Prevalence of the Lyme disease spirochete in populations of white-tailed deer and white-footed mice

The prevalence of the Ixodes dammini spirochete (IDS) in white-tailed deer (Odocoileus virginianus) and white-footed mice (Peromyscus leucopus) was studied on the eastern end of Long Island, New York. Both species commonly occur in a variety of habitats, are preferred hosts of Ixodes dammini, and can harbor the spirochetes in the blood. Each animal was examined for spirochetemia, tick infestation, and IDS infection rates in the ticks that were removed from it. The results obtained suggest that in winter deer can be infected by questing adult I. dammini. Adult ticks apparently are infected through transtadial transmission of spirochetes from subadult ticks which had fed earlier in their life history on infected animals. Deer are important hosts of adult ticks and the IDS in winter and probably are a reservoir host in other seasons. The patterns of spirochete prevalence suggest that deer and mice are reservoirs of the organism and thus are fundamental to the ecology of Lyme disease on Long Island.     

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.     

The role of medium-sized mammals as reservoirs of Borrelia burgdorferi in southern New York

The ability of raccoons (Procyon lotor), striped skunks (Mephitis mephitis) and opossums (Didelphis virginiana) to serve as reservoirs of Borrelia burgdorferi, the spirochetal agent of Lyme disease, was compared with that of white-footed mice (Peromyscus leucopus). Twenty-eight (28) medium-sized mammals and 34 white-footed mice were captured in Westchester County, New York (USA) in summer 1986. Animals were caged over pans of water for 1 to 2 days to recover engorged tick larvae (Ixodes dammini) that detached from the hosts after feeding. With the exception of mice, numbers of engorged tick larvae recovered exceeded those counted during initial examinations of the hosts by 30% (opossums) to nearly 90% (raccoons). Newly-molted nymphal ticks derived from the engorged larvae were examined for the presence of spirochetes by darkfield microscopy. Percentage infection was 5% (n = 22) for ticks from skunks and 14% (n = 191) for ticks from raccoons. None of 24 nymphs from larvae that fed on opossums survived long enough for spirochete examination. By comparison, 40% (n = 72) of nymphs from larvae which fed on white-footed mice were infected. Of the individual hosts from which molted nymphs had fed as larvae, 67% of mice, 33% of skunks, and 55% of raccoons produced spirochete-positive ticks.     

Spatial and temporal dispersion of immature Ixodes dammini on Peromyscus leucopus in northwestern Illinois.

Infestation by immature Ixodes dammini and infection by Borrelia burgdorferi of the white-footed mouse Peromyscus leucopus were studied in Castle Rock State Park in northwestern Illinois during June-October 1990. Prevalence and intensity of infestation of larvae on mice were highest in August with a smaller peak in early June. The distribution of larvae on mice was highly aggregated during each of the sampling periods. Aggregation appears to be the result of a series of nonrandom successful attachments by single larvae, rather than of simultaneous attachment by clumps of larvae. Infection rate of mice by B. burgdorferi averaged 21.4% with a peak of 28.6% in August. A comparison of the numbers of attached immature ticks collected from mice and of questing ticks collected through dragging indicated that the larvae-to-nymph ratio was higher on mice than on drags. Given the low total numbers of nymphs collected from mice, this suggests a potential role for other hosts of I. dammini nymphs in northwestern Illinois.     

Vectorial capacity of North American Ixodes ticks.

Ixodes dammini, the vector of Lyme disease and babesiosis, is distributed in various locations in the northeastern quadrant of the United States and nearby Canada. The life cycle of this tick, which includes larval, nymphal, and adult stages, spans at least two years. The tick over-winters between larval and nymphal feeding. Horizontal transmission of pathogens is facilitated by a feeding pattern in which both the larval and nymphal stages feed on the white-footed mouse, Peromyscus leucopus, and by a seasonal pattern of activity in which nymphs precede larvae. The species range appears to have expanded from a single island location, and has invaded new sites since the 1940s, some as recently as 1980. This increased abundance appears to be related to the increased abundance of deer, the preferred host of the adult stage. I. muris predominated in coastal Massachusetts before I. dammini became abundant, but is probably now extinct. I. scapularis, which is present in the southern U.S., is a poor vector of mouse parasites because about 90 percent of these immature ticks feed on lizards. To the extent that horizontal transmission occurs, we suggest that mice serve as the principal reservoir for the Lyme spirochete as well as Babesia microti.     

Prevalence of Borrelia burgdorferi and Babesia microti in mice on islands inhabited by white-tailed deer.

Borrelia burgdorferi and Babesia microti were isolated from 35 of 51 white-footed mice (Peromyscus leucopus) and meadow voles (Microtus pennsylvanicus) captured on two Narragansett Bay, R.I., islands inhabited by deer, the principal host for the adult stages of the vector tick, Ixodes dammini. Immature ticks parasitized mice from both islands. From 105 mice captured on four other islands not inhabited by deer neither pathogen was isolated, nor were I. dammini found.     

Prevalence of Borrelia burgdorferi and Babesia microti in mice on islands inhabited by white-tailed deer

Borrelia burgdorferi and Babesia microti were isolated from 35 of 51 white-footed mice (Peromyscus leucopus) and meadow voles (Microtus pennsylvanicus) captured on two Narragansett Bay, R.I., islands inhabited by deer, the principal host for the adult stages of the vector tick, Ixodes dammini. Immature ticks parasitized mice from both islands. From 105 mice captured on four other islands not inhabited by deer neither pathogen was isolated, nor were I. dammini found.     

Discovery of the Lyme disease spirochete and its relation to tick vectors.

The various hypotheses concerning the etiologic agent of erythema chronicum migrans of Europe and of Lyme disease in the United States are reviewed, and an account of events that led to the discovery of the causative spirochetal agent in Ixodes dammini is presented. Spirochetes morphologically and antigenically similar, if not identical to, the organism detected in I. dammini were also found for the first time in Ixodes pacificus and Ixodes ricinus, the vectors hitherto incriminated, respectively, in western United States and Europe. In most infected ticks, spirochetal development was found to be limited to the midgut. Ticks with generalized infections were shown to transmit spirochetes via eggs, but infections decreased in intensity and became restricted to the central ganglion as filial ticks developed to adults. Although the mechanisms of transmission to a host are still under investigation, the spirochetes may be transmitted by saliva of ticks with generalized infectious and possibly also by regurgitation of infected gut contents, or even by means of infected fecal material.     

Effectiveness of Metarhizium anisopliae (Deuteromycetes) against Ixodes scapularis (Acari: Ixodidae) engorging on Peromnyscus leucopus.

With the incidence of Lyme disease increasing throughout the United States, reducing risk of exposure to the disease is of the utmost concern. In the northeastern U.S., the blacklegged tick, Ixodes scapularis, is the primary vector and the white-footed mouse, (Peromyscus leucopus), the primary reservoir for Borrelia burgdorteri, the bacterium causing Lyme disease. Targeting I. scapularis engorging on white-footed mice with an effective biological control agent, such as the fungus Metarhizium anisopliae, could be an effective and relatively safe control technique. In 2002-2003, we performed laboratory and field experiments to determine whether M anisopliae-treated nesting material could effectively control larval I. scapularis ticks engorging on white-footed mice, and therefore reduce the number of infected nymphal I. scapularis questing the following summer. Our laboratory experiment demonstrated a strong negative effect of M. anisopliae-treated nesting material on survival of I. scapularis larvae feeding on P. leucopus, with 75% versus 35% larval mortality in treatment versus control nests. Our field trials caused only modest, localized reductions in nymphal abundance and had no effect on the proportion of nymphal I. scapularis infected with B. burgdorferi. Field results probably could be improved by increasing the density of nestboxes to allow fungal delivery to a higher proportion of the mouse population and by deploying nestboxes in an area with lower mammalian diversity, such as a suburban landscape.     

Differential distribution of immature Ixodes dammini (Acari: Ixodidae) on rodent hosts

Ectoparasites such as ixodid ticks that remain attached to hosts for several days while feeding on blood are able to overcome the inflammatory and immune responses of some hosts and not others. The immature stages of the deer tick Ixodes dammini are found more frequently on the white-footed mouse, Peromyscus leucopus, than on other rodents. We propose that P. leucopus is more tolerant to I. dammini than is a less common host, the meadow vole, Microtus pennsylvanicus. To test this hypothesis, the distribution patterns and engorgement indices were determined for larval and nymphal I. dammini collected from wild-caught P. leucopus and M. pennsylvanicus. There were more immature ticks, which were more fully engorged, on P. leucopus than on M. pennsylvanicus. There were more and better engorged ticks on male than on female hosts. Laboratory studies on the number and weights of larval I. dammini collected off naive and previously exposed P. leucopus and M. pennsylvanicus support the results of the field study. Fewer larval ticks were recovered from previously exposed M. pennsylvanicus than P. leucopus, and the ticks weighed less. Larval and nymphal ticks aggregated among hosts in the study grid, and higher densities per male P. leucopus were correlated with higher engorgement indices, suggesting that immature I. dammini feed better at higher densities. The feeding success of I. dammini on its preferred host species might be due to its adaptation to the immune and inflammatory reactions of the host.     

Microgeographic distribution of immature Ixodes dammini ticks correlated with that of deer

In order to determine whether the small-scale distribution of immature Ixodes dammini Spielman et al. corresponds closely to the activity patterns of white-tailed deer, Odocoileus virginianus (Zimmerman), these relationships were examined in a site on Long Island, New York, U.S.A. We first determined the extent and temporal pattern of adult ticks feeding on deer by examining twenty-three resident deer tranquilized during September-December 1985. I. dammini adults infested deer throughout this fall period, most abundantly during October and November. With radio-telemetry collars attached to deer we determined the relative frequency that they occupied 0.25 ha quadrats of the study site. During the following summer, we examined white-footed mice, Peromyscus leucopus (Rafinesque), that inhabited these quadrats and removed immature ticks from each. 8975 larval and 163 nymphal I. dammini were removed from 208 mice trapped in forty-three such quadrats. The frequency of deer using these quadrats was positively correlated with both the number of larval and of nymphal ticks per mouse. These results suggest that risk of I. damminiborne zoonotic disease may be decreased by locally reducing deer density in sites that experience intense human activity.     

Bird-feeding ticks transstadially transmit Borrelia burgdorferi that infect Syrian hamsters

Bird-feeding Ixodes dammini ticks were documented for the first time to successfully molt and transstadially pass Borrelia burgdorferi spirochetes that were indistinguishable by sodium dodecyl sulfate-polyacrylamide gel electrophoresis from the type B31 strain. Forty-six of 73 blood-engorged larvae and 50 of 66 fully-fed nymphs, removed from wild-caught birds, successfully molted. Borreliae were isolated from 21 of 78 partially- and fully-fed larvae off birds, including six specimens that molted. Spirochete-positive cultures also were obtained from 35 of 60 partially- and fully-fed nymphs that had fed from birds, including 20 nymphs that molted into adult ticks. Transstadially passed borreliae by bird-feeding larval and nymphal I. dammini were infectious to hamsters, leading us to suggest that these ticks are capable of subsequently transmitting infectious spirochetes to mammals, including humans. An isolated of B. burgdorferi, recovered from a bird-feeding larval Ixodes dentatus, was indistinguishable by sodium dodecyl sulfate-polyacrylamide gel electrophoresis from the B31 strain. This isolate, unlike another from I. dentatus off a cottontail rabbit (Sylvilagus floridanus), had a protein band with a molecular weight of approximately 31,000 that reacted with murine monoclonal antibodies H3TS and H5332 in western blot analysis. Thus, closely related borreliae are present in both I. dentatus and I. dammini.     

森林革蜱、草原革蜱感染和经期传播莱姆病螺旋体的实验研究

以实验室培育的非感染森林革蜱Dermacentor silvarum、草原革蜱D. nuttalli刺叮人工感染21天后的阳性KM鼠,利用分离培养和PCR方法检测蜱对螺旋体的保持能力以及体内螺旋体对敏感动物的感染能力。结果如下：非感染幼蜱均可以通过吸血获得莱姆病螺旋体,饱血森林革蜱和草原革蜱幼蜱PCR阳性率均为50.0%而分离阳性率都为20.0%。饱血脱落后,这些幼蜱只能在饱血后2天内分离到莱姆病螺旋体。PCR检测阳性也只能持续到4天,均不能跨越蜕皮阶段。蜕化为若蜱后,若蜱以及分别受到这些若蜱刺叮的KM鼠均未发现阳性感染。非感染若蜱吸食感染的KM鼠后,饱血森林革蜱和草原革蜱获得了莱姆病螺旋体,PCR检测阳性率分别为50.0%和20.0%。分离阳性率分别达到33.3%和60.0%。这些若蜱分别于饱血后2天和3天可以分离到莱姆病螺旋体,PCR扩增阳性也只能分别持续到饱血后4天和6天,均不能跨越蜕皮阶段;蜕化为成蜱后,成蜱以及受到它们攻击的KM鼠均未获阳性检测结果。同种蜱不同地理株在感染和保持莱姆病螺旋体的能力上也没有差异。森林革蜱、草原革蜱的幼蜱和若蜱虽可以吸血感染但均不具备经期传播莱姆病螺旋体Borrelia garinii CHNM4的能力,作为莱姆病媒介的可能性不大。     

Spirochetes in ticks and antibodies to Borrelia burgdorferi in white-tailed deer from Connecticut, New York State, and North Carolina

Ticks were screened for spirochetes and serum samples from white-tailed deer (Odocoileus virginianus) were assayed for antibodies to Borrelia burgdorferi during 1983-1984. Using fluorescein isothiocyanate-labeled rabbit antibodies produced to B. burgdorferi, the etiologic agent of Lyme disease, spirochetes were detected in Ixodes dammini (10.5% of 1,193) and Dermacentor albipictus (0.6% of 157) adults from Connecticut, I. dammini nymphs (49.1% of 108) and adults (64.7% of 99) from Armonk, New York, and in I. scapularis (0.4% of 531) and Amblyomma americanum (3.5% of 173) adults from North Carolina. Infected ticks were either seeking hosts or feeding on deer during the summer and fall. Direct fluorescent antibody staining also revealed spirochetes in two larvae of I. scapularis that emerged from eggs deposited by separate females in the laboratory. Using indirect immunofluorescence tests, antibodies to B. burgdorferi were identified in white-tailed deer living in tick-infested areas of all three states. Aside from minor cross-reactivity, there was no serologic evidence of Treponema or Leptospira infections. Ixodes dammini is a primary vector of B. burgdorferi in northeastern United States, but in North Carolina, other ixodid ticks may transmit this spirochete to humans and wildlife.     

Lyme disease and migrating birds in the Saint Croix River Valley.

During a study of migrating land birds in 1987, we examined over 9,200 individual birds representing 99 species from the Saint Croix River Valley, a Lyme disease-endemic area of east central Minnesota and northwestern Wisconsin. We found that 250 deer tick (Ixodes dammini) larvae and nymphs infested 58 birds from 15 migrant species; 56 ticks (22.4%) were positive for the Lyme disease spirochete Borrelia burgdorferi. Five ground-foraging migrant bird species favoring mesic habitats, veery (Catharus fuscescens), ovenbird (Seiurus aurocapillus), northern waterthrush (S. novaboracensis), common yellowthroat (Geothlypis trichas), and swamp sparrow (Melospiza georgiana), accounted for nearly three-quarters of parasitized individuals. Nearly half of the spirochete-positive ticks were removed from migrating birds taken in a riparian floodplain forest. Recaptured migrants with infected ticks indicate that they transmit B. burgdorferi to hexapod larvae. We suggest that birds may be both an important local reservoir in the upper Mississippi Valley and long-distance dispersal agents for B. burgdorferi-infected ticks to other regions of the continent.     

Lyme disease and migrating birds in the Saint Croix River Valley

During a study of migrating land birds in 1987, we examined over 9,200 individual birds representing 99 species from the Saint Croix River Valley, a Lyme disease-endemic area of east central Minnesota and northwestern Wisconsin. We found that 250 deer tick (Ixodes dammini) larvae and nymphs infested 58 birds from 15 migrant species; 56 ticks (22.4%) were positive for the Lyme disease spirochete Borrelia burgdorferi. Five ground-foraging migrant bird species favoring mesic habitats, veery (Catharus fuscescens), ovenbird (Seiurus aurocapillus), northern waterthrush (S. novaboracensis), common yellowthroat (Geothlypis trichas), and swamp sparrow (Melospiza georgiana), accounted for nearly three-quarters of parasitized individuals. Nearly half of the spirochete-positive ticks were removed from migrating birds taken in a riparian floodplain forest. Recaptured migrants with infected ticks indicate that they transmit B. burgdorferi to hexapod larvae. We suggest that birds may be both an important local reservoir in the upper Mississippi Valley and long-distance dispersal agents for B. burgdorferi-infected ticks to other regions of the continent.     

Differential detachment from resting hosts of replete larval and nymphal Ixodes ticks

To determine whether replete subadult Ixodes ticks detach more frequently from resting than from active hosts, diverse rodents and lizards were caged in an apparatus designed to record the ticks' sites of detachment relative to the resting site of the host. Replete larval Ixodes ricinus and Ixodes dammini accumulated mainly beneath the resting places of the mice (Apodemus agrarius and Peromyscus leucopus) most frequently parasitized in nature. Although nymphal I. ricinus similarly detached where these mice rested, nymphal I. dammini detached more randomly. When lizards were used as hosts, both subadult stages of I. ricinus tended to detach away from their main resting sites; these ticks detached from squirrels more randomly. Detachment ratios for other rodent hosts, that are abundantly infested by the larvae of these ticks in nature (Apodemus flavicollis and Clethrionomys glareolus), could not be derived because nymphs generally failed to attach. Our observations are consistent with reports that both subadult stages of I. dammini, but not the adult, feed on the same kind of nest-dwelling hosts and that the host range of I. ricinus is less focused. Detachment of mouse-feeding larvae from resting mice promotes subsequent nymphal attachment to conspecific hosts, and the absence of such behavior among nymphs facilitates access of the resulting adults to deer.     

Host associations of ticks parasitizing rodents at Borrelia burgdorferi enzootic sites in South Carolina.

A total of 237 rodents was collected in 4 regions of South Carolina from July 1994 through December 1995. Eight species were collected, including cotton mouse, hispid cotton rat, eastern woodrat, marsh rice rat, white-footed mouse, eastern harvest mouse, golden mouse, and black rat. Of the 1,514 ticks recovered from these hosts, Ixodes minor Neumann, including larvae, nymphs, and adults, was the most abundant species, representing 54% of the total. Only immature stages of other tick species were found, including larvae and nymphs of Dermacentor variabilis (Say), Amblyomma maculatum Koch, Ixodes affinis Neumann, and Ixodes scapularis Say. All 5 tick species parasitized cotton mice, cotton rats, and woodrats, which were the most important small mammal hosts for ticks at the localities studied. Rice rats were hosts of A. maculatum, D. variabilis, and L. minor. Amblyomma maculatum was more strongly associated with cotton rats than other rodent species. Ixodes scapularis was most strongly associated with cotton mice, and I. minor was more strongly associated with both woodrats and cotton mice than other species of rodents. Ixodes minor parasitized hosts in the Coastal Zone only, where among spirochete-infected hosts, it was present in significantly greater numbers than other ticks. Furthermore, I. minor was the only tick species that showed a statistically significant positive association with spirochetal infection in rodents. More I. affinis parasitized spirochete-infected hosts than I. scapularis, but fewer than I. minor. The findings discussed herein provide evidence that implicates I. minor as the possible primary enzootic vector of the Lyme disease spirochete Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt and Brenner in the Coastal Zone of South Carolina. They also indicate that the high level of B. burgdorferi infection in rodents from this region may be a function of the combined involvement of I. minor, I. affinis, and I. scapularis in the enzootic transmission of the spirochete.     

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.     

Migratory songbirds disperse ticks across Canada, and first isolation of the Lyme disease spirochete, Borrelia burgdorferi, from the avian tick, Ixodes auritulus

During a 3-yr comprehensive study, 196 ixodid ticks (9 species) were collected from 89 passerine birds (32 species) from 25 localities across Canada to determine the distribution of avian-associated tick species and endogenous Lyme disease spirochetes, Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt, and Brenner. We report the following first records of tick parasitism on avian hosts: the rabbit-associated tick, Ixodes dentatus Marx, from Manitoba and Ontario; the mouse tick, Ixodes muris Bishopp and Smith, from British Columbia; and the blacklegged tick, Ixodes scapularis Say, from New Brunswick. Moreover, we provide the first record of the Neotropical tick, Amblyomma humerale Koch (1 nymph), in Canada and its parasitism of any bird. This tick was compared morphologically with nymphs of other Neotropical Amblyomma spp., and genetically, using a 344-bp fragment of the 12S rDNA sequence of 41 New World Amblyomma species. The first collections of the western blacklegged tick, Ixodes pacificus Cooley and Kohls, from passerine species in Alberta and British Columbia, are also reported. Notably, we further report the first isolation of B. burgdorferi from the bird tick, Ixodes auritulus Neumann, collected from an American robin, Turdus migratorius L., on Vancouver Island. Furthermore, B. burgdorferi-positive I. auritulus larvae were collected from a reservoir-competent fox sparrow, Passerella iliaca (Merrem). Our findings indicate that ground-dwelling passerines, in particular, are parasitized by certain ixodid ticks and play an important role across Canada in the wide dispersal of B. burgdorferi-infected ticks and increased risk of Lyme disease exposure.