Mortality in Pennsylvania Captive Elk (Cervus Elaphus): 1998–2006

In contrast to the significant amount of information published regarding causes of mortality in free ranging deer and other cervids, retrospective reports regarding mortality of farm raised elk are much less prevalent in the literature.²,⁵,⁷,⁸,⁹ Unlike New Zealand and Europe, cervid farming operations are still in a relatively early stage of development in the United States but are growing rapidly in North America, including Pennsylvania.¹,²,³,⁶,⁷,⁸,⁹ Maximizing the health of the elk within each operation is of utmost concern to attending veterinarians, owners, and managers of these facilities.

To more fully describe the causes of mortality in farmed elk in Pennsylvania, the postmortem records of 65 captive elk (Cervus elaphus) submitted to the Animal Diagnostic Laboratory at the Pennsylvania State University, Pennsylvania Animal Diagnostic Laboratory System (PADLS-PSU) from June 5, 1998 through June 23, 2006 were reviewed to determine the primary cause of death of each animal. The animals were received from 22 separate captive elk operations located within central and western Pennsylvania. Only animals that were submitted intact were included in this study.

Postmortem procedures included gross and microscopic examination of lung, heart, rumen, abomasum, small intestine, large intestine, mesenteric lymph nodes, liver, kidney, spleen, and skeletal muscle (semimembranosus). Gross and microscopic examination of the brain was performed in selected cases. The tissues were fixed in 10% buffered formalin, routinely processed, paraffin embedded, sectioned at 5 microns and stained with hematoxylin and eosin. Grocott's Methenamine-Silver, and Ziehl-Neelsen acid-fast staining procedures were used in selected cases to detect fungal organisms and acid-fast bacteria in tissues.

Bacteriology (aerobic and anaerobic cultures) and mycology procedures were performed on selected cases. Tissues (other than intestinal) processed for aerobic culture were inoculated onto Tryptic Soy Agar with 5% sheep blood^a, Columbia CNA Agar with blood^a, and MacConkey Agar plates^a and incubated overnight in air at 37°C. Intestinal tissues processed for aerobic/Salmonella sp. culture were inoculated directly onto MacConkey Agar^a, XLT-4 Agar^a plates and into tetrathionate enrichment broth^a. The plates and broth were incubated overnight in air at 37°C. Tetrathionate broth was subcultured onto MacConkey Agar and XLT-4 Agar plates, which were incubated as before. For anaerobic culture, tissues were inoculated onto CDC Anaerobic Blood Agar^a, Kanamycin-Vancomycin (KV)^a, KV with laked blood (LKV)^a, Phenyl-ethyl Alcohol Agar (PEA)^a, McClung Egg Yolk Agar^a, and B. frag Isolation Agar^a and incubated at 37°C using the Mitsubishi AnaeroPack system^b. For anaerobic culture (for Clostridium sp. only), tissues were inoculated onto Anaerobic PEA^a and McClung Egg Yolk Agar plates^a and incubated at 37°C using the Mitsubishi AnaeroPack system^b. All plates were examined after overnight incubation for bacterial growth. Isolates were identified by using traditional biochemical methods or a commercially available automated identification system.^d Tissues submitted for fungal culture were inoculated onto Sabouraud Dextrose Agar and Inhibitory Mold Agar.^a The plates were examined at weekly intervals for up to 4 weeks and organisms identified by LactoPhenol Cotton Blue^c staining of fungal structures.

Fecal parasitology procedures, using the McMaster fecal flotation technique, were performed on all but 2 animals over the age of 15 days. Abomasal ostertagiasis was diagnosed by examination of abomasal mucosal scrapings and formalin-fixed abomasal tissues using light microscopy.

The elk examined ranged in age from 1 day to 13 1/2 years. The exact age of 1 adult elk was not determined. Twenty-seven females and 36 males were included in the study. Information regarding the sex of 2 elk was not available. In those animals in which multiple diagnoses were made, only the lesion considered the actual cause of death or the primary lesion responsible for euthanasia was included in this study.

Gastrointestinal parasitism, the major cause of elk death in this study, was considered responsible for mortality in 21 animals that ranged in age from 3 months to 11 1/2 years. The diagnosis of gastrointestinal parasitism was made on the basis of severe loss of body condition associated with fecal nematode counts ranging from 400 to 5,800 ova per gram of feces, fecal coccidial counts of 15,000 oocysts per gram of feces, the presence of numerous gastrointestinal nematode parasites on gross postmortem examination or the presence of Ostertagia sp. organisms in abomasal mucosal scrapings with associated histologic lesions including dilated abomasal crypts and abomasitis and the lack of lesions in other major organ systems. The primary organisms identified in fecal samples via qualitative egg and oocyst counts included strongylid (15/21) and Eimeria sp. parasites (1/21). Ostertagia sp. organisms with associated gross and microscopic abomasal lesions were present in 5 elk.

Pneumonia, the second leading cause of elk mortality, was present in 7 animals ranging in age from 6 1/2 months to 5 years. On gross postmortem examination, severe consolidation of the pulmonary tissue was present in all cases. The presence of numerous variably sized fluctuant to firm nodules containing thick tan purulent material was a prominent feature in 6 of the 7 affected lungs. Microscopically, the majority (4/6) of the pulmonary nodules consisted of pyogranulomas characterized by central accumulations of neutrophils, macrophages, numerous fungal organisms consistent with Aspergillus sp. and necrotic cellular debris rimmed by lymphocytes, multinucleated giant cells, and immature fibrous connective tissue. Acid-fast staining procedures performed on pulmonary tissue from the 4 animals were negative for the presence of acid-fast bacteria. In the remaining 2 of the 6 elk, the nodules consisted of abscesses characterized by large central accumulations of neutrophils, lesser numbers of macrophages and cellular debris rimmed by lymphocytes and immature fibrous connective tissue. Numerous fungal organisms consistent with Aspergillus sp. were present in the pulmonary nodules of 1 animal in this group (1/2). Pneumonic lungs from 6 of the 7 animals were submitted for bacterial culture procedures, which included aerobic (6/6) and anaerobic (1/6) culture techniques. Aerobically, Arcanobacterium pyogenes (3/6), Escherichia coli (3/6) and Streptococcus sp. (2/6) were recovered. No significant aerobic bacterial growth was obtained from the affected lung in 1 case (1/6). No bacterial growth was obtained from the 1 affected elk in which anaerobic procedures were performed. The use of antibiotics before the death of the animal, severe autolysis of the tissues at the time of necropsy and performance of the necropsy too late in the disease process may be contributing factors for the lack of isolation of bacterial etiologic agents in 1 case of pneumonia included in our study. Histologically, fungal organisms with morphology consistent with Aspergillus sp. were present within the pulmonary lesions in 5 of the 7 elk. Fungal culture procedures were performed on the affected lungs of 2 elk within this group (2/5) and yielded Aspergillus sp. In a recently published retrospective study of mortality in farmed elk, Arcanobacterium pyogenes, Pasteurella sp., E. coli, Aspergillus sp., and Mycobacterium sp. were cultured from pneumonic lungs.⁹ Although Arcanobacterium pyogenes, E. coli and Streptococcus sp. were recovered from affected lung tissue in our study, the significance of these specific etiologic agents as primary pulmonary pathogens in elk is unknown. The high rate of pulmonary fungal infection found in Pennsylvania captive elk in this study is in contrast to a recent study in which fungal agents were not considered an important etiologic agent associated with fatal pneumonia in captive Pennsylvania white-tailed deer⁶ and may indicate a vulnerability of captive elk to develop mycotic pulmonary infections.

Enterocolitis was diagnosed in 5 elk ranging from 1 day to 10 1/4 years of age. Using both aerobic (5/5) and anaerobic (2/5) bacterial culture procedures, Clostridium perfringens (2/2), E. coli (1/5), Salmonella Newport (1/5) and Salmonella Thompson (1/5) were recovered from intestinal tissues. The microscopic lesions present in the 2 cases of enterocolitis associated with C. perfringens were consistent with clostridial enteropathy in other ruminant species and were characterized by large accumulations of red blood cells and small foci of cellular necrosis intermixed with variable amounts of fibrin within the lamina propria of the intestinal wall. The rapid introduction of high carbohydrate rations to animals unaccustomed to this diet and the subsequent proliferation of intestinal C. perfringens are often associated with acute enterotoxemia in both domestic and nondomestic ruminants. Although specific data regarding feeding practices were not obtained from managers of the captive elk operations, ration mismanagement may have been an important factor in the cases of enterocolitis associated with C. perfringens in this study. The significance of the E. coli as a primary enteric pathogen in our study is unknown.

Severe malnutrition was present in 5 elk that ranged from 6 months to 8 years of age. On gross postmortem examination, cases were characterized by a thin carcass, minimal body fat, and variable amounts of subcutaneous edema with no significant lesions present microscopically in other organ systems.

Rumenitis was present in 5 elk, occurring primarily in young adults and older animals with affected animals ranging from 2 years to 11 1/4 years of age. Although the age of 1 animal in this group was not determined, the elk was considered an adult. All animals in this category exhibited severe acute rumenitis characterized microscopically by large accumulations of neutrophils and necrotic cellular debris within the mucosa of the rumen and underlying submucosal tissues. Large amounts of corn were present within the forestomachs of 4 of the 5 elk. All 4 of the elk were determined to have ruminal acidosis, with ruminal pH values of 5 or less. Ration mismanagement may have been an important factor as the rapid introduction of high carbohydrate feedstuffs to elk unaccustomed to this diet and the subsequent lowering of ruminal pH and associated rumenitis can produce mortality in cervids.¹⁰

Severe acute hepatic necrosis was present in 3 elk in this study, occurring primarily in young animals from 2 weeks to 5 months of age. Microscopically, large multifocal sites of acute hepatocellular necrosis characterized by cytoplasmic hypereosinophilia with nuclear pyknosis and karyorrhexis were present scattered throughout the hepatic tissue.

Septicemia was responsible for the death of 3 elk, ranging from 1 week to 3 1/2 months of age. Aerobic bacterial cultures performed on all animals yielded Listeria monocytogenes (1/3), E. coli (1/3) and Salmonella Oslo (1/3).

Trauma was considered responsible for the death of 2 elk in this study and was characterized by full thickness perforation of the thoracic wall in each of the affected animals. Although trauma was found to be to be a relatively uncommon cause of death in our study, accounting for only 2 elk deaths, this condition was considered a major cause of mortality in captive cervids in previous publications.²,⁴,⁷,⁹ The traumatic injuries to elk in our study, which included thoracic perforations in both cases, may have been inflicted by herdmates owing to change of social status within the herd, overcrowding, fighting of bulls during the rut, competition over limited feeder space, and addition of animals into the herd from an outside source or from a different herd on the farm. Inappropriate animal handling procedures and equipment or improper pen design in addition to the presence of dogs or other animals on the farm, which may overly excite elk in the herd, may also be important factors contributing to traumatic injuries.

Other major causes of mortality in this study, in decreasing order of frequency, included nephrosis (2 cases), systemic abscessation (2 cases), and 1 case of each of the following conditions: pulmonary edema, bronchiolitis, intra-abdominal hemorrhage, hepatic parasitic granulomas, synovitis, and eosinophilic encephalitis. A definitive cause of death was not made in 4 cases.

In recently published studies involving mortality in captive cervids, respiratory and enteric diseases and trauma were considered relatively common causes of death.²,⁴,⁶,⁷,⁸,⁹ In our current study, gastrointestinal parasitism (21 cases), pneumonia (7 cases), enterocolitis (5 cases), malnutrition (5 cases), and rumenitis/acidosis (5 cases) were the most common causes of elk mortality, collectively representing 66.2% of all cases.

According to the findings in this study, the first year of life for captive elk is critical, representing the majority (56.3%) of the total death loss for all known age groups. In addition, 71.4% of the gastrointestinal parasitism, 60.0% of the malnutrition, 60.0% of the enterocolitis, and 57.1% of the pneumonia cases occurred in animals within this age range. Although specific conclusions regarding nutrition and environment cannot be made in this study because of the fact that herd management information was not available, general factors that may contribute to death rates in animals during the first year of life include poor quality colostrum and inadequate colostrum ingestion and absorption by the calf, immaturity of the immune system, and inadequate milk production by the cow. Poor maternal care, inappropriate postweaning nutrition (including transitional diet immediately after weaning), inadequate shelter from temperature extremes, contaminated calving areas, lack of effective vaccination and parasite control programs, and high elk population density on the farms may also be important factors.

By determining the major causes of death and specific age groups most vulnerable to mortality, a variety of effective preventative measures can be instituted. Such measures would include employing nutritional programs appropriate for the age of the animal and implementation of effective vaccination and parasite control programs. Conducting herd health checks throughout the day, especially during the calving season, routine collection of fecal samples to determine parasite loads, rotation of paddocks, moving cows to clean paddocks prior to calving, avoiding animal overcrowding, periodic moving of feeders to clean areas, and providing clean and adequate shelter for protection from temperature extremes should also be instituted. Additional preventative management techniques such as proper pen designs to prevent animals from being cornered by bulls in hard antler, allowing animals to become accustomed to handling areas, fence lines and gates before they are handled and protection of chemically immobilized elk from herdmates should be implemented.

Acknowledgements. The authors would like to acknowledge the veterinarians and producers that submitted animals for postmortem examination and to thank Lola Hubler and William Weaver for necropsy assistance, Roberta Horner and Inese Benks for histology services, and Dr. Walter Cottrell (Pennsylvania Game Commission) for his professional assistance.