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.     

Lyme disease in Wisconsin: epidemiologic, clinical, serologic, and entomologic findings

In 1980-82, 80 individuals (71 Wisconsin residents) had confirmed Lyme disease (LD-c) reported; 39 additional patients had probable or possible LD. All cases of LD-c occurred during May-November; 73 percent occurred during June-July; 54 (68 percent) occurred in males. The mean age was 38.7 years (range, 7-77 years). Among LD-c patients, likely exposure to the presumed vector Ixodes dammini (ID) occurred in 22 different Wisconsin counties. Antibodies to the ID spirochete that causes LD occurred in 33 of 49 LD-c cases versus 0 of 18 in ill controls (p less than .001) and in 13 of 26 LD-c cases treated with penicillin or tetracycline versus 16 of 19 LD-c cases not treated. Early antibiotic therapy appears to blunt the antibody response to the ID spirochete. Regional tick surveys conducted in Wisconsin during each November in 1979-82 have demonstrated regions of greater density of ID. Utilizing comparable tick collection in these surveys, increases were noted in the percentage of deer with ID from 24 percent (31/128) in 1979 to 38 percent (58/152) in 1981, in the standardized mean value of ID/deer from 1.0 in 1979 to 2.2 in 1981, in the percentage of ID of the total ticks collected from 13 percent in 1979 to 71 percent in 1981, or in the ratio of ID to Dermacentor albipictus ticks from 0.14 in 1979 to 2.44 in 1981. However, a reduction in the density of ID/deer was noted generally throughout Wisconsin in 1982 when compared to 1981. LD is widespread in Wisconsin, with ecologic and clinical features similar to those occurring along the eastern seaboard.     

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.     

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.     

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.     

Geographic Risk for Lyme Disease and Human Granulocytic Ehrlichiosis in Southern New York State

Ixodes scapularis, the tick vector of Lyme disease and human granulocytic ehrlichiosis (HGE), is prevalent in much of southern New York state. The distribution of this species has increased, as have reported cases of both Lyme disease and HGE. The unreliability of case reports, however, demonstrates the need for tick and pathogen surveillance in order to accurately define areas of high risk. In this study, a total of 89,550 m² at 34 study sites was drag sampled in 1995 and a total of 51,540 m² at 40 sites was sampled in 1996 to determine tick and pathogen distribution in southern New York state. I. scapularis was collected from 90% of the sites sampled, and regionally, a 2.5-fold increase in nymphal abundance occurred from 1995 to 1996. I. scapularis individuals from all sites were infected with Borrelia burgdorferi in 1995, while an examination of ticks for both B. burgdorferi and the agent of HGE in 1996 confirmed that these organisms were present in all counties; the average coinfection rate was 1.9%. No correlation was found between estimated risk and reported cases of Lyme disease. The geographic disparity of risk observed among sites in this study underscores the need for vector and pathogen surveillance on a regional level. An entomologic risk index can help identify sites for targeted tick control efforts.     

The New Zealand white rabbit: an experimental host for infecting ticks with Lyme disease spirochetes

Efficiency of the New Zealand white rabbit as a host for infecting larval Ixodes dammini, I. pacificus, and I. ricinus with Lyme disease spirochetes was evaluated. Rabbits inoculated with infected midgut suspensions of I. dammini from Shelter Island, New York, or fed upon by infected ticks from the same area, responded with spirochetemias of sufficient concentrations to infect as many as 30 percent of the ticks. When infected ticks were used as indicators, it appeared that spirochetemias persisting for up to ten days occurred as early as the tenth day after inoculation or feeding of ticks.     

Borreliosis in free-ranging black bears from Wisconsin

Blood, kidney and tick samples were obtained from 18 hunter-killed black bears (Ursus americanus) from three sites in northern Wisconsin. A Borrelia sp., morphologically and antigenically similar to Borrelia burgdorferi, was isolated from the blood of two of the animals, and from the kidney of a third. Ixodes dammini and Dermacentor variabilis were found on the bears. This is the first report of borreliosis in the Ursidae, and of the primary vector of Lyme disease, I. dammini, from this host.     

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.     

Enzootic Babesia microti in Maine

Human babesiosis in the northeastern United States caused by Babesia microti (Apicomplexa: Piroplasmida) is mainly reported from coastal New England sites, where deer ticks (Ixodes dammini) are common. However, the piroplasm has been detected in microtine rodents elsewhere in association with I. angustus or other nidicolous ticks, suggesting that the agent is widely distributed but zoonotically significant only where a human-biting "bridge" vector is present. To determine whether this piroplasm may be enzootic in areas where I. dammini is absent, we surveyed small mammals collected from 2 sites in Maine, where I. angustus or I. muris is common but I. dammini is not. Of 43 chipmunks, voles, deer mice, and shrews examined, 3 (6.9, 95% confidence interval 0 to 14.5) were parasitemic, as determined by blood smear or polymerase chain reaction targeting a piroplasm-specific portion of the 18S ribosomal DNA gene. Phylogenetic analysis of the sequenced amplification products demonstrates the presence of 2 forms of B. microti. We conclude that B. microti may be enzootic in the absence of I. dammini but that human risk relates to dense infestations of this human-biting tick.     

Lyme disease in New Jersey, 1978-1982

From 1978 to 1982, 117 cases of Lyme disease were reported in New Jersey. The number of cases increased each year from four in 1978 and 1979 to 56 in 1982. Forty-eight percent of cases occurred in a four-township area in central Monmouth County. The proportion of cases with arthritis decreased in 1982 because of early antibiotic treatment and better reporting of milder cases. The proportion of cases with positive serology increased with severity of the clinical syndrome. About 25 percent of patients had exposure to ticks because of occupations that required outdoor activities. Lyme disease is a growing public health problem in New Jersey.     

Ixodes dammini: occurrence and prevalence of infection with Borrelia spp. in Minnesota

The distribution of Ixodes dammini in Minnesota was studied by collecting adult ticks from hunting dogs during the grouse seasons in September and October of 1985 and 1986. The tick was most frequently found in the east-central part of the state. Borrelia spp. were observed by immunofluorescence in 10% of the ticks. The locations where ticks were found coincide with the primary endemic areas for Lyme disease in the state.     

Real-time PCR for simultaneous detection and quantification of Borrelia burgdorferi in field-collected Ixodes scapularis ticks from the Northeastern United States

The density of spirochetes in field-collected or experimentally infected ticks is estimated mainly by assays based on microscopy. In this study, a real-time quantitative PCR (qPCR) protocol targeting the Borrelia burgdorferi-specific recA gene was adapted for use with a Lightcycler for rapid detection and quantification of the Lyme disease spirochete, B. burgdorferi, in field-collected Ixodes scapularis ticks. The sensitivity of qPCR for detection of B. burgdorferi DNA in infected ticks was comparable to that of a well-established nested PCR targeting the 16S-23S rRNA spacer. Of the 498 I. scapularis ticks collected from four northeastern states (Rhode Island, Connecticut, New York, and New Jersey), 91 of 438 (20.7%) nymphal ticks and 15 of 60 (25.0%) adult ticks were positive by qPCR assay. The number of spirochetes in individual ticks varied from 25 to 197,200 with a mean of 1,964 spirochetes per nymphal tick and a mean of 5,351 spirochetes per adult tick. No significant differences were found in the mean numbers of spirochetes counted either in nymphal ticks collected at different locations in these four states (P = 0.23 by one-way analysis of variance test) or in ticks infected with the three distinct ribosomal spacer restriction fragment length polymorphism types of B. burgdorferi (P = 0.39). A high degree of spirochete aggregation among infected ticks (variance-to-mean ratio of 24,877; moment estimate of k = 0.279) was observed. From the frequency distribution data and previously published transmission studies, we estimated that a minimum of 300 organisms may be required in a host-seeking nymphal tick to be able to transmit infection to mice while feeding on mice. These data indicate that real-time qPCR is a reliable approach for simultaneous detection and quantification of B. burgdorferi infection in field-collected ticks and can be used for ecological and epidemiological surveillance of Lyme disease spirochetes.     

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.     

Lyme disease in Minnesota: epidemiologic and serologic findings

During the four years, 1980 to 1983, 83 Minnesota residents have been diagnosed with Lyme disease. Sixty-five of the patients were male. The median age of patients was 39 years with a range from one to 77 years. Seventy-five (90 percent) had onset in 1982 and 1983. Of these latter cases, 56 (75 percent) recalled a tick bite three to 27 days prior to the development of erythema chronicum migrans. Patients experienced possible exposure to Ixodes dammini in at least 24 (28 percent) of the 87 Minnesota counties; however, over 50 percent had reported exposure in one of eight east-central counties near or immediately west of the Wisconsin border. Serologic studies for antibody against the Ixodes dammini spirochete were completed on 30 patients with onset in 1982 and 1983. Of 28 patients with paired acute and convalescent serum samples, only two (7 percent) had fourfold rises in antibody titers. Lyme disease is an emerging public health problem in Minnesota. Additional studies are needed to define the risk of disease by geographic area within the state. Physicians statewide should be alert to the possibility of Lyme disease among their patients, since only 39 percent of patients with onset in 1982 and 1983 were exposed in their county of residence.     

A comprehensive multiple matrix model representing the life cycle of the tick that transmits the agent of Lyme disease.

An extension of Leslie matrix methodology was developed to describe the life cycle of Ixodes dammini, the tick that transmits the agent of Lyme disease in eastern North America. Thereby, we described the seasonally changing pattern of interactions of the tick with its various hosts in a well-studied site on Nantucket Island, Massachusetts. Particular numerical values representing the site were estimated mainly on the basis of published values and interpreted on the basis of experience. The model was used to predict seasonal abundance and annual rate of increase of this vector tick. Although these ticks quest for hosts during two consecutive feeding seasons, all but a few feed during the first such season. The relative distribution of developmental stages of the tick stabilized after 35 years. Abundance of the simulated population increased exponentially and doubled every 6 years. The simulations produced realistic seasonal feeding distributions of the ticks in its various developmental stages.     

Impact of the experimental removal of lizards on Lyme disease risk

The distribution of vector meals in the host community is an important element of understanding and predicting vector-borne disease risk. Lizards (such as the western fence lizard; Sceloporus occidentalis) play a unique role in Lyme disease ecology in the far-western United States. Lizards rather than mammals serve as the blood meal hosts for a large fraction of larval and nymphal western black-legged ticks (Ixodes pacificus--the vector for Lyme disease in that region) but are not competent reservoirs for the pathogen, Borrelia burgdorferi. Prior studies have suggested that the net effect of lizards is to reduce risk of human exposure to Lyme disease, a hypothesis that we tested experimentally. Following experimental removal of lizards, we documented incomplete host switching by larval ticks (5.19%) from lizards to other hosts. Larval tick burdens increased on woodrats, a competent reservoir, but not on deer mice, a less competent pathogen reservoir. However, most larvae failed to find an alternate host. This resulted in significantly lower densities of nymphal ticks the following year. Unexpectedly, the removal of reservoir-incompetent lizards did not cause an increase in nymphal tick infection prevalence. The net result of lizard removal was a decrease in the density of infected nymphal ticks, and therefore a decreased risk to humans of Lyme disease. Our results indicate that an incompetent reservoir for a pathogen may, in fact, increase disease risk through the maintenance of higher vector density and therefore, higher density of infected vectors.