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Experimental infection of the rabbit tick, Haemaphysalis leporispalustris, with the bacterium Rickettsia rickettsii, and comparative biology of infected and uninfected tick lineages

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Abstract

The present study consisted of two experiments that evaluated experimental infections of Haemaphysalis leporispalustris ticks by a Brazilian strain of Rickettsia rickettsii, and their effect on tick biology. In experiment I, ticks were exposed to R. rickettsii during the larval, nymphal or adult stages by feeding on rabbits (Oryctolagus cuniculus) needle-inoculated with R. rickettsii, and thereafter reared on uninfected rabbits for the entire next tick generation. Regardless of the tick stage that acquired the infection, all subsequent tick stages were shown to be infected by PCR (infection rates varying from 1.3 to 41.7%), and were able to transmit R. rickettsii to uninfected rabbits, as demonstrated by rabbit seroconversion, guinea pig inoculation with rabbit blood, and PCR on rabbit blood. In Experiment II, ticks were exposed to R. rickettsii during the larval stage by feeding on rabbits co-infested with R. rickettsii-infected adult ticks, and thereafter reared on uninfected rabbits until the next generation of larvae. Again, all subsequent tick stages were shown to be infected by PCR (infection rates varying from 3.0 to 40.0%), and were able to transmit R. rickettsii to uninfected rabbits. Thus, it was demonstrated that larvae, nymphs, and adults of H. leporispalustris were able to acquire and maintain the R. rickettsii infection by transstadial and transovarial transmissions within the tick population, with active transmission of the bacterium to susceptible rabbits by all parasitic stages. Analyses of biological parameters of uninfected and R. rickettsii-infected tick lineages were performed in order to evaluate possible deleterious effects of R. rickettsii to the infected tick lineages. Surprisingly, all but one of the four R. rickettsii-experimental groups of the present study showed overall better biological performance than their sibling uninfected control ticks. Results of the present study showed that H. leporispalustris could support infection by a high virulent strain of R. rickettsii for at least two generations, in which infected tick lineages tended to have better performance than uninfected ticks. Our results support a possible role of H. leporispalustris in the enzootic maintenance of R. rickettsii in Latin America, as previously suggested by earlier works.

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References

  • Angerami RN, Resende MR, Feltrin AF, Katz G (2006) Brazilian spotted fever. A case-series from an endemic area in southeastern Brazil: clinical aspects. Ann N Y Acad Sci 1078:252–254. doi:10.1196/annals.1374.044

    Article  PubMed  Google Scholar 

  • Boese JL (1974) Rabbit immunity to the rabbit tick, Haemaphysalis leporis-palustris (Acari: Ixodidae). I. The development of resistance. J Med Entomol 11:503–512

    PubMed  CAS  Google Scholar 

  • Burgdorfer W (1988) Ecological and epidemiological considerations of Rocky mountain spotted fever and Scrub typhus. In: Walker DH (ed) Biology of rickettsial diseases, vol 1. CRC Inc, Boca Raton, pp 33–50

    Google Scholar 

  • Burgdorfer W, Brinton LP (1975) Mechanisms of transovarial infection of spotted fever rickettsiae in ticks. Ann N Y Acad Sci 266:61–72. doi:10.1111/j.1749-6632.1975.tb35088.x

    Article  PubMed  CAS  Google Scholar 

  • Burgdorfer W, Friedhoff KT, Lancaster JL (1966) Natural history of tick-borne spotted fever in the USA. Susceptibility of small mammals to virulent Rickettsia rickettsii. Bull Wld Hlth Org 35:149–153

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Burket CT, Vann CN, Pinger RR, Chatot CL, Steiner FE (1998) Minimum infection rate of Amblyomma americanum (Acari: Ixodidae) by Ehrlichia chaffeensis (Rickettsiales: Ehrlichieae) in Southern Indiana. J Med Entomol 35:653–659

    PubMed  CAS  Google Scholar 

  • Bustamante ME, Varela G (1947) Distribuicion de las rickettsiasis en Mexico. Rev Inst Salubr Enferm Trop 8:3–14

    Google Scholar 

  • Chapman AS, Bakken JS, Folk SM, Paddock CD, Bloch KC, Krusell A, Sexton DJ, Buckingham SC, Marshall GS, Storch GA, Dasch GA, McQuiston JH, Swerdlow DL, Dumler SJ, Nicholson WL, Walker DH, Eremeeva ME, Ohl CA (2006) Tickborne rickettsial diseases working group CDC, diagnosis and management of tickborne rickettsial diseases: Rocky mountain spotted fever, ehrlichioses, and anaplasmosis—United States: a practical guide for physicians and other health-care and public health professionals. MMWR Recomm Rep 55:1–27

    Google Scholar 

  • Cooley RA (1946) The genera Boophilus, Rhipicephalus and Haemaphysalis (ixodidae) of the new world. In: National Institute of Health, 79th Congress 2d session house document 603. Washington DC

  • Demma LJ, Traeger M, Nicholson WL, Paddock C, Blau D, Eremeeva M, Dasch G, Levin M, Singleton J, Zaki SR, Cheek J, Swerdlow D, McQuiston J (2005) Rocky mountain spotted fever from an unexpected tick vector in Arizona. N Engl J Med 353:587–594. doi:10.1056/NEJMoa050043

    Article  PubMed  CAS  Google Scholar 

  • Drummond RO, Whetstone TM (1970) Oviposition of the Gulf coast tick. J Econ Entomol 66:130–133

    Google Scholar 

  • Dumler JS, Walker DH (2005) Rocky mountain spotted fever-changing ecology and persisting virulence. N Engl J Med 353:551–553. doi:10.1056/NEJMp058138

    Article  PubMed  CAS  Google Scholar 

  • Eremeeva ME, Klemt RM, Santucci-Domotor LA, Silverman DJ, Dasch GA (2003) Genetic analysis of isolates of Rickettsia rickettsii that differ in virulence. Ann N Y Acad Sci 990:717–722

    Article  PubMed  CAS  Google Scholar 

  • Evans DE, Martins JR, Guglielmone AA (2000) Review of the ticks (Acari, Ixodida) of Brazil, their hosts and geographic distribution-1.The State of Rio Grande do Sul, Southern Brazil. Mem Inst Oswaldo Cruz 95:453–470. doi:10.1590/S0074-02762000000400003

    Article  PubMed  CAS  Google Scholar 

  • Freitas LHT, Daemon E, Prata MCA, Faccini JLH (2000) Relação entre o peso e o número de larvas e ninfas ingurgitadas e entre o período de ingurgitamento ninfal e o sexo dos adultos de Haemaphysalis leporispalustris (Packard 1869) (Acari: Ixodidae) em condições experimentais. Rev Bras Zooc 2:21–32

    Google Scholar 

  • Freitas LHT, Cardoso ACB, Prata MCA, Faccini JLH (2004) Influência da temperatura de manutenção da fase não parasitária sobre a fase parasitária de Haemaphysalis leporispalustris (Packard 1869) (Acari: Ixodidae). Rev Bras Parasitol Vet 13:115–123

    Google Scholar 

  • Fuentes L, Calderón A, Hun L (1985) Isolation and Identification of Rickettsia rickettsii from rabbit tick (Haemaphysalis leporis-palustris) in the Atlantic zone of costa rica. Am J Trop Med Hyg 34:464–567

    Google Scholar 

  • Guedes E, Leite RC, Prata MC, Pacheco RC, Walker DH, Labruna MB (2005) Detection of Rickettsia rickettsii in the tick Amblyomma cajennense in a new Brazilian spotted fever-endemic area in the state of Minas Gerais. Mem Inst Oswaldo Cruz 100:841–845. doi:10.1590/S0074-02762005000800004

    Article  PubMed  Google Scholar 

  • Harrison BA, Engber BR, Apperson CS (1997) Ticks (Acari: Ixodida) uncommonly found biting humans in North Carolina. J Vector Ecol 22:6–12

    PubMed  CAS  Google Scholar 

  • Hillyer EV, Quesenberry KE (1997) Ferrets, rabbits and rodents. Clinical medicine and surgery, 1st edn. Sauders

  • Joyce CR, Eddy GW (1943) Host and seasonal notes on the rabbit tick Haemaphysalis leporis-palustris. J Sci 17:205–212

    Google Scholar 

  • Karpathy SE, Dasch GA, Eremeeva ME (2007) Molecular typing of isolates of Rickettsia rickettsii by use of DNA sequencing of variable intergenic regions. J Clin Microbiol 45:2545–2553. doi:10.1128/JCM.00367-07

    Article  PubMed  CAS  Google Scholar 

  • Kollars TM, Oliver JH (2003) Host Associations and seasonal occurrence of Haemaphysalis leporispalustris, Ixodes brunneus, I. cookei, I. dentatus, and I. texanus (Acari: Ixodidae) in Southeastern Missouri. J Med Entomol 40:103–107

    Article  PubMed  Google Scholar 

  • Labruna MB (2006) Epidemiologia da Febre maculosa no Brasil e nas Américas. I Simpósio Brasileiro de Acarologia-I SIBAC, Viçosa, 11–12 de maio de 2006. Universidade Federal de Viçosa, Anais, pp 63–78

  • Labruna MB, Leite RC, Faccini JLH, Ferreira F (2000) Life-cycle of the tick Haemaphysalis leporis-palustris (Acari: Ixodidae) under laboratory conditions. Exp Appl Acarol 24:683–694. doi:10.1023/A:1010768511790

    Article  PubMed  CAS  Google Scholar 

  • Labruna MB, Whitworth T, Horta MC, Bouyer DH, Macbridge J, Pinter A, Popov V, Gennari SM, Walker DH (2004) 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 42:90–98. doi:10.1128/JCM.42.1.90-98.2004

    Article  PubMed  Google Scholar 

  • Labruna MB, Horta MC, Aguiar DM, Cavalcante GT, Pinter A, Gennari SM, Camargo LM (2007) Prevalence of Rickettsia infection in dogs from the urban and rural areas of Monte Negro municipality, western Amazon, Brazil. Vector Borne Zoonotic Dis 7:249–255. doi:10.1089/vbz.2006.0621

    Article  PubMed  Google Scholar 

  • Labruna MB, Ogrzewalska M, Martins TF, Pinter A, Horta MC (2008) Comparative susceptibility of the larval stage of Amblyomma aureolatum, Amblyomma cajennense, and Rhipicephalus sanguineus to the infection by Rickettsia rickettsii. J Med Entomol 45:1156–1159

    Article  PubMed  Google Scholar 

  • Mertins JW, Schlater JL, Corn JL (1992) Ectoparasites of the blackbuck antelope (Antilope cervicapra). J Wildl Dis 28:481–484

    PubMed  CAS  Google Scholar 

  • Monteiro JL (1931) Estudos sobre o typho exanthematico de S. Paulo. Mem Inst Butantan 6:5–135

    Google Scholar 

  • Monteiro JL (1933) Comportamento Experimental do Coelho aos virus do typho Exanthemático de São Paulo e da febre maculosa das Montanhas Rochosas. Mem Inst Butantan 8:3–80

    Google Scholar 

  • Need JT, Dale WE, Keirans JE, Dasch GA (1991) Annotated list of ticks (Acari: Ixodidae, Argasidae) reported in Peru: distribution, hosts, and bibliography. J Med Entomol 28:590–597

    PubMed  CAS  Google Scholar 

  • Neitz WO, Boughton F, Walters HS (1971) Laboratory investigations on the karoo paralysis tick (Ixodes rubicundus Neumann 1904). Onderst J Vet Res 38:215–224

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Paddock CD, Fernandez S, Echenique GA, Sumner JW, Reeves WK, Zaki SR, Remondegui CE (2008) Rocky mountain spotted fever in Argentina. Am J Trop Med Hyg 78:687–692

    PubMed  Google Scholar 

  • Parker RR (1923) Transmission of Rocky mountain spotted fever by the rabbit tick Haemaphysalis leporispalustris Packard. Am J Trop Med 3:39–45

    Google Scholar 

  • Parker RR, Philip CB, Jellison WL (1933) Rocky mountain spotted fever: potentialities of tick transmission in relation to geographical occurrence in the United States. Am J Trop Med 13:341–378

    Google Scholar 

  • Parker RR, Pickens EG, Lackman DB, Bell EJ, Thraikill FB (1951) Isolation and characterization of Rocky mountain spotted fever rickettsiae from the rabbit tick Haemaphysalis leporis-palustris packard. Public Health Rep 66:455–463

    PubMed  CAS  Google Scholar 

  • Parker RR, Bell JF, Chalgren WS, Thrailkill FB, Mckee MT (1952) The recovery of strains of Rocky mountain spotted fever and tularemia from ticks of the eastern United States. J Infect Dis 91:231–237

    PubMed  CAS  Google Scholar 

  • Philip CB (1959) Some epidemiological considerations in Rocky mountain spotted fever. Public Health Rep 74:595–600

    PubMed  CAS  Google Scholar 

  • Philip RN, Casper EA, Burgdorfer W, Gerloff RK, Hughes LE, Bell EJ (1978) Serologic typing of rickettsiae of the spotted fever group by microimmunofluorescence. J Immunol 121:1961–1968

    PubMed  CAS  Google Scholar 

  • Pinter A, Labruna MB (2006) Isolation of Rickettsia rickettsii and Rickettsia bellii in cell culture from the tick Amblyomma aureolatum in Brazil. Ann N Y Acad Sci 1078:523–529. doi:10.1196/annals.1374.103

    Article  PubMed  CAS  Google Scholar 

  • Sangioni LA, Horta MC, Vianna MCB, Gennari SM, Soares RM, Galvão MAM, Schumaker TTS, Ferreira F, Vidotto O, Labruna MB (2005) Rickettsial infection in animals and Brazilian spotted fever endemicity. Emerg Infect Dis 11:265–270

    PubMed  Google Scholar 

  • Shirai A, Bozeman M, Perri S, Humphries JW, Fuller HS (1961) Ecology of Rocky mountain spotted fever. I. Rickettsia rickettsii recovered from a cottontail rabbit from Virginia. Proc Soc Exp Biol Med 107:211–214

    Google Scholar 

  • Weiss E, Moulder JW (1984) The rickettsias and chlamydias. Chlamydias. Order l. Rickettsiales. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. Williams & Wilkins, Baltimore, pp 687–729

    Google Scholar 

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Acknowledgments

We thank Laboratório Biovet, Brazil, for supplying naive guinea pigs for the present study. This work was supported by Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

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Correspondence to Marcelo B. Labruna.

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Freitas, L.H.T., Faccini, J.L.H. & Labruna, M.B. Experimental infection of the rabbit tick, Haemaphysalis leporispalustris, with the bacterium Rickettsia rickettsii, and comparative biology of infected and uninfected tick lineages. Exp Appl Acarol 47, 321–345 (2009). https://doi.org/10.1007/s10493-008-9220-4

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