Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae

Chapter 5

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Megan E.B. Jones*, David J. Gasper**, Emily Mitchell (née Lane),†,‡ *Institute for Conservation Research, San Diego Zoo Global, San Diego, CA, United States; **Pacific Zoo & Wildlife Diagnostics, San Diego, CA, United States; †National Zoological Gardens of South Africa, Pretoria, South Africa; ‡University of Pretoria, Pretoria, South Africa

INTRODUCTION The families Bovidae, Antilocapridae, Giraffidae, Tragulidae, and Hippopotamidae represent a large and diverse group of ruminant and pseudoruminant artiodactyls. Full common and scientific names in these taxa are presented in Supplemental Table e1 and dental formulae are included in Supplemental Table e2. Additional information about these taxa is presented in the supplemental materials. Bovidae is the largest family, with 8 subfamilies, 50 genera, and approximately 140 species.

UNIQUE FEATURES Notable features of the respiratory anatomy include the enlarged nasal proboscis and complex rostral vestibule present in the saiga antelope (Clifford and Witmer, 2004), and enlarged larynx and elongated vocal tract in the takin and Mongolian and goitered gazelles (Fig. 5.1) (Frey et al., 2011). The family Antilocapridae is monotypic, with pronghorn antelope being the sole member. Free-ranging pronghorn are restricted to the Central and Western North America. The family Giraffidae includes 2 genera represented by the giraffe and okapi. Multiple jugular vein valves prevent retrograde venous flow when the head is lowered (Fig. 5.2). The family Tragulidae includes 3 genera and at least 10 species of chevrotains or mouse deer, and includes the smallest living ungulates. The family Hippopotamidae includes 2 genera represented by the common or river hippo and the pygmy hippo.

NON-INFECTIOUS DISEASES Nutritional Nutritional deficiencies occur in captive browsing animals offered a limited variety of feed and free-ranging animals Pathology of Wildlife and Zoo Animals. http://dx.doi.org/10.1016/B978-0-12-805306-5.00005-5 Copyright © 2018 Elsevier Inc. All rights reserved.

with restricted habitats or in regions with known mineral deficiencies (Dierenfeld et al., 1988). Copper deficiency is well described in domestic ruminants, and has been documented in species representative of most groups in this chapter (Dierenfeld et al., 1988). Primary deficiency is associated with a lack of dietary copper; however, secondary deficiencies often are associated with feed components such as molybdenum that impair copper uptake in ruminants. In nondomestic species, lesions associated with copper deficiency include anemia, generalized poor body condition, diarrhea, dermatopathy, and neonatal degenerative neuropathy with generalized weakness and posterior paresis (enzootic ataxia/swayback), developmental defects including cardiovascular and skeletal malformation, and reduced fertility and abortion. An unsteady gait disease characterized by pica, dyskinesia, and unsteady gate due to secondary copper deficiency has been reported in freeranging Tibetan gazelles (Shen et al., 2010). Dermatopathy secondary to impaired tyrosinase activity is characterized by progressive bleaching of the haircoat and straightening or coarsening of the hair fibers and may be more prominent in dark-coated animals. Although the pathogenesis is unclear, in utero and neonatal copper deficiency causes a neuropathy characterized by neuronal degeneration, malacia of the cerebral white matter, and Wallerian degeneration in the spinal cord (Fig. 5.3). Severity is dependent on the age at onset. Copper deficiency may also increase susceptibility to gastrointestinal parasitism, especially Haemonchus spp. abomasal nematodes. While copper wire bolus therapy is used as a component of anthelmintic therapy in many zoos, it is not a replacement for normal dietary copper sources. Vitamin E and selenium (Se) deficiencies most significantly result in nutritional myopathies; however, they are also associated with oxidative damage in many organ 117

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FIGURE 5.1  Normal laryngeal anatomy of a Sichuan takin, showing larynx and cranial portion of the trachea—cut section. In both males and females, the larynx is greatly expanded due to the enlargement of the thyroid cartilage, which forms a rigid-walled, ventral, and caudal pouch-like expansion. (Photo courtesy of Disease Investigations, San Diego Zoo Global)

FIGURE 5.2  Normal valves in the lumen of a jugular vein from a reticulated giraffe. These prevent retrograde blood flow when the head is lowered. The surfaces of the valves are smooth and contiguous with the surrounding intima. (Photo courtesy of the University of Illinois Zoological Pathology Program)

systems. The primary lesion of nutritional myopathy is multifocal, polyphasic myofiber degeneration. This should be distinguished from exertional myopathy (see section, Metabolic), which often exhibits a monophasic pattern. A distinguishing feature in nutritional myopathy is retention

FIGURE 5.3  Coronal section of formalin-fixed brain from a stillborn Kenya impala with profound copper deficiency and hydranencephaly. Bilaterally, there is nearly complete absence of the cerebral hemispheres and replacement by large, cavitary spaces enclosed by thin membranes of remnant cortical tissue. In contrast to hydrocephalus, the cavities are formed by loss of tissue rather expansion of the ventricles and the calvarium is usually morphologically unaffected. (Photo courtesy of Disease Investigations, San Diego Zoo Global)

of ­damaged myofiber basal laminae and satellite cells that facilitate myofiber regeneration and repair. Regions with selenium-deficient soils are distributed on all continents. Secondary deficiency due to ingestion of selenium-antagonizing heavy metals is also common and lesions cannot be distinguished from those of primary deficiency. Even in intensively managed ruminant livestock, nutritional

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

­ yopathies are often present with an irregular temporal m pattern and distribution within the population, likely due in part to the influence of periodic climatic variations on forage growth and feed crops. Osteoporosis of undetermined etiology has been described in the skulls of free-ranging mountain sheep in the southwestern United States (Bleich et al., 1990). Possible etiologies include dietary deficiency of copper or magnesium, and increased demand for calcium due to pregnancy or lactation. “Stiffness of the Extremities Disease” is a recently described condition associated with low dietary phosphorus in the eastern Asian yak; similar diseases have been reported in water buffalo (Shen and Zhang, 2012). The mandible, scapulae, sacrum, ilium, and ribs are most severely affected and exhibit varying degrees of osteoporosis and brittle fragility with thinning of the cortical bone and expansion of the marrow cavity into the epiphyses. Additional gross lesions include nonmineralizing expansion of the epiphyses of long bones, with concurrent diaphyseal bowing, and are similar to those observed in hypophosphatemic rickets. Dietary imbalances in calcium and phosphorus also occur in captive and free-ranging animals in areas overlapping with Se-deficiency regions. These imbalances often result in metabolic bone diseases (e.g., Vitamin D deficiencies). It is notable that free-ranging animals deficient in calcium and phosphorus may exhibit pica, and subsequent geophagia and osteophagia may predispose to botulism.

Metabolic Ruminal acidosis is widely reported in captive nondomestic ruminant animals. The condition commonly occurs secondary to dietary grain excess, and the clinical presentation is similar to that described in domestic ruminants. Lesions include rumen papillary blunting with epithelial hyperplasia and parakeratosis; acute or chronic rumenitis, with or without pustules, may be present but is not always seen. Secondary bacterial and fungal rumenitis, hepatic absessation and necrosis, and laminitis are common in captive animals, particularly springbok, deer and pronghorn (Wiedner et al., 2014). Acidosis may also result in neurologic signs, and hemorrhagic foci in the thalamus and brainstem and cortical laminar necrosis resembling thiamine-responsive polioencephalomalacia have been reported in free-ranging pronghorn with access to grain. Urolithiasis, with or without obstruction, occurs with some frequency in this group of animals, and diet has been identified as a significant contributing factor. Similar to domestic ruminant species, the sigmoid urethral flexure and urethral process in male animals are common sites of obstruction, but uroliths can occur anywhere in the urinary tract. Calcium carbonate uroliths are most commonly reported in giraffe and wildebeest, and elevated dietary phosphorus and high ratios of feed concentrate to forage have been suggested as possible contributing factors (Miller

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and Fowler, 2015). Gross and microscopic lesions are often referable to chronic irritation or obstruction. Important sequelae include hydronephrosis, azotemia, and urinary bladder rupture. A brief summary of urolithiasis adapted from Osborne et al. (2009) is presented in Supplemental Table e3. Peracute mortality syndrome in captive giraffe refers to a syndrome in which animals are suddenly found dead, with poor body condition and serous atrophy of fat as the principle postmortem findings (Fowler, 1978). This has subsequently been characterized as a chronic condition related to the unintentional provision of inadequate or inappropriate nutrition, with acute environmental or other stressors (Potter and Clauss, 2005). This syndrome, as well as significant differences in dental wear exhibited by captive and free-ranging giraffe, illustrate the incomplete understanding of the dietary requirements of Giraffidae, and highlight the importance of standardized body condition scoring (Clauss et al., 2007). Cardiovascular disease is rarely described in freeranging animals but has been recognized as a poorly characterized disease in captivity. A syndrome of recurrent pregnancy-associated congestive heart failure has been described in okapi (Warren et al., 2017). The syndrome is of uncertain etiology, and presents in mid-gestation with left-sided heart failure. Grossly, globoid cardiac enlargement with severe left atrial dilatation, left atrial epicardial and mural myocardial hemorrhage, pericardial hemorrhage, and pleural effusion have been noted. Microscopic changes include severe left atrial fibrosis and acute hemorrhage, bilateral ventricular fibrosis, arteriosclerosis of the great vessels, and chronic passive congestion in the lungs and liver. A review of mortality in 121 adult captive pygmy hippopotamuses from 129 zoological institutions revealed that cardiovascular disease accounted for 17% of all deaths in animals ranging from 3 to 30 years of age. Infection with encephalomyocarditis virus (EMCV) was the primary cause (see section, Infectious Diseases); however, chronic diseases including dilated cardiomyopathy, degenerative valvular disease, and myocardial degeneration and fibrosis were also documented (Flacke et al., 2016). Exertional (capture) myopathy (Figs. 5.4 and 5.5) may be the most significant and well-described metabolic disease affecting animals in this chapter, and has been reviewed in detail in nondomestic ruminants (Paterson, 2007). Exertional myopathy was originally described as a fatal sequela to capture in free-ranging ruminants, and has subsequently been described in capture- and noncapture-related morbidity and mortality in a broad range of free-ranging and captive ­nondomestic bovids, as well pronghorn, giraffe, okapi, and hippos (Flacke et al., 2016; Miller and Fowler, 2015; Paterson, 2007). The clinical presentations and lesions of exertional myopathy have been grouped into four syndromes: hyperacute (capture shock), acute (ataxic myoglobinuric), subacute (ruptured muscle), and chronic (delayed peracute).

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Clinical presentations and lesions may be influenced by numerous factors including nutritional status, comorbidities, and degree and duration of the exertion (Meyer et al., 2008). The hyperacute or capture shock syndrome of capture myopathy is uncommon and primarily characterized by severe metabolic alterations presenting as weakness or muscle stiffness, ataxia, hyperthermia, acidosis, shock, and sudden death occurring less than 6 h after the insult. Gross musculoskeletal lesions may be absent or nonspecific and reflect the effects of shock. Microscopic lesions include acute coagulative necrosis of individual or small groups of skeletal and

FIGURE 5.4  Gross appearance of skeletal muscle from a Defassa waterbuck with subacute exertional myopathy. There is moderate regional pallor to the muscle bellies with faint white/tan streaking, and the tissue has a “dry” appearance. (Photo courtesy of Disease Investigations, San Diego Zoo Global)

FIGURE 5.5  Exertional myopathy in fringe-eared oryx. There is coagulative and contraction-band necrosis of the individual myofibers, with hyalinization of the sarcoplasm and loss of cross striation. (Photo courtesy of Disease Investigations, San Diego Zoo Global)

cardiac myofibers. These changes may be accompanied by microvascular thrombi and microscopic foci of acute necrosis in most tissues susceptible to acute hypoxia and acidosis. The acute or ataxic myoglobinuric syndrome in capture myopathy is the most common presentation. It is characterized by acute skeletal and cardiac myodegeneration and necrosis resulting in weakness, ataxia, and release of myoglobin with subsequent myoglobinuria. Myoglobinuric nephrosis and renal failure occur hours to days after the initial insult. Gross lesions are present in the heart, axial and appendicular skeletal muscles, and kidneys, with pulmonary congestion and edema and adrenocortical hemorrhage evident in many cases. Myocardial and skeletal muscle lesions are influenced by the time interval between insult and examination. Acute lesions in the heart and major axial and appendicular muscle groups include soft, red to black, congested or hemorrhagic muscle bellies with regions of pallor or linear, pale streaking. With chronicity, affected muscles may become firm, pale, or tan, with a putty-like, gritty, or chalky texture. Kidneys are swollen and dark brown; a darker brown band may be present within the cortex. Urine is dark brown, and may exhibit a nonspecific positive dipstick reaction for blood. Myoglobinuria is distinguished from hemoglobinuria by a positive ammonium sulfate precipitation test on the urine. In the acute syndrome, microscopic lesions in the cardiac and skeletal muscle are often monophasic and characterized by hemorrhage, myofiber swelling, loss of cross-striations, hypereosinophilia, contraction band or retraction cap formation, sarcoplasmic vacuolation or fragmentation, and nuclear pyknosis. In skeletal muscle, type II and modified type I myofibers are primarily affected; however, all myofiber types may be affected in severe cases. Neutrophilic inflammation may be present in acutely affected regions. With chronicity, there is increased infiltration by mononuclear inflammatory cells, myofiber satellite cell proliferation, and fibroplasia and fibrosis. Myofiber mineralization may be present. Renal lesions are most prominent in the cortices with extensive tubular ectasia, degeneration, and necrosis. Tubules frequently contain hypereosinophilic hyaline and granular casts. The subacute syndrome may present 24–48 h after insult. Gross lesions are typical of those in the acute syndrome with the addition of rupture of affected muscles and extensive hemorrhage. The appendicular weight-bearing muscles and those subject to greater loads are typically affected and can rupture along regions of necrosis. Microscopic lesions are more extensive with entire muscle bellies and muscle groups affected. Inflammatory and reparative changes may be evident and characterized by increased sarcoplasmic basophilia, nuclear centralization, multinucleation, and nuclear rowing. The chronic or peracute-delayed syndrome of capture myopathy is uncommon. The syndrome manifests in animals that survive the acute syndrome with without significant clinical or gross abnormalities but die suddenly following a

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

subsequent stressor, such as recapture. In affected animals, there are few gross lesions and the microscopic lesions in the heart and skeletal muscle are similar to, but less severe than, those described in the acute syndrome.

Toxic Toxicoses in captive and free-ranging wildlife may result from exposure to a number of natural and anthropogenic agents including toxic plants and animals, agricultural and industrial toxins, and intentional poisonings secondary to illegal hunting. Although toxic plants occupy an important ecological niche in most range lands, plant toxicoses are infrequent. Evolutionary pressures have likely resulted in avoidance behaviors and physiological adaptations that enable some ruminant species to ingest plants that would otherwise be toxic (Miller and Fowler, 2015). Intentional fatal pesticide toxicoses due to illegal hunting of African antelope have recently been reviewed, and represent an ongoing threat to free-ranging animals (Ogada, 2014). Supplemental Table e4 summarizes select toxins affecting the animals in this section.

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but also present in inner medulla and cortex. In one report, springbok with polycystic kidneys were also diagnosed with lysosomal storage disease (Herder et al., 2015). Fetal developmental anomalies and malformations, such as cyclopia, arthrogryposis, schistosomus reflexus, laryngeal atresia, and amorphus globosus occur in various captive nondomestic hoofstock species (Fig. 5.7). Malformations are most likely spontaneous, rather than hereditary (Rideout, 2012).

Congenital/Genetic The prevalence of polycystic kidney disease (PKD) in captive pygmy hippopotamuses is reported to exceed 35% in adult and geriatric animals (Flacke et al., 2016). Though most affected animals have been female, both sexes are affected (Nees et al., 2009). The relatedness of some affected individuals suggests a familiar pattern of inheritance, and the condition shares similarities with autosomal dominant forms of polycystic kidney disease in cats and humans. However, specific genetic mutations have not yet been identified in pygmy hippos with PKD. Grossly, few to myriad cysts up to several centimeters in diameter are distributed throughout the renal cortex and medulla, often effacing normal parenchyma (Raymond et al., 2000). Histologically, ectatic tubules and cysts are lined by cuboidal to flattened epithelium, with occasional epithelial hyperplasia or dysplasia. Bowman’s capsules are dilated and membranous glomerulopathy has been described. Cysts are surrounded by interstitial fibrosis and may contain cell debris or pale, eosinophilic fluid (Fig. 5.6). In some cases, cysts are also described in the liver (biliary cysts), duodenum (cystic Brunner’s glands), thyroid glands, and/or pancreas, but these appear to be clinically insignificant. A lethal, neonatal polycystic kidney disease has also been described in captive springbok, affecting up to 18% of live births in one captive population (Herder et al., 2015; Iverson et al., 1982). In these cases, there was no sex predilection and inheritance was most consistent with an autosomal recessive pattern. Grossly, affected animals exhibited bilaterally ­symmetric nephromegaly. Cysts were approximately 1–3 mm in diameter and were most frequent in the outer medulla

FIGURE 5.6  Polycystic kidney from a pygmy hippopotamus. Dilated renal tubules and Bowman’s capsules are scattered throughout the renal cortex. Cysts contain pale, eosinophilic fluid. There is relatively high prevalence of polycystic kidney disease in pygmy hippopotamuses. Some cases are accompanied by elevated BUN and creatinine. (Photo courtesy of Disease Investigations, San Diego Zoo Global)

FIGURE 5.7  Complete laryngeal atresia in a stillborn Indian blackbuck. A congenital failure of formation of the laryngeal opening leads to chronic accumulation of pulmonary secretions and progressive ectasia of pulmonary spaces during development. The underlying cause of this malformation in this case is not known. (Photo courtesy of Disease ­Investigations, San Diego Zoo Global)

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Age-Related/Degenerative Degenerative joint disease is common in captive, aged bovids, giraffe, okapi, and hippopotamuses, and may be a significant factor in decisions to euthanize geriatric animals. Any joint may be involved, including the atlanto-occipital joint. Due to challenges in diagnosis, laminitis may be an underdiagnosed cause of lameness in captive nondomestic hoofstock. Laminitis with pedal bone rotation and protrusion of the third phalanx through the sole has been described in multiple species, including takin, eland, greater Malayan chevrotain, and giraffe (Wiedner et al., 2014). Advanced imaging of the limbs may aid in antemortem and postmortem evaluation of bony and soft tissue changes in the hooves; however, postmortem examination of parasagittal sections through the foot is often necessary to identify subclinical or mild cases of laminitis. Dental attrition and wear result in inadequate mastication and poor body condition in captive, geriatric bovids; malocclusion is a common cause of disease in captive and free-ranging ruminants, and in particular predisposes them to mixed bacterial infections and chronic bacterial alveoloar osteomyelitis (Knightly and Emily, 2003). Free-ranging North American thinhorn (Dall’s) and bighorn sheep have a high prevalence of dental disease, with a high rate of concomitant lumpy-jaw-type lesions (Hoefs and Bunch, 2001). Significant differences have been noted in the extent and severity of dental attrition in free-ranging and captive giraffe, with dietary differences resulting in the functional classification of free-ranging giraffe as browsers, and captive giraffe as grazers (Clauss et al., 2007). Cheek teeth of captive giraffe tend to have a rounded cusp, with only the first molar commonly having a blunted cusp. This contrasts with a predominance of sharp cusps on the cheek teeth of free-ranging giraffe. These differences suggest that traditional captive diets may have been overly abrasive. The resulting dental alterations have been further implicated as a contributing factor in giraffe acute mortality syndrome (see section, Metabolic). In hippos, canine teeth and incisors grow continuously, and there are several reports of canine tooth overgrowth and malocclusion in both pygmy and common hippopotamuses (Flacke et al., 2016).

Trauma Trauma is a common cause of death in captive nondomestic hoofstock. Trauma from conspecifics or other species sharing an exhibit can include blunt force fractures, bites, and gore wounds. Environmental trauma from running into fences is a potential cause of death for African antelope as well as giraffe. In these cases, healthy, well-fleshed animals are found dead at the base of fences. Gore wounds

can elicit significant internal hemorrhage and can be associated with pneumothorax, myocardial laceration, or gastrointestinal perforations. Frequently, there is surprisingly minimal external evidence of a perforating wound despite the presence of severe, fatal internal trauma. Neonatal trauma, typically inflicted by a parent, is a significant cause of death in captive pygmy and common hippopotamuses (Flacke et al., 2016).

Inflammatory Non-infectious Amyloidosis (Fig. 5.8) refers to group of diseases characterized by the accumulation of amyloid, an amorphous, hyaline, extracellular proteinaceous material, in various tissues. The condition is diagnosed relatively frequently in captive nondomestic hoofstock. Published reports include both wild and captive caprids, captive gazelles, and captive bongo (Fox and Sanderson, 2001; Hadlow and Jellison, 1962; Kingston et al., 1982; Linke et al., 1986; Rideout et al., 1989; Wessels et al., 2011; Woolf and Kradel, 1973), but amyloidosis has been diagnosed in many other species and presumably any member of Bovidae is susceptible. In cases where amyloid has been characterized in non-domestic bovids, only reactive systemic or secondary (AA) amyloidosis has been recognized. Clinical signs vary depending on the amyloid distribution, but animals are often emaciated, and there may be clinical evidence of renal or hepatic failure. Tissues most frequently involved in nondomestic Bovidae include liver, kidney, spleen, gastrointestinal tract (lamina propria and submucosa), adrenal glands (cortical interstitium), thyroid gland, exocrine pancreas, lymph nodes, salivary glands, and blood vessels in multiple sites (Rideout et al., 1989; Fox and Sanderson, 2001). Grossly, the liver may be firm and more prone to fracture and hemorrhage. Kidneys may be pale and waxy. If glomeruli are involved, the cortex may have a granular texture. Amyloid in the gastrointestinal tract may cause generalized or segmental, submucosal thickening; Johne’s disease is a differential for intestinal amyloidosis. With hematoxylin and eosin (HE) staining, amyloid is hyaline, pale eosinophilic, and often induces atrophy and loss of adjacent tissues. Amyloid in blood vessels causes mural thickening and sometimes reduced luminal diameter. In the liver, amyloid tends to be deposited initially in the space of Dissé and then extends along sinusoids, inducing hepatic cord atrophy. Renal amyloidosis in nondomestic bovids most often involves both medullary and glomerular deposition, sometimes also involving cortical interstitium and blood vessels. One exception is a case series of captive dorcas gazelles in which renal amyloidosis was exclusively medullary and glomeruli were spared (Rideout et al., 1989). When severe, renal amyloidosis may be accompanied by papillary or renal crest necrosis, presumably secondary

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FIGURE 5.8  Kidney in an adult bongo antelope with severe renal medullary and interstitial amyloidosis. (A) The cortical surface is uneven and there are streaks of pallor extending from medulla to cortex. (B) Amorphous, hyaline extracellular material has accumulated in both the medulla and interstitium, widely separating remaining collecting ducts and tubules, and replacing the normal interstitial tissue. There are patches of lymphoplasmacytic interstitial nephritis. (C) Arteries throughout the kidney and other tissues were disrupted by mural accumulation of amorphous, hyaline material. (D) AA amyloid in the renal interstitium and in blood vessels throughout the kidney. AA amyloid IHC. (Photos courtesy P. Gaffney, University of California, Davis)

to ischemia (Rideout et al., 1989). Renal tubular dilation and protein casts may also be present. Chronic tubulointerstitial nephropathy has been described in captive okapi housed in European and North American zoos (Benirschke, 1978; Haenichen et al., 2001). Histologic lesions include tubular atrophy, degeneration, and loss with interstitial fibrosis and mononuclear cell interstitial nephritis. There is thickening of tubular basement membranes, and hyaline and granular cast formation. Glomeruli are often also affected to a lesser degree, with thickening of Bowman’s capsule basal laminae, periglomerular fibrosis, and focal glomerular obsolescence. The character of the lesions suggests primary tubular insult, and although unproven, toxicosis from ingestion of plants such as willow (Salix spp.) has been suggested as a possible etiology. Multicentric vesicular and ulcerative dermatopathy has been described in captive common hippos (Helmick et al., 2007; Spriggs and Reeder, 2012). The gross lesions are erosive and ulcerative and may be widely distributed over the nonhaired skin, especially the axillary, inguinal, perineal, and limb regions; seasonality has been described

(Clyde et al., 1998). Microscopic changes include dermal edema, epidermal necrosis with individual keratinocyte necrosis, and neutrophilic dermal vasculitis with thrombosis. The etiopathogenesis has not been determined. In most cases, mixed bacteria have been cultured from the lesions, but a primary pathogen has not been identified. Clinical lesions respond to various combinations of increased water salinity, broad-spectrum antibiotics, and immunosuppression with pentoxifylline. Since 2000, proliferative and crusting skin lesions have been reported in free-ranging giraffe in multiple sites in Tanzania (Lee and Bond, 2016). Published investigations into this entity, referred to as giraffe skin disease, have been limited to prevalence studies and gross descriptions. Prevalence in Ruaha National Park in ­Tanzania may exceed 90% and is significantly higher in adults. Lesions are most frequent on the palmar aspects of the carpi, and are usually bilateral. Less commonly, lesions may be present on the skin of the brisket region, hindlimbs, or vulva; occasional lesions are present in distal forelimbs and hindlimbs. Early skin lesions consist

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of small nodules that coalesce to form 10–15 cm diameter plaques. Early superficial scaling leads to crusting and fissure formation. No etiology has been identified, though a parasitic etiology has been proposed. There may be an association with certain soil features (Lee and Bond, 2016). Abdominal and perirenal fat saponification and necrosis occur in nondomestic bovid species in zoos. Grossly, small to large, individual to coalescing masses of necrotic and mineralized fat may be present in the mesentery, retroperitoneum, or omentum. Masses may be yellow, hemorrhagic, or white, and are gritty on cut section. Histologically, lesions include necrosis and mineralization of adipocytes, sometimes accompanied by histiocytic and mixed steatitis. Rarely, osseous metaplasia and even extraskeletal osteosarcoma can occur. Secondary ureteral or gastrointestinal obstruction can occur, and the presence of masses in the pelvic canal can lead to dystocia (Rideout, 2012). Lesions can be spontaneous, especially in obese animals, but association with endophyte-infected fescue has been reported in cervids.

Miscellaneous Rectal prolapse and stenosis have been reported in captive okapi in the Netherlands and North America (Benirschke, 1978). This is often accompanied by dilation of the orad rectum and colon and accumulation of obstipative fecal material. Excessive grooming by dams with insertion of the elongated tongue into the rectum is a proposed etiology. This behavior can result in rectal erosion, ulceration, and eventual strictures. A variety of non-infectious factors have been associated with abortion, stillbirth or neonatal death. These include nutritional imbalances, immobilization, or anesthesia of pregnant dams; advanced maternal age; fetal malformations; algal toxins and toxic plants; trauma; twinning in some species; or hereditary/genetic causes (Rideout, 2012). Dystocia is relatively common in captive bovids, and may be related to maternal nutritional status, fetal malposition, or other causes. Fetal lesions after fatal dystocia often include nonspecific indicators of stress, such as external meconium staining and meconium and squamous cell aspiration in the lungs.

Neoplastic Neoplasia is uncommonly reported in this group. It has only recently been recognized as a threat to conservation in a few species (McAloose and Newton, 2009). Supplemental Table e5 presents a variety of neoplastic conditions described in these taxa. Paranasal sinus tumors occur in free-ranging bighorn sheep, and have been experimentally transmitted between

bighorn and domestic sheep (Fox et al., 2011, 2015). Grossly, tumors are white, shiny, soft to gelatinous cystic masses that fill the nasal sinuses and extend into the underlying bone, frontal or palatine sinus, or nasal turbinates. Sinus cavities may be filled with seromucinous exudate associated with coinfections by Pastuerellaceae spp. or Myocoplasma ovipneumoniae. Microscopically, there are proliferative epithelial and mesenchymal components, with malignant transformation of both tissue types. Most tumors are composed of well-differentiated spindle to stellate cells and loose edematous, myxomatous, or dense fibroplastic stroma; bone production is a prominent feature in some cases. Variable hyperplasia of pseudostratified ciliated respiratory epithelium, submucosal serous glands, and mucous glands is present. Masses frequently contain deep submucosal sheets and nests of well-differentiated acini and large cystic structures that are lined by epithelial cells and contain intraluminal PAS positive mucin. The predominating neoplastic spindle cell population is immunoreactive for vimentin, S100, alpha smooth muscle actin, and osteocalcin; a periosteal cell origin is suspected. Tumor transmission studies using cell-free filtered tumor preparations suggest a viral etiology. The predominance of the mesenchymal component in the tumors in bighorn sheep helps distinguish it from enzootic nasal adenocarcinoma in domestic sheep.

INFECTIOUS DISEASES DNA Viruses Malignant catarrhal fever (MCF) is a severe, often fatal systemic disease of artiodactyls caused by multiple gammaherpesviruses in the genus Macavirus. A key feature of the disease is virus transmission from a reservoir artiodactyl species in which infection is largely asymptomatic, to a susceptible artiodactyl species in which it causes significant morbidity and mortality (Miller and Fowler, 2015; O’Toole and Li, 2014). Of the 10 currently recognized Macavirus species, six are known to cause MCF. However, due to their significant impact on livestock production, ovine herpesvirus-2 (OvHV-2) and alcelaphine herpesvirus-1 (AlHV-1) are the best characterized (O’Toole and Li, 2014). Both of these viruses also cause diseases in nondomestic artiodactyls, as do AlHV-2, caprine herpesvirus-2 (CpHV-2), malignant catarrhal fever virus-white tailed deer (MCFV-WTD), and MCFV-Ibex. Molecular analyses have identified several additional Macavirus spp. and unclassified gammaherpesviruses in captive artiodactyls, a subset of which of have been associated with fatal malignant catarrhal fever-like disease in captive nondomestic Bovidae (Gasper et al., 2012). Classically, OvHV-2 and AlHV-1 present with distinct epidemiologic manifestations. Disease pathogenesis, clinical presentation, and lesions are very similar.

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OvHV-2 is ­ typically carried by asymptomatic domestic sheep. They transmit the virus to wildlife or other susceptible domestic ungulates causing infrequent epidemics of ­ “sheep-associated” MCF (SA-MCF). AlHV-1 is carried by asymptomatic wildebeest and causes “wildebeest-­ associated” MCF (WA-MCF). Most reports of WA-MCF involve transmission to domestic cattle in Africa where disease occurs annually during wildebeest calving season. Aerosol transmission occurs via dispersion of reproductive fluids or direct contact with nasal or ocular secretions from infected juvenile wildebeest. WA-MCF has also been recognized globally in cattle and exotic hoofstock species in zoological gardens and game reserves that house wildebeest. MCF virus transmission in zoological settings appears to be more frequently associated with aerosol transmission or direct exposure to asymptomatic carrier species, with sporadic outbreaks rather than seasonal disease. It is notable that MCF viruses are still being identified in nondomestic artiodactyls, and in some cases the host and target species may not have been previously associated with MCF. Following exposure, MCF viruses enter the body through oral cavity or tonsillar mucosae with subsequent viremia and infection and transformation of lymphoid cells. Transformation results in systemic lymphoproliferative disease manifested by functional and architectural disruption of the secondary lymphoid tissues, perivascular accumulation and proliferation of transformed lymphoid cells with subsequent vasculitis, and lymphoid invasion into mucosal or cutaneous tissues. The target lymphoid cells are incompletely characterized; however, cytotoxic CD8+ T lymphocytes and possibly natural killer cells likely contribute significantly to the disease. Lymphoproliferation and T-cell dysregulation appear to play a central role in disease development; the host and pathogen factors contributing to lymphoproliferation are poorly characterized.

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Experimentally, host tissue damage appears to be the result of cytotoxicity. In the case of SA-MCF, recent studies employing reverse-transcriptase PCR have identified viral gene transcripts that support the presence of both latent and replicating virus in lesions and in the respiratory tract of clinically unaffected sheep shedding OvHV-2. Several current hypotheses assert that latently infected CD8+ cells or progenitor T cells could induce growth dysregulation and activation, leading to uncontrolled, polyclonal cell proliferation (O’Toole and Li, 2014). Clinical signs and gross findings of MCF are variable but frequently include fever, severe mucopurulent nasal discharge, corneal opacity, diarrhea, lymphadenopathy, and neurologic disease. The classic distinctive features of MCF are (1) lymphocyte proliferation in tissues and lymph node paracortices (T-cell zones); (2) widespread mucosal necrosis; and (3) systemic necrotizing vasculitis with perivascular and intramural infiltration of large lymphocytes. The degree of each lesion varies depending on chronicity, species, and individual animal. This “classic” spectrum of lesions may not be present in nondomestic ruminants, especially if the causative agent is a virus other than AlHV-1 or OvHV-2 (O’Toole and Li, 2014) (Figs. 5.9 and 5.10). In bison infected with OvHV-2, disease progresses very rapidly and is characterized by prominent gastrointestinal mucosal necrosis and minimal lymph node hyperplasia. Contagious ecthyma, contagious pustular dermatitis, or orf is a highly contagious zoonotic disease caused by infection with orf virus (ORFV), genus Parapoxvirus. Orf occurs worldwide in domestic sheep and goats, and many nondomestic members of the subfamily Caprinae are susceptible including free-ranging bighorn sheep, thinhorn (Dall’s) sheep, mountain goats, captive and wild muskoxen, Sichuan takin, chamois, Himalayan tahr, and serow (Guo et al., 2004; Lance et al., 1981; Samuel et al., 1975; Suzuki

FIGURE 5.9  Ulcers in the oral mucosa of a bongo antelope with malignant catarrhal fever. (A) Early lesions result in the formation of numerous vesicles that may coalesce and rupture, or progress to extensive ulceration as in this image. (B) Liver from the same animal. Portal areas are expanded and disrupted by dense, predominantly lymphocytic infiltrate. A large, well-demarcated region of coagulative necrosis is present at the lower right. (Photos courtesy of Disease Investigations, San Diego Zoo Global)

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et al., 1986). In some cases, molecular testing may be necessary to distinguish ORFV lesions from Capripoxvirus lesions (see below). Isolated cases of parapoxvirus-associated disease have also been reported in noncaprid species, such as blackbuck, mountain gazelle, and steenbok, and it is likely that the host range is broad (Sharma et al., 2016). Experimental infection causes mild disease in pronghorn, though natural infection has not been reported (Lance et al., 1983). Outbreaks of contagious ecthyma occur in both captive and free-ranging populations, and higher morbidity rates

FIGURE 5.10  Lung from a yellow-backed duiker with malignant catarrhal fever. Lymphocytic vasculitis and perivascular infiltrate can be relatively mild compared to the more severe, classic lymphoproliferative lesions observed in domestic animals. (Photo courtesy of Disease Investigations, San Diego Zoo Global)

are associated with higher population densities. Young animals are usually most severely affected, and infection may be fatal if lesions interfere with feeding or lead to secondary infections. Infection most likely occurs through defects in skin or mucous membranes. Virus in sloughed skin crusts in the environment may be infectious for prolonged periods of time, and may be a source of indirect infection. ORFV is epitheliotropic and causes proliferative, necrotizing, and vesicular lesions on the skin and mucous membranes (Fig. 5.11). The muzzle, lips, and gingiva are most often involved, but lesions also occur on the tongue, periocular region, distal limbs, interdigital cleft, heel bulb, mammary gland, vulva, prepuce, and skin of the dorsum. Lesions progress from papules to flat vesicles to pustules that rupture and become covered by very thick crusts. Animals may become emaciated and secondary infections leading to cellulitis, stomatitis, aspiration pneumonia, or mastitis can occur. Histologically, orf is characterized by marked epidermal proliferation, swelling of cells in the stratum spinosum, intraepidermal vesicles and pustules, and dense superficial crusting. One or more, intracytoplasmic, eosinophilic viral inclusion bodies may be present. Dermal lesions include edema and neutrophilic and mixed superficial inflammation. Differentials for orf lesions include other parapoxviruses, such as bovine popular stomatitis virus and pseudocowpoxvirus. Viruses in the genus Capripoxvirus cause sheep pox and goat pox in small ruminants, and lumpy skin disease (LSD) in cattle. These viruses are serologically cross-reactive but have differing, minimally-overlapping geographic distribution. There are no reports of sheep or goat pox in nondomestic ruminants. LSD in cattle is an OIE listed, reportable ­disease caused by lumpy skin disease virus, LSDV. The

FIGURE 5.11  Proliferative and necrotizing lesions on the muzzle of a thinhorn (Dall’s) sheep infected with orf parapoxvirus. (A) Epithelial hyperplasia with degeneration and necrosis. Infections of this severity can inhibit eating and serve as a portal for secondary infections. (B) Degenerating subcorneal epithelial cells within the center of the image exhibit vacuolar degeneration and contain eosinophilic intracytoplasmic inclusion bodies characteristic of parapoxvirus infection. (Photos courtesy of University of Illionois, Zoological Pathology Program)

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virus is found in much of Africa and has recently also been identified in the Middle East, Turkey, Greece, Russia, and the Republic of Georgia (OIE, 2017). Unconfirmed LSD was reported in Arabian oryx in Saudi Arabia, but a broad serosurvey of African wildlife revealed a low seroprevalence in impala, giraffe, kudu, waterbuck, reedbuck, and springbok (Hedger and Hamblin, 1983). Experimental infection of giraffe and impala calves resulted in fatal, systemic disease with proliferative and necrotizing dermatitis and panniculitis similar to classical LSD in cattle; African buffalo calves and adult wildebeest were not affected (Young et al., 1970). Gross lesions in the giraffe and impala included widespread dermal nodules up to 10 cm in diameter that turned black and ruptured with the release of serosanguinous fluid. The disease progressed over several weeks to include diffuse lymphadenopathy, multifocal mucosal and lingual ulceration and necrosis leading to anorexia, severe weight loss, and death. Microscopic lesions in the skin were predominantly characterized by epidermal proliferation and vacuolar degeneration and necrosis with chronic neutrophilic panniculitis and myositis, and varying degrees of acute and chronic dermal vasculitis. Epithelial cells in and around the lesions contained intracytoplasmic inclusion bodies, and intranuclear inclusion bodies were present within affected skeletal myofibers or stromal support cells. Macrophages within the lesions contained both intracytoplasmic and intranuclear inclusion bodies. Additional lesions included necrotizing esophagitis, necrotizing lymphadenitis, mild multifocal acute hepatocellular necrosis, and suppurative bronchopneumonia. A small number of papillomaviruses, including bovine papillomavirus 1 (BPV 1) and BPV 2 have been shown to cross species and cause significant lesions in other hosts. Papillomavirus infection in bovids typically causes proliferative epithelial lesions and benign neoplasms in the skin and mucous membranes of the gastrointestinal and urinary tracts. Tumors are classified, based on the proportion of epithelial and mesenchymal components, as papillomas, fibropapillomas, or fibromas. Many benign papillomavirusinduced lesions regress spontaneously, but malignant transformation can occur in response to incompletely understood, host and environmental conditions (Sundberg et al., 2001). Grossly, typical papillomas are often exophytic, 1–2 cm diameter, hyperkeratotic, verrucous nodules that may be pigmented or nonpigmented, and single or multiple. Histologically, they are characterized by hyperplasia of keratinocytes in the strata spinosum and granulosum and are accompanied by cell swelling and cytoplasmic pallor (koilocytes); orthokeratotic and parakeratotic hyperkeratosis; prominent, eosinophilic, cytoplasmic granules; and occasional amphophilic, intranuclear viral inclusion bodies. Fibropapillomas contain a much greater mesenchymal component and are covered by variably hyperplastic and hyperkeratotic epithelium that typically extends thin rete pegs into the under-

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lying tissue. The mesenchymal component is composed of fibroblastic cells arranged in bundles, whorls, or storiform patterns; cells may be well differentiated or anaplastic. The epithelium may be unremarkable or ulcerated, in which case the tumor must be differentiated from other tumors of the dermis and from granulation tissue. Typical viral cutaneous papillomas and fibropapillomas have been reported in nondomestic bovids, giraffe, and pronghorn antelope (Sundberg et al., 1983, 2001; Williams et al., 2011). In most of these reports, a papillomaviral etiology is supported by electron microscopy or immunohistochemistry, but complete phylogenetic viral characterization has not been performed. Various bovine papillomaviruses have been detected in skin and mucous membranes of clinically healthy chamois and mouflon (Savini et al., 2016), which demonstrates that infection is not always associated with disease. A novel papillomavirus was identified in a large, nasolabial tumor in an alpine Chamois (Mengual-Chuliá et al., 2014). The tumor was composed predominantly of hyperplastic, parakeratotic, and dyskeratotic epithelium, and it was histologically benign but had grown sufficiently large to completely obstruct one naris and partially obstruct the other. The novel virus, Rupicapra r. rupicapra papillomavirus 1 (RrupPV1) is most closely related to a papillomavirus associated with squamous cell carcinoma in domestic sheep (OaPV3). Equine sarcoidlike fibropapillomatous disease associated with BPV-1 and BPV-2 has been reported in a sable antelope and two giraffe in South Africa (van Dyk et al., 2011; Williams et al., 2011). Giraffe in Kruger National Park had coalescent, verrucous to nodular masses variably involving large proportions of the trunk, neck, head, and/or limbs (Fig. 5.12). Histologically, epidermal changes typical of papillomaviral infection included marked acanthosis, orthokeratotic hyperkeratosis, and koilocytes in one case. In both cases, the dermis was

FIGURE 5.12  Free-ranging giraffe with disseminated fibropapillomatosis associated with bovine papillomavirus (BPV) infection. The lesions resemble equine sarcoids. Grossly, there are multiple, coalescent, verrucous to nodular cutaneous masses involving much of the neck. Lesions variably affect the dorsum, base of tail, and legs. (Photo courtesy of R. Bengis)

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FIGURE 5.13  Sable antelope with cutaneous fibropapilloma associated with bovine papillomavirus infection. The superficial dermis is replaced by moderately pleomorphic, fibroblastic cells arranged in whorls, and bundles. Epidermal changes include mild acanthosis and orthokeratotic hyperkeratosis.

replaced by a population of variably pleomorphic, fibroblast-type cells that displaced adnexa. The sable antelope had smaller, focal nodular lesions on the distal right hind limb, right shoulder, and lip; the limb mass recurred after excision. The dermis was replaced by fibroblastic cells arranged in whorls and bundles, and the epidermis was only moderately hyperplastic, contained few koilocytes, and was multifocally ulcerated (Fig. 5.13).

RNA Viruses Bluetongue virus (BTV) causes bluetongue (BT), a vector-borne hemorrhagic fever of ruminants, particularly sheep. Biting midges (Culicoides sp.) act as biological vectors in tropical and temperate areas worldwide. Vertical and oral transmission can also occur but are not considered to be important for the epidemiology of the virus. There are currently at least 26 recognized BTV serotypes with considerable genetic variation among naturally occurring strains within each serotype (Maclachlan et al., 2015). The virus is endemic throughout tropical and subtropical regions. In the last decade, there have also been numerous virus incursions into Northern Europe (Maclachlan et al., 2015). The severity of disease varies significantly with virus serotype and strain, host species, and breed (Maclachlan et al., 2009). For example, the strain of BTV-8 that emerged in northern Europe in 2006 is particularly pathogenic in multiple species, and is associated with increased rates of transplacental infection compared to most wild-type field strains. The disease is most severe in domestic sheep, with similar but more subtle lesions in cattle and nondomestic ruminants (Maclachlan et al., 2009). A survey of zoos conducted during the BTV-8 Europe outbreak revealed significant disease in American bison, European bison, yak, mouflon, alpine ibex, Siberian ibex, and muskoxen

(Sanderson, 2012). Large outbreaks of BT have also been reported in pronghorn in North America (Thorne et al., 1988). Bluetongue disease is characterized by widespread vascular injury, with the most significant lesions in the upper gastrointestinal tract, lungs, and skin. Clinically, animals are febrile, with erosions and ulcers in oral mucosa, muzzle, and teats; conjunctivitis; serous, mucous, or hemorrhagic nasal discharge; edema of the head and limbs; and, in some cases, hyperemia of the coronary band. This spectrum of lesions is not consistently present; some animals may exhibit only lameness, and in some cases sudden death may occur with no other signs (Sanderson et al., 2008). Cyanosis and edema of the lips and tongue (from which the disease gets its name) are uncommon but have been observed in captive yak (Mauroy et al., 2008). Pulmonary edema can be severe and develop late in the disease. Grossly, there may be pleural and pericardial effusion and hemorrhage in multiple sites including upper gastrointestinal serosa and mucosa, lymph nodes, subcutis, and the subintima of the pulmonary artery. Acute hemorrhagic enteritis is reported in captive yaks dying from BT. Histologic lesions are compatible with gross findings, and there may be acute to chronic myocardial and skeletal muscle necrosis and hemorrhage. Smallvessel changes may be mild, consisting only of endothelial cell hypertrophy, but there may also be lesions compatible with disseminated intravascular coagulation (Maclachlan et al., 2009). Prior to the emergence of the BTV-8 strain affecting northern Europe in 2006, transplacental transmission of BTV was uncommon in natural infections (Maclachlan et al., 2009, 2015). Infected pregnant animals may abort, and fetuses infected early in gestation may be born with congenital defects including hydranencephaly. Epizootic hemorrhagic disease virus (EHDV), like BTV, is a Culicoides-vectored orbivirus capable of infecting and causing hemorrhagic fever in domestic and wild ruminants. EHDV is an especially significant disease in cervids but disease is also reported in cattle, and sporadic outbreaks have been reported in other species, such as bighorn sheep and yak (Noon et al., 2002). Lesions are described in Cervidae (see Chapter 6). Foot and mouth disease (FMD) is a highly contagious disease of artiodactyls. FMD is characterized by high morbidity but low mortality in susceptible species. FMD is an OIE listed, reportable disease that is endemic in large regions of Africa, Asia, and South America. Its importance lies in the economic implications of production losses in infected livestock, and in the significant trade restrictions imposed when foot and mouth disease virus (FMDV) is present. Conservation activities, such as translocation and reintroduction programs, can be severely limited by FMDV detection in species of concern. There are seven FMDV serotypes (O, A, C, SAT 1, SAT 2, SAT 3, and Asia 1), and infection with one serotype does not confer immunity to another. Each serotype

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contains several antigenic subtypes or strains that can vary considerably in virulence. Numerous case reports describing both natural and experimental infection in nondomestic artiodactyl species have been reviewed and summarized (Arzt et al., 2011a; Hedger and Hamblin, 1983; Pinto, 2004; Schaftenaar, 2002; Weaver et al., 2013). In regions of the world outside of sub-Saharan Africa, infection of captive and free-ranging wildlife with FMDV tends to coincide with FMD outbreaks in domestic animals, with virus typically spreading from livestock to wildlife (Thomson et al., 2003). In sub-Saharan Africa, the African buffalo is the only nondomestic species conclusively shown to transmit virus and exhibit a prolonged carrier state, playing a role in the maintenance and spread of disease. In South Africa, for example, numerous unrelated outbreaks of FMD have been documented in Kruger National Park, where routine surveillance has been in place since the 1960s. There, most outbreaks of clinical FMD have occurred in impala, and viral sequencing has demonstrated that the source is often African buffalo. Reserve perimeter fencing and livestock vaccination are used frequently to prevent spread between wildlife (primarily buffalo) and livestock. The pathogenesis of FMD is reviewed in Alexandersen et al. (2003); Arzt et al. (2011a) (cattle); and Arzt et al. (2011b). FMDV may be transmitted via direct contact with body secretions or vesicular fluid of infected animals, via aerosol, or via contaminated fomites. Long distance airborne spread can occur under appropriate environmental conditions. Primary replication occurs in pharyngeal epithelial cells, particularly in the follicle-associated epithelium of the mucosa-associated lymphoid tissue, and in pulmonary alveolar epithelium. Primary replication can also take place at the portal of entry and in regional lymph nodes if infection occurs via skin abrasion. Viremia then leads to widespread surface epithelial dissemination, and lesions develop in areas of mechanical or physiologic stress. The incubation period can be as short as 1–2 days, ranging up to 2 weeks. Early gross lesions consist of mucosal or epidermal swelling, blanching, or reddening. Vesicles can occur in the oral cavity, especially the dental pad and tongue; coronary band and interdigital region; and mammary gland. Lesions are also apparent in the forestomachs, particularly rumenal pillars, on postmortem exam. Histologically, epidermal and mucosal vesicles begin in the stratum spinosum as epithelial degeneration and necrosis, ballooning degeneration, and intercellular edema. These regions progress to form fluidfilled spaces whose surfaces often slough to form erosions. Vesicles can be very large, and vesicle fluid harbors large quantities of virus. In young animals, the virus can be myotropic, leading to myocardial degeneration, necrosis, myocarditis, and sudden death. Nondomestic bovid species in which significant FMDassociated disease has been documented include mountain gazelles, impala, saiga, and blackbuck. Outbreaks in

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free-ranging mountain gazelles in Israel have coincided with disease in livestock, with gazelle mortality rates of 10%–50% of the population in reserves. Clinical signs and gross lesions in nondomestic species are similar to those in domestic livestock. Affected animals are often lame, may display arched backs, shake their feet, and lag behind the herd. Piloerection has been reported in impala, presumably reflecting fever, and hoof wall defects may be present for several months in recovered animals. Gross findings include vesicles that progress to erosions and ulcers on the mouth and feet, especially affecting the dental pad and oral mucosa; coronitis; and, pale streaking of the myocardium. During outbreaks in mountain gazelles, in addition to vesicles, gross lesions include sloughing of horns and degeneration and necrosis in both cardiac and skeletal muscle. Pancreatic necrosis and pancreatitis are also described in natural outbreaks and experimental infections in mountain gazelles, and in experimentally infected pronghorn antelope. Infection in African buffalo is usually subclinical, though typical clinical cases with oral vesicles and ulcers have been reported. There have been no documented FMDV infections in the common hippopotamus and a serosurvey in an endemic FMDV region (Kruger National Park, South Africa) detected no evidence of exposure in this species. Differentials for the gross lesions of FMD in wild artiodactyl species include the relevant vesicular viral diseases vesicular stomatitis, swine vesicular disease, and vesicular exanthema in suids. Other etiologies of mucosal and cutaneous ulceration must also be considered, including bluetongue virus, epizootic hemorrhagic disease virus, malignant catarrhal fever virus, mucosal disease/BVDV, photosensitization, and exposure to irritant or caustic chemicals. As FMD is an OIE listed disease, diagnosis of suspect cases should be referred to the relevant regulatory authorities. Assays including virus isolation, detection of viral antigen by ELISA, and identification of viral nucleic acid by reverse-transcriptase PCR can be performed at accredited laboratories. Death due to encephalomyocarditis virus (ECMV) infection has been documented in multiple species in zoological settings, including pygmy hippopotamuses, Thomson’s gazelle, and an oryx-addax cross (Reddacliff et al., 1997; Wells et al., 1989). Outbreaks of ECMV infection tend to occur across multiple mammalian taxa and are associated with sudden death. Lesions of acute to subacute, necrotizing to nonsuppurative myocarditis are present, sometimes accompanied by pericardial effusion, pulmonary edema, or other signs of acute heart failure. Myocardium is the most useful tissue for laboratory confirmation via virus isolation or PCR. Rodent control is critical for management in zoo settings. A novel border disease virus (BDV-4) has been associated with mass mortality events in wild chamois since 2001 (Arnal et al., 2004; Frolich et al., 2005). In contrast to BDV

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infection in domestic sheep, natural, postnatal BDV infection in chamois is usually associated with a high mortality rate, though some populations appear to be resistant to disease (Marco et al., 2015). Persistent infection with BDV has not been definitively documented in chamois, though vertical transmission has been confirmed experimentally (Cabezon et al., 2010). Clinically, affected animals exhibit depression and decreased flight distance, or are found dead. Gross lesions include emaciation, patchy to widespread alopecia, and epidermal hyperpigmentation (Marco et al., 2007). Secondary bacterial infections, including pneumonia and subcutaneous abscesses, may also be present. Microscopic lesions are most consistent in the brain, and include spongiosis, perivascular edema, neuronal degeneration and necrosis, glial nodules, and mononuclear perivascular cuffing. Microscopic skin lesions include follicular atrophy, excessive tricholemmal keratin deposition (flame follicles), telogenization of follicles, acanthosis, melanosis, and orthokeratotic hyperkeratosis. Other reported lesions include lymph node cortical necrosis and histiocytosis. Pestiviral antigen may be present in splenic and lymph node macrophages; epithelial cells of skin, kidney, or rumen; and in cells in the brain and bone marrow. Diagnosis of BDV in chamois can be confirmed via RT-PCR, virus isolation, antigen-capture ELISA, or virus neutralization tests. Peste des petits ruminants (PPR) is an OIE listed, reportable disease that primarily affects domestic goats and sheep. Significant clinical disease and mortality have been reported in nondomestic caprids (bharal, Barbary sheep, Nubian ibex, Afghan markhor), several gazelle species (Gazella sp., Dorcas gazelle, Thomson’s gazelle, springbok), as well as impala, gemsbok, and bushbuck (Abu-Elzein et al., 1990; Furley et al., 1987; Kinne et al., 2010). A recent outbreak of PRR in early 2017 among critically endangered Mongolian saiga resulted in catastrophic losses; the magnitude of the outbreak may have been influenced by the immunologically naive status of the population. Serologic evidence of exposure has been documented in several other species, including freeranging Grant’s gazelle, wildebeest, and impala in Tanzania (Mahapatra et al., 2015). Spillover from domestic sheep and goats is an important source of virus for nondomestic ruminants. PPRV is closely related to rinderpest virus, and the two morbilliviruses share common antigenic determinants. PPR is an acute disease, with an incubation period of 3–10 days (OIE, 2013a). Animals are febrile with serous to mucopurulent oculonasal discharge, and often have pneumonia and hemorrhagic diarrhea. Gross lesions include oropharyngeal erosion, ulceration, and pseudomembrane formation, but the typical oral lesions of goats and sheep may be absent in nondomestic species. Gastrointestinal lesions can include esophageal pseudomembrane formation, hemorrhagic colitis, and hemorrhagic enteritis. There

is severe lymphoid necrosis that is often evident in the gutassociated lymphoid tissue (GALT), with associated intestinal mucosal ulceration in regions overlying Peyer’s patches. Fibrinous peritonitis has been reported in gazelles. In gazelles dying peracutely of PPR, lesions may be limited to abomasal ulcers. In contrast to rinderpest (see below), PPR also involves the respiratory tract. Gross lesions include fibrinonecrotizing tracheitis, fibrinous pleuritis, and cranioventral lung consolidation. Histologically, lesions can include lymphocytolysis and lymphoid depletion in GALT, lymph nodes, and spleen; necrotizing and ulcerative enterocolitis; oropharyngeal necrosis and ulceration; random acute hepatic necrosis; and bronchointerstitial pneumonia. Microscopic lung lesions include necrosis of large and small airway epithelium, type II pneumocyte hyperplasia, and alveolar epithelial syncytial cells. Syncytial cells may be present in other sites including oral mucosa, liver, and lymphoid tissue. Eosinophilic, intranuclear, and intracytoplasmic viral inclusion bodies may be found in syncytia, in epithelial cells in affected tissues, and in monocyte-macrophage lineage cells in lymphoid tissues. Laboratory confirmation of PPRV infection can be achieved through competitive ELISA, immunocapture ELISA, PCR, or virus isolation. Virus neutralization tests are considered to be the gold standard but are time consuming. PPRV will cross-react with rinderpest virus in agar gel immunodiffusion and complement fixation tests. Depending on lesion distribution, differentials include caprine pleuropneumonia, pasteurellosis, bluetongue, bovine viral diarrhea, and foot and mouth disease. Immunosuppression due to lymphoid depletion can lead to secondary infections that can complicate the diagnosis. Rinderpest, a morbillivirus closely related to PPRV, was declared to be globally eradicated in 2011 (FAO and OIE, 2011). Rinderpest was a severe and highly fatal disease of cattle, with a potentially wide host range in other artiodactyls (Scott, 1981). Confirmed outbreaks of rinderpest were documented in several wild bovid species, though clinical disease and pathologic lesions are best described in the highly susceptible African buffalo, lesser and greater kudu, and common eland (Barrett and Rossiter, 1999; Kock et al., 1999a,b). Clinically, animals may have diarrhea, oculonasal discharge, and blindness. Gross lesions are similar to PPR with less involvement of the respiratory system. Mucosal erosion and ulceration may be present anywhere in the gastrointestinal tract, with frequent involvement of the oropharynx, abomasum, and colon. Linear submucosal congestion and hemorrhage along the longitudinal folds of the colonic and cecal mucosa (tiger striping) are frequently cited, though this is a nonspecific finding. Lymph nodes are edematous and hemorrhagic, and there is necrosis of Peyer’s patches with ulceration of the overlying intestinal mucosa. Necrosis, congestion, and inflammation may also be present in the urogenital tract. Ocular lesions in some

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wild bovids and giraffe tend to be more pronounced than in domestic cattle, and include corneal opacity due to keratoconjunctivitis and corneal ulceration, uveitis, and cataract formation (Rossiter et al., 2001). Dermatitis and plaque-like hyperkeratosis are described in African buffalo, and swollen joints and tenosynovitis in lesser kudu, though these lesions may reflect secondary infection. Histologically, lesions include mucosal epithelial cell necrosis, erosion, and ulceration; lymphocytic to mixed-cellular enterocolitis; and necrosis of liver, spleen, renal tubules, and salivary or bile ducts. Syncytial cells with or without nuclear and cytoplasmic inclusion bodies may be present in affected mucosal epithelium and lymphoid tissue.

Bacteria Mycobacteria are nonmotile, nonspore-forming coccobacilli that are Gram-positive but resist Gram staining due to their cell wall lipid component. They are positive with acidfast stains, such as Ziehl-Neelsen, though in some cases modified acid fast stains such as Fite-Furaco may be more sensitive. Bovine tuberculosis (BTB), caused by Mycobacterium bovis, is an OIE listed, reportable, zoonotic disease with potentially significant impacts on trade, wildlife conservation, and human public health (Fig. 5.14). It is found worldwide in domestic cattle, but can also affect wild and captive nondomestic ruminants, and other wildlife species (Lisle et al., 2002). M. caprae, a recently defined species in the M. tuberculosis complex, has caused similar disease in Europe and can be diagnosed using the same tests (OIE, 2015). Sporadic cases of infection with M. tuberculosis have also been reported in several species of nondomestic bovids as well as giraffe, and lesions may be indistinguishable from BTB. Antemorem diagnosis in nondomestic

FIGURE 5.14  Necrogranuloma in a nyala with bovine tuberculosis caused by infection with Mycobacterium bovis. A region of central liquefactive necrosis is surrounded by regions of caseous necrosis. These may be encircled by a fibrous capsule.

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ruminants, especially for screening of clinically healthy animals, can be challenging because the classic intradermal tuberculin test lacks sensitivity and specificity. Several direct and indirect diagnostic tests have been recently developed (Lecu and Ball, 2011). Clinical cases of BTB have become less common in cattle since the development of eradication programs in many countries, and regulatory attention has focused increasingly on wildlife (OIE, 2015). Globally, the management of M. bovis at the wildlife—domestic animal interface is challenging, complex, and sometimes controversial. While many species are susceptible to infection, only a proportion can act as maintenance hosts capable of transmitting disease. Other than domestic cattle, reported BTB reservoirs include certain wild ruminants, such as the African buffalo (South Africa), lechwe (Zambia), wood bison (Canada), and white-tailed deer (United States) (Michel et al., 2006; Nishi et al., 2006). Greater kudu may act as maintenance hosts at high population densities, but are often considered spillover hosts. The presence of M. bovis in a population can limit wildlife translocations or reintroduction programs, having conservation effects that extend beyond direct impacts of disease on mortality or reproduction rates (Wobeser, 2009). Chronicity and severity of disease and characteristics of lesions depend on infectious dose, type of immune response by the host, and the tissue inoculated. Lesions may be rare and require a painstaking search in subclinical cases where BTB is suspected. African buffalo, which act as reservoir hosts, may maintain subclinical infections for several years prior to manifesting clinical signs that include weight loss, cough, and dull coat (Renwick et al., 2007). Lesions are similar to those in cattle, with respiratory transmission and classic, encapsulated granulomas in the lungs and lymph nodes of the thorax and head, particularly mediastinal and retropharyngeal (Fig. 5.14). BTB in lechwe tends to affect the respiratory system most often, with lesions reported in the mesenteric lymph nodes in some cases. Both captive and free-ranging greater kudu exhibit swelling in the parotid and submandibular areas, often with draining fistulae; this lesion has been described as “almost pathognomonic.” Hematogenous dissemination can occur in many species. Histologically, granulomas have a central region of necrotic cellular debris or caseous material, surrounded by a layer of activated, epithelioid macrophages and multinucleated giant cells. The outer rim often contains lymphocytes and a collagenous capsule, depending on species and chronicity. Acid-fast bacilli may be present in low numbers, so definitive diagnosis may require culture of lesion-containing tissue in appropriate media. PCR on tissue is also available but sensitivity will depend on the number of bacilli in the sample. Infection with Mycobacterium avium subsp. paratuberculosis (MAP) causes paratuberculosis or Johne’s

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FIGURE 5.15  Granulomatous inflammation within the intestinal mucosa of a transcaspian urial with Johne’s disease caused by infection with Mycobacterium avium sup sp. paratuberculosis. (A) The mucosal lamina propria is severely expanded by sheets of epithelioid macrophages which separate and replace the crypts, and there is blunting and fusion of villi. Inflammation is also present below the muscularis mucosa. (B) Macrophages and multinucleated cells contain clusters of red-staining, acid-fast bacilli consistent with mycobacteria, Ziehl-Neelson. (Photos courtesy of Disease Investigations, San Diego Zoo Global)

disease. Johne’s disease is characterized by chronic, granulomatous enteritis and progressive wasting that principally affect ruminants, though infection with or without disease is reported in several nonruminant species. Johne’s disease is documented in a wide range of captive and free-ranging, nondomestic ruminant species (Carta et al., 2013; Lecu and Ball, 2011; Manning and Sleeman, 2012; Witte et al., 2009). Johne’s disease and the presence of MAP infection in a herd can impede animal transfers between institutions. This can have important implications for captive breeding efforts in support of endangered or threatened species. The epidemiology of MAP in captive ruminants is assumed to be similar to that observed in domestic cattle and sheep. Fecal–oral transmission is the primary route of infection, and young calves or lambs are much more susceptible than adults. In utero infection and neonatal exposure via milk or colostrum are also possible (Whittington and Windsor, 2009). In clinically affected animals, signs include chronic wasting and diarrhea, but the latter may be intermittent. Submandibular or generalized edema and effusion may be present in hypoproteinemic animals (Williams et al., 1983), and there may be serous atrophy of fat. Gross lesions in advanced cases include intestinal mucosal thickening, particularly distal small intestine, mesenteric lymphadenomegaly, and mesenteric lymphangitis. In nondomestic ruminants, lesions may be mild relative to classic Johne’s disease in cattle, and in early cases there may be few gross changes (Fig. 5.15). Diagnosis of MAP infection in nondomestic ruminants depends on the stage of infection. Fecal culture using specialized mycobactin-supplemented media is generally considered to be the gold standard for diagnosis of MAP

infection in live animals. Fecal culture is reported to have specificity approaching 100%; however, there may be a chance of false-positive results due to “pass-through” effect if an individual animal ingests large numbers of organisms from a contaminated environment (Sweeney et al., 1992). Though more sensitive than other antemortem tests, fecal culture may not identify all infected animals, especially in early stages where shedding may be minimal or intermittent (Nielsen and Toft, 2008). Microscopic lesions of Johne’s disease include granulomatous enteritis, colitis, lymphadenitis, and lymphangitis, with intracellular, acid-fast bacilli (Fig. 5.15). Two general forms of Johne’s disease are described in domestic sheep (tuberculoid or paucibacillary, and lepromatous or pleuribacillary), but lesions in nondomestic ruminants may not always fall clearly in to one category. The tuberculoid form is characterized by infiltrates of epithelioid macrophages, multinucleated giant cells, and lymphocytes, necrosis with or without mineralization, and often few positive bacteria on acid-fast stains (Williams and Barker, 2000). Similar lesions have been described in bighorn sheep, though in some cases acid-fast bacilli may be plentiful. The lepromatous form is characterized by a more diffuse lamina proprial infiltrate of epithelioid macrophages with numerous intracellular acid-fast bacilli. Both forms can be accompanied by villus blunting and fusion, wide separation of intestinal glands, and transmural inflammatory cell infiltrates. In early or mild cases, especially if paucibacillary, aggregates of epithelioid macrophages may be uncommon and small, and acid-fast staining and examination of multiple sections is required for diagnosis. Isolation of organisms from intestinal or lymph node tissue samples can provide a definitive diagnosis and may be more sensitive than histologic

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FIGURE 5.16  Necrohemorrhagic enteritis in a neonatal transcaspian urial infected with Clostridium perfringens type C. There is transmural necrosis and submucosal hemorrhage and edema. Ghosts of necrotic villi are lined by bacilli. Diagnosis must be confirmed by PCR to identify the toxin-producing genes, or by ELISA for the toxin, as C. perfringens is a normal inhabitant of gastrointestinal flora. (Photo courtesy of Disease Investigations, San Diego Zoo Global)

examination in early or mild cases. As with fecal culture, isolation from tissue samples requires specialized media and prolonged incubation time. A wide variety of nondomestic ruminants may be affected by enteric infection with one or more C. perfringens toxinotypes; however, significant disease is most frequently associated with type C, which causes hemorrhagic enteritis. C. perfringens type C is defined by the production of alpha and beta toxins. Lesions in neonatal nondomestic bovids are comparable to those described in domestic ruminants, and include mural acute necrotizing enteritis with ulceration and peritonitis. Diagnosis may be made based on the clinical history and clinical signs, and gross and histological findings with isolation of C. perfringens type C from jejunal lesions (Fig. 5.16). Toxin identification through ELISA, or identification of the toxin-producing genes, is required for definitive diagnosis, as C. perfringens is a normal inhabitant of gastrointestinal flora. C. perfringens type A has been implicated as the cause of fatal hemorrhagic enteritis in a neonatal hippopotamus. C. perfringens type A has also been associated with fatal cases of necrotizing and hemorrhagic enteritis in a variety of neonatal bovids. Malignant edema or gas gangrene is caused by C. septicum. Other clostridial species including C. novyi may produce similar disease. Most species of nondomestic Bovidae, Antilocapridae, Tragulidae, and Hippopotamidae are susceptible. Disease usually results from contamination of skin wounds. Clinical signs include sudden death, sometimes preceded by febrile disease. Gross findings include trauma involving muscle necrosis with or without crepitation. Microscopic findings are those typically observed in traumatic injuries, with significant necrosis, gas bubble formation, and the possible presence of large numbers of

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bacilli. Diagnosis is based upon clinical history, signs, and identification of bacteria within tissues. Confirmation is achieved through isolation of relevant Clostridium species from lesions, fluorescent antibody assay on tissue impressions, and bacterial culture. Blackleg or clostridial myositis is caused by Clostridium chauvoei. Blackleg is poorly characterized in animals other than domestic cattle. Most species of nondomestic Bovidae, Antilocapridae, and Tragulidae, may be susceptible; susceptibility in Hippopotamidae is not known. In wildlife, contamination of deep wounds has been suggested as a potential route of infection (Miller and Fowler, 2015). Clinical signs are poorly characterized in nondomestic species; however, they may include peracute death, or sudden onset of muscle stiffness, anorexia, and depression rapidly leading to death. Gross findings include significant regions of muscle necrosis and hemorrhage with or without crepitation. Ancillary diagnostics include culture, Gram stain, IHC, fluorescent antibody testing, and PCR. Anthrax is an OIE listed, reportable, zoonotic bacterial disease with worldwide distribution. It is primarily a disease of herbivores, though any mammalian species is potentially susceptible. Outbreaks occur sporadically in a diverse array of ecosystems and species. Ecological and epidemiological factors that contribute to outbreaks of disease in wildlife are reviewed elsewhere (Hugh-Jones and Vos, 2002). The causative agent, Bacillus anthracis, is a Gram-positive, spore forming, rod-shaped bacterium that gains entry to a host via skin or mucous membrane defects, ingestion, or inhalation. In acute cases, infection by spores is followed by rapid replication in regional lymph nodes, bacteremia, and toxemia. Massive elaboration of exotoxins leads to widespread, acute edema, hemorrhage, and terminal shock. Death may occur within hours in highly susceptible species. Carcasses often become bloated very quickly due to accelerated putrefaction, and they may exhibit petechial and ecchymotic hemorrhages and leak hemorrhagic fluid from body orifices If anthrax is suspected based on the appearance of the carcass, a blood smear from distal tail or ear (areas likely to be least autolyzed) should be examined. Bacilli have a characteristic clear capsule and blunt to squared ends where they join in pairs or chains in vivo (Bengis 2012; OIE, 2012a.). Necropsy should not be performed without appropriate personal protective equipment due to biosafety concerns. Gross lesions are those of septicemia, and include generalized edema, splenomegaly with a soft, gelatinous texture, and multicavitary effusions. Confirmation of the diagnosis typically relies on bacterial culture. Serology and molecular techniques are available but usually limited to research settings. Clinical samples and laboratory cultures of anthrax require biosafety level 3 facilities. Anthrax has been reported in numerous wild artiodactyl species, including wood bison in northern Alberta and Northwest Territories, Canada, and numerous African

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parks and game reserves. Greater kudu, nyala, waterbuck, and roan antelope are reportedly more susceptible than other species, such as the African buffalo, and consistently exhibit higher levels of bacteremia in outbreaks in Southern Africa. Mortality due to anthrax is also relatively high in hippopotamuses when compared to other species, and sporadic mass outbreaks occur in hippos in Uganda and Zambia (Hang’ombe et al., 2012; Turnbull et al., 1991). Facultative carnivorous behavior has been proposed as a contributing factor to increased mortality and large-scale outbreaks in hippos (Dudley et al., 2016). Hemorrhagic septicemia (HS) is an acute, epizootic, highly fatal disease of ruminants caused by infection with certain serotypes of Pasteurella multocida (OIE, 2012b). Hemorrhagic septicemia is an OIE listed and reportable disease that occurs in Asia, Africa, and the Middle East and has been reported in southern Europe and North America (Shivachandra et al., 2011). The disease is most common in water buffaloes and domestic cattle but has been reported in American bison, various cervid species (fallow deer, elk), pronghorn, and, most strikingly, in mass mortality events in saiga antelope in Kazakhstan (Kock et al., 2016). P. multocida is a common component of the normal nasopharyngeal flora of many ruminants, and usually acts as an opportunistic pathogen (for example, as a component of bighorn sheep pneumonia). However, in cases of hemorrhagic septicemia, serotypes B2, E2, or, occasionally, other serotypes of P. multocida can act as primary pathogens and cause rapidly fatal septicemia with case fatality rates approaching 100%. P. multocida has many virulence factors that likely play a role in the rapid progression of disease, though endotoxin may be the most significant. P. multocida serotype B was implicated in a catastrophic mortality event in free-ranging saiga antelope in Kazakhstan in 2015 in which more than 130,000 adults died over a period of less than 2 weeks (Kock et al., 2015). In this case, it is thought that an unidentified environmental trigger contributed to the shedding of bacteria from latently infected animals, leading to an unusually synchronous occurrence of disease within large herd. Hemorrhagic septicemia is typically a peracute to acute disease, and animals may be found dead or die less than 24 h after initial clinical signs. Clinically, there is fever, excessive salivation, dyspnea, recumbency, and sometimes diarrhea that may be hemorrhagic. Grossly, petechial and ecchymotic hemorrhages may be present in the subcutis, serosa, endocardium, lymph nodes, and muscle. In cases of longer duration, there may be prominent subcutaneous edema in the submandibular, cervical, and brisket regions. The lungs may be congested or consolidated, with fibrinous pleuritis or pneumonia and variably hemorrhagic effusions in body cavities. Histologically, lesions are those of septicemia, and include acute hemorrhagic gastroenteritis, fibrinohemorrhagic interstitial pneumonia, pulmonary edema, and randomly distributed foci of acute inflamma-

tion in multiple sites. Diagnosis may be suspected based on epidemiologic and postmortem findings, and on the presence in blood smears of Gram-negative, short bacilli that are bipolar staining with methylene blue. Confirmation of hemorrhagic septicemia requires culture of blood, heart swab, or bone marrow, followed by identification of capsular serotype (A, B, D, E, or F) and somatic type (1–16). Molecular techniques are also available to identify specific serotypes. Pneumonic pasteurellosis can be caused by infection by Gram-negative bacteria in the family Pasteurellaceae. P. multocida, Mannheimia hemolytica, and Bibersteinia trelahosi have been reported in nondomestic ruminants (Miller, 2001). Infection is usually opportunistic, and disease tends to occur in association with primary viral or mycoplasmal infections, trauma, or parasitic infections (Miller, 2001; see bighorn sheep pneumonia, later). Lesions include hemorrhagic to suppurative bronchopneumonia and fibrinous pleuritis. Contagious caprine pleuropneumonia (CCPP) and contagious bovine pleuropneumonia (CBPP) are OIE listed, reportable diseases caused by Mycoplasma sp. bacteria belonging to the “mycoides cluster” (OIE, 2014a). CCPP, caused by Mycoplasma capricolum subsp. capripneumoniae (Mccp), is a severe disease that exclusively affects the respiratory system. CCPP is primarily a disease of domestic goats, but mortality has also been reported in captive, nondomestic caprids (Nubian ibex, Laristan mouflon), gazelles (sand gazelles, gerenuk), an Arabian oryx in the Arabian Peninsula, free-ranging Tibetan antelope in China, and markhors in Tajikistan (Arif et al., 2007; Chaber et al., 2014; Nicholas et al., 2008; Ostrowski et al., 2011; Yu et al., 2013). CBPP, caused by Mycoplasma mycoides subsp. mycoides sc, is primarily a disease of bovids of genera Bos and Bubalas and has not been widely reported in nondomestic wildlife species. Lesions of the two diseases are similar, and include pleuropneumonia with a thick layer of pleural fibrin deposition and abundant, straw-colored pleural effusion. Lungs are often dark red to gray with lobular areas of consolidation and there may be a granular texture on cut section. Fibrinous pericarditis is often present. Pulmonary sequestra may form in chronic cases, and have been reported in gazelles with CCPP. Histologically, CCPP is an acute, serofibrinous to chronic fibrinonecrotic pleuropneumonia and interstitial pneumonia, with prominent edema and neutrophilic to lymphocytic interstitial and alveolar infiltrates. There may be thrombosis and vasculitis, and coagulative necrosis may be present. Differential diagnoses include Mannheimia hemolytica infection, PPR, or other mycoplasmas. Other organisms from the “mycoides” cluster can also cause similar disease (Fig. 5.17). Definitive diagnosis can be achieved using PCR. Culture requires enriched media and prolonged incubation time. Serologic testing is also available, though some cross-reactivity can occur with other Mycoplasma species, depending on the test.

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FIGURE 5.17  Fibrinous pleuropneumonia and epicarditis in a Vaal rhebok infected with a mycoides-cluster Mycoplasma sp. (A) There is consolidation of the ventral lung lobe and the pleural surface and surface of the heart are covered by a pale yellow fibrinous exudate. (B) The pleural surface and subpleural alveoli are obscured by a band of fibrin that entraps large numbers of neutrophils and cellular debris. The inflammation extends along interlobular septa to the right of the image. (Photos courtesy of Disease Investigations, San Diego Zoo Global)

Population-limiting, epizootic bronchopneumonia of bighorn sheep (bighorn sheep pneumonia) has been documented in North America since early in the 20th century. Primary etiology(ies) have long been debated. At varying times, lungworm infection (Protostrongylus sp.), Pasteurellaceae (Bibersteinia trelahosi, Mannheimia hemolytica, Pasteurella multocida), respiratory viruses (bovine parainfluenza-3, bovine respiratory syncytial virus), and Mycoplasma ovipneumoniae (Besser et al., 2013; Cassirer et al., 2013; Miller, 2001; Rudolph et al., 2007) have been proposed as underlying causes and/or contributing factors. Pasteurellaceae including leukotoxin-positive (ltk + ) M. hemolytica and B. trelahosi are often isolated from pneumonic bighorn sheep, and lesions compatible with ltkinduced leukocytolysis may be present (George et al., 2008; Wolfe et al., 2010; Wood et al., 2017). However, several recent studies have provided support for a primary role of M. ovipneumoniae (Besser et al., 2008, 2014). Epizootic bighorn sheep pneumonia has been linked to contact with domestic sheep (Besser et al., 2012; Cassirer et al., 2013) and occasionally other domestic ruminants including cattle (Wolfe et al., 2010). In a naive population, animals of all ages may be affected and mortality rates can be greater than 90%. Subsequently, disease may be maintained in a population and pneumonia-related mortality mainly occurs in lambs, with occasional outbreaks affecting adults. The disease is characterized by acute to chronic, fibrinous, suppurative, or necrotizing sinusitis and bronchopneumonia sometimes accompanied by pleuritis (Fig. 5.18). Ventral regions of lung are dark red, firm, and sink in formalin, and over half the lung area may be affected. Chronic lesions include abscess formation, bronchiectasis, and pleural adhesions. Histologically, lesions include acute fibrinous or necrotizing bronchopneumonia and pleuritis; acute hemorrhage; bronchiolar epithelial hyperplasia;

FIGURE 5.18  Severe pleuropneumonia in a bighorn sheep with “bighorn sheep pneumonia” (epizootic bronchopneumonia of bighorn sheep). (A) Fibrinosuppurative exudate covers the consolidated, middle and cranioventral lung. (Photo courtesy of Washington Animal Disease Diagnostic Laboratory). (B) Purulent material within the cornual diverticulum of the frontal sinus (visible when the horns are removed). Epizootic bronchopneumonia of bighorn sheep can be accompanied by sinusitis, tracheitis, rhinitis, and otitis. (Photo courtesy of Washington Animal Disease Diagnostic Laboratory)

l­ymphocyte cuffing around airways and extending into adjacent tissue; neutrophilic exudate in lumina of bronchioles, bronchi, and some alveoli; and alveolar histiocytosis. Bacterial colonies may be present. In some cases, there

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is necrosis of neutrophils and macrophages with formation of “oat cells” (necrotic neutrophils with a distinctive streaming hyperchromatic nuclei). Concomitant lesions can include tracheitis, rhinitis, sinusitis, and suppurative otitis media with osteomyelitis. Affected animals may also have concurrent but incidental lungworm infection. Outbreaks of infectious keratoconjunctivitis (IKC) have been described in alpine and Pyrenean chamois, ibex, other European caprinae (Arnal et al., 2013; Giacometti et al., 2002; Mayer et al., 1997), and in wild bighorn sheep in North America. In European species, Mycoplasma conjunctivae has been identified as a primary etiologic agent, though co- or secondary infection by other bacteria may be present (Giacometti et al., 2002). M. conjunctivae is transmitted readily through direct contact via ocular secretions and exudate, or indirectly by insects; aerosol transmission has also been documented. Lesions affect multiple animals in a herd. Histologically, there is mixed mononuclear conjunctival infiltrate. Over days to weeks, lesions progress to keratitis with mononuclear to neutrophilic, limbic and corneal infiltrates, edema, and neovascularization accompanied by conjunctival lymphofollicular hyperplasia. Corneal edema, erosion, ulceration, and stromal necrosis can progress to perforation in advanced cases, with anterior synechiae and staphyloma formation. Corneal fibrosis may be present in animals that survive. Death during outbreaks of IKC is usually secondary to blindness with lesions of trauma, predation, or emaciation (Arnal et al., 2013; Mayer et al., 1997). Laboratory confirmation of M. conjunctivae keratoconjunctivitis is through mycoplasma-specific culture techniques on conjunctival swabs, or by PCR. In an outbreak of IKC in bighorn sheep in North America, inclusions consistent with Chlamydia sp. were identified on histologic examination and Chlamydiaceae were confirmed by immunofluorescent antibody testing on conjunctival swabs (Meagher et al., 1992). Lesions were similar to those described in mycoplasma-associated IKC. Sporadically, other organisms, such as Moraxella ovis, Staphylococcus aureus, Corynebacterium sp., and Rickettsia conjunctivae are detected in cases of IKC. Brucellosis is a zoonotic disease caused by Gramnegative, intracellular bacteria in the genus Brucella. The primary Brucella species that cause disease in the nondomestic Bovidae, Giraffidae, Antilocapridae, and Hippopotamidae are B. abortus and B. suis, with fewer reports of B. melitensis (Godfroid et al., 2013). Experimental infection with B. ovis has been investigated in captive mouflon and bighorn sheep but natural infection has not been recognized in wild populations. All four of these Brucella species are recognized as notifiable pathogens listed by the OIE. B. abortus is recognized as a significant endemic pathogen in free-ranging American bison in the western United States and Canada, and in freeranging African buffalo in sub-Saharan Africa. B. abortus

has been isolated from a broad range of nondomestic bovid species. B. suis biovar four has been identified in muskoxen; B. mellitensis has been identified in free-ranging chamois, ibex, yaks, Sable antelope, and captive Arabian oryx. B. mellitensis has not been identified in free ranging wildlife in the United States. Reproductive lesions may include placental retention (as observed in bison), placentitis, and significant hemorrhage that may also involve the fetus. Intercotyledonary exudate or pericotyledonary inflammation may be observed, and fetal membranes may be edematous. Metritis and orchitis are commonly observed and can be accompanied by localized or widely disseminated acute and chronic abscesses. Abscesses may be liquefactive or caseating, and mineralization of affected tissues often progresses with chronicity. Focal and polyarthritis and tenosynovitis have also been reported. Microscopically, the most notable finding in the placenta is large numbers of Gram-negative, intracellular bacteria within chorionic trophoblasts. Lymphohistiocytic, necrotizing, or suppurative inflammation may also be evident. In aborted fetuses, mild to severe fibrinosuppurative bronchopneumonia and multisystemic hemorrhages may be prominent. Microscopic findings in adult animals reflect the subacute to chronic, suppurative inflammation and abscessation observed grossly in the reproductive tract or other organs. Large numbers of Gram-negative bacteria may be present within regions of necrosis and within macrophages in affected areas (Rhyan, 2013). Granulation tissue and fibrosis may be associated with chronic and mineralized lesions. Definitive diagnosis requires bacterial isolation or PCR in tissues or clinical samples (Godfroid et al., 2013). Regulatory agencies may also require specific laboratory testing including biotyping. Heartwater (cowdriosis) is an OIE listed, reportable disease caused by the tick-borne, obligate intracellular, Gram-negative rickettsial agent Erlichia ruminantium. Heartwater is endemic throughout sub-Saharan Africa, offshore African islands, and in some areas of the Caribbean (Allsopp, 2015). It is transmitted by ticks of the genus Amblyomma. Though the disease is less significant in wild ruminants, both natural and experimental infections have been demonstrated in several African ungulate species (Peter et al., 2002). Heartwater-associated mortality has been reported in naturally infected eland, springbok, steenbok, lechwe, and sitatunga. Individuals of several other species have been experimentally infected and may act as reservoirs without exhibiting significant disease (Peter et al., 1998, 1999). Coxiella burnetii is a Gram-negative, obligate intracellular bacterium that can cause reproductive losses in nondomestic ruminants. Coxiellosis or Q fever is an OIE listed, reportable zoonotic disease with a very low infectious dose in humans and suspected cases should be managed using appropriate biosecurity. Coxiella-associated placentitis, abortion, and stillbirth have been reported in several s­ pecies

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of captive Bovidae including waterbuck, sable antelope, dama gazelle, Cuvier’s gazelle, greater kudu, bongo, and giraffe (Clemente et al., 2008; Lloyd et al., 2010; Winkel et al., 2008). It is likely that most ruminants are susceptible to infection and disease. Disease in nondomestic ruminants is similar to that in cattle, sheep, and goats. Infection can result in late-gestation fetal losses or weak neonates. Fetal lesions are nonspecific and secondary to fetal distress; alveolar meconium aspiration and increased alveolar squamous cells may be present. Grossly, the placenta may be within normal limits, or there may be pale discoloration or mineralization of cotyledons. Histologically, there is usually widespread necrosis of cotyledonary villi and intercotyledonary trophoblasts, with accumulation of necrotic cell debris, fibrin, and neutrophils between villi (Fig. 5.19). Lymphoplasmacytic and neutrophilic infiltrates may be present in the interstitium. Trophoblasts contain finely granular, pale basophilic to gray aggregates of organisms that can distend the cytoplasm. Organisms can be stained using modified ZiehlNeelsen, Stamp, Gimenez, or Macchiavello stains. Chlamydiaceae are Gram-negative, obligate, intracellular bacteria that cause reproductive loss, infectious keratoconjunctivitis, and several other clinical syndromes in artiodactyls. Chlamydia (Chlamydophila) abortus is a common cause of placentitis and abortion in domestic sheep and goats, and is zoonotic. Though there are few confirmed case reports of Chlamydia-associated abortion in nondomestic ruminants, C. abortus DNA or anti-C. abortus antibodies have been detected in several free-ranging ungulate species (e.g., Holzwarth et al., 2011a, b; Salinas et al., 2009;

FIGURE 5.19  Placental villi from an Eastern white-bearded gnu with coxiellosis. There is multifocal villus necrosis with sloughing of the trophoblast layer. Individual trophoblasts contain dense granular colonies of intracytoplasmic bacteria. In some presentations, cellular debris and neutrophils fill the intervillus spaces. Important differential diagnoses include Brucella and Chlamydia spp. (Photo courtesy of Disease Investigations, San Diego Zoo Global)

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Pospischil et al., 2012). Given the potentially wide host range, C. abortus should be considered as a differential for fetal loss in nondomestic ruminants (Rideout, 2012) and appropriate biosecurity should be enacted in suspect cases. In domestic ruminants, vasculitis is described as a prominent feature of chlamydial placentitis that distinguishes it from coxiellosis, but this may not be relevant in nondomestic ruminants. Chlamydial organisms have been identified in lesions of IKC in bighorn sheep in North America, and in other species in Europe (see above). Other significant bacterial diseases that are less frequently reported in nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae are summarized in Supplemental Table e6 in the Supplemental Materials.

Fungi Fungal infections are sporadically reported in nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae. Disease most often occurs in individual animals, and outbreaks affecting herds are uncommon. Significant fungal diseases affecting captive and free-ranging species are summarized in Supplemental Table e7.

Metazoa Gastrointestinal nematodes may be clinically significant in captive settings, especially on permanent pasture or when naive animals are exposed to novel parasites through translocation or reintroduction programs. The presence of parasites does not necessarily imply disease, and other factors should be evaluated when assessing the significance for an individual animal or a population. A detailed inventory of gastrointestinal nematodes reported in free-ranging ruminants of North America is provided in Hoberg et al. (2001). The abomasal trichostrongyles are among the most important and common gastrointestinal parasites in the Giraffidae and nondomestic Bovidae. Haemonchosis is caused by infection with Haemonchus sp. nematodes, including H. contortus and H. placei. Larvae and adults are hematophagous, and heavy worm burdens are associated with significant anemia and hypoproteinemia. The life cycle is direct, and environmental parasite loads can build up rapidly on feces-contaminated pastures in warm, moist conditions, or where there is regular watering. Copper deficiency may predispose ruminants to gastrointestinal parasitism. A wide range of species is susceptible, including giraffe, nondomestic caprids (mouflon, Sudan Barbary sheep, transcaspian urial), and various antelope, sable, gazelle, hippotragid, and other species (Garretson et al., 2009). Grossly, mucous membranes, muscles, and viscera are pale and there may be subcutaneous or submandibular edema, hydrothorax, and ascites due to hypoproteinemia. Diarrhea is usually absent unless there is coinfection

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with other gastrointestinal helminths (Georgi et al., 1990). Abomasal contents may be hemorrhagic. Adult Haemonchus sp. females are 20–30 mm long and can be identified in abomasal contents by the “barber pole” appearance imparted by the white uterus spiraling around the bloodfilled gut (Georgi et al., 1990). Ostertagia ostertagi in cattle, Teladorsagia circumcincta in sheep, related nematodes of genera Teladorsagia, Marshallagia, Spiculopteragia, and Camelostrongylus in other nondomestic ruminants (Flach, 2008; Fowler, 1978; Goossens et al., 2005, 2006; Haigh et al., 2002; Kock, 1986; Kutz et al., 2004, 2012; Ortiz et al., 2001; Pauling et al., 2016; Sloan, 1965) can be the primary cause of an Ostertagiosislike syndrome (Uzal et al., 2016). Lesions of chronic abomasitis, glandular hyperplasia, and mucous metaplasia are due to larval development within abomasal glands. Grossly, the abomasal mucosa may be irregularly thickened by small nodules, each of which may contain small, protruding nematodes detectable if examined under magnification. Clinically, affected animals may be emaciated and hypoproteinemic, and abomasal pH may be elevated due to a loss of parietal cells in the metaplastic abomasal mucosa. Quantification of worm burden can be performed on abomasal contents. Adult and larval worms are small (<1.5 cm long) and brown, and may require magnification for detection. On histology, adults have longitudinal ridges visible in cross-section, and are smaller than the morphologically similar Haemonchus spp. Trichuris sp. nematodes, commonly called whipworms, infect the cecum and, less frequently, colon of ruminants and other species. Heavy infections in captive, nondomestic ruminants can cause mucohemorrhagic typhlocolitis and associated chronic diarrhea, hypoproteinemia, and poor body condition. Trichuris spp. are hematophagous, but anemia is a less important component of trichuriasis than inflammation and protein loss. Grossly, the intestine may contain hemorrhagic or blood-flecked contents, and there may be mucosal erosion or thickening. Worms are visible on the mucosal surface. Histologically, sections of anterior ends of adult nematodes may be found embedded in the mucosa, and there may be erosion, glandular hyperplasia, mixed inflammatory cell infiltrates, and superficial hemorrhage. Eleaophorosis is caused by infection with Elaeophora schneideri (superfamily Filarioidea, family Onchocercidae), the arterial nematode of mule deer and black-tailed deer in western North America (Anderson 2001). Infection is usually incidental in definitive mule- and black-tailed deer hosts, but in aberrant hosts, such as Barbary and bighorn sheep, E. schneideri can cause severe, ulcerative to crusting facial skin lesions, pneumonia, rhinitis, and meningomyelitis associated with the presence of degenerating microfilaria (Boyce et al., 1999; Pence and Gray, 1981). Skin lesions can be both necrotizing and proliferative, may be complicated by secondary infection, and should be differentiated from poxvirus infection (orf or contagious ecthyma). ­Histologically,

affected skin is infiltrated by mixed, eosinophilic to granulomatous inflammation, and microfilaria may be present within foci of necrosis. Lesions in lung and brain may be similarly associated with mixed inflammation, necrosis, and intact or degenerating microfilaria. Thrombosis and direct vascular damage may lead to ischemic necrosis. Adult nematodes up to 10 cm long are most often present in the carotid arteries but may be found in any large artery. Significant proliferative arterial intimal lesions are described in elk; arterial lesions in sheep appear to be less pronounced. Elaeophorosis caused by E. sagitta (Cordophilus sagittus) has been described in African bovids including greater kudu, blackbuck, bushbuck, nyala, eland, and African buffalo (Pletcher et al., 1989). Adult E. sagitta worms inhabit the heart chambers, coronary arteries, and large and small branches of pulmonary arteries including those in caudal regions. Gross lesions include coronary artery aneurysms that contain several adult worms. Histologic findings include myocardial fibrosis, arterial mural fibrosis and smooth muscle hypertrophy, lymphoplasmacytic and eosinophilic arteritis and periarteritis; villous intimal proliferation is seen in pulmonary arteries. Occasional mineralized parasites are present in nodular foci of fibrosis, and small numbers of microfilaria may be present in the myocardium or other tissues. Disease associated with the meningeal worm Parelephostrongylus tenuis (superfamily Metastrongyloidea, family Protostrongylidae), is reported in several wild and captive bovids and in pronghorn. The definitive host of P. tenuis is the white-tailed deer, in which infection is incidental or associated with minimal lesions. Lesions in aberrant hosts are usually associated with nematode migration in the spinal cord and brain and include foci of malacia, hemorrhage, Wallerian degeneration, and meningoencephalitis often with eosinophilic infiltrate (Pybus et al., 1996; Simmons et al., 2002; Weiss et al., 2008). Adult nematodes may be present in white or gray matter or on meninges. Eggs and developing larvae in the lung may be associated with granulomatous interstitial pneumonia. Susceptible species include bighorn sheep, pronghorn, eland, sable antelope, bongo antelope, scimitar horned oryx, blackbuck, and American bison. Parelaphostrongylus odocoilei are small, thread-like worms that can be found in the skeletal muscle of various cervid and bovid species. Like P. tenuis, they are transmitted through ingestion of gastropod intermediate hosts (Jenkins et al., 2005; Lankester, 2001). In thinhorn (Dall’s) sheep, encephalomalacia and myelomalacia have been associated with migrating worms, eggs, and larvae. Granulomatous interstitial pneumonia and myositis, sometimes associated with hemorrhage, are also reported. Verminous pneumonia caused by other nematode species including Dictyocaulus sp., Muellerius sp., and Protostrongylus sp., may manifest as interstitial pneumonia

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

or pulmonary granulomas. These conditions could be mistaken for tuberculosis in regions where these parasites are endemic. Secondary bacterial infections can occur, and lung worms have been implicated as a component of multipathogen pneumonias, such as bighorn sheep pneumonia (Besser et al., 2013) (see above). Specific endoparasites that have demonstrated clinically significant disease or pose zoonotic risk are listed in Supplemental Table e8.

Protozoa Babesia sp. parasites (order Piroplasmida) of mammals are obligate intracellular, tick-borne, apicomplexan protozoa that almost exclusively infect erythrocytes. Zoonotic babesiosis is described as an emerging disease. Clinically significant or fatal babesiosis has been reported sporadically in a variety of nondomestic bovid species, including sable antelope in Africa (Oosthuizen et al., 2008) and European chamois (Hoby et al., 2007). In the former report, captive animals had been recently imported to South Africa from Germany; it is possible their naive status increased their susceptibility to infection and clinical disease. Lesions consistent with babesiosis, including hemoglobinuria, were also reported in small numbers of giraffe in South Africa infected with a novel Babesia species, though a link between infection and death was not definitively established (Oosthuizen et al., 2009). B. ocodoilei, which usually causes disease in cervids, can cause fatal babesiosis in captive muskoxen and has been identified in clinically healthy bighorn sheep (Schoelkopf et al., 2005). Babesiosis may be distinguished from anaplasmosis based on the lack of hemolysis in the latter. Histologically, there is marked congestion of capillaries, with erythrophagocytosis and hemosiderin accumulation in macrophages in multiple tissues. In the kidneys, there may be hemoglobin casts, tubular degeneration, and tubular epithelial hemosiderosis. In the liver, hypoxic lesions characterized by centrilobular degeneration and necrosis may be present, and there can be canalicular cholestasis. Organisms are visible as pale basophilic structures in erythrocytes in HE stained sections, and may be more prominent in capillaries. On blood smears or impression cytology of organs, morphology varies depending on the species. Sporozoites and merozoites may be located centrally or near the erythrocyte margin, and organisms may be single, or paired and oriented at obtuse angles. Single forms may be pyriform, round, or elongate. Differentials for the presence of intraerythrocytic organisms include Theileria sp., Cytauxzoon sp., and Anaplasma sp. Confirmation of babesiosis and identification of Babesia species requires PCR. Piroplasmids of the genus Theileria are tick-vectored, apicomplexan hemoparasites that infect both leukocytes and erythrocytes in mammalian hosts. Theileria are transmitted by various ixodid ticks (Bishop et al., 2004). The most economically significant and well-studied members

139

of the genus are T. parva, subspecies of which cause East Coast fever and corridor disease in cattle in sub-Saharan Africa, and T. annulata, the cause of tropical theileriosis in North Africa and Asia. Vectors for T. parva are Rhipicephalus appendiculatus, R. zambesiensis, and R. duttoni; Hyalomma species transmit T. annulata. Bovine theileriosis is an OIE listed and reportable disease. The parasite life cycle, pathogenesis, and diagnosis in domestic animals are reviewed in Bishop et al. (2004); OIE (2014b), and Mans et al. (2015). Taxonomy and phylogeny are reviewed elsewhere, but it should be noted that historic cases of cytauxzoonosis in several African ungulate species are now generally attributed to Theileria infection (Nijhof et al., 2005). Infection with Theileria has been reported in giraffe (Oosthuizen et al., 2009) and in numerous bovid species, including African buffalo, blue wildebeest, tsessebe, waterbuck, Grant’s gazelle, klipspringer, blesbok, reedbuck, bushbuck, nyala, common eland, sable, roan, kudu, gray duiker, and American bison (Brothers et al., 2011; Githaka et al., 2014; Grootenhuis et al., 1980; Hooge et al., 2015; Kocan and Waldrup, 2001; Mans et al., 2015; Nijhof et al., 2005; Oura et al., 2011; Wamuyu et al., 2015). In most cases, infection of free-ranging wildlife is subclinical but disease is most common in roan and sable. Disease due to Theileria infection has been reported in association with stressful events such as translocation, and with scenarios that lead to higher than normal tick burdens (Steyl et al., 2012). Clinical findings include depression, fever, anemia, and icterus. Prominent, generalized lymphadenomegaly is a common feature and may be visually detectable. Dyspnea, diarrhea, or neurologic signs may be present. Theileria schizonts are visible in aspirates of lymphoid tissue or in circulation (Fig. 5.20). Depending on the host and the species of

FIGURE 5.20  Blood smear from a giraffe with Theileria infection. A large circulating mononuclear cell contains a basophilic protozoal schizont, and a few erythrocytes contain basophilic, punctate piroplasms. Depending on the host and species of Theileria involved, schizonts may be uncommon, but piroplasms can be visible in erythrocytes.

140 Pathology of Wildlife and Zoo Animals

FIGURE 5.21  Myocardium from a roan antelope with theileriosis. The myocardium is infiltrated by several multinucleated giant cells and mononuclear cells containing basophilic protozoal schizonts.

Theileria, schizonts may be uncommon in circulating lymphocytes but piroplasms may be visible in erythrocytes. Schizonts are multinucleate and may be extracellular if cells rupture during smear preparation. Gross findings at necropsy include lymphadenopathy, splenomegaly, pulmonary edema, and petechial and ecchymotic hemorrhage. Histologically, there is widespread lymphoid proliferation, infiltration of multiple tissues by schizont-containing lymphoblasts, lymphocytolysis and necrosis, thrombosis, and hemorrhage (Fig. 5.21). Bone marrow hypoplasia is reported in cattle. In addition to lymphoid tissue, infiltration of schizont-containing cells may occur in any tissue including kidney, gastrointestinal tract, liver, lung, heart, and brain. PCR can be used for laboratory confirmation and species identification. Trypanosomes are insect-vectored protozoal hemoparasites that cause a group of diseases collectively known as trypanosomiasis or trypanosomosis in a wide range of species, including humans. Significant disease has not been reported in nondomestic bovids in endemic areas. Wild African ruminants are reservoirs for the agents of tsetse-transmitted bovine trypanosomiasis or nagana (Trypanosoma congolense, T. vivax, T. brucei brucei), an OIE listed, reportable disease (Auty et al., 2012; OIE, 2013b; van Vuuren and Penzhorn, 2015). Wild African bovids, giraffe, and hippopotamuses are also important hosts for tsetse flies (Glossina spp.) in some regions. There are many species of pathogenic and nonpathogenic trypanosomes, some are polymorphic. Thus, identification to species based on morphology in blood smears is not reliable, and molecular techniques should be used instead if species identification is desired. Toxoplasma gondii is a coccidian protozoan parasite with worldwide distribution. Toxoplasma-associated disease can include placentitis, abortion, early neonatal death, pneumonia, or disseminated, fatal disease (Dubey and Odening, 2001). Bovid species susceptible to toxoplasmosis include gazelles (dama, Cuvier’s, slender-horned), ­gerenuk,

dik dik, and saiga (Bulmer 1971; Dubey et al., 2002; Junge et al., 1992; Sedlák et al., 2004; Stover et al., 1990). Pronghorn are highly susceptible to experimental infection (Dubey et al., 1982). Abortion and neonatal death have been reported in muskoxen and nilgai. In acute, disseminated infections, Toxoplasma sporozoites from ingested oocysts or bradyzoites from ingested tissue cysts invade intestinal epithelial cells and multiply asexually as tachyzoites that spread to mesenteric lymph nodes and systemically via blood and lymphatics. Gross lesions include mesenteric lymphadenopathy and lymph node necrosis; hemorrhagic or catarrhal enteritis; hemorrhagic to fibrinous peritoneal effusion; serosal and endocardial petechiae and ecchymoses; pulmonary edema and hemorrhage; and pale foci of necrosis in tissues, notably liver, spleen, or kidney. Histologically, necrosis and variably intense mononuclear to mixed inflammatory cell infiltrates are present in multiple tissues, sometimes centered on blood and lymphatic vessels (necrotizing vasculitis). Necrosis is usually due to intracellular tachyzoites, but tissue cysts may also be present. In transplacental infections, dams may remain asymptomatic and lesions may be limited to the placenta, where there is necrosis associated with the presence of tachyzoites. In domestic sheep and goats, gross findings include dark red cotyledons with multiple, small, white foci of necrosis. Histologically, cysts or tachyzoites may be present in the placenta, and occasionally there are lesions in fetal heart, lungs, brain, or other tissues (Rideout, 2012). Tachyzoites are approximately 6 µm long, often curved, may be uni- or binucleate, and may be present individually, paired, or in clusters in tissue sections or impression smears. Tissue cysts vary in size and are most often found in brain, muscle, and eye but can occur anywhere. Note that tissue cysts may be found in clinically healthy animals, not associated with inflammation; in these cases, cysts could serve as a source of infection to humans who may eat game. Cysts are round to elongate and may be up to 60 µm long. Diagnosis can be confirmed by immunohistochemistry or PCR. Serosurveys have identified exposure to Toxoplasma in free-ranging giraffe, common hippopotamuses, and many additional species of Bovidae (Bakal et al., 1980; Riemann et al., 1975). Neospora caninum is an apicomplexan protozoan parasite closely related, and morphologically similar, to Toxoplasma gondii. Infection has been associated with stillbirth in lesser kudu. Lesions include nonsuppurative encephalitis with gliosis, and nonsuppurative myocarditis (Peters et al., 2001). Tissue cysts may be present and can be identified using immunohistochemistry. Placental necrosis with protozoal zoites may also be present (Rideout, 2012). Other confirmed reports of neosporosis in nondomestic ruminants are limited to cervids (Donahoe et al., 2015). Sarcocystis sp. protozoa usually have a 2-host life cycle with carnivore definitive hosts. Many species of Sarcocystis

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

have been identified, and most are relatively species-specific to their mammalian or avian intermediate hosts (Dubey and Odening, 2001). For many Sarcocystis sp. of wildlife, the life cycle and definitive hosts are not known. Sarcocystis infection in wild Bovidae, Giraffidae, and Hippopotamidae is usually not clinically significant. Large tissue cysts may be observed histologically, or sometimes grossly, in skeletal and cardiac muscle of African buffalo (Dubey et al., 2014). In domestic ruminants, systemic infection may be associated with acute hemorrhage, vasculitis, and necrosis in multiple tissues. Intestinal protozoal disease, including Giardiasis, Cryptosporidiosis, and Coccidiosis are primarily entities of captivity and are similar in epidemiology, clinical features, and postmortem findings to disease reported in domestic ruminants.

Ectoparasites Dermatitis and pruritis associated with sarcoptic mange (etiology: Sarcoptes scabiei) has been reported in over 100 mammalian species. Outbreaks are occasionally reported in free-ranging animals. For example, sarcoptic mange was diagnosed in several giraffe in Kenya in 2010 (Alasaad et al., 2012). Psoroptic mange associated with Psoroptes sp. infection is moderately common in some populations of free-ranging bighorn sheep (Cassirer and Sinclair, 2007). Lesions can include alopecia, erythema, papule formation, lichenification, crusting, and acanthosis on legs, back, shoulders, neck, and muzzle. Diagnosis is through identification of mites and eggs on skin scraping. Wild ruminants and hippopotamuses may have a wide range of ectoparasites including ticks, mites, lice, rectal leeches, and flies. The clinical significance of many of these infestations is variable and often unclear. A brief summary of specific ectoparasites that have demonstrated clinically significant disease or pose a zoonotic risk is presented in Supplemental Table e9.

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Prions Transmissible spongiform encephalopathies (TSEs) of ungulates include chronic wasting disease (See Cervidae Chapter 6), scrapie, and bovine spongiform encephalopathy (BSE) (OIE listed, reportable diseases). Scrapie, which has been recognized in domestic sheep and goats for hundreds of years, also occurs naturally in mouflon and possibly other species of wild Caprinae. TSEs reported in several species of captive, nondomestic ruminants housed in zoological gardens in the United Kingdom were coincident with the epidemic of BSE in the 1980s (Jeffrey and Wells, 1988; Kirkwood and Cunningham, 1994; Cunningham et al., 2004). Cases of TSE in nyala, greater kudu, gemsbok, Arabian oryx, scimitar-horned oryx, eland, and American bison are now recognized as BSE acquired through ingestion of affected ruminant-derived meat and bone meal in feed (Sigurdson and Miller, 2003). During the BSE epidemic, greater kudu appeared to be highly susceptible. Mouse bioassay studies demonstrate a very wide tissue distribution of the BSE agent in kudu, and horizontal transmission of the BSE agent during the epidemic has been proposed. Diagnosis is through demonstration of typical neuronal vacuolation, which is most often present in the medulla oblongata at the level of the obex in both BSE and scrapie. Specialized instruments for sampling the obex via the foramen magnum have been developed for both cattle and sheep, and may be appropriate for testing nondomestic ruminants. However, samples from multiple regions of brain may be required to identify “atypical” scrapie, which affects the cerebellum and only minimally involves the medulla (OIE, 2016). Vacuolation of neuron cell bodies may be accompanied by neuropil vacuolation and astrogliosis (OIE, 2016). IHC can be used to confirm the presence of PrPsc and to detect PrPsc prior to induction of vacuolar change in the brain. Other methods such as western immunoblot and ELISA can be used as rapid tests, but these should be followed by confirmatory tests. There are no reliable tests for detecting BSE or scrapie in a live animal.

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

141.e1

E-SLIDES 5.e1 Transcaspian urial, Johne’s disease (M. avium subsp. paratuberculosis), intestine. Granulomatous inflammation within the intestinal mucosa of a transcaspian urial with Johne’s disease caused by infection with Mycobacterium avium supsp. paratuberculosis. The mucosal lamina propria is severely expanded by sheets of epithelioid macrophages which separate and replace the crypts, and there is blunting and fusion of villi. Inflammation is also present below the muscularis mucosa. (see Fig. 5.15). eSlide: VM05251 5.e2 Transcaspian urial, Johne’s disease (M. avium susp. paratb), intestine, Ziehl-Neelsen. Same section as slide SS05.01 stained with Ziehl-Neelsen acid fast stain. Numerous acid-fast positive bacilli are present within macrophages. (see Fig. 5.15). eSlide: VM05252 5.e3 Eastern white-bearded gnu, Coxiellosis, placenta. Placental villi from an Eastern white-bearded gnu with coxiellosis. There is multifocal villus necrosis with sloughing of the trophoblast layer. Individual trophoblasts contain dense granular colonies of intracytoplasmic bacteria. In some presentations, cellular debris and neutrophils may fill the intervillus spaces. Important differential diagnoses include Brucella and Chlamydia spp. (see Fig. 5.19). eSlide: VM05253 5.e4 Cape blue duiker, Malignant catarrhal fever, kidney and adrenal. Perivascular and interstitial lymphocytic infiltrates with mild vasculitis. In non-domestic ruminants, OvHV-2 and AlHV-1 are best characterized but infections can also occur with CpHV-2 and AlHV-2. Lymphocytic vasculitis and perivascular infiltrate can be relatively mild compared to the more severe, “classic” lymphoproliferative lesions often observed in domestic animals. (see Figs 5.9 and 5.10). eSlide: VM05254

E-ONLY CONTENTS Family

Subfamily

Genus Species

Common Name

Bovidae

Aepycerotinae

Aepyceros melampus

Impala

Alcelaphus

Alcelaphus buselaphus

Hartebeest

Beatragus hunteri

Hunter’s hartebeest, hirola

Connochaetes gnou, C. taurinus

Black, blue wildebeest

Damaliscus lunatus, D. pygargus

Topi, blesbok

Ammodorcas clarkei

Dibatag

Antidorcas marsupialis

Springbok

Antilopinae

Antilope cervicapra

Blackbuck

Antidorcas

Dorcatragus megalotis

Beira

Eudorcas albonotata, E. rufifrons, E. rufina, E. thomsonii

Mongalla, red-fronted, red, Thomson’s gazelle

Gazella arabica, G. bennettii, G. bilkis, G. cuvieri, G. dorcas, G. gazella, Arabian, Indian, Queen of Sheba’s, Cuvier’s, Dorcas, mountain, slender-horned, Saudi, Peke’s, goitered gazelle G. leptoceros, G. saudiya, G. spekei, G. subgutturosa

Bovinae

Litocranius walleri

Gerenuk

Madoqua guentheri, M. kirkii, M. piacentinii, M. saltiana

Guenther’s, Kirk’s, Silver, Salt’s dik-dik

Nanger dama, N. granti, N. soemmerringii

Dama, Grant’s, Soemmerring’s gazelle

Neotragus batesi, N. moschatus, N. pygmaeus

Bates’s pygmy antelope, Suni, Royal antelope

Oreotragus oreotragus

Klipspringer

Ourebia ourebi

Oribi

Procapra gutturosa, P. picticaudata, P. przewalskii

Mongolian, Tibetan, Przewalski’s gazelle

Raphicerus campestris, R. melanotis, R. sharpei

Steenbok, Southern, Northern grysbok

Saiga tatarica

Saiga

Bison bison, B. bonasus

American, European bison

Bos gaurus, B. javanicus, B. mutus, B. primigenius, B. sauveli

Gaur, Bantena, wild yak, aurochs, Kouprey

Boselaphus tragocamelus

Nilgai

Bubalus arnee, B. depressicornis, B. mindorensis, B. quarlesi

Asian water buffalo, lowland anoa, Tamaraw, mountain anoa

Pseudoryx nghetinhensis

Saola

Syncerus caffer

African buffalo

Tetracerus quadricornis

Four-horned antelope

Tragelaphus angasii, T. buxtoni, T. derbianus, T. eurycerus, T. imberbis, T. oryx, T. scriptus, T. spekii, T. strepsiceros

Nyala, mountain nyala, gaint eland, bongo, lesser kudu, common eland, bushbuck, Sitatunga, greater kudu

141.e2 Pathology of Wildlife and Zoo Animals

TABLE e1 Taxonomy of Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidaea

TABLE e1 Taxonomy of Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.) Family

Subfamily

Genus Species

Common Name

Caprinae

Ammotragus lervia

Barybary sheep

Arabitragus jayakari

Arabian tahr

Budorcas taxicolor

Takin

Capra aegagrus, C. caucasica, C. cylindricornis, C. falconeri, C. ibex, C. wild goat, west, east caucasian tur, Markhor, Alpine, Nubian, Spanish, Siberian, Walia ibex nubiana, C. pyrenaica, C. sibirica, C. walie

Reduncinae

Hemitragus jemlahicus

Himalayan tahr

Naemorhedus baileyi, N. caudatus, N. goral, N. griseus

Red, long-tailed, gray, Chinese goral

Nilgiritragus hylocrius

Nilgiri tahr

Oreamnos americanus

Rocky mountain goat

Ovibos moschatus

Musk ox

Ovis ammon, O. canadensis, O. dalli, O. nivicola, O. orientalis

Argali, bighorn, Dall’s, snow sheep, Urial

Pantholops hodgsonii

Tibetan antelope

Pseudois nayaur, P. schaeferi

Himalayan, dwarf blue sheep

Rupicapra pyrenaica, R. rupicapra

Pyrenean, Alpine chamois

Cephalophus adersi, C. callipygus, C. dorsalis, C. harveyi, C. jentinki, C. leucogaster, C. natalensis, C. niger, C. nigrifrons, C. ogilbyi, C. rufilatus, C. silvicultor, C. spadix, C. weynsi, C. zebra

Ader’s, Peter’s, Bay, Harvey’s, Jentink’s, white-bellied, red, black, black-fronted, Ogilby’s, red-flanked, yellow-backed, Abbott’s, Weyn’s, zebra duiker

Philantomba maxwellii, P. monticola

Maxwell’s, blue duiker

Sylvicapra grimmia

Gray duiker

Addax nasomaculatus

Addax

Hippotragus equinus, H. leucophaeus, H. niger

Roan antelope, blue buck, Sable antelope

Oryx beisa, O. dammah, O. gazella, O. leucoryx

East African, Scimitar-horned, South African, Arabian oryx

Kobus ellipsiprymnus, K. kob, K. leche, K. megaceros, K. vardonii

Waterbuck, Kob, Lechwe, Mrs. Gray’s lechwe, Puku

Pelea capreolus

Rhebok Southern, mountain reedbuck

Antilocapra americana

Pronghorn

Giraffidae

Giraffa camelopardalis

Giraffe

Okapia johnstoni

Okapi

Hyemoschus aquaticus

Water chevrotain

Moschiola indica, M. kathygre, M. meminna

Indian, yellow-striped, white-spotted chevrotain

Tragulus javanicus, T. kanchil, T. napu, T. nigrican, T. versicolor, T. williamsoni

Javan, lesser oriental, greater oriental, Balabac, silver-backed, yunnan chevrotain

Hexaprotodon liberiensis

Pygmy hippopotamus

Hippopotamus amphibious

River hippopotamus

Hippopotamidae

Nowak, R., 1999. Walker’s Mammals of the World, sixth ed.. Johns Hopkins University Press, Baltimore, MD, USA.

141.e3

Redunca arundinum, R. fulvorufula, R. redunca Antilocapridae

Tragulidae

a

Japanese, Chinese, red, Southern, Formosan, Himalayan serow

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

Hippotraginae

Capricornis crispus, C. milneedwardii, C. rubidus, C. sumatraensis, C. swinhoei, C. thar

141.e4 Pathology of Wildlife and Zoo Animals

TABLE e2 Dentition in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae Family

Dentition (Dental Formula)

Dental Notes

Bovidae

I 0/3, C 0/1, P2-3/3, M3/3

Hypsodont, maxillary incisors replaced by a dental pad

Antilocapridaea

I 0/3, C 0/1, P 3/3, M 3/3

Hypsodont, maxillary incisors replaced by a dental pad

Giraffidaea

I 0/3, C 0/1, P 3/3, M 3/3

Hypsodont, maxillary incisors replaced by a dental pad

Tragulidaeb

I 0/3, C 1/1, P 3/3, M 3/3

Hypsodont, maxillary incisors replaced by a dental pad, male maxillary canines form short tusks

Hippopotamidaec,d

Hippo: I 2/2, C 1/1, P 3-4/3-4, M 3/3; Pygmy hippo: I 2/1, C 1/1, P 3/3, M 3/3

Hypsodont incisors and canines grow continuously; canines elongate into large curved tusks

a

Dental formulae are unilateral, double for total number; Maxillary/Mandibular; I, incisors; C, canines; P, premolars; M, molars. a Miller, R.E., Fowler, M.E., 2015. Fowler’s Zoo and Wild Animal Medicine, eighth ed. Elsevier/Saunders, St. Louis, Missouri. b Kingdon, J., Happold, D., Butynski, T., Hoffmann, M., Happold, M., Kalina, J., 2013. Mammals of Africa, Vol. 1., A&C Black, Bloomsbury Publishing, London. c Renvoise, E., Michon, F., 2014. An evo-devo perspective on ever-growing teeth in mammals and dental stem cell maintenance. Front. Physiol. 5, 324. d Knightly, F., Emily, P., 2003. Oral disorders of exotic ungulates. Vet. Clin. North Am. Exot. Anim. Pract. 6, 565–570.

TABLE e3 Urolithiasis in Nondomestic Bovidae, Antliocapridae, Giraffidae, Hippopotamidae, and Tragulidae Urolith Composition

Species Affected

References

Calcium carbonate

Wildebeest,a giraffe,

Osborne et al. (2009)

Calcium oxalate

Bison, bongo, hippopotamus

Osborne et al. (2009)

Calcium phosphate

Gemsbok, greater kudu, mouflon, tahr,

Osborne et al. (2009)

Magnesium calcium phosphate

Giraffe, greater kudu, mouflon,

Osborne et al. (2009)

a

Osborne et al. (2009)

Magnesium calcium phosphate carbonate

Duiker, giraffe,

Mixed

Duiker, mouflon, giraffe

Bertelsen (2015); Osborne et al. (2009)

Other

a

Giraffe, greater kudu

Osborne et al. (2009)

Purines

Duiker, gazelle (not specified), tahr, wildebeest

Osborne et al. (2009)

Struvite

Duiker, giraffe, mouflon,

Osborne et al. (2009)

Bertelsen, M.F., 2015. Giraffidae, in: Miller, R.E., Fowler, M.E. (Eds.), Fowler’s Zoo and Wild Animal Medicine. Elsevier. Osborne, C.A., Albasan, H., Lulich, J.P., Nwaokorie, E., Koehler, L.A., Ulrich, L.K., 2009. Quantitative analysis of 4468 uroliths retrieved from farm animals, exotic species, and wildlife submitted to the Minnesota Urolith Center: 1981 to 2007. Vet Clin North Am Small Anim Pract 39, 65-78. a Most common type of urolith in this species (Osborne et al., 2009).

TABLE e4 Select Toxic Diseases of Bovidae, Antliocapridae, Giraffidae, Hippopotamidae, and Tragulidae Etiology (Family, Genus)

Toxic Agent

Clinical Signs/Gross Lesions

Histologic lesions

Species Affected

Keys to Diagnosis

References

Evidence of ingesKnight and Walter tion, “bitter almond” (2001); Plumlee odor may be present. (2004) Laboratory analysis of feed or forage for cyanide content

Systemic Toxins Cyanogenic glycosides, cyanide

Plant cyanogenic Prunus spp., Sorghum in general and glycosides Johnson grass, Sudan grass, intentional exposure to sodium cyanide (illegal hunting)

Sudden death-peracute signs of hypoxemia, cherry red mucosa, hyperventilation

May be absent, nonspecific-abomasal, subendocardial, or subepicardial hemorrhage

Plants-all ruminants; sodium cyanide-kudu, buffalo secondary to intentional poisoning of water and salt licks targeting elephants

Cardiac glycosides

Digitalis spp. Urginea Cardiac glycosides sanguinea, Oleander, Moreaea sp., Drimia sp.

Sudden death, ruminal stasis, bloat, dyspnea

Subacute to acute and subacute myocardial necrosis, fibrosis

All ruminants, some Identification of plant may be more resistant. parts or toxins in the Most plants in this rumen group are unpalatable to most ruminants, but may be the only forage available under certain conditions

Knight and Walter (2001); Basson (1987); Plumlee (2004); Botha and Penrith (2008)

Yew

Taxus spp. evergreen Taxine alkaloids

Sudden death, nonspeVascular congescific vascular congestion tion in abomasum, in abomasum, pulmonary pulmonary edema edema.

ID of evergreen Antilocapridae, freeranging ruminants, zoo needles in rumen exposure

Oneal (2017)

Wild tobacco

Nicotiana spp.

Nicotine, anabasine

Acute-weakness, muscle, Myocardial degenAfrican antelope, most fasciculation, respiraeration, hepatocellu- ruminants tory, and cardiac arrest; lar degeneration polycavitary effusion and serosal petechial hemorrhage

Oxalate

Halogeton spp.

Sodium oxalate

Acute-hypocalcemia leading to bloat, tetany, or seizures, bradycardia

Willow

Salix spp.

Salicylic acid, susTan or brown discolorpected not confirmed ation to kidneys, liver, hydropericardium

Cardiotoxins

Nephrotoxins All ruminants, Ovinae and Caprinae may be more susceptible

Oxalate crystals in renal lesions, access to plants, and laboratory analysis of sodium oxalate content in forage

Haenichen et al. (2001); Botha and Penrith (2008); Plumlee (2004)

Renal tubular atrophy, replacement fibrosis, focal glomerular atrophy

Captive okapi

Clinical history of renal disease, gross and microscopic lesions subsequent to feeding of willow twigs or branches

Haenichen et al. (2001)

(Continued)

141.e5

Acute nephrosis, birefringent oxalate crystals in renal tubules with tubular degeneration, ectasia, and cast formation

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

Basson (1987)

TABLE e4 Select Toxic Diseases of Bovidae, Antliocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.) Toxic Agent

Clinical Signs/Gross Lesions

Histologic lesions

Species Affected

Keys to Diagnosis

References

Hepatotoxins Pyrrolizidine alkaloids

Numerous, esp. Senecio spp., Heliotropium spp., and Crotolaria spp.

Bluegreen algae

Nitrates

Pyrrolizidine alkaloids

Acute toxicity: acute liver failure; chronic toxicity: photosensitivity, icterus, tenesmus, diarrhea

Acute: submassive/ Free-ranging African massive hepatic necro- antelope sis; chronic–chronicactive or piecemeal hepatitis with hepatocyte megalocytosis portal fibrosis, terminal cirrhosis

Clinical history and signs, microscopic findings of chronicactive hepatitis with megalocytosis and biliary fibrosis are characteristic but not specific

Basson (1987); Plumlee (2004); Botha and Penrith (2008)

Microcystins, Multiple, esp. Microcystis, Anabaena, nodularin, anatoxins, and Panktothrix spp. saxitoxins, others. Released by lysis of algal cells.

Peracute-sudden death. May be group mortality of herd animals at watering sites. Microcystin: acute/ subacute-icterus, photosensitization, pulmonary edema, hepatopathy: hepatomegaly, copper orange color, friable, necrosis hemorrhage; systemic hemorrhages. Chronic (prolonged low-level exposure)-inappetance, weight loss, photosensitivity, alopecia

(Microcystin) hepatomegaly ± hemorrhage, Histo: acute centrilobular to midzonal necrosis (submassive or massive necrosis) and multisystemic hemorrhage. Anatoxins, saxitoxins: depolarizing neuromuscular blockademay have no gross or microscopic findings

History of algal bloom, ID cyanobacteria or toxins in water supply or ingesta, clinical signs, gross and histological lesions

Masango et al. (2010); Buss and Bengis (2012); Plumlee (2004); Bengis et al. (2016)

Exposure to nitrated Nitrates and nitrites feed; urea poisoning; some cereal crops (e.g. oat, millet, rye, sorghum)

Methemoglobinemia, serosal petechiae and ecchymosis, pulmonary edema, emphysema, pericardial effusion, ruminal and abomasal congestion

Serosal petechiae, Free-ranging bison, severe pulmonary captive blackbuck, congestion and most ruminants at risk edema, multisystemic vascular congestion

Clinical signs, gross appearance of methemoglobinemia (fades within 5 hours of death), history of exposure, laboratory analysis of feed, rumen contents, nitrate levels >10–20 ppm in ocular fluid in adults, fetal intraocular nitrite is normally >20 ppm

Plumlee (2004); Knight and Walter (2001); Aiello et al. (2016)

Salivary neurotoxins Africa-esp. Ixodes rubicundus (­Karoo paralysis tick), Rhipicephalus evertsi, Hyalomma spp; Australia-Ixodes holocyclus, I. cornuatus, I. hirstii; Europe-North America-Dermacentor variablis, D. occidentalis, D. andersoni

Severity may correlate None specific, secwith tick burden-ascend- ondary to effects of ing flaccid paralysis, reascending paralysis spiratory paralysis, death, gross findings associated with ascending paralysis, trauma, bloat, aspiration pneumonia

Free-ranging ruminants Clinical signs in conjunction with tick infestation, in some tick species the presence of a single tick may result in severe disease

Aiello et al. (2016); Miller and Fowler (2015); Mullen and Durden (2009); Botzler and Brown (2014); Mans et al. (2003)

Most vertebrates. All Bovidae, Giraffidae, Antilocapridae, and Hippopotamidae

Tick Paralysis Exposure to bites from certain ticks ∼80 tick species

141.e6 Pathology of Wildlife and Zoo Animals

Etiology (Family, Genus)

TABLE e4 Select Toxic Diseases of Bovidae, Antliocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.) Etiology (Family, Genus)

Toxic Agent

Clinical Signs/Gross Lesions

Histologic lesions

Species Affected

Keys to Diagnosis

References

Clinical signs, presence of tick infestation

Mullen and Durden (2009); Botzler and Brown (2014); Mans et al. (2003); Dolan and Newson (1980)

Low brain acetylcholinesterase activity tested on fresh frozen brain (1 hemisphere), eye (retina), liver, stomach contents

Ogada (2014); Buss and Bengis (2012); Plumlee (2004)

Tick Toxicosis Exposure to bites Africa-Ornithodoros Salivary toxins from certain distinct from neurosavignyi; Eastern ticks Europe-O. lahorensis, toxins Hyalomma truncatum; Australia-Ixodes holocyclus; North America-I. pacificus

Most ruminants O. savignyi-necrotizing dermatitis, necrotizing lesions with pseudomembrane formation in oronasal, esophageal, and reproductive mucosa, exudative dermatitis with minimal changes: vascular congestion, intravascular neutrophil accumulation, serosuppurative exudate, ± neutrophilic and histiocytic perivascular cuffs

Pesticides Organophosphates, Acetylcholinesterase carbamates, esp. Car- inhibitors bofuran and Aldicarb in African wildlife

Muscarinic +/or nicotinic No specific microclinical presentation. No scopic findings specific gross necropsy findings. Sudden death.

Common in African avian and mammalian carnivores, less common in hippos, poorly reported in ruminants

Aiello, S.E., Moses, M.A., Allen, D.G., 2016. The Merck Veterinary Manual, eleventh ed. Merck, Kenilworth, pp. 1824–1828. Basson, P.A., 1987. Poisoning of wildlife in southern Africa. J. S. Afr. Vet. Assoc. 58, 219–228. Botha, C.J., Penrith, M.L., 2008. Poisonous plants of veterinary and human importance in southern Africa. J. Ethnopharmacol. 119, 549–558. Botzler, R.G., Brown, R.N., 2014. Foundations of Wildlife Diseases, pp. 1 online resource (viii, 449 pages). Buss, P.E., Bengis, R.G., 2012. Cyanobacterial biointoxication in free-ranging wildlife. In: Miller, R.E., Fowler, M.E. (Eds.), Fowler’s Zoo and Wild Animal Medicine: Current Therapy, seventh ed. Elsevier/Saunders, St. Louis, Mo., pp. xviii, 669 p. Dolan, T.T., Newson, R.M., 1980. Sweating sickness in adult cattle. Trop. Anim. Health Prod. 12, 119–124. Haenichen, T., Wisser, J., Wanke, R., 2001. Chronic tubulointerstitial nephropathy in six okapis (Okapia johnstoni). J. Zoo Wildl. Med. 32, 459–464. Knight, A.P., Walter, R.G., 2001. A guide to plant poisoning of animals in North America. Teton NewMedia, Jackson, Wyo. Mans, B.J., Louw, A.I., Neitz, A.W., 2003. The major tick salivary gland proteins and toxins from the soft tick, Ornithodoros savignyi, are part of the tick Lipocalin family: implications for the origins of tick toxicoses. Mol. Biol. Evol. 20, 1158–1167. Masango, M.G., Myburgh, J.G., Labuschagne, L., Govender, D., Bengis, R.G., Naicker, D., 2010. Assessment of microcystis bloom toxicity associated with wildlife mortality in the Kruger National Park, South Africa. J. Wildl. Dis. 46, 95–102. Miller, R.E., Fowler, M.E., 2015. Fowler’s Zoo and Wild Animal Medicine, eighth ed. Elsevier/Saunders, St. Louis, Missouri. Mullen, G.R., Durden, L.A., 2009. Medical and Veterinary Entomology, second ed. Elsevier, Academic, Amsterdam, Boston. Ogada, D.L., 2014. The power of poison: pesticide poisoning of Africa’s wildlife. Ann. N Y Acad. Sci. 1322, 1–20. Oneal, E., 2017. Pronghorn Deaths Blamed On Japanese Yew, Press Release. Idaho Department of Fish and Game. Plumlee, K.H., 2004. Clinical Veterinary Toxicology. Mosby, St. Louis, Mo.

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

General signs-acute febrile illness, lacrimation, sweating, salivation; gross findings-O. savignyi-sudden death; H. trucantum-“sweating sickness”-wet or matted hair coat, eczematous skin lesions, oronasal mucosal necrosis, secondary infection; multisystemic vascular congestion

141.e7

141.e8 Pathology of Wildlife and Zoo Animals

TABLE e5 Select Neoplasia in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae from the Literature and the Authors’ Files Species

Tumor Type

Location

Addax

Adenoma

Thyroid

Cutaneous T-cell lymphoma

Lymph node

Leiomyoma

Uterine

Adenocarcinoma

Uterine

Black-faced impala

References Gyimesi et al. (2017)

Blue duiker

Bronchiocarcinoma

Dama gazelle

Cortical adenoma

Adrenal

Schmidt et al. (1979)

Giraffe

Teratoma

Umbilical cord

Murai et al. (2007)

Chondrosarcoma

Pelvic

Juan-Salles et al. (2008)

Adenoma

Thyroid

Leiomyoma

Uterine

Subependymal glioneuronal hamartoma

Mesencephalic aqueduct

Keohler et al. (2012)

Embryonal rhabdomyosarcoma

Subjacent parietal bone

Woc-Colburn et al. (2010)

Grey duiker

Carcinoma

Bile duct

Hippopotamus

Adenocarcinoma

Brain and adrenal gland

Mouflon

Adenocarcinoma

Cutaneous apocrine sweat gland Morandi et al. (2005)

Cortical adenoma

Adrenal

Pheochromocytoma

Adrenal gland

Thymoma

Thymus

Nyala

Teratoma

Testes

Keep and Basson (1973)

Pygmy hippoptamus

T-cell lymphoblastic leukemia

Blood

McCurdy et al. (2014)

Sable

Teratoma

Oropharynx

Haefele et al. (2008)

Springbok

Pheochromocytoma

Adrenal gland

Wildebeest

Cutaneous melanoma

With color dilution hair coats

Nilgai

Shiaffino et al. (2016) Schmidt et al. (1979)

Adetunji et al. (2018)

Adetunji SA, Krecek RC, O'Dell N, Prozesky L, Steyl J, Arenas-Gamboa AM. Melanoma in golden and king wildebeests (Connochaetes taurinus). J Zoo Wildl Med. 2018;49(1):134-142. Gyimesi ZS, Burns RB, Coutermarsh-Ott S, Schiller CA, McManamon R. Cutaneous T-Cell lymphoma with lymph node metastasis in an adult addax (Addax nasomaculatus). J Zoo Wildl Med. 2017;48(3):933-936. Haefele HJ, Guthrie A, Trupkiewicz JG, Garner MM. Oropharyngeal teratoma in a neonatal sable antelope (Hippotragus niger). J Zoo Wildl Med. 2008;39(2):266-269. Juan-Salles C, Martinez G, Garner MM, Parás. Fatal dystocia in a giraffe due to a pelvic chondrosarcoma. Vet Rec. 2008;162(11):349-351. Keep ME, Basson PA. A testicular teratoma in a nyala (Tragelaphus angasi Gray, 1848). J S Afr Vet Assoc. 1973;44(3):288. Koehler J, Cox N, Passler T, Wolfe D. Subependymal glioneuronal hamartoma in the mesencephalic aqueduct of a giraffe. J Zoo Wildl Med. 2012;43(3):629-631. McCurdy P, Sangster C, Lindsay S, Vogelnest L. Acute lymphoblastic leukemia in a pygmy hippopotamus (Hexaprotodon liberiensis). J Zoo Wildl Med. 2014;45(4):906-910. Morandi F, Benazzi C, Simoni P. Adenocarcinoma of apocrine sweat glands in a mouflon (Ovis musimon). J Vet Diagn Invest. 2005;17(4):389-392. Murai A, Yanai T, Kato M, Yonemaru K. Sakai H, Masegi T. Teratoma of the umbilical cord in a giraffe (Giraffa camelopardalis reticulata). Vet Pathol. 2007;44(2):204-206. Schiaffino F, Sander SJ, Bacares ME, Barnes KJ, Kiupel M, Walsh T, Murray Sl. Cerebellar and mesencephalon neoplasia in a Nile hipoppotamus (Hippopotamus amphibious). J Zoo Wildl Med. 2016;47(4):1093-1096. Schmidt RE, Fletcher KC. Adrenal cortical adenoma in a dama gazelle (Gazella dama). J Wildl Dis. 1979;15(2):299-301. Woc-Colburn M, Murray S, Boedeker N, Viner T, Fleetwood ML, Barthel TC, Newman KD, Sanchez CR. Embryonal rhabdomyosarcoma in a Rothschild's giraffe (Giraffa camelopardalis rothschildi). J Zoo Wildl Med. 2010;41(4):717-720.

TABLE e6 Bacterial Diseases of Importance in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae Diseases

Etiology (Genus, Species) Species Affected Gross Lesions Most artiodactyls

Acute or subacute enterocolitis, enteric disease. May be mild to severe and may rapidly progress to fatal septicemic diseases. Gross findings: Similar to those observed in Cervidae, other mammals. Enteric disease with mild to severe fibrinohemorrhagic enteritis and colitis, hemorrhagic mesenteric lymphadenitis. Enteritis may include pseudomembrane or cast formation. Septic animals may also have acute necrotizing and hemorrhagic lesions in viscera, esp. liver, gallbladder, spleen; may affect most viscera and brain.

Enteric disease: Necrotizing and fibrinosuppurative to pseudomembranous enteritis or enterocolitis and lymphadenitis with intralesional colonies of small Gram-negative rod bacteria. Ileum and colon may be most severely affected. Sepsis: Embolic pattern of fibrinonecrotizing and hemorrhagic lesions to extensive necrotizing and hemorrhagic lesions secondary to coagulopathy.

Culture of bacteria from Brown et al. lesions, Polymerase (2007) Chain Reaction (PCR) Morner (2001) and multiplex PCR. S. abortusovis is an OIE listed reportable disease.

References

Yersiniosis

Yersinia pseudotuberculosis, less frequently Y. enterocolitica

Most artiodactyls

Acute disease, sudden death. Y. pseudotuberculosis-hemorrhagic enterocolitis ± ulceration, enlarged hemorrhagic mesenteric lymph nodes, hepatomegaly, splenomegaly, sepsis may result in embolic pattern of necrosis in multiple organs. Subacute to chronic cases may result in mastitis, abortion.

Acute-necrotizing and hemorrhagic enterocolitis and mesenteric lymphadenitis, sepsis, embolic lesions-necrosuppurative foci in liver, spleen, other tissues, interstitial pneumonia, large numbers of small Gram-negative rods in systemic lesions.

Clinical presentation, gross and microscopic lesions, identification (ID) of bacteria in cultures of systemic lesions (esp. liver, spleen, lung), PCR of bacteria in fresh or fixed tissues.

Allchurch (2003) Brown et al. (2007) (Gasper and Watson, 2001)

Listeriosis

Listeria monocytogenes, L. ivanovii (uncommon, only causes disease in ruminants, does not cause CNS lesions)

All artiodactyls susceptible, but diseases is uncommon and sporadic

Systemic/septicemic disease in neonates and juveniles with or without CNS involvement, CNS disease is more common in adult animals. Systemic disease-widespread serosal and subserosal visceral hemorrhage, embolic/milliary pattern of necrosis in viscera, esp. liver, spleen, lung, kidney, lymph nodes. Placentitis in giraffe; multifocal necrotizing lesions in brain and spinal cord.

Systemic disease—embolic pattern ID of bacteria on culture of coagulative necrosis ± suppurative of fresh or frozen tissue inflammation in viscera, esp. liver and spleen. Gram-positive rod bacteria around periphery of necrotic foci. Giraffe brain-typical of neurolisteriosis in other species. Acute suppurative leukoencephalitis and cervical myelitis, intracellular Gram-positive bacteria, also subacute-chronic nonsuppurative meningoencephalitis and gliosis with lymphocytic perivascular cuffing. Suppurative encephalitis and malacia may extend to gray matter. Trigeminal and myenteric ganglioneuritis may be present. Necrotizing and suppurative placentitis, cotyledons often affected.

Cranfield et al. (1985); Ferroglio (2001); Webb and Rebar (1987)

141.e9

Keys to Diagnosis

Salmonella enterica, numerous subspecies and serovars

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

Microscopic Lesions

Salmonellosis

(Continued)

Diseases

Etiology (Genus, Species) Species Affected Gross Lesions

Actinomycosis, “lumpy jaw”

Actinomyces spp., All artiodactyls esp. A. bovis

Trueperellosis (Arcanobacteriosis)

Trueperella pyogenes Formerly Arcanobacterium pyogenes, Actinomyces pyogenes, Corynebacterium pyogenes Often present in mixed anaerobic infections, esp. with Fusobacterium necrophorum and Dichelobacter nodosus.

All artiodactyls, esp. ruminants. Blackbuck reportedly may be at increased risk.

Microscopic Lesions

Keys to Diagnosis

References

One or more firm to hard foci of mandibular swelling (lumpy jaw) with ulcerative gingivitis and stomatitis with draining tracts, and exudate containing firm yellow concretions (sulfur granules). Mandible has honeycombappearance on section with abscesses surrounded by proliferative bone, periosteal proliferation may be extensive.

Similar to lesions in domestic cattle. ID of bacteria on culture Chronic mandibular osteomyelitis of fresh or frozen tissue. with chronic intraosseous abscesses surrounded by woven bone. Draining tracts extend from medulla to mucosa or skin. Abscesses may contain bacterial aggregates surrounded by inflammatory cells. Aggregates are radiating arrangements of clubshaped and mixed filamentous and coccobacilli (sulfur granules). Bacteria within the granules are typically Gram-positive, but degenerating bacteria around the periphery are Gram-negative.

Handeland et al. (2001); Thompson (2007); Wobeser (2001)

Common opportunistic pathogen may cause localized abscesses, mastitis, pneumonia, chronic fibrinous pleuritis, peritonitis, or systemic disease/sepsis. Adhesions may be present in chronic pleuritis and peritonitis.

Cutaneous or multisystemic abscesses with intralesional pleomorphic Grampositive coccobacilli to short rods. In more severe cases abscesses and inflammation may extend to pleural and peritoneal cavities and the development of pyothorax and ascites

Handeland et al. (2001); Portas and Bryant (2005)

ID of bacteria cultured from fresh or frozen tissue, infections are often mixed bacteria.

(Continued)

141.e10 Pathology of Wildlife and Zoo Animals

TABLE e6 Bacterial Diseases of Importance in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.)

TABLE e6 Bacterial Diseases of Importance in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.) Diseases

Etiology (Genus, Species) Species Affected Gross Lesions Fusobacterium necrophorum Oral lesions are often mixed anaerobic infections, esp. with Trueperella pygenes. Digital dermatitis is often a mixed anaerobic infection, esp. with Dichelobacter nodosus

Leptospirosis

All artiodactyls, Leptospira spp., esp. serovars of L. Pygmy hippos; captive interrogans

All artiodactyls susceptible, especially springbok, impala, roan antelope

Microscopic Lesions

Keys to Diagnosis

References

Gross: acute to chronic, necrotizing dermatitis and cellulitis, esp. feet (interdigital) and oral cavity. Pododermatitis/digital necrobacillosis-necrotizing and ulcerative dermatitis and cellulitis with draining tracts, chronic lesions may extend to arthritis, tenosynovitis, and osteomyelitis. Oral necrobacillosis-focal to multifocal necrotizing and ulcerative stomatitis, pharyngitis, laryngitis, osteomyelitis. Pseudomembrane formation may result in aspiration pneumonia, esophagitis, necrotizing forestomach lesions. Sepsis may occur from any lesion, reported in pronghorn with pododermatitis and necrotic stomatitis. Balanoposthitis reported in European bison, likely secondary to extensive fecal contamination of ventral hair coat and skin.

Necrosis with acute to chronic suppurative inflammation, vasculitis, and thrombosis. Filamentous rod bacteria in inflammatory infiltrate around periphery of lesions. Granulation tissue, fibrosis, osteomyelitis increase with chronicity.

ID of bacteria cultured from fresh or frozen tissue, infections are often mixed bacteria.

Edwards et al. (2001); Handeland et al. (2001); Jakob et al. (2000); Wobeser (2001)

Gross lesions are nonspecific. In acute cases, lesions are secondary to acute septicemia, hepatitis, and nephritis: hemolytic anemia with hemorrhage, hemoglobinuria, icterus, hepatomegaly with enhanced lobular pattern, renomegaly and edema, disseminated serosal and parenchymal hemorrhage. Chronic renal lesions may be severe, end-stage with extensive fibrosis.

Microscopic lesions vary with disease presentation. Acute septicemic and hemolytic lesions: pulmonary edema, acute zonal hepatic necrosis (esp. centrilobular) with Kupffer cell hemosiderosis; acute renal tubular necrosis with granular and cellular casts, tubular epithelial pigment (hemoglobin, hemosiderin, bile), mats of spiral bacteria in affected tubules. Chronic disease-nonspecific chronic renal changes Hippos-chronic tubulointerstitial nephritis with glomerulonephritis, glomerulosclerosis, and fibrosis

Microscopic identification of silver-positive spiral bacteria in renal tubular lesions; IFA or IHC for leptospires in lesions; simple or multiplex PCR of fresh, frozen, or fixed tissues.

Ahmed et al. (2012); Flacke et al. (2016); Maxie and Newman (2007); Wobeser (2001)

141.e11

(Continued)

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

Necrobacillosis, Fusobacteriosis

Diseases

Etiology (Genus, Species) Species Affected Gross Lesions

Microscopic Lesions

Keys to Diagnosis

Epidermal hyperplasia and hyperkeratosis with serosuppurative exudation and crusting, with intraepidermal and dermal abscesses. Cytological preparation of material from moist dermatitis-linear/filamentous colonies of Gram-positive coccoid bacteria with transverse and longitudinal septation, resulting in a “tram-track” appearance

Identification of charHandeland et al. acteristic pleomorphic (2001) Gram-positive bacterial colonies with cytologic preparations of material from moist skin lesions

References

Dermatophilosis, Dermatophilus streptothricosis, congolensis contagious dermatitis

All artiodactyls, Focal, multifocal, or generalized disease infreproliferative and exudative dermaquently reported titis. Matted hair coat, crusting in free-ranging animals despite moderate seroprevalence, disease more common in captivity

Foot rot

Dicheobacter nodosus, Treponema spp. Often present in mixed anaerobic infections, esp. with Fusobacterium necrophorum

All artiodactyls, Ovinae and Caprinae, esp. ibex, more susceptible.

Necrotizing and ulcerative digital Similar to F. necrophorum digital derand pododermatitis with digital matitis swelling; similar to F. necrophorum, often more severe. Separation and sloughing of horn starting at heel occurs Some keratinolytic strains of D. nodosus

ID of bacteria cultured from fresh or frozen tissue, infections are often mixed bacteria. A two-step PCR reported for detection of D. nodosus in foot rot in free-ranging European ibex and mouflon.

Belloy et al. (2007) Handeland et al. (2001)

Erysipelas

Erysipelothrix rhusiopathiae

All artiodactyls. Uncommon, often associated with access to water/ marshlands. Recent outbreak reported in free-ranging Canadian muskoxen

May cause localized abscesses and cellulitis, endocarditis, or sepsis with disseminated embolic disease. Polyarthritis in domestic Ovinae and Caprinae not reported in nondomestics.

ID of bacteria cultured from fresh or frozen tissue, PCR

Handeland et al. (2001) Kutz et al. (2015)

With embolic disease, septic thrombi are widely disseminated and may be prominent in liver, kidney, spleen lung, heart, and other viscera. Vessels may contain increased numbers of marginated phagocytes with large numbers of intracytoplasmic Gram-positive rods

Esp, especially; ID, identification; IFA, immunofluorescent antibody; IHC, immunohistochemistry; PCR, polymerase chain reaction. Ahmed, S.A., Sandai, D.A., Musa, S., Hoe, C.H., Riadzi, M., Lau, K.L., Tang, T.H., 2012. Rapid diagnosis of leptospirosis by multiplex PCR. Malays. J. Med. Sci. 19, 9–16. Allchurch, A.F., 2003. Yersiniosis in all taxa. In: Fowler, M.E., Miller, R.E., Morris Animal Foundation. (Eds.), Zoo and Wild Animal Medicine, fifth ed. Saunders, St. Louis, Mo, pp. xvi, 782 p. (Chapter 74). Belloy, L., Giacometti, M., Boujon, P., Waldvogel, A., 2007. Detection of Dichelobacter nodosus in wild ungulates (Capra ibex ibex and Ovis aries musimon) and domestic sheep suffering from foot rot using a two-step polymerase chain reaction. J. Wildl. Dis. 43, 82–88. Brown, C.C., Baker, D.C., Barker, I.K., 2007. Bacterial diseases of the alimentary tract. In: Maxie, M.G., Jubb, K.V.F., Kennedy, P.C., Palmer, N. (Eds.), Jubb, Kennedy, and Palmer’s Pathology of Domestic Animals, fifth ed. Elsevier Saunders, Edinburgh, New York, pp. 183–228. Cranfield, M., Eckhaus, M.A., Valentine, B.A., Strandberg, J.D., 1985. Listeriosis in Angolan giraffes. J. Am. Vet. Med. Assoc. 187, 1238–1240. Edwards, J.F., Davis, D.S., Roffe, T.J., Ramiro-Ibanez, F., Elzer, P.H., 2001. Fusobacteriosis in captive wild-caught pronghorns (Antilocapra americana). Vet. Pathol. 38, 549–552. Ferroglio, E., 2001. Listeria infections. In: Williams, E.S., Barker, I.K. (Eds.), Infectious Diseases of Wild Mammals, third ed. Iowa State University Press, Ames, pp. viii, 558 p. Flacke, G.L., Tkalcic, S., Steck, B., Warren, K., Martin, G.B., 2016. A retrospective analysis of mortality in captive pygmy hippopotamus (Choeropsis liberiensis) from 1912 to 2014. Zoo Biol. 35, 556–569. Gasper, P.W., Watson, R.P., 2001. Plague and yersiniosis. In: Williams, E.S., Barker, I.K. (Eds.), Infectious Diseases of Wild Mammals, third ed. Iowa State University Press, Ames, pp. viii, 558 p. Handeland, K., Spec, S., Birtles, R., Jansson, D.S., Gortazar, C., Gavier-Widén, D., Weissenbock, H., Duff, J.P., 2001. Other bacterial infections. In: Williams, E.S., Barker, I.K. (Eds.), Infectious Diseases of Wild Mammals, third ed. Iowa State University Press, Ames, pp. 428–451. Jakob, W., Schroder, H.D., Rudolph, M., Krasinski, Z.A., Krasinska, M., Wolf, O., Lange, A., Cooper, J.E., Frolich, K., 2000. Necrobacillosis in free-living male European bison in Poland. J. Wildl. Dis. 36, 248–256. Kutz, S., Bollinger, T., Branigan, M., Checkley, S., Davison, T., Dumond, M., Elkin, B., Forde, T., Hutchins, W., Niptanatiak, A., Orsel, K., 2015. Erysipelothrix rhusiopathiae associated with recent widespread muskox mortalities in the Canadian Arctic. Can. Vet. J. 56, 560–563. Maxie, M.G., Newman, S.J., 2007. Urinary system. In: Maxie, M.G., Jubb, K.V.F., Kennedy, P.C., Palmer, N. (Eds.), Jubb, Kennedy, and Palmer’s Pathology of Domestic Animals, fifth ed. Elsevier Saunders, Edinburgh, New York, p. 1 online resource (3 v.). Morner, T., 2001. Salmonellosis, third ed. Iowa State University Press, Ames. Portas, T.J., Bryant, B.R., 2005. Morbidity and mortality associated with Arcanobacterium pyogenes in a group of captive blackbuck (Antilope cervicapra). J. Zoo Wildl. Med. 36, 286–289. Thompson, K., 2007. Bones and joints. In: Maxie, M.G., Jubb, K.V.F., Kennedy, P.C., Palmer, N. (Eds.), Jubb, Kennedy, and Palmer’s Pathology of Domestic Animals, fifth ed. Elsevier Saunders, Edinburgh, New York, pp. 1–184. Webb, D.M., Rebar, A.H., 1987. Listeriosis in an immature black buck antelope (Antilope cervicapra). J. Wildl. Dis. 23, 318–320. Wobeser, G., 2001. Miscellaneous bacterial infections. In: Williams, E.S., Barker, I.K. (Eds.), Infectious Diseases of Wild Mammals, third ed. Iowa State University Press, Ames, pp. viii, 558 p.

141.e12 Pathology of Wildlife and Zoo Animals

TABLE e6 Bacterial Diseases of Importance in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.)

TABLE e7 Fungal Diseases of Importance in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae

Disease

Etiology (Family, Genus)

Species Affected

Gross Lesions

Histologic Lesions

Keys to Diagnosis

References

All artiodactyls, worldwide

Dermatopathy similar to those in other species. Alopecia, hyperkeratosis, pustular dermatitis or folliculitis.

Acute to chronic proliferative and hyperkeratotic dermatitis, folliculitis, furunculosis, intralesional dermatophytes.

ID of dermatophytes in tissue section, culture on selective medium.

Burek (2001); Cafarchia et al. (2012)

Cryptococcosis Cryptococcus gattii, C. neoformans

All artiodactyls, worldwide, uncommon; esp. captive animals, coastal Western USA.

Similar to other mammals, chronic mucinous to granulomatous rhinitis, sinusitis, meningoencephalitis. Large amounts of clear gelatinous mucinous material may be present in lesions.

Histiocytic to pyogranulomatous inflammation with variable amounts of clear to mucinous matrix. Lesions contain round 5–20 µm diameter yeast. Inflammation around yeast is often minimal and separated from the yeast by the prominent capsule.

ID of yeast in lesions: PAS-and silver- positive yeast with thick clear capsule that stains pink-red with mucicarmine stains; blue with Alcian blue stains. India ink staining of cytologic preparations outlines the thick yeast capsule. PCR.

Burek (2001); Cafarchia et al. (2012)

Blastomycosis

Blastomyces dermatitidis

All artiodactyls, uncommon regional disease, esp. central and Eastern USA, occurs worldwide.

Similar to other mammals, granulomatous pneumonia, possibly disseminated granulomatous disease.

Pyogranulomatous pneumonia or extrapulmonary inflammation with extracellular and intracellular (phagocytized) round 5–25 µm diameter yeast.

ID of yeast in lesions: PAS-and silver- positive yeast with doublecontoured wall. Yeast may exhibit broad-based budding. PCR.

Burek (2001); Cafarchia et al. (2012)

Histoplasmosis Histoplasma capsulatum

All artiodactyls, uncommon, regional disease, esp. central and Eastern USA.

Similar to other mammals, granulomatous pneumonia, possibly disseminated granulomatous disease, esp. affecting the digestive tract. Miliary foci of granulomatous inflammation may be disseminated in lungs, liver, spleen, viscera

Histiocytic to pyogranulomatous pneumonia or extrapulmonary inflammation with 5–15 µm diameter round to oval intracellular yeast.

ID of yeast in lesions: PAS-and silver- positive yeast with very thin cell wall and no capsule. PCR, IHC.

Cafarchia et al. (2012)

Coccidioidomycosis

All artiodactyls, uncommon, regional disease, esp. in Southwestern USA

Chronic pyogranulomatous pneumonia, may progress to disseminated pyogranulomatous disease. Fungal osteomyelitis with periosteal proliferation is recognized in domestic mammals.

Suppurative to pyogranulomatous inflammation with fungal spherules 20–200 µm in diameter. Multinucleated giant cells may predominate in chronic active infections.

Some spherules may contain distinct endospores.

Burek (2001); Cafarchia et al. (2012)

All artiodactyls, uncommon and opportunistic, often secondary to other diseases.

Gross lesions are variable and depend on agent and affected tissues, typically similar to those in other mammals. Variable, granulomatous to pyogranulomatous inflammation, esp. wound contamination; Mucor sp. and Rhizopus sp. cause necrotizing encephalitis.

Microscopic lesions depend on agent and tissue affected. Identification of nonpigmented or pigmented hyphal structures in lesions.

Identification of nonpigmented or pigmented hyphal structures in lesions. ID of classes of fungi by hyphal morphology and pigmentation. Aspergillus sp. may be normal aural flora in Giraffidae.

Allender et al. (2008) ; Cafarchia et al. (2012)

Dermatophytosis

Primarily Microsporum spp., Trichophyton spp.

Coccidioides immitis, C. posadasii

Opportunistic Aspergillus fungal diseases spp., Mucor spp., Fusarium spp., Rhizopus spp.

ID, identification; PCR, polymerase chain reaction; IHC, immunohistochemistry; PAS, Periodic acid-Schiff. Allender, M.C., Langan, J., Citino, S., 2008. Investigation of aural bacterial and fungal flora following otitis in captive okapi (Okapia johnstoni). Vet. Dermatol. 19, 95–100. Burek, K., 2001. Mycotic diseases. In: Williams, E.S., Barker, I.K. (Eds.), Infectious Diseases of Wild Mammals, third ed. Iowa State University Press, Ames, pp. 514–531. Cafarchia, C., Eatwell, K., Jansson, D.S., Meteyer, C.U., Wibbelt, G., 2012. Other fungal infections. In: Gavier-Widén, D., Duff, J.P., Meredith, A. (Eds.), Infectious Diseases of Wild Mammals and Birds in Europe. Blackwell Publishing, Chichester, West Sussex, UK, Malden, MA, pp. 466–745.

Parasite Cestodes

Etiology (Family, Genus) Species Affected

Gross Lesions

Histologic Lesions

Keys to Diagnosis

References

Cystic echinococcosis, hydatidosis Echinococcus granulosus

Worldwide. Intermediate hosts: Bovidae, Giraffidae, Antilocapridae, Hippopotamidae. Definitive hosts: Canid definitive host: dogs, wolves, foxes, jackals, dingos. Zoonotic.

Lesions in intermediate hosts: Early disease-small indistinct nodules, white to yellow. Subacute and chronic disease-fluid-filled unilocular cysts within liver, lungs, other viscera. Cysts are often white to yellow, variable amounts of fluid, with finely granular lining consisting of larval cestodes.

Expansile unilocular parasitic cysts. Cysts are lined by an eosinophilic layer and internal brood capsules containing metacestode protoscolices and calcareous corpuscles. Hooklets are acidfast. Brood capsules may exhibit external budding, resulting large proliferative cystic masses, though most are unilocular. Granulation tissue and fibrosis are common in affected parenchymal organs.

Identification of unilocular parasitic cysts with metacestodes and characteristic protoscolices. PCR of cyst material to differentiate from metacestodes of other taeniid cestodes (e.g., T. hydatigena, E. multilocularis).

Craig et al. (2015); Boufana et al. (2017); Maxie and Jubb (2007)

Alveolar echinococcosis, hydatidosis Echinococcus multilocularis

Worldwide. Intermediate hosts Primarily Bovidae, also Hippopotamidae, Giraffidae, Antilocapridae, Tragulidae Definitive hosts: Canid definitive host: dogs, wolves, foxes, jackals. Zoonotic.

Lesions in intermediate hosts: Variably-sized fluid-filled unilocular to multilocular cysts in abdominal cavity, within liver and bulge from surface. Lungs, other viscera less frequently affected. Cysts are often white to yellow, variable amounts of fluid, with finely granular lining consisting of larval cestodes.

Expansile multilocular or alveolar parasitic cysts. Cysts are lined by an eosinophilic layer and internal brood capsules containing metacestode protoscolices and calcareous corpuscles. Hooklets are acid-fast. Brood capsules may exhibit external budding, resulting large proliferative cystic masses. Granulation tissue and fibrosis are common in affected parenchymal organs.

Identification of multilocular parasitic cysts with metacestodes and characteristic protoscolices. PCR of cyst material to differentiate from metacestodes of other taeniid cestodes.

Boufana et al. (2017); Maxie and Jubb (2007)

Taeniaisis Taenia spp.

Intermediate hosts: Hippopotamidae, Bovidae, Giraffidae, Antilocapridae, Tragulidae Definitive hosts: carnivores, omnivores, esp. Canidae and Felidae

Lesions in intermediate hosts: cysticercosis/coenurosismetacestode cysts in liver, abdominal cavity, striated muscle, brain (cestode species influences tissue distribution), possible larval parasite migration tracts in liver, other viscera, nervous system.

Parasitic cysts in tissues, serosal surfaces. Cysts have thin walls lined by a thin eosinophilic outer layer and enclose metacestode with tegument, cystic body, with suckers, inverted scolices and calcareous corpuscles. Hooklets (absent in T. saginata) are acid-fast.

Identification of unilocular parasitic cysts with metacestodes and characteristic protoscolices.

Miller and Fowler (2015); Bowman and Georgi (2009); Maxie and Jubb (2007)

141.e14 Pathology of Wildlife and Zoo Animals

TABLE e8 Specific Cestodes and Trematodes That Have Demonstrated Clinically Significant Disease or Pose Zoonotic Risk in Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae

TABLE e8 Specific Cestodes and Trematodes That Have Demonstrated Clinically Significant Disease or Pose Zoonotic Risk in Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.) Parasite

Etiology (Family, Genus) Species Affected

Gross Lesions

Histologic Lesions

Keys to Diagnosis

References

Identification of adult cestodes in rumen, ova in feces.

Miller and Fowler (2015); Bekenov et al. (1998); Munang’andu et al. (2012)

Intermediate host: orobatid mites. Definitive host: Hippopotamidae, Bovidae, Giraffidae, Antilocapridae, Tragulidae

Monezia: Adults in rumen; Thsanosoma, Avitellina, Stilesia, adults in bile ducts, small intestine. Gross lesions are rare. Heavy parasite burdens may contribute to outbreaks of enterotoxemia, esp. M. expansa) in migrating saigaantelope (Saiga tatarica). Stilesia may cause cystic bile duct changes in some animals.

Adult cestodes in rumen, bile ducts, or small intestine. Scolex of adult cestodes lacks rostellum and hooklets.

Trematodes Fasciola hepatica

Worldwide. Intermediate hosts: snails. Definitive hosts: Freeranging ruminants, Ovinae, Caprinae, American bison others, similar to domestic animals, free-ranging cervids.

Adult flukes in bile ducts, biliary cysts, portal fibrosis. American bison, Ovinae, Caprinae, many other noncervid ruminants: Severe liver, lung damage, peritonitis due to larval parasite migration. Migration tracts on subcapsular surface of liver.

Trematodes in bile ducts, chronic Adults in bile ducts with bilisuppurative cholangiohepatitis, ary cysts, duct fibrosis. cystic biliary hyperplasia, portal fibrosis. Bison, American bison, Ovinae, Caprinae: necrotizing peritonitis and hepatitis and hemorrhage along parasite migration tracts. Eosinophilic inflammation followed by granuloma formation.

Foreyt (2009); Foreyt and Drew (2010); Miller and Fowler (2015)

Similar to F. hepatica

Similar to F. hepatica

Similar to F. hepatica

Miller and Fowler (2015); Munang’andu et al. (2012)

Adult flukes in cysts within hepatic parenchyma, not in bile ducts. Cysts may be mistaken for pigmented neoplasms. Larval migration similar to that described for F. Hepatica.

Necrotic and hemorrhagic migration tracts similar to those in F. Hepatica. Heavily pigmented cysts within hepatic parenchyma, abundant iron-porphyrin pigment. Ova within parenchyma around cysts induce granulomata.

Identification of adult trematodes within hepatic parenchymal cysts, larval trematodes in necrotic migration tracts.

Foreyt (2009); Foreyt and Drew (2010)

Fasciola gigantica African Bovidae, esp. African buffalo and antelope spp., for example, lechwe Fascioloides magna

North America and Europe, rarely reported in noncervid ruminants, severe liver damage due to parasite migration, esp. Ovinae, Caprinae.

(Continued)

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

Anoplocephaliasis Moniezia spp., Thysanosoma spp., Avitellina spp., Stilesia spp.

141.e15

Parasite

Etiology (Family, Genus) Species Affected Schistosoma: Schistosoma hippopotami, S. edwardiense

Intermediate host: snails Definitive host: Free-ranging Hippopotamidae

Paramphistomes: Intermediate host: snails Paramphistomum Definitive host: Bovidae spp., Calicophoron spp., Cotylophoron spp.

Gross Lesions

Histologic Lesions

Keys to Diagnosis

References

H. hippopotami-adult schistosomes in heart chambers and systemic vessels, esp. mesentery. H. edwardiense-adults and ova in the hepatic vessels, granulomas in the liver.

H. hippopotami in heart and vessels, possible endocarditis pulmonary and systemic endarteritis. H. edwardiense-granulomatous portal and periportal hepatitis with portal fibrosis progressing to cirrhosis

S. edwardiense in hepatic blood vessels and ova have a lateral spike/spine, S. hippopotami from heart, great vessels, mesentery-ova with subterminal spike or spine.

Cowan et al. (1967); Miller and Fowler (2015)

Adults in rumen. Metacercaria excyst in small intestine, gross lesions include migration tracts from small intestine to reticulum and rumen.

Subacute to chronic necrotizing and eosinophilic enteritis and reticulorumentitis with larval trematodes.

Identification of adult cestodes in rumen, ova in feces.

Bowman and Georgi (2009)

Bekenov, A.B., Grachev, I.A., Milner-Gulland, E.J., 1998. The ecology and management of the Saiga antelope in Kazakhstan. Mamm. Rev. 28, 1–52. Boufana, B., Said, Y., Dhibi, M., Craig, P.S., Lahmar, S., 2017. Reprint of Echinococcus granulosus sensu stricto (s.s.) from the critically endangered antelope Addax nasomaculatus in Tunisia. Acta Trop. 165, 17–20. Bowman, D.D., Georgi, J.R., 2009. Georgis’ Parasitology for Veterinarians, ninth ed. Saunders/Elsevier, St. Louis, Mo. Cowan, D.F., Thurlbeck, W.M., Laws, R.M.., 1967. Some diseases of the hippopotamus in Uganda. Pathol. Vet. 4, 552–567. Craig, P., Mastin, A., van Kesteren, F., Boufana, B., 2015. Echinococcus granulosus: epidemiology and state-of-the-art of diagnostics in animals. Vet. Parasitol. 213, 132–148. Flacke, G.L., Tkalcic, S., Steck, B., Warren, K., Martin, G.B., 2016. A retrospective analysis of mortality in captive pygmy hippopotamus (Choeropsis liberiensis) from 1912 to 2014. Zoo Biol. 35, 556–569. Foreyt, W.J., 2009. Experimental infection of bighorn sheep with liver flukes (Fasciola hepatica). J. Wildl. Dis. 45, 1217–1220. Foreyt, W.J., Drew, M.L., 2010. Experimental infection of liver flukes, Fasciola hepatica and Fascioloides magna, in Bison (Bison bison). J. Wildl. Dis. 46, 283–286. Maxie, M.G., Jubb, K.V.F., 2007. Pathology of domestic animals, fifth ed. Elsevier Saunders, Edinburgh, New York. Miller, R.E., Fowler, M.E., 2015. Fowler’s Zoo and Wild Animal Medicine, eighth ed. Elsevier/Saunders, St. Louis, Missouri. Munang’andu, H.M., Siamudaala, V.M., Munyeme, M., Nalubamba, K.S., 2012. Detection of parasites and parasitic infections of free-ranging wildlife on a game ranch in zambia: a challenge for disease control. J. Parasitol. Res. 2012, 296475.

141.e16 Pathology of Wildlife and Zoo Animals

TABLE e8 Specific Cestodes and Trematodes That Have Demonstrated Clinically Significant Disease or Pose Zoonotic Risk in Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.)

TABLE e9 Ectoparasites of Importance in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae Disease

Parasite

Species Affected

Clinical Signs/Gross Lesions

Histologic Lesions

Keys to Diagnosis

References

Sarcoptic mange, scabies

Sarcoptes scabiei

Worldwide-Many free-ranging ungulates including multiple species of nondomestic Bovidae, Antilocapridae, Giraffidae. Fatal outbreaks in European chamois and ibex, African giraffe. Zoonotic.

Localized or generalized pruritic and exudative dermatitis: matted and crusted coat, alopecia, serous exudate and crusting, hyperkeratosis, hyperpigmentation.

Primarily epidermal lesions, acanthosis, hyperkeratosis, serocellular crusts entrapping keratin rafts. Parakeratosis, pustules, edema, suppurative inflammation in regions of excoriation, eosinophilic and mast cell dermatitis. Mite eggs, larvae, nymphs, and adults in burrows within epidermis, predominantly strata spinosum, granulosum, and corneum.

Identification of mites in epidermal lesions, morphology of mites on cytologic preparations of deep skin scrapings. Adult mites have characteristic triangular dorsal spines. Type I and IV hypersensitivity to mite antigens likely contribute to lesions.

Alasaad et al. (2012); Bornstein et al. (2001); Pence and Ueckermann (2002)

Demodicosis

Demodex spp.

Most ruminants may be affected, but not commonly reported. Mites exhibit some species specificity. D. cafferi commonly infests African buffalo. Other Demodex sp. infest American and European bison, and free-ranging European chamois.

Nodular, papular, or pustular dermatitis over head and neck may be widely disseminated. Nodules may be up to 1 cm in diameter and exude viscous to waxy keratinaceous material, if disrupted. Lesions may be periocular and perineal in American bison.

Primarily follicular cysts and mild chronic lymphoplasmacytic dermatitis. Cysts contain myriad mites and accumulated keratin and debris. Ruptured cysts may evoke a local foreign-body-type reaction.

Identification of mites in epidermal lesions, morphology of mites on cytologic preparations of cyst material.

Maxie and Jubb (2007); Wolhuter et al. (2009)

Psoroptic mange

Psoroptes spp.

P. ovis infection is moderately common in some populations of free-ranging bighorn sheep

Localized or regional pruritic crusting and alopecic dermatitis. May primarily affected ears, face, and muzzle, or extend to neck, shoulders, back, or legs. Crusting and alopecia, erythema, papule formation, lichenification.

Mites are limited to the skin surface and stratum corneum, but do not burrow into stratum granulosum or deeper epidermis. Epidermal acanthosis and hyperkeratosis, edema, ± serous exudate. Eosinophilic and lymphoplasmacytic dermatitis with severe edema. Type IV hypersensitivity may contribute to disease.

Diagnosis is through identification of mites and eggs on ear swabs and skin scraping. May be a reportable disease in some regions.

Cassirer and Sinclair (2007); Miller and Fowler (2015)

Acariasis

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

(Continued)

141.e17

Disease

Parasite

Species Affected

Clinical Signs/Gross Lesions

Histologic Lesions

Keys to Diagnosis

References

Oestrinae Nasal bots

Multiple genus and species. Pharyngomyia spp., Cephenemyia spp., Kirkioestrus spp., Rhinoestrus spp.,Oestrus spp., Gedoelstia spp.,Oestrus spp., others

Primarily affects the Bovidae, mixed infestations are common in free-ranging African bovids.

1st, 2nd, and 3rd instar larvae in nasal passages, sinuses, palatal and pharyngeal pouches. Mucopurulent nasal discharge or may be no gross lesions.

Chronic suppurative and/or eosinophilic inflammation at the site of infestation.

Identification of 1st to 3rd instar larvae in lesions or 3rd instar larvae exiting the nasal passages.

Colwell (2001)

Hypodermatinae Subcutaneous bots/warbles

Hypoderma spp., Primarily affects the Bovidae, especially Cuterebra spp. klipspringer but all ungulate species may be affected

Nodular dermatitis. Nodules are subcutaneous or dermal sinus cavities that communicate with the surface and contain 2nd to 3rd instar larvae. Possible anaphylactoid type I hypersensitivity if larvae are ruptured in the cyst.

Larval stages enclosed in subdermal cysts, chronic suppurative or eosinophilic dermatitis with foreign-bodytype reaction.

Calliphoridae Primary screwworms, secondary blowflies/ bottleflies

Primary infestations of living tissues: Cochilomyia hominovorax (new world screwworm), Chrysomya bezziana (old world screwworm), Secondary infestations of necrotic tissues: blowflies/bottle flies, others

All mammals

Primary: Circular wounds that enlarge, with fetid purulent discharge. Larvae/maggots in lesions, may be deep and not externally visible. Navel infestations in newborn animals, otherwise infect traumatic injuries.

Ulceration with fibrinosuppurative and necrotizing dermatitis, panniculitis, and myositis. Larval stages/ maggots of primary screwworms embedded deep in wounds, secondary worms in superficial necrotic tissues. Severe secondary bacterial infection is common.

Multiple, esp. Aedes spp., Culex tarsalis, Coquillettidia spp., Psorophora columbiae

Most ungulate species are affected by multiple mosquito spp.

Local or generalized pruritic papules. Overwhelming swarming (esp. P. columbiae and Aedes spp.) may result in acute hypovolemia and death. Some species are important vectors for transmission of arboviruses, nematodes (e.g., Setaria labiatopalillosa).

Papular dermatitis with neutrophilic, Identification of adult eosinophilic, and lymphoplasmamosquitoes. cytic inflammation. Exsanguination in cases of overwhelming swarms. Type IV hypersensitivity may contribute to delayed reactions and persistence of papules.

Myiasis

Colwell (2001)

Identification of larvae in deepest part of wounds. Primary screwworm infestation is a reportable disease.

De Deken (2004); Samuel et al. (2001)

Biting Flies Mosquitoes

Allan (2001a)

141.e18 Pathology of Wildlife and Zoo Animals

TABLE e9 Ectoparasites of Importance in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.)

TABLE e9 Ectoparasites of Importance in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.) Parasite

Biting midges

Phlebotomine sand flies

Lutzomyia spp. (New world), Phlebotomus spp. (Africa and Asia)

Glossinidae

Species Affected

Clinical Signs/Gross Lesions

Histologic Lesions

Keys to Diagnosis

References

Most ungulate Culicoides spp., species, esp. North Leptoconops spp., Forcipomyia America, Europe spp., others

Papular, pustular, or vesicular dermatitis. Vector for Bluetongue virus and epizootic hemorrhagic disease (esp. pronghorn antelope, bighorn sheep), vesicular stomatitis virus, other viruses.

Similar to mosquitoes, may have bulla formation, petechial hemorrhage. Type IV hypersensitivity may contribute to delayed reactions and persistence of papules

Identification of adult midges.

Allan (2001a); van Vuuren and Penzhorn (2015)

Most ungulate species.

Papular dermatitis at bite wound sites, drops of blood may be present on surface. Lutzomyia vector for leishmaniosis, vesicular stomatitis virus

Similar to mosquitoes

Identification of adult flies Allan (2001a)

Subsaharan ungulate Glossina spp., multiple subgen- species era, “tsetse” flies, esp. G. morsitans and G. pallidipes.

Most important as vectors of African trypanosomiasis, nagana.

Similar to mosquitoes

Identification of adult flies van Vuuren and Penzhorn (2015)

Ixodidae Hard ticks

Numerous species. Important genera of Ixodidae in N. America-Ixodes, Amblyomma, and Dermacentor. Africa-Amblyomma, Rhipicephalus, Hyalommma. Also see tick toxicosis subsection.

All species are affected. A survey of free-ranging southern African giraffe, buffalo, and eland, 28 spp of tick were identified, the most common ticks were A. hebraeum, R. appendulatus, R. decoloratus, H. truncatum.

Papules at tick bite wound sites. Large numbers of ticks adherent to the host, with localized papular dermatitis at bite wound sites. Naive animals moving into infested areas may suffer mortality due to exsanguination. Most important as vectors for protozoal, rickettsial, and viral disease, and tick toxicoses.

Similar to mosquitoes, more severe. Identification of larvae, May develop dermal and subcutane- nymphs, and adults ous eosinophilic and lymphohistiocytic nodules.

Allan (2001b); Horak et al. (2007); van Vuuren and Penzhorn (2015)

Argasidae Soft ticks

Numerous species. North Americaesp. Otobius spp. Africa-esp. Ornithodoros spp.

Most ungulates affected, generally less significant than Ixodidae.

Papules at tick bite wound sites. Most commonly infest ears. Most important as vectors for protozoal, rickettsial, and viral disease, and tick toxicoses.

Similar to Ixodidae

Identification of larvae, nymphs, and adults

Allan, (2001b); Horak et al. (2007); van Vuuren and Penzhorn (2015)

Acariasis

141.e19

(Continued)

Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae Chapter | 5

Disease

Disease

Parasite

Species Affected

Clinical Signs/Gross Lesions

Histologic Lesions

Keys to Diagnosis

References

Numerous spp. within suborders Anoplura (suckinglice) and Mallophaga (biting lice)

Most ungulates

Often incidental. May result in epidermal hyperplasia, hyperkeratosis, and alopecia. May reach high parasite burdens in captive animals and free-ranging animals in increased population densities. Death due to exsanguination is possible in untreated animals. May transmit hemoprotozoa, viruses, see relevant subsections.

Alopecia, epidermal hyperplasia, hyperkeratosis, eosinophilic and lymphoplasmacytic dermatitis. May induce Type I and Type IV hypersensitivities.

Identification of adults on skin.

Durden (2001)

Other ectoparasites Lice

Alasaad, S., Ndeereh, D., Rossi, L., Bornstein, S., Permunian, R., Soriguer, R.C., Gakuya, F., 2012. The opportunistic Sarcoptes scabiei: a new episode from giraffe in the drought-suffering Kenya. Vet. Parasitol. 185, 359–363. Allan, S.A., 2001a. Biting flies. In: Samuel, W.M., Kocan, A.A., Pybus, M.J., Davis, J.W. (Eds.), Parasitic Diseases of Wild Mammals, second ed. Iowa State University Press, Ames, pp. viii, 559 p. Allan, S.A., 2001b. Ticks. In: Samuel, W.M., Kocan, A.A., Pybus, M.J., Davis, J.W. (Eds.), Parasitic Diseases of Wild Mammals, second ed. Iowa State University Press, Ames, pp. viii, 559 p. Bornstein, S., Morner, T., Samuel, W.M., 2001. Sarcoptes scabiei and sarcoptic mange. In: Samuel, W.M., Kocan, A.A., Pybus, M.J., Davis, J.W. (Eds.), Parasitic Diseases of Wild Mammals, second ed. Iowa State University Press, Ames, pp. viii, 559 p. Cassirer, E.F., Sinclair, A.E., 2007 Dynamics of pneumonia in a bighorn sheep metapopulation. J. Wildl. Manage. 71, 1080–1088 Colwell, D.D., 2001. Bot flies and warble flies. In: Samuel, W.M., Kocan, A.A., Pybus, M.J., Davis, J.W. (Eds.), Parasitic Diseases of Wild Mammals, second ed. Iowa State University Press, Ames, pp. viii, 559 p. De Deken, R., 2004. EAZWV Transmissible Disease Handbook. In: Kaandorp, J., Chai, N., Byaens, A. (Eds.), p. 662. Durden, L.A., 2001. Lice. In: Samuel, W.M., Kocan, A.A., Pybus, M.J., Davis, J.W. (Eds.), Parasitic Diseases of Wild Mammals, second ed. Iowa State University Press, Ames, pp. viii, 559 p. Horak, I.G., Golezardy, H., Uys, A.C., 2007. Ticks associated with the three larges wild ruminant species in Southern Africa. Onderstepoort J. Vet. Res. 74, 231–242. Maxie, M.G., Jubb, K.V.F., 2007. Pathology of domestic animals, fifth ed. Elsevier Saunders, Edinburgh, New York. Miller, R.E., Fowler, M.E., 2015. Fowler’s Zoo and Wild Animal Medicine, eighth ed. Elsevier/Saunders, St. Louis, Missouri. Pence, D.B., Ueckermann, E., 2002. Sarcoptic manage in wildlife. Rev. Sci. Tech. 21, 385–398. Samuel, W.M., Kocan, A.A., Pybus, M.J., Davis, J.W., 2001. Parasitic Diseases of Wild Mammals, second ed. Iowa State University Press, Ames. van Vuuren, M., Penzhorn, B.L., 2015. Geographic range of vector-borne infections and their vectors: the role of African wildlife. Rev. Sci. Tech. 34, 139–149. Wolhuter, J., Bengis, R.G., Reilly, B.K., Cross, P.C., 2009. Clinical demodicosis in African buffalo (Syncerus caffer) in the Kruger National Park. J. Wildl. Dis. 45, 502–504.

141.e20 Pathology of Wildlife and Zoo Animals

TABLE e9 Ectoparasites of Importance in Nondomestic Bovidae, Antilocapridae, Giraffidae, Hippopotamidae, and Tragulidae (Cont.)

142 Pathology of Wildlife and Zoo Animals

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