J. Parasitol., 95(5), 2009, pp. 1129–1133 F American Society of Parasitologists 2009

SEROPREVALENCE OF TOXOPLASMA GONDII AND CONCURRENT BARTONELLA SPP., FELINE IMMUNODEFICIENCY VIRUS, AND INFECTIONS IN FROM GRENADA, WEST INDIES

J. P. Dubey, M. R. Lappin*, O. C. H. Kwok, S. Mofya, A. Chikweto`, A. Baffa`, D. Doherty`, J. Shakeri`, C. N. L. Macpherson§, and R. N. Sharma` 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; all of these viruses are immunosuppressive. In the present study, the prevalence of antibodies to T. gondi, Bartonella spp., FIV, as well as FeLv antigen were determined in sera from 75 domestic and 101 feral cats (Felis catus) from the Caribbean island of Grenada, West Indies. Using a modified agglutination test, antibodies to T. gondii were found in 23 (30.6%) of the 75 cats with titers of 1:25 in 1, 1:50 in 3, 1:400 in 4, 1:500 in 12, 1:800 in 2, and 1:1,600 in 1, and 28 (27.7%) of 101 feral cats with titers of 1:25 in 4, 1:50 in 7, 1:200 in 4, 1:400 in 1, 1:500 in 3, 1:800 in 2, 1:1,600 in 3, and 1:3,200 in 4. Overall, in both pet and feral cats, the seroprevalence increased with age. Antibodies to Bartonella spp. were found in 38 (50.6%) of the 75 pet cats and 52.4% of 101 feral cats. Antibodies to FIV were found in 6 domestic and 22 feral cats. None of the 176 cats was positive for FeLv antigen. There was no correlation among T. gondii, Bartonella spp., and FIV seropositivity.

Cats are essential in the life cycle of Toxoplasma gondii because were those brought by their owners to the Small Animal hospital (SVM) for they are the only hosts that can excrete the environmentally treatment and or vaccination. Feral cats were trapped in different parishes of resistant oocysts in nature (Dubey and Beattie, 1988). We recently Grenada and brought to the SVM. These cats, after physical examination, were treated for their ailments, bled from a jugular vein, vaccinated for summarized worldwide serologic prevalences of T. gondii in cats , neutered, and either released to their original places of collection or for the past 20 yr (Dubey, 2009; Jones and Dubey, 2009). given for adoption; none of them seemed to be sick. General data, including Prevalence of T. gondii antibodies varies with age, life style of the age, sex, physical examination, and any abnormalities were noted. There (stray versus domestic), the serologic test, the screening were 75 (35 domestic, 40 stray) females and 101 (40 domestic, 61 stray) males. The cats were 4 to 9 yr old with the exception of 1 that was 16 yr old. dilution, and undefined factors. Sera were separated and stored at 220 C until tested. Concurrent infections with certain feline pathogens can affect T. gondii infections in cats. Bartonella spp. are bacterial zoonotic Serologic examination pathogens that can cause cat scratch disease, endocarditis, and several other syndromes in humans. Feline immunodeficiency Toxoplasma gondii: Sera were tested at the Animal Parasitic Diseases virus (FIV) is a retrovirus related to human immunodeficiency Laboratory, U.S. Department of Agriculture (Beltsville, Maryland). Two- fold serial dilutions were made (1:25 to 1:3,200) and tested with a modified virus (HIV), and it is known to cause immunosuppression in some agglutination test (MAT), as described previously (Dubey and Desmonts, cats, depending on the stage of infection. Feline leukemia virus 1987). A titer of 1:25 or higher was considered indicative of T. gondii (FeLv) is related to human leukemia virus and also can cause exposure based on experimental studies in cats (Dubey and Thulliez, 1989; immunosuppression in cats. Witt et al. (1989) reported that both Dubey et al., 1995a, 1995b). All sera were tested in 2 runs. In the first run, the seroprevalence and the magnitude of T. gondii antibodies were sera were screened at 1:25 dilution. In the second run, sera were diluted 1:25 to 1:3,200. higher in FIV-infected cats. This interaction of T. gondii and other Bartonella spp.: Sera were examined at the Center for Companion feline pathogens is intriguing, and there are conflicting reports on Studies at Colorado State University (CSU; Fort Collins, this topic. In the present article, we summarize past publications Colorado). The sera were assayed in a Bartonella spp. enzyme-linked of coinfections with T. gondii, FIV, and FeLv in naturally exposed immunosorbent assay (ELISA) that uses B. henselae as the antigen source. This assay detects antibodies against both B. henselae and B. clarridgeaie; cats (Table I), and we report a serologic survey for these the lowest positive titer is defined as 1:64 (Lappin et al., 2009). infections in cats from Genada, West Indies. FELV and FIV testing: Serum samples were assayed at CSU for FeLVantigen and FIV antibodies using commercial kits (SNAPH FeLV/ FIV, IDEXX Laboratories, Portland, Maine). MATERIALS AND METHODS Naturally exposed cats RESULTS All 176 cats comprising 101 feral and 75 pet cats were examined from June 2004 to December 2007 at the Small Animal Hospital, School of Veterinary Antibodies to T. gondii were found in 23 (30.6%) of the 75 pet Medicine (SVM), St George’s University, Grenada, West Indies. Pet cats cats with titers of 1:25 in 1, 1:50 in 3, 1:400 in 4, 1:500 in 12, 1:800 in 2, and 1:1,600 in 1, and 28 (27.7%) of 101 feral cats with titers Received 30 March 2009; revised 14 April 2009; accepted 20 April 2009. of 1:25 in 4, 1:50 in 7, 1:200 in 4, 1:400 in 1, 1:500 in 3, 1:800 in 2, *Department of Clinical Sciences, College of Veterinary Medicine, Colorado State University, Fort Collins, Colorado 80523. 1:1,600 in 3, and 1:3,200 in 4. Overall, in both pet and feral cats, {Small Animal Hospital, School of Veterinary Medicine, St. George’s seroprevalence increased with age (Tables II, III); 9.6% (5 of 52) University, Grenada, West Indies. cats younger than 12 mo old and 37.9% (47 of 124) cats older {Pathobiology Academic Program School of Veterinary Medicine, St. than 12 mo of age had antibodies to T. gondii. Seroprevalence of George’s University, Grenada, West Indies. T. gondii was 25.3% of 75 females and 37.6% of 101 males. }Windward Islands Research and Education Foundation, St. George’s University, Grenada, West Indies. Antibodies to Bartonella spp. were found in 38 (50.6%) of the DOI: 10.1645/GE-2114.1 75 pet cats (Table IV) and 52.4% of 101 feral cats (Table V).

1129 1130 THE JOURNAL OF PARASITOLOGY, VOL. 95, NO. 5, OCTOBER 2009

TABLE I. Reports of T. gondii and other concurrent infections in naturally exposed cats.

T. gondii % prevalence Bartonella Country No. of cats (test, cut-off titer)* spp. FIV FeLv Reference

Belgium 346, stray 70.2 (MAT, 40) ND{ 11.3 3.8 Dorny et al. (2002) Grenada, West Indies 75, 30.6 (MAT, 25) 50.6 8 0 Present study 101, feral 27.7 (MAT, 25) 52.4 21.8 0 Guatemala 30, stray 53 (MAT, 32) ND 3 17 Lickey et al. (2005) Japan 471, pets 8.7 (LAT, 64) 9.1 23.8 (16 of 67) 8.9 Maruyama et al. (1998) 1,447, pets 5.4 (LAT, 64) 8.8 9.6 (107 of 1,088) 2.9 Maruyama et al. (2003) Poland 200, stray 52.5 (LAT) ND 0 0 S´mielewska-Łosˇ and Pacon´ (2002) Portugal 207, pets 76 (MAT, 20) ND 14.6 (16 of 108) ND Lopes et al. (2008) Spain 220, pets 45 (MAT, 25) ND 4 (6 of 149) 4.6 Gauss et al. (2003) St Kitts, West Indies 96, feral 63.5 (MAT, 20) ND 15.6 (15 of 96) 0 Dubey, Moura et al. (2009) United States 585{ 15.2 (IFAT, 32) ND 2.4 3 of 34 selected Witt et al. (1989) samples 592{ 11.8 ND ND Childs et al. (1994) 195, stray 12.2 345, pets 618, pets 22 (LAT, 64) ND 10 15 Rodgers and Waldwin (1990) 117, pets, stray, 7.7 (ELISA) ND 0.9 7.6 Lin et al. (1990) sick 124, sick (uveitis) 74.2 (ELISA) ND 12.9 12.1 Lappin et al. (1992) 553, stray 10.8 (ELISA) 33.6 5.2 3.3 Luria et al. (2004) 76, pets 34 (MAT, 25) 75 4 1 Nutter et al. (2004) 100, stray 63 (MAT, 25) 93 5 4 67, stray 37.3 (ELISA) ND 8.8 16.2 Danner et al. (2007) 210, pets 19.5 (MAT, 25) 25.7 ND ND Dubey, Bhatia et al. (2009)

* ELISA, enzyme-linked immunosorbent assay; IFAT, immunofluorescent antibody test; LAT, latex agglutination test; MAT, modified agglutination test. { ND, not determined. { Same cats.

TABLE II. Seroprevalence of T. gondii antibodies and number of feline immunodeficiency virus (FIV) positive in 75 domestic cats from Grenada, West Indies.

Age No.. No. positive (titer) % Positive No. FIV positive

5–9 wk 1 0 (,25) 0 0 4–11 mo 21 3 (25 in 1; 500 in 2) 14.3 1 1 yr 25 10 (50 in 2; 400 in 2; 500 in 4; 800 in 1; 1,600 in 1) 40 1 2 yr 9 1 (50) 11 1 3 yr 4 1 (500) 25 1 4–16 yr 15 8 (400 in 2; .500 in 5; 800 in 1) 53.3 2

TABLE III. Seroprevalence of T. gondii antibodies and number of feline immunodeficiency virus (FIV) positive in 101 feral cats from Grenada, West Indies.

Age No. No. positive (titer) % Positive No. FIV positive

5–9 wk 4 0 (,25) 0 1 4–11 mo 26 2 (25 in 1; 50 in 1) 7.6 2 1 yr 38 12 (25 in 1; 50 in 2; 200 in 2; 800 in 2; 1,600 in 2; 3,200 in 3) 31.6 11 2 yr 18 6 (25 in 2; 200 in 1; 500 in 2; 3,200 in 1) 33.3 3 3 yr 7 2 (50 in 3) 28.5 2 4–16 yr 8 6 (50 in 1; 200 in 1; 400 in 1; 500 in 1; 3,200 in 1; 1,600 in 1) 75 3 DUBEY ET AL.—T. GONDII AND CONCURRENT INFECTIONS IN CATS 1131

TABLE IV. Seroprevalence of Bartonella spp. antibodies in 75 domestic cats from Grenada, West Indies.

Age No.. No. positive (titer) % Positive

5–9 wk 1 1 (128) 100 4–11 mo 21 5 (128 in 2; 256 in 1; 512 in 1; 4,096 in 1) 23.8 1 yr 25 18 (64 in 3; 128 in 6; 256 in 4; 512 in 2; 1,024 in 2; 16,384 in 1) 72 2 yr 9 5 (64 in 1; 128 in 3; 256 in 1; 512 in 1) 55.5 3 yr 4 2 (128 in 1; 1,024 in 1) 50 4–16 yr 15 7 (64 in 3; 128 in 1; 256 in 1; 1,024 in 1; 8,192 in 1) 46.6

Seropositivity occurred in both young and old cats, with highest 2.4% had FIV, and 15.2% were seropositive to T. gondii; all 3 prevalence in 2 yr olds. infections were higher in older cats. Both the magnitude of T. Antibodies to FIV were found in 6 domestic and 22 feral cats gondii titer and the seroprevalence were higher in FIV-infected (Tables II, III). All cats were negative for FeLv antigen. Cats with cats (Witt et al., 1989). Dorny et al. (2002) from Ghent, Belgium, multiple infections are shown in Table VI. also reported similar findings in stray cats (Table I); the FIV- infected cats were more likely to be seropositive for T. gondii and DISCUSSION with higher antibody titers, but the seroprevalence of T. gondii was too high (70.2%) in this population of cats to make an Cats older than 11 mo had a markedly higher frequency of T. accurate assessment. In the study reported by Nutter et al. (2004) gondii infection than younger cats. Higher seroprevalence in adult from North Carolina, all infections were higher in stray cats than cats versus , observed in the present study, supports in pets (Table I). Maruyama et al. (1998, 2003) did not find a previous findings (Dubey, 1973; Ruiz and Frenkel, 1980b; Pena et positive association among T. gondii, Bartonella spp., and FIV al., 2006) and relates to the life cycle of T. gondii. In general, infections in cats in Japan. seroprevalence of T. gondii is higher in feral cats (Jones and In the remaining surveys listed in Table I, not all cats were Dubey, 2009), but in the present study seroprevalence in feral cats surveyed uniformly for all 3 infections to reach any conclusion. In was slightly lower than the pet cats. Most cats are thought to 2 other reports, not listed in Table I, FIV-infected cats had higher become infected with T. gondii after weaning when they begin to prevalence of immunoglobulin (Ig)M T. gondii antibodies than hunt for food. The prevalence of T. gondii in cats is thought to IgG antibodies (O’Neil et al., 1991; Lappin et al., 1993). In reflect prevalence of T. gondii in animals that cats access for food. summary, there is no conclusive evidence that Bartonella spp., For example, Ruiz and Frenkel (1980a, 1980b) found a very high FIV, and FeLv infections modify the tissue phase of T. gondii prevalence of T. gondii in cats and rodents and free-range infection or immune responses to the organism in naturally chickens from Costa Rica. However, we found a very low infected cats. In most of the studies, including the present study, prevalence of T gondii in local rats (Dubey et al., 2006) and a high fecal samples were not collected concurrently, and so there is prevalence in free-range chickens from Grenada (Dubey et al., minimal information concerning the effect of these co-infections 2005). Antibodies to T. gondii were found in only 2 of 238 feral on T. gondii oocyst shedding. In Nutter et al. (2004), T. gondii rats, and viable parasite was recovered from only 1 of the 238 rats oocysts were not detected in any fecal sample, including those cats bioassayed (Dubey et al., 2006). Unlike rats, T. gondii antibodies positive for Bartonella spp., FeLv, or FIV. In cats experimentally were found in 52% of 102 free-range chickens, and viable infected with FIV and T. gondii, coinfection had minimal effects parasites were isolated from 36 chickens (Dubey et al., 2005). on primary oocyst shedding and oocyst shedding did not occur on Compared with the present study, T. gondii seroprevalence was repeat infection (Lappin et al., 1996). more than twice (61% of 96) feral cats from another Caribbean Island, St Kitts (Dubey, Moura et al., 2009). There is a considerable variability with respect to T. gondii ACKNOWLEDGMENTS prevalence and concurrent infections. There could be many The Bartonella spp. ELISA was performed by Arianne Morris in the reasons for this observation, including different serologic tests, Center for Companion Animal Studies at Colorado State University, Fort Collins, Colorado. We thank IDEXX Laboratories for donating the FeLv/ cut-off titers, and types of cats surveyed (Table I). Witt et al. FIV test kit used in this study and the Center for Companion Animal (1989) and Childs et al. (1994) tested stray and pets cats from Studies donors (www.csuvets.colostate.edu/companion) for the Bartonella Baltimore, Maryland, and found that 14.7% had Bartonella spp., spp. ELISA reagents and technical support to complete these assays.

TABLE V. Seroprevalence of Bartonella spp. antibodies in 101 feral cats from Grenada, West Indies.

Age No. No. positive (titer) % Positive

5–9 wk 4 2 (64 in 1; 128 in 1) 50 4–11 mo 26 12 (64 in 3; 128 in 1; 256 in 2; 512 in 3; 1,024 in 1; 2,048 in 1; 4,096 in 1) 38.5 1 yr 38 24 (64 in 8; 128 in 8; 256 in 2; 512 in 4; 2,048 in 2) 63.1 2 yr 18 9 (64 in 3; 128 in 2; 512 in 2; 256 in 2) 50 3 yr 7 3 (128 in 1; 256 in 2) 42.8 4–16 yr 8 3 (64 in 1; 128 in; 512 in 1) 1132 THE JOURNAL OF PARASITOLOGY, VOL. 95, NO. 5, OCTOBER 2009

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