Spinal neurenteric cyst in a dog

Daniela S. Alder From the Section of Neurology, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland.

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Anna Oevermann Division of Neurological Sciences, DCR-VPH, Vetsuisse Faculty, University of Bern, 3012 Bern, Switzerland.

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Stephan A. Pfister Institute for Radiology and Nuclear Medicine, Hirslanden Klinik St. Anna, 6006 Lucerne, Switzerland.

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Frank Steffen From the Section of Neurology, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland.

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Abstract

CASE DESCRIPTION An 11-year-old English Cocker Spaniel was evaluated because of chronic progressive ataxia of the hind limbs.

CLINICAL FINDINGS The dog had no history of previous illness, and findings of physical examination and laboratory tests were unremarkable. Neurologic examination revealed that the dog was ambulatory with severe ataxia of the hind limbs. Proprioception was decreased in the right and left hind limbs (right affected more than left), and spinal reflexes were bilaterally unremarkable. Moderate signs of pain were detected during palpation of the lumbar portion of the vertebral column. Findings suggested a lesion within the thoracolumbar or lumbar segments of the spinal cord. Magnetic resonance imaging revealed extradural spinal cord compression attributable to an extradural space-occupying lesion originating from or infiltrating the L4 lamina on the right side.

TREATMENT AND OUTCOME Hemilaminectomy was performed to remove the extradural lesion. Histologic findings for tissue samples collected during the procedure were consistent with a neurenteric cyst. The late onset and progression of clinical signs of this rare congenital malformation were suspected to have been the result of enlargement of the neurenteric cyst through continuous production of mucus by goblet cells. The dog responded favorably to surgical decompression and was clinically normal 1 year after surgery. It was euthanized 2 years after surgery for an unrelated reason (end-stage heart disease), and no neurologic deficits were evident before that point.

CLINICAL RELEVANCE Congenital neurenteric cysts should be considered as a differential diagnosis for neoplastic disease in dogs in which results of diagnostic imaging indicate the presence of an extradural mass affecting vertebral structures.

Abstract

CASE DESCRIPTION An 11-year-old English Cocker Spaniel was evaluated because of chronic progressive ataxia of the hind limbs.

CLINICAL FINDINGS The dog had no history of previous illness, and findings of physical examination and laboratory tests were unremarkable. Neurologic examination revealed that the dog was ambulatory with severe ataxia of the hind limbs. Proprioception was decreased in the right and left hind limbs (right affected more than left), and spinal reflexes were bilaterally unremarkable. Moderate signs of pain were detected during palpation of the lumbar portion of the vertebral column. Findings suggested a lesion within the thoracolumbar or lumbar segments of the spinal cord. Magnetic resonance imaging revealed extradural spinal cord compression attributable to an extradural space-occupying lesion originating from or infiltrating the L4 lamina on the right side.

TREATMENT AND OUTCOME Hemilaminectomy was performed to remove the extradural lesion. Histologic findings for tissue samples collected during the procedure were consistent with a neurenteric cyst. The late onset and progression of clinical signs of this rare congenital malformation were suspected to have been the result of enlargement of the neurenteric cyst through continuous production of mucus by goblet cells. The dog responded favorably to surgical decompression and was clinically normal 1 year after surgery. It was euthanized 2 years after surgery for an unrelated reason (end-stage heart disease), and no neurologic deficits were evident before that point.

CLINICAL RELEVANCE Congenital neurenteric cysts should be considered as a differential diagnosis for neoplastic disease in dogs in which results of diagnostic imaging indicate the presence of an extradural mass affecting vertebral structures.

An 11-year-old 9-kg (19.8-lb) sexually intact female English Cocker Spaniel was referred for evaluation because of gait abnormalities that had developed several weeks previously and had since progressed. The dog had no history of previous illness, and findings of physical examination, CBC, and serum biochemical analysis were unremarkable.

Results of neurologic examination indicated the dog was ambulatory with severe ataxia of the hind limbs. Proprioception was decreased in the right and left hind limbs (right more affected than left), and spinal reflexes were bilaterally unremarkable. Moderate signs of pain were detected during palpation of the lumbar portion of the vertebral column. No history of urinary incontinence was reported by the owner, and abdominal palpation revealed that the urinary bladder was moderately filled. The cutaneous trunci reflex was unremarkable on both sides. Findings suggested a lesion in the T3-L3 spinal cord segment. The degree of neurologic impairment was graded as 3/5 (nonambulatory paraparesis) on the basis of a published grading scheme.1

To further characterize the lesion, the decision was made to perform MRI of the thoracolumbar and lumbar portion of the spinal cord. In preparation for imaging, the dog received a fentanyl bolus administered IV and was anesthetized with propofol. Endotracheal intubation was performed, and anesthesia was maintained with isoflurane in oxygen.

Magnetic resonance imaginga was performed with a 1.5-T magnet. T2-weighted sagittal and transverse scans, T1-weighted precontrast dorsal scans, and T1-weighted sagittal and transverse postcontrast scans with fat saturation were acquired, revealing a labulated mass originating from the right pedicle of L4 (Figure 1). The lesion was extradural in nature, causing considerable compression of the spinal cord (50% stenosis of the vertebral canal). The mass was well demarcated with sharp margins and was generally hypointense relative to healthy myelon on T2-weighted images but had isolated hyperintense areas. The mass was 11.4 mm long, 7.8 mm high, and 6.5 mm wide. In the T1-weighted precontrast dorsal images, the lesion was markedly hypointense relative to CSF, was slightly inhomogeneous, and had sharp margins. T1-weighted postcontrasat transverse images with fat saturation revealed heterogeneous enhancement with infiltration of the L4 lamina on the right side as well as bilateral contrast enhancement in the angle between the L4 processus spinosus and lamina.

Figure 1—
Figure 1—

T2-weighted sagittal (A) and transverse (B), T1-weighted sagittal (C) and transverse postcontrast (D), and T1-weighted dorsal precontrast (E) MRI views of an extradural neurenteric cyst located at the level of L4 in an 11-year-old English Cocker Spaniel with chronic progressive ataxia of the hind limbs. In panels A, B, and E, a mildly inhomogeneous, lobulated mass with sharp margins (asterisks) is seen compressing the lumbar portion of the spinal cord (arrow). In panels C and D, images obtained with fat saturation reveal heterogeneous contrast enhancement of the mass and infiltration of the L4 lamina on the right side (arrows). Notice contrast enhancement of soft tissue in the corner of the L4 lamina and processus spinosus, bilaterally visible (arrowheads).

Citation: Journal of the American Veterinary Medical Association 250, 7; 10.2460/javma.250.7.775

On the basis of these findings, an extradural compressive lesion infiltrating or originating from the vertebral arch and reactive soft tissue changes adjacent to the lesion were suspected. Differential diagnoses included a primary or secondary bone tumor or an inflammatory or infectious process, such as a bacterial or fungal granuloma.

The decision was made to perform decompressive surgery. The dog was premedicated and anesthetized as described for the MRI examination. A right lateral approach was chosen to expose the lateral aspects of the vertebral bodies at L4–5. The integrity of the right L4 pedicle was disturbed by a white space-occupying structure that protruded slightly just cranial to the origin of the dorsal articular facet of L4. The lesion was of fibrous consistency and had a cystic center containing a small amount of mucoid, white fluid (approx 0.5 mL), which flowed out when the structure was penetrated with a dental scraper. The vertebral canal was opened with the aid of a pneumatic drill by removal of the intact bone cranial and ventral to the lesion and removal of abnormal tissue with rongeurs. The articular processes caudal to the lesion were removed during the hemilaminectomy. Abnormal tissue was excised in pieces from the vertebral canal. Adhesions of the mass to the dura were identified that could be relieved with gentle blunt dissection. The dura remained intact.

After complete removal of the mass, an imprint was visible on the lateral aspect of the myelon. The surgical site was rigorously flushed with sterile saline (0.9% NaCl) solution, and the wound was closed in layers in a routine fashion. The fascia and subcutaneous tissues were apposed in a simple interrupted pattern with 3–0 polydioxanone synthetic absorbable suture, and the skin was closed in a simple interrupted pattern with 4–0 polyamide synthetic nonabsorbable suture.

The dog recovered from surgery without complication, and neurologic function improved completely within 14 days after surgery. Excised tissue fragments were fixed in neutral-buffered 4% formalin solution, processed, embedded in paraffin, sectioned at 5 μm, and stained with H&E stain. Histologic examination revealed a cyst and several fragments of collagenous fibrous tissue with large foci of mineralization. The cyst was similar in histologic appearance to intestinal tissue (Figure 2). It was delineated by smooth muscle, collagenous fibrous tissue, and epithelium. The smooth muscle was arranged in 2 layers of varying thickness, with the inner layer concentrically arranged and the outer layer longitudinally arranged. These 2 layers were separated in several places by a plexus containing nerve fibers and rare small ganglion cells, resembling the myenteric plexus (Auerbach plexus) found in intestinal tissue. The muscle layer was covered by collagenous tissue, which was covered by a layer of monolayered to pseudostratified columnar epithelium without cilia. Single goblet cells filled with mucus were identified. Multifocal nodular infiltrations of lymphocytes were identified, resembling rudimentary follicles of a gut-associated lymphoid tissue. The epithelium was multifocally ulcerated over large areas. Beneath the ulcerations, the collagenous fibrous tissue was thickened and infiltrated with macrophages. The lumen of the cyst was filled with basophilic, amorphous, mineralized material containing cholesterol clefts.

Figure 2—
Figure 2—

Representative photomicrographs of specimens of abnormal tissue (neurenteric cyst epithelium) obtained at hemilaminectomy from the dog in Figure 1. A—Two layers of smooth muscle (O = Outer longitudinal smooth muscle layer; I = Inner circular smooth muscle layer) and follicle-like lymphoid tissue (asterisk) resemble the layering of the intestinal tube. The epithelium is ulcerated and replaced by collagenous tissue and macrophage infiltrate (arrow). The lumen is filled with mineralized material (M). H&E stain; bar = 250 μm. B—The concentrically arranged inner muscle layer (I) and the longitudinally arranged outer muscle layer (O) are separated by a plexus containing nerve fibers (arrows) resembling the myenteric plexus of the intestines The nerve plexus contains rare ganglion cells (arrow in inset). H&E stain; bar = 100 μm. C—Collagenous tissue appears covered by a layer of monolayered columnar epithelium. The epithelium contains scattered goblet cells filled with mucus (arrow). The goblet cells are expelling mucus and lack cilia (inset). H&E stain; bar = 100 μm. D—Beneath the epithelium, multifocal nodular infiltrations of lymphocytes (asterisk) are visible that resemble rudimentary follicles of gut-associated lymphoid tissue. H&E stain; bar = 100 μm.

Citation: Journal of the American Veterinary Medical Association 250, 7; 10.2460/javma.250.7.775

One year after surgery, the owner reported complete resolution of previously observed clinical signs, and findings of neurologic examination were unremarkable. Two years after surgery, the dog was euthanized for an unrelated reason (end-stage heart disease), and no neurologic deficits were evident before that point. The owner declined necropsy.

Discussion

Neurenteric cysts, also called enterogenous or endodermal cysts, are benign congenital lesions affecting the CNS that are classified as disorders of midline notochordal integration within the category of closed spinal dysraphisms.2 In humans, such cysts are rare, accounting for 0.3% to 0.5%3 of intracranial and 0.7% to 1.3%4 of spinal space-occupying lesions in the neuraxis. Neurenteric cysts predominantly develop as intradural, extramedullary lesions in the spinal cord,5 but they can be found in the cerebellopontine angle or other intracranial locations.3

Reports of neurenteric cysts in veterinary medicine are restricted to 2 case reports6,7 of neurenteric cysts affecting the spinal cord of horses. To the authors’ knowledge, the present report represents the first description of a neurenteric spinal cyst in a dog. In veterinary medicine, neurenteric cysts (which include intraspinal or extraspinal cysts)6,7 are defined as generally benign cysts that are lined by epithelium and possibly other structures of the gastrointestinal tract.8 In rare instances, malignant transformation of these cysts may occur.9 According to a published human histologic grading scheme,8 the characteristics of the cyst in the dog of the present report were consistent with type B neurenteric cysts, which have an epithelial lining and other features such as serous or mucous glands, smooth muscle, striated muscle, fat, cartilage, bone, lymphoid tissue, nerve fibers, and ganglion cells.

In humans, neurenteric cysts can develop as solitary lesions or in association with a broad spectrum of spinal malformations, including vertebral abnormalities, associated intradural lipomas, a tethered spinal cord, dorsal meningocele, or syringomyelia as well as cutaneous stigmata.10 In the dog of the present report, the neurenteric cyst was a solitary lesion, whereas the previously reported cysts in horses had associated vertebral malformations.6,7

Various hypotheses have been proposed in human medicine to explain the development of neurenteric cysts.3,11 Generally, it is accepted that a neurenteric cyst is caused by abnormal detachment of the endoderm from the neuroectoderm in the third week of gestation.11 A persisting neurenteric canal during the third week of gestation can cause so-called splitnotochord syndrome12 and displacement of endodermal cells. Depending on the location of the ectopic endodermal cells, various gastrointestinal, vertebral, or spinal cord anomalies can develop.13,14

In humans, the ratio of spinal neurenteric cysts between males and females is approximately 2:1.4 The most common site for these cysts is the thoracic portion of the spinal cord (40%), followed by the cervical and lumbar portions. Ten percent of all neurenteric cysts are intracranial.15 Most spinal neurenteric cysts are diagnosed in the first decade of life, particularly more complicated cases involving additional malformations or neurologic dysfunction. Older humans generally have pain and myelopathy and usually have less complicated cases of neurenteric cysts than do younger humans,16 similar to the situation for the dog reported here. The late onset of clinical signs in the dog could have been attributable to a slow increase in the size of the cyst through the activity of goblet cells, which would have produced mucoid secretions, resulting in the slowly progressive enlargement of the structure with concurrent compression of the adjacent spinal cord. Alternatively, an increase in collagenous fibrous tissue and local inflammatory reactions could have contributed to the progression of clinical dysfunction.

One of the 2 reported cases of neurenteric cysts in horses involved a 7-month-old colt with progressive hind limb ataxia and weakness with the lesion at the level of T6–7; this colt had an intramedullary neurenteric cyst associated with a so-called butterfly vertebra.7 The second case involved a 3-month-old Arabian foal born with hind limb ataxia, which was discovered to have an extradural neurenteric cyst and vertebral cleft ventrally at the level of T5–6, with further vertebral malformations from T3 through T7.6 Disease in these horses was noticed early in life because of the combination of the neurenteric cyst and vertebral malformation, resulting in early onset of clinical signs, as has also been reported for children with similar cysts.17,18 Neurenteric cysts appear isointense to hyperintense relative to CSF in T2-weighted MRI scans; in T1-weighted images, they appear isointense or slightly hyperintense and are rarely hypointense to CSF (high protein content in the cyst).4,15,17,19 Usually, there is no uptake of contrast medium by the cysts.4

Most (80%) neuroenteric cysts in humans develop in an intradural-extramedullary location in the anterior thoracic portion of the spine; intramedullary cysts are less common (12%).20,21 Extradural intraspinal neurenteric cysts have been reported, most of them in association with spina bifida.10,15 Purely extradural neurenteric cysts have also been reported.17,22 In the dog of the present report, the lesion was extradural in location, with concurrent infiltration of the L4 lamina on the right side. In T2-weighted scans and T1-weighted precontrast MRI scans, the lesion appeared hypointense; in T1-weighted postcontrast scans with fat saturation, uptake of contrast medium occurred bilaterally in the paravertebral musculature in the angle of the L4 processus spinosus and lamina, most likely representing perilesional inflammatory reactions. No vertebral malformation was identified.

In human medicine, complete surgical excision of neurenteric cysts is recommended.4,19 Partially removed cysts generally redevelop,19 and malignant transformation after incomplete surgical removal has been reported in a case report.23 We presumed that the neurenteric cyst in the dog of the present report was removed completely because the discernible abnormal tissue was fully resected and, after complete removal of the mass, an imprint was visible on the lateral aspect of the myelon. However, no follow-up MRI examination was performed to confirm this presumption.

To the authors’ knowledge, the present report provides the first description of spinal neurenteric cyst in a dog. In agreement with findings in humans, the dog had a less complicated form of neurenteric cyst that, because of the long-lasting, slow development and absence of vertebral malformations, led to clinical signs later in life, resulting in progressive neurologic dysfunction and pain. The MRI findings for this dog, particularly the pattern of contrast-medium uptake, did not agree with the classic findings in human medicine, although cases with partial contrast-medium uptake by the neurenteric cyst have been reported in the human literature.22 The difference in the behavior of contrast medium during MRI might be explained by differences in protein content of cyst fluid.

The published human histologic grading scheme8 used for classification of neurenteric cysts appears to be applicable to veterinary cases. Such cysts should be considered as a differential diagnosis for neoplastic spinal cord lesions originating from or intruding into the vertebral bone. From a clinical perspective, this is important because the prognosis differs markedly between these 2 disease groups: (infiltrative) neoplastic diseases close to the spinal cord have a much worse prognosis than a benign cyst. Often, spinal neoplasias lead to euthanasia because no adequate treatment can be offered. A cyst can be removed and the patient can recover to a good quality of life. Because MRI findings for the neurenteric cyst in the dog of the present report were nonspecific and given the variable MRI findings in humans with neurenteric cysts, histologic examination of the abnormal tissue is recommended to achieve a definitive diagnosis in dogs with similar lesions.

Footnotes

a.

MAGNETOM Espree, Siemens, Berlin, Germany.

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