Chapter 3

Bovine Tuberculosis Eradication Programs

Evaluation of Robert Koch's old tuberculin (OT) as a diagnostic tool began in January 1891, just 5 years after its discovery. Skin testing with OT soon became the chief diagnostic tool for both human and animal tuberculosis. It was not until 1932, when Florence Seibert purified OT into a material that she designated “purified protein derivative” (PPD), that there was an advance, an increased specificity, in diagnosing tuberculosis.

THE UNITED STATES

Historical Perspectives

In 1897 Massachusetts initiated testing of all cattle so that tuberculous cattle could be identified and destroyed rather than used for production of meat and milk for human consumption. In 1906 federal meat inspection was initiated; at this time, 4 to 5 percent of all cattle and 16 percent of swine carcasses were partially or totally condemned because of tuberculosis lesions. Also in 1906 the Bureau of Animal Industries of the USDA first started testing cattle with the OT skin test in the District of Columbia. This initial testing was conducted to evaluate the procedure and educate animal health officials in preparation for an eradication program.

In 1908 tuberculosis testing of cattle was required for all animals entered in county and state fairs. In 1911 municipalities began passing regulations that required mandatory milk pasteurization and/or certification of dairy herds as tuberculosis free (Meyers and Steele, 1969). In 1917, under pressure from medical, veterinary, and animal industry lobbies, Congress passed a $1 million appropriations bill initiating the State-Federal Cooperative Bovine Tuberculosis Eradication Program (Meyers, 1940; Daniel and Janick, 1978).

This national eradication program entailed whole-herd testing and slaughter of all reactors. The OT skin test was the basis for the official eradication program that called for the step-wise quarantine and removal of reactors from infected herds. When a herd was deemed to be free of tuberculosis, it was classified as accredited free. This process was repeated sequentially until a herd, an area, or state had no infected animals and could be declared tuberculosis free.

At the onset of the eradication program, 4.9 percent of all cattle tested were reactors (Meyers, 1940). In 1928, North Carolina became the first state to achieve modified accredited-free status. In 1935, 25,237,532 tests were administered and 376,623 reactors were found (1.5 percent). This represented the peak of the tuberculosis program in terms of tests and expenditures. The entire nation became modified accredited tuberculosis free with a reactor rate of 0.46 percent in 1940, falling to 0.11 percent in 1952.



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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM Chapter 3 Bovine Tuberculosis Eradication Programs Evaluation of Robert Koch's old tuberculin (OT) as a diagnostic tool began in January 1891, just 5 years after its discovery. Skin testing with OT soon became the chief diagnostic tool for both human and animal tuberculosis. It was not until 1932, when Florence Seibert purified OT into a material that she designated “purified protein derivative” (PPD), that there was an advance, an increased specificity, in diagnosing tuberculosis. THE UNITED STATES Historical Perspectives In 1897 Massachusetts initiated testing of all cattle so that tuberculous cattle could be identified and destroyed rather than used for production of meat and milk for human consumption. In 1906 federal meat inspection was initiated; at this time, 4 to 5 percent of all cattle and 16 percent of swine carcasses were partially or totally condemned because of tuberculosis lesions. Also in 1906 the Bureau of Animal Industries of the USDA first started testing cattle with the OT skin test in the District of Columbia. This initial testing was conducted to evaluate the procedure and educate animal health officials in preparation for an eradication program. In 1908 tuberculosis testing of cattle was required for all animals entered in county and state fairs. In 1911 municipalities began passing regulations that required mandatory milk pasteurization and/or certification of dairy herds as tuberculosis free (Meyers and Steele, 1969). In 1917, under pressure from medical, veterinary, and animal industry lobbies, Congress passed a $1 million appropriations bill initiating the State-Federal Cooperative Bovine Tuberculosis Eradication Program (Meyers, 1940; Daniel and Janick, 1978). This national eradication program entailed whole-herd testing and slaughter of all reactors. The OT skin test was the basis for the official eradication program that called for the step-wise quarantine and removal of reactors from infected herds. When a herd was deemed to be free of tuberculosis, it was classified as accredited free. This process was repeated sequentially until a herd, an area, or state had no infected animals and could be declared tuberculosis free. At the onset of the eradication program, 4.9 percent of all cattle tested were reactors (Meyers, 1940). In 1928, North Carolina became the first state to achieve modified accredited-free status. In 1935, 25,237,532 tests were administered and 376,623 reactors were found (1.5 percent). This represented the peak of the tuberculosis program in terms of tests and expenditures. The entire nation became modified accredited tuberculosis free with a reactor rate of 0.46 percent in 1940, falling to 0.11 percent in 1952.

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM In 1965 the direction of the program was changed to slaughter surveillance instead of repetitious whole-herd testing. The finding of a tuberculous animal at slaughter initiated a traceback with intradermal testing of the herd of origin and any other cattle that might have been exposed. By 1965 New Hampshire had no M. bovis infections for 12 consecutive years and became the first state to be designated accredited free. As the overall frequency of tuberculosis decreased, a supplementary test was required to decrease the number of false-positive tests and the number of animals unnecessarily slaughtered. Thus in 1973 the Uniform Methods and Rules (UMR) were changed so that animals with a caudal fold response in routine testing would be retested by the comparative cervical test (CCT). In 1978 the infection rate was 0.03 percent, and in 1991 the infection rate had fallen to 0.02 percent with 293 tuberculous carcasses found out of 36,000,000 head slaughtered (U.S. Department of Agriculture, 1992b). Despite the dramatic progress in the early years of the eradication campaign, from 1983 to 1992 an average of 12 newly infected cattle herds were detected each year (Figure 3-1). This plateau of infected herd discovery reflects no apparent progress toward the goal of eradication. The prevalence of 0.02 percent has remained steady for approximately 10 years in the nation's cattle population. If species other than cattle were included in the calculation, however, this prevalence rate FIGURE 3-1 Number of newly infected and exposed herds. Source: USDA Bovine Tuberculosis Eradication Program.

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM would have increased, since there has been an increase in the reported cases of M. bovis infection in bison and domestic deer and elk populations (U.S. Department of Agriculture, 1990; Hosker, 1987). Legal Authority for the Eradication Program The basic authority for eradication of bovine tuberculosis is provided in the Animal Industry Act of 1884 and the Cattle Contagious Disease Act of 1903 as amended. The authority to proceed with the tuberculosis eradication program began with the 1917 Agricultural Appropriations Act, which provided funds to start the program. The federal authorities for bovine tuberculosis eradication arise from a variety of sources (U.S. Department of Agriculture, 1989): 21 U.S. Code 111, 114, 114a, 115-117, 120-126, 134b, 134f 7 U.S. Code 391, 450 7 Code of Federal Regulations 2.17, 2.51, 371.2(d) 9 Code of Federal Regulations 50, 71, 77 These regulations cover all interstate movements of cattle, bison, and dairy goats. They also deal with the disposition of herds found to be infected with bovine tuberculosis and standard testing procedures. Control of the federal eradication program is the responsibility of APHIS, with advisory input from the U.S. Animal Health Association, a group of federal, state, and industry officials. APHIS publishes guidelines concerning the testing, interstate movement, and disposition of tuberculosis exposed/infected animals. These guidelines are considered minimum standards and do not preclude adoption of more stringent standards by any geographic or political subdivision of the United States. This flexibility has resulted in a patchwork of policies, strategies, and programs. There are also variations in legislation and enforcement among individual states. For example, this diversity is manifest in the various levels of supplementary indemnity (if any) that the states may provide to the owners of depopulated herds. States also vary in the way they control the movement of potentially infected and exposed cattle. Both state and federal authorities exist to administer a program such as the Tuberculosis Eradication Program. Each state, however, has separate and individual regulations that cover bovine tuberculosis in many animal species. For a complete record of each state's regulations, it would be necessary to contact each state and compile their regulations. As noted below, there is only one overriding national rule--a law that prohibits the interstate movement of any animal known to be affected with bovine tuberculosis (Code of Federal Regulations, 1992). Animal movements are regulated under the auspices of both the federal and state governments (Code of Federal Regulations, 1992). In general, federal regulations cover interstate movements; state regulations cover intrastate movements of official program species and interstate movement of all other species. Some states may have regulations for importation of animals that are more stringent than the existing federal regulations; the state regulations would take precedence over federal regulations in those instances. Federal movement requirements are chronicled in both the UMR and title 9 Code of Federal Regulations (U.S. Department of Agriculture, 1989; Code of Federal Regulations, 1992). These regulations require that no animal with a response to an official tuberculosis test is eligible for either international or interstate movement (U.S. Department of Agriculture, 1990).

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM Until 1993 the Cooperative State-Federal Bovine Tuberculosis Eradication Program applied only to cattle and bison, with provisions for voluntary herd accreditation for goats and camelids. Until recently the USDA 's authority did not include Cervidae; therefore, each state applied individual regulations if state regulations existed. As with cattle, state authority differs widely with regard to testing, quarantine, animal destruction requirements, and availability of indemnity funds. A UMR incorporating Cervidae into the national program and official testing procedures has been developed by APHIS. Official Tests The official skin tests as mandated by the UMR (U.S. Department of Agriculture, 1989) are the intradermal caudal fold test, the comparative cervical test, and the single cervical test. The tests can only be administered by veterinarians authorized by USDA, and the same veterinarian must both inject and evaluate the animal. The standard tuberculin test in cattle for screening purposes is the caudal fold test using 0.1 ml of bovine PPD (U.S. Department of Agriculture, 1988). The tuberculin is injected intradermally in either of the caudal folds just lateral to the base of the tail and the response is evaluated 72 ± 6 hours later. This test is a presumptive diagnostic test, and any response is recorded as a suspect reaction, requiring supplemental testing and epidemiological evaluation. The comparative cervical test was adopted in the United States in 1973 in an attempt to better differentiate M. bovis-caused tuberculous responses from other responses detected with the caudal fold screening test (Roswurm and Konyha, 1973; Duffield et al., 1985; U.S. Department of Agriculture, 1988). The test is administered within 10 days or after 60 days of the caudal fold injection. This test consists of injecting both avian PPD and bovine PPD into the sensitive skin of the neck. The relative responses to each tuberculin are compared in order to classify the animal's tuberculosis status (Suther et al., 1974; Hosker, 1987). The single cervical test is applied in some situations when cattle are known to have been exposed to M. bovis, such as animals originating from or present in an infected herd (U.S. Department of Agriculture, 1988). This test is used to increase the sensitivity of test procedures because the cervical skin is considered to be more sensitive than the caudal fold skin for tuberculin responses (de Kantor et al., 1984). Double-strength bovine PPD is used in the test, again, to enhance sensitivity. Slaughter Surveillance Although slaughter surveillance has always been a part of the tuberculosis eradication program, whole-herd testing was the primary surveillance system until the mid 1960s. Because of the extremely low prevalence of the disease by that time (< 0.1 percent) and the high cost of whole-herd testing by the caudal fold test, USDA changed the primary method of case-finding from whole-herd testing to slaughter surveillance. The slaughter surveillance system includes epidemiological follow-up of infected carcasses at slaughter as a primary diagnostic tool. The surveillance program requires USDA's Food Safety Inspection Service (FSIS) to submit samples from the slaughter plant to the APHIS National Veterinary Services Laboratory (NVSL) for diagnosis. Positive histopathological results or culture of M. bovis initiates a follow-up investigation by APHIS Veterinary Services (VS).

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM The official back-tag identification system that was implemented in 1960 for market cattle was a great aid in tracing most slaughter cattle back to herds of origin. For example, one outbreak of tuberculosis found by traceback of a single infected cow at slaughter to an infected beef farm in Oklahoma has been described (Schoenbaum et al., 1992). Historically, secondary surveillance programs such as adjacent herd testing, tracing the movement of cattle into and out of infected herds, and high-risk area testing are essential components of the program's success. Although slaughter tracebacks have been particularly effective with adult cattle, feedlot cattle present a unique problem. The nature of feedlot cattle marketing activities in the United States prevents traceback of individual tuberculous feedlot animals beyond the feedlot of origin. This is because most feedlot operators assemble pens of cattle either from numerous different lots purchased at livestock markets or by purchasing cattle through order buyers who deal directly with farms and ranches to assemble the appropriate numbers, ages, and types of cattle needed by the feedlot. Thus cattle from many sources are mixed before reaching the feedlot and their farm of origin often is unknown to the feedlot owner. Most experts agree that the ultimate eradication of bovine tuberculosis from the United States would be greatly facilitated by a national compulsory animal identification program. In 1969 it was determined by APHIS, based on statistical principles, that a submission rate of one suspect lesion per 2,000 adult cattle slaughtered would constitute optimal surveillance. In 1970 APHIS/VS adopted a goal of one granulomatous lesion per 2,500 cattle of any age inspected at regular slaughter as optimal for tuberculosis surveillance (Kryder, 1970). There has been and continues to be serious concern about the low rate of submission of suspect lesions. The “Report of Tuberculosis Lesions or Thoracic Granulomas” (VS form 6-35), which reports on regular-kill animals, shows that an average of 3,708 lesions were submitted annually from regular kill during 1989 and 1991. This submission rate from regular kill averaged one submission per 8,654 adult cattle inspected--considerably lower than the desired one per 2,000 slaughtered. In 1993, 4,040 samples were submitted, which was only 35 percent of the ideal submissions based on an annual slaughter rate of approximately 36,000,000 cattle (VanTiem and Essey, 1993). The average number of infected cattle identified annually through slaughter surveillance from 1980 through 1993 was 131 head, ranging from a low of 27 head in 1983 to a high of 613 head in 1992. Since the late 1980s most of the positive slaughter reactors have been traced to steers from Mexico; 84 percent of the 388 slaughter feedlot reactors in 1993 were traced to Mexican steers. Another serious concern is correct identification of the carcass from which the sample was taken. The inclusion of individual animal identification with slaughter samples is essential for the traceback of M. bovis-infected animals to their herd of origin. In 1993 only 25 percent of the samples submitted to NVSL had adequate identification (VanTiem and Essey, 1993). An incorrect identification tag attributed to an affected carcass causes substantial losses in time, money, and failed traceback cases. Experience has indicated that the reliance on slaughter surveillance was the correct decision, although concern continues about the low and variable rates of lesion submission between plants within an area and from area to area in the nation (U.S. Department of Agriculture, Animal Plant Health Inspection Service, Veterinary Service, 1992). Because we know of no formal studies on the efficiencies of various case-finding methods in the United States, it may be worthwhile to note the results of an assessment of slaughter surveillance in Australia. In the Australian program, slaughter surveillance was also the chief disease detection method; however, because infected herds were being found by other methods, a formal study was initiated. This study included the complete testing of

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM 3,000 herds to ascertain the infection status of the population. The results indicated that only 2 new infected herds were found, 35 infected herds were already known of because of direct slaughter traceback, and 23 other infected herds were known of for other reasons. Many of these herds had been in contact with the herds identified as infected by slaughter traceback. Thus slaughter traceback was almost 500 times more efficient than routine testing of dairy herds (Scott-Orr, 1985). In the United States, between 1982 and 1991, a total of 123 tuberculous herds were found. Of these 118 (96 percent) were found directly, or indirectly, from slaughter tracebacks, only 5 were found by other means. Although no structured study has been performed, these data clearly substantiate the efficacy of this program. Epidemiological evidence has correctly promoted the shift in the target of tuberculosis surveillance from the individual herd to the slaughterhouse. Changes, however, in meat inspection techniques and the adoption of a Hazard Analysis and Critical Control Points (HACCP) System (National Research Council, 1985; 1987) will shift attention from individual carcass inspections to control of hazards (especially disease hazards) at the critical points in the packing plant. This system may decrease the time available for detection of granulomas and identification of animals for traceback purposes. To maintain the sensitivity of the program's major surveillance method, detection techniques to supplement visual inspection are needed. Species Included in the Program When the Cooperative State-Federal Bovine Tuberculosis Eradication Program was initiated in 1917, only cattle and dairy goats were included. The program was mandatory for cattle and voluntary for goats. In 1987 the program was expanded to include bison. As of 1993, 41 states and the U.S. Virgin Islands are accredited free of tuberculosis, meaning they have had no M. bovis confirmed in cattle or bison herds for at least 5 years, and the state programs meet or exceed all tuberculosis program standards. Nine states and Puerto Rico have achieved modified accredited-free status. Cattle Since 1983 and the outbreak of M. bovis infection in the El Paso milkshed, the majority of known infected cattle herds are dairy herds. In 1993 there were 12 herds infected with bovine tuberculosis. Nine were carried over from the previous year and three were newly detected in 1993. The newly detected herds consisted of two dairy herds in Texas and one herd in a game park in Oklahoma. Figure 3-2 shows the locations of the 12 infected herds (VanTiem and Essey, 1993). Approximately 15 of the 38 dairies in the El Paso milkshed area have been infected since 1985, and the epidemiology of the situation is complicated by the proximity to a heavily infected area in Mexico (U.S. Department of Agriculture, 1992). Currently, infected herds tend to be large; consequently they are more expensive to depopulate (see Figure 3-3). From 1984 to 1993, 108 tuberculosis-infected and exposed herds were discovered. Of these, 84 (78 percent) were depopulated leaving 24 herds not depopulated. In FY 1992 only 3 of 16 tuberculous herds were depopulated. All 3 were small herds with a combined total of 800 animals. Of the 12 infected herds reported during FY 1993, 3 were depopulated. Two of these 3 were Texas dairy herds that together totaled about 1,300 animals. In recent years the recrudescence rate for bovine tuberculosis has risen from 33 percent to 50 percent; for example, of 10

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM FIGURE 3-2 Bovine tuberculosis state status and location of 12 tuberculosis-infected herds during FY 1993. Source: USDA Bovine Tuberculosis Eradication Program. dairy herds under quarantine in 1991, 5 had previously been quarantined. This may be a function of the large herd sizes in the El Paso area. The depopulated herds contained only about 5 percent of the total number of cattle exposed to tuberculosis. From 1981 to 1991 reactors were removed from 24 herds, but the herds were not depopulated. Eleven of these formerly infected herds were again found to be infected 2 or more years after release from quarantine. Bison As mentioned previously, the eradication program was expanded to include bison in 1987. This action was a consequence of finding a tuberculous bull at slaughter in 1984. The investigation of this single case led to a total of 24 infected bison herds in 10 states (Essey, 1985; LaBranche, 1987).

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM FIGURE 3-3 Location of 13 tuberculosis (infected and exposed) Cervidae herds during FY 1993. Source: USDA Bovine Tuberculosis Eradication Program. Cervidae and Other Nondomestic Ungulates During the past decade in the United States there has been a significant emergence of commercial ranching enterprises involving captive elk and various species of deer. Data on the prevalence of tuberculosis in these species is not as complete as for cattle, as there are no federal requirements for reporting the disease in these species, and only some states mandate the disease as reportable. There is no organized surveillance program; available data have been established by passive surveillance. The earliest reports of M. bovis infections in nondomestic captive ungulates in the United States appeared in 1950 in aoudad sheep (Ammotragus lervia), in a reticulated giraffe in 1959, in white-tailed deer (Odocoileus virginianus) in 1962, and in axis deer (Cervus axus) in 1969 (Thoen and Himes, 1981; Beli, 1962). In 1974 M. bovis infection occurred in a herd of 130 sika deer (Cervus nippon) and fallow deer (Cervus dama) in a deer park in southern California (Kollias, 1978). In 1981 there was an outbreak of M. bovis infection in cervids in South Dakota, which, it is believed, was

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM transmitted from the cervids to bison (Stumpff, 1982). Exposed bison were subsequently traced to 24 states. Nevertheless, tuberculosis in nondomestic ungulates was not considered a serious threat to the U.S. livestock industry until recently (U.S. Department of Agriculture, Animal and Plant Health Inspection Service, 1992a). In the fall of 1990 Canada closed its border to importations of camelids and cervids from the United States (Thorne and Nettles, 1991; LaBranche, 1991). In 1991 M. bovis infection was found in a Montana elk herd suspected as the source of tuberculosis in an outbreak involving elk herds in Alberta, Canada. Exposed animals from this Alberta outbreak were traced to most of the 120 licensed game farms in Alberta. As part of the investigation, a red deer herd in Wisconsin was found to be infected after the death of an elk that had recently been added to the herd from New York. In 1989 bovine tuberculosis was confirmed in a small llama herd in Iowa that was managed under agricultural conditions (Zecha, 1990). Further episodes of M. bovis infection were discovered in captive fallow deer herds in Florida and Texas (Thorne and Nettles, 1991) and a captive elk herd in Colorado. This elk herd was linked, through animal movements, with an infected herd in Montana. Limited surveillance has not revealed infection in free-living native elk and deer living in proximity to the game farm animals (Miller et al., 1991). An epidemiological study of an outbreak of bovine tuberculosis in confined elk was made in 1982 (Stumpff, 1982); it was noted that M. bovis infection in elk was rare in the United States. Reports that existed were of occasional incidents involving elk maintained under zoo conditions. Tuberculous elk, however, were shown to be the source of a 1985 bovine tuberculosis outbreak in bison that resulted in 24 infected bison herds in 10 states. The first apparent case of elk transmitting tuberculosis to cattle was diagnosed in 1991 (Essey, 1991). Bovine tuberculosis in captive Cervidae became an important issue in 1991 (U.S. Department of Agriculture, Animal and Plant Health Inspection Service, 1992a). Investigation of captive deer and elk herds began after reports were received from Canadian officials that U.S. deer and elk herds may have been the sources of an outbreak of tuberculosis in Canada. Bovine tuberculosis has since been confirmed in a U.S. captive elk herd epidemiologically linked with the Canadian outbreak. Montana is the focal point of tuberculosis investigations of elk with four confirmed herds. Numerous movements of exposed deer and elk are being traced in Montana and several other states. Seven infected cervid herds were located in FY 1991, one each in Idaho, Colorado, Nebraska, Oklahoma, Texas, Wisconsin, and New York. Two additional herds were detected in New York in FY 1992. Since January 1, 1991, bovine tuberculosis has been confirmed in a total of 13 captive cervid herds located in eight states. Eight of the infected cervid herds have been depopulated or donated for research by the owners. In FY 1993 there were 13 captive cervid herds with M. bovis confirmed in one or more animals. Eleven of these herds were newly detected in 1993 and two were carried over from the previous year. These herds are located in 11 states, 7 of which are accredited free of bovine tuberculosis (Figure 3-3). More than one-half of these herds contain a number of animal species and are classified as exotic exhibits (see Figure 3-4). In 1993 a UMR for Cervidae was developed by APHIS in response to recommendations from the U.S. Animal Health Association. These rules provide for accredited cervid herds, official tuberculosis tests, and requirements for interstate movement.

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM FIGURE 3-4 Distribution of infected Cervidae herds during FY 1993. Source: USDA Bovine Tuberculosis Eradication Program. Zoo Animals Although tuberculosis exists in zoological collections, the prevalence of infection is not known. The disease is not officially reportable in species other than cattle and bison and there is no organized surveillance. There are vast differences among institutions referred to as zoos, ranging from members of the American Association of Zoological Parks and Aquariums (AAZPA) to nonaccredited zoos to private exotic animal collections. There is an equally wide range of internal, self-imposed health controls within these institutions. Most AAZPA zoos have health programs that include testing and monitoring for tuberculosis control. Free-Ranging Wildlife Infection in free-ranging native deer and elk has not been detected in the United States. However, detection is based primarily on passive surveillance, so uncertainty about the existence of infection in these free-ranging species persists. Fiscal Responsibility Fiscal responsibility for the Bovine Tuberculosis Eradication Program has been shared between both federal and state governments (U.S. Department of Agriculture, 1989; Code of Federal Regulations, 1992; U.S. Department of Agriculture, 1992a). A total of $255,189,560 in federal funds has been expended for the national program from its inception in 1917 through 1991. Program costs for the Cooperative State-Federal Bovine Tuberculosis Eradication Program for 1983-1991 are shown in Table 3-1 (U.S. Department of Agriculture, Animal and Plant Health Inspection Service,

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM TABLE 3-1 Expenditures of Cooperative State and Federal Bovine Tuberculosis Eradication Program, FY 1983 to 1991   Funding by Fiscal Year Constant Dollars (1967) FY Federal Nonfederal Federal Nonfederal 1983 3,705,608 9,136,416 1,254,013 3,091,850 1984 2,581,968 1,239,060 836,130 401,250 1985 9,496,273 11,678,070 2,966,658 3,648,257 1986 3,757,813 9,390,854 1,155,184 2,886,829 1987 3,068,564 8,212,634 908,666 2,431,932 1988 2,402,328 9,135,617 684,814 2,604,224 1989 3,963,190 8,159,971 1,074,618 2,212,573 1990 3,615,150 12,321,363 936,082 3,190,410 1991 3,755,150 9,587,673 926,969 2,366,742 1992c). The nonfederal contribution to this program, since 1955, exceeds $303,374,165. The combined state contribution for 1991 was $9,587,673 (U.S. Department of Agriculture, 1992a). The 1993 federal budget for bovine tuberculosis was $4,095,941; of that, $1,602,476 was earmarked for individual state disbursement (U.S. Department of Agriculture, 1992b). A single state, on average, contributes up to six times as much as the federal government will spend in that state. Hence there is a heavy reliance on an individual state's contribution to this program. NOTE: Nonfederal includes state funds and industry contributions. SOURCE: U.S. Department of Agriculture, Animal and Plant Health InspectionService, 1992c. The federal and many state governments pay indemnity for animals that are reactors to official tuberculosis tests (U.S. Department of Agriculture, 1989; Code of Federal Regulations, 1992) (Table 3-2). The federal government will pay $750 for any animal (program species only) that reacts to an official tuberculosis test (U.S. Department of Agriculture, 1989). They will also pay $450 for nonreactor animals (program species only) that reside in known infected herds and are removed as part of the control program. In fiscal year 1993 the federal budget for indemnity and depopulation of infected herds was $261,107 (U.S. Department of Agriculture, 1992b). State governments may also pay accredited veterinarians for tuberculosis tests that they perform. States may provide additional indemnity for reactors and exposed nonreactors. State indemnities range from no indemnity payments in some states to indemnity payments in a few states that exceed the amounts paid by the federal government. The owners of indemnified reactor cattle also receive the slaughter salvage value of the animals. However, in most cases the slaughter value for reactor cattle is negligible because of carcass cooking requirements. Carcasses of indemnified, exposed nonreactor cattle are allowed to enter the food chain and command the current market price. The domestic livestock industry also incurs a significant expense related to the testing of animals; the largest component is the loss of production related to the actual testing and retesting of

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM TABLE 3-2 U.S. Department of Agriculture Funding for Tuberculosis Indemnity, 1983 to 1992 Fiscal Year Allocated for Indemnity Obligated for Indemnity 1983 $475,000 $1,224,000 1984 1,209,000 830,000 1985 1,600,000 5,053,000 1986 1,350,000 1,299,000 1987 1,310,000 489,000 1988 1,202,000 739,000 1989 0 248,000 1990 174,500 1,134,000 1991 932,305 535,000 1992 761,107 423,000 animals for tuberculosis. The national herd size averages 80 animals (U.S. Department of Agriculture, 1992), and the producer costs associated with herd testing are shown in Table 3-3 (based on USDA/APHIS/VS estimates). It can be seen that an average producer has the potential to lose up to $476 in the testing process alone. Additional losses can be incurred if the value of reactor and exposed animals exceeds the federal and state indemnity figures. SOURCE: U.S. Department of Agriculture, Animal and Plant Health InspectionService, 1992b TABLE 3-3 Producer Costsa Associated with Herd Testing Time associated with herd testing - 2 days Average production staff and salary - 1 manager $15.00/hour 2 workers $5.00/hour Equipment use per day - $50.00 Average work day - 10 hours   -------- Total loss $300.00 Additional dairy production loss due to 5 percent decrease in milk production: (16,000 lbs/cow × 80 cattle)/305 lactation days/cow = 4,197 lbs/lactation day 4,197 lbs/lactation day × 5 percent loss = 210 lbs lost 210 lbs/lactation day × 7 days of loss = 1,470 lbs lost/week $12/cwt × 14.7 cwt = $176.40   aU.S. Department of Agriculture/Animal Plant and Health Inspection Service/Veterinary Services, 1993

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM In the proposed UMR for cervids, the cervid industry has suggested an industry-supported fund to indemnify cervid owners with herds infected with tuberculosis. This would be a significant step toward reducing the financial burden on owners and accelerating the eradication of the disease in cervids (VanTiem and Essey, 1993). Agency Responsibility, Interaction, and Training USDA/APHIS/VS is central in coordinating and disseminating information for the Cooperative State-Federal Bovine Tuberculosis Eradication Program. The benefits of a dedicated computer-based system for the collection, organization, and analysis of field data have been discussed (Meyer et al., 1988). VS has a representative in every state--an Area Veterinarian in Charge or an Area Veterinary Medical Officer. This allows for the quick dissemination of information between a variety of regulatory agencies and interest groups. There is also intradepartmental interaction within USDA. VS provides FSIS with informational materials related to tissue sample submission and includes FSIS personnel in their national training courses. The training of regulatory officials in the Cooperative State-Federal Tuberculosis Eradication Program is predominantly accomplished through official USDA training exercises. VS sponsors at least one training course per year that includes representatives of FSIS, state agencies, and foreign governments. At their training center in College Station, Texas, FSIS conducts continuous training in the disposition of carcasses thought to be tuberculous. Private-practice veterinarians and veterinary students are taught the proper methods for application of tuberculin tests during the veterinary accreditation process. Accredited veterinarians must be able to demonstrate their proficiency in the application of intradermal tuberculin tests and give written affirmation as to their willingness to apply this test in a manner prescribed by both federal and state authorities. CANADA Cattle imported from Canada essentially present no risk of introducing tuberculosis because of the progress that country has made in eradicating the disease. From 1983 to 1992 about 4.3 million cattle have been imported into the United States from Canada (Table 3-4). Rarely has tuberculosis been found in Canadian cattle after importation. Canada is on the verge of official eradication of M. bovis from its national herd. The development and requirements of Canada 's Bovine Tuberculosis Eradication Program parallel those of the U.S. program. For example, in 1923 the Canadian program became mandatory, requiring all cattle producers to participate in the program. Disease surveillance activities have been modified from whole-herd testing (1923 to 1978) to intensive surveillance for tuberculosis-like lesions in federally inspected slaughtering establishments--these plants process more than 95 percent of the more than 3 million cattle slaughtered annually in Canada. The target submission rate of suspect lesions to the laboratory has been established at one tuberculosis-like lesion per 2,000 adult slaughter cattle. Nationally the submission rate of almost one lesion per 1,000 cattle slaughtered, or 200 percent of the target, is being achieved.

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM TABLE 3-4 Number of Cattle Imported to the United States from Canada and Mexico, 1983 to 1993 Year Mexico Canada 1983 766,376 457,550 1984 438,521 348,982 1985 179,060 374,242 1986 606,289 289,628 1987 810,871 165,853 1988 946,002 363,884 1989 615,087 511,118 1990 1,062,507 603,576 1991 1,197,323 820,997 1992 856,117 a 1993 1,200,000   aData for 4 months only. SOURCE: U.S. Department of Agriculture, Animal Plant Health InspectionService, Veterinary Services, 1993. Changing patterns in the marketing of slaughter cattle are requiring Canada to increasingly rely on the United States for slaughter surveillance and traceback information. Slaughter surveillance and traceback in Canada also suffers from the same limitations of animal identification, particularly in feedlot cattle, as experienced in the United States. Disease elimination activities underwent a series of modifications in response to a lack of progress in decreasing the level of infection similar to that being experienced in the United States. Not much progress had been made during the decade preceding 1978, thus stimulating a major program review. As part of the review's recommendations, a policy of mandatory depopulation of all infected herds was phased in during 1978 to 1984. Since 1984 all infected cattle herds have been depopulated. The success of this approach has been reflected in a significant decrease in the number of infected herds. Disease elimination activities also involve the tracing and investigation of sales, sources of cattle, and other contacts; the testing of perimeter herds; premises decontamination, and a strategy to repopulate the premises. Area accreditation is used to evaluate the disease eradication activities in each province and then ascribe a health status to that area. As of March 1993, all provinces except Ontario and Quebec were classified as tuberculosis-free areas, indicating a satisfactory level of surveillance and no disease detected during the preceding 5 years. Ontario's free status has been suspended for 1 year pending satisfactory resolution of an outbreak, the first since 1984, involving one cattle herd that acquired the infection from infected cervids. Quebec is classified as a tuberculosis accredited area, indicating a satisfactory level of surveillance and less than 0.2 percent of its cattle herds infected. Having

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM depopulated its last infected cattle herd in 1989 and barring the identification of new infection, Quebec will attain free status in 1994. Nonbovine Species In Canada the decision to extend the bovine tuberculosis eradication program for cattle into secondary but potentially significant reservoirs on game farms and in zoos was first considered in 1982. Aimed at the detection and elimination of infection in the various captive ungulate species, the Captive Ungulate Program was developed from 1984 to 1988 and was implemented nationally in 1989. Disease surveillance in captive ungulates is carried out primarily through on-farm testing, supplemented by limited slaughter surveillance, and the investigation of suspect clinical cases and postmortem findings. The disease elimination procedures used on infected herds of captive ungulates are identical to those used in the cattle program. Indemnity Funding Market value compensation is paid to the owners of bovine species ordered destroyed during the course of disease detection and elimination activities. Maximum amounts for cattle, per head, are currently set at $1,000 (grade beef), $1,200 (grade dairy), $1,500 (purebred beef), and $1,800 (purebred dairy). Market-value compensation for nonbovine species is paid to the owners of all animals ordered destroyed, with maximum amounts currently legislated for elk only ($7,000 for females, $3,500 for males). Revisions to the compensation legislation, scheduled for implementation in April 1993, establish a series of compensation maximums for all species of animals. The highest category, which includes elk, set a maximum of $2,000. All compensation payments require that any carcass salvage value be deducted from the amount paid. In addition to its domestic programs aimed at the eradication of bovine tuberculosis, Canada has instituted various inspection, testing, and certification requirements for tuberculosis for imported animals with the objective of preventing incursions of infection. As Canada 's largest trading partner in animals, the progress of the U.S. tuberculosis program is of vital importance to the Canadian program and its policies. MEXICO For more than a decade disease control officials have been increasingly concerned about tuberculosis found at slaughter in steers imported from Mexico (Thompson, 1991). These steers are frequently pastured in the United States prior to being sent to feedlots for finish feeding. This practice provides ample opportunity for Mexican steers to commingle on pasture with U.S. breeding stock. Some feedlots custom raise dairy heifers in addition to feeding Mexican steers. Recently there have been documented cases of cattle imported from Mexico transmitting tuberculosis to U.S. cattle (Hosker, 1983; Thompson, 1989; Davidson-York, 1991).

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM From 1983 to 1992 about 7.5 million cattle were imported into the United States from Mexico (Table 3-4). Almost all of these were steers that required further feeding prior to slaughter. A record number, more than 1,200,000 cattle, were imported in 1993; (VanTiem and Essey, 1993). Approximately 68 percent of all tuberculosis cases detected by slaughter inspection of feedlot cattle between 1982 and 1991 were traced back to Mexico. In 1993, 84 percent (327 cases) of compatible case slaughter investigations determined to be of feedlot origin were from Mexico (VanTiem and Essey, 1993). This is a decrease from 1992 levels. Table 3-5 shows the number of tuberculous cases reported at slaughter from 1983 to 1993 that following investigation were determined to have originated in Mexico. Mexico's Bovine Tuberculosis Eradication Program started in 1971. The program began on a voluntary basis, although export beef stock were required to participate in the program. Unfortunately over the 20-year period since the inception of this program, the Ministry of Agriculture has emphasized and deemphasized the importance of this program, hampering any continuous effort to eradicate tuberculosis. In 1976 the program became mandatory in regions where there were milk producers. Some milksheds, such as Tizayuca and Hildalgo near Mexico City have reduced the disease prevalence to 0.5 percent since 1976. Since 1989, 1,200 licensed veterinarians have been accredited to participate in tuberculin testing of animals; 90 percent of the veterinarians are private practitioners. The use of private practitioners in federally regulated programs represents a radical change of policy by the Mexican government. There were 1,741,750 doses of tuberculin sold in 1992. Federally inspected slaughter establishments have full-time meat inspectors. Approximately TABLE 3-5 Slaughter Investigations of Bovine Tuberculosis, Compatible Cases, FY 1983 to 1993 FY Total Number Slaughter Investigations Total Number Closed Slaughter Investigations of Feedlot Origin Total Number Feedlot Slaughter Investigations Mexican Origin Persent Mexican Origin 1983 27 18 13 72 1984 82 71 44 62 1985 108 90 49 55 1986 40 34 24 70 1987 161 156 114 73 1988 266 258 191 74 1989 281 270 167 62 1990 135 80 53 66 1991 258 243 188 77 1992 535 523 436 83 1993 448 388 327 84

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM 750,000 head of cattle are slaughtered in this type of facility where a system of reporting of tuberculosis cases is being installed. It is hoped that in the next few years all of the slaughter will occur in this type of establishment; this will provide a better surveillance system than presently exists. SOURCE: U.S. Department of Agriculture, 1993; VanTiem and Essey,1993. Mexico officially announced implementation of a national Bovine Tuberculosis Eradication Program in 1993. As a part of this program, a national animal identification system was developed using a blue metal eartag that has a numerical code identifying the herd of origin. The program divides the country into the northern states that are in the eradication phase; this includes the states of Baja California, Southern Baja California, Chihuahua, Coahuila, Durango; Nuevo Leon, Sonora, and Tamaulipas. The central and southern states are in control phase including certification of free herds. In the north, the eradication phase includes official supervision of accredited veterinarians and detection and elimination of all positive reactors and suspects in 100 percent of beef and dairy herds, epidemiological trace of positive cases found at slaughter, and inter-and intrastate movement control. A state must go 5 years with no reported cases to be accredited free of tuberculosis. A joint United States-Mexico Tuberculosis Committee has been formed to support initiatives aimed at disease eradication in both countries. In support of Mexico's tuberculosis efforts, APHIS has sponsored training programs in the areas of postmortem inspection, laboratory procedures, and field testing. Slaughterhouse findings of tuberculosis in Mexican steers and related traceback information in the United States is shared with Mexican disease control officials. In addition, APHIS has provided the Mexican government with laboratory supplies and equipment for a regional tuberculosis laboratory. Mexico 's goal is to have a network of 110 laboratories, including 8 regional labs and 2 national reference labs. Epidemiologic investigations involving Mexican steers in the United States have shown that approximately 67 percent of the infected imports are of the Holstein breed. This information has prompted the Mexican government to temporarily ban the export of all Holstein cattle to the United States until they can act to minimize the presence of tuberculosis in such exported animals. Indemnity Funding Mexico's campaign to eradicate tuberculosis has never provided indemnity for producers. This is considered to be one of the major drawbacks of the program. The current campaign requires the producer to pay the testing veterinarian, pay for the tuberculin and the metal ear tag, and sacrifice the positive and suspect reactors. The present administration in Mexico recognizes that Mexico's animal health status is essential in maintaining good standing with partners belonging to the North American Free Trade Agreement. OTHER COUNTRIES Bovine tuberculosis is a global problem. Countries that have official tuberculosis control programs are listed in Table 3-6; twenty-eight countries report being free of bovine tuberculosis in cattle (Food and Agriculture Organization, International Office of Epizootics-World Health Organization, 1991). The countries listed include independent nations, internally independent political entities that are under the protection of other countries, and other independent political units and major administrative subdivisions. With the further development of international free trade agreements, a country's livestock disease status will be an increasingly important economic factor in export considerations.

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LIVESTOCK DISEASE ERADICATION: EVALUATION OF THE COOPERATIVE STATE–FEDERAL BOVINE TUBERCULOSIS ERADICATION PROGRAM TABLE 3-6 Countries with Tuberculosis Programs Albania Greece Papua New Guinea Algeria Grenada Paraguay Angola Honduras Peru Antigua and Barbuda Hungary Philippines Argentina India Poland Australia Iran Portugal Austria Iraq Reunion Bangladesh Ireland Romania Barbados Israel Russian Federation Belize Italy Seychelles Bhutan Jamaica Solomon Islands Bolivia Korean Republic South Africa Botswana Kuwait Spain British Virgin Islands Lesotho St. Kitts and Nevis Bulgaria Libya St. Lucia Cameroon Lithuania St. Vincent Canada Luxembourg Swaziland Chile Macau Sweden Colombia Malaysia Switzerland Costa Rica Malta Syria Cuba Mauritius Thailand Cyprus Mexico Tonga Czechoslovakia Mongolia Tunisia Denmark Morocco Turkey Djibouti Mozambique United Kingdom Dominican Republic Myanmar United States Egypt Namibia Uruguay El Salvador Nepal Vanuatu Falkland Netherlands Viet Nam Fiji New Caledonia Yugoslavia Finland New Zealand Zaire France Nicaragua Zambia French Polynesia Nigeria Zimbabwe SOURCE: Food and Agriculture Organization, International Office ofEpizootics-World Health Organization, 1991.