Amy J. Kuenzi

DEMOGRAPHIC FACTORS ASSOCIATED WITH PREVALENCE OF ANTIBODY TO SIN NOMBRE VIRUS IN DEER MICE IN THE WESTERN UNITED STATES

We used long-term data collected for up to 10 yr (1994–2004) at 23 trapping arrays (i.e., webs and grids) in Arizona, Colorado, Montana, and New Mexico to examine demographic factors known or suspected to be associated with risk of infection with Sin Nombre virus (SNV) in its natural host, the deer mouse (Peromyscus maniculatus). Gender, age (mass), wounds or scars, season, and local relative population densities were statistically associated with the period prevalence of antibody (used as a marker of infection) to SNV in host populations. Nevertheless, antibody prevalence and some of the risk factors associated with antibody prevalence, such as relative population density, gender bias, and prevalence of wounding, varied significantly among sites and even between nearby trapping arrays at a single site. This suggests that local microsite-specific differences play an important role in determining relative risk of infection by SNV in rodents and, consequently, in humans. Deer mouse relative population density varied among sites and was positively and statistically associated with infection prevalence, an association that researchers conducting shorter-term studies failed to demonstrate. Both wounding and antibody prevalence increased with mass class in both males and females; this increase was much more pronounced in males than in females and wounding was more frequent in adult males than in adult females. Prevalence of wounding was greatest among seropositive deer mice, regardless of mass class, but many deer mice without detectable wounds or scars eventually became infected. Many of these patterns, which will be useful in the development of predictive models of disease risk to humans, were only detected through the application of data collected over a long (10-yr) period and with abundant replication.

A longitudinal study of Sin Nombre virus prevalence in rodents, southeastern Arizona.

We determined the prevalence of Sin Nombre virus antibodies in small mammals in southeastern Arizona. Of 1,234 rodents (from 13 species) captured each month from May through December 1995, only mice in the genus Peromyscus were seropositive. Antibody prevalence was 14.3% in 21 white-footed mice (P. leucopus), 13.3% in 98 brush mice (P. boylii), 0.8% in 118 cactus mice (P. eremicus), and 0% in 2 deer mice (P. maniculatus). Most antibody-positive mice were adult male Peromyscus captured close to one another early in the study. Population dynamics of brush mice suggest a correlation between population size and hantavirus-antibody prevalence.

LONG-TERM DYNAMICS OF SIN NOMBRE VIRAL RNA AND ANTIBODY IN DEER MICE IN MONTANA

Infections with hantaviruses in the natural host rodent may result in persistent, asymptomatic infections involving shedding of virus into the environment. Laboratory studies have partially characterized the acute and persistent infection by Sin Nombre virus (SNV) in its natural host, the deer mouse (Peromyscus maniculatus). However, these studies have posed questions that may best be addressed using longitudinal studies involving sequential sampling of individual wild-caught, naturally infected mice. Using enzyme immunoassay and polymerase chain reaction (PCR) analysis of monthly blood samples, we followed the infection status of deer mice in a mark-recapture study in Montana for 2 yr. Only six of 907 samples without IgG antibody to SNV contained detectable SNV RNA, suggesting that there is a very brief period of viremia before the host develops detectable antibody. The simultaneous presence of both antibody and viral RNA in blood was detected in consecutive monthly samples for as long as 3 mo. However, chronic infection was typified by alternating characteristics of PCR positivity and PCR negativity. Two possible interpretations of these results are that 1) viral RNA may be consistently present in the blood of chronically infected deer mouse, but that viral RNA is near the limits of PCR detectability or 2) SNV RNA sporadically appears in blood as a consequence of unknown physiological events. The occurrence of seasonal patterns in the proportion of samples that contains antibody and that also contained SNV RNA demonstrated a temporal association between recent infection (antibody acquisition) and presence of viral RNA in blood.

Translocation as a nonlethal alternative for managing California ground squirrels

To evaluate the efficacy of translocation as a nonlethal management alternative, we determined trapability, post-release survival, site fidelity, and homing ability of experimentally translocated California ground squirrels (Spermophilus beecheyi). Trapability of squirrels was low (0.04 captures/trap-day). Most squirrels (71-79%) survived until ≥18 days after translocation; mortality was highest shortly after release, and was attributed mostly to predation. Of those squirrels that survived but did not return home, 85% established a new home range, but most settled away from the release site. Homing success decreased with translocation distance. Our data do not support the hypothesis that homing results from navigation, but they do support the hypothesis that homing results from piloting when squirrels are inside their area of familiarity, perhaps extended by visual detection of distant landmarks, and random search when outside. Translocation probably is infeasible for control of squirrels over large areas because of low trapability, but shows potential for smaller localities. Squirrels, however, must be translocated far enough (ca. 1,500 m) to prevent homing, and lack of fidelity to the release site may result in squirrels settling in undesirable locations.

Temporal patterns of bat activity in Southern Arizona

Knowledge of temporal variation in bat activity within an area is an essential component in designing bat surveys. Yet few studies have thoroughly examined this aspect of bat biology. We measured bat activity at 3 temporal scales in the southern Arizona Sonoran Desert to develop recommendations for designing bat inventory programs and to provide baseline data on activity within this region. We studied bat temporal activity at 17 water sources from May 1995-August 1996 using mistnets and ultrasonic detectors. Indices of bat activity were higher during the reproductive season (May-Aug) than the nonreproductive season (Sep-Apr). Bat activity did not differ between any of the 2-week time periods within the reproductive season. We found that the pattern of bat activity over the course of the night differed by season and year within seasons. Our results indicate that it is important to determine bat activity in an area before designing bat surveys. Activity measured in a portion of the night may not always reflect total activity. We recommend that when possible, activity should be monitored throughout the night.

Environmental monitoring to enhance comprehension and control of infectious diseases

In a world of emerging and resurging infectious diseases, dominated by zoonoses, environmental monitoring plays a vital role in our understanding their dynamics and their spillover to humans. Here, we critically review the ecology, epidemiology and need for monitoring of a variety of directly transmitted (Sin Nombre virus, Avian Influenza) and vector-borne (Ross River virus, West Nile virus, Lyme disease, anaplasmosis and babesiosis) zoonoses. We focus on the valuable role that existing monitoring plays in the understanding of these zoonoses, the demands for new monitoring, and how improvements can be made to existing monitoring. We also identify the fruitful outcomes which would result from implementation of the monitoring demands we have highlighted. This review aims to promote improvements in our understanding of zoonoses, their management, and public health by encouraging discussion among researchers and public health officials.

Deer Mouse Movements in Peridomestic and Sylvan Settings in Relation to Sin Nombre Virus Antibody Prevalence

Prevalence of antibody to Sin Nombre virus (SNV) has been found to be nearly twice as high in deer mice (Peromyscus maniculatus) in peridomestic settings as in sylvan settings in two studies in Montana and one in New Mexico. We investigated whether this difference may be related to a difference in deer mouse movements in the two settings. We used radiotelemetry to determine home range size and length of movement for 22 sylvan (1991–1992) and 40 peridomestic deer mice (1995–1999). We also determined the percentage of locations inside versus outside of buildings for peridomestic mice. Though variable, average home range size for female deer mice was significantly smaller for peridomestic deer mice than for sylvan deer mice. The smaller home range in peridomestic settings may concentrate shed SNV, and protection from solar ultraviolet radiation inside buildings may increase environmental persistence of SNV. Both these factors could lead to increased SNV exposure of deer mice within peridomestic populations and result in higher antibody prevalence. Peridomestic deer mice moved between buildings and outside areas, which is evidence that SNV can be transmitted between peridomestic and sylvan populations.

Seroprevalence Against Sin Nombre Virus in Resident and Dispersing Deer Mice

Through dispersal, deer mice (Peromyscus maniculatus) enter peridomestic settings (e.g., outbuildings, barns, cabins) and expose humans and other deer mouse populations to Sin Nombre virus (SNV). In June 2004, research on deer mouse dispersal was initiated at 2 locations in Montana. During the course of the study, over 6000 deer mouse movements were recorded, and more than 1000 of these movements were classified as dispersal movements. More than 1700 individual deer mice were captured and tested for SNV, revealing an average SNV antibody prevalence of approximately 11%. Most of the dispersing and antibody-positive individuals were adult males. Among the few subadult dispersing mice discovered during the study, none were seropositive for SNV. Our results suggest that dispersal rates are higher in high abundance populations of deer mice and that during peak times of dispersal, human exposure to SNV, which commonly occurs in peridomestic settings, could increase.

DELAYED DENSITY-DEPENDENT PREVALENCE OF SIN NOMBRE VIRUS INFECTION IN DEER MICE (PEROMYSCUS MANICULATUS) IN CENTRAL AND WESTERN MONTANA

Understanding how transmission of zoonoses takes place within reservoir populations, such as Sin Nombre virus (SNV) among deer mice (Peromyscus maniculatus), is important in determining the risk of exposure to other hosts, including humans. In this study, we examined the relationship between deer mouse populations and the prevalence of antibodies to SNV, a system where the effect of host population abundance on transmission is debated. We examined the relationship between abundance of deer mice in late summer–early autumn and SNV antibody prevalence the following spring–early summer (termed delayed density-dependent [DDD] prevalence of infection) at both regional and local scales, using 12 live-trapping grids for 11–14 yr, across central and western Montana. When all trapping grids were combined (regional scale), there was a significant DDD relationship for individual months and when months within seasons were averaged. However, within individual grids (local scale), evidence of DDD prevalence of infection was observed consistently at only one location. These findings suggest that, although there is evidence of DDD prevalence of infection at regional scales, it is not always apparent at local scales, possibly because the regional pattern of DDD infection prevalence is driven by differences in abundance and prevalence among sites, rather than in autumn-spring delays. Transmission of SNV may be more complex than the original hypothesis of autumn-spring delayed density dependence suggests. This complexity is also supported by recent modeling studies. Empirical investigations are needed to determine the duration and determinants of time-lagged abundance and antibody prevalence. Our study suggests predicting local, human exposure risk to SNV in spring, based on deer mouse abundance in autumn, is unlikely to be a reliable public health tool, particularly at local scales.

Transmission Ecology of Sin Nombre Hantavirus in Naturally Infected North American Deermouse Populations in Outdoor Enclosures

Sin Nombre hantavirus (SNV), hosted by the North American deermouse (Peromyscus maniculatus), causes hantavirus pulmonary syndrome (HPS) in North America. Most transmission studies in the host were conducted under artificial conditions, or extrapolated information from mark-recapture data. Previous studies using experimentally infected deermice were unable to demonstrate SNV transmission. We explored SNV transmission in outdoor enclosures using naturally infected deermice. Deermice acquiring SNV in enclosures had detectable viral RNA in blood throughout the acute phase of infection and acquired significantly more new wounds (indicating aggressive encounters) than uninfected deermice. Naturally-infected wild deermice had a highly variable antibody response to infection, and levels of viral RNA sustained in blood varied as much as 100-fold, even in individuals infected with identical strains of virus. Deermice that infected other susceptible individuals tended to have a higher viral RNA load than those that did not infect other deermice. Our study is a first step in exploring the transmission ecology of SNV infection in deermice and provides new knowledge about the factors contributing to the increase of the prevalence of a zoonotic pathogen in its reservoir host and to changes in the risk of HPS to human populations. The techniques pioneered in this study have implications for a wide range of zoonotic disease studies.