A Case of Normal-pressure Hydrocephalus Caused by Cauda Equina Capillary Malformation

Abstract

Capillary malformations in the central nervous system, especially in the cauda equina, are rare. Although the typical symptoms are lower back pain and motor weakness in the lower extremities, we report here a rare case in which the initial symptom of a capillary malformation in the cauda equina was normal-pressure hydrocephalus. A 67-year-old woman was admitted to our hospital for close examination of hydrocephalus. Imaging studies showed no abnormalities other than an 8-mm intradural extramedullary tumor at the lumbar 2 level. Given lumbar puncture revealed a high protein level and the pressure was within the normal range, we assumed the hydrocephalus was caused by a schwannoma in the cauda equina. Within 7 days after admission, the patient's consciousness level decreased rapidly. Therefore, we immediately placed a ventriculoperitoneal shunt. Nine months after admission, the tumor increased from 8 mm to 12 mm in diameter, and tumor resection was performed. Because intraoperative neuromonitoring revealed that the tumor arose from a motor nerve, and the appearance of the tumor was not that of a typical schwannoma, we decided to remove the tumor subcapsularly. The pathological diagnosis was a capillary malformation. No neurological deficits developed in the patient postoperatively, and the high cerebrospinal fluid protein level normalized after the tumor resection. Although hydrocephalus caused by a capillary malformation in the cauda equina is relatively rare, it should be differentiated, and the strategy for its resection should be considered using the information obtained from preoperative neurological symptoms and intraoperative neuromonitoring.

Introduction

Capillary malformations (CMs) commonly occur in the skin, with occurrences within the central nervous system, particularly the spinal cord, being quite rare.¹⁾ CMs of the central nervous system are considered congenital anomalies and exhibit a higher prevalence in males, with a mean age of presentation at around 50 years. Approximately 60% of cases are located in the lumbar region and are frequently associated with pain corresponding to the affected nerve innervation region. Imaging studies typically reveal homogeneous enhancement with gadolinium contrast. The prognosis for symptomatic cases is generally favorable after surgical excision. Although most CMs of the central nervous system are typically intramedullary in origin, reports of such lesions occurring in the cauda equina are exceedingly rare. Most documented cases present with symptoms such as lower back pain, lower limb weakness, and sensory deficits.²⁾ However, to the best of our knowledge, no cases of cauda equina CMs associated with hydrocephalus have been reported in previous literature.

This study reports a case of cauda equina CM presenting with normal-pressure hydrocephalus in the absence of other neurological symptoms.

Case Report

History and radiological diagnosis

A 67-year-old woman presented to a physician with the chief report of impaired consciousness characterized by diurnal fluctuations. An initial head computed tomography (CT) scan revealed enlargement of all ventricles (Fig. 1A-C). Two months later, she was admitted to our neurology department for further assessment of hydrocephalus. Upon admission, her Glasgow Coma Scale (GCS) score was E3V3M6. Her vital signs, pupillary reactions, and motor and sensory functions were normal. A second cranial CT scan revealed progression of the hydrocephalus (Fig. 1D-F). Further study of the head and entire spine using magnetic resonance imaging (MRI) revealed an intradural enhanced mass lesion at the lumbar 2 vertebral level, with homogeneous enhancement after contrast administration (Fig. 2A and B). Subsequently, the patient underwent lumbar puncture, which revealed a normal opening pressure (18.5 cmH₂O) and high total protein level (326 mg/dL). Considering the elevated cerebrospinal fluid (CSF) protein levels and the mass lesion in the cauda equina, we diagnosed the tumor as a schwannoma that caused CSF malabsorption and hydrocephalus.

Fig. 1

Preoperative images of the cerebral ventricles.

A-C: CT showed mild enlargement of all ventricles. D-F: Two months later, there was clear enlargement of all the ventricles, especially the anterior and inferior horns of the lateral ventricles, in addition to the third ventricle, as indicated by the arrowheads.

CT: computed tomography

Fig. 2

Preoperative image of the spine.

A: Preoperative Gd contrast-enhanced T1-weighted sagittal MRI showed a mass lesion approximately 8 mm in size in the dura at the L2 lumbar spine level. B: T1-weighted axial MRI with Gd. C: At follow-up 9 months later, T1-weighted sagittal MRI with Gd showed tumor enlargement from approximately 8 to 12 mm. D: T1-weighted axial MRI with Gd.

Gd: gadolinium; MRI: magnetic resonance imaging; T1: type 1

Within 7 days after hospitalization, given the patient's consciousness level decreased from GCS E3V3M6 to GCS E2V1M4, a ventriculoperitoneal (VP) shunt was immediately implanted. By the 23rd day after the VP shunt implantation, the patient's level of consciousness recovered completely, and by the 33rd day, she could walk by herself.

Surgery and pathological diagnosis

Follow-up spinal MRI performed eleven months after the hydrocephalus presentation showed that the tumor in the cauda equina had increased from 8 mm to 12 mm in diameter (Fig. 2C and D), although without any neurological symptoms. Hence, tumor resection was performed. During surgery, L1/L2 laminectomy was performed to expose the tumor. The tumor exhibited a reddish color, firm consistency, and multifocal structure with a significant internal component, without evidence of seroma, hematoma, or discernible feeder or drainer vessels. It appeared to be occurring on the motor nerve root and firmly attached to it (Fig. 3A and B). Stimulation of the proximal and distal nerves of the tumor elicited responses exclusively on the left side in the quadriceps muscles, anterior tibialis muscles, lower limb muscles, short flexor muscles of the thumb, anal sphincter muscles, and bladder and rectal muscles (Fig. 3C). However, no response was observed when the tumor itself was stimulated. The appearance of the tumor was atypical for schwannoma, and rapid intraoperative pathological examination showed small lymphocyte clusters in fibrous tissue with a few spindle cells without significant atypia, not confirming schwannoma. Therefore, the nerve root was not resected, and only intracapsular tumor removal was performed. There was no decrease in transcranial motor evoked potentials observed during the surgery. Histopathological examination revealed the excised specimen to predominantly comprise fibrous tissue with diffuse capillaries, and areas of capillary hyperplasia, leading to the diagnosis of CM (Fig. 4A and B). CD34 staining showed dense clusters of blood vessels (Fig. 4C), whereas Mindbomb E3 Ubiquitin Protein Ligase 1 (MIB-1) staining showed positive results for only a few cells (Fig. 4D), and hematoxylin-eosin staining showed a large amount of fibrous tissue in the stroma (Fig. 4E), indicating an organizing hematoma.

Fig. 3

Intraoperative images

A: Intraoperative gross image of the tumor. The arrowhead indicates the inlet of nerve, and the arrow shows the outlet of nerve. The asterisk indicates the organizing hematoma. The appearance of the tumor differed from that of a typical schwannoma, and there was no obvious hemorrhage. B: Postoperative gross image of the resection site. The arrowhead indicates inlet of nerve, and the arrow shows the outlet of nerve. C: Nerve monitoring during intraoperative nerve stimulation of the tumor, before resection. The arrows show the responses to tumor nerve stimulation

Fig. 4

Pathological images of the tumor

A: HE staining showed the resected specimen as being mainly occupied by fibrous tissue, with increased capillary vascularity within the fibrous tissue, as indicated by each arrow. B: EVG staining clearly showed diffuse focal capillary hyperplasia, as indicated by each arrow. C: CD34 staining showed densely clustered blood vessels. D: MIB-1 staining showed positive results for vascular endothelium, as indicated by the arrows, in a small number of regions. E: HE staining showed a capillary hemangioma on the left side of the Fig. and an organizing hematoma on most of the right side.

EVG: Elastica van Gieson; HE: hematoxylin-eosin; MIB-1: Mindbomb E3 Ubiquitin Protein Ligase 1

Postoperative course

CSF analysis performed 5 months after the tumor resection revealed a marked reduction in total protein concentration from 326 mg/dL to 38 mg/dL. Approximately one year after surgery, the patient exhibited no neurological deficit or tumor recurrence. Valve pressure of the VP shunt was maintained at 15 cmH₂O, with no signs of ventricular enlargement.

Discussion

In this study, we report a rare case of CM occurring in the cauda equina, which presented with normal-pressure hydrocephalus. Notably, there have been no documented cases of CMs directly associated with normal-pressure hydrocephalus. Makino et al.³⁾ previously reported a case of hydrocephalus secondary to subarachnoid hemorrhage resulting from a cavernous hemangioma in the cauda equina. However, in the present case, the etiology of hydrocephalus was assumed to differ from that of hemangiomas, because the pathological characteristics of CMs differ from those of cavernous hemangiomas, and subarachnoid hemorrhage was absent in our case.

Numerous cases of hydrocephalus related to spinal cord tumors have been reported, and most of the cases were attributed to schwannomas. Besides cases of schwannomas in the cauda equina,⁴⁾ vestibular schwannomas are also known to cause non-obstructive hydrocephalus.⁵⁾ The proposed mechanisms of schwannoma-related hydrocephalus include obstruction of CSF absorption by the tumor within the cauda equina, which plays an essential role in CSF absorption, or a tumor-induced increase in protein production, subsequently impairing CSF absorption in the arachnoid granules,^6-10) although details of these mechanisms remain unclear. The elevated protein concentration in the CSF sample, which normalized after tumor resection, suggests the possibility of CSF malabsorption akin to that observed in schwannoma cases. In this case, although the tumor showed rapid enlargement over a short period, immunostaining did not indicate a high proliferative potential of the tumor cells. The presence of an organizing hematoma suggests that the growth might have been driven by bleeding from the vascular malformation rather than cellular proliferation. In addition, the elevated CSF protein levels could be attributed to partial disruption of the blood-nerve barrier caused by tumor-associated hemorrhage, leading to leakage of intratumoral proteins into the CSF cavity, although further investigation is needed for conclusive evidence.

The decision to perform nerve root resection for cauda equina tumors typically hinges on factors such as tumor size, preoperative motor and sensory deficits, and intraoperative neuromonitoring.¹¹⁾ Although nerve root resection is preferable for minimizing tumor recurrence,¹²⁾ it carries the potential risk of exacerbating postoperative neurological symptoms. In a few previous reports detailing nerve root resection for cauda equina CM,¹³⁾ the patients exhibited preoperative dysesthesia, with intraoperative findings revealing vascular malformation of the sensory nerves, facilitating safe nerve root resection.¹⁴⁾ Conversely, in our case, preoperative motor paralysis and sensory deficits were absent, and intraoperative neuromonitoring indicated that the tumor invaded a motor nerve. In cases of cauda equina schwannoma, even if the tumor originates from motor nerves, postoperative exacerbation of motor paralysis after nerve root resection is reportedly mild owing to the extensive innervation of lower limb muscles by multiple nerves.¹⁵⁾ These observations have been documented in cases in which motor paralysis had advanced owing to tumor progression, with subsequent innervation presumably developing from adjacent nerves. In this case, however, there was no preoperative motor paralysis, making it uncertain whether compensation by the adjacent nerves could be anticipated. In addition, because the tumor was firmly attached to the nerve, subcapsular resection was selected, although a definitive diagnosis could not be determined by intraoperative rapid pathology. Although this approach carries a risk of tumor recurrence, the patient did not experience any new neurological symptoms postoperatively. In this case, determining the optimal resection strategy necessitated thorough consideration of intraoperative findings and responses to nerve monitoring, in addition to preoperative nerve assessments.

Conclusion

We encountered an infrequent CM in the cauda equina presenting with normal-pressure hydrocephalus. The tumor was diagnosed as occurring on the motor nerve by intraoperative nerve stimulation responses and was resected subcapsularly while preserving the nerve root. The patient's postoperative course was good. Our experience suggests the importance of performing surgery by comprehensively evaluating preoperative symptoms, intraoperative findings, and intraoperative neuromonitoring.

Conflicts of Interest Disclosure

All authors have no conflict of interest.

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