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when the live poultry market surveillance program began in september 1999 , eight of a total of 80 live poultry markets were selected to represent the 3 major regions of hong kong : hong kong island , kowloon , and the new territories . since then
, the number of markets has declined , and by may 2011 , only 5 of the 8 selected live poultry markets continued in operation ( of a total of 39 operating live poultry markets ) .
we previously published data on the effect of introducing various interventions in live poultry markets , which included the ban on the sales of live quail and the introduction of rest days ( 7 ) .
in addition to collecting fecal droppings from the cage floors for virus isolation , we collected data on the total sales of chickens and minor poultry , the proportion of chickens imported as a ratio of the whole , the temperature and relative humidity , and the type of ventilation used , as described ( 7 ) .
samples collected in virus transport medium were inoculated into 911-day - old embryonated eggs , and allantoic fluid with positive hemagglutination was confirmed and subtyped using standard antiserum . because hpai a virus ( h5n1 ) is rarely detected in live poultry markets in hong kong , we used isolation rates of influenza a virus ( h9n2 ) as an indicator of the effect of these interventions on avian influenza virus circulation .
the median numbers of samples collected weekly from chickens and minor poultry were 107 ( range 3722 ) and 23 ( range 1397 ) , respectively ( see technical appendix for weekly numbers of samples ) .
the poisson generalized model ( 8) with influenza virus ( h9n2 ) weekly isolation counts as the outcome variable was fitted as described ( 7 ) and adjusted for proportion of chickens imported ; total sales of chickens and minor poultry ; ventilation system ; weekly average temperature ; relative humidity ; seasonal variations ; sample size ; and periods corresponding to the respective interventions : period i ( no rest day ) , ii ( 1 monthly rest day with quail being sold in the live poultry market ) , iii ( 1 monthly rest day with elimination of live quail from the live poultry market ) , iv ( 2 monthly rest days ) , and v ( ban on holding poultry overnight in live poultry market ) .
these variables were considered potentially important confounders related to transmission efficiency of avian influenza virus ( 9 ) , source , type , and volume of poultry .
weekly virus isolation counts were analyzed from september 22 , 1999 , through may 31 , 2011 . a separate model for poultry and minor poultry was fitted , and all analyses were implemented by using r version 2.12.1 software ( r development core team , vienna , austria ) .
the figure shows overall isolation rates by week for chicken and minor poultry from 1999 through 2011 ; the table gives the parameter estimates for the final fitted models , which were adjusted for the effect of covariables that could affect the isolation of influenza in the study . for chickens and minor poultry , compared with the reference category of 2 monthly rest days ,
the ban on keeping live poultry overnight in live poultry markets was associated with dramatic and significant reduction of influenza virus ( h9n2 ) isolation .
the isolation rate of influenza virus ( h9n2 ) among chickens declined 84% ( adjusted relative risk 0.16 ; p = 0.006 ) , and no influenza subtype h9n2 viruses were isolated from minor poultry after the ban on holding poultry overnight in live poultry markets was implemented .
higher volume of minor poultry sales was also significantly associated with higher isolation rate of influenza virus ( h9n2 ) .
weekly influenza virus a ( h9n2 ) isolation rates for chickens ( a ) and minor poultry ( b ) in live poultry markets , hong kong , september 1999may 2011 .
vertical lines denote periods for different interventions : i , no rest day ; ii , 1 monthly rest day with quail sold in live poultry markets ; iii , 1 monthly rest day with no sales of quail in live poultry markets ; iv , : 2 monthly rest days ; v , ban on keeping live poultry overnight in live poultry markets . *
reliable confidence interval can not be estimated because of zero isolation of influenza virus ( h9n2 ) from minor poultry after introduction of a ban on keeping live poultry overnight in live poultry markets .
the seasonality coefficients  and  contribute to the estimated isolation rate in week t via the terms cos(2t/52 ) + sin(2t/52 ) .
a previous study that used a stochastic metapopulation model showed that frequent rest days in live poultry markets were effective for reducing transmission of avian influenza ( h5n1 ) ( 10 ) .
our findings show a large additional decline in the influenza virus ( h9n2 ) isolation rate after implementation of a ban on keeping live poultry overnight , which suggests that this intervention has an even greater effect on reducing viral load in live poultry markets than the previous intervention of 1 or 2 rest days per month .
while low pathogenic influenza virus ( h9n2 ) was the indicator virus in our study , it is likely that these interventions would have comparable effects on highly pathogenic viruses such as avian influenza ( h5n1 ) ; this effect has been demonstrated by mathematical modeling ( 10 ) .
studies by others on social network analysis have shown that daily cage cleaning and disinfection of live poultry markets in southern china ( 11 ) , and protective factors including removal of waste in indonesia ( 12 ) contributed to a reduction of hpai ( h5n1 ) in live poultry markets . taken together , these studies show that eliminating the carryover of live poultry in markets from one day to the next , in the form of rest days or a total ban , is highly effective for reducing viral amplification and persistence in live poultry markets and consequently minimizes zoonotic risk .
weekly number of samples and influenza virus ( h9n2 ) isolation rates for live poultry markets , by poultry type , hong kong , september 1999013;may 2011 .
we analyzed 12 years of surveillance data on avian influenza in hong kong live poultry markets . 
 a ban on keeping live poultry overnight in these markets reduced virus isolation rates by 84% in chickens ( p = 0.006 ) and 100% ( p = 0.01 ) in minor poultry .