Risk for infection with highly pathogenic influenza a virus in chickens, Hong Kong, 2002

Emerging Infectious Diseases, March, 2007 by Nina Y. Kung, Roger S. Morris, Nigel R. Perkins, Les D. Sims, Trevor M. Ellis, Lucy Bissett, Mary Chow, Ken F. Shortridge, Yi Guan, Malik J.S. Peirist

We used epidemiologic evaluation, molecular epidemiology, and a case-control study to identify possible risk factors for the spread of highly pathogenic avian influenza A virus (subtype H5N1) in chicken farms during the first quarter of 2002 in Hung Kong. Farm profiles, including stock sources, farm management, and biosecurity measures, were collected from 16 case and 46 control chicken farms by using a pretested questionnaire and personal interviews. The risk for influenza A (H5N1) infection was assessed by using adjusted odds ratios based on multivariate logistic regression analysis. Retail marketing of live poultry was implicated as the main source of exposure to infection on chicken farms in Hung Kong during this period. Infection control measures should be reviewed and upgraded as necessary to reduce the spread of influenza A (H5N1) related to live poultry markets, which are commonplace across Asia.

The spread of highly pathogenic avian influenza (HPAI) type A virus (subtype H5N1) infection in poultry in Asia and beyond poses threats to both human and animal health. Attempts to control outbreaks of this disease in poultry have become a regional and global priority (1,2). However, little reliable epidemiologic data exist on routes of virus transmission and perpetuation in poultry within affected countries.

Repeated outbreaks of HPAI (H5N1) outbreaks in poultry occurred in farms and live poultry markets within the Hong Kong Special Administrative Region beginning in 1997 (3-6). The first outbreak was associated with the first recorded transmission of influenza A (H5N1) to humans, with 18 cases and 6 deaths (7, 8). These outbreaks were controlled by slaughtering all poultry in all markets and local farms and stopping all trading of live poultry for 7 weeks. No additional human cases were reported after these interventions, and this particular genotype of influenza A (H5N1) virus has not been detected since (4).

No further outbreaks of influenza A (H5N1) in poultry were recorded until 2001, when the virus was detected in live poultry retail markets in Hong Kong. Poultry farms were unaffected. This outbreak led to a slaughter of poultry in live poultry markets in Hong Kong. However, in January 2002, influenza A (H5N1) was again detected in Hong Kong wholesale and retail poultry markets (3,9). Trace-back from the wholesale poultry market led to detection of the virus on February 1, 2002, on a chicken farm in a densely populated chicken farming area of the New Territories area of Hong Kong. By late March, 17 chicken farms located within 2 km of the index farm, and 4 farms located within 2 to 5 km, were confirmed as infected (5, 6). This outbreak was controlled by a combination of depopulation of infected and contact farms, quarantine and enhanced biosecurity, and vaccination (10).

We report the results of an epidemiologic investigation of the 2002 outbreak, including a case-control study to identify risk factors associated with poultry infection in farms. These findings may provide insight into the mechanisms of the spread of HPAI (H5N1) in Asia.

Materials and Methods

Study Population

At the time of the 2002 outbreak, 146 commercial chicken farms in Hong Kong were operating, with a combined holding capacity of [approximately equal to]3 million birds. These farms supplied [approximately equal to]20% of the poultry consumed within Hong Kong, with the remaining [approximately equal to]80% imported from farms in the nearby southern provinces of China. Land-based poultry shipments from both Hong Kong and China were usually delivered to 1 wholesale poultry market and then resold to individual live poultry retail markets. Ducks and geese that were reared on poultry farms in China and imported by boat were delivered daily to a geographically separate wholesale market for slaughter and sale as chilled poultry in the live poultry markets.

A cultural preference in Asian countries for freshly killed poultry has resulted in a large volume of sales through live poultry markets, with [approximately equal to]850 retail poultry market stalls in operation across Hong Kong. Several process changes were introduced in 1998 to reduce the risk of reintroducing the virus into the live market system. Plastic poultry cages were introduced for transporting land-based poultry, and cages that contained poultry from local poultry farms or from China were washed in the wholesale market and then returned to the place of origin. At the wholesale markets, poultry were sorted according to weight and transferred to other washed plastic cages and then transported to the retail poultry markets the next day. Direct sale of poultry from farms to retail markets was discouraged but continued to occur on a limited basis. Details of the live poultry marketing system and compliance requirements imposed by Hong Kong authorities are described separately (N.Y. Kung et al., unpub, data).

After 1997, the Hong Kong government set up a Farm Hygiene section under the Agriculture, Fishery, and Conservation Department for local poultry farm surveillance. This entailed monthly testing for avian influenza and Newcastle disease viruses, testing for serologic evidence of influenza A (H5), and on-farm monitoring of disease and production. Discovery of influenza A (H5N1) in retail poultry markets triggered trace-back, which identified clinically affected farms and led to intensive on-farm investigations that identified more infected farms.