Bovine Tuberculosis in Swedish Farmed Deer: Detection and Control of the Disease

Bovine tuberculosis (BTB) was introduced into Swedish farmed deer herds in 1987. Epidemiological investigations showed that 10 deer herds had become infected (July 1994) and a common source of infection, a consignment of 168 imported farmed fallow deer, was identified (I). As trace-back of all imported and in-contact deer was not possible, a control program, based on tuberculin testing, was implemented in July 1994. As Sweden has been free from BTB since 1958, few practicing veterinarians had experience in tuberculin testing. In this test, result relies on the skill, experience and conscientiousness of the testing veterinarian. Deficiencies in performing the test may adversely affect the test results and thereby compromise a control program. Quality indicators may identify possible deficiencies in testing procedures. For that purpose, reference values for measured skin fold thickness (prior to injection of the tuberculin) were established (II) suggested to be used mainly by less experienced veterinarians to identify unexpected measurements. Furthermore, the within-veterinarian variation of the measured skin fold thickness was estimated by fitting general linear models to data (skin fold measurements) (III). The mean square error was used as an estimator of the within-veterinarian variation. Using this method, four (6%) veterinarians were considered to have unexpectedly large variation in measurements. In certain large extensive deer farms, where mustering of all animals was difficult, meat inspection was suggested as an alternative to tuberculin testing. The efficiency of such a control was estimated in paper IV and V. A Reed Frost model was fitted to data from seven BTB-infected deer herds and the spread of infection was estimated (< 0.6 effective contacts per deer and year) (IV). These results were used to model the efficiency of meat inspection in an average extensive Swedish deer herd. Given a 20% annual slaughter and meat inspection, the model predicted that BTB would be either detected or eliminated in most herds (90%) 15 years after introduction of one infected deer. In 2003, an alternative control for BTB in extensive Swedish deer herds, based on the results of paper V, was implemented.

Wild Boar and Red Deer Display High Prevalences of Tuberculosis-Like Lesions in Spain

We describe the distribution of tuberculosis-like lesions (TBL) in wild boar (Sus scrofa) and red deer (Cervus elaphus) in Spain. Animals with TBL were confirmed in 84.21% of mixed populations (n = 57) of red deer and wild boar and in 75% of populations of wild boar alone (n = 8) in central and southern Spain (core area). The prevalence of TBL declined towards the periphery of this region. In the core area, the prevalence ranged up to 100% in local populations of wild boar (mean estate prevalence 42.51%) and up to 50% in red deer (mean estate prevalence 13.70%). We carried out exploratory statistical analyses to describe the epidemiology of TBL in both species throughout the core area. Prevalence of TBL increased with age in both species. Wild boar and red deer mean TBL prevalence at the estate level were positively associated, and lesion scores were consistently higher in wild boars than in red deer. The wild boar prevalence of TBL in wild boar did not differ between populations that were or were not cohabiting with red deer. Amongst the wild boars with TBL, 61.19% presented generalized lesions, and the proportion of generalized cases was similar between sex and age classes. In red deer, 57.14% of TBL-positive individuals presented generalized lesions, and the percentage of generalized cases increased with age class, but did not differ between the sexes. These results highlight the potential importance of wild boar and red deer in the maintenance of tuberculosis in south central Spain.

Risk Factors Associated With the Prevalence of Tuberculosis-Like Lesions in Fenced Wild Boar and Red Deer in South Central Spain

In recent decades the management of large game mammals has become increasingly intensive in south central Spain (SCS), resulting in complex epidemiological scenarios for disease maintenance, and has probably impeded schemes to eradicate tuberculosis (TB) in domestic livestock. We conducted an analysis of risk factors which investigated associations between the pattern of tuberculosis-like lesions (TBL) in wild boar (Sus scrofa) and red deer (Cervus elaphus) across 19 hunting estates from SCS and an extensive set of variables related to game management, land use and habitat structure. The aggregation of wild boar at artificial watering sites was significantly associated with an increasing risk of detecting TBL in both species, which probably relates to enhanced opportunities for transmission. Aggregation of wild boar at feeding sites was also associated with increased risks of TBL in red deer. Hardwood Quercus spp. forest availability was marginally associated with an increased risk of TB in both species, whereas scrubland cover was associated with a reduced individual risk of TBL in the wild boar. It is concluded that management practices that encourage the aggregation of hosts, and some characteristics of Mediterranean habitats could increase the frequency and probability of both direct and indirect transmission of TB. These findings are of concern for both veterinary and public health authorities, and reveal tuberculosis itself as a potential limiting factor for the development and sustainability of such intensive game management systems in Spanish Mediterranean habitats.

VS - Bovine Tuberculosis (Mycobacterium bovis) Surveillance Standards 11/2001

Bovine tuberculosis (TB) is an infectious and communicable granulomatous disease caused by the acidfast bacilli bacteria of Mycobacterium bovis (M. bovis). It is commonly a chronic, debilitating disease, but occasionally may assume an acute, rapidly progressive course. M. bovisis a widespread zoonosis that is global in magnitude and affects nearly all species of vertebrates (cattle, sheep, goats, pigs, bison, buffalo, and camelids.) Disease is spread by direct contact, inhalation of infected droplets expelled from infected lungs, and ingestion of contaminated feed or milk. In most countries, TB is a notifiable disease. Overall, TB has an important world-wide impact on animal industries and human health. Control measures are based on prevention and eradication. Surveillance is a key element for management of preventions and control programs. Surveillance for TB serves the purpose of enabling Veterinary Services to obtain an accurate picture of the scope of the disease in the US livestock populations; in the event of a disease outbreak, the course TB follows in livestock and wildlife populations for a given area over time; and permits timely intervention if the trend observed deviates from what is expected.

Seasonality of tuberculosis in India: is it real and what does it tell us?

India has a third of the world’s tuberculosis cases. Large-scale expansion of a national program in 1998 has allowed for population-based analyses of data from tuberculosis registries. We assessed seasonal trends using quarterly reports from districts with stable tuberculosis control programs (population 115 million). In northern India, tuberculosis diagnoses peaked between April and June, and reached a nadir between October and December, whereas no seasonality was reported in the south. Overall, rates of new smear-positive tuberculosis cases were 57 per 100 000 population in peak seasons versus 46 per 100 000 in trough seasons. General health-seeking behavior artifact was ruled out. Seasonality was highest in paediatric cases, suggesting variation in recent transmission.

Monitoring of Transmission of Tuberculosis between Wild Boars and Cattle: Genotypical Analysis of Strains by Molecular Epidemiology Techniques

An epidemiological survey for the monitoring of bovine tuberculosis transmission was carried out in western Liguria, a region in northern Italy. Fifteen Mycobacterium bovis strains were isolated from 63 wild boar samples (62 from mandibular lymph nodes and 1 from a liver specimen). Sixteen mediastinal lymph nodes of 16 head of cattle were collected, and 15 Mycobacterium bovis strains were subsequently cultured. All M. bovisstrains isolated from cattle and wild boars were genotyped by spoligotyping and by restriction fragment length polymorphism (RFLP) analysis with the IS6110 and IS1081 probes. All M. bovis strains showed the typical spoligotype characterized by the absence of the 39 to 43 spacers in comparison with the number in M. tuberculosis. A total of nine different clusters were identified by spoligotyping. The largest cluster included 9 strains isolated from wild boars and 11 strains isolated from cattle, thus confirming the possibility of transmission between the two animal species. Fingerprinting by RFLP analysis with the IS6110 probe showed an identical single-band pattern for 29 of 30 strains analyzed, and only 1 strain presented a five-band pattern. The use of IS1081 as a second probe was useful for differentiation of M. bovis from M. bovis BCG but not for differentiation among M. bovis strains, which presented the same undifferentiated genomic profile. In relation to the epidemiological investigation, we hypothesized that the feeding in pastures contaminated by cattle discharges could represent the most probable route of transmission of M. bovis between the two animal species. In conclusion, our results confirmed the higher discriminatory power of spoligotyping in relation to that of RFLP analysis for the differentiation of M. bovis genomic profiles. Our data showed the presence of a common M. bovis genotype in both cattle and wild boars, confirming the possible interspecies transmission of M. bovis.

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.

Risk of Disease from Wildlife Reservoirs: Badgers, Cattle, and Bovine Tuberculosis

Livestock face complex foraging options associated with optimizing nutrient intake while being able to avoid areas posing risk of parasites or disease. Areas of tall nutrient-rich swards around fecal deposits may be attractive for grazing, but might incur fitness costs from parasites. We use the example of dairy cattle and the risks of tuberculosis transmission posed to them by pastures contaminated with badger excreta to examine this trade-off. A risk may be posed either by aerosolized inhalation through investigation or by ingestion via grazing contaminated swards. We quantified the levels of investigation and grazing of 150 dairy cows at badger latrines (accumulations of feces and urine) and crossing points (urination-only sites). Grazing behavior was compared between strip-grazed and rotation-grazed fields. Strip grazing had fields subdivided for grazing periods of <24 h, whereas rotational grazing involved access to whole fields for 1 to 7 d each. A higher proportion of the herd investigated badger latrines than crossing points or controls. Cattle initially avoided swards around badger latrines but not around crossing points. Avoidance periods were shorter in strip- compared with rotation-grazing systems. In rotation-grazing management, latrines were avoided for longer times, but there were more investigative contacts than with strip-grazing management. If investigation is a major route of tuberculosis transmission, the risk to cattle is greatest in extensive rotation-grazing systems. However, if ingestion of fresh urine is the primary method of transmission, strip-grazing management may pose a greater threat. Farming systems affect the level and type of contact between livestock and wildlife excreta and thus the risks of disease.

Bovine Tuberculosis in a Free-ranging Mule Deer (Odocoileus hemionus) from Montana

A survey of 41 mule deer (Odocolleus hemionus) and three white-tailed deer (O. virginianus) for bovine tuberculosis was conducted on a Montana (USA) cattle ranch from 2 November 1993 through January 1994. Gross and microscopic lesions typical of tuberculosis were present in tonsil and lymph nodes of the head, thorax, and abdomen of one adult female mule deer. Additionally, a single microgranuloma considered morphologically suggestive of tuberculosis was present in one lymph node of the head of a second mule deer. Mycobacterial isolates from lymph nodes of the head and thorax of the first deer were identified as Mycobacterium bovis.

Comparison of Gross Pathology, Histopathology, and Mycobacterial Culture for the Diagnosis of Tuberculosis in Elk (Cervus elaphus)

Using the isolation of Mycobacterium bovis as the reference standard, this study evaluated the sensitivity, specificity and kappa statistic of gross pathology (abattoir postmortem inspection), histopathology, and parallel or series combinations of the two for the diagnosis of tuberculosis in 430 elk and red deer. Two histopathology interpretations were evaluated: histopathology I, where the presence of lesions compatible with tuberculosis was considered positive, and histopathology II, where lesions compatible with tuberculosis or a select group of additional possible diagnoses were considered positive. In the 73 animals from which M. bovis was isolated, gross lesions of tuberculosis were most often in the lung (48), the retropharyngeal lymph nodes (36), the mesenteric lymph nodes (35), and the mediastinal lymph nodes (16). Other mycobacterial isolates included: 11 M. paratuberculosis, 11 M. avium, and 28 rapidly growing species or M. terrae complex. The sensitivity estimates of gross pathology and histopathology I were 93% (95% confidence limits [CL] 84,97%) and 88% [CL 77,94%], respectively, and the specificity of both was 89% [CL 85,92%]). The sensitivity and specificity of histopathology II were 89% (CL 79,95%) and 77% (CL 72,81%), respectively. The highest sensitivity estimates (93- 95% [CL 84,98%]) were obtained by interpreting gross pathology and histopathology in parallel (where an animal had to be positive on at least one of the two, to be classified as combination positive). The highest specificity estimates (94-95% [CL 91-97%]) were generated when the two tests were interpreted in series (an animal had to be positive on both tests to be classified as combination positive). The presence of gross or microscopic lesions showed moderate to good agreement with the isolation of M. bovis (Kappa = 65-69%). The results show that post-mortem inspection, histopathology and culture do not necessarily recognize the same infected animals and that the spectra of animals identified by the tests overlaps.

Emergence of Diseases From Wildlife Reservoirs

Interest in the epidemiology of emerging diseases of humans and livestock as they relate to wildlife has increased greatly over the past several decades. Many factors, most anthropogenic, have facilitated the emergence of diseases from wildlife. Some livestock diseases have ‘‘spilled over’’ to wildlife and then ‘‘spilled back’’ to livestock. When a population is exposed to an infectious agent, depending on an interaction of factors involving the host, agent, and environment, the population may be resistant to infection or may become a dead-end host, a spillover host, or a maintenance host. Each exposure is unique; the same species of host and agent may respond differently in different situations. Management actions that affect the environment and behavior of a potential host animal may allow the emergence of a new or as yet undetected disease. There are many barriers in preventing, detecting, monitoring and managing wildlife diseases. These may include political and legal hurdles, lack of knowledge about many diseases of wildlife, the absence of basic data on wildlife populations, difficulties with surveillance, and logistical constraints. Increasing interaction between wildlife and humans or domestic animals may lead to disease emergence and require innovative methods and strategies for disease surveillance and management in wildlife.

The Role of a Wildlife Reservoir in the Epidemiology of Bovine Tuberculosis

The objective of this project was to study the epidemiology of bovine tuberculosis in the presence of a wildlife reservoir species. Cross-sectional and longitudinal studies of possum populations with endemic bovine tuberculosis infection were analyzed. The results were used to develop a computer simulation model of the dynamics of bovine tuberculosis infection in possum populations. A case-control study of breakdowns to tuberculosis infection in cattle herds in the Central North Island of New Zealand was conducted to identify risk factors other than exposure to tuberculosis in local possum populations.

Recommendations for Elimination of Bovine Tuberculosis in Free-Ranging White-Tailed Deer in Michigan

A significant infection rate of bovine TB in the deer population of the northeastern lower peninsula poses a potential risk to several important values including public health, United States Department of Agriculture (U.S.D.A.) TB-free accreditation for Michigan cattle, wildlife health, wildlife-related recreation and tourism and economic stability in several sectors. A risk assessment study by the U.S. D.A. Centers for Epidemiology and Animal Health (Fort Collins, CO) predicted that if no changes were made in the management of the affected free-ranging deer population, the TB prevalence (compared to the current prevalence of 2.3%). Although the current annual risk of TB transfer to cattle in the affected area is .I%, the report estimated a 12% cumulative risk that at least one head of cattle would become infected over the next 25 years if no changes are made in deer and/or cattle management.

Vaccination with Mycobacterium bovis BCG Strains Danish and Pasteur in White-tailed Deer (Odocoileus virginianus) Experimentally Challenged with Mycobacterium bovis

Wildlife reservoirs of Mycobacterium bovis represent serious obstacles to the eradication of tuberculosis in domestic livestock and the cause for many faltering bovine tuberculosis eradication programs. One approach in dealing with wildlife reservoirs of disease is to interrupt inter-species and intraspecies transmission through vaccination of deer or cattle. To evaluate the efficacy of BCG vaccination in white-tailed deer, 35 deer were assigned to one of three groups; one s.c. dose of 107 CFU of M. bovis BCG Pasteur (n = 12); 1 s.c. dose of 107 CFU of M. bovis BCG Danish (n = 11); or unvaccinated deer (n = 12). After vaccination, deer were inoculated intratonsilarly with virulent M. bovis. Lesion severity scores of the medial retropharyngeal lymph node, as well as all lymph nodes combined, were reduced in vaccinated deer compared to unvaccinated deer. BCG Danish vaccinated deer had no late stage granulomas characterized by coalescent caseonecrotic granulomas containing numerous acid-fast bacilli compared to BCG Pasteur vaccinated or unvaccinated deer where such lesions were present. Both BCG strains were isolated as late as 250 days after vaccination from deer that were vaccinated but not challenged. In white-tailed deer, BCG provides protection against challenge with virulent M. bovis. Issues related to vaccine persistence, safety and shedding remain to be further investigated.

Vaccination of White-Tailed Deer (Odocoileus virginianus) with Mycobacterium bovis Bacillus Calmette Guerin

Wildlife reservoirs of Mycobacterium bovis represent serious obstacles to the eradication of tuberculosis in domestic livestock. In Michigan, USA tuberculous white-tailed deer transmit M. bovis to cattle. One approach in dealing with this wildlife reservoir is to vaccinate deer in order to interrupt the cycle of deer to deer and deer to cattle transmission. Thirty-one white-tailed deer were assigned to one of three groups; 2 SC doses of 107 CFU of M. bovis BCG (n = 11); 1 SC dose of 107 CFU of M. bovis BCG (n = 10); or unvaccinated deer (n = 10). After vaccination, deer were inoculated intratonsilarly with 300 CFU of virulent M. bovis. Gross lesion severity scores of the medial retropharyngeal lymph node were significantly reduced in deer receiving 2 doses of BCG compared to unvaccinated deer. Vaccinated deer had fewer lymph node granulomas than unvaccinated deer, and most notably, fewer late stage granulomas characterized by coalescent caseonecrotic granulomas containing numerous acid-fast bacilli. BCG was isolated from 7/21 vaccinated deer as long as 249 days after vaccination. In one case BCG was transmitted from a vaccinated deer to an unvaccinated deer. In white-tailed deer BCG provides measurable protection against challenge with virulent M. bovis. However, persistence of vaccine within tissues as well as shedding of BCG from vaccinates remain areas for further investigation.