J. Parasitol., 98(3), 2012, pp. 679–680 F American Society of Parasitologists 2012

Seroprevalence of Toxoplasma gondii in Domestic and Wild Animals From the Fernando de Noronha,

D. G. C. Costa, M. F. V. Marvulo*, J. S. A. Silva, S. C. Santana, F. J. R. Magalha˜es, C. D. F. Lima Filho, V. O. Ribeiro, L. C. Alves, R. A. Mota, J. P. Dubey`, and J. C. R. Silva, Departamento de Medicina Veterina´ria, Universidade Federal Rural de , , Pernambuco 52. 171-900, Brazil; *Instituto Brasileiro para Medicina da Conservac¸a˜o – Trı´ade, Recife, Pernambuco 52. 061-030, Brazil; Distrito Estadual de Fernando de Noronha, Fernando de Noronha, Pernambuco 52. 120-010, Brazil; `United States Department of Agriculture, Agriculture Research Service, Animal and Natural Resources Animal Parasitic Diseases Laboratory, Building 1001, Beltsville, Maryland 20705. e-mail: [email protected]

ABSTRACT: Fernando de Noronha is an archipelago of 21 and in Fernando de Noronha archipelago: black rats 5 34/2,000 estimative islets in the , state of Pernambuco, Brazil, which has a (1.7%); cats 5 118/700 (16.9%); cattle 5 100/183 (54.6%); cattle egret 197/ varied biodiversity including alien species or sinantropic animals. The 650 (30.3%); chicken 5 100/1,506 (6.6%); dog 5 91/700 (13.0%); goat 5 objective here was to determine the seroprevalence of Toxoplasma gondii 11/17 (64.7%); horse 5 16/23 (69.6%); and sheep 5 97/305 (31.8%). The in domestic and wild animals from Fernando de Noronha archipelago, cats sampled were more than 3-mo-old. Of the 100 chickens, 50 were those Brazil. Between July 2007 and May 2010, blood samples were collected reported in Dubey et al. (2010). from 764 animals (533 domestic and 231 wild animals). Sera were tested by Antibodies for T. gondii were found in 264 of 533 (49.5%) domestic the indirect fluorescence antibody test (IFAT) or the modified agglutina- animals and in 170 of 231 (73.6%) wild animals (Table I). Seroprevalence tion test (MAT), or by both. Antibodies to T. gondii were found in 80 was higher (66.6%) in feral cats than in domestic cats (54.2%), probably (80.0%) of 100 chickens (Gallus domesticus), 3 (3.0%) of 100 cattle (Bos related to their respective life styles; i.e., prevalence is higher in feral taurus), 59 (60.8%) of 97 sheep (Ovis aries), 9 (81.8%) of 11 goats (Capra cats that hunt for their food than in domestic cats (Dubey, 2010). hircus), 7 (43.7%) of 16 horses (Equus caballus), 70 (59.3%) of 118 cats Seroprevalence was higher in males (65.5% of 58) than in females (53.3% (Felis catus), 36 (39.6%) of 91 dogs (Canis familiaris), 13 (38.2%)of34 of 60). Seropositivity increased with age (0% of 10 kittens, 61.5% of 26 black rats (Rattus rattus), and 157 (79.7%) of 197 cattle egrets (Bubulcus juveniles, and 65.8% of adults), indicating post-natal acquisition of ibis). Results indicate endemic infection by this zoonotic parasite among infection. The kittens sampled were more than 3-mo-old. the animal and avian fauna in this archipelago from Brazil. In the present study, we screened avian sera starting with a 1:5 dilution because viable T. gondii was isolated from 1 of 2 chickens from Fernando Toxoplasma gondii infections are widely prevalent in animals and de Noronha with a MAT titer of 1:5 (Dubey et al., 2010). In the present humans worldwide, particularly in Brazil where up to 90% of humans study, T. gondii antibodies were detected in 157 of 197 cattle egrets have been exposed to this parasite (Dubey, 2010). During the last decade, (Bubulcus ibis). Although most of these birds had a titer of only 1:5, 53 there have been numerous studies in animals in Brazil, including humans, had a MAT titer of 1:50 and 3 had a titer of 1:500. To our knowledge, where strains of T. gondii are biologically and genetically different from this is the first record of T. gondii infection in a Pelicaniformes bird. The strains found in North America and Europe (Dubey et al., 2008; Dubey only other reference to T. gondii infection from this order of birds was and Su, 2009; Dubey, 2010; Khan et al., 2011). Studies on T. gondii from a red-footed booby (Sula sula) that died of toxoplasmosis on the isolates from feral chickens from different areas of mainland Brazil of Oahu, Hawaii (Work et al., 2002). The cattle egret feeds in indicated no major differences based on geography. However, T. gondii relatively dry, grassy habitats, often accompanying cattle or other large strains from the archipelago of Fernando de Noronha were genetically mammals because it catches insects and small vertebrate prey disturbed different from isolates from the mainland of Brazil (Dubey et al., 2010). by these animals. Some populations of B. ibis are migratory and others exhibit post-breeding dispersal. Infection in these birds may be an Fernando de Noronha (03u459570S, 032u199410W) is an archipelago of 21 islands and islets in the Atlantic Ocean approximately 354 km offshore indication of soil contamination with T. gondii oocysts in environment. from the Brazilian coast. The main island has an area of 18.4 km2 with a These birds may serve as prey for feral cats but the frequency is population of approximately 3,000 humans. The archipelago is a special unknown. of the state of Pernambuco (Brazil) and is regarded by In the present study, T. gondii antibodies were detected in 59% of 118 UNESCO as natural site of patrimony of humanity. Fernando de cats, and seropositive cats were found at all sampling locations on the Noronha has a varied biodiversity, with both alien species or synantropic island. The high prevalence of T. gondii infection in rats and chickens on animals, and including 700 domestic or feral cats. There is a governmental the island suggests that these animals are likely sources of infection for program to retreat and control the alien and synanthropic animals of this cats. archipelago. The objective of the present study was to determine the Among the food animals surveyed, 81% of goats, 60% of sheep, and seroprevalence of T. gondii in domestic and wild animals from Fernando 80% of chickens were seropositive for T. gondii compared with only 3% de Noronha archipelago, Brazil. seropositivity in cattle, which had low antibody levels. These findings are Between July 2007 to May 2010, blood samples were collected from 533 similar to studies in other parts of the world (Dubey, 2010). The results domestic and 231 wild animals (Table I). Serum from each animal was indicate that poultry and mutton should be thoroughly cooked before centrifuged and stored at 220 C until analysis by an indirect fluorescence human consumption. The geographic separation of the island, and the antibody test (IFAT) as described by Camargo (1974), or by the modified restricted movement of animals between the island and the mainland, agglutination test (MAT) as described by Dubey and Desmonts (1987). offers an opportunity for reducing prevalence of T. gondii in Fernando de For IFAT, species-specific conjugates were purchased from Sigma (St. Noronha. Louis, Missouri). The authors are grateful to the Administration of Fernando de The different cut-off values used for IFAT and MAT were partly Noronha, state district, Pernambuco state for logistic support, and to arbitrary and partly based on published reports by others. The cut-off for the Fundac¸a˜o O Botica´rio de Protec¸a˜o a` Natureza and the Fundac¸a˜o de IFAT was 1:64 for cattle, sheep, and goats (Faria et al., 2007; Santos et al., Amparo a` Cieˆncia e Tecnologia do Estado de Pernambuco – FACEPE. 2009; Soares et al., 2009) and 1:16 for dogs and cats (Azevedo et al., 2005; Branda˜o et al., 2006). The cut-off for MAT was 1:25 for black rats (DeFeo LITERATURE CITED et al., 2002) and 1:5 for avian species (Dubey et al., 2010). The number of animals sampled as a proportion of estimated AZEVEDO, S. S., C. S. A. BATISTA,S.A.VASCONCELLOS,D.M.AGUIAR, population (2007–2008 census) is as follows: Total examined/total animal A. M. A. RAGOZO,A.A.R.RODRIGUES,C.J.ALVES, AND S. M. GENNARI. 2005. Seroepidemiology of Toxoplasma gondii and Neos- pora caninum in dogs from the state of Paraı´ba, northeast region of DOI: 10.1645/GE-2910.1 Brazil. Research in Veterinary Science 79: 51–56.

679 680 THE JOURNAL OF PARASITOLOGY, VOL. 98, NO. 3, JUNE 2012

TABLE I. Seroprevalence of Toxoplasma gondii in domestic and wild animals from the Fernando de Noronha archipelago, Brazil.

Seropositivity Titers Species No. tested No. positive (%) Test (cut–off) 5–10 16–25 32–64 80–160 256–320 500–512 $640

Black rats (Rattus rattus) 34 13 (38.2%) .MAT (1:25) — 8 3 — — 2 — Cat (Felis catus) 118 70 (59.3%) Feral 48 32 (66.6%) .MAT (1:25) — 2 7 — — 23 — Pets 25 18 (72.0%) .IFAT (1:16) — 2 6 1 1 2 6 45 20 (44.4%) .MAT (1:25) — 6 7 ..7 . Cattle (Bos taurus) 100 3 (3.0%) .IFAT (1:16) — — 3* — — — — Cattle egret (Bubulcus ibis) 197 157 (79.7%) .MAT (1:5) 101 — 53 — — 3 — Chicken (Gallus domesticus) 100 80 (80.0%) .MAT (1:5) 14 7 12 23 9 — 15 Dog (Canis familiaris) 31 12 (38.7%) .IFAT (1:16) — 1 3 2 3 1 2 60 24 (40.0%) .MAT (1:25) — 15 9 .. .. Goat (Capra hircus) 11 9 (81.8%) .IFAT (1:16) — — 9* — — — — Horse (Equus caballus) 16 7 (43.7%) .MAT (1:25) — 4 2 — — 1 — Sheep (Ovis aries) 97 59 (60.8%) .IFAT (1:16) — — 59* — — — —

* Not titrated.

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