Am. J. Trop. Med. Hyg., 75(2), 2006, pp. 315-317
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene
THE SEROLOGIC PREVALENCE OF Q FEVER (COXIELLA BURNETII) COMPLEMENT-FIXING ANTIBODIES IN THE PENINSULAR BIGHORN SHEEP OF SOUTHERN CALIFORNIA
JAMES R. DEFORGE AND
LAWRENCE A. CONE*
Bighorn Institute, Palm Desert, CA; Eisenhower Medical Center, Rancho Mirage, CA
 |
ABSTRACT
|
Q fever is a rare illness in the Southern California desert. During the past 34 years only 6 patients have been diagnosed with the disease at the Eisenhower Medical Center, a referral center for much of the desert and surrounding mountains. In all but 2 instances, Q fever was identified in patients who have been in contact with imported domestic sheep who are brought to the desert to graze and lamb in the fall and winter. The sheep are sent back to Idaho, Wyoming, and Montana in the spring. With frequent infection by Coxiella burnetii established in domestic sheep, we elected to study the prevalence of complement fixing antibodies to Coxiella burnetii in native bighorn sheep who reside in the lower levels of the mountains surrounding the desert. From 1992 to 1999, of 268 serum samples drawn from male and female lambs and adult sheep, 27 tested positive (10%), which is strikingly low when compared with Dall sheep in Alaska (12 of 15), kangaroos, wild rabbits, and brown rats. Because changes have been made in Peninsular bighorn sheep habitat since the animals were listed as endangered in 1998, further follow-up in Q fever serology testing will be of interest.
|
INTRODUCTION
|
Q (query) fever was initially described by Derrick1 in Brisbane, Australia in 1937 after investigating an influenza-like illness in abattoir workers, and later Burnet and Freeman recovered a rickettsial-like organism from infected mice,2 and named it Rickettsia burnetii, then subsequently
Coxiella burnetii.3 Coxiella burnetii exists globally except for Antarctica and probably New Zealand.4 It infects arthropods of the class Arachnida including primarily ticks, and also reptiles and other vertebrates including humans, but causes natural disease predominantly only in humans. Domestic sheep, cattle, and goats are most commonly infected and often transmit the disease to humans by excretory products, milk, and hide but most effectively by parturient products. In 1949, an epidemiologic survey among domestic sheep in California indicated that 24% had microagglutinating antibodies to C. burnetii.5 More recent studies6,7 suggest that seroprevalence in these domestic ruminants is currently higher than it was 20 to 30 years ago. In most instances the diagnosis of Q fever is established serologically in humans as well as exposure in animals.4 There are several serologic methods that are used including complement fixation (CF), indirect immunofluorescence assay (IFA), and enzyme-linked immunosorbent fluorescence assay (ELISA). CF is quite specific but less sensitive than IFA and ELISA.4 C. burnetii exhibits an host-dependent antigenic variation termed phase variation 1 and 2 due to mutational changes in lipopolysaccharide profiles, which results in small-cell and large-cell variants; the former survives in the environment whereas the latter multiplies in the host monocyte or macrophage. Bacteria isolated directly from patients or laboratory animals are in phase 1 whereas those isolated after repeated passage through embryonated hens’ eggs are in phase 2. In an apparent paradox, antibodies to phase 2 antigen is associated with an acute illness and an antibody rise to phase 1 antigen occurs in chronic disease. In particular, the IgM antibody response to phase 2 antigen indicates an acute reaction, whereas repetitive replication in cell cultures results in poor antigenic stimulation and a less virulent organism resulting in a type 1 antibody of IgG and IgA subclasses and indicative of chronic infection.8 Impaired maturation of phagosomes and defective killing of C. burnetii appear to be responsible for the development of chronic Q fever9 and perhaps carriage of the organism and the absence of disease in ungulates.
Native American bighorn sheep (Ovis canadensis) have inhabited the United States for more than 25,000 years. Originally described by Lewis and Clark in 1804 the bighorn population was estimated to constitute more than 1 million animals ranging from the prairies in the mid-west to the mountains near the Pacific Ocean. Currently less than 75,000 bighorn inhabit the continental United States. Two subspecies currently exist in Southern California, Ovis canadensis cremnobates and O. canadensis nelsoni. The former were listed as an endangered species in 1998 and inhabit the San Jacinto and Santa Rosa mountains extending from eastern Riverside county in California to the Mexican border.
Peninsular bighorn sheep are unique in that they are low level sheep. Typically, other subspecies of bighorn range from 4,000–10,000 feet elevation when given the choice, whereas peninsular bighorn access habitat from 400–4,000 feet despite having access to mountains as high as 10,000 feet. Peninsular bighorn sheep are gregarious and usually spend time in groups of 2–10 bighorn, but may form larger groups, especially during the lambing season when ewes and lambs often congregate. There are 8 subgroups of Peninsular bighorn in the Peninsular ranges that are connected by ram movement. It is important to have connectivity to maintain herd health.
The Peninsular mountains surround the western limits of the Coachella and Imperial Valleys of the Colorado desert of Southern California, which has virtually no large scale animal husbandry in the area, However, for nearly 4 decades ranchers from Idaho, Wyoming, and Montana have imported their sheep to areas near Palm Springs and Blythe, California to graze and lamb during the fall and winter months. Occasional cases of Q fever have been seen at the Eisenhower Medical Center, a 265-bed general hospital that has also served as a referral facility to the area over the past 34 years. Most infections have been attributed to contact with these sheep often indirectly by living near or intruding into these sheep areas. Since the habitats of domestic and bighorn sheep are so strikingly different, we were interested in evaluating C. burnetii serologies of Peninsular bighorn sheep.
|
MATERIALS AND METHODS
|
From 1992–2004 blood was drawn from 268 Peninsular bighorn sheep and the serum separated and frozen. An aliquot of serum was sent to National Veterinary Services Laboratories (Ames, Iowa) for C. burnetii complement fixing antibodies. Phase 2 antibody was assayed. Both male and female bighorn were included as well as lambs and adult animals. A total of 64 male and 118 female adult bighorn were tested as well as 86 lambs (45M,41F). On average, 21 bighorn sheep were sampled each year of the study. Animals were tested from the northern Santa Rosa Mountains, San Jacinto Mountains, and Bighorn Institute’s captive herd. Lambs were sampled between day 1 and 3 months of age. Ewes and rams were primarily sampled during October, approximately 6 months after the peak of lambing season. Birth was not often observed in the wild, but with those bighorn ewes that gave birth to lambs at Bighorn Institute no evidence of parturition problems were noted.
|
RESULTS
|
Of the 268 bighorn sheep tested 109 were male and 159 female. Twenty-seven bighorn tested positive (11 male and 16 female), 25 having titers of 1:20, 1 each had titers of 1:40 and 1:80. None of the animals appeared ill.
Positive results were obtained in the years 1992–1999, and are divided as follows: 1992, 2/18 positive, 1:20(1), 1:80(1); 1993, 1/19 positive, 1:20(1); 1994,2/20 positive, 1:20(2); 1995, 2/21 positive, 1:20(2); 1996, 9/28 positive, 1:20(9); 1997, 5/7 positive, 1:20(5); 1998, 4/30 positive, 1:40(1), 1:20(3);1999, 2/30 positive, 1:20(2).
Since the Peninsular bighorn were listed as endangered in 1998, the Recovery Plan established guidelines and recommendations limiting livestock operations in the Peninsular ranges.10 These livestock restrictions may give us some understanding of the change of Q fever antibody testing in Peninsular bighorn since 1999.
|
DISCUSSION
|
Q fever is a disease of humans characterized by an influenza-like disease with pneumonia or hepatitis. In about 3% of individuals with symptomatic infection, a chronic infection of the liver (granulomatous hepatitis) or in individuals with valvular heart disease or prosthetic valves8,9 endocarditis ensues. Domestic ruminants are by far the major reservoir of animals that lead to human disease. Sheep, cattle, and goats in the United States who are most often infected by ticks (over 40 species are known), and then transfer C. burnetii in their excretions, hides, milk, and particularly byproducts of parturition by aerosolization and consequent inhalation by humans. In sheep, infection can cause an influenza-like syndrome and rarely abortion. Additionally in Nova Scotia and Maine outbreaks have been noted to be caused by parturient cats.11
The existence of C. burnetii infection in feral animals has been documented in kangaroos, wallabies, and wallaroos in Australia12 as well as deer in central Europe and Alaska13–16 and marsupials and rodents in French Guiana.17 In Alaska complement fixing antibodies > 1:10 to C. burnetii are found in the sera of 12 of 18 Dall sheep16 suggesting that infection is widespread in Dall sheep of the Central Alaska Range. In California the seroprevalence in wildlife animals includes coyotes (78%), gray foxes (55%), skunks (21%), raccoons (8%), rabbits (53%), deer (22%), mice (22%), birds (20%), and bears (7%), In Idaho 6% of bears, and in Florida 10% of bears have Q-fever antibody whereas in Arkansas 80% of wild sheep possess antibodies to Coxiella burnetii.
We have not found any previous reports detailing exposure of bighorn sheep to C. burnetii in the United States. Our current serologic study of 268 peninsular sheep from Southern California indicates antibody to C. burnetii occurs in about 10% of animals. This prevalence is far less than has been reported from elsewhere where the infection exists in feral animals.
Implicit in this observation is that Q fever has not been a major factor in the decline in population of the Peninsular bighorn sheep. Indeed, pneumonia has been a prominent and major cause of lamb mortality but has been shown to be secondary to viral infection (usually parainfluena3) complicated by Pasteurella hemolytica superinfection.18 Our opinion is that the decline of peninsular bighorn sheep in Southern California results from loss of habitat due to human intrusion into bighorn habitat and not to infection. Supporting this conclusion is the recent observation that the number of bighorn sheep has increased by 100% since measures have been initiated to protect their habitat from human intrusion.
The absence of exposure to C. burnetii in Peninsular bighorn sheep but its high prevalence in imported domestic sheep into the Southern California desert certainly implies that their distant habitats exert a major influence on this observation. Furthermore it would also imply the natural absence of C. burnetii-infected arachnids in the remote areas of Southern California deserts and mountains appears to be due to the absence of animal husbandry in the area. When this does occur as with the importation of infected domestic sheep, human Q fever serves to identify habitat contamination.
In our study the CF test was used and although it is not as sensitive as the IFA and ELISA the blood was drawn within 3 months of lambing. In primary Q fever in humans, phase 2 antibody ordinarily persists at moderate titers for 3 months to 1 year.8 Thus, assuming a similar quantitative serologic response in mammals, it would appear that the interval of up to 3 months would accurately detect exposure to C. burnetii.
Received July 17, 2005.
Accepted for publication April 18, 2006.
* Address correspondence to Lawrence A. Cone, Eisenhower Medical Center, Probst Professional Building, Suite 308, 39000 Bob Hope Drive, Rancho Mirage, CA 92270. E-mail: laconemedico{at}aol.com 
Authors’ addresses: James R. Deforge, Bighorn Institute, P.O. Box 262, Palm Desert, CA 92261-0262, Telephone: 760-346-7334, Fax: 760-340-3987. Lawrence A. Cone, Eisenhower Medical Center, Probst Professional Building, Suite 308, 39000, Bob Hope Drive, Rancho Mirage, CA 92270. E-mail: laconemedico{at}aol.com.
|
REFERENCES
|
- Derrick EH, 1937. "Q" fever, new fever entity: clinical features, diagnosis and laboratory investigation. Med J Aust 2: 281–299.
- Burnet FM, Freeman M, 1937. Experimental studies on the virus of Q fever. Med J Aust 2: 299–302.
- Dyer RE, 1938. A filter-passing infectious agent isolated from ticks. IV. Human infection. Public Health Rep 53: 2277–2282.
- Fournier P-E, Marrie TJ, Raoult D, 1998. Diagnosis of Q fever. J Clin Microbiol 36: 1823–1834.[Free Full Text]
- Ruppanner R, Brooks D, Morrish D, Spinelli J, Franti CE, Behymer DE, 1982. Q fever hazards from sheep and goats used in research. Arch Environ Health 37: 103–110.
- Beck MD, Bell JA, Shaw EW, Huebner RJ, 1949. Q fever studies in Southern California. II. An epidemiological study of 300 cases. Public Health Rep 64: 41–56.[Web of Science][Medline]
- Enright JB, Franti CE, Longhurst WM, Behymer DE, Wright ME, Dutson VJ, 1971. Coxiella burnetii in a wildlife-livestock environment: antibody responses of ewes and lambs in an endemic Q fever area. Am J Epidemiol 94: 62–71.[Abstract/Free Full Text]
- Peacock MG, Philip RN, Williams JC, Faulkner RS, 1983. Serological evaluation of Q fever in humans: enhanced phase 1 titers of immunoglobulins G and A are diagnostic for Q fever endocarditis. Infect Immun 41: 1089–1098.[Abstract/Free Full Text]
- Ghigo E, Honstettre A, Capo C, Gorvel J-P, Raoult D, Mege J-L, 2004. Link between impaired maturation of phagosomes and defective Coxiella burnetii killing in patients with chronic Q fever. J Infect Dis 190: 1767–1772.[Web of Science][Medline]
- United States Fish and Wildlife Service (USFWS), 2000. Recovery Plan for Bighorn Sheep in the Peninsular Ranges. U.S. Fish and Wildlife Service, Portland, Oregon.
- Langley JM, Marrie TJ, Covert A, Waag DM, Williams JC, 1988. Poker players pneumonia. An urban outbreak of Q fever following exposure to a parturient cat. N Engl J Med 319: 354–356.[Web of Science][Medline]
- Pope JH, Scott W, Dwyer R, 1960. Coxiella burnetii in kangaroos and kangaroo ticks in Western Queensland. Aust J Exp Biol 38: 17–28.
- McQuiston JH, Childs JE, 2002. Q fever in humans and animals in the United States. Vector Borne Zoonotic Dis 2: 179–191.[Medline]
- Zvizdic S, Bajrovic T, Beslagic E, Puvacic S, Velic R, Maglajlia J, Hamzic S, Kapic E, Zvizdic A, 2002. Q-fever, human and animal morbidity in some regions of Bosnia and Herzegovina, in 2000. Med Arh 56: 131–133.[Medline]
- Hubalek Z, Juricova Z, Svobodova S, Halouzka J, 1993. A serologic survey for some bacterial and viral zoonoses in game animals in the Czech Republic. J Wildl Dis 29: 604–607.[Abstract]
- Zarnke RL, 1983. Serologic survey for selected microbial pathogens in Alaskan wildlife. J Wildl Dis 19: 324–329.[Abstract]
- Gardon J, Heraud J-M, Laventure S, Ladam A, Capot P, Fouquet E, Favre J, Weber S, Hommel D, Hulin A, Couratte Y, Talarmin A, 2001. Suburban transmission of Q fever in French Guiana: evidence of a wild reservoir. J Infect Dis 184: 278–284.[Web of Science][Medline]
- DeForge JR, Scott JE, 1982. Ecological investigations into high lamb mortality. Desert Bighorn Council Transactions 26: 65–76.
TOP
ABSTRACT
INTRODUCTION
