IMAGING OF ADULT BRACHIAL PLEXUS TRACTION INJURIES A. TAVAKKOLIZADEH, A. SAIFUDDIN and R. BIRCH From the Peripheral Nerve Injury and Children’s Hand Unit and the Department of Radiology, The Royal National Orthopaedic Hospital NHS Trust, Stanmore, Middlesex, UK
Closed, high-energy transfer traction injuries of the adult brachial plexus lead to rupture or avulsion of the spinal nerves. Accurate preoperative diagnosis is crucial for surgical planning and reconstruction. Myelography, computerised tomographic myelography and magnetic resonance imaging are the main radiological methods for preoperative diagnosis of the lesion. This article reviews the current status of imaging of traction injuries of the adult brachial plexus. Journal of Hand Surgery (British and European Volume, 2001) 26B: 3: 183–191 intradural rupture may be made on histological grounds (Schenker and Birch, 2000). Clinical examination cannot regularly distinguish between the pre- and the post-ganglionic injury. Physiological methods of diagnosis (Bonney, 1954; Bonney and Gilliatt, 1958) rest on the demonstration of persisting conduction of afferent fibres after preganglionic injury. These investigations are limited by variation in the distribution of the spinal nerves, by the time necessary before Wallerian degeneration is complete, and by the presence of ‘double’ lesions, with both pre- and post-ganglionic elements. Inspection of the spinal nerve in the posterior triangle of the neck may be misleading since the roots may appear intact extradurally whilst being avulsed intradurally. Per-operative recording of Somatosensory Evoked Potentials (SEP) is valuable (Landi et al., 1980) but the presence of a SEP does not exclude an isolated ventral root avulsion, and cannot differentiate between a partial avulsion and an intact nerve root (Hayashi et al., 1998). For these reasons, preoperative imaging of the brachial plexus is necessary to determine the status of the intradural nerve roots.
INTRODUCTION Severe traction injuries of the brachial plexus are most commonly caused by motorcycle accidents, and occur typically in young men (Birch et al., 1998). They lead to rupture or avulsion of the spinal nerves. Accurate preoperative diagnosis is necessary for surgical planning and reconstruction of the brachial plexus. ANATOMY AND PATHOLOGY OF TRAUMATIC BRACHIAL PLEXUS LESIONS The brachial plexus is formed by the anterior rami of the lower four cervical nerves and the first thoracic nerve. These form the trunks, divisions and cords of the brachial plexus in their course towards the arm. Injuries to the brachial plexus can be divided into penetrating injuries, compression injuries and traction injuries. By far the most common is the traction injury, in which the head is separated violently from the forequarter, and the peripheral nerves are stretched longitudinally. In pre-ganglionic injury, the lesion is central to the dorsal root ganglion. In post-ganglionic injury, the level of injury is peripheral to the ganglion. Establishing whether an injury is pre- or post-ganglionic is important as the treatment methods, prognosis and functional outcomes are very different, being worse for pre-ganglionic injuries (Birch, 1987). With the possibility of intradural repair and re-implantation of avulsed nerve roots (Carlstedt, 1995), the level of pre-ganglionic lesions must be further subdivided into those that are central to the transition zone (TZ) within the spinal cord, as defined by Berthold et al., and those which are peripheral (Berthold et al., 1993). Direct inspection of the spinal cord, via hemilaminectomy, has shown two patterns of intradural rupture. In the first, the roots are ruptured in their intradural course, leaving small stumps of varying length protruding from the cord surface. This type of injury has been termed peripheral intradural rupture (Birch et al., 1998). In the second type of injury, the avulsion of the root is accompanied by avulsion of a part of the cord itself, leaving a small defect in the surface of the cord. Recent studies have suggested that the differentiation between central and peripheral
MANAGEMENT OF BRACHIAL PLEXUS INJURIES A comprehensive history of the mechanism of injury and detailed clinical examination are mandatory. Exploration and repair of the plexus within the first week after injury results in a better outcome (Birch et al., 1998). However, early surgery may be contraindicated by associated injuries. Repair in the pre-ganglionic lesion rests on transfer of spinal accessory, cervical plexus or intercostal nerves to a distal portion of the brachial plexus or transfer of nerves from the opposite brachial plexus. Post-ganglionic ruptures are grafted (Birch et al., 1998). More recently, experiments on animals have shown that re-implantation of avulsed nerve roots into the spinal cord may lead to re-innervation 2 to 3 months after surgery, if the procedure is carried out immediately to avoid loss of the motor neurone pool. Generally motor recovery only occurs in cases operated within a month of injury (Carlstedt, 1995). The success of 183
re-implantation may depend upon whether the injury is proximal or distal to the transition zone. IMAGING OF BRACHIAL PLEXUS TRACTION INJURIES Myelography The first description of the use of myelography in adult brachial plexus trauma was by Murphey et al. (1947). They introduced the term ‘traumatic meningocele’ to describe a bulge of arachnoid membrane through a dural tear, with leakage of contrast medium beyond the spinal foramen. They assumed this to indicate the presence of intradural cervical root avulsion (Fig 1). Further studies using lipid soluble contrast media were limited by poor opacification of the subarachnoid space (Davies et al., 1966; Yeoman, 1968). The introduction of water-soluble contrast agents enabled better demonstration of the pathology and the display of root avulsion by
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the absence of the filling defect of the normal cervical roots within the root sleeve (Cobby et al., 1988). Nagano et al. produced a detailed classification of myelographic abnormalities in 90 patients and correlated their appearances with the findings at exploratory surgery, which included extradural inspection and measurement of SEPs (Nagano et al., 1989). Their results are worth discussing in detail. N, normal myelographic appearance, was seen in 72 roots of which 65 roots (90.3%) were normal or associated with postganglionic injury while seven were pre-ganglionic injuries. A1, a slightly abnormal root sleeve shadow, was seen in 48 cases, of which 21 roots (43.8%) were avulsed, 25 (52.8%) had post-ganglionic lesions, and two were normal. A2 represents obliteration of the tip of the root sleeve but with the filling defect of the nerve root present. Thirty-eight of 43 roots (88.4%) showing this appearance were pre-ganglionic injuries while five (11.6%) were post-ganglionic. A3 represents obliteration of the tip of the root sleeve with absence of the filling defect of the nerve root. Seventy-eight of 80 roots showing this appearance were pre-ganglionic injuries. D represents a defect in the contrast column instead of a nerve root sleeve, with 16 of 19 roots (84.2%) being preganglionic injuries. Finally M represents a traumatic meningocele. This appearance occurred at 107 levels of which 105 injuries were pre-ganglionic and only two roots were normal. Overall, the absence of filling defects of the nerve roots within the root sleeve was associated with a pre-ganglionic injury in 96.5% of cases. It is clear from this study that with progressive myelographic abnormality, the incidence of pre-ganglionic injury increases, but also that myelography can be associated with both false positive and false negative results (Fig 2). One reason for this is the occurrence of isolated ventral root avulsion. In this situation, myelography will show filling defects within the root sleeve and SEP recordings may be normal since the dorsal roots are intact. The relatively high incidence of erroneous results at the C5 and C6 levels is probably related to poor opacification of the CSF space. Leak of contrast medium through dural tears causes difficulty in display of the nerve roots in early cases while, in late cases, epidural scarring may obliterate the CSF space. Computerised Tomographic Myelography
Fig 1 Cervical myelogram in a 47-year-old male patient who sustained a right brachial plexus injury 10 months before examination. A right C7/T1 traumatic meningocele is evident, indicating intradural avulsion of the C8 root.
Unenhanced computerised tomography (CT) plays no role in the evaluation of the injured brachial plexus but may identify associated vertebral fractures (Volle et al., 1992). Computerised Tomographic Myelography (CTM) allows demonstration of the intradural nerve root in the axial plane and also differentiation between the ventral and dorsal roots. Root avulsion is identified by the absence of continuity of the root with the cord. Traumatic meningoceles are also clearly demonstrated and CTM better identifies their intraspinal extent (Fig 3).
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Fig 3 CTM of an 18-year-old girl who sustained a left brachial plexus injury 5 months before examination. An extensive multiloculated intraspinal meningocele is demonstrated (arrow).
Fig 2 Cervical myelogram in a 32-year-old male patient who sustained a right sided brachial plexus injury 1 week prior to referral. This case serves to illustrate the discrepancies between myelographic findings and extradural exploration and SEP recording. The myelogram shows relatively normal appearances at C5 and C6 with small traumatic meningoceles at C7 and T1. A filling defect representing the C8 nerve root is seen within the slightly abnormal, blunted root sleeve (white arrow) corresponding to a Nagano A2 lesion. A thickened T1 nerve root is identified within the meningocele at C7/T1 (black arrowhead). SEP recordings were present only at C5 and T1.
Marshall and De Silva (1986) first reported the use of CTM in 27 patients with brachial plexus injuries. Comparing cervical myelography and CTM with extradural operative findings, the diagnostic accuracy for intradural rupture for myelography was only 37.5%,
which increased to 75% with the addition of CT. They noted that roots and rootlets were not consistently visualised, possibly because relatively thick CT slices (4 mm) were employed. Walker et al. investigated seven adult patients with traumatic brachial plexus injuries using high resolution CTM (Walker et al., 1996). They emphasised the use of thin slices (typically 2–3 mm) and also the need to cover the spine from the C3 level to T2, because of the variability of level at which the cervical roots arise from the cord. Using this technique, they were able to display 95% of nerve roots. Roots on the injured side were considered adequately assessed only if the normal contralateral root could be visualised. These authors achieved 95% sensitivity and 98% specificity for the diagnosis of complete nerve root avulsion shown at extradural inspection of the plexus with intraoperative SEPs. Problems encountered included the inability to identify partial root avulsion and difficulty in two cases in demonstrating the T1 roots due to beam hardening artefact from the shoulders. Traumatic meningoceles were found in only 57% of root avulsions. The true ‘gold standard’ for imaging is direct intradural inspection of the injured roots via hemilaminectomy. This was performed by Carvalho et al. and Oberle et al. The former authors showed perfect correlation between CT myelography and intradural inspection in 85% of roots assessed in 25 patients (Carvalho et al., 1997). The results of Oberle et al. were less impressive, with inaccurate results in up to 27% of cases and also a poor correlation between observers, further reducing the value of the test (Oberle et al., 1998).
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Fig 4 Imaging of a 33-year-old nurse who sustained a left brachial plexus injury 5 days prior to referral: (a) Cervical myelogram demonstrates a subtle dural tear at the C5/6 intervertebral foramen level with leak of contrast medium into the neck (arrow). The intradural roots appear intact; (b) CTM at the C5/6 foramen level demonstrating isolated avulsion of the left C6 ventral root (arrowhead).
A particular difficulty with CTM is assessment of the C8 and T1 roots. This occurs for two reasons. Firstly, for patients with relatively short necks and broad shoulders, beam hardening artefact will significantly reduce the quality of the image. Secondly, as the spinal nerves run in a progressively more oblique direction from C4 down to T1, the lower roots are not seen in continuity from the cord to the exit foramen. This may result in false positive diagnoses of root avulsion. Therefore, CTM should always be assessed in combination with myelography. In our experience, the major advantage that CT adds to a good quality myelogram is the ability to identify isolated ventral root avulsion (Fig 4). In the early case, when re-implanation is a surgical option, high resolution CT may be able to demonstrate the presence of a residual root stump on the surface of the cord, indicating that the level of intradural injury is peripheral to the transition zone (Fig 5). Similarly, a central rupture may be indicated by the presence of a small pit in the cord, at the entry point of the root. However, no studies are available to determine the
accuracy of CT in this regard and further research should have this as a major aim.
Magnetic Resonance Imaging The earliest reports of the use of magnetic resonance imaging (MRI) in evaluation of the injured brachial plexus concentrated on the extradural appearances. Rapoport et al. identified post-traumatic neuromas and traumatic meningocele formation in three patients (Rapoport et al., 1988). Gupta et al. assessed ten patients between 3 months and 2 years post-injury and demonstrated neuromas and fibrosis in the plexus indicating the presence of extradural damage (Gupta et al., 1989). Traumatic meningoceles were also identified. The extradural findings do not identify the exact site of injury (Hems et al., 1999), nor do they reliably distinguish between rupture and stretching of the nerve trunk. Direct evidence of root avulsion from the cord is limited by MRI slice thickness. This is typically in the
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Fig 5 CTM of a 21-year-old male who sustained a right brachial plexus injury 3 months prior to referral. Complete C6 root avulsion is shown. A small bump is seen at the entry zone of the ventral root, suggesting a peripheral intradural rupture, whereas a pit is seen in the cord at the entry zone of the dorsal root, suggesting that this may represent a central intradural rupture. Unfortunately, the patient presented too late for intradural repair.
range of 4 to 5 mm for axial sequences whereas the nerve roots measure 1 to 3 mm (Carvalho et al., 1997). Volle et al. could directly identify only one of 18 root avulsions with MRI (Volle et al., 1992). Ochi et al. used axial and axial oblique planes to predict root avulsions at the C5 and C6 levels, comparing the findings with exploration of the brachial plexus and intraoperative SEPs (Ochiet al., 1994). Their criteria for root avulsion were as previously described for CTM; i.e. inability to identify the dorsal or ventral root in continuity with the cord. They achieved a diagnostic accuracy of 73% for the C5 root and 64% for C6. However, they did not state whether the intradural roots on the uninjured side were consistently visualised, so it is difficult to appreciate the validity of their results. Carvalho et al. used the criterion of ability to identify the contralateral normal root before commenting on the abnormal side (Carvalho et al., 1997). They found MRI to be unreliable or unable to identify avulsed roots in 48% of cases when compared with intradural surgical inspection. The causes for this failure were poor image quality due to motion artefact and intradural scarring. Hems et al. reviewed the use of MRI in 26 patients with brachial plexus trauma, imaging having been performed between 3 and 246 days post-injury (Hems et al., 1999). They described several secondary MRI features which were associated with root avulsion. These included spinal cord oedema in the acute stage (Fig 6), a feature also described by others (Volle et al., 1992). Other relevant findings included lateral displacement of the spinal cord, a post-traumatic syrinx, haemorrhage/
Fig 6 Sagittal T2 weighted MRI of the cervical spine of a 38-year-old man who sustained a left brachial plexus injury 3 days prior to referral. Oedema is seen within the spinal cord at the C4 and C5 levels (arrowhead), possibly indicating root avulsion central to the transition zone.
scarring in the spinal canal (Fig 7), absence of roots in the canal or intervertebral foramina (Fig 8), traumatic meningoceles (Fig 9) and denervation of erector spinae muscles, shown by wasting and fatty replacement. One or more of these signs was present in every patient with root avulsion. This implies that a normal MR study of the cervical spine excludes the presence of pre-ganglionic injury. However, when considering individual roots, MRI had a sensitivity of 81%; there were no false positive diagnoses. The finding of central spinal cord oedema in the acute stage probably signifies root avulsion central to the transition zone. However, this was only seen in one case and it was commented that the exact levels of root injury could not be assessed. Postganglionic injury was also identified, appearing as swelling of the nerve trunks on T1 weighted images and increased signal intensity on T2 weighted images
Fig 7 Axial T1 weighted MRI of a 35-year-old man who sustained a right brachial plexus injury 1 week prior to referral. An intradural haematoma is present at the C5/6 disc level (arrow).
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(Fig 10) on those studies obtained within a few weeks of the injury. Hems et al. concluded that a completely normal MRI of the supraclavicular plexus excluded significant post-ganglionic nerve disruption (Hems et al., 1999). Uetani et al. investigated signal intensity changes in the posterior cervical paraspinal muscles in association with traction injuries to the plexus (Uetani et al., 1997). These muscles are supplied by posterior primary rami, which branch from the spinal roots immediately after they leave the intervertebral foramina. Therefore, denervation of these muscles suggests a pre-ganglionic injury. Signal changes could be seen as soon as 15 days after injury and were identified in five of seven patients with nerve root avulsion. Abnormal signal was seen at levels both proximal and distal to the levels of root avulsion and, therefore, the assessment of muscle denervation does not indicate the segmental levels of intradural root avulsion. In four patients without nerve root avulsion, the MR appearance of the deep cervical paraspinal muscles was normal. However, this finding does not necessarily exclude root avulsion if imaging is performed in the acute stage. 3-D MR myelography (MRM) is a technique in which a myelogram-like image is produced by using a heavily T2 weighted sequence together with fat suppression. A
Fig 8 Axial T2 weighted MRI of a 21-year-old man who sustained a left brachial plexus injury 4 days prior to imaging. The C7 nerve root is not identified in the left C6/7 foramen (open arrow) and the cord is displaced to the right. A normal C7 root is seen on the right side (arrow).
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Fig 9 MRI of a 19-year-old man who sustained a left brachial plexus injury 1 month prior to imaging: (a) Sagittal T1 (left) and T2 (right) weighted MRI of the cervical spine showing traumatic meningoceles within the C5/6, C6/7 and C7/T1 intervertebral foramina (arrowheads); (b) Axial T2 weighted MRI at the C7/T1 intervertebral foramen level showing typical appearances of a traumatic meningocele. The cord is deviated to the right.
multiple intensity projection (MIP) algorithm is then applied to the data volume and the resulting image can be rotated to produce oblique views similar to conventional myelography. The technique has been used in the
assessment of adult brachial plexus trauma (Gasparotti et al., 1997; Nakamura et al., 1997). In a detailed study of ten patients, Nakamura et al. compared the accuracy of MRM, conventional
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The use of enhanced MRI has been studied by Hayashi et al. In the evaluation of 500 nerve roots, they identified enhancement of 12 intradural nerve roots and enhancement of the cord surface at the root entry zone, termed ‘root stump’ enhancement, at 42 sites (Hayashi et al., 1998). Comparing the results of enhanced MRI with surgical exploration and intraoperative SEPs, the sensitivity and specificity of nerve root enhancement for a pre-ganglionic injury were 8% and 97% respectively. Similarly, the sensitivity and specificity of ‘root stump’ enhancement for a pre-ganglionic injury were 47% and 98% respectively. The pathological basis for the enhancement could not be ascertained since intradural inspection was not carried out. Therefore, enhanced MRI seems to add little to the imaging of adult brachial plexus injury. CONCLUSIONS
Fig 10 MRI of a 16-year-old school boy who sustained a left brachial plexus injury. Coronal STIR sequence demonstrates swelling and oedema in the plexus (arrow).
myelography and CTM with surgical exploration for the identification of traumatic meningoceles, injured nerve roots and abnormal nerve root sleeves (Nakamura et al., 1997). MRM and myelographic findings were classified according to the system of Nagano et al. MRM had a sensitivity, specificity and accuracy in detecting traumatic meningoceles of 88%, 100% and 98%, and in detecting complete root avulsion of 91%, 92% and 92%. One problem of the technique is the difficulty in identifying exactly the levels involved since there are no bony landmarks. The authors appeared to determine levels by comparison with the conventional myelogram. However, since the technique is suggested as a replacement for myelography, the problem of determining level needs to be further considered. Gasparotti et al. matched MRM with conventional myelography and CTM as the gold standards, and achieved 89% sensitivity, 95% specificity and 92% diagnostic accuracy. However, the accuracy of their ‘gold standard’ was not determined with reference to surgical findings, so the results are difficult to assess (Gasparotti et al., 1997).
The imaging of traction injuries to the adult brachial plexus poses great challenges to the interested radiologist. In the acute phase, when intradural repair is a surgical option, the aim of imaging must be to differentiate between central and peripheral intradural rupture. High resolution CTM may be able to differentiate the two by the demonstration of residual tufts of the avulsed root or by showing a defect in the surface of the cord. However, the acutely injured patient is often the most difficult to image. The identification of oedema within the cord on T2 weighted MRI studies may also indicate central avulsion. For patients referred late, the aim should be to improve MRI techniques for identifying pre-ganglionic injury, and so save the patient from the invasive and unpleasant experience of cervical myelography. References Berthold C-H, Carlstedt T, Corneliuson O (1993). The central-peripheral transition zone. In: Dyck PJ, Thomas PK (eds), Peripheral neuropathy, Third Edition. Philadelphia, WB Saunders, 1993: 73–91. Birch R (1987). Brachial plexus injuries. Current Orthopaedics, 1: 316–323. Birch R, Bonney G, Wynn Parry CB. Chapters 6 and 9. In: Surgical disorders of the peripheral nerves, Edinburgh, Churchill Livingstone, 1998 Bonney G (1954). The value of axon responses in determining the site of lesion in traction lesions of the brachial plexus. Brain, 77: 588–609. Bonney G, Gilliatt RW (1958). Sensory Nerve Conduction after Traction Lesion of the Brachial Plexus. Proceedings of the Royal Society of Medicine, 51: 365–367. Carlstedt T (1995). Spinal nerve root injuries in brachial plexus lesions: basic science and clinical application of new surgical strategies. A review. Microsurgery, 16: 13–16. Carvalho GA, Nikkhah G, Matthies G et al. (1997). Diagnosis of root avulsions in traumatic brachial plexus injuries: value of computerised tomography myelography and magnetic resonance imaging. Journal of Neurosurgery, 86: 69–76. Cobby MJD, Leslie IJ, Watt I (1988). Cervical Myelography of Nerve Root Avulsion injuries using water-soluble contrast media. British Journal of Radiology, 61: 673–678. Davies ER, Sutton D, Bligh AS (1966). Myelography in brachial plexus injury. British Journal of Radiology, 39: 362–371. Gasparotti R, Ferraresi S, Pinelli L et al. (1997). Three-dimensional MR myelography of traumatic injuries of the brachial plexus. American Journal of Neuroradiology, 18: 1733–1742. Gupta RK, Mehta VS, Banerji AK et al. (1989). MR evaluation of brachial plexus injuries. Neuroradiology, 31: 377–381.
BRACHIAL PLEXUS IMAGING Hayashi N, Yamamoto S, Okubo T et al. (1998). Avulsion injury of cervical nerve roots: Enhanced intradural nerve roots at MR imaging. Radiology, 206: 817–822. Hems TEJ, Birch R, Carlstedt T (1999). The role of magnetic resonance imaging in the management of traction injuries of the adult brachial plexus. Journal of Hand Surgery 24B: 550–555. Landi A, Copeland SA, Wynn Parry CB, Jones SJ (1980). The role of somatosensory evoked potentials and nerve conduction studies in the surgical management of brachial plexus injuries. Journal of Bone and Joint Surgery, 82B: 492–496. Marshall RW, De Silva RDD (1986). Computerised axial tomography in traction injuries of the brachial plexus. Journal of Bone and Joint Surgery, 68B: 734–738. Murphey F, Hartung W, Kirklin JW (1947). Myelographic demonstration of avulsion injury of the brachial plexus. American Journal of Roentgenology, 58: 102–105. Nagano A, Ochiai N, Sugioka H et al. (1989). Usefulness of myelography in brachial plexus injuries. Journal of Hand Surgery, 14B: 59–64. Nakamura T, Yabe Y, Horiuchi Y et al. (1997). Magnetic resonance myelography in brachial plexus injury. Journal of Bone and Joint Surgery, 79B: 764–769. Oberle J, Antoniadis G, Rath SA et al. (1998). Radiological investigations and intra-operative evoked potentials for the diagnosis of nerve root avulsion: evaluation of both modalities by intradural root inspection. Acta Neurochirurgica, 140: 527–531. Ochi M, Ikuta Y, Watanabe M et al. (1994). The diagnostic value of MRI in traumatic brachial plexus injury. Journal of Hand Surgery, 19B: 55–59.
191 Rapoport S, Blair DN, McCarthy SM et al. (1988). Brachial plexus: Correlation of MR imaging with CT and pathologic findings. Radiology, 167: 161–165. Schenker M, Birch R (2000). Diagnosis of the level of intradural ruptures of the ventral and dorsal rootlets in traction lesions of the brachial plexus. Journal of Bone and Joint Surgery, B [in press]. Uetani M, Hayashi K, Hashmi R et al. (1997). Traction injuries of the brachial plexus: signal intensity changes of the posterior cervical paraspinal muscles on MRI. Journal of Computer Assisted Tomography, 21: 790–795. Volle E, Assheuer J, Hedde JP et al. (1992). Radicular avulsion resulting from spinal injury: assessment of diagnostic modalities. Neuroradiology, 34: 235–240. Walker AT, Chaloupka JC, De Lotbiniere ACJ et al. (1996). Detection of nerve rootlet avulsion on CT myelography in patients with birth palsy and brachial plexus injury after trauma. American Journal of Roentgenology, 167: 1283–1287. Yeoman PM (1968). Cervical myelography in traction injuries of the brachial plexus. Journal of Bone and Joint Surgery, 50B: 253–260. Received: 4 October 2001 Accepted after revision: 19 December 2000 Mr Asif Saifuddin, The Radiology Dept, The Royal National Orthopaedic Hospital, Brockley Hill, Stanmore, Middlesex HA7 4LP, UK. E-mail: [email protected]
# 2001 The British Society for Surgery of the Hand doi: 10.1054/jhsb.2000.0555, available online at http://www.idealibrary.com on