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Domestic ducks and H5N1 influenza epidemic, Thailand.

In addition to causing 12 human deaths and 17 cases of human infection, the 2004 outbreak of H5N1 influenza virus influenza virus
Any of three viruses of the genus Influenzavirus designated type A, type B, and type C, that cause influenza and influenzalike infections.
 in Thailand resulted in the death or slaughter of 60 million domestic fowl and the disruption of poultry production and trade. After domestic ducks were recognized as silent carriers of H5N1 influenza virus, government teams went into every village to cull flocks in which virus was detected; these team efforts markedly reduced H5N1 infection. Here we examine the pathobiology pathobiology /patho·bi·ol·o·gy/ (-bi-ol´ah-je) pathology.

The study or practice of pathology with greater emphasis on the biological than on the medical aspects.
 and epidemiology of H5N1 influenza virus in the 4 systems of duck raising used in Thailand in 2004. No influenza viruses were detected in ducks raised in "closed" houses with high biosecurity. However, H5N1 influenza virus was prevalent among ducks raised in "open" houses, free-ranging (grazing) ducks, and backyard ducks.


The continuing spread of H5N1 avian influenza avian influenza: see influenza.  viruses from eastern Asia to domestic and wild birds in central Asian countries, including Mongolia, Kazakhstan, Russia, and Turkey, indicates the extent to which the geographic range of this highly pathogenic influenza virus has expanded. The highly pathogenic H5N1 viruses were first detected in 1996 in geese in Guangdong, China (1); they later spread to ducks in the coastal provinces of South China (2) and to Hong Kong's live poultry markets (3). These viruses infected at least 18 persons in Hong Kong, 6 of whom died (4). The viruses were eradicated in 1998 by the culling of all poultry in Hong Kong and by changing marketing practices. Although these particular genotypes have not been detected again, other H5N1 genotypes continued to emerge in 2000 and 2001 (5).

The biology of the H5N1 viruses changed dramatically for the first time in late 2002, when the viruses were isolated from dead wild aquatic birds in Hong Kong and from decorative waterfowl waterfowl, common term for members of the order Anseriformes, wild, aquatic, typically freshwater birds including ducks, geese, and screamers. In Great Britain the term is also used to designate species kept for ornamental purposes on private lakes or ponds, while in  that died in Kowloon Park, Hong Kong (6,7). After the Z genotype of H5N1 influenza became established as the dominant H5N1 influenza virus in eastern Asia, it was transmitted to persons in Vietnam, Thailand, and Cambodia. In 2004, a distinguishable genotype was transmitted to persons in Indonesia (8). Most human cases have resulted from the direct transmission of virus from poultry to humans (9). To date, evidence for human-to-human transmission is limited (10,11). In Thailand, 13 persons infected with an H5N1 influenza virus died in 2004, and 2 additional human deaths occurred in October 2005. By contrast, in neighboring Vietnam, 42 human deaths caused by H5N1 influenza virus were reported in 2005. What accounts for these differences? Here we examine the hypothesis that the lower death rate in Thailand resulted in part from that government's recognition of the role of backyard chickens and domestic ducks in the spread and perpetration per·pe·trate  
tr.v. per·pe·trat·ed, per·pe·trat·ing, per·pe·trates
To be responsible for; commit: perpetrate a crime; perpetrate a practical joke.
 of H5N1 influenza virus and the government's aggressive culling of flocks in which the virus was detected (12).

Thai health officials recognized that the spread of H5N1 influenza viruses to domestic chickens correlated with the distribution of free-grazing ducks (13). At the beginning of the 2004 poultry outbreak, ducks were raised in 1 of 4 systems: 1) in high-biosecurity closed houses, 2) in moderately high-biosecurity open houses (ducks raised for meat and laying ducks); 3) in rice fields after harvest (free-range or so-called grazing ducks); or 4) in backyards (backyard ducks). We discuss each method, particularly emphasizing the role of grazing ducks in the perpetuation and spread of H5N1 in the country. We also describe the clinical and pathologic changes in ducks and consider the current policies regarding duck raising in Thailand. We conclude that the traditional methods of raising ducks in Thailand and the rest of Southeast Asia must be modified if we are to control the spread of avian influenza virus.

Methods of Duck Raising in Thailand

Four systems were in use during 2004 (Figure 1).


Closed High-Biosecurity System

Pekin ducks and white Cherry Valley ducks are raised in closed sheds housing 5,000-6,000 birds each. Day-old ducklings are raised for meat in 50 to 55 days by using an "all-in/all-out" system. Before the ducks are sent to slaughter, 60 cloacal cloacal

emanating from or pertaining to cloaca.

cloacal kiss
the contact which occurs during insemination in birds when the vent of the female is everted exposing the cloacal mucosa against which the phallus of the male is pressed.
 samples ([approximately equal to] 1%) are collected for virus isolation. In the slaughterhouse slaughterhouse: see abattoir; meatpacking. , 60 additional samples are collected from the same flock for virologic analysis. At the end of every 50- or 55-day cycle, each poultry house is cleaned and disinfected Disinfected
Decreased the number of microorganisms on or in an object.

Mentioned in: Isolation
. After 3 to 4 weeks, the farm is repopulated with day-old ducklings and the cycle is repeated. In 2005, [approximately equal to] 2-3 million ducks were raised in this system.

Open House System

In the open house system, ducks are raised for meat or as egg layers. The species raised for meat, Pekin Pekin (pē`kĭn), city (1990 pop. 32,254), seat of Tazewell co., central Ill., a port on the Illinois River; inc. 1839. A processing, rail, and shipping point in a grain, livestock, and dairying area, Pekin has a large food industry.  and white Cherry Valley ducks, are raised essentially as in the closed-house system with the all-in/all-out strategy. Virologic sampling is conducted as described above. At present [approximately equal to] 1 million to 2 million ducks are being raised in this system. The species raised as egg layers are khaki Campbell Khaki Campbell

English egg-laying duck. Khaki in color, head and neck green in the drake, with a dark green bill and deep orange legs. Bred by mating Rouen and a white Indian Runner.
, native laying ducks, and a crossbreed of the khaki Campbell and native laying duck. Layer ducks are housed in flocks of 3,000 to 4,000 birds. After they begin laying eggs (at 5 to 6 months of age), these ducks are kept for 12 to 13 months or until they stop laying, at which point they are sent for slaughter. After a short period for cleaning the houses, additional ducks are added as space becomes available. Presently, [approximately equal to] 5 million to 8 million laying ducks are raised in this system in Thailand. Laying ducks are sampled for virologic analysis every 3 months. Influenza-positive flocks are culled.

Grazing System (Free-range Ducks)

In 2004, ducks were also raised in the open on rice fields. Most free-range ducks are egg-laying ducks such as khaki Campbell or a crossbreed of khaki Campbell and native laying ducks. However, a small number of "meat" ducks, such as Pekin and white Cherry Valley ducks, are also raised in the open. After hatching and spending 3 weeks in a brooder brooder

stage two of the usual bird rearing sequence. After hatching the baby birds are put into a brooder house, usually with a heat source attached, for rearing. Also used as a management strategy for baby pigs which are weaned early, at 3 weeks.
, young female ducks are moved to rice paddy fields. For the next 5 to 6 months, they grow by eating snails and residual rice after the harvest. When the food supply in 1 field is exhausted, the ducks are moved by truck to another field, often over considerable distances, and even from 1 province to another (Figure 2). When the grazing female ducks are 5-6 months old, they are brought back to the farms, as in the open system described above. However, some flocks of female laying ducks are kept in the rice fields. Male ducks of the species, who are raised with egg-laying hens, and others that are produced for meat are raised in the grazing system for 2 months and are then taken to the slaughterhouses. If they have not reached the optimal weight for slaughter, they are fed supplementary rations for 1 to 2 weeks. During the nationwide surveillance campaign in 2004, 60 cloacal swab samples from each flock were collected for virologic analysis, and the whole flock was culled if a single duck was positive for H5N1 by virus isolation. Flocks that were negative for virus were monitored and put into houses. At the beginning of 2004, [approximately equal to] 10 million to 11 million grazing ducks were being raised in Thailand. Raising free-range ducks is currently illegal in Thailand; all are housed.


Backyard Ducks

Mixed species of ducks continue to be raised in the backyards of village homes together with other animals, including chickens, geese, and pigs. The duck species raised in backyards include Pekin, white Cherry Valley, Barbary Muscovy, khaki Campbell, native laying ducks, and mule ducks (a sterile crossbreed of Muscovy ducks and native ducks). If a single case of H5N1 infection is detected in a village, all the poultry in the village are culled. Approximately 1.0 million to 1.5 million ducks were raised as backyard ducks at the beginning of the outbreak in 2004; culling reduced that number to <1 million by August 2005.

National Surveillance Program

In response to the H5N1 influenza outbreaks in 2004, the government of Thailand dispatched teams to villages to identify infected birds and cull flocks in which infection was detected.

Sample Collection, Histopathology his·to·pa·thol·o·gy
The science concerned with the cytologic and histologic structure of abnormal or diseased tissue.

The study of diseased tissues at a minute (microscopic) level.
, Virus Isolation, and Serology Serology

The division of biological science concerned with antigen-antibody reactions in serum. It properly encompasses any of these reactions, but is often used in a limited sense to denote laboratory diagnostic tests, especially for syphilis.

During the study period (February to September 2004), our laboratory received 450 sick, moribund, or dead ducks from 25 flocks in the western and central provinces of Thailand <onlyinclude> Thailand is divided into 75 provinces (Thai: จังหวัด, changwat, singular and plural), which are grouped into 5 groups of provinces - sometimes the East and Central are . In the detailed studies (Table 1), blood was sampled for serologic se·rol·o·gy  
n. pl. se·rol·o·gies
1. The science that deals with the properties and reactions of serums, especially blood serum.

 analysis by the hemagglutination hemagglutination /he·mag·glu·ti·na·tion/ (he?mah-gloo-ti-na´shun) agglutination of erythrocytes.

 inhibition (HI) test. All moribund ducks were euthanized, and their internal organs were collected, fixed with 10% buffered formalin formalin /for·ma·lin/ (for´mah-lin) formaldehyde solution.

An aqueous solution of formaldehyde that is 37 percent by weight.
, and processed for histopathologic analysis. Additionally, parts of the brain, lung, trachea trachea (trā`kēə) or windpipe, principal tube that carries air to and from the lungs. It is about 4 1-2 in. (11.4 cm) long and about 3-4 in. (1.9 cm) in diameter in the adult. , intestine, liver, pancreas, kidney, ovary ovary, ductless gland of the female in which the ova (female reproductive cells) are produced. In vertebrate animals the ovary also secretes the sex hormones estrogen and progesterone, which control the development of the sexual organs and the secondary sexual , oviduct oviduct: see fallopian tube. , testes testes
 or testicles

Male reproductive organs (see reproductive system). Humans have two oval-shaped testes 1.5–2 in. (4–5 cm) long that produce sperm and androgens (mainly testosterone), contained in a sac (scrotum) behind the penis.
, heart, and tight muscle were collected for virus isolation. The tissues were ground and filtered through 0.2-[mu] filters. The filtrates of each organ were injected into 9- to 11-day-old embryonated chicken eggs and incubated at 37[degrees] C for 2 days. The eggs were observed daily to determine whether death occurred. The allantoic allantoic /al·lan·to·ic/ (al?an-to´ik) pertaining to the allantois.


pertaining to the allantois.

allantoic fluid
see fetal fluids.
 fluid was harvested and tested for influenza virus by HI assay. Any positive sample was then subtyped for H5N1. A second egg passage was performed if the embryonated eggs were still alive 72 hours after injection.

H5N1 Subtyping

Avian influenza virus was subtyped by HI assay by using antiserum antiserum /an·ti·se·rum/ (an´ti-se?rum) a serum containing antibody(ies), obtained from an animal immunized either by injection of antigen or by infection with microorganisms containing antigen.  specific against the H5 hemagglutinin hemagglutinin /he·mag·glu·ti·nin/ (-gloo´ti-nin) an antibody that causes agglutination of erythrocytes.

cold hemagglutinin  one which acts only at temperatures near 4° C.
. Reverse-transcription polymerase chain reaction polymerase chain reaction (pŏl`ĭmərās') (PCR), laboratory process in which a particular DNA segment from a mixture of DNA chains is rapidly replicated, producing a large, readily analyzed sample of a piece of DNA; the process is  (RTPCR RTPCR Reverse Transcriptase Polymerase Chain Reaction ) analysis was used for H5 and N1 typing (14).

Immunohistochemical Testing

To evaluate histologic changes, we used immunohistochemical testing by indirect immunoperoxidase staining immunoperoxidase staining

a technique of histological staining that provides morphological details and immunological identification. Analogous to immunofluorescence techniques, but uses peroxidase conjugated to immunoglobulin instead of fluorescent dyes.
 as described (15). Tissue was fixed in formalin before being embedded in paraffin, then cut in 5-[mu]-thick sections and mounted onto silanized slides.

Criteria for Culling Ducks

The criteria for culling duck flocks were based on H5N1 virus isolation and identification by serologic and RT-PCR RT-PCR

reverse transcriptase-polymerase chain reaction. See PCR1.
 analysis (12). During the screening of village poultry in 2004, a single positive virus isolation resulted in the culling of all poultry (e.g., chicken, ducks, geese, quail) in the entire village. If serologic evidence of infection was detected, cloacal swabs of 60 ducks in that flock were collected and processed for virus isolation in embryonated chicken eggs.


Detection of Influenza Viruses in Different Duck-raising Systems

Closed High-Biosecurity System

As mentioned earlier, [approximately equal to] 1% of every duck flock was sampled for H5N1 detection before being sent to slaughter. More than 10,000 ducks were tested during the study period. No virologic or serologic evidence of H5N1 virus infection was detected in the birds raised in this closed system in western Thailand, including Nakornpathom and Kanchanaburi provinces, despite cocirculation of H5N1 influenza viruses in other duck-raising systems in the region.

Open House System

Most farms that raised ducks with the open house system are in western Thailand, including the 4 provinces of Nakornpathom, Kanchanaburi, Suphanburi, and Rachaburi. Birds from 17 farms were tested for infection with virus; in birds from 4 (23.5%), infection with the H5N1 virus was detected.

Grazing System

In 28 (45.9%) of the 61 free-range duck flocks tested, infection with H5N1 influenza virus was detected. Investigators studied H5N1 infection in 10 flocks of grazing ducks in Ayuthdhaya, Nakornpathom, and Suphanburi provinces between February and July 2004 to determine the biologic and pathologic features of H5N1 infection in the field (Table 1). No virologic or serologic evidence of H5N1 infection was detected in any of the flocks while they were located in the brooding houses. However, after they were moved outdoors to the rice fields, infection with H5N1 influenza was detected in all 10 flocks; the earliest infection was detected 12 days after the ducks left the brooding houses (flock 3, at 42 days of age). The interval between leaving the brooding houses and detection of H5N1 infection was 12-63 days. Of the 10 flocks, 3 (flocks 2, 8, and 9) showed disease signs; only a few birds (<1%) in each flock were clinically affected. However, the interval between initial detection of H5N 1 viruses in the flock and culling was 5-10 days, which supports the contention that most ducks in the flocks showed no disease signs.

Serologic evaluation of the flocks showed that low titers of HI antibody were detected before culling, which indicates that an immune response immune response
An integrated bodily response to an antigen, especially one mediated by lymphocytes and involving recognition of antigens by specific antibodies or previously sensitized lymphocytes.
 had already begun without disease signs in most birds. Cloacal virus titers in individual ducks showing disease signs before culling were 2.0 3.8 [log.sub.10] 50% egg infectious dose [(EID EID Emerging Infectious Diseases (journal)
EID Electronic Identification
EID Endpoint Identifier
EID Employee Identification
EID Ecological Interface Design
EID Earned Income Disregard
EID Education and Information Division
).sub.50]/mL which shows that virus was being shed in feces (Table 1). Similar virus titers were detected in asymptomatic ducks.

Signs of disease in flocks, 2, 8, and 9 were depression, lethargy, cloudy cornea cornea: see eye. , and blindness. However, no deaths were observed in the 10 days before culling.

Backyard Ducks

Of the backyard poultry, chickens were the most frequently infected; 56% of the chicken flocks tested were positive for H5N1 influenza (12). Ducks were the second most frequently infected; 27% of backyard duck flocks were positive for H5N1. During the second wave of H5N1 infection of poultry and humans in Thailand (August-November 2004), 47% of backyard duck flocks were H5N1 positive. During this time, scientists realized that most ducks infected with H5N1 were asymptomatic.

Pathologic Features

As previously mentioned, our laboratory received 450 sick, moribund, or dead ducks, which were studied for pathologic features of H5N1 infection. These birds had been raised in the open house system or were from backyard flocks. They exhibited signs of disease such as high fever, dyspnea dyspnea /dysp·nea/ (disp-ne´ah) labored or difficult breathing.dyspne´ic

paroxysmal nocturnal dyspnea
, depression, and diarrhea, and nervous signs such as ataxia ataxia (ətăk`sēə), lack of coordination of the voluntary muscles resulting in irregular movements of the body. Ataxia can be brought on by an injury, infection, or degenerative disease of the central nervous system, e.g. , incoordination incoordination /in·co·or·di·na·tion/ (in?ko-or?di-na´shun) ataxia.

See ataxia.
, and convulsions Convulsions
Also termed seizures; a sudden violent contraction of a group of muscles.

Mentioned in: Heat Disorders
 (Figure 3A). Most had ocular and nasal discharge accompanied by conjunctivitis conjunctivitis (kənjəngtəvī`təs), inflammation or infection of the mucosal membrane that covers the eyeball and lines the eyelid, usually acute, caused by a virus or, less often, by a bacillus, an allergic reaction, or an ; 20%-100% of the birds in each flock from which these ducks originated were dead. All cloacal and tracheal tracheal

pertaining to or emanating from trachea.

tracheal aspiration
see transtracheal aspiration.

tracheal band sign
on contrast radiography of a dilated esophagus, the impression made ventrally by the trachea.
 swabs and tissue samples were positive for H5N1 by HI and RT-PCR (results not shown).


At necropsy necropsy /nec·rop·sy/ (nek´rop-se) examination of a body after death; autopsy.

See autopsy.


examination of a body after death. See also autopsy.
, gross lesions were detected, including ecchymotic ec·chy·mo·sis  
The passage of blood from ruptured blood vessels into subcutaneous tissue, marked by a purple discoloration of the skin.

[New Latin, from Greek
 or petechial hemorrhage of leg and footpad footpad

the thick, spongy structure located on each digit, and under the metacarpal- and metatarsal-phalangeal joints, and the carpus of dogs and cats. The skin is thickened, tough, and may be hyperpigmented and the hypodermis contains large amounts of adipose tissue.
; serous fluid surrounding the heart, pancreas, liver, and abdomen; cyanosis cyanosis (sī'ənō`sĭs), bluish coloration of the skin, mucous membranes, and nailbeds, resulting from a lack of oxygenated hemoglobin in the blood.  of the oral cavity; and mild pleural effusion. On histopathologic examination, the most striking lesions were found in the lung, with extensive pneumonia and severe pulmonary edema with hyaline hyaline /hy·a·line/ (hi´ah-lin) glassy and translucent.

Resembling glass, as in translucence or transparency; glassy.

 material in the alveolar alveolar /al·ve·o·lar/ (al-ve´o-lar) [L. alveolaris ] pertaining to an alveolus.

Relating to an alveolus.
 space and slight mononuclear mononuclear /mono·nu·cle·ar/ (-noo´kle-er)
1. having but one nucleus.

2. a cell having a single nucleus, especially a monocyte of the blood or tissues.

 infiltration in the area surrounding congested con·gest·ed
Affected with or characterized by congestion.

congested ENT adjective Referring to a boggy blood-filled tissue. See Nasal congestion.
 vessels (Figure 3B). Nonsuppurative encephalitis encephalitis (ĕnsĕf'əlī`təs), general term used to describe a diffuse inflammation of the brain and spinal cord, usually of viral origin, often transmitted by mosquitoes, in contrast to a bacterial infection of the meninges  with perivascular perivascular /peri·vas·cu·lar/ (-vas´ku-lar) near or around a vessel.


around a vessel.

perivascular cellulitis
 cuffing of mononuclear cells and gliosis were detected in the brains of ducks that displayed nervous signs. Hyaline degeneration and necrosis of myocardium myocardium /myo·car·di·um/ (-kahr´de-um) the middle and thickest layer of the heart wall, composed of cardiac muscle.

hibernating myocardium  see myocardial hibernation, under
 with mononuclear infiltration were detected predominantly in dead ducks from fast-growing breeds such as the Pekin and white Cherry Valley ducks. Necrotizing necrotizing /nec·ro·tiz·ing/ (nek´ro-tiz?ing) causing necrosis.
Causing the death of a specific area of tissue. Human bites frequently cause necrotizing infections.
 pancreatis with mononuclear infiltration was detected in all affected ducks. Most affected ducks exhibited focal hepatitis, tubulonephritis, splenic splenic /splen·ic/ (splen´ik) pertaining to the spleen.

Of, in, near, or relating to the spleen.


pertaining to the spleen.
 lymphoid lymphoid /lym·phoid/ (lim´foid) resembling or pertaining to lymph or tissue of the lymphoid system.

Of or relating to lymph or the lymphatic tissue where lymphocytes are formed.
 depletion or necrosis, and enteritis enteritis (ĕn'tərī`tĭs), inflammation of the gastrointestinal tract. Acute enteritis is not usually serious except in infants and older people, in whom the accompanying diarrhea can cause dehydration through the loss of fluids. . Virus antigen was detected by immunohistochemical tests in all organs tested, including trachea, lung, liver, pancreas, rectum, bursa of Fabricius bursa of Fa·bri·ci·us  
A thymuslike lymphoid gland in birds that is an outgrowth of the cloaca and the site of B cell maturation.

[After Hieronymus Fabricius (1537-1619), Italian anatomist.]
, spleen, brain, heart, and kidney (Figure 4).


Experimental Infection of Khaki Campbell Ducks

Because culling of all H5N1-positive ducks was mandated in Thailand, we could not determine the natural outcome of infection in birds raised in the open on rice fields. Therefore, khaki Campbell ducks were experimentally infected with 4 representative H5N1 viruses isolated in Thailand in 2004 and 2005. All animal experiments were performed in biosafety level 3+ facilities. All 4 viruses caused the deaths of infected ducks; however, their degree of lethality varied (Table 2). The most lethal virus tested was A/duck/Thailand/71.1/2004, which caused death in 10/10 of the infected khaki Campbell ducks, a death rate comparable to that previously reported for Mallard mallard: see duck.

Abundant “wild duck” (Anas platyrhynchos, family Anatidae) of the Northern Hemisphere, ancestor of most domestic ducks. The mallard is a typical dabbling duck in its general habits and courtship display.
 ducks (16). Also tested was a human virus isolated in 2004, A/Thailand/MK2/2004, which resulted in the death of 2/10 khaki Campbell ducks. Of the two 2005 viruses tested, 1 caused very slight disease and resulted in only 1/10 deaths (A/quail/Thailand/551/2005) whereas the other (A/duck/Thailand/144/2005) resulted in 5/10 deaths. Ducks inoculated with A/Thailand/MK2/04 shed virus for the longest period of time (day 10 postinfection), whereas the 2005 virus isolates were shed only until day 8 postinfection. These results indicate that the H5N1 avian viruses recently isolated in Thailand can cause death in khaki Campbell ducks; however, several infected ducks remained completely healthy with no signs of disease throughout the study.

Current Status of Duck Raising in Thailand

As of October 2005, the government of Thailand forbids the practice of raising ducks in open fields and moving grazing ducks from 1 region to another. Farmers who do so are subject to fines and other punishments. Additionally, they receive no compensation if they raise ducks in the open free-range system, and the ducks become infected with H5N1. Farmers were initially compensated for the culling of their ducks. Duck raising is now confined to the high-biosecurity system.

After a lull of almost 1 year, a case of human H5N1 infection was reported in Thailand in October 2005. The report was preceded by the illegal grazing of 3 flocks of 3,000 to 5,000 free-range ducks in rice fields in the area (Kanchanaburi Province). Although no direct contact between the grazing ducks and backyard chickens was known, within 2 weeks of the arrival of the ducks, chickens in the area began dying, and a person who had direct contact with the diseased chickens died of H5N1 infection. Approximately 500 backyard chickens were culled in the village. Sequence analysis of the human isolate and avian isolates (duck and chicken) from this area would be essential to confirm the epidemiologic link between these cases and, coupled with the chronology of events, to assess whether free-grazing ducks were indeed the source of infection for this outbreak.


The 4 duck-raising systems in wide use at the beginning of the 2004 Thai epidemic differed markedly in cases of influenza detected. No infections with H5N1 influenza virus were detected in ducks raised in the closed system, attesting to the effectiveness of the biosecurity employed. In contrast, H5N1 infection was detected in ducks raised in all 3 open systems. Notably, infection in the hatchery hatchery

a commercial establishment dedicated to the hatching of bird eggs to provide day old chicks and poults to the poultry industry.

hatchery liquid
the contents of unfertilized eggs. Used in petfood manufacture.
 or during the 3 weeks of brooding was detected only after the ducks were released into the rice fields. The source of the H5N1 viruses infecting domestic ducks in the rice fields remains controversial. Because H5N1 viruses were detected in herons, storks, egrets, and other dead waterfowl in Eastern Asia, the initial spread of the highly pathogenic viruses in this region of the world has been attributed to wild migrating birds. What role wild migrating birds had in the spread of H5N1 influenza virus is now a moot question. The widespread outbreaks and massive die-off of bar-headed geese and other species in western China (17,18), and the spread of H5N1 to central Asia (Kazakhstan, southern Russia, and Turkey) and more recently to Romania and Croatia in eastern Europe, are likely caused by wild migratory birds.

Detailed studies of 10 flocks of grazing ducks in Thailand in the present study showed infection with H5N1 influenza virus in all flocks. Although the ducks shed virus for 5 to 10 days, few ducks showed disease signs, and in some flocks, no ducks were symptomatic. Prolonged shedding of H5N1 viruses in experimentally infected ducks has been previously described (16,19), but prolonged shedding in free-range ducks has not. Therefore, free-range (grazing) ducks that are moved long distances by truck and that do not necessarily show disease signs are an optimal vehicle for the spread of H5N1 viruses throughout the country. These findings support the need for regulations that forbid the practice of raising ducks on the free range, a need underscored by the association of the recent human infection with illegal free-range duck grazing.

This study also points out the dangers of raising ducks in the open systems without complete biosecurity. Although stopping the commercial raising of ducks in open system may be impossible, the more problematic issue is that of backyard ducks, which are part of traditional village livestock. Highly pathogenic H5N1 influenza virus is now likely endemic in poultry in Vietnam, Cambodia, China, and Indonesia. The vaccine option should be considered if backyard duck raising is to continue in Southeast Asia.

Although no human cases of H5N1 have been attributed to direct contact with ducks in Thailand, free-grazing ducks have been identified as a risk factor for the occurrence of H5N1 outbreaks among chickens (13). In Vietnam, however, reported human cases of H5N1 influenza have potentially been linked to the consumption of raw duck blood dishes ( Therefore, H5N1-infected ducks are a risk factor for both commercial and backyard poultry and potentially for humans as well. Since the introduction of the nationwide comprehensive surveillance program ("x-ray surveys") in Thailand (12) and the culling of all infected poultry, human cases of H5N1 infection have been markedly reduced. Traditional methods of duck raising in Thailand and in the rest of Southeast Asia must be modified if we are to control highly pathogenic H5N1 avian influenza.


We thank Carol Walsh and Amanda Ball for manuscript preparation and Margaret Carbaugh for editing the manuscript.

Support for Thaweesak Songerm, Rungroj Jun-on, Namdee Sae-Heng, and Noppadol Meemak was provided by Kasetsart University Research and Development Institute, Thailand. Support for Robert G. Webster, Diane Hulse-Post, and Katharine M. Sturm-Ramirez was provided by US Public Health Service grant AI95357 and by the American Lebanese Syrian Associated Charities The American Lebanese Syrian Associated Charities (ALSAC) has been the exclusive fund-raising organization of St. Jude Children's Research Hospital since 1957. ALSAC is the third largest healthcare related charity in the United States. .

Dr Songserm is a veterinary pathologist in the Faculty of Veterinary Medicine, Kasetsart University, Kamphaengsaen Campus, Nakornpathom, Thailand. His research interests include avian pathology, diseases of ducks and geese, and emerging diseases in animals.


(1.) Tang X, Tian Tian
 or T'ien
(Chinese; “Heaven”)

In indigenous Chinese religion, the supreme power reigning over humans and lesser gods. The term refers to a deity, to impersonal nature, or to both.
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(2.) Chen H, Deng G, Li Z, Tian G, Li Y, Jiao jiao   also chiao
n. pl. jiao also chiao
See Table at currency.

[Chinese ji
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(5.) Guan guan: see curassow.  Y, Peiris JSM JSM Journal of Sexual Medicine
JSM Just Shoot Me (sitcom)
JSM Journal of Sport Management
JSM Journal of Software Maintenance
JSM Jabber Session Manager
JSM John Sidney McCain
JSM JEOL Scanning Microscope
, Lipatov AS, Ellis TM, Dyrting KC, Krauss S, et al. Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR (Segmentation And Reassembly) The protocol that converts data to cells for transmission over an ATM network. It is the lower part of the ATM Adaption Layer (AAL), which is responsible for the entire operation. See AAL.

SAR - segmentation and reassembly
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1. a widespread epidemic of a disease.

2. widely epidemic.

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Thaweesak Songserm, * Rungroj Jam-on, * Numdee Sae-Heng, * Noppadol Meemak, ([dagger]) Diane J. Hulse-Post, ([double dagger]) Katharine M. Sturm-Ramirez, ([double dagger]) and Robert G. Webster ([double dagger])

* Kasetsart University, Nakornpathom, Thailand; (dagger]) Western Veterinary Research and Development Center, Rachaburi, Thailand; and ([double dagger]) St. Jude Children's Research Hospital St. Jude Children's Research Hospital, founded in 1962, is a leading pediatric treatment and research facility focused on children's catastrophic diseases. It is located in Memphis, Tennessee.

In 1996, Peter Doherty, Ph.D., of St.
, Memphis, Tennessee, USA

Address for correspondence: Robert G. Webster, St. Jude Children's Research Hospital, Department of Infectious Diseases, Division of Virology virology, study of viruses and their role in disease. Many viruses, such as animal RNA viruses and viruses that infect bacteria, or bacteriophages, have become useful laboratory tools in genetic studies and in work on the cellular metabolic control of gene expression , 332 N Lauderdale, Mailstop 330, Memphis, TN 38105, USA; fax: 901-523-2622; email:
Table 1. Studies of H5N1 influenza in grazing ducks in Thailand,
February to July 2004 *

                                                          Duration of
                                                         virus shedding
                                                          detection of
                    Approximate    Age when positive       illness or
Flock no.            no. ducks     for H5N1 virus (d)     culling (d)

 1 ([dagger])          4,600               66                   8
 2 ([section])         5,200               78                  10
 3 ([dagger])          8,000               42                   5
 4 ([dagger])          6,800               74                   7
 5 ([dagger])          4,300               93                   5
 6 ([paragraph])       7,200               59                   5
 7 ([paragraph])      10,000               82                   7
 8 ([dagger])          6,300               60                   9
 9 ([dagger])          9,800               71                  10
10 ([dagger])          5.500               51                   6

                    Highest viral titer     Antibody titers to H5N1
                       ([log.sub.10]       (HI) ([log.sub.2]) before
Flock no.            EI[D.sub.50]/mL)               culling

 1 ([dagger])               2.0              <1 ([double dagger])
 2 ([section])              3.1                        2
 3 ([dagger])               2.0                       <1
 4 ([dagger])               2.5                        2
 5 ([dagger])               3.3                        2
 6 ([paragraph])            3.6                        2
 7 ([paragraph])            ND                        ND
 8 ([dagger])               3.8                        2
 9 ([dagger])               ND                        ND
10 ([dagger])               3.4                       ND

* EI[D.sub.50], 50% egg infectious dose; HI, hemagglutination
inhibition; ND, not done.

([dagger]) Suphanburi Province.

([double dagger]) Serum samples collected [approximately equal to] 12 d
after flock moved to rice field.

([section]) Nakompathom Province.

([paragraph]) Ayuthdhaya Province.

Table 2. Experimental infection of khaki Campbell ducks with viruses
isolated in Thailand, 2004-2005

Virus *                    Deaths ([dagger])    Illness ([dagger])

A/duck/Thailand/144/05            5/10                 3/10
A/quail/Thailand/551/05           1/10                 2/10
A/Thailand/MK2/04                 2/10                 2/10
A/duck/Thailand/71.1/04          10/10                10/10

                              Day detectable virus was shed ([double

Virus *                      2        4           6          8     10

A/duck/Thailand/144/05     10/10     9/9         1/5        0/5    0/5
A/quail/Thailand/551/05     8/10     8/10        1/9        0/9    0/9
A/Thailand/MK2/04           9/10    10/10        6/8        2/8    2/8
A/duck/Thailand/71.1/04    10/10     1/1         --         --     --

* Eight 4-week-old khaki Campbell ducks were injected with [10.sup.6]
50% egg infectious dose of virus by intranasal and intratracheal
infection, and 2 contact ducks were introduced 1 day later.

([dagger]) Total number of deaths or birds showing disease/total number
of birds. Birds were observed daily for signs of infection or death.

([double dagger]) Number of ducks shedding by the trachea or
cloacae/total number of ducks remaining alive. Ducks were swabbed every
other day beginning on day 2 postinfection.

([section]) All of the ducks in this group died.
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Author:Webster, Robert G.
Publication:Emerging Infectious Diseases
Geographic Code:9THAI
Date:Apr 1, 2006
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