Monitoring Human Babesiosis Emergence through Vector Surveillance New England, USA

Maria A. Diuk-Wasser

, Yuchen Liu, Tanner K. Steeves, Corrine Folsom-O’Keefe, Kenneth R. Dardick, Timothy Lepore, Stephen J. Bent, Sahar Usmani-Brown, Sam R. Telford, Durland Fish, and Peter J. Krause

Author affiliations: Yale School of Public Health, New Haven, Connecticut, USA (M.A. Diuk-Wasser, Y. Liu, T.K. Steeves, C. Folsom-O’Keefe,; S.J. Bent, S. Usmani-Brown, D. Fish, P.J. Krause); Uppsala University, Uppsala, Sweden (Y. Liu); Audubon Connecticut, Southbury, Connecticut, USA (C. Folsom-O’Keefe);Mansfield Family Practice, Storrs, Connecticut, USA (K.R. Dardick);Nantucket Cottage Hospital, Nantucket, Massachusetts, USA (T. Lepore); University of Adelaide, Adelaide, South Australia, Australia (S.J. Bent); Tufts University, Boston, Massachusetts, USA (S.R. Telford III); L2 Diagnostics, New Haven (S. Usmani-Brown)

Abstract

Human babesiosis is an emerging tick-borne disease caused by the intraerythrocytic protozoan Babesia microti. Its geographic distribution is more limited than that of Lyme disease, despite sharing the same tick vector and reservoir hosts. The geographic range of babesiosis is expanding, but knowledge of its range is incomplete and relies exclusively on reports of human cases. We evaluated the utility of tick-based surveillance for monitoring disease expansion by comparing the ratios of the 2 infections in humans and ticks in areas with varying B. microti endemicity. We found a close association between human disease and tick infection ratios in long-established babesiosis-endemic areas but a lower than expected incidence of human babesiosis on the basis of tick infection rates in new disease-endemic areas. This finding suggests that babesiosis at emerging sites is underreported. Vector-based surveillance can provide an early warning system for the emergence of human babesiosis.

Human babesiosis is an emerging tick-borne disease in the United States, caused primarily by the intraerythrocytic protozoan Babesia microti and by other Babesia species (1,2). B. microti also may be transmitted through infected blood and is the most commonly reported transfusion-transmitted pathogen in the United Sates (3,4). The outcome of B. microti infection varies from asymptomatic or moderate disease in previously healthy persons to severe and sometimes fatal disease in persons who are elderly or immunocompromised (1). Fatality rates of 6% to 9% have been reported among hospitalized patients and of ≈20% among those who are immunosuppressed or who experience transfusion-transmitted babesiosis (3–7). Although B. microti shares the same tick vector (Ixodes scapularis ticks) and primary reservoir host (Peromyscus leucopus mice) (1,8) as the Lyme disease agent (Borrelia burgdorferi), the number of Lyme disease cases reported nationally in 2011 was ≈25 times greater than that of babesiosis cases. This disparity probably results from the more limited geographic distribution of B. microti,although lower B. microti tick infection prevalence in babesiosis-endemic areas or lower tick-to-human transmission rates may also be contributing factors. Babesiosis has expanded in a pattern similar to that of Lyme disease, albeit at a slower pace (9,10). Both diseases are following the range expansion of I. scapularis ticks over the past 30 years (9,11). If B. microticontinues its current rate of expansion, it may ultimately have the same distribution as B. burgdorferi.

Current knowledge of the geographic range of babesiosis is incomplete and relies exclusively on human case reports. Case reports are poor indicators of risk for babesiosis because of the low index of suspicion on the part of many physicians and the lack of distinctive clinical signs such as the erythema migrans rash of Lyme disease. An alternative approach to determining infection risk is tick-based surveillance, which is likely to be a more sensitive method for identifying areas where babesiosis is emerging and can be used to estimate zoonotic prevalence in established areas. The incidence of tick-borne disease is primarily determined by 2 factors: human–tick contact rates and the proportion of the tick population that is infected (12,13). Human–tick contact rates are difficult to measure accurately because they are highly spatially heterogeneous and are determined by complex interactions between human and tick populations, depending on particular tick densities and human behaviors associated with human exposure.

We proposed an integrative measure of tick-borne disease risk that combines tick infection prevalence and human incidence data for an established disease (Lyme disease) and an emerging disease (babesiosis). We hypothesized that the ratio of human Lyme disease to babesiosis incidence rates (hereafter termed “human ratio”) is directly proportional to the prevalence ratio of I. scapularis ticks infected with B. burgdorferi and that of those infected withB. microti (hereafter termed “tick ratio”) in babesiosis – and Lyme disease–endemic areas. We based this hypothesis on the fact that the ratio of incidence rates for >1 infection transmitted by the same tick should depend only on the ratio of tick infection prevalence with the respective pathogens because human–tick contact rates are the same for both. We further hypothesized that the human ratio would be relatively higher than the tick ratio in areas where babesiosis is newly emerging because of underreporting of emerging disease. Accordingly, we determined the relationship between the human ratio and the tick ratio in regions in southern New England where the disease is endemic and emerging.