Abstract
Farmed cervids are of growing economic importance in the midwestern United States. Although diseases of wild and captive cervids have been examined in more northerly climates, little information exists on the health challenges of deer in the Midwest. We characterized and summarized the causes of mortality in farmed white-tailed deer (Odocoileus virginianus) submitted to the University of Missouri Veterinary Medical Diagnostic Laboratory (Columbia, MO, USA) over a 19-y period (2004–2023). Of 388 cases examined, 253 (65%) were carcasses submitted for autopsy, and 135 (35%) cases were tissue samples harvested by field veterinarians. Infectious disease was the most common cause of mortality (n = 335; 86.3%). Of infectious causes, primary pneumonia was most common (n = 140; 41.7%), followed by septicemia (n = 68; 20.1%), and primary enteritis (n = 64; 19.1%). Viruses were detected in 18% of pneumonia cases. The most common non-infectious diagnoses were emaciation and trauma (both 4 each; 1%). Thirteen animals (3.4%) died of unknown causes. Forty-nine percent of cases were juvenile deer <1-y-old. Most cases were received in the summer (212; 54.6%). Infectious diseases, particularly bacteria and viruses, pose a significant health challenge to farmed deer in the midwestern United States.
Captive cervids, such as white-tailed deer (WTD; Odocoileus virginianus), are an important and growing fraction of agriculture in Missouri. An estimated nationwide direct economic impact of the deer farming industry exceeds $2.6 billion annually. 3 As of 2016, there were >250 deer farms in Missouri. 25 Given the expanding economic importance of captive cervids, it is crucial to understand the causes of morality in these populations. Despite this, few large-scale studies exist that examine the diseases affecting farmed deer populations. Studies that do exist are focused on more northerly populations, such as Wisconsin, Pennsylvania, and Canada.1,8,15,18,26 Based on the more southern location of the University of Missouri Veterinary Medical Diagnostic Laboratory (VMDL; Columbia, MO, USA), we hypothesized that the main causes of mortality of farmed deer in our cohort would differ from previous reports. Our aim was to provide producers and veterinarians with an overview of the diseases seen in farmed WTD in the midwestern United States and compare our findings to previous studies.
Materials and methods
We searched the Laboratory Information Management System of the VMDL for WTD postmortem cases submitted between January 2004 and August 2023. Samples consisted of whole carcasses and fresh and fixed tissues collected during field postmortem examinations. Samples had been submitted by veterinarians and producers from Missouri, Kansas, and Kentucky, as well as from cases investigated by veterinarians at the University of Missouri Veterinary Health Center. The type of submission (autopsy or fresh/fixed tissue), sex, age, principal and secondary diagnoses, and identified etiologic agents were recorded. Many animals had several potential causes of death, and these were grouped into principal and secondary diagnoses to classify disease into categories, such as pneumonia, septicemia, enterocolitis, and non-infectious.
We defined principal diagnosis as the primary postmortem finding. Secondary diagnosis was defined as any additional significant finding that likely contributed to the animal’s death. Up to 4 etiologic agents were included per animal. Pneumonia was used to describe any cases diagnosed with pneumonia, bronchopneumonia, pleuropneumonia, or interstitial pneumonia. Septicemia was defined as any cases with evidence of infection in multiple body systems or organs, such as multifocal random hepatic necrosis in conjunction with interstitial pneumonia. Animals diagnosed with enteritis and enterocolitis were grouped together. Cases in which no cause of death was identified were classified as unknown. For identification of Mycoplasma (Mycoplasmopsis) spp. by PCR, a pair of primers based on nucleotides common to the 16S-23S rRNA intergenic transcribed spacer region of all species of the organism was used. PCR products were then sequenced, followed by phylogenetic analysis to characterize the isolates. We did not include chronic wasting disease (CWD) testing results in our study because CWD has not been detected in farmed deer by our laboratory despite extensive testing according to USDA guidelines.
Cases were classified by estimated or reported age: juvenile (<1-y-old) or adult (≥1-y-old). Autopsy reports consisted of gross and microscopic examination of entire carcasses or fresh and fixed tissues submitted following field autopsy. Dates were classified into seasons: winter (December–February), spring (March–May), summer (June–August), and fall (September–November). Ancillary testing included aerobic culture (n = 290), PCR (n = 286), fecal flotation and/or smear (n = 174), anaerobic culture (n = 132), serology (n = 26), and electron microscopy (n = 4). Rumen pH was tested during autopsy using pH strips; analysis with a pH meter was used in 20 cases. Testing was performed at the request of submitters or the discretion of the primary pathologist performing the autopsy. Tissue processing for histopathology and ancillary tests was performed according to the standard operating procedures of the VMDL.
Results
We included 388 submissions from WTD in our study (Fig. 1). There were 253 whole carcasses (65.2%), and 135 fresh or fixed tissues (34.8%); 175 (45.1%) cases were male, 160 (41.2%) were female, and sex was not reported for 53 animals (13.7%). One hundred eighty-nine (48.7%) cases were juvenile animals, 155 (39.9%) were adults, and 44 (11.3%) were of unknown age. The largest number of submissions arrived in the summer (212; 54.6%), followed by fall (92; 23.7%), spring (51; 13.1%), and winter (33; 8.5%).
Counts of mortality in farmed white-tailed deer in the midwestern United States by season. Major causes of death are shown as the proportion of animals of all ages that died from a given cause. Enteritis = mortality due to enteritis or enterocolitis; miscellaneous infectious/inflammatory = mortality due to another infectious or inflammatory disease (e.g., parasitism, rumenitis, meningitis); other = mortality due to a non-infectious or unknown cause (e.g., trauma, emaciation, neoplasia); pneumonia = mortality due to pneumonia; sepsis = mortality due to sepsis.
Infectious disease was the most common primary diagnosis (Table 1), with pneumonia most frequent (140; 36.1%) followed by septicemia (68; 17.5%) and enteritis/enterocolitis (55; 14.2%). Non-infectious diseases (Table 2) comprised a small fraction of mortality in our study (17; 4.4%). Infectious agents identified included bacterial, viral, fungal, parasitic, and protozoal agents.
Infectious disease conditions that caused death in farmed white-tailed deer in order of frequency of diagnosis.
BTV = bluetongue virus; BVDV = bovine viral diarrhea virus; EHDV = epizootic hemorrhagic disease virus.
Non-infectious disease conditions that caused death in farmed white-tailed deer.
In animals diagnosed with primary pneumonia (n = 140), Trueperella pyogenes was the most frequently isolated bacterium (61; 43.6%), followed by Pasteurella multocida (37; 26.4%), Mycoplasma spp. (33; 23.6%), Bibersteinia trehalosi (23; 16.4%), and Fusobacterium necrophorum (16; 11.4%). Less frequently isolated bacteria included Escherichia coli (11; 7.9%), members of the Streptococcaceae family (10; 7.1%), Mannheimia haemolytica (6; 4.3%) and M. granulomatis (2; 1.4%), Corynebacterium spp. (2; 1.4%), Salmonella spp. (2; 1.4%), and Klebsiella pneumoniae (1; 0.07%). Viruses were detected in 26 cases of pneumonia (18.6%) by PCR. Epizootic hemorrhagic disease virus (EHDV) was most frequently detected (14; 10%), then bluetongue virus (BTV) and herpesvirus (5 each; 3.6%). Two animals were positive for bovine parainfluenza virus 3 (BPIV3; 1.4%). A single case was consistent with fungal pneumonia, but fungal identification was unsuccessful. Fifty-eight cases (41.4%) had multiple viral or bacterial etiologies identified. Coinfections of Trueperella spp. and Fusobacterium spp. were seen with the greatest frequency (12; 20.6%). The most common bacterial and viral coinfection was by Trueperella spp. and EHDV (5; 8.6%). Pneumonia was diagnosed based on gross and histologic examination in 24 cases (17.1%) with no identified etiologic agent. Cases of pneumonia were most frequently diagnosed in the summer (68; 48.5%) followed by fall (36; 25.7%), winter (22; 15.7%), and spring (14; 10%). However, the relative frequency of pneumonia diagnosis was highest in winter (22 of 33; 66.7%), followed by fall (36 of 92; 39.1%), summer (68 of 212; 32.1%), and spring (15 of 51; 29.4%). Diagnoses of pneumonia were distributed evenly among ages and sexes, with 63 cases in juveniles (45%), 60 in adults (42.9%), and 59 female deer (42.1%) and 58 males (41.4%).
Septicemia was the second most frequent infectious disease diagnosis (68 [17.5%] principal diagnoses). E. coli was identified in the highest number of septicemia cases (22; 32.4%). Staphylococcus spp. and T. pyogenes were each cultured 8 times (11.8%). Additional organisms identified included Mycoplasma spp. (5; 7.4%), Clostridium perfringens (4; 5.9%), F. necrophorum (3; 4.4%), Pasteurella spp. (3; 4.4%), B. trehalosi (3; 4.4%), Mannheimia spp. (2; 3.1%), Salmonella spp. (1; 1.5%), and Pseudomonas spp. (1; 1.5%). Viruses were detected in 9 cases of septicemia (13.2%) including EHDV (4; 5.9%), nonspecific herpesvirus (3; 4.4%), and one case each of BTV and bovine viral diarrhea virus (BVDV; 1.5%). No etiologic agent was identified in 16 cases (23.5%). Septicemia was diagnosed most frequently in the summer (47; 69.1%), followed by fall (12; 17.6%), and spring (8; 11.8%), with one case (1; 1.5%) in the winter. The relative frequency of septicemia diagnoses among the submissions was also highest in the summer (48 of 212; 22.6%), followed by spring (8 of 51; 15.7%), fall (12 of 92; 13%), and winter (1 of 33; 3%). Most cases were in juveniles (n = 49; 72%) with 11 (16.2%) cases in adults, and 8 (11.8%) cases in deer of unknown age. Males and females were approximately equally likely to be diagnosed with septicemia (29 [42.6%], 33 [48.5%], respectively).
Enteritis and enterocolitis were also significant infectious causes of mortality in captive WTD. The primary diagnosis was enteritis or enterocolitis in 64 (16.5%) submissions. The most frequently cultured bacteria were E. coli (41; 64%) and C. perfringens (23; 36%). Additional bacterial pathogens included Salmonella spp. (2; 3.1%), Pseudomonas spp. (1; 1.5%), Clostridioides difficile (1; 1.5%), Corynebacterium spp. (1; 1.5%), and Campylobacter jejuni subsp. jejuni (1; 1.5%). The most frequently detected virus in enteritis cases was BVDV in 5 cases (7.8%). Other viral pathogens included bovine coronavirus (3; 4.7%), rotavirus (3; 4.7%), EHDV (2; 3.1%), nonspecific herpesvirus (2; 3.1%), and one case of BTV (1.5%). Four cases had Cryptosporidium spp. identified on fecal smear (6.3%). No etiology was identified in 8 cases (12.5%). One case was diagnosed with rotaviral infection by transmission electron microscopy (TEM). In the other 3 cases in which TEM was used, no agent was identified. Enteritis was most frequently diagnosed in the summer (39; 60.9%), followed by spring (11; 17.2%), fall (9; 14.1%), and winter (4; 6.3%). The relative frequency of enteritis diagnosis among the submissions was highest in the spring (11 of 51; 21.6%), followed by summer (39 of 212; 18.4%), winter (4 of 33; 12.2%), and fall (9 of 92; 9.8%). Over half of the enteritis cases were juveniles (41; 64.1%), 18 (28.1%) were adults, and 5 (7.8%) animals were of unknown age. Males (28; 43.8%) and females (27; 42.2%) were roughly equally represented, with 9 cases (14.1%) of unstated sex.
Fecal flotations and/or smears were performed on 174 (44.8%) cases. Parasites most commonly identified included coccidia (20; 11.5%), strongylids (9; 5.2%), Cryptosporidium spp. (8; 4.6%), trichostrongyles (8; 4.6%), and Giardia spp. (3; 1.7%). Cryptosporidium spp. was listed as the principal diagnosis for 1 case (0.1%) and the secondary diagnosis in 3 animals with enterocolitis (1.7%).
EHD was the primary diagnosis listed in 12 cases (3.1%) and was identified in 47 animals (12.2%). Secondary bacterial pathogens in animals with EHDV included B. trehalosi (2; 4.3%), Haemophilus spp. (1; 2.1%), Mycoplasma spp. (1; 2.1%), Streptococcus bovis (1; 2.1%), and Salmonella spp. (1; 2.1%). Herpesvirus was also detected by PCR in 2 cases (2; 4.3%) with EHDV. The most common postmortem findings in all animals positive for EHDV were pneumonia (10; 21.3%) and pulmonary edema with congestion or hemorrhage (9; 19.1%). In animals with a primary diagnosis of EHDV, hemorrhages were the most common finding (5; 41.7%), with locations including the myocardium (3; 60%), gastrointestinal mucosa (1; 20%), and lymph nodes (1; 20%). Other findings (1 each; 8.3%) in deer diagnosed with EHD included emaciation, pleuritis, myocarditis, tracheitis, meningoencephalitis, and lymphoid hyperplasia. EHDV was detected in an average of 2.75 deer/y in 2006–2023, with 13 cases identified in 2012. Most cases of primary EHD were diagnosed in the summer (6; 50%) or fall (6; 50%), with no cases diagnosed in the spring or winter. Most EHDV cases were in adult animals (n = 9; 75%), with 2 (16.7%) juveniles and 1 (8.3%) animal of unknown age. Six were male (50%) and 5 female (41.7%), with 1 (8.3%) of unstated sex. BTV was detected in 14 (4.2%) animals, and a primary diagnosis of BT was given to 3 (0.9%) animals, 1 of which was also positive for a nonspecific herpesvirus.
Two juvenile deer were given primary or secondary diagnoses of Tyzzer disease. No bacteria were cultured from the liver of either animal, but thin, filamentous bacilli morphologically consistent with Clostridium piliforme were identified with Warthin–Starry staining in hepatocytes at the periphery of necrotic foci.
Non-infectious causes of morbidity and mortality were assigned to 17 cases (4.4%; Table 2). Emaciation and trauma were the most frequent diagnoses among non-infectious conditions, with 4 cases each (1%). Two animals had oxalate nephrosis (0.5%), and 2 had pigment nephropathy (0.5%). Neoplasia was uncommonly encountered in our cohort; 1 patient had a tracheal squamous cell carcinoma and another an acanthomatous ameloblastoma.
Discussion
Previous surveys of mortality in captive deer have identified trauma, parasitism, pneumonia, and enterocolitis as frequent causes of death in captive cervids.8,15,17,27 Similar to our findings, T. pyogenes was identified most commonly in deer with pneumonia, as were P. multocida and B. trehalosi.8,18 We found that multiple pathogens were often involved in the development of pneumonia in WTD. The 3 most common respiratory bacterial etiologies were Trueperella spp., Pasteurella spp., and Mycoplasma spp., similar to the findings described in farmed deer in Wisconsin and elk in Pennsylvania.8,18 However, Mycoplasma spp. were more commonly identified in our cohort than in previous studies, possibly due to our approach to detecting Mycoplasma spp. The general Mycoplasma spp. PCR performed on the cases in our study detected the organism more frequently in juveniles (23; 69.7%) than adults (10; 30.3%). M. bovis and M. ovipneumoniae were the most frequently detected species in our study. A previous report described M. bovis as a cause of pneumonia in farmed WTD fawns and suggested that it acted synergistically with other bacterial pathogens to increase the severity of respiratory disease. 13 In a 2023 report, M. ovipneumoniae was implicated as a significant respiratory pathogen in WTD, in which it caused disease in a greater number of juveniles than adults. 6 In the bovine respiratory disease complex (BRDC), Trueperella spp. is considered an opportunistic secondary invader, and this likely holds true for farmed deer as well. 24 Administration of antimicrobials may play a role in obscuring primary pathogens in deer as with other livestock. B. trehalosi was the fourth most frequently isolated bacterium associated with pneumonia in our cohort, differing from previous reports in which it was diagnosed with greater frequency.8,18
In our study, 18.6% of pneumonias were associated with viral pathogens. Of these, EHDV was the most commonly detected virus, followed by BTV and a nonspecific herpesvirus. As described in cattle, viral infections in deer may predispose them to secondary infection by opportunistic bacterial and fungal pathogens. Environmental stressors such as handling, high population density, extreme weather, and transportation may play an additional and potentially more significant role in the development of disease in farmed cervids than in domesticated species.8,11
Generally, viruses appear to have played a greater role in mortality of captive cervids in our cohort compared to reports focusing on more northern areas.5,9,18,27,28 BTV and EHDV were the most frequently isolated viral pathogens in our study and are considered important endemic pathogens of deer in the United States. BTV and EHDV are closely related orbiviruses that can cause distinct and separate disease entities or simultaneous infections.9,16 Both are transmitted via Culicoides spp. midges. The distribution of these viruses is geographically consistent with the range of their insect vectors. The most important vector in North America is C. sonorensis, an insect whose range has historically been limited to the southern midwestern United States, perhaps explaining the marked absence of BTV and EHDV cases in farmed deer in more northern areas.2,5,8,9,18,26-28 However, in the face of increasingly warmer weather in recent years, Culicoides spp. can be expected to expand, exposing deer in historically protected northern climates to BTV and EHDV.2,26,28 Infections are most frequently seen in summer, which is supported by our data.
Cattle are considered the natural hosts of BTV, with WTD functioning as short-term carriers that are susceptible to severe clinical disease. 16 WTD are considered the species most susceptible to EHDV, and infection often manifests as high-mortality events within a herd. 16 BTV and EHDV infections can result in identical clinical and postmortem findings. Most often, they are described as acute or peracute hemorrhagic diseases, with hemorrhage and edema frequent postmortem findings.16,19,20 Myocardial hemorrhage was the most frequently encountered lesion in animals with a primary diagnosis of EHD in our study. Other findings included pulmonary edema, emaciation, pleuritis, myocarditis, tracheitis, lymphoid hyperplasia, meningoencephalitis, and no lesions. In the 3 animals with a primary diagnosis of BT in our cohort, the only microscopic lesions described were none or splenic lymphoid depletion and necrosis. BT and EHD were the primary diagnoses in only 15 of 47 animals that were PCR positive for the virus. As both viruses are endemic in deer populations in the midwestern United States, detection of the viruses may indicate subclinical infection. The role of BTV and EHDV as co-pathogens warrants further investigation.
Other viral pathogens identified by PCR include bovine coronavirus, BPIV3, BVDV, and rotavirus. BVDV infection in deer has been demonstrated both experimentally and through high seroprevalence rates in epidemiologic data. 23 Additionally, persistent infection with BVDV has been demonstrated in cervids.12,23 Despite this, cervids are considered an unlikely reservoir of BVDV infection for domestic cattle. 23 Although BPIV3 infrequently causes clinical disease as a primary pathogen, it is commonly recognized as part of BRDC. 10 Frequently, it is part of a coinfection with other viral or bacterial agents, as it can impair mucociliary clearance and predispose the animal to opportunistic infections. 10 Two juvenile female deer from the same farm were positive by PCR for BPIV3 in our study. Both animals were diagnosed with primary sepsis and had several comorbidities, including herpesviral PCR positivity and infection with P. multocida. As in cattle, it is possible that BPIV3 infection decreased immunity and increased susceptibility to other infectious agents in these fawns. In species other than cattle, BPIV3 infection has been identified via serology in sheep, Old and New World camelids, and fallow deer.10,22 Rotavirus and coronavirus are established causes of diarrhea in fawns, particularly in conjunction with potential bacterial pathogens such as E. coli and protozoal infections such as by Cryptosporidium spp.7,10,17
Malignant catarrhal fever, or ovine gammaherpesvirus 2 infection, is considered one of the most important viral diseases of farmed deer worldwide. 14 Twenty-three cases of herpesvirus were detected by nonspecific herpesviral PCR in our study, but no further species-specific analysis was conducted; hence, the significance of herpesviral DNA identification in our study is unknown.
Although uncommon in ruminants, there is a single case report of Tyzzer disease in fawns. 4 Small animal species often have a triad of lesions of hepatitis, myocarditis, and colitis. 21 Foals, by contrast, most often have multifocal necrotizing hepatitis, with a 2022 study finding colitis and myocarditis in less than half of cases. 14 The only lesion in both cases in our cohort was necrotizing hepatitis. In other species, young or immunocompromised animals are most susceptible to infection with C. piliforme.4,14,20 Both of the deer in our cohort were juveniles.
In our cohort, parasitism was not considered a major contributor to mortality. This is in contrast to previous studies of captive cervids, in which parasitism was frequently identified as a cause of death.8,15–17,27 In captive elk in Pennsylvania, gastrointestinal parasitism was considered the major cause of death, with emaciation as the preeminent finding, and strongylid eggs and Eimeria spp. oocysts identified most frequently. 18 One animal in our cohort was given a principal diagnosis of emaciation with a secondary diagnosis of parasitism; many strongylid nematode eggs and moderate numbers of coccidial oocysts were identified by fecal flotation. In captive cervids in Canada and Pennsylvania, the liver fluke Fascioloides magna and coccidiosis were identified as significant causes of morbidity and mortality.18,27 A single animal in our study was diagnosed with liver flukes based on gross and histologic examination.
Juvenile animals were 49.7% of animals in our study. In previous research, fawn mortality rates between birth and 1-y-old have been described as high as 30%, causing a significant economic loss to producers. 17 We identified pneumonia as the most frequent primary cause of death in this age group, followed by sepsis and enterocolitis. As seen in previous reports, juveniles were significantly more likely to be diagnosed with sepsis than adults. Additionally, enteritis was diagnosed in juvenile animals in the summer more than other times of year, possibly reflecting the increased susceptibility of young animals to pathogens resulting in gastrointestinal disease. The highest number of juvenile animal submissions was in the summer, which likely is correlated with WTD fawning season.
Although trauma was one of the most common non-infectious causes of mortality in our study, it was only diagnosed in 1% of total cases. Trauma is identified as a frequent cause of death in wild cervids, who are more susceptible to predation, hunting, and automobile-related incidents than their captive counterparts. 1 In other studies of captive cervids, trauma associated with handling was considered an important cause of death;15,26 however, both of these studies were based on surveys of producers, not autopsy examination. The low incidence of trauma in captive WTD in our cohort may be due to producers not submitting such animals for postmortem testing. Further investigation into the handling procedures used for captive cervids would be useful to mitigating trauma-related injuries and death.
Footnotes
Acknowledgements
We thank the current and former staff of the University of Missouri VMDL for their assistance in the collection of these data, and Karen Clifford for her assistance with figures.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with respects to the research, authorship, and/or publication of this article.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
