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Prevalence of naturally occurring
Dirofilaria immitis infection
among nondomestic cats housed
in an area in which heartworms are endemic
Clarke Atkins, DVM, DACVIM; Anneke Moresco, MS, DVM; Annette Litster, BVSc, PhD
H
eartworm disease (dirofilariasis), caused by infection with Dirofilaria immitis, primarily affects members of the family Canidae. Dirofilariasis is widely distributed, having been identified in northern and southern temperate zones and in the tropics and subtropics.
Infections are recognized in most of the United States,
although the prevalence is greatest in the Southeast and
Mississippi River Valley.1 A recent survey1 of veterinari-
Materials and Methods
Study animals—Medical records of nondomestic cats
housed at the Carnivore Preservation Trust in rural North
Carolina between 1990 and 2002 were reviewed to determine
eligibility for inclusion in the study. The Carnivore Preservation
Trust is a 55-acre facility located in the rural North Carolina
piedmont (longitude, 79.2o W; latitude, 37.5o N) approximately
5 miles from a large lake (Jordan Lake) and in proximity to the
Haw, Rocky, and Cape Fear Rivers. The facility contains a pond
and large enclosures separated by chain-link fences. During the
time of this study, animals were housed outdoors year-round.
Although all animals had den boxes and the smaller cats had
From the Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27606 (Atkins); the
Carnivore Preservation Trust, 1940 Hanks Chapel Rd, Pittsboro, NC 27312 (Moresco); and the Centre for Companion Animal Health, School
of Veterinary Science, University of Queensland, Brisbane, Queensland 4072, Australia (Litster). Dr. Moresco’s present address is the
Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, CA 95616.
Supported in part by a grant from Dr. Terry G. Seaks, Greensboro, NC.
The authors thank Kathryn Bertok, Julie Coats, and Laurie Parish-Chaffey for technical assistance, and Dr. David E. Kenny, Denver Zoo; Dr.
Jon Hangar, Dreamworld, Coomera, Queensland, Australia; Dr. Richard Jakob-Hoff, Auckland Zoo, Auckland, New Zealand; and Drs. Michael
Gorra and Nicole Siegel, Carnivore Preservation Trust, for providing case materials.
Address correspondence to Dr. Atkins.
JAVMA, Vol 227, No. 1, July 1, 2005
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Objective—To determine prevalences of heartworm
exposure (ie, positive heartworm antibody test
results) and heartworm infection (ie, positive heartworm antigen test results or identification of mature
heartworms at necropsy) among nondomestic cats
housed in an area in rural North Carolina where
Dirofilaria immitis is known to be endemic and among
nondomestic cats housed in areas with a low prevalence of dirofilariasis or in an area considered to be
free from heartworms.
Design—Cross-sectional prevalence survey.
Animals—97 nondomestic cats in North Carolina
(study population) and 29 nondomestic cats in
Colorado; Queensland, Australia; or Auckland, New
Zealand (control population).
Procedure—Results of serologic tests and postmortem examinations were reviewed.
Results—Results of heartworm antibody tests were
positive for 57 of 75 (76%) study cats and 1 of 29
(3%) control cats. Male study cats had a significantly higher risk of heartworm exposure than did
female study cats (relative risk, 1.3). Results of heartworm antigen tests were negative for all 47 study
cats and 16 control cats that were tested.
Postmortem examinations were performed on 21
study cats, and 1 (5%) was found to be infected with
heartworms.
Conclusions and Clinical Relevance—Results suggested that nondomestic cats housed outdoors in the
southeastern United States are at risk for heartworm
exposure and infection, with male cats having a greater
risk of exposure than female cats. (J Am Vet Med Assoc
2005;227:139–143)
ans indicated that in 2001, there were approximately
240,000 canine cases diagnosed in the United States.
The number of reports of heartworm infection in
domestic cats has been increasing, although the prevalence of dirofilariasis appears to be much lower in cats
than in dogs.2 Heartworm infection has been reported
in a variety of nondomestic species, including primates3; procyonids4; ursids5; mustelids6,7; nondomestic
canids8-12; and nondomestic cats, specifically the golden cat (Felis temminckii),13 black-footed cat (Felis
nigripes),14 wild cat (Felis bangsi costariensis),15 tiger
(Panthera tigris),15,16 clouded leopard (Neofelis nebulosa),17 bobcat (Lynx rufus),18 leopard (Panthera pardus),19 and ocelot (Leopardus pardalis).20 From these
reports, we know that nondomestic cats are susceptible
to infection with D immitis, but to our knowledge, no
large study of the prevalence of dirofilariasis in nondomestic cats has been published. The purpose of the
study reported here, therefore, was to determine prevalences of heartworm infection (defined as infection
with mature heartworms) and heartworm exposure
(defined as detection of serum anti-heartworm antibodies) among nondomestic cats housed in an area in
rural North Carolina where D immitis is known to be
endemic. Furthermore, prevalence of heartworm exposure among nondomestic cats in this area was compared with prevalence among nondomestic cats housed
in areas with low prevalences of dirofilariasis in dogs
and cats (Colorado and Queensland, Australia) and in
an area considered to be free from heartworms
(Auckland, New Zealand).
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access to heating elements, none of the enclosures were mosquito-proof. Animals received water daily, but the grounds were
not irrigated. Precipitation ranged from 42 to 44 inches annually. Starting in July 1999, all animals housed at the facility were
treated with ivermectina (24 to 39 µg/kg [11 to 17.7 µg/lb], PO,
once a month) for heartworm prophylaxis.
Cats were included in the study if the medical record contained data on exposure to (ie, antibody test results) or mature
infection with (ie, antigen test or necropsy results) heartworms. In addition, to be considered in analyses of prevalence
of heartworm exposure, cats must have been exposed to mosquitoes for at least 1 season (ie, spent 3 summer months in the
facility) prior to testing, and to be considered in analyses of
prevalence of mature heartworm infection, cats must have
been exposed to mosquitoes for at least 1 season during which
they did not receive heartworm prophylaxis.
quito-proof. Mean ± SD age at the time of blood sample collection for heartworm antibody testing was 2.5 ± 2.8 years.
Determination of heartworm exposure and infection—
To determine prevalence of heartworm exposure, serum or
plasma was submitted for testing for anti-heartworm antibodies. Samples were submitted fresh or immediately frozen for
later submission, as recommended by the testing laboratories.
For animals housed at the Carnivore Preservation Trust, tests
were performed by 1 of 2 commercial laboratoriesb,c; which
laboratory performed tests on samples from individual cats
was not consistently recorded. For the control animals, tests
were performed by a single commercial laboratory.c
To determine prevalence of heartworm infection, serum
or plasma was submitted for testing for heartworm antigen.
Samples were submitted fresh or immediately frozen for later
submission, as recommended by the testing laboratories. For
animals housed at the Carnivore Preservation Trust, tests
were performed by 1 of 2 commercial laboratoriesb,c; which
laboratory performed tests on samples from individual cats
was not consistently recorded. For the control animals, tests
were performed by a single commercial laboratory.c
In addition, when possible, postmortem examinations
were performed by the attending veterinarians at Carnivore
Preservation Trust on cats that died or were euthanatized during the study period. Necropsy examinations, although complete, were not specifically directed at detecting heartworms.
Control animals—To determine validity of commercial
antibody tests in nondomestic cats, 29 nondomestic cats representing 7 species (18 males and 11 females) that were housed in
areas with low prevalences of dirofilariasis in dogs and cats
(Colorado and Queensland, Australia) or in an area considered
to be free from heartworms (Auckland, New Zealand) were
used. Three of these cats (a serval, golden cat, and lion; mean
± SD age, 4.2 ± 5.7 years) were housed at the Auckland Zoo in
Auckland, New Zealand (longitude, 174.5o E; latitude, 37o S),
which was considered to be free from heartworms. Sixteen (7
leopards, 5 tigers, and 4 snow leopards; mean age, 2.5 ± 4.9
years) were housed at the Denver Zoo in Denver, Colo (longitude, 105.1o W; latitude, 38.9o N), where the prevalence of dirofilariasis in dogs and cats was unknown but considered to be
low; none of these cats had received heartworm prophylaxis.
The remaining 10 cats (8 tigers and 2 cougars; mean age, 3.7 ±
3.0 years) were housed at Dreamworld in Queensland, Australia
(longitude, 174.8o E; latitude, 37.0o S), where the prevalence of
dirofilariasis in cats was considered to be low (0.45%)21; these
cats had received ivermectin (40 µg/kg [18.2 µg/lb], PO, once a
month) for heartworm prophylaxis since March of 1997.
Cats housed at the Denver Zoo had spent their entire
lives in Denver. Cats housed at Dreamworld in Queensland,
Australia, had been imported from the United States as cubs
without experiencing a heartworm season prior to importation (n = 4) or were native to Australia (6). The lion and golden cat housed at the Auckland Zoo had spent their entire lives
in New Zealand or Australia, and the serval had spent 1 heartworm season in Germany before being imported into New
Zealand. All control animals were housed in facilities that
allowed both outdoor and indoor exposure and were not mos-
Statistical analyses—Descriptive statistics (mean and
SD) were calculated. Values for categoric variables (eg, heartworm antibody test results) were compared between study
and control animals by means of χ2 or Fisher exact tests.
Values for continuous variables (eg, age) were compared
between groups by use of nonpaired t tests. Statistical analyses were performed with commercial software.d In all
instances, values of P < 0.05 were considered significant.
Results
Study animals—Medical records of 103 nondomestic cats housed at the Carnivore Preservation Trust during the study period were reviewed. Of these, 97 animals, representing 11 species, met the inclusion criteria
(Table 1). There were 47 males and 50 females. Mean
± SD age was 7.5 ± 4.9 years (range, 0.8 to 20.5 years).
Mean exposure time to mosquitoes was 7.3 ± 5.0 years.
Heartworm exposure (antibody test results)—
Results of heartworm antibody tests were available for
Table 1—Prevalences of heartworm exposure (ie, positive heartworm antibody test results) and heartworm infection (ie, positive heartworm antigen test results or identification of mature heartworms at necropsy) among nondomestic cats housed in an area in rural
North Carolina where Dirofilaria immitis is known to be endemic (study population) and among nondomestic cats housed in areas with
low prevalences of dirofilariasis in dogs and cats or in an area considered to be free from heartworms (control population).
No. of cats
Species
Caracal (Caracal caracal)
Tiger (Panthera tigris)
Serval (Leptailurus serval)
Ocelot (Leopardus pardalis)
Leopard (Panthera pardus)
Clouded leopard (Neofelis nebulosa)
Cougar (Puma concolor)
Jaguar (Panthera onca)
Snow leopard (Panthera uncia)
Lion (Panthera leo)
Margay (Felis weidii)
Golden cat (Felis temminckii)
Total
Antibody test results
Antigen test results
Study
Control
Study
Control
Study
Control
Necropsy results
28
21
21
7
6
4
3
3
2
1
1
0
97
0
13
1
0
7
0
2
0
4
1
0
1
29
20/23
15/18
12/18
5/6
3/4
0/1
0/3
1/1
0/0
0/0
1/1
0/0
57/75
0/0
0/13
1/1
0/0
0/11
0/0
0/2
0/0
0/0
0/1
0/0
0/1
1/29
0/9
0/11
0/10
0/4
0/4
0/2
0/0
0/3
0/2
0/1
0/1
0/0
0/47
0/0
0/5
0/0
0/0
0/7
0/0
0/0
0/0
0/4
0/0
0/0
0/0
0/16
0/5
1/7
0/3
0/2
0/0
0/3
0/0
0/0
0/0
0/1
0/0
0/0
1/21
Data are given as number with positive test result/number tested.
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75 of the 97 cats included in the study population.
Thirty-eight of the 75 were female, and 37 were male.
Mean ± SD age at the time of blood collection for testing was 7.15 ± 5.0 years (range, 0.8 to 20.5 years).
Results of antibody tests were positive for 57 of the 75
(76%) cats (Table 1). In comparison, results of antibody tests were positive for only 1 of the 29 (3%) control cats. These proportions were significantly (P
< 0.001) different. The single control cat with positive
antibody test results was a 1-year-old male serval from
New Zealand. Antibody test results for this cat were
only weakly positive (1:6 initially and 1:5 when reevaluated 2 months later), and heartworm antigen test
results were negative. In addition, results of thoracic
radiography and electrocardiography in this cat were
not suggestive of heartworm disease.
Mean age of study animals with positive heartworm antibody test results (7.3 ± 5.1 years) was not
significantly different from mean age of study animals
with negative antibody test results (6.6 ± 4.9 years),
and mean age of male cats (7.9 ± 5.5 years) was not
significantly different from mean age of female cats
(6.4 ± 4.3 years). The proportion of male study cats
with positive heartworm antibody test results (32/37
[86%]) was, however, significantly higher than the
proportion of female study cats with positive test
results (25/38 [66%]), indicating that male cats had a
significantly higher risk of heartworm exposure (ie,
positive antibody test result) than did female cats (relative risk, 1.3; 95% confidence interval, 1.01 to 1.71).
Postmortem examination—Postmortem examinations were performed on 21 of 27 study cats that died
during the study period. Mean age at the time of death
for the 21 cats was 12.3 ± 5.9 years; mean time cats
were exposed to mosquitoes without receiving heartworm prophylaxis was 11.2 ± 5.8 years (range, 1.6 to
23.1 years). Heartworms were identified during postmortem examination in only 1 of 21 (5%) cats. An 11.3year-old male tiger was found to be infected with a single heartworm. Infection was considered to be fatal as
the tiger died suddenly and had postmortem evidence
of severe pulmonary congestion and hemorrhage, and
no other cause of death was identified. Serologic tests
had never been performed on this animal.
Serologic testing was performed on 19 of 21 animals
that underwent postmortem examination. Antibody
tests alone were performed in 5 (results were positive in
3), antigen tests alone were performed in 7 (results were
negative in all 7), and antigen and antibody tests were
performed in 7 (results of antibody tests were positive in
6 and results of antigen tests were negative in all 7).
Thus, none of these 19 cats had postmortem or serologic evidence of mature heartworm infection, but 9 of 12
had evidence of heartworm exposure. Results of antigen
JAVMA, Vol 227, No. 1, July 1, 2005
Discussion
Results of the present study, conducted in an area
where D immitis is endemic, suggested that the prevalence of heartworm exposure (defined as detection of
serum anti-heartworm antibodies) among nondomestic
cats housed outdoors may be high, in that results of
heartworm antibody tests were positive for 57 of the 75
(76%) nondomestic cats housed at the Carnivore
Preservation Trust in North Carolina. In contrast, the
prevalence of mature heartworm infection was low,
with results of heartworm antigen tests being negative
in all 47 nondomestic cats housed at this facility that
were tested. Additionally, heartworms were detected
postmortem in only 1 of 21 (5%) nondomestic cats that
underwent necropsy.
Published estimates2,21-31 of the prevalence of heartworm exposure in domestic cats vary depending on geographic location, health status (eg, healthy cats vs cats
with clinical signs of respiratory tract disease), and living
conditions (privately owned vs shelter owned vs feral) of
the cats tested. For instance, in 1 study,25 26% of cats with
signs of cardiorespiratory disease examined at the North
Carolina State University or Texas A&M University veterinary teaching hospitals were found to be positive for
anti-heartworm antibodies. In another study,26 43% of
215 cats from 4 southeastern states examined because of
respiratory or gastrointestinal tract signs had anti-heartworm antibodies. On the other hand, a study27 of healthy
cats in College Station, Tex, found that 38% were positive
for anti-heartworm antibodies, and a national study28 (21
sites in 19 states) of 2,181 domestic cats, most of which
did not have any clinical abnormalities, found that 11.9%
had anti-heartworm antibodies.
Although less well defined, the geographic pattern
of heartworm infection in cats is similar to the geographic pattern of heartworm infection in dogs.2
Published estimates2,22-24,32 of the prevalence of heartworm infection in cats range from 0% to 14%, with a
median of 4% among cats in the southeastern United
States. Although there are no published data on prevalence of heartworm infection among domestic cats in
North Carolina, a recent unpublished studye found that
2% of shelter-owned cats in Raleigh, NC, that underwent necropsy were infected with heartworms.
Virtually all previous reports of heartworm infection
in nondomestic cats are single case reports. Heartworm
infection has been reported13-20,33 in 12 species of nondomestic cats, but to the authors’ knowledge, there has been
no systematic evaluation of the prevalence of heartworm
infection among nondomestic cats. A necropsy study33 of
16 bobcats in the Carolinas did not reveal any indications
of adult D immitis infection, and a study34 of 47 Florida
panthers did not reveal microfilariae of D immitis.
However, it is generally accepted that nondomestic cats
rarely have circulating D immitis microfilariae.15
The present study sought to determine prevalences
of heartworm exposure and mature infection among
nondomestic cats residing in central North Carolina, an
area in which D immitis is known to be endemic.
Because serologic tests for anti-heartworm antibodies
Scientific Reports: Original Study
141
WILDLIFE
Heartworm infection (antigen test results)—Results
of heartworm antigen tests performed on 47 study and 16
control cats were negative. Mean age of the study cats at
the time of heartworm antigen testing was 9.1 ± 5.3 years,
and mean time cats were exposed to mosquitoes was 9.0
± 5.4 years. Both antigen and antibody tests were performed in only 28 cats; results were concordant (ie,
results for both tests were negative) in only 4 cats.
tests and postmortem examination were negative in all
14 cats that had undergone both evaluations.
WILDLIFE
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and heartworm antigen have not been and are not likely
to be validated in nondomestic cats, we also reviewed
test results for 29 nondomestic cats of 6 species residing
in areas thought to be free from heartworms or to have
only low prevalences of heartworm infection to demonstrate that false-positive results would be uncommon.
In the present study, results of heartworm antibody
tests were positive for 57 of 75 (76%) study cats, indicating that these cats had been exposed to the organism
and that at least partial larval development had
occurred. This proportion was significantly higher than
the proportion of control cats with positive heartworm
antibody test results (1/29 [3%]). Cats in the study population with positive test results were not significantly
older than cats with negative test results, but males were
significantly more likely to have positive test results than
were females, even though ages and exposure periods
for male and female cats were not significantly different.
Results of heartworm antigen tests were negative
for all 47 cats in the study population and all 16 control cats that were tested. This was not surprising as the
antigen test has been shown to be positive in < 50% of
heartworm-infected domestic cats.35-38 Results of antigen testing and postmortem examination were concordant for all 14 cats that underwent both tests, although
the clinical importance of this finding in a population
with such a low prevalence of heartworm infection is
not clear. These data, however, do indicate that heartworm antigen tests do not result in a high percentage
of false-positive results in nondomestic cats.
In the present study, heartworm infection was also
identified by means of postmortem examination of 21
nondomestic cats with a mean ± SD time of exposure to
mosquitoes of 11.2 ± 5.6 years. Of these, only 1 (5%), a
tiger, was positive. Infection was considered to be fatal as
the tiger died suddenly, severe pulmonary congestion and
hemorrhage were seen during the postmortem examination, and no other cause of death was identified. To our
knowledge, the only previous report16 of heartworm-related death in a nondomestic cat involved a tiger,16 and of the
12 nondomestic cats previously confirmed to have heartworm infection by means of postmortem examination, 3
were tigers.15,16 On the other hand, in the present study, 21
of 97 cats in the study population and 7 of 21 cats that
underwent a postmortem examination were tigers. Thus,
the single positive result in a tiger may merely be reflective of the population studied.
Results of the present study, in regard to heartworm
infection, were in agreement with published results for
domestic cats. For instance, the mean reported prevalence
of heartworm infection among domestic cats in the southeastern United States is 5.5% (median, 4%).2,22,24 However,
the prevalence of heartworm exposure among nondomestic cats in the present study (76%) was higher than that
reported for domestic cats. Although the reported prevalence of heartworm exposure in domestic cats varies with
geographic location, health status, and living conditions,2,21-25,27-31 the highest reported prevalences have been
38% for cats without any apparent signs of clinical disease27 and 43% for cats with clinical signs of disease.26 The
higher prevalence of heartworm exposure in the present
study was most likely reflective of the outdoor lifestyle
and years of exposure (mean ± SD, 7.15 ± 5 years) of the
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Scientific Reports: Original Study
nondomestic cats included in the study as well as the high
prevalence of exposure among domestic and nondomestic dogs in the study region.1,e,f The higher risk of heartworm exposure among male nondomestic cats in the present study was similar to results of a previous study,39 but
higher prevalence in males has not been apparent in every
study.40 In the present study, the ratio of antibody-positive
cats to necropsy-positive cats was 12.5:1, which was
slightly higher than the reported ratio for domestic cats,
which in previous studies3,24,28,39,41,42 ranged from 1.4:1 to
13:1 (mean, 5.1:1; median, 6:1). This supports the previous suggestion that nondomestic cats may be more resistant to heartworm infection than domestic cats and
dogs.15 The discrepancy between antigen and antibody
test results in the present study (76% of heartworm antibody test results positive vs 0% of heartworm antigen test
results) was not surprising as the antigen test is known to
be insensitive in cats,35,38,41,42 yielding negative results in
cats infected with male heartworms or immature heartworms, whereas the antibody test typically yields positive
results in > 80% of infected cats and in cats exposed to
heartworms that do not develop mature infections.37,40
Weaknesses of the present study included its retrospective nature and the small number of cats studied.
Each animal did not undergo all diagnostic tests. In
addition, serologic tests were performed by 2 commercial laboratories, and records as to which laboratory performed tests for which animals were not always available. Another weakness of the present study was that the
serologic tests that were used have not been validated in
the species studied. We attempted to address this by testing control cats with a low likelihood of exposure to
demonstrate that these serologic tests did not yield a
high proportion of false-positive results. It should be
noted that although unlikely, it is possible that a parasite
other than D immitis infected the study cats, but not the
control cats, and caused the false-positive results for the
antibody test. A previous study,35 however, showed no
cross-reactivity with other gastrointestinal or respiratory
tract parasites for antibody tests used in domestic cats.
Unfortunately, the control population was not completely reflective of the study population in terms of species
included, and there was no positive control group. In
addition, postmortem examinations were not specifically directed at detection of heartworms, and some infected cats may therefore have not been identified. This and
the fact that cats exposed to or infected with heartworms
can revert to an antibody-negative status over time
might have resulted in underestimation of heartworm
exposure and infection rates in the present study.
Certain conclusions can be drawn from results of
the present study regarding the prevalence of heartworm exposure and infection in nondomestic cats. Our
results suggested that in areas where the organism is
endemic, such as the southeastern United States, nondomestic cats are at risk for heartworm infection, and
chemoprophylaxis should be considered, even though
this represents an extralabel use of these products.
Infection rates in nondomestic cats appear to approximate those of domestic cats in the same geographical
region, but exposure rates are higher, indicating that
nondomestic cats may be more resistant to heartworm
infection than domestic cats. Nondomestic male cats
JAVMA, Vol 227, No. 1, July 1, 2005
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appear to be at greater risk for heartworm exposure
than nondomestic female cats.
a.
b.
c.
d.
e.
f.
Heartgard Plus, Merial, Duluth, Ga.
Antech Diagnostics, Irvine, Calif.
Heska Corp, Fort Collins, Colo.
GraphPad Software Inc, version 4, San Diego, Calif.
Kolstad A, Newcome M, Smith A, College of Veterinary
Medicine, North Carolina State University, Raleigh, NC:
Personal communication, 2004.
Ferris K, Department of Clinical Sciences, College of Veterinary
Medicine, North Carolina State University, Raleigh, NC:
Personal communication, 2003.
References
JAVMA, Vol 227, No. 1, July 1, 2005
Scientific Reports: Original Study
143
WILDLIFE
1. Canine heartworm disease survey. In: Seward RL, ed.
Proceedings of the Heartworm Symposium ’01. Batavia, Ill: American
Heartworm Society, 2001;frontpiece.
2. Ryan WG, Newcomb KM. Prevalence of feline heartworm
disease—a global review. In: Soll MD, Knight DH, eds. Proceedings of
the Heartworm Symposium ’95. Batavia, Ill: American Heartworm
Society, 1995;79–86.
3. Gamble K, Rubin GJ. Dirofilaria immitis in a pale-faced saki
(Pithecia pithecia), in Proceedings. Annu Meet Am Assoc Zoo Vet
1996;418–420.
4. Snyder DE, Hamir AN, Nettles VF, et al. Dirofilaria immitis
in a raccoon (Procyon lotor). J Wildl Dis 1989;25:130–131.
5. Neiffer DL, Klein EC, Calle PP, et al. Mortality associated
with melarsomine dihydrochloride administration in two North
American river otters (Lontra canadensis) and a red panda (Ailurus
fulgens fulgens). J Zoo Wildl Med 2002;33:242–248.
6. Kiku M, Byeong-Kirl B, Chae-Woong L. Eurasian otter
(Lutra lutra), a definitive host for Dirofilaria immitis. J Zoo Wildl Med
2003;34:200–201.
7. Sasai HKK, Sasaki T, Koyama S, et al. Echocardiographic diagnosis of dirofilariasis in a ferret. J Small Anim Pract 2000;41:172–174.
8. Sacks BN, Caswell-Chen EP. Reconstructing the spread of
Dirofilaria immitis in California coyotes. J Parasitol 2003;89:319–323.
9. Crooks KRS, Scott C, Van Vuren DH. Exotic disease and an
insular endemic carnivore, the island fox. Biol Conserv 2001;98:55–60.
10. Loomis MR, Lee CD. Canine heartworm infection in African
cape hunting dogs (Lycaon pictus), in Proceedings. Annu Meet Am
Assoc Zoo Vet 1984;137.
11. Kazacos KR, Edberg EO. Dirofilaria immitis infection in
foxes and coyotes in Indiana. J Am Vet Med Assoc 1979;175:909–910.
12. Kreeger TJ, Seal US, Callahan M, et al. Treatment and prevention with ivermectin of dirofilariasis and ancylostomiasis in captive gray wolves (Canis lupus). J Zoo Wildl Med 1990;21:310–317.
13. Vellayan S, Omar B, Oothuman P, et al. The golden cat, Felis
temminckii, as a new host for Dirofilaria immitis. J Vet Malaysia 1989;
1:87–89.
14. Deem SL, Heard DJ, LaRock R. Heartworm (Dirofilaria
immitis) disease and glomerulonephritis in a black-footed cat (Felis
nigripes). J Zoo Wildl Med 1998;29:199–202.
15. Otto GF. Occurrence of heartworm in unusual locations and
unusual hosts. In: Morgan HC, ed. Proceedings of the Heartworm
Symposium ’74. Bonner Springs, Kan: VM Publishing, 1975;6–13.
16. Kennedy S, Patton S. Heartworms in a Bengal tiger. J Zoo
Anim Med 1981;12:20–22.
17. Zahedi M, Vellayan S, Jeffery J, et al. A case of double infection with Brugia pahangi and Dirofilaria immitis in a Malaysian
clouded leopard, Neofilis nebulosa. Vet Parasitol 1986;21:135–137.
18. Forrester DJ. Florida panthers and bobcats. In: Parasites and
diseases of wild mammals in Florida. Gainesville, Fla: University of
Florida Press, 1992;174–203.
19. Strauss JM, Sivanandam S. A double infection of filariasis in a
black panther (Panthera pardus) from Pahang. Med J Malaya 1966;20:336.
20. Pence DB, Tewes ME, Laack LL. Helminths of the ocelot
from southern Texas. J Wildl Dis 2003;39:683–689.
21. Atwell RB, Evans EA, Platt SR, et al. Feline dirofilariasis: epidemiology and diagnostics over 20 years in Australia. In: Seward RL,
ed. Proceedings of the Heartworm Symposium ’01. Batavia, Ill: American
Heartworm Society, 2001;35–39.
22. Snyder PS, Levy JK, Salute ME, et al. Performance of serologic tests used to detect heartworm infection in cats. J Am Vet Med Assoc
2000;216:693–700.
23. Hermesmeyer M, Limberg-Child RK, Murphy AJ, et al.
Prevalence of Dirofilaria immitis infection among shelter cats.
J Am Vet Med Assoc 2000;217:211–212.
24. Nelson CT, Young TS. Incidence of Dirofilaria immitis in
shelter cats from southeast Texas. In: Seward RL, Knight DH, eds.
Proceedings of the Heartworm Symposium ’98. Batavia, Ill: American
Heartworm Society, 1998;63–73.
25. Atkins CE, DeFrancesco TC, Miller MW, et al. Prevalence of
heartworm infection in cats with signs of cardiorespiratory abnormalities. J Am Vet Med Assoc 1998;212:517–520.
26. Robertson-Plouch CK, Dillon AR, Brawner WR, et al.
Prevalence of feline heartworm infections among cats with respiratory and gastrointestinal signs: results of a multicenter study. In:
Seward RL, Knight DH, eds. Proceedings of the Heartworm Symposium
’98. Batavia, Ill: American Heartworm Society, 1998;57–62.
27. Miller MW, Zoran DL, Relford RL, et al. Seroprevalence of
antibodies to Dirofilaria immitis in asymptomatic cats in the
Bryan/College Station area of Texas. In: Otto GF, ed. Proceedings of the
Heartworm Symposium ’89. Washington, DC: American Heartworm
Society, 1989;159–160.
28. Miller MW, Atkins CE, Stemme K, et al. Prevalence of exposure
to Dirofilaria immitis in cats in multiple areas of the United States. In:
Seward RL, Knight DH, eds. Proceedings of the Heartworm Symposium
’98. Batavia, Ill: American Heartworm Society, 1998;161–166.
29. Kramer L, Genchi C. Feline heartworm infection: serological survey of asymptomatic cats living in northern Italy. Vet Parasitol
2002;104:43–50.
30. Kendall K, Collins GH, Pope SE. Dirofilaria immitis in cats
from inner Sydney. Aust Vet J 1991;68:356–357.
31. Kalkstein TS, Kaiser L, Kaneene JB. Prevalence of heartworm infection in healthy cats in the lower peninsula of Michigan.
J Am Vet Med Assoc 2000;217:857–861.
32. Levy JK, Snyder PS, Taveres LM, et al. Prevalence and risk
factors for heartworm infection in cats from northern Florida.
J Am Anim Hosp Assoc 2003;39:533–537.
33. Miller GC, Harkema R. Helminths of some wild mammals
in the southeastern United States. Proc Helminthological Soc 1968;
35:118–125.
34. Lamm MG, Roelke ME, Greiner EC. Microfilariae in the
free-ranging Florida panther (Felis concolor coryi), in Proceedings.
Annu Meet Am Assoc Zoo Vet 1995;275–276.
35. McCall JW, Guerrero J, Suakorndej P, et al. Evaluation of the
accuracy of heartworm antigen and antibody tests for cats. In:
Seward RL, Knight DH, eds. Proceedings of the Heartworm Symposium
’98. Batavia, Ill: American Heartworm Society, 1998;127–133.
36. Knight DH, Doiron DW, Longhofer SL, et al. Guidelines for the
diagnosis, prevention, and management of heartworm (Dirofilaria immitis) infection in cats. In: Seward RL, ed. Proceedings of the Heartworm
Symposium ’01. Batavia, Ill: American Heartworm Society, 2001;267–273.
37. Atkins C. The diagnosis of feline heartworm infection.
J Am Anim Hosp Assoc 1999;35:185–187.
38. Genchi C, Kramer L, Venco L, et al. Comparison of antibody and antigen testing with echocardiography for detection of
heartworm (Dirofilaria immitis) in cats. In: Seward RL, Knight DH,
eds. Proceedings of the Heartworm Symposium ’98. Batavia, Ill:
American Heartworm Society, 1998;173–177.
39. Dillon R. Clinical significance of feline heartworm disease.
Vet Clin North Am Small Anim Pract 1998;28:1547–1565.
40. Atkins CE, DeFrancesco TC, Coats JR, et al. Heartworm
infection in cats: 50 cases (1985–1997). J Am Vet Med Assoc 2000;
217:355–358.
41. Piche C, Cavanaugh MT, Donoghue AR, et al. Result of antibody and antigen testing for feline heartworm infection at HESKA
Veterinary Laboratories. In: Seward RL, Knight DH, eds. Proceedings
of the Heartworm Symposium ’98. Batavia, Ill: American Heartworm
Society, 1998;139–143.
42. Watkins BF, Toro M, Toro G. Prevalence of heartworm antibody
and antigen-positive sera among submissions to a commercial laboratory
in the USA. In: Seward RL, Knight DH, eds. Proceedings of the Heartworm
Symposium ’98. Batavia, Ill: American Heartworm Society, 1998;145–152.