J. Parasitol., 97(2), 2011, pp. 256–258 F American Society of Parasitologists 2011

SEROPREVALENCE OF TOXOPLASMA GONDII AND CONCURRENT BARTONELLA SPP., FELINE IMMUNODEFICIENCY VIRUS, , AND INFECTIONS IN EGYPTIAN

Y. M. Al-Kappany, M. R. Lappin*, O. C. H. Kwok, S. A. Abu-Elwafa, M. Hilali`, and J. P. Dubey United States Department of Agriculture, Agricultural Research Service, and Natural Resources Institute, Animal Parasitic Diseases Laboratory, Building 1001, Beltsville, Maryland 20705–2350. e-mail: [email protected]

ABSTRACT: Toxoplasma gondii and Bartonella spp. are zoonotic pathogens of cats. Feline immunodeficiency virus (FIV) and feline leukemia virus (FeLv) are related to human immunodeficiency virus and human leukemia virus, respectively, and these viruses are immunosuppressive. In the present study, the prevalence of antibodies to T. gondii, Bartonella spp., FIV, as well as FeLv and Dirofilaria immitis antigens was determined in sera from feral cats (Felis catus) from Cairo, Egypt. Using a modified agglutination test, antibodies to T. gondii were found in 172 (95.5%) of the 180 cats with titers of 1:5 in 9, 1:10 in 9, 1:20 in 3, 1:40 in 5, 1:80 in 5, 1:160 in 15, 1:320 in 22, and 1:640 or higher in 104. Thus, 57.4% had high T. gondii titers. Antibodies to Bartonella spp. were found in 105 (59.6%) of 178, with titers of 1:64 in 45, 1:128 in 39, 1:256 in 13, 1:512 in 3, 1:1,024 in 4, and 1:2,048 in 1 . Antibodies to FIV were detected in 59 (33.9%) of 174 cats. Of 174 cats tested, antigens to FeLv, and D. immitis were detected in 8 (4.6%) and 6 (3.4%) cats, respectively. The results indicate a high prevalence of T. gondii, Bartonella spp., and FIV infections in cats from Cairo, Egypt. This is the first report of Bartonella spp., and D. immitis infection in cats in Egypt.

Cats are essential in the life cycle of Toxoplasma gondii because Laboratory (APDL), United States Department of Agriculture, Beltsville, they are the only hosts that can excrete the environmentally Maryland, in 4 batches in 2008 and 2009. Three to 5 days elapsed between death of the cat and receipt of samples at APDL; during this time samples resistant oocysts in nature. We summarized worldwide serological were kept cold. prevalence of T. gondii in cats for the past 20 yr (Dubey, 2009; Jones and Dubey, 2010). Prevalence of T. gondii antibodies varies Detection of T. gondii antibodies in cat serum with age, lifestyle of the cat (stray versus or domestic), serologic Sera from cats were first screened for T. gondii antibodies at 1:5–1:640 test, screening dilution, and undefined factors. dilutions with the modified agglutination test (MAT) as described Concurrent infections with certain feline pathogens can affect previously (Dubey and Desmonts, 1987). T. gondii infections in cats. Bartonella spp. are bacterial zoonotic pathogens that can cause cat scratch disease, endocarditis, and Examination for concurrent infections several other syndromes in humans (Chomel et al., 2004; Plasma or serum from selected cats were shipped to Colorado State Breitschwerdt et al., 2007). Feline immunodeficiency virus (FIV) University (CSU), Fort Collins, Colorado, and stored at 270 C until is a retrovirus related to human immunodeficiency virus and is assayed. Bartonella spp. IgG antibodies in serum were detected using a known to cause immunosuppression in some cats, depending on previously reported technique with a titer of ,1:64 considered negative (Lappin et al., 2009). This assay detects antibodies against Bartonella the stage of infection (Levy et al., 2008). Feline leukemia virus henselae, Bartonella clarridgeaie, and Bartonella koehlerae (Lappin et al., (FeLv) is related to human leukemia virus and can also cause 2009). immunosuppression in cats. Cats exposed to D. immitis often limit Plasma or serum samples were assayed at CSU for FeLV antigen, FIV the infection but can develop clinical illness relating to immune antibodies, and D. immitis using commercial kits (SNAP Feline Triple, IDEXX Laboratories, Portland, Maine). reactions to larvae or to adult worms (Nelson et al., 2005). The interaction of T. gondii and other feline pathogens is intriguing, and there are conflicting reports on this topic. Dubey RESULTS et al. (2009) summarized reports of co-infections with T. gondii, Antibodies to T. gondii were found in 172 (95.5%) of the 180 FIV, and FeLv in naturally exposed cats, mostly from the cats; 57.4% had high T. gondii titers (Table I). Antibodies to Western Hemisphere. Here we report a serological survey for Bartonella spp. were found in 105 (59.6%) of 178, with titers of these infections in feral cats from Cairo, Egypt. 1:64 in 45, 1:128 in 39, 1:256 in 13, 1:512 in 3, 1:1,024 in 4, and 1:2,048 in 1 cat. Antibodies to FIV were detected in 59 (33.9%)of MATERIALS AND METHODS 174 cats. Of 174 cats tested, antigens to FeLv and D. immitis were Naturally exposed cats detected in 8 (4.6%) and 6 (3.4%) cats, respectively. The distribution of T. gondii MAT titers with respect to concurrent During the course of a parasitological survey, blood samples were infections is shown in Table I. collected from 180 feral Felis catus from Abou-rawash, Giza, Egypt, as described previously (Al-Kappany et al., 2010). Samples were transported refrigerated by air from Egypt to the Animal Parasitic Diseases DISCUSSION

The high (95%) prevalence of T. gondii in cats in the present Received 20 September 2010; revised 12 October 2010; accepted 14 October 2010. study is probably related to the lifestyle of these cats; all cats were *Department of Clinical Sciences, College of Veterinary Medicine, feral and very wild. Although we do not have data on their age, Colorado State University, Fort Collins, Colorado 80523. they were most likely adults. This seroprevalence was higher than {Parasitology Department, Faculty of Veterinary Medicine, Mansoura 58.8% of 177 cats from Cairo (indirect fluorescent antibody test, University, Mansoura, Egypt. {Parasitology Department, Faculty of Veterinary Medicine, Cairo IFA) reported by Aboul-Magd et al. (1988), 18.4% of 114 cats University, Giza, Egypt. from Gharbia (indirect hemagglutination test, IHA) by Abu- DOI: 10.1645/GE-2654.1 Zakham et al. (1989), and 57.7% of 97 cats (latex agglutination

256 AL-KAPPANY ET AL.—SEROPREVALENCE OF T.GONDII IN CATS FROM EGYPT 257

TABLE I. Concurrent infections in Toxoplasma gondii–infected cats from Belgium, also reported similar findings in stray cats; the FIV- Egypt. infected cats were more likely to be seropositive for T. gondii and with higher antibody titers, but the seroprevalence of T. gondii MAT Toxoplasma Bartonella Dirofilaria was too high (70.2%) in this population of cats to make an titer gondii spp. IgG FeLv Ag FIV Ab immitis Ag accurate assessment. In the study reported by Nutter et al. (2004) ,58 1011from North Carolina, all infections were higher in stray cats than 593021in . Maruyama et al. (1998, 2003) did not find a positive 10 9 3 0 0 0 association among T. gondii, Bartonella spp., and FIV infections 20 3 0 1 1 0 in cats in Japan. 40 5 2 0 2 0 Recently Akhtardaesh et al. (2010) reported seroprevalences of 80 5 6 0 3 1 32.1% for T. gondii, 19.2% for FIV, and 14.2% for FeLv in 140 160 15 7 1 7 0 cats from Iran, and seropositivity for all 3 infections was higher in 320 22 14 2 7 0 older cats. In general FIV and FeLv infections are higher in stray $640 104 69 4 36 3 male cats. Unfortunately, data for sex and age for cats in the Total 180 105 8 59 6 present study were not available. Nevertheless, we were able to definitively document FeLv, FIV, and D. immitis infections in cats in Egypt for the first time. test, LAT) from Giza, Cairo, and Kalubya, Egypt, by Hassanain et al. (2008). The serological tests used could also account for differences among these surveys. Three decades earlier, Rifaat et ACKNOWLEDGMENTS al. (1976) had reported dye test antibodies in 39.6% of 318 cats The Bartonella spp. ELISA was performed by Arianne Morris in the from Cairo, Egypt. Nothing is known of the validity of IFA, IHA, Center for Companion Animal Studies at Colorado State University, Fort Collins, Colorado. The authors thank IDEXX Laboratories for do- and LAT for the detection of T. gondii antibodies in naturally nating the SNAP Feline Triple test kits used in this study and the Center infected cats. Tissues of 158 of the 180 cats in the present study for Companion Animal Studies donors (www.csuvets.colostate.edu/ were bioassayed in mice, and T. gondii was isolated from 114 of companion) for the Bartonella spp. ELISA reagents and technical support 130 seropositive (1:25 or higher) cats and from 1 (MAT ,1:5) of to complete these assays. 7, suggesting the specificity of the MAT. The prevalence of Bartonella spp. infections in the present study LITERATURE CITED was also high (59%), and 104 (57%) cats had both T. gondii and ABOUL-MAGD, L. A., M. S. TAWFIK,M.S.ARAFA, AND A. M. S. EL-RIDI. Bartonella spp. antibodies. The Bartonella assay performed here 1988. Toxoplasma infection of cats in Cairo area as revealed by IFAT. used B. henselae antigens. However, it appears that antibodies to Journal of the Egyptian Society of Parasitology 18: 403–409. ABU-ZAKHAM, A. A., A. M. EL-SHAZLY,M.E.YOSSEF,S.A.ROMELA, AND B. koehlerae and B. clarridgeaie are also detected in the assay. A. E. HANDOUSSA. 1989. The prevalence of Toxoplasma gondii Thus, is cannot be stated with certainly which Bartonella species antibodies among cats from Mahalla El-Kobra, Gharbia Governor- infected the cats. Each of these agents is thought to be transmitted ate. Journal of the Egyptian Society of Parasitology 19: 225–229. by fleas, Ctenocephalides felis. Bartonella spp. DNA was found in AKHTARDANESH, B., N. ZIAALI,H.SHARIFI, AND S. REZAEI. 2010. Feline immunodeficiency virus, feline leukemia virus and Toxoplasma gondii fleas collected from rats in Egypt (Loftis et al., 2006). To our in stray and household cats in Kerman-Iran: Seroprevalence and knowledge, this is the first report of Bartonella spp. infections in correlation with clinical and laboratory findings. 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