Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-26T13:04:03.811Z Has data issue: false hasContentIssue false
  • English
  • Français

Epidemiology of Brazilian spotted fever in the Atlantic Forest, state of São Paulo, Brazil

Published online by Cambridge University Press:  01 May 2012

MARIA OGRZEWALSKA ,
DANILO G. SARAIVA ,
JONAS MORAES-FILHO ,
THIAGO F. MARTINS ,
FRANCISCO B. COSTA ,
ADRIANO PINTER  and
MARCELO B. LABRUNA
MARIA OGRZEWALSKA*
Affiliation:
Departamento de Medicina Veterinaria Preventiva e Saude Animal, Faculdade de Medicina Veterinaria e Zootenia, Universidade de Sao Paulo, Sao Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87 São Paulo, SP, Brazil, 05508-270
DANILO G. SARAIVA
Affiliation:
Departamento de Medicina Veterinaria Preventiva e Saude Animal, Faculdade de Medicina Veterinaria e Zootenia, Universidade de Sao Paulo, Sao Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87 São Paulo, SP, Brazil, 05508-270
JONAS MORAES-FILHO
Affiliation:
Departamento de Medicina Veterinaria Preventiva e Saude Animal, Faculdade de Medicina Veterinaria e Zootenia, Universidade de Sao Paulo, Sao Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87 São Paulo, SP, Brazil, 05508-270
THIAGO F. MARTINS
Affiliation:
Departamento de Medicina Veterinaria Preventiva e Saude Animal, Faculdade de Medicina Veterinaria e Zootenia, Universidade de Sao Paulo, Sao Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87 São Paulo, SP, Brazil, 05508-270
FRANCISCO B. COSTA
Affiliation:
Departamento de Medicina Veterinaria Preventiva e Saude Animal, Faculdade de Medicina Veterinaria e Zootenia, Universidade de Sao Paulo, Sao Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87 São Paulo, SP, Brazil, 05508-270
ADRIANO PINTER
Affiliation:
Superintendência de Controle de Endemias (Sucen), São Paulo, Brazil
MARCELO B. LABRUNA
Affiliation:
Departamento de Medicina Veterinaria Preventiva e Saude Animal, Faculdade de Medicina Veterinaria e Zootenia, Universidade de Sao Paulo, Sao Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87 São Paulo, SP, Brazil, 05508-270
*
*Corresponding author: Departamento de Medicina Veterinaria Preventiva e Saude Animal, Faculdade de Medicina Veterinaria e Zootenia, Universidade de Sao Paulo, Sao Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87 São Paulo, SP, Brazil, 05508-270. Tel: +55 11 3091 1394. Fax: +55 11 3091 7928. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The tick-borne bacterium Rickettsia rickettsii is the aetiological agent of Brazilian spotted fever (BSF). The present study evaluated tick infestations on wild and domestic animals, and the rickettsial infection in these animals and their ticks in 7 forest areas adjacent to human communities in the São Paulo Metropolitan Area (SPMA). The results were compared to ecological traits of each sampled area. Two main tick species, Amblyomma aureolatum and Rhipicephalus sanguineus, were collected from dogs. The major ticks found on small mammals and birds were Ixodes loricatus and Amblyomma longirostre, respectively. Both anti-R. rickettsii antibodies and R. rickettsii-infected ticks were detected on dogs from only 2 areas in the southern part of the SPMA, which were considered to be endemic for BSF; the remaining 5 areas were considered to be non-endemic. Ecologically, the BSF-endemic areas clearly differed from the non-endemic areas by the presence of significantly more degraded forest patches in the former. The present results corroborate historical observations that have indicated that all human cases of BSF in the SPMA were contracted in the southern part of this metropolitan area. However, not all forest patches in the southern part of the SPMA were shown to be associated with BSF endemism.

Keywords

Rickettsia rickettsiiticksAmblyomma aureolatumspotted feverAtlantic Forest
Type
Research Article
Information
Parasitology , Volume 139 , Issue 10 , September 2012 , pp. 1283 - 1300
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Aragão, H. B. (1936). Ixodidas brasileiros e de alguns paizes limitrophes. Memórias do Instituto Oswaldo Cruz 31, 759–843. doi: 10.1590/S0074-02761936000400004.CrossRefGoogle Scholar
Arzua, M., Onofrio, V. C. and Barros-Battesti, D. M. (2005). Catalogue of the tick collection (Acari, Ixodida) of the Museu de História Natural Capão da Imbuia, Curitiba, Paraná, Brazil. Revista Brasileira de Zoologia 22, 623–632. doi: 10.1590/S0101-81752005000300015.CrossRefGoogle Scholar
Barros-Battesti, D. M., Arzua, M. and Bechara, G. H. (2006). Carrapatos de importância médico-veterinária da Região Neotropical: Um guia ilustrado para identificação de espécies. São Paulo, Vox/ICTTD-3/Butantan.Google Scholar
Bonvicino, C. R., Oliveira, J. A. and D'andrea, P. S. (2008). Guia de Roedores do Brasil, com chaves para gêneros baseados em caracteres externos. Rio de Janeiro: Centro Pan-Americano de Febre Aftosa – OPAS/OMS.Google Scholar
Burgdorfer, W. (1988). Ecological and epidemiological considerations of Rocky Mountain spotted fever and scrub typhus. In Biology of Rickettsial Diseases (ed. Walker, D. H.), pp. 33–50. CRC Inc., Boca Raton, FL, USA.Google Scholar
Burgdorfer, W. and Brinton, L. P. (1975). Mechanisms of transovarial infection spotted fever rickettsiase in ticks. Annals of the New York Academy of Sciences 266, 61–72.CrossRefGoogle ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostaka, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Dantas-Torres, F., Aléssio, F. M., Siqueira, D. B., Mauffrey, J. F., Marvulo, M. F., Martins, T. F., Moraes-Filho, J., Camargo, M. C., D'Auria, S. R., Labruna, M. B., and Silva, J. C. (2012). Exposure of small mammals to ticks and rickettsiae in Atlantic Forest patches in the metropolitan area of Recife, North-eastern Brazil. Parasitology 139, 83–91.CrossRefGoogle ScholarPubMed
Fonseca, F. (1935). Validade da especie e cyclo evolutivo de Amblyomma striatum Koch, 1844 (Acarina, Ixodidae). Memórias do Instituto Butantan 9, 43–58.Google Scholar
Gomes, L. S. (1933). Typho exanthematico de Sao Paulo. Brasil-Medico 17, 919–921.Google Scholar
Guglielmone, A. A., Beati, L., Barros-Battesti, D. M. M., Labruna, M. B., Nava, S., Venzal, M., Mangold, A. J., Szabo, M. P. J., Martins, J. R., Gonzalez-Acuna, D. and Estrada-Pena., (2006). Ticks (Ixodidae) on humans in South America. Experimental and Applied Acarology 40, 83–100. doi: 10.1007/s10493-006-9027-0.CrossRefGoogle ScholarPubMed
Guglielmone, A. A., Estrada-Peña, A., Keirans, J. E. and Robbins, R. G. (2003 a). Ticks (Acari: Ixodida) of the Neotropical Zoogeographic Region. International Consortium on Ticks and Tick-borne Diseases (ICTTD-2), Atlanta, Houten, The Netherlands.Google Scholar
Guglielmone, A. A., Estrada-Peña, A., Mangold, A. J., Barros-Battesti, D. M., Labruna, M. B., Martins, J. R., Venzal, J. M., Arzua, M. and Keirans, J. E. (2003 b). Amblyomma aureolatum (Pallas, 1772) and Amblyomma ovale Kock, 1844: hosts, distribution and 16S rDNA sequences. Veterinary Parasitology 113, 273–288. doi:10.1016/S0304-4017(03)00083-9.CrossRefGoogle Scholar
Guglielmone, A. A. and Nava, S. (2010). Rodents of the subfamily caviinae (hystricognathi, caviidae) as hosts for hard Ticks (acari: ixodidae). Mastozoología Neotropical 17, 279–286.Google Scholar
Horta, M. C., Labruna, M. B., Durigon, E. L., and Schumaker, T. T. S. (2006). Isolation of Rickettsia felis in the mosquito cell line C6/36. Applied and Environmental Microbiology 72, 1705–1707. doi: 10.1128/AEM.72.2.1705-1707.2006.CrossRefGoogle ScholarPubMed
Horta, M. C., Labruna, M. B., Pinter, A., Linardi, P. M., and Schumaker, T. T. S. (2007). Rickettsia infection in five areas of the state of São Paulo, Brazil. Memórias do Instituto Oswaldo Cruz 102, 793–801. doi: 10.1590/S0074-02762007000700003.CrossRefGoogle ScholarPubMed
Horta, M. C., Labruna, M. B., Sangioni, L. A., Vianna, M. C., Gennari, S. M., Galvão, M. A. M., Mafra, C. L., Vidotto, O., Schumaker, T. T. S. and Walker, D. (2004). Prevalence of antibodies to spotted fever group Rickettsiae in humans and domestic animals in a Brazilian spotted fever endemic area in the state of São Paulo, Brazil: serological evidence for infection by Rickettsia rickettsii and another spotted fever group Rickettsia . American Society of Tropical Medicine and Hygiene 71, 93–97.CrossRefGoogle Scholar
Katz, G., Neves, V. L. F. C., Angerami, R. N., Nascimento, E. M. M. and Colombo, S. (2009). Situação epidemiológica e importância da febre maculosa no Estado de São Paulo. Boletim Epidemiológico Paulista 6, 4–13.Google Scholar
Krebs, C. (1989). Ecological Methodology . HarperCollins, New York.Google Scholar
Labruna, M. B. (2009). Ecology of rickettsia in South America. Annals of the New York Academy of Sciences 1166, 156–66. doi:10.1111/j.1749-6632.2009.04516.x.CrossRefGoogle ScholarPubMed
Labruna, M. B., Ogrzewalska, M., Martins, T. F., Pinter, A., and Horta, M. C. (2008). Comparative susceptibility of larval stages of Amblyomma aureolatum, Amblyomma cajennense, and Rhipicephalus sanguineus to infection by Rickettsia rickettsii . Journal of Medical Entomology 45, 1156–1159. doi: 10.1603/0022-2585(2008)45[1156:CSOLSO]2.0.CO;2.CrossRefGoogle ScholarPubMed
Labruna, M. B., Ogrzewalska, M., Soares, J. F., Martins, T. F., Soares, H. S., Moraes-Filho, J., Nieri-Bastos, F. A., Almeida, A. P. and Pinter, A. (2011). Experimental infection of Amblyomma aureolatum ticks with Rickettsia rickettsii . Emerging Infectious Diseases 17, 829–834. doi: 10.3201/eid1705.101524.CrossRefGoogle ScholarPubMed
Labruna, M. B., Sanfilippo, L. F., Demetrio, C., Menezes, A. C., Pinter, A., Guglielmone, A. A. and Silveira, L. F. (2007 b). Ticks collected form birds in the state of São Paulo, Brazil. Experimental and Applied Acarology 43, 147–160. doi: 10.1007/s10493-007-9106-x.CrossRefGoogle Scholar
Labruna, M. B., Pacheco, R. C., Leonardo, J. Richtzenhain, and Szabó, M. P. J. (2007 a). Isolation of Rickettsia rhipicephali and Rickettsia belli from Haemaphysalis juxtakochi ticks in the State of São Paulo, Brazil. Applied Environmental Microbiology, 73, 869–873. doi: 10.1128/AEM.02249-06.CrossRefGoogle Scholar
Labruna, M. B., Whitworth, T., Bouyer, D. H., McBride, J., Camargo, L. M. A., Camargo, E. P., Popov, V. and Walker, D. H. (2004 b). Rickettsia bellii and Rickettsia amblyommii in Amblyomma ticks from the State of Rondônia, Western Amazon. Journal of Medical Entomology 41, 1073–1081. doi: 10.1603/0022-2585-41.6.1073.CrossRefGoogle ScholarPubMed
Labruna, M. B., Whitworth, T., Horta, M. C., Bouyer, D. H., McBride, J. W., Pinter, A., Popov, V., Gennari, S. M. and Walker, D. H. (2004 a). Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of Sao Paulo, Brazil, where Brazilian spotted fever is endemic. Journal of Clinical Microbiology 42, 90–98. doi: 10.1128/JCM.42.1.90-98.2004.CrossRefGoogle Scholar
Lundgren, D. L., Thorpe, B. D. and Haskell, C. D. (1966). Infectious diseases in wild animals in Utah. VI. Experimental infection of birds with Rickettsia rickettsii . Journal of Bacteriology 91, 963–966.CrossRefGoogle ScholarPubMed
Mangold, A. J., Bargues, M. D. and Mas-Coma, S. (1998). Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitology Research 84, 478–484. doi: 10.1007/s004360050433.CrossRefGoogle ScholarPubMed
Marques, S., Barros-Battesti, D. M., Onofrio, V. C., Famadas, K. M., Faccini, J. L. and Keirans, J. E. (2004). Redescription of larva, nymph and adults of Ixodes (I.) loricatus Neumann, 1899 (Acari: Ixodidae) based on light and scanning electron microscopy. Systematic Parasitology 59, 135–146. doi: 10.1023/B:SYPA.0000044430.05551.44 CrossRefGoogle Scholar
Martins, T. F., Onofrio, V. C., Barros-Battesti, D. M. and Labruna, M. B. (2010). Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks and Tick-borne Diseases 1, 75–99. doi:10.1016/j.ttbdis.2010.03.002.CrossRefGoogle ScholarPubMed
Moraes-Filho, J., Pinter, A., Pacheco, R. C., Gutmann, T. B., Barbosa, S. O., Gonzáles, M. A., Muraro, M. A., Cecílio, S. R. and Labruna, M. B. (2009). New epidemiological data on Brazilian spotted Fever in an endemic area of the state of São Paulo, Brazil. Vector Borne and Zoonotic Diseases 9, 73–78. doi:10.1089/vbz.2007.0227.CrossRefGoogle Scholar
Nava, S., Velazco, P. M., and Guglielmone, A. A. (2010). The first record of Amblyomma longirostre (Koch, 1844) (Acari: Ixodidae) from Peru, with a revision of its host range. Systematic and Applied Acarology 15, 21–30.CrossRefGoogle Scholar
Niebylski, M. L., Peacock, M. G. and Schwan, T. G. (1999). Lethal effect of Rickettsia rickettsii on its tick vector (Dermacentor andersoni). Applied and Environmental Microbiology 65, 773–778.CrossRefGoogle ScholarPubMed
Ogrzewalska, M., Pacheco, R., Uezu, A., Ferreira, F. and Labruna, M. B. (2008). Ticks (Acari: Ixodidae) infesting wild birds in an Atlantic Forest area in the state of São Paulo, Brazil, with isolation of Rickettsia from the tick Amblyomma longirostre . Journal of Medical Entomology 45, 770–774. doi: 10.1603/0022-2585(2008)45[770:TAIIWB]2.0.CO;2.CrossRefGoogle Scholar
Ogrzewalska, M., Pacheco, R., Uezu, A., Richtzenhain, L. J., Ferreira, F. and Labruna, M. B. (2009). Ticks (Acari: Ixodidae) infesting birds in an Atlantic Rain Forest region of Brazil. Journal of Medical Entomology 46, 1225–1229. doi: 10.1603/033.046.0534.CrossRefGoogle Scholar
Ogrzewalska, M., Uezu, A. and Labruna, M. B. (2010). Ticks (Acari: Ixodidae) infesting wild birds in the Atlantic Forest in northeastern Brazil, with notes on rickettsial infection in ticks. Parasitology Research 108, 665–670. doi: 10.1007/s00436-010-2111-8.CrossRefGoogle ScholarPubMed
Pacheco, R. C., Arzua, M., Nieri-Bastos, F., Moraes-Filho, J., Marcili, A., Richtzenhain, L., Barros-Battesti, D. and Labruna, M. B. (2012). Rickettsial infection in ticks (Acari: Ixodidae) collected on birds in southern Brazil. Journal of Medical Entomology (in the Press).CrossRefGoogle ScholarPubMed
Pacheco, R. C., Moraes-Filho, J., Guedes, E., Silveira, I. and Richtzenhain, L. J., Leite, R. C. and Labruna, M. B. (2011). Rickettsial infections of dogs, horses and ticks in Juiz de Fora, southeastern Brazil, and isolation of Rickettsia rickettsii from Rhipicephalus sanguineus ticks. Medical and Veterinary Entomology 25, 148–155. doi:10.1111/j.1365-2915.2010.00915.x.CrossRefGoogle ScholarPubMed
Parker, R. R., Philip, C. B. and Jellison, W. L. (1933). Potentialities of tick transmission in relation to geographical occurrence in the United States. American Journal of Tropical Medicine and Hygiene 13, 341–379.CrossRefGoogle Scholar
Parker, T. A., Stotz, D. F. and Fitzpatrick, J. W. (1996). Ecological and distributional databases. In Neotropical Birds: Ecology and Conservation (ed. Stotz, D. F., Fitzpatrick, J. W., Parker, T. A. and Moskovits, D. K.), pp. 113–436. The University of Chicago Press, Chicago, IL, USA.Google Scholar
Pinter, A., Dias, R. A., Gennari, S. M. and Labruna, M. B. (2004). Study of the seasonal dynamics, life cycle, and host specificity of Amblyomma aureolatum (Acari: Ixodidae). Journal of Medical Entomology 41, 324–332. doi: 10.1603/0022-2585-41.3.324.CrossRefGoogle ScholarPubMed
Pinter, A. and Labruna, M. B. (2006). Isolation of Rickettsia rickettsii and Rickettsia bellii in cell culture from the tick Amblyomma aureolatum in Brazil. Annals of the New York Academy of Sciences 1078, 523–529. doi: 10.1196/annals.1374.103.CrossRefGoogle ScholarPubMed
Pinter, A., Pacheco, R. C., Horta, M. C., Moraes-Filho, J. and Labruna, M. B. (2008). Sero evaluation on dogs and humans from a spotted fever endemic area in the state of Sao Paulo, Brazil. Cadernos de Saúde Pública 24, 247–252.CrossRefGoogle Scholar
Piranda, E. M., Faccini, J. L., Pinter, A., Pacheco, R. C., Cançado, P. H. and Labruna, M. B. (2011). Experimental infection of Rhipicephalus sanguineus ticks with the bacterium Rickettsia rickettsii, using experimentally infected dogs. Vector Borne and Zoonotic Diseases 11, 29–36. doi: 10.1089/vbz.2009.0250.CrossRefGoogle ScholarPubMed
Regnery, R. L., Spruill, C. L. and Plikaytis, B. D. (1991). Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. Journal of Bacteriology 173, 1576–1589.CrossRefGoogle ScholarPubMed
Reiczigel, J. and Rózsa, L. (2005). Quantitative Parasitology 3.0, Budapest, Hungary.Google Scholar
Reiczigel, J., Zakarias, I. and Rózsa, L. (2005). A bootstrap test of stochastic equality of two populations. The American Statistician 59, 1–6. doi: 10.1198/000313005X23526.CrossRefGoogle Scholar
Reis, N. R., Peracchi, A. L., Pedro, W. A. and Lima, I. P. (2006). Mamíferos do Brasil. Imprensa da UEL, Londrina, Brazil.Google Scholar
Sabatini, G. A., Pinter, A., Nieri-Bastos, F. A., Marcili, A., and Labruna, M. B. (2010). Survey of ticks (Acari: Ixodidae) and their Rickettsia in an Atlantic Rain Forest Reserve in the State of Sao Paulo, Brazil. Journal of Medical Entomology 47, 913–916. doi: 10.1603/ME10073.CrossRefGoogle Scholar
Sangioni, L. A., Horta, M. C., Vianna, M. C. B., Gennari, S. M., Soares, R. S., Galvão, M. A. M., Schumaker, T. T. S., Ferreira, F., Vidotto, O. and Labruna, M. B. (2005). Rickettsial infection in animals and Brazilian spotted fever endemicity. Emerging Infectious Diseases 11, 265–270. doi: 10.3201/eid1102.040656.CrossRefGoogle ScholarPubMed
Sigrist, T. (2007). Aves do Brasil Oriental - Birds of Eastern Brazil. Avis Brasilis, São Paulo, Brazil.Google Scholar
Silveira, I., Pacheco, R. C., Szabó, M. P. J., Ramos, H. G. C. and Labruna, M. B. (2007). Rickettsia parkeri in Brazil. Emerging Infectious Diseases 13, 1111–1113. doi: 10.3201/eid1307.061397.CrossRefGoogle ScholarPubMed
Souza, C. E., Moraes-Filho, J., Ogrzewalska, M., Uchoa, F. V., Horta, M. C., Souza, S. S. L., Borba, R. C. M. and Labruna, M. B. (2009). Experimental infection of capybaras Hydrochoerus hydrochaeris by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense . Veterinary Parasitology 161, 116–121. doi:10.1016/j.vetpar.2008.12.010.CrossRefGoogle ScholarPubMed
Uezu, A., Metzger, J. and Vielliard, J. (2005). Effects of structural and functional connectivity and patch size on the abundance of seven Atlantic Forest bird species. Biological Conservation 123, 507–519. doi. 10.1016/j.biocon.2005.01.001.CrossRefGoogle Scholar
Wilson, D. E. and Reeder, D. M. (2005). Mammal Species of the World. Johns Hopkins University Press, Baltimore, MD, USA.CrossRefGoogle Scholar
Woods, C. A. and Kilpatrick, C. W. (2005). Infraorder Hystricognathi. In Mammal Species of the World: A Taxonomic and Geographic Reference. 3rd Edn (ed. Wilson, D. E. and Reeder, D. M.), pp. 1538–1600. Johns Hopkins University Press, Baltimore, MD, USA.Google Scholar
Zar, J. H. (1996). Biostatistical Analysis. Prentice Hall, Upper Saddle River, New Jersey, USA.Google Scholar