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Co-feeding as a route for transmission of Rickettsia conorii israelensis between Rhipicephalus sanguineus ticks

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Abstract

Rickettsia conorii is widely distributed in Europe, Asia, and Africa. The brown dog tick, Rhipicephalus sanguineus, is the recognized vector of R. conorii. In this study, we assessed the efficiency of R. conorii israelensis transmission between co-feeding Rh. sanguineus ticks. Infected Rh. sanguineus adults and uninfected nymphs were fed simultaneously upon either naïve dogs or a dog previously exposed to this agent. When ticks were placed upon naïve dogs, 92–100% of nymphs acquired the infection and 80–88% of infected engorged nymphs transmitted it transstadially. When ticks were placed upon a seropositive dog, only 8–28.5% of recipient nymphs became infected. Our results establish the first evidence for efficient natural transmission of R. conorii israelensis between co-feeding ticks upon both naïve and seropositive dogs. This route of transmission can ensure continuous circulation of R. conorii israelensis in tick vectors even in the absence of naïve reservoir hosts.

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References

  • Ackerman S, Clare FB, McGill TW et al (1981) Passage of host serum components, including antibody, across the digestive tract of Dermacentor variabilis (Say). J Parasitol 67:737–740

    Article  CAS  PubMed  Google Scholar 

  • Alekseev AN, Chunikhin SP (1990) Exchange of the tick-borne encephalitis virus between Ixodidae, simultaneously feeding on the animals with subthreshold levels of viremia [Russian]. Med Parazitol Parazit Bolezn 59:48–50

    Google Scholar 

  • Alekseev AN, Chunikhin SP (1991) Virus exchange between feeding ticks in the absence of viremia in a vertebrate host (distant transmission) [Russian]. Med Parazitol Parazit Bolezn 60:50–54

    Google Scholar 

  • Alekseev AN, Chunikhin SP (1992) Differences in the distant transmission of the tick-borne encephalitis virus by ixodid ticks of two subfamilies [Russian]. Parazitologiia 26:506–515

    CAS  PubMed  Google Scholar 

  • Bacellar F, Nuncio MS, Rehacek J et al (1991) Rickettsiae and rickettsioses in Portugal. Eur J Epidemiol 7:291–293

    Article  CAS  PubMed  Google Scholar 

  • Baldridge GD, Kurtti TJ, Burkhardt N et al (2007) Infection of Ixodes scapularis ticks with Rickettsia monacensis expressing green fluorescent protein: a model system. J Invertebr Pathol 94:163–174

    Article  CAS  PubMed  Google Scholar 

  • Ben-Yakir D (1989) Quantitative studies of host immunoglobulin G in the hemolymph of ticks (Acari). J Med Entomol 26:243–246

    CAS  PubMed  Google Scholar 

  • Ben-Yakir D, Fox CJ, Homer JT et al (1987) Quantification of host immunoglobulin in the hemolymph of ticks. J Parasitol 73:669–671

    Article  CAS  PubMed  Google Scholar 

  • Bernasconi MV, Casati S, Peter O et al (2002) Rhipicephalus ticks infected with Rickettsia and Coxiella in Southern Switzerland (Canton Ticino). Infect Genet Evol 2:111–120

    Article  CAS  PubMed  Google Scholar 

  • Blanc G, Caminopetros J (1932) Epidemiological and experimental studies on Boutonneuse fever done at the Pasteur Institute in Athens. Arch Inst Pasteur Tunis 20:343–394

    Google Scholar 

  • Brossard M, Rais O (1984) Passage of hemo lysins through the mid gut epithelium of female Ixodes ricinus fed on rabbits infested or reinfested with ticks. Experientia 40:561–563

    Article  CAS  PubMed  Google Scholar 

  • Chinzei Y, Minoura H (1987) Host immunoglobulin G titre and antibody activity in haemolymph of the tick, Ornithodoros moubata. Med Vet Entomol 1:409–416

    Article  CAS  PubMed  Google Scholar 

  • Chunikhin SP (1990) Experimental research on the ecology of the tick-borne encephalitis virus [Russian]. Vopr Virusol 35:183–188

    CAS  PubMed  Google Scholar 

  • de Silva AM, Telford SR III, Brunet LR et al (1996) Borrelia burgdorferi OspA is an arthropod-specific transmission- blocking Lyme disease vaccine. J Exp Med 183:271–275

    Article  PubMed  Google Scholar 

  • Eremeeva ME, Dasch GA, Silverman DJ (2003) Evaluation of a PCR assay for quantitation of Rickettsia rickettsii and closely related spotted fever group rickettsiae. J Clin Microbiol 41:5466–5472

    Article  CAS  PubMed  Google Scholar 

  • Fikrig E, Telford SR 3d, Barthold SW et al (1992) Elimination of Borrelia burgdorferi from vector ticks feeding on OspA-immunized mice. Proc Natl Acad Sci USA 89:5418–5421

    Article  CAS  PubMed  Google Scholar 

  • Fujisaki K, Kamio T, Kitaoka S (1984) Passage of host serum components, including antibodies specific for Theileria sergenti, across the digestive tract of argasid and ixodid ticks. Ann Trop Med Parasitol 78:449–450

    CAS  PubMed  Google Scholar 

  • Gern L, Rais O (1996) Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). J Med Entomol 33:189–192

    CAS  PubMed  Google Scholar 

  • Giammanco GM, Mansueto S, Ammatuna P et al (2003) Israeli spotted fever Rickettsia in sicilian Rhipicephalus sanguineus ticks. Emerg Infect Dis 9:892–893

    PubMed  Google Scholar 

  • Jain SK, Khan JA, Mittal V et al (2008) Indian tick typhus mimicking as rocky mountain spotted fever: a case report. J Commun Dis 40:83–85

    CAS  PubMed  Google Scholar 

  • Jones LD, Davies CR, Steele GM et al (1987) A novel mode of arbovirus transmission involving a nonviremic host. Science 237:775–777

    Article  CAS  PubMed  Google Scholar 

  • Jones LD, Davies CR, Williams T et al (1990) Non-viraemic transmission of Thogoto virus: vector efficiency of Rhipicephalus appendiculatus and Amblyomma variegatum. Trans R Soc Trop Med Hyg 84:846–848

    Article  CAS  PubMed  Google Scholar 

  • Jones LD, Gaunt M, Hails RS et al (1997) Transmission of Louping ill virus between infected and uninfected ticks co-feeding on mountain hares. Med Vet Entomol 11:172–176

    Article  CAS  PubMed  Google Scholar 

  • Kocan KA, de la Fuente J (2003) Co-feeding studies of ticks infected with Anaplasma marginale. Vet Parasitol 112:295–305

    Article  PubMed  Google Scholar 

  • Labuda M, Jones LD, Williams T et al (1993a) Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. J Med Entomol 30:295–299

    CAS  PubMed  Google Scholar 

  • Labuda M, Nuttall PA, Kozuch O et al (1993b) Non-viraemic transmission of tick-borne encephalitis virus: a mechanism for arbovirus survival in nature. Experientia 49:802–805

    Article  CAS  PubMed  Google Scholar 

  • Lennette EH, Lennette DA, Lennette ET (1995) Diagnostic procedures for viral, rickettsial, and chlamydial infections. American Public Health Association, Washington, DC, 633 pp

  • Levin ML, Fish D (2000) Immunity reduces reservoir host competence of Peromyscus leucopus for Ehrlichia phagocytophila. Infect Immun 68:1514–1518

    Article  CAS  PubMed  Google Scholar 

  • Levin ML, Killmaster LF, Zemtsova G et al (2009) Incongruent effects of two isolates of Rickettsia conorii on the survival of Rhipicephalus sanguineus ticks. Exp Appl Acarol 48:347–359

    Article  Google Scholar 

  • Matsumoto K, Ogawa M, Brouqui P et al (2005) Transmission of Rickettsia massiliae in the tick, Rhipicephalus turanicus. Med Vet Entomol 19:263–270

    Article  CAS  PubMed  Google Scholar 

  • Mbogo SK, Osir EO, Mongi AO (1992) Host immunoglobulin G in the haemolymph of the brown ear tick, Rhipicephalus appendiculatus (Neumann, 1901). Insect Sci Appl 13:481–485

    CAS  Google Scholar 

  • Mumcuoglu KY, Keysary A, Gilead L (2002) Mediterranean spotted fever in Israel: a tick-borne disease. IMAJ 4:44–49

    PubMed  Google Scholar 

  • Neitz WO, Alexander RA, Mason JH (1941) The transmission of tick-bite fever by the dog tick Rhipicephalus sanguineus. Onderstepoort J Vet Sci Anim Indust 16:9–17

    Google Scholar 

  • Ogden NH, Nuttall PA, Randolph SE (1997) Natural Lyme disease cycles maintained via sheep by cofeeding ticks. Parasitology 115:591–599

    Article  PubMed  Google Scholar 

  • Peter O, Burgdorfer W, Aeschlimann A et al (1984) Rickettsia conorii isolated from Rhipicephalus sanguineus introduced into Switzerland on a pet dog. Z Parasit 70:265–270

    Article  CAS  Google Scholar 

  • Péter O, Raoult D, Gilot B (1990) Isolation by a sensitive centrifugation cell culture system of 52 strains of spotted fever group rickettsiae from ticks collected in France. J Clin Microbiol 28:1597–1599

    PubMed  Google Scholar 

  • Piesman J, Happ CM (2001) The efficacy of co-feeding as a means of maintaining Borrelia burgdorferi: a North American model system. J Vector Ecol 26:216–220

    CAS  PubMed  Google Scholar 

  • Psaroulaki A, Loukaidis F, Hadjichristodoulou C et al (1999) Detection and identification of the aetiological agent of Mediterranean spotted fever (MSF) in two genera of ticks in Cyprus. Trans R Soc Trop Med Hyg 93:597–598

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Raoult D, Tissot Dupont H, Caraco P et al (1992) Mediterranean spotted fever in Marseille: descriptive epidemiology and the influence of climatic factors. Eur J Epidemiol 8:192–197

    Article  CAS  PubMed  Google Scholar 

  • Richter D, Allgower R, Matuschka FR (2002) Co-feeding transmission and its contribution to the perpetuation of the Lyme disease spirochete Borrelia afzelii. Emerg Infect Dis 8:1421–1425

    Article  PubMed  Google Scholar 

  • Schwartz I, Varde S, Nadelman RB et al (1997) Inhibition of efficient polymerase chain reaction amplification of Borrelia burgdorferi DNA in blood-fed ticks. Am J Trop Med Hyg 56:339–342

    CAS  PubMed  Google Scholar 

  • Socolovschi C, Bitam I, Raoult D et al (2009) Transmission of Rickettsia conorii in naturally infected Rhipicephalus sanguineus. Clin Microbiol Infect 15:319–321

    Article  PubMed  Google Scholar 

  • Tarasevich IV, Mediannikov OY (2006) Rickettsial diseases in Russia. Ann NY Acad Sci 1078:48–59

    Article  CAS  PubMed  Google Scholar 

  • Tringali G, Intonazzo V, Perna AM et al (1986) Epidemiology of boutonneuse fever in western Sicily. Distribution and prevalence of spotted fever group rickettsial infection in dog ticks (Rhipicephalus sanguineus). Am J Epidemiol 123:721–727

    CAS  PubMed  Google Scholar 

  • Troughton DR, Levin ML (2007) Life cycles of seven ixodid tick species (Acari: Ixodidae) under standardized laboratory conditions. J Med Entomol 44:732–740

    Article  PubMed  Google Scholar 

  • Zhu Y, Fournier PE, Eremeeva M et al (2005) Proposal to create subspecies of Rickettsia conorii based on multi-locus sequence typing and an emended description of Rickettsia conorii. BMC Microbiol 5:1–11

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Davidia N. Grant and Maria L. Zambrano for their invaluable help with handling live ticks and robotic equipment. We gratefully acknowledge Dr. Sandor E. Karpathy, Dr. Marina Eremeeva, and Dr. Gregory Dasch for their contributions to this study.

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Correspondence to M. L. Levin.

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The findings and conclusions described in this manuscript are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention and the Department of Health and Human Services.

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Zemtsova, G., Killmaster, L.F., Mumcuoglu, K.Y. et al. Co-feeding as a route for transmission of Rickettsia conorii israelensis between Rhipicephalus sanguineus ticks. Exp Appl Acarol 52, 383–392 (2010). https://doi.org/10.1007/s10493-010-9375-7

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  • DOI: https://doi.org/10.1007/s10493-010-9375-7

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