• View in gallery

    Municipalities sampled in this study, according to geopolitical regions (A), biomes (B), and climate zones (C) of continental Brazil. Numbers refer to municipality names in Table 1.

  • 1.

    Adams JR, Schmidtmann ET, Azad AF, 1990. Infection of colonized cat fleas, Ctenocephalides felis (Bouché), with a Rickettsia-like microorganism. Am J Trop Med Hyg 43: 400409.

    • Search Google Scholar
    • Export Citation
  • 2.

    Bouyer DH, Stenos J, Crocquet-Valdes P, Moron CG, Popov VL, Zavala-Velazquez JE, Foil LD, Stothard DR, Azad AF, Walker DH, 2001. Rickettsia felis: molecular characterization of a new member of the spotted fever group. Int J Syst Evol Microbiol 51: 339347.

    • Search Google Scholar
    • Export Citation
  • 3.

    Choi YJ, Lee EM, Park JM, Lee KM, Han SH, Kim JK, Lee SH, Song HJ, Choi MS, Kim IS, Park KH, Jang WJ, 2007. Molecular detection of various rickettsiae in mites (Acari: Trombiculidae) in southern Jeolla Province, Korea. Microbiol Immunol 51: 307312.

    • Search Google Scholar
    • Export Citation
  • 4.

    Tsui PY, Tsai KH, Weng MH, Hung YW, Liu YT, Hu KY, Lien JC, Lin PR, Shaio MF, Wang HC, Ji DD, 2007. Molecular detection and characterization of spotted fever group rickettsiae in Taiwan. Am J Trop Med Hyg 77: 883890.

    • Search Google Scholar
    • Export Citation
  • 5.

    Thepparit C, Sunyakumthorn P, Guillotte ML, Popov VL, Foil LD, Macaluso KR, 2011. Isolation of a rickettsial pathogen from a non-hematophagous arthropod. PLoS ONE 6: e16396.

    • Search Google Scholar
    • Export Citation
  • 6.

    Abarca K, López J, Acosta-Jamett G, Martínez-Valdebenito C, 2013. Rickettsia felis in Rhipicephalus sanguineus from two distant Chilean cities. Vector Borne Zoonotic Dis 13: 607609.

    • Search Google Scholar
    • Export Citation
  • 7.

    Socolovschi C, Pagés F, Raoult D, 2012. Rickettsia felis in Aedes albopictus mosquitoes, Libreville, Gabon. Emerg Infect Dis 18: 16871689.

  • 8.

    Socolovschi C, Pagés F, Ndiath MO, Ratmanov P, Raoult D, 2012. Rickettsia species in African Anopheles mosquitoes. PLoS ONE 7: e48254.

  • 9.

    Pérez-Osorio CE, Zavala-Velazquez JE, Arias Leon JJ, Zavala-Castro JE, 2008. Rickettsia felis as emergent global threat for humans. Emerg Infect Dis 14: 10191023.

    • Search Google Scholar
    • Export Citation
  • 10.

    Reif KE, Macaluso KR, 2009. Ecology of Rickettsia felis: a review. J Med Entomol 46: 723736.

  • 11.

    Mediannikov O, Cabre O, Qu F, Socolovschi C, Davoust B, Marié J, Parola P, Raoult D, 2011. Rickettsia felis and Bartonella clarridgeiae in fleas from New Caledonia. Vector Borne Zoonotic Dis 11: 181183.

    • Search Google Scholar
    • Export Citation
  • 12.

    Troyo A, Aìlvare D, Taylor L, Abdalla G, Calderon-Arguedas O, Zambrano ML, Dasch GA, Lindblade K, Hun L, Eremeeva ME, Esteìvez A, 2012. Rickettsia felis in Ctenocephalides felis from Guatemala and Costa Rica. Am J Trop Med Hyg 86: 10541056.

    • Search Google Scholar
    • Export Citation
  • 13.

    Oliveira RP, Galvao MA, Mafra CL, Chamone CB, Calic SB, Silva SU, Walker DH, 2002. Rickettsia felis in Ctenocephalides spp. fleas, Brazil. Emerg Infect Dis 8: 317319.

    • Search Google Scholar
    • Export Citation
  • 14.

    Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TT, 2007. Rickettsia infection in five areas of the State of São Paulo, Brazil. Mem Inst Oswaldo Cruz 102: 793801.

    • Search Google Scholar
    • Export Citation
  • 15.

    Gehrke FS, Gazeta GS, Souza ER, Ribeiro A, Marrelli MT, Schumaker TT, 2009. Rickettsia rickettsii, Rickettsia felis and Rickettsia sp. TwKM03 infecting Rhipicephalus sanguineus and Ctenocephalides felis collected from dogs in a Brazilian spotted fever focus in the State of Rio De Janeiro/Brazil. Clin Microbiol Infect S2: 267268.

    • Search Google Scholar
    • Export Citation
  • 16.

    Raoult D, La Scola B, Enea M, Fournier PE, Roux V, Fenollar F, Galvao MA, Lamballerie X, 2001. A flea-associated Rickettsia pathogenic for humans. Emerg Infect Dis 7: 7381.

    • Search Google Scholar
    • Export Citation
  • 17.

    Maina AN, Knobel DL, Jiang J, Halliday J, Feikin DR, Cleaveland S, Nganga Z, Junghae M, Breiman RF, Richards AL, Njenga MK, 2012. Infection in febrile patients, western Kenya, 2007–2010. Emerg Infect Dis 18: 328331.

    • Search Google Scholar
    • Export Citation
  • 18.

    Nilsson K, Wallménius K, Hartwig S, Norlander T, Pahlson C, 2013. Bell's palsy and sudden deafness associated with Rickettsia spp. Infection in Sweden. A retrospective and prospective serological survey including PCR findings. Eur J Neurol 21: 206214.

    • Search Google Scholar
    • Export Citation
  • 19.

    Linardi PM, Guimarães LR, 2000. Sifonápteros do Brasil. São Paulo: Museu de Zoologia USP/FAPESP.

  • 20.

    Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, Popov V, Gennari SM, Walker DH, 2004. Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of Sao Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol 42: 9098.

    • Search Google Scholar
    • Export Citation
  • 21.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, 1990. Basic local alignment search tool. J Mol Biol 215: 403410.

  • 22.

    Junk WJ, Cunha CN, Wantzen KM, Petermann P, Strussmann C, Marques MI, Adis J, 2006. Biodiversity and its conservation in the Pantanal of Mato Grosso, Brazil. Aquat Sci 68: 278309.

    • Search Google Scholar
    • Export Citation
  • 23.

    Mendonça F, Danni-Oliveira IM, 2007. Climatologia: noções básicas e climas do Brasil. São Paulo: Oficina de Textos.

  • 24.

    Parola P, 2011. Rickettsia felis: from a rare disease in the USA to a common cause of fever in sub-Saharan Africa. Clin Microbiol Infect 17: 9961000.

    • Search Google Scholar
    • Export Citation
  • 25.

    Mediannikov O, Abdissa A, Diatta G, Trape J-F, Raoult D, 2012. Rickettsia felis in fleas, southern Ethiopia. Emerg Infect Dis 18: 13851386.

  • 26.

    Katz G, Camargo Neves VL, Angerami RN, Nascimento EM, Colombo S, 2009. Situação epidemiológica e importância da febre maculosa brasileira no Estado de São Paulo. Boletim Epidemiológico Paulista 6: 413.

    • Search Google Scholar
    • Export Citation
  • 27.

    Del Fiol FS, Junqueira FM, Rocha MC, Toledo MI, Filho SB, 2010. Rocky Mountain spotted fever in Brazil. Rev Panam Salud Publica 27: 461466.

  • 28.

    Horta MC, Scott FB, Correia TR, Fernandes JI, Richtzenhain LJ, Labruna MB, 2010. Rickettsia felis infection in cat fleas Ctenocephalides felis felis. Braz J Microbiol 41: 813818.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 
 
 

 

 

 

 

 

 

Rickettsia felis in Ctenocephalides felis felis from Five Geographic Regions of Brazil

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  • Federal University of São Francisco Valley, Petrolina, PE, Brazil; Faculty of Veterinary Medicine, University of São Paulo, São Paulo, SP, Brazil

This study evaluated rickettsial infection in 701 Ctenocephalides felis felis fleas that were collected from dogs and cats in 31 municipalities, encompassing all regions and major biomes of Brazil. A total of 268 (38.2%) fleas from 30 municipalities were polymerase chain reaction (PCR) positive for the rickettsial gltA gene. The PCR products from 44 fleas, consisting of at least 1 PCR-positive flea from each of 30 municipalities, generated DNA sequences identical to Rickettsia felis. Rickettsial prevalence was highly variable among 30 municipalities, with values ranging from 2.9% to 100%. Significantly higher infection rates by R. felis were associated with the Pampa biome (southern Brazil), and the temperate climate that prevails in southern Brazil. In contrast, lowest R. felis-infection rates were significantly associated with the Caatinga biome, and its semiarid climate. Further studies should evaluate the effect of temperature and moisture on the R. felis infection in Ctenocephalides fleas world widely.

Introduction

Rickettsia felis, an obligate intracellular Gram-negative bacterium, was first described infecting internal tissues of the flea Ctenocephalides felis felis in the United States.1,2 Since then, the bacterium has been reported infecting a number of invertebrate species, including fleas, mosquitoes, ticks, mites, and booklice.38 Despite an apparent broad host range, the majority of the literature reports of R. felis have been on fleas of the genus Ctenocephalides; namely, C. felis felis and Ctenocephalides canis collected from domestic dogs and cats.912 In Brazil, R. felis was reported infecting Ctenocephalides fleas in the states of São Paulo, Minas Gerais, and Rio de Janeiro, all in the Southeastern region of the country.1315

Rickettsia felis has been reported globally as an emerging disease agent. Human disease attributed to R. felis infection, have been reported in all continents, mostly during the last 5 years.9,1618 In Brazil, R. felis was associated with a febrile rash in two patients from the state of Minas Gerais.16

Brazil is a continental country, divided into five geopolitical regions (North, Northeast, Middle-West, Southeast, and South) and six major biomes: Amazon (rainforest), Caatinga (semiarid), Cerrado (savannah), Pantanal (wetlands), Pampa (open fields), and the Atlantic rainforest. Because only a few studies have investigated R. felis infection in Brazil (all in the Southeast region), this study evaluated rickettsial infection in fleas collected from different areas of all five geopolitical regions of the country, encompassing the six major biomes.

Material and Methods

From 2006 to 2009, fleas were collected on domestic dogs and cats of 31 municipalities (mean: 23 fleas per municipality) among the five geopolitical regions of Brazil: North (5 municipalities); Northeast (7); Middle-West (4); Southeast (8); and South (7) (Table 1). Sampling localities were chosen by convenience, depending on the availability of collaborators in each locality, as stated in the Acknowledgment section. Care was taken to include only fleas that were collected from animals living in outdoor conditions. Collected fleas were preserved in absolute ethanol and brought to the laboratory, where they were identified to species following Linardi and Guimarães,19 and individually submitted to DNA extraction by boiling at 100°C for 20 min following Horta and others.14 Fleas were individually tested for the presence of Rickettsia by polymerase chain reaction (PCR) using primers CS-78 and CS-323, targeting a 401 fragment of the rickettsial gltA gene.20 In each PCR run, Rickettsia parkeri DNA was used as a positive control, and at least two negative controls (water). The PCR products were DNA sequenced and submitted to basic local alignment search tool (BLAST) analysis to determine similarities to other Rickettsia species.21

Table 1

Rickettsial infection in Ctenocephalides felis felis fleas collected from dogs and cats in the five geopolitical regions of Brazil

RegionMunicipalityStateNo. in Figure 1No. infected fleas/no. tested fleas (%)
MunicipalityRegion
North    38/111 (34.2)
BelémPará11/25 (4) 
MacapáAmapá20/20 (0) 
ManausAmazonas318/20 (90) 
MarabáPará417/21 (81) 
Monte NegroRondônia52/25 (8) 
Northeast    33/168 (19.6)
FortalezaCeará62/25 (8) 
Jaboatão dos GuararapesPernambuco710/24 (41.7) 
MossoróRio G. do Norte82/25 (8) 
NatalRio G. do Norte92/20 (10) 
PatosParaíba107/20 (35) 
SalvadorBahia119/20 (45) 
TeresinaPiauí121/34 (2.9) 
Middle-West    25/88 (28.4)
BrasíliaDistrito Federal137/22 (31.8) 
CuiabáMato Grosso141/25 (4) 
DouradosMato G. do Sul1514/20 (70) 
PoconéMato Grosso163/21 (14.3) 
Southeast    68/188 (36.3)
Juiz de ForaMinas Gerais178/20 (40) 
Montes ClarosMinas Gerais1817/20 (85) 
Presidente PrudenteSão Paulo1911/21 (52.4) 
Rio de JaneiroRio de Janeiro203/26 (11.5) 
São José do Rio PretoSão Paulo2110/38 (26.3) 
São PauloSão Paulo227/20 (35) 
UberlândiaMinas Gerais236/22 (27,3) 
Vila VelhaEspírito Santo246/21 (28.6) 
South    104/146 (71.2)
AraranguáSanta Catarina2520/20 (100) 
BandeirantesParaná2610/20 (50) 
BlumenauSanta Catarina2719/20 (95) 
Cândido de AbreuParaná2815/25 (60) 
PelotasRio G. do Sul2919/20 (95) 
RolândiaParaná307/20 (35) 
Santa MariaRio G. do Sul3114/21 (66.7) 
Total    268/701 (38.2)

The proportions of Rickettsia-infected fleas were compared between geopolitical regions (North, Northeast, Middle-West, Southeast, South), between biome types (Amazon, Caatinga, Cerrado, Atlantic rainforest, Pampa, Pantanal), and between major Climate types (Equatorial, Temperate, Tropical Central Brazil, Tropical Oriental Northeast, Tropical Equatorial Zone) by the χ2 distribution, using the program Minitab 16.1.0. Values were considered significantly different when P < 0.05. The geographical distributions of the sampled municipalities according to biome and climate types were retrieved from the official database of the Brazilian Institute of Geography and Statistics (http://www.ibge.gov.br/). For comparison purposes, the Pantanal biome was considered as belonging to the Cerrado biome, following Junk and others.22

Results

A total of 701 fleas were collected, 665 from dogs and only 36 from cats. All fleas were identified as C. felis felis. A total of 268 (38.2%) individual fleas, 255 from dogs and 13 from cats, yielded PCR products of the expected size for the rickettsial gltA gene. Only one of the 31 municipalities did not yield at least one PCR-positive flea (Table 1). Rickettsial prevalence was highly variable among 30 municipalities, with values ranging from 2.9% to 100%. The gltA product from 44 fleas, consisting of at least one or two PCR-positive fleas from each of 30 municipalities, yielded DNA sequences identical to each other, and 100% identical to the corresponding sequence of the R. felis type strain (GenBank accession no. CP000053).

The geographic distributions of the 31 municipalities sampled in this study are shown in Figure 1, according to the geopolitical region, biome type, and climate type. The proportions of infected fleas were significantly different (P < 0.05) between the five geopolitical regions, with the South region having the highest prevalence (71.2%), and the Northeast region the lowest prevalence (19.6%) (Table 1). The proportions of infected fleas were significantly different (P < 0.05) between biome, with the highest rickettsial prevalence in Pampa (33 of 41; 80.5%), followed by Atlantic rainforest (141 of 297; 47.5), Amazon (38 of 111; 34.2%), Atlantic rainforest (44 of 148; 29.7), and Caatinga (12 of 104; 11.5%). The proportions of infected fleas were significantly different (P < 0.05) between climate types, with the highest rickettsial prevalence in Temperate (87 of 106; 82.1%), followed by Tropical Central Brazil (110 of 206; 34.8), Equatorial (38 of 111; 34.2%), Tropical Oriental Northeast (21 of 64; 32.8%), and Tropical Equatorial Zone (12 of 104; 11.5%).

Figure 1.
Figure 1.

Municipalities sampled in this study, according to geopolitical regions (A), biomes (B), and climate zones (C) of continental Brazil. Numbers refer to municipality names in Table 1.

Citation: The American Society of Tropical Medicine and Hygiene 91, 1; 10.4269/ajtmh.13-0699

Discussion

This study shows that the infection by R. felis is widespread along flea populations in continental Brazil, encompassing all geopolitical regions or all biome types. Although we generated DNA sequences for only 1–2 fleas per locality, we assume that the remaining PCR-positive fleas referred to R. felis because it has been the major agent (most of time the sole agent) infecting C. felis worldwide.9,10 Rickettsial infection rates were highly variable among flea populations from the 31 sampled localities, in accordance with literature reports that have shown that R. felis is found infecting 0% to 100% of fleas from populations sampled word widely.10 Interestingly, significantly higher infection rates by R. felis were associated with the Pampa biome (southern Brazil), and the temperate climate that prevails in southern Brazil. This part of Brazil is characterized by having the lowest winter temperatures of the country, typically below 10°C, with occasional snow.23 In contrast, lowest R. felis-infection rates were significantly associated with the Caatinga biome, and its Tropical Equatorial zone climate. This climate is characterized mainly by having the lowest precipitation rates of Brazil, in strong association with the Caatinga biome, forming the only semiarid region of Brazil.23 Rickettsia felis-infection rates were of intermediate values among the remaining biomes or climate types of Brazil, where temperature is not as cold as in Pampas, or where precipitation rates are not as low as in the Caatinga. Because all flea samples were collected from animals living at outdoors conditions, we can assume that free-living stages of these fleas were, at some extent, affected by the different temperature and precipitation rate conditions inherent to each biome.

This is the first study that associates flea-R. felis infection with environmental conditions. Because it has been shown that infection rates by R. felis is highly variable among flea populations in all continents of the world,912 further studies should evaluate the effect of temperature and moisture on the R. felis infection in Ctenocephalides fleas.

Recent studies have considered R. felis as a global emerging pathogen.24 This scenario, in conjunction with our present study, indicates that humans are at risk of acquiring R. felis-caused spotted fever in all regions of Brazil, because a large number of recent studies have reported that Ctenocephalides fleas are major vectors of R. felis.10,24,25 Contrastingly, only two cases of human infection by R. felis have been reported in Brazil,16 where modern diagnostic tools are available for surveillance of spotted fever in some areas (Southeastern region) that have reported hundreds of cases of tick-borne spotted fever, caused mainly by Rickettsia rickettsii.26,27 Interestingly, one study in Rio de Janeiro (southeastern Brazil) reported no history of spotted fever among 15 persons that were frequently bitten by R. felis-infected fleas.28 Indeed, further studies are needed to evaluate the real risk of humans to acquire spotted fever caused by R. felis in Brazil, because there is no doubt that humans live in close association with R. felis-infected fleas throughout the country.

ACKNOWLEDGMENTS

We are deeply grateful to the following colleagues that kindly provided flea specimens (municipality in parentheses) for this study: Ana Paula Mundim (Manaus), Christina Whiteman (Belém), Cleide Campostrini (Marabá), Daniela Chiebao (Blumenau), Diógenes Soares da Silva (Natal), Eliane Piranda (Rio de Janeiro), Elizandra Matos (Macapá), Elizângela Guedes (Juiz de Fora), Flavio Otomura (Cândido de Abreu), Francisco Silva (Teresina), Herbert Soares (Fortaleza), Ingrid Rosso (Araranguá), Jonas Moraes Filho (Cuiabá), Juçara Gomes (Vila Velha), Julia Lima (Natal), Leandra Ferreira (São Paulo), Luciana Viero (Santa Maria), Luciane Silveira (Bandeirantes), Magno Borges (Montes Claros), Marcelo Zanutto (Salvador), Márcio Castro (Brasília), Matias Szabó (Uberlândia), Nara Arruda (Jaboatão dos Guararapes), Nilton C. Filho (Pelotas), Patricia Ferreira (São Paulo), Richard Pacheco (Dourados), Roberta Toledo (Rolândia), Sergio Azevedo (Patos), Sílvia Ahid (Mossoró), and Tatiana Ueno (São José do Rio Preto).

  • 1.

    Adams JR, Schmidtmann ET, Azad AF, 1990. Infection of colonized cat fleas, Ctenocephalides felis (Bouché), with a Rickettsia-like microorganism. Am J Trop Med Hyg 43: 400409.

    • Search Google Scholar
    • Export Citation
  • 2.

    Bouyer DH, Stenos J, Crocquet-Valdes P, Moron CG, Popov VL, Zavala-Velazquez JE, Foil LD, Stothard DR, Azad AF, Walker DH, 2001. Rickettsia felis: molecular characterization of a new member of the spotted fever group. Int J Syst Evol Microbiol 51: 339347.

    • Search Google Scholar
    • Export Citation
  • 3.

    Choi YJ, Lee EM, Park JM, Lee KM, Han SH, Kim JK, Lee SH, Song HJ, Choi MS, Kim IS, Park KH, Jang WJ, 2007. Molecular detection of various rickettsiae in mites (Acari: Trombiculidae) in southern Jeolla Province, Korea. Microbiol Immunol 51: 307312.

    • Search Google Scholar
    • Export Citation
  • 4.

    Tsui PY, Tsai KH, Weng MH, Hung YW, Liu YT, Hu KY, Lien JC, Lin PR, Shaio MF, Wang HC, Ji DD, 2007. Molecular detection and characterization of spotted fever group rickettsiae in Taiwan. Am J Trop Med Hyg 77: 883890.

    • Search Google Scholar
    • Export Citation
  • 5.

    Thepparit C, Sunyakumthorn P, Guillotte ML, Popov VL, Foil LD, Macaluso KR, 2011. Isolation of a rickettsial pathogen from a non-hematophagous arthropod. PLoS ONE 6: e16396.

    • Search Google Scholar
    • Export Citation
  • 6.

    Abarca K, López J, Acosta-Jamett G, Martínez-Valdebenito C, 2013. Rickettsia felis in Rhipicephalus sanguineus from two distant Chilean cities. Vector Borne Zoonotic Dis 13: 607609.

    • Search Google Scholar
    • Export Citation
  • 7.

    Socolovschi C, Pagés F, Raoult D, 2012. Rickettsia felis in Aedes albopictus mosquitoes, Libreville, Gabon. Emerg Infect Dis 18: 16871689.

  • 8.

    Socolovschi C, Pagés F, Ndiath MO, Ratmanov P, Raoult D, 2012. Rickettsia species in African Anopheles mosquitoes. PLoS ONE 7: e48254.

  • 9.

    Pérez-Osorio CE, Zavala-Velazquez JE, Arias Leon JJ, Zavala-Castro JE, 2008. Rickettsia felis as emergent global threat for humans. Emerg Infect Dis 14: 10191023.

    • Search Google Scholar
    • Export Citation
  • 10.

    Reif KE, Macaluso KR, 2009. Ecology of Rickettsia felis: a review. J Med Entomol 46: 723736.

  • 11.

    Mediannikov O, Cabre O, Qu F, Socolovschi C, Davoust B, Marié J, Parola P, Raoult D, 2011. Rickettsia felis and Bartonella clarridgeiae in fleas from New Caledonia. Vector Borne Zoonotic Dis 11: 181183.

    • Search Google Scholar
    • Export Citation
  • 12.

    Troyo A, Aìlvare D, Taylor L, Abdalla G, Calderon-Arguedas O, Zambrano ML, Dasch GA, Lindblade K, Hun L, Eremeeva ME, Esteìvez A, 2012. Rickettsia felis in Ctenocephalides felis from Guatemala and Costa Rica. Am J Trop Med Hyg 86: 10541056.

    • Search Google Scholar
    • Export Citation
  • 13.

    Oliveira RP, Galvao MA, Mafra CL, Chamone CB, Calic SB, Silva SU, Walker DH, 2002. Rickettsia felis in Ctenocephalides spp. fleas, Brazil. Emerg Infect Dis 8: 317319.

    • Search Google Scholar
    • Export Citation
  • 14.

    Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TT, 2007. Rickettsia infection in five areas of the State of São Paulo, Brazil. Mem Inst Oswaldo Cruz 102: 793801.

    • Search Google Scholar
    • Export Citation
  • 15.

    Gehrke FS, Gazeta GS, Souza ER, Ribeiro A, Marrelli MT, Schumaker TT, 2009. Rickettsia rickettsii, Rickettsia felis and Rickettsia sp. TwKM03 infecting Rhipicephalus sanguineus and Ctenocephalides felis collected from dogs in a Brazilian spotted fever focus in the State of Rio De Janeiro/Brazil. Clin Microbiol Infect S2: 267268.

    • Search Google Scholar
    • Export Citation
  • 16.

    Raoult D, La Scola B, Enea M, Fournier PE, Roux V, Fenollar F, Galvao MA, Lamballerie X, 2001. A flea-associated Rickettsia pathogenic for humans. Emerg Infect Dis 7: 7381.

    • Search Google Scholar
    • Export Citation
  • 17.

    Maina AN, Knobel DL, Jiang J, Halliday J, Feikin DR, Cleaveland S, Nganga Z, Junghae M, Breiman RF, Richards AL, Njenga MK, 2012. Infection in febrile patients, western Kenya, 2007–2010. Emerg Infect Dis 18: 328331.

    • Search Google Scholar
    • Export Citation
  • 18.

    Nilsson K, Wallménius K, Hartwig S, Norlander T, Pahlson C, 2013. Bell's palsy and sudden deafness associated with Rickettsia spp. Infection in Sweden. A retrospective and prospective serological survey including PCR findings. Eur J Neurol 21: 206214.

    • Search Google Scholar
    • Export Citation
  • 19.

    Linardi PM, Guimarães LR, 2000. Sifonápteros do Brasil. São Paulo: Museu de Zoologia USP/FAPESP.

  • 20.

    Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, Popov V, Gennari SM, Walker DH, 2004. Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of Sao Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol 42: 9098.

    • Search Google Scholar
    • Export Citation
  • 21.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, 1990. Basic local alignment search tool. J Mol Biol 215: 403410.

  • 22.

    Junk WJ, Cunha CN, Wantzen KM, Petermann P, Strussmann C, Marques MI, Adis J, 2006. Biodiversity and its conservation in the Pantanal of Mato Grosso, Brazil. Aquat Sci 68: 278309.

    • Search Google Scholar
    • Export Citation
  • 23.

    Mendonça F, Danni-Oliveira IM, 2007. Climatologia: noções básicas e climas do Brasil. São Paulo: Oficina de Textos.

  • 24.

    Parola P, 2011. Rickettsia felis: from a rare disease in the USA to a common cause of fever in sub-Saharan Africa. Clin Microbiol Infect 17: 9961000.

    • Search Google Scholar
    • Export Citation
  • 25.

    Mediannikov O, Abdissa A, Diatta G, Trape J-F, Raoult D, 2012. Rickettsia felis in fleas, southern Ethiopia. Emerg Infect Dis 18: 13851386.

  • 26.

    Katz G, Camargo Neves VL, Angerami RN, Nascimento EM, Colombo S, 2009. Situação epidemiológica e importância da febre maculosa brasileira no Estado de São Paulo. Boletim Epidemiológico Paulista 6: 413.

    • Search Google Scholar
    • Export Citation
  • 27.

    Del Fiol FS, Junqueira FM, Rocha MC, Toledo MI, Filho SB, 2010. Rocky Mountain spotted fever in Brazil. Rev Panam Salud Publica 27: 461466.

  • 28.

    Horta MC, Scott FB, Correia TR, Fernandes JI, Richtzenhain LJ, Labruna MB, 2010. Rickettsia felis infection in cat fleas Ctenocephalides felis felis. Braz J Microbiol 41: 813818.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Mauricio C. Horta, Colegiado de Medicina Veterinária, Universidade Federal do Vale do São Francisco, Rodovia BR 407, Km 12, Lote 543, Petrolina, Pernambuco, Brazil 56304-410. E-mail: maurivet@hotmail.com

Financial support: This work was supported by Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP); Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE); and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Authors' addresses: Mauricio C. Horta and Milka C. Azevedo, Colegiado de Medicina Veterinária, Universidade Federal do Vale do São Francisco, Petrolina, PE, Brazil, E-mails: maurivet@hotmail.com and milkaazevedo@yahoo.com.br. Maria Ogrzewalska, Francisco B. Costa, Fernando Ferreira, and Marcelo B. Labruna, Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, SP, Brazil, E-mails: mogrzewalska@gmail.com, franc.borges@yahoo.com.br, fernando@vps.fmvz.usp.br, and labruna@usp.br.

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