Intramedullary Spinal Cord Cavernous Malformations Frank P. K. Hsu, MD, PhD, Richard E. Clatterbuck, Robert F. Spetzler, MD
lntramedullary spinal cord cavernous malformations are rare lesions and account for a small percentage of clinically evident cavernous malformations. However, the reported incidence rates likely underestimate their true rate of occurrence. The advent of magnetic resonance imaging has increased the diagnosis of these lesions as it has that of their intracranial counterparts. Our understanding of their natural history, however, is less well developed given their relative rarity and the devastating consequences of conservative management of symptomatic cavernous malformations of the spinal cord. Nevertheless, surgical management of these lesions with meticulous microsurgical technique and appropriate perioperative care has been quite successful. We report our experience with intramedullary spinal cord cavernous malformations and detail our surgical technique and perioperative management. Copyright 2003, Elsevier Science (USA). All rights reserved.
malformations consist of endothelial-lined vasembedded in a collagenous matrix. They are surroundedby gliotic, hemosiderin-stained neural tissue. In addition to flo+ng blood, these channels are filled with thrombosed blood and degrading blood products of various ages. This fact, in conjunction with the clustered arrangement of the channels, gives rise to the classic mulberry description of their gross appearance. Cavernous malformations arise from the capillary venous side of the central nervous system (CNS) circulation as evidenced by the low pressure and slow flow within their vascular channels. Ultrastructural studies show that these vascular channels are poorly organized with gaps between adjacent endothelial cells. An abnormal basal lamina likely contributes to their propensity to b1eed.l Radiographically, these lesions have a pathognomonic popcorn appearance characterized by a reticulated core surrounded by a hypointense ring (Fig 1). This radiographic appearance is also explained by blood products in various stages of degradation;- including the hypointense ring created by the magnetic susceptibility of hemosiderin in the adjacent neural tissue.2 The radiographic and histologic appearances of intramedullary spinal cavernous malformations are similar if not identical to those found elsewhere in the CNS, and they represent the same disease process. 324Lesi’ons in the spinal cord, like those in the brainstem, appear to have an aggressive natural history. This characteristic does not necessarily change the indications’
C,cular channels avernous
From the Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, AZ, USA. Address reprint requests to Robert F. Spetzler, MD, c/o Neuroscience Publications; Barrow Neurological Institute, 350 W. Thomas Road; Phoenix, AZ 85013-4496; [email protected]
Copyright 2003, Elsevier Science (USA). All rights reserved. 1092-440X/03/0601-0001$35.00/O doi:l0.1053/otns.2003.36333
MD, PhD, Louis J. Kiti, MD, and
for surgical intervention; however, it does lower the threshold for surgery and the percentage of patients undergoing operations. This article reviews the natural history and treatment of intramedullary spinal cord cavernous malformations as well as our experience with these lesions. The discussion focuses on the perioperative management and surgical techniques associated with treating patients with these lesions.
Natural History of Rntramedullary Spinal Cord Cavernous Malformations There ark several prospective studies on the natural history of cerebral cavernous malformations.5-11 Given their relative rarity, however, no analo$ous data exist for intramedullary spinal cord cavernous malformations. Nonetheless, it is widely believed that the latter are more aggressive than their cerebral counterparts, much like brain stem and deep cavernous malformations.*J2 It is intuitive that densely organized, eloquent structures such as the brainstem and spinal cord would be more susceptible to the effects of even microscopic hemorrhages. Consequently, cavernous malformations in the brain stem and spinal cord might exhibit much more aggressive clinical behavior despite identical biological behavior compared to lesions elsewhere in the CNS. The findings from large magnetic resonance imaging (MRI)based11J3 and autopsy14J5 series suggest that cavernous malformations account for 1 of every 10 cerebrovascular malformations and are found in less than 1% of the population. The literature suggests that intramedullary spinal cord cavernous malformations represent only a small percentage (less than 5%) of all CNS cavernous malformations.16 Although authors disagree on the exact number, 17-19the worlds literature on intramedullary spinal cord cavernous malformations consists of less than 200 cases, making discussions of their incidence of questionable value. However, a review of the cases in the literature does provide insight into the clinical presentation and course of patients harboring intramedullary spinal cord cavernous malformations. In the largest published literature review, Zevgaridis et al. reviewed the clinical presentation and course of 116 patients (47 males, 69 females) with 117 lesions. The patients ranged from 12 to 88 years old. The peak incidence of presentation was in the fourth decade. The distribution of cavernous malformations along the spinal cord was consistent with the volume of tissue in each region. Cervical lesions accounted for 39%, thoracic lesions for 54%, and lumbar lesions for 7% of the total number. Clinical presentation w?s divided into three major patterns. Thirty percent of patients experienced episodic neurological deterioration with intervening and variable recovery. Forty-one percent experienced slow, progressive neurological deterioration. Of the remaining 29% of patients, 26% experienced an abrupt onset of symptoms followed by neurological
Vol 6, No 1 (March), 2003: pp 32-40
mained stable, and 6% were worse. The only clinical variable predictive of, outcome was the duration of symptoms before treatment. Of patients with symptoms for less than 3 years, 76% improved after surgery. Of patients with symptoms for longer than 3 years, only 52% improved after surgery. These findings led the authors to recommend surgery for symptomatic patients.
The Barrow Neurological Institute Experience
Fig 1. (A) Sagittal TP-weighted image shows an intramedullaty lesion behind the bodies of the fourth and fifth thoracic vertebrae with the classic radiographic appearance of a cavernous malformation. (B) Axial image at this level also shows the lesion.
decline (16% rapidly and 10% gradually). Based on radiological criteria, 58% ofpatients experienced a hemorrhage. Of the 91 patients who underwent surgery, 66% improved, 28% reSPINAL
Between 1988 and 2002, 44 patients with symptomatic intramedullary spinal cord cavemqus malformations presented for surgical management at our institution. Age at diagnosis ranged from 14 to 71 years (mean, 41.5 years). There were 22 cervical, 18 thoracic, 3 conus, and 1 lumbar lesions. At surgery 8 patients had an episodic course, 10 patients exhibited progressive neurological decline, and 26 patients had acute neurological symptoms.20 Assuming that intramedullary spinal cord cavernous malformations were present since birth, we retrospectively determined that 54 acute neurological events (representing hemorrhage) occurred in 1673 patient-years (unpublished data). These findings equate to an event rate of 3.2% per patient-year for intramedullary spinal cord cavernous malformations, which is higher than the previously reported values of 1.4 to 1.6% per patient-year calculated from meta-analyses of reported intramedullary spinal cavernous malformations.i7~2i Our value may reflect the selection bias of our surgically treated population. However, it also suggests that a detailed account of patient symptoms related to their lesion may reveal that the rate of hemorrhage is higher than previously thought. Furthermore, this value must underestimate the true rate ,of hemorrhage because most lesions likely develop after birth, many perhaps in adulthood. Eleven of our patients suffered multiple hemorrhages with a mean interval of 6.1 years between hemorrhages. All patients were approached posteriorly. For more ventrally situated lesions, a transpedicular-posterolateral approach was employed. Lesions at the spinal cord surface were excised directly while deeper intramedullary spinal cavernous malformations required dorsal myelotomies. In most cases, the location of the lesion was evident when the spinal cord was visualized. However, when no stigmata of hemorrhage or the malformation itself was evident, ultrasonography was helpful. Postoperatively, new or worsening deficits were identified in 55% of cases. This finding supports the notion that surgical extirpation mimics a hemorrhagic episode. During follow-up, 91% of these patients improved. Overall, Frankel grades improved in 91% of patients. Glasgow Outcome Scale scores were good or excellent in 65%, fair in 26%, and poor in 9%. The overall complication rate was 16%. The complications included two patients who re-hemorrhaged after incomplete resection, and one patient with a cerebrospinal fluid (CSF) leak requiring wound revision. Two patients developed postoperative cervical kyphosis that required stabilization. After their initial surgery, five patients experienced recurrent hemorrhages because of residual cavernous malformation. The mean interval between hemorrhages in this subset was 3.4 years compared to 6. I years among patients with untreated intramedullary spinal cord cavernous malformations. Although the number of recurrent lesions is small, this finding suggests that incompletely resected intramedullary spinal cord cavernous
Fig 2. lntraoperative photograph shows the laminoplasty resection of intramedullary cavernous malformations.
malformations are associated with a higher risk of hemorrhage than untreated ones. During long-term follow-up (mean, 3 years), 8 of 11 patients (79%) who presented with pain symptoms continued to experience significant pain. The quality of pain consisted of burning and numbness radiating through the affected extremities. This chronic pain syndrome has been largely refractory to medication. It may be related to hemosiderin staining of spinal cord parenchyma affecting ascending sensory pathways. Although intramedullary spinal cord cavernous malformations are rare lesions, our relatively large single-institution.series indicates that their natural history may be worse than previously reported. Complete surgical excision can halt the
used to access,and
the spinal ,canal for
progression of neurological decline and prevent further hemorrhagic episodes.
Ouerative Techniaue for Resect&m bf Int~amedullary Spfnal Cord Cavernous Malformations Intramedullary spinal cord cavernous malformations can be resected safely with microsurgical techniques. The principles of gentle manipulation of eloquent tissues, meticulous hemostasis, and watertight dural closure need to be strictly applied. Most lesions can be removed through a posterior approach, but
Fig 3. lntraoperative photograph taken after dural opening. The intact arachnoid is clearly seen as is discoloration representing the cavernous malformation. Tenting sutures are being pJaced to retract the dura.
Fig 4. Hemosiderin staining of the surface of the spinal cord as visualized through the operating allows a direct approach to the lesion, avoiding a midline myelotomy.
more ventral lesions may require posterolateral or anterior approaches. The patient is intubated and placed on the operating table. Final positioning depends on the approach selected, but most patients are placed prone because most lesions can be approached from posteriorly. Prone positioning can be accomplished on any of the commercially available frames (eg, Wilson frame, Jackson table). However, chest rolls on a standard operating table are sufficient for patients with an average body
habitus. For cervical lesions, patients are placed in the Mayfield headholder. Care must be taken to pad all pressure points adequately to protect vulnerable peripheral nerves. Somatosensory evoked potentials are monitored. In patients with preoperative deficits, baseline testing before final positioning or surgery can prove valuable in the interpretation of intraoperative recordings. Preoperative antibiotics are administered, as is methylprednisolone according to the protocol established by the National Acute Spinal Cord Injury Study.22 First, meth-
Fig 5. Suture @cement through a cut dentate ligament allows gentle retraction and rotation of the spinal cord. Thiis maneuver helps center the lesion in the operative field. SPINAL
Fig 6. High-magnification intraoperative photograph shows the sharp dissection technique used to resect intramedullary cavernous malformations. A sharp microdissector is being used to deliver the lesion into the field while microsuction is used to apply gentle counter-traction. _ ylprednisolone is given in a bolus dose of 30 mg/Kg body weight over 15 to 20 minutes. An infusion (5.4 mg/Kg body
later. The laminoplasty
by making small laminotomies
at the caudal margin
weight) follows in 40 to 45 minutes and each hour thereafter for
of the lamina. A high-speed
the lamina bilaterally in a rostra1 direction. If possible, the intraspinous ligaments should be maintained to allow reconsti-
A *midline incision expose the appropriate radiography
are used to
is used to localize the appropriate level. Fishhooks
drill with a footplate is used to cut
tution of the posterior tension band. The removed segments of lamina are replaced at the end of the case v&h microplates and
and bilateral Leyla bars are used to retract soft tissue laterally. A
screws or sutures (Fig 2):.
For more ventral lesions, a costotransversectomy or a transpedicular approach may be required.23 The lateral elements and
We prefer laminoplasty
at the levels of the
Fig 7. Thorough inspection of the surgical bed under high magnification after removal of the cavernous nnalformation is ess;ential to ensure complete resection and to prevent a recurrence. Often a venous structure consistent with a venom.lS am )maly is seen and should be preserved.
klsu ET I4L
Fig 8. (A) Sagittal and (B) axial MRls of the lower thoracic
the pedicle at the appropriate level can be removed using a high-speed drill on the side of the lesion to provide a wider corridor of approach and to minimize spinal cord retraction and rotation. Rarely, an anterior approach with corpectomy or vertebrectomy is necessary for a midline anterior intramedullary spinal cord cavernous malformation. Anterior approaches require fusion and instrumentation after resection. They are less popular because their working depth is greater and the dural closure is more difficult than in a laminoplasty. Hemostasis is essential before the dura is opened to obtain clear visualization of the surface of the spinal cord. Epidural bleeding is controlled with bipolar coagulation. Hemostatic agents and cottonoids can be used to line the lateral limits of laminoplasty. An operating microscope is used for the remainder of the procedure. The dura is opened in the midline with a No. 11 blade. Tenting sutures are placed to retract the dura laterally (Fig 3). The arachnoid layer is opened separately using sharp dissection SPINAL
spine show an intramedullaty
with microscissors. It is attached to the dural layer with microclips. Ideally, visualization of hemosiderin staining on the surface of the spinal cord and the lesion beneath allows a direct approach to the lesion. The surgeon can then avoid a midline or lateral myelotomy (Fig 4). When the lesion is not apparent, ultrasonography is helpful in localizing it. Myelotomy in the midline or dorsal root entry zone may be necessary to reach deeper lesions. Resection of ventrolateral lesions may require sectioning the dentate ligaments at several levels to allow safe rotation of the spinal cord. Once cut, the dentate ligaments can be retracted gently using sutures to rotate the spinal cord. This maneuver offers a more direct angle of approach to ventral lesions (Fig 5). Once the cavernous malformation is identified, great care must be taken to minimize retraction of normal spinal cord tissue. Under high-power magnification, the lesion is dissected using gentle suction and countertraction (Fig 6). Microscissors, microdissectors, microcurettes, and microrongeurs are helpful
Fig 9. An area of bluish discoloration cord. instruments
tions are composed
indicates the location of the cavernous
nels, and major bleeding is seldom encountered
in the dorsal midline of the spinal
fashion using 6-O Prolene.
to prevent a potential Postoperatively,
tion. The lesions are removed in a piecewise fashion. Typically,
unit. In our experience,
a gliotic, hemosiderin-stained
typical, and its severity is comparable
ery of the lesion facilitates and gentle cauterization Venous anomalies,
(Fig 7). Incomplete
which are often visible during dissection
should be preserved.
cavity is thoroughly resection
may be used sparingly to
can lead to a recur-
The dura is closed
rhage from the cavernous sient worsening
of the lesion increase working,space.
a spinal cord cavernous malformation, Low-current
ment includes described
Fibrin glue may be used
in the intensive
earlier and maximization
spinal cord protocol of spinal perfusion
fluids and the artificial
arterial pressure if necessary.
to an episode of,hemor-
resolves in most patients. the methylprednisolone
CSF is diverted as needed to treat
leakage across the incision
after surgery. Aggressive and early
with a pain specialist
should be considered
Fig 10. A lesion with the classic mulberry appearance is seen just below the pia and corresponds to the bluish discoloration seen in Fig 9. The large overlying vessel has been preserved and retracted! out of the resection site.
Fig 11. Photograph
tients with persistent tion.
of the resection
pain in an anatomic distribu-
seen in situ in Figs 9 and IO.
The dentate ligaments
and used to rotate the
spinal cord gently to obtain a direct angle of approach
The lesion was resected as described in the section on operative technique.
the patient’s lower extremity weakand she needed rehabilitation.
patient progressively regained strength in her leg comparable her preoperative status.
Case 1 A 51-year-old
female presented with the acute onset of midtho-
racic pain that progressed
to left leg dysesthesia
in a month. MRI revealed an intramedullary mation (Fig 1). Given her progressive underwent
The lesion was located ven-
trally on the right side of the spinal cord. Through
scope it was observed to have reached the pial surface (Fig 4).
Case2 A 25-year-old
male had experienced
weakness ‘and numbness
in his legs for 1.5 years. MRI revealed an intramedullary ernous malformation plasty at TlO and Tll
(Fig 8). He underwent
(Fig 3). The lesion was immediately
Fig 12. Inspection of the hemosiderin-stained cavity after resection of the cavernous malformation reveals the ubiquitous underlying venous anomaly. Unlike the resection of supratentorial cavernous malformations, the surrounding hemosiderinstained spinal cord tissue must be preserved given the eloquence of the structure. SPINAL CORD CAVERNOUS MALFORMATIONS
identified by the area of bluish discoloration (Fig 9). The mulberry-like lesion was carefully resected using microsurgical (Figs. 10 and 11). After the cavernous malformation
was resected, an associated venous anomaly was preserved (Fig. 12).
spinal cord cavernous
tions are identical to their cerebral counterparts. in the exquisitely
sensitive and eloquent spinal cord, however,
is likely responsible
for their more aggressive clinical behavior.
These lesions can manifest with episodic and stepwise deficits, slow progressive
or an acute deficit that progresses
slowly or rapidly. Their aggressive early surgical intervention sible. Most lesions
can be resected
proach. Lesions reaching resected
malformations Patients, immediate
elotomy with the aid of ultrasonography. crosurgical
spinal cord cavernous
can be removed with good clinical
the surface of the spinal cord can be
should be approached
course argues for
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natural history of cerebral venous malformations. Neurosurgery 43: 195-200, 1998 8. Porter RW, Detwiler PW, Spetzler RF, et al: Cavernous malformations of the brainstem: Experience with 100 patients. J Neurosurg 90:5058, 1999 9. Kondziolka D, Lunsford LD, Kestle JR: The natural history of cerebral cavernous malformations. J Neurosurg 83:820-824, 1995 10. Zabramski JM, Wascher TM, Spetzler RF, et al: The natural history of familial cavernous malformations: Results of an ongoing study. J Neurosurg 80:422-432, 1994 11. Robinson JR, Awad IA, Little JR: Natural history of the cavernous angioma. J Neurosurg 75:709-714, 1991 12. Fritschi JA, Reulen HJ, Spetzler RF, et al: Cavernous malformations of the brain stem. A review of 139 cases. Acta Neurochir (Wien) 130:35-46, 1994 13. Del Curling 0 Jr, Kelly DL Jr, Elster AD, et al: An analysis of the natural history of cavernous angiomas. J Neurosurg 75:702-708, 1991 14. Otten P, Pizzolato GP, Rilliet B, et al: 131 cases of cavernous angioma (cavernomas) of the CNS, discovered by retrospective analysis of 24,535 autopsies [French]. Neurochirurgie 35:82-3-128.. 31, 1989 15. Sarwar M, McCormick WF: lntracerebral venous angioma. Case report: and review. Arch Neurol 35:323-325, 1978 16. McCormick PC, Michelsen WJ, Post KD, et al: Cavernous malformations of the spinal,cord. Neurosurgery 23:459-463, 1988 17. Zevgaridis D, Medele RJ, Hamburger C, et al: Cavernous haemangiomas of the spinal cord. A review of 117 cases. Acta Neurochir (Wien) 141:237-245, 1999 18. Deutsch H, Jallo GI, Faktorovich A, et al: Spinal intramedullary cavernoma: Clinical presentation and surgical outcome. J Neurosurg 93:65-70, 2000 19. Ghogawala Z, Ogilvy CS: lntramedullary cavernous malformations of the spinal cord. Neurosurg Clin N Am 10:101-l 11, 1999 20. Vishteh AG, Sankhla S, Anson JA,,et al: Surgical ‘resect/on of intramedullary spinal cord cavernous malformations: Delayed complications, long-term outcomes, and association with cryptic venous malformations. Neurosurgery 41:1094-l i 01, 1997 21. Canavero S, Pagni CA, Duca S, et al: Spinal intramedullary cavernous angiomas: A literature meta-analysis. Surg Neurol 41:381-388, 1994 22. Bracken MB, Shepard MJ, Collins WF, et al: A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal-cord injury. Results of the Second National Acute Spinal Cord Injury Study. N Engl J Med 322:1405-1411, 1990 23. Martin NA, Khanna RK, Batzdorf U: Posterolateral cervical or thoracic approach with spinal cord rotation for vascular malformations or tumors of the ventrolateral spinal cord. J Neurosurg 83:254-261, 1995
(,HSU ET AL