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Dennis M. Heisey

Publications and source records attributed to Dennis M. Heisey.

At least 19 recordsLinked to original sources

Applying a Bayesian weighted surveillance approach to detect chronic wasting disease in white‐tailed deer

Surveillance is critical for early detection of emerging and re‐emerging infectious diseases. Weighted surveillance leverages heterogeneity in infection risk to increase sampling efficiency. Here, we apply a Bayesian approach to estimate weights for 16 surveillance classes of white‐tailed deer in Wisconsin, USA, relative to hunter‐harvested yearling males. We used these weights to conduct a surveillance programme for detecting chronic wasting disease (CWD) in white‐tailed deer at Shenandoah National Park (SHEN) in Virginia, USA. Generally, for surveillance, risk of infection increased with age and was greater in males. Clinical suspect deer had the highest risk, with weight estimates of 33.33 and 9.09 for community‐reported and hunter‐reported suspect deer, respectively. Fawns had the lowest risk with an estimated weight of 0.001. We used surveillance weights for Wisconsin deer to determine sampling effort required to detect a CWD‐positive case in SHEN if prevalence in yearling males ≥0.025. The sampling required to detect CWD was 37–91 adult deer, depending on the adult male:female ratio in the surveillance stream. We collected rectal biopsies from 49 female and 21 male adult deer, and 10 additional samples from vehicle‐killed deer. CWD was not detected and we concluded with 95% probability that prevalence in the reference population (yearling males) was between 0.0% and 3.6%. Synthesis and applications . Our approach allows managers to estimate relative surveillance weights for different host classes and quantify limits of disease detection in real time when only a sample of animals from a population can be tested, resulting in considerable cost savings for agencies performing wildlife disease detection surveillance. Additionally, it provides a rigorous means of estimating prevalence limits when a disease/pathogen is not detected in a sample set. It is therefore applicable to other wildlife, domestic animal and human disease systems, which can be characterized by surveillance classes with heterogeneous probability of infection. This methodology is also extendable to other disciplines such as invasive species, environmental toxicology, and generally, any ecological question seeking to efficiently use scarce financial and human resources to maximize the detection probability of a rare event.

Journal of Applied Ecology

Survival of female mallards along the Vermont-Quebec border region

Understanding effects of location and timing of harvest seasons on mortality of ducks and geese from hunting is important in forming regulations that sustain viable waterfowl populations throughout their range. During 1990 and 1991 we alternately marked 80 hatching year (HY), female mallards along the Vermont–Quebec border; half with radio-transmitters and bands and half with only aluminum leg bands. We monitored radio-marked ducks daily and recorded survival status weekly for 15 weeks from August until December each year. Mallard mortalities began 25 September when the hunting season opened in the Province of Quebec, Canada. Overall survival of mallards at week 10 did not differ between years (0.51 in 1990 vs. 0.43 in 1991) or differ from that of HY American black ducks (0.44 females, 0.42 males) based on proportional hazard analysis in a Bayesian framework. The mortality rates for mallards from hunting (0.47) and causes unrelated to hunting (0.06) were similar between years and to those rates for HY black ducks at that same site. Hunter harvest accounted for most of the mortality recorded during this study and illegal feeding (i.e., baiting) at sites just before and during the hunting season was observed. Females with lower body condition index had greater mortality rates; a 1-standard-deviation increase in condition index would reduce mortality hazard by about 29%. Management options that may increase mallard survival in the area include lowering daily bag limit in Quebec and suspending split hunting seasons in Vermont that increase harvest, delaying opening date of hunting in Quebec to allow for increased body condition before hunting season opens, and improving enforcement of baiting restrictions.

Quebec, Vermont

Mortality patterns and detection bias from carcass data: An example from wolf recovery in Wisconsin

We developed models and provide computer code to make carcass recovery data more useful to wildlife managers. With these tools, wildlife managers can understand the spatial, temporal (e.g., across time periods, seasons), and demographic patterns in mortality causes from carcass recovery datasets. From datasets of radio-collared and non-collared carcasses, managers can calculate the detection bias by mortality cause in a non-collared carcass dataset compared to a collared carcass dataset. As a first step, we provide a standard procedure to assign mortality causes to carcasses. We provide an example of these methods for radio-collared wolves ( n  = 208) and non-collared wolves ( n  = 668) found dead in Wisconsin (1979–2012). We analyzed differences in mortality cause relative to season, age and sex classes, wolf harvest zones, and recovery phase (1979–1995: initial recovery, 1996–2002: early growth, 2003–2012: late growth). Seasonally, illegal kills and natural deaths were proportionally higher in winter (Oct–Mar) than summer (Apr–Sep) for collared wolves, whereas vehicle strikes and legal kills were higher in summer than winter. Spatially, more illegally killed collared wolves occurred in eastern wolf harvest zones where wolves reestablished more slowly and in the central forest region where optimal habitat is isolated by agriculture. Natural mortalities of collared wolves (e.g., disease, intraspecific strife, or starvation) were highest in western wolf harvest zones where wolves established earlier and existed at higher densities. Calculating detection bias in the non-collared dataset revealed that more than half of the non-collared carcasses on the landscape are not found. The lowest detection probabilities for non-collared carcasses (0.113–0.176) occurred in winter for natural, illegal, and unknown mortality causes.

Wisconsin

Estimating the phenology of elk brucellosis transmission with hierarchical models of cause-specific and baseline hazards

Understanding the seasonal timing of disease transmission can lead to more effective control strategies, but the seasonality of transmission is often unknown for pathogens transmitted directly. We inserted vaginal implant transmitters (VITs) in 575 elk ( Cervus elaphus canadensis ) from 2006 to 2014 to assess when reproductive failures (i.e., abortions or still births) occur, which is the primary transmission route of Brucella abortus , the causative agent of brucellosis in the Greater Yellowstone Ecosystem. Using a survival analysis framework, we developed a Bayesian hierarchical model that simultaneously estimated the total baseline hazard of a reproductive event as well as its 2 mutually exclusive parts (abortions or live births). Approximately, 16% (95% CI = 0.10, 0.23) of the pregnant seropositive elk had reproductive failures, whereas 2% (95% CI = 0.01, 0.04) of the seronegative elk had probable abortions. Reproductive failures could have occurred as early as 13 February and as late as 10 July, peaking from March through May. Model results suggest that less than 5% of likely abortions occurred after 6 June each year and abortions were approximately 5 times more likely in March, April, or May compared to February or June. In western Wyoming, supplemental feeding of elk begins in December and ends during the peak of elk abortions and brucellosis transmission (i.e., Mar and Apr). Years with more snow may enhance elk-to-elk transmission on supplemental feeding areas because elk are artificially aggregated for the majority of the transmission season. Elk-to-cattle transmission will depend on the transmission period relative to the end of the supplemental feeding season, elk seroprevalence, population size, and the amount of commingling. Our statistical approach allowed us to estimate the probability density function of different event types over time, which may be applicable to other cause-specific survival analyses. It is often challenging to assess the cause of death, or in this case whether the reproductive event was an abortion or live birth. Accounting for uncertainty in the event type is an important future addition to our methodological approach.

Wyoming

Integrated survival analysis using an event-time approach in a Bayesian framework

Event-time or continuous-time statistical approaches have been applied throughout the biostatistical literature and have led to numerous scientific advances. However, these techniques have traditionally relied on knowing failure times. This has limited application of these analyses, particularly, within the ecological field where fates of marked animals may be unknown. To address these limitations, we developed an integrated approach within a Bayesian framework to estimate hazard rates in the face of unknown fates. We combine failure/survival times from individuals whose fates are known and times of which are interval-censored with information from those whose fates are unknown, and model the process of detecting animals with unknown fates. This provides the foundation for our integrated model and permits necessary parameter estimation. We provide the Bayesian model, its derivation, and use simulation techniques to investigate the properties and performance of our approach under several scenarios. Lastly, we apply our estimation technique using a piece-wise constant hazard function to investigate the effects of year, age, chick size and sex, sex of the tending adult, and nesting habitat on mortality hazard rates of the endangered mountain plover (Charadrius montanus) chicks. Traditional models were inappropriate for this analysis because fates of some individual chicks were unknown due to failed radio transmitters. Simulations revealed biases of posterior mean estimates were minimal (&le; 4.95%), and posterior distributions behaved as expected with RMSE of the estimates decreasing as sample sizes, detection probability, and survival increased. We determined mortality hazard rates for plover chicks were highest at <5 days old and were lower for chicks with larger birth weights and/or whose nest was within agricultural habitats. Based on its performance, our approach greatly expands the range of problems for which event-time analyses can be used by eliminating the need for having completely known fate data.

Ecology and Evolution

Experimental infection of meadow voles ( Microtus pennsylvanicus ) with sheep scrapie

Meadow voles (Microtus pennsylvanicus) are permissive to chronic wasting disease (CWD) infection, but their susceptibility to other transmissible spongiform encephalopathies (TSEs) is poorly characterized. In this initial study, we intracerebrally challenged 6 meadow voles with 2 isolates of sheep scrapie. Three meadow voles acquired a TSE after the scrapie challenge and an extended incubation period. The glycoform profile of proteinase K-resistant prion protein (PrP(res)) in scrapie-sick voles remained similar to the sheep inocula, but differed from that of voles clinically affected by CWD. Vacuolization patterns and disease-associated prion protein (PrP(Sc)) deposition were generally similar in all scrapie-affected voles, except in the hippocampus, where PrP(Sc) staining varied markedly among the animals. Our results demonstrate that meadow voles can acquire a TSE after intracerebral scrapie challenge and that this species could therefore prove useful for characterizing scrapie isolates.

Canadian Journal of Veterinary Research

Using auxiliary information to improve wildlife disease surveillance when infected animals are not detected: A Bayesian approach

There are numerous situations in which it is important to determine whether a particular disease of interest is present in a free-ranging wildlife population. However adequate disease surveillance can be labor-intensive and expensive and thus there is substantial motivation to conduct it as efficiently as possible. Surveillance is often based on the assumption of a simple random sample, but this can almost always be improved upon if there is auxiliary information available about disease risk factors. We present a Bayesian approach to disease surveillance when auxiliary risk information is available which will usually allow for substantial improvements over simple random sampling. Others have employed risk weights in surveillance, but this can result in overly optimistic statements regarding freedom from disease due to not accounting for the uncertainty in the auxiliary information; our approach remedies this. We compare our Bayesian approach to a published example of risk weights applied to chronic wasting disease in deer in Colorado, and we also present calculations to examine when uncertainty in the auxiliary information has a serious impact on the risk weights approach. Our approach allows “apples-to-apples” comparisons of surveillance efficiencies between units where heterogeneous samples were collected

PLoS ONE

Red-backed vole brain promotes highly efficient in vitro amplification of abnormal prion protein from macaque and human brains infected with variant Creutzfeldt-Jakob disease agent.

Rapid antemortem tests to detect individuals with transmissible spongiform encephalopathies (TSE) would contribute to public health. We investigated a technique known as protein misfolding cyclic amplification (PMCA) to amplify abnormal prion protein (PrP TSE ) from highly diluted variant Creutzfeldt-Jakob disease (vCJD)-infected human and macaque brain homogenates, seeking to improve the rapid detection of PrP TSE in tissues and blood. Macaque vCJD PrP TSE did not amplify using normal macaque brain homogenate as substrate (intraspecies PMCA). Next, we tested interspecies PMCA with normal brain homogenate of the southern red-backed vole (RBV), a close relative of the bank vole, seeded with macaque vCJD PrP TSE . The RBV has a natural polymorphism at residue 170 of the PrP-encoding gene (N/N, S/S, and S/N). We investigated the effect of this polymorphism on amplification of human and macaque vCJD PrP TSE . Meadow vole brain (170N/N PrP genotype) was also included in the panel of substrates tested. Both humans and macaques have the same 170S/S PrP genotype. Macaque PrP TSE was best amplified with RBV 170S/S brain, although 170N/N and 170S/N were also competent substrates, while meadow vole brain was a poor substrate. In contrast, human PrP TSE demonstrated a striking narrow selectivity for PMCA substrate and was successfully amplified only with RBV 170S/S brain. These observations suggest that macaque PrP TSE was more permissive than human PrP TSE in selecting the competent RBV substrate. RBV 170S/S brain was used to assess the sensitivity of PMCA with PrP TSE from brains of humans and macaques with vCJD. PrP TSE signals were reproducibly detected by Western blot in dilutions through 10 -12 of vCJD-infected 10% brain homogenates. This is the first report showing PrP TSE from vCJD-infected human and macaque brains efficiently amplified with RBV brain as the substrate. Based on our estimates, PMCA showed a sensitivity that might be sufficient to detect PrP TSE in vCJD-infected human and macaque blood.

PLoS ONE

Underestimating the effects of spatial heterogeneity due to individual movement and spatial scale: infectious disease as an example

Many ecological and epidemiological studies occur in systems with mobile individuals and heterogeneous landscapes. Using a simulation model, we show that the accuracy of inferring an underlying biological process from observational data depends on movement and spatial scale of the analysis. As an example, we focused on estimating the relationship between host density and pathogen transmission. Observational data can result in highly biased inference about the underlying process when individuals move among sampling areas. Even without sampling error, the effect of host density on disease transmission is underestimated by approximately 50 % when one in ten hosts move among sampling areas per lifetime. Aggregating data across larger regions causes minimal bias when host movement is low, and results in less biased inference when movement rates are high. However, increasing data aggregation reduces the observed spatial variation, which would lead to the misperception that a spatially targeted control effort may not be very effective. In addition, averaging over the local heterogeneity will result in underestimating the importance of spatial covariates. Minimizing the bias due to movement is not just about choosing the best spatial scale for analysis, but also about reducing the error associated with using the sampling location as a proxy for an individual’s spatial history. This error associated with the exposure covariate can be reduced by choosing sampling regions with less movement, including longitudinal information of individuals’ movements, or reducing the window of exposure by using repeated sampling or younger individuals.

Landscape Ecology

Wildlife contact analysis: Emerging methods, questions, and challenges

Recent technological advances, such as proximity loggers, allow researchers to collect complete interaction histories, day and night, among sampled individuals over several months to years. Social network analyses are an obvious approach to analyzing interaction data because of their flexibility for fitting many different social structures as well as the ability to assess both direct contacts and indirect associations via intermediaries. For many network properties, however, it is not clear whether estimates based upon a sample of the network are reflective of the entire network. In wildlife applications, networks may be poorly sampled and boundary effects will be common. We present an alternative approach that utilizes a hierarchical modeling framework to assess the individual, dyadic, and environmental factors contributing to variation in the interaction rates and allows us to estimate the underlying process variation in each. In a disease control context, this approach will allow managers to focus efforts on those types of individuals and environments that contribute the most toward super-spreading events. We account for the sampling distribution of proximity loggers and the non-independence of contacts among groups by only using contact data within a group during days when the group membership of proximity loggers was known. This allows us to separate the two mechanisms responsible for a pair not contacting one another: they were not in the same group or they were in the same group but did not come within the specified contact distance. We illustrate our approach with an example dataset of female elk from northwestern Wyoming and conclude with a number of important future research directions.

Behavioral Ecology and Sociobiology

The effect of swab sample choice on the detection of avian influenza in apparently healthy wild ducks

Historically, avian influenza viruses have been isolated from cloacal swab specimens, but recent data suggest that the highly pathogenic avian influenza (HPAI) H5N1 virus can be better detected from respiratory tract specimens. To better understand how swab sample type affects the detection ability of low pathogenic avian influenza (LPAI) viruses we collected and tested four swab types: oropharyngeal swabs (OS), cloacal swabs (CS), the two swab types combined in the laboratory (LCS), and the two swab types combined in the field (FCS). A total of 1968 wild waterfowl were sampled by each of these four methods and tested for avian influenza virus using matrix gene reverse-transcription (RT)-PCR. The highest detection rate occurred with the FCS (4.3%) followed by the CS (4.0%). Although this difference did not achieve traditional statistical significance, Bayesian analysis indicated that FCS was superior to CS with an 82% probability. The detection rates for both the LCS (2.4%) and the OS (0.4%) were significantly different from the FCS. In addition, every swab type that was matrix RT-PCR positive was also tested for recovery of viable influenza virus. This protocol reduced the detection rate, but the ordering of swab types remained the same: 1.73% FCS, 1.42% CS, 0.81% LCS, and 0% OS. Our data suggest that the FCS performed at least as well as any other swab type for detecting LPAI viruses in the wild ducks tested. When considering recent studies showing that HPAI H5N1 can be better detected in the respiratory tract, the FCS is the most appropriate sample to collect for HPAI H5N1 surveillance while not compromising LPAI studies.

California, Colorado, North Dakota

Modeling routes of chronic wasting disease transmission: Environmental prion persistence promotes deer population decline and extinction

Chronic wasting disease (CWD) is a fatal disease of deer, elk, and moose transmitted through direct, animal-to-animal contact, and indirectly, via environmental contamination. Considerable attention has been paid to modeling direct transmission, but despite the fact that CWD prions can remain infectious in the environment for years, relatively little information exists about the potential effects of indirect transmission on CWD dynamics. In the present study, we use simulation models to demonstrate how indirect transmission and the duration of environmental prion persistence may affect epidemics of CWD and populations of North American deer. Existing data from Colorado, Wyoming, and Wisconsin's CWD epidemics were used to define plausible short-term outcomes and associated parameter spaces. Resulting long-term outcomes range from relatively low disease prevalence and limited host-population decline to host-population collapse and extinction. Our models suggest that disease prevalence and the severity of population decline is driven by the duration that prions remain infectious in the environment. Despite relatively low epidemic growth rates, the basic reproductive number, R0, may be much larger than expected under the direct-transmission paradigm because the infectious period can vastly exceed the host's life span. High prion persistence is expected to lead to an increasing environmental pool of prions during the early phases (i.e. approximately during the first 50 years) of the epidemic. As a consequence, over this period of time, disease dynamics will become more heavily influenced by indirect transmission, which may explain some of the observed regional differences in age and sex-specific disease patterns. This suggests management interventions, such as culling or vaccination, will become increasingly less effective as CWD epidemics progress.

Colorado, Wisconsin, Wyoming

Alteration of the chronic wasting disease species barrier by in vitro prion amplification

Chronic wasting disease (CWD) is a transmissible spongiform encephalopathy (TSE) of cervids now detected in 19 states of the United States, three Canadian provinces, and South Korea. Whether noncervid species can be infected by CWD and thereby serve as reservoirs for the infection is not known. To investigate this issue, we previously used serial protein misfolding cyclic amplification (sPMCA) to demonstrate that CWD prions can amplify in brain homogenates from several species sympatric with cervids, including prairie voles ( Microtus ochrogaster ) and field mice ( Peromyscus spp. ). Here, we show that prairie voles are susceptible to mule deer CWD prions in vivo and that sPMCA amplification of CWD prions in vole brain enhances the infectivity of CWD for this species. Prairie voles inoculated with sPMCA products developed clinical signs of TSE disease approximately 300 days prior to, and more consistently than, those inoculated with CWD prions from deer brain. Moreover, the deposition patterns and biochemical properties of protease-resistant form of PrP (PrP RES ) in the brains of affected voles differed from those in cervidized transgenic (CerPrP) mice infected with CWD. In addition, voles inoculated orally with sPMCA products developed clinical signs of TSE and were positive for PrP RES deposition, whereas those inoculated orally with deer-origin CWD prions did not. These results demonstrate that transspecies sPMCA of CWD prions can enhance the infectivity and adapt the host range of CWD prions and thereby may be useful to assess determinants of prion species barriers.

Journal of Virology

Mapping brucellosis increases relative to elk density using hierarchical Bayesian models

The relationship between host density and parasite transmission is central to the effectiveness of many disease management strategies. Few studies, however, have empirically estimated this relationship particularly in large mammals. We applied hierarchical Bayesian methods to a 19-year dataset of over 6400 brucellosis tests of adult female elk ( Cervus elaphus ) in northwestern Wyoming. Management captures that occurred from January to March were over two times more likely to be seropositive than hunted elk that were killed in September to December, while accounting for site and year effects. Areas with supplemental feeding grounds for elk had higher seroprevalence in 1991 than other regions, but by 2009 many areas distant from the feeding grounds were of comparable seroprevalence. The increases in brucellosis seroprevalence were correlated with elk densities at the elk management unit, or hunt area, scale (mean 2070 km 2 ; range = [95–10237]). The data, however, could not differentiate among linear and non-linear effects of host density. Therefore, control efforts that focus on reducing elk densities at a broad spatial scale were only weakly supported. Additional research on how a few, large groups within a region may be driving disease dynamics is needed for more targeted and effective management interventions. Brucellosis appears to be expanding its range into new regions and elk populations, which is likely to further complicate the United States brucellosis eradication program. This study is an example of how the dynamics of host populations can affect their ability to serve as disease reservoirs.

Wyoming

Rejoinder: Sifting through model space

Observational data sets generated by complex processes are common in ecology. Traditionally these have been very challenging to analyze because of the limitations of available statistical tools. This seems to be changing, and these are exciting times to be involved with ecological statistics, not just because of the neo-Bayesian revival but also because of the proliferation of computationally intensive methods in general. It is now possible to fit much richer models to observational data than in the relatively recent past, which in turn has stimulated much interest in how to evaluate and compare such models. In such an immature, vibrant, and rapidly growing field, not everyone is going to agree on the best way to do things. This is reflected in the contrast of opinions offered by the discussants. Each offers a thoughtful and thought-provoking critique of our work that reflects the current thinking in a non-negligible segment of the ecological data analysis community. We want to thank them for their insights.

Ecology

Elodontoma in captive southern red-backed voles ( Myodes gapperi )

Five southern red-backed voles ( Myodes gapperi ) of the first generation of a wild-caught breeding colony were presented with lesions at the maxillary incisors consistent with elodontoma. The affected animals had a history of chronic weight loss, were >16 months of age, and were siblings. Radiographs of the head showed multiglobular to irregularly outlined mineral opacity masses at the apices of the maxillary incisors. On necropsy, maxillary incisor teeth were not grossly visible, and a gingival ulceration was observed at the expected site of eruption. Microscopically, the apical region of the maxillary incisors was thickened or replaced by irregular dental tissue masses consistent with elodontoma. This is the first report to describe elodontoma in red-backed voles.

Journal of Zoo and Wildlife Medicine

Genetic susceptibility to chronic wasting disease in free-ranging white-tailed deer: complement component C1q and Prnp polymorphisms

The genetic basis of susceptibility to chronic wasting disease (CWD) in free-ranging cervids is of great interest. Association studies of disease susceptibility in free-ranging populations, however, face considerable challenges including: the need for large sample sizes when disease is rare, animals of unknown pedigree create a risk of spurious results due to population admixture, and the inability to control disease exposure or dose. We used an innovative matched case&ndash;control design and conditional logistic regression to evaluate associations between polymorphisms of complement C1q and prion protein (Prnp) genes and CWD infection in white-tailed deer from the CWD endemic area in south-central Wisconsin. To reduce problems due to admixture or disease-risk confounding, we used neutral genetic (microsatellite) data to identify closely related CWD-positive ( n = 68) and CWD-negative ( n = 91) female deer to serve as matched cases and controls. Cases and controls were also matched on factors (sex, location, age) previously demonstrated to affect CWD infection risk. For Prnp, deer with at least one Serine (S) at amino acid 96 were significantly less likely to be CWD-positive relative to deer homozygous for Glycine (G). This is the first characterization of genes associated with the complement system in white-tailed deer. No tests for association between any C1q polymorphism and CWD infection were significant at p < 0.05. After controlling for Prnp, we found weak support for an elevated risk of CWD infection in deer with at least one Glycine (G) at amino acid 56 of the C1qC gene. While we documented numerous amino acid polymorphisms in C1q genes none appear to be strongly associated with CWD susceptibility.

Wisconsin

Estimating cause-specific mortality rates using recovered carcasses

Stranding networks, in which carcasses are recovered and sent to diagnostic laboratories for necropsy and determination of cause of death, have been developed to monitor the health of marine mammal and bird populations. These programs typically accumulate comprehensive, long-term datasets on causes of death that can be used to identify important sources of mortality or changes in mortality patterns that lead to management actions. However, the utility of these data in determining cause-specific mortality rates has not been explored. We present a maximum likelihood-based approach that partitions total mortality rate, estimated by independent sources, into cause-specific mortality rates. We also demonstrate how variance estimates are derived for these rates. We present examples of the method using mortality data for California sea otters ( Enhydra lutris nereis ) and Florida manatees ( Trichechus manatus latirostris ).

California, Florida