Reducing the Public Health Impact of Bovine Tuberculosis by Controlling Disease Transmission Between Cattle and White-Tailed Deer in Northwestern Minnesota

Bovine tuberculosis, caused by infection with Mycobacterium bovis, is a re-emerging zoonotic disease. It has staged a comeback by establishing infections in wildlife and cattle, creating the potential for human disease in locations where it was thought to be under control. In northwestern Minnesota, infected cattle and white-tailed deer were first discovered in 2005. A major bovine tuberculosis eradication campaign is underway in the state, with multiple efforts employed to control M. bovis infection in both cattle and deer populations. In order to effectively eradicate bovine tuberculosis in Minnesota, there is a need for better understanding of the factors that increase the risk of deer and cattle interacting in a way that facilitates tuberculosis transmission. By reducing the risk of disease transmission within the animal populations, we will also reduce the risk that bovine tuberculosis will again become a common disease in human populations. The purpose of this study is to characterize the risk of interactions between cattle and white-tailed deer in northern Minnesota in order to prevent M. bovis transmission. A survey originally developed to assess deer-cattle interactions in Michigan was modified for use in Minnesota, introducing a scoring method to evaluate the areas of highest priority at risk of potential deer-cattle interaction. The resulting semi-quantitative deer-cattle interaction risk assessment was used at 53 cattle herds located in the region adjacent to the bovine tuberculosis “Core Area”. Two evaluators each scored the farm separately, and then created a management plan for the farm that prioritized the areas of greatest risk for deer-cattle interactions. Herds located within the “Management Zone” were evaluated by Minnesota Board of Animal Health staff, and results from these surveys were used as a point of comparison.

Estimating the extent of spatial association of Mycobacterium bovis infection in badgers in Ireland

Mycobacterium bovis infects the wildlife species badgers Meles meles who are linked with the spread of the associated disease tuberculosis (TB) in cattle. Control of livestock infections depends in part on the spatial and social structure of the wildlife host. Here we describe spatial association of M. bovis infection in a badger population using data from the first year of the Four Area Project in Ireland. Using second-order intensity functions, we show there is strong evidence of clustering of TB cases in each the four areas, i.e. a global tendency for infected cases to occur near other infected cases. Using estimated intensity functions, we identify locations where particular strains of TB cluster. Generalized linear geostatistical models are used to assess the practical range at which spatial correlation occurs and is found to exceed 6 in all areas. The study is of relevance concerning the scale of localized badger culling in the control of the disease in cattle.

Hidden Effects of Chronic Tuberculosis in African Buffalo

Infectious diseases can bring about population declines and local host extinctions, contributing significantly to the global biodiversity crisis. Nonetheless, studies measuring population-level effects of pathogens in wild host populations are rare, and taxonomically biased toward avian hosts and macroparasitic infections. We investigated the effects of bovine tuberculosis (bTB), caused by the bacterial pathogen Mycobacterium bovis, on African buffalo (Syncerus caffer) at Hluhluwe-iMfolozi Park, South Africa. We tested 1180 buffalo for bTB infection between May 2000 and November 2001. Most infections were mild, confirming the chronic nature of the disease in buffalo. However, our data indicate that bTB affects both adult survival and fecundity. Using an age-structured population model, we demonstrate that the pathogen can reduce population growth rate drastically; yet its effects appear difficult to detect at the population level: bTB causes no conspicuous mass mortalities or fast population declines, nor does it alter host-population age structure significantly. Our models suggest that this syndrome—low detectability coupled with severe impacts on population growth rate and, therefore, resilience—may be characteristic of chronic diseases in large mammals.

The Duration of the Effects of Repeated Widespread Badger Culling on Cattle Tuberculosis Following the Cessation of Culling

Background: In the British Isles, control of cattle tuberculosis (TB) is hindered by persistent infection of wild badger (Meles meles) populations. A large-scale field trial—the Randomised Badger Culling Trial (RBCT)—previously showed that widespread badger culling produced modest reductions in cattle TB incidence during culling, which were offset by elevated TB risks for cattle on adjoining lands. Once culling was halted, beneficial effects inside culling areas increased, while detrimental effects on adjoining lands disappeared. However, a full assessment of the utility of badger culling requires information on the duration of culling effects. Methodology/Principal Findings: We monitored cattle TB incidence in and around RBCT areas after culling ended. We found that benefits inside culled areas declined over time, and were no longer detectable by three years post-culling. On adjoining lands, a trend suggesting beneficial effects immediately after the end of culling was insignificant, and disappeared after 18 months post-culling. From completion of the first cull to the loss of detectable effects (an average five-year culling period plus 2.5 years post-culling), cattle TB incidence was 28.7% lower (95% confidence interval [CI] 20.7 to 35.8% lower) inside ten 100 km2 culled areas than inside ten matched no-culling areas, and comparable (11.7% higher, 95% CI: 13.0% lower to 43.4% higher, p = 0.39) on lands #2 km outside culled and no-culling areas. The financial costs of culling an idealized 150 km2 area would exceed the savings achieved through reduced cattle TB, by factors of 2 to 3.5. Conclusions/Significance: Our findings show that the reductions in cattle TB incidence achieved by repeated badger culling were not sustained in the long term after culling ended and did not offset the financial costs of culling. These results, combined with evaluation of alternative culling methods, suggest that badger culling is unlikely to contribute effectively to the control of cattle TB in Britain.

Spatial Management of Wildlife Disease

The spread of wildlife diseases is a major threat to livestock, human health, resource-based recreation, and biodiversity conservation (Cleaveland, Laurenson, and Taylor). The development of economically sound wildlife disease-management strategies requires an understanding of the links between ecological functions (e.g., disease transmission and wildlife dispersal) and economic choices, and the associated tradeoffs. Spatial linkages are particularly relevant. Yet while ecologists have long-argued that space is important (Hudson et al.), prior economic work has largely ignored spatial issues. For instance, Horan and Wolf analyzed a case study of bovine tuberculosis (bTB) in Michigan deer, a problem where the disease appears to be confined to a single, spatially confined, wildlife population—an island. But wildlife disease matters generally are not spatially confined. Barlow, in analyzing bTB in possums in New Zealand, accounted for immigration of susceptible possums into a disease reservoir. However, he modeled immigration as fixed and unaffected by management. Bicknell, Wilen, and Howitt, also focusing on possums in New Zealand, developed a model that incorporates simple density-dependent net migration. This allowed the authors to account for endogenous immigration when deriving optimal culling strategies.

The Economics of Managing Wildlife Disease

The spread of infectious disease among and between wild and domesticated animals has become a major problem worldwide. Upon analyzing the dynamics of wildlife growth and infection when the diseased animals cannot be identified separately from healthy wildlife prior to the kill, we find that harvest-based strategies alone have no impact on disease transmission. Other controls that directly influence disease transmission and/or mortality are required. Next, we analyze the socially optimal management of infectious wildlife. The model is applied to the problem of bovine tuberculosis among Michigan white-tailed deer, with non-selective harvests and supplemental feeding being the control variables. Using a two-state linear control model, we find a two-dimensional singular path is optimal (as opposed to a more conventional bang-bang solution) as part of a cycle that results in the disease remaining endemic in the wildlife. This result follows from non-selective harvesting and intermittent wildlife productivity gains from supplemental feeding.

Spatial and Temporal Spread of Bovine Tuberculosis in Wild White-Tailed Deer in Michigan

In 1975, a wild white-tailed deer infected with bovine tuberculosis was shot in the northeastern Lower Peninsula, Michigan. The shooting of a second infected deer in the same area in 1994 triggered ongoing disease surveillance in the region. By 2002, bovine tuberculosis had been confirmed in 12 Michigan counties: from 449 deer; two elk; 41 non-cervid wildlife; one captive cervid facility and 28 cattle herds. We analyzed geographic spread of disease since the surveillance began and investigated factors influencing the prevalence of disease within the infected area. These analyses reveal that 78 percent of tuberculous deer came from within a 1560 km2 'core' area, within which the prevalence of apparent disease averaged 2.5 percent. Prevalence declined dramatically outside of the core and was an order of magnitude lower 30 km from its boundary. This prevalence gradient was highly significant (P<0.0001) and did not alter over the 6 year surveillance period (P= 0.98). Within the core, deer density and supplemental feeding by hunters were positively and independently correlated with tuberculosis prevalence in deer. Together, these two factors explained 55 percent of the variation in prevalence. We conclude that bovine tuberculosis was already well established in the deer population in 1994, that the infected area has not expanded significantly since that time, and that deer over-abundance and food supplementation have both contributed to ongoing transmission of disease. Managers are currently enforcing prohibitions on deer feeding in the core and are working to lower deer numbers there through increased hunting pressure.

Wildlife-Cattle Interactions in Northern Michigan: Implications for the Transmission of Bovine Tuberculosis

Bovine tuberculosis (Mycobacterium bovis) was discovered in northern Michigan white-tailed deer (Odocoileus virginianus) in 1994, and has been known to exist in Michigan cattle herds since 1998. Despite efforts to eradicate the disease in cattle, infection and re-infection of farms continues to occur, suggesting transmission among cattle, deer, or other wildlife reservoirs. The goals of this study were to document wildlife activity on farms and evaluate the possible role wildlife play in the ecology of bovine tuberculosis (TB) in Michigan. Visual observations were conducted on farms in a 5-county area of northern Michigan to document direct wildlife-cattle interactions (i.e., <5 m between individuals) and indirect interactions (e.g., wildlife visitations to food stores and areas accessible to cattle). Observations were conducted primarily during evening and early morning hours between January and August, 2002, and on a 24-hour schedule between January and August, 2003. Total observation time accumulated through the duration of the study was 1,780 hours. Results indicated that direct interaction between deer and cattle was a rare event; no direct interactions were observed during the first year, and only one direct interaction was observed during the second year. However, through the duration of the study 21 direct interactions were documented between cattle and turkey, and 11 direct interactions were documented between cattle and mammals other than deer. In total, 273 indirect interactions by deer, 112 indirect interactions by turkeys, and 248 indirect interactions by mammals other than deer were observed during the 2 field seasons combined. These data supported the hypothesis that indirect interactions among wildlife and cattle are a potential mechanism for the transmission of TB in Michigan. If direct interactions were important mechanisms of TB transmission to cattle in northern Michigan, my data suggested that feral cats were the species of most concern, even though there were more observations between turkey and cattle. Unlike cats, which can become infected with and transmit TB, there is no evidence for such pathogenesis in turkey.

RB32-270 A Seven Year Study of a Milk Supply

The amount of butter produced by the grain-belt states is evidence that a great many cows are milked by the midwestern farmer. Most of this milk is separated on the farm, the cream is sold, and the skimmilk is fed to hogs and other livestock. As the market for fluid milk has developed, many farmers near the cities have turned to the sale of milk, because it affords a better return for the butterfat sold. Much of the milk produced for sale as fluid milk is produced under practically the same conditions as milk which is produced primarily for the same of cream. The Department of Dairy Husbandry of the University of Nebraska, in conducting its instructional and investigational work, comes in contact with the milk producer. An effort has been made, therefore, to study the relation of milk quality to farm conditions as found among the milk producers or patrons who have delivered milk to the department. The study was carried on in an effort to find possible ways of bettering the conditions without upsetting the economic balance existing between the production of cream and fluid milk.

EC32-713 The Trench Silo in Nebraska

The original idea of using a trench for the storing of ensilage seems to have been the outgrowth of the practice long used in several European countries of storing clover and beet tops in pits. Shortly after the World War, western Canada followed by Montana and North Dakota began to use the trench silo. In Nebraska the true trench silo made its appearance about 1925 or 1926. The trench silo as described in this circular, unless lined with some permanent material such as brick, concrete or stone, must be considered a temporary structure which will serve for a few years only and then must be discarded or rebuilt. In an emergency it will save a crop even though the farmer has little capital to expend other than his own labor.

RB25-207 The Spindle-Tuber Disease: One Cause of "Run-Out" Seed Potatoes

The spindle-tuber disease is one of the most prevalent potato diseases occurring in all parts of Nebraska. It has been found in all varieties tested. It does much damage to the potato crop, in that it reduces the yield and injures the market quality of the potatoes. This 1925 publication discusses the spindler-tuber disease also known as "running-out" or degeneracy of seed potatoes; the distribution of the disease; effect upon yield and quality; symptoms of the different potato varieties; transmission of the disease and experiments; rate of increase of the disease; dry land versus irrigation in western Nebraska; straw mulching versus cultivation in eastern Nebraska; planting times; harvesting; and control.

Development of a Model of Natural Infection with Mycobacterium bovis in White-Tailed Deer

The objective of this study was to develop a suitable experimental model of natural Mycobacterium bovis infection in white-tailed deer (Odocoileus virginianus), describe the distribution and character of tuberculous lesions, and to examine possible routes of disease transmission. In October 1997, 10 mature female white-tailed deer were inoculated by intratonsilar instillation of 2 3 103 (low dose) or 2 3 105 (high dose) colony forming units (CFU) of M. bovis. In January 1998, deer were euthanatized, examined, and tissues were collected 84 to 87 days post inoculation. Possible routes of disease transmission were evaluated by culture of nasal, oral, tonsilar, and rectal swabs at various times during the study. Gross and microscopic lesions consistent with tuberculosis were most commonly seen in medial retropharyngeal lymph nodes and lung in both dosage groups. Other tissues containing tuberculous lesions included tonsil, trachea, liver, and kidney as well as lateral retropharyngeal, mandibular, parotid, tracheobronchial, mediastinal, hepatic, mesenteric, superficial cervical, and iliac lymph nodes. Mycobacterium bovis was isolated from tonsilar swabs from 8 of 9 deer from both dosage groups at least once 14 to 87 days after inoculation. Mycobacterium bovis was isolated from oral swabs 63 and 80 days after inoculation from one of three deer in the low dose group and none of four deer in the high dose group. Similarly, M. bovis was isolated from nasal swabs 80 and 85 days after inoculation in one of three deer from the low dose group and 63 and 80 days after inoculation from two of four deer in the high dose group. Intratonsilar inoculation with M. bovis results in lesions similar to those seen in naturally infected white-tailed deer; therefore, it represents a suitable model of natural infection. These results also indicate that M. bovis persists in tonsilar crypts for prolonged periods and can be shed in saliva and nasal secretions. These infected fluids represent a likely route of disease transmission to other animals or humans.

Evaluation of Blood Assays for Detection of Mycobacterium bovis in White-Tailed Deer (Odocoileus virginianus) in Michigan

Surveillance and control activities related to bovine tuberculosis (TB) in free-ranging, Michigan white-tailed deer (Odocoileus virginianus) have been underway for over a decade, with significant progress. However, foci of higher TB prevalence on private lands and limited agency ability to eliminate them using broad control strategies have led to development and trial of new control strategies, such as live trapping, testing, and culling or release. Such strategies require a prompt, accurate live animal test, which has thus far been lacking. We report here the ability of seven candidate blood assays to determine the TB infection status of Michigan deer. Our aims were twofold: to characterize the accuracy of the tests using field-collected samples and to evaluate the feasibility of the tests for use in a test-and-cull strategy. Samples were collected from 760 deer obtained via five different surveys conducted between 2004 and 2007. Blood samples were subjected to one or more of the candidate blood assays and evaluated against the results of mycobacterial culture of the cranial lymph nodes. Sensitivities of the tests ranged from 46% to 68%, whereas specificities and negative predictive values were all .92%. Positive predictive values were highly variable. An exploratory analysis of associations among several host and sampling-related factors and the agreement between blood assay and culture results suggested these assays were minimally affected. This study demonstrated the capabilities and limitations of several available blood tests for Mycobacterium bovis on specimens obtained through a variety of field surveillance methods. Although these blood assays cannot replace mass culling, information on their performance may prove useful as wildlife disease managers develop innovative methods of detecting infected animals where mass culling is publicly unacceptable and cannot be used as a control strategy.

Shared Feed as a Means of Deer-to-Deer Transmission of Mycobacterium bovis

To determine the ability of experimentally inoculated white-tailed deer (Odocoileus virginianus) to transmit Mycobacterium bovis to naive deer through the sharing of feed, four deer were intratonsillarly inoculated with 4x105 colony-forming units of M. bovis. On a daily basis, feed not consumed by inoculated deer after approximately 8 hr was offered to four naıve deer maintained in a separate pen, where direct contact, aerosol transmission, or transmission through personnel were prevented. After 150 days, naıve deer were euthanized and examined. All naıve deer had lesions consistent with tuberculosis and M. bovis was isolated from various tissues. The most commonly affected tissues were lung, tracheobronchial lymph nodes, and mediastinal lymph nodes. This study demonstrates the potential for indirect transmission of M. bovis through the sharing of feed. Intentional or unintentional feeding of deer by wildlife or agricultural interests in regions where M. bovis infection is endemic should be avoided because both direct and indirect transmission through sharing of feed are enhanced.

Investigation of the Transmission of Mycobacterium bovis from Deer to Cattle Through Indirect Contact

Objective—To investigate the infection of calves with Mycobacterium bovis through oral exposure and transmission of M bovis from experimentally infected white-tailed deer to uninfected cattle through indirect contact. Animals—24 11-month-old, white-tailed deer and 28 6-month-old, crossbred calves. Procedure—In the oral exposure experiment, doses of 4.3 X 106 CFUs (high dose) or 5 X 103 CFUs (low dose) of M bovis were each administered orally to 4 calves; as positive controls, 2 calves received M bovis (1.7 X 105 CFUs) via tonsillar instillation. Calves were euthanatized and examined 133 days after exposure. Deer-to-cattle transmission was assessed in 2 phases (involving 9 uninfected calves and 12 deer each); deer were inoculated with 4 X 105 CFUs (phase I) or 7 X 105 CFUs (phase II) of M Bovis. Calves and deer exchanged pens (phase I; 90 days’ duration) or calves received uneaten feed from deer pens (phase II; 140 days’ duration) daily. At completion, animals were euthanatized and tissues were collected for bacteriologic culture and histologic examination. Results—In the low- and high-dose groups, 3 of 4 calves and 1 of 4 calves developed tuberculosis, respectively. In phases I and II, 9 of 9 calves and 4 of 9 calves developed tuberculosis, respectively. Conclusions and Clinical Relevance—Results indicated that experimentally infected deer can transmit M bovis to cattle through sharing of feed. In areas where tuberculosis is endemic in free-ranging white-tailed deer, management practices to prevent access of wildlife to feed intended for livestock should be implemented.