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ISRAEL JOURNAL OF
VETERINARY MEDICINE
Vol. 54 (2), 1999
A SEROEPIDEMIOLOGICAL STUDY OF FELINE CORONAVIRUS,
FELINE IMMUNODEFICENCY VIRUS AND FELINE LEUKEMIA
VIRUS
AMONG CATS IN ISRAEL
G. Baneth1, P. H. Kass2, D. Steinfeld1 and M. Besser1
1. School of Veterinary Medicine, Hebrew University of Jerusalem, Israel
2. Department of Population Health and Reproduction, School of Veterinary Medicine,
University of California, Davis, California.
Summary
The prevalence of antibodies to feline coronavirus (FCoV), feline immunodeficency virus
(FIV), and feline leukemia virus (FeLV) antigenemia was examined in 180 Israeli cats. FCoV
antibodies were detected in 60% of the cats, with the highest prevalence among cats from
animal shelters, followed by feral cats and client-owned cats. Antibodies to FIV were
detected in 12% of the cats, while FeLV antigenemia was found in only 4%. FCoV
seropositivity was significantly associated with nasal discharge and negatively correlated
with age, with the highest prevalence in cats 1 year old and a drop of approximately 18% in
the prevalence odds of seropositivity for each additional year. FIV antibodies were
significantly associated with gingivitis, and the prevalence odds of FIV seropositivity rose
with age up to 8 years, when the odds was approximately 7-fold greater than in 1 year old
cats. No statistical association was found between FCoV, FIV, and FeLV infections.
Introduction
Feline coronavirus (FCoV), feline immunodeficency virus (FIV) and feline leukemia virus
(FeLV) are 3 of the most important viral pathogens of domestic cats. FeLV and FIV both
induce an immunosupression that leads to the development of secondary infections by
opportunist microorganisms, haematopoeitic tumors and anaemia (1,2). FCoV may cause
enteritis and upper respiratory tract disease, and in a small percentage of infections may
progress to fatal feline infectious peritonitis (FIP)(3). Although FCoV, FIV and FeLV have
been reported from many areas of the world, the seroprevalence of these viruses varies
among different geographic locations (4-10).
The aims of this study were to assess the infection rate of cats from Israel with FCoV,
FIV and FeLV, and to explore possible associations between infection, signalment, clinical
signs and co-infection among the 3 viruses examined.
Materials and Methods
Blood samples
Blood samples were taken by jugular or cephalic venipuncture into heparinized tubes.
Plasma was separated by centrifugation at 100 x g for 10 minutes, and samples were stored
at -200C until tested.
Cats
The cats sampled were classified into 3 groups representing the type of environment in
which the cat lived: animal shelters, feral cats and client-owned cats. Age, sex, spayed/intact
status, and the presence of clinical signs of disease were also recorded. The ages of clientowned cats were determined from the patient's records. Ages of cats at animal shelters and
feral cats were estimated on the basis of a combination of the facility's records and/or a
dental and clinical examination. Cats were sampled from 4 different cities in Israel:
Jerusalem, Haifa, Tel Aviv and Beer Sheva. In addition, plasma from sick client-owned
patient cats referred to the Hebrew University Veterinary Teaching Hospital (VTH) was also
included in the study.
Diagnostic tests
A commercial enzyme-linked immunosorbent assay (ELISA) (PetCheck ® FeLV test kit,
IDEXX Laboratories, Westbrook, Maine) was used to test samples for FeLV p27 antigen.
The PetCheck® Anti-FIV test kit (IDEXX Laboratories, Westbrook, Maine) was employed to
detect antibodies against FIV.
Anti-FCoV antibodies were detected using the Immunocomb® test kit (Biogal, Israel). This
test is based on FIP-1 type antigen and reacts with feline coronavirus antigen in general. The
Immunocomb® test has recently been recommended as having a high degree of correlation
with the indirect fluorescent antibody test (IFAT) for FCoV as performed in the Feline Virus
Unit at the University of Glasgow (11).
Statistical analysis
Prevalence odds ratios (POR) were calculated by exact logistic regression as cross-sectional
measures of association between disease status and putative risk factors. P-values of the
null hypothesis (i.e., POR=1) less then 0.05 were considered statistically significant.
Results
A total of 180 cats were included in the study, of which 39% were feral cats, 32% originated
from animal shelters belonging to the Society for Prevention of Cruelty to Animals (SPCA),
and 29% were client-owned sick cats admitted to the VTH for veterinary care (Table 1).
FIV+
FeLV+
FCoV
Gender
Male
13.7 (14/102)
3.9 ( 4/102)
53.5 ( 46/86)
9 (7/78)
3.8 (3/78)
68.1 (47/69)
11.7 (21/180)
3.9 (7/180)
60 (93/155)
0- < 1
3.1
(1/32)
3.1 (1/32)
75 (21/28)
1- < 2
4.26
(2/47)
4.3 (2/47)
67.4 (31/46)
2- < 3
15.4
(4/26)
3.9 (1/26)
64 (16/25)
Female
Total
Age groups (years)
3- < 4
19
(4/21)
0 (0/21)
70.6 (12/17)
4- < 5
20
(3/15)
6.7 (1/15)
60 (6/10)
>= 5
19
(7/37)
5.4 (2/37)
22.2 (6/27)
Total
11.8
(21/178)
3.9 (7/178)
60.1 (92/153)
(3/28)
0 (0/28)
76.5 (13/17)
(18/152)
4.6 (7/152)
58 (80/138)
Spay/neuter status
Neutered
Intact
10.7
11.8
Source
Feral
11.4
(8/70)
4.3 (3/70)
60.3 (41/68)
Animal shelters
5.17
(3/58)
1.7 (1/58)
83.3 (45/54)
5.8 (3/52)
21.2 (7/33)
Client owned
19.23 (10/52)
Origin
Jerusalem
0
(0/30)
3.3 (1/30)
81.5 (22/27)
Haifa
10.7
(3/28)
0 (0/28)
85.2 (23/27)
Tel Aviv
10.8
(8/74)
4 (3/74)
60.9 (42/69)
Beer Sheva
14.8
(4/27)
17.4 (2/27)
19.2 (5/26)
VTH
28.6
(6/21)
4.8 (1/21)
16.7 (1/6)
Nasal discharge
0
(0/13)
0 (0/13)
100 (13/13)
Gingivitis
55
(5/11)
0 (0/11)
55.6 (5/9)
Assosiation with other diseases
FIV+
0 (0/21)
FeLV +
0 (0/7)
FCoL +
8.6 (8/93)
53.3 (8/15)
28.6 (2/7)
2.2 (2/93)
- Prevalence (%) of FIV antibodies, FeLV antigenemia and FCoV
antibodies among cats from Israel. In parentheses: number of cats
(numerator equals number of positives in the specific category; denominator
equals total number of cats tested in the category).
Table 1
Of the clinical findings noted on physical examination, nasal discharge found in 13 cats and
gingivitis in 11 were the two most common symptoms recorded. These were statistically
analyzed for association with other parameters.
In total, FeLV antigen was detected in plasma samples from 4% of the cats, 12% were
seropositive for FIV and 60% seropositive for FCoV (of 155 tested for FCoV). Co-infection
with FIV and FCoV was found in 8 (5%) of the cats and FeLV with FCoV was found in 1 (1%)
cat. No cats were co-infected with FIV and FeLV.
Logistic regression analysis indicated that for FCoV infection, a significant negative linear
trend was found between the cat 's estimated age in years and coronavirus antibodies. For
each additional year of age in the cat the prevalence odds of coronavirus positivity fell
approximately 18% (POR = 0.82; 95% confidence interval (95% CI) = 0.68-0.99) (Fig. 1).
Fig. 1 - Prevalence
of antibodies for feline coronavirus (FCoV) and feline
immunodeficency (FIV) virus among Israeli cats of six age groups.
The prevalence of coronavirus antibodies was higher in feral cats than patient cats
(POR=1.52; 95% CI = 1.20-1.85), and was significantly higher in animal shelter cats than
patients cats (POR=8.29; 95% CI = 2.33-29.45). The presence of coronavirus antibodies was
strongly associated with the prevalence odds of nasal discharge (POR=8.39, 95% CI = 1.18(). For each additional year of age in a cat’s life the prevalence odds of nasal discharge fell
approximately 43% (POR=0.57, 95% CI= 0.30-0.94).
For FIV infection, the prevalence odds of positive serology rose with age up to 8 years, when
the odds was approximately 7-fold greater than in 1 year old cats (POR=6.79; 95% CI =2.9015.89). After 8 years the prevalence odds began to decline in the population of cats studied.
After accounting for the association between estimated age and FIV prevalence, there was
no evidence to suggest that the source of the cat had any residual association with FIV
prevalence. FIV seropositivity was strongly associated with the prevalence odds of gingivitis
(POR=12.16, 95% CI = 1.86-99.66).
Only 7 cats were positive for FeLV, too few a number for reliable or precise inferences about
the role of putative risk factors on seropositivity. In all, no statistical relationship was found
between seropositivity with any of the 3 viruses and gender (male/female), neuter/spay
status, city of origin, and co-infection with another virus tested
Discussion
The main findings from this study are that while the prevalence of FcoV and FIV antibodies is
high in the cats tested from Israel, FeLV antigenemia is rarer and was found in only 4% of
the samples. The prevalence found for FIV and FeLV differ from those in most countries in
Western and Central Europe where FeLV seems to be more prevalent than FIV (5,8), and
from Britain where the seroprevalence for both infections was found roughly similar among
sick cats (18-19%) and among healthy ones (5-6%) (4). The prevalence in cats from Israel
follows the same pattern as cats in Norway (7) and free-ranging cats from Finland (6) where
FIV is more prevalent than FeLV. Interestingly, the prevalence of FeLV among stray and
privately owned cats in Beirut, Lebanon, which neighbours Israel to the north, was only 3.1%
(12), roughly similar to the findings from Israel.
The reasons why a low incidence of FeLV is found in some geographic locations are
unknown. The differences in the prevalence of FeLV reported in surveys from various
countries could be accounted for by several possible explanations including: genetic
resistance to infection in some populations or breeds, the effect of climate conditions on the
transmission of the virus, behavioural differences among cats in different areas affecting
disease transmission, and the presence of less virulent viral strains that successfully
establish an infection in a smaller percentage of exposed cats. None of these theories has
been shown to be responsible for a lower or higher incidence of FeLV in a certain region.
Another possible explanation is if FeLV spread from where the virus initially appeared to
other regions through importation of infected animals or natural migration, than perhaps
there are still some cat populations to which the disease has not yet spread, or in which the
virus is gradually spreading but still has a low prevalence.
An important finding for veterinarians in Israel that emerges from this study is that every fifth
cat above 3 years of age in this survey was positive for FIV. FIV should certainly be high on
the list of differential diagnoses when clinical signs compatible with this disease are observed
in cats presented for medical care. Most studies on FIV that compared the prevalence of
disease in sick and healthy cats have reported a higher incidence in sick cats (4,7,10,13,14).
Although in the present study the differences in prevalence of FIV among client-owned sick
cats (19%) and feral and animal shelter cats (11% and 5% respectively) were not statistically
significant, a trend of a higher prevalence among sick cats can be seen and could have
possibly been significant if the number of animals in the study was larger. The significant
association between gingivitis and FIV infection found in this study can be explained by
secondary infection of the oral cavity commonly found in immunosupressed cats with FIV
(13,15).
Due to the close antigenic relation of Feline Enteric Corona Virus (FECV) strains with FIP
strains no serological test developed to date can distinguish between these related infections
(16). Furthermore, studies analyzing gene sequences from FECV and FIP strains have
indicated that local isolates of FECV and FIP are more closely related than strains of FIP
from different geographic locations (17). These findings support the hypothesis made earlier
by Pedersen and colleagues (18) that FIP arises from spontaneous mutations in some of the
cats infected with FECV. A longitudinal study from Britain revealed that about 5-10% of cats
seropositive for FCoV will develop fatal FIP (19). If these findings can be universally applied,
than FIP should be present among a subset of the FCoV positive animals in this study,
probably in less than 6% of the cats sampled.
Our findings that the seroprevalence of FCoV decreased with estimated age from 75% in
cats younger than 1 year to 22% in cats above 5 years old, and that the prevalence of this
infection was highest among cats from animal shelters followed by feral cats and significantly
less prevalent in client-owned cats, are in agreement with findings of other workers. FCoV
infection has been reported to be highly prevalent in young cats living in catteries under
conditions where many cats are concentrated and share the same food sources and litter
facilities (20). Such conditions are present in animal shelters included in this study. In
contrast to the high frequency of FCoV antibodies among young cats (< 4 years) in the
present study, the prevalence of FIV infection in the same group of cats increased until the
age of 8 years. The drop in prevalence of FIV antibodies after that age could be explained by
the possibility that after 8 years, the number of cats that die of FIV following a prolonged
course of infection with this virus exceeds the number of cats that acquire the disease. The
significant association between nasal discharge and FCoV antibodies found in this study is
probably due to upper respiratory tract infections often found in cats infected with
coronavirus (4).
No significant association linking infections with FCoV and FIV or FeLV in this study was
found. Although this may be a result of the relatively small sample of cats included in the
survey, the findings of no apparent epidemiologic relationship between infection with FIV and
FeLV are in agreement with those from other studies on cats from North America, Japan
and Britain (4,13,15). Additionally, Lutz and colleagues (5) who compared the
seroprevalence of FCoV with FIV and FeLV in cats from Switzerland did not present
evidence for an epidemiologic association between these three infections. The reason for the
lack of apparent relationship between FIV and FCoV could be due to the different routes of
infection and typical environment in which transmission takes place. FIV is transmitted
mainly by bite wounds during aggressive behavior between cats that are allowed to roam
freely and often engage in defending their territories (22), while FCoV is chiefly transmitted
by exposure to excretions containing infective virus which occurs intensively in catteries and
multiple cat households where many cats share the same premises, food and litter boxes
(20). Cats kept indoors in stable social structures often keep a hierarchy where little
aggression is demonstrated.
In conclusion, the seroepidemiological findings from this study have demonstrated that FIV
and coronavirus are important feline pathogens in Israel. While FCoV infection affected
mainly young cats that were not client-owned and had a high prevalence of nasal discharge,
FIV was found mostly in middle aged to older cats with a high prevalence of gingivitis.
Acknowledgments
The authors thank Lea Graziani, Maria Griber, Drs. Zvi Galin, Sergei Weinstein and Tamar
Ben Zvi for their help in obtaining blood samples. We thank IDEXX laboratories and Biogal
laboratories for donating the test kits used in this study.
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