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PREVALENCES OF FCOV, FPV, FELV AND FIV INFECTIONS IN CATS IN TURKEY 511 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 512 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 513 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, 511-516 514 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. 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