- Email: [email protected]
Recovery of brachial plexus injuries
Review special article Recovery of brachial plexus injuries R.T.W.M.
Thomeer”
Introduction Summary
A lesion to the brachial plexus usually leads to a disabling condition, in particular when it affects the dominant arm. The vast majority of these lesions is caused by road traffic accidents and particularly involves high-kinetic motor vehicle traumata in young males“‘. Other mechanical lesions result from birth injury (‘obstetrical pal~y’)‘-~,stab wounds, and surgical errors. Moreover, plexopathy can be due to a cervical rib, neural tumors, carcinomatous infiltration and radiotherapy’-~.l~‘-l~. Finally, although aetiologically indefinite, neuralgic amyotrophy is a kind of plexopathy”. Seriously wounded motorcycle or moped victims survive more often since the wearing of crash helmets has become compulsory in most European countries. Associated life threatening injuries may initially overshadow a brachial plexus lesion. The elective treatment of a traumatic brachial plexus lesion presents a complex medical, surgical and rehabilitation problem. Functional rehabilitation of the patient has substantial social and economic impact. Anatomy The brachiat plexus is usually constituted by the spinal nerves (roots) C5 to Thl (Fig. 1). In the supraclavicular area these roots join to form * Lkpartment of Neurosurgery,
Despite technical advances, the ability to restore function following severe brachial plexus traction lesions is limited. Major problems hampering good results are the inability to recognize corresponding fascicles in case of a large nerve gap and the lack of a proximal nerve stump in root avulsions. This article discusses the diagnosis and treatment of such injuries in combination with research in this field. Key words: brachial plexus lesion - regeneration - nerve transplantation.
three trunks: C5 and C6 join to form the superior, C7 continues in the middle, and C8 and Thl join to form the inferior trunk. Retrociavicularly the ventral divisions of the superior trunk and middle trunk constitute the lateral fascicle, which divides in the subpectoral space in the musculocutaneus nerve and the lateral root of median nerve. The medial fascicle is the extension of the ventral division of the inferior trunk. This fascicle divides into the medial root of the median nerve and the ulnar nerve. The dorsal fascicle is constituted from the dorsal divisions of all three primary trunks. Running dorsal to the subclavian-axillary artery, its splits up in the axillary and the radial nerve.
University State Hospital, The Netheriunds
Addres for correspondence und reprint requests: Profl Dr. R. T. W. M. Thornear, Hospitul. P. 0. Box 9600, 2300 RC Leiden, The Netherlands Accepted 17-12-90 c’lin Neuro/ Neurosrrrg I99I.
Vol. 9.7-I
Dept. of Neurosurger_v,University State
N. phrenicus N. dorsalis scapulae _.
N. suprascapularis
N. thoracicus
longus
N. mus~ulo~utaneus
N. cut. brachii med. N. cut. antebrachii N. medianus
med.
/ N. ulnaris
Fig. 1 Anatomy of brachial plexus. TS: superior trunk, TM: middle trunk, TI: inferior trunk, FL: lateral fasicle, FP: posterior fascicle, FM: medial fascicle.
Over its entire course, nerves to the shoulder muscles leave the plexus. One must be aware that variations in the anatomy of the brachial plexus can exist, which hampers the clinical efforts to localize the site of a lesion.
Traumatic brachial plexus injury may be caused by penetration, compression or traction. Penetration can occur by sharp objects such as knife and glass, or by bullet. Stab wounds and iatrogenic lesions produce sharp tissue lesions, in which the transected nerves can be easily identified and re-united. Immediate neurosurgical repair favors anatomical reconstruction with optimal coaptation of the corresponding fascicles. Shot wounds initially produce a far more serious functional deficit than would be expected on the basis of the mechanical lesion of the bullet alone. This is due to shock wave distortion. After a lapse of time spontaneous recovery from the latter will clarify the site and 4
extent of the lesion produced by the bullet itself”‘. Compression injury occurs between the clavicle and the first or second rib, when an external force presses the clavicle down. This kind of lesion most frequently occurs in combination with an upper root traction injury which can be understood from the mechanism of the trauma14. Root tension varies with the position of the arm. Widening of the angle between neck and shoulder with a pendulant arm exerts greatest traction on roots (2.5and C6. Lateral abduction of the arm puts all roots under stress, but C7 most. With the arm in elevated position, the roots C8 and Thf. are under greatest traction. If traction force is excessive, all roots might become avulsed from the spinal cord, regardless of the position of the arm. The first mentionned mechanism of injury, depression of the shoulder with a pendulant arm, occurs most frequently. When a moped hits an obstacle, the patient is launched from it to crash down into the road, his shoulder and his
head hitting the ground resulting in a forceful widening of the angle between the neck and shoulder’“. The commonest mechanism of obstetrical plexus injury occurs to the upper roots both in vertex delivery when shoulder dystocia necessitates excessive lateral flexion of the neck, as well as in breech’ birth during delivery of the arms or the aftercoming head. The majority of lower plexus lesions occurs during face presentation with hyperextension of the cervical spine’. Haftek” studied the sequential phenomena resulting from progressive stretch on a peripheral nerve (Fig. 2). First. the nerve looses its undulating aspect, the fascicles and the nerve become straight. Stronger tension reduces the cross-sectional area within the epineurium, causing an increase in intrafascicular pressure, ischemia due to capillary/arteriolar compression. myelin disruption and in places axonal interruption (axonotmesis). Subsequently, at this point the elastic limit of the stretched nerve has been reached and the epineurium ruptures. Further elongation produces perineurial rupture. Only a slight further increase in traction force is needed for all axons to rupture, including the endoneurium and basement membranes. This finally leads to complete rupture of the nerve. In accordance with the increasing severity, Sunderland” proposed a clinical classification consisting of five degrees, the first degree being a short lasting loss of conduction of the axons, while the fifth degree denotes a total loss of continuity of the nerve. In clinical practice, however. the functional classification of Sed-
gr
traction
don16, neurapraxia, axonotmesis and neurotmesis, is of more practical value. Traction at the brachial plexus exerts forces also on the nerve roots. The nerve root-ganglion complex is laterally secured to the meninges and only both upper spinal nerves (C5 and C6) have a protective fibrous attachment of their epineurium to the transverse process”. If this fibrous attachment holds on severe traction, the nerve ruptures intra- or extraforaminarly. With the failure or abscence (C8 and Thl) of this protective anchor, the nerve root complex with its meningeal sleeve is pulled laterally through the pertinent intervertebral foramen, the dura tears, and the tensed fila radicularia avulse at their weakest point, viz. their attachment to the cord. Traction injuries to the brachial plexus may result in widespread lesions, combining root avulsion with lesions of the extravertebral parts of the plexus. Thus root avulsions do not produce a pure supraganglionic lesion, because tensile forces cause a combined pre- and postganglionic lesion. Clinically, there might be loss of axon reflexes in the presence of root avulsion. Clinical assessment History
The nature of the trauma is important to determine the severity of the lesion and its chance of spontaneous recovery. In traction injuries, motorcycle accidents are likely to produce severe lesions as high kinetic energy is invariably transferred, while e.g. shoulder luxation due to a
load epineurial rupture
200
-
1” stage --
cm elongation Fig. 2 Three stages during nerve stretching according to Haftek (1970). See text.
perineurial rupture 5
Fig. 3 Chart of all muscles m-
-
nervated by the brachial plexus according Deburge’. arranged overlap);
d’AubignC vertically
thick
pass muscles one particular nerve.
-----.
and
The myotomes
-
are
(note
lines enconrinnervated
by -_-___
peripheral TER
MIN
BRACHIALIS
TRICEPS ECR
M2
trivial fall in one’s home is likely to produce mild traction injury*‘. Severe pain in an anaesthetic arm is suggestive for root avulsions (de-afferentiation pain)‘*-**, General examination Brachial plexus palsies due to traffic accidents frequently present with associated lesions, both in the affected area (fractures of vertebral transverse processes, clavicle, scapula, humerus, rarely rupture of the subclavian artery) and/or at distance (cerebral contusion, fractures)23‘25. Neurological examination Motor function of all the muscles innervated by the plexus is tested. The power of each individual muscle is graded on the traditional O-5 scale. The findings are transcribed to the sophisticated chart (Fig. 3) designed by Merle d’Aubigne and Deburge”. This chart combines the information by which spinal nerves and by which peripheral nerve the individual muscle is innervated. It is most helpful in determining the site of the lesion. Sensory examination of the segmental or peripheral nerve innervation areas provides further information. However, due to overlap of neighbouring dermatomes the resulting sensory deficit might be smaller than expected. Sympathetic dysfunction presents itself with changes in colour, sweating and temperature of the affected extremity. The presence of Horner’s syndrome is indicative of root avulsion of
ECU
M3
M4
M5
at least Thl and therefore associated with poor prognosis for recovery of the total brachial plexus palsy. Finally, the Tinel-Hoffmann sign may provide useful information”. This sign refers to the radiating tingling sensation which is felt in its sensory innervation area on percussion of a nerve. If present, the sensation is evoked by highly sensitive regenerating axons, which have not yet become myelinated. The most distal point at which the sign is elicited determines the rate of growth of regenerating axons upon successive examinations. If the site of provocation by percussion does not progress with time and remains within the same place, this is the result of neuroma formation, which excludes spontaneous recovery. Electra-physiological examination Electromyography (EMG) provides information on the function of the muscle. It may reveal normal action potentials, or fibrillation which indicates denervation. or polyphasic action potentials in case of reinnervation. EMG is most useful in the assessment of brachial plexus lesions. It adds objective documentation of motor dysfunction, particularly of muscles that are hard to evaluate clinically. If, for example, exorotation in the shoulder is weak, this might be due to either inferior spinate or teres minor paresis or both; EMG examination resolves this dilemma as it will show denervation in only one or both muscles. Nerve conduction studies are of little value.
Due to Wallerian
degeneration
duction
fibers
of motor
Theoretically, (SNAP)
there is no con-
to paralysed
sensory
nerve
offer information
action
muscles. potentials
on the level of nerve
injury, since in preganglionic injury (i.e. root avulsion) T-cells in the ganglion remain in continuity with their peripheral axons, contrary to postganglionic lesions. In the first case SNAP’s are present
(although
ing) and in the second injuries, method
however, between
the
the patient
‘feels’ noth-
abolished.
In traction
discrimination
pre- and postganglionic
is as a rule hampered
due to simultaneous
by this lesion pres-
ence of both. Moreover segmental overlap might provide false positive informatior?~“. SEP (somatosensory evoked potentials) does not really add information, since recordings are positive in clinically non-anaesthetic and negative in anaesthetic dermatomes. Moreover, findings may be difficult to interprete. Peroperative SEP recordings, however, are useful in that they provide information on the sensory function of the directly stimulated spinal nerve. The clinical value of SNAP lesions remains debatable3”.
and SEP in plexus
Neuroradiological investigation Along with EMG, cervical myelography is indispensable for the analysis of brachial plexus traction injuries. The contrast dye is instillated by lateral puncture between Cl and C2. The roentgenograms offer information on the presence or abscence of the fila radicularia of all cervical roots and Thl (Fig. 4). In case of doubt, additional CT examination is helpful”‘. This method of investigation also enables one to differentiate between dorsal and ventral rootlets which is of particular interest in partial root avulsions. Meningeal tears result frequently in (pseudo) meningoceles which may accompany root avulsions. Nevertheless meningoceles may be present without avulsion of the pertinent root. At this stage MRI (Magnetic Resonance Imaging) does not yield a sufficiently high resolution to visualize spinal rootlets. Finally, X-ray examination of the diaphragm during in - and exspiration offers information on the involvement of C4 in traction injuries, because (part of) the phrenic nerve fascicles arise from this root.
Fig. 4 Cervical myelography showing abscence of fila radicularia of roots C7. C8 and Thl right. At Thl, a pseudomeningocele (avulsion cyst) is visible.
Neurosurgical treatment In sharp lesions, such as stab wounds, surgical repair has to be carried out immediately. Anatomical reconstruction of severed parts is relatively easy and functional results are correspondingly good. Traction injuries, however, generally present with extensive loss of function and initially it is impossible to predict which parts of the plexus will spontaneously recover and which not. Spontaneous recovery will occur in case of axonotmesis, but axonal outgrowth takes a long time in these cases (at least a year) due to the limited growth rate and the long distance to their targets. Waiting carries the risk of no recovery and after one year muscle atrophy has proceeded to such a degree that surgical nerve repair beyond that time can no more produce motor recovery. Early surgical exploration. however, exposes
a group of patients to a non-indicated operation as they were to recover spontaneously. Thus selection of patients for surgery is difficult”?. Factors influencing the decision include the severity of trauma, the findings on myelography, and possible early clinical (or EMG) signs of recovery, including the stationary or moving Tinel sign. It is generally agreed upon that, when signs of recovery fail to appear, surgical exploration should preferentially be carried out within three to five months after the injury”.“‘.‘3,‘J,‘3-‘h. The same holds for obstetrical palsies, which occur with an incidence of l-3 per 1000 living births3’. As 10 to 15 per cent of these babies have a poor functional prognosis”, attempts should be made to identify this group early in order to treat them surgically as wel17~n~37-3y. At the exploration, which is carried out with microsurgical techniques and the operating microscope, the final diagnosis on the site and extent of the lesion is made. Neuromata are excised and continuity of the injured parts is restored by bridging the gaps with nerve grafts. Most frequently, free grafts are used (autolobut de_ gous sural nerve) I 2 4 6,10,23.24.33.34.16.JO-4K, pending on the case other techniques such as free vascularized or pedicled nerve grafts are in current practice too4y-52.If the spinal nerves are found to be fibrosed, these nerves are first serially transected in a distal to proximally dissection until normal fascicles re-appear on the cross-sectional surface. The final nerve-tranch can be examined intraoperatively on frozen sections to ascertain the presence of myelin. Intraoperative nerve recording is also used”“. If one or more spinal nerves are suited for transplantation, a plan for reconstruction is made. Connection to its distal counterparts is one feasible option but, in case e.g. only C5 is available and all other roots avulsed, bypassing of the whole plexus by connecting C5 to the musculocutaneus nerve is preferable (Fig. 5). In the latter case (a flail arm), it is better to restore one function (elbow flexion) well, instead of dispersing the axons over a major part of the plexus which would inevitably fail to render functional results. Priorities in repair are elbow flexion, wrist and finger flexion with restoration of protective median sensation and shoulder control. 8
lat. ff
0C8 OTI
N. musculocutaneus
N. mediinus
Fig. 5 Transplantation of C5 to the lateral fascicle in case of root avulsion C6 through Thl
Except for intraplexal reconstructions, extraintraplexal nerve transfers can restore (a part of) the function lost in case of root avulsionss3-60. Among these are the accessory-suprascapular transfer (shoulder abduction) and intercostalmusculocutaneous transfer. The latter patients learn to keep their reinnervated biceps muscle strained independent of respiration57. In planning a neurosurgical reconstructive procedure, the surgeon should be aware of the plastic-orthopedic possibilities for muscle-tendon transposition and arthrodesis. It needs no saying that analysis and nerve repair are only a part of the whole medical and social attendance of these badly handicapped patients. Results of reconstructive brachial plexus surgery are hard to evaluate. Direct repair after sharp transection yields more or less the same results as in peripheral nerve repair, but the majority of these lesions consists of traction injuries which carries worse results due to a variety of reasons. Moreover it is hardly impossible to constitute comparable groups of patients for evaluation, as the severity and extent of the neural trauma in traction injuries differs from patient to patient. However, as recent literature teaches, it is obvious that results of surgical repair are far better than conservative treatment, provided the intervention has been carried out at the appropriate time.
In order to further improve the results of reconstructive brachial plexus surgery two major problems have to be solved, which can only be accomplished by laboratory research. The first and foremost is the problem of matching. Due to intermingling, the funicular pattern of the cross sectional surface of a nerve differs from place to place, even over short distances. The ideal in nerve grafting, viz. to restore continuity of corresponding funiculi, is difficult to achieve for this reason. Although the pattern of bundle-groups changes with short distances, their axial locaiisation remains constant for some longer distances”‘. Thus it is possible to re-connect fibres of the same group over short gaps, if one maintains correct axial alignment, which implies that the graft is apposed to the same quadrant of proximal and distal nerve stump. However, this does not hold for long distances. Sometimes gaps of 10 cm or more have to be bridged (Fig. 6). In these cases, it would be of great help if at least discrimination of motor and sensory bundles were possible in order to connect motor to motor and sensory to sensory fibers. Today, there is no such a method available. Theoretically there must be a biochemical difference between motoric and sensory fibers. It would really be a breakthrough in peripheral nerve surgery if a discriminatory staining method became available. This method should preferentially be applicable to both proximal (vital) and distal (degenerated) nerve stumps and moreover results should be available per-operatively. The second major problem concerns the root avulsions. Is there a chance for regeneration after reimplantation of the root in the cord? In contradistinction to what is noted in the peripheral nervous system (PNS), axonal re-
PROBLEM
OF MAfCHlNG
_
0
;? -tIIY.z f
l
0
Fig. 6 Note the differences of the fascicular pattern in the cross-sectional areas of both stumps in case of a nerve gap.
growth after CNS injury is poor, though elongation of spinal cord pathways in mammals after transection and grafting with peripheral nerves has been demonstrated~‘.~. In spite of this, restoration of function has never been achieved. Probably, there are crucial differences in the local tissue microenvironment of CNS and PNS. The role of extracellular matrix (ECM) macromolecules in axonal regeneration is subject to neurobiological research%. A properly synthesized ECM seems essential in guiding neuronal outgrowth. In the severed PNS, the linear organization of ECM tubes in the distal part of the nerve enables axonal regrowth”. Because of the paucity of similar ECM materials in the CNS, no such framework is available to assist in the process of axonal outgrowth, which might explain the failure of CNS to regenerate. Savio and Schwab”’ investigated the substrate properties of adult mammalian nervous tissue using frozen sections on which neuronal ceils from e.g. dorsal root ganglia, were cultured. The results showed that CNS white matter has a dramatic nonpermissive effect on cell adhesion and fiber outgrowth, in contrast to gray matter which allowed cell adhesion and neurite elongation. This inhibitory property of oiigodendroglia and CNS myelin was significantly reduced by an antibody administration against membrane proteins present on the surface of these myelin-forming cells. In vivo experiments showed the same hostility of CNS white matter. Carlstedt” anastomosed ventral rootlets to the ipsilateral dorsal root. Regrowth of ventral axons into the dorsal rootlets occurred, but only in its PNS part. Fibers ended at the PNS-CNS border. Entrance of the CNS might have been prohibited by the same hostile factors in the white matter as described by Savio et al”. Axons of spinal motoneurons in the PNS have the capacity of regeneration. The question is if the same capacity remains present if the lesion is inflicted to the CNS segment of these axons, as is the case in root avulsion. Does the cell body survive such a proximal lesion and, if so, under what condition could it exert its presumed regenerative capacity. Outgrowth of fibers from the CNS into the PNS has recently been reportedh3.‘“. The interpretation of the findings however is still puzz9
ling. Nevertheless, research in this field seems promising and is very important from a clinical point of view. Acknowledgments The author is indebted to Mrs. W.J. Ouwehand for typing the manuscript and Mr. G.J. van der Giessen for the photography.
References NAKAKAS A. Indications et resultats du traitement chirurgical direct dans les lesions par elongation du plexus brachial. Rev Chir Orthop 1977; 63:44-54. NARAKAS A. Surgical treatment of traction injuriesof the brachial plexus. Clin Orthop 1978; 133:71-90. NARAKAS A. Neurosurgical approach to brachial plexus lesions. In: Het fraumatische letsei van de plexus brachialis. Boerhaave Committee Leiden, 1982. NARAKAS A. Pathomechanics, diagnosis and surgical treatment of supraclavicular brachial plexus injuries. Ned Tijdschr Geneeskd 1986; 130:1967-8. ALNOT JY, JOLLY A, FROT 8. Traitement direct des lesions nerveuses dans les paralysies traumatiques du plexus brachial chez I’adulte. Intern Orthop 1981; 5:151-68. SEDEL L. The results of surgical repair of brachial plexus injuries. J. Bone Joint Surg 1982; 64B: 54. CXLBERTA,KHOURI N,CARLIOZH. Explorationchirurgitale du plexus brachial dans le paralysie obstetricale. Rev chir Orthop 1980; 66:33-42. TASSIN JL. Paralysies obstttricales du plexus brachial. These, Universite Paris VII 1983. BROWN KLB. Review of obstetrical palsies. Nonoperative treatment. In: TERZIS I (ed): Clinics in Plastic Surgery. Philadelphia/London/Toronto: WB Saunders Co, 1984 Vol 11, pp 181-7. LEFFEKT RD. Brachial plexus injuries. New York: Churchill Livingstone, 1985. LUSKMD, KLINEDG,GARCIA CA. Tumors ofthebrachial plexus. Neurosurg 1987; 21:439-53. AMPIL FL. Radiotherapy for carcinomatous brachial plexopathy. Cancer 1985; 56:2185-S. PARSONAGE MJ, TURNER JWA. Neuralgic amyotrophy. Lancet 1957; 209-12. SUNDERLAND s. Nerves and nerve injuries. 2nd ed. Edinburgh: Churchill Livingstone, 1978. HAFTEK J. Stretch injury of peripheral nerve, acute effects of stretching on rabbit nerve. J Bone Joint Surg 1970; 52B:534-65. SEDDON HJ. Three types of nerve injury. Brain 1943; 66:237. COENE LNJEM. Axillary nerve lesions and associated injuries. Thesis: Leiden 1985 pp 63-78. BONNARD c, NARAKAS A. Syndromes douloureux et lesions traumatiques du plexus brachial. Helv Chir Acta 1985; 52:621-7. BRUXELLEJ,TRAVERS V,THIEBAUTJB. Occurrence and treatment of pain after brachial plexus injury. Clin Orthop Rel Res 1988; 237:87-95. THOMAS DGT, SHEEHY JPR. Dorsal root entry zone lesions (Nashold’s procedure) for pain relief following brachial plexus avulsion. J Neurol Neurosurg Psychiatry 1983; 46:924-8.
10
/OKUH i>s. NASHOLD HS. cu~tt WA.Avulsion ot the hrachial plexus. A review with implications on the therap! of intractable pain. Surg Nemo1 1974; 2:347-T ;. NAKAKAS A. The surgical treatment of traumatic brachial plexus lesions. Intern Surg 1980: 65521-7 UAKAKAS A. The treatment of hrachial plexus injuries. Inter Orthop 1985: 9:29-X. NARAKAS A. Plexus brachialis und naheliegende periphere Nervenverletzungen bei Wierbelfrakturen und andere Traumen der Halswirhelsaule. Orthopade 1987: 16:81-6. M~RLED‘AUBIGNE KM.D~BL:RG~ A. Etiologie, eVOuItiOII et pronostique des paralysies traumatiques du plexus brachial. Rev Chir Orthop 1967; 53:23. LANDI A, ~OPPLANU SA. Value of the Tine1 sign in brachial plexus lesions. Ann R Co11Surg Engl 1979; 61:470-l. BONNEY G. C~II.LIAT~ RW. Sensory nerve conduction after traction injuries of the brachial plexus. Proc R Sot med 1958; 51:365-7. LANDI A,~OPELAND SA.WYNN PARRY CII,JONESSJ. The role of somatosensory evoked potentials and nerve conduction studies in the surgical management of brachial plexus injuries. J Bone Joint Surg 1980; 62B:492-5. SYNEK v~, (‘OWAN JC. Somatosensory evoked potentials in patients with supraclavicular brachial plexus injuries. Neurology 1982; 32: 1347-52. MARSHALL Rw, DE WILVA RDD. Computerised axial tomography in traction injuries of the brachial plexus. J Bone Joint Surg 1986; 68B:734-8. JASPEKS KBM. Medical decision support. An approach in the domain of brachial plexus injuries. Thesis: Delft 1990. KLINE DG, HACKETT ER, HAPPEL LH. Surgery for lesions of the brachial plexus. Arch Neural 1986; 43: 170-81. MERLE M. La chirurgie directe du plexus brachial traumatique. Rev Readapt Fonct Sot 1980; 6:45-52. MILLES H. Trauma involving the brachial plexus. In: Omer, Spinner (eds): Management of peripheral nerve problems. Philadelphia/London/Toronto: WB Saunders Co, 1980, pp 548-68. SEDEL L. The management of supraclavicular (plexus) lesions. In: TERZIS J (ed): Microreconstruction of Nerve Injuries. Philadelphia/London/Toronto: Saunders WB co. 1987. KAWAMATAH,MASADAK,
ISUYUGUCHI
Y,KAWAIH,ONO
Early microsurgical reconstruction in birth palsy. Clin Orthop Rel Res 1987; 215:233-42. SOLONEN KA. KY~PPY s, 'TELARANTA T. Early reconstruction of the brachial plexus after birth injuries. Acta Orthop Scan 1980; 51:365-9. SOLONEN KA,TELERANTAT,RYoPPYS. Early IeCOIISIrUCIion of birth injuries of the brachial plexus. J Pediatr Orthop 1981; 1:367-7(X AI I.IEU Y. Exploration et traitement direct des lesions nerveuses dans les paralysies traumatique par Clongation du plexus brachial chez I‘adulte. Rev Chir Orthop 1977; 63: 107-22. JAMIESON A, HUC~HES s. The role of surgery in the management of closed injuries to the brachial plexus. Clin Orthop 1980; 147:210-5. KLINE DG, JUDI~E DJ. Operative management of selected brachial plexus lesions. J Neurosurg 1983; 58:631-49. MILLESI H. Surgical management of brachial plexus injuries. J. Hand Surg 1977; 2:367-79. MILLESI H. Brachial plexus injuries: nerve grafting. Clin Orthop Rel Res 1988; 237:36-42. K, TADA
K.
NAR-ZKAS A. Brachial plexus surgery. Orthop Clin North Am 1981; 12:303-23. SEDI:L L. Repair of severe traction lesions of the brachial plexus. Clin Orthop Rel Res 1988; 237:62-6. SOLONEN KA, ~ASTAMAKIM, STROMB. Surgery Of the brachial plexus. Acra Orthop Scan 1984; .55:436-40. YEOMAN PM. SEDDON HJ. Brachial plexus injuries. treatment of the flail arm. J Bone Joint Surg 1961; 43B:493. BIRCH
R. KLINKERSTON
M,BONNEY
G,JAMIESON
AM.EX-
perience with the free vascularized ulnar nerve graft in repair of supraclaviculair lesions of the brachial plexus. Clin Orthop Rel Res 1988: 237:96-104. NARAKAS A. Personal communication 1985. STRANGEFGSC’.An operation for nerve pedicle grafting: Preliminary communication. Br J Surg 1947; 34:423. TAYLOR GI. HAM FJ. The free vascularised nerve graft: A further experimental and clinical application of microvascular techniques. Plast Reconstr Surg 1976; 57:413. ALLIEU Y. PRI~AT ~hf. BoNNEL F. Paralysis in rootavulsion of the brachial plexus. Neurotization by the spinal accessory nerve. In: TERZIS I. (ed): Clinics in Plastic Surgery. Philadelphia/London/Toronto: WB Saunders Co. 1984, Vol 11, pp 113-6. BRLJY~LLI G. Neurotization of avulsed roots of the brachial plexus by means of anterior nerves of the cervical plexus. Int J Microsurg 1980: 255-S. HRLINELLI G. Neurotization of avulsed rootsof the brachial plexus by means of anterior nerves of the cervical plexus. In: TERZIS J (ed): Microreconstruction of Nerve Injuries. Philadelphia/London/Toronto: Saunders WB Co, 1987 Vol 11. pp 435-4s. FANI IS A. SLEZAK z. On the possibility of reinnervation of total lesions of the brachial plexus by intercostoplexual anastomosis. Cesk Neurol 1965; Z&412-8. FRltDMANA,NUNLEY,,GOLDMANRD,OAKESWJ.GOLDIL, ~RBANIAK JR. Nerve transposition for the restoration of elbow flexion following brachial plexus avulsion injuries. J Neurosurg 1990; 72:59-64. NAKAKAS A. Thoughts on neurotization or nerve transfers in irreparable nerve lesions. In: TERZIS J fed): Clinics in Plastic Surgery. Philadelphi~Londo~Toronto: WB Saunders Co, 1984 Vol 11,pp 153-9. NARAKAS A, HENTZ VR. Neurotization in brachial plexus injuries. Indication and results. Clin Orthop Rel Res 198X; 237:43-56. MAN
H. Intercostal nerve transfer into the musculocutaneus nerve. In: Surgical Disorders of the Peripheral Nerves. Edingburgh: Churchill Livingstone. 1972. AGUAYO AJ. Axonal regeneration from injured neurons in the adult mammalian central nervous system. In: Cotman CW. ed. Synaptic plasticity. New-York: Guilford Press, 1985, pp 457-M. UASGD. Neural transplantation in the spinal cord of the adult mammal. In: Kao CC, Bunge RP. Reier PJ. eds. Spinal cord reconstruction. New-York: Raven Press, 1983. pp 367-96. H~Rv~~T~~,P~~oT-DE~HA~~ESS~NE~*.MIRAJC. Reinnervation fonctionelle d’un muscle squelettique du rat adulte au moyen d’un greffon de nerf pCriph&ique introduit dans la motlle kpiniere par voie dorsale. C.r. hebd. Stanc Acad Sci Paris 1987; 304:143-S. KAO CC,CHANG LW,BI.OODWORTH JRJMR. The mechanism of spinal cord cavitation following spinal cord transection. Part III J Neurosurg 1977: 46:757-66. vOOR.MOLEN JHC, DE BEER Fc. MARANIE. THOMEER RTWM.Spinal cord regeneration: an experimental study in cats. In: Cohadon F. Lobo Antunes J, eds. Recovery of function in the nervous system. Padova: Liviana Press. 1988:lWlS. RCITKA JT. APODACA ci, STERN R. ROSENBIJM M. The extracellular matrix of the central and peripheral nervous system: structure and function. J Neurosurg 1988; 69: 155-70. BUNGE RP. BUNGE M13. Interrelationship between Schwann cell function and extracellular matrix production. Trends Neurosci 1983; 6:499-X)5. SAVIOT. SCHWAB ME. Rat CNS white matter. but not gray matter. is nonpermissive for neuronal cell adhesion and fiber outgrowth. J Neurosci 1989: 9:1126-33. CAKLSTEDT T. Regrowth of anastomosed ventral root nerve fibers in the dorsal root of rats. Brain Res 1983; 272: 162-5. C‘ULLHtlMS.cARLSTEDTT.LlNDAH, RlSLlNGM,ULFHAKE B. Motoneurons reinnervate skeletal muscle after ventral root implantation into the spinal cord of the cat. Neurosci 1989; 29; 3:725-33. SEDDON
I1
Thomeer”
Introduction Summary
A lesion to the brachial plexus usually leads to a disabling condition, in particular when it affects the dominant arm. The vast majority of these lesions is caused by road traffic accidents and particularly involves high-kinetic motor vehicle traumata in young males“‘. Other mechanical lesions result from birth injury (‘obstetrical pal~y’)‘-~,stab wounds, and surgical errors. Moreover, plexopathy can be due to a cervical rib, neural tumors, carcinomatous infiltration and radiotherapy’-~.l~‘-l~. Finally, although aetiologically indefinite, neuralgic amyotrophy is a kind of plexopathy”. Seriously wounded motorcycle or moped victims survive more often since the wearing of crash helmets has become compulsory in most European countries. Associated life threatening injuries may initially overshadow a brachial plexus lesion. The elective treatment of a traumatic brachial plexus lesion presents a complex medical, surgical and rehabilitation problem. Functional rehabilitation of the patient has substantial social and economic impact. Anatomy The brachiat plexus is usually constituted by the spinal nerves (roots) C5 to Thl (Fig. 1). In the supraclavicular area these roots join to form * Lkpartment of Neurosurgery,
Despite technical advances, the ability to restore function following severe brachial plexus traction lesions is limited. Major problems hampering good results are the inability to recognize corresponding fascicles in case of a large nerve gap and the lack of a proximal nerve stump in root avulsions. This article discusses the diagnosis and treatment of such injuries in combination with research in this field. Key words: brachial plexus lesion - regeneration - nerve transplantation.
three trunks: C5 and C6 join to form the superior, C7 continues in the middle, and C8 and Thl join to form the inferior trunk. Retrociavicularly the ventral divisions of the superior trunk and middle trunk constitute the lateral fascicle, which divides in the subpectoral space in the musculocutaneus nerve and the lateral root of median nerve. The medial fascicle is the extension of the ventral division of the inferior trunk. This fascicle divides into the medial root of the median nerve and the ulnar nerve. The dorsal fascicle is constituted from the dorsal divisions of all three primary trunks. Running dorsal to the subclavian-axillary artery, its splits up in the axillary and the radial nerve.
University State Hospital, The Netheriunds
Addres for correspondence und reprint requests: Profl Dr. R. T. W. M. Thornear, Hospitul. P. 0. Box 9600, 2300 RC Leiden, The Netherlands Accepted 17-12-90 c’lin Neuro/ Neurosrrrg I99I.
Vol. 9.7-I
Dept. of Neurosurger_v,University State
N. phrenicus N. dorsalis scapulae _.
N. suprascapularis
N. thoracicus
longus
N. mus~ulo~utaneus
N. cut. brachii med. N. cut. antebrachii N. medianus
med.
/ N. ulnaris
Fig. 1 Anatomy of brachial plexus. TS: superior trunk, TM: middle trunk, TI: inferior trunk, FL: lateral fasicle, FP: posterior fascicle, FM: medial fascicle.
Over its entire course, nerves to the shoulder muscles leave the plexus. One must be aware that variations in the anatomy of the brachial plexus can exist, which hampers the clinical efforts to localize the site of a lesion.
Traumatic brachial plexus injury may be caused by penetration, compression or traction. Penetration can occur by sharp objects such as knife and glass, or by bullet. Stab wounds and iatrogenic lesions produce sharp tissue lesions, in which the transected nerves can be easily identified and re-united. Immediate neurosurgical repair favors anatomical reconstruction with optimal coaptation of the corresponding fascicles. Shot wounds initially produce a far more serious functional deficit than would be expected on the basis of the mechanical lesion of the bullet alone. This is due to shock wave distortion. After a lapse of time spontaneous recovery from the latter will clarify the site and 4
extent of the lesion produced by the bullet itself”‘. Compression injury occurs between the clavicle and the first or second rib, when an external force presses the clavicle down. This kind of lesion most frequently occurs in combination with an upper root traction injury which can be understood from the mechanism of the trauma14. Root tension varies with the position of the arm. Widening of the angle between neck and shoulder with a pendulant arm exerts greatest traction on roots (2.5and C6. Lateral abduction of the arm puts all roots under stress, but C7 most. With the arm in elevated position, the roots C8 and Thf. are under greatest traction. If traction force is excessive, all roots might become avulsed from the spinal cord, regardless of the position of the arm. The first mentionned mechanism of injury, depression of the shoulder with a pendulant arm, occurs most frequently. When a moped hits an obstacle, the patient is launched from it to crash down into the road, his shoulder and his
head hitting the ground resulting in a forceful widening of the angle between the neck and shoulder’“. The commonest mechanism of obstetrical plexus injury occurs to the upper roots both in vertex delivery when shoulder dystocia necessitates excessive lateral flexion of the neck, as well as in breech’ birth during delivery of the arms or the aftercoming head. The majority of lower plexus lesions occurs during face presentation with hyperextension of the cervical spine’. Haftek” studied the sequential phenomena resulting from progressive stretch on a peripheral nerve (Fig. 2). First. the nerve looses its undulating aspect, the fascicles and the nerve become straight. Stronger tension reduces the cross-sectional area within the epineurium, causing an increase in intrafascicular pressure, ischemia due to capillary/arteriolar compression. myelin disruption and in places axonal interruption (axonotmesis). Subsequently, at this point the elastic limit of the stretched nerve has been reached and the epineurium ruptures. Further elongation produces perineurial rupture. Only a slight further increase in traction force is needed for all axons to rupture, including the endoneurium and basement membranes. This finally leads to complete rupture of the nerve. In accordance with the increasing severity, Sunderland” proposed a clinical classification consisting of five degrees, the first degree being a short lasting loss of conduction of the axons, while the fifth degree denotes a total loss of continuity of the nerve. In clinical practice, however. the functional classification of Sed-
gr
traction
don16, neurapraxia, axonotmesis and neurotmesis, is of more practical value. Traction at the brachial plexus exerts forces also on the nerve roots. The nerve root-ganglion complex is laterally secured to the meninges and only both upper spinal nerves (C5 and C6) have a protective fibrous attachment of their epineurium to the transverse process”. If this fibrous attachment holds on severe traction, the nerve ruptures intra- or extraforaminarly. With the failure or abscence (C8 and Thl) of this protective anchor, the nerve root complex with its meningeal sleeve is pulled laterally through the pertinent intervertebral foramen, the dura tears, and the tensed fila radicularia avulse at their weakest point, viz. their attachment to the cord. Traction injuries to the brachial plexus may result in widespread lesions, combining root avulsion with lesions of the extravertebral parts of the plexus. Thus root avulsions do not produce a pure supraganglionic lesion, because tensile forces cause a combined pre- and postganglionic lesion. Clinically, there might be loss of axon reflexes in the presence of root avulsion. Clinical assessment History
The nature of the trauma is important to determine the severity of the lesion and its chance of spontaneous recovery. In traction injuries, motorcycle accidents are likely to produce severe lesions as high kinetic energy is invariably transferred, while e.g. shoulder luxation due to a
load epineurial rupture
200
-
1” stage --
cm elongation Fig. 2 Three stages during nerve stretching according to Haftek (1970). See text.
perineurial rupture 5
Fig. 3 Chart of all muscles m-
-
nervated by the brachial plexus according Deburge’. arranged overlap);
d’AubignC vertically
thick
pass muscles one particular nerve.
-----.
and
The myotomes
-
are
(note
lines enconrinnervated
by -_-___
peripheral TER
MIN
BRACHIALIS
TRICEPS ECR
M2
trivial fall in one’s home is likely to produce mild traction injury*‘. Severe pain in an anaesthetic arm is suggestive for root avulsions (de-afferentiation pain)‘*-**, General examination Brachial plexus palsies due to traffic accidents frequently present with associated lesions, both in the affected area (fractures of vertebral transverse processes, clavicle, scapula, humerus, rarely rupture of the subclavian artery) and/or at distance (cerebral contusion, fractures)23‘25. Neurological examination Motor function of all the muscles innervated by the plexus is tested. The power of each individual muscle is graded on the traditional O-5 scale. The findings are transcribed to the sophisticated chart (Fig. 3) designed by Merle d’Aubigne and Deburge”. This chart combines the information by which spinal nerves and by which peripheral nerve the individual muscle is innervated. It is most helpful in determining the site of the lesion. Sensory examination of the segmental or peripheral nerve innervation areas provides further information. However, due to overlap of neighbouring dermatomes the resulting sensory deficit might be smaller than expected. Sympathetic dysfunction presents itself with changes in colour, sweating and temperature of the affected extremity. The presence of Horner’s syndrome is indicative of root avulsion of
ECU
M3
M4
M5
at least Thl and therefore associated with poor prognosis for recovery of the total brachial plexus palsy. Finally, the Tinel-Hoffmann sign may provide useful information”. This sign refers to the radiating tingling sensation which is felt in its sensory innervation area on percussion of a nerve. If present, the sensation is evoked by highly sensitive regenerating axons, which have not yet become myelinated. The most distal point at which the sign is elicited determines the rate of growth of regenerating axons upon successive examinations. If the site of provocation by percussion does not progress with time and remains within the same place, this is the result of neuroma formation, which excludes spontaneous recovery. Electra-physiological examination Electromyography (EMG) provides information on the function of the muscle. It may reveal normal action potentials, or fibrillation which indicates denervation. or polyphasic action potentials in case of reinnervation. EMG is most useful in the assessment of brachial plexus lesions. It adds objective documentation of motor dysfunction, particularly of muscles that are hard to evaluate clinically. If, for example, exorotation in the shoulder is weak, this might be due to either inferior spinate or teres minor paresis or both; EMG examination resolves this dilemma as it will show denervation in only one or both muscles. Nerve conduction studies are of little value.
Due to Wallerian
degeneration
duction
fibers
of motor
Theoretically, (SNAP)
there is no con-
to paralysed
sensory
nerve
offer information
action
muscles. potentials
on the level of nerve
injury, since in preganglionic injury (i.e. root avulsion) T-cells in the ganglion remain in continuity with their peripheral axons, contrary to postganglionic lesions. In the first case SNAP’s are present
(although
ing) and in the second injuries, method
however, between
the
the patient
‘feels’ noth-
abolished.
In traction
discrimination
pre- and postganglionic
is as a rule hampered
due to simultaneous
by this lesion pres-
ence of both. Moreover segmental overlap might provide false positive informatior?~“. SEP (somatosensory evoked potentials) does not really add information, since recordings are positive in clinically non-anaesthetic and negative in anaesthetic dermatomes. Moreover, findings may be difficult to interprete. Peroperative SEP recordings, however, are useful in that they provide information on the sensory function of the directly stimulated spinal nerve. The clinical value of SNAP lesions remains debatable3”.
and SEP in plexus
Neuroradiological investigation Along with EMG, cervical myelography is indispensable for the analysis of brachial plexus traction injuries. The contrast dye is instillated by lateral puncture between Cl and C2. The roentgenograms offer information on the presence or abscence of the fila radicularia of all cervical roots and Thl (Fig. 4). In case of doubt, additional CT examination is helpful”‘. This method of investigation also enables one to differentiate between dorsal and ventral rootlets which is of particular interest in partial root avulsions. Meningeal tears result frequently in (pseudo) meningoceles which may accompany root avulsions. Nevertheless meningoceles may be present without avulsion of the pertinent root. At this stage MRI (Magnetic Resonance Imaging) does not yield a sufficiently high resolution to visualize spinal rootlets. Finally, X-ray examination of the diaphragm during in - and exspiration offers information on the involvement of C4 in traction injuries, because (part of) the phrenic nerve fascicles arise from this root.
Fig. 4 Cervical myelography showing abscence of fila radicularia of roots C7. C8 and Thl right. At Thl, a pseudomeningocele (avulsion cyst) is visible.
Neurosurgical treatment In sharp lesions, such as stab wounds, surgical repair has to be carried out immediately. Anatomical reconstruction of severed parts is relatively easy and functional results are correspondingly good. Traction injuries, however, generally present with extensive loss of function and initially it is impossible to predict which parts of the plexus will spontaneously recover and which not. Spontaneous recovery will occur in case of axonotmesis, but axonal outgrowth takes a long time in these cases (at least a year) due to the limited growth rate and the long distance to their targets. Waiting carries the risk of no recovery and after one year muscle atrophy has proceeded to such a degree that surgical nerve repair beyond that time can no more produce motor recovery. Early surgical exploration. however, exposes
a group of patients to a non-indicated operation as they were to recover spontaneously. Thus selection of patients for surgery is difficult”?. Factors influencing the decision include the severity of trauma, the findings on myelography, and possible early clinical (or EMG) signs of recovery, including the stationary or moving Tinel sign. It is generally agreed upon that, when signs of recovery fail to appear, surgical exploration should preferentially be carried out within three to five months after the injury”.“‘.‘3,‘J,‘3-‘h. The same holds for obstetrical palsies, which occur with an incidence of l-3 per 1000 living births3’. As 10 to 15 per cent of these babies have a poor functional prognosis”, attempts should be made to identify this group early in order to treat them surgically as wel17~n~37-3y. At the exploration, which is carried out with microsurgical techniques and the operating microscope, the final diagnosis on the site and extent of the lesion is made. Neuromata are excised and continuity of the injured parts is restored by bridging the gaps with nerve grafts. Most frequently, free grafts are used (autolobut de_ gous sural nerve) I 2 4 6,10,23.24.33.34.16.JO-4K, pending on the case other techniques such as free vascularized or pedicled nerve grafts are in current practice too4y-52.If the spinal nerves are found to be fibrosed, these nerves are first serially transected in a distal to proximally dissection until normal fascicles re-appear on the cross-sectional surface. The final nerve-tranch can be examined intraoperatively on frozen sections to ascertain the presence of myelin. Intraoperative nerve recording is also used”“. If one or more spinal nerves are suited for transplantation, a plan for reconstruction is made. Connection to its distal counterparts is one feasible option but, in case e.g. only C5 is available and all other roots avulsed, bypassing of the whole plexus by connecting C5 to the musculocutaneus nerve is preferable (Fig. 5). In the latter case (a flail arm), it is better to restore one function (elbow flexion) well, instead of dispersing the axons over a major part of the plexus which would inevitably fail to render functional results. Priorities in repair are elbow flexion, wrist and finger flexion with restoration of protective median sensation and shoulder control. 8
lat. ff
0C8 OTI
N. musculocutaneus
N. mediinus
Fig. 5 Transplantation of C5 to the lateral fascicle in case of root avulsion C6 through Thl
Except for intraplexal reconstructions, extraintraplexal nerve transfers can restore (a part of) the function lost in case of root avulsionss3-60. Among these are the accessory-suprascapular transfer (shoulder abduction) and intercostalmusculocutaneous transfer. The latter patients learn to keep their reinnervated biceps muscle strained independent of respiration57. In planning a neurosurgical reconstructive procedure, the surgeon should be aware of the plastic-orthopedic possibilities for muscle-tendon transposition and arthrodesis. It needs no saying that analysis and nerve repair are only a part of the whole medical and social attendance of these badly handicapped patients. Results of reconstructive brachial plexus surgery are hard to evaluate. Direct repair after sharp transection yields more or less the same results as in peripheral nerve repair, but the majority of these lesions consists of traction injuries which carries worse results due to a variety of reasons. Moreover it is hardly impossible to constitute comparable groups of patients for evaluation, as the severity and extent of the neural trauma in traction injuries differs from patient to patient. However, as recent literature teaches, it is obvious that results of surgical repair are far better than conservative treatment, provided the intervention has been carried out at the appropriate time.
In order to further improve the results of reconstructive brachial plexus surgery two major problems have to be solved, which can only be accomplished by laboratory research. The first and foremost is the problem of matching. Due to intermingling, the funicular pattern of the cross sectional surface of a nerve differs from place to place, even over short distances. The ideal in nerve grafting, viz. to restore continuity of corresponding funiculi, is difficult to achieve for this reason. Although the pattern of bundle-groups changes with short distances, their axial locaiisation remains constant for some longer distances”‘. Thus it is possible to re-connect fibres of the same group over short gaps, if one maintains correct axial alignment, which implies that the graft is apposed to the same quadrant of proximal and distal nerve stump. However, this does not hold for long distances. Sometimes gaps of 10 cm or more have to be bridged (Fig. 6). In these cases, it would be of great help if at least discrimination of motor and sensory bundles were possible in order to connect motor to motor and sensory to sensory fibers. Today, there is no such a method available. Theoretically there must be a biochemical difference between motoric and sensory fibers. It would really be a breakthrough in peripheral nerve surgery if a discriminatory staining method became available. This method should preferentially be applicable to both proximal (vital) and distal (degenerated) nerve stumps and moreover results should be available per-operatively. The second major problem concerns the root avulsions. Is there a chance for regeneration after reimplantation of the root in the cord? In contradistinction to what is noted in the peripheral nervous system (PNS), axonal re-
PROBLEM
OF MAfCHlNG
_
0
;? -tIIY.z f
l
0
Fig. 6 Note the differences of the fascicular pattern in the cross-sectional areas of both stumps in case of a nerve gap.
growth after CNS injury is poor, though elongation of spinal cord pathways in mammals after transection and grafting with peripheral nerves has been demonstrated~‘.~. In spite of this, restoration of function has never been achieved. Probably, there are crucial differences in the local tissue microenvironment of CNS and PNS. The role of extracellular matrix (ECM) macromolecules in axonal regeneration is subject to neurobiological research%. A properly synthesized ECM seems essential in guiding neuronal outgrowth. In the severed PNS, the linear organization of ECM tubes in the distal part of the nerve enables axonal regrowth”. Because of the paucity of similar ECM materials in the CNS, no such framework is available to assist in the process of axonal outgrowth, which might explain the failure of CNS to regenerate. Savio and Schwab”’ investigated the substrate properties of adult mammalian nervous tissue using frozen sections on which neuronal ceils from e.g. dorsal root ganglia, were cultured. The results showed that CNS white matter has a dramatic nonpermissive effect on cell adhesion and fiber outgrowth, in contrast to gray matter which allowed cell adhesion and neurite elongation. This inhibitory property of oiigodendroglia and CNS myelin was significantly reduced by an antibody administration against membrane proteins present on the surface of these myelin-forming cells. In vivo experiments showed the same hostility of CNS white matter. Carlstedt” anastomosed ventral rootlets to the ipsilateral dorsal root. Regrowth of ventral axons into the dorsal rootlets occurred, but only in its PNS part. Fibers ended at the PNS-CNS border. Entrance of the CNS might have been prohibited by the same hostile factors in the white matter as described by Savio et al”. Axons of spinal motoneurons in the PNS have the capacity of regeneration. The question is if the same capacity remains present if the lesion is inflicted to the CNS segment of these axons, as is the case in root avulsion. Does the cell body survive such a proximal lesion and, if so, under what condition could it exert its presumed regenerative capacity. Outgrowth of fibers from the CNS into the PNS has recently been reportedh3.‘“. The interpretation of the findings however is still puzz9
ling. Nevertheless, research in this field seems promising and is very important from a clinical point of view. Acknowledgments The author is indebted to Mrs. W.J. Ouwehand for typing the manuscript and Mr. G.J. van der Giessen for the photography.
References NAKAKAS A. Indications et resultats du traitement chirurgical direct dans les lesions par elongation du plexus brachial. Rev Chir Orthop 1977; 63:44-54. NARAKAS A. Surgical treatment of traction injuriesof the brachial plexus. Clin Orthop 1978; 133:71-90. NARAKAS A. Neurosurgical approach to brachial plexus lesions. In: Het fraumatische letsei van de plexus brachialis. Boerhaave Committee Leiden, 1982. NARAKAS A. Pathomechanics, diagnosis and surgical treatment of supraclavicular brachial plexus injuries. Ned Tijdschr Geneeskd 1986; 130:1967-8. ALNOT JY, JOLLY A, FROT 8. Traitement direct des lesions nerveuses dans les paralysies traumatiques du plexus brachial chez I’adulte. Intern Orthop 1981; 5:151-68. SEDEL L. The results of surgical repair of brachial plexus injuries. J. Bone Joint Surg 1982; 64B: 54. CXLBERTA,KHOURI N,CARLIOZH. Explorationchirurgitale du plexus brachial dans le paralysie obstetricale. Rev chir Orthop 1980; 66:33-42. TASSIN JL. Paralysies obstttricales du plexus brachial. These, Universite Paris VII 1983. BROWN KLB. Review of obstetrical palsies. Nonoperative treatment. In: TERZIS I (ed): Clinics in Plastic Surgery. Philadelphia/London/Toronto: WB Saunders Co, 1984 Vol 11, pp 181-7. LEFFEKT RD. Brachial plexus injuries. New York: Churchill Livingstone, 1985. LUSKMD, KLINEDG,GARCIA CA. Tumors ofthebrachial plexus. Neurosurg 1987; 21:439-53. AMPIL FL. Radiotherapy for carcinomatous brachial plexopathy. Cancer 1985; 56:2185-S. PARSONAGE MJ, TURNER JWA. Neuralgic amyotrophy. Lancet 1957; 209-12. SUNDERLAND s. Nerves and nerve injuries. 2nd ed. Edinburgh: Churchill Livingstone, 1978. HAFTEK J. Stretch injury of peripheral nerve, acute effects of stretching on rabbit nerve. J Bone Joint Surg 1970; 52B:534-65. SEDDON HJ. Three types of nerve injury. Brain 1943; 66:237. COENE LNJEM. Axillary nerve lesions and associated injuries. Thesis: Leiden 1985 pp 63-78. BONNARD c, NARAKAS A. Syndromes douloureux et lesions traumatiques du plexus brachial. Helv Chir Acta 1985; 52:621-7. BRUXELLEJ,TRAVERS V,THIEBAUTJB. Occurrence and treatment of pain after brachial plexus injury. Clin Orthop Rel Res 1988; 237:87-95. THOMAS DGT, SHEEHY JPR. Dorsal root entry zone lesions (Nashold’s procedure) for pain relief following brachial plexus avulsion. J Neurol Neurosurg Psychiatry 1983; 46:924-8.
10
/OKUH i>s. NASHOLD HS. cu~tt WA.Avulsion ot the hrachial plexus. A review with implications on the therap! of intractable pain. Surg Nemo1 1974; 2:347-T ;. NAKAKAS A. The surgical treatment of traumatic brachial plexus lesions. Intern Surg 1980: 65521-7 UAKAKAS A. The treatment of hrachial plexus injuries. Inter Orthop 1985: 9:29-X. NARAKAS A. Plexus brachialis und naheliegende periphere Nervenverletzungen bei Wierbelfrakturen und andere Traumen der Halswirhelsaule. Orthopade 1987: 16:81-6. M~RLED‘AUBIGNE KM.D~BL:RG~ A. Etiologie, eVOuItiOII et pronostique des paralysies traumatiques du plexus brachial. Rev Chir Orthop 1967; 53:23. LANDI A, ~OPPLANU SA. Value of the Tine1 sign in brachial plexus lesions. Ann R Co11Surg Engl 1979; 61:470-l. BONNEY G. C~II.LIAT~ RW. Sensory nerve conduction after traction injuries of the brachial plexus. Proc R Sot med 1958; 51:365-7. LANDI A,~OPELAND SA.WYNN PARRY CII,JONESSJ. The role of somatosensory evoked potentials and nerve conduction studies in the surgical management of brachial plexus injuries. J Bone Joint Surg 1980; 62B:492-5. SYNEK v~, (‘OWAN JC. Somatosensory evoked potentials in patients with supraclavicular brachial plexus injuries. Neurology 1982; 32: 1347-52. MARSHALL Rw, DE WILVA RDD. Computerised axial tomography in traction injuries of the brachial plexus. J Bone Joint Surg 1986; 68B:734-8. JASPEKS KBM. Medical decision support. An approach in the domain of brachial plexus injuries. Thesis: Delft 1990. KLINE DG, HACKETT ER, HAPPEL LH. Surgery for lesions of the brachial plexus. Arch Neural 1986; 43: 170-81. MERLE M. La chirurgie directe du plexus brachial traumatique. Rev Readapt Fonct Sot 1980; 6:45-52. MILLES H. Trauma involving the brachial plexus. In: Omer, Spinner (eds): Management of peripheral nerve problems. Philadelphia/London/Toronto: WB Saunders Co, 1980, pp 548-68. SEDEL L. The management of supraclavicular (plexus) lesions. In: TERZIS J (ed): Microreconstruction of Nerve Injuries. Philadelphia/London/Toronto: Saunders WB co. 1987. KAWAMATAH,MASADAK,
ISUYUGUCHI
Y,KAWAIH,ONO
Early microsurgical reconstruction in birth palsy. Clin Orthop Rel Res 1987; 215:233-42. SOLONEN KA. KY~PPY s, 'TELARANTA T. Early reconstruction of the brachial plexus after birth injuries. Acta Orthop Scan 1980; 51:365-9. SOLONEN KA,TELERANTAT,RYoPPYS. Early IeCOIISIrUCIion of birth injuries of the brachial plexus. J Pediatr Orthop 1981; 1:367-7(X AI I.IEU Y. Exploration et traitement direct des lesions nerveuses dans les paralysies traumatique par Clongation du plexus brachial chez I‘adulte. Rev Chir Orthop 1977; 63: 107-22. JAMIESON A, HUC~HES s. The role of surgery in the management of closed injuries to the brachial plexus. Clin Orthop 1980; 147:210-5. KLINE DG, JUDI~E DJ. Operative management of selected brachial plexus lesions. J Neurosurg 1983; 58:631-49. MILLESI H. Surgical management of brachial plexus injuries. J. Hand Surg 1977; 2:367-79. MILLESI H. Brachial plexus injuries: nerve grafting. Clin Orthop Rel Res 1988; 237:36-42. K, TADA
K.
NAR-ZKAS A. Brachial plexus surgery. Orthop Clin North Am 1981; 12:303-23. SEDI:L L. Repair of severe traction lesions of the brachial plexus. Clin Orthop Rel Res 1988; 237:62-6. SOLONEN KA, ~ASTAMAKIM, STROMB. Surgery Of the brachial plexus. Acra Orthop Scan 1984; .55:436-40. YEOMAN PM. SEDDON HJ. Brachial plexus injuries. treatment of the flail arm. J Bone Joint Surg 1961; 43B:493. BIRCH
R. KLINKERSTON
M,BONNEY
G,JAMIESON
AM.EX-
perience with the free vascularized ulnar nerve graft in repair of supraclaviculair lesions of the brachial plexus. Clin Orthop Rel Res 1988: 237:96-104. NARAKAS A. Personal communication 1985. STRANGEFGSC’.An operation for nerve pedicle grafting: Preliminary communication. Br J Surg 1947; 34:423. TAYLOR GI. HAM FJ. The free vascularised nerve graft: A further experimental and clinical application of microvascular techniques. Plast Reconstr Surg 1976; 57:413. ALLIEU Y. PRI~AT ~hf. BoNNEL F. Paralysis in rootavulsion of the brachial plexus. Neurotization by the spinal accessory nerve. In: TERZIS I. (ed): Clinics in Plastic Surgery. Philadelphia/London/Toronto: WB Saunders Co. 1984, Vol 11, pp 113-6. BRLJY~LLI G. Neurotization of avulsed roots of the brachial plexus by means of anterior nerves of the cervical plexus. Int J Microsurg 1980: 255-S. HRLINELLI G. Neurotization of avulsed rootsof the brachial plexus by means of anterior nerves of the cervical plexus. In: TERZIS J (ed): Microreconstruction of Nerve Injuries. Philadelphia/London/Toronto: Saunders WB Co, 1987 Vol 11. pp 435-4s. FANI IS A. SLEZAK z. On the possibility of reinnervation of total lesions of the brachial plexus by intercostoplexual anastomosis. Cesk Neurol 1965; Z&412-8. FRltDMANA,NUNLEY,,GOLDMANRD,OAKESWJ.GOLDIL, ~RBANIAK JR. Nerve transposition for the restoration of elbow flexion following brachial plexus avulsion injuries. J Neurosurg 1990; 72:59-64. NAKAKAS A. Thoughts on neurotization or nerve transfers in irreparable nerve lesions. In: TERZIS J fed): Clinics in Plastic Surgery. Philadelphi~Londo~Toronto: WB Saunders Co, 1984 Vol 11,pp 153-9. NARAKAS A, HENTZ VR. Neurotization in brachial plexus injuries. Indication and results. Clin Orthop Rel Res 198X; 237:43-56. MAN
H. Intercostal nerve transfer into the musculocutaneus nerve. In: Surgical Disorders of the Peripheral Nerves. Edingburgh: Churchill Livingstone. 1972. AGUAYO AJ. Axonal regeneration from injured neurons in the adult mammalian central nervous system. In: Cotman CW. ed. Synaptic plasticity. New-York: Guilford Press, 1985, pp 457-M. UASGD. Neural transplantation in the spinal cord of the adult mammal. In: Kao CC, Bunge RP. Reier PJ. eds. Spinal cord reconstruction. New-York: Raven Press, 1983. pp 367-96. H~Rv~~T~~,P~~oT-DE~HA~~ESS~NE~*.MIRAJC. Reinnervation fonctionelle d’un muscle squelettique du rat adulte au moyen d’un greffon de nerf pCriph&ique introduit dans la motlle kpiniere par voie dorsale. C.r. hebd. Stanc Acad Sci Paris 1987; 304:143-S. KAO CC,CHANG LW,BI.OODWORTH JRJMR. The mechanism of spinal cord cavitation following spinal cord transection. Part III J Neurosurg 1977: 46:757-66. vOOR.MOLEN JHC, DE BEER Fc. MARANIE. THOMEER RTWM.Spinal cord regeneration: an experimental study in cats. In: Cohadon F. Lobo Antunes J, eds. Recovery of function in the nervous system. Padova: Liviana Press. 1988:lWlS. RCITKA JT. APODACA ci, STERN R. ROSENBIJM M. The extracellular matrix of the central and peripheral nervous system: structure and function. J Neurosurg 1988; 69: 155-70. BUNGE RP. BUNGE M13. Interrelationship between Schwann cell function and extracellular matrix production. Trends Neurosci 1983; 6:499-X)5. SAVIOT. SCHWAB ME. Rat CNS white matter. but not gray matter. is nonpermissive for neuronal cell adhesion and fiber outgrowth. J Neurosci 1989: 9:1126-33. CAKLSTEDT T. Regrowth of anastomosed ventral root nerve fibers in the dorsal root of rats. Brain Res 1983; 272: 162-5. C‘ULLHtlMS.cARLSTEDTT.LlNDAH, RlSLlNGM,ULFHAKE B. Motoneurons reinnervate skeletal muscle after ventral root implantation into the spinal cord of the cat. Neurosci 1989; 29; 3:725-33. SEDDON
I1