Surveillance and Monitoring of White-Tailed Deer for Chronic Wasting Disease in the Northeastern United States

Understanding tools used to monitor diseases when they are new and emerging is integral to surveillance and containment efforts at local and regional scales. Chronic wasting disease (CWD) is a transmissible spongiform encephalopathy that was first detected in 1967 in a captive research facility in Fort Collins, Colorado (Williams and Young 1980). Chronic wasting disease is unique to members of the Cervidae family, including white-tailed deer Odocoileus virginianus, mule deer O. hemionus, elk Cervus elaphus, and moose Alces alces. Since initial detection, CWD has spread to more than 22 states, as well as two Canadian provinces and South Korea (Sohn et al. 2002; Rees et al. 2012). Of the states affected by CWD, five are in the northeastern United States (Northeast; Figure 1). By the turn of the 21st century, many states had adopted surveillance plans as CWD became increasingly prevalent. Additionally, most states banned importation of farmed or captive cervids from states with CWD to prevent the disease from being introduced into wild populations (Salman 2003). Movement of infected, captive cervids from South Dakota game farms has been identified as the cause of CWD in Canada (Kahn et al. 2004; Argue et al. 2008), and these transfers are also the most commonly accepted explanation for the presence of CWD in Wisconsin (Joly et al. 2003).

Increasing concerns over captive elk importation from infected game farms in the west prompted the state of Wisconsin to implement a CWD surveillance plan in 1999 (WDNR 2010). During the 2001 hunting season, three hunter-harvested male deer in the south-central region of the state tested positive for CWD. The earliest estimate of overall prevalence of CWD in Wisconsin's herd reduction zone was 1.5% from 21,285 deer tested between April 2002 and January 2004 (Joly et al. 2003; Grear et al. 2006). The most recent estimates in Wisconsin show prevalence as high as 23% in the CWD management zone (WDNR 2009). In Illinois, surveillance did not begin until after the disease crossed the northern border and was identified 2 wk before the firearms season in November 2002 (Miller 2003). Several measures have been taken to contain the spread of CWD in Illinois, including unlimited bag limits for antlerless deer. However, the increase in hunting opportunities for antlerless deer has not resulted in higher harvest rates in those areas. Additionally, sharpshooting—defined as the targeted culling of deer exhibiting signs characteristic of CWD—has been unsuccessful in preventing the spread of CWD (Shelton and McDonald 2012; Manjerovic et al. 2014).

Unlike the endemic areas of Colorado, Wyoming, and the Midwest, there has been no reputable determination of the mechanism that resulted in the presence of CWD in the Northeast in 2005, and there is no published information on CWD occurrence since its first detection in a captive deer herd in New York. These facts and the varied success that states in other regions have had in preventing the introduction of CWD and containing spread in local populations prompted us to conduct surveys of state agencies in the Northeast to gain a better understanding of surveillance measures taken to detect CWD. The objectives of our survey were to determine 1) the number of hunter-harvested deer tested for CWD by year in each state, 2) tissues that were most commonly submitted for testing, and 3) the laboratory used by each state to test CWD samples. Our results provide valuable information for agencies responsible for CWD testing regarding issues of sample size, appropriate tissues, and laboratories available for CWD diagnosis.

We initiated surveys of state agencies in June 2012 to gain a better understanding of the surveillance measures taken by 14 states in the Northeast. The survey area included Connecticut, Delaware, Maine, Maryland, Massachusetts, New Hampshire, New Jersey, New York, Ohio, Pennsylvania, Rhode Island, Vermont, Virginia, and West Virginia. An agency representative (e.g., cervid biologist, wildlife veterinarian) from each state provided information via email regarding their state's surveillance efforts for detecting CWD. This information included the number of deer harvested and tested for CWD each year, the tissue(s) collected, and the United States Department of Agriculture (USDA)–certified laboratory at which the samples were tested. Although many states use a variety of testing protocols that include hunter-harvested, road-killed, and targeted (e.g., culled) deer, we chose to focus on the hunter harvest for means of comparison.

Intensive CWD surveillance in the Northeast did not begin until 2002, but all states had established surveillance plans by 2005 (Table 1). The number of harvested deer collected for testing ranged from 41 in Rhode Island in 2003 to 8,164 in New York in 2005. The intensive surveillance efforts in New York were in response to the discovery of CWD in two captive herds and two wild deer in Oneida County, New York. Between 2005 and 2012, states in the Northeast tested 121,730 harvested deer, or approximately 15,216/y. However, recent surveillance efforts have decreased sample sizes (e.g., 9,778 for all states in 2012) because of the use of alternate methods (e.g., road-kill) of surveillance in many states. Prevalence (proportion of positive samples to total number of samples tested) for all years combined was highest in West Virginia (0.71%) using hunter-harvested deer, whereas no other state had prevalence that exceeded 0.07%.

Alternate methods included use of weighted surveillance in New York (e.g., testing of high-risk deer based on sex and age; Walsh and Miller 2010), testing of road-killed deer, and targeted surveillance of deer exhibiting signs characteristic of CWD. West Virginia and Pennsylvania were the only states in the Northeast that detected CWD in road-killed deer, totaling three positive cases since 2005. West Virginia also identified 63 positives using targeted surveillance and was the only state in the Northeast that detected CWD using this method. Because of high costs associated with processing thousands of samples, weighted surveillance became the preferred method for detecting CWD in New York, where it is unknown whether CWD still persists in the state's deer herd (NYSDEC 2013). All states dealing with CWD in the Northeast drastically increased surveillance efforts after initial detection of CWD in their respective states, but later reduced these efforts after either failing to detect additional cases of CWD in large sample sizes (e.g., New York) or implementing alternate methods of surveillance. Pennsylvania also followed this trend by increasing surveillance efforts after detecting CWD in both captive and free-ranging deer in 2012, but it remains to be seen how sampling will change over time.

Tissues submitted for CWD testing included retropharyngeal lymph nodes, tonsil lymph nodes, and the medulla oblongata sectioned at the obex. Retropharyngeal lymph nodes were most common, as 13 of 14 states (92.9%) in the Northeast submitted this type of tissue. However, some states, including Maryland and Pennsylvania, also extracted the obex from hunter-harvested deer, and others extracted the obex only from deer exhibiting signs characteristic of CWD. Connecticut was the only state surveyed that relied primarily on testing of tonsil tissue (Table 2).

Miller and Williams (2002) found that immunohistochemistry staining of the three major tissues collected from infected deer resulted in detection inconsistencies. Deer in the early stages of infection stained positive only in retropharyngeal lymph nodes and tonsil lymph nodes but the obex provided negative results in the same deer. In a different study, 80% of 269 infected deer tested positive based on prion detections in both the retropharyngeal lymph nodes and obex, but retropharyngeal lymph nodes were the only indicators of CWD in the remaining 55 positive deer (Keane et al. 2008). The effectiveness of using retropharyngeal lymph nodes to detect CWD in nearly all stages of infection is presumably the reason that this tissue was most commonly submitted by state agencies in the Northeast.

The Wisconsin Veterinary Diagnostic Laboratory in Madison, Wisconsin, was the most-used USDA-certified laboratory prior to 2012, and was still used by 29% of states (4 of 14) in the Northeast to analyze CWD samples in 2012. Six states sent CWD samples to laboratories within the Pennsylvania Animal Diagnostic Laboratory System, consisting of the Pennsylvania Veterinary Laboratory in Harrisburg and New Bolton Center Veterinary Laboratory in Kennett Square (Table 2). Location and lower overall costs associated with processing samples were identified as primary reasons for using these Pennsylvania laboratories. Certified laboratories in other states, including the Animal Disease Diagnostic Laboratory in Reynoldsburg, Ohio, and the Colorado State University Diagnostic Laboratory in Fort Collins, Colorado, also were used to analyze samples from the Northeast. The laboratory chosen by each state was not as important as the tissue submitted for detection of CWD, because all states sent samples to laboratories that were certified by the USDA and therefore appropriate for processing CWD samples.

Given the postulated spread of CWD from captive facilities to wild populations that is believed to have occurred in the CWD endemic region of Colorado and Wyoming (Miller et al. 2000), this seemed likely to be the case elsewhere. New York confirmed CWD in two captive herds in March 2005 and later in two wild deer in April 2005. However, investigations into the causes of these cases were inconclusive because of complexities that occurred within the captive herd in which CWD was first detected. Complexities ranged from captive deer escaping the fenced facilities to undocumented transfers between facilities. Surveillance efforts have continued in New York since 2005 but no additional cases have been found in wild or captive herds.

West Virginia had its first case of CWD in a wild, road-killed deer in Hampshire County in 2005. Between 2005 and 2012, testing of harvested deer in West Virginia has yielded 63 CWD-positive cases out of 8,860 test samples (Table 1). All but two of these deer were collected in Hampshire County, with the remaining deer found in bordering Hardy County. Despite the proximity between Hampshire County, West Virginia, and bordering states (such as Virginia, Maryland, and Pennsylvania), CWD was not detected in these states until Virginia confirmed its first case in 2009 in a wild deer that was harvested <2 km from the West Virginia state line. Similarly, Maryland's only two cases to date were detected in deer harvested in 2010 and 2013 in Allegany County, just north of the initial Hampshire County outbreak in West Virginia. In October 2012, Pennsylvania's first case of CWD was detected in a captive deer from a farm in Adams County, and CWD was also found in three wild deer that were harvested during the 2012 rifle season. Two of these deer were harvested in Blair County and the other came from Bedford County. In November 2013, Bedford County's second case was found in a road-killed deer. Although it is possible that CWD crossed the Potomac River into these bordering areas, studies examining movements of deer between populations are needed to determine routes of transmission. There is also a difference between CWD not being “detected” and CWD not being “present,” and the dates of initial detection in each state may not provide an accurate timeline of CWD in the Northeast.

As of 2002, Wisconsin and Illinois were the only states east of the Mississippi River that had confirmed cases of CWD (Saunders et al. 2012). However, CWD has been found in five states in the Northeast during the past decade. New York is the only state that has detected CWD but not redetected it in subsequent sampling efforts. In New York, a containment area 16 km in diameter was established around the 2005 index cases with the following emergency regulations to prevent further spread of the disease: mandatory check stations and testing of all harvested deer within the containment area; bans on deer rehabilitation, movement of intact carcasses, use of deer or elk urine, and possession of deer killed by motor vehicles in the containment area. Requirements were also increased for taxidermist record keeping and reporting. All states dealing with CWD in the Northeast have containment and/or management plans with similar regulations.

Potential spread of CWD into new regions, specifically if expedited by transfer of captive cervids, may be a serious issue for additional states in the future. As of fiscal year 2012, the USDA provided the primary source of funding for CWD surveillance taking place at the state level. However, lack of USDA funding since 2012 has been problematic for states currently dealing with CWD or those at risk to have CWD in populations of wild cervids in the future. The loss of funding provided by the USDA for surveillance suggests that each state's future plans will require state funds or some other source to continue to monitor for CWD. Pennsylvania, West Virginia, and Virginia spend considerable state funding on CWD sampling, but this is not the case with many other states in the Northeast. After years of USDA-funded testing, Colorado documented a 90% reduction in samples submitted for CWD testing in response to a sample fee of US$25 that was imposed on hunters that wanted their deer tested (CDPW 2011). States in the Northeast may alter surveillance efforts with an emphasis on weighted (Walsh and Miller 2010) or targeted surveillance to reduce sample size and cost, and others that are at risk for CWD infection may not continue surveillance without the availability of federal funding.

Weighted sampling efforts appear to be warranted in areas that are at the greatest risk for CWD infection based on associations of CWD with environmental and landscape covariates (Osnas et al. 2009; Walsh and Miller 2010; Walter et al. 2011). For example, a 1% increase in clay particle content increased odds of infection by up to 8.9% in mule deer in Colorado, because clay soil binds the infectious prion that causes CWD, making it bio-available for long durations (Walter et al. 2011). Other studies have documented that the presence of landscape characteristics such as low-lying grasslands that provide high-quality winter habitat, as well as riparian ecosystems, concentrate deer and increased the odds of CWD infection in north-central Colorado and Saskatchewan, Canada, respectively (Farnsworth et al. 2006; Rees et al. 2012). Assessing variables specific to the Northeast, such as forest cover linked to deer dispersal and habitats that concentrate deer during the winter, may provide the information needed to improve surveillance for CWD throughout the Northeast and is currently ongoing (T. S. Evans, The Pennsylvania State University, unpublished data). Furthermore, with new financial constraints, collaborations among state agencies have been initiated in the Northeast and may improve efficiency of disease surveillance at a regional scale.

We would like to express our gratitude to the following state agencies that assisted us by providing surveillance data: Pennsylvania Game Commission, West Virginia Division of Natural Resources, Maryland Department of Natural Resources, New Hampshire Fish and Game Department, Maine Department of Inland Fisheries and Wildlife, Virginia Department of Game and Inland Fisheries, Connecticut Department of Energy and Environmental Protection, Vermont Fish and Wildlife Department, Delaware Division of Fish and Wildlife, New York Department of Environmental Conservation, New Jersey Division of Fish and Wildlife, Rhode Island Division of Fish and Wildlife, Ohio Division of Wildlife, and Massachusetts Division of Fisheries and Wildlife. We would also like to thank the reviewers and Subject Editor for their assistance in improving the manuscript.

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