Pathology in Practice

Ryan A. Yanez from the Department of Veterinary Clinical Sciences, College of Veterinary Medicine at the Ohio State University (Yanez); and Departments of Pathology (Yanez, Kirejczyk, Howerth) and Infectious Diseases (Sanchez), and Athens Veterinary Diagnostic Laboratory (Sanchez), College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Shannon G.M. Kirejczyk from the Department of Veterinary Clinical Sciences, College of Veterinary Medicine at the Ohio State University (Yanez); and Departments of Pathology (Yanez, Kirejczyk, Howerth) and Infectious Diseases (Sanchez), and Athens Veterinary Diagnostic Laboratory (Sanchez), College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Susan Sanchez from the Department of Veterinary Clinical Sciences, College of Veterinary Medicine at the Ohio State University (Yanez); and Departments of Pathology (Yanez, Kirejczyk, Howerth) and Infectious Diseases (Sanchez), and Athens Veterinary Diagnostic Laboratory (Sanchez), College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Elizabeth W. Howerth from the Department of Veterinary Clinical Sciences, College of Veterinary Medicine at the Ohio State University (Yanez); and Departments of Pathology (Yanez, Kirejczyk, Howerth) and Infectious Diseases (Sanchez), and Athens Veterinary Diagnostic Laboratory (Sanchez), College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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History

A 12-year-old sexually intact female llama (Lama glama) was submitted for necropsy following euthanasia (by IV injection of an unspecified drug) by the referring veterinarian. The llama had a 1-year-long history of a mass on the right mandible that was refractory to antimicrobial treatment. The llama was submitted with the carcass of a 2-year-old female llama that had a firm swelling on the left maxilla but was euthanized for unrelated reasons.

Gross Findings

On external examination, the llama had a body condition score of 1/5 with scant subcutaneous adi-pose stores. The oral cavity had a large amount of hay within the right buccal pouch. On cut section, the right mandible had a 15 X 8 X 8-cm, hard, expansile mass near the ramus of the mandible; as a result, the right mandible was approximately 4 times the thickness of the left mandible and the tongue was deviated to the left of midline (Figure 1). There was soft, gritty, pale tan to yellow material in the center of the mass. On the ventral surface of the mandible there were two 2- to 3-cm-diameter, irregular, ulcerated skin lesions. There was no notable deviation of the right mandibular premolar or molar teeth, and the mass did not appear to be centered on a specific tooth. There were no major gross changes observed in the nasal cavity. Most of the lung lobes were dark red to purple, and the cranial 15% of the lung lobes oozed serosanguineous fluid on cut section. The dorsal surfaces of the lungs had multifocal, white to tan, flat foci on the visceral pleura. There were multiple foci of air trapped beneath the visceral pleura on the dorsal surface of the left caudal lung lobe.

Figure 1
Figure 1

Photograph of a transverse section through the nasal turbinates and jaw of a 12-year-old llama (Lama glama) with a 1-year-long history of a mass on the right mandible that was refractory to antimicrobial treatment. The right mandible is markedly expanded by a 15 X 8 X 8-cm, ill-defined mass, which deviates the tongue to the left and has a central core of soft to gritty, tan to yellow material.

Citation: Journal of the American Veterinary Medical Association 259, 6; 10.2460/javma.259.6.613

Ancillary Testing

Aerobic culture of soft tissue from the center of the right mandibular lesion yielded very light growth of Actinomyces sp, α-hemolytic Streptococcus sp, and Aeromonas hydrophila/ punctata group bacteria. The isolated Actinomyces sp underwent DNA sequencing, and comparison of the 1,417-bp 16S rRNA sequence in a bioinformatics search toola revealed a best match (98% similarity) with Actinomyces cardiffensis.

Histopathologic Findings

Tissue samples, including a specimen of the right mandibular bone lesion, were collected for histologic examination. A preliminary diagnosis of pyogranulomatous filamentous bacterial osteomyelitis was made on the basis of histologic evaluation of necrotic tissue from the center of the mandibular mass. A transverse section of the bony mandibular lesion and surrounding soft tissue was decalcified; at the center of the mass, fragments of necrotic bone (Figure 2) characterized by hypereosinophilic matrix material and necrotic or absent osteocytes were surrounded by sheets of neutrophils, fewer macrophages, and large colonies of slender, 2- to 4-μm-long, gram-positive bacilli mixed with fewer gram-positive cocci and plant material (Figure 3). The necrotic core was surrounded by marked amounts of fibrosis, which extended into the surrounding soft tissues. The surrounding tissues were infiltrated by high numbers of lymphocytes, plasma cells, and macrophages and few neutrophils and multinucleated giant cells. There was abundant plant material embedded at the gingival sulcus of the overlying tooth and marked hyperplasia of the surrounding gingival mucosa. The slender bacilli were acid-fast negative, as determined by use of Ziehl-Neelsen and Fite-Faraco modified acid-fast staining methods.

Figure 2
Figure 2

Photomicrograph of a decalcified section of the right mandibular bone lesion. Notice the irregular fragments of necrotic trabecular bone (asterisks) composed of hypereosinophilic matrix and lacunae that are frequently empty. Necrotic bone is surrounded by intact and necrotic neutrophils mixed with large colonies of bacteria (arrowhead). H&E stain; bar = 20 μm.

Citation: Journal of the American Veterinary Medical Association 259, 6; 10.2460/javma.259.6.613

Figure 3
Figure 3

Photomicrograph of another section of the right mandibular bone lesion. Notice the large colonies of gram-positive filamentous bacilli. At the periphery of the colonies, the morphology of the slender, 2- to 4-μm-long, gram-positive bacilli is evident (arrows). Modified Brown and Brenn Gram stain; bar = 10 μm.

Citation: Journal of the American Veterinary Medical Association 259, 6; 10.2460/javma.259.6.613

Within sections of cranioventral lung tissue, a bronchiole had a moderate amount of karyorrhectic cellular debris admixed with small numbers of sloughed bronchial epithelium and lesser numbers of degenerated neutrophils. Small numbers of lymphocytes and plasma cells and occasional fibroblasts surrounded the bronchiole. The pleural surface had multifocal, small aggregates of lymphocytes; scattered plasma cells; and lesser numbers of fibroblasts with a large amount of disorganized collagen fibers.

The pericardial fat had extensive areas of adipocyte atrophy with accumulation of basophilic ground substance (serous atrophy of fat). In the third gastric compartment (C3), there was a mild proliferation of goblet cells and lymphoplasmacytic inflammation within the adjacent lamina propria.

Morphologic Diagnosis and Case Summary

Morphologic diagnosis: severe, chronic, multi-focal, pyogranulomatous mandibular osteomyelitis with intralesional gram-positive filamentous rods; mild, chronic, multifocal, lymphoplasmacytic pleuritis with fibrosis; chronic, diffuse serous atrophy of pericardial fat; and marked emaciation.

Case summary: mandibular actinomycosis (lumpy jaw) in a domestic llama.

Comments

The gross and microscopic findings for the llama of the present report were consistent with chronic mandibular actinomycosis. Mandibular osteomyelitis, also known as lumpy jaw, most commonly develops in cattle but also sporadically develops in horses, pigs, deer, sheep, and dogs.1 Actinomyces spp are gram-positive, filamentous anaerobes found in the oral cavity and respiratory and digestive tracts of healthy humans and domestic animals.2 Oral trauma, commonly as a result of poor husbandry, allows endogenous Actinomyces spp and other commensal organisms to invade and colonize the mucosa and underlying bone, likely forming a biofilm; the resulting chronic, deep-seated infection leads to multiple foci of bone resorption and proliferation and the accumulation of small, necrotic bone fragments.1 Consequently, bones of the mandible or maxilla become misshapen from abscesses, fibrosis, and fistulas.3

Actinomyces infection is commonly refractory to treatment, largely because of poor antimicrobial penetration of the resulting lesion and the difficulty of resolving opportunistic infections with potentially multiple commensal organisms. To our knowledge, the normal oral flora of camelid species has not been elucidated. Thus, the organisms cultured in the case described in the present report could potentially have represented commensals or exogenous pathogens. Although large aggregates of gram-positive bacilli may be surrounded by club-shaped, eosinophilic bodies (Splendore-Hoeppli material), this was not a feature in the present case.

Mandibular osteomyelitis caused by Actinomyces infection is rare in camelids, and the etiologic agents have proved to be difficult to grow in culture. Characteristic mandibular granulomas with filamentous gram-positive rods in exudate in camels have been reported, but the causative pathogens in those cases could not be determined.2 Horses typically develop cutaneous infections with Actinomyces spp; however, Actinomyces odontolyticus and Actinomyces viscosus have been identified in a severe mandibular infection in a horse.4 Infections with Actinomyces spp can result in nodules, abscesses, and draining fistulas in the mammary chains of swine.2 Dogs commonly develop cutaneous lesions when infected with A viscosus from bite wounds or foreign body–related trauma.5 In humans, 70% of actinomycosis cases involve Actinomyces israelii or Actinomyces gerencseriae in pulmonary infections related to aspiration, pelvic infections related to use of intrauterine devices, abdominal infections following appendectomy, and craniofacial infections following oral surgery.6

In the llama of the present report, serous atrophy of pericardial adipose tissue was indicative of a severe negative energy balance, which was likely multifactorial. Although gross or histologic evidence of parasitism was not evident, this possibility could not be completely ruled out as a contributing factor to the llama's emaciated state.

Sequencing of the DNA of the cultured Actinomyces sp in this case yielded a sequence that had 98% similarity with A cardiffensis, which has not been reported as an infective agent of camelids or other domestic animal species. Actinomyces cardiffensis was first described in 2002 as a novel Actinomyces sp in human clinical specimens.7 It has since been isolated from a 67-year-old man with septicemia and liver and lung abscesses.8 Although most cases of actinomycosis in humans are the result of opportunistic invasion of endogenous actinomycetes, zoonotic transmission has the potential to occur via an animal bite wound.9

Footnotes

a.

BLAST, National Center for Biotechnology Information, National Institutes of Health, Bethesda, Md. Available at: blast.ncbi.nlm.nih.gov/Blast.cgi?PROGRAM=blastn&PAGE_TYPE=BlastSearch&LINK_LOC=blasthome. Accessed May 9, 2018.

References

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