Neuro--

Neuroradiology (1992) 35:30-35

radiology 9 Springer-Verlag 1992

MRI in chronic spinal cord trauma W. L. Curati 1, D. P. E. Kingsley 1'2, B. E. Kendall 1'2, and I. F. Moseley t, 2 I MRI Unit, Queen Square Imaging Centre and 2National Hospital for Neurology and Neurosurgery, London, UK

Summary. Eighty-seven patients aged 16~58 years have been examined by magnetic resonance imaging (MRI) following spinal injury. T h e M R I findings have been correlated with length of history between t r a u m a and investigation, extent of residual function and site of injury. They include changes at the site of injury consistent with myelomalacia in 37 %, a syrinx in 40 %, persistent cord compression in 32 % and atrophy in 18 %. A n extensive syrinx can develop within 2 months of injury and it is nearly twice as c o m m o n in patients with complete paralysis as in those whose paralysis was incomplete. It is suggested that investigation and m a n a g e m e n t of spinal t r a u m a should include early and repeated M R I examinations to detect sequelae at an early stage.

cord at a distance from the site of injury has been found at surgery to be due to myelomalacia [4]. There are few studies comparing CT myelography with M R I in spinal trauma, but evidence suggests that M R I is at least as good at demonstrating large cysts and better at demonstrating myelomalacia and small cystic cavities [5]. It is the only noninvasive imaging procedure which can adequately demonstrate bony and soft tissue structures and its lack of ionising radiation and the fact that it entails no interference with the normal or pathological spinal hydrodynamics m a k e it the ideal procedure for initial diagnosis and long-term management.

Patients and methods Key words: Spinal t r a u m a - Spinal cord d a m a g e - Magnetic resonance imaging

Spinal t r a u m a tends to involve young people. The effects are catastrophic on the social fabric of the family and management is expensive. Delayed complications, particularly the d e v e l o p m e n t of syringomyelia, once thought to occur in only 1-4 % of cases, are now increasingly recognised as a major cause of morbidity. Accurate estimates of their prevalence are not available, since imaging is usually p e r f o r m e d only once complications arise. Magnetic resonance imaging ( M R I ) has, however, allowed baseline and sequential studies to be p e r f o r m e d which should eventually answer m a n y of the questions concerning the origin and evolution of thes complications. Before M R I became available the diagnosis of posttraumatic m y e l o p a t h y depended mainly on myelography followed by delayed CT [1-3]. Filling of the cyst occurs at a variable rate and if scanning is not undertaken at the appropriate time, the cyst m a y be overlooked. Nevertheless, false-negative and false-positive results have b e e n documented; radiology has failed to demonstrate a cyst when one was present and diffusion of contrast m e d i u m into the

During the past 5 years, 87 patients have been examined at the Queen Square Imaging Centre of the National Hospital for Neurology and Neurosurgery following severe trauma to the spine. They were referred from a number of sources and thus are a selected group and do not provide an indication of the incidence or prevalence of complications. They were examined for a number of indications and 26 had already undergone spinal surgery at the time of the examination, laminectomy and exploration only in 17, bony fusion in 6 and syringoperitoneal diversion in 6. The age of the patients ranged between 16 and 68 years (mean 35 years) at the time of imaging. All were examined on a 0.3 T cryogenic magnet operating at 0.26 T. A sagittal Tl-weighted spin echo (TR500-640, TE40) sequence was performed routinely. An axial Tl-weighted spin echo sequence was undertaken through the region of cord damage in 43 cases and a sagittal T2-weigted sequence (TR1500, TE80) was added in 35. Thirty-one patients were examined between 1 and 18 months, 37 during the period 18 months10 years and 19 more than 10 years after the injury. All patients were assessed with reference to clinical state, the interval between injury and MRI, the site of injury and the state of the cord at that level on T1- and T2-weighted sequences, the presence and extent of atrophy and/or syrinx above and below the injury and the extent of cord changes beyond the syrinx on T2 weighting. Myelomalacia was considered to be present at the site of injury if areas of patchy low intensity were demonstrated on Tl-weighted images with corresponding high intensity on T2-weighted images, where available. Cord damage, possibly myelomalacic, was also considered to be present if there was elevated T2 signal extending beyond the site of injury or beyond identifiable syrinx. (With T1

31 Table 1. Nature of the trauma and region affected

Type of trauma Traffic accident Fall Diving Riding Gunshot Total

Cervical 28 6 4 2 0 40

Thoracic 36 8 0 1 2 47

Table 2. Relative extent of abnormal signal on T1- and T2-weighted

images in 27 patients patients with paraplegia or incomplete paraparesis Time between trauma and MRI study < 18 months 18 months- > 10 years 10 years Paraplegia Paraparesis

T2 : T1 T2 > T1 T2 = T1 T2 > T1

3 (2) 3 (2) 3 (0) 3 (0)

1 (0) 5 (2) 0 (0) 1 (0)

0 (0) 5 (4) 2 (2) 1 (1)

( ) , Patients with syrinx

weighting, the intensity of myelomalacic tissue was lower than that of the adjacent cord but usually higher than that of any associated syrinx; occasionally myelomalacia resembled a localised cyst on T1 weighting, but the signal on T2 weighting was usually higher than that within a syrinx due to motion in the latter.) A syrinx was identified as a low intensity linear or septate structure on Tl-weighting within cord tissue above or below the site of injury, which was also associated with low signal thought to be due to movement in at least part of the cyst on the T2-weighted sequences without motion-suppression, when these were available.

level was spared. In the 24 patients in w h o m it was unassociated with a syrinx, myelomalacia was situated in an area of focal swelling at the level of injury in 8, in 6 of w h o m there was a more clearly marginated "cyst-like" appearance. Five were examined within 18 months and others 7, 11 and 18 years after the injury. T2-weighted sequences were undertaken in 35 cases, but the images could be assessed in only 30; 5 were excluded because of metal-induced artefact or because imaging did not include the whole of the spinal cord. There was no high signal in 3 patients, 2 of w h o m had minor symptoms and 1 paraparesis. In the other 27 the other abnormalities were at least as extensive as on Tl-weighted images (Table 2). T2-weighted sequences were undertaken in 16 patients with a syrinx, but the extent of abnormal signal could not be assessed because of artefact or an incomplete study in 3. In 9 of the 13 patients with adequate images, signal changes were m o r e extensive than the syrinx, extending up to five segments cephalad of the identifiable margin of the syrinx in 4 and involving the medulla and lower pons in 2 (Fig. 1). High signal extended beyond the syrinx below the site of injury in 2 cases and only for one segment.

Traumatic syrinx A syrinx was encountered in 35 patients (40), 11 of 31 (35.5%) of those examined within 18 months, 11 of 37 ( 3 0 % ) between 1 8 m o n t h s and 10years and 13 of 19 (68.5 % ) m o r e than 10 years after injury. The extent of the

Results

The large majority of patients (82/87 - 94 % ) were paretic below the level of injury, although in 35 (40 %), the paresis was incomplete. T h e injury involved the cervical spine in 40 (46 % ) cases and the thoracic spine in 47 (54 %). The cause of the injuries is shown in Table 1. There was evidence of metallic artefact in i of the patients with gunshot injuries, but this did not significantly degrade the images. However, in 2 patients artefact from previous surgery rendered assessment of the spinal cord in that region impossible. M R I findings consisted of abnormalities at the level of injury and m o r e extensive changes of syrinx formation and cord atrophy.

Mye~maNcm Changes consistent with myelomalacia were encountered at the site of injury in 32 (37 % ) patients: all had abnormalities on T1 weighting and in 15 T2 changes were also shown. Twenty-four (28 %) did not have associated syringes but in the other 8 (9 % ) "myelomalacic changes" could be d e a r l y identified separately from a syrinx. T h e y were seen at all ages, were present as early as 2 months after injury and persisted for up to 25 years. No spinal segmental

Fig.la, b. Man aged 36 years. Road traffic accident 18 years previously, a Tl-weighted (500/40) sagittal MRI demonstrates an apparently multiseptate syrinx extending from the level of the fracture at T3/4 up to the cervicomedullary junction. The spinal cord is markedly expanded, b T2-weighted (1500/80) image, without motionsuppression technique demonstrates high signal extending into the lower medulla

32 VERTEBRAL SEGMENTS 20 16 12

8 4

Fracture Level -4

-8 -12 -16 -20 1.5 a

2

6

8

12

12

12

15

18

18

18

TIME BETWEEN TRAUMA and MRI (months)

VERTEBRAL LEVEL 20

12 8 4 Fracture Level

-8 -12 -16 2

b

2

2

2.5

5

6

6

7

8

9

10

TIME BETWEEN TRAUMA and MRI (years)

VERTEBRAL LEVEL 20 16 12

ges involving 3 and 17 segments respectively. There were 17 patients with a syrinx involving 9 or more segments on either side of the fracture, of whom 14 (82 % ) had a thoracic injury. Smaller syringes involved the cervical region as frequently as the thoracic; syringes extending only caudal from the site of trauma involved no more than 3 segments, whereas those which extended only upwards involved from 2 to 19 (mean 8) segments. Syringes were present in 25 of 47 (53 %) patients with complete para- or tetraplegia, in 10 of 35 (28.5 %) of those with incomplete lesions and in none of 5 with minor residual symptoms. All patients who were shown to have developed syringes within 18 months of injury had suffered complete paralysis. The signal returned from the syringes on the T1weighted sequence was usually close to that of cerebrospinal fluid (CSF) but higher signal, suggesting a raised protein level, was seen in 8 patients; it was not related to the extent of the cyst nor to the time between the injury and the MRI study. Most syringes had smooth walls, but multiple "septations" were apparent in 10 patients, in 9 of whom the cyst contents resembled CSF. The sagittal diameter of the syringes was measured at the widest point: the cyst was of maximum diameter at its midpoint in 12 patients, close to the fracture in site in 9, at the far end of the cavity in 4 and diffusely in the remaining 10). It varied between 4 mm and 14 mm (mean 8.35 mm) in diameter above the fracture and between 2 mm and 10 mm (mean 5.64 ram) below but in 2 cases was larger below the fracture than above. There was no relationship be-

8 4 Fracture Level -4

-8 -12 -16 -20 11 11 11 11 14 15 16 18 22 23 25 27 30 C

TIME BETWEEN TRAUMA and MRI (years)

Fig.2. Comparison of extent of syrinx with length of time between injury and imaging: a 6 weeks-18 months; b 2-10 years; c 11-30 years

syrinx is shown in Fig. 2. In the 6 patients examined after syringoperitoneal diversion the syrinx may originally have been more extensive than was apparent at the time of the imaging. A cavity was present as early as 6 weeks after injury and a long syrinx by 2 months (Fig. 3) and, although the diagnosis was sometimes not made until much later (up to 30 years), there was no evident relationship between the extent of the cyst and the time taken for it to develop (Fig. 2): 4 of the 7 patients presenting within a year of trauma had a syrinx involving at least 11 segments. The cyst extended upwards from the level of injury in 17 patients, downwards in 3, upwards and downwards in 14, and was situated between two fracture sites in 1. Twelve patients had suffered cervical and 23 thoracic injuries; there was no significant difference in the location of the syrinx with respect to the site of injury in either of these regions. Two patients with trauma at L1 vertebral level had syrin-

Fig.3a, b. Man aged 20 years. Traffic accident with fracture at T4/5 2 months before MRI. Tl-weighted (500/40) sagittal images, a Ascending syrinx between the fracture site and C5. There is no tonsillar ectopia, b Extensive syrinx between the fracture site and at least T l l . The descending syrinx is smooth-walled and thinner than the ascending portion

33 tween the length and maximum width of the cyst or with the severity of paralysis.

Atrophy A thin cord, measuring 6 mm or less in anteroposterior diameter, thought to be atrophic, was present in 16 patients (18 % ). Atrophy occurred in 6 patients with syringes and affected parts of the cord apparently uninvolved by syrinx, both above and below the level of injury. In the majority, it involved less than 5 segments, but in two patients studied 23 and 28 years after the injury it extended caudally for 12 and 18 segments respectively; it was seen as early as 2 years after injury and was more common in patients with paraplegia (12/47 - 25 To) than in those with incomplete pareses (4/35 - 11%).

Cord compression Identifiable narrowing of the spinal canal sufficient to cause persistent cord compression was encountered with approximately equal frequency in total paraplegia (14/47 - 30 %), incomplete paralysis (12/35 - 34 %) and in patients with minor signs (2/5 - 40 % ). The degree of compression could not be adequately assessed. Its presence was associated with syringes in only 6 patients (5 with complete and 1 with incomplete paraparesis) and with atrophy in 2, both with complete paralysis. Compression was due to fracture-dislocation in 7 cases of complete and 1 of incomplete paralysis, to wedging in 6 complete and 8 incomplete lesions as well as in 2 minor injuries and to disc prolapse in 3 patients with incomplete paresis.

Discussion

The pathological changes at the microscopic level which follow spinal trauma depend on the force applied. Experimental studies in the acute phase suggest that, with limited force, damage is mainly to the grey matter. Initial haemorrhage leads to changes caused by rupture of membranes of the nerve cell bodies, with release of lysosomes and subsequent cytolysis, liquefaction and necrosis leading to the development of small cystic cavities [6]. More severe injury by larger forces leads to damage to grey and white matter, the damage to the axons leading to release of lysosomes at a distance from the site of injury [7]. More extensive microcyst formation and rupture lead to coalescence, with the production on either side of the site of damage of larger cysts usually lined by a single continuous sheet of glial basement membrane [8], and occasionally by ependymal cells [9]. The central canal sometimes opens into these traumatic cavities and it is thought that this may be the initiating factor in post-traumatic syringes if the rate of flow of fluid into the cavity is greater than that of its absorption [10]. MRI studies demonstrate a close correlation between acute haemorrhage, hypointense loci on T2-weighted sequences and pathological changes [11]. In patients with

demonstrable spinal cord haemorrhage neurological recovery is poor or absent whereas some recovery may occur if only contusion and oedema are present. In one study, traumatic haemorrhage was demonstrated in 5 of the patients and high signal on T2-weighted images in a further 12 patients scanned acutely: some patients with high signal on T2-weighted sequences had recoverable lesions, but in many, such changes persisted into the chronic phase [121. An abnormal cord was encountered at the site of trauma without an identifiable syrinx in nearly a third of our patients. Changes were of two types: patchy low intensity on Tl-weighted sequences with more extensive high signal on T2 weighting (T1/T2 low/high) in 18 (75 %), and more dearly marginated cyst-like lesions localised to the site of trauma in the other 6 (25 % ), 5 of whom were studied within 18 months and the other 5 years after injury. The radiological diagnosis of myelomalacia in the latter group is less secure, since these appearances could represent focal cysts [13]. Whether either appearance is a precursor to syrinx formation is uncertain. T1/T2 low/high areas were also more common in patients imaged within 18 months of injury, but were present in 7 of 18 scanned 6-23 years after the trauma, 3 of whom had a persistently swollen cord. A thin cord, probably due to atrophy, was demonstrated above or below the level of injury in 4 of the 7. Although a thin cord could have represented a collapsed syrinx, none of these patients had other positive evidence of an intramedullary cavity. Similar "myelomalacic" changes were clearly identified at the site of trauma in at least 8 patients with syringes and were almost certainly present in the remainder. However, 3 patients, scanned 6, 7 and 11 years later, showed only local damage, indicating that syrinx formation does not necessarily follow severe damage. With resolution of the acute changes, a period usually elapses before there is clinical evidence of syringomyelia (post-traumatic myelopathy). Prior to MRI, conventional neuroradiological studies suggested an incidence of syrinx formation of less than 5 % [2,10,13]; this is almost certainly an underestimate [1]. In our series new symptoms were difficult to assess in the subacute phase, particularly when the lesion was complete. The time of commencement of syrinx formation is thus impossible to determine. The process of repair is initiated immediately after trauma with cell death and liquefaction. At what point the cyst itself develops is less certain, but central cores of necrotic tissue can extend for several segments from the site of injury and these could coalesce to form a cavity [14]. A cyst can already be established within 3 months, as is evident from the case described by Quencer et al. [1] and our own series, and early change is present within 6 weeks. What is perhaps surprising is the high incidence of syrinx (40 % ) in our series, and particularly that of early cyst formations. Kerslake et al. [15] encountered only ten syringes in their series of 74 patients (13.5 %) scanned 3 weeks to 40 years after injury, and none earlier than 6 months. Because of the lack of availability of MRI in the United Kingdom the indication for MRI is likely to have been similar in our two series and it is therefore surprising that there should be such a discrepancy between the two studies. We found 11

34 of 31 patients with complete tetra- or paraplegia studied within 18 months of injury to have established syringes, although none of 13 patients with incomplete paraplegia developed a syrinx by this stage. This is at variance with the experience of Yamashita et al. [13], who found that the average delay to demonstration of the syrinx was 230 months, but is borne out by other studies [1, 5]. The first clinical suggestion of a syrinx is usually the onset of ascending signs or the development of new symptoms after an apparently quiescent period. This was the indication for MRI in 42 patients (48%) examined after 18 months or more and was the presenting feature in all our patients found to have syringes. Despite this, a syrinx has been reported without new clinical features being apparent [1]. Previous studies have suggested that the development of a post-traumatic syrinx is independent of the site and severity of the injury [1, 5]. Our much larg.er series confirms the lack of relationship with the site of injury, but is in agreement with the findings of Barnett and Jousse [16] that patients with the most severe damage are at much greater risk of developing a syrinx, 51% of patients with complete paraplegia, 26 % with incomplete paraparesis, and none of those with less severe signs having a syrinx. The extent and appearances of the syringes in this series are also worthy of comment. There is little information in the literature concerning the longitudinal extent of post-traumatic syringes. They are frequently very extensive, and can extend upwards, downwards or in both directions. Kerslake et al. [15] found both ascending and descending syringes in eight of their ten cases with ascent or descent only in one each. The lesions in our larger series were nearly equally divided into ascending only or ascending and descending cysts and there were only three which only descended. Both series demonstrate a high proportion of extensive syringes, nine or more segments being involved in 40 % and 50 % of the cases respectively. Ascending syringes are usually larger than descending cysts. Kerslake et al. [15] found this to be the case in patients with an injury involving the cervical and upper dorsal region; in our series it was the same of fractures at all sites. No consistent information is available concerning the rapidity of development of large cysts. There is at least one documented case of a long cyst (7.5 cm) being present within 4 months of injury [1]. In our series assessment of the extent of the syrinx was based on the number of vertebral segments involved, each segment measuring at least 2 cm. Whilst there is no correlation with the time elapsed between injury and imaging, one of our patients with a 2-month interval between trauma and MRI had an established cyst involving seven segments above and seven below the site of injury at T3/4 (Fig. 3). Progression of the syrinx is harder to assess since current treatment favours intervention with cyst drainage [17]. Abnormal high signal on T2-weighted sequences indicates changes in the water content of the cord beyond the site of the visible syrinx and in spinal cord distant from the site of injury (Fig. 1). In the acute phase changes adjacent to the fracture might be explained on the basis of local tissue injury, with cord swelling, which could be revers-

ible. However, these changes were present beyond the syrinx in 9 patients, of whom 6 were scanned between 6 a n d 27 years after injury, extending to involve the ports and medulla in 2. It could be that this high signal area represents a stage in the development of a syrinx, but whether and how frequently these changes are the precursor to syrinx formation must remain speculative. Although intraoperative sonography demonstrates small cysts and septation better than MRI [5], the morphology of the cysts can be well appreciated on the latter, which is important if syringoperitoneal diversion is being considered. A surprisingly large percentage (10/31 32 %) of the intramedullary cavities had apparent septations, often extensive. In the 4 cases in which the syrinx was present above and below the level of injury the septations were found only above, a finding supporting the work of Kerslake et al. [15]. These septations often appear incomplete, however, and although MRI may not resolve intact bands between cysts, it may suggest loculation if adjacent cysts return different signal; this was never observed in this series and evidence from endomyelography suggests that the syrinx is usually in continuity over the whole of its length [18]. Furthermore, MRI after shunting, which often shows extensive reduction in size of the cavities, even when apparently "septate", provides the most reliable indication of intercommunication. There is thus good evidence from endomyelography and from MRI of developmental hydromyelia that the "septations" are more correctly "corrugations" and that the cysts are usually in communication throughout. It has been suggested that atrophy develops with time [9]. We cannot comment on this from our series since numbers are too small, but a thin cord was already apparent in 3 patients studied within 2 years of injury. In general atrophy was limited to the region immediately adjacent to the damaged vertebra. In 2 patients with long delays between injury and MRI, in whom paraplegia was complete, atrophy extended from the site of the fracture caudally to the conus medullaris over 12 and 18 segments respectively, associated in the former with a syrinx. In a further patient scanned after a long delay, in whom paresis was incomplete, atrophy extended over only two segments. Cord compression, a common finding in this series, was not significantlymore frequent in patients with paraplegia than in those with incomplete paralysis or even minor residual symptoms. It did not seem to have any relationship to changes in cord morphology and lack of compression seems to provide no protection against the subsequent formation of a syrinx. Compression due to disc protrusion did not cause complete paralysis. However, not all of these patients were explored Surgically at the time of injury and it is possible that had intervention occurred, significant clinical improvement might have ensued. Since it is noninvasive and does not alter craniospinal hydrodynamics, MRI permits meaningful assessment of the traumatised spinal cord. The onset of severe sequelae has now been demonstrated at a very early Stage after injury and it is suggested that if a more preventive management protocol is to be developed in these patients, MRI should be undertaken acutely and more frequently as a follow-up investigation before symptoms have developed.

35

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Dr. D. E E. Kingsley Lysholm Department of Radiology National Hospital for Neurology and Neurosurgery Queen Square London WC1N 3BG, UK

MRI in chronic spinal cord trauma.

Eighty-seven patients aged 16-68 years have been examined by magnetic resonance imaging (MRI) following spinal injury. The MRI findings have been corr...
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