Continuing Threat of Influenza (H5N1) Virus Circulation in Egypt

Reservoirs for the continuing influenza (H5N1) outbreaks in Egypt are ill-defined. Through active surveillance, we detected highly pathogenic influenza subtype H5 viruses in all poultry sectors; incidence was 5%. No other subtypes were found. Continued circulation of influenza (H5N1) viruses in various regions and poultry sectors perpetuates human exposure in Egypt.

Reservoirs for the continuing infl uenza (H5N1) outbreaks in Egypt are ill-defi ned. Through active surveillance, we detected highly pathogenic infl uenza subtype H5 viruses in all poultry sectors; incidence was 5%. No other subtypes were found. Continued circulation of infl uenza (H5N1) viruses in various regions and poultry sectors perpetuates human exposure in Egypt.
A fter 150 confi rmed human cases and continuous outbreaks in its different poultry production sectors, Egypt became an epicenter for highly pathogenic avian infl uenza (H5N1) virus activity and one of the few countries where this virus is endemic. The long-term endemicity of infl uenza (H5N1) virus in poultry in Egypt has generated substantial viral genetic and antigenic diversity, as has been seen in other areas (1)(2)(3), yet the ecology and epizootology of the virus in the various poultry sectors remains unknown. To determine the incidence and diversity of infl uenza viruses among poultry in 6 governorates in Egypt, we conducted surveillance for 1 year.
A total of 243-764 samples were collected monthly, depending on the number of poultry available at the sites during the sample collection visit (Figure 1). At least 2 samples tested positive in every surveillance month except June 2010. The positivity rate was highest (11.1%) in October 2009. We were not able to detect a seasonal pattern  of infl uenza outbreaks in poultry ( Figure 1); however, during our surveillance period, human cases of infl uenza (H5N1) virus infection were reported throughout the year and peaked in January and February 2009 (8) (Figure 1). By species, ≈82% of the swab samples were collected from chickens, followed by ducks (14.7%) and other species of domestic birds (3.2%). Positivity rates differed signifi cantly (p<0.001, Pearson χ 2 test). Among chickens, 13.7% of the samples from layers, 10.0% from breeders, and 4.3% from broilers were positive. Among ducks, 1.2% of samples were positive. Only 1 pigeon swab sample was positive ( Figure 2). By collection location, the highest positivity rate (≈12%) came from poultry abattoirs (p<0.001, Pearson χ 2 test). The next highest rates came from commercial farms (6.8%), followed by live-bird markets (3.3%). Only 0.9% of swab samples from backyard fl ocks were positive. Most (94.5%) samples were collected from apparently healthy birds; of those, 4.5% were positive. In contrast, 13.4% of samples from sick or dead birds were positive (p<0.001, Pearson χ 2 test).
To identify other putative sources of human infection with infl uenza (H5N1) virus, we also examined a population of wild egrets (Bubulcus ibis) in urban greater Cairo. These birds congregate on trees next to the Giza Zoo in a heavy traffi c area with a dense human population. RT-PCR detected infl uenza (H5N1) viruses in the feces of these wild egrets. Infl uenza (H5N1) virus shedding by the egrets threatens the exotic bird population at the zoo as well as humans in that area.

Conclusions
In Egypt, most swab samples positive for infl uenza (H5N1) virus were from chickens. Among ducks, the positivity rate was as low as 1.2%, although in other regions, ducks have been shown to play a key role in avian infl uenza transmission (9). All samples with positive results by RT-PCR contained highly pathogenic infl uenza (H5N1) viruses. The surprising lack of detection of other infl uenza subtypes in our surveillance may be explained by establishment of subtype H5N1 as the dominant infl uenza strain in poultry in Egypt. Alternatively, low-pathogenicity viruses may be circulating in different regions or different host populations not covered by our surveillance. Whatever the reason, the lack of substantial cocirculation of multiple infl uenza viruses reduces the chances of infl uenza (H5N1) virus evolution occurring in Egypt by reassortment.
In Egypt, commercial farms are major reservoirs for infl uenza (H5N1) virus; the positivity rate was higher for those farms (7.2%) than for backyard farms (0.9%). Because the sampled poultry at commercial farms, where biosecurity measures were generally lax, were vaccinated with commercially available subtype H5 vaccines, the effectiveness of such vaccines becomes highly questionable. The lower positivity rate among backyard poultry may be explained by the fact that the growers slaughter these birds at the fi rst sign of disease. Reports of infl uenza (H5N1) virus infections in humans in Egypt show that most of these persons had had contact with sick poultry, primarily in backyards (8,10), as has been reported in Asia (11)(12)(13). Our fi ndings indicate that the threat to humans in Egypt is much more widespread than previously reported. We detected infl uenza (H5N1) viruses in poultry from all production sectors and from wild egrets in Cairo. Among specimens collected from live-bird markets and slaughterhouses in Cairo, ≈6% had positive results; these birds usually come from commercial farms in rural areas. This fi nding indicates that the public health concern applies not only to rural poultry growers but also to persons in urban areas.
Although we were able to detect infl uenza virus among poultry continuously during surveillance, we did not establish a clear seasonal pattern of outbreaks, an indicator of continuous evolution of subtype H5N1 viruses endemic to Egypt. During the same period covered by our surveillance, human cases were reported during 8 of the 12 months; incidence was highest in January and February, refl ecting a seasonal pattern conforming to the climate, with infl uenza activity peaks in the colder months. These data suggest that the seasonality of infl uenza (H5N1) in humans is not explained by increased virus activity in the associated poultry population but rather by other unidentifi ed behavioral or environmental factors.
Our surveillance fi ndings reveal that highly pathogenic infl uenza (H5N1) viruses are abundant and persistent in Egypt. Closer surveillance of avian infl uenza viruses in domestic poultry and expansion of such surveillance to include wild and migratory birds is warranted in an effort to continuously monitor the evolution of subtype H5N1 and other infl uenza viruses in Egypt.