Spinal Cord Cavernous Malformations G. Michael Lemole, Jr, MD, Giuseppe Lanzino, MD, Jeffrey S. Henn, MD, and Robert F. Spetzler, MD
With the widespread availability of magnetic resonance imaging, spinal cord cavernous malformations are diagnosed frequently, even in patients with mild symptoms. Increasing experience with the surgical resection of these lesions has also led to excellent outcomes in most patients. This article details the indications for surgery and the techniques used to resect spinal cord cavernous malformations. Copyright 2002, Elsevier Science (USA). All rights reserved.
lthough cavernous malformations of the spinal cord have
A long been known to occur, their clinical spectrum has been
characterized only since the recent widespread availability and use of magnetic resonance imaging (MRI). As understanding of the clinical course of these lesions has improved, a definitive role for surgical treatment has emerged, particularly for lesions involving the spinal cord. This article reviews current indications for surgery and the operative techniques used in the resection of spinal cord cavernous malformations. Although extradural and intradural-extramedullary lesions are sometimes encountered, 1~this article focuses on intramedullary cavernous malformations only.
Epidemiology and Clinical Presentation Previous studies have suggested that spinal cord cavernous malformations represent 5 to 12% of all spinal vascular abnormalities, 5,19 and 3 to 5% ~2 of all cavernous malformations occurring in the central nervous system. There is a slight female predominance. HaSaF,t9 The mean age at symptomatic presentation and diagnosis is usually in the fourth decade of life. 15,19 The thoracic cord is most often involved followed by the cervical cord. ~5 Lumbar lesions or lesions involving the conus medullaris or cauda equina are the least common. 15,17 Preliminary observations suggest that patients with spinal cord cavernous malformations might be at increased risk for multiple cavernous malformations throughout the neuraxis, is ' T h e color of spinal cord cavernous malformations ranges from dark blue to reddish brown. Although the lesions are well circumscribed, the adjacent spinal cord typically shows evidence of old hemorrhage in the form of yellow or orange discoloration caused by hemosiderin. Occasionally, this discoloration is the only visual clue that a cavernous malformation may be under the pial surface. A gliotic plane is present around the
From the Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, AZ iAddress reprint requests to Robert F. Spetzler, MD, c/o Neuroscience P~blications; Barrow Neurological Institute, 350 West Thomas Road; Phoenix, AZ 85013-4496; [email protected]
iCopyright 2002, Elsevier Science (USA). All rights reserved. doi:10.1053/otns.2002.32485
malformation. "Tongues" of cavernous malformations often infiltrate the surrounding gliotic plane. These;extensions stress the importance of inspecting the resection bed to prevent recurrences (see Surgical Principles). The size of cavernous malformations of the spinal cord varies from a few millimeters to centimeters. The slow growth of the malformation can cause the !esion to displace almost the entire cross section of the spinal cord without visibly enlarging the spinal cord itself. Consequently, before MRI was available, lesions might not be visualized on myelography despite their significant size. As with cerebral cavernous malformations, a developmental venous anomaly is almost always associated with a spinal cord cavernous malformation. IF ! The clinical course of spinal cord cavernous malformations is variable. Patients can become symptomatic with acute, progressive symptoms, or a stepwise deterioration can mimic demyelihating disorders such as multiple sclerosis.n, ~9 An acute presentation is usually the result of hemorrhage. Hemorrhage can occur within the malformation in the sinusoidal spaces, causing rapid, acute expansion. Frank hemat0myelia (ie, hemorrhage within the spinal cord) associated with devastating neurological sequelae has also been documented.3, > Typically, acute presentations are characterized by pain corresponding to the level of the cavernous malformation. In such cases, neurologi-, cal deterioration can evolve over hours or even days, 6a5 differentiating hemorrhage from a cavernous malformation from hemorrhage from arteriovenous malformations of the spinal cord (in which neurological deterioration is concomitant with acute pain). 12 Initial hemorrhage can cause paraplegia or tetraplegia; usually, however, the original hemorrhage causes incomplete neurological deficits followed by some level of recovery. In untreated lesions, repeated hemorrhages can occur months to years after the initial hemorrhage. 11 ,1 5 A more subtle presentation also occurs. Patients initially complain of intermittent paresthesias when the lesion is primarily localized on the dorsal aspect of the spinal cord. Lesions near the dorsal root entry zone can mimic a corresponding level of radiculopathy. 4 With the widespread use of MRI even in patients with transient or minimal symptoms, cavernous malformations are now often discovered at an early stage or even while asymptomatic. Analysis of early series reveals a common pattern of progressive neurological deterioration after a variable period that follows the initial presentation of untreated lesions, z5 Unfortunately, most of the available series are surgical series. Therefore, a selection bias for treating and reporting more aggressive cases cannot be excluded. Studies on the natural history of spinal cord cavernous malformations are lacking; thus, the true hemorrhage rate and the incidence of neurological deterioration in patients harboring these lesions are unknown. Trauma, pregnancy, and strenuous activity have all been associated with acute deterioration caused by spinal cord cav-
Operative Techniques in Neurosurgery, Vol 5, No 3 (September), 2002: pp 155-160
ernous malformations; a causal link, however, has not been established. Occasionally, lesions at the pial surface cause subarachnoid hemorrhage. 2,8,~3 Hydrocephalus, probably related to a high protein content resulting from subclinical spillage of blood in the subarachnoid space, has also been associated with a cavernous malformation of the conus medullaris and cauda equina. 16
Diagnosis and Indications for Treatment The appearance of small cavernous malformations on MRI mirrors that of their cerebral counterparts and can be diagnostic. On T1- and T2-weighted MRI sequences, spinal cavernous malformations typically exhibit a mixed-density signal. Blood of various ages present from chronic hemorrhage gives malformations a mixed popcorn-like appearance. T2-weighted images especially demonstrate blood of various ages within the lesion as well as a hypointense ring of hemosiderin in the gliotic plane around the malformation (Figs 1 and 2). Cavernous malformations in the spinal cord rarely enhance with the administration of gadolinium contrast. Unlike their supratentorial counterparts, the diagnosis of spinal cord cavernous malformations with MRI is not always straightforward, especially small lesions. In some cases, spinal MRI can also be misleading for surgicalplanning when trying to estimate where the malformation comes closest to the surface of the spinal cord. Malformations thought on MRI to be located at the surface of the spinal cord may be found to be deeper on surgical exploration. Nevertheless. MRI represents an incredi-
ble improvement over other imaging modalities for the proper diagnosis and localization of intramedullary cavernous malformations. In terms of diagnosing these lesions, computed tomography and myelography are now obsolete and of historical interest only. The increasing experience with surgical excision of intramedullary cavernous malformations s,3,15ar and the high probability of neurological symptoms progressing, have expanded the role of surgical treatment for cavernous malformations. Studies published in the 1980s and early 1990s when patients were often diagnosed years after their initial presentation suggest that symptom progression is the rhle rather than the exception} 5 It is also clear that neurological outcome and the chance of useful recovery after surgical excision are closely related to a patient's preoperative level of neurological function. The best results and return to normal function are observed in patients with good preoperative neurological scores. Another important consideration is that the spinal cord, with its small cross section and high eloquence, is unlikely to tolerate even minor expansions of intramedullary cavernous malformations before significant neurological disability ensues.~S Recent surgical series have uniformly reported good outcomes and an acceptable rate of neurological morbidity after the surgical resection of cavernous malformations.l 1.ss,lr !Given these considerations, surgery should be recommended to appropriate candidates with symptomatic lesions, especiall3/when the cavernous malformation extends to the pial surface. Minimal controversy surrounds the issue of recommending surgical excision for the treatment of symptomatic patients.
Fig 1. A 28-year-old female presented with progressive paresthesiae involving her upper back over a period of 8 months. Sagittal T2-weighted MRIs show a heterogenous lesion with the characteristic appearance of a cavernous malformation involving the dorsal aspect of the cervical spinal cord at C3 to 4. Her father had underqone resection of a supratentorial cavernous malformation 1 year earlier, 156
LEMOLE ET AL
The decision, however, is considerably more difficult for patients with asymptomatic lesions or for those who have experienced minor and only transient symptoms. In such cases, recommendations for radical surgical excision must be tailored to the specific characteristics of each individual. We have observed sudden, devastating neurological deficits in patients with known, previously minimally symptomatic spinal cord cavernous malformations. This experience, combined with the knowledge that safe microsurgical resection of the lesion can be achieved in most cases, has led us to recommend surgery to an increasing number of patients with minor symptoms or with asymptomatic, incidental lesions when the cavernous malformation reaches the pial surface of the spinal cord. This statement is particularly true for young patients and for those harboring large cavernous malformations (when it is reasonable to believe that the spinal cord has a decreased neurological reserve to accommodate further expansion of the lesion from frank hemorrhage).
Surgical Technique The paradigm for treating spinal cord cavernous malformations closely parallels that of treating brain stem cavernous malformations. Like the brain stem, the highly eloquent spinal cord parenchyma poorly tolerates surgical intrusion outside the limits of the cavernous malformation. Most spinal cord' cavernous malformations can be exposed effectively and resected through a posterior approach. In our series of 17 lesions treated up to 1995, all were resected posteriorly through a laminectomy (n-= 9) or laminoplasty (n = 8). tr For dorsally situated spinal cord cavernous malformations, a simple laminectomy or laminoplasty a t the appropriate level should suffice. The proper level is identified radiographically once the patient has been positioned prone on the operating table. Intraoperative localization with fluoroscopy or plain film radiography with either anteroposterior or lateral views helps correlate the appropriate laminar level. For thoracic lesions, which may be difficult to localize intraoperatively, the skin level corresponding to the spinal cord level to be exposed can be marked preoperatively with an indelible marker after radiographic imaging. The patient's skin must be marked while the patient lies supine with arms above the shoulders or along the body, depending on the level of the lesion (for higher or lower thoracic lesions, respectively). For cervical and upper thoracic lesions in young patients, we recommend a laminoplasty to try to prevent a progressive kyphotic deformity, which can follow the removal of the posterior spinal elements. As long as there is no significant underlying degenerative disease, a laminoplasty can be performed safely by placing a Midas Rex B1 drill bit with a foot plate attachment under the lamina through a small laminotomy previously drilled in the inferior aspect of the lamina. The drill is then moved rostrally through the laminae to be removed. The same maneuver is repeated on the other side. The single piece of bone is then separated and lifted en bloc. Once the bone has been set aside and the underlying ligamentous structures have been
Fig 2. Same patient as in Figure 1. T2-weighted axial MRI images through the lower (A), middle (13), and upper (C) portion of the cavernous malformation confirm that the malformation reaches to the pial surface. SPINAL CORD CAVERNOUS MALFORMATIONS
Fig 3. Same patient as in Figure 1, intraoperative picture. The cavernous malformation was approached posteriorly through a C3 to 4 laminoplasty. The dura is opened under the microscope sharply along the midline. Care is exerted to maintain the arachnoidal layer intact. Note the bluish discoloration of the malformation visible through the opened dura.
removed, the lateral epidural gutters can be packed with hemostatic agents such as Gelfoam| (Upjohn, Kalamazoo, MI). At this point the surgical microscope is brought in to the surgical field. Under the magnification provided by the microscope, the dura is opened along the midline with care exerted to leave the arachnoid intact (Fig 3). The dural edges are retracted laterally and superiorly with tack-up sutures. The arachnoid is opened sharply in the midline, and its edges are secured to the ipsilateral dural leaflet. Absolute hemostasis must be obtained before the dura is opened to insure that the surface of the spinal cord is visible and to remove the malformation in a clean field under optimal conditions. After the dura and arachnoid are opened, the dorsal surface of the spinal cord is inspected closely under high magnification. Some cavernous malformations that extend to the surface are clearly visible at this point (gig 4). In other cases, a bluish or reddish-brown discoloration of the spinal cord surface (caused by hemosiderin staining of the pial surface from prior hemorrhage) is the only clue to the presence of an underlying lesion. In such cases, a small myelotomy performed at the level of the malformation provides adequate exposure. If the malformation is not clearly visible on the surface of the spinal cord or indirect clues about its presence are lacking, intraoperative ultrasonography aids proper localization of the malformation at its closest point to the pial surface. 7,~7 In such cases, a midline mye[otomy through the dorsal median sulcus or a more lateral myelotomy along the dorsal root entry zone is usually well tolerated and affords adequate access to the deeper portion of the lesion. Again, the incision over the cavernous malformation or myelotomy is performed under high magnification. Meticulous care must be exerted to avoid damaging adjacent normal spinal cord parenchyma. Resection of the lesion requires meticulous use of microcurretes and gentle suction aspiration (Fig 5). Typically, lesions must be removed piecemeal although sometimes they can be resected en bloc. Although not truly encapsulated, cavernous malformations have a Well-defined gliotic plane separating them from the spinal cord. Because cavernous malformations are formed by low-pressure sinusoidal vascular channels, bleeding is seldom a problem 1
during resection and can easily be controlled with gentle com-~ pression and the use of a hemostatic agent. We caution against the use of extensive electrocauterization within the spinal cord. Microfibrillar collagen or absorbable cellulose hemostatic agents are preferable. If bipolar cauterization is used, it should be very low power. We have observed an intimate association between venous draining anomalies and cavernous malformations of the spinal cord. t7 Our .experience with these lesions in the brain stem suggests that the venous anomalies should be left intact. These venous anomalies can drain adjacent eloquent tissue and their sacrifice could place those neural structures a~'risk. Often the venous anomaly is located adjacent to the cavernous malformation within or embedded in the side of the resection bed. Bleeding encountered toward the end of resection often may be from the portion of the venous anomaly draining the cavernous malformation. After meticulous hemostasis is obtained using the principles outlined above, careful inspection of the surgical bed under high magnification is imperative to identify and resect small "tongues" or nodules of the cavernous malformation that may extend into adjacent tissues (Fig 6). Incompletely resected lesions have a propensity to recur and rehemorrhage. 17 Every attempt should be made during the first surgery to resect the cavernous malformation fully (Fig 7). The dura is closed in a watertight fashion. Valsalva maneuvers can help identify areas of leakage, which can be reinforced with additional sutures. The dura may be further reinforced with fibrin glue. The laminoplasty piece is replaced with sutures or microplates and screws, if so desired. The paraspinous musculature and fascia are closed along with the subcutaneous tissues and skin in a meticulous fashion. Lesions involving the anterior and lateral aspects of the spinal cord must be approached with greater trepidation given the eloquent motor struetures contained therein. If a lesion is symptomatic and reaches an anterior or lateral pial surface, surgery can be attempted. Anterior spinal approaches may be used to access the anterior spinal cord, particularly the cervical region where the ventral surface of the spinal cord is easily visualized through a cervical c0rpectomy. Such an approach may necessitate a cervical fusion and fixation procedure after the spinal cord cavernous malformation is resected. The surgical technique is challenging because of the depth and narrowness of the operating field. Similar principles apply to the dural opening and closure as well as to entry through the spinal cord parenchyma and resection of the cavernous malformation. In the thoracic region, anterior approaches can be pursued through a thoracotomy with a corpectomy. While these approaches amply visualize the anterolateral ventral spinal cord, the depth of surgical field and the need for a surgical thoracot~ omy make them less than ideal. If an absolutely water-tight dural closure is not obtained, a spinal-to-pulmonary cerebrospinal fluid fistula could develop and will be further exacerbated if a chest tube is used to re-expand the ipsilateral lung. In these instances, the less intuitive, but equally efficacious approach as described by Martin and coworkers should be used. 9 These authors reported a patient with an anterolateral spinal cord cavernous malformation that was resected through a posterolateral transpedicular spinal approach in the thoracic spine, They combined a linear midline incision with a transverse incision to expose the posterolateral thoracic spine. The bony elements of the posterolateral thoracic spine were removed LEMOLE ET AL
Fig 4. Same patient as Fig 1, intraoperative picture. Under high magnification, the dorsal surface of the cervical spinal cord is exposed. The malformation is seen to reach the pial surface. Note the characteristic bluish appearance. Brownish discoloration of the surface of the spinal cord, caused by hemosiderin deposition, is also near the cavernous malformation.
Fig 6. Same patient as in Fig 1, intraoperative picture. After meticulous hemostasis is obtained, the cavity bed is inspected under high magnification for residual lesion or small "tongues" of cavernous malformation infiltrating the surrounding tissues.
ing and closure as well as careful handling of the parenchymal spinal cord tissue apply. Close observation in the immediate perioperative period is recommended. We routinely admit these patients to the intensive care unit after surgery. Their neurological deficits often worsen immediately after surgery, almost as if another hemorrhage from the cavernous malformation had occurred. If tissue handling was meticulous, however, this transient postoperative neurological worsening routinely resolves. MRI is obtained the day after surgery to serve as a baseline, and the patient is reimaged within 6 to 12 months.
with rongeurs and a high-speed drill. The ipsilateral pedicle at the relevant level was resected down to its insertion with the vertebral body. Once the thoracic dura was exposed, it was opened in a linear fashion along its lateral aspect. The underlying spinal cord parenchyma was visualized and arachnoid lesions were lysed. The critical portion of this procedure was identification of the ipsilateral dentate arachnoid ligaments, which were sectioned several levels above and below the level of the spinal cord cavernous malformation. Stitches were placed in the dentate ligaments to permit gentle rotation of the spinal cord, bringing its ipsilateral ventral surface into view. The portion of a lesion that reached the pial surface was then easily resected. Limitations of this approach include the inability to see beyond the ventral midline and anterior spinal artery, Theoretically, bilateral transpedicular approaches could be used for lesions that cross the midline that need to be accessed bilaterally. However, such aggressive bony resections would necessitate postoperative instrumentation and surgical fusion. As with all other techniques, the same principles of dural open-
Vishteh and coworkers observed neurological worsening immediately after surgery in 23.5% of 17 patients. 17 One patient (5.9%) improved and 12 (70.6%) remained the same. In the same study, at long-term follow up, 16 patients were either the same (6, 35.3%) or better (10, 58.8%). Only one patient was worse. This relatively large series stresses that safe and satisfactory results can be achieved with contemporary microsurgical
Fig 5. Same patient as in Fig 1, intraoperative picture. After the cavernous malformation is incised, the lesion is removed piecemeal with microcurettes and gentle suction and aspiration.
Fig 7. Same patient as in Fig 1, intraoperative picture. The cavity left after resection of the cavernous malformation is visualized under lower magnification through the opened dura.
SPINAL CORD CAVERNOUS MALFORMATIONS
techniques. A large meta-analysis by Zevgaridis and coworkers further supports that patients tend to improve after surgery. 19 As long as the lesion has been resected fully, no evidence suggests that these patients are at further risk of hemorrhage or decline related to the Surgical site. However, because symptoms have recurred (including hemorrhage) after incomplete resection, ~7 surveillance with MRI 6 to 12 months after the initial surgery and 2 to 3 years thereafter is recommended. If recurrence of a lesion is suspected on both imaging studies and clinically, a reoperation may be considered.
The diagnosis of both symptomatic and asymptomatic spinal cavernous malformations is greatly facilitated by MRI. The varied clinical presentation of these lesions can mimic other spinal cord disease entities. If symptomatic lesions reach the plat surface, surgery should be considered. Most spinal cord cavernous malformations are easily exposed through standard posterior approaches, and careful and meticulous microsurgical technique are necessary for their successful resection. Neurological deterioration after surgery is common, but transient in most cases. Close inspection of the cavity bed under high magnification is critical because residual lesions can regrow and re-hemorrhage. Prognosis for patients after surgical resection is very good. Most return to their preoperative level of neurological function or even improve.
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