Stephen M. Schmitt

Bovine Tuberculosis in Free-Ranging White-Tailed Deer From Michigan

A 4.5 yr-old male white-tailed deer (Odocoileus virginianus) killed by a hunter during the 1994 firearm hunting season in northeastern Michigan (USA) had lesions suggestive of tuberculosis and was positive on culture for Mycobacterium bovis the causative agent for bovine tuberculosis. Subsequently, a survey of 354 hunter-harvested white-tailed deer for tuberculosis was conducted in this area from 15 November 1995 through 5 January 1996. Heads and/or lungs from deer were examined grossly and microscopically for lesions suggestive of bovine tuberculosis. Gross lesions suggestive of tuberculosis were seen in 15 deer. Tissues from 16 deer had acid-fast bacilli on histological examination and in 12 cases mycobacterial isolates from lymph nodes and/or lungs were identified as M. bovis. In addition, lymph nodes from 12 deer (11 females and 1 male) without gross or microscopic lesions were pooled into 1 sample from which M. bovis was cultured. Although more male (9) than female (3) deer had bovine tuberculosis infections, this difference was not statistically significant. Mycobacterium bovis culture positive deer ranged in age from 1.5 to 5.5 yr with a mean of 2.7 yr (median 2.5 yr) for males and 3.2 yr (median 3.5 yr) for females. This appears to be the first epidemic occurrence of M. bovis in free-ranging cervids in North America. A combination of environmental (high deer density and poor quality habit) and management-related factors (extensive supplemental feeding) may be responsible for this epizootic.

Epidemiology of Mycobacterium bovis in free-ranging white-tailed deer, Michigan, USA, 1995–2000

An endemic area of bovine tuberculosis (TB) (Mycobacterium bovis) currently affecting wild white-tailed deer (Odocoileus virginianus) in northern lower Michigan, USA, constitutes the first self-sustaining outbreak of the infection in free-ranging North American cervids. Given this precedent, epidemiologic insights gained from the outbreak afford the opportunity to guide not only current surveillance and intervention but also control efforts for future outbreaks involving wildlife reservoirs. Our specific objectives were to evaluate retrospective data from field surveillance conducted from 1995 to 2000 to determine apparent prevalence, trends in apparent prevalence, and the effects of various factors on the odds of being M. bovis positive. Data were gathered from post-mortem examinations of 62,560 wild deer collected from all 83 Michigan counties. Records of survey method, sex, age, geographic area and infection status as determined by mycobacterial culture were subjected to trend analysis and multivariable logistic regression. Apparent prevalence for the period was 0.54% (336/62,560) statewide. Prevalence varied widely with geographic area, but significantly decreased since 1995 in the core area of the outbreak-which coincided with implementation of control strategies. Significant risk factors were geographic area, sex, age, and the sex-by-age interaction. The survey method by which deer were obtained for testing was not a predictor of infection. Our results to date suggest an outbreak characterized by broad areas of very low prevalence surrounding focal areas where prevalence is sometimes orders-of-magnitude higher (e.g., deer originating from the core area were up to 147 times more likely to be TB positive than deer from other areas). Our results also identify older male deer as most likely to be M. bovis positive (OR=11.3, 95% CI 3.2, 40.3 for bucks > or =5 years vs. does < or =1.5 years)-an observation consistent with the biology and behavior of the species. Synthesizing these results with those of other ongoing investigations, we hypothesize a two-stage model of disease transmission where TB is maintained at very low prevalence in matriarchal groups, with primary dissemination of the disease attributable to the dispersal and movements of bucks (as well as to the large aggregations of animals created by human activities).

Bovine tuberculosis in free-ranging carnivores from Michigan

During a survey of carnivores and omnivores for bovine tuberculosis conducted in Michigan (USA) since 1996, Mycobacterium bovis was cultured from lymph nodes pooled from six coyotes (Canis latrans) (four adult female, two adult male), two adult male raccoons (Procyon lotor), one adult male red fox (Vulpes vulpes), and one 1.5-yr-old male black bear (Ursus americanus). One adult, male bobcat (Felis rufus) with histologic lesions suggestive of tuberculosis was negative on culture but positive for organisms belonging to the Mycobacterium tuberculosis complex when tested by polymerase chain reaction. All the tuberculous animals were taken from three adjoining counties where M. bovis is known to be endemic in the free-ranging white-tailed deer (Odocoileus virginianus) population. There were two coyotes, one raccoon, one red fox, and one bobcat infected in Alpena county. Montmorency County had two coyotes and one raccoon with M. bovis. Two coyotes and a bear were infected from Alcona County. These free-ranging carnivores/omnivores probably became infected with M. bovis through consumption of tuberculous deer. Other species included in the survey were opossum (Didelphis virginiana), gray fox (Urocyon cinereoargenteus), and badger (Taxidea taxus); these were negative for M. bovis.

Tuberculous lesions in free-ranging white-tailed deer in Michigan.

Descriptions of the anatomical distribution of Mycobacterium bovis gross lesions in large samples of white-tailed deer (Odocoileus virginianus) are lacking in the scientific literature. This report describes the distribution of gross lesions in the 58 white-tailed deer that cultured positive for M. bovis among the 19,500 submitted for tuberculosis testing in Michigan (USA) in 1999. For the vast majority (19,348) of those tested, only the head was submitted; for others, only extracranial tissues (33) or both the head and extracranial tissues (119) were available. Among those deer that cultured positive, cranial gross lesions were noted most frequently in the medial retropharyngeal lymph nodes, although solitary, unilateral parotid lymph node lesions also were found. Extracranial lesions occurred most commonly in the thorax. The distribution of lesions largely agreed with the few existing case reports of the M. bovis in white-tailed deer, although gross lesions were also found in sites apparently not previously reported in this species (liver, spleen, rumen, mammary gland). Some practical issues that may assist future surveillance and public education efforts are also discussed.

Comparison of postmortem techniques for the detection of Mycobacterium bovis in white-tailed deer (Odocoileus virginianus)

A retrospective study of various diagnostic postmortem techniques used in a 4-year surveillance program for detection of Mycobacterium bovis infection in wild white-tailed deer (Odocoileus virginianus) was conducted. The tests evaluated were routine histopathology, acid-fast staining, detection of acid-fast bacilli in culture, and an M. tuberculosis group-specific genetic probe applied to pure cultures. Each of these techniques were compared with a reference or “gold standard” of mycobacterial culture and identification. Histopathology, the most rapid form of testing for M. bovis infection in white-tailed deer samples, had a sensitivity of 98% and a specificity of 87%, resulting in a positive predictive value of 94%. The detection of acid-fast bacilli by staining was less sensitive than histopathology (90%), but its higher specificity (97%) resulted in a positive predictive value of 99%. The detection of acid-fast bacilli on culture was both highly specific (93%) and sensitive (100%). The group-specific genetic probe had the highest sensitivity and specificity and produced results in complete agreement with those of mycobacterial culture, suggesting that this technique could be used as the new “gold standard” for this particular wildlife tuberculosis surveillance program.

Mycobacterium bovis in Coyotes from Michigan

During a survey for tuberculosis in wild carnivores and omnivores, Mycobacterium bovis was cultured from pooled lymph nodes of three adult female coyotes (Canis latrans) harvested by hunters in Michigan (USA). No gross or histologic lesions suggestive of tuberculosis were seen in these animals. One coyote was taken from Montmorency county and two coyotes from Alcona county located in the northeastern portion of Michigans Lower Peninsula where free-ranging white-tailed deer (Odocoileus virginianus) have been found infected with bovine tuberculosis. It is thought that these coyotes became infected with M. bovis through the consumption of tuberculous deer. Other species included in the survey were the opossum (Didelphis virginiana), raccoon (Procyonlotor), red fox (Vulpes vulpes), bobcat (Felis rufus), and badger (Taxidea taxus).

Public acceptance as a determinant of management strategies for bovine tuberculosis in free-ranging U.S. wildlife.

When bovine tuberculosis (bTB) is detected in free-ranging wildlife populations, preventing geographic spread and the establishment of a wildlife reservoir requires rapid, often aggressive response. Public tolerance can exert a significant effect on potential control measures available to managers, and thus on the success of disease management efforts. Separate outbreaks of bTB in free-ranging white-tailed deer (Odocoileus virginianus) in two midwestern states provide a case study. In Minnesota, bTB was first discovered in cattle in 2005 and subsequently in deer. To date, 12 beef cattle farms and 26 white-tailed deer have been found infected with the disease. From 2005 to 2008, disease prevalence in deer has decreased from 0.4% (SE=0.2%) to <0.1% and remained confined to a small (<425 km(2)) geographic area. Deer population reduction through liberalized hunting and targeted culling by ground sharpshooting and aerial gunning, combined with a prohibition on baiting and recreational feeding, have likely been major drivers preventing disease spread thus far. Without support from cattle producers, deer hunters and the general public, as well as politicians, implementation of these aggressive strategies by state and federal authorities would not have been possible. In contrast, Michigan first discovered bovine bTB in free-ranging deer in 1975, and disease management efforts were not instituted until 1995. The first infected cattle herd was diagnosed in 1998. Since 1995, disease prevalence in free-ranging deer has decreased from 4.9% to 1.8% in the ∼ 1500 km(2) core outbreak area. Culture positive deer have been found as far as 188 km from the core area. Liberalized harvest and restrictions on baiting and feeding have facilitated substantial reductions in prevalence. However, there has been little support on the part of hunters, farmers or the general public for more aggressive population reduction measures such as culling, and compliance with baiting and feeding restrictions has been variable and often problematic. We compare and contrast the Minnesota and Michigan outbreaks with respect to temporal, social, economic, and logistical factors that shape public attitudes toward aggressive disease control strategies, the limitations these factors place on management, and the implications for bTB eradication from wildlife reservoirs in the U.S.

ESTIMATING THE TRUE PREVALENCE OF MYCOBACTERIUM BOVIS IN HUNTER-HARVESTED WHITE-TAILED DEER IN MICHIGAN

Apparent prevalence, although useful as a consistent index, may underestimate the true prevalence of disease. In Michigan, the ability to estimate the true prevalence of bovine tuberculosis (TB; caused by Mycobacterium bovis) in free-ranging white-tailed deer (Odocoileus virginianus) will become increasingly important to accurately assess progress towards eradication. Our objectives were threefold: to estimate the true prevalence of M. bovis in free-ranging deer in Michigan, to evaluate the effectiveness of existing TB surveillance methods, and to indirectly assess whether TB epidemiologic data from captive cervid herds can be meaningfully extrapolated to free-ranging populations. The study population consisted of all free-ranging deer submitted for TB testing in 2001 from six townships in northeastern Lower Michigan. Tissue samples of tonsil and cranial lymph nodes were collected bilaterally from all deer eligible for the study that did not have gross lesions suggestive of TB (n = 701). Samples were subjected to histopathologic, acid-fast (AF) staining, mycobacterial culture, and polymerase chain reaction (PCR) testing. Seven deer cultured positive for M. bovis that would not have been detected by current surveillance, yielding apparent and true prevalence estimates (95% confidence limits) of 2.7% (1.6, 3.8) and 3.6% (2.3, 4.9), respectively. The sensitivity, specificity, and positive and negative predictive values of the current surveillance protocol were 75, 100, 100, and 99%, respectively. Histologic lesions were present only in tonsils, and ranged from simple necrosis to caseation, suppuration, and granuloma formation. Acid-fast staining and PCR detected M. bovis in only one of the seven culture-positive deer. Our study provides the first estimate of the true prevalence of M. bovis in Michigans free-ranging deer population and suggests modest underestimation of that prevalence by current surveillance. This study also suggests that caution is warranted when extrapolating epidemiologic data on TB in captive cervids to free-ranging populations and confirms the pivotal role of the tonsil in early infections.

Production and Survival of Elk (Cervus elaphus) Calves in Michigan

Abstract We determined production and survival of elk (Cervus elaphus nelsoni) calves in Michigan using a variety of methods to index herd productivity. Calf production in Michigan was comparable with the highest rates ever recorded for North American elk. Calf survival averaged 0.90 (sd = 0.05), 0.97 (sd = 0.04) and 0.87 (sd = 0.05) for summer, winter and annually, 1987–1991. Calf survival rates in Michigan were higher than in other North American elk populations. Continued high calf production, in combination with high calf survival, indicates that elk condition is excellent in Michigan, as habitat quality allows cow elk to breed and successfully raise a calf, essentially every year, despite the high energetic demands associated with late gestation and lactation.

AN OUTBREAK OF TYPE E BOTULISM AMONG COMMON LOONS (GAVIA IMMER) IN MICHIGAN'S UPPER PENINSULA

An epizootic of type E botulism (Clostridium botulinum) occurred among common loons (Gavia immer) along the Lake Michigan shore of Michigans Upper Peninsula (USA) during October and November 1983. An estimated 592 dead loons washed ashore along the Garden Peninsula. Type E botulinal toxin was demonstrated in blood samples and stomach contents of dead loons, and in samples of three species of dead fish found on the Lake Michigan shore. We suspect that loons acquired botulism by ingesting sick or dead fish containing type E toxin.