Pathology in Practice

Marika MenchettiDepartment of Veterinary Medical Sciences (UNI EN ISO 9001:2008), University of Bologna, 40064 Ozzano dell'Emilia, Bologna, Italy.

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Maria MoriniDepartment of Veterinary Medical Sciences (UNI EN ISO 9001:2008), University of Bologna, 40064 Ozzano dell'Emilia, Bologna, Italy.

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Luciano PisoniDepartment of Veterinary Medical Sciences (UNI EN ISO 9001:2008), University of Bologna, 40064 Ozzano dell'Emilia, Bologna, Italy.

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Teresa GagliardoDepartment of Veterinary Medical Sciences (UNI EN ISO 9001:2008), University of Bologna, 40064 Ozzano dell'Emilia, Bologna, Italy.

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Filippo CintiDepartment of Veterinary Medical Sciences (UNI EN ISO 9001:2008), University of Bologna, 40064 Ozzano dell'Emilia, Bologna, Italy.

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Giuliano BettiniDepartment of Veterinary Medical Sciences (UNI EN ISO 9001:2008), University of Bologna, 40064 Ozzano dell'Emilia, Bologna, Italy.

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Gualtiero GandiniDepartment of Veterinary Medical Sciences (UNI EN ISO 9001:2008), University of Bologna, 40064 Ozzano dell'Emilia, Bologna, Italy.

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History

A 10-week-old male French Bulldog was referred for evaluation because of a 2-week history of recurrent episodes of signs of acute diffuse pain and mild depression and decreased appetite. The dog's vaccination protocol was incomplete. No previous trauma was reported. The history of the dog's littermates was unknown.

Clinical and Gross Findings

The general physical examination findings for the dog were unremarkable. A neurologic examination revealed a kyphotic posture, mild proprioceptive ataxia, and abnormal postural and proprioceptive reactions on all 4 limbs. Signs of severe pain were elicited by neck manipulation. Radiography of the cervical vertebral column revealed an irregularly shaped ill-defined area characterized by an increased bone radiopacity, which was located on the right arch of the second cervical vertebra. No other radiographic lesions were detected. Magnetic resonance imaging of the cervical region revealed a space-occupying lesion on the right caudal portion of the C2 vertebral body and transverse process that was causing severe spinal cord compression. The lesion was inhomogeneously hyperintense on T2-weighted images and iso- to hyponintense on T1-weighted images, compared with gray matter, with inhomogeneous contrast enhancement. Given the lesion's location and extent, a palliative right hemilaminectomy at C2 (to decompress the spinal cord) was performed; the excised bone was fixed in neutral-buffered 10% formalin and submitted for histologic examination. However, because of the small size of the bone fragments, results of the histologic examination were not diagnostic.

After the dog had an initial postsurgical improvement, the clinical signs soon relapsed with increasingly marked ataxia, tetraparesis, and daily clusters of dramatic painful crises that were not responsive to any aggressive analgesic treatment. A second MRI examination, performed 3 weeks after surgery, revealed an increase in the size of the mass and the worsening of the spinal cord compression. Owing to the dog's untreatable signs of pain and the progressive neurologic deterioration, the owner elected euthanasia (performed by IV infusion of embutramide, mebezonium iodide, and tetracaine hydrochloride while the dog was anesthetized).

On necropsy, a 2 × 1.5 × 1-cm, irregularly shaped, cribriform, hard mass localized at the C2 vertebral body and right transverse process was observed (Figure 1). The mass protruded ventrolaterally into the vertebral canal, causing partial stenosis and severe spinal cord compression. No other lesions were detected, and there was no evidence of metastases.

Figure 1—
Figure 1—

Sagittal formalin-fixed and decalcified sections of the second cervical vertebra of a 10-week-old French Bulldog that was evaluated because of recurrent episodes of signs of acute diffuse pain and mild depression and decreased appetite over a 2-week period. The dog had a mass lesion compressing the cervical spinal cord at the level of C2. In the first section (A), a 0.5-cm-long mass that apparently originates from the right side of the vertebral body (asterisk) is evident. In the central section (B), the mass has attained a maximum size of 2 cm in diameter and has replaced almost entirely the vertebral body (asterisk), thereby causing partial stenosis of the vertebral canal and severe compression and dislocation of the spinal cord (dagger); the mass has an irregular shape, has a cribriform-osseous appeareance, and is apparently bordered by white cartilagineous tissue. In the third section (C), the mass is still evident in the C2–3 intervertebral space (asterisk). Bar = 1 cm.

Citation: Journal of the American Veterinary Medical Association 252, 4; 10.2460/javma.252.4.423

Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page→

Histopathologic Findings

Samples of the cervical mass were fixed in neutral-buffered 10% formalin, decalcified,a processed routinely in paraffin, sectioned at 4 μm, and stained with H&E stain. Histologically, the lesion consisted of a welldelineated, unencapsulated, and multilobulated mass composed of lamellar trabecular bone and bone marrow that was continuous with the marrow cavity of the original bone. The mass was covered with a thin and discontinuous apical cap of hyaline cartilage (Figure 2). Bony trabeculae were irregular in shape and distribution and multifocally lined by active osteoblasts and osteoclasts. Endochondral ossification had developed between the bone and the cartilage. At the right caudal aspect of C2, the enlarged mass from the vertebral body and right transverse process protruded into the vertebral canal, causing focal spinal cord compression. Extensive loss of myelin, axonal degeneration with numerous spheroids, and extensive secondary astrogliosis were observed. No features suggestive of malignancy were evident.

Figure 2—
Figure 2—

Photomicrographs of sections of the cervical vertebral mass in the dog in Figure 1. A—An apical cap of hyaline cartilage (asterisk) is evident at the periphery of the mass; the cartilage cap overlies a base of mature bone with intervening marrow spaces. H&E stain; bar = 400 μm. B—The mass is composed of irregular bony trabeculae (dagger) outlining hematopoietic medullary spaces (double dagger). H&E stain; bar = 150 μm.

Citation: Journal of the American Veterinary Medical Association 252, 4; 10.2460/javma.252.4.423

Morphologic Diagnosis and Case Summary

Morphologic diagnosis: vertebral osteochondroma.

Case summary: vertebral osteochondroma causing severe cervical spinal cord compression in a French Bulldog puppy.

Comments

On the basis of the macroscopic findings, the differential diagnoses for the dog of the present report included neoplasia (osteochondroma, osteosarcoma, or chondrosarcoma) or a cartilaginous growth subsequent to a traumatic lesion. For this dog, the radiographic pattern of skeletal involvement was mostly indicative of an osteochondroma; an osteochondroma is usually described as a mass in the region of endochondral ossification, which is radiopaque in the case of cancellous bone and radiolucent in the case of hyaline cartilage.1 The histologic findings confirmed that the mass was an osteochondroma. The peripheral portion of the mass contained cartilaginous areas, whereas the central portion contained lamellar trabecular bone; endochondral ossification was evident at the interface between the cartilage and the bone.

Osteochondroma is a disease of endochondral bone and is of uncertain origin, characterized by single or multiple cartilage-capped exostoses arising from focal or extensive perturbations of the perichondrial ring of the metaphysis of bones.2–5 Different terms have been used to describe the disease, including multiple cartilaginous exostoses, multiple osteochondromas, multiple hereditary exostoses, diaphyseal aclasis, and hereditary deforming chondrodysplasia. However, according to the current nomenclature, a solitary lesion is defined as an osteochondroma, whereas the presence of multiple lesions is defined as multiple cartilaginous exostoses.2,4,5 The latter condition has been described in humans, dogs, and horses. The hereditary origin of multiple cartilaginous exostoses is associated with a single dominant autosomal gene.4 Multiple cartilaginous exostoses in cats have also been reported, but in that species they are an acquired skeletal disorder that develops in young adults after growth plate closure.4

In dogs, osteochondroma typically affects young animals with no breed or sex predilection, and has self-limiting development, ceasing at the time of skeletal maturity.5 However, possible malignant transformations of solitary osteochondromas in dogs and in 1% to 5% of human patients have been reported.2,5,6 In dogs, the vertebrae, ribs, and long bones are most commonly affected. With regard to the vertebral column, any region may be involved, but the spinous processes of the thoracic vertebrae are the most commonly affected sites.5 In humans, the vertebral column is less frequently affected; however, when lesions develop, they are more commonly found in the upper cervical portion, and the second cervical vertebra is most commonly affected.7,8 Compared with the human medical literature, cervical osteochondroma involvement has been rarely described in the veterinary medical literature.1,2,9,10 There are only 2 reports1,9 of single cases of atlantoaxial osteochondroma of which the authors are aware. In those cases, the axis was secondarily involved and the lesion was dorsally located.1,9 In humans and dogs, an osteochondroma usually remains subclinical, unless its growth causes dysfunctions through the compression of a vital structure, such as the spinal cord, or the limitation of joint movements.4,5 Removal of multiple cartilaginous exostoses with subsequent spinal cord decompression has been reported1,5,11 to have good results.

The prognosis is good for those skeletally mature dogs with subclinical multiple cartilaginous exostoses without evidence of neoplastic transformation.12 For clinically affected growing dogs, as was the case described in the present report, the prognosis is guarded to poor; prognosis is influenced by the site of the lesion and the likelihood of performing complete excision.

To the authors' knowledge, this is the first report describing the clinical, diagnostic, and pathological features of an osteochodroma involving the body of the second cervical vetrtebra in a French Bulldog puppy. Osteochondroma should be considered as a possible differential diagnosis in young dogs that have signs of severe pain associated with the vertebral column.

Acknowledgments

Presented in abstract form at the 85th Annual Congress of the Italian Companion Animal Veterinary Association (SCIVAC), Verona, Italy, March 2015.

Footnotes

a.

Histo-Decal, Histo-Line, Milan, Italy.

References

  • 1. Engel S, Randall EK, Cuddon PA, et al. Imaging diagnosis: multiple cartilaginous exostoses and calcinosis circumscripta occurring simultaneously in the cervical spine of a dog. Vet Radiol Ultrasound 2014;55:305309.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Green EM, Adams WM, Steinberg H. Malignant transformation of solitary spinal osteochondroma in two mature dogs. Vet Radiol Ultrasound 1999;40:634637.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Doige CE. Multiple cartilaginous exostoses in dogs. Vet Pathol 1987;24:276278.

  • 4. Mozos E, Novales M, Ginel PJ, et al. A newly recognized pattern of canine osteochondromatosis. Vet Radiol Ultrasound 2002;43:132137.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Franch J, Font J, Ramis A, et al. Multiple cartilaginous exostosis in a Golden Retriever cross-bred puppy. Vet Comp Orthop Traumatol 2005;18:189193.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Calvo CE, Cruz M, Ramos E. An unusual complication in a 9-year-old patient with hereditary multiple osteochondromatosis. PM R 2013;5:348350.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Tarassoli P, Amirfeyz R, Gargan M. Multiple hereditary exostoses. Orthop Trauma 2009;23:456459.

  • 8. Ashraf A, Larson AN, Ferski G, et al. Spinal stenosis frequent in children with multiple hereditary exostoses. J Child Orthop 2013;7:183194.

  • 9. Bhatti S, Van Ham L, Putcuyps I, et al. Atlantoaxial cartilaginous exostosis causing spinal cord compression in a mature Bernese Mountain Dog. J Small Anim Pract 2001;42:7981.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Caporn TM, Read RA. Osteochondromatosis of the cervical spine causing compressive myelopathy in a dog. J Small Anim Pract 1996;37:133137.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Atabay H, Kuyucu Y, Kormaz O, et al. Myelopathy due to hereditary multiple exostoses: CT and MR studies. Clin Neurol Neurosurg 1996;98:186188.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Gambardella PC, Osborne CA, Stevens JB. Multiple cartilaginous exostoses in the dog. J Am Vet Med Assoc 1975;166:761768.

Contributor Notes

Dr. Cinti's present address is Centro Veterinario Luni Mare, Via Palmiro Togliatti, 8, 19034 Ortonovo, Italy.

Address correspondence to Dr. Menchetti (marika.menchetti3@unibo.it).
  • View in gallery
    Figure 1—

    Sagittal formalin-fixed and decalcified sections of the second cervical vertebra of a 10-week-old French Bulldog that was evaluated because of recurrent episodes of signs of acute diffuse pain and mild depression and decreased appetite over a 2-week period. The dog had a mass lesion compressing the cervical spinal cord at the level of C2. In the first section (A), a 0.5-cm-long mass that apparently originates from the right side of the vertebral body (asterisk) is evident. In the central section (B), the mass has attained a maximum size of 2 cm in diameter and has replaced almost entirely the vertebral body (asterisk), thereby causing partial stenosis of the vertebral canal and severe compression and dislocation of the spinal cord (dagger); the mass has an irregular shape, has a cribriform-osseous appeareance, and is apparently bordered by white cartilagineous tissue. In the third section (C), the mass is still evident in the C2–3 intervertebral space (asterisk). Bar = 1 cm.

  • View in gallery
    Figure 2—

    Photomicrographs of sections of the cervical vertebral mass in the dog in Figure 1. A—An apical cap of hyaline cartilage (asterisk) is evident at the periphery of the mass; the cartilage cap overlies a base of mature bone with intervening marrow spaces. H&E stain; bar = 400 μm. B—The mass is composed of irregular bony trabeculae (dagger) outlining hematopoietic medullary spaces (double dagger). H&E stain; bar = 150 μm.

  • 1. Engel S, Randall EK, Cuddon PA, et al. Imaging diagnosis: multiple cartilaginous exostoses and calcinosis circumscripta occurring simultaneously in the cervical spine of a dog. Vet Radiol Ultrasound 2014;55:305309.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Green EM, Adams WM, Steinberg H. Malignant transformation of solitary spinal osteochondroma in two mature dogs. Vet Radiol Ultrasound 1999;40:634637.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Doige CE. Multiple cartilaginous exostoses in dogs. Vet Pathol 1987;24:276278.

  • 4. Mozos E, Novales M, Ginel PJ, et al. A newly recognized pattern of canine osteochondromatosis. Vet Radiol Ultrasound 2002;43:132137.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Franch J, Font J, Ramis A, et al. Multiple cartilaginous exostosis in a Golden Retriever cross-bred puppy. Vet Comp Orthop Traumatol 2005;18:189193.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Calvo CE, Cruz M, Ramos E. An unusual complication in a 9-year-old patient with hereditary multiple osteochondromatosis. PM R 2013;5:348350.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Tarassoli P, Amirfeyz R, Gargan M. Multiple hereditary exostoses. Orthop Trauma 2009;23:456459.

  • 8. Ashraf A, Larson AN, Ferski G, et al. Spinal stenosis frequent in children with multiple hereditary exostoses. J Child Orthop 2013;7:183194.

  • 9. Bhatti S, Van Ham L, Putcuyps I, et al. Atlantoaxial cartilaginous exostosis causing spinal cord compression in a mature Bernese Mountain Dog. J Small Anim Pract 2001;42:7981.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Caporn TM, Read RA. Osteochondromatosis of the cervical spine causing compressive myelopathy in a dog. J Small Anim Pract 1996;37:133137.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Atabay H, Kuyucu Y, Kormaz O, et al. Myelopathy due to hereditary multiple exostoses: CT and MR studies. Clin Neurol Neurosurg 1996;98:186188.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Gambardella PC, Osborne CA, Stevens JB. Multiple cartilaginous exostoses in the dog. J Am Vet Med Assoc 1975;166:761768.

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