Reservoir Competence of Wildlife Host Species for Babesia microti

Michelle H. Hersh

, Michael Tibbetts, Mia Strauss, Richard S. Ostfeld, and Felicia Keesing

Author affiliations: Bard College, Annandale-on-Hudson, New York, USA (M.H. Hersh, M. Tibbetts, M. Strauss, F. Keesing); and Cary Institute of Ecosystem Studies, Millbrook, New York, USA (M.H. Hersh, R.S. Ostfeld)

Abstract

Human babesiosis is an increasing health concern in the northeastern United States, where the causal agent, Babesia microti, is spread through the bite of infected Ixodes scapularis ticks. We sampled 10 mammal and 4 bird species within a vertebrate host community in southeastern New York to quantify reservoir competence (mean percentage of ticks infected by an individual host) using real-time PCR. We found reservoir competence levels >17% in white-footed mice (Peromyscus leucopus), raccoons (Procyon lotor), short-tailed shrews (Blarina brevicauda), and eastern chipmunks (Tamias striatus), and <6 but="but">0% in all other species, including all 4 bird species. Data on the relative contributions of multiple host species to tick infection with B. microti and level of genetic differentiation between B. microti strains transmitted by different hosts will help advance understanding of the spread of human babesiosis.

Human babesiosis is a growing public health concern, especially in the northeastern United States. Babesiosis is a zoonotic, malaria-like illness that can be particularly severe and sometimes fatal in elderly, asplenic, or immunocomprised persons (1). In the lower Hudson Valley region of New York State, 5 locally acquired cases of babesiosis were documented in 2001 (2), and incidence has increased 20-fold from 2001 through 2008 (3).
The causal agent of human babesiosis, Babesia microti (Apicomplexa: Piroplasmida), is a protozoan blood parasite that is transmitted in nature by the bite of an infected tick. In the northeastern United States, the vector of this disease is Ixodes scapularis, the black-legged tick, which is also the primary vector of Borrelia burgdorferi and Anaplasma phagocytophilum, the causal agents of Lyme disease and human granulocytic anaplasmosis, respectively. B. microti is not known to be transmitted transovarially on the basis of available evidence (4–7), indicating that it is not passed from infected adult ticks to eggs, and therefore must be acquired from a blood meal on an infected host. Larval ticks bite infected animals and obtain the pathogen, molt into nymphs, and overwinter. The following year, they then can infect additional hosts when seeking a second blood meal as nymphs or a third blood meal as adults. B. microti has been detected in questing adult and nymphal ticks in studies across the northeastern United States (8–12). In the case of Lyme disease, which is transmitted by the same vector, the nymphal stage is most relevant to human health because bites from nymphs often go undetected and provide greater opportunities to transmit the pathogen (13,14). Babesiosis can also be acquired through blood transfusions, another growing concern for public health (15).
B. microti can infect a range of animal species, but the reservoir competence of many wildlife hosts in the northeastern United States is not well known. We define reservoir competence as the mean percentage of ticks infected by any individual host of a given species. Furthermore, many studies test for the presence of or exposure to the pathogen in host blood or tissue, which provides useful information about host infection, but not information on how often infected animals transmit the pathogen to tick vectors. White-footed mice (Peromyscus leucopus) and meadow voles (Microtus pennsylvanicus) have been established as reservoir hosts on the basis of seroprevalence (16,17), and P. leucopus mice are known to transmit the pathogen to ticks (18). Other rodent species, including species in other genera of mice (Apodemus and Sicista) and voles (Eothenomys, Lagurus, and Myodes) are known hosts in Europe (19–21) and Asia (22–24). B. microti or B. microti–like infection has been observed in other common eastern US mammal species, such as short-tailed shrews (Blarina brevicauda) (25), eastern cottontail rabbits (Sylvilagus floridanus) (17), eastern chipmunks (Tamias striatus) (17), raccoons (Procyon lotor) (26) and foxes (27), and congeneric species in other regions or countries, including Sciurus spp. squirrels (28) and Sorex spp. shrews (29). Birds have not been extensively tested for B. microti, but in Europe, evidence of B. microti infection has recently been discovered in engorged larval ticks that had been feeding on birds of several species (30–32). Determining the role that any of these species play in B. microti dynamics in nature requires information on the rate at which hosts transmit B. microti to tick vectors.
Few systematic surveys have been conducted that compare reservoir competencies of multiple potential host species for B. microti. Testing a broad sample of wildlife species would enable us not only to identify which species transmit the pathogen, but also which species act as weakly competent or incompetent hosts, providing blood meals to ticks but rarely or never transmitting the pathogen (33). Infection of nymphs by other tickborne pathogens, such as B. burgdorferi, is affected by the presence of strongly and weakly competent reservoir hosts in the same communities (34,35). On Nantucket Island, an area well studied for B. microti, multiple hosts transmit the pathogen but differ in infection prevalence (17). Although several studies have extensively sampled small mammal communities for seroprevalence of B. microti (19–23), comprehensive surveys of more diverse host communities, for either seroprevalence or reservoir competence, are rare.
In this study, we sought to determine the level of reservoir competence for B. microti for as many host species as possible in a babesiosis-endemic region (Dutchess County, New York) where human babesiosis cases are rapidly increasing (3). We designed and tested a real-time PCR method to determine whether ticks were infected with B. microti. To determine the relative levels of reservoir competence in as many potential host species as possible, we applied this method to sample newly molted nymphal ticks that fed as larvae on a range of potential wildlife hosts. We tested the hypothesis that white-footed mice (P. leucopus) were the predominant host of B. microti in this community. We also compared these results to levels of prevalence in questing nymphal ticks from the same region. Our overall goal was to improve understanding of the role of multiple wildlife host species in B. microti transmission.