Exposure To Selected Pathogens in Geoffroy's Cats and Domestic Carnivores From Central Argentina
Exposure To Selected Pathogens in Geoffroy's Cats and Domestic Carnivores From Central Argentina
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ABSTRACT: Wild carnivores share a high percentage of parasites and viruses with closely related
domestic carnivores. Because of increased overlap and potential contact with domestic species, we
conducted a retrospective serosurvey for 11 common carnivore pathogens in 40 Geoffroy’s cats
(Leopardus geoffroyi) sampled between 2000 and 2008 within or near two protected areas in central
Argentina (Lihué Calel National Park, La Pampa, and Campos del Tuyú National Park, Buenos
Aires), as well as five domestic cats and 11 domestic dogs from cattle ranches adjacent to Lihué Calel
Park. Geoffroy’s cats had detectable antibody to canine distemper virus (CDV), feline calicivirus
(FCV), feline coronavirus, feline panleukopenia virus (FPV), Toxoplasma gondii, Leptospira
interrogans (serovars Ictero/Icter and Ballum), and Dirofilaria immitis. None of the wild cats had
antibodies to feline herpesvirus, feline immunodeficiency virus (FIV), feline leukemia virus, or rabies
virus. Domestic dogs had antibodies to CDV, canine adenovirus, canine herpesvirus, and canine
parvovirus. Antibodies to FPV, FCV, FIV, and T. gondii were found in domestic cats. We provide the
first data on exposure of free-ranging Geoffroy’s cats to pathogens at two sites within the core area of
the species distribution range, including the first report of antibodies to CDV in this species. We
encourage continued monitoring for diseases in wild and domestic carnivores as well as preventive
health care for domestic animals, particularly in park buffer zones where overlap is greatest.
Key words: Argentina, domestic carnivores, domestic–wild interface, Leopardus geoffroyi,
pathogens, serosurvey.
899
900 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 4, OCTOBER 2012
FIGURE 1. Geoffroy’s cat (Leopardus geoffroyi) sample collection sites from Buenos Aires (A. Campos del
Tuyú National Park) and La Pampa (B. Lihué Calel National Park and neighboring ranches) provinces in
Argentina. Towns and cities near sampling sites are provided for reference. Numbers and sex (M 5 male; F 5
female) of Geoffroy’s cats sampled at each site are included.
Five Geoffroy’s cats (three females and two domestic–wild interface, there were no domes-
males) were sampled at Tuyú in February tic animal samples from this area.
2000 and 35 (15 females and 20 males) were Geoffroy’s cats were tested for antibodies to
sampled at Lihué in two different periods FHV, FPV, FCV, CDV, feline coronavirus
(2002–2003 n510, and 2007–2008 n525). Of (FcoV), feline immunodeficiency virus (FIV),
the cats sampled at Lihué, 21 were captured feline leukemia virus (FeLV), rabies, Toxo-
within the national park and 14 in adjacent plasma gondii, Leptospira interrogans (sero-
cattle ranches. All were adults, except for one vars Pomona, Hardjo, Icterohaemorrhagiae/
young male (6–8 mo old) from Lihué, and Copenhageni, Grippotyphosa, and Canicola),
appeared to be in good physical condition at and Dirofilaria immitis. Thirteen additional
capture (i.e., no apparent disease), although serovars of L. interrogans (Australis, Pyro-
body weights of cats captured in Lihué in 2003 genes, Bratislava, Sejroe, Javanica, Szwajizak,
were slightly lower (8%) than those captured in Saxoebing, Ballum, Icterohaemorrhagiae/Ic-
2007–2008 (Pereira, 2009). Blood samples were terohaemorrhagiae, Wolffi, Autumnalis, Bata-
collected by venipuncture of the jugular, viae, and Tarassovi) were tested only on
cephalic, or saphenous veins in heparinized Geoffroy’s cats sampled in 2007–2008 (n525).
syringes, and centrifuged at 1,100 3 G Domestic cats were tested for the same
(Mobilespin, model 128, Cardinal Health, diseases as Geoffroy’s cats, except for rabies.
Dublin, Ohio, USA) in the field within 4 hr of Domestic dogs were tested for CDV, canine
collection. Plasma was stored in liquid nitrogen adenovirus (CAV), canine herpesvirus (CHV),
in the field, and transferred to a 220 C freezer canine parvovirus (CPV), and D. immitis. All
until exported for analysis. serologic tests were performed at Cornell
All sampling events in Lihué (see below), and Veterinary Diagnostic Laboratory, Ithaca,
particularly in 2003, coincided with periods of New York, and test methods and cutoff values
severe prolonged drought that led to significant are shown in Table 1. Antibody prevalence for
food shortage for Geoffroy’s cats (Pereira et al., the most common pathogens was compared
2006). As a result, six cats included in this study between sexes using a Fisher’s exact test. Also,
were found dead 1–3 mo after capture (Pereira we compared antibody prevalence between
et al., 2006; Pereira, 2009). Gross and histologic park and ranches in Lihué using chi-square
findings in dead cats were consistent with poor tests of homogeneity for 2 3 2 contingency
nutritional status and included emaciation (low tables (Daniel, 1990).
body weight, loss of subcutaneous and pericar-
dial fat, hepatic fatty change) and high parasite RESULTS
loads (Beldoménico et al., 2005). Clinical or
histologic signs consistent with infectious dis- Geoffroy’s cats were positive for seven
ease were not observed. This scenario coupled of 11 infectious agents studied (details on
with postmortem findings suggests that the
dead cats were severely affected by the lack location, sex, and titers are provided in
of prey. Table 2). Serologic tests for FIV, FeLV,
Domestic cats (four females and one male) rabies, and FHV were negative. In Tuyú, all
and domestic dogs (two females and nine five Geoffroy’s cats were positive for
males) were sampled in May–July 2007 in cattle antibody to T. gondii and FCV, two (40%)
ranches near Lihué, except for a 12-year-old
female domestic cat that belonged to a park
to FPV, and one (20%) to CDV (Table 2).
ranger based at the national park. This cat was One adult had detectable antibody titers
the only vaccinated animal in this study. It was against these four pathogens, one for three,
vaccinated 11 yr before the study with one dose and the remaining three individuals for two
of inactivated triple vaccine for feline herpes- of them.
virus (FHV), FPV, and FCV (Felocell, Pfizer).
In Lihué, 22 of 35 (63%) Geoffroy’s cats
All domestic animals appeared to be in good
physical condition and were adults at the time had antibody to FCV, 14 (40%) to T.
of sampling, except for one young male dog gondii, seven (20%) to CDV, two (6%) to
(4 mo) and one female cat (6 mo). Domestic FPV, and one (3%) to FcoV (Table 2). In
carnivores were manually restrained with the addition, 15 of 25 (60%) had antibody to L.
assistance of their owners, and blood samples interrogans serovar Ictero/Icter, two (8%)
were collected, processed, and stored as
described above. Because samples from Tuyú to serovar Ballum, and one individual (3%)
were collected previously for another study that was positive for adult D. immitis antibody
did not include the assessment of diseases at the (Table 2). Thirty Geoffroy’s cats (86%)
902 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 4, OCTOBER 2012
TABLE 1. Serologic tests and positive cutoff values used by Cornell Veterinary Diagnostic Laboratory,
Ithaca, New York, USA to detect exposure of Geoffroy’s cats (Leopardus geoffroyi) and domestic carnivores to
selected disease agents.
Canine adenovirus SN $4
Canine distemper virus SN $8
Canine herpesvirus SN $8
Canine parvovirus HI $20c
Feline calicivirus SN $8
Feline coronavirus KELA $8
Feline herpesvirus SN $8
Feline immunodeficiency virus (FIV) KELA P/N
FIV confirmatory WB P/N
Feline leukemia virus ELISA P/N
Feline panleukopenia virus HI $20c
Rabies RFFIT $5
Dirofilaria immitis (occult) I-ELISA P/N
Leptospira interrogans MAT $100
Toxoplasma gondii KELA $48
a
SN 5 serum neutralization; HI 5 hemagglutination inhibition; KELA 5 kinetic enzyme-linked immunosorbent assay;
WB 5 Western blot; ELISA 5 enzyme-linked immunosorbent assay; RFFIT 5 rapid fluorescent focus inhibition test; I-
ELISA 5 indirect enzyme-linked immunosorbent assay; MAT 5 microscopic agglutination test.
b
P/N 5 test scored as positive or negative.
c
In domestic carnivores positive titers are $10.
from Lihué had antibodies for at least one (a 12-year-old vaccinated female) had
of the 11 agents tested, with one (3%) antibody to three of these agents (FPV,
being positive for four agents, six (17%) to FCV, and FIV; Table 4).
three, 17 (49%) to two, and six (17%) to
only one agent. DISCUSSION
Prevalences between females and males
were not significantly different (P.0.05). We provide the first data on exposure of
Overall prevalences (and 95% confidence Geoffroy’s cats to selected infectious
interval) for antibody to the three most agents at two sites in Argentina, within
represented pathogens in Lihué Geof- the core area of the distribution range of
froy’s cats (FCV: 64% [43–84] in the park this species. Our results show evidence of
and 62% [35–88] in ranches; L. inter- exposure to 4/11 and 7/11 pathogens in
rogans serovar Ictero/Icter: 53% [28–79] Tuyú and Lihué, respectively. Positive
in the park and 70% [42–98] in ranches; T. titers to FCV and FPV were also found
gondii: 45% [25–66] in the park and 31% by Fiorello et al. (2007) in a Geoffroy’s cat
[6–56] in ranches) were not significantly population near the northern limit of the
different (P.0.05) between park and species distribution in Bolivia. Similarly to
ranches. these authors, we detected that Geoffroy’s
Of the 11 domestic dogs sampled, 10 cats in Lihué are exposed to various
(91%) were positive to CPV antibody, six pathogens common to domestic carnivores
(55%) to CAV, four (36%) to CDV and with which they overlap.
CHV, and none to D. immitis (Table 3). For FCV, high titers (up to 768 in four
Domestic cats were positive for four (FPV, individuals) and high antibody prevalence
FCV, FIV, and T. gondii) of nine antibod- (100% and 62.8% at Tuyú and Lihué,
ies, with a single positive for each except respectively) were found in Geoffroy’s
for FPV (four of five animals were cats. Feline calicivirus is extremely conta-
antibody positive). A single domestic cat gious, especially in areas with high felid
UHART ET AL.—PATHOGEN EXPOSURE IN GEOFFROY’S CATS AND DOMESTIC CARNIVORES 903
TABLE 2. Site and year of sampling and antibody titers found in five Geoffroy’s cats (Leopardus geoffroyi)
from Campos del Tuyú National Park, Buenos Aires, and 35 from Lihué Calel National Park, La Pampa,
Argentina, evaluated for exposure to selected pathogens. All Geoffroy’s cats were negative to feline
herpesvirus, feline immunodeficiency virus, feline leukemia virus, and rabies.a
densities (Lenghaus et al., 2001). Geof- the high antibody prevalences. High titers
froy’s cats occur at high densities in Lihué of antibodies to FCV ($500) were ob-
(up to 120 individuals per 100 km2; Pereira served in 15% of the animals (6/40),
et al., 2011) and Tuyú (Lucherini et al., suggesting an active response to the virus
2000), probably resulting in high contact at the time of sampling. Feline calicivirus
rates among individuals, thus explaining infection can produce disease character-
904 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 4, OCTOBER 2012
TABLE 3. Antibody titers to selected pathogens in 11 domestic dogs sampled in 2007 around Lihué Calel
National Park, Argentina. All dogs were negative to Dirofilaria immitis.
Pathogens evaluateda
ized by vesicles, erosion, and ulceration of ranging wild felid species in America and
oral cavity and muzzle epithelium, con- Africa, but clinical disease has not been
junctivitis, rhinitis, tracheitis, or pneumo- described (Lenghaus et al., 2001).
nia (Lenghaus et al., 2001). However, no All Geoffroy’s cats sampled in Tuyú were
clinical signs of disease were observed in positive for T. gondii antibodies and the
sampled individuals and the absence of prevalence in Lihué was also high (40%).
macro- and microscopic lesions in the six Warm-blooded animals are reservoirs of T.
necropsied animals with FCV antibodies gondii in nature and the most likely mode
(titer range 5 6–768) suggests previous or of infection is by ingestion of infected prey
repeated exposure to this agent and the or transplacentally (Hill and Dubey, 2002).
probability that FCV is endemic in these Since Geoffroy’s cat diet in both Lihué
populations. At least for the Lihué site, the (Bisceglia et al., 2008; Pereira et al., 2012)
low FCV antibody prevalence detected in and Tuyú (Vuillermoz, 2001) consists
domestic cats indicates that the infection mostly of rodents and other small verte-
circulates in Geoffroy’s cats independently brates, ingestion is the most likely route of
of the domestic cat population. Antibodies exposure, though infection in prey has not
to FCV have been reported in several free- been evaluated. Conversely, prevalence in
TABLE 4. Antibody titers to selected pathogens in five domestic cats sampled in 2007 around Lihué Calel
National Park, Argentina. All domestic cats were negative to feline leukemia virus, feline coronavirus, canine
distemper virus, feline herpesvirus, and Leptospira interrogans. Four cats were negative to Dirofilaria immitis
(cat 4 was not tested).
Pathogens evaluateda
domestic cats was lower than expected Geoffroy’s cats is unlikely. Although CDV
given that they mostly live outdoors and susceptibility appeared to be confined to
hunt for their food, which would facilitate large felids, on the basis of findings in
exposure. Infection with Toxoplasma spp. is bobcats (Lynx rufus) and domestic cats,
common in felids, whereas clinical disease Munson (2001) indicates that this is no
is rare (Dubey et al., 1987), and therefore is longer the case. Nonetheless, the absence
unlikely to represent a significant threat to of signs in the Geoffroy’s cats sampled in
wild felid populations (Ramos-Silva et al., this study, even in those with high antibody
2001). titers, suggests that these individuals de-
Antibodies to CDV were found in both veloped protective neutralizing antibodies.
Geoffroy’s cat populations studied, and one However, it is possible that part of the
cat in Lihué had a high positive titer population was affected at the time of
(2,048). This animal was one of six found exposure to this pathogen, and only survi-
dead postcapture. However, though clini- vors were sampled in this study. To the best
cal signs have been reported in wild felids of our knowledge, this is the first report of
with lower titers (i.e., 1,445, Daoust et al., exposure to CDV in free-ranging Geoffroy’s
2009), no clinical or postmortem (macro- or cats. The impact of this virus on Geoffroy’s
microscopic) signs of disease were ob- cat populations remains unknown and
served in this cat, except for emaciation merits further investigation due to its high
and a body mass loss of over 40% between conservation relevance.
capture and death, 40 days later. Never- Antibodies to FPV were found in asymp-
theless, tissues in which histologic evidence tomatic Geoffroy’s cats at both Tuyú and
of distemper can be seen, such as brain and Lihué. Antibodies to this virus have been
lungs, were not available for histologic documented in free-ranging populations of
examination because of the poor condition felids, including Geoffroy’s cats from Boli-
of the carcass when found. Therefore, the via (Fiorello et al., 2007). Mortality with
significance of this finding remains un- clinical signs has been reported in free-
known. All other CDV antibody-positive ranging bobcats (Wassmer et al., 1988),
Geoffroy’s cats showed titers similar to whereas fatal cases in captive Eurasian lynx
those reported for asymptomatic free- (Lynx lynx) and European wildcat (Felis
ranging lynx (Daoust et al., 2009). silvestris) have been associated with out-
Four of 11 domestic dogs were serolog- breaks in coexisting domestic cats (Wasieri
ically positive for CDV. Domestic dogs are et al., 2009). Eighty percent of domestic
considered a source of CDV and, in some cats tested in Lihué were positive for FPV
cases, have been implicated in large antibody with low titers (#20), whereas
mortality events of wild felids (lions, one 12-year-old vaccinated female living
Panthera leo; Roelke-Parker et al., 1996) inside the park had high titers but no
or wild canids (African wild dogs, Lycaon clinical signs, suggesting recent contact
pictus; Alexander and Appel, 1994). Crab- with the virus. Although FPV is very
eating fox (Cerdocyon thous) deaths attrib- pathogenic for felids, does not require
uted to CDV of domestic dog origin have direct contact for transmission, and can
recently been documented in Argentina persist for long periods in the environment
(Ferreyra et al., 2009). Because of the wide (Barker and Parrish, 2001), antibody prev-
host range of this virus (Williams, 2000) alence in coexisting Geoffroy’s cats was low
and the presence of other susceptible wild (6%). Nevertheless, two of five Geoffroy’s
carnivores in our study areas such as the cats had detectable antibody to FPV in
Pampas fox (Lycalopex gymnocercus), the Tuyú, but information on domestic carni-
hog-nosed skunk (Conepatus chinga), and vore prevalence from this area is lacking.
the lesser grison (Galictis cuja), identifying Given that parvoviruses are potent immu-
the source of exposure to CDV for nogens, higher prevalences and titers
906 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 4, OCTOBER 2012
would be expected if Geoffroy’s cats were temperate areas (Bowman et al., 2009;
repeatedly exposed (Barker and Parrish, Genchi et al., 2009). In Argentina, D.
2001). Therefore, viral circulation in sym- immitis is thought to not reach latitudes
patric domestic cats suggested by the .34u (Vezzani et al., 2011). The necropsy
prevalences observed is a cause for concern and subsequent histology of the positive cat
for Geoffroy’s cat conservation. confirmed severe emaciation and high
Prevalence of FcoV in free-ranging parasite loads, but filaria were not seen in
felids is reported to be near 2% (Evermann the lungs even though the carcass was very
and Benfield, 2001). Illness and associated fresh. Although larvae or adult worms
death have only been described in captive provide a definitive postmortem diagnosis
felids and these cases included animals that of infection, ectopic location of the parasite
were antibody negative, although the virus can hinder diagnosis (Kalkstein et al.,
was detected in their feces through PCR 2000). Further studies are needed to assess
(Heeney et al., 1990; Kennedy et al., 2002). the potential implications of this finding.
Thus, even though only one Geoffroy’s cat The lack of antibodies to FHV and FIV
in our study had antibodies to this virus, the in Geoffroy’s cats sampled in this study
possibility that other exposed individuals contrast with reported antibody preva-
may not have been detected by serologic lence in cats from Bolivia (Fiorello et al.,
methods should be considered. Exposure 2007). Only an old domestic cat, also
to a coronavirus in cheetahs (Acinonyx positive for FPV, was serologically positive
jubatus) has been thought to result from for FIV with a high titer (2,560). Accord-
contact with domestic cats or from cross- ing to Yamamoto et al. (1989), high
reactions with other (non-FcoV) antigeni- enzyme-linked immunoassay titers are a
cally similar coronaviruses of dietary origin strong indicator of active FIV infection.
(i.e., from feral swine; Heeney et al., 1990). However, given that this animal was
The wild boar (Sus scrofa) was introduced negative upon confirmatory Western blot
in Argentina in the late 1800s and is present test and that repeated samples were not
in both Lihué and Tuyú (Novillo and available, our results are inconclusive.
Ojeda, 2008). Nonetheless, it has never We found evidence of exposure to seven
been detected as prey for Geoffroy’s cats in pathogens in Geoffroy’s cats, three of
these areas (Vuillermoz, 2001; Bisceglia which were shared with domestic animals.
et al., 2008). Even though FcoV is highly In Lihué, however, prevalence did not
species-specific, cross-infection between differ between the ranches (where all
wild and domestic carnivores has been people have cats and dogs) and the park
reported (Evermann et al., 1980; Ballou, (where domestic carnivores are rare).
1993). However, the lack of FcoV antibod- These results may be partially explained
ies in domestic cats and the low antibody by the existence of pathogen sources in
titer (12) in the only positive Geoffroy’s cat the area other than domestic carnivores, as
renders this finding irrelevant. was previously suggested for T. gondii. An
Evidence of heartworm (D. immitis) alternative (or complementary) explana-
infection in a Geoffroy’s cat from Lihué tion might be related to Geoffroy’s cat
was unexpected, as this parasite is normally spatial ecology at the time of this study.
associated with tropical and subtropical Radiocollared cats showed an active
climates that are favorable for the repro- movement pattern, with long mean daily
duction of mosquito vectors. Consequently, movements (up to 5 km), frequent long-
D. immitis has been reported in free-ranging distance emigrations (up to 130 km), and
carnivores from the tropics (Nakagaki periodic shifts in home ranges (Pereira
et al., 2000; Deem and Emmons, 2005). et al., 2006; Pereira, 2009). Exposed cats
Nevertheless, the geographic distribution dispersing to and from ranches could have
of D. immitis seems to be expanding into transmitted infections to new areas where
UHART ET AL.—PATHOGEN EXPOSURE IN GEOFFROY’S CATS AND DOMESTIC CARNIVORES 907
domestic carnivores were absent. Further- Iowa State University Press, Ames, Iowa, pp.
131–146.
more, the severe drought that affected
BELDOMÉNICO, P. M., J. M. KINSELLA, M. M. UHART,
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