Conference 24 - 2015 Case: 03 20160504

Signalment:

5 year-old, castrated male, bovine (Bos taurus)The head was deformed by a hard swelling of the right maxilla of several months of evolution that resulted in difficult breathing and weight loss. Due to poor prognosis, the practitioner advised the owner to send the steer to the slaughterhouse.

Gross Description:
A 25x12cm hard mass extended from the base of the right ear to around the right eye. In the rostral end of the mass there was a 7x4 cm cavity filled with dark, friable necrotic tissue. At the cut surface of a section in middle part of the bridge of the nose, the nasal cavity was deformed by a mass consisting of bony proliferation. Within the mass, there were focally extensive semisolid (caseous) yellow areas of irregular contour. These areas were surrounded by a dark green halo (necrotic tissue). Extensive firm white fibrotic tissue was also noticed at the cut surface of the lesion. The lesion destroyed the nasal turbinates and markedly displaced the nasal septum to the left.

Histopathologic Description:
Lesions consist of multiple pyogranulomas surrounded by well-defined and well differentiated osseous trabeculae. In the center of these pyogranulomas there are structures co-nsisting of an inner mass of filamentous bacilli that stained blue (gram-positive) in the Gram stain. This center is su-rrounded by strongly eosinophilic radial clubs (Splendore Hoeppli [SH] ph-enomenon) which are, in turn, surrounded by an inner layer of neutrophils and an outer layer of epithelioid macrophages and occasionally multinucleated giant cells. Occasionally, these SH structures are mineralized. Extensive fibrous tissue sprinkled with neutrophils, lymphocytes, and plasma cells surrounds the inflammatory reaction and extend into adjacent soft tissues. In some HE-stained sections, weakly basophilic bacilli are seen in the cytoplasm of epithelioid cells, multinucleated giant cells, and in the center of the SH phenomenon; fragments of these structures were also phagocytosed by multinucleated giant cells.

Morphologic Diagnosis:
Maxillary pyogranulomatous osteomyelitis, castrated male, mixed breed, bovine.
Etiologic diagnosis: Bacterial osteomyelitis.

Etiology: Actinomyces bovis

Name of the condition: Actinomycosis.

Lab Results:
None.

Condition:
Lumpy jaw, Actinomyces bovis

Contributor Comment:
Actinomycosis is a pyogranulomatous osteomyelitis that primarily affects cattle and is caused by the gram-positive bacterium Actinomyces bovis.⁹ Occasionally other species such as pigs, deer, sheep, goats and horses are affected.⁹A similar species of bacterium, A. israeli, is responsible for the disease in human beings.⁶ The affected bone is thickened from multiple coalescing py-ogranulomas that impart to the bone tissue a honeycomb appearance.⁵ The inoculation of A. bovis – a commensal organism of the oral cavity – into the oral mucosa of animals can be facilitated by small wounds from hard straw present in the feed, foreign bodies and dental eruption.⁹

Although actinomycosis has been described in cattle at unusual sites such as the penis and in the maxilla, as in the case presented here, the classical presentation in cattle is in the mandible and rarely in the maxilla.^9,12 It is likely that the reason the mandible is the preferred site is because the direction of vegetal fibers being chewed is downwards forcing the fiber between the teeth and the gums, providing an entrance for the bacterium and resulting initially in a dental alveolitis.
Lesions of actinomycosis grow slowly over time^5,12 and the involvement of the bone and muscle tissue becomes so marked that it interferes with feeding,⁹ which would explain the emaciation of the ox of this report. In osteomyelitis caused by actinomycosis, initially there is development of suppurative sinus tracts in the medullary spaces of the bone leading to multiple foci of both bone tissue resorption and proliferation. Bone sequestration does not occur; even if the cortical bone is invaded, probably due to the progressive course of the disease.⁹ The small granules – known colloquially as sulfur granules – observed grossly at the center of the caseous nodules¹ represents the bacterial colonies and the associated SH phenomenon and are typical of actinomycosis, although can be seen in other pyogranulomatous diseases of cattle such as actinobacillosis and sta-phyloccocosis.⁸
Little is known about the virulence factors of A. bovis. The interaction between ligand-receptor in the target cells, toxins, molecules in the bacterial capsule that compromise phagocytosis, and other factors are probably involved in the pathogenicity of A. bovis. It is also probable that A. bovis is capable of escaping destruction by neutrophils and macrophages and is capable of colonizing the tissue abscesses. This peculiar resistance of the agent to phagocytosis leads to the formation – around itself – of proteinaceous eosinophilic aggregates consisting of immunoglobulins, which are observed histologically as the SH reaction.¹³Other bacteria induce similar tissue reactions, particularly Actinobacillus lig-nieresii. However A. bovis colonies are larger and the radiating clubs in the SH reaction are shorter and less marked that in actinobacillosis, and generally localized at the periphery of the colonies.^4,8,10 Ad-ditionally, actinobacillosis is a disease of soft tissues and the microorganisms of A. lignieresii, in contrast to those of A. bovis, are gram-negative.^5,8Fusobacterium nec-rophorum and other bacteria can cause osteomyelitis by direct extension of per-iodontitis; however lesions induced by F. necrophorum are usually more destructive and less proliferative.⁹

Grossly, a lesion such as the one described here can be mistaken for - and the lesion was initially interpreted as - a squamous cell carcinoma at the slaughterhouse. Due to great extension of the lesions and the invasive characteristics of the mass reported here, an intranasal squamous cell carcinoma should be in the top of the list as a differential diagnosis at gross examination since this is one of the tumors more frequently observed in the nasal cavity or ruminants.¹¹At cursory gross examination, the keratin commonly formed in these tumors may resemble the sulfur granules of actinomycosis.

JPC Diagnosis:
Bone: Osteomyelitis, pyogranulomatous, chronic, diffuse, severe, with bone resorption, Splendore-Hoeppli material, and numerous bacterial colonies

Conference Comment:
"Lumpy jaw" not only occurs in domestic species, but also occurs in many wild ungulates, where it can be particularly problematic due to ch-allenges associated with treating an ag-gressive infection in fractious animals. Ac-tinomyces bovis is the most commonly associated agent resulting in py-ogranulomatous mandibular (or rarely maxillary) osteomyelitis but bony ma-lformations of the jaw may also occur secondary to periodontal infection. Man-dibular osteomyelitis involving the dentition is an important casue of morbidity in older exotic hoofstock, where it has also been referred to as chronic alveolar os-teomyelitis.³ Inciting lesions may include a periodontal or tooth root abscess and/or a chronic pulpitis secondary to enamel or dentin abnormalities. Anaerobic bacteria can result in persistent dental infections which are challenging to treat successfully resulting in a chronic condition.³ Organisms such as Fusobacterium necrophorum and other non-specific bacteria that result in osteomyelitis as an extension from periodontal infection are generally more de-structive and less proliferative than lesions caused by A. bovis but lesions retain some similarities with actinomycosis in location and gross appearance.² "Lumpy jaw" has also been described in a domestic cat and resembles the condition described in cattle. The cat in that case report did not have a history of trauma and the infection was due to Nocardia sp. The mass demonstrated progressive enlargement but was non-painful and initially did not interfere with eating or drinking. The proliferative lesion revealed new bone formation, osteolysis and clusters of filamentous bacteria surrounded by eosinophilic amorphous material and mixed inflammatory cells, predominantly neutrophils. The patient in that report demonstrated poor response to treatment and was humanely euthanized. On sectioning, the enlarged mandible had numerous brown nodules, contained a brownish granular material and had a "honeycomb" appearance,⁷ which is also often used to describe the affected mandible in cases of bovine lumpy jaw. The causative agent was identified as Nocardia cyriacigeorgica, which is a relatively new species of Nocardia and is apparently a common Norcardia sp. pathogen in people. Traumatic gingival introduction was postulated as the source of infection in that case.⁷

References:
1.      Brewer JS. Discussion and case history: Actinomycosis. Iowa St. Univ Vet. 1956; 18:145-208.

2.      Craig LE, Dittmer KE, Thompson KG. Bones and Joints. In: Maxie MG, ed. Jubb, Kennedy, and Palmer's Pathology of Domestic Animals. 6th ed. Vol 1. St. Louis, MO: Elsevier; 2016:101.

3.      Fagan DA, Oosterhius JE, Benirschke K. "Lumpy jaw" in exotic hoofstock: A histopathologic interpretation with a treatment proposal. J Zoo Wildl Med. 2005; 36(1):36-43.

4.      Ginn PE, Mansell JEKL, Rakich PM. Skin and appendages, In: Maxie MG. ed. Jubb, Kennedy and Palmer Pathology of Domestic Animals. 5th ed. Vol1. St. Louis, MO: Elsevier-Saunders; 2007: 553-781.

5.      Grist A. Conditions encountered at bovine post mortem inspection (non parasitic). In: Ibid. eds. Bovine Meat Inspection. 2nd ed. Nottingham, UK: Nottingham University Press; 2008: 160-239.

6.      Miller M, Haddad AJ. Cervicofacial actinomycosis. Oral Surg. Oral Med. Oral Pathol. 1998;85:496-508.

7.      Soto E, Arauz M, Gallagher CA, Illanes O. Nocardia cyriacigeorgica as the causative agent of mandibular osteomyelitis (lumpy jaw) in a cat. J Vet Diagn Invest. 2014; 26(4):580-584.

8.      Tessele B, Martins TB, Vielmo A et al. 2014. LesÕes granulomatosas Encon–tradas em bovinos abatidos para consumo. [Granulomatous lesions found in cattle slaughtered for meat production.] Pesq Vet Bras. 2014; 34:763-769.

9.      Thompson K. Inflammatory diseases of bones In: Maxie MG. ed. Jubb, Kennedy and Palmer Pathology of Domestic Animals. 5th ed. Vol1. St. Louis, MO: Elsevier-Saunders; 2007: 92-105.

10. Till DH and Palmer FPA. A review of actinobacillosis with a study of the causal organism. Vet Rec. 1960; 72:527-543.

11. Wilson DW, Dungworth DL. Tumors of the respiratory tract, In: Tumors in Domestic Animals. ed. Meuten DJ. 4th. Ames, IA: Iowa State Press; 2002:365-374.

12. Wilson WG. Wilson's Practical Meat Inspection. 7th ed. Oxford, UK: Blackwell. 2005.

13. Zachary J.F. Mechanisms of microbial infections, In: Zachary JF and McGavin MD. eds. Pathologic Basis of Veterinary Disease. 5th ed. St. Louis, MO: Elsevier-Saunders. 2012:147-241: 2012.