Date Published: June 13, 2017
Publisher: Public Library of Science
Author(s): Angela Brennan, Paul C. Cross, Katie Portacci, Brandon M. Scurlock, William H. Edwards, Emmanuel Serrano Ferron.
Tracking and preventing the spillover of disease from wildlife to livestock can be difficult when rare outbreaks occur across large landscapes. In these cases, broad scale ecological studies could help identify risk factors and patterns of risk to inform management and reduce incidence of disease. Between 2002 and 2014, 21 livestock herds in the Greater Yellowstone Area (GYA) were affected by brucellosis, a bacterial disease caused by Brucella abortus, while no affected herds were detected between 1990 and 2001. Using a Bayesian analysis, we examined several ecological covariates that may be associated with affected livestock herds across the region. We showed that livestock risk has been increasing over time and expanding outward from the historical nexus of brucellosis in wild elk on Wyoming’s feeding grounds where elk are supplementally fed during the winter. Although elk were the presumed source of cattle infections, occurrences of affected livestock herds were only weakly associated with the density of seropositive elk across the GYA. However, the shift in livestock risk did coincide with recent increases in brucellosis seroprevalence in unfed elk populations. As increasing brucellosis in unfed elk likely stemmed from high levels of the disease in fed elk, disease-related costs of feeding elk have probably been incurred across the entire GYA, rather than solely around the feeding grounds. Our results suggest that focused disease mitigation in areas where seroprevalence in unfed elk is high could reduce the spillover of brucellosis to livestock. We also highlight the need to better understand the epidemiology of spillover events with detailed histories of disease testing, calving, and movement of infected livestock. Finally, we recommend using case-control studies to investigate local factors important to livestock risk.
Brucellosis is an important zoonotic disease of livestock and wildlife that affects more than 500,000 people annually across the globe [1,2]. Though incidence of brucellosis in humans has dramatically declined where the disease has been reduced or eliminated from livestock [1,2], disease control can be cost prohibitive and complicated by disease re-emergence in countries where unregulated animal movement occurs across borders [1–3]. Spillover infections from wildlife reservoirs can also fuel local outbreaks in livestock, ultimately limiting the success of eradication programs. In the United States, for example, an expensive eradication program reduced prevalence of brucellosis in adult cattle from 11.5% in 1934 to a national herd prevalence of 0.0001% in 2007 , but complete eradication was not possible due to periodic and recently increasing  spillover from wild elk of the Greater Yellowstone Area (GYA; see [5–7] regarding evidence of elk to cattle transmission). This has forced the livestock industry to impose interstate trade restrictions and costly testing requirements  to identify infected livestock and reduce the potential for additional outbreaks as GYA livestock are moved to outside markets and grazing areas. Thus, it has become increasingly important to better understand risk to GYA livestock in an effort to refine mitigation efforts and reduce spillover from elk.
We examined occurrences of brucellosis-affected livestock herds (including cattle and domestic bison) during 1990–2014 within the region referred to as the Designated Surveillance Area (DSA), where additional livestock testing and mitigation occurs because of brucellosis spillover risk to livestock . Montana, Idaho and Wyoming each independently design and implement a Designated Surveillance Area (DSA) that is approved by the United States Department of Agriculture (USDA). These DSAs, which we refer to collectively as the DSA, encompass the GYA and most surrounding areas where brucellosis exposure has been detected in wild elk (Fig 1). We obtained epidemiologic reports for each brucellosis-affected cattle or domestic bison herd from the USDA-Animal and Plant Health Inspection Service (USDA-APHIS) to identify the probable spillover season and the detection method that was used to identify infected livestock (see Table A in S1 Appendix for a description of detection methods). Spillover seasons were described as winter (February–March), spring (April–May), or summer (June), but often specific months were not reported.
There were 21 brucellosis-affected livestock herds between 2002 and 2014, nine of which occurred in Montana, seven in Wyoming, and five in Idaho (Fig 1). Only four of the affected livestock herds occurred in elk hunt districts (HDs) with operating feeding grounds (three in Wyoming and one in Idaho). Two additional affected livestock herds occurred in the Idaho feed ground-HD in years after the feeding ground closed (Fig 1). No brucellosis positive livestock were detected between 1990 and 2001. Affected livestock herd sizes ranged from roughly 30 to 2300 and within herd brucellosis seroprevalence ranged from less than 0.01 to 0.22. Descriptions of elk-livestock comingling, testing history, calving history, and time spent in the DSA for each affected livestock herd’s initial B. abortus-positive animal helped to narrow identification of a spillover season for only 11 of the affected herds (Table B in S1 Appendix). Four of the affected livestock herds were probably infected in winter, because elk were being fed during this time in close proximity to the affected livestock or because elk were seen comingling with the affected livestock during winter. Two of the affected livestock herds were probably infected in the spring, because elk were seen on spring grazing property or in close proximity to the affected livestock during the spring months. One affected livestock herd was probably infected in the summer, because the initial affected animal was moved from outside the DSA to summer grazing inside the DSA only months before testing positive. Four of the affected livestock herds were probably affected sometime during spring or summer, based on descriptions of movement from outside the DSA to spring/summer grazing inside the DSA, successful calving in early spring (before testing positive in the late fall), or previous negative test history. The remaining 10 affected livestock herds lacked any information to identify a spillover season. We also found that all detection methods detected similar numbers of affected livestock herds (each method detected 3–5 affected herds; Table B in S1 Appendix).
Occurrences of brucellosis-affected livestock herds within the DSA have been relatively rare, but on the rise since the early 2000’s. The vast majority of these affected livestock herds (17 of 21) occurred in elk hunt districts (HDs) without operating elk feeding grounds (Fig 1), where brucellosis seroprevalence in elk has been increasing (Fig 2). In these HDs, the mean probability of having an affected livestock herd was estimated to increase from roughly 0.01 to 0.08 with an increase in elk seroprevalence from 0.20 to 0.35 (Fig 4). These probabilities should be interpreted with caution, however, given there were only 21 occurrences of affected livestock herds and estimated parameter uncertainty was high. Focusing instead on the broad patterns, our results suggest that spillover from elk to livestock could occur more often in areas with increasing seroprevalence in unfed elk, but that occurrences of brucellosis-affected livestock are still likely to be rare overall. In contrast to unfed elk, fed elk seroprevalence was not important to occurrences of affected livestock herds (Fig 4), probably because fed elk have had consistently higher levels of exposure to B. abortus and there were only four affected livestock herds in feed ground HDs across the study period. Feeding grounds help to control elk distribution away from livestock and to reduce comingling. Additionally, there is little tolerance for elk on private lands in the feeding ground area, and WGFD personnel actively haze elk away from livestock. This elk-livestock separation during the feeding season (roughly January through early April ) could explain why fed elk HDs have had fewer affected livestock herds, despite also having higher levels of elk seroprevalence. However, feeding grounds have likely served as foci of brucellosis in the GYA, contributing to disease spread in elk and spillover to livestock in many of the unfed elk HDs (see  for evidence of brucellosis spread from fed to unfed elk). In this case, feeding grounds could incur costs across the broader region, in terms of disease impacts on elk and livestock, while also being protective to livestock at a local level.