Causes of Pneumonia Epizootics among Bighorn Sheep, Western United States, 2008–2010

Thomas E. Besser

, Margaret A. Highland, Katherine Baker, E. Frances Cassirer, Neil J. Anderson, Jennifer M. Ramsey, Kristin Mansfield, Darren L. Bruning, Peregrine Wolff, Joshua B. Smith, and Jonathan A. Jenks

Author affiliations: Washington State University, Pullman, Washington, USA (T.E. Besser, M.A. Highland, K. Baker); Washington Animal Disease Diagnostic Laboratory, Pullman (T.E. Besser); US Department of Agriculture Agricultural Research Service, Pullman (M.A. Highland); Idaho Department of Fish and Game, Lewiston, Idaho, USA (E.F. Cassirer); Montana Fish, Wildlife and Parks, Bozeman, Montana, USA (N.J. Anderson, J.M. Ramsey); Washington Department of Fish and Wildlife, Spokane Valley, Washington, USA (K. Mansfield); US Department of Agriculture Animal and Plant Health Inspection Service, Olympia, Washington, USA (D.L. Bruning); Nevada Department of Wildlife, Reno, Nevada, USA (P. Wolff); South Dakota State University, Brookings, South Dakota, USA (J.B. Smith, J.A. Jenks)

Abstract

Epizootic pneumonia of bighorn sheep is a devastating disease of uncertain etiology. To help clarify the etiology, we used culture and culture-independent methods to compare the prevalence of the bacterial respiratory pathogens Mannheimia haemolytica, Bibersteinia trehalosi, Pasteurella multocida, and Mycoplasma ovipneumoniae in lung tissue from 44 bighorn sheep from herds affected by 8 outbreaks in the western United States. M. ovipneumoniae, the only agent detected at significantly higher prevalence in animals from outbreaks (95%) than in animals from unaffected healthy populations (0%), was the most consistently detected agent and the only agent that exhibited single strain types within each outbreak. The other respiratory pathogens were frequently but inconsistently detected, as were several obligate anaerobic bacterial species, all of which might represent secondary or opportunistic infections that could contribute to disease severity. These data provide evidence that M. ovipneumoniae plays a primary role in the etiology of epizootic pneumonia of bighorn sheep.

In North America, epizootic pneumonia is a devastating, population-limiting disease of bighorn sheep (Ovis canadensis) (1–5). Anecdotal and experimental evidence suggests that in at least some instances, this disease may be introduced into bighorn sheep populations by contact with domestic sheep or goats (5,6). When the disease is first introduced, outbreaks affect animals of all ages (1–3). During subsequent years or decades, sporadic cases of pneumonia in adult sheep and annual epizootics of pneumonia in lambs may continue (7–10).

Considering the dramatic and severe character of epizootic bighorn sheep pneumonia, the etiology is surprisingly unclear. Findings of gross and histopathologic examinations of lung tissue strongly suggest bacterial etiology: anterior–ventral distribution, suppurative inflammation, and abundant bacterial colonies. In domestic ruminants, bacterial pneumonia frequently occurs secondary to viral infections or other pulmonary insults, but extensive efforts to detect such underlying factors for bighorn sheep pneumonia have generally been nonproductive. For example, although evidence of infection or exposure to respiratory viruses, especially respiratory syncytial virus and parainfluenza virus, is frequently found in healthy and pneumonia-affected populations, no consistent association between the disease and any virus has been found (11–13). As a result, most research attention has been directed toward bacterial respiratory pathogens that may act as primary infectious agents, particularly leukotoxin-expressing Mannheimia haemolytica, which is highly lethal to bighorn sheep after experimental challenge (5,14). Other Pasteurellaceae, particularly Bibersteinia trehalosi and Pasteurella multocida, have been more frequently isolated from pneumonia-affected animals during natural outbreaks than has M. haemolytica (11,12,15). Another candidate pathogen, Mycoplasma ovipneumoniae, has recently been isolated from pneumonia-affected bighorn sheep during 2 epizootics (11,16,17); antibodies against this agent were detected in bighorn sheep from 9 populations undergoing pneumonia epizootics but were absent in 9 nonaffected populations (17). In experiments, M. ovipneumoniae has been shown to predispose bighorn sheep to M. haemolytica pneumonia (18). When M. ovipneumoniae–free domestic sheep were commingled with bighorn sheep, the bighorn sheep survived at unprecedented rates (19).

Development of effective methods for managing, preventing, or treating an infectious disease requires a clear understanding of its underlying etiology. However, clarifying the etiology can be difficult, particularly for primary infections (e.g., HIV) that are characteristically associated with multiple opportunistic infections that may be more lethal than the epidemic agent itself. During 2008–2010, epizootic pneumonia of bighorn sheep was detected in at least 5 western US states. These epizootics provided an opportunity to conduct a comparative study of the etiology of this disease (Table 1).

Conventional microbiological methods can fail to isolate agents because of their fastidious in vitro growth requirements or intermicrobial interactions; thus, for agent isolation, we used 2 culture-independent methods (agent-specific PCRs and 16S clone libraries) in addition to conventional bacterial cultures (17,20–22). We expected that primary etiologic agents could be differentiated from opportunistic agents by 1) their detection at high prevalence in affected animals, 2) the presence of single (clonal) strain types within each outbreak, and 3) their uncommon or lack of detection in animals from healthy populations (11,22–24). Therefore, to clarify the etiology of epizootic pneumonia, we applied these criteria to the bacterial respiratory pathogens detected in multiple bighorn sheep epizootics.