Executive Summary

Tuberculosis, a disease caused by infection by Mycobacterium tuberculosis, Mycobacterium bovis, or Mycobacterium avium, is contagious in humans and other mammals as well as in birds. The focus of this report, Mycobacterium bovis, causes disease primarily in cattle but also in other mammals, including humans. Because bovine tuberculosis poses a potent threat to animal and human health, its eradication has been sought in the United States since 1917. Transmission of the disease from infected animals to the general human population was effectively halted with the pasteurization of raw milk in the first quarter of the century. By 1985, federal and state government campaigns had dramatically reduced the population of cattle exposed to--and so possibly infected by--bovine tuberculosis from 5 percent of the nation's cattle to fewer than 0.03 percent. However, as the disease has persisted in livestock, it reduces productivity and presents a health threat to animal industry workers.

In the mid 1980s, eradication efforts appeared stymied even as new disease threats appeared. The persistence of infection in large dairy herds in the southwest, the apparent rise in the number of infected Mexican cattle imported into the United States, and the appearance of infected bison, elk, and deer in the rapidly growing captive herds all contributed to the enhanced potential for spread of bovine tuberculosis. As a consequence, both the feasibility of attaining the goal of eradication and the effectiveness of the cooperative state-federal eradication strategy were called into question. The Animal and Plant Health Inspection Service (APHIS) of the U.S. Department of Agriculture (USDA) requested that the National Research Council (NRC) evaluate the prospects for eradication and the appropriateness of the existing strategy.

TUBERCULOSIS IN THE UNITED STATES

Bovine tuberculosis probably entered the United States in cattle imported from Europe in the 1600s. In the 1800s and early 1900s, bovine tuberculosis was a significant health risk to people and caused considerable losses in the cattle industry as subclinical and full-blown disease decreased productivity and caused animals to suffer. Because the disease was widespread, it was clear that a concerted national program would be required for its control, and, if successful, society in general as well as the cattle industry would benefit significantly. The program initiated in 1917 had as its goal the eradication of bovine tuberculosis (the elimination of M. bovis) from all U.S. cattle (the only known reservoir at the time).

To detect disease in cattle, the initial program relied on a tuberculin skin test. Animals that responded with an increased skin thickness at the site of the intradermal injection were deemed to have been infected with M. bovis. Those cattle that reacted positively, called “reactors,” were slaughtered. Testing of cattle in each herd was repeated until each herd in an area and, ultimately, each state became free of reactors. Approximately 5 percent of cattle were reactors in initial testing in 1917. By 1940 the reactor rate had decreased to approximately 0.5 percent; by 1952 it was 0.1 percent.

In 1959 the reactor rate had declined to such a low level that it was not economically feasible to continue the area herd testing. Surveillance of carcasses at slaughter became the major detection



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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM Executive Summary Tuberculosis, a disease caused by infection by Mycobacterium tuberculosis, Mycobacterium bovis, or Mycobacterium avium, is contagious in humans and other mammals as well as in birds. The focus of this report, Mycobacterium bovis, causes disease primarily in cattle but also in other mammals, including humans. Because bovine tuberculosis poses a potent threat to animal and human health, its eradication has been sought in the United States since 1917. Transmission of the disease from infected animals to the general human population was effectively halted with the pasteurization of raw milk in the first quarter of the century. By 1985, federal and state government campaigns had dramatically reduced the population of cattle exposed to--and so possibly infected by--bovine tuberculosis from 5 percent of the nation's cattle to fewer than 0.03 percent. However, as the disease has persisted in livestock, it reduces productivity and presents a health threat to animal industry workers. In the mid 1980s, eradication efforts appeared stymied even as new disease threats appeared. The persistence of infection in large dairy herds in the southwest, the apparent rise in the number of infected Mexican cattle imported into the United States, and the appearance of infected bison, elk, and deer in the rapidly growing captive herds all contributed to the enhanced potential for spread of bovine tuberculosis. As a consequence, both the feasibility of attaining the goal of eradication and the effectiveness of the cooperative state-federal eradication strategy were called into question. The Animal and Plant Health Inspection Service (APHIS) of the U.S. Department of Agriculture (USDA) requested that the National Research Council (NRC) evaluate the prospects for eradication and the appropriateness of the existing strategy. TUBERCULOSIS IN THE UNITED STATES Bovine tuberculosis probably entered the United States in cattle imported from Europe in the 1600s. In the 1800s and early 1900s, bovine tuberculosis was a significant health risk to people and caused considerable losses in the cattle industry as subclinical and full-blown disease decreased productivity and caused animals to suffer. Because the disease was widespread, it was clear that a concerted national program would be required for its control, and, if successful, society in general as well as the cattle industry would benefit significantly. The program initiated in 1917 had as its goal the eradication of bovine tuberculosis (the elimination of M. bovis) from all U.S. cattle (the only known reservoir at the time). To detect disease in cattle, the initial program relied on a tuberculin skin test. Animals that responded with an increased skin thickness at the site of the intradermal injection were deemed to have been infected with M. bovis. Those cattle that reacted positively, called “reactors,” were slaughtered. Testing of cattle in each herd was repeated until each herd in an area and, ultimately, each state became free of reactors. Approximately 5 percent of cattle were reactors in initial testing in 1917. By 1940 the reactor rate had decreased to approximately 0.5 percent; by 1952 it was 0.1 percent. In 1959 the reactor rate had declined to such a low level that it was not economically feasible to continue the area herd testing. Surveillance of carcasses at slaughter became the major detection

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM mechanism, an activity that is still the pivotal part of the program today. Animals with tuberculous lesions were traced back to their original herds and all cattle that had been in contact with the infected or exposed individual were tested for tuberculosis. Using this approach, the prevalence of bovine tuberculosis continued to decline, and by 1978 the reactor rate was 0.03 percent. In 1991 the reactor rate was 0.02 percent. Given this slow but steady decline in disease rates, one might conclude that continued testing and slaughter would eventually result in eradication. However, within the past 10 years three persistent sources of infection have been identified, and their impact on the eradication program must be considered. In recent years, the number of feeder cattle entering the United States from Mexico has increased dramatically. Unfortunately, although these cattle may be certified as having negative tuberculin skin tests, a small percentage are in fact tuberculous and may pose a risk to the U.S. cattle population. Bovine tuberculosis in cattle is now concentrated in a small number (approximately 10) of dairies in Texas and New Mexico near the Mexican border. The official test and slaughter program has not been successful in clearing infection from these herds. In these large dairies (milking more than 2,000 cows each) slaughter of all cattle that had contact with a reactor would impose large economic losses. The number of ranched and farmed Cervidae, such as elk and deer (and wild ungulates in general), and their movement around the country has increased dramatically. Some of the original animals in the founding herds were infected with M. bovis, and these animals were traded and transported widely, spreading infection. Moreover, the infection spread rapidly because there was little awareness of its existence in Cervidae and there were no requirements or recommendations for routine testing. Until recently, there have been no federal or state requirements for the testing of Cervidae or provisions for compensation if slaughter of exposed animals is indicated. As a result, the bovine tuberculosis problem in these exotic species went largely undetected. Infected captive ungulates may spread the disease back to cattle, to wild ungulates, and to humans. It is important to consider bovine tuberculosis in the context of the wider North American setting. Enhanced international trade, increased livestock mobility, and public health concerns about disease in animals are impacted by the biology and methods of transmission of M. bovis. Canada is essentially free of bovine tuberculosis and may soon declare that eradication has been achieved in its national herd. Recently, tuberculosis in nonbovine ungulates has led to implementation of a test and slaughter campaign to stamp out that source of infection. So far as is known, Canada has no wildlife reservoir save one infected isolated bison herd in northern Alberta. In contrast, Mexico has only recently initiated a country-wide eradication campaign; the extent of tuberculosis in Mexico's national herd is not known. The recent formation of a National Commission for the Eradication of Bovine Tuberculosis signals the Mexican government's commitment to control the disease. Little evidence exists to suggest the presence of a wildlife reservoir of bovine tuberculosis in the continental United States. Although some species of animals in zoos are infected, these animals must be treated differently than domestic or wild species because of their scarcity and value. In any

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM event, zoo populations do not appear to be a significant risk as a source of infection to the animal industries. DIAGNOSTIC TECHNOLOGY Detection of bovine tuberculosis is the first step in any eradication or control effort. Improvements in test accuracy and application to nonbovine species as well as detection of infected animals at slaughter may be possible with new and anticipated developments in the basic scientific understanding of the infection. Much of the current work is focused on detection of tuberculous lesions, M. bovis organisms, M. bovis antigens, or the animal's response to infection. As noted previously, the detection of lesions has formed the basis of the surveillance for bovine tuberculosis at slaughter. Overall, this approach has been highly effective; however, individual infected animals may not have readily observable lesions (tubercles), and there is the general problem that the majority of granulomatous lesions are not caused by M. bovis. New tests may allow more rapid and accurate detection of M. bovis (alive or dead organisms) in tissues. Newer immunologic-based tests may circumvent the current protracted culture period (3 to 12 weeks) required to isolate and identify M. bovis. Enhancements of historically favored growth media plus modern organism detection systems can also improve the success rate of culture and isolation by at least twofold. Nucleic acid probes for identifying M. bovis isolated from tissue specimens are available commercially. The isolation of M. bovis organisms will still be necessary, however, for “fingerprinting” strains to enhance the ability to trace a specific organism to its source and identify its method of transmission. Detection of the animal's response to infection with M. bovis may be facilitated by newer cell-mediated tests such as lymphocyte transformation or the detection of lymphocyte products such as lymphokines [e.g., the gamma interferon (γ-IFN) test]. Newer serological tests based on specific antigens, coupled with immunoblotting and ELISA techniques, will become very useful secondary (to cell-mediated) tests to help determine the true health status of individual animals. In the long term, bovine tuberculosis will continue to be a problem for the United States even if it is eradicated domestically. There will be a continuing need for up-to-date knowledge and technology to protect against reintroduction and/or spread of the infection in international trade. Limited knowledge regarding novel or alternate tests and control procedures weakens the credibility of the program, particularly with owners of nonbovine species, and prevents improvements in the program's efficiency. Newer concepts and technologies consistent with evolving scientific advances will be necessary to meet the expectations of society and the needs of the global livestock industry. In addition to development of better tests and greater understanding of the basic biology of bovine tuberculosis, the role of epidemiology in test evaluation and usage is crucial. Ultimately, the definitive test would correctly identify all of the infected/diseased animals (100 percent sensitivity), avoiding false-negative results, and would correctly identify all of the noninfected/nondiseased animals (100 percent specificity), avoiding false-positives. The latter are particularly crucial at low prevalences of infection because a test with 99.9 percent specificity produces 100 false-positives for every 100,000 healthy animals tested. Surprisingly, there is little public documentation of the sensitivity and specificity of the traditional tests. In addition, there has been little formal work to bridge the use of tests at the individual animal level to their use at the herd or population level. It

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM does appear, however, that a theoretical evaluation of the efficacy of testing large herds agrees with the U.S. experience; namely, that the testing regimes that worked in small herds may not work in large herds such as those in the El Paso milkshed. Depopulation would be effective but it has not been financially possible to use it in the El Paso milkshed PUBLIC HEALTH From a public health perspective, the potential for direct transmission from animals to humans, particularly in farm families and others exposed by virtue of their occupation, remains a concern. Neither can the potential for spread from one infected animal in a petting zoo to large numbers of people be ignored. Nonetheless, the current resurgence of human tuberculosis is largely independent of the status of bovine tuberculosis. EVALUATION OF ERADICATION AND CONTROL OPTIONS The committee also considered the biologic and economic factors impinging on disease control and eradication efforts, believing it necessary to question whether eradication is feasible and, if so, how it might be most effectively achieved. In answering such questions, bioeconomic modeling has become a central technique. These mathematical models describe the factors that promote or constrain the spread of infection taking into account both biological and economic conditions that exist in the livestock industry. Examination of the results of bioeconomic models of bovine tuberculosis used in the United States, Canada, Australia, and Ireland revealed that the only nation of this group that had chosen control rather than eradication of the infection was Ireland, which is afflicted with an uncontrollable wildlife reservoir of bovine tuberculosis. The Australian model results suggested that eradication of tuberculosis in the northern territories would be demanding and perhaps not economically viable. Further, there were concerns about the limitations of the tuberculin skin test and the Australians were awaiting the development of a new (the γ-IFN) test to aid their program. Despite this caution, the cattle industry wished to forge ahead with the eradication program; currently the program is nearing successful completion using the traditional tuberculin skin test as the primary disease detection device. CONCLUSIONS AND RECOMMENDATIONS The committee has concluded that the goal of eradication of bovine tuberculosis in the United States is biologically and economically feasible. International experience has shown that the only developed countries that have chosen to control rather than eradicate bovine tuberculosis are those where the disease is endemic in wildlife populations. However, in order to achieve eradication, the existing State-Federal Cooperative Bovine Tuberculosis Eradication Program must be modified. Our central recommendation is as follows:

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM USDA should vigorously pursue eradication of bovine tuberculosis in cattle, bison, elk, deer, and other farmed exotic hoofed species. Although improvements in tests used to detect infection appear possible and should be pursued, the committee believes existing diagnostic technology is adequate to support a strengthened eradication effort. The application of bioeconomic modeling to historical United States and Canadian experience with bovine tuberculosis suggested the superiority of depopulation compared to test and slaughter as an eradication strategy. Depopulation produces the largest excess of benefits over costs to society because, in achieving eradication sooner, program costs are smaller and losses from disease are reduced. While the earlier models assumed adequate funds were available to compensate fully producers whose animals were designated for slaughter, the committee believes this assumption is unwarranted under the current fiscal constraints. Our second major recommendation is: Recognizing the constraints on public funds and the benefits from eradication that accrue to livestock enterprises, the committee recommends that producers of all affected species financially support the eradication program. In sharing responsibility for funding an eradication program with taxpayers, the livestock industry's involvement will promote attainment of a mutually beneficial goal and simultaneously acquire a direct interest in ensuring that the program is operated effectively. The optimal extent of producer participation and the choice of eradication strategy (e.g., depopulation or test and slaughter) could be evaluated with the use of bioeconomic models, updated to reflect changes in industry structure and public attitudes in the two decades since a comprehensive analysis for the United States was last undertaken. Any U.S. eradication strategy must address the three remaining sources of infection: (1) the persistent infection in large dairy herds in the southwest; (2) the apparent rise in the number of infected Mexican beef, dairy, and rodeo cattle imported into the United States; and (3) the appearance of infected bison, elk, and deer in captive herds. Each source implies the need for changes in the operation of the State-Federal Cooperative Bovine Tuberculosis Eradication Program. To combat endemic tuberculosis in Texas dairy herds, USDA should assemble and assign a field investigation and management team to the El Paso milkshed to perform or oversee all testing and test interpretation in infected and exposed herds, to ensure accurate animal identification and tracking, as well as appropriate recordkeeping and data collection, to identify key sources of disease risk, and to enforce quarantine and take other steps toward eradication as necessary, including depopulation. In the interest of both the United States and Mexico, the United States should provide Mexico with epidemiological, laboratory, and training support for bovine tuberculosis control. More immediately, uniform regulations controlling movement and identification of Mexican cattle should be adopted by all states to require specification of the destination of a shipment and allow shipment only to quarantine pastures, feedlots, or to designated holding areas for retest.

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM To protect the national livestock herd and wildlife, a program should be initiated to eradicate bovine tuberculosis in farmed elk, deer, and other hoofed exotic species. Federal authority to pursue eradication should be exercised by APHIS in issuing Uniform Methods and Rules separate from those for cattle and bison. Although the likelihood of M. bovis infection in humans has been greatly reduced by the control of tuberculosis in animals and animal products, subgroups of the human population still experience risk. Consequently, it is prudent to take measures to minimize the possibility of disease transmission between animals and humans. To protect human and animal health, all confirmed diagnoses of M. bovis should be reported to public veterinary and medical officials. Federal public health authorities should differentiate among organisms in the M. tuberculosis complex in reporting disease incidence, initiate surveillance in all instances in which risk of transmission between animals and humans exists, and consider educational efforts aimed at those who may come into contact with infected animals. There is always a danger that success in the eradication program removes incentives to learn more about bovine tuberculosis. However, continuing efforts in research and in training animal health personnel are needed to assure effectiveness in disease detection and management, to meet changing requirements of food safety regulations, and to cope with the inexperience of animal industry workers with this disease. USDA should institute ongoing evaluation of new diagnostic technologies to complement the routine application of existing tests. Ongoing collaborative research should investigate pathogenesis, immunology, diagnostic approaches, genetic resistance, and the epidemiology of bovine tuberculosis. New surveillance methods for bovine tuberculosis at slaughter, designed to detect M. bovis infection in the absence of gross lesions and compatible with Hazard Analysis Critical Control Point (HACCP) inspection, should be developed. More immediately, USDA's Food Safety Inspection Service should reconfigure its goals for sampling carcasses for lesions in order to reflect accurately the probability of infection that varies by animal species, animal type, and region. To ensure that new scientific programs and technologies are used effectively, USDA should allocate the resources necessary to expand training of current and newly hired animal health workers according to their need to know about bovine tuberculosis. Experienced field personnel who have worked with naturally occurring bovine tuberculosis must be available as needed, allowing the testing program to reduce its reliance on accredited veterinarians.