In February 2006, avian influenza (H5N1) emerged among domestic poultry in the Nile Delta of Egypt. Within 4–5 weeks, it had affected commercial farms and backyard flocks throughout Egypt and resulted in zoonotic transmission to 10 persons in many governorates. Currently, Egypt has reported the third largest number of cases of avian influenza (H5N1) after Indonesia and Vietnam (1
The mortality rate for avian influenza (H5N1) in Egypt (38%) is lower than that in other countries. As of March 2009, mortality rates were 82% in Indonesia, 50% in Vietnam, 66% in the People’s Republic of China, and 68% in Thailand. Explanations for this observation include lower mortality rates for certain demographic groups, clinician awareness resulting in improved medical care, or less pathogenic virus. The most striking finding is the low mortality rate for children. Although children represent 54% of reported infections, they account for only 8% of deaths. This high survival rate is unlikely to be caused by young age alone. Children were hospitalized earlier in the clinical course of their illness, were more likely to receive oseltamivir within the first 2 days, and appeared to be less ill than adults, as noted by the high proportion of chest radiographs with no abnormal findings and the low proportion of children with respiratory failure. Differences in sensitivity of surveillance methods among countries must also be considered.
One must also consider whether the 2.2 virus clade is less virulent. This suggestion is not supported by a report of the 2005–2006 outbreak of clade 2.2 virus (H5N1) in Turkey, where of 8 patients 5–15 years of age, 4 (50%) died (6
Despite overall low mortality rates, particularly among children, the mortality rate in women was >52%. This rate could be due to reasons that include receiving a higher virus inoculum to the lungs through activities associated with slaughtering and defeathering birds, a more profound proinflammatory cytokine response, or delay in receiving healthcare. Only delay in receiving healthcare was examined in this study. Women reported a longer time between illness onset and hospitalization and a longer time until the first dose of oseltamivir than men. Women and men who sought healthcare were admitted to the same facilities and received identical care.
More than 5,000 asymptomatic persons known to have been exposed to poultry infected with avian influenza virus (H5N1) or in contact with confirmed human case-patients were followed up clinically and tested by using real-time PCR. Although prophylaxis was not given, influenza-like illnesses were not observed and all persons showed negative results. Although serologic testing is needed to exclude infection with avian influenza virus (H5N1), it was unlikely that a large proportion of these persons with high-level exposures to infected birds or humans became infected and supports the decision of the MOH to discontinue testing asymptomatic persons. This finding is consistent with those of studies in Thailand (12
) and Cambodia (13
Although infection and illness do not develop in most persons exposed to infected poultry, all but 2 cases were attributed directly to exposure to poultry likely infected with avian influenza virus (H5N1). No illnesses were attributed to exposure to wild birds. Although 3 family clusters were identified, all 7 persons in these clusters had independent exposures. Many families in Egypt raise backyard flocks for eggs and purchase live poultry for meat. Among case-patients, the likely route of infection appears to be direct handling, slaughtering, or defeathering infected birds recently purchased for meat and mingling of recently purchased birds with egg-laying flocks. Recently purchased birds were frequently slaughtered before illness was noted, and purchase was often followed by illness and death among egg-producing flocks.
Contact between backyard flocks and wild infected birds could not be estimated, but exposure to feral poultry in canals and waterways near affected households was common. Because persons in Egypt rely on live poultry purchased at markets for dietary protein, the price of poultry influences poultry-buying practices of families. Women in several affected families noted exceptionally low prices for healthy looking birds. These prices indicated that they might be buying infected birds. This finding was true when prices of beef increased in response to decreased availability or increased demand. Despite this knowledge, most persons believed they would be able to slaughter and prepare birds before they became ill or died. This belief was true in most cases but recently purchased birds frequently infected egg-laying flocks, which died within days of exposure.
Despite knowledge of overall exposure patterns and identification of groups at risk for exposure, little detailed information on activities that result in infection is available. Although slaughtering and defeathering infected birds appear to be high-risk practices, there have likely been thousands of infected birds sold and slaughtered in homes in Egypt over the past 3 years. Despite this suggestion, we have reports of only 63 cases. Although exposure to avian influenza virus (H5N1) infection is necessary for infection, exposure is not sufficient to explain the epidemiology of cases of avian influenza (H5N1) in Egypt. Whether there is another unknown risk factor or variation in the way women slaughter poultry in Egypt is unclear.
Demographics of influenza cases in Egypt are different from those in other highly affected countries and are useful for determining exposures and activities that result in infection. Women appear to be at greater risk than men of becoming infected, and, once ill, at greater risk of death. In Egypt, the male:female ratio among patients is 1:1.7 and differs markedly from the 1:1 ratio seen globally (14,15
). Caring for or slaughtering poultry is generally the responsibility of women and may explain a higher exposure rate for women. Similarly, age distribution of case-patients differs. In Egypt, 54% of case-patients were <15 years of age, compared with <
35% in Indonesia, Vietnam, and China. In Egypt, small children follow their mothers during routine chores, such as feeding and slaughtering poultry. At other times, children will play with poultry, which roam freely around the home. There is a general belief that parents in Egypt will quickly seek medical care for their ill children. This belief is strongly suggested by the fact that children with fever and exposure to dead or ill poultry were consistently evaluated and hospitalized sooner than adults. In addition, many children had mild illness. Mild clinical illness may be caused by early hospitalization, early doses of oseltamivir, or a low virus inoculum.
This report describes 63 human cases of avian influenza (H5N1) in Egypt during March 2006–March 2009. During April–July 2009, a total of 20 additional cases were identified (83 cases by the end of July 2009) for which data were not available. Analysis of limited information reported to the World Health Organization showed a median age of 4 years (compared with 10 years for the 63 cases), a case-fatality rate of 15% (compared with 38%), and faster hospitalization after illness onset. Ongoing transmission in the summer of 2009 is indicative of persistent disease in poultry, and limited analysis reflects the high proportion of influenza in children. Thus, avian influenza virus (H5N1) remains endemic throughout Egypt. However, human infections are rare and disproportionately affect women and their children, who are responsible for caring for and slaughtering birds within the home. To reduce their risk, specific slaughtering practices and other transmission risk factors should be identified and appropriate interventions implemented. In addition, emphasis on controlling domestic poultry populations and increased use of bird cages, hand washing, and other protective measures specific for women and children should continue.