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      Food Markets with Live Birds as Source of Avian Influenza


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          Highly pathogenic avian influenza virus (HPAI) H5N1 infected 202 persons worldwide and killed 113 as of April 30, 2006 ( 1 ). Most patients were exposed to ill or dead birds or were involved in the slaughter or preparation of birds for human food ( 2 ). However, of 19 patients with confirmed cases in the People's Republic of China, 5 had no history of direct contact with ill or diseased birds and resided in urban or periurban areas that did not have farmed birds. We studied an infected patient from Guangzhou who did not report contact with birds. The Study The patient was from Guangzhou, the capital of the southern province of Guangdong. A fever (39°C) developed on February 22, 2006. He was hospitalized on February 26 and died on March 2. Diagnosis of influenza virus infection was made on March 3. Throat swab specimens obtained on March 1 and 2 tested positive for HPAI H5N1 virus by reverse transcription (RT)–PCR. Virus was isolated and named A/Guangzhou/1/2006 (H5N1). Epidemiologic studies showed that the patient did not slaughter, process, or cook birds. However, while looking for work before his illness, he visited 9 food markets that had live birds. All 9 markets were located in the central part of the city (Table). He visited food market F twice a day from January 23 to 27 and food market G on February 17 for 30 minutes. Before his illness, he and his girlfriend (whom he lived with) shopped at markets B and F on February 20–22. He also visited food market I from February 10 to February 20. The dates he visited the other food markets could not be determined. Onset of fever occurred on February 22. Table Serum and swab sample results from live birds and animal cages sampled at markets in Guangzhou, People's Republic of China* Source Food market A B C D E F G H I T S T S T S T S T S T S T S T S T S T S Serum Poultry purveyors 22 22 22 21 6 5 2 2 14 12 14 13 14 14 12 11 15 10 121 110 Swabs Animal cages 20 10 27 0 8 8 4 0 16 3 28 8 27 18 24 8 27 24 181 79 Anal swabs Chicken 160 10 190 6 64 6 36 5 95 6 268 7 195 3 160 1 205 13 1,373 57 Duck 10 0 5 1 4 1 0 0 0 0 3 1 3 3 2 1 10 5 37 12 Goose 5 0 0 0 0 0 0 0 3 1 3 1 0 0 3 1 6 4 20 7 Pigeon 15 0 20 3 10 2 0 0 0 0 0 0 15 2 10 1 70 5 140 13 Partridge 30 0 45 0 30 1 0 0 0 0 0 0 0 0 10 1 20 2 135 4 Quail 80 0 110 0 60 0 0 0 0 0 0 0 0 0 0 0 15 1 265 1 *T, total no.; S, no. sampled. Markets and samples from which specimens tested positive for virus genes or neutralizing antibody against highly pathogenic avian influenza virus H5N1 are in boldface. The food markets were typically large, clean, and well managed and had vendors selling vegetables, fruits, raw and cooked meats, food flavorings, beverages, and other goods. They are typical of larger food markets in cities in the People's Republic of China. The only difference between markets in Guanzhou in southern China and those in cities in northern China is that more ( 2 – 9 ) booths are used to sell live birds in Guanzhou. Wire cages are stacked next to each other with ≈5–10 birds in each cage (chickens, geese, ducks, and pigeons). Each species of bird is placed in separate cages; chickens are the most common species. All cages are located in a closed room separated by a glass window from customers, who choose the bird they prefer. When a live bird is selected, it is slaughtered in view of the customer. Sanitation inspections are routinely performed by municipal authorities. No diseased or dead birds were observed during this investigation. Animal cages were swabbed and anal swabs of live birds were obtained at the food markets (Table) on March 3 and 4 and tested for HPAI by using RT-PCR ( 3 ) for the hemagglutinin (H5), neuraminidase (N1), and membrane (M) genes. Positive PCR results were confirmed by sequencing. None of 94 anal swabs from live birds tested positive for HPAI H5N1. However, 1 of 79 animal cage swabs tested positive for HPAI H5N1 (Figure 1). The positive swab was from a goose cage at market I (Table), the market that the patient visited from February 10 to February 20. The nucleotide sequences of H and M genes from specimens from this patient were compared with those from the animal cage swab and submitted to GenBank (accession nos. DQ842487–90). Forty-eight variations were found in the NA gene and 15 were found in the HA gene, which resulted in 17 HA amino acid and 3 NA amino acid changes, respectively. Phylogenetic analysis with the neighbor-joining method using the ClustalX program ( 4 ) suggested that the 2 strains are related to each other and to duck isolates (Figure 2). Figure 1 Detection of avian influenza virus H5N1 from an animal cage for geese by reverse transcription–PCR. Viral RNA was extracted from the sample and amplified by using 3 pairs of primers specific for membrane (M), hemagglutinin (H5), and neuraminidase (N1) virus genes. Sample buffer was used as a negative control, and viral RNA from a human H5N1 virus strain (A/Hong Kong/486/97) was included as a positive control. First lane, molecular mass ladder. Figure 2 Phylogenetic relationships of representative H5N1 influenza virus strains and patient and animal cage isolates (indicated by asterisks) used in this study. A) Hemagglutinin gene (nt positions 29–1650). B) Neuramidase gene (nt positions 28–1323). Gs, goose; GD, Guangdong; Ck, chicken; CN, People's Republic of China; Dk, duck; HK, Hong Kong; HB, Hebei; FJ, Fujian; GZ, Guangzhou; ST, Shantou; HN, Hunan; WDK, wild duck; GX, Guangxi; AH, Anhui; Qa, quail; YN, Yunnan; BH Gs, brown-headed goose; QH, Qinghai; THA, Thailand, NP, Nakhon Pathom; Vnm, Vietnam; ZJ, Zhejiang; Sw, swine. Scale bars show percentage relatedness. Serum samples were obtained from 110 of 121 poultry purveyors working at the live bird food markets and screened for antibody to H5N1 to determine if subclinical infections occurred. One of 110 serum samples was positive (titer 320) by hemagglutination-inhibition assay with turkey erythrocytes (Lampire Biologic Laboratories, Pipersville, PA, USA) and H5N1 virus strains A/Hong Kong/486/97 and A/Vietnam/1194/04/H5N1 ( 5 ). Neutralizing antibody titers against the 2 strains of virus were 1,280 and 640, respectively. The positive serum sample was from a 44-year-old man who slaughtered birds for 5 years. He slaughtered ≈100 chickens/day and did not report any recent respiratory diseases. He denied any contact with ill birds. Conclusions Our investigation suggests that the patient may have been infected by an unknown mechanism at a food market that had live birds. We detected H5N1 virus genes in a swab from a goose cage and neutralizing antibody against H5N1 in a poultry worker in 1 of the food markets the patient visited. This case from Guangzhou was not an isolated event. Five patients with H5N1 infection with no history of exposure to diseased or dead birds before the onset of avian influenza have been reported in the People's Republic of China; 4 of these 5 patients visited markets that had live birds. The first patient was a 41-year-old woman from Fuzhou, the capital of Fujian Province, whose diagnosis was made in December 2005 ( 6 ). She visited a market that had live birds 2 weeks before her illness. Another patient lived in a periurban area of Chengdu, the capital of Sichuan Province; her diagnosis was made in January 2006. She was self-employed in a shop selling dry goods at a market that had live birds in Jinhua Town in Chengdu ( 7 ). Two other patients in urban areas were reported, 1 in Shanghai and 1 in Shenzhen. Influenza was diagnosed in the patient in Shanghai in March 2006, but this patient had no history of visiting a food market that had live birds or contact with diseased birds ( 8 ). Influenza was diagnosed in the patient in Shenzhen in April 2006; this patient reported visiting a food market that had live poultry before becoming infected with influenza virus. Our findings suggest that food markets or farmers' markets that have live poultry may be a source for avian influenza infection in which healthy live birds may carry the virus. This was previously shown in Hanoi, Vietnam, in 2001, where H5N1 virus was detected in domestic birds in a live bird market ( 9 ). Serologic investigation also demonstrated low seroprevalence of antibody against HPAI H5N1 in poultry workers from this market. However, no outbreaks of HPAI among birds were reported until early 2004 ( 10 ). H5N1 virus may be sustained in poultry largely through the movement of poultry and poultry products, especially through domestic ducks ( 11 , 12 ). The introduction of H5N1 virus from healthy poultry (such as ducks) may be occurring where no outbreaks in healthy flocks have been observed. Therefore, the virus is likely reintroduced at low levels and can infect persons visiting live poultry markets. The cultural preference of eating freshly slaughtered birds is not unique to the People's Republic of China; it is also common in other Asian countries. Our results suggest that the practice of selling live birds directly to consumers in food markets should be discouraged in areas currently experiencing influenza outbreaks among birds, especially in large modern cities where there may be a threat to the casual market visitor ( 2 , 13 , 14 ).

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          Avian influenza A (H5N1) in 10 patients in Vietnam.

          Recent outbreaks of avian influenza A (H5N1) in poultry throughout Asia have had major economic and health repercussions. Human infections with this virus were identified in Vietnam in January 2004. We report the clinical features and preliminary epidemiologic findings among 10 patients with confirmed cases of avian influenza A (H5N1) who presented to hospitals in Ho Chi Minh City and Hanoi, Vietnam, in December 2003 and January 2004. In all 10 cases, the diagnosis of influenza A (H5N1) was confirmed by means of viral culture or reverse transcriptase-polymerase chain reaction with primers specific for H5 and N1. None of the 10 patients (mean age, 13.7 years) had preexisting medical conditions. Nine of them had a clear history of direct contact with poultry (median time before onset of illness, three days). All patients presented with fever (temperature, 38.5 to 40.0 degrees C), respiratory symptoms, and clinically significant lymphopenia (median lymphocyte count, 700 per cubic millimeter). The median platelet count was 75,500 per cubic millimeter. Seven patients had diarrhea. In all patients, there were marked abnormalities on chest radiography. There was no definitive evidence of human-to-human transmission. Eight patients died, one patient has recovered, and one is recovering. Influenza A (H5N1) infection, characterized by fever, respiratory symptoms, and lymphopenia, carries a high risk of death. Although in all 10 cases the infection appears to have been acquired directly from infected poultry, the potential exists for genetic reassortment with human influenzaviruses and the evolution of human-to-human transmission. Containment of influenza A (H5N1) in poultry throughout Asia is therefore urgently required. Copyright 2004 Massachusetts Medical Society
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            Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control.

            Preparedness for a possible influenza pandemic caused by highly pathogenic avian influenza A subtype H5N1 has become a global priority. The spread of the virus to Europe and continued human infection in Southeast Asia have heightened pandemic concern. It remains unknown from where the pandemic strain may emerge; current attention is directed at Vietnam, Thailand, and, more recently, Indonesia and China. Here, we report that genetically and antigenically distinct sublineages of H5N1 virus have become established in poultry in different geographical regions of Southeast Asia, indicating the long-term endemicity of the virus, and the isolation of H5N1 virus from apparently healthy migratory birds in southern China. Our data show that H5N1 influenza virus, has continued to spread from its established source in southern China to other regions through transport of poultry and bird migration. The identification of regionally distinct sublineages contributes to the understanding of the mechanism for the perpetuation and spread of H5N1, providing information that is directly relevant to control of the source of infection in poultry. It points to the necessity of surveillance that is geographically broader than previously supposed and that includes H5N1 viruses of greater genetic and antigenic diversity.
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              Isolation and characterization of avian influenza viruses, including highly pathogenic H5N1, from poultry in live bird markets in Hanoi, Vietnam, in 2001.

              Since 1997, outbreaks of highly pathogenic (HP) H5N1 and circulation of H9N2 viruses among domestic poultry in Asia have posed a threat to public health. To better understand the extent of transmission of avian influenza viruses (AIV) to humans in Asia, we conducted a cross-sectional virologic study in live bird markets (LBM) in Hanoi, Vietnam, in October 2001. Specimens from 189 birds and 18 environmental samples were collected at 10 LBM. Four influenza A viruses of the H4N6 (n = 1), H5N2 (n = 1), and H9N3 (n = 2) subtypes were isolated from healthy ducks for an isolation frequency of over 30% from this species. Two H5N1 viruses were isolated from healthy geese. The hemagglutinin (HA) genes of these H5N1 viruses possessed multiple basic amino acid motifs at the cleavage site, were HP for experimentally infected chickens, and were thus characterized as HP AIV. These HA genes shared high amino acid identities with genes of other H5N1 viruses isolated in Asia during this period, but they were genetically distinct from those of H5N1 viruses isolated from poultry and humans in Vietnam during the early 2004 outbreaks. These viruses were not highly virulent for experimentally infected ducks, mice, or ferrets. These results establish that HP H5N1 viruses with properties similar to viruses isolated in Hong Kong and mainland China circulated in Vietnam as early as 2001, suggest a common source for H5N1 viruses circulating in these Asian countries, and provide a framework to better understand the recent widespread emergence of HP H5N1 viruses in Asia.

                Author and article information

                Emerg Infect Dis
                Emerging Infect. Dis
                Emerging Infectious Diseases
                Centers for Disease Control and Prevention
                November 2006
                : 12
                : 11
                : 1773-1775
                [* ]Guangzhou Center for Disease Control and Prevention, Guangzhou, People's Republic of China;
                []The University of Hong Kong, Hong Kong Special Administrative Region, People's Republic of China;
                []National Institute for Communicable Disease Control and Prevention, Beijing, People's Republic of China;
                [§ ]State Key Laboratory for Infectious Disease Prevention and Control, Beijing, People's Republic of China
                Author notes
                Address for correspondence: Jianguo Xu, National Institute of Communicable Diseases Control and Prevention, Chinese Center for Disease Control and Prevention, PO Box 5, Changping, Beijing 102206, People’s Republic of China; email: xujg@ 123456public.bta.net.cn

                Infectious disease & Microbiology
                dispatch,highly pathogenic avian virus,food markets,live birds


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