Dissertation/Thesis Abstract

Neglected Components of Tick-Borne Disease in the Western United States
by Stephenson, Nicole, Ph.D., University of California, Davis, 2016, 145; 10182831
Abstract (Summary)

Across much of the world, tick-borne disease is an emerging problem in people, domestic animals, and wildlife, with hundreds of thousands of cases each year in the United States alone. However, numerous aspects of the sylvatic cycles of these diseases remain poorly understood, despite extensive surveillance and research programs in many states targeting human cases and testing of wildlife and ticks. In the western US, tick-borne disease ecology is particularly complex due to the diversity of pathogens present, potential vectors, and host species. Although the pathogens that cause Lyme borreliosis, granulocytic anaplasmosis and spotted fever are common in both wildlife and tick vectors in rural northern California, we have limited understanding of how diverse strains and pathogens interact with environmental, host, and vector determinants in the epidemiological triad and how this affects human disease risk. Lack of insight into the epidemiologic dynamics of these diseases precludes progress in protecting at-risk people. Most research in the western US has focused on Borrelia burgdorferi, the agent of Lyme borreliosis and its vector Ixodes pacificus, in wildlife and the general human population. Here we focus on some of the neglected components of this vector-pathogen-host system in the western US. First we investigate a rarely studied tick species, I. angustus, which has been implicated in a case of Lyme disease in Washington State and has been shown to be vector competent for B. burgdorferi in experimental studies. Next, we focus on the presence of a cryptic group of bacterial Rickettsia spp. in a community of people, domestic animals and human biting arthropod vectors, which have diverse clinical outcomes and are often mis- or underdiagnosed. Lastly, we examine a socioeconomically disadvantaged and medically underserved, rural community of people and their domestic animals with high risk for tick-borne diseases.

Ixodes angustus is vector-competent experimentally for the bacterial pathogen Borrelia burgdorferi sensu stricto and may also be capable of transmitting Anaplasma phagocytophilum, the etiologic agent of granulocytic anaplasmosis. Of 261 I. angustus ticks collected throughout California study sites, the most common hosts were tree squirrels (20% of attached ticks) and chipmunks (37%), but ground dwelling small mammal species (43%) also served as hosts. Estimated PCR-prevalence of for A. phagocytophilum and B. burgdorferi in ticks was 2% and zero respectively, and the minimum infection prevalence was 10% for Candidatus Rickettsia angustus, a putative endosymbiont. When host species within each study site were included in a zero-inflated negative binomial generalized linear mixed model as nested random effects, the best-fitting model for I. angustus abundance included decreasing monthly mean minimum temperature and increasing latitude as fixed effects. Together with published data, these findings suggest that I. angustus is a host generalist, has a broad geographic distribution and has the potential to play a role as a vector of A. phagocytophilum and B. burgdorferi. Because I. angustus appears to be rarely infected, it might serve as a dilution vector if in competition with more competent vectors, such as I. pacificus.

Members of the spotted fever group of rickettsias can cause various clinical outcomes in people and are diagnostically challenging. Several species may co-circulate in sylvatic cycles and can infect human-biting vectors. Here we document exposure to rickettsial pathogens in people and domestic animals in a rural community. Despite a seroprevalence of 3% in people, 42% in dogs, 79% in cats, 33% in gray foxes, and 83% in bobcats, RT-PCR on blood was consistently negative, likely because the sensitivity of this test is low, as Rickettsia spp. do not often circulate in high numbers in the blood. Rickettsia spp. DNA was found in four flea species collected from bobcats and Ctenocephalides felis collected from domestic dogs. All amplicons sequenced from fleas were R. felis. Ixodes pacificus collected by flagging were commonly infected with a Rickettsia sp. endosymbiont. Rickettsia rhipicephali DNA was found in Dermacentor variabilis ticks from dogs, black bears, a gray fox, and a D. occidentalis collected by flagging. Dermacentor variabilis from dogs and black bears also contained R. montanensis DNA. Multiple Rickettsia spp. (including species with zoonotic and pathogenic potential) were found among human biting arthropod vectors of both wild and domestic carnivores and on flags. Knowledge of the diversity of Rickettsia spp. that is present within arthropod vectors to which people and domestic animals are exposed is an essential first step is making an accurate diagnosis and in better understanding the epidemiology of these potential pathogens. Within-host and vector interaction among these species may play a role in spillover into human and domestic animals.

Rural residents can suffer from a variety of health disparities including limited access to health care and lower socioeconomic status, which can result in poorer health status, shorter life expectancy, higher infant mortality, and higher prevalence of obesity. Humboldt County residents may be at increased risk of tick bites either at their residences or during occupational or recreational activities that bring them into contact with tick-infested habitat. We administered a questionnaire to Humboldt County residents to gather basic demographic information, history of previous testing or diagnosis with tick-borne diseases, history of exposure to ticks, development of symptoms after a tick bite, exposure to domestic animals and wildlife, and participation in outdoor activities. We also collected blood samples from some of the participants and their domestic animals for testing for Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, and Rickettsia spp. infection and exposure by PCR and serology, respectively. Our study participants tended to have low socioeconomic status (42% of participants reported a median household income of <$25,000), commonly experienced tick bites (81% reported tick bites), and despite experiencing symptoms of tick-borne illness after a bite, usually were not tested for tick-borne diseases. Risk of self-reported tick bites increased with age (beta=0.5, p<0.001), time spent watching birds or other wildlife (beta=0.2, p=0.009), and time spent hiking (beta=0.2, p=0.028). We also documented seropositivity for exposure to all tick-borne diseases we tested for in both people and domestic animals and risk was increased in people that had a bird feeder (beta=1.3, p=0.036). These results highlight the importance of research in rural communities that suffer from health disparities and may be at increased risk for tick-borne diseases, and that public health and medical care for underserved residents should incorporate proactive outreach about tick-borne disease risk for residents and doctors.

Indexing (document details)
Advisor: Foley, Janet
Commitee: Clifford, Deana, Martinez-Lopez, Beatriz
School: University of California, Davis
Department: Epidemiology
School Location: United States -- California
Source: DAI-B 78/03(E), Dissertation Abstracts International
Subjects: Entomology, Public health, Epidemiology
Keywords: Anaplasmosis, Borreliosis, Disease, Rickettsiosis, Ticks
Publication Number: 10182831
ISBN: 9781369311464