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JAMA. 2003;290:2793-2796.

MMWR. 2003;52:1017-1019

1 table omitted

In 2002, Wisconsin public health officials were notified of two cases of febrile illness in workers at a commercial turkey breeder farm (farm A) in county A. The Wisconsin Division of Public Health (WDPH) initiated an investigation that found a high prevalence of West Nile virus (WNV) antibody among farm A workers and turkeys. An associated high incidence of febrile illness among farm A workers also was observed. This report summarizes the results of this investigation, which indicate possible nonmosquito transmission among birds and subsequent infection of humans at farm A. Because the mode of transmission in this outbreak is unknown, turkey handlers should take appropriate precautions, including use of DEET containing mosquito repellents, protective clothing and gloves, respiratory protection, and proper hand hygiene. Suspected occupationally acquired WNV infections should be reported immediately to local and state health departments.

During November 2002, WDPH and the Wisconsin State Laboratory of Hygiene (WSLH) confirmed that two ill residents of county A had been infected with WNV. Before these reports, only one human WNV infection had been reported in this county. Both persons worked at farm A and had febrile illness with rash during late September-early October. These human illnesses occurred after a suspected fowl pox outbreak among farm A turkeys in September. Workers were concerned the pox outbreak might be associated with their illnesses.

Farm A is one of six turkey breeder farms in county A owned by a company that also operates nonbreeder farms and a turkey meat processing plant in county A. The five other turkey breeder farms are located within 10 miles of farm A, and multiple private residences are within a quarter mile. In February 2003, county and state public health staff, in collaboration with the company, identified workers at the six turkey breeder farms, the nonbreeder farms, and the plant, and requested their consent to participate in a serosurvey. Serum samples were collected from participating workers (N = 93) to identify persons infected recently. A questionnaire was administered to identify persons who had a febrile illness during August-October 2002. Serum samples also were collected from residents (N = 14) who lived within a quarter mile of farm A. All serum samples were tested for WNV-specific IgM antibody at WSLH.¹ IgM-positive specimens were confirmed by plaque-reduction neutralization tests at CDC.² Of 107 total participants, 10 (9%) were seropositive. Of approximately 90 workers at the six breeder farms, 57 (63%) participated; of these, 10 (18%) were infected recently with WNV. None of the meat processing workers or other area residents was infected. Of 11 persons who worked exclusively at farm A, six (55%) were WNV IgM-positive, compared with two (25%) of eight who worked at both farm A and other breeder farms and two (5%) of 38 who worked only at other breeder farms. Of the 10 IgM-positive workers, six (60%) reported febrile headaches during August-October (all occurring during the last week of September), compared with seven (7%) of 97 IgM-negative persons sampled (p = 0.0002 by Fisher exact test). All six IgM-positive persons who reported febrile headache had worked at farm A. All six noted a skin rash, and one had meningoencephalitis and was hospitalized; no deaths occurred. Reported mosquito exposures and bites were similar for IgM-positive (nine [90%] and eight [80%] of 10, respectively) and IgM-negative workers (67 [85%] and 54 [68%] of 79, respectively). Only one (2%) of 57 breeder farm workers reported using insect repellent while working.

Farm A includes two breeder bird barns and a juvenile flock barn. The breeder barns separate uncaged females from male turkeys with a solid plywood wall. The sides of the barns housing the female turkeys are covered with 1 in. x 1 in. mesh wire fencing and plastic curtains that can be adjusted to lower the temperature during warm months.

Serum from farm A turkeys and turkeys from the nearest breeder farm were collected in late January 2003. The farm A flock sampled was the group of birds housed in the juvenile flock barn from mid-June to early December 2002, at which time this flock was moved to a breeder barn on farm A to replace a flock slaughtered in November. The flock sampled on the nearby farm was a breeder flock also in place in September. Both flocks had suspected fowl pox outbreaks during September. Serum samples were submitted to the U.S. Department of Agriculture's National Veterinary Services Laboratories for WNV-neutralizing antibody testing. Of 135 farm A female turkeys, 130 (96%) had WNV-neutralizing antibody (measured at two dilutions, 1:10 and 1:100, and considered to be positive if a given dilution neutralized 90% of virus growth). No WNV-neutralizing antibody was found in 135 female turkeys tested from the nearby farm or 30 male turkeys tested from either farm.

Reported by:

LC Glaser, DVM, MV Wegner, MD, JP Davis, MD, Div of Public Health, State of Wisconsin Dept of Health and Family Svcs. ML Bunning, DVM, AA Marfin, MD, GL Campbell, MD, Div of Vector-Borne Infectious Diseases, National Center for Infectious Diseases; B Bernard, MD, SW Lenhart, MSPH, Div of Surveillance, Hazard Evaluations, and Field Studies, National Institute for Occupational Safety and Health; MJ Sotir, PhD, EIS Officer, CDC.

CDC Editorial Note:

The investigation described in this report found that workers at farm A had a higher incidence of febrile illness and prevalence of WNV antibodies than workers at other breeder and nonbreeder farms, workers at a turkey meat processing facility, or persons who lived on or near the affected farm and who did not work in the turkey barns. The mode of transmission to these workers is unknown. Although the majority of human WNV infections are mosquito-borne, transmission by less typical routes might have occurred, including percutaneous (e.g., exposure of broken skin or mucosa to infected turkey feces or serous exudates from dually-infected pox lesions), fecal-oral, or respiratory (e.g., exposure to aerosolized infected turkey feces).

The WNV seroprevalence (96%) among female turkeys on farm A was high. However, experimental evidence suggests that turkeys develop insufficient levels of WNV viremia to contribute to a bird-mosquito-bird amplification cycle.³ Although WNV was detected in the feces of these turkeys, no oropharyngeal shedding or transmission to cage mates was observed.³ Nonvector-borne WNV transmission has been demonstrated experimentally among rodents and among certain bird species other than turkeys.^4-5 Once WNV was introduced to female turkeys at farm A (presumably by mosquitoes), widespread transmission within that flock might have taken place by fecal-oral, respiratory, or another atypical (e.g., percutaneous exposure associated with pecking behavior or vaccination) route. In addition, other unique conditions at farm A, including possible co-infection with an avian pox virus, might have resulted in higher WNV viremias or infectious materials with higher WNV titers than laboratory studies have suggested.

Despite uncertainty over the mode(s) of transmission, epidemiologic evidence suggests that this outbreak was related to occupational exposure. Occupationally acquired WNV infections have been reported previously among laboratory or field workers who experienced a known percutaneous injury or aerosol exposure while working with high concentrations of WNV in cell culture or infected animal tissues.^6-9 In this investigation, no such exposure was documented. Because the mode of transmission in this outbreak is unknown, turkey handlers should (1) take personal protective measures, including wearing protective clothing and using mosquito repellents (e.g., those containing DEET on skin and clothing and those containing permethrin on clothing), as recommended for outdoor workers; (2) wear gloves; and (3) wash hands frequently. In addition, respiratory protection has been recommended for reducing other exposures to workers in turkey barns.¹⁰ Respiratory protection should be selected and used in accordance with the Occupational Safety and Health Administration (OSHA) respiratory protection standard (Title 29 CFR 1910.134).

Workers should receive training that reinforces awareness of potential occupational hazards and risks and stresses the importance of timely reporting of all injuries and illnesses of suspected occupational origin. Health-care workers should inquire about a patient's outdoor exposure and occupation when a human WNV infection is suspected or identified and consider WNV as a possible etiology among turkey farm workers with febrile headache or rash, meningitis, encephalitis, or other severe neurologic illness, especially when WNV illnesses exist among co-workers or birds. Suspected occupationally acquired WNV infections should be reported immediately to local and state health departments.

The investigation of turkey breeder farm workers in county A is ongoing. In addition, further studies are needed to determine the factors involved in this outbreak, to better define the occupational risk for WNV infections, and to assess appropriate personal protective measures. On the basis of recommendations from public health staff, the company has made mosquito repellent containing 30% DEET available at farm A and other turkey breeder farms. Recommendations that were outlined previously in place at the company farms include protective clothing, frequent hand washing, and an OSHA-required respiratory protection program. Gloves and safety glasses also are available to workers.

Acknowledgments

The data in this report are based on contributions by the local health department and company in county A; M Doering, Wisconsin State Laboratory of Hygiene. National Veterinary Svcs Laboratories, Animal and Plant Health Inspection Svc; Agriculture Research Svc; U.S. Dept of Agriculture. S Montgomery, DVM, N Komar, PhD, D O'Leary, DVM, P Schneider; laboratory staff; Div of Vector-Borne Infectious Diseases, National Center for Infectious Diseases, CDC.

REFERENCES

1. Martin DA, Muth DA, Brown T, Johnson AJ, Karabatsos N, Roehrig JT. Standardization of immunoglobulin M capture enzyme-linked immunosorbent assays for routine diagnosis of arboviral infections. J Clin Microbiol. 2000;38:1823-36. FREE FULL TEXT 2. Beaty BJ, Calisher CH, Shope RE. Arboviruses. In: Lennette EH, Lennette DA, Lennette ET, eds. Diagnostic Procedures for Viral, Rickettsial, and Chlamydial Infections, 7th ed. Washington, DC: American Public Health Association, 1995. 3. Swayne DE, Beck JR, Zaki S. Pathogenicity of West Nile virus for turkeys. Avian Diseases. 2000;44:932-7. FULL TEXT | ISI | PUBMED 4. Odelola HA, Oduye O. West Nile virus infection of adult mice by oral route. Archives of Virology. 1977;54:251-3. ISI | PUBMED 5. Komar N, Langevin S, Hinten S, et al. Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis. 2003;9:311-22. ISI | PUBMED 6. Pike RM. Laboratory-associated infections: summary and analysis of 3,921 cases. Health Laboratory Science. 1976;13:105-14. ISI | PUBMED 7. Sewell DL. Laboratory-associated infections and biosafety. Clin Microbiol Rev. 1995;8:389-405. ABSTRACT 8. Nir YD. Airborne West Nile virus infection. Am J Trop Med Hyg. 1959;8:537-9. FREE FULL TEXT 9. CDC. Laboratory-acquired West Nile virus infection—United States, 2002. MMWR. 2002;51:1133-5. PUBMED 10. Reynolds SJ, Parker D, Vesley D, Janni K, McJilton C. Occupational exposure to organic dusts and gases in the turkey growing industry. Appl Occup Environ Hyg. 1994;9:493-502.

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