Rickettsioses are among the oldest known infectious diseases. In spite of this, and of the extensive research carried out, many aspects of the biology and epidemiology of tick-borne rickettsiae are far from being completely understood. Their association with arthropod vectors, the importance of vertebrates as reservoirs, the rarity of clinical signs in animals, or the interactions of pathogenic species with rickettsial endosymbionts and with the host intracellular environment, are only some examples. Moreover, new rickettsiae are continuously being discovered. In this review, we focus on the 'neglected' aspects of tick-borne rickettsioses and on the gaps in knowledge, which could help to explain why these infections are still emerging and re-emerging threats worldwide.

Center of Rickettsiosis and Arthropod Borne Diseases Hospital San Pedro CIBIR C Piqueras 98 26006 Logroño Spain

Department of Biology and Wildlife Diseases Faculty of Veterinary Hygiene and Ecology University of Veterinary and Pharmaceutical Sciences Brno Palackého 1946 1 612 42 Brno Czech Republic

Department of Biology Faculty of Medicine Masaryk University Kamenice 5 625 00 Brno Czech Republic

Department of Veterinary Sciences University of Turin Largo Braccini 2 10095 Grugliasco Italy

National Institute of Health Dr Ricardo Jorge Av da Liberdade 5 2965 575 Aguas de Moura Portugal

Zobrazit více v PubMed

Raoult D, Roux V. Rickettsioses as paradigms of new or emerging infectious diseases. Clin Microbiol Rev. 1997;10:694–719. PubMed PMC

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. PubMed PMC

Maxey EE. Some observations of the so-called spotted fever of Idaho. Med Sentinel. 1899;10:433–438.

Ricketts HT. Some aspects of Rocky Mountain spotted fever as shown by recent investigations. Med Rec. 1909;76:843–845. PubMed

Walker DH, Fishbein DB. Epidemiology of rickettsial diseases. Eur J Epidemiol. 1991;7:237–245. PubMed

Noda H, Munderloh UG, Kurtti TJ. Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Appl Environ Microbiol. 1997;63:3926–3932. PubMed PMC

Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM. Evolution and diversity of Rickettsia bacteria. BMC Biol. 2009;7:6. PubMed PMC

Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ. The incidence of bacterial endosymbionts in terrestrial arthropods. Proc Biol Sci. 2015;282:20150249. PubMed PMC

Olano JP. Rickettsial infections. Ann N Y Acad Sci. 2005;1063:187–196. PubMed

Murray GGR, Weinert LA, Rhule EL, Welch JJ. The phylogeny of Rickettsia using different evolutionary signatures. How tree-like is bacterial evolution? Syst Biol. 2016;65:265–279. PubMed PMC

Socolovschi C, Mediannikov O, Raoult D, Parola P. The relationship between spotted fever group Rickettsiae and ixodid ticks. Vet Res. 2009;40:34. PubMed PMC

Řeháček J. Ecological relationships between ticks and rickettsiae. Eur J Epidemiol. 1989;5:407–413. PubMed

Philip CB. Some epidemiological considerations in Rocky Mountain spotted fever. Public Health Rep. 1959;74:595–600. PubMed PMC

Hayes SF, Burgdorfer W, Aeschlimann A. Sexual transmission of spotted fever group rickettsiae by infected male ticks detection of rickettsiae in immature spermatozoa of Ixodes ricinus. Infect Immun. 1980;27:638–642. PubMed PMC

McDade JE, Newhouse VF. Natural history of Rickettsia rickettsii. Annu Rev Microbiol. 1986;40:287–309. PubMed

Řeháček J. Rickettsia slovaca, the organism and its ecology. Acta SC Nat Brno. 1984;18:1–50.

Estrada-Peña A, Jongejan F. Ticks feeding on humans a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol. 1999;23:685–715. PubMed

Perlman SJ, Hunter MS, Zchori-Fein E. The emerging diversity of Rickettsia. Proc Biol Sci. 2006;273:2097–2106. PubMed PMC

Niebylski ML, Peacock MG, Schwan TG. Lethal effect of Rickettsia rickettsii on its tick vector (Dermacentor andersoni) Appl Environ Microbiol. 1999;65:773–778. PubMed PMC

Levin ML, Killmaster LF, Zemtsova GE, Grant D, Mumcuoglu KY, Eremeeva ME, et al. Incongruent effects of two isolates of Rickettsia conorii on the survival of Rhipicephalus sanguineus ticks. Exp Appl Acarol. 2009;49:347–359. PubMed

Labruna MB, Ogrzewalska M, Soares JF, Martins TF, Soares HS, Moraes-Filho J, et al. Experimental infection of Amblyomma aureolatum ticks with Rickettsia rickettsii. Emerg Infect Dis. 2011;17:829–834. PubMed PMC

Krawczak FS, Agostinho WC, Polo G, Moraes-Filho J, Labruna MB. Comparative evaluation of Amblyomma ovale ticks infected and noninfected by Rickettsia sp. strain Atlantic rainforest, the agent of an emerging rickettsiosis in Brazil. Ticks Tick-borne Dis. 2016;7:502–507. PubMed

Socolovschi C, Gaudart J, Bitam I, Huynh TP, Raoult D, Parola P. Why are there so few Rickettsia conorii conorii-infected Rhipicephalus sanguineus ticks in the wild? PLoS Negl Trop Dis. 2012;6:e1697. PubMed PMC

Hunter DJ, Torkelson JL, Bodnar J, Mortazavi B, Laurent T, Deason J, et al. The Rickettsia endosymbiont of Ixodes pacificus contains all the genes of de novo folate biosynthesis. PLoS One. 2015;10:e0144552. PubMed PMC

Bodnar JL, Fitch S, Rosati A, Zhong J. The folA gene from the Rickettsia endosymbiont of Ixodes pacificus encodes a functional dihydrofolate reductase enzyme. Ticks Tick-borne Dis. 2017;9:443–449. PubMed PMC

Macaluso KR, Sonenshine DE, Ceraul SM, Azad AF. Rickettsial infection in Dermacentor variabilis (Acari: Ixodidae) inhibits transovarial transmission of a second Rickettsia. J Med Entomol. 2002;39:809–813. PubMed

Wright CL, Sonenshine DE, Gaff HD, Hynes WL. Rickettsia parkeri transmission to Amblyomma americanum by co-feeding with Amblyomma maculatum (Acari: Ixodidae) and potential for spillover. J Med Entomol. 2015;52(5):1090. PubMed

Burgdorfer W, Hayes SF, Mavros AJ. Non-pathogenic rickettsiae in Dermacentor andersoni: a limiting factor for the distribution of Rickettsia rickettsii. In: Burgdorfer WAA, Anacker RL, editors. Rickettsia and Rickettsial Disease. New York: Academic Press; 1981. pp. 585–594.

Gall CA, Reif KE, Scoles GA, Mason KL, Mousel M, Noh SM, et al. The bacterial microbiome of Dermacentor andersoni ticks influences pathogen susceptibility. ISME J. 2016;10:1846–1855. PubMed PMC

Bonnet SI, Binetruy F, Hernández-Jarguín AM, Duron O. The tick microbiome: why non-pathogenic microorganisms matter in tick biology and pathogen transmission. Front Cell Infect Microbiol. 2017;7:236. PubMed PMC

Václav R, Ficová M, Prokop P, Betáková T. Associations between coinfection prevalence of Borrelia lusitaniae, Anaplasma sp., and Rickettsia sp. in hard ticks feeding on reptile hosts. Microb Ecol. 2011;61:245–253. PubMed

Lommano E, Bertaiola L, Dupasquier C, Gern L. Infections and coinfections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in western Switzerland. Appl Environ Microbiol. 2012;78:4606–4612. PubMed PMC

Driscoll TP, Verhoeve VI, Guillotte ML, Lehman SS, Rennoll SA, Beier-Sexton M, et al. Wholly Rickettsia! Reconstructed metabolic profile of the quintessential bacterial parasite of eukaryotic cells. MBio. 2017;8:e00859–e00817. PubMed PMC

Harris EK, Verhoeve VI, Banajee KH, Macaluso JA, Azad AF, Macaluso KR. Comparative vertical transmission of Rickettsia by Dermacentor variabilis and Amblyomma maculatum. Ticks Tick Borne Dis. 2017;8:598–604. PubMed PMC

Matsumoto K, Ogawa M, Brouqui P, Raoult D, Parola P. Transmission of Rickettsia massiliae in the tick, Rhipicephalus turanicus. Med Vet Entomol. 2005;19:263–270. PubMed

Davoust B, Mediannikov O, Marie JL, Socolovschi C, Parola P, Raoult D. Are vertebrates reservoir hosts for Rickettsia? Bull Acad Vet France. 2010;163:291–302.

Levin ML, Snellgrove AN, Zemtsova GE. Comparative value of blood and skin samples for diagnosis of spotted fever group rickettsial infection in model animals. Ticks Tick Borne Dis. 2016;7:1029–1034. PubMed PMC

Haydon DT, Cleaveland S, Taylor LH, Laurenson MK. Identifying reservoirs of infection a conceptual and practical challenge. Emerg Infect Dis. 2002;8:1468–1473. PubMed PMC

Levin ML, Killmaster LF, Zemtsova GE. Domestic dogs (Canis familiaris) as reservoir hosts for Rickettsia conorii. Vector Borne Zoonotic Dis. 2012;12:28–33. PubMed

Burgdorfer W, Friedhoff KT, Lancaster Jr JL. Natural history of tick-borne spotted fever in the USA: Susceptibility of small mammals to virulent Rickettsia rickettsii. Bull World Health Organ. 1966;35:149–53. PubMed PMC

Bozeman FM, Shirai A, Humphries JW, Fuller HS. Ecology of Rocky Mountain spotted fever II. Natural infection of wild mammals and birds in Virginia and Maryland. Am J Trop Med Hyg. 1967;16:48–59. PubMed

Burgdorfer W, Cooney JC, Mavros AJ, Jellison WL, Maser C. The role of cottontail rabbits (Sylvilagus spp.) in the ecology of Rickettsia rickettsii in the United States. Am J Trop Med Hyg. 1980;29:686–690. PubMed

Horta MC, Moraes-Filho J, Casagrande RA, Saito TB, Rosa SC, Ogrzewalska M, et al. Experimental infection of opossums Didelphis aurita by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Vector Borne Zoonotic Dis. 2009;9:109–118. PubMed

Souza CE, Moraes-Filho J, Ogrzewalska M, Uchoa FC, Horta MC, Souza SS, et al. Experimental infection of capybaras Hydrochoerus hydrochaeris by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Vet Parasitol. 2009;161:116–121. PubMed

Lukovsky-Akhsanov N, Keating MK, Spivey P, Lathrop Jr GW, Powell N, Levin ML. Assessment of domestic goats as models for experimental and natural infection with the North American isolate of Rickettsia slovaca. PLoS One. 2016;11:e0165007. PubMed PMC

Heylen D, Fonville M, van Leeuwen AD, Sprong H. Co-infections and transmission dynamics in a tick-borne bacterium community exposed to songbirds. Env Microbiol. 2016;18:988–996. PubMed

Zemtsova G, Killmaster LF, Mumcuoglu KY, Levin ML. Co-feeding as a route for transmission of Rickettsia conorii israelensis between Rhipicephalus sanguineus ticks. Exp Appl Acarol. 2010;52:383–392. PubMed

Randolph SE, Gern L, Nuttall PA. Co-feeding ticks epidemiological significance for tick-borne pathogen transmission. Parasitol Today. 1996;12:472–479. PubMed

Levin ML, Zemtsova GE, Montgomery M, Killmaster LF. Effects of homologous and heterologous immunization on the reservoir competence of domestic dogs for Rickettsia conorii (israelensis) Ticks Tick Borne Dis. 2014;5:33–40. PubMed PMC

Martello E, Selmi M, Ragagli C, Ambrogi C, Stella MC, Mannelli A, et al. Rickettsia slovaca in immature Dermacentor marginatus and tissues from Apodemus spp. in the northern Apennines, Italy. Ticks Tick Borne Dis. 2013;4:518–521. PubMed

Paddock CD, Allerdice MEJ, Karpathy SE, Nicholson WL, Levin ML, Smith TC, et al. Unique strain of Rickettsia parkeri associated with the hard tick Dermacentor parumapertus Neumann in the western United States. Appl Environ Microbiol. 2017;83. PubMed PMC

Piranda EM, Faccini JLH, Pinter A, Saito TB, Pacheco RC, Hagiwara MK, et al. Experimental infection of dogs with a Brazilian strain of Rickettsia rickettsii clinical and laboratory findings. Mem Inst Oswaldo Cruz. 2008;103:696–701. PubMed

Labruna MB, Kamakura O, Moraes J, Horta MC, Pacheco RC. Rocky Mountain spotted fever in dogs, Brazil. Emerg Infect Dis. 2009;15:458–460. PubMed PMC

Solano-Gallego LJ, Kidd L, Trotta M, Di Marco M, Caldin M, Furlanello T, et al. Febril illness associated with Rickettsia conorii infection in dogs from Sicily. Emerg Infect Dis. 2006;12:1985–1989. PubMed PMC

Alexandre N, Santos AS, Bacellar F, Boinas FJ, Nuncio MS, de Sousa R. Detection of Rickettsia conorii strains in Portuguese dogs (Canis familiaris) Ticks Tick Borne Dis. 2011;2:119–122. PubMed

Solano-Gallego L, Caprì A, Pennisi MG, Caldin M, Furlanello T, Trotta M. Acute febrile illness is associated with Rickettsia spp. infection in dogs. Parasit Vectors. 2015;8:216. PubMed PMC

Curto P, Simões I, Riley SP, Martinez JJ. Differences in intracellular fate of two Spotted Fever Group Rickettsia in macrophage-like cells. Front Cell Infect Microbiol. 2016;6:80. PubMed PMC

Mannelli A, Mandola ML, Pedri P, Tripoli M, Nebbia P. Associations between dogs that were serologically positive for Rickettsia conorii relative to the residences of two human cases of Mediterranean spotted fever in Piemonte (Italy) Prev Vet Med. 2003;60:13–26. PubMed

Demma LJ, Traeger M, Blau D, Gordon R, Johnson B, Dickson J, et al. Serologic evidence for exposure to Rickettsia rickettsii in eastern Arizona and recent emergence of Rocky Mountain spotted fever in this region. Vector Borne Zoonotic Dis. 2006;6:423–429. PubMed

McQuiston JH, Guerra MA, Watts MR, Lawaczeck E, Levy C, Nicholson WL, et al. Evidence of exposure to spotted fever group rickettsiae among Arizona dogs outside a previously documented outbreak area. Zoonoses Public Health. 2011;58:85–92. PubMed

Wächter M, Wölfel S, Pfeffer M, Dobler G, Kohn B, Moritz A, et al. Serological differentiation of antibodies against Rickettsia helvetica, R. raoultii, R. slovaca, R. monacensis and R. felis in dogs from Germany by a micro-immunofluorescent antibody test. Parasit Vectors. 2015;8:216. PubMed PMC

Segura-Porta F, Diestre-Ortin G, Ortuño-Romero A, Sanfeliu-Sala I, Font-Creus B, Muñoz-Espin T, et al. Prevalence of antibodies to spotted fever group rickettsiae in human beings and dogs from and endemic area of Mediterranean spotted fever in Catalonia, Spain. Eur J Epidemiol. 1998;14:395–398. PubMed

Harrus S, Lior Y, Ephros M, Grisaru-Soen G, Keysary A, Strenger C, et al. Rickettsia conorii in humans and dogs a seroepidemiologic survey of two rural villages in Israel. Am J Trop Med Hyg. 2007;77:133–135. PubMed

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. PubMed

Portillo A, de Sousa R, Santibáñez S, Duarte A, Edouard S, Fonseca IP, et al. Guidelines for the detection of Rickettsia spp. Vector Borne Zoonotic Dis. 2017;17:23–32. PubMed

Oteo JA, Ibarra V, Blanco JR, Martínez de Artola V, Márquez FJ, Portillo A, Raoult D, Anda P. Dermacentor-borne necrosis erythema and lymphadenopathy: clinical and epidemiological features of a new tick-borne disease. Clin Microbiol Infect. 2004;10:327–331. PubMed

Portillo A, Ibarra V, Santibáñez S, Pérez-Martínez L, Blanco JR, Oteo JA. Genetic characterisation of ompA, ompB and gltA genes from Ca. R. rioja. Clin Microbiol Infect. 2009;15(Suppl 2):307–308. PubMed

Pérez-Pérez L, Portillo A, Allegue F, Zulaica A, Oteo JA, Caeiro JL, et al. Dermacentor-borne Necrosis Erythema and Lymphadenopathy (DEBONEL): a case associated with Rickettsia rioja. Acta Derm Venereol. 2010;90:214–215. PubMed

Matsumoto K, Parola P, Rolain JM, Jeffery K, Raoult D. Detection of “Rickettsia sp. strain Uilenbergi” and “Rickettsia sp. strain Davousti” in Amblyomma tholloni ticks from elephants in Africa. BMC Microbiol. 2007;7:74. PubMed PMC

Lopez-Velez R, Palomar AM, Oteo JA, Norman FF, Pérez-Molina JA, Portillo A. Novel Candidatus Rickettsia species detected in nostril tick from human, Gabon, 2014. Emerg Infect Dis. 2015;21:325–7. PubMed PMC

Paddock CD, Sumner JW, Comer JA, Zaki SR, Goldsmith CS, Goddard J. Rickettsia parkeri a newly recognized cause of spotted fever rickettsiosis in the United States. Clin Infect Dis. 2004;38:805–811. PubMed

Portillo A, Oteo JA. New tools, new tick-borne diseases? World J Clin Infect Dis. 2015;5:51–54.

Medlock JM, Hansford KM, Bormane A, Derdakova M, Estrada-Peña A, George JC, et al. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit Vectors. 2013;6:1. PubMed PMC

Karbowiak G. The occurrence of the Dermacentor reticulatus tick - its expansion to new areas and possible causes. Ann Parasitol. 2014;60:37–47. PubMed

Oteo JA, Portillo A. Tick-borne rickettsioses in Europe. Ticks Tick Borne Dis. 2012;3:271–278. PubMed

Parola P, Socolovschi C, Jeanjean L, Bitam I, Fournier PE, Sotto A, et al. Warmer weather linked to tick attack and emergence of severe rickettsioses. PLoS Negl Trop Dis. 2008;2:e338. PubMed PMC

Millán J, Proboste T, Fernández de Mera IG, Chirife AD, de la Fuente J, Altet L. Molecular detection of vector-borne pathogens in wild and domestic carnivores and their ticks at the human-wildlife interface. Ticks Tick Borne Dis. 2016;7:284–290. PubMed

Pesquera C, Portillo A, Palomar AM, Oteo JA. 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. Parasit Vectors. 2015;8:46. PubMed PMC

Palomar AM, Santibáñez P, Mazuelas D, Roncero L, Santibáñez S, Portillo A, et al. Role of birds in dispersal of etiologic agents of tick-borne zoonoses, Spain, 2009. Emerg Infect Dis. 2012;18:1188–1191. PubMed PMC

Sparagano O, George D, Giangaspero A, Špitalská E. Arthropods and associated arthropod-borne diseases transmitted by migrating birds. The case of ticks and tick-borne pathogens. Vet Parasitol. 2015;213:61–66. PubMed

Randolph SE. To what extent has climate change contributed to the recent epidemiology of tick-borne diseases? Vet Parasitol. 2010;167:92–94. PubMed

Portillo A, Oteo JA. Rickettsiosis as threat for the traveller. In: Rodriguez-Morales A, editor. Current Topics in Tropical Medicine. Rijeka: InTech; 2012. pp. 3–24.

Pietzsch ME, Hansford KM, Cull B, Jahfari S, Sprong H, Medlock JM. Detection of Dermacentor marginatus and a possible Rickettsia slovaca case in the United Kingdom-the risk of the visiting traveller. Travel Med Infect Dis. 2015;13:200–201. PubMed

Jahfari S, de Vries A, Rijks JM, Van Gucht S, Vennema H, Sprong H, et al. Tick-borne encephalitis virus in ticks and roe deer, the Netherlands. Emerg Infect Dis. 2017;23:1028–1030. PubMed PMC

de Graaf JA, Reimerink JH, Voorn GP, Bij de Vaate EA, de Vries A, Rockx B, et al. First human case of tick-borne encephalitis virus infection acquired in the Netherlands, July 2016. Euro Surveill. 2016;21:30318. PubMed PMC

Weststrate AC, Knapen D, GD Laverman BS, Prick JJ, Spit SA, et al. Increasing evidence of tick-borne encephalitis (TBE) virus transmission, the Netherlands, June 2016. Euro Surveill. 2017;22:30482. PubMed PMC

García Rada A. First outbreak of Crimean-Congo haemorrhagic fever in western Europe kills one man in Spain. BMJ. 2016;354:i4891. PubMed

Estrada-Peña A, Palomar AM, Santibáñez P, Sánchez N, Habela MA, Portillo A, et al. Crimean-Congo hemorrhagic fever virus in ticks, southwestern Europe, 2010. Emerg Infect Dis. 2012;18:179–80. PubMed PMC

European Centre for Disease Prevention and Control. Epidemiological situation of rickettsioses in EU/EFTA countries. Stockholm: ECDC; 2013. https://ecdc.europa.eu/en/publications-data/epidemiological-situation-rickettsioses-euefta-countries. Accessed 18 Jan 2018.

Stärk KD, Arroyo Kuribreña M, Dauphin G, Vokaty S, Ward MP, Wieland B, et al. One Health surveillance - More than a buzz word? Prev Vet Med. 2015;120:124–130. PubMed

Dietrich M, Lebarbenchon C, Jaeger A, Le Rouzic C, Bastien M, Lagadec E, et al. Rickettsia spp. in seabird ticks from western Indian Ocean islands, 2011–2012. Emerg Infect Dis. 2014;20:838–842. PubMed PMC

Reeves WK, Loftis AD, Sanders F, Spinks MD, Wills W, Denison AM, et al. Borrelia, Coxiella, and Rickettsia in Carios capensis (Acari, Argasidae) from a brown pelican (Pelecanus occidentalis) rookery in South Carolina, USA. Exp Appl Acarol. 2006;39:321–329. PubMed

Pader V, Nikitorowicz Buniak J, Abdissa A, Adamu H, Tolosa T, Gashaw A, et al. Candidatus Rickettsia hoogstraalii in Ethiopian Argas persicus ticks. Ticks Tick Borne Dis. 2012;3:338–345. PubMed

Kawabata H, Ando S, Kishimoto T, Kurane I, Takano A, Nogami S, et al. First detection of Rickettsia in soft-bodied ticks associated with seabirds, Japan. Microbiol Immunol. 2006;50:403–406. PubMed

Mattila JT, Burkhardt NY, Hutcheson HJ, Munderloh UG, Kurtt TJ. Isolation of cell lines and a rickettsial endosymbiont from the soft tick Carios capensis (Acari Argasidae Ornithodorinae) J Med Entomol. 2007;44:1091–1101. PubMed

Milhano N, Palma M, Marcili A, Núncio MS, de Carvalho IL, de Sousa R. Rickettsia lusitaniae sp. nov. isolated from the soft tick Ornithodoros erraticus (Acarina Argasidae). Comp Immunol Microbiol Infect Dis. 2014;37:189–93. PubMed

Sánchez-Montes S, Guzmán-Cornejo C, Martínez-Nájera Y, Becker I, Venzal JM, Labruna MB. Rickettsia lusitaniae associated with Ornithodoros yumatensis (Acari: Argasidae) from two caves in Yucatan, Mexico. Ticks Tick Borne Dis. 2016;7:1097–1101. PubMed

Moreira-Soto RD, Moreira-Soto A, Corrales-Aguilar E, Calderón-Arguedas Ó, Troyo A. ‘Candidatus Rickettsia nicoyana’: A novel Rickettsia species isolated from Ornithodoros knoxjonesi in Costa Rica. Ticks Tick Borne Dis. 2017;8:532–536. PubMed

Tahir D, Socolovschi C, Marié JL, Ganay G, Berenger JM, Bompar JM, et al. New Rickettsia species in soft ticks Ornithodoros hasei collected from bats in French Guiana. Ticks Tick Borne Dis. 2016;7:1089–1096. PubMed

Řeháček J, Urvölgyi J, Kovácová E. Massive occurrence of rickettsiae of the spotted fever group in fowl tampan, Argas persicus, in the Armenian SSR. Acta Virol. 1977;21:431–438. PubMed

Socolovschi C, Kernif T, Raoult D, Parola P. Borrelia, Rickettsia, and Ehrlichia species in bat ticks, France, 2010. Emerg Infect Dis. 2012;18:1966–1975. PubMed PMC

Lafri I, Leulmi H, Baziz-Neffah F, Lalout R, Mohamed C, Mohamed K, et al. Detection of a novel Rickettsia sp. in soft ticks (Acari Argasidae) in Algeria. Microbes Infect. 2015;17:859–861. PubMed

Loftis AD, Gill JS, Schriefer ME, Levin ML, Eremeeva ME, Gilchrist MJ, et al. Detection of Rickettsia, Borrelia, and Bartonella in Carios kelleyi (Acari: Argasidae) J Med Entomol. 2005;42:473–480. PubMed

Cutler SJ, Browning P, Scott JC. Ornithodoros moubata, a soft tick vector for Rickettsia in East Africa? Ann N Y Acad Sci. 2006;1078:373–7. PubMed

Burgdorfer W, Newhouse VF, Pickens EG, Lackman DB. Ecology of Rocky Mountain spotted fever in Western Montana I. Isolation of Rickettsia rickettsii from wild mammals. Am J Hyg. 1962;76:293–301. PubMed

Moreira JA, Magalhães O. Thypho exanthematico em Minas Gerais. Brasil-Médico. 1935;44:465–470.

Travassos J. Identification d’un virus semblable a celui du “Typhus exanthématique de Sao Paulo,” isolé de la sarigue marsupiale (Didelphis paraguayensis) Compt Rend Soc Biol. 1937;126:1054–1056.

Ueno TE, Costa FB, Moraes-Filho J, Agostinho WC, Fernandes WR, Labruna MB. Experimental infection of horses with Rickettsia rickettsii. Parasit Vectors. 2016;9:499. PubMed PMC

Horta MC, Sabatini GS, Moraes-Filho J, Ogrzewalska M, Canal RB, Pacheco RC, et al. Experimental infection of the opossum Didelphis aurita by Rickettsia felis, Rickettsia bellii, and Rickettsia parkeri and evaluation of the transmission of the infection to ticks Amblyomma cajennense and Amblyomma dubitatum. Vector Borne Zoonotic Dis. 2010;10:959–967. PubMed

Tomassone L, Conte V, Parrilla G, De Meneghi D. Rickettsia infection in dogs and Rickettsia parkeri in Amblyomma tigrinum ticks, Cochabamba Department, Bolivia. Vector Borne Zoonotic Dis. 2010;10:953–958. PubMed

Grasperge BJ, Wolfson W, Macaluso KR. Rickettsia parkeri infection in domestic dogs, Southern Louisiana, USA, 2011. Emerg Infect Dis. 2012;18:995–997. PubMed PMC

Joyeux C, Pieri J. Le lapin peut constituer un réservoir de virus pour la fièvre boutonneuse (exanthématique) C R Acad Sci. 1932;194:2342.

Ruiz-Beltrán R, Herrero-Herrero JI, Martín- Sanchez AM, Criado-Gutiérrez LA. Role of Lagomorpha in the wild cycle of Rickettsia conorii in Salamanca (Spain) Eur J Epidemiol. 1992;8:136–139. PubMed

Segura F, Pons I, Miret J, Pla J, Ortuño A, Nogueras MM. The role of cats in the eco-epidemiology of spotted fever group diseases. Parasit Vectors. 2014;7:353. PubMed PMC

Dietrich M, Tjale MA, Weyer J, Kearney T, Seamark EC, Nel LH, et al. Diversity of Bartonella and Rickettsia spp. in bats and their blood-feeding ectoparasites from South Africa and Swaziland. PLoS One. 2016;11:e0152077. PubMed PMC

Inokuma H, Seino N, Suzuki M, Kaji K, Takahashi H, Igota H, et al. Detection of Rickettsia helvetica DNA from peripheral blood of sika deer (Cervus nippon yesoensis) in Japan. J Wild Dis. 2008;44:164–167. PubMed

Sprong H, Wielinga PR, Fonville M, Reusken C, Brandenburg AH, Borgsteede F, et al. Ixodes ricinus ticks are reservoir hosts for Rickettsia helvetica and potentially carry flea-borne Rickettsia species. Parasit Vectors. 2009;2:41. PubMed PMC

Hornok S, Kováts D, Csörgő T, Meli ML, Gönczi E, Hadnagy Z, et al. Birds as potential reservoirs of tick-borne pathogens first evidence of bacteraemia with Rickettsia helvetica. Parasit Vectors. 2014;7:128. PubMed PMC

Speck S, Perseke L, Petney T, Skuballa J, Pfäffle M, Taraschewski H, et al. Detection of Rickettsia helvetica in ticks collected from European hedgehogs (Erinaceus europaeus Linnaeus, 1758). Ticks Tick Borne Dis. 2013;4:222–6. PubMed

De Sousa R, Lopes de Carvalho I, Santos AS, Bernardes C, Milhano N, Jesus J, et al. Role of the lizard Teira dugesii as a potential host for Ixodes ricinus tick-borne pathogens. Appl Environ Microbiol. 2012;78:3767–3769. PubMed PMC

Tomassone L, Ceballos LA, Ragagli C, Martello E, de Sousa R, Stella MC, et al. Importance of common wall lizards in the transmission dynamics of tick-borne pathogens in the northern Apennine Mountains, Italy. Microb Ecol. 2017;74:961–8. PubMed

Schex S, Dobler G, Riehm J, Müller J, Essbauer S. Rickettsia spp. in wild small mammals in Lower Bavaria, south-eastern Germany. Vector Borne Zoonotic Dis. 2011;11:493–502. PubMed

Schmidt S, Essbauer SS, Mayer-Scholl A, Poppert S, Schmidt-Chanasit J, Klempa B, et al. Multiple infections of rodents with zoonotic pathogens in Austria. Vector Borne Zoonotic Dis. 2014;14:467–475. PubMed PMC

Hornok S, Földvári G, Rigó K, Meli ML, Gönczi E, Répási A, et al. Synanthropic rodents and their ectoparasites as carriers of a novel haemoplasma and vector-borne, zoonotic pathogens indoors. Parasit Vectors. 2015;8:27. PubMed PMC

Lauzi S, Maia JP, Epis S, Marcos R, Pereira C, Luzzago C, et al. Molecular detection of Anaplasma platys, Ehrlichia canis, Hepatozoon canis and Rickettsia monacensis in dogs from Maio Island of Cape Verde archipelago. Ticks Tick-borne Dis. 2016;7:964–969. PubMed

Liesner JM, Krucken J, Schaper R, Pachnicke S, Kohn B, Muller E, et al. Vector-borne pathogens in dogs and red foxes from the federal state of Brandenburg, Germany. Vet Parasitol. 2016;224:44–51. PubMed

Řeháček J, Urvölgyi J, Kocianová E, Jedlička L. Susceptibility of some species of rodents to rickettsiae. Folia Parasitol (Praha). 1992;39:265–284. PubMed

Márquez FJ, Rojas A, Ibarra V, Cantero A, Rojas J, Oteo JA, et al. Prevalence data of Rickettsia slovaca and other SFG rickettsiae species in Dermacentor marginatus in the southeastern Iberian Peninsula. Ann N Y Acad Sci. 2006;1078:328–30. PubMed

Ortuño A, Quesada M, Lopez-Claessens S, Castella J, Sanfeliu I, Anton E, et al. The role of wild boar (Sus scrofa) in the ecoepidemiology of R. slovaca in northeastern Spain. Vector Borne Zoonotic Dis. 2007;7:59–64. PubMed

Selmi M, Martello E, Bertolotti L, Bisanzio D, Tomassone L. Rickettsia slovaca and Rickettsia raoultii in Dermacentor marginatus ticks collected on wild boars (Sus scrofa) in Tuscany, Italy. J Med Entomol. 2009;46:1490–1493. PubMed

Ortuño A, Pons I, Quesada M, Lario S, Anton E, Gil A, et al. Evaluation of the presence of Rickettsia slovaca infection in domestic ruminants in Catalonia, Northeastern Spain. Vector Borne Zoonotic Dis. 2012;12:1019–1022. PubMed PMC

Shpynov S, Fournier PE, Rudakov N, Raoult D. “Ca. R. tarasevichiae” in Ixodes persulcatus ticks collected in Russia. Ann N Y Acad Sci. 2003;990:162–172. PubMed

Jia N, Zheng YC, Jiang JF, Ma L, Cao WC. Human infection with Candidatus Rickettsia tarasevichiae. N Engl J Med. 2013;369:1178–1180. PubMed

Sréter-Lancz Z, Széll Z, Kovács G, Egyed L, Márialigeti K, Sréter T. Rickettsiae of the spotted-fever group in ixodid ticks from Hungary: identification of a new genotype (‘Ca. R. kotlanii’) Ann Trop Med Parasitol. 2006;100:229–236. PubMed

Mura A, Masala G, Tola S, Satta G, Fois F, Piras P, et al. First direct detection of rickettsial pathogens and a new rickettsia, ‘Candidatus Rickettsia barbariae’, in ticks from Sardinia, Italy. Clin Microbiol Infect. 2008;14:1028–1033. PubMed

Eremeeva ME, Stromdahl EY. New spotted fever group Rickettsia in a Rhipicephalus turanicus tick removed from a child in eastern Sicily, Italy. Am J Trop Med Hyg. 2011;84:99–101. PubMed PMC

Igolkina YP, Rar VA, Yakimenko VV, Malkova MG, Tancev AK, Tikunov AY, et al. Genetic variability of Rickettsia spp. in Ixodes persulcatus/Ixodes trianguliceps sympatric areas from Western Siberia, Russia: identification of a new Candidatus Rickettsia species. Infect Genet Evol. 2015;34:88–93. PubMed

Hajduskova E, Literak I, Papousek I, Costa FB, Novakova M, Labruna MB, et al. ‘Candidatus Rickettsia mendelii’, a novel basal group rickettsia detected in Ixodes ricinus ticks in the Czech Republic. Ticks Tick Borne Dis. 2016;7:482–486. PubMed

Jiang J, Blair PJ, Felices V, Moron C, Cespedes M, Anaya E, et al. Phylogenetic analysis of a novel molecular isolate of spotted fever group Rickettsiae from northern Peru: Candidatus Rickettsia andeanae. Ann N Y Acad Sci. 2005;1063:337–342. PubMed

Rolain JM, Mathai E, Lepidi H, Somashekar HR, Mathew LG, Prakash JA, et al. “Ca. R. kellyi”, India. Emerg Infect Dis. 2006;12:483–485. PubMed PMC

Mediannikov O, Sidelnikov Y, Ivanov L, Fournier PE, Tarasevich I, Raoult D. Far eastern tick-borne rickettsiosis: identification of two new cases and tick vector. Ann N Y Acad Sci. 2006;1078:80–88. PubMed

Izzard L, Graves S, Cox E, Fenwick S, Unsworth N, Stenos J. Novel rickettsia in ticks, Tasmania, Australia. Emerg Infect Dis. 2009;15:1654–1656. PubMed PMC

Tomassone L, Nuñez P, Ceballos LA, Gürtler RE, Kitron U, Farber M. Detection of “Ca. R. sp. strain Argentina” and Rickettsia bellii in Amblyomma ticks (Acari: Ixodidae) from Northern Argentina. Exp Appl Acarol. 2010;52:93–100. PubMed PMC

Williamson PC, Billingsley PM, Teltow GJ, Seals JP, Turnbough MA, Atkinson SF. Borrelia, Ehrlichia, and Rickettsia spp. in ticks removed from persons, Texas, USA. Emerg Infect Dis. 2010;16:441–446. PubMed PMC

Zou Y, Wang Q, Fu Z, Liu P, Jin H, Yang H, et al. Detection of spotted fever group Rickettsia in Haemaphysalis longicornis from Hebei Province, China. J Parasitol. 2011;97:960–962. PubMed

Mediannikov O, Diatta G, Zolia Y, Balde MC, Kohar H, Trape JF, et al. Tick-borne rickettsiae in Guinea and Liberia. Ticks Tick Borne Dis. 2012;3:43–48. PubMed

Mutai BK, Wainaina JM, Magiri CG, Nganga JK, Ithondeka PM, Njagi ON, et al. Zoonotic surveillance for rickettsiae in domestic animals in Kenya. Vector Borne Zoonotic Dis. 2013;13(6):360. PubMed

Anstead CA, Chilton NB. A novel Rickettsia species detected in vole ticks (Ixodes angustus) from western Canada. Appl Environ Microbiol. 2013;79:7583–9. PubMed PMC

Anstead CA, Chilton NB. Detection of a novel Rickettsia (Alphaproteobacteria: Rickettsiales) in rotund ticks (Ixodes kingi) from Saskatchewan, Canada. Ticks Tick Borne Dis. 2013;4:2012–2016. PubMed

Mediannikov O, Aubadie-Ladrix M, Raoult D. Candidatus ‘Rickettsia senegalensis’ in cat fleas in Senegal. New Microbes New Infect. 2014;3:24–28. PubMed PMC

Kho KL, Koh FX, Tay ST. Molecular evidence of potential novel spotted fever group rickettsiae, Anaplasma and Ehrlichia species in Amblyomma ticks parasitizing wild snakes. Parasit Vectors. 2015;8:112. PubMed PMC

Ereqat S, Nasereddin A, Al-Jawabre hA, Azmi K, Harrus S, Mumcuoglu K, et al. Molecular detection and identification of Spotted Fever Group rickettsiae in ticks collected from the West Bank, Palestinian territories. PLoS Negl Trop Dis. 2016;10:e0004348. PubMed PMC

Yang J, Tian Z, Liu Z, Niu Q, Han R, Li Y, et al. Novel spotted fever group rickettsiae in Haemaphysalis qinghaiensis ticks from Gansu, Northwest China. Parasit Vectors. 2016;9:146. PubMed PMC

Takajo I, Sekizuka T, Fujita H, Kawano A, Kawaguchi T, Matsuda M, et al. Possible case of novel spotted fever group rickettsiosis in traveler returning to Japan from India. Emerg Infect Dis. 2016;22:1079–1082. PubMed PMC

Kimita G, Mutai B, Nyanjom SG, Wamunyokoli F, Waitumbi J. Phylogenetic variants of Rickettsia africae, and incidental identification of “Candidatus Rickettsia moyalensis” in Kenya. PLoS Negl Trop Dis. 2016;10:e0004788. PubMed PMC

Sabatini GS, Pinter A, Nieri-Bastos FA, Marcili A, Labruna MB. Survey of ticks (Acari: Ixodidae) and their rickettsia in an Atlantic rain forest reserve in the State of São Paulo, Brazil. J Med Entomol. 2010;47:913–916. PubMed

Spolidorio MG, Labruna MB, Mantovani E, Brandao PE, Richtzenhain LJ, Yoshinari NH. Novel spotted fever group rickettsiosis, Brazil. Emerg Infect Dis. 2010;16(3):521. PubMed PMC

Almeida AP, Cunha LM, Bello AC, da Cunha AP, Domingues LN, Leite RC, et al. A novel Rickettsia infecting Amblyomma dubitatum ticks in Brazil. Ticks Tick Borne Dis. 2011;2:209–212. PubMed

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;49:960–965. PubMed

Dubska L, Literak I, Kverek P, Roubalova E, Kocianova E, Taragelova V. Tick-borne zoonotic pathogens in ticks feeding on the common nightingale including a novel strain of Rickettsia sp. Ticks Tick Borne Dis. 2012;3:265–268. PubMed

Sandalakis V, Chochlakis D, Ioannou I, Psaroulaki A. Identification of a novel uncultured Rickettsia species strain (Rickettsia species strain Tselenti) in Cyprus. Am J Trop Med Hyg. 2013;88:698–700. PubMed PMC

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(6):883. PubMed

Wild ungulates as sentinels of flaviviruses and tick-borne zoonotic pathogen circulation: an Italian perspective