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PREVALENCES OF FCOV, FPV, FELV AND FIV INFECTIONS IN CATS IN TURKEY
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Prevalences of Feline Coronavirus (FCoV), Feline
Leukaemia Virus (FeLV), Feline Immunodeficiency
Virus (FIV) and Feline Parvovirus (FPV) among
domestic cats in Ankara, Turkey
T.Ç. OĞUZOĞLU1*, D. MUZ2, M.Ö. TİMURKAN3, N. MARAL4, İ.S. GURCAN5
Department of Virology, Faculty of Veterinary Medicine, Ankara University, 06110 Dışkapı Ankara, Turkey
Department of Virology, Faculty of Veterinary Medicine, Mustafa Kemal University, 31000, Tayfur Sökmen Kampüsü, Hatay, Turkey
3
Department of Virology, Faculty of Veterinary Medicine, Atatürk University, 25240 Yakutiye, Erzurum, Turkey
4
Başkent Animal Hospital, 06550 A.Ayrancı, Ankara, Turkey.
5
Department of Biostatistics, Faculty of Veterinary Medicine, Ankara University, 06110 Dışkapı, Ankara, Turkey
1
2
*Corresponding author: [email protected]
SUMMARY
RESUME
Feline Coronavirus (FCoV), Feline Leukaemia Virus (FeLV), Feline
Immunodeficiency Virus (FIV) and Feline Parvovirus (FPV) cause important
viral infections in domestic and wild cats. In this study, these viruses were
assessed using PCR protocols from whole blood samples from 200 domestic
cats living in Ankara with clinical chronic gastrointestinal, urinary tract and
respiratory symptoms (n = 138) or apparently healthy (n = 62). A total of 146
cats (73.0%) were positive for at least one of these viruses, and 41.8% of them
were co-infected, mainly by FPV, FeLV and/or FIV. The prevalences were
45.5%, 39.0%, 20.5% and 9.5% for FCoV, FPV, FeLV and FIV, respectively.
Age, lifestyle and health status were found significantly associated with an
increased risk of virus positivity. These results allow a direct determination
of virus infection instead of seroprevalences and emphasize the frequency of
virus poly-infections.
Prévalences des Coronavirus félins (FCoV), du virus félin de la leucémie
(FeLV), du virus félin de l’immunodéficience (FIV) et du Parvovirus félin
(FPV) chez les chats domestiques à Ankara, Turquie
Keywords: Cat, Feline Coronavirus (FCoV), Feline
Leukaemia Virus (FeLV), Feline Immunodeficiency Virus
(FIV), Feline Parvovirus (FPV), PCR, prevalence, risk
factors, Turkey
Les Coronavirus félins (FCoV), le virus félin de la leucémie (FeLV), le
virus félin de l’immunodéficience (FIV) et le parvovirus félin (FPV) sont
responsables d’importantes infections virales chez les chats domestiques et
sauvages. Dans cette étude, ces virus ont été recherchés par des protocoles de
PCR dans des échantuillons de sang total prélevés sur 200 chats domestiques
d’Ankara présentant des symptômes d’atteintes chroniques de l’appareil
gastro-intestinal, de l’appareil urinaire ou de l’appareil respiratoire (n = 138)
ou apparemment sains (n = 62). Au total, 146 chats (73.0%) ont été positifs
pour au moins 1 de ces virus et 41.8% d’entre eux présentaient une infection
mixte associant surtout le FPV, le FeLV et/ou le FIV. Des prévalences de
45.5%, 39.0%, 20.5% et de 9.5% ont été respectivement obtenues pour le
FCoV, le FPV, le FeLV et le FIV. L’âge, le style de vie et l’état général ont été
significativement associés à un risque accru de positivité virale. Ces résultats
ont permis, à la différence des séroprévalences, une détermination directe
des prévalences des infections virales et soulignent la fréquence des polyinfections.
Mots-clés : Chat, Coronavirus félin (FCoV), virus félin
de la leucémie (FeLV), virus félin de l’immunodéficience
(FIV), parvovirus félin (FPV), PCR, prévalence, facteurs
de risque, Turquie.
Introduction
Feline Coronavirus (FCoV), Feline Leukaemia Virus
(FeLV), Feline Immunodeficiency Virus (FIV) and Feline
ParvoVirus (FPV) are significantly important viral agents in
domestic and wild cats, cause prevalently immunosuppressive
infections in cat population in worldwide [5, 11, 14, 17,
18, 27]. These diseases are commonly characterized by
immune pathological defects such immunodeficiency,
immunosuppression, lymphomas, leukopenia and tumours,
leading to numerous deaths and opportunistic infections
especially in kittens, shelters and owned cats [24].
Low virulent FCoV strain induces subclinical or mild
enteric disease in felids [14, 25], but only highly pathogenic
Revue Méd. Vét., 2013, 164, 11, 511-516
FCoV mutants [27], termed feline infectious peritonitis (FIP)
virus mostly lead to fatal infections [31] and sometimes
superinfections with FeLV and FIV in affected cats [34]. FeLV
and FIV belong to Retroviridae family, induce similar clinical
signs such as anaemia, lymphomas and immunodeficiency
which promote the development of co-infections [2]. These
immunosuppressive viruses are followed by opportunistic
infections, and they cannot usually cause major problem by
oneself, however they can become fatal with other pathogenic
infectious agents such FCoV and FPV [2, 5, 31, 34].
FPV is known as the most important pathogen in cats,
causing feline gastrointestinal disease, characterized by a
generalized infection including signs of enteritis, diarrhoea,
leukopenia, thrombocytopenia, anaemia [30]. FPV is highly
contagious and is transmitted via faecal-oral route, placenta
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and fomites. However, the mortality rate is high in kittens,
but it causes immunosuppression in adults. FPV can be
detected simultaneously with other enteric viruses such as
coronaviruses [9], and these mixed viral infections might
also be accompanied with retroviruses [30].
OĞUZOĞLU (T.Ç.) AND COLLABORATORS
analyzed in 1% agarose gels containing ethidium bromide
and visualized on a UV transilluminator. The amplicons were
shown in figure 1.
Infections caused by these four viruses are sometimes
clinically covered and differential diagnosis may be very
difficult for veterinary practitioners despite their similar
clinical signs. This study investigated the prevalence of these
four viral infections in domestic cats using PCR techniques
and described the risk factors associated with virus positivity
according to gender, age, breed, lifestyle (indoor or outdoor),
health status (healthy or sick) and immune status.
Materials and methods
ANIMALS
A total of the 200 cats were sampled from February 2007
to August 2009 with permission of the cats’ owners. The
sampled cats had been brought to veterinary clinics in order
to vaccine application, routine controls or with complaints
associated to some clinical signs (chronic gingivitis or any
mouth ulcerations, chronic gastrointestinal, urinary tract and
respiratory symptoms). A high mortality rate in kittens had
also been notified during some periods. Data such as gender,
age, breed (Tekir, Siamese, Persian, etc.), lifestyle (indoor or
outdoor), health status (sick or healthy) and information
about previous vaccinations (many vaccine are available in
the country from different firms for protection of FeLV and
FPV) have been collected.
VIRUS IDENTIFICATION BY RT-PCR AND PCR
The collected EDTA-treated blood samples were tested
for the presence of FCoV, FeLV, FIV and FPV infections
using polymerase chain reaction (PCR) protocols. For the
FCoV identification, total RNA was extracted from buffy
coats using High Pure Viral RNA Extraction Kit (Roche,
Germany) according to the manufacturer’s instructions.
DNA extraction was carried out for FeLV, FIV and FPV
identifications with phenol-chloroform-isoamyl alcohol
(25:24:1) method described by ARJONA et al. [3].
PCR assays were achieved using specific primers for
FeLV, FIV and FPV genomes reported by ARJONA et al. [3],
ENDO et al. [10] and BUONAVOGLIA et al. [7] (obtained
from PEREIRA et al. [26]), respectively. PCR mix was
composed in a 30 µL final volume consisting in 10x reaction
buffer, 2 mM MgCl2, 0.2 mM dNTP, 0.2 pmol each primer,
1.25U Taq DNA polymerase (Frementas, Lithuania). The
PCR cycle profiles of FeLV, FIV and FPV were carried out
according to ARJONA et al. [3], OĞUZOĞLU et al. [23]
and MUZ et al. [21], respectively. The FCoV detection was
performed using a reverse-transcription PCR (RT-PCR)
assay as previously described by CAN-SAHNA et al. [8]
with a FIP specific primer pair [29]. All PCR products were
Figure 1: PCR results of four different viral infections in cats: PCR amplified fragments observed in FCoV (lane 1, 295 bp with FIP specific
primers), FeLV (lane 3, 306 bp with FE7-FE4 primers [3]), FIV (lane 4,
1230 bp with nested PCR primers [10]) and FPV (lane 5, 406 bp with
Pbs-Pbas primers [7]).
Lane M: DNA ladder, 100 bp; lane 2: RT-PCR control using GADPH primers; lane 6: negative control.
FCoV: Feline Coronavirus; FPV: Feline Parvovirus; FeLV: Feline Leukaemia
Virus; FIV: Feline Immunodeficiency Virus
STATISTICAL ANALYSIS
The obtained results were analyzed according to gender,
age, breed, immune status, health status and lifestyle of cats
using a standard statistical software program (SPSS v.15.0).
Descriptive statistics and frequency distributions were
calculated and the prevalences of positive cats for the four
viral infections were determined. The logistic regression
analysis method was performed for determination of risk
factors in affected FCoV, FeLV, FIV and FPV infections
described by HOSMER and LEMESHOW [15].
Results
A total of 146 (73.0%) cats were positive for at least one
virus among the 4 tested: the global FCoV, FPV, FeLV and FIV
prevalences were 45.5%, 39.0%, 20.5% and 9.5%, respectively,
as shown in Table I. Single infections were detected only in
58.2%of the positive cats (85/146) and were majority FCoV
positivity, whereas the positivities of FIV and FeLV were high
in multiple infection cases with rates of 94.5% (18/19) and
78.0% (32/41), respectively.
The associations between the virus prevalences and
gender, age, breed, lifestyle and health status determined
using logistic regression analysis are reported in Table II.
The clinical sick cats were found more frequently positive for
FCoV than the healthy ones (p < 0.01). The positivity rates for
FIV (p < 0.01) and FPV (p < 0.05) infections in outdoor cats
were significantly higher than those of permanently indoor
cats. The FeLV positivity rate was found as independent
from gender, lifestyle and clinical status of cats. However,
the older cats of this study (more than 48 months old) were
significantly more often infected with FeLV than the other
Revue Méd. Vét., 2013, 164, 11, 511-516
PREVALENCES OF FCOV, FPV, FELV AND FIV INFECTIONS IN CATS IN TURKEY
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Positive cases (number)
Prevalence (%)
Total
FCoV
FPV
FeLV
FIV
146
91
78
41
19
73.0
45.5
39.0
20.5
9.5
Mono-infection
FCoV
FPV
FeLV
FIV
85
48
27
9
1
42.5
24.0
13.5
4.5
0.5
Poly-infection
FCoV
FPV
FeLV
FIV
61
43
51
32
18
30.5
21.5
25.5
16.0
9.0
FCoV: Feline Coronavirus; FPV: Feline Parvovirus; FeLV: Feline Leukaemia Virus; FIV: Feline Immunodeficiency Virus.
Table I: Frequencies of FCoV, FPV, FeLV and FIV infections determined by RT-PCR and PCR in 200 cats.
FCoV
FPV
FeLV
FIV
Gender
Female (n = 100)
Male (n = 88)
Undetermined1 (n = 12)
p - value
45 (45.0%)
42 (47.7%)
4 (33.3%)
> 0.05
37 (37.0%)
39 (44.3%)
2 (16.7%)
> 0.05
23 (23.0%)
17 (19.3%)
1 (8.3%)
> 0.05
10 (10.0%)
9 (10.2%)
0 (0.0%)
> 0.05
Age (in months)
0 - 6 (n = 71)
7 - 12 (n = 36)
13 - 48 (n = 55)
> 48 (n = 28)
Undetermined (n = 10)
p - value
32 (45.1%)
11 (30.6%)
25 (45.5%)
20 (71.4%)
3 (30.0%)
> 0.05
36 (50.7%)
9 (25.0%)
17 (30.9%)
15 (53.6%)
1 (10.0%)
> 0.05
16 (22.5%)
3 (8.3%)
8 (14.5%)
13 (46.4%)
1 (10.0%)
0.05
2 (2.8%)
4 (11.1%)
6 (10.9%)
7 (25.0%)
0 (0.0%)
> 0.05
Breed
Tekir (n = 47)
Black-White (n = 20)
Persian (n = 12)
Sarman (n = 8)
Siamese (n = 5)
Mixed (n = 12)
Others2 (n = 15)
Undetermined (n = 81)
p - value
27 (57.4%)
8 (40.0%)
6 (50.0%)
4 (50.0%)
3 (60.0%)
5 (41.7%)
7 (46.7%)
31 (38.3%)
> 0.05
18 (38.3%)
6 (30.0%)
2 (16.7%)
5 (62.5%)
2 (40.0%)
8 (66.7%)
9 (60.0%)
28 (34.6%)
> 0.05
15 (31.9%)
1 (5.0%)
2 (16.7%)
1 (12.5%)
7 (58.3%)
6 (40.0%)
9 (11.1%)
> 0.05
3 (6.4%)
1 (5.0%)
1 (8.3%)
2 (25.0%)
1 (8.3%)
1 (6.7%)
10 (12.3%)
> 0.05
Lifestyle
Indoor (n = 157)
Outdoor (n = 43)
p - value
70 (44.6%)
21 (48.8%)
> 0.05
54 (34.4%)
24 (55.8%)
< 0.05
30 (19.1%)
11 (25.6%)
> 0.05
12 (7.6%)
7 (16.3%)
< 0.01
Health status
Health (n = 62)
Sick (n = 138)
p - value
17 (27.4%)
74 (53.6%)
< 0.01
31 (50.0%)
47 (34.1%)
> 0.05
16 (25.8%)
25 (18.1%)
> 0.05
3 (4.8%)
16 (11.5%)
> 0.05
the sex was not specified in the questionnaire when the blood sample was performed; 2Other breeds including Chinchilla (n = 4), Van cat (n = 4), 3 colours (n =
3), Angora cat (n = 1), Tiffany (n = 1), Russian Blue (n = 1) and British Scottish (n = 1); FCoV: Feline Coronavirus; FPV: Feline Parvovirus; FeLV: Feline Leukaemia
Virus; FIV: Feline Immunodeficiency Virus.
1
Table II: Frequencies of FCoV, FPV, FeLV and FIV infections determined by RT-PCR and PCR in 200 cats according to gender, age, breed, lifestyle and
health status.
Revue Méd. Vét., 2013, 164, 11, 511-516
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OĞUZOĞLU (T.Ç.) AND COLLABORATORS
age groups (p = 0.05). The influence of breed on the virus
prevalence was not determined because of the low breed
group sizes. In addition, it was found that the FeLV and FIV
prevalences were not affected by previous vaccinations (Table
III).
Discussion
Although no informative database about how many
domestic cats live in Ankara is available, the cat population in
Ankara can be described as free-roaming stray cats and owned
cats. This paper describes the prevalence of FCoV, FPV, FeLV
and FIV infections among domestic cats in Ankara. FCoV
and FPV were found as the most common infectious agents
in all categories of sampled cats, but positivity for FeLV and
FIV infections were also detected. Furthermore FCoV and
FPV infections are also widely reported in domestic cats
from Germany [6] and in not domestic cats from East Africa
[14]. The present results showed that the FCoV and FPV are
the two main agents that causes viral infections in cats in
Ankara but the FeLV and FIV infections may also constitute
a risk for the cat population.
Several risk factors may affect the prevalence of FCoV,
FPV, FeLV, FIV infections. Age, breed, sex, lifestyle, health
status have been discussed associated with the prevalence of
viral infections in cat population [4, 8, 20, 22, 23, 32, 33].
The FCoV positivity in young cats, especially under 12
months age has been reported as higher than in older cats
in several studies [8, 22]. On the other hand, the positivity of
FCoV was significantly higher in cats older than 48 months
compared to young ones in this study. However, this fact
may be related to the clinical status of animals: FCoV needs
a long incubation period to mutate into lethal FIPV and viral
loads in monocytes/macrophages can occur for a longer
period in infected cats with FIP than in healthy infected ones
[16]. Therefore, blood samples were used rather than faecal
samples in this study for determining the FIP infection by
RT-PCR. Although FCoV is found in blood of cats without
any clinical signs [22], most FCoV infections are primarily
enteric infections. Few studies reported the detection of
FCoV from blood samples [13].
FPV is known as a highly pathogenic agent causing
fatal infection in kittens whereas it induces mild
immunosuppressive infections in adult cats. The adult cats
vaccinated or not for FPV may constitute reservoirs and
carriers of the virus for a certain time, helping in this way
Immune status
Vaccinated (n = 95)
Unvaccinated (n = 85)
Undetermined (n = 20)
p - value
to spread the disease and can be considered as a potential
risk for kittens. The positivity of FPV infection was found
highly similiar to FCoV, in comparison to FeLV and FIV
rates. The prevalence of FPV infection in the cat population
from Turkey was first reported in this study, whereas the
molecular detection, characterization and phylogenetic
analysis of Canine Parvoviruses (CPVs) from blood samples
in domestic cats were previously reported by MUZ et al.
[21]. The field CPV strains in domestic cats in Turkey were
described as CPV-2a, CPV-2c and FPV in this prior study.
Faeces are usually used in commercially available latex
agglutination or immunochromatography tests to detect
FPV antigen in veterinary practice. TRUYEN et al. [30]
reported that specialised laboratories offer PCR-based testing
of whole blood or faeces for cats. Whole blood samples for
the purpose of the CPV detection in cat population may be
preferred when animals exhibit no clinical signs or when no
faecal samples are available [21, 28]. Therefore, whole blood
samples may be recommended for the FPV detection in cats
in epidemiological surveys or routine control of cats before
a vaccination program. The FPV frequency was slightly
(but not significantly) higher in male cats, in those younger
than 6 months and older than 48 months compared to the
other groups. As 60.3% (47/78) FPV positive cats exhibited
clinical symptoms such as high fever, diarrhoea, vomiting,
depression, anorexia and dehydration, suggesting especially
both gastroenteritis and myocarditis, it was stated that blood
samples should be taken for detection of FPV infection by
PCR if clinical signs are available. In this study, the frequency
of FPV infection in outdoor cats was proportionally 1.37
times higher than in indoor ones. It is also pointed out that
outdoor cat population has much more predisposition then
indoor cats because of environment risk factors for infection.
FeLV and FIV cause an immune-mediated disease
characterized by the lack of the activity of the T suppressor
cells and sustained formation of immune complexes, leading
to haemolytic anaemia, glomerulonephritis and polyarthritis
[2, 14]. The prevalence of the FeLV infection was found to be
higher than that of the FIV infection among cats in Ankara,
similarly to studies conducted in the Czech Republic,
Guatemala and Costa Rica [5, 17, 19]. The prevalence of
FeLV and FIV infections in Turkey has been reported by
some researchers [22, 23, 33]. The molecular detection of
FeLV in Turkey by PCR was firstly described in this study
whereas the molecular detection, characterization and
phylogenetic analysis of field FIV strains were previously
described by OĞUZOĞLU et al. [23]. Enzyme-linked
FeLV
FIV
19 (20.0%)
17 (20.0%)
5 (25.0%)
> 0.05
38 (40.0%)
36 (42.4%)
4 (20.0%)
> 0.05
FeLV: Feline Leukaemia Virus; FIV: Feline Immunodeficiency Virus.
Table III: Prevalences of FeLV and FIV infections according to the vaccinated status of cats (n = 200).
Revue Méd. Vét., 2013, 164, 11, 511-516
PREVALENCES OF FCOV, FPV, FELV AND FIV INFECTIONS IN CATS IN TURKEY
immunosorbent assay (ELISA) was previously and usually
used to detect FeLV antigens, while detection of the FeLV
proviral DNA using PCR was accomplished in the current
study. RT-PCR is based on detection of the viral RNA, and
does not provide the information as proviral DNA especially
in persistently infected cats without clinical signs [12]. PCR
based on detection of proviral DNA may be more useful,
sensitive and specific to clarify the false negative results
rather than FeLV antigen ELISA. Additionally, determination
of the proviral DNA in blood cells allows identification of
the virus independently from antibodies or viremia [3]. For
the same purpose, a nested PCR technique was performed
to detect the proviral FIV genome in our study. Thus, use of
highly sensitive techniques for viral nucleic acid detection
from whole blood samples may probably help to clarify the
relatively high prevalences of FeLV and FIV infections in
this study. The age, sex and lifestyle status of cats may be risk
factors for feline retrovirus infections. The positivity rates
of the infections are positively correlated with the age and
increased antibody response could be easily detected in adult
ages in feline retrovirus infections [18, 20]. Additionally, the
retrovirus expression varies according to the differentiation
from monocyte to macrophage and the virus load increases
intermittently and time-dependent in adult ages [14, 17, 34].
Positivity rates have been reported to be significantly higher
in adult age groups [20] in accordance with results observed
here, specifically for the FeLV infection. The infection
positivity in male and female cats has been discussed
according to their neutered, intact and free-roaming status
[18, 32, 33]. It is admitted that males are directly involved
in the transmission of FeLV and FIV infections [32, 33].
Nevertheless, FeLV and FIV prevalences in the present
study were not significantly different between males and
females, suggesting an important vertical transmission of
FIV and FeLV. YAMAMOTO et al. [32] reported that the
high positivity rates of FIV and FeLV in the sampled stray
cats naturally resulted from the retrovirus transmission ways,
vertically by mothers and horizontally via biting with freeroaming indoor cats. Similarly, high positivity rates for FeLV
and FIV infections were found in stray cats in the present
study.
The prevalences of these viral infections in the cat
population of Ankara are relatively high, and they are higher
in outdoor cats than indoor cats, particularly in the cases of
retrovirus and FPV infections. Indeed the lifestyle of outdoor
cats may increase the infection risk. Besides, viral reactivation
and the pathogenicity of low pathogen species may be seen
with susceptibility to other infections in latent infected
immunosuppressed cats. In this way, to limit retrovirus
spreading in the cat population and indirectly the gravity
of other viral infections, FIV-positive cats in multiple-cat
households can be vaccinated against FeLV with inactivated
preparations. However, the cats should be diagnosed with
regard to the presence of some viral infectious agents before
beginning of a viral vaccination program. Because infected
cats may not developed satisfactory immune responses to
vaccine antigens, an infected cat may become persistently
Revue Méd. Vét., 2013, 164, 11, 511-516
515
infected by various exogenous infectious agents in spite of
vaccination. TRUYEN et al. [30] reported that cats with
a chronic disease, such as a retrovirus infection, should
be preferentially vaccinated against FPV with inactivated
preparations. On the other hand, it has been reported that
FIP may develop in cats infected with low pathogen FCoV
despite the presence of specific antibodies [1]. Therefore, it
is important to detect the presence or absence of infectious
disease and antibody response in cats.
As a conclusion, it would be relevant to determine the
infection rates in the cat population with major viruses, such as
FCoV, FPV, FeLV and FIV, known to be immunosuppressive,
before the application of a vaccination program in order
to evaluate the interest of the vaccination and to choose a
valuable vaccination protocol.
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