History

A 6-year-old 16-kg castrated male Australian Shepherd was evaluated because of a sudden-onset of tetraplegia following a traumatic event. While running out of the house through a dog door, the dog hit the doorframe, cried out, and then was immediately unable to stand or walk. Prior to this injury, the dog had no other medical issues.

Clinical and Gross Findings

On physical examination, the dog was in lateral recumbency, tetraplegic, and open-mouth breathing with abdominal effort. No other abnormalities were detected on physical examination. Neurologic examination revealed signs of clinically normal mentation. In the pelvic limbs, the patellar reflexes were increased, and the withdrawal reflexes were clinically normal. In the thoracic limbs, the withdrawal reflexes were absent. There was increased muscular tone in all 4 limbs. Nociception was absent in the thoracic limbs but present in the pelvic limbs. Cranial nerves were considered clinically normal with the exception of miosis and elevated third eyelids in both eyes. There was no obvious sign of cervical pain; however, extensive movement of the neck was not performed given the traumatic history. The neuroanatomic diagnosis was consistent with a focal or diffuse lesion involving the C1 through C5 spinal cord segments. The lack of withdrawal reflexes in the thoracic limbs was considered secondary to spinal shock. The miosis and elevated third eyelids were considered reflective of Horner syndrome secondary to dysfunction of the lateral tectotegmental tracts, which provide upper motor neuron innervation to the sympathetic preganglionic neurons in the cranial thoracic spinal cord. The differential diagnosis included traumatic vertebral fracture, luxation, or subluxation; traumatic intervertebral disk (IVD) herniation; acute noncompressive nucleus pulposus extrusion; and ischemic myelopathy, such as fibrocartilagenous embolic myelopathy. No abnormalities were detected with radiographic examination of the cervical vertebral column.

On sagittal and transverse plane MRI images, there was a focal, linear T2 hyperintensity in the center of the spinal cord at the level of the C4-C5 IVD space. On transverse T1-weighted, postcontrast MRI images, the central aspect of the spinal cord was T1 hypointense at the level of the C4-C5 IVD space. There was also abnormal contrast enhancement of the meninges, periosteum of C4 and C5 vertebrae, and epaxial muscles at the level of the C4-C5 IVD space. There was a loss of the normal high T2 signal intensity of the nucleus pulposus of the C4-C5 IVD. The MRI findings were interpreted as consistent with intramedullary IVD extrusion (IIVDE). Given the severity of neurologic signs, a grave prognosis for regaining the ability to walk was discussed with the owner. Consequently, the owner elected euthanasia. The dog was euthanized by an IV overdose of pentobarbital. Only the cervical portions of the vertebral column and spinal cord were evaluated on postmortem examination.

At the level of the emergence of the C5 spinal nerves, visible through the dura mater was an approximately 0.75 X 0.5-cm, dark-red, irregular area (hemorrhage) on the dorsal surface of the spinal cord (Figure 1). Ventrally, there was an approximately 1.0-cm linear sagittal rent in the meninges on the midline. The spinal cord at this level palpated soft (malacia). On transverse section at the level of the C5 spinal nerve roots, there was cavitation of the central aspect of the spinal cord extending through the entire dorsoventral axis, with hemorrhage in the adjacent parenchyma. Within the vertebral canal, there was disruption of the dorsal longitudinal ligament and dorsal protrusion of the annulus fibrosus of the C4-C5 IVD. On median sagittal section of the vertebral column, the C4-C5 IVD had loss of the nucleus pulposus and bulging of the annulus fibrosus (Figure 2).

Postmortem images of the dorsal (A) and ventral (B) aspects of the formalin preserved spinal cord from the C4 (top) through C6 (bottom) spinal cord segments and transverse section at the level of the C5 spinal nerves (C) of a 6-year-old 16-kg castrated male Australian Shepherd that became immediately tetraplegic after running into the doorframe of a dog door. A—Hemorrhage is visible through the meninges at the level of the C5 spinal nerves (arrow). B—There is a linear rent in the meninges (arrow) at the level of the C5 spinal nerves. Bar = 1 cm. C—At the level of the C5 spinal nerves (arrowheads), a central cavitation contains hemorrhage that splits the spinal cord on the sagittal plane. Note the rent in the ventral meninges (arrow). Bar = 5 mm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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Postmortem images of the dorsal (A) and ventral (B) aspects of the formalin preserved spinal cord from the C4 (top) through C6 (bottom) spinal cord segments and transverse section at the level of the C5 spinal nerves (C) of a 6-year-old 16-kg castrated male Australian Shepherd that became immediately tetraplegic after running into the doorframe of a dog door. A—Hemorrhage is visible through the meninges at the level of the C5 spinal nerves (arrow). B—There is a linear rent in the meninges (arrow) at the level of the C5 spinal nerves. Bar = 1 cm. C—At the level of the C5 spinal nerves (arrowheads), a central cavitation contains hemorrhage that splits the spinal cord on the sagittal plane. Note the rent in the ventral meninges (arrow). Bar = 5 mm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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Postmortem images of the dorsal (A) and ventral (B) aspects of the formalin preserved spinal cord from the C4 (top) through C6 (bottom) spinal cord segments and transverse section at the level of the C5 spinal nerves (C) of a 6-year-old 16-kg castrated male Australian Shepherd that became immediately tetraplegic after running into the doorframe of a dog door. A—Hemorrhage is visible through the meninges at the level of the C5 spinal nerves (arrow). B—There is a linear rent in the meninges (arrow) at the level of the C5 spinal nerves. Bar = 1 cm. C—At the level of the C5 spinal nerves (arrowheads), a central cavitation contains hemorrhage that splits the spinal cord on the sagittal plane. Note the rent in the ventral meninges (arrow). Bar = 5 mm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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Postmortem images of the dorsal (A) and ventral (B) aspects of the formalin preserved spinal cord from the C4 (top) through C6 (bottom) spinal cord segments and transverse section at the level of the C5 spinal nerves (C) of a 6-year-old 16-kg castrated male Australian Shepherd that became immediately tetraplegic after running into the doorframe of a dog door. A—Hemorrhage is visible through the meninges at the level of the C5 spinal nerves (arrow). B—There is a linear rent in the meninges (arrow) at the level of the C5 spinal nerves. Bar = 1 cm. C—At the level of the C5 spinal nerves (arrowheads), a central cavitation contains hemorrhage that splits the spinal cord on the sagittal plane. Note the rent in the ventral meninges (arrow). Bar = 5 mm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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Postmortem images of the dorsal (A) and ventral (B) aspects of the formalin preserved spinal cord from the C4 (top) through C6 (bottom) spinal cord segments and transverse section at the level of the C5 spinal nerves (C) of a 6-year-old 16-kg castrated male Australian Shepherd that became immediately tetraplegic after running into the doorframe of a dog door. A—Hemorrhage is visible through the meninges at the level of the C5 spinal nerves (arrow). B—There is a linear rent in the meninges (arrow) at the level of the C5 spinal nerves. Bar = 1 cm. C—At the level of the C5 spinal nerves (arrowheads), a central cavitation contains hemorrhage that splits the spinal cord on the sagittal plane. Note the rent in the ventral meninges (arrow). Bar = 5 mm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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Median sagittal section of the vertebral column from the same dog, showing protrusion of the disrupted dorsal aspect of the annulus fibrosus (white arrow) and loss of a normal nucleus pulposus (open arrow) of the C4-C5 intervertebral disk (IVD). Grossly, the nuclei pulposi of the C3-C4 IVD and C5-C6 IVD (open arrowheads) appear normal. Bar = 1 cm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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Median sagittal section of the vertebral column from the same dog, showing protrusion of the disrupted dorsal aspect of the annulus fibrosus (white arrow) and loss of a normal nucleus pulposus (open arrow) of the C4-C5 intervertebral disk (IVD). Grossly, the nuclei pulposi of the C3-C4 IVD and C5-C6 IVD (open arrowheads) appear normal. Bar = 1 cm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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Median sagittal section of the vertebral column from the same dog, showing protrusion of the disrupted dorsal aspect of the annulus fibrosus (white arrow) and loss of a normal nucleus pulposus (open arrow) of the C4-C5 intervertebral disk (IVD). Grossly, the nuclei pulposi of the C3-C4 IVD and C5-C6 IVD (open arrowheads) appear normal. Bar = 1 cm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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Formulate differential diagnoses, then continue reading.

Histopathologic Findings

The C5 spinal cord segment had a central area of cavitation, tissue loss, and replacement by hemorrhage and hyaline chondroid lacunae embedded in pale basophilic extracellular matrix, consistent with extruded nucleus pulposus (Figure 3). Degenerate and nondegenerate neutrophils were scattered throughout this area. Fragments of degenerative hyaline cartilage were present in the subarachnoid space of the C5 segment and as far cranial as the C4 spinal nerves.

Photomicrographs of tissue sections of the C5 spinal cord segment from the dog described in Figure 1. A—The spinal cord architecture is severely disrupted. Hemorrhage and chondroid fragments fill the central cavitation. H&E stain; bar = 1 mm. B—In a gray matter area, there are a few necrotic neurons (arrows) with pale eosinophilic cytoplasm and an absence of Nissl substance. H&E stain; bar = 50 µm. C—The white matter adjacent to the median ventral fissure is severely disrupted. Abundant axonal swellings (spheroids) are present (arrows). Neutrophils are scattered throughout the white matter. H&E stain; bar = 50 µm. D—Although less affected, the lateral funiculus also contains dilated myelin sheath and spheroids. H&E stain; bar = 50 µm. E—The central cavitation in the spinal cord contains fragments of chondroid matrix. The lacunae within the chondroid matrix are largely devoid of chondrocytes. H&E stain; bar = 100 µm. F—Within the subarachnoid space adjacent to the dura matter (asterisk), fragments of extruded cartilage are present. In some lacunae, there is cellular debris and pyknotic nuclei from degenerate chondrocytes (arrows). H&E stain; bar = 100 µm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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Photomicrographs of tissue sections of the C5 spinal cord segment from the dog described in Figure 1. A—The spinal cord architecture is severely disrupted. Hemorrhage and chondroid fragments fill the central cavitation. H&E stain; bar = 1 mm. B—In a gray matter area, there are a few necrotic neurons (arrows) with pale eosinophilic cytoplasm and an absence of Nissl substance. H&E stain; bar = 50 µm. C—The white matter adjacent to the median ventral fissure is severely disrupted. Abundant axonal swellings (spheroids) are present (arrows). Neutrophils are scattered throughout the white matter. H&E stain; bar = 50 µm. D—Although less affected, the lateral funiculus also contains dilated myelin sheath and spheroids. H&E stain; bar = 50 µm. E—The central cavitation in the spinal cord contains fragments of chondroid matrix. The lacunae within the chondroid matrix are largely devoid of chondrocytes. H&E stain; bar = 100 µm. F—Within the subarachnoid space adjacent to the dura matter (asterisk), fragments of extruded cartilage are present. In some lacunae, there is cellular debris and pyknotic nuclei from degenerate chondrocytes (arrows). H&E stain; bar = 100 µm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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Photomicrographs of tissue sections of the C5 spinal cord segment from the dog described in Figure 1. A—The spinal cord architecture is severely disrupted. Hemorrhage and chondroid fragments fill the central cavitation. H&E stain; bar = 1 mm. B—In a gray matter area, there are a few necrotic neurons (arrows) with pale eosinophilic cytoplasm and an absence of Nissl substance. H&E stain; bar = 50 µm. C—The white matter adjacent to the median ventral fissure is severely disrupted. Abundant axonal swellings (spheroids) are present (arrows). Neutrophils are scattered throughout the white matter. H&E stain; bar = 50 µm. D—Although less affected, the lateral funiculus also contains dilated myelin sheath and spheroids. H&E stain; bar = 50 µm. E—The central cavitation in the spinal cord contains fragments of chondroid matrix. The lacunae within the chondroid matrix are largely devoid of chondrocytes. H&E stain; bar = 100 µm. F—Within the subarachnoid space adjacent to the dura matter (asterisk), fragments of extruded cartilage are present. In some lacunae, there is cellular debris and pyknotic nuclei from degenerate chondrocytes (arrows). H&E stain; bar = 100 µm.

Citation: Journal of the American Veterinary Medical Association 259, S2; 10.2460/javma.20.12.0690

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The transverse section of C5 spinal cord had complete loss of architecture and distinction between gray and white matter. Rare necrotic neurons were identified in the gray matter area, with ill-defined outlines, pale eosinophilic cytoplasm, loss of Nissl substance, and when present, a pale basophilic nucleus.

The remnant white matter was pale eosinophilic containing abundant axonal swellings with central accumulation of amphophilic material (spheroids) and dilated myelin sheaths throughout all funiculi. The ventral funiculus, predominately in the white matter immediately adjacent to the ventral median fissure, was most severely affected, whereas the lateral funiculi were least affected. Neutrophils and pyknotic round nuclei with coarse chromatin (necrotic glial cells) were present in all funiculi. The spinal nerve roots were histologically normal.

In adjacent sections immediately cranial and caudal to the C5 segment, the gray and white matter were within normal limits, with the exception of rare dilated axons, which were most numerous in the ventral funiculus, adjacent to the ventral median fissure. Hemorrhage was noted in the ventral median fissure.

Morphologic Diagnosis and Case Summary

Morphologic diagnosis: spinal cord, C5 segment: severe, acute liquefactive necrosis with hemorrhage and extruded nucleus pulposus material, consistent with IIVDE.

Case summary: acute traumatic IIVDE of the C4-C5 IVD in a dog.

Comments

Intramedullary intervertebral disk extrusion is a type of IVD disease rarely reported in dogs and cats.¹ Affected dogs range from middle to older aged dogs without a gender predilection.^2–8 In contrast to classical degenerative IVD herniation, nonchondrodystrophic breeds make up most of reported cases,^2–8 as was seen in this case. In cats, most affected animals are adults; however, too few cats have been reported to identify specific age, breed, and gender predilections.^9,10

Like the dog of the present report, affected dogs typically have a sudden-onset of signs, often in association with physical activity (eg, running or jumping) or a traumatic impact or injury. In some cases, an inciting event may not be identified. Commonly affected sites along the vertebral column are cervical, caudal thoracic, and lumbar IVDs.

In the present case, the definitive diagnosis was established by finding intramedullary cartilage in a spinal cord segment overlying a grossly visible rent in the ventral dura and disruption of the annulus fibrosus of the adjacent IVD. The chondroid tissue observed in the spinal cord resembled hyaline cartilage of the nucleus pulposus^2,7; hence, the origin of the intramedullary chondroid was extruded nucleus pulposus. Presumably, IVD material extrudes with enough force, velocity, or both to cause tearing of the ventral dura matter and subsequent penetration into the spinal cord parenchyma.^3,7 Alternatively, it is possible that trauma, as occurred in the present case, may have resulted in excessive flexion or extension of the vertebral column and in doing so placed excessive traction on the meninges via the meningovertebral ligament to have caused tearing of the meninges, allowing intradural access for extruded IVD material. Dural tears are occasionally seen with trauma and classical Hansen type I degenerative IVD herniation.^8,11,12

Findings on MRI consistent with IIVDE include a focal, often vertically oriented, linear spinal cord T2 hyperintensity located dorsal to an IVD. Such changes to the signal intensity within the spinal cord parenchyma can be secondary to edema, myelomalacia, hemorrhage, and inflammation from extruded nucleus pulposus material.^3,9,13,14 Focal areas of T2, T1, and T2* hypointensity, suggestive of hemorrhage, also may be present.^3,9,13,14 Additionally, decreased volume and T2 signal intensity of the nucleus pulposus also may be observed. The subgross appearance of the spinal cord in the present case corroborates the reported MRI findings in dogs with IIVDE.

Traumatic spinal cord injury can be secondary to exogenous (ie, hit by a car) or endogenous (ie, IVD herniation) trauma. Regardless of the cause, traumatic spinal cord injury can result in gross and microscopic changes to gray and white matter that range from minimal or no change to complete necrosis involving the total cross-sectional area of the spinal cord.^15–19 With destruction of the total cross-sectional area of the spinal cord, it may be difficult to distinguish between gray and white matter. In some cases of exogenous trauma, there may be gross transection of the spinal cord and loss of continuity of the meninges.¹⁶ Where gray matter can be distinguished, there is often a loss of neurons. Remaining neurons display degenerative changes such as chromatolysis and ischemic cell change.^15,16,18 At the epicenter of the lesion, focal areas of hemorrhage and edema may occur throughout the spinal cord.

Frequently, white matter changes predominate; commonly affected sites include the ventral funiculus, dorsolateral aspect of the lateral funiculi, and base of the dorsal funiculus.¹⁵ Changes in the white matter include swollen axons and dilated myelin sheaths, axonal fragmentation, and myelin dissolution.¹⁸ In some instances, there may be relative sparing of the subpial white matter.¹⁸ Additional changes may be present depending on chronicity. As was observed in the dog herein, neutrophilic inflammation occurs with acute lesions. With chronic lesions, the dilated myelin sheaths and overall loss of myelin gives a “moth-eaten” appearance to the white matter. Likely as a result of parenchymal loss, intramedullary cavitation may develop.²⁰ Lipid-laden macrophages (gitter cells), gliosis, and vascular proliferation with reactive vessels are present in affected white matter.^15,16,18 Reactive astrocytes can be observed bordering areas of loss of white matter. In some cases, complete loss of gray matter with variable degrees of sparing of the white matter may be present.²⁰

Similar pathological changes may be observed with fibrocartilagenous embolic myelopathy and the syndrome of ascending-descending myelomalacia.²¹ This likely reflects a common underlying ischemic pathophysiology. Obviously, the observation of fibrocartilage emboli defines the diagnosis of fibrocartilagenous myelopathy. Emboli may be observed in parenchymal vessels, meningeal vessels, or both. The use of stains such as Masson’s trichrome or Alcian blue may help increase the conspicuity of fibrocartilage emboli. Ascending-descending myelomalacia is a pathologic sequela of IVD herniation. The spinal cord pathology spans multiple spinal cord segments and depending on the chronicity may affect spinal cord segments far distant from the initial site of IVD herniation. Ascending-descending myelomalacia is characterized by marked intraparenchymal and subarachnoid hemorrhage.²² At the cranial and caudal ends, necrosis and hemorrhage are often seen at the base of the dorsal funiculus and region of the central canal.²² In the present case, ascending-descending myelomalacia was not considered likely given the focal nature of the spinal cord pathology. However, it is possible that in time, the lesion may have extended cranial and caudally to develop into ascending and descending myelomalacia. Additionally, typically ascending and descending myelomalacia start with a disk herniation in the thoracolumbar region of the spinal cord.

Treatment of IIVDE includes conservative treatment with exercise restriction, anti-inflammatory medications, and analgesics. In some cases, surgical intervention consisting of a myelotomy and removal of the extruded IVD material has led to successful return to normal function.^2,9,14 The prognosis varies widely. Severity of neurologic signs may serve as a prognostic indicator.³ In the present case, the severity of the neurologic signs suggested a grave prognosis for regaining the ability to walk. Although the destruction of the spinal cord parenchyma was not discernable on MRI, the gross and microscopic findings affirmed the grave prognosis provided to owner. Further understanding of the pathophysiologic mechanism that leads to the observed pathology may help expand therapeutic measures. Ultimately, too few cases have been reported to define optimal treatment or determine accurate prognostic indicators.