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Canine Visceral Leishmaniasis, United States and Canada, 2000–2003 Zandra H RESEARCH Canine Visceral Leishmaniasis, United States and Canada, 2000–2003 Zandra H. Duprey,* Francis J. Steurer,* Jane A. Rooney,* Louis V. Kirchhoff,† Joan E. Jackson,‡ Edgar D. Rowton,‡ and Peter M. Schantz* Visceral leishmaniasis, caused by protozoa of the human disease have been reported (4). Infection in dogs genus Leishmania donovani complex, is a vectorborne may indicate human risk for leishmaniasis, especially in zoonotic infection that infects humans, dogs, and other HIV-positive persons, in many areas (5); infected but mammals. In 2000, this infection was implicated as causing asymptomatic dogs can infect sandflies that feed on them, high rates of illness and death among foxhounds in a ken- posing a risk to uninfected dogs and humans (6). nel in New York. A serosurvey of >12,000 foxhounds and other canids and 185 persons in 35 states and 4 Canadian Until recently, visceral leishmaniasis was thought to be provinces was performed to determine geographic extent, primarily an imported disease in North America; infected prevalence, host range, and modes of transmission within dogs had usually been imported from regions in southern foxhounds, other dogs, and wild canids and to assess pos- Europe or South America where L. infantum and L. cha- sible infections in humans. Foxhounds infected with gasi were enzootic (2,3). However, sporadic cases of leish- Leishmania spp. were found in 18 states and 2 Canadian maniasis have been reported in foxhounds and dogs of provinces. No evidence of infection was found in humans. other breeds with no history of travel to areas where leish- The infection in North America appears to be widespread in maniasis was enzootic, and the origin of these infections foxhounds and limited to dog-to-dog mechanisms of trans- remains unknown (7,8). mission; however, if the organism becomes adapted for vector transmission by indigenous phlebotomines, the In the late summer of 1999, foxhounds at a New York probability of human exposure will be greatly increased. foxhunting club began showing signs of epistaxis, weight loss, muscle atrophy, seizures, alopecia, dermal lesions, swollen limbs and joints, and renal failure (9). Of the 250 isceral leishmaniasis, caused by geographic variants dogs in the kennel, 112 (44.8%) were sick and 29 (11.6%) Vof the Leishmania donovani complex (L. donovani, L. had died at the time of the investigation. Cytopathologic infantum, L. chagasi), is a progressive wasting disease of examination of joint fluid of 1 hound showed amastigote dogs and humans that is often fatal if untreated (1). Agents forms of Leishmania spp. These parasites were found at of the L. donovani complex occur in parts of necropsy of several dogs by using indirect immunofluores- Mediterranean Europe, the Middle East, Asia, Africa, and cent assay (IIF), polymerase chain reaction, culture, and Central and South America (1–3). In infections involving cytologic and histopathologic studies (9). At that time, the L. donovani complex in the Mediterranean region (L. autochthonous leishmaniasis had not been reported in infantum) and in South America (L. chagasi), dogs are dogs, other animals, or humans in New York. reservoirs for human infection (1,2). Parasites are usually Diagnostic surveys were initiated to measure the preva- transmitted between hosts by phlebotomine sandflies lence of Leishmania infection at the index hunt club and to (Lutzomyia or Phlebotomus spp.) (2,3). determine how infection was introduced into and transmit- Direct quantitative relationships between prevalence of ted among these dogs; the investigation was extended to leishmaniasis in local dog populations and incidence of foxhounds, other breeds of dogs, and wild canids in other states. We describe the results of the 3-year investigation *Centers for Disease Control and Prevention, Atlanta, Georgia, of canine visceral leishmaniasis in the United States and USA; †University of Iowa, Iowa City, Iowa, USA; and ‡Walter Reed Canada through February 2003. Army Institute of Research, Washington, DC, USA 440 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 12, No. 3, March 2006 Canine Visceral Leishmaniasis, 2000–2003 Materials and Methods the United States where foxhounds were tested, all sam- The Masters of Foxhounds Association of America ples that yielded Leishmania IIF titers >128 were tested in (MFHA) represents >200 foxhound kennels and hunt clubs the radioimmunoprecipitation assay (RIPA) for T. cruzi at that house >12,000 foxhounds in 35 US states and 4 the University of Iowa (12,13). Sera that gave positive Canadian provinces. In conjunction with MFHA and results in both tests were considered positive for T. cruzi numerous state health departments, the Centers for Disease infection because Leishmania antibodies do not give false- Control and Prevention (CDC) invited all MFHA-regis- positive reactions in the T. cruzi RIPA. A group of sera that tered foxhound owners to participate in this investigation. yielded Leishmania spp. IIF titers <128 were randomly Owners of nonregistered foxhound hunt clubs that were in selected from foxhounds that were kenneled in southern close proximity to MFHA-registered hunt clubs were also states (where T. cruzi occurs enzootically in wildlife) to invited to participate. Dog owners were asked to submit further assess the prevalence of T. cruzi infection. We samples in 3- to 4-month intervals. From hounds identified defined a confirmed case of Leishmania infection as being as seropositive for Leishmania spp., bone marrow and culture-positive for L. infantum, regardless of antibody other specimens were requested for parasitologic diagno- titer. A probable case was defined as Leishmania IIF titer sis. Serum samples from dogs of breeds other than fox- >128 with a negative RIPA for antibodies to T. cruzi. hounds and from wild canids (e.g., foxes and coyotes) Selected isolates of Leishmania spp. cultured from fox- were also obtained and tested for antibodies to Leishmania hounds were shipped for subtyping and zymodene analysis spp. and Trypanosoma cruzi. Samples from other dog to the Istituto Superiore di Sanità in Rome, Italy. breeds were obtained from kenneled “pound dogs” in Montpelier Centre nomenclature for the identification of Virginia and New York, where infection in foxhounds had agents of human leishmaniases was used to classify the been identified, and from pet dogs whose sera were tested organisms. at CDC for Leishmania antibodies before the pets traveled to countries that require such testing. Fox and coyote sam- Results ples were provided from animals trapped in various loca- From April 2000 to December 2003, >20,000 serum tions of the southeastern United States. samples were collected from >12,000 canines and submit- IIF assays for antibodies to Leishmania spp. were per- ted to CDC for antibody testing. The dogs ranged in age formed on human and canine serum samples submitted to from 2 months to 13 years. Foxhounds, basset hounds, and CDC (10). IIF was considered positive when fluorescence beagle hounds represented 91.7%, 2.4%, and 1.3% of the was observed around the organisms on the slide. Fourfold population, respectively. The remainder (4.6%) included dilutions were used to reach the final endpoint titer. The >50 other breeds of dogs, foxes, and coyotes. CDC standard IIF diagnostic cutoff titer for infection by MFHA-registered fox-hunting clubs are widely dis- Leishmania spp. belonging to the donovani complex in persed in the eastern half of the United States and Canada, dogs is >128 (10). and fewer are located in western states. Of the 210 kennels To assess possible infection in humans, persons associ- or hunt clubs that participated in this study, only 29 (14%) ated with dogs in the study were invited to submit serum were located in states west of the Mississippi River. In samples for testing. After explaining the purpose of the contrast, 69 (33%) are located in the 3 states of study and obtaining informed consent, participants were Pennsylvania, Maryland, and Virginia. asked about their contact with foxhounds and their person- A total of 12,411 dog serum samples from throughout al health status. Serum samples were tested for Leishmania the United States and Canada were submitted to CDC in antibodies by using the same technique, with the same titer the first round of sample collection. The distributions of value for determining a positive reaction (3,10). IIF titers in the initial and subsequent rounds of serologic Other antemortem samples submitted from dogs testing are shown in Table 1. Each subsequent round of included aspirates of spleen, liver, or lymph nodes and testing was less comprehensive than the preceding rounds excisional lymph node biopsy specimens. Postmortem as a result of financial constraints related to collecting specimens submitted included blood, bone marrow, lymph blood samples dogs shipping specimens as well as waning nodes, kidney, spleen, liver, brain, testes, epididymis, interest of owners. ovaries, and neoplasms. Two media were used to culture Infection with Leishmania spp. was confirmed in fox- Leishmania spp: Novy-MacNeal-Nicolle (NNN) medium hounds from 58 hunt clubs or kennels in 18 states and 2 with Offutt modification and modified NNN medium with Canadian provinces (Table 2 and Figure 1). The distribu- Roswell Park Memorial Institute medium overlay (11). tion of T. cruzi–infected kennels is shown in Table 3 and T. cruzi antibodies cross-react and give false-positive Figure 2. reactions in the CDC Leishmania IIF. Because T. cruzi is Collections of multiple serum specimens from individ- enzootic in domestic dogs and wild canids in some areas of ual hounds during the course of the investigation allowed Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 12, No. 3, March 2006 441 RESEARCH detection of seroconversion over time (Table 4). Discussion Seroprevalence in each subsequent round of testing was Our survey of foxhounds, other breeds of dogs, and artificially skewed toward higher values as a result of wild canids showed that canine visceral leishmaniasis is selective and repeated submission of samples drawn from enzootic in 18 US states and 2 Canadian provinces.
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