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EXECUTIVE SUMMARY In the winter of 1996-1997, the Yellowstone National Park (YNP) bison (Bison bison) population was more than 3,400 animals. Harsh weather that winter forced record numbers of bison to leave the park in search of forage; other animals in the park starved. National attention focused on management strategies—including shooting bison—used to prevent the possible spread of brucellosis from park bison to cattle that are grazed on land adjacent to the park. Brucellosis in the Greater Yellowstone Area (GYA) is a disease caused by Brucella abortus, a bacterial organism transmitted primarily by contact with products of birth or abortion or by milk. B. abortus probably is not native to North America but was introduced with European cattle and then transmitted to wildlife; it was first detected in YNP bison in 1917 and has been present ever since. Brucellosis can be transmitted from one species to another, and concern has been expressed for many years over the potential for wildlife in the GYA to spread brucellosis to cattle that graze on land in or adjacent to the GYA and for cattle then to transmit the disease to other species, including humans. In response to public discussion of whether brucellosis transmission by bison or elk (Cervus elaphus) is a threat to domestic livestock and whether vaccination or other management strategies might prove useful in controlling potential transmission, Secretary of the Interior Bruce Babbitt asked the National Academy of Sciences to undertake a 6-month study of brucellosis in the GYA. The Board on Agriculture and the Board on Environmental Studies and Toxicology began the study in May 1997 to look specifically at the following issues:
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The extent of bison infection with brucellosis in the Greater Yellowstone Area and the potential of developing a vaccine program. The transmission of B. abortus among cattle, bison, elk, and other wildlife species. The relationship, if any, between bison population dynamics and brucellosis. The ability of serology testing to estimate true infectiousness. The efficacy and safety of existing vaccines for target and nontarget species and the need for new (including bison-specific) vaccines. The nature and likely successes or limitations of a wild animal vaccination program. Key factors in reducing risk of transmission from wildlife to cattle and among cattle. Some claim that the possibility that bison or other wildlife transmit brucellosis to cattle is remote and that no management strategies are needed. Others claim that any risk of transmission is unacceptable for public health and economic reasons, and brucellosis must be eradicated from the wild. This study assesses the current state of knowledge about brucellosis infection and transmission, makes recommendations for further research, and examines the implications of various management options. CHARACTERIZATION OF BRUCELLOSIS INFECTION Brucellosis can be transmitted among species; in humans, it is usually characterized by a fluctuating body temperature. Although rarely fatal, human brucellosis is recurrent and debilitating. The success of treating individuals varies widely, and lifelong infection is not unusual. Human brucellosis is not a widespread health threat today in North America because of efforts to eradicate brucellosis in cattle and the use of sanitary procedures (such as pasteurization) in milk processing; human infection that does occur today generally is among people who handle infected tissues, such as veterinary workers and hunters. The hallmark sign of brucellosis in cattle, bison, and elk is abortion or birth of nonviable calves. Because of its potential to be transmitted to humans, brucellosis is one of the most regulated diseases of cattle in the United States. Cattle shipped interstate are tested routinely only for brucellosis and tuberculosis, although other diseases cause markedly more morbidity and mortality. The U.S. Department of Agriculture (USDA) established the national brucellosis eradication
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effort in 1934 to address public health concerns and the economic consequences to the cattle industry resulting from infected herds; that effort implemented the standards for testing, quarantine, and elimination that remain in place today. Since 1934, an estimated $3.5 billion in federal, state, and private funds has been spent on brucellosis eradication in domestic livestock. The present National Brucellosis Program is run by the USDA Animal and Plant Health Inspection Service (APHIS), which has a goal of eradicating brucellosis from U.S. cattle and captive bison herds by 1998. Only 12 cattle herds were infected at the time of this report. As part of its efforts to eradicate brucellosis, APHIS certifies states as brucellosis-free, class A, class B, or class C, depending on the rate of infection in all cattle herds in a state. No states carry class B or C status today—an indication of the success of eradication strategies. A state's classification is important because if B. abortus is detected, numerous costs are incurred, such as those related to testing procedures, but perhaps the most important costs are those associated with the refusal of other states to accept a state's cattle because of the perception that B. abortus might be present. Many states prohibit importation of unvaccinated breeding cattle. By authorizing USDA to regulate brucellosis transmission in cattle, the federal government has demonstrated concern that although a low risk, brucellosis poses a potentially great-loss situation in terms of potential economic consequences and possible human health effects. This report was written with that federal recognition in mind. DETECTION OF BRUCELLOSIS When present, B. abortus usually is found in the organs and tissues of the reproductive system and mammary gland, associated lymph nodes, and lymph nodes of the head and neck. Bison with non-reproductive-tract infection generally do not pose a risk of transmission to elk or cattle, although there are exceptions. But it is unlikely that large numbers of animals in a herd would be infected in lymphoid tissues without also being infected in the reproductive system or mammary gland. The two most likely events during which transmission could occur are abortion or birth. Animals are tested for brucellosis using serologic tests (blood tests to detect that antibodies are present as a result of an infection) and bacterial cultures (where bacteria from tissue samples are grown under laboratory conditions). Both methods have flaws. A serologic result can be a good indicator of infection, but because it detects antibodies, not living bacteria,
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it is indirect evidence of infection or vaccination. Thus, a seropositive animal might not be infectious. Some 30-40% of bison in YNP have positive blood tests for antibodies (are ''seropositive") for B. abortus; in the Jackson bison herd, 77% of the animals sampled are seropositive. About 1-2% of elk that do not frequent winter feeding grounds are seropositive, but in some feeding grounds, the rate is much higher—about 37%—because dense concentrations of elk create conditions favorable to disease transmission. An animal might be infected but test seronegative in several situations, such as when antibodies have not yet developed because the test is taken in early stages of disease incubation, when a test is not sensitive enough to detect low levels of antibodies, or when the test itself is defective. False-positive tests also occur. Finding: Seronegative results do not necessarily establish the absence of infection, because some seronegative animals in chronically infected herds are carrying live B. abortus. Bacterial culture is the definitive test of infection, but in chronic infections, such as those present in the YNP bison herd, few bacteria might be present in an animal. That makes accurate culture difficult—obtaining the correct tissue and the correct sample size can be problematic. Therefore, although bacterial culture does not yield false-positive results, it does give false-negative results. Although high serologic responses correlate well with bacterial cultures in bison, the relationship between serologic tests and bacterial culture is difficult to ascertain, because quantitative assessments to examine the relationships have not been done. A substantial part of the differences in GYA bison between the high percent of seropositivity and the much lower percent of positive bacterial results most likely is due to culture or sampling techniques. Multiple serologic tests and bacterial cultures on the same animals over time are the most reliable method to determine infection in live animals. Recommendation: Because of testing insufficiencies, seropositive bison should be assumed for management purposes to be carrying live B. abortus. RISK OF TRANSMISSION Much of what we know about brucellosis in the GYA has been extrapolated
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from research conducted on cattle. Almost no controlled research has been done concerning transmission between wildlife species and cattle. YNP and Grand Teton National Park (GTNP) bison populations are chronically infected with B. abortus, as are elk populations, but the true prevalence of brucellosis in GYA bison and elk is unknown. The risk of transmission is determined by the number of abortions that occur, the presence and survival of B. abortus in aborted tissues, and the exposure of a susceptible host. The number of abortions or fetal deaths in bison since brucellosis first was detected in the GYA in 1917 is unknown, but in the past decade, two cases have been documented. Cattle, bison, and elk are susceptible to the same strain of B. abortus, and transmission between species has been demonstrated experimentally. Epidemiologic evidence, particularly that from GTNP and the National Elk Refuge (NER) points to transmission between free-roaming bison and elk and cattle as well. Finding: The risk of bison or elk transmitting brucellosis to cattle is small, but it is not zero. Transmission of B. abortus from elk to cattle is unlikely in a natural setting, because elk usually avoid areas used by cattle and isolate themselves for birth, but elk are capable of transmitting the bacteria to cattle. If cattle in the GYA mingled with aborting elk on the feeding grounds (which are maintained to promote herd growth for recreational hunting, to keep elk from straying where cattle are present, and to prevent damage to private hay crops) they would be at high risk for infection because of the high abortion rate among feeding-ground elk and the high concentration of animals. Elk also can transmit the bacteria to bison, and this might have occurred in the GYA. Under present conditions, even if low infection rates were attained for bison, an elk-to-bison or bison-to-elk transmission eventually would occur. Many more elk than bison are present in the GYA. Finding: If infection rates are not substantially reduced in elk, reinfection of bison is inevitable. Finding: B. abortus is unlikely to be maintained in elk if the elk winter-feeding grounds were closed. There is no risk of B. abortus transmission to cattle from bison if bison do not leave YNP. Strategies such as discontinuing road grooming (packing snow on park roads, which some believe provides an energy-efficient travel route
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for bison) have been suggested to relieve the need for artificial control outside the park. But an expanding bison population searching for forage is the fundamental force pushing bison out of YNP, and the bison population will continue to increase over several years until a high population combined with a harsh winter reduces the population again. (In contrast, northernherd elk are fluctuating about a dynamic equilibrium in response to the local food-resource carrying capacity, as well as winter stress conditions.) Finding: Brucellosis is not a major factor in herd survival for elk or bison; among natural variables, winter mortality is the most important. Finding: Bison leave YNP as a result of an increasing population and harsh winter weather, and under current management practices within the boundaries of YNP, the bison population will continue to grow. Other species in the GYA, such as coyotes, grizzly bears, and wolves, can be infected by B. abortus. The transfer of infection among elk, bison, and cattle by those species is rare, although it cannot be ruled out completely. Carnivores and predators might contribute to transmission by transporting infectious materials from one site to another, but this probably is outweighed by the fact that carnivores and predators typically sanitize a site, thereby reducing the chance of transmission. REDUCING THE RISK OF TRANSMISSION Although the risk of B. abortus transmission is low, it can be reduced further with a combination of management options. The options for dealing with brucellosis range from doing nothing to attempting eradication of the disease. If nothing is done, bison and elk will be infected at the balance between the rate of transmission within and among species and the frequency of natural (that is, genetic) resistance to B. abortus. If a program to control brucellosis were undertaken, a variety of approaches could be exercised, some of which could be undertaken at the same time. The approaches taken would depend on short- and long-term goals. Several approaches to control and eventual eradication of brucellosis are available, including vaccination, establishment of perimeter zones, spatial and temporal separation of cattle and bison, and vaccination with herd
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management (which might include testing and eliminating infected animals). Those approaches could be used individually or combined, depending on the degree of control determined to be in the best national interest. Other possibilities for control might arise, particularly as vaccine development progresses. A program to eradicate brucellosis entirely would need to include an extensive vaccination effort, as well as a test-and-slaughter component with simultaneous elimination of all infected bison, elk, and cattle. If brucellosis were eradicated from those species, the reservoirs of B. abortus in other wild species are expected to disappear on their own. Total eradication of brucellosis as a goal is more a statement of principle than a workable program at present; neither sufficient information nor technical capability is available to implement a brucellosis-eradication program in the GYA. No good vaccine or vaccine delivery mechanism is available at present—it would be impossible to vaccinate all GYA elk, and attempts to vaccinate bison (for example, by rounding them up) likely would be very intrusive. Some measures can be taken immediately that would provide a good first step in reducing the risk of transmission from wildlife to cattle, regardless of final goals. The concept of surveillance zones might well be applicable to risk control for brucellosis in the entire GYA. This report emphasizes bison in YNP because of the importance of that problem in recent years when bison movements in hard winters forced a response by management agencies. Recommendation: USDA and DOI should develop a plan to maintain a series of YNP perimeter zones with progressively increasing disease surveillance, vigorous monitoring, vaccination, and contact-reporting programs as one nears the park. The boundaries of the zones and management needed to maintain the zones should be determined jointly by USDA, DOI, and the states surrounding YNP. The plan should remain in place until brucellosis is eliminated from YNP. It is important that a team of scientists be involved in this program and that results be analyzed and published in a refereed scientific journal. Vaccination is an essential component of any program to control or eradicate brucellosis. Two vaccines—Strain 19 (S19) and Strain RB51—are used in cattle to protect against B. abortus infection. The vaccines do not produce complete protection in cattle, and the data available suggest that is also true for bison and elk. However, appropriate efficacy (the ability of a vaccine to produce desired effects) and safety tests have not been conducted for bison
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or elk; doses for commercial bison herds follow recommended doses for cattle. There are many unknowns besides correct ranges of dose for bison and elk, including appropriate routes, duration of immunity, and age and sex differences. Recommendation: A long-term, controlled vaccination study must be conducted to assess the complete role of vaccination in brucellosis control and eradication for bison and elk. An effective vaccination program would aid in reaching short-term disease control measures. Any program with a vaccination component would need to account for the large numbers of elk in the GYA, the high seropositivity rates in feeding-ground elk, and the potential for reinfection of bison by elk. Recommendation: Any vaccination program for bison must be accompanied by a concomitant program for elk. Recommendation: If the current vaccination program in elk feeding grounds is continued, it should include collection of serologic and culture data and appropriate epidemiologic analysis. A coordinated, phased plan could be developed for research on the vaccination of bison, with phases that begin in sequence but could occur simultaneously. Such a plan might include collection and analyses of data from commercial bison herd vaccination programs that are under way, expansion of current experimental research on characterization of candidate vaccines in bison, and development of a field vaccination study of bison that are inside the GYA, but outside YNP. The steps beyond a vaccination program are unclear. Whether a test-and-slaughter program is needed will depend on whether eradication is a feasible and desirable end point; further research on transmission and efficacious vaccines will be needed. The outcome of maintaining perimeter zones also will be important in determining whether eradication of brucellosis in the GYA is desirable. An adaptive management approach that had research designed to provide data to reduce areas of current uncertainty should eventually give a more realistic assessment of the feasibility of eradication of B. abortus in the GYA. In adaptive management, management and research are combined so that projects are specifically designed to reveal causal relationships between interventions and outcomes, that is, to maximize learning.
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Recommendation: A brucellosis program for wildlife in the GYA should be approached in an adaptive management framework. It might prove impossible for various reasons to eliminate brucellosis from bison and elk in the GYA, so the best that could be achieved would be risk control. Bison might continue to require artificial control (such as shooting bison that leave the park), either at current or redrawn lines. Nevertheless, a cooperative arrangement to pursue systematically a pragmatic program is the best route to the highest result that can be achieved. Recommendation: Clear short-term strategies to arrive at long-term goals must be defined and agreed upon by the federal and state entities that are involved in GYA management. Current research and funding cannot be relied upon to sustain any long-term program effectively. As is evident from the science reviewed for this report, studies have been characterized by stop-and-go funding and elusive goals. Sample sizes have been inadequate and studies have been of insufficient duration. Recommendation: Research priorities with sufficient funding need to be determined cooperatively and with the support of the secretaries of the U.S. Department of the Interior and U.S. Department of Agriculture. If public opinion and political directions are aligned to a common goal, and if long-term commitments can be made by the federal departments and agencies involved, it is likely that brucellosis can be eliminated from YNP without loss of large numbers of bison or loss of genetic diversity. To be successful, society and government must support, over the long term, studies that define the ecology of the GYA, develop new vaccine technologies and delivery mechanisms for bison and elk, and produce diagnostic reagents with greater sensitivity and specificity. Other factors will affect efforts to control or eradicate brucellosis in the GYA. They are as varied as weather, environmental change, and funding for research and management in our parks. As an added variable, future shifts in public opinion could determine the fate of any eradication effort—opinion not only on how we view bison and elk, but on the acceptability of having brucellosis in the park.
Representative terms from entire chapter: