A survey of ectoparasites infesting urban and rural dogs of

A Survey of Ectoparasites Infesting Urban and Rural Dogs of MaranhĂŁo State, Brazil Author(s): Andrea P. Costa , Arannadia B. Silva , Francisco B. Costa , Gabriel S. Xavier , Thiago F. Martins , Marcelo B. Labruna , and Rita M.S.N.C Guerra Source: Journal of Medical Entomology, 50(3):674-678. 2013.

Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/ME12243

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A Survey of Ectoparasites Infesting Urban and Rural Dogs of Maranha˜ o State, Brazil ANDREA P. COSTA,1 ARANNADIA B. SILVA,1 FRANCISCO B. COSTA,2 GABRIEL S. XAVIER,1 THIAGO F. MARTINS,2 MARCELO B. LABRUNA,2 AND RITA M.S.N.C. GUERRA1,3

J. Med. Entomol. 50(3): 674Ð678 (2013); DOI: http://dx.doi.org/10.1603/ME12243

ABSTRACT This study evaluated for the Þrst time, ectoparasite infestations on dogs from urban and rural areas of the continental land of the state of Maranha˜o, northeastern Brazil. In total, 622 dogs were examined for ectoparasite infestations. Overall, 392 (63.0%) were infested with ectoparasites, 154 (51.3%) of 300 urban dogs and 238 (73.9%) of 322 rural dogs. Five species of ectoparasites were found, three ticks [Rhipicephalus sanguineus (Latreille), Amblyomma ovale Koch, and Amblyomma cajennense (F.)], one ßea [Ctenocephalides felis (Bouche´ )], and one louse [(Heterodoxus spininger (Enderlein)].

The frequency of infestation by R. sanguineus tended to be higher in urban than in rural areas, whereas infestations by Amblyomma ticks and C. felis ßeas tended to be higher among rural dogs. Louse (H. spininger) infestations were similarly low among all areas. Mixed infestations by at least two species of ectoparasites on the same dog were signiÞcantly more frequent on rural than on urban dogs. The most frequent mixed infestation was by R. sanguineus and C. felis, found on 11.4% of the dogs. Further studies are warranted to evaluate canine vector-borne agents in Maranha˜o, especially because most of the ectoparasites here reported are vectors of major vector-borne diseases, including zoonoses of continental importance.

KEY WORDS Acari, Siphonaptera, Phthiraptera, dog, Maranha˜o

Ectoparasites are known to infest dogs worldwide, causing various diseases due to their irritant action, blood-feeding action, or both on the host, besides the transmission of infectious agents that many times are also zoonotic agents (Dantas-Torres 2008). In Brazil, multiple studies have evaluated ectoparasite infestations (mostly by ticks) among domestic dogs from the southern region (Ribeiro et al. 1997, Labruna et al.

2001, Bellato et al. 2003), southeastern region (Linardi and Nagem 1973, Szabo´ et al. 2001, Soares et al. 2006, Rodrigues et al. 2008), central western region (Lustosa et al. 1973, Melo et al. 2011), northern region (Labruna et al. 2000, 2005; Castro and Rafael 2006), and in the state of Pernambuco, northeastern Brazil (Dantas-Torres et al. 2004, 2009; Dantas-Torres 2009).

The state of Maranha˜o, located in northeastern Brazil, has an area of 333,366 km2 and a population of ⬃6,500,000 inhabitants. It is located in a large transition area of three major Brazilian biomes: Amazonia (rain forest), Cerrado (savannah), and Caatinga (semiarid). To our knowledge, reports of ectoparasites infesting domestic dogs in Maranha˜o have been 1 Laborato ´ rio de Parasitologia, Curso de Medicina Veterina´ria, Universidade Estadual do Maranha˜o (UEMA), Campus Universita´rio Paulo VI, S/N, Tirirical, CEP 65055-150 Sa˜o Luõ´s, MA, Brazil.

2 Departamento de Medicina Veterina ´ria Preventiva e Sau´ de Animal (VPS), Faculdade de Medicina Veterina´ria e Zootecnia (FMVZ), Universidade de Sa˜o Paulo (USP), CEP 05508-270 Sa˜o Paulo, SP, Brazil.

3 Corresponding author, e-mail: grita62@hotmail.com.

restricted to Sa˜o Luis Island (the state capital), where dogs were found to be infested by Rhipicephalus sanguineus (Latreille) ticks, Ctenocephalides felis (Bouche´ ) ßeas, and Heterodoxus spiniger (Enderlein) lice (Guerra and Brito 2004, Franco-Amorim et al. 2010); therefore, the current study evaluated for the Þrst time the ectoparasite infestations on dogs from urban and rural areas of continental Maranha˜o.

Materials and Methods Study Area. This study was carried out in two microregions (⫽counties) of Maranha˜o state, northeastern Brazil: one county was located in the eastern part of Chapadinha microregion (3⬚ 44⬘ S, 43⬚ 21⬘ W; elevation, 110 m) and the other country was located in the western part of Imperatriz microregion (5⬚ 31⬘ S, 47⬚ 28⬘ W, elevation 450 m) (Fig. 1).

The Chapadinha microregion is located in the eastern region of Maranha˜o state and comprises nine municipalities from which Chapadinha, Mata-Roma, and Anapurus were sampled for the current study. The climate is tropical humid. The rainy season extends from December to May, and the dry season extends from July to November. The annual average temperature is 27⬚C, with a maximum of 37⬚C and minimum 21⬚C; mean annual rainfall ranges from 1,200 to 1,400 mm. The predominant vegetation is Cerrado with a ßoristic composition featuring two diverse types of

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Fig. 1. Map of the microregions (⫽counties) of Chapadinha and Imperatriz in Maranha˜o State, Brazil.

vegetation: deciduous forest and aeasonal forest (Selbach and Leite 2008).

Imperatriz microregion is located in the western region of Maranha˜o state and is divided into 16 municipalities from which Imperatriz, Governador Edison Loba˜o, and Davino´ polis were sampled for the current study. The climate is warm-dry from May to September and warm-humid from October to April.

The annual average temperature is 29⬚C, with a maximum of 38⬚C and minimum of 21⬚C; mean annual rainfall is 1,600 mm. It presents mixed vegetation types with characteristics of both Cerrado and Amazon rain forest.

Collection and Identification of Ectoparasites. In total, 622 owned dogs were randomly sampled in urban and rural areas of Chapadinha (during March 2010) and Imperatriz (during March 2011) microregions, on request to their owners. Samples were divided into 300 dogs from urban areas (150 from Chapadinha, 150 from Imperatriz) and 322 dogs from rural areas (172 from Chapadinha, 150 from Imperatriz).

These sample numbers were previously calculated to be representative of each area, as stated later in the text. Whereas rural dogs were sampled in the three municipalities of each microregion, urban dogs were restricted to Chapadinha and Imperatriz municipalities. Rural dogs were sampled at least 30 km far from the nearest urban area. Dogs were all crossbred, of either sex, and different ages. All dogs were evaluated by visual inspection and palpation for the presence of ectoparasites. The whole dog body was examined, and efforts were taken to collect the maximum possible number of ectoparasites per dog; however, representative samples were collected from highly infested animals. After manual collection, ectoparasites were kept in vials containing 70% ethanol. Fleas and lice were slide-mounted in Canada balsam. Ectoparasites

were identiÞed according to current taxonomic keys, including Araga˜o and Fonseca (1961), Onofrio et al.

(2006), and Martins et al. (2010) for ticks; Furman and Catts (1977) for lice; and Linardi and Guimara˜es (2000) for ßeas. Voucher specimens were deposited at the National Tick Collection of the University of Sa˜o Paulo.

Statistical Analyses. The minimum number (150) of sampled dogs in each urban or rural area was statistically calculated considering a canine population, representing one Þfth of the human population, expected ectoparasite frequency of 30% (10% conÞdence limits [CL]), and 99% sample conÞdence level.

The chi-square test or Fisher exact test (when indicated) was used to compare the number of infested dogs between rural and urban areas. Analyses were performed using Epi Info software, version 6.04d (Centers for Disease Control and Prevention, Atlanta, GA). A 5% signiÞcance level was applied.

Results In total, 622 dogs in both microregions were examined. Overall, 392 (63.0%) were infested with ectoparasites, 154 (51.3%) of 300 urban dogs and 238 (73.9%) of 322 rural dogs; signiÞcantly more rural dogs were infested than urban dogs (P ⬍ 0.05). Five species of ectoparasites were found, three ticks [R. sanguineus, Amblyomma ovale Koch, and Amblyomma cajennense (F.)], one ßea (C. felis), and one louse (H. spininger). In total, 1,584 specimens of ectoparasites were collected. R. sanguineus was by far the most abundant, represented by 1,235 (78.0%) specimens (486 males, 648 females, and 101 nymphs). The ßea C. felis was the second most frequent ectoparasite, represented by 255 (16.0%) specimens (57 males, 198 females). The remaining ectoparasites were repre-

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Table 1. Ectoparasites infesting dogs from the urban and rural areas of Chapadinha and Imperatriz microregions in the state of Maranhão, northeastern Brazil No. of infested dogs (%) Ectoparasitea Ticks Rsangu Acajen Aovale Fleas Cfelis Lice Hspini

Chapadinhab

Imperatrizc

Total

Urban

Rural

Urban

Rural

91 (60.7)a 2 (1.3)a,b 0a

111 (64.5)a 9 (5.2)b 17 (9.9)b

45 (30.0)b 0a 0a

71 (47.3)c 0a 0a

318 (51.1) 11 (1.8) 17 (2.7)

31 (20.7)a

59 (34.3)b

11 (7.3)c

43 (28.7)a,b

144 (23.2)

4 (2.7)a

8 (4.7)a

2 (1.3)a

2 (1.3)a

16 (2.6)

Numbers followed by different letters in the same line indicate statistically signiÞcant differences (P ⬍ 0.05). a Rsangu, Rhipicephalus sanguineus; Acajen, Amblyomma cajennense; Aovale, Amblyomma ovale; Cfelis, Ctenocephalides felis; and Hspini: Heterodoxus spiniger. b 150 and 172 dogs were sampled in the urban and rural areas, respectively. c 150 and 150 dogs were sampled in the urban and rural areas, respectively.

sented by 39 (2.5%) specimens of A. cajennense (11 males, 22 females, and 6 nymphs), 24 (1.5%) of A. ovale (15 males and 9 females), and 31 (2.0%) of H. spiniger (9 males and 22 females).

The frequency of infestation by R. sanguineus was higher in urban than in rural areas, although this difference was signiÞcant only for Imperatriz microregion (P ⬍ 0.05) (Table 1). Two Amblyomma species were found infesting dogs from only Chapadinha, where rural dogs presented higher infestations (signiÞcantly different for A. ovale, but not for A. cajennense). In both microregions, ßea infestations were signiÞcantly more frequent among rural than on urban dogs (P ⬍ 0.05), whereas the frequency of lice infestation was similarly low among all areas (Table 1).

Considering each of the two microregions separately, mixed infestations by at least two species of ectoparasites on the same dog were signiÞcantly more frequent on rural than on urban dogs (Table 2). The rural area of Chapadinha accounted for most of the mixed infestation reports. The most frequent mixed

infestation was by R. sanguineus and C. felis that were found concomitantly on 11.4% of the infested dogs, including urban and rural areas. All other mixed infestation types were found on only 0.3Ð1.3% of the infested dogs (Table 2).

Discussion The current study reports Þve species of ectoparasites infesting dogs in the state of Maranha˜o. To our knowledge, this is the Þrst report of A. ovale in Maranha˜o, as previous reviews did not include the state of Maranha˜o in the distribution area of A. ovale (Guglielmone et al. 2003, Labruna et al. 2005). Regarding ticks, we found that dogs of both urban and rural areas were infested mostly or only by R. sanguineus, although some rural dogs were also infested by two Amblyomma species, and only two urban dogs were infested by Amblyomma ticks. Overall, these results agree with previous studies in other Brazilian regions, where R. sanguineus has been the most prevalent tick

Table 2. Mixed species ectoparasite infestation on dogs from the urban and rural areas of Chapadinha and Imperatriz microregions in the state of Maranhão, northeastern Brazil No. of infested dogs (%) Ectoparasitea Three species Rsangu ⫹ Aovale ⫹ Cfelis Rsangu ⫹ Cfelis ⫹ Hspini Two species Rsangu ⫹ Acajen Rsangu ⫹ Aovale Rsangu ⫹ Cfelis Rsangu ⫹ Hspini Cfelis ⫹ Acajen Cfelis ⫹ Aovale Cfelis ⫹ Hspini Total

Chapadinhab

Imperatrizc

Total

Urban

Rural

Urban

Rural

0a 0a

5 (2.9)a 1 (0.6)a

0a 0a

0a 1 (0.3)a

5 (0.8) 2 (0.3)

1 (0.7)a,b 0a 21 (14.0)a 3 (2.0)a 1 (0.7)a 0a 1 (0.7)a 27 (18.0)a

7 (4.1)a 8 (4.7)b 29 (16.9)a 3 (1.7)a 1 (0.6)a 2 (1.2)a 1 (0.6)a 57 (33.1)b

0b 0a 4 (2.7)b 0a 0a 0a 1 (0.7)a 5 (3.3)c

0b 0a 17 (7.0)a 0a 0a 0a 0a 18 (12.0)a

8 (1.3) 8 (1.3) 71 (11.4) 6 (1.0) 2 (0.3) 2 (0.3) 3 (0.5) 107 (17.2)

Numbers followed by different letters in the same line indicate statistically signiÞcant differences (P ⬍ 0.05). a Rsangu, Rhipicephalus sanguineus; Acajen, Amblyomma cajennense; Aovale, Amblyomma ovale; Cfelis, Ctenocephalides felis; and Hspini, Heterodoxus spiniger. b 150 and 172 dogs were sampled in the urban and rural areas, respectively. c 150 and 150 dogs were sampled in the urban and rural areas, respectively.

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infesting dogs in urban areas (Ribeiro et al. 1997, Szabo´ et al. 2001, Bellato et al. 2003, Dantas-Torres et al. 2004, Labruna et al. 2005, Soares et al. 2006). The tick R. sanguineus is native to Africa and was introduced in Brazil by humans (Guglielmone et al. 2003). In this country, R. sanguineus exhibits a typical nidicolous life cycle inside human dwellings (Labruna et al. 2000). As human dwellings are also present in rural areas, R. sanguineus has established in these areas but usually in low numbers compared with urban areas (Szabo´ et al.

2001, 2010; Labruna et al. 2005). However, Amblyomma-infested dogs have been associated mostly with rural areas, as these ticks are native to Brazil, where they are established in natural biomes (Labruna et al.

2005). In Maranha˜o, two Amblyomma species (A. cajennense and A. ovale) were found infesting rural dogs.

These results agree with previous studies in other regions of Brazil, where A. cajennense and A. ovale were the only Amblyomma species infesting rural dogs (Szabo´ et al. 2001, 2010; Dantas-Torres 2009; Melo et al. 2011).

The ßea C. felis is the most common ßea species infesting dogs in Brazil, both in urban and rural areas (Linardi and Guimara˜es 2000, Castro and Rafael 2006).

In the current study, ßea-infested dogs were signiÞcantly higher in the rural than in the urban area. This scenario is similar to what was reported in the state of Pernambuco, northeastern Brazil (Dantas-Torres et al. 2004, 2009), where it was suggested that most owners of rural dogs could not afford the cost of ectoparasite control. Our Þndings of the louse H. spiniger in dogs from urban and rural areas corroborate recent studies in central western, northern, and northeastern Brazil, where H. spiniger was the main louse species infesting dogs (Dantas-Torres et al. 2004, 2009; Castro and Rafael 2006; Melo et al. 2011). However, these results contrast to southeastern and southern Brazil, where Trichodectes canis (De Geer) has been reported as the main louse species infesting dogs (Bellato et al.

2003; Rodrigues et al. 2001, 2008).

Mixed infestations by two or three ectoparasites on the same individual dogs were signiÞcantly more frequent in the rural area. Indeed, this Þnding is related to a greater contact of rural dogs with different environmental types (e.g., human dwellings, forests, livestock pastures), where different ticks are found (Labruna et al. 2005). However, this ectoparasite diversity also could be associated with acaricide pressure that tends to be greater on urban than on rural dogs, as observed in southeastern Brazil (Szabo´ et al.

2001).

In other areas of Brazil, R. sanguineus is recognized as the vector of the canine pathogens Ehrlichia canis, Rickettsia rickettsii, and Babesia vogeli (Dantas-Torres 2008, Pacheco et al. 2011); A. cajennense is a major vector of R. rickettsii (Soares et al. 2012); A. ovale is vector of R. parkeri and Hepatozoon canis (Rubini et al.

2009, Medeiros et al. 2011); and the ßea C. felis is the vector of several bacterial pathogens, besides being an intermediate host of canine helminths (Dantas-Torres 2008). As all these ectoparasites were found infesting dogs in the state of Maranha˜o, further studies are

677

warranted to evaluate the occurrence of such vectorborne agents among vertebrate and invertebrate hosts in Maranha˜o, especially because some of these agents can also infect humans, causing zoonosis of continental importance.

Acknowledgments We thank Fundac¸ a˜o de Amparo a´ Pesquisa e ao Desenvolvimento Cientõ´Þco e Tecnolo´ gico do Maranha˜o (FAPEMA) for Þnancial support and Conselho Nacional de Desenvolvimento Cientõ´Þco e Tecnolo´ gico (CNPq) and Coordenac¸ a˜o de Aperfeic¸ oamento de Pessoal de Nõ´vel Superior (CAPES) for scholarships to G.S.X., A.P.C., and A.B.S.

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Received 30 October 2012; accepted 28 February 2013.