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