Microcystic spinal cord degeneration causing posttraumatic myelopathy
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1 J Neurosurg 68: , 1988 Microcystic spinal cord degeneration causing posttraumatic myelopathy Report of two cases ROBERT L. MACDONALD, M.D., J. MAX FINDLAY, M.D., AND CHARLES n. TATOR, M.D., PH.D., F.R.C.S.(C) Division of Neurosurgery and the Spinal Cord Injury Treatment, Research, and Prevention Centre, Toronto Western Hospital, University of Toronto, Toronto, Ontario, Canada o- Two cases of progressive myelopathy occurring years after incomplete cervical spinal cord injury are presented. In both patients, the clinical features, as well as the "bull's-eye" appearance of the delayed computerized tomography (CT) myelography study and the circumscribed low density of the magnetic resonance image, were consistent with posttraumatic syringomyelia, but surgical exploration including intraoperative spinal sonography failed to reveal a syrinx. Although arachnoiditis was present in both patients, the striking abnormality found at surgery was the softened appearance and the microcystic degeneration of the cord. The microcystic spinal cord degeneration found in these cases represents a previously undescribed cause of late deterioration after spinal cord injury that may mimic the clinical, CT-myelographic, and magnetic resonance features of posttraumatic syringomyelia. KEY WORDS " posttraumatic progressive myelopathy 9 syringomyelia 9 spinal cord injury 9 magnetic resonance imaging p OSTTRAUMATIC progressive myelopathy is an increasingly recognized clinical problem after spinal cord injury, with recent series indicating a prevalence of approximately 3% among spinal cordinjured patients. 15 This delayed neurological deterioration after spinal cord injury represents an enormous threat to the already disabled patient, and it is imperative that the clinician recognize any potentially correctable cause. This disorder is usually attributed to posttraumatic syringomyelia, 1'5 although other possible causes include arachnoiditis, 3'~9 spinal column instability with spinal cord compression, 16 and spinal cord tetheringj 4 The correct identification of these various processes (in particular, posttraumatic syringomyelia) has been facilitated in recent years by the introduction of delayed computerized tomography (CT)-myelography and magnetic resonance (MR) imaging which have enabled appropriate therapeutic intervention, such as shunting of the syrinx in posttraumatic syringomyelia. This paper describes two patients with posttraumatic progressive myelopathy whose preoperative clinical, radiological, and MR evaluation was consistent with posttraumatic syringomyelia, but in whom operative exploration revealed arachnoiditis and a striking microcystic myelomalacia. The recognized causes and investigation of posttraumatic progressive myelopathy, as well as this newly described entity which we have termed "posttraumatic microcystic spinal cord degeneration," are discussed. Case 1 Case Reports This 29-year-old woman was involved in a motorvehicle accident 3 years prior to referral, in which she suffered burst fractures of C-4 and C-5, a C3-4 dislocation with unilateral locked facets, and an incomplete spinal cord injury. She was treated with an anterior corpectomy of C-4 with decompression of the spinal cord, and fusion with iliac crest bone graft and metal plates from C-3 to C-5. She remained in a halo thoracic brace for 3 months. She improved neurologically for 1 year after the injury to the point where she was ambulatory but had a spastic right hemiparesis, diminished 466 J. Neurosurg. / Volume 68/March, 1988
2 Posttraumatic myelopathy FIG. 1. Case 1. Computerized tomography scan at the C-3 level obtained 24 hours after iohexol myelography showing a hyperdense area (arrow) in the center of the cord. pinprick sensation bilaterally below T-2, and a fight posterior column sensory loss. She was hyperesthetic in the right upper extremity, and bowel and bladder function was clinically normal. Two years prior to her present admission, the patient began to notice diminishing strength and increased spasticity in her fight upper extremity, and severe burning pain in her fight shoulder. The dysesthetic pain spread further in her fight upper extremity and to both lower extremities, and sensory loss in her limbs increased. She had several episodes of bowel and bladder incontinence. Examination. Examination on admission revealed wasting of the right deltoid, biceps, and triceps muscles, and a severe right lower-extremity spastic paresis. The left side had virtually normal muscle strength and tone. Sensory examination showed that pain and temperature sensation was decreased below C-4 on the right side, completely absent in the C-5 dermatome, and decreased below T-3 on the left. Touch was mildly impaired from T-3 down on the left, and proprioception and vibration sense were mildly impaired on the right. The neurological deterioration and pain suggested posttraumatic syringomyelia. Plain radiographs showed evidence of a solid C3-5 fusion with a metal plate present. Cervical myelography with contrast material introduced through a lumbar puncture showed a patent subarachnoid space, but the cord was noted to be irregular from C-3 to C-5. Computerized tomography scanning confirmed an irregular cord outline at C4-5, and the CT study obtained 24 hours after myelography demonstrated a well-defined lesion in the cord at the C-3 level (Fig. 1). Magnetic resonance imaging was FIG. 2. Case I. Spin-echo magnetic resonance image, sagittal projection, demonstrating a low-intensity area (arrow) in the center of the cord from C-3 to C-5. performed with a 0.15-tesla resistant magnet unit and an 8-in. surface coil with spin-echo pulse sequences. The echo time was 30 msec, the repetition time 1030 msec, and the slice thickness 1 cm. Sagittal images were interpreted as showing a syrinx extending from C-3 to C-5 on the right side of the spinal cord (Fig. 2). Operation. Operative exploration with somatosensory evoked potential (SEP) monitoring was performed through a C4-5 laminectomy. The spinal cord appeared atrophied, and there was dense arachnoiditis over the right side. The right side of the cord was very abnormal in appearance with grayish discoloration and a reduction in overlying vessels. Intraoperative spinal sonography showed abnormal echogenicity in the cord, but failed to reveal an intramedullary cavity. A dorsal midline myelotomy was performed and under microscopy exploration extended anteriorly to the midpoint of the cord. No syrinx was found, but the right side of the cord was soft and gelatinous in consistency and appeared to exude fluid from numerous microcystic cavities less than 1 mm in diameter. In the absence of a syrinx, the intended shunt placement was not performed. The myelotomy was approximately 3 mm long and remained open. The patient showed no neurological changes at 6 months postoperatively. Case 2 This 39-year-old man suffered a burst fracture of C-5 in a diving accident 16 years prior to admission. Initially, he sustained an incomplete spinal cord injury with near quadriplegia, and was treated with a C4-6 decompressive laminectomy and halo thoracic bracing for 3 months. He recovered substantially and 5 years later was walking without leg stiffness and was active in sports with only mild residual impairment of fine motor control in all four limbs. However, during the 4 years J. Neurosurg. / Volume 68/March,
3 R. L. Macdonald, J. M. Findlay, and C. H. Tator FIG. 3. Case 2. Spin-echo magnetic resonance image, sagittal projection, showing an expanded cord (arrows) from C-4 to C-6 with central low-intensity signal compatible with posttraumatic syringomyelia. prior to his present admission, he noted increasing stiffness and spasm in both lower extremities and worsening motor control in his upper extremities. He developed dysesthetic pain in the left interscapular area not aggravated by coughing or straining, and he began to suffer a painless burning sensation in his hands. Examination. On admission, neurological examination revealed markedly increased tone in both lower extremities, and there was thenar and interosseus muscle wasting. Power was mildly decreased in all extremities in a pyramidal distribution. Reflexes in the upper extremities were normal, but in the lower extremities they were hyperactive with upgoing toes. Sensory examination showed decreased pinprick from C-6 to T-1 bilaterally with normal touch sensation. Position sense was mildly diminished in the toes, and vibration sense was decreased below the shoulder level bilaterally. The delay in neurological deterioration and the presence of a suspended, dissociated sensory loss raised the suspicion of posttraumatic syringomyelia. Plain radiographs of the cervical spine showed evidence of a C4-6 laminectomy with old compression and deformity of the C-5 vertebral body, a fixed reversal of the normal lordotic curve at C4-5, and posterior displacement of the C-5 vertebral body. Cervical myelography performed after lumbar injection showed a patent subarachnoid space and no apparent arachnoidiris. Immediate and 24-hour delayed CT scanning revealed an irregular cord from C-3 to C-7 with an illdefined central hyperdensity on the delayed CT scan. Magnetic resonance imaging of the cervical spine performed with the same unit and same parameters as in Case 1 showed an expanded cord from C-4 to C-6 with a central circumscribed low-density area diagnosed as a central syrinx cavity (Fig. 3). Operation. The patient was operated on through a C-7 laminectomy, and intraoperative SEP monitoring was performed. The dura was opened from C-5 to C-7. The cord was relatively normal in size with arachnoiditis over its dorsal aspect bilaterally; however, the cord and the cord parenchyma appeared abnormal with grayyellow discoloration. Intraoperative spinal sonography failed to reveal a discrete intramedullary cavity, but showed multiple ill-defined lucencies within the cord. Two dorsal midline myelotomies, each approximately 2 mm long, were made at the C-5 and C-6 levels with the use of the operative microscope. Tiny multiloculated cysts containing clear fluid and with numerous glial or fibrovascular trabeculae were found honeycombing the cord substance bilaterally at each site, but no cavity large enough to accept a shunt tube was found. Postoperatively, the patient awoke neurologically unchanged, and there has been no change in his condition during the 6-month follow-up period. Discussion The recognized causes of delayed neurological deterioration after spinal cord injury or "posttraumatic progressive myelopathy," as it has more recently been termed, 5 include posttraumatic syringomyelia, arachnoiditis, spinal column instability with spinal cord compression, and spinal cord tethering. Late deterioration can be a catastrophic development in an already disabled patient, and may reduce an ambulatory individual to a wheelchair, or render bedridden a paraplegic patient who has been competent in a wheelchair. In addition, the development of a pain syndrome can become equally incapacitating to the spinal cord-injured patient. Thus, it is essential for the physician caring for these patients to identify and correct, if possible, the cause of delayed-onset deterioration or pain. The most common cause of posttraumatic progressive myelopathy is posttraumatic syringomyelia, with onset months to years after a spinal cord injury. The course is characterized by pain, followed by sensory loss and progressive weakness. 1'~5'18 Usually, the pain is a dull ache or burning felt in the neck, back, or arms, which is often initiated and then exacerbated by an exertional event or Valsalva maneuver. The sensory loss is usually asymmetric and dissociated. Although neither of our patients had pain that began or was exacerbated with straining, the clinical course was nevertheless consistent with posttraumatic syringomyelia. The radiological diagnosis of postraumatic syringomyelia has been markedly improved by delayed CT myelography and more recently by MR imaging. With the advent of these techniques, gas and positive-contrast myelography have been employed less often for investigating posttraumatic progressive myelopathy as these methods rely largely upon demonstration of an enlarged or (rarely) a collapsing cord. It has been shown, however, that the size of the cord as determined by CT scanning or surgery often does not correlate with that suggested by myelography. 4'1~ In addition, syrinx cavities that have responded to shunting procedures have 468 J. Neurosurg. / Volume 68/March, 1988
4 Posttraumatic myelopathy been detected in normal-sized and even atrophic spinal cords. 12,13,15.20 Thus, these older diagnostic techniques do not accurately indicate cord size or the presence of a syrinx. Central cord enhancement on CT scanning delayed at least 4 hours after myelography with a water-soluble contrast medium has been estimated to have a sensitivity of 91% and specificity of 87% for detecting syringomyelia of any etiology. 4 Unfortunately, falsenegative delayed CT studies for posttraumatic syringomyelia, ~5"~72~ as well as false-positive studies such as in our patients, b3'2~ have been described in detail in the literature. For example, Quencer, et al.,~3 failed to find syringes at surgery in two patients with posttraumatic progressive myelopathy who had exhibited well-defined areas of central cord hyperdensity on delayed CT myelography. In their cases, intraoperative spinal sonography demonstrated areas of abnormal echogenicity similar to those seen in our cases, but they did not open the dura or explore the spinal cord. They suggested but did not confirm that these areas consisted of "scar tissue and multiple vacuoles or microcysts." Our experience proves that not all centrally enhancing lesions on delayed CT myelography represent syringes, and that they may represent microcystic degeneration of the spinal cord. Although MR imaging is a safer, more accurate, and painless way of detecting spinal cord cavities, this neuroimaging technique can also yield false-negative s,l~ and false-positive IL studies for syringomyelia. For example, Pojunas, et al., ~ reported the case of a false-positive diagnosis of syringomyelia with MR studies: the MR image showed a low-intensity lesion in the center of a minimally enlarged spinal cord consistent with syringomyelia, but surgical exploration and biopsy revealed viral myelomalacia. It seems probable, however, that with improved MR technology such as superconducting magnets, surface coils, and paramagnetic contrast agents, this technique will provide more precise preoperative diagnosis in the future. Posttraumatic arachnoiditis is occasionally implicated as the cause of posttraumatic progressive myelopathy, although it remains a poorly defined entity. A satisfactory explanation for the associated myelopathy (when it occurs) has been lacking. 3~ However, it is noteworthy that arachnoiditis was present in both of our patients, and we believe that it may play an important role in the pathogenesis of the posttraumatic microcystic spinal cord degeneration which was found, as discussed below. Ragnarsson, et al., 14 recently described posttraumatic tethering of the spinal cord as a cause of posttraumatic progressive myelopathy. At surgery, the spinal cord was found to be enveloped in dense circumferential arachnoidal adhesions; after cord transection and release of the adhesions, the spinal cord retracted rostrally almost 1 cm. Marked postoperative clinical improvement was noted. We found no evidence of such tethering in our patients. Delayed spinal instability with the development of fibrous or osseous extradural compression is another possible cause of posttraumatic progressive myelopathy, 15 and should be assessed by routine radiological investigations including dynamic (flexion-extension) studies, as were performed in our patients. Patients suffering such spinal cord compression would benefit from surgical decompression and/or stabilization. In our cases, the striking abnormality found at microsurgical exploration was microcystic degeneration of the cord at the site of previous injury, beneath a moderate to severe amount of fibrous arachnoiditis. The spinal cord had a gelatinous, multiloculated appearance with clear, colorless fluid exuding from the microcystic surfaces of the myelotomy tract giving the cord a "marshy" appearance which we have termed "posttraumatic microcystic spinal cord degeneration." This was the appearance under magnification with the surgical microscope and hence is only a gross morphological description; histological confirmation by biopsy was thought to be unsafe in these patients. Such cystic changes occurring years after spinal cord injury have been described in some detail in the pathology literature, j'6'7 but have not been previously correlated with delayed neurological deterioration. It seems possible that microcystic degeneration may account for some previously reported cases of posttraumatic progressive myelopathy in which no discernible cause for the progressive myelopathy was found. ~3.2o Although the pathogenesis of this microcystic degeneration is uncertain, one possible explanation is that it is a consequence of spinal cord ischemia. For example, arachnoiditis may encroach upon the segmental blood supply to the spinal cord and, if the cord has been rendered especially vulnerable to ischemia such as from previous injury to its microcirculation and collateral blood supply, then myelomalacia may develop. Such a role for ischemia in the pathogenesis of posttraumatic spinal cord cystic myelopathy has been proposed in the past, l but remains unproven. A close relationship between the arachnoiditis and the spinal cord changes is supported by the operative findings in our Case 1 where both the arachnoiditis and degeneration were restricted to the fight side of the cord, the predominant side of the progressive deficit. It is possible that some of the cases of posttraumatic progressive myelopathy attributed to arachnoiditis "alone" may in fact have had an associated microcystic spinal cord degeneration as the actual substrate for the myelopathy. Posttraumatic arachnoiditis may not cause an accompanying myelopathy if the blood supply to the spinal cord is spared or if the cord has not been predisposed to ischemia by other processes such as previous trauma. It has been suggested that microcystic spinal cord changes may be a precursor to macrocystic syrinx cavities, 15~2~3~7 the smaller cysts coalescing within the cord and the larger cavity later extending up and down the cord. Enlargement of the cavity has been postulated J. Neurosurg. / Volume 68/March,
5 R. L. Macdonald, J. M. Findlay, and C. H. Tator to be secondary to various mechanical factors such as stretching of the cord during flexion and extension with increases in the intracavitary pressure. 29 In addition, there is the well-recognized association between arachnoiditis and syringomyelia. ~ Thus, there may be a spectrum of posttraumatic spinal cord pathology from arachnoiditis to microcystic degeneration to syringomyelia (Fig. 4). Although this spectrum may not be applicable to all patients with posttraumatic syringomyelia, this is a useful theory, and we are following our two cases closely with MR imaging for any changes in spinal cord morphology. Conclusions When delayed neurological deterioration occurs after spinal cord injury, all potentially treatable conditions such as syringomyelia, spinal instability, and the recently described posttraumatic tethering of the spinal cord should be considered. If the imaging studies suggest posttraumatic syringomyelia, surgical exploration is indicated in order to perform a shunting procedure from the syrinx. 2~ Because microcystic cord degeneration can mimic posttraumatic syringomyelia, intraoperative spinal cord sonography should be employed; if this study fails to demonstrate a syrinx cavity, our experience would indicate that myelotomy is not warranted. At present, we can suggest no effective treatment for arachnoiditis or its associated microcystic spinal cord degeneration. It is unlikely that the myelotomies that we performed in our two cases will have any therapeutic value since the presence of fluid in the cord FIG. 4. Diagrams illustrating the postulated pathogenesis of posttraumatic microcystic spinal cord degeneration with progression to syringomyelia. Trauma results in damage to the microcirculation and arachnoiditis, as well as causing the initial cord injury (a). Progressive fibrosing arachnoiditis leads to vascular encroachment and ischemic microcystic myelomalacia (b). The microcysts coalesce and form a syrinx, which extends up and down the cord secondary to mechanical forces (c). is more likely to be the result of the degeneration than its cause. Acknowledgments We thank our colleague Dr. Marty Simons of the Department of Radiology for performing and interpreting the intraoperative ultrasonography, and Miss Mafia Vespa for preparing the manuscript. References 1. Barnett HJM, Foster JB, Hudgson P (eds): Syringomyelia. Major Problems in Neurology, Vol 1. London: WB Saunders, Barnett HJM, Jousse AT: Posttraumatic syringomyelia (cystic myelopathy), in Vinken PJ, Bruyn GW (eds): Injuries of the Spine and Spinal Cord, Part II. Handbook of Clinical Neurology, Vol 26. Amsterdam: North-Holland, 1976, pp Donaldson I, Gibson R: Spinal cord atrophy associated with arachnoiditis as demonstrated by computed tomography. Neuroradiology 24: , Gates PC, Fox A J, Barnett HJM: CT metrizamide myelography in syringomyelia: sensitivity and specificity. Neurology 36: , Gebarski SS, Maynard FW, Gabrielsen TO, et al: Posttraumatic progressive myelopathy. Clinical and radiologic correlation employing MR imaging, delayed CT metrizamide myelography, and intraoperative sonography. Radiology 157: , Jellinger K: Neuropathology of cord injuries, in Vinken PJ, Bruyn GW (eds): Injuries of the Spine and Spinal Cord, Part I. Handbook of Clinical Neurology, Vol 25. Amsterdam: North-Holland, 1976, pp Kakulas BA, Bedbrook GM: Pathology of injuries of the vertebral column with emphasis on the macroscopical aspects, in Vinken PJ, Bruyn GW (eds): Injuries of the Spine and Spinal Cord, Part I. Handbook of Clinical Neurology, Vol 25. Amsterdam: North-Holland, 1976, pp Lee BCP, Zimmerman RD, Manning J J, et al: MR imaging of syringomyelia and hydromyelia. A JR 144: , McLean DR, Miller JDR, Allen PBR, et al: Posttraumatic syringomyelia. J Neurosurg 39: , Osborne DRS, Vavoulis G, Nashold BS Jr, et al: Late sequelae of spinal cord trauma. Myelographic and surgical correlation. J Neurosurg 57:18-23, Pojunas K, Williams AL, Daniels DL, et al: Syringomyelia and hydromyelia: magnetic resonance evaluation. Radiology 153: , Quencer RM, Green BA, Eismont FJ: Posttraumatic spinal cord cysts: clinical features and characterization with metrizamide computed tomography. Radiology 146: , Quencer RM, Morse BMM, Green BA, et al: Intraoperative spinal sonography: adjunct to metrizamide CT in the assessment and surgical decompression of posttraumatic spinal cord cysts. A JR 142: , Ragnarsson TS, Durward QJ, Nordgren RE" Spinal cord tethering after traumatic paraplegia with late neurological deterioration. J Neurosurg 64: , Rossier AB, Foo D, Shillito J, et al: Posttraumatic cervical syringomyelia. Incidence, clinical presentation, electrophysiological studies, syrinx protein and results of con- 470 J. Neurosurg. / Volume 68/March, 1988
6 Posttraumatic myelopathy servative and operative treatment. Brain 108: , Schneider RC, Knighton R: Chronic neurological sequelae of acute trauma to the spine and spinal cord. Part III. The syndrome of chronic injury to the cervical spinal cord in the region of the central canal. J Bone Joint Surg 41 (Am): , Seibert CE, Dreisbach JN, Swanson WB, et al: Progressive posttraumatic cystic myelopathy: neuroradiologic evaluation. AJNR 2: , Shannon N, Symon L, Logue V, et al: Clinical features, investigation and treatment of post-traumatic syringomyelia. J Neurol Neurosurg Psychiatry 44:35-42, Shaw MDM, Russell JA, Grossart KW: The changing pattern of spinal arachnoiditis. J Nenrol Neurosurg Psychiatry 41:97-107, Stevens JM, Olney JS, Kendall BE: Posttraumatic cystic and non-cystic myelopathy. Neuroradiology 27:48-56, Tator CH, Meguro K, Rowed DW: Favorable results with syringosubarachnoid shunts for treatment of syringomyelia. J Neurosurg 56: , 1982 Manuscript received June 17, Address reprint requests to: Charles H. Tator, M.D., Suite 4-034, Edith Cavell Wing, Toronto Western Hospital, 399 Bathurst Street, Toronto, Ontario M5T 2S8, Canada. J. Neurosurg. / Volume 68/March,
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