Tick-borne disease risk in a forest food web.

High burdens of Ixodes scapularis larval ticks on white-tailed deer may limit Lyme disease risk in a low biodiversity setting

Borrelia burgdorferi sensu lato prevalence in Ixodes scapularis from Canada: A thirty-year summary and meta-analysis (1990-2020)

Global changes such as deforestation, climate change, and invasive species have the potential to greatly alter zoonotic disease systems through impacts on biodiversity. This study examined the impact of the invasive pathogen that causes sudden oak death (SOD) on the ecology of Lyme disease in California. The Lyme disease bacterium, Borrelia burgdorferi, is maintained in the far western United States by a suite of animal reservoirs including the dusky-footed woodrat (Neotoma fuscipes) and deer mouse (Peromyscus maniculatus), and is transmitted by the western black-legged tick (Ixodes pacificus). Other vertebrates, such as the western fence lizard (Sceloporus occidentalis), are important tick hosts but are not reservoirs of the pathogen. Previous work found that higher levels of SOD are correlated with greater abundance of P. maniculatus and S. occidentalis and lower N. fuscipes abundance. Here we model the contribution of these tick hosts to Lyme disease risk and also evaluate the potential impact of SOD on infection prevalence of the tick vector. By empirically parameterizing a static model with field and laboratory data on tick hosts, we predict that SOD reduces an important index of disease risk, nymphal infection prevalence, leading to a reduction in Lyme disease risk in certain coastal woodlands. Direct observational analysis of the impact of SOD on nymphal infection prevalence supports these model results. This study underscores the important direct and indirect impacts of invasive plant pathogens on biodiversity, the transmission cycles of zoonotic diseases, and ultimately human health.

Lyme disease is the most prevalent vector-borne disease in North America, and both the annual incidence and geographic range are increasing. The emergence of Lyme disease has been attributed to a century-long recovery of deer, an important reproductive host for adult ticks. However, a growing body of evidence suggests that Lyme disease risk may now be more dynamically linked to fluctuations in the abundance of small-mammal hosts that are thought to infect the majority of ticks. The continuing and rapid increase in Lyme disease over the past two decades, long after the recolonization of deer, suggests that other factors, including changes in the ecology of small-mammal hosts may be responsible for the continuing emergence of Lyme disease. We present a theoretical model that illustrates how reductions in small-mammal predators can sharply increase Lyme disease risk. We then show that increases in Lyme disease in the northeastern and midwestern United States over the past three decades are frequently uncorrelated with deer abundance and instead coincide with a range-wide decline of a key small-mammal predator, the red fox, likely due to expansion of coyote populations. Further, across four states we find poor spatial correlation between deer abundance and Lyme disease incidence, but coyote abundance and fox rarity effectively predict the spatial distribution of Lyme disease in New York. These results suggest that changes in predator communities may have cascading impacts that facilitate the emergence of zoonotic diseases, the vast majority of which rely on hosts that occupy low trophic levels.

To determine whether Norway rats contribute to the risk of human Lyme disease in a central European city park, densities of endemic rodents were compared as were feeding densities of vector ticks and prevalence of infection by the Lyme disease spirochete. Only Norway rats and yellow-necked mice were abundant, and three times as many mice as rats were present. More larval ticks fed on rats than on mice, and far more nymphs engorged on the rats. All rats but only about half of the mice infected ticks. Each rat was more infectious than each infectious mouse. Infected rats were distributed throughout the city. Spirochetes infected about a quarter of the questing nymphal ticks. The capacity of rats to serve as reservoir hosts for the Lyme disease spirochete, therefore, increases risk of infection among visitors to this and other urban parks.

Lyme disease is a bacterial pathogen that spreads from animals to humans through bites from blacklegged ticks (Ixodes scapularis). The disease is a public health problem causing both physical suffering and increased health care spending since the 1980s. A snapshot of Lyme disease coverage in the popular media shows that most people prioritize conversations about Lyme disease diagnosis and treatment over prevention concerns. Anthropology has recently examined peoples’ anxieties and debates regarding the diagnosis and treatment of Lyme disease in the United States. There has been less work within the discipline on Lyme and tick-borne disease risk perceptions. This dissertation is the first anthropological study of regionally specific interpretations of Lyme disease risk. It investigates New York State (NYS), Hudson River corridor residents’ beliefs about blacklegged ticks, the diseases they carry, and the things that people do to prevent their bites. Based on fieldwork conducted over 18 months that included participant observation and open-ended interviews, the author argues people interpret Lyme disease risk through their place-based experiences, meaning the ways they interact and understand themselves (identities) in connection with the socio-regional environment of the Hudson River corridor. In five substantive dissertation chapters, the author elaborates on interlocutor’s shared, regional interpretations of tick-borne disease risk in the NYS Hudson River corridor.

This study highlights the collection of ticks from wild-caught birds in central and eastern Canada. Using polymerase chain reaction (PCR), 32 (33%) of 98 Ixodes species ticks tested were positive for the Lyme disease bacterium, Borrelia burgdorferi sensu lato (s.l.) Johnson, Schmid, Hyde, Steigerwalt, and Brenner (hereafter B. burgdorferi). Immature blacklegged ticks, Ixodes scapularis Say, which are competent vectors of B. burgdorferi, constituted the predominant Ixodes species tick collected from parasitized songbirds; specifically, 31(35%) of 89 I. scapularis nymphs were positive for B. burgdorferi. Notably, we report the first B. burgdorferi-positive I. scapularis (nymph) on a migratory passerine in Prince Edward Island; this is the first record of a tick on a bird in this maritime province. First-time records of B. burgdorferi-infected, I. scapularis nymphs on passerines in northwestern Ontario include rose-breasted grosbeak, Pheucticus ludovicianus (Linnaeus), eastern bluebird, Sialia sialis (L.), and indigo bunting, Passerina cyanea (L.). Similarly, we furnish a new host record in Canada for an I. scapularis (nymph) on a worm-eating warbler, Helmitheras vermivorus (Gmelin); this engorged nymph tested positive for B. burgdorferi. We document the first recorded collection of a B. burgdorferi-infected Ixodes muris Bishopp and Smith (female) on a songbird in Ontario. We provide the first account of a live culture of B. burgdorferi from an I. scapularis (nymph) collected from a brown-headed cowbird Molothrus ater (Boddaert) in Manitoba. We make available new host records for I. scapularis on a clay-coloured sparrow Spizella pallida (Swainson) and a Gambel’s white-crowned sparrow Zonotrichia leucophrys gambelii (Nuttall). An I. scapularis on a songbird during southward autumn migration in northwestern Ontario is a first record reported. As well, we document the first-ever account of a reptile-associated tick, a nymph of Amblyomma sabanerae Stoll, on a veery Catharus fuscescens (Stephens) in northwestern Ontario. Migratory songbirds play an integral role in the wide dispersal of B. burgdorferi-infected ticks, especially during northward spring migration. Clinicians need to be aware that people can be bitten by B. burgdorferi-infected ticks released by songbirds across Canada.

Integrated human behavior and tick risk maps to prioritize Lyme disease interventions using a 'One Health' approach

Background:Debates over whether climate change could lead to the amplification of Lyme disease (LD) risk in the future have received much attention. Although recent large-scale disease mapping studies project an overall increase in Lyme disease risk as the climate warms, such conclusions are based on climate-driven models in which other drivers of change, such as land-use/cover and host population distribution, are less considered.Objectives:The main objectives were to project the likely future ecological risk patterns of LD in Europe under different assumptions about future socioeconomic and climate conditions and to explore similarity and uncertainty in the projected risks.Methods:An integrative, spatially explicit modeling study of the ecological risk patterns of LD in Europe was conducted by applying recent advances in process-based modeling of tick-borne diseases, species distribution mapping, and scenarios of land-use/cover change. We drove the model with stakeholder-driven, integrated scenarios of plausible future socioeconomic and climate change [the Shared Socioeconomic Pathway (SSPs) combined with the Representative Concentration Pathways (RCPs)].Results:The model projections suggest that future temperature increases may not always amplify LD risk: Low emissions scenarios (RCP2.6) combined with a sustainability socioeconomic scenario (SSP1) resulted in reduced LD risk. The greatest increase in risk was projected under intermediate (RCP4.5) rather than high-end (RCP8.5) climate change scenarios. Climate and land-use change were projected to have different roles in shaping the future regional dynamics of risk, with climate warming being likely to cause risk expansion in northern Europe and conversion of forest to agriculture being likely to limit risk in southern Europe.Conclusions:Projected regional differences in LD risk resulted from mixed effects of temperature, land use, and host distributions, suggesting region-specific and cross-sectoral foci for LD risk management policy. The integrated model provides an improved explanatory tool for the system mechanisms of LD pathogen transmission and how pathogen transmission could respond to combined socioeconomic and climate changes. https://doi.org/10.1289/EHP4615

Lyme disease is the most commonly reported vector-borne illness and sixth most commonly reported notifiable infectious disease in the United States. The majority of cases occur in the Northeast and upper-Midwest, and the number and geographic distribution of cases is steadily increasing. The blacklegged tick (Ixodes scapularis Say) is the principal vector of the Lyme disease spirochete (Borrelia burgdorferi sensu stricto) in eastern North America. Although Lyme disease risk has been studied in residential and recreational settings across rural to urban landscapes including metropolitan areas, risk within U.S. cities has not been adequately evaluated despite the presence of natural and undeveloped public parkland where visitors could be exposed to B. burgdorferi-infected I. scapularis. We studied the occurrence of I. scapularis and infection prevalence of B. burgdorferi in four insular regional parks within the city of Pittsburgh to assess Lyme disease risk of exposure to infected adults and nymphs. We found that the density of I. scapularis adults (1.16 ± 0.21 ticks/100 m2) and nymphs (3.42 ± 0.45 ticks/100 m2), infection prevalence of B. burgdorferi in adults (51.9%) and nymphs (19.3%), and density of infected adults (0.60 ticks/100 m2) and nymphs (0.66 ticks/100 m2) are as high in these city parks as nonurban residential and recreational areas in the highly endemic coastal Northeast. These findings emphasize the need to reconsider, assess, and manage Lyme disease risk in greenspaces within cities, especially in high Lyme disease incidence states.

Lone Star ticks (Amblyomma americanum) have been suggested as a vector of the agent of Lyme disease (Borrelia burgdorferi sensu lato) in the USA, based on associations with an infection manifesting mainly as erythema migrans. In laboratory experiments, however, they failed to transmit B. burgdorferi sensu stricto. In this study, carried out from 1994 to 1996, we determined the seroprevalences of B. burgdorferi (1.2%), Ehrlichia chaffeensis (7%), E. phagocytophila (0%), Rickettsia rickettsii (0%), R. typhi (0%), Coxiella burneti (0%), Francisella tularensis (0%), and Babesia microti (0%) by standard serological methods for 325 residents (97% of the total population) of Gibson Island, coastal Maryland, USA, where 15% of the residents reported having had Lyme disease within a recent 5-year span. Of the 167 seronegative individuals who were followed up prospectively for 235 person-years of observation, only 2 (0.85%) seroconverted for B. burgdorferi. Of 1556 ticks submitted from residents, 95% were identified as Lone Star ticks; only 3% were deer ticks (Ixodes dammini), the main American vector of Lyme disease. B. burgdorferi s.s. infected 20% of host-seeking immature deer ticks, and borreliae ("B. lonestari") were detected in 1-2% of Lone Star ticks. Erythema migrans was noted in 65% of self-reports of Lyme disease, but many such reports indicated that the rash was present while the tick was still attached, suggesting a reaction to the bite itself rather than true Lyme disease. Sera from individuals reporting Lyme disease generally failed to react to B. burgdorferi or any other pathogen antigens. The residents of Gibson Island had an exaggerated perception of the risk of Lyme disease because they were intensely infested with an aggressively human-biting and irritating nonvector tick. In addition, a Lyme disease mimic of undescribed etiology (named Masters' disease) seems to be associated with Lone Star ticks, and may confound Lyme disease surveillance. The epidemiological and entomological approach used in this study might fruitfully be applied wherever newly emergent tickborne zoonoses have been discovered.

Toward a more complete appreciation of the clinical spectrum of Borrelia burgdorferi infection: early lyme disease without erythema migrans

Animal behavior can have profound effects on pathogen transmission and disease incidence. We studied the questing (= host-seeking) behavior of blacklegged tick (Ixodes scapularis) nymphs, which are the primary vectors of Lyme disease in the eastern United States. Lyme disease is common in northern but not in southern regions, and prior ecological studies have found that standard methods used to collect host-seeking nymphs in northern regions are unsuccessful in the south. This led us to hypothesize that there are behavior differences between northern and southern nymphs that alter how readily they are collected, and how likely they are to transmit the etiological agent of Lyme disease to humans. To examine this question, we compared the questing behavior of I. scapularis nymphs originating from one northern (Lyme disease endemic) and two southern (non-endemic) US regions at field sites in Wisconsin, Rhode Island, Tennessee, and Florida. Laboratory-raised uninfected nymphs were monitored in circular 0.2 m2 arenas containing wooden dowels (mimicking stems of understory vegetation) for 10 (2011) and 19 (2012) weeks. The probability of observing nymphs questing on these stems (2011), and on stems, on top of leaf litter, and on arena walls (2012) was much greater for northern than for southern origin ticks in both years and at all field sites (19.5 times greater in 2011; 3.6–11.6 times greater in 2012). Our findings suggest that southern origin I. scapularis nymphs rarely emerge from the leaf litter, and consequently are unlikely to contact passing humans. We propose that this difference in questing behavior accounts for observed geographic differences in the efficacy of the standard sampling techniques used to collect questing nymphs. These findings also support our hypothesis that very low Lyme disease incidence in southern states is, in part, a consequence of the type of host-seeking behavior exhibited by southern populations of the key Lyme disease vector.

Risk of human exposure to vector-borne zoonotic pathogens is a function of the abundance and infection prevalence of vectors. We assessed the determinants of Lyme-disease risk (density and Borrelia burgdorferi-infection prevalence of nymphal Ixodes scapularis ticks) over 13 y on several field plots within eastern deciduous forests in the epicenter of US Lyme disease (Dutchess County, New York). We used a model comparison approach to simultaneously test the importance of ambient growing-season temperature, precipitation, two indices of deer (Odocoileus virginianus) abundance, and densities of white-footed mice (Peromyscus leucopus), eastern chipmunks (Tamias striatus), and acorns ( Quercus spp.), in both simple and multiple regression models, in predicting entomological risk. Indices of deer abundance had no predictive power, and precipitation in the current year and temperature in the prior year had only weak effects on entomological risk. The strongest predictors of a current year's risk were the prior year's abundance of mice and chipmunks and abundance of acorns 2 y previously. In no case did inclusion of deer or climate variables improve the predictive power of models based on rodents, acorns, or both. We conclude that interannual variation in entomological risk of exposure to Lyme disease is correlated positively with prior abundance of key hosts for the immature stages of the tick vector and with critical food resources for those hosts.

Lyme disease, recognized as one of the most important vector-borne diseases worldwide, has been increasing in incidence and spatial extend in United States. In the Northeast and Upper Midwest, Lyme disease is transmitted by Ixodes scapularis. Currently, many studies have been conducted to identify factors influencing Lyme disease risk in the Northeast, however, relatively few studies focused on the Upper Midwest. In this study, we explored and compared the climatic and landscape factors that shape the spatial patterns of human Lyme cases in these two regions, using the generalized linear mixed models. Our results showed that climatic variables generally had opposite correlations with Lyme disease risk, while landscape factors usually had similar effects in these two regions. High precipitation and low temperature were correlated with high Lyme disease risk in the Upper Midwest, while with low Lyme disease risk in the Northeast. In both regions, size and fragmentation related factors of residential area showed positive correlations with Lyme disease risk. Deciduous forests and evergreen forests had opposite effects on Lyme disease risk, but the effects were consistent between two regions. In general, this study provides new insight into understanding the differences of risk factors of human Lyme disease risk in these two regions.