Thursday, June 8, 2017

Revisiting Brucellosis in the Greater Yellowstone

Recently a committee of the National Academy of Sciences issued its report, Revisiting Brucellosis in the Greater Yellowstone Area as an update to the 1998 report by the National Research Council. The report examined the changing dynamic of brucellosis in the Greater Yellowstone Area (GYA) and explored various options for addressing the challenge of brucellosis disease management.  

Figure 1. Elk and Bison graze Yellowstone National Park. Photo © by Timothy Pearce, Creative Commons

The Disease
Brucellosis is a contagious disease of ruminant animals that also affects humans. Although brucellosis can attack other animals, its main threat is to cattle, bison, cervids (elk and deer), and swine. The disease is also known as contagious abortion or Bang's disease. In humans, it's known as undulant fever because of the severe intermittent fever accompanying human infection or Malta fever because it was first recognized as a human disease on the island of Malta. As a result of efforts begun more than 80 years ago in the United States, however, the incidence of brucellosis in humans is now less than 0.5 cases/million population, as compared with over 6,000 cases annually in 1947. The disease was first noted in the GYA in 1917, and has been present since.

In cattle, the primary cause of brucellosis is Brucella abortus, a zoonotic bacterial pathogen that also affects wildlife, including bison and elk. Bovine brucellosis posed significant animal health and international trade consequences. In livestock it is known to cause decreased milk production, weight loss, loss of young, infertility and lameness. The generally accepted path of transmission is direct contact with infected animals or with an environment that has been contaminated with discharges from infected animals -- aborted fetuses, placental membranes or fluids, and other vaginal discharges present after an infected animal has aborted or calved (USDA).

Brucellosis in the GYA
The only remaining reservoir of B. abortus infection in the United States is in the GYA, where brucellosis is endemic in bison and elk, and where wildlife transmitted cases spill over into domestic cattle and domestic bison. This spill-over is now occurring with increasing frequency, raising the possibility of brucellosis reoccurrence outside the GYA.

From 1998-2016, 22 cattle herds and five privately-owned bison herds were affected in Idaho, Montana, and Wyoming. During the same period, all other states achieved and maintained brucellosis-free status. A 2010 interim rule enabled the three GYA states to create designated surveillance areas (DSAs) to monitor brucellosis in specific zones and to reduce the economic impact for producers in non-affected areas. However, brucellosis has expanded beyond the original DSAs, resulting in the outward adjustment of DSA boundaries. Most cattle in the GYA are vaccinated with B. abortus strain RB51 which reduces abortions but does not necessarily prevent infection. The increase in cattle infections in the GYA, coupled with the spread in wildlife is a cause of alarm for area producers; moreover, the risk of additional spread to other areas across the United States is increasing due to the lack of guidance and surveillance.

Report Findings
The report’s primary finding is the clear evidence that elk are a primary host for brucellosis and the major transmitter of B. abortus to cattle. All recent cases of brucellosis in GYA cattle are traceable from elk, not bison.[1] This conclusion, long-suspected by ranchers and others in the Paradise Valley, poses greater challenges for control of transmission from wildlife to domestic species.

Ecological changes with the GYA since 1998, including the reintroduction of the gray wolf and increases in grizzly bear numbers, have affected the density and distribution of elk. Elk populations have expanded on the periphery of the GYA but have decreased inside Yellowstone National Park.

The panel observed that reducing the population size of cattle, bison, or elk are all likely to reduce the risk of brucellosis transmission to cattle by reducing the area of potential contact or the number of infected individuals in those areas, even if the disease prevalence in the wildlife hosts remains constant. However, each species has a constituency that would likely oppose any population reduction.

The report’s conclusions:

1.       Brucellosis control efforts in the GYA need to sharply focus on approaches that reduce transmission from elk to cattle and domestic bison.

2.       No single management approach can independently result in reducing risk to a level that will prevent transmission of B. abortus among wildlife and domestic species.

3.       Reducing the elk population is an option for reducing the risk of transmission among elk, cattle, and bison. Unlike bison, transmission among elk appears to be influenced by density. Thus, reducing elk group sizes and/or density may decrease elk seroprevalence over time, and potentially decrease the risk of elk transmission.

4.       While the primary focus would be on elk, bison remain an important reservoir for brucellosis. For this reason, if reduction of brucellosis prevalence is a goal, removal of bison for population management purposes will need to target brucellosis infected individuals, whenever possible.

5.       The weight of evidence nonetheless suggests that reduced use or incremental closure of feedgrounds could benefit elk health in the long-term, and could reduce the overall prevalence of brucellosis in elk on a broad population basis.  This is not a stand-alone solution to control of brucellosis in the GYA, and will need to be coupled with other management actions to address the problem at a systems level.

6.       The lack of data-based guidance and uniformity in conducting wildlife surveillance outside the DSA, the absence of a GYA focused approach for national surveillance, and the infrequent oversight of state brucellosis management plans in the midst of expanding seroprevalence of elk has increased the risk for spread of brucellosis in cattle and domestic bison outside the DSA boundaries and beyond the GYA.

7.       The significant reduction in risk of transmission among vaccinated cattle provides sufficient reason to continue calf-hood and adult vaccination of high-risk cattle when coupled with other risk reduction approaches.

8.       A coupled systems/bioeconomic framework is vital for evaluating the socioeconomic costs and benefits of reducing brucellosis in the GYA, and would be needed to weigh the potential costs and benefits of particular management actions within an adaptive management setting. A bioeconomic framework is also needed to identify appropriate management actions to target spatial-temporal risks, including risks beyond the GYA.

9.       Managing an ecosystem as complex as the Greater Yellowstone Ecosystem will require coordination and cooperation from multiple stakeholders, and will require expertise across many disciplines to understand the intended and unintended costs and benefits of actions.

10.   A strategic plan is needed to coordinate future efforts, fill in critical knowledge and information gaps, and determine the most appropriate management actions under a decision-making frame-work that is flexible and accounts for risks and costs. 

11.   Coordinated efforts across federal, state, and tribal jurisdictions are needed, recognizing firstly that B. abortus in wildlife spreads without regard to political boundaries, and secondly that the current spread of brucellosis will have serious future implications if it moves outside of the GYA.

Report Recommendations
1.       Federal and state agencies should prioritize efforts on preventing B. abortus transmission by elk. Modelling should be sued to characterize and quantify the risk of disease transmission and spread from and among elk which requires an understanding of the spatial and temporal processes involved in the epidemiology of the disease and economic impacts across the GYA. Models should include modern, statistically rigorous estimates of uncertainty. 

2.       In making timely and data-based decisions for reducing the risk of B. abortus transmission from elk, federal and state agencies should use an active adaptive management approach that would include iterative hypothesis testing and mandated periodic scientific assessments. Management actions should include multiple, complementary strategies over a long period of time, and should set goals demonstrating incremental progress toward reducing the risk of transmission from and among elk. 

3.       Use of supplemental feedgrounds should be gradually reduced. A strategic, stepwise, and science-based approach should be undertaken by state and federal land managers to ensure that robust experimental and control data are generated to analyze and evaluate the impacts of feedground reductions and incremental closure on elk health and populations, risk of transmission to cattle, and brucellosis prevalence. 

4.       Agencies involved in implementing the Interagency Bison Management Plan should continue to maintain a separation of bison from cattle when bison are outside YNP boundaries.

5.       In response to an increased risk of brucellosis transmission and spread beyond the GYA, USDA-APHIS should take the following measures:
a.       Work with appropriate wildlife agencies to establish an elk wildlife surveillance program that uses a modeling framework to optimize sampling effort and incorporates multiple sources of uncertainty in observation and biological processes. 
b.       Establish uniform, risk-based standards for expanding the DSA boundaries in response to finding seropositive wildlife. The use of multiple concentric DSA zones with, for example, different surveillance, herd management, biosecurity, testing, and/or movement requirements should be considered based on differing levels of risk, similar to current disease outbreak response approaches. 
c.        Revise the national brucellosis surveillance plan to include and focus on slaughter and market surveillance streams for cattle in and around the GYA. 

6.       All federal, state, and tribal agencies with jurisdiction in wildlife management and in cattle and domestic bison disease control should work in a coordinated, transparent manner to address brucellosis in multiple areas and across multiple jurisdictions. Effectiveness is dependent on political will, a respected leader who can guide the process with goals, timelines, measured outcomes, and a sufficient budget for quantifiable success. Therefore, participation of leadership at the highest federal (Secretary) and state (Governor) levels for initiating and coordinating agency and stakeholder discussions and actions, and in sharing information is critical. 

7.       The research community should address the knowledge and data gaps that impede progress in managing or reducing risk of B. abortus transmission to cattle and domes-tic bison from wildlife. 
a.       Top priority should be placed on research to better understand brucellosis disease ecology and epidemiology in elk and bison, as such information would be vital in informing management decisions. 
b.       To inform elk management decisions, high priority should be given to studies that would provide a better understanding of economic risks and benefits.
c.        Studies and assessments should be conducted to better understand the drivers of land use change and their effects on B. abortus transmission risk. 
d.       Priority should be given to developing assays for more accurate detection of B. abortus infected elk, optimally in a format capable of being performed “pen-side” to provide reliable rapid results in the field.
e.       Research should be conducted to better understand the infection biology of B. abortus.
f.         To aid in the development of an efficacious vaccine for elk, studies should be conducted to understand elk functional genomics regulating immunity to B. abortus.
g.       The research community should (1) develop an improved brucellosis vaccine for cattle and bison to protect against infection as well as abortion, and (2) develop a vaccine and vaccine delivery system for elk.

References
National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting  Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: https://doi.org/10.17226/24750.

USDA APHIS. Facts about Brucellosis. https://www.aphis.usda.gov/animal_health/animal.../brucellosis/.../bruc-facts.pdf



[1] There have been no cases of transmission from GYA bison to cattle in the 27 herds infected with brucellosis since 1998.

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