Investigation of tick-borne bacteria (Rickettsia spp., Anaplasma spp., Ehrlichia spp. and Borrelia spp.) in ticks collected from Andean tapirs, cattle and vegetation from a protected area in Ecuador

Particle and Fibre Toxicology

José A Oteo¹  Ana M Palomar¹  Aránzazu Portillo¹  Cristina Pesquera¹ 

[1] Departamento de Enfermedades Infecciosas, Hospital San Pedro- Centro de Investigación Biomédica de La Rioja (CIBIR), C/ Piqueras 98, 26006 - Logroño, La Rioja, Spain

关键词: Ecuador;    Borrelia;    Ehrlichia;    Anaplasma;    Rickettsia;    Ixodes sp.;    Ixodes boliviensis;    Ixodes lasallei;    Rhipicephalus microplus;    Amblyomma sp.;    Amblyomma scalpturatum;    Amblyomma multipunctum;    Ticks;   

Others  :  1147466
DOI  :  10.1186/s13071-015-0662-3

 received in 2014-07-12, accepted in 2015-01-15,  发布年份 2015

【 摘 要 】

Background

Ixodid ticks play an important role in the transmission and ecology of infectious diseases. Information about the circulation of tick-borne bacteria in ticks is lacking in Ecuador. Our aims were to investigate the tick species that parasitize Andean tapirs and cattle, and those present in the vegetation from the buffer zone of the Antisana Ecological Reserve and Cayambe-Coca National Park (Ecuador), and to investigate the presence of tick-borne bacteria.

Methods

Tick species were identified based on morphologic and genetic criteria. Detection of tick-borne bacteria belonging to Rickettsia, Anaplasma, Ehrlichia and Borrelia genera was performed by PCRs.

Results

Our ticks included 91 Amblyomma multipunctum, 4 Amblyomma spp., 60 Rhipicephalus microplus, 5 Ixodes spp. and 1 Ixodes boliviensis. A potential Candidatus Rickettsia species closest to Rickettsia monacensis and Rickettsia tamurae (designated Rickettsia sp. 12G1) was detected in 3 R. microplus (3/57, 5.3%). In addition, Anaplasma spp., assigned at least to Anaplasma phagocytophilum (or closely related genotypes) and Anaplasma marginale, were found in 2 A. multipunctum (2/87, 2.3%) and 13 R. microplus (13/57, 22.8%).

Conclusions

This is the first description of Rickettsia sp. in ticks from Ecuador, and the analyses of sequences suggest the presence of a potential novel Rickettsia species. Ecuadorian ticks from Andear tapirs, cattle and vegetation belonging to Amblyomma and Rhipicephalus genera were infected with Anaplasmataceae. Ehrlichia spp. and Borrelia burgdorferi sensu lato were not found in any ticks.

【 授权许可】

   
2015 Pesquera et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Sonenshine DE, Lane RS, Nicholson WL. Ticks (Ixodida). In: Medical and Veterinary Entomology. Mullen G, Durden L, editors. Academic Press, New York; 2002: p.517-58.
• [2]Guglielmone AA, Estrada-Peña A, Keirans JE, Robbins RG. Ticks (Acari: Ixodida) of the Neotropical Zoogeographic Region. Atalanta, Houten; 2003.
• [3]Barros-Battesti D, Arzua M, Bechara GH. Carrapatos de Importância Medico-Veterinaria da Região Neotropical: Um Guia Ilustrado para Identificação de Espécies. Vox/ICTTD-3/ Butantan, Sao Pablo; 2006.
• [4]Spolidorio MG, Andreoli GS, Martins TF, Brandão PE, Labruna MB. Rickettsial infection in ticks collected from road-killed wild animals in Rio de Janeiro, Brazil. J Med Entomol. 2012; 49:1510-4.
• [5]André MR, Dumler JS, Scorpio DG, Teixeira RH, Allegretti SM, Machado RZ. Molecular detection of tick-borne bacterial agents in Brazilian and exotic captive carnivores. Ticks Tick Borne Dis. 2012; 3:247-53.
• [6]Barbosa da Silva J, Vinhote WM, Oliveira CM, André MR, Machado RZ, DaFonseca AH et al.. Molecular and serological prevalence of Anaplasma marginale in water buffaloes in northern Brazil. Ticks Tick Borne Dis. 2014; 5:100-4.
• [7]Diaz AG, Castellanos A, Piñeda C, Downer C, Lizcano DJ, Constantino E, et al. Tapirus pinchaque. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.1. 2008. http://www.iucnredlist.org/details/21473/0.
• [8]Labruna MB, Whitworth T, Bouyer DH, McBride J, Camargo LM, Camargo EP et al.. Rickettsia bellii and Rickettsia amblyommii in Amblyomma ticks from the State of Rondônia, Western Amazon, Brazil. J Med Entomol. 2004; 41:1073-81.
• [9]Guglielmone AA, Beati L, Barros-Battesti DM, Labruna MB, Nava S, Venzal JM et al.. Ticks (Ixodidae) on humans in South America. Exp Appl Acarol. 2006; 40:83-100.
• [10]Szabó MP, Pinter A, Labruna MB. Ecology, biology and distribution of spotted-fever tick vectors in Brazil. Front Cell Infect Microbiol. 2013; 3:27.
• [11]Londoño AF, Díaz FJ, Valbuena G, Gazi M, Labruna MB, Hidalgo M et al.. Infection of Amblyomma ovale by Rickettsia sp. strain Atlantic rainforest, Colombia. Ticks Tick Borne Dis. 2014; 5:672-5.
• [12]Fairchild GB, Kohls GM, Tipton VJ. The ticks of Panama (Acarina: Ixodoidea). In: Ectoparasites of Panama. Wenzel WR, Tipton VJ, editors. Field Museum of Natural History, Chicago; 1966: p.167-219.
• [13]Jones EK, Clifford CM, Keirans JE, Kohls GM. The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in the western hemisphere. Brigham Young University Science Bulletin, Biological Series. 1972; 17:1-40.
• [14]Black WC, Piesman J. Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proc Natl Acad Sci U S A. 1994; 91:10034-8.
• [15]Beati L, Keirans JE. Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNA gene sequences and morphological characters. J Parasitol. 2001; 87:32-48.
• [16]Zahler M, Gothe R, Rinder H. Genetic evidence against a morphologically suggestive conspecificity of Dermacentor reticulatus and Dermacentor marginatus (Acari: Ixodidae). Int J Parasitol. 1995; 25:1413-9.
• [17]Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991; 173:697-703.
• [18]Jado I, Oteo JA, Aldámiz M, Gil H, Escudero R, Ibarra V et al.. Rickettsia monacensis and human disease, Spain. Emerg Infect Dis. 2007; 13:1405-7.
• [19]Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A et al.. Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol. 2004; 42:90-8.
• [20]Roux V, Fournier PE, Raoult D. Differentiation of spotted fever group rickettsiae by sequencing and analysis of restriction fragment length polymorphism of PCR-amplified DNA of the gene encoding the protein rOmpA. J Clin Microbiol. 1996; 34:2058-65.
• [21]Regnery RL, Spruill CL, Plikaytis BD. Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol. 1991; 173:1576-89.
• [22]Choi YJ, Lee SH, Park KH, Koh YS, Lee KH, Baik HS et al.. Evaluation of PCR-based assay for diagnosis of spotted fever group rickettsiosis in human serum samples. Clin Vaccine Immunol. 2005; 12:759-63.
• [23]Sekeyova Z, Roux V, Raoult D. Phylogeny of Rickettsia spp. inferred by comparing sequences of ‘gene D’, which encodes an intracytoplasmic protein. Int J Syst Evol Microbiol. 2001; 51:1353-60.
• [24]Márquez FJ, Muniain MA, Soriguer RC, Izquierdo G, Rodríguez-Baño J, Borobio MV. Genotypic identification of an undescribed spotted fever group rickettsia in Ixodes ricinus from southwestern Spain. Am J Trop Med Hyg. 1998; 58:570-7.
• [25]Oliveira RP, Galvão MA, Mafra CL, Chamone CB, Calic SB, Silva SU et al.. Rickettsia felis in Ctenocephalides spp. fleas, Brazil. Emerg Infect Dis. 2002; 8:317-9.
• [26]Zeidner NS, Burkot TR, Massung R, Nicholson WL, Dolan MC, Rutherford JS et al.. Transmission of the agent of human granulocytic ehrlichiosis by Ixodes spinipalpis ticks: evidence of an enzootic cycle of dual infection with Borrelia burgdorferi in Northern Colorado. J Infect Dis. 2000; 182:616-9.
• [27]Massung R, Slater K, Owens JH, Nicholson WL, Mather TN, Solberg VB et al.. Nested PCR assay for detection of granulocytic ehrlichiae. J Clin Microbiol. 1998; 36:1090-5.
• [28]Inokuma H, Raoult D, Brouqui P. Detection of Ehrlichia platys DNA in brown dog ticks (Rhipicephalus sanguineus) in Okinawa Island, Japan. J Clin Microbiol. 2000; 38:4219-21.
• [29]Eddlestone SM, Diniz PP, Neer TM, Gaunt SD, Corstvet R, Cho D et al.. Doxycycline clearance of experimentally induced chronic Ehrlichia canis infection in dogs. J Vet Intern Med. 2007; 21:1237-42.
• [30]Clark K, Hendricks A, Burge D. Molecular identification and analysis of Borrelia burgdorferi sensu lato in lizards in the southeastern United States. Appl Environ Microbiol. 2005; 71:2616-25.
• [31]Rijpkema SG, Molkenboer MJ, Schouls LM, Jongejan F, Schellekens JF. Simultaneous detection and genotyping of three genomic groups of Borrelia burgdorferi sensu lato in Dutch Ixodes ricinus ticks by characterization of the amplified intergenic spacer region between 5S and 23S rRNA genes. J Clin Microbiol. 1995; 33:3091-5.
• [32]Raoult D, Fournier PE, Eremeeva M, Graves S, Kelly PJ, Oteo JA et al.. Naming of Rickettsiae and rickettsial diseases. Ann N Y Acad Sci. 2005; 1063:1-12.
• [33]Labruna MB, Guglienmone AA. Ticks of New World Tapirs. Tapir Conservation. 2009; 18:21-8.
• [34]Vásquez CL, Muro JJ, Clavijo JJ. Garrapatas del género Ixodes Latreille, 1795 y Rhipicephalus (Boophilus) Koch, 1844 (Acari: Ixodidae) presentes en la colección de Zoología Agrícola, Decanato de Agronomía, UCLA, Lara, Venezuela. Entomotropica. 2011; 26:89-97.
• [35]Neumann LG. Révision de la famille des Ixodidés. Mémoires de la Société de Zoologie de France. 1899; 12:211-7.
• [36]Voltzit OV. A review of Neotropical Amblyomma species (Acari: Ixodidae). Acarina. 2007; 15:3-134.
• [37]Labruna MB, Martins TF, Nunes PH, Costa FB, Portero F, Venzal JM. New records of Amblyomma multipunctum and Amblyomma naponense from Ecuador, with description of A. multipunctum nymph. J Parasitol. 2013; 99:973-7.
• [38]Alvarez V, Bonilla R, Chacón I. Relative abundance of Amblyomma spp. (Acari: Ixodidae) in bovines (Bos taurus and B. indicus) from Costa Rica. Rev Biol Trop. 2003; 51:435-43.
• [39]Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T et al.. Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev. 2013; 26:657-702.
• [40]Imaoka K, Kaneko S, Tabara K, Kusatake K, Morita E. The first human case of Rickettsia tamurae infection in Japan. Case Rep Dermatol. 2011; 3:68-73.
• [41]Miranda J, Portillo A, Oteo JA, Mattar S. Rickettsia sp. strain Colombianensi (Rickettsiales: Rickettsiaceae): A New Proposed Rickettsia Detected in Amblyomma dissimile (Acari: Ixodidae) from iguanas and free-living larvae ticks from vegetation. J Med Entomol. 2012; 49:960-5.
• [42]Troyo A, Moreira-Soto A, Carranza M, Calderón-Arguedas O, Hun L, Taylor L. Detection of an undescribed Rickettsia sp. in Ixodes boliviensis from Costa Rica. Ticks Tick Borne Dis. 2014; 5:672-5.
• [43]Rymaszewska A. Variability within the msp2 gene in populations of Anaplasma phagocythopilum. Folia Biol (Praha). 2010; 56:269-75.
• [44]Barbet AF, Meeus PF, Bélanger M, Bowie MV, Yi J, Lundgren AM et al.. Expression of multiple outer membrane protein sequence variants from a single genomic locus of Anaplasma phagocytophilum. Infect Immun. 2003; 71:1706-18.
• [45]Lin M, Kikuchi T, Brewer HM, Norbeck AD, Rikihisa Y. Global proteomic analysis of two tick-borne emerging zoonotic agents: Anaplasma phagocytophilum and Ehrlichia chaffeensis. Front Microbiol. 2011; 2:24.
• [46]Wuritu, Ozawa Y, Gaowa, Kawamori F, Masuda T, Masuzawa T et al.. Structural analysis of a p44/msp2 expression site of Anaplasma phagocytophilum in naturally infected ticks in Japan. J Med Microbiol. 2009; 58:1638-44.
• [47]Clark KL. Anaplasma phagocytophilum in small mammals and ticks in northeast Florida. J Vector Ecol. 2012; 37:262-8.
• [48]Santos HA, Pires MS, Vilela JA, Santos TM, Faccini JL, Baldani CD et al.. Detection of Anaplasma phagocytophilum in Brazilian dogs by real-time polymerase chain reaction. J Vet Diagn Invest. 2011; 23:770-4.
• [49]Sacchi AB, Duarte JM, André MR, Machado RZ. Prevalence and molecular characterization of Anaplasmataceae agents in free-ranging Brazilian marsh deer (Blastocerus dichotomus). Comp Immunol Microbiol Infect Dis. 2012; 35:325-34.
• [50]André MR, Baccarim Denardi NC, de Sousa KC M, Gonçalves LR, Henrique PC, Grosse Rossi Ontivero CR et al.. Arthropod-borne pathogens circulating in free-roaming domestic cats in a zoo environment in Brazil. Ticks Tick Borne Dis 2014. 2014; 5:545-51.
• [51]Zhang L, Liu H, Xu B, Lu Q, Li L, Chang L et al.. Anaplasma phagocytophilum infection in domestic animals in ten provinces/cities of China. Am J Trop Med Hyg. 2012; 87:185-9.
• [52]Vidotto O, Barbosa CS, Andrade GM, Machado RZ, Da Rocha MA, Silva SS. Evaluation of a frozen trivalent attenuated vaccine against babesiosis and anaplasmosis in Brazil. Ann N Y Acad Sci. 1998; 849:420-3.
• [53]Kocan KM, de la Fuente J, Blouin EF, Coetzee JF, Ewing SA. The natural history of Anaplasma marginale. Vet Parasitol. 2010; 167:95-107.
• [54]Soto KK. Determinación de la prevalencia de anaplasmosis en el ganado bovino faenado en la empresa metropolitana de Rastro de Quito (EMRQ) mediante la aplicación de las técnicas de diagnóstico: microscopía de frotis sanguíneos, reacción en cadena de la polimerasa (PCR) y ensayo inmunoenzimático competitivo (cELISA) [PhD thesis]. Escuela Politécnica del Ejército, Sangolquí; 2010.
• [55]Ybañez AP, Sivakumar T, Ybañez RH, Ratilla JC, Perez ZO, Gabotero SR et al.. First molecular characterization of Anaplasma marginale in cattle and Rhipicephalus (Boophilus) microplus ticks in Cebu, Philippines. J Vet Med Sci. 2013; 75:27-36.
• [56]Cabezas-Cruz A, Vancová M, Zweygarth E, Ribeiro MF, Grubhoffer L, Passos LM. Ultrastructure of Ehrlichia mineirensis, a new member of the Ehrlichia genus. Vet Microbiol. 2013; 167:455-8.
• [57]Zweygarth E, Schöl H, Lis K, Cabezas-Cruz A, Thiel C, Silaghi C et al.. In vitro culture of a novel genotype of Ehrlichia sp. from Brazil. Transbound Emerg Dis. 2013; 60:86-92.
• [58]Barbieri AM, Venzal JM, Marcili A, Almeida AP, Gonzalez EM, Labruna MB. Borrelia burgdorferi sensu lato infecting ticks of the Ixodes ricinus complex in Uruguay: first report for the Southern Hemisphere. Vector Borne Zoonotic Dis. 2013; 13:147-53.
• [59]Ivanova LB, Tomova A, González-Acuña D, Murúa R, Moreno CX, Hernández C et al.. Borrelia chilensis, a new member of the Borrelia burgdorferi sensu lato complex that extends the range of this genospecies in the Southern Hemisphere. Environ Microbiol. 2014; 16:1069-80.