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In vitro isolation from Amblyomma ovale (Acari: Ixodidae) and ecological aspects of the Atlantic rainforest Rickettsia, the causative agent of a novel spotted fever rickettsiosis in Brazil

Published online by Cambridge University Press:  30 January 2013

M. P. J. SZABÓ ,
F. A. NIERI-BASTOS ,
M. G. SPOLIDORIO ,
T. F. MARTINS ,
A. M. BARBIERI  and
M. B. LABRUNA
M. P. J. SZABÓ*
Affiliation:
Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Orlando Marques de Paiva, 87 Cidade Universitária, CEP: 05508-270, São Paulo, SP Brasil Faculdade de Medicina Veterinária e Zootecnia, Universidade Federal de Uberlândia Av. Pará, 1720/Campus Umuarama-Bloco 2T, Uberlândia, Minas Gerais, Brasil
F. A. NIERI-BASTOS
Affiliation:
Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Orlando Marques de Paiva, 87 Cidade Universitária, CEP: 05508-270, São Paulo, SP Brasil
M. G. SPOLIDORIO
Affiliation:
Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Orlando Marques de Paiva, 87 Cidade Universitária, CEP: 05508-270, São Paulo, SP Brasil
T. F. MARTINS
Affiliation:
Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Orlando Marques de Paiva, 87 Cidade Universitária, CEP: 05508-270, São Paulo, SP Brasil
A. M. BARBIERI
Affiliation:
Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Orlando Marques de Paiva, 87 Cidade Universitária, CEP: 05508-270, São Paulo, SP Brasil
M. B. LABRUNA
Affiliation:
Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Orlando Marques de Paiva, 87 Cidade Universitária, CEP: 05508-270, São Paulo, SP Brasil
*
*Corresponding author: Faculdade de Medicina Veterinária e Zootecnia, Universidade Federal de Uberlândia Av. Pará, 1720/Campus Umuarama-Bloco 2T, Uberlândia, Minas Gerais, Brasil. Tel: +55 34 3218 2691. Fax: +55 34 3218 2521. E-mail: szabo@famev.ufu.br
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Summary

Recently, a novel human rickettsiosis, namely Atlantic rainforest spotted fever, was described in Brazil. We herein report results of a survey led around the index case in an Atlantic rainforest reserve in Peruibe municipality, southeastern Brazil. A Rickettsia parkeri-like agent (Rickettsia sp. Atlantic rainforest genotype) and Ricketsia bellii were isolated from adult Amblyomma ovale ticks collected from dogs. Molecular evidence of infection with strain Atlantic rainforest was obtained for 30 (12·9%) of 232 A. ovale adult ticks collected from dogs. As many as 88·6% of the 35 examined dogs had anti-Rickettsia antibodies, with endpoint titres at their highest to R. parkeri. High correlation among antibody titres in dogs, A. ovale infestations, and access to rainforest was observed. Amblyomma ovale subadults were found predominantly on a rodent species (Euryoryzomys russatus). From 17 E. russatus tested, 6 (35·3%) displayed anti-Rickettsia antibodies, with endpoint titres highest to R. parkeri. It is concluded that Atlantic rainforest genotype circulates in this Atlantic rainforest area at relatively high levels. Dogs get infected when bitten by A. ovale ticks in the forest, and carry infected ticks to households. The role of E. russatus as an amplifier host of Rickettsia to A. ovale ticks deserves investigation.

Keywords

Atlantic rainforest spotted feverAmblyomma ovaleBrazilisolationecology
Type
Research Article
Information
Parasitology , Volume 140 , Issue 6 , May 2013 , pp. 719 - 728
Copyright
Copyright © Cambridge University Press 2013

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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
Barros-Battesti, D. M. B., Arzua, M. and Bechara, G. H. (2006). Carrapatos de Importância Medico-Veterinária da Região Neotropical: um Guia Ilustrado para Identificação de Espécies. Vox/ICTTD-3/Butantan, São Paulo/Brasil.Google Scholar
Berrada, Z. L., Goethert, H. K., Cunningham, J. and Telford, S. R. 3rd (2011). Rickettsia rickettsii (Rickettsiales: Rickettsiaceae) in Amblyomma americanum (Acari: Ixodidae) from Kansas. Journal of Medical Entomology 48, 461–467. doi: http://dx.doi.org/10.1603/ME10130.CrossRefGoogle ScholarPubMed
Burgdorfer, W. (1970). The hemolymph test. American Journal of Tropical Medicine and Hygiene 19, 1010–1014.CrossRefGoogle ScholarPubMed
Burgdorfer, W. and Brinton, L. P. (1975). Mechanisms of transovarial infection of spotted fever rickettsiae 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
Carmichael, J. R. and Fuerst, P. A. (2010). Molecular detection of Rickettsia bellii, Rickettsia montanensis, and Rickettsia rickettsii in a Dermacentor variabilis tick from nature. Vector Borne and Zoonotic Diseases 10, 111–115. doi:10.1089/vbz.2008.0083.CrossRefGoogle Scholar
Conti-Díaz, I. A., Moraes-Filho, J., Pacheco, R. C. and Labruna, M. B. (2009). Serological evidence of Rickettsia parkeri as the etiological agent of rickettsiosis in Uruguay. Revista do Instituto de Medicina Tropical de São Paulo 51, 337–339. doi: http://dx.doi.org/10.1590/S0036-46652009000600005.CrossRefGoogle ScholarPubMed
Cragun, W. C., Bartlett, B. L., Ellis, M. W., Hoover, A. Z., Tyring, S. K., Mendoza, N., Vento, T. J., Nicholson, W. I., Eremeeva, M. E., Olano, J. P., Rapini, R. P. and Paddock, C. D. (2010). The expanding spectrum of eschar-associated Rickettsioses in the United States. Archives of Dermatology 146, 641–648. doi:10.1001/archdrmatol.2010.48).CrossRefGoogle ScholarPubMed
Gimemez, D. F. (1964). Staining rickettsiae in yolk-sac cultures. Stain Technology 39, 135–140.CrossRefGoogle Scholar
Goddard, J. (2009). Historical and recent evidence for close relationships among Rickettsia parkeri, R. conorii, R. africae, and R. sibirica: implications for rickettsial taxonomy. Journal of Vector Ecology 34, 238–242. doi:10.1111/j.1948-7134.2009.00032.x.CrossRefGoogle 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). Amblyomma aureolatum (Pallas, 1772) and Amblyomma ovale Koch, 1844 (Acari: Ixodidae): hosts, distribution and 16S rDNA sequences. Veterinary Parasitology 113, 273–288.CrossRefGoogle ScholarPubMed
Guglielmone, A. A., Szabó, M. P. J., Martins, J. R. S. and Estrada-Peña, A. (2006). Diversidade e importância de carrapatos na sanidade animal. In Carrapatos de Importância Medico-Veterinária da Região Neotropical: um Guia Ilustrado para Identificação de Espécies (ed. Barros-Battesti, D. M. B., Arzua, M. and Bechara, G. H.), pp. 115–138. Vox/ICTTD-3/Butantan, São Paulo/Brasil.Google Scholar
Hayes, S. F. and Burgdorfer, W. (1982). Reactivation of Rickettsia rickettsii in Dermacentor andersoni ticks: an ultrastructural analysis. Infection and Immunity 37, 779–785.CrossRefGoogle ScholarPubMed
Hayes, S. F., Burgdorfer, W. and Aeschlimann, A. (1980). Sexual transmission of spotted fever group rickettsiae by infected male ticks: detection of rickettsiae in immature spermatozoa of Ixodes ricinus. Infection and Immunity 27, 638–642.CrossRefGoogle ScholarPubMed
Labruna, M. B. (2009). Ecology of Rickettsia in South America. Annals of the New York Academy of Sciences 1166, 156–166. doi:10.1111/j.1749-6632.2009.04516.x.CrossRefGoogle ScholarPubMed
Labruna, M. B., Camargo, L. M. A., Terrassini, F. A., Ferreira, F., Schumaker, T. T. and Camargo, E. P. (2005). Ticks (Acari: Ixodidae) from the state of Rondônia, western Amazon, Brazil. Systematic and Applied Acarology 10, 17–32.CrossRefGoogle Scholar
Labruna, M. B., Horta, M. C., Aguiar, D. M., Cavalcante, G. T., Pinter, A., Gennari, S. M. and Camargo, L. M. A. (2007). Prevalence of Rickettsia infection in dogs from the urban and rural areas of Monte Negro Municipality, Western Amazon, Brazil. Vector Borne and Zoonotic Diseases 7, 249–256.CrossRefGoogle Scholar
Labruna, M. B., Whitworth, T., Bouyer, D. H., McBride, J. L., Camargo, M. A., Camargo, E. P., Popov, V. and Walker, D. H. (2004). Rickettsia bellii and Rickettsia amblyommii in Amblyomma ticks from the state of Rondonia, Western Amazon, Brazil. Journal of Medical Entomology 41, 1073–1081.CrossRefGoogle ScholarPubMed
Labuda, M. and Nuttall, P. A. (2004). Tick-borne viruses. Parasitology 129 (Suppl.), S221–S245.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.CrossRefGoogle Scholar
Marrero, M. D. and Raoult, D. (1989). Centrifugation-shell vial technique for rapid detection of Mediterranean spotted fever rickettsia in blood culture. American Journal of Tropical Medicine and Hygiene 40, 197–199.CrossRefGoogle ScholarPubMed
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.2010.03.0022.CrossRefGoogle ScholarPubMed
Medeiros, A. P., de Souza, A. P., de Moura, A. B., Lavina, M. S., Belatto, V., Sartor, A. A., Nieri-Bastos, F. A., Richtzenhain, L. J. and Labruna, M. B. (2011). Spotted fever group Rickettsia infecting ticks (Acari: Ixodidae) in the state of Santa Catarina, Brazil. Memórias do Instituto Oswaldo Cruz 106, 926–930. doi:10.1590/S0074-02762011000800005.CrossRefGoogle ScholarPubMed
Mertins, J. W., Moorhouse, A. S., Alfred, J. T. and Hutcheson, H. J. (2010). Amblyomma triste (Acari: Ixodidae): new North American collection records, including the first from the United States. Journal of Medical Entomology 47, 536–542. doi: http://dx.doi.org/10.1603/ME09165.CrossRefGoogle ScholarPubMed
Nava, S., Elshenawy, Y., Eremeeva, M. A., Mastropaolo, M. and Paddock, C. D. (2008). Rickettsia parkeri in Argentina. Emerging Infectious Diseases 14, 1894–1897.CrossRefGoogle ScholarPubMed
Pacheco, R. C., Arzua, M., Nieri-Bastos, F. A., Moraes-Filho, J., Marcili, A., Richtzenhain, L. J., Barros-Battesti, D. M. and Labruna, M. B. (2012). Rickettsial infection in ticks (Acari: Ixodidae) collected on birds in southern Brazil. Journal of Medical Entomology 49, 710–716. doi: http://dx.doi.org/10.1603/ME11217.CrossRefGoogle ScholarPubMed
Pacheco, R. C., Moraes-Filho, J., Marcili, A., Richtzenhain, L. J., Szabó, M. P., Catroxo, M. H., Bouyer, D. H. and Labruna, M. B. (2011). Rickettsia monteiroi sp. nov., infecting the tick Amblyomma incisum in Brazil. Applied and Environmental Microbiology 77, 5207–5211. doi:10.1128/AEM.05166-11.CrossRefGoogle ScholarPubMed
Paddock, C. D., Sumner, J. W., Comer, J. A., Zaki, S. R., Goldsmith, C. S., Goddard, J., McLellan, S. L. F., Tamminga, C. L. and Ohl, C. A. (2004). Rickettsia parkeri: a newly recognized cause of spotted fever rickettsiosis in the United States. Clinical and Infectious Diseases 38, 812–813.CrossRefGoogle ScholarPubMed
Parker, R. R., Kohls, G. M., Cox, G. W. and Davis, G. E. (1939). Observations on an infectious agent from Amblyomma maculatum. Public Health Reports 54, 1482–1484.CrossRefGoogle Scholar
Philip, C. B. (1959). Some epidemiological considerations in Rocky Mountain spotted fever. Public Health Reports 74, 595–600.CrossRefGoogle ScholarPubMed
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
Romer, Y., Seijo, A., Crudo, F., Nicholson, W. L., Varela-Stokes, A., Lash, R. R. and Paddock, C. (2011). Rickettsia parkeri rickettsiosis, Argentina. Emerging Infectious Diseases 17, 1169–1173. doi:10.3201/eid1707.101857.CrossRefGoogle ScholarPubMed
Roux, V., Fournier, P. E. and Raoult, D. (1996). Differentiation of spotted fever group rickettsiae by sequencing and analysis of restriction fragment length polymorphism of PCR-amplifed DNA of the gene encoding the protein rOmpA. Journal of Clinical Microbiology 34, 2058–2065.CrossRefGoogle Scholar
Roux, V. and Raoult, D. (2000). Phylogenetic analysis of members of the genus Rickettsia using the gene encoding the outer membrane protein rOmpB (ompB). International Journal of Systematic and Evolutionary Microbiology 50, 1449–1455.CrossRefGoogle ScholarPubMed
Sabatini, G. S., Pinter, A., Nieri-Bastos, F., Marcili, A. and Labruna, M. B. (2010). Survey of ticks (Acari: Ixodidae) and their Rickettsia in an Atlantic rainforest reserve in the State of São Paulo, Brazil. Journal of Medical Entomology 47, 913–916. doi: http://dx.doi.org/10.1603/ME10073.CrossRefGoogle Scholar
Sangioni, L. A., Horta, M. C., Vianna, M. C. B., Gennari, S. M., Soares, R. M., 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.CrossRefGoogle ScholarPubMed
Silva, N., Eremeeva, M. E., Rozental, T., Ribeiro, G. S., Paddock, C. D., Ramos, E. A. G., Favacho, A. R. M., Reis, M. G., Dasch, G. A., de Lemos, E. R. S. and Ko, A. I. (2011). Eschar-associated spotted fever Rickettsiosis, Bahia, Brazil. Emerging Infectious Diseases 17, 275–278. doi:10.3201/eid1702.100859.CrossRefGoogle ScholarPubMed
Silveira, I., Pacheco, R. P., Szabó, M. P. J., Ramos, H. G. C. and Labruna, M. B. (2007). Rickettsia parkeri in Brazil. Emerging Infectious Diseases 13, 1111–1113.CrossRefGoogle ScholarPubMed
Spolidorio, M. G., Labruna, M. B., Mantovani, E., Brandão, P., Richtzenhain, L. J. and Yoshinari, N. H. (2010). Novel spotted fever group rickettsioses, Brazil. Emerging Infectious Diseases 16, 521–523. doi:10.3201/eid1603.091338.CrossRefGoogle ScholarPubMed
Szabó, M. P. J., Olegário, M. M. M. and Santos, A. L. Q. (2007). Tick fauna from two locations in the Brazilian savannah. Experimental and Applied Acarology 43, 73–84.CrossRefGoogle ScholarPubMed
Terassini, F. A., Barbieri, F. S., Albuquerque, S., Szabó, M. P. J., Camargo, L. M. A. and Labruna, M. B. (2010). Comparison of two methods for collecting free-living ticks in the Amazonian forest. Ticks and Tick-borne Diseases 1, 194–196. doi:10.1016/j.ttbdis.2010.08.002.CrossRefGoogle ScholarPubMed
Varela-Stokes, A., Paddock, C. D. and Engber, B. M. T. (2011). Rickettsia parkeri in Amblyomma maculatum ticks, North Carolina, USA, 2009–2010. Emerging Infectious Diseases 17, 2350–2353. doi: http://dx.doi.org/10.3201/eid1712.110789.CrossRefGoogle ScholarPubMed
Venzal, J. M., Portillo, A., Estrada Peña, A., Castro, O., Cabrera, P. A. and Oteo, J. A. (2004). Rickettsia parkeri in Amblyomma triste from Uruguay. Emerging Infectious Diseases 10, 1493–1495.CrossRefGoogle ScholarPubMed
Walker, D. H. and Ismail, N. (2008). Emerging and re-emerging rickettsioses: endothelial cell infection and early disease events. Nature Review Microbiology 6, 375–386.CrossRefGoogle ScholarPubMed
Wikswo, M. E., Hu, R., Dasch, G. A., Krueger, L., Arugay, A., Jones, K., Hess, B., Bennett, S., Kramer, V. and Eremeeva, M. E. (2008). Detection and identification of spotted fever group rickettsiae in Dermacentor species from southern California. Journal of Medical Entomology 45, 509–516.CrossRefGoogle ScholarPubMed
Zemtsova, G., Killmaster, L. F., Mumcuoglu, K. Y. and Levin, M. L. (2010). Co-feeding as a route for transmission of Rickettsia conorii israelensis between Rhipicephalus sanguineus ticks. Experimental and Applied Acarology 52, 383–392. doi:10.1007/s1049301093757.CrossRefGoogle ScholarPubMed