Chapter 59 Primer on Tick-Borne Diseases in Exotic Carnivores

Tick-borne diseases include bacterial, viral, protozoal, and even toxic diseases transmitted or caused by ticks. Ticks, especially Amblyomma spp., also may cause anemia and direct trauma leading to secondary infections and myiasis.¹ Tick-borne diseases of microbial origin are infectious but not contagious. For some organisms, such as Ehrlichia canis and Cytauxzoon felis, carnivores are the definitive host and serve as the reservoir for infection in other species, whereas for Hepatozoon spp., carnivores serve as the intermediate host. For other diseases, such as borreliosis, they are a dead-end or incidental host and do not play an important role in the epizootiology of the disease. These hosts, however, may be important in maintaining tick populations. Many infectious diseases, such as tularemia and yersiniosis, are more frequently transmitted by other mechanisms or vectors, but also may be transmitted by ticks. Recent advances in molecular analyses have improved sensitivity and, in many cases, have demonstrated that a much larger percentage of a given population is infected. These advances also have led to the identification of additional organisms and have changed the taxonomic classification of the causative agent for some diseases. Depending on geographic region and climate, there may be seasonal variation to disease occurrence because activity patterns of ticks, intermediate hosts, and definitive hosts vary through the year. The geographic distribution of tick-borne diseases generally is going to follow the distribution of competent vectors and hosts.

Coinfections with tick-borne organisms should be considered the rule rather than the exception. Individual ticks have been shown to be infected with multiple pathogens and carnivores are often infected with multiple tick species. Furthermore, infection with one pathogen may impair the immune response and increase susceptibility to other tick-borne pathogens. For example, coinfections of Babesia spp., possibly other tick-borne diseases, and canine distemper virus may have resulted in a die-off of African lions (Panthera leo) in Ngorongoro Crater in 2001.²⁰

Often, knowledge of clinical disease resulting from tick-borne infections in wildlife is lacking. Mortality studies using primarily adult animals (e.g., telemetry studies) may overlook morbidity and mortality in younger age groups, a demographic group particularly susceptible to many tick-borne pathogens. Also, clinical signs and hematologic changes resulting from tick-borne infections in exotic carnivores may be transient, only occurring during the acute stages. Captive adult animals also may be fully susceptible if never exposed at a young age. This could affect translocation projects because captive-bred animals, which were not exposed to tick-borne pathogens at a young age, may be susceptible when released into the wild.²³ Additionally, extreme stress, immunosuppressive coinfections, splenectomy, and other factors may precipitate clinical disease in infected carnivores.^5,^20,³¹

Diagnosis of infectious tick-borne diseases is based on clinical signs and history, direct visualization of organisms on histology or stained blood smears, serology, polymerase chain reaction (PCR) assay, and response to treatment. Most tick-borne bacteria are either obligate intracellular parasites or are otherwise difficult to grow, and some organisms such as Rickettsia rickettsii require enhanced biocontainment and select agent registration.²² Therefore, culture is not routinely used as a diagnostic tool. Diagnostics should include tests for all potential tick-borne pathogens.

The control and prevention of tick-borne diseases are directed at control of ticks and management of their intermediate and/or definitive hosts. Topical acaricides may be used to control ticks on some host species and have been shown to reduce the transmission of some rickettsial diseases.²²

Many tick-borne organisms infecting carnivores are zoonotic, including Borrelia spp., Ehrlichia canis, E. chaffeensis, E. ewingii, Anaplasma phagocytophilum, Rickettsia rickettsii, Coxiella burnetii, Bartonella spp., and Powassan virus, and thus carnivores may serve as sentinels for zoonotic tick-borne diseases. Ectoparasites in zoo settings have been found to carry zoonotic pathogens ²¹ and zoo animals, personnel, and visitors potentially are at risk if bitten by ticks. Appropriate personal protection equipment should be worn when handling blood or conducting necropsies on animals possibly infected with tick-borne diseases. Finally, the diagnosis, occurrence, and distribution of tick-borne diseases are increasing. This is likely the result of improved diagnostics, increased awareness, and changes in the environment and climate, resulting in an increase and expansion of tick populations and reservoir hosts.^20,²² Additionally, alterations in land management (e.g., prevention of natural wildfires) may lead to increased tick numbers and tick-borne diseases.

Bacteria

Borreliosis

Lyme borreliosis is caused by a gram-negative spirochete belonging to the genus Borrelia. In the United States, Borrelia burgdorferi sensu lato is the primary cause of Lyme disease. This species complex shows considerable genetic diversity and includes the genotypes B. burgdorferi sensu scricto, B. andersoni, B. bissettii, and B. carolinensis. Transmission is primarily by Ixodes ticks, which usually parasitize different hosts as a larva, nymph, or adult. Borrelia is maintained in the vector by transstadial transmission and rodents are the principal reservoirs. For some Borrelia species, certain mammals are not important reservoirs but contribute to disease persistence by serving as a host for adult ticks (e.g., role of white-tailed deer [Odocoileus virginianus] in the ecology of Lyme disease).⁶ Transplacental transmission has been demonstrated in several species, including the coyote (Canis latrans). Among carnivores, infection with or antibodies reactive to Borrelia burgdorferi s.l. have been detected in captive and/or free-ranging canids, felids, ursids, mustelids, procyonids, and pinnipeds.²⁹

In domestic dogs, clinical signs following experimental infection with B. burgdorferi sensu stricto occur months after exposure and include fever, inappetence, lethargy, lymphadenopathy, and polyarthritis.¹³ An experimentally infected wolf (Canis lupus) developed a transient lymphadenopathy following intravenous inoculation of B. burgdorferi. Otherwise, clinical disease has not been described in naturally infected carnivores. The diagnosis of borreliosis may be difficult and is based on clinical signs, diagnostic tests (culture, PCR assay or, more commonly, serology), history of exposure, and elimination of other differential diagnoses.⁶ Treatment is most beneficial early in the infection, and doxycycline is the antibiotic of choice. Other effective antibiotics include ampicillin or amoxicillin, some third- generation cephalosporins, and erythromycin. The development of an effective vaccine for borreliosis has been difficult because of the number of strains and species responsible for the disease; however, killed whole bacterin and recombinant vaccines labeled for use in dogs are available.

Rickettsial Diseases

Ehrlichiosis and Anaplasmosis

Ehrlichia and Anaplasma spp. are gram-negative obligate intracellular cocci in the family Anaplasmataceae that primarily infect leukocytes, although some species infect platelets. Several species have been described and each has a somewhat unique epizootiology, but all are transmitted by ticks. Ehrlichia canis, the cause of canine ehrlichiosis, is transmitted by the brown dog tick (Rhipicephalus sanguineus), although Dermacentor variabilis also has been shown to be a competent vector. The reservoir hosts are domestic dogs and wild canids.²² Antibodies to or infection with E. canis have been demonstrated in free-ranging and captive canids, felids, and procyonids.

In domestic dogs, the disease is characterized initially by depression and anorexia and may include weight loss, lymphadenopathy, nasal and ocular discharge, dyspnea, and edema. These transient signs may be followed by thrombocytopenia and leukopenia. Chronic infections may be mild or severe and may include bleeding tendencies, severe weight loss, debilitation, and neurologic signs. Putative E. canis infection and clinical signs have been reported in a captive gray wolf and in experimentally infected wild dogs (Lycaon pictus). Wild dogs exhibited anorexia, depression, anemia, leukopenia, and mild thrombocytopenia. Experimentally infected jackals (Canis mesomelas) and foxes (Vulpes and Urocyon) did not show disease, although a mild thrombocytopenia, leukopenia, and anemia were seen in the acute stages of infection in foxes. Clinical disease has not been reported in other free-ranging carnivores.

Ehrlichia chaffeensis infects monocytes and is the cause of human monocytic ehrlichiosis. E. chaffeensis is transmitted by Amblyomma americanum and the white-tailed deer serves as its principal reservoir. This agent is zoonotic and also may infect domestic dogs. Antibodies reactive to E. chaffeensis have been reported from raccoons (Procyon lotor) throughout the southeastern United States.³² Experimental inoculations of raccoons have resulted in short-term rickettsemias, but infected raccoons failed to transmit infections to ticks. Natural E. chaffeensis infections have been identified in free-ranging coyotes. Following experimental inoculation with E. chaffeensis, red foxes (Vulpes vulpes) became bacteremic, but gray foxes (Urocyon cinereoargenteus) were refractory. Clinical signs of E. chaffeensis infection in dogs may be similar to those of E. canis infections but typically are milder,⁴ and clinical disease has not been reported in naturally or experimentally infected exotic carnivores.