examine the infection history of the swine from farms and during transportation. We found that transport and holding settings provided a favorable environment for swine-to-swine cross transmission per unit time when compared with farms. However, the longer period of time a pig spends on the farm means that the cumulative risk of acquiring infection in the farm is higher. The risk posed by the transport process was co-infection with new viruses which may provide opportunities for virus reassortment providing some risk to those involved in the transportation and slaughtering processes. There may also be the possibility of viruses being introduced back to naïve source farms via fomites and trucks, although this study was not able to investigate this possibility. Further assessment of the relative contribution of influenza transmission at different processes during transportation is needed to identify high risk area for improving disease control.
Acknowledgments: We acknowledge research funding from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, under Contract No. 75N93021C00016, HHSN266200700005C and HHSN272201400006C and the Theme Based Research grant (T11-712/19-N) from the Research Grants Council of Hong Kong SAR and the Health Medical Research Fund (Ref no: HKS-15-E02) from the Food and Health Bureau of Hong Kong SAR.
Conflicts of interest: The authors declare no conflicts of interest.
Data availability statement: All data from this study have been disclosed.
Orchid: Malik Peiris ID https://orcid.org/0000-0001-8217-5995