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Low frequency of infection with avian influenza virus (H5N1) among poultry farmers, Thailand, 2004.

In Thai provinces where avian influenza avian influenza: see influenza.  outbreaks in poultry had been confirmed in the preceding 6 months, serum from 322 poultry farmers was tested for antibodies to avian influenza virus subtype (programming) subtype - If S is a subtype of T then an expression of type S may be used anywhere that one of type T can and an implicit type conversion will be applied to convert it to type T.  H5N1 by microneutralization assay. No study participant met the World Health Organization 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.

 criteria for confirmed infection.


During late 2003 and 2004, highly pathogenic avian influenza virus (H5N1) caused extensive outbreaks and die-offs in poultry flocks in Thailand and several other countries in Southeast Asia Southeast Asia, region of Asia (1990 est. pop. 442,500,000), c.1,740,000 sq mi (4,506,600 sq km), bounded roughly by the Indian subcontinent on the west, China on the north, and the Pacific Ocean on the east.  (1). From January through March 2004, 12 cases, 8 fatal, in humans resulted from infection with 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.
 (H5N1) in Thailand (2). In response, the Thailand Department of Livestock Development enlisted government employees to conduct a large-scale cull cull

the act of culling. Called also cast.
 of poultry in the affected provinces (www.dld. This effort began on January 23, 2004, and resulted in the slaughter of >21 million birds ( diseases-cards/avian_bg.html). Poultry farmers and persons involved in culling culling

removal of inferior animals from a group of breeding stock. The removal is premature, i.e. before completion of its life span, disposal of an animal from a herd or other group.
 are at increased risk for infection (3). In May 2004, we conducted a seroepidemiologic investigation of Thai poultry farmers to determine the frequency of avian influenza (H5N1) transmission to humans.

The Study

We conducted a cross-sectional study cross-sectional study
See synchronic study.

cross-sectional study,
n the scientific method for the analysis of data gathered from two or more samples at one point in time.
 among poultry farmers and cullers from 1 district in each of the 5 provinces (Chachoengsao, Kanchanaburi, Khon Kaen This article is about the town Khon Kaen. For other uses, see Khon Kaen (disambiguation).

Located at the heart of the Northeastern Thailand (Isan), Khon Kaen
, Sukhothai, and Suphanburi) where outbreaks of avian influenza (H5N1) among poultry and human infections had been confirmed since January 2004 (Figure). With the assistance of provincial human and animal health authorities, we contacted farmers living in these districts. Informed consent was obtained, and a brief interview was conducted. Because the precise timing of potential exposures could not be determined, a single serum sample was collected from each patient and stored at -20[degrees]C until tested under Bio-safety Level 3 (BSL-3) conditions. Specimens were tested, according to adapted methods described by Katz et al. (4), at the Department of Microbiology, Faculty of Medicine, Siriraj Hospital, Mahidol University by Microneutralization assay (micro-Nt) for antibody to H5N1 viruses. Before this study, senior laboratory staff from Siriraj Hospital received 2 weeks of on-site training by a visiting scientist from the US Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center.  who had expertise with this assay. The World Health Organization (WHO) defines a positive test result as a microneutralization antibody titer antibody titer The amount of a specific antibody present in the serum, usually as a result of an acquired infection; titers for IgM usually rise abruptly at the time of infection–acute phase and fall slowly; during the 'convalescent' phase, IgG ↑ and is  for influenza virus (H5N1) of >80 with a confirmatory ELISA ELISA (e-li´sah) Enzyme-Linked Immuno-Sorbent Assay; any enzyme immunoassay using an enzyme-labeled immunoreactant and an immunosorbent.

 or Western blot Western blot
A technique developed in 1979 that is used to confirm ELISA results. HIV antigen is purified by electrophoresis and attached by blotting to a nylon or nitrocellulose filter.
 assay (3,4) (www. definition2006_08_29/en/index.html). Serum samples from persons >50 years of age were excluded from laboratory analysis because the microneutralization assay for antibodies against subtype H5N1 has been reported to be less specific for older persons (5).


Of 350 farmers asked to participate, 322 (92%) enrolled in the study, of which 167 (52%) were women, and 28 (8%) persons declined to participate. The mean age of participants was 34 years (range 5-50 years) (Table). Among participants, 188 (58%) reported handling sick or dying poultry, 107 (33%) were involved in culling operations of apparently well poultry in outbreak areas, and 27 (9%) reported only contact with well poultry in the context of routine farming practices. Although no study participant had an anti-H5N1 antibody titer of [greater than or equal to] 80, 7 (2.2%) farmers had lower reactive antibody titers. Of these, 4 had titers of 10, 2 had titers of 20, and 1 had a titer titer /ti·ter/ (ti´ter) the quantity of a substance required to react with or to correspond to a given amount of another substance.  of 40. The small number of study participants with anti-H5 antibody titers precluded statistical comparisons to those without reactive antibodies.


Poultry farmers and cullers are at increased occupational risk for exposure to avian influenza viruses. However, since 2004, infections have been less commonly reported in cullers, while poultry farmers have made up a large proportion of cases worldwide. A study in Hong Kong Special Administrative Region A special administrative region may be:
People's Republic of China
  • Special administrative regions, present-day administrative divisions (as of 2006) set up by the People's Republic of China to administer Hong Kong (since 1997) and Macau (since 1999)
, People's Republic of China, examined influenza virus (H5N1) transmission and risk factors among poultry workers and government workers involved in culling during the 1997-98 outbreak (3). The study concluded that although no hospitalized poultry workers were identified among the 18 patients in that outbreak, 3% of 293 cullers and 10% of 1,525 poultry workers had antibody titers against influenza (H5N1) of [greater than or equal to] 80, which suggested that a substantial number of mild or asymptomatic infections had occurred in this occupationally exposed population. In contrast, we found that no poultry workers had microneutralization titers [greater than or equal to] 80, whereas 7 (2%) had lower titers that did not meet the WHO definition for seropositivity Seropositivity is the presence of a certain antibody in a blood sample. A patient with seropositivity for a particular antigen or agent is termed seropositive. .

These findings could have several possible explanations. The lower titers may have resulted from cross-reactivity with circulating antibodies after previous human influenza virus infections (5,6). These low titers could be the result of mild or asymptomatic influenza (H5N1) infections because not all influenza virus infections invariably in·var·i·a·ble  
Not changing or subject to change; constant.

 result in marked antibody responses (7). Likewise, these results could reflect the decay of antibody titers over time (8). Finally, the Micro-NT assay is a highly specific and strain-sensitive test. Although we used the same virus that was circulating in Thailand at that time, these lower titers could be attributable to infections with another virus variant.

Most human influenza (H5N1) infections have occurred in persons who had had direct contact with sick or dying poultry (9-11). While human infections with avian influenza (H5N1) continue to be reported to be spoken of; to be mentioned, whether favorably or unfavorably.

See also: Report
, growing evidence indicates that this virus is not easily transmitted from poultry to humans and that mild or asymptomatic infections in humans are not common. A seroepidemiologic investigation in rural Cambodia surveyed 351 participants from 93 households in an area where influenza (H5N1) infections in poultry and a single fatal human case had been documented (10). Despite frequent, direct contact with poultry suspected of having influenza (H5N1) infection, none of the Cambodian study participants had antibodies reactive to this subtype. A similar study in Nigeria found that all of 295 poultry workers had negative test results for influenza (H5N1) neutralizing antibodies (12). Studies of healthcare workers suggest that transmission of influenza virus (H5N1) to hospital staff who cared for infected patients also appears to be uncommon (13-15).

Our study provides additional evidence to suggest that influenza virus (H5N1) is not easily transmitted to humans. However, the wide geographic distribution of this subtype, ubiquitous exposures, and the high case-fatality ratio case-fatality ratio Epidemiology A value calculated as 100 cases of a disease 'X', divided by the number of persons with the disease who died in a given period of time; the resulting ratio is equal to the rate of a disease's occurrence. See Cause-fatality ratio.  from the infection underscore the importance of adherence to poultry-handling practices recommended by the Food and Agriculture Organization and WHO (www. BAF British Athletics Federation 7-13E7-42DBB DBB Deutscher Beamtenbund (German: National Union of Civil Servants)
DBB Dynamic Bass Boost
DBB Double Block & Bleed (valve)
DBB Design Bid Build
DBB Digital Baseband
DBB DescentBB
92B-004CF5D517E7/0/ WHOinterimrecommendation 26012004.pdf, diseases-cards/avian_qa.html#8). Molecular surveillance indicates that the avian influenza virus (H5N1) continues to evolve rapidly ( guidelines/recommendationvaccine.pdf). Additional seroepidemiologic studies are warranted to monitor for changes in transmissibility trans·mis·si·ble  
That can be transmitted: transmissible signals.

 and the spectrum of clinical illness.


We thank the following for their valuable assistance during this study: the staff of Chachoengsao, Kanchanaburi, Khon Kaen, Sukhothai and Suphanburi Provincial Health Office; the staff of Communicable Disease communicable disease
A disease that is transmitted through direct contact with an infected individual or indirectly through a vector. Also called contagious disease.
 Section, Surveillance and Investigation Section (Bureau of Epidemiology, Department of Disease Control); the International Emerging Infectious Program (Thailand MOPH-US CDC See Control Data, century date change and Back Orifice.

CDC - Control Data Corporation
 Collaboration); and Robert Gibbons, Preecha Prempre, Rungnapa Prasantong, Pravit Choomkasien, and Prasert Thongcharoen.

This study was supported by the Department of Disease Control, Thailand Ministry of Public Health.


(1.) Tiensin T, Chaitaweesub P, Songserm T, Chaisingh A, Hoonsuwan W, Buranathai C, et al. Highly pathogenic avian influenza H5N1, Thailand, 2004. Emerg Infect Dis. 2005;11:1664-72.

(2.) Ungchusak K, Auewarakul P, Dowell SF, Kitphati R, Auwanit W, Puthavathana P, et al. Probable person-to-person transmission of avian influenza A (H5N1). N Engl J Med. 2005;352:333-40.

(3.) Bridges CB, Lim W, Hu-Primmer J, Sims L, Fukuda K, Mak KH et al. Risk of influenza A influenza A
Influenza caused by infection with a strain of influenza virus type A.

influenza A Infectious disease An avian virus, especially of ducks–which in China live near the pig reservoir and 'vector';
 (H5N1) infection among poultry workers, Hong Kong, 1997-1998. J Infect Dis. 2002;185:1005-10.

(4.) Katz JM, Lim W, Bridges CB, Rowe T, Hu-Primmer J, Lu X, et al. Antibody response in individuals infected with avian influenza A (H5N1) viruses and detection of anti-H5 antibody among household and social contacts. J Infect Dis. 1999; 180:1763-70.

(5.) Rowe T, Abernathy RA, Hu-Primmer J, Thompson WW, Lu X, Lim W, et al. Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J Clin Microbiol. 1999;37:937-43.

(6.) Couch RB. An overview of serum antibody responses to influenza virus antigens. Dev Biol (Basel). 2003;115:25-30.

(7.) Fox JP, Hall CE, Cooney MK, Foy HM. Influenzavirus infections in Seattle families, 1975-1979. I. Study design, methods and the occurrence of infections by time and age. Am J Epidemiol. 1982;116: 212-27.

(8.) Gerhard W. The role of the antibody response in influenza virus infection. Curt Top Microbiol Immunol. 2001;260:171-90.

(9.) Dinh PN, Long HT, Tien NT, Hien NT, Mai le TQ, Phong le H, et al. Risk factors for human infection with avian influenza A H5N1, Vietnam, 2004. Emerg Infect Dis. 2006;12:1841-7.

(10.) Vong S, Coghlan B, Mardy S, Holl D, Seng H, Ly S, et al. Low frequency of poultry-to-human H5NI virus transmission, southern Cambodia, 2005. Emerg Infect Dis. 2006;12:1542-7.

(11.) Investigation of avian influenza (H5N1) outbreak in humans--Thailand, 2004. MMWR MMWR Morbidity & Mortality Weekly Report Epidemiology A news bulletin published by the CDC, which provides epidemiologic data–eg, statistics on the incidence of AIDS, rabies, rubella, STDs and other communicable diseases, causes of mortality–eg,  Morb Mortal Wkly Rep. 2006;55(Suppl 1): 3-6.

(12.) Ortiz JR, Katz MA, Mahmoud MN, Ahmed S, Bawa SI, Farnon EC, et al. H5N1 poultry worker serosurvey, Nigeria, 2006. J Infect Dis. 2007:196; 1685-91.

(13.) Apisarnthanarak A, Erb S, Stephenson I, Katz JM, Chittaganpitch M, Sangkitporu S, et al. Seroprevalence seroprevalence Immunology The proportion of a population that is seropositive–ie, has been exposed to a particular pathogen or immunogen; the seropositivity of a population is calculated as the number of individuals who produce a particular antibody divided  of anti-H5 antibody among Thai health care workers after exposure to avian influenza (H5N1) in a tertiary care center tertiary care center Hospital care A hospital or medical center for Pts often referred from secondary care centers, which provides subspecialty expertise

Tertiary care center  

. Clin Infect Dis. 2005;40:e16-8.

(14.) Schultsz C, Dong VC, Chau NV, Le NT, Lim W, Thanh TT, et al. Avian influenza H5N1 and healthcare workers. Emerg Infect Dis. 2005;11:1158-9.

(15.) Liem NT, Lim W; World Health Organization International Avian Influenza Investigation Team, Vietnam. Lack of H5N1 avian influenza transmission to hospital employees, Hanoi, 2004. Emerg Infect Dis. 2005;11:210-5.

Address for correspondence: James M. Simmerman, International Emerging Infections Program, Thailand MOPH-US CDC Collaboration, DDC See VESA DDC.  Building 7, 4th Floor, Thailand MOPH MOPH Ministry of Public Health
MOPH Military Order of the Purple Heart
, Nonthaburi, Thailand 11000; email:

Soawapak Hinjoy, * Pilaipan Puthavathana, ([dagger]) Yongjua Laosiritaworn, * Khanchit Limpakarnjanarat, ([double dagger]) Phisanu Pooruk, ([dagger]) Teerasak Chuxnum, * James M. Simmerman, ([double dagger]) and Kumnuan Ungchusak *

* Ministry of Public Health, Nonthaburi, Thailand; ([dagger]) Mahidol University, Bangkok, Thailand; and ([double dagger]) Global Disease Detection/International Emerging Infections Program, Nonthaburi, Thailand

Dr Hinjoy is a veterinarian veterinarian /vet·er·i·nar·i·an/ (vet?er-i-nar´e-an) a person trained and authorized to practice veterinary medicine and surgery; a doctor of veterinary medicine.

 and epidemiologist at the Bureau of Epidemiology, Thailand Ministry of Public Health. She was extensively involved in the case investigations and control efforts for avian influenza outbreaks in Thailand during 2004-2006.
Table. Characteristics of 322 persons living on poultry farm in
areas where avian influenza (H5N1) infections among poultry
and humans had been confirmed since January 2004, Thailand

Variable                                No. persons (%)

  Chachoengsao                             61 (18.9)
  Kanchanaburi                              32 (9.9)
  Khon Kaen                                65 (20.2)
  Sukhothai                                84 (26.1)
  Suphanburi                               80 (24.8)

  M                                        155 (48.1)
  F                                        167 (51.9)

Age, y *
[less than or equal to] 10                  15 (4.7)
  11-20                                     32 (9.9)
  21-30                                    49 (15.2)
  31-40                                    121 (37.6)
  41-50                                    105 (32.6)

Current smokers                            67 (20.8)
Chronic illness                            74 (23.0)

Type of poultry maintained
  Layer hen                                111 (34.5)
  Broiler                                  42 (13.0)
  Fighting cock                            88 (27.3)
  Backyard chicken                         89 (27.6)
  Egg-laying duck                           7 (2.2)
  Meat duck                                 8 (2.5)
  Ornamental birds                          3 (0.9)

Type of poultry farm
  Company farm                             125 (38.8)
  Individual farm (backyard)               197 (61.2)

Observed increased deaths of poultry       231 (71.7)
Living on a mixed swine/poultry farm        24 (7.5)

* Age range 5-50 y; median 35 y.

([dagger]) Not mutually exclusive.
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Title Annotation:DISPATCHES
Author:Hinjoy, Soawapak; Puthavathana, Pilaipan; Laosiritaworn, Yongjua; Limpakarnjanarat, Khanchit; Pooruk
Publication:Emerging Infectious Diseases
Geographic Code:9THAI
Date:Mar 1, 2008
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