MAGNETIC RESONANCE MYELOGRAPHY IN BRACHIAL PLEXUS INJURY

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1 MAGNETIC RESONANCE MYELOGRAPHY IN BRACHIAL PLEXUS INJURY TOSHIYASU NAKAMURA, YUTAKA YABE, YUKIO HORIUCHI, SHINICHIROU TAKAYAMA From Keio University, Tokyo, Japan We used magnetic resonance (MR) myelography in ten patients with injuries to the brachial plexus and compared the findings with those obtained by conventional myelography and postmyelographic CT (CTM). In the presence of complete nerve-root avulsion (seven cases), a post-traumatic meningocele was detected by MR myelography. In injuries to the upper roots (three cases) MR myelography showed abnormal findings with a high signal intensity in the nerve root, obliteration of the damaged nerve root, or enlargement and obliteration of the root sleeve. No pseudomeningoceles were detected in these upper-root injuries by MR myelography and CTM. The overall accuracy of detection of damaged nerve roots or root sleeves was better with MR myelography than with conventional myelography and was similar to that of CTM. MR myelography is non-invasive, relatively quick, requires no contrast medium, provides imaging in multiple projections, and is comparable in diagnostic ability to the more invasive, time-consuming techniques of conventional myelography and CTM. J Bone Joint Surg [Br] 1997;79-B: Received 10 February 1997; Accepted after revision 1 April 1997 In the last five years, a new MR technique utilising threedimensional fast spin-echo volume acquisition with maximum intensity projection (MIP) has been developed. 1-6 It provides T2-weighted images in which the CSF in the thecal sac is very bright. The MIP algorithm then creates a T. Nakamura, MD, PhD, Associate Professor Department of Orthopaedic Surgery, Fujita Health University, Second Hospital, Otobashi, Nakagawa-ku, Nagoya 454, Japan. Y. Yabe, MD, PhD, Professor Y. Horiuchi, MD, PhD, Associate Professor S. Takayama, MD, PhD, Director Department of Orthopaedic Surgery, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160, Japan. Correspondence should be sent to Dr T. Nakamura British Editorial Society of Bone and Joint Surgery X/97/57679 $2.00 three-dimensional myelogram-like image (MR myelogram). Background vessel signal is suppressed by a T2- weighted fast spin-echo pulse sequence with a long echo time, and the fat signal obliterated by a presaturation pulse for fat suppression. Preoperative imaging of brachial plexus injuries has previously been by conventional myelography, 7-11 and postmyelographic CT (CTM) Both, however, involve considerable exposure to radiation, a possible reaction to the contrast material, and the surgical risk of lumbar puncture. Although recent MR studies have been useful in assessing brachial plexus injury, these were not superior to conventional imaging. 19,20 We have now evaluated patients with brachial plexus injuries by MR myelography, conventional cervical myelography, and with CTM to compare the three techniques. PATIENTS AND METHODS Between 1993 and 1996, we studied ten patients with brachial plexus injuries who had had surgical exploration. There were nine men and one woman, with a mean age of 22 years (16 to 38). In six patients, the injury was on the right side and in four on the left; all had occurred during motorcycle accidents. The damaged nerve roots were C5 to C8 in five patients, C5 to T1 in two, C5 to C7 in two and C5 and C6 in one (Table I). We performed conventional myelography in all patients by lumbar puncture using a water-soluble contrast medium and CT of the cervical spine within two hours of myelography. The CT images were obtained at each nerve root from C4 to T1 with three slices and a slice gap of 3 mm. A 1.5 Tesla Signa MR system (GE Medical, Milwaukee, Wisconsin) and a cervical surface coil were used for acquisition of the MRI. After localisation using T2-weighted images in the sagittal and axial planes, we obtained the MR myelogram using a three-dimensional fast spin-echo sequence (TR 2000 ms; TE 200 ms; slice thickness 2 to 5 mm; field of view 24 cm; matrix; no slice gap). Thirty to forty slices were produced in six to eight minutes, and were then projected into a MR myelogram using the MIP algorithm. The MR myelograms were performed 1 to 30 months after the injury. The three techniques were compared for their ability to 764 THE JOURNAL OF BONE AND JOINT SURGERY

2 MAGNETIC RESONANCE MYELOGRAPHY IN BRACHIAL PLEXUS INJURY 765 Table I. Details of ten patients with injury to the brachial plexus Age Injured Date of MR myelography Case (yr) Gender side Level of avulsion after injury (mth) 1 17 Male Left C5 to C Male Left C5 to C Male Right C5 to C Male Right C5 to T Male Right C5 to C Male Right C5 to C Female Left C5 to T Male Right C5 and C Male Left C5 to C Male Right C5 to C7 6 Table II. Results of MR myelography, myelography, CTM and the surgical or SEP findings for each nerve root (C5 to T1) for all ten patients. For definition of abbreviations see footnote below C5 C6 C7 C8 T1 SEP/ SEP/ SEP/ SEP/ SEP/ Case MRM Myl CTM Surg MRM Myl CTM Surg MRM Myl CTM Surg MRM Myl CTM Surg MRM Myl CTM Surg 1 A2 A2 Pre/ A2 A2 Pre/ M M M Pre/M M M M Pre/M N N N Post/ -- 2 A / A / M -- M --/M M -- M --/M N -- N --/-- 3 A1 A1 Post/ A3 A3 Pre/ M M M Pre/M M M M Pre/M N N N --/-- 4 A3 N --/ A2 N --/ M M M --/M M N M --/M N N M Pre/ M 5 D D Pre/ A3 D M Pre/ M M M Pre/M M M M Pre/M N N N --/-- 6 A2 -- Post/ A2 -- Post/ M -- M Pre/M M -- M Pre/M N -- N --/-- 7 A3 N Pre/ D N --/ M M M --/M M M M --/M N N M Pre/ M 8 N A3 Post/ A3 A3 Post/ N N N N/N N N N --/N N N -- --/-- 9 D D Pre/ A2 A2 Pre/ N N Pre/ N N N --/N N N -- --/-- 10 A3 A3 Pre/ A3 A3 Pre/ A3 A Pre/ N N N --/N N N -- --/-- MRM, MR myelography; Myl, myelography; CTM, CT myelography; SEP, somatosensory evoked potentials; Surg, surgical findings; N, normal findings; A1, slightly abnormal root-sleeve shadow, in which the shadow of the root and rootlets are recognised but are different from the unaffected side; A2, obliteration of the tip of the root sleeve with the shadow of the root or rootlets showing; A3, obliteration of the tip of the root sleeve with no root or rootlet; D, defect instead of a root sleeve; M, traumatic pseudomeningocele (MR myelographic and myelographic findings were evaluated by the classification of Nagano et al 11 );, avulsed nerve root;, injured but not avulsed nerve root; Pre, preganglionic SEP findings; Post, postganglionic or normal SEP findings detect a traumatic pseudomeningocele, an injured nerve root and an abnormal nerve-root sleeve, and then checked with the findings at operation and intraoperative measurement of somatosensory evoked potentials (SEP) for each injured nerve root. The corresponding nerve roots on the uninjured side were used for comparison. We calculated the sensitivity (true-positive cases/true-positive cases + falsenegative cases), specificity (true-negative cases/true-negative cases + false-positive cases), and accuracy (true-positive cases + true-negative cases/total cases) for the detection of traumatic pseudomeningocele and of injury to the nerve root. RESULTS Table II gives the results for all three techniques for each nerve root. Traumatic pseudomeningocele. The shape of the thecal sac on MR myelography was identical to that seen on conventional myelography. Pseudomeningoceles of the C7 and C8 nerve roots were clearly visible on the MR myelograms in all seven patients with C5 to C8 and C5 to T1 avulsions (Fig. 1). Conventional myelography in these seven patients showed pseudomeningoceles of the C7 and C8 roots in four and of the C7 root in another. In the other VOL. 79-B, NO. 5, SEPTEMBER 1997

3 766 T. NAKAMURA, Y. YABE, Y. HORIUCHI, S. TAKAYAMA Fig. 1a Fig. 1b Fig. 1c Case 3. A 21-year-old man with a right brachial plexus injury (C5 to C8). Pseudomeningoceles are clearly observed at the C7 and C8 roots on the conventional myelogram (a), CTM (b) and MR myelogram (c) (arrows). Enlargement of the C5 nerve-root sleeve (star) and obliteration of the C6 root (arrowhead) are seen on the conventional myelogram (a) and MR myelogram (c). The intraoperative SEP findings showed a postganglionic injury or a normal C5 root and preganglionic injuries on the C6, C7 and C8 roots. The surgical findings were rupture, not avulsion, of the C5 root, avulsion of the C6 root and pseudomeningoceles of both the C7 and C8 roots. two, conventional myelograms did not show a pseudomeningocele (Fig. 2). CTM clearly showed pseudomeningoceles of the C7 and C8 roots in these same seven patients and in two of the patients with C5 to T1 lesions also in the T1 root. A pseudomeningocele of a C6 nerve root was also demonstrated, but its presence was not confirmed at operation (false-positive). No traumatic pseudomeningoceles were detected by any of the techniques in lesions of the upper plexus. Taking the findings at operation as correct the sensitivity, specificity and accuracy for MR myelography in detecting pseudomeningoceles were 88%, 100% and 98%; for conventional myelography 56%, 100% and 93%; and for CTM 100%, 98% and 99% (Table III). Detection of abnormal nerve roots and nerve-root sleeves. MR myelography showed a high signal intensity at the C5 and C6 nerve roots, obliteration of the tip of the root sleeve with no identifiable root or a defect of the root sleeve in all seven patients with C5 to C8 and C5 to T1 lesions. Conventional myelography showed avulsion of the C5 and C6 nerve roots only in three patients with C5 to C8 Table III. Comparison of diagnostic accuracy in detecting pseudomeningocele and avulsion of the nerve root by MR myelography, myelography and CTM compared with surgical findings and SEP Surgical findings and SEP Pseudomeningocele ulsion (+) (-) (+) Normal (n = 16) (n = 84) (n = 17) (n = 67) MR myelography Pseudomeningocele (+) 14 0 Pseudomeningocele (-) 2 84 ulsion 16 5 Normal 1 62 Myelography Pseudomeningocele (+) 9 0 Pseudomeningocele (-) 7 84 ulsion 9 3 Normal 8 64 CT myelography Pseudomeningocele (+) 16 1 Pseudomeningocele (-) 0 83 ulsion 15 6 Normal 2 61 THE JOURNAL OF BONE AND JOINT SURGERY

4 MAGNETIC RESONANCE MYELOGRAPHY IN BRACHIAL PLEXUS INJURY 767 Fig. 2a Fig. 2b Fig. 2c Fig. 2d Fig. 2e Fig. 2f Case 2. A 16-year-old boy with a left brachial plexus injury (C5 to C8). Conventional myelography does not clearly show a pseudomeningocele or an abnormal nerve root or root sleeve (a). CTM shows obliteration and enlargement of the nerve-root sleeves with no roots at C5 and C6, and traumatic pseudomeningoceles of the C7 and C8 roots (arrows) (b). The MR myelogram shows enlargement of the C5 and C6 root sleeves (arrowheads) and pseudomeningoceles of the C7 and C8 roots (arrows) (c). Conventional two-dimensional axial MR images are almost identical to the CTM (d). The pseudomeningocele (arrows) is detectable on both axial (d), coronal (e) and sagittal MR views (f). Operation revealed avulsion of the C5 and C6 roots and traumatic pseudomeningoceles of the C7 and C8 roots. injury, while in the other four it did not delineate abnormal findings in the upper nerve roots. Obliteration of the tip of the root sleeve with no identifiable root and/or enlargement of the root sleeve on both injured nerve roots (Figs 3 and 4) were shown by all three techniques in one patient with a C5 to C7 injury (case 10), while in the other patient with a C5 to C7 injury (case 9), avulsion of the C7 root was detected only by CTM and avulsion of the C5 and C6 nerve roots only was seen. In one patient with a C5 to C6 injury, a clear MR myelogram was not obtained because of a motion artefact. CTM showed nine of the C5 and nine of the C6 roots which were avulsed. Intraoperative SEP findings showed that the lesions in the C5 nerve root in three patients and in the C6 nerve root in two were postganglionic. Compared with the surgical and SEP findings, the sensitivity, specificity and accuracy of detection of total nerve-root injury for MR myelography were 91%, 92% and 92%; for conventional myelography 54%, 94% and 81%; and for CTM 94%, 91% and 92% (Table III). DISCUSSION Myelography and CTM have been used for imaging both preganglionic and postganglionic injury to the brachial plexus. 14,15 One advantage of myelography is its ability to delineate the entire injury. 7-9,11 Both techniques, however, VOL. 79-B, NO. 5, SEPTEMBER 1997

5 768 T. NAKAMURA, Y. YABE, Y. HORIUCHI, S. TAKAYAMA Case 9. A 38-year-old man with a left-sided injury from C5 to C7. Conventional myelography shows a defect of the C5 root and root sleeve, and obliteration of the tip of the C6 nerve-root sleeve (arrowheads) (a). The MR myelogram shows a defect of the C5 root sleeve and abnormalities of the C6 nerve-root sleeve with absence of the root (arrows) (b). ulsion of the C7 nerve root was not detected by these two techniques. Surgical and SEP findings supported avulsion of the C5 to C7 roots. Fig. 3a Fig. 3b Fig. 4 Case 10. A 29-year-old man with injury to C5 to C7. MR myelography shows obliteration of the C5, C6 and C7 nerve roots (arrowheads). involve considerable exposure to radiation and the possibility of reaction to the contrast medium. Myelography is reported to be unreliable at the level of the C5 and C6 nerve roots. 11 CTM is superior to conventional myelography in visualising the nerve rootlets because of axial imaging, 12 but it is difficult to detect the entire extent of the injuries. Vielvoye and Hoffmann 20 concluded that detection of partial or complete cervical root damage was not fully reliable in either myelography or CTM. Recently, the usefulness of MRI as a non-invasive diagnostic tool for injury to the brachial plexus has been reported, 16,17,21 but the acquisition time for conventional MRI is long, and the injury is not always clearly visible. 19,22 Furthermore, it is difficult to determine the entire extent of the injury with single axial MRI, as in CTM, and thus combinations of multiple slices or multiple planes are needed. 20 This requires further acqui- THE JOURNAL OF BONE AND JOINT SURGERY

6 MAGNETIC RESONANCE MYELOGRAPHY IN BRACHIAL PLEXUS INJURY 769 sition time and is difficult for the patients. A combination of conventional myelography and CTM has thus been the standard imaging technique for injury to the brachial plexus. 23 MR myelography is a new method for generating myelogram-like images of the CSF by MRI. Recent reports of MR myelography have been limited to the lumbar spine. 3-5,24 Previous results with cervical MR myelography have been poor, 1,2 but we were able to obtain nine excellent cervical MR myelograms by using a cervical surface coil, heavy T2- weighting and thin slices with no slice gap on the threedimensional volume scan. Although the vertebral arteries and spinal venous plexus were shown by myelography, the bony landmarks were not, but this made little difference diagnostically when compared with conventional myelography. MR myelography demonstrated pseudomeningoceles better than myelography, because in the latter technique detection is affected by the quantity of intrathecal contrast medium injected. CTM does not delineate the full extent of injuries because it uses only axial images. MRI depends only on the presence of CSF and the appropriate imaging parameters to create a myelographic-like image. The image of a pseudomeningocele is also emphasised by superpositioning the multiple images by three-dimensional reconstruction on MR myelography. Slow flow of CSF in the meningocele is also emphasised in MR myelography because there is no flow void artefact. Abnormal nerve roots and root sleeves were shown equally well by MR myelography as by CTM. Myelography did not outline damaged nerve roots and root sleeves as well as CTM and MR myelography. MR myelography has several advantages over conventional and CT myelography. It is a non-invasive technique with a relatively short imaging time. No contrast medium is required, but excellent images of the thecal sac are provided. It can be used in the acute phase of injury to the brachial plexus whereas in such patients lumbar puncture and the use of contrast medium carry a slight risk. 17 When carrying out MR myelography the patient is placed in a comfortable, supine position and does not have to move about because the multiple projection is produced by threedimensional reconstruction (Fig. 4). The disadvantages of MR myelography include artefacts due to CSF pulsation and movement by the patient, and inclusion of the vertebral arteries and spinal venous plexus. It is also quite difficult to determine the exact level of injury since no bony landmarks are included on the images. It is able, however, to provide results similar to CTM in a non-invasive manner. We wish to thank T. Asakura for his help with producing MR myelograms and K. Yamanaka, MD, PhD, for his help with the surgical and intraoperative SEP findings. Part of this study was supported by the clinical funds of the Marine and Fire Insurance Association of Japan. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. REFERENCES 1. Krudy AG. MR myelography using heavily T2-weighted fast spinecho pulse sequences with fat presaturation. Am J Roentgenol 1992; 159: Schnarkowski P, Wallner B, Goldmann A, Friedrich JM. MRmyelography of the lumbar spine using a PSIF-sequence: first experiences. Aktuelle Radiol 1993;3: Eberhardt KE, Hollenbach HP, Huk WJ. 3D-MR myelography in diagnosis of lumbar spinal nerve root compression syndromes: comparative study with conventional myelography. Aktuelle Radiol 1994; 4: El-Gammal T, Brooks BS, Freedy RM, Crews CE. MR myelography: imaging findings. Am J Roentgenol 1995;164: Hergan K, Amann T, Vonbank H, Hefel C. MR-myelography: a comparison with conventional myelography. Eur J Radiol 1996;21: Nakamura T, Yabe Y, Horiuchi Y, Takayama S, Yamanaka K. Diagnostic value of MR myelography for brachial plexus injury. J Jap Soc Surg Hand 1996;13: Murphey F, Hartung W, Kirklin JW. Myelographic demonstration of avulsion injury of the brachial plexus. AJR 1947;58: Davies ER, Sutton D, Bligh AS. Myelography in brachial plexus injury. Brit J Radiol 1966;39: Yeoman PM. Cervical myelography in traction injuries of the brachial plexus. J Bone Joint Surg [Br] 1968;50-B: Cobby MJD, Leslie IJ, Watt I. Cervical myelography of nerve root avulsion injuries using water-soluble contrast media. Br J Radiol 1988;61: Nagano A, Ochiai N, Sugioka H, Hara T, Tsuyama N. Usefulness of myelography in brachial plexus injuries. J Hand Surg [Br] 1989;14: Morris RE, Hasso AN, Thompson JR, Hinshaw DB Jr, Vu LH. Traumatic dural tears: CT diagnosis using metrizamide. Radiology 1984;152: Marshall RW, de Silva RD. Computerised axial tomography in traction injuries of the brachial plexus. J Bone Joint Surg [Br] 1986; 68-B: Hashimoto T, Mitomo M, Hirabuki N, et al. Nerve root avulsion of birth palsy: comparison of myelography with CT myelography and somatosensory evoked potential. Radiology 1991;178: Trojaborg W. Clinical, electrophysiological, and myelographic studies of 9 patients with cervical spinal root avulsions: discrepancies between EMG and X-ray findings. Muscle Nerve 1994;17: Gupta RK, Mehta VS, Banerji AK, Jain RK. MR evaluation of brachial plexus injuries. Neuroradiology 1989;31: Ochi M, Ikuta Y, Watanabe M, Kimori K, Itoh K. The diagnostic value of MRI in traumatic brachial plexus injury. J Hand Surg [Br] 1994;19: Francel PC, Koby M, Park TS, et al. Fast spin-echo magnetic resonance imaging for radiological assessment of neonatal brachial plexus injury. J Neurosurg 1995;83: Rapoport S, Blair DN, McCarthy SM, et al. Brachial plexus: correlation of MR imaging with CT and pathologic findings. Radiology 1988;167: Vielvoye GJ, Hoffmann CF. Neuroradiological investigations in cervical root avulsion. Clin Neurol Neurosurg 1993;95:Suppl S Mehta VS, Banerji AK, Tripathi RP. Surgical treatment of brachial plexus injuries. Br J Neurosurg 1993;7: de Verdier HJ, Colletti PM, Terk MR. MRI of the brachial plexus: a review of 51 cases. Comput Med Imaging Graph 1993;17: Roger B, Travers V, Laval-Jeantet M. Imaging of posttraumatic brachial plexus injury. Clin Orthop 1988;237: Van Dyke CW, Modic MT, Beale SM, Amartur S, Ross JS. 3D MR myelography. J Comput Assist Tomogr 1992;16: VOL. 79-B, NO. 5, SEPTEMBER 1997

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