A stochastic epidemic model for the dynamics of two pathogens in a single tick population.

Understanding tick-transmitted pathogens in tick infested areas is crucial for the development of preventive and control measures in response to the increasing cases of tick-borne diseases. A stochastic model for the dynamics of two pathogens, Rickettsia parkeri and Rickettsia amblyommii, in a single tick, Amblyomma americanum, is developed and analysed. The model, a continuous-time Markov chain, is based on a deterministic tick-borne disease model. The extinction threshold for the stochastic model is computed using the multitype branching process and conditions for pathogen extinction or persistence are presented. The probability of pathogen extinction is computed using numerical simulations and is shown to be a good estimate of the probability of extinction calculated from the branching process. A sensitivity analysis is undertaken to illustrate the relationship between co-feeding and transovarial transmission rates and the probability of pathogen extinction. Expected epidemic duration is estimated using sample paths and we show that R. amblyommii is likely to persist slightly longer than R. parkeri. Further, we estimate the duration of possible coexistence of the two pathogens.

A Stochastic Tick-Borne Disease Model: Exploring the Probability of Pathogen Persistence.

We formulate and analyse a stochastic epidemic model for the transmission dynamics of a tick-borne disease in a single population using a continuous-time Markov chain approach. The stochastic model is based on an existing deterministic metapopulation tick-borne disease model. We compare the disease dynamics of the deterministic and stochastic models in order to determine the effect of randomness in tick-borne disease dynamics. The probability of disease extinction and that of a major outbreak are computed and approximated using the multitype Galton-Watson branching process and numerical simulations, respectively. Analytical and numerical results show some significant differences in model predictions between the stochastic and deterministic models. In particular, we find that a disease outbreak is more likely if the disease is introduced by infected deer as opposed to infected ticks. These insights demonstrate the importance of host movement in the expansion of tick-borne diseases into new geographic areas.

Invasion of two tick-borne diseases across New England: harnessing human surveillance data to capture underlying ecological invasion processes.

Modelling the spatial spread of vector-borne zoonotic pathogens maintained in enzootic transmission cycles remains a major challenge. The best available spatio-temporal data on pathogen spread often take the form of human disease surveillance data. By applying a classic ecological approach-occupancy modelling-to an epidemiological question of disease spread, we used surveillance data to examine the latent ecological invasion of tick-borne pathogens. Over the last half-century, previously undescribed tick-borne pathogens including the agents of Lyme disease and human babesiosis have rapidly spread across the northeast United States. Despite their epidemiological importance, the mechanisms of tick-borne pathogen invasion and drivers underlying the distinct invasion trajectories of the co-vectored pathogens remain unresolved. Our approach allowed us to estimate the unobserved ecological processes underlying pathogen spread while accounting for imperfect detection of human cases. Our model predicts that tick-borne diseases spread in a diffusion-like manner with occasional long-distance dispersal and that babesiosis spread exhibits strong dependence on Lyme disease.

New Records of Ixodes affinis (Acari: Ixodidae) Parasitizing Avian Hosts in Southeastern Virginia.

Ixodes affinis Neumann (Acari: Ixodidae) is a hard-bodied tick species distributed throughout much of the southeastern United States. Although I. affinis does not parasitize humans, it is a competent vector of Borrelia burgdorferi sensu stricto, the causative-agent of Lyme disease, and thus contributes to the enzootic maintenance of this pathogen. This study presents evidence of I. affinis parasitizing five new host passerine species. During 2012-2014, 1,888 birds were captured and examined for ticks, and 18 immature I. affinis were collected from 12 birds-six Carolina Wrens (Thyrothorus ludovicianus); two Brown Thrashers (Toxostoma rufum); and one American Robin (Turdus migratorius), Eastern Towhee (Pipilo erythrophthalmus), Northern Cardinal (Cardinalis cardinalis), and White-throated Sparrow (Zonotrichia albicollis). Of 15 larvae and 3 nymphs collected, one nymph tested positive for B. burgdorferi DNA. I. affinis was found co-feeding on birds with immature Amblyomma americanum (L.), Ixodes brunneus Koch, Ixodes dentatus Marx, Ixodes scapularis Say, and Haemaphysalis leporispalustris Packard. The results of this research provide a better understanding of I. affinis hosts and identify avian taxa that may play a role in the maintenance and dispersal of this tick species.

Rickettsia parkeri Transmission to Amblyomma americanum by Cofeeding with Amblyomma maculatum (Acari: Ixodidae) and Potential for Spillover.

Amblyomma americanum (L.) is a human-biting ixodid tick distributed throughout much of the southeastern United States. Rickettsia parkeri is a member of the spotted fever group rickettsiae and causes a febrile illness in humans commonly referred to as "Tidewater spotted fever" or "R. parkeri rickettsiosis." Although the Gulf Coast tick, Amblyomma maculatum Koch, is the primary vector of R. parkeri, a small proportion of A. americanum have also been shown to harbor R. parkeri. The purpose of this investigation was to determine whether R. parkeri is spilling over into A. americanum in eastern Virginia and also to determine through laboratory experiments, whether A. americanum can acquire R. parkeri by cofeeding alongside infected ticks. Of 317 wild-caught, flat adult A. americanum tested from 29 counties and independent cities in coastal Virginia, a single female A. americanum was positive for R. parkeri, suggesting that R. parkeri is spilling over into this species, but at very low rates (<1.0%). Laboratory studies using guinea pigs indicated that nymphal A. americanum were able to acquire R. parkeri while feeding alongside infected A. maculatum and then transstadially maintain the infection. Nymphal A. americanum infected with Rickettsia amblyommii, however, were less likely to acquire R. parkeri, suggesting that infection with R. amblyommii may prevent R. parkeri from establishing infection in A. americanum.

Release the hens: a study on the complexities of guinea fowl as tick control.

Established tick control strategies often involve methods that can be damaging to existing environmental conditions or natural host ecology. To find more environmentally friendly methods, biological controls, like predators of ticks, have been suggested. There are natural predators of ticks, but most are generalists and not expected to control tick populations. Helmeted guinea fowl (Numida meleagris (L.) (Galliformes: Numididae)) have been suggested to be biological controls of ticks, and therefore, tick-borne pathogens, but their potential role as hosts for ticks complicates the relationship. A study was conducted to assess whether guinea fowl reduces the abundance of lone star ticks, Amblyomma americanum (L.) (Acari: Ixodidae), or whether they are hosts of ticks. Using mark-recapture techniques, painted lone star ticks were placed into 3 different treatments: penned, excluded, and free range. The recapture rates of painted ticks were compared. There was a significant difference between excluded and free-range treatments, but not between excluded and penned or between free range and penned. To investigate the role of guinea fowl as hosts of ticks, coop floors were examined for engorged ticks. Engorged lone star nymphs that had fed on guinea fowl were found. Lastly, ticks collected were tested to identify the potential reduction in risk of tick-borne pathogens. This study found no evidence that guinea fowl are an effective biological control of lone star ticks or tick-borne pathogens, but they are hosts of lone star nymphs. Future studies are needed to assess the complex ecology of a biological control of ticks that is also a host.

Newer Surveillance Data Extends our Understanding of the Niche of Rickettsia montanensis (Rickettsiales: Rickettsiaceae) Infection of the American Dog Tick (Acari: Ixodidae) in the United States.

Background: Understanding the geographic distribution of Rickettsia montanensis infections in Dermacentor variabilis is important for tick-borne disease management in the United States, as both a tick-borne agent of interest and a potential confounder in surveillance of other rickettsial diseases. Two previous studies modeled niche suitability for D. variabilis with and without R. montanensis , from 2002-2012, indicating that the D. variabilis niche overestimates the infected niche. This study updates these, adding data since 2012. Methods: Newer surveillance and testing data were used to update Species Distribution Models (SDMs) of D. variabilis , and R. montanensis infected D. variabilis , in the United States. Using random forest (RF) models, found to perform best in previous work, we updated the SDMs and compared them with prior results. Warren's I niche overlap metric was used to compare between predicted suitability for all ticks and 'pathogen positive niche' models across datasets. Results: Warren's I indicated <2% change in predicted niche, and there was no change in order of importance of environmental predictors, for D. variabilis or R. montanensis positive niche. The updated D. variabilis niche model overpredicted suitability compared to the updated R. montanensis positive niche in key peripheral parts of the range, but slightly underpredicted through the northern and midwestern parts of the range. This reinforces previous findings of a more constrained pathogen-positive niche than predicted by D. variabilis records alone. Conclusions: The consistency of predicted niche suitability for D. variabilis in the United States, with the addition of nearly a decade of new data, corroborates this is a species with generalist habitat requirements. Yet a slight shift in updated niche distribution, even of low suitability, included more southern areas, pointing to a need for continued and extended monitoring and surveillance. This further underscores the importance of revisiting vector and vector-borne disease distribution maps.

Newer Surveillance Data Extends our Understanding of the Niche of Rickettsia montanensis (Rickettsiales: Rickettsiaceae) Infection of the American Dog Tick (Acari: Ixodidae) in the United States.

Background: Understanding the geographic distribution of Rickettsia montanensis infections in Dermacentor variabilis is important for tick-borne disease management in the United States, as both a tick-borne agent of interest and a potential confounder in surveillance of other rickettsial diseases. Two previous studies modeled niche suitability for D. variabilis with and without R. montanensis, from 2002 to 2012, indicating that the D. variabilis niche overestimates the infected niche. This study updates these, adding data since 2012. Methods: Newer surveillance and testing data were used to update Species Distribution Models (SDMs) of D. variabilis, and R. montanensis-infected D. variabilis, in the United States. Using random forest models, found to perform best in previous work, we updated the SDMs and compared them with prior results. Warren's I niche overlap metric was used to compare between predicted suitability for all ticks and "R. montanensis-positive niche" models across datasets. Results: Warren's I indicated <2% change in predicted niche, and there was no change in order of importance of environmental predictors, for D. variabilis or R. montanensis-positive niche. The updated D. variabilis niche model overpredicted suitability compared with the updated R. montanensis-positive niche in key peripheral parts of the range, but slightly underpredicted through the northern and midwestern parts of the range. This reinforces previous findings of a more constrained R. montanensis-positive niche than predicted by D. variabilis records alone. Conclusions: The consistency of predicted niche suitability for D. variabilis in the United States, with the addition of nearly a decade of new data, corroborates this is a species with generalist habitat requirements. Yet a slight shift in updated niche distribution, even of low suitability, included more southern areas, pointing to a need for continued and extended monitoring and surveillance. This further underscores the importance of revisiting vector and vector-borne disease distribution maps.

Tick Species Composition, Collection Rates, and Phenology Provide Insights into Tick-Borne Disease Ecology in Virginia.

To better understand tick ecology in Virginia and the increasing Lyme disease incidence in western Virginia, a comparative phenological study was conducted in which monthly collections were performed at twelve sampling locations in southwestern Virginia (high Lyme disease incidence) and 18 equivalent sampling locations in southeastern Virginia (low Lyme disease incidence) for one year. In western Virginia, we also explored the effect of elevation on collection rates of Ixodes scapularis Say (Acari: Ixodidae) and Amblyomma americanum (L.) (Acari: Ixodidae). In total, 35,438 ticks were collected (33,106 A. americanum; 2,052 I. scapularis; 134 Ixodes affinis Neumann [Acari: Ixodidae]; 84 Dermacentor variabilis [Say] [Acari: Ixodidae]; 49 Dermacentor albipictus [Packard] [Acari: Ixodidae]; 10 Haemaphysalis leporispalustris [Packard] [Acari: Ixodidae]; 2 Ixodes brunneus Koch [Acari: Ixodidae]; 1 Haemaphysalis longicornis Neumann [Acari: Ixodidae]). Within southwestern Virginia, Ixodes scapularis collection rates were not influenced by elevation, unlike A. americanum which were collected more frequently at lower elevations (e.g., below 500 m). Notably, I. scapularis larvae and nymphs were commonly collected in southwestern Virginia (indicating that they were questing on or above the leaf litter) but not in southeastern Virginia. Questing on or above the leaf litter is primarily associated with northern populations of I. scapularis. These findings may support the hypothesis that I. scapularis from the northeastern United States are migrating into western Virginia and contributing to the higher incidence of Lyme disease in this region. This comparative phenological study underscores the value of these types of studies and the need for additional research to further understand the rapidly changing tick-borne disease dynamics in Virginia.

Estimating the impact of human papillomavirus (HPV) vaccination on HPV prevalence and cervical cancer incidence in Mali.

Human papillomavirus vaccines have potential to reduce cervical cancer incidence and mortality; however, cultural and economic barriers may hinder success in developing countries. We assessed impact of a single vaccine campaign in Mali with use of mathematical modeling. Our model shows that decreases in the prevalence of Human papillomavirus infection are proportional to achieved vaccination coverage.

Rickettsia parkeri in gulf coast ticks, southeastern Virginia, USA.

We report evidence that Amblyomma maculatum tick populations are well established in southeastern Virginia. We found that 43.1% of the adult Gulf Coast ticks collected in the summer of 2010 carried Rickettsia parkeri, suggesting that persons living in or visiting southeastern Virginia are at risk for infection with this pathogen.

Trends and Opportunities in Tick-Borne Disease Geography.

Tick-borne diseases are a growing problem in many parts of the world, and their surveillance and control touch on challenging issues in medical entomology, agricultural health, veterinary medicine, and biosecurity. Spatial approaches can be used to synthesize the data generated by integrative One Health surveillance systems, and help stakeholders, managers, and medical geographers understand the current and future distribution of risk. Here, we performed a systematic review of over 8,000 studies and identified a total of 303 scientific publications that map tick-borne diseases using data on vectors, pathogens, and hosts (including wildlife, livestock, and human cases). We find that the field is growing rapidly, with the major Ixodes-borne diseases (Lyme disease and tick-borne encephalitis in particular) giving way to monitoring efforts that encompass a broader range of threats. We find a tremendous diversity of methods used to map tick-borne disease, but also find major gaps: data on the enzootic cycle of tick-borne pathogens is severely underutilized, and mapping efforts are mostly limited to Europe and North America. We suggest that future work can readily apply available methods to track the distributions of tick-borne diseases in Africa and Asia, following a One Health approach that combines medical and veterinary surveillance for maximum impact.

Focus Stacking Images of Morphological Character States for Differentiating the Adults of Ixodes affinis and Ixodes scapularis (Acari: Ixodidae) in Areas of Sympatry.

Adult females and males of Ixodes affinis and Ixodes scapularis are illustrated by focus stacking image photography, and morphological character states are described that reliably differentiate the two species. In conjunction with other environmental cues, such as the questing phenology of adults, these characteristics will enable the rapid identification of adults of either sex along the southern Coastal Plain of the United States, where these species are sympatric.

Orofacial Manifestations of Lyme Disease: A systematic review.

Purpose: Orofacial manifestations of Lyme disease can affect head and neck anatomical structures that are frequently examined by dental professionals. The purpose of this systematic review was to examine the literature for types and frequencies of orofacial manifestations documented in populations in the United States (US) with Lyme disease.Methods: Four electronic databases (Dentistry and Oral Sciences, PubMed, Cinahl Plus, and Medline) were systematically searched during the summer of 2019 using keywords and MeSH terms to identify relevant studies. Search term alterations and synonyms were cross-checked using the US National Library of Medicine Unified Medical Language System Metathesaurus. Full-text, English language studies were included if they reported on US populations with Centers for Disease Control and Prevention confirmed cases of Lyme disease. The review followed guidelines set forth in Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA). Quality was assessed with a modified version of the Cochrane Data Collection Form for Randomized Control Trials and Non-randomized Control Trials. Extracted data was organized by themes of manifestations and the frequencies were calculated.Results: An initial search extracted 217,381 articles; 43 met the inclusion criteria and were further reviewed for quality. Twelve articles published from 1992-2017 were deemed appropriate for inclusion. All were from non-dental journals and fewer than half (n=6) reported on Lyme disease endemic states. Eight incidences of orofacial manifestations within head/neck regions were documented in Lyme disease patients (n=951) and included: headache (39.5%), facial palsy (42.5%), temporomandibular joint arthralgia (42.0%), altered taste (11.0%), stiff neck (13.6%), sore throat (3.0%), neck pain/arthralgia (7.5%), and erythema migrans rash (5.2%).Conclusion: Eight orofacial manifestations of Lyme disease were revealed by this systematic review. Future research regarding the orofacial manifestations of Lyme disease is needed so this medical condition can be better understood by oral health care providers and result in improved health outcomes for infected patients.

Scoping review of distribution models for selected Amblyomma ticks and rickettsial group pathogens.

The rising prevalence of tick-borne diseases in humans in recent decades has called attention to the need for more information on geographic risk for public health planning. Species distribution models (SDMs) are an increasingly utilized method of constructing potential geographic ranges. There are many knowledge gaps in our understanding of risk of exposure to tick-borne pathogens, particularly for those in the rickettsial group. Here, we conducted a systematic scoping review of the SDM literature for rickettsial pathogens and tick vectors in the genus Amblyomma. Of the 174 reviewed articles, only 24 studies used SDMs to estimate the potential extent of vector and/or pathogen ranges. The majority of studies (79%) estimated only tick distributions using vector presence as a proxy for pathogen exposure. Studies were conducted at different scales and across multiple continents. Few studies undertook original data collection, and SDMs were mostly built with presence-only datasets from public database or surveillance sources. The reliance on existing data sources, using ticks as a proxy for disease risk, may simply reflect a lag in new data acquisition and a thorough understanding of the tick-pathogen ecology involved.

A Comparison of Tick Collection Materials and Methods in Southeastern Virginia.

In field studies of tick ecology, observed patterns may be biased by sampling methods. Results can vary by species, life stage, and habitat, and understanding these biases will improve comparisons of data across studies as well as assessment of human disease risk. A direct comparison of flagging versus dragging was conducted in southeastern Virginia. Transects were surveyed over a 6-wk period to identify differences in species and life stage collected, as well as differences between corduroy and denim material and inspection method for drags. Flagging collected more Ixodes affinis Neumann (Acari: Ixodidae) adults and Amblyomma americanum L. (Acari: Ixodidae) adults than dragging. Ground inspection was more efficient than tree inspection for collection of I. affinis adults, with no significant difference in inspection method for any other species or life stage. Corduroy was found to be more effective than denim in collecting nymphal A. americanum, although this may be an artifact of three large samples for corduroy collection of these ticks. There was no significant difference in Ixodes scapularis Say (Acari: Ixodidae) collection in any comparison. Dragging, tree inspection, and denim were not found to be more efficient in any scenario. This is the first comparison of flagging and dragging conducted in the southeastern United States. The community composition of ticks in this region greatly differs from regions where studies of these commonly used sampling techniques have been conducted. As the distributions of ticks continue to change over time, it will be important to evaluate best practices annually.

Passerine birds as hosts for Ixodes ticks infected with Borrelia burgdorferi sensu stricto in southeastern Virginia.

The ecology of vector-borne diseases in a region can be attributed to vector-host interactions. In the United States, tick-borne pathogens are the cause of the highest number of reported vector-borne diseases. In the mid-Atlantic region of the eastern United States, tick-borne diseases such as Lyme disease, have increased in incidence, with tick-host-pathogen interactions considered a contributing factor to this increase. Ticks become infected with pathogens after taking a blood meal from a systemically infected host or through a localized infection while co-feeding on a host with other infected ticks. The host not only plays a role in pathogen acquisition by the tick, but can also facilitate dispersal of the tick locally within a region or over greater distances into new geographical ranges outside of their historical distributional range. In this study conducted in southeastern Virginia (USA), we examined the interaction between both resident and migratory bird species and Ixodes ticks, the primary vectors of Borrelia burgdorferi sensu stricto (s.s.) the main causative agent of Lyme disease on the East coast of the United States. Over a two-year period (2012-2014), 1879 passerine birds were surveyed, with 255 Ixodes ticks tested for the presence of Borrelia spp. Eighty passerine birds (4.3 %) representing 17 bird species were parasitized by at least one Ixodes tick, but only three bird species were parasitized by Ixodes ticks that tested positive for B. burgdorferi s.s. Twenty Ixodes ticks (7.8 %) tested positive for B. burgdorferi s.s. with nearly all collected from resident bird species including the Carolina wren (Thryothorus ludovicianus) and brown thrasher (Toxostoma rufum). Given that millions of birds pass through southeastern Virginia during migration, even with the low number of Ixodes ticks parasitizing passerine birds and the low prevalence of B. burgdorferi s.s. found within Ixodes ticks collected, the sheer volume of passerine birds suggests they may play a role in the maintenance and dispersal of B. burgdorferi s.s. in southeastern Virginia.

Exploring the Niche of Rickettsia montanensis (Rickettsiales: Rickettsiaceae) Infection of the American Dog Tick (Acari: Ixodidae), Using Multiple Species Distribution Model Approaches.

The American dog tick, Dermacentor variabilis (Say) (Acari: Ixodidae), is a vector for several human disease-causing pathogens such as tularemia, Rocky Mountain spotted fever, and the understudied spotted fever group rickettsiae (SFGR) infection caused by Rickettsia montanensis. It is important for public health planning and intervention to understand the distribution of this tick and pathogen encounter risk. Risk is often described in terms of vector distribution, but greatest risk may be concentrated where more vectors are positive for a given pathogen. When assessing species distributions, the choice of modeling framework and spatial layers used to make predictions are important. We first updated the modeled distribution of D. variabilis and R. montanensis using maximum entropy (MaxEnt), refining bioclimatic data inputs, and including soil variables. We then compared geospatial predictions from five species distribution modeling frameworks. In contrast to previous work, we additionally assessed whether the R. montanensis positive D. variabilis distribution is nested within a larger overall D. variabilis distribution, representing a fitness cost hypothesis. We found that 1) adding soil layers improved the accuracy of the MaxEnt model; 2) the predicted 'infected niche' was smaller than the overall predicted niche across all models; and 3) each model predicted different sizes of suitable niche, at different levels of probability. Importantly, the models were not directly comparable in output style, which could create confusion in interpretation when developing planning tools. The random forest (RF) model had the best measured validity and fit, suggesting it may be most appropriate to these data.

Comparative population genetics of Amblyomma maculatum and Amblyomma americanum in the mid-Atlantic United States.

The Gulf Coast tick, Amblyomma maculatum, is undergoing a northward expansion along the United States East Coast, most recently establishing populations in Virginia, Maryland, and Delaware. This expansion has human health implications, as A. maculatum is the primary natural vector of the bacterium Rickettsia parkeri, which causes a spotted fever-type rickettsiosis. Newly established populations of A. maculatum in Virginia tend to have high prevalence of R. parkeri, compared to lower infection rates in the historical range. The factors contributing to high R. parkeri prevalence in Virginia are not known. Investigating connectivity between sites colonized with A. maculatum can help determine whether sites with higher prevalence are isolated or well-connected through migration, thus serving as a source of infected individuals. We characterized 16S rRNA haplotypes of A. maculatum and, for comparison, the congeneric Amblyomma americanum collected from sites where these species co-occur. We then explored connectivity and genetic structure among Virginia populations using pairwise ΦST and AMOVA analyses. Our study identified one recently restored native grassland site with low A. maculatum haplotype diversity and strong evidence of a founder effect, whereas most sites are haplotypically diverse but with no clear genetic structure or connectivity between sites. These findings contrast with high connectivity and a slight mainland/island structure among A. americanum populations. Our results suggest that A. maculatum populations occasionally arise following long-distance drop-offs of few individual ticks in suitable habitat, but no clear migration patterns were observed. The distinct population genetic patterns between species might result from differences in host utilization.

First report of Candidatus Rickettsia mendelii in Ixodes brunneus from the United States.

Candidatus Rickettsia mendelii is a novel rickettsial species recently identified in Ixodes ricinus. In this study, Ixodes brunneus collected from wild birds (n = 77 ticks) or vegetation (n = 4 ticks) in southeastern Virginia were surveyed for rickettsial agents. Candidatus Rickettsia mendelii was confirmed in I. brunneus through sequencing of the gltA and 16S rRNA genes. This is the first report of this rickettsial species in Ixodes ticks in North America.