Evaluation of host-targeted applications of permethrin for control of Borrelia-infected Ixodes ricinus (Acari: Ixodidae).
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Biomedical subjects
T N Mather
Publications and source records attributed to T N Mather.
Hemocytic rickettsia-like organisms in ticks: serologic reactivity with antisera to Ehrlichiae and detection of DNA of agent of human granulocytic ehrlichiosis by PCR.
Ixodid ticks were collected from Connecticut, Massachusetts, Missouri, Pennsylvania, Rhode Island, and British Columbia (Canada) during 1991 to 1994 to determine the prevalence of infection with hemocytic (blood cell), rickettsia-like organisms. Hemolymph obtained from these ticks was analyzed by direct and indirect fluorescent antibody (FA) staining methods with dog, horse, or human sera containing antibodies to Ehrlichia canis, Ehrlichia equi, or Rickettsia rickettsii. Of the 693 nymphal and adult Amblyomma americanum, Dermacentor variabilis, Ixodes scapularis, and Ixodes pacificus ticks tested with dog anti-E. canis antiserum, 209 (32.5%) contained hemocytic bacteria. The prevalence of infected ticks varied greatly with species and locale. In parallel tests of duplicate hemolymph preparations from adult I. scapularis ticks, the hemocytic organisms reacted positively with E. canis and/or E. equi antisera, including sera from persons who had granulocytic ehrlichiosis. In separate PCR analyses, DNA of the agent of human granulocytic ehrlichiosis was detected in 59 (50.0%) of 118 adult and in 1 of 2 nymphal I. scapularis ticks tested from Connecticut. There was no evidence of Ehrlichia chaffeensis DNA in these ticks. In indirect FA tests of hemolymph for spotted fever group rickettsiae, the overall prevalence of infection was less than 4%. Specificity tests of antigens and antisera used in these studies revealed no cross-reactivity between E. canis and E. equi or between any of the ehrlichial reagents and those of R. rickettsii. The geographic distribution of hemocytic microorganisms with shared antigens to Ehrlichia species or spotted fever group rickettsiae is widespread.
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Competence of dogs as reservoirs for Lyme disease spirochetes (Borrelia burgdorferi).
Dogs become infected with Borrelia burgdorferi after being bitten by infected adult ticks. However, it is not known whether dogs are competent reservoirs of the organism, that is, it is not known whether infected dogs can subsequently transmit the bacterium to feeding immature ticks. To determine reservoir competence of dogs, 11 Beagles were experimentally infected by means of challenge exposure to infected adult deer ticks (Ixodes scapularis). Three weeks later, larval ticks were allowed to feed on the dogs. Engorged larvae were collected, allowed to molt to the nymph stage, and tested, by means of a direct fluorescent antibody assay, to detect the presence of B burgdorferi organisms. Overall, 78% of immature ticks tested were found to have become infected. We concluded that dogs might serve to increase human risk of exposure to B burgdorferi-infected ticks and, therefore, should be protected from exposure to infected ticks as well as immature ticks seeking a blood meal.
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Isolation of Borrelia burgdorferi from saliva of the tick vector, Ixodes scapularis.
A method for cultivating and isolating Lyme disease spirochetes, Borrelia burgdorferi, from the saliva of vector ticks, Ixodes scapularis (formerly known as Ixodes dammini), is described. Saliva was collected from partially engorged ticks after application of pilocarpine to induce salivation. B. burgdorferi was isolated from 8 of 14 (57%) of the saliva samples derived from ticks infected with the bacteria, as determined by direct immunofluorescent-antibody assay of tick hemolymph. A comparison of the protein profiles of the salivary isolates and a highly passaged strain (B31) showed that the salivary isolates all lacked a 22-kDa protein known to increase with continuous passage, but exhibited larger amounts of the OspA and OspB proteins than did the highly passaged B31 strain.
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Occurrence and distribution in Rhode Island of Hunterellus hookeri (Hymenoptera: Encyrtidae), a wasp parasitoid of Ixodes dammini.
The wasp Hunterellus hookeri Howard parasitizes several species of ixodid ticks including Ixodes dammini Spielman, Clifford, Piesman & Corwin, the vector of Lyme disease spirochetes, Borrelia burgdorferi, in the northeastern United States. We detected the occurrence and evaluated the distribution of this wasp parasitoid in populations of I. dammini in Rhode Island. There has been no intentional introduction of a tick parasitoid recorded anywhere in Rhode Island; yet, we found this wasp at one of the six study sites (Prudence Island), where it parasitized 21 (n = 243) and 17% (n = 284) of nymphal I. dammini collected during 1988 and 1989, respectively. The proportion of nymphs parasitized was greatest during May (46%) and was less in June (18%), July (18%), and August (11%). In Rhode Island, the wasp was only found parasitizing ticks at the site with the highest (by a factor of 2) tick population, confirming similar observations in Massachusetts and New York. It is suggested that establishment as well as the distribution of H. hookeri depends upon a super abundant deer tick population. The usefulness of this parasitoid as a biological control agent is yet unknown.
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An unexpected result from burning vegetation to reduce Lyme disease transmission risks.
The risk for human infection with Lyme disease appears linked to the abundance of infected vector ticks, principally Ixodes dammini Spielman, Clifford, Piesman & Corwin, in the eastern United States. Habitat destruction by burning, although not well studied, has long been considered as an effective alternative to synthetic insecticides as a means of reducing tick populations. We evaluated the effect of a single spring burning of the woodland understory on the transmission risk of Lyme disease spirochetes (Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt & Brenner) on Shelter Island, Long Island, NY. Following a burn in early April 1991, the abundance of nymphal I. dammini was 49% lower in the burned portion of a woodlot compared with the unburned portion. However, risk of encountering nymphs infected with B. burgdorferi remained similar in both burned and unburned woods. It is suggested that burning vegetation may disproportionately kill deer-derived rather than rodent-derived nymphs, significantly reducing tick abundance without affecting transmission risk.
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Seasonal variation in the capacity of the bank vole to infect larval ticks (Acari: Ixodidae) with the Lyme disease spirochete, Borrelia burgdorferi.
Seasonal variation in the capacity of bank voles, Clethrionomys glareolus (Schreber), to infect larval Ixodes ricinus (L.) ticks with Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt & Brenner was examined from May through October 1991 at Bogesund, near Stockholm in south-central Sweden. Although larval infestations of bank voles were greatest in June and July, nearly 70% of all larval ticks infected with spirochetes by bank voles at this site became infected during August and September. Seasonality of infectivity was related to the degree of earlier nymphal infestation on voles as well as to the age composition of the vole population. These factors may influence the infectivity of other rodent reservoirs of B. burgdorferi, both in Europe and North America. Moreover, in determining the reservoir potential of tick hosts, a host population's spirochetal infectivity should be determined for the entire period of larval infestation rather than just during the period of peak larval infestation.
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Absence of transplacental transmission of Lyme disease spirochetes from reservoir mice (Peromyscus leucopus) to their offspring.
Lyme disease spirochetes (Borrelia burgdorferi) are naturally maintained in an enzootic cycle mainly by vector ticks (Ixodes dammini) infesting white-footed mice (Peromyscus leucopus). Suggestions that mice may become infected without exposure to ticks prompted a study to evaluate whether mice could transmit spirochetes transplacentally to their offspring. Mice were live-captured in two Massachusetts sites where Lyme disease spirochetes are intensely enzootic. Pregnant females were housed separately in the laboratory through delivery, and mothers and their offspring were caged together until weaning. Each female and two offspring were then examined for evidence of infection serologically and by tick xenodiagnosis. All 14 mother mice examined produced infected ticks and exhibited serum antibodies to B. burgdorferi. However, none of 28 offspring tested produced infected ticks and only a few had evidence of circulating antibody. In a separate experiment, no young CD-1 mice, born of infected mothers, had IgM antibody to B. burgdorferi. It would appear that immature mice are not transplacentally infected with spirochetes and must be exposed to infected ticks before becoming infected and infective themselves.
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Methods for control of tick vectors of Lyme borreliosis.
During the IVth International Conference on Lyme Borreliosis in Stockholm, 1990, a workshop on control of Lyme disease vectors briefly reviewed: basic ecological principles for tick control; biocontrol of ticks; chemical control, including the use of repellents and use of permethrin-treated rodent nest material; tick control by habitat modification; and reduction of tick host availability. It was concluded that, although much research work remains, Lyme borreliosis is to a large extent a preventable infection. Avoidance of heavily tick-infested areas, personal protection using proper clothing, and prompt removal of attached ticks remain the most effective protective measures. Many other prophylactic measures are available and could be efficiently integrated into schemes to reduce the abundance of vectors. However, since the ecology of the infection varies greatly between different localities it may be necessary to apply different combinations of control methods in different endemic regions.
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Borrelia burgdorferi and Babesia microti: efficiency of transmission from reservoirs to vector ticks (Ixodes dammini).
In endemic regions, Peromyscus leucopus, the mouse reservoir of the Lyme disease spirochete (Borrelia burgdorferi) and the piroplasm causing human babesiosis (Babesia microti), is nearly universally infected with both agents. Paradoxically, spirochetal infection is nearly twice as prevalent as is babesial infection in populations of field-collected nymphal Ixodes dammini, the tick vector. In the laboratory, a similarly disproportionate rate of infection was observed among nymphal ticks, feeding as larvae, on either B. burgdorferi- or B. microti-infected mice. Ticks which fed on mice with concurrent spirochetal and babesial infections also exhibited twice the incidence of spirochetal infection over that of the piroplasm. These data suggest that the efficiency of acquisition and transstadial passage of B. burgdorferi and B. microti infection differ by a factor of two. This discrepancy may explain differences observed both in the prevalence of infection in ticks collected in the field, as well as the apparently greater risk of spirochetal infection to humans in endemic areas.
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Intrinsic competence of three ixodid ticks (Acari) as vectors of the Lyme disease spirochete.
We compared the intrinsic vector competence of Ixodes dammini Spielman et al., Dermacentor variabilis (Say), and Amblyomma americanum (L.) for the Lyme disease spirochete (Borrelia burgdorferi Johnson et al.) on Prudence Island, Rhode Island, a Lyme disease-endemic site where all three ticks occur together. Natural and experimental spirochete infection rates were determined in those ticks and their degree of contact with white-footed mice (Peromyscus leucopus), the principal reservoir host, was compared. Host-seeking nymphal and adult I. dammini and A. americanum, collected by flagging, were nearly equally abundant, as were adult D. variabilis, but only I. dammini were infected with B. burgdorferi. Larvae and nymphs of both I. dammini and D. variabilis were found infesting mice, but A. americanum never were found on this host. Furthermore, although larvae of all three tick species became infected by ingesting spirochetes while feeding on experimentally infected mice, only I. dammini remained infected following the transstadial molt. These findings suggest that of these three tick species, only I. dammini is competent as a vector of the Lyme disease spirochete.
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Short-tailed shrews as reservoirs of the agents of Lyme disease and human babesiosis.
To determine whether short-tailed shrews (Blarina brevicauda) serve as reservoir hosts for the Lyme disease spirochete (Borrelia burgdorferi) and the agent of human babesiosis (Babesia microti), we examined nymphal ticks that had fed as larvae on shrews collected from 3 enzootic sites in coastal Massachusetts for evidence of infection by either or both of these agents. Xenodiagnosis indicated that 11 of 14 shrews were infected by B. burgdorferi. One of 3 piroplasm-infected shrews also infected ticks with B. microti. In a site where the piroplasm is endemic, 11 of 17 shrews showed patent parasitemias by thin blood smears. Of these, 4 had parasitemias exceeding 40%. Few immature ticks infested shrews, however, suggesting that B. brevicauda, although abundant in some endemic sites and serving as a competent reservoir, would contribute minimally to the population of infected nymphs.
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Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi).
The authors compared the contribution of white-footed mice (Peromyscus leucopus), chipmunks (Tamias striatus), and meadow voles (Microtus pennsylvanicus) to infection of vector ticks with the Lyme disease spirochete, Borrelia burgddorferi. At one Massachusetts location where Lyme disease is endemic, all three species of rodents were found to be infected. Prevalence of infection, however, varied from 90% for mice, and 75% for chipmunks to just 5.5% for meadow voles. Infectivity of these hosts for larval Ixodes dammini also varied, but mice were found to be the most infective, followed by chipmunks and meadow voles. Density estimates of these three hosts, collected between 1981 and 1986 in three coastal Massachusetts locations, revealed that mice were more abundant than the other two rodents in areas in which ticks were abundant. In addition, mice were infested more abundantly with larval I. dammini than the other two host species. Integrating these results, we determined each species' "reservoir potential," a novel term which describes the relative contribution made by a host species to the horizontal infection of a vector population. The authors' findings demonstrate that, at least in coastal Massachusetts, P. leucopus is the most important small mammal reservoir for B. burgdorferi.
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Incompetence of catbirds as reservoirs for the Lyme disease spirochete (Borrelia burgdorferi).
We compared the relative infectivity to vector ticks of gray catbirds (Dumetella carolinensis) and white-footed mice (Peromyscus leucopus) for the Lyme disease spirochete (Borrelia burgdorferi). Of 28 catbirds captured in a site enzootic for this agent, 18 were infested by immature Ixodes dammini, the tick vector. By comparison, each of 32 mice sampled concurrently from the same site was infested, and by about 10 times as many ticks as were found infesting the 3 most commonly netted bird species. Although 76% of noninfected larval ticks placed on these mice in a xenodiagnosis became infected, none of the ticks similarly placed on 12 catbirds did so. Spirochetes were detected in ticks derived from 2 Carolina wrens (Thryothorus ludovicianus) and a common yellowthroat (Geothlypis trichas), but these species' potential contribution to infecting ticks does not compare with that of mice. Thus, although birds may help establish new foci of ticks, catbirds, at least, do not appear to contribute as reservoirs of infection.
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Incompetence of deer as reservoirs of the Lyme disease spirochete.
To determine whether deer may serve as reservoir hosts for the Lyme disease spirochete, we sought evidence of infection in nymphal Ixodes dammini derived from larvae that had engorged on white-tailed deer. A total of 19 deer were shot in two Lyme disease foci in Massachusetts during September 1986, the season in which larvae were most abundant. An average of 342 larval ticks of this species were collected from each deer. Of those that developed to the nymphal stage, the gut contents of 185 were examined for Borrelia burgdorferi by a direct fluorescent antibody test. Spirochetes were detected in about 1% of these nymphs, a rate of infection attributable to transovarial transmission. In contrast, infection was detected in 23% of 39 field-swept nymphal ticks of the same cohort that were collected during the following season. Although deer may be infested by numerous larval I. dammini, such ticks appear not to become infected by Lyme disease spirochetes.
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Dissemination and salivary delivery of Lyme disease spirochetes in vector ticks (Acari: Ixodidae).
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Seasonal variation of transmission risk of Lyme disease and human babesiosis.
The seasonal host-seeking pattern of nymphal Ixodes dammini infected with Babesia microti or Borrelia burgdorferi was determined on Nantucket Island, Massachusetts, during 1985. The peak period of host-seeking by infected nymphal I. dammini occurred in May and June. On a per person-hour basis, the number of infected ticks collected reached a maximum in May (Babesia = 17.3; Borrelia = 16.2). The number of infected ticks remained high in June, but decreased notably in July, August, and September. Transmission risk of the tick-borne etiologic agents of Lyme disease and human babesiosis in Massachusetts is greatest during the late spring-early summer months of May and June.
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Absence of spirochaetes (Borrelia burgdorferi) and piroplasms (Babesia microti) in deer ticks (Ixodes dammini) parasitized by chalcid wasps (Hunterellus hookeri).
An entomophagous wasp (Hunterellus hookeri Howard) parasitizes about a third of the host-seeking nymphal Ixodes dammini Spielman et al. ticks on Naushon Island in Massachusetts (U.S.A.) where the agents of Lyme disease (Borrelia burgdorferi Johnson et al.) and human babesiosis (Babesia microti Franca) are enzootic. Following blood-feeding, wasp-parasitized ticks are destroyed by the developing wasp. The prevalence of either human pathogen in host-seeking ticks collected in wasp-infested sites is nearly 40% lower than that found in other sites. Nymphal ticks, collected early in their season of activity, are more frequently parasitized by the wasp and less frequently by the Lyme disease spirochaete than those collected later in the summer. Spirochaetes never infected wasp-infected ticks, and few wasp-infected ticks were concurrently infected by the Babesia piroplasm. Taken together, these correlations indicate that the wasp may render the tick inhospitable to both pathogens. The presence of the wasp may have reduced risk of human infection on the island by either pathogen by as much as a third.
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