Professional Documents
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www.elsevier.com/locate/jfms
a
Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida,
2015 S.W. 16th Avenue, Box 100126, Gainesville, FL 32610, USA
b
Department of Large Animal Clinical Sciences, College of Veterinary Medicine,
University of Florida, Gainesville, FL 32610, USA
c
Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences,
Colorado State University, Fort Collins, CO 80523, USA
d
Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University,
Raleigh, NC 27606, USA
e
Department of Small Animal Clinical Sciences, College of Veterinary Medicine,
University of Tennessee, Knoxville, TN 37996, USA
1098-612X/$30.00/0 Ó 2003 ESFM and AAFP. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.jfms.2003.11.005
288 B.J. Luria et al.
PCR assays
DNA was extracted from whole blood as previously Results
described. PCR assays that amplify M. haemofelis
DNA, M. haemominutum DNA, Ehrlichia spp. DNA, The most common infections in feral cats were
and A. phagocytophilum DNA were performed B. henselae and FCoV, followed by Mycoplasma
on each DNA sample (Brewer et al., 2003; spp., D. immitis, and T. gondii (Table 1). Of the
Jensenet al., 2001). 101 (18.3%) cats that had antibodies to FCoV, most
had low antibody titers with only 7 cats having
Statistical analysis titers of 1:320 or greater. Three of 553 cats (0.5%)
were positive for both FeLV and FIV. All D. immitis
Presence of FeLV antigen, FIV antibody, D. immitis Ag positive cats were D. immitis Ab positive, but
antigen, M. haemofelis DNA, M. haemominutum only 7 of 64 (10.9%) D. immitis Ab positive cats
DNA, Ehrlichia spp. DNA, or A. phagocytophilum were D. immitis Ag positive. Concurrent M. haemo-
DNA in the blood or serum documents current felis and M. haemominutum infections were
infection. Presence of antibodies against FCoV, detected in 19 of 484 cats (3.9%). Of the 67
Table 3 Risk of disease (outcome) associated with infection with other organisms (exposure)
Outcome Exposure Odds 95% confidence P-value
ratio interval
FeLV FIV 3.91 1.07e14.36 0.03
M. haemominutum 3.19 1.08e9.38 0.03
FIV Coronavirus 2.50 1.13e5.56 0.02
M. haemofelis 10.71 4.67e24.56 !0.001
M. haemominutum 4.74 1.86e12.10 0.001
Coronavirus T. gondii IgM 2.99 1.13e7.89 0.02
M. haemominutum 2.14 1.14e4.03 0.01
D. immitis Ab T. gondii IgG 3.34 1.73e6.48 !0.001
D. immitis Ag 59.8 7.5e476.3 !0.01
D. immitis Ag T. gondii IgG 6.98 1.52e32.01 0.01
M. haemominutum M. haemofelis 9.14 4.54e18.37 !0.001
Ehrlichia spp. None e e e
T. gondii IgM T. gondii IgG 6.31 2.34e17.02 !0.001
T. gondii IgG T. gondii IgM 6.31 2.34e16.99 !0.001
M. haemominutum 2.48 1.18e5.18 0.01
B. henselae Ab None e e e
Infectious diseases in feral cats 291
1989). Variations in reported prevalence rates are antibody never develop FIP. A serologic survey in
most likely due to regional variations in the popula- Davis, CA reported antibodies to FCoV in 20% of
tions tested, the health of the cats tested and pet cats (nZ33) and 87% of purebred cats (nZ108)
whether cats were selected from high vs. low risk in catteries (Pedersen, 1976). A recent study of
populations. Infection rates were highest (43.9%) stray cats in Britain (nZ517) identified a prevalence
in clinically ill cats (nZ3323) in a population sam- of FCoV antibodies in 22.4% of cats (Muirden, 2002).
pled in Japan (Ishida et al., 1989). In the United In the current study, the prevalence of FCoV anti-
States, most serosurveys are reported in sick and bodies (18.3%) was lower than reported in pet cats
high-risk pet cats. In a national survey of sick and and the antibody titers were low in most seroreac-
highrisk pet cats, prevalence of FeLV and FIV in tive cats. This suggests minimal exposure to FCoV
Florida (nZ2643) was 12.8% and 8.4%, respectively in feral cats. Thus, feral cats in this population do
(O’Connor et al., 1991). A smaller study of pet cats not appear to be a greater source than pet cats for
in southeastern Florida (nZ95) also reported an FIV shedding of coronavirus in the environment. This
prevalence of 8.4% (Fisch and Altman, 1989). In the might be due to the lower population density of
current study, FeLV and FIV prevalences were rela- feral cats compared to pet cats and their practice
tively low (FeLV 3.3%, FIV 5.2%) when compared of burying feces outside in contrast to sharing a
to infection rates reported for owned cats in the litter box. The presence of coronavirus antibodies
United States. Thus, feral cats do not appear to was statistically associated with FIV, T. gondii
be a greater reservoir for these retroviruses than IgM, and M. haemominutum, however, none of
pet cats. the relationships were very strong (Table 3). Oro-
Historically, free-roaming, sexually intact male nasal contact with feces is a route of transmission
cats have been found to have the highest infection for both T. gondii and FCoV, thus this could be an
rate for FIV since they are more likely to be territo- explanation for the association between these
rial and to be engaged in catfights (Ishida et al., two organisms. However, one might have expected
1989). The increased risk of Mycoplasma spp. in an association between FCoV and T. gondii IgG
males and strong association between FIV and antibody as well. In a study of cattery and stray
Mycoplasma spp. identified in the current study cats (nZ275) in Davis, CA, concurrent infections
suggest that bite wounds may play a role in trans- with multiple other infectious diseases were not
mission of Mycoplasma spp. as well. The associa- found to be associated with increased risk for
tion of retrovirus infections with Mycoplasma developing FIP (Foley et al., 1997).
infection also suggests that either the immunosup- Haemoplasmosis ( formerly haemobartonellosis)
pressive effects of the retroviruses enhance Myco- is caused by M. haemofelis and M. haemominutum.
plasma spp. as a secondary infection or that the Haemobartonella felis has undergone recent
risk factors are similar for both retroviruses and reclassification into the genus Mycoplasma based
mycoplasmas. A recent study of pet cats (nZ46) on analysis of 16S ribosomal ribonucleic acid gene
in Israel also identified a correlation between ret- sequences. H. felis large form (Ohio variant) and
roviruses and detection of Mycoplasma spp. via H. felis small form (California variant) have been
blood smear and reported an increased morbidity renamed M. haemofelis and M. haemominutum,
in cats with coinfection (Harrus et al., 2002). Simi- respectively (Foley and Pedersen, 2001;
lar findings were documented in experimentally in- Neimarket al., 2001, 2002; Rikihisa et al., 1997).
fected cats (George et al., 2002). In experimentally inoculated cats, increased mor-
The clinical condition of feline infectious perito- bidity is associated with M. haemofelis compared
nitis (FIP) is caused by a pathogenic coronavirus. It to M. haemominutum (Foley et al., 1998; Jensen
manifests in a variety of clinical signs and can et al., 2001; Westfall et al., 2001). Mycoplasma
affect nearly any body system. It is thought that haemominutum has been detected in both natu-
the FIP virus (FIPV) is the result of de novo muta- rally exposed cats and their fleas. It is taken into
tions of the minimally pathogenic feline enteric fleas during a blood meal, but transmission to naı̈ve
coronavirus (FECV) (Vennema et al., 1998). The cats was not documented in a preliminary study of
term feline coronavirus (FCoV) includes both three cats (Woods et al., 2003). However, M. hae-
viruses. The major route of transmission of FECV mofelis was transmitted from an infected cat into
is via fecal shedding of the virus and subsequent a naı̈ve cat by C. felis (Woods and Lappin, Unpub-
oronasal contact. Establishing a diagnosis of FIP lished data, 2003). These results suggest that
can be difficult, but commonly includes testing C. felis may be a mode of transmission of these or-
for antibodies to coronavirus. Positive tests are ganisms between cats. Our findings that Mycoplas-
not diagnostic of disease, but rather only indicate ma spp. infection is more common in male cats and
exposure to FCoV. In fact, most cats with FCoV FIV-infected cats suggest that bite wounds may
292 B.J. Luria et al.
play a role in transmission. Based on cytology, detection, resulting in false-negative Ag test re-
which cannot accurately differentiate M. haemofe- sults. In a recent study evaluating the efficacy of
lis and M. haemominutum, worldwide prevalence serologic tests for the detection of heartworm, Ag
of haemoplasmosis ranges from 3.6% to 42% of cats tests detected 79e86% of heartworm infections
(Grindem et al., 1990; Harbutt, 1969; Nash and and were highly specific, whereas Ab tests were
Bobade, 1986; Yamaguchi et al., 1996). The highest less sensitive, detecting 62e72% of heartworm
prevalence was in an isolated group of farm cats infections, and had a wider range of false-positive
(nZ48) studied in Oxford, UK (Yamaguchi et al., results than Ag tests (Berdoulay et al., 2002). Infec-
1996). In another study of pet cats (nZ123) in Wake tions in cats diagnosed mostly by necropsy in the
County, NC, a prevalence rate of 4.6% was identi- United States have been reported in 38 of the 50
fied (Grindem et al., 1990). A third prevalence states with a prevalence of 0 to 14% (Atkins et al.,
study was in pet cats (nZ155) at the University of 2000; Hermesmeyer et al., 2000; Kalkstein et al.,
Glasgow, Scotland, where the prevalence was 2000; Kendall et al., 1991; Labarthe et al., 1997;
23.2% (Nash and Bobade, 1986). Genetically, McCall et al., 1994; Willard et al., 1988). A preva-
M. haemominutum from the United States and lence study of pet cats (nZ7969) in the United
United Kingdom are virtually identical (Tasker States identified Ab and Ag prevalence in Florida
et al., 2001). A recent report surveyed 426 pet cats to be 22.5% and 4.8%, respectively (Watkins
using a PCR assay at the University of Bristol, UK et al., 1998). The prevalence of infection in the
and identified a prevalence of 1.4% and 16.9% for current study is lower than the previous report
M. haemofelis and M. haemominutum, respec- from this region. Consequently, this population of
tively (Tasker et al., 2003a,b). In 220 pet cats in cats does not appear to be at greater risk of
the United States surveyed with a PCR assay, 4.5% D. immitis infection when compared to pet cats.
were infected with M. haemofelis, 12.7% with M. All of the Ag positive cats in this study were also
haemominutum, and 2.3% were infected with both Ab positive, but only 10.9% of Ab positive cats were
Mycoplasma spp. giving an overall prevalence of Ag positive.
19.5% (Jensen et al., 2001). These studies demon- Experimentally, cats have been infected with
strate considerable variation in percent prevalence Neorickettsia risticii ( previously E. risticii)
depending on the population studied and the tech- and A. phagocytophilum ( previously E. equi) (Daw-
nique used to establish infection. The prevalence son et al., 1988; Dumler et al., 2001; Lewis et al.,
in the current study falls within the lower end of 1975; Neer et al., 2002). Naturally occurring ehrli-
the reported ranges for pet cats, thus, feral cats chial infections in cats have been documented via
do not serve as a greater reservoir of mycoplasmas antibody assays with seroprevalences ranging from
than pet cats. In the current study, cats infected 12% to 82.4% depending on location and infecting
with one Mycoplasma species were at increased risk species (Bouloy et al., 1994; Dawson et al., 1988;
to be infected with the other, which supports the Peavy et al., 1997; Perry et al., 1989). A national
hypothesis that the route of transmission for both seroprevalence study of cats identified antibodies
may be similar. Associations were found between against E. canis and N. risticii in 29.2% of 583 cats
FeLV, FIV and Mycoplasma spp. as well. There is tested with the predominant species being N. risti-
no clear explanation for the associations between cii (28.5%) (Stubbs et al., 2000). Although these
Mycoplasma spp. and FCoV or T. gondii based on studies report seroprevalences based on antibody
the known biologic behavior of these agents. testing, the relationship between antibodies and
Dirofilaria immitis is a parasite that primarily infection with ehrlichiosis or anaplasmosis in cats
affects dogs, however, diagnosis in cats is on the remains to be determined (Breitschwerdt et al.,
rise (Atkins et al., 1998, 2000; Kalkstein et al., 2002; Neer et al., 2002). Some pet cats in the
2000; Snyder et al., 2000). This challenging diagno- United States have been shown by PCR testing
sis is made based on clinical signs, radiographic and and genetic sequencing to be infected by an
echocardiographic findings, and serologic testing. E. canis-like organism and A. phagocytophilum
Tests are available for both Ag and Ab (Goodwin, (Breitschwerdt et al., 2002; Lappin et al., 2003).
1998; Prieto et al., 1997), however, neither has Cats in this study were tested using PCR primers
proven to be solely efficacious for definitive diag- that can amplify Ehrlichia, Anaplasma and Neorick-
nosis. The presence of antibody does not neces- ettsia spp (Brewer et al., 2003). As no amplification
sarily indicate a current infection, only exposure products were obtained from any of the cats sur-
at some previous time. Antigen tests detect pro- veyed in the current study, species-specific PCR
teins from mature female worms. Low worm bur- tests which are also available were not utilized
den and male-only heartworm infections in cats in this study (Breitschwerdt et al., 1998). It is
reduce the quantity and type of Ag available for likely that A. phagocytophilum is transmitted by
Infectious diseases in feral cats 293
Ixodes spp. ticks which are uncommon in Florida Bartonella henselae, the organism that causes
(Akucewich et al., 2002). The failure to detect in- cat scratch disease (CSD) in humans, is a curved
fections in this population of feral cats suggests that gram-negative bacillus that infects multiple spe-
they are not associated with infection of pet cats. cies, including cats. The domestic cat is considered
Toxoplasma gondii is an obligate intracellular the reservoir for this organism. Infected cats can
protozoan parasite. Felids serve as definitive hosts, remain bacteremic for months to years. The patho-
transiently passing oocysts into the environment. genicity of B. henselae in cats remains undeter-
Virtually all warm blooded animals serve as inter- mined, however, most infected cats appear
mediate hosts. Infection is usually acquired trans- healthy (Breitschwerdt and Kordick, 2000). The or-
placentally, by ingestion of tissue cysts or by ganism is associated with multiple human diseases,
ingestion of sporulated oocysts. In humans, T. gon- including CSD, bacillary angiomatosis, visceral pel-
dii is of particular risk to pregnant women, with up iosis, bacteremia and endocarditis (Adal et al.,
to 50% of infections during pregnancy transmitted 1994; Tompkins, 1997). These conditions can be life
to the fetus (Jones et al., 2001). Since most cats threatening in immunosuppressed humans. The cat
and people do not clear the organism from tissues flea, C. felis, is the primary vector of Bartonella
once infected, presence of IgM or IgG antibodies spp. between cats (Chomel et al., 1996). Diagnosis
generally denotes infection (Lappin, 1996). Howev- is commonly made via IFA for antibodies to the or-
er, since the oocyst shedding period is short, most ganism. Alternative diagnostic tests include blood
seroreactive cats have completed the oocyst shed- culture (Brenner et al., 1997) and PCR (Jensen
ding period. Previously infected cats can occasion- et al., 2000). A serologic study of pet cats (nZ
ally repeat oocyst shedding, but the numbers are 628) throughout the United States and in some
generally low and are not likely a significant public areas of Canada identified an overall seropreva-
health risk. Serologic prevalence data indicate that lence of 27.9% (range 3.7% to 54.6%) (Jameson
toxoplasmosis is one of the most common infec- et al., 1995). Seroprevalence was highest in warm,
tions of cats and humans throughout the world humid areas where flea infestation is more likely. A
(Dubey, 1973; Dubey et al., 2002; Hill et al., study of both pet and feral cats in Baltimore, MD
2000; Jones et al., 2001). Approximately 30% of found an association between seroreactivity to
pet cats and 22% of humans in the United States B. henselae and T. gondii (Childs et al., 1994).
have T. gondii antibodies (Dubey, 1973; Hill Although B. henselae was the most common infec-
et al., 2000; Jones et al., 2001). A recent study of tion identified in this study (33.6%), it was the only
pet cats (nZ275) in rural Ohio identified a preva- organism that did not have any associated risks for
lence of 48% (Dubey et al., 2002). Another study coinfection with other organisms. Female cats
of cats (nZ205) from Colorado found a prevalence were at slightly greater risk for being infected than
of 19.7% in pet cats and 29.8% in cats from a humane males. Flea infestations have been identified in 92%
shelter (Hill et al., 2000). In the only national sero- of feral cats in Florida (Akucewich et al., 2002),
prevalence study of clinically ill pet cats in the thus grooming and ingestion of fleas could explain
United States (nZ12,628) an overall prevalence an increased rate of infection, particularly females
of 31.6% was documented, with 37.4% in the south- grooming flea infested kittens. Exposure to kittens
eastern region of the United States (Vollaire et al., with fleas is the highest risk factor for CSD in
2003). The prevalence observed in the current humans as well (Zangwill et al., 1993).
study (2.0% IgM, 8.9% IgG, 1.3% IgMCIgG) was lower The results of this study should be interpreted
than that reported for pet cats. Thus, feral cats do with some caution. The samples were collected
not appear to be more likely to shed the organism from feral cats that were trapped by caretakers
into the human environment than pet cats. It has for the purposes of neutering. Thus, the tested
been hypothesized that feral cats may be more population is skewed toward feral cats that have
likely than pet cats to ingest intermediate hosts some association with humans and is not a random
harboring tissue cysts, however, there is no associ- sample of feral cats. However, since feral cat inter-
ation between T. gondii prevalence in feral cats action with humans is a primary issue that concerns
and wild rodents (DeFeo et al., 2002). Although public health officials, this is an appropriate popu-
previous studies have recognized an association lation of cats to test. Some testing techniques,
between infections with FIV and T. gondii (Witt such as heartworm antibody, indicate only expo-
et al., 1989), no association was observed in this sure to infection, but not necessarily current infec-
study. Based on the known biologic behavior of tion. This is an unavoidable limitation of the
these agents, there is no clear explanation for the current assays available, and is a problem also
associations between T. gondii IgG antibodies and encountered in the diagnosis of infections in pet
D. immitis or M. haemominutum. cats. We did not test cats for all of the important
294 B.J. Luria et al.
infectious diseases of public health concern. The Breitschwerdt, E.B., Abrams-Ogg, A.C., Lappin, M.R., Bienzle,
most noticeable omission is rabies, for which there D., Hancock, S.I., Cowan, S.M., Clooten, J.K., Hegarty, B.C.,
Hawkins, E.C., 2002. Molecular evidence supporting Ehrlichia
are no accurate ante-mortem tests. In addition, we canis-like infection in cats. Journal of Veterinary Internal
did not test for internal or external parasites or Medicine 16, 642e649.
enteropathogens. Breitschwerdt, E.B., Hegarty, B.C., Hancock, S.I., 1998. Se-
Feral cats in this study had similar prevalence of quential evaluation of dogs naturally infected with Ehrlichia
infections compared to those published for pet cats canis, Ehrlichia chaffeensis, Ehrlichia equi, Ehrlichia ewingii,
or Bartonella vinsonii. Journal of Clinical Microbiology 36,
in the United States. This suggests that feral cats 2645e2651.
assessed in this study appear to be of no greater Breitschwerdt, E.B., Kordick, D.L., 2000. Bartonella infection in
risk to human beings or other cats than pet cats. animals: carriership, reservoir potential, pathogenicity, and
zoonotic potential for human infection. Clinical Microbiology
Reviews 13, 428e438.
Breitschwerdt, E.B., Kordick, D.L., Malarkey, D.E., Keene, B.,
Hadfield, T.L., Wilson, K., 1995. Endocarditis in a dog due to
Acknowledgements infection with a novel Bartonella subspecies. Journal of
Clinical Microbiology 33, 154e160.
Supported in part by The Winn Feline Foundation Brenner, S.A., Rooney, J.A., Manzewitsch, P., Regnery, R.L.,
1997. Isolation of Bartonella (Rochalimaea) henselae: effects
and the Harold H. Morris Trust Fund. Feline leuke- of methods of blood collection and handling. Journal of
mia virus and feline immunodeficiency virus testing Clinical Microbiology 35, 544e547.
materials and services were contributed by IDEXX Brewer, M., Lappin, M.R., Jensen, W.A., 2003. Detection of
Laboratories. The authors acknowledge Melissa Mycoplasma haemofelis, Mycoplasma haemominutum, and
Brewer, Jennifer Hawley, Julie Bradley, Kim Seitz, Ehrlichia spp. DNA in a multiplex polymerase chain reaction
assay (abstract). Journal of Veterinary Internal Medicine 17,
Juli Hester, and Hasuna Hines for technical 425e426.
assistance. Childs, J.E., Rooney, J.A., Cooper, J.L., Olson, J.G., Regnery,
R.L., 1994. Epidemiologic observations on infection with
Rochalimaea species among cats living in Baltimore, Md.
Journal of the American Veterinary Medical Association 204,
1775e1778.
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