Identifying Key Transmission Route of Avian Influenza A(H9N2) in Live Poultry Markets
Authors: Lau Eric , Zhang Shengqiu , Leung Connie , Cowling Benjamin J. , Wu Joseph T. , Peiris Malik 
Published: May 2017

ObjectiveThis study assessed the transmission of low pathogenic avianinfluenza in live poultry market setting, using paired fecal anddrinking water samples from a longitudinal surveillance program.The relative contribution of transmission via direct fecal-oral routeversus drinking water will be determined.IntroductionLive poultry markets (LPMs) continue to operate in many Asiancountries. Low pathogenic avian influenza (LPAI) viruses areoften endemic in the poultry, and LPM presents the opportunity forhuman-poultry interactions and potential human infections with avianinfluenza viruses.As a series of interventions to control avian influenza transmissionin Hong Kong LPMs, local health authority implemented marketrest days once every month since mid-2001, and an additional restday every month since 2003, during which all unsold poultry wereslaughtered and the stalls cleaned and disinfected. Rest days werefound to effectively reduce avian influenza A(H9N2) isolation rateto baseline level for a few days following the rest days. However,H9N2 isolation rate was still observed to be increasing between therest days, indicating the existence of efficient transmission in spite ofrapid turnover of poultry.In LPMs, poultry are usually stored in cages where drinkingwater is shared among poultry. This is analogous to environmentalcontamination in the wild, but transmissibility may even be higherdue to the dense environment. The use of drinking water for avianinfluenza surveillance in LPM setting was suggested to be moresensitive than fecal samples (1). However, the relative contributionof direct fecal-oral versus water transmission routes in the LPMsetting was not yet understood. This study aimed to determine theirrole, which will have implications in the control of avian influenzatransmission.MethodsWe analyzed 7,321 paired fecal and drinking water samplesfrom a longitudinal surveillance programme during the period with2 monthly rest days in the LPMs. Samples were collected fromchicken cages and subsequently cultured. Positive isolates weresubtyped by hemagglutination-inhibition tests and neuraminidaseinhibition test. Data were aggregated by sampling occasion and daysafter the rest days.A compartmental transmission model which incorporated turnoverand overnight stay of poultry, virus contamination and decay indrinking water was fitted to the data (Figure 1). A 12-hour tradingday was assumed. Based on the parameterized model, we simulatedthe scenario that water transmission was prohibited to assess the roleof transmission via drinking water.ResultsH9N2 isolation rates ranged from 0-25% for fecal samples and0-56% for drinking water samples. A clear increasing trend can beseen over days after the rest days (Figure 2). The estimated parameterfor water transmission is higher than the parameter for direct fecal-oraltransmission. Simulation results show that transmission via drinkingwater plays a major role in the amplification of LPAI in the LPMsetting (Figure 2).ConclusionsOur study showed that drinking water has a major role in thetransmission and amplification of LPAI H9N2 in LPMs, comparingto direct fecal-oral transmission route. Given the relatively lowprevalence of H9N2 in chicken, direct transmission is governed bychance events, while chickens are consistently exposed to viruses indrinking water if contaminated. Drinking water could be targeted forintervention to control LPAI transmission in LPM. The use of drinkingfountain or frequent disinfection of drinking water may be considered.Avian influenza viruses (e.g. H5N1) may differ in their pattern ofvirus shedding via oral versus fecal routes and thus extrapolation ofthese results to other viruses needs to be done with caution. However,H7N9 viruses are similar to H9N2 viruses by being shed primarilyvia the respiratory / oral route (2) and it is reasonable to assume thatthese conclusions would apply to H7N9 virus which is of major publichealth concern. However, our model could not differentiate the effectof indirect fecal-oral transmission through contamination of drinkingwater by droppings versus contamination through drinking.