Experimental and Applied Acarology

, Volume 52, Issue 4, pp 383–392

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

  • G. Zemtsova
  • L. F. Killmaster
  • K. Y. Mumcuoglu
  • M. L. Levin
Article

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.

Keywords

Rickettsia conorii Rhipicephalus sanguineus Co-feeding Transstadial transmission Infection Immunity 

References

  1. 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 67:737–740CrossRefPubMedGoogle Scholar
  2. 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 59:48–50Google Scholar
  3. 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 60:50–54Google Scholar
  4. Alekseev AN, Chunikhin SP (1992) Differences in the distant transmission of the tick-borne encephalitis virus by ixodid ticks of two subfamilies [Russian]. Parazitologiia 26:506–515PubMedGoogle Scholar
  5. Bacellar F, Nuncio MS, Rehacek J et al (1991) Rickettsiae and rickettsioses in Portugal. Eur J Epidemiol 7:291–293CrossRefPubMedGoogle Scholar
  6. 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 94:163–174CrossRefPubMedGoogle Scholar
  7. Ben-Yakir D (1989) Quantitative studies of host immunoglobulin G in the hemolymph of ticks (Acari). J Med Entomol 26:243–246PubMedGoogle Scholar
  8. Ben-Yakir D, Fox CJ, Homer JT et al (1987) Quantification of host immunoglobulin in the hemolymph of ticks. J Parasitol 73:669–671CrossRefPubMedGoogle Scholar
  9. Bernasconi MV, Casati S, Peter O et al (2002) Rhipicephalus ticks infected with Rickettsia and Coxiella in Southern Switzerland (Canton Ticino). Infect Genet Evol 2:111–120CrossRefPubMedGoogle Scholar
  10. Blanc G, Caminopetros J (1932) Epidemiological and experimental studies on Boutonneuse fever done at the Pasteur Institute in Athens. Arch Inst Pasteur Tunis 20:343–394Google Scholar
  11. 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 40:561–563CrossRefPubMedGoogle Scholar
  12. Chinzei Y, Minoura H (1987) Host immunoglobulin G titre and antibody activity in haemolymph of the tick, Ornithodoros moubata. Med Vet Entomol 1:409–416CrossRefPubMedGoogle Scholar
  13. Chunikhin SP (1990) Experimental research on the ecology of the tick-borne encephalitis virus [Russian]. Vopr Virusol 35:183–188PubMedGoogle Scholar
  14. 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 183:271–275CrossRefPubMedGoogle Scholar
  15. 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 41:5466–5472CrossRefPubMedGoogle Scholar
  16. 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 89:5418–5421CrossRefPubMedGoogle Scholar
  17. 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 78:449–450PubMedGoogle Scholar
  18. Gern L, Rais O (1996) Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). J Med Entomol 33:189–192PubMedGoogle Scholar
  19. Giammanco GM, Mansueto S, Ammatuna P et al (2003) Israeli spotted fever Rickettsia in sicilian Rhipicephalus sanguineus ticks. Emerg Infect Dis 9:892–893PubMedGoogle Scholar
  20. Jain SK, Khan JA, Mittal V et al (2008) Indian tick typhus mimicking as rocky mountain spotted fever: a case report. J Commun Dis 40:83–85PubMedGoogle Scholar
  21. Jones LD, Davies CR, Steele GM et al (1987) A novel mode of arbovirus transmission involving a nonviremic host. Science 237:775–777CrossRefPubMedGoogle Scholar
  22. 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 84:846–848CrossRefPubMedGoogle Scholar
  23. 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 11:172–176CrossRefPubMedGoogle Scholar
  24. Kocan KA, de la Fuente J (2003) Co-feeding studies of ticks infected with Anaplasma marginale. Vet Parasitol 112:295–305CrossRefPubMedGoogle Scholar
  25. Labuda M, Jones LD, Williams T et al (1993a) Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. J Med Entomol 30:295–299PubMedGoogle Scholar
  26. 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 49:802–805CrossRefPubMedGoogle Scholar
  27. Lennette EH, Lennette DA, Lennette ET (1995) Diagnostic procedures for viral, rickettsial, and chlamydial infections. American Public Health Association, Washington, DC, 633 ppGoogle Scholar
  28. Levin ML, Fish D (2000) Immunity reduces reservoir host competence of Peromyscus leucopus for Ehrlichia phagocytophila. Infect Immun 68:1514–1518CrossRefPubMedGoogle Scholar
  29. 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 48:347–359CrossRefGoogle Scholar
  30. Matsumoto K, Ogawa M, Brouqui P et al (2005) Transmission of Rickettsia massiliae in the tick, Rhipicephalus turanicus. Med Vet Entomol 19:263–270CrossRefPubMedGoogle Scholar
  31. 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 13:481–485Google Scholar
  32. Mumcuoglu KY, Keysary A, Gilead L (2002) Mediterranean spotted fever in Israel: a tick-borne disease. IMAJ 4:44–49PubMedGoogle Scholar
  33. 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 16:9–17Google Scholar
  34. Ogden NH, Nuttall PA, Randolph SE (1997) Natural Lyme disease cycles maintained via sheep by cofeeding ticks. Parasitology 115:591–599CrossRefPubMedGoogle Scholar
  35. Peter O, Burgdorfer W, Aeschlimann A et al (1984) Rickettsia conorii isolated from Rhipicephalus sanguineus introduced into Switzerland on a pet dog. Z Parasit 70:265–270CrossRefGoogle Scholar
  36. 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 28:1597–1599PubMedGoogle Scholar
  37. 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 26:216–220PubMedGoogle Scholar
  38. 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 93:597–598CrossRefPubMedGoogle Scholar
  39. Randolph SE, Gern L, Nuttall PA (1996) Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitol Today 12:472–479CrossRefPubMedGoogle Scholar
  40. 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 8:192–197CrossRefPubMedGoogle Scholar
  41. 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 8:1421–1425CrossRefPubMedGoogle Scholar
  42. 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 56:339–342PubMedGoogle Scholar
  43. Socolovschi C, Bitam I, Raoult D et al (2009) Transmission of Rickettsia conorii in naturally infected Rhipicephalus sanguineus. Clin Microbiol Infect 15:319–321CrossRefPubMedGoogle Scholar
  44. Tarasevich IV, Mediannikov OY (2006) Rickettsial diseases in Russia. Ann NY Acad Sci 1078:48–59CrossRefPubMedGoogle Scholar
  45. 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 123:721–727PubMedGoogle Scholar
  46. Troughton DR, Levin ML (2007) Life cycles of seven ixodid tick species (Acari: Ixodidae) under standardized laboratory conditions. J Med Entomol 44:732–740CrossRefPubMedGoogle Scholar
  47. 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 5:1–11CrossRefGoogle Scholar

Copyright information

© U.S. Government 2010

Authors and Affiliations

  • G. Zemtsova
    • 1
  • L. F. Killmaster
    • 1
  • K. Y. Mumcuoglu
    • 2
  • M. L. Levin
    • 1
  1. 1.Rickettsial Zoonoses Branch, Mail Stop G-13, National Center for Zoonotic, Vector-Borne and Enteric DiseasesCenters for Disease Control and PreventionAtlantaUSA
  2. 2.Department of Microbiology and Molecular GeneticsThe Kuvin Center for the Study of Infectious and Tropical DiseasesJerusalemIsrael

Personalised recommendations