Prevalence of Antibodies to Coxiella burnetii in Japan

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Dec 21, 1992 - Coxiella burnetii has been shown to cause human Q fever, a disease .... serological study of Rocky mountain spotted fever and typhus. J. Clin.
Vol. 31, No. 3

JOURNAL OF CLINICAL MICROBIOLOGY, Mar. 1993, p. 722-723 0095-1137/93/030722-02$02.00/0

Copyright © 1993, American Society for Microbiology

Prevalence of Antibodies to Coxiella burnetii in Japan KHIN KHIN HTWE,1 TETSUYA YOSHIDA,' SEIZO HAYASHI,' TAKASHI MIYAKE,2 KEN-ICHI AMANO,3 CHIHARU MORITA,4 TSUYOSHI YAMAGUCHI,' HIDETO FUKUSHI,1 AND KATSUYA HIRAIl* Department of Veterinary Microbiology, Gifu University, Gifu, 1 Department of Virology, Aichi Prefectural Institute of Public Health, Nagoya,2 Central Research Laboratory, Akita University, Akita, and Department of Veterinary Public Health, Rakuno Gakuen University, Hokkaido,4 Japan Received 13 July 1992/Accepted 21 December 1992 We evaluated the prevalence of CoxieUla burnetii antibodies in 626 human serum samples (275 from veterinarians, 107 from meat-processing workers, 184 from respiratory-disorder patients, and 60 from healthy humans) by the indirect immunofluorescence test. Of the serum samples examined, 54 (8.6%) and 103 (16.5%) reacted positively to phase I and II antigens, respectively, of C. burnetii. The rates differed for healthy humans and respiratory-disorder patients. Antibody prevalence was high for healthy humans living in close contact with animals (e.g., veterinarians and meat-processing workers). Coxiella burnetii has been shown to cause human Q fever, disease whose symptoms include pneumonia, hepatitis, and endocarditis. The major reservoir of human infection arises through contact with infected ruminant livestock and their contaminated products (4). Most recently, endemic infection due to C. burnetii was reported (9). Serologic studies indicate the worldwide distribution of C. burnetii, and endemic Q fever in humans has been reported from several areas (1, 5, 7). In Japan, Kitaoka has reported complement fixation antibodies to C. bumetii (i.e., Q fever antibodies) in 22 of 901 (2.4%) slaughterhouse workers in 1952 (3). In the following 40 years, serological surveys of Q fever in humans and various animals were not carried out in Japan. Most recently, Yoshiie et al. have reported indirect immunofluorescence (IF) antibodies to C. burnetii in 96 of 329 (29.0%) dairy cattle (10). In a previous study, we found Q fever antibodies in 262 of 562 (46.6%) dairy cattle, 72 of 256 (28.1%) sheep, 20 of 85 (23.5%) goats, and 95 of 632 (15.0%) dogs (2). This report describes the prevalence of Q fever antibodies in humans in Japan. A total of 626 serum samples were collected from 1978 to 1991 from healthy veterinarians and meat-processing workers (MPW) in three prefectures. Sera from respiratorydisorder patients (RDP) were collected from university hospitals in two prefectures. Serum samples from 60 healthy individuals served as controls. Follow-up serum samples were not obtained from the individuals. The prevalence of antibodies to C. burnetii was determined by IF test by the method of Philip et al. (8). Twofold serum dilutions in phosphate-buffered saline (pH 7.2) from 1:16 to 1:4,096 were tested against fixed and purified antigens of Nine Mile phase I and II strains of C. burnetii. A fluorescein isothiocyanate polyvalent conjugate to goat anti-human immunoglobulin G (IgG) (heavy and light chains) (Organon Teknika N-V. Cappel Products) was used for the determination of antibodies. Positive serum samples were further examined with monovalent fluorescein isothiocyanate goat anti-human IgG and IgM (Tago, Inc., Burlingame, Calif.) and IgA (Cappel Laboratories, Cochranville, Pa.) conjugates. Titers of 1:16 or higher were considered positive. A positive and negative control was run with each test. a

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Corresponding author. 722

The distribution of antibodies to C. bumetii is shown in Table 1. The overall seroprevalence rates of C. burnetii antibodies were 54 (8.6%) and 103 (16.5%) of 626 sera for phase I and II antigens, respectively. In veterinarians, 36 (13.0%) and 62 (22.5%) of 275 serum samples were found to have Q fever antibodies to phase I and II antigens, respectively. Two of the 36 individuals with the antibody to phase I antigen had no antibody to phase II antigen, while 28 of the 62 individuals with the antibody to phase II antigen had no antibody to phase I antigen. In the MPW, 8 (7.5%) and 12 (11.2%) of 107 serum samples were found to have Q fever antibodies to phase I and II antigens, respectively. One of the 8 individuals with antibody to phase I antigen had no antibody to phase II antigen, while 5 of the 12 individuals with antibody to phase II antigen had no antibody to phase I antigen. Among veterinarians and MPW, many serum samples were positive at the higher-titer levels of 1:256. In addition, some positive sera from veterinarians and MPW exhibited specific IgG and IgM antibody titers higher than 1:256 to both phase I and II antigens. In RDP, 9 (4.9%) and 28 (15.2%) of 184 serum samples were positive for phase I and II antigens, respectively. One of the 9 individuals with antibody to phase I antigen had no antibody to phase II antigen, while 26 of the 28 individuals with antibody to phase II antigen had no antibody to phase I antigen. Some positive sera of RDP had high titers (over 1:256) to phase II antigen and low titers (1:32) to phase I antigen for IgG and IgM antibodies. One of 60 healthy controls had IgG and IgM antibody titers of 1:32 to phase I and II antigens, respectively. The overall seroprevalence was high for phase II antigen but low for phase I antigen. Among healthy individuals associated with animals and animal products, C. bumetii antibodies seem rather common in Japan, as in other countries. Seropositivity to C. burnetii has been variously reported to be 4.2 to 15.9% in Canada, 0.6 to 9.4% in Central American countries, 3.1 to 6.3% in European countries (5), 2.0% in the United Kingdom (7), and 4 to 17% in the United States (1). Antibodies to C. burnetii were 64% in veterinarians and 35% in slaughterhouse workers from Canada (6), 40% in MPW from the United States (1), 20 to 30% in veterinarians and abattoir workers from the United Kingdom (7), and 25.7% in veterinarians from Switzerland (5). In the data we present here, the positive rates for veterinarians, MPW, and RDP were higher than those for

VOL. 31, 1993

NOTES

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TABLE 1. Prevalence of IF antibodies to phase I and II antigens of C. bumetii in human sera in Japan No. of positive antibody responses to C. bumetii antigena

Origin of serum

Yr

No. of sam

Veterinarians MPW RDP Healthy humans Total

1978-1991 1985 1982-1990 1990

Phase II

Phase I

ples

___

Poly

IgG

IgM

IgA

Poly

IgG

IgM

IgA

275 107 184 60

36 8 9 1

26 6 4 1

11 2 6 1

4 1 0 0

62 12 28 1

48 8 12 1

17 4 15 1

11 2 2 0

626

54

37

20

5

103

69

37

15

a Samples for which titers were 1:16 or higher were considered positive. Poly, polyvalent antibodies (heavy and light chains).

healthy controls. Thus, there is no doubt that Q fever poses an occupational hazard to humans living in close contact with animals. Our serologic data show that C. bumnetii infection occurs in Japan often subclinically, but also that clinical Q fever is not uncommon in humans, and specific tests should be included in the serodiagnostic routine of the RDP complex so that when C. burnetii is detected, the best possible and sustained treatment can be administered to the patient. We are continuing epidemiologic surveillance of Q fever infection and isolation of this organism to confirm the antibody study. We are deeply indebted to J. C. Williams (United States), M. G. Peacock (United States), 0. Peter (Switzerland), and G. H. Lang (Canada) for invaluable help in providing the purified antigens and control serum samples. REFERENCES 1. Behymer, D., and H. P. Riemann. 1989. Zoonosis update, Coxiella burnetii infection. J. Am. Vet. Med. Assoc. 194:764767. 2. Htwe, K. K., K. Amano, Y. Sugiyama, K. Yagami, N. Minamoto, A. Hashimoto, T. Yamaguchi, H. Fukushi, and K. Hirai. 1992. Seroepidemiology of Coxiella burnetii in domestic and companion animals in Japan. Vet. Rec. 131:490.

3. Kitaoka, M. 1954. Q fever. J. Public Health 15:67-73. (In Japanese.) 4. Lang, G. H. 1990. Coxiellosis (Q Fever) in animals, p. 23-48. In T. J. Marrie (ed.), Q fever. The disease, vol. 1. CRC Press, Boca Raton, Fla. 5. Marre, T. J. 1990. Epidemiology of Q fever, p. 49-69. In T. J. Marrie (ed.), Q fever. The disease, vol. 1. CRC Press, Boca Raton, Fla. 6. Marrie, T. J., and J. Fraser. 1985. Prevalence of antibodies to Coxiella bumetii among veterinarians and slaughterhouse workers in Nova Scotia. Can. Vet. J. 26:181-184. 7. Moffat, M. A. J. 1990. Zoonotic implications of Q fever and chlamydial infections in animals and man. Part 1-Q fever. Ir. Vet. J. 43:115-117. 8. Philip, R. N., E. A. Casper, R. A. Ormsbee, M. G. Peacock, and W. Burgdorfer. 1976. Microimmuno-fluorescence test for the serological study of Rocky mountain spotted fever and typhus. J. Clin. Microbiol. 3:51-56. 9. Pinsky, R. L., D. B. Fishbein, C. R. Greene, and K. F. Gensheimer. 1991. An outbreak of cat-associated Q fever in the United States. J. Infect. Dis. 164:202-204. 10. Yoshiie, K., H. Oda, and S. Matayoshi. 1991. Serological evidence that the Q fever agent Coxiella bumetii has spread widely among dairy cattle of Japan. Microbiol. Immunol. 35:577-581.