Early-phase Transmission of Yersinia pestis by Cat Fleas (Ctenocephalides felis) and Their Potential Role as Vectors in a Plague-endemic Region of Uganda

Rebecca J. Eisen Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Jeff N. Borchert Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Jennifer L. Holmes Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Gerald Amatre Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Kristen Van Wyk Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Russell E. Enscore Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Nackson Babi Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Linda A. Atiku Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Aryn P. Wilder Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Sara M. Vetter Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Scott W. Bearden Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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John A. Montenieri Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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Kenneth L. Gage Bacterial Diseases Branch, Division of Vector Borne Infectious Diseases, National Center for Zoonotic, Enteric and Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe Uganda

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In recent decades, the majority of human plague cases (caused by Yersinia pestis) have been reported from Africa. In northwest Uganda, which has had recent plague outbreaks, cat fleas (Ctenocephalides felis) have been reported as the most common fleas in the home environment, which is suspected to be a major exposure site for human plague in this country. In the past, C. felis has been viewed as only a nuisance-biting insect because limited laboratory studies suggested it is incapable of transmitting Y. pestis or is an inefficient vector. Our laboratory study shows that C. felis is a competent vector of plague bacteria, but that efficiency is low compared with another flea species collected in the same area: the oriental rat flea, Xenopsylla cheopis. On the other hand, despite its low vector efficiency, C. felis is the most common flea in human habitations in a plague-endemic region of Uganda (Arua and Nebbi Districts), and occasionally infests potential rodent reservoirs of Y. pestis such as the roof rat (Rattus rattus) or the Nile rat (Arvicanthis niloticus). Plague control programs in this region should remain focused on reducing rat flea populations, although our findings imply that cat fleas should not be ignored by these programs as they could play a significant role as secondary vectors.

  • 1

    Pollitzer R, 1954. Plague. World Health Organization Monograph Series No. 22. Geneva, Switzerland: World Health Organization.

  • 2

    Gage KL, Kosoy MY, 2005. Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50 :505–528.

  • 3

    Hinnebusch BJ, 2005. The evolution of flea-borne transmission in Yersinia pestis.Curr Issues Mol Biol 7 :197–212.

  • 4

    Eskey CR, Haas VH, 1940. Plague in the western part of the United States. Publ Hlth Bull 254 :1–83.

  • 5

    WHO, 2004. Human plague in 2002 and 2003. Wkly Epidemiol Rec 79 :301–308.

  • 6

    WHO, 2005. Outbreak news index 2005. Wkly Epidemiol Rec 80 :433–440.

  • 7

    Hopkins GHE, 1949. Report on rats, fleas and plague in Uganda: East African Standard, Ltd., 52.

  • 8

    Kilonzo BS, Makundi RH, Mbise TJ, 1992. A decade of plague epidemiology and control in the western Usambara mountains, north-east Tanzania. Acta Trop 50 :323–329.

    • Search Google Scholar
    • Export Citation
  • 9

    Dryden MW, Rust MK, 1994. The cat flea: biology, ecology and control. Vet Parasitol 52 :1–19.

  • 10

    Kwochka KW, 1987. Fleas and related disease. Veterinary Clinics of North America. Small Animal Practice 17 :1235–1262.

  • 11

    Verjbitski DT, 1908. The part played by insects in the epidemiology of plague. J Hyg (Lond) 8 :162–208.

  • 12

    Bacot AW, Martin CJ, 1914. Observations on the mechanism of the transmission of plague by fleas. J Hyg (Lond) 13 (Plague Suppl. III):423–439.

    • Search Google Scholar
    • Export Citation
  • 13

    Burroughs AL, 1947. Sylvatic plague studies: the vector efficiency of nine species of fleas compared with Xenopsylla cheopis.J Hyg (Lond) 43 :371–396.

    • Search Google Scholar
    • Export Citation
  • 14

    Eisen RJ, Wilder AP, Bearden SW, Montenieri JA, Gage KL, 2007. Early-phase transmission of Yersinia pestis by unblocked Xenopsylla cheopis (Siphonaptera: pulicidae) is as efficient as transmission by blocked fleas. J Med Entomol 44 :678–682.

    • Search Google Scholar
    • Export Citation
  • 15

    Engelthaler DM, Hinnebusch BJ, Rittner CM, Gage KL, 2000. Quantitative competitive PCR as a technique for exploring flea-Yersina pestis dynamics. Am J Trop Med Hyg 62 :552–560.

    • Search Google Scholar
    • Export Citation
  • 16

    Laudisoit A, Leirs H, Makundi RH, Van Dongen S, Davis S, Neerinckx S, Deckers J, Libois R, 2007. Plague and the human flea, Tanzania. Emerg Infect Dis 13 :687–693.

    • Search Google Scholar
    • Export Citation
  • 17

    Hopkins GHE, 1947. Annotated and illustrated keys to the known fleas of East Africa. Ugandan Journal 11 :133–191.

  • 18

    Wheeler CM, Douglas JR, 1945. Sylvatic plague studies. V. The determination of vector efficiency. J Inf Dis 77 :1–12.

  • 19

    Devignat R, 1946. Aspects de l’epidemiologie de al peste au Lac Albert. Ann Soc Belg Med Trop 26 :13–54.

  • 20

    Herms WB, 1953. Medical Entomology. New York: MacMillan.

  • 21

    Hirst LF, 1953. The Conquest of Plague. Oxford: Claredon Press.

  • 22

    Eisen RJ, Bearden SW, Wilder AP, Montenieri JA, Antolin MF, Gage KL, 2006. Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc Natl Acad Sci USA 103 :15380–15385.

    • Search Google Scholar
    • Export Citation
  • 23

    Fine PEM, 1981. Epidemiological principles of vector-mediated transmission. McKelvey JJ, Eldridge BF, Maramorosch K, eds. Vectors of Disease Agents: Interactions with Plants, Animals, and Man. New York: Praeger Publishers.

  • 24

    Garrett-Jones C, Schidrawi GR, 1969. Malaria vectorial capacity of a population of Anopheles gambiae: an exercise in epidemiological entomology. Bull World Health Organ 40 :531–545.

    • Search Google Scholar
    • Export Citation
  • 25

    Lorange EA, Race BL, Sebbane F, Hinnebusch BJ, 2005. Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis.J Infect Dis 191 :1907–1912.

    • Search Google Scholar
    • Export Citation
  • 26

    Macdonald G, 1961. Epidemiologic models in studies of vector-borne diseases. Public Health Rep 76 :753–764.

  • 27

    Delany MJ, 1975. The Rodents of Uganda. Kettering Northamptonshire: The George Press.

  • 28

    Haselbarth E, 1966. Siphonaptera. Zumpt F, ed. The Arthropod Parasites of Vertebrates in Africa South of the Sahara (Ethiopia Region). Johannesburg: South African Institute of Medical Research, 117–212.

  • 29

    Smit FGAM, 1973. Siphonaptera (Fleas). Smith KGV, ed. Insects and Other Arthropods of Medical Importance. London: British Museum of Natural History, 325–371.

  • 30

    Chu MC, 2000. Laboratory Manual of Plague Diagnostics. Geneva: Centers for Disease Control and Prevention and World Health Organization, 129.

  • 31

    Kilonzo BS, 1977. A simple light trap for field collections of adult fleas: studies on its efficiency and suitability in north-east Tanzania. WHO/VBC/77.673, 11.

  • 32

    Eisen RJ, Lowell JL, Montenieri JA, Bearden SW, Gage KL, 2007. Temporal dynamics of early-phase transmission of Yersinia pestis by unblocked fleas: secondary infectious feeds prolong efficient transmission by Oropsylla montana (Siphonaptera: Ceratophyllidae). J Med Entomol 44 :672–677.

    • Search Google Scholar
    • Export Citation
  • 33

    Wilder AP, Eisen RJ, Bearden SW, Montenieri JA, Gage KL, Antolin MF, 2008. Oropsylla hirsuta (Siphonaptera: Ceratophyllidae) can support plague epizootics in black-tailed prairie dogs (Cynomys ludovicianus) by early-phase transmission of Yersinia pestis. Vector Borne Zoonotic Dis.

  • 34

    Wilder AP, Eisen RJ, Bearden SW, Montenieri JA, Tripp DT, Brinkerhoff RJ, Gage KL, Antolin MF, 2008. Transmission efficiency of two flea species (Oropsylla tuberculata cynomuris and Oropsylla hirsuta) involved in plague epizootics among prairie dogs. EcoHealth.

  • 35

    Davis DH, 1953. Plague in Africa from 1935 to 1949; a survey of wild rodents in African territories. Bull WHO 9 :665–700.

  • 36

    Drancourt M, Houhamdi L, Raoult D, 2006. Yersinia pestis as a telluric, human ectoparasite-borne organism. Lancet Infect Dis 6 :234–241.

    • Search Google Scholar
    • Export Citation
  • 37

    Hopla CE, 1980. A study of the host associations and zoogeography of Pulex. Traub R, Starcke H, eds. Fleas. Rotterdam: A.A. Balkema, 185–207.

  • 38

    Hunter KW Jr, Campbell AR, Sayles PC, 1979. Human infestation by cat fleas, Ctenocephalides felis (Siphonaptera: Pulicidae), from suburban raccoons. J Med Entomol 16 :547.

    • Search Google Scholar
    • Export Citation
  • 39

    Beati L, Humair PF, Aeschlimann A, Raoult D, 1994. Identification of spotted fever group rickettsiae isolated from Dermacentor marginatus and Ixodes ricinus ticks collected in Switzerland. Am J Trop Med Hyg 51 :138–148.

    • Search Google Scholar
    • Export Citation
  • 40

    Kent RJ, Thuma PE, Mharakurwa S, Norris DE, 2007. Seasonality, blood feeding behavior, and transmission of Plasmodium falciparum by Anopheles arabiensis after an extended drought in southern Zambia. Am J Trop Med Hyg 76 :267–274.

    • Search Google Scholar
    • Export Citation
  • 41

    Kirstein F, Gray JS, 1996. A molecular marker for the identification of the zoonotic reservoirs of Lyme borreliosis by analysis of the blood meal in its European vector Ixodes ricinus.Appl Environ Microbiol 62 :4060–4065.

    • Search Google Scholar
    • Export Citation
  • 42

    Moran Cadenas F, Rais O, Humair PF, Douet V, Moret J, Gern L, 2007. Identification of host bloodmeal source and Borrelia burgdorferi sensu lato in field-collected Ixodes ricinus ticks in Chaumont (Switzerland). J Med Entomol 44 :1109–1117.

    • Search Google Scholar
    • Export Citation
  • 43

    Pichon B, Egan D, Rogers M, Gray J, 2003. Detection and identification of pathogens and host DNA in unfed host-seeking Ixodes ricinus L. (Acari: Ixodidae). J Med Entomol 40 :723–731.

    • Search Google Scholar
    • Export Citation
  • 44

    Pichon B, Rogers M, Egan D, Gray J, 2005. Blood-meal analysis for the identification of reservoir hosts of tick-borne pathogens in Ireland. Vector Borne Zoonotic Dis 5 :172–180.

    • Search Google Scholar
    • Export Citation
  • 45

    Vobis M, D’Haese J, Mehlhorn H, Mencke N, Blagburn BL, Bond R, Denholm I, Dryden MW, Payne P, Rust MK, Schroeder I, Vaughn MB, Bledsoe D, 2004. Molecular phylogeny of isolates of Ctenocephalides felis and related species based on analysis of ITS1, ITS2 and mitochondrial 16S rDNA sequences and random binding primers. Parasitol Res 94 :219–226.

    • Search Google Scholar
    • Export Citation
  • 46

    Krasnov BR, Shenbrot GI, Mouillot D, Khokhlova IS, Poulin R, 2006. Ecological characteristics of flea species relate to their suitability as plague vectors. Oecologia 149 :474–481.

    • Search Google Scholar
    • Export Citation
  • 47

    Eisen RJ, Bearden SW, Wilder AP, Montenieri JA, Antolin MF, Gage KL, 2006. Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc Natl Acad Sci USA 103 :15380–15385.

    • Search Google Scholar
    • Export Citation
  • 48

    MMWR, 2006. Human plague-four states, 2006. MMWR 55 :1–3.

  • 49

    Poland JD, Barnes AM, 1979. Plague. Steele JH, ed. CRC Handbook Series in Zoonoses. Section A: Bacterial, rickettsial and mycotic diseases. Volume I. Boca Raton, FL: CRC Press Inc., 515–559.

  • 50

    Gratz NG, 1999. Control of Plague Transmission. Plague Manual: Epidemiology, Distribution, Surveillance and Control. Geneva: World Health Organization, 97–134.

  • 51

    Akiev AK, 1982. Epidemiology and incidence of plague in the world, 1958–79. Bull WHO 60 :165–169.

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