The Journal of Bone and Joint Surgery 81:20-28 (1999)
© 1999 The Journal of Bone and Joint Surgery, Inc.
Complete Traumatic Brachial Plexus Palsy. Treatment and Outcome After Repair*
VINCENT BENTOLILA, M.D. ,
REMY NIZARD, M.D. ,
PASCAL BIZOT, M.D. and
LAURENT SEDEL, M.D. , PARIS, FRANCE
Investigation performed at Service de Chirurgie Orthopédique et Traumatologique, Hôpital Lariboisière, Paris
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Abstract
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Seventy-eight patients who had a complete brachial plexus palsy caused by a stretching injury were operated on by the same surgeon between January 1980 and December 1991. The aim of the operative intervention was to obtain the best functional result, including at the level of the hand, that was possible in view of the initial lesions and the intraoperative findings. Therefore, the treatment strategy included not only nerve repair with grafting (124 grafts) or nerve transfer (twenty-seven transfers) but also palliative procedures, the latter of which sometimes were performed several years later.
Sixty-three patients were evaluated by an independent observer at least three years postoperatively. The results associated with each type of lesion and each type of nerve repair were assessed according to the function of the muscles that were innervated by the recipient nerve. Six patients had a neurolysis only. The remaining fifty-seven patients had grafts or nerve transfers to repair the biceps. Thirty-six of the fifty-seven received a rating of 3+ or more (meaning that the patient was able to flex the elbow repeatedly); the remaining twenty-one received a rating of 3 or less (meaning that the patient was able to flex the elbow only once or not at all), which we considered unsatisfactory. The function of the triceps recovered after eleven of thirty-one procedures that were performed to restore that nerve; that of the extensor carpi radialis, after five of thirty-one procedures; that of the flexor carpi radialis, after six of thirty-one procedures; and that of the flexor digitorum, after four of thirty-one procedures.
A statistical analysis revealed that an operative delay of less than six months was a significant factor with respect to recovery of the function of the biceps (p = 0.003). The thirty-nine grafts that were sutured onto the lateral or posterior cord produced better results than did the thirty-six that were sutured onto the distal branches (the musculocutaneous and radial nerves); however, with the numbers available, this difference was not found to be significant (p = 0.08).
Eleven patients had a successful result (a rating of 3+ or more) and eight, a fair or poor result, with respect to recovery of biceps function after transfer of the spinal accessory nerve to the musculocutaneous nerve. Overall, twenty-nine patients had relief of pain postoperatively. Sixteen patients had grade-3 pain preoperatively compared with only three after the operation. According to a self-rating scale, twenty-five patients were satisfied with the overall result, sixteen were fairly satisfied, and twenty-two were dissatisfied.
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Introduction
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Complete traumatic brachial plexus palsy is a very severe condition that usually affects young adults and leaves them markedly handicapped. It has been our goal, for more than twenty years, to improve the clinical outcome of treatment by using all available modalities, such as microsurgical nerve repair, nerve transfer, and palliative procedures. In 1982, one of us (L. S.) reported the results of operative management of thirty-two patients who had a complete brachial plexus palsy21.
Since the time of the original report, we slightly modified our strategy by using accessory nerve transfers more frequently and by trying to increase the probability of restoring some function at the level of the hand. To obtain such function, we used a technique that differs in two ways from those reported previously3,18. First, we did not use nerve-root grafts or nerve transfers for the proximal nerves going to the shoulder girdle, in order to reserve the axons for more distal branches. Second, we prioritized the functions that were desired, with flexion of the elbow being the most important, followed by extension of the wrist, flexion of the fingers, and abduction of the shoulder23. The treatment included palliative procedures, such as shoulder arthrodesis, which were scheduled at the initial planning stage. During the nerve repair, we attempted to attach the grafts as distally as possible in order to obtain better muscle strength or, alternately, we attempted to reduce the length of the graft by attaching it to the lateral or posterior cord. This choice was not related to the type of lesion but rather to the preference of the surgeon, which, in the earlier period of the study, was to attach the grafts distally and, in the later period, was to attach them proximally.
The goals of the current study were to determine whether it was sometimes possible to restore the function of the hand; to compare the benefits of attaching the grafts to the distal branches or to the cords; to compare the results of accessory nerve transfer and intercostal nerve transfer; and to assess the functional improvement, satisfaction of the patient, and relief of pain after the operative intervention. The study consisted of a consecutive series of patients who had a complete brachial plexus palsy and had been operated on between January 1980 and December 1991. All patients were evaluated by an independent observer (V. B.) after a minimum duration of follow-up of three years. These patients were not included in the previous report21.
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Materials and Methods
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Since 1972, we have performed more than 500 brachial plexus repairs and various associated secondary procedures. Between 1980 and 1991, 205 consecutive patients who had had a recent brachial plexus injury were operated on by the same surgeon (L. S.). The first criterion for inclusion in the current study was a complete traumatic brachial plexus palsy at the time of the procedure. One hundred and eleven patients who had a partial palsy, twelve who had a palsy that was caused by radiation therapy, and four who had a lesion secondary to a tumor were excluded. This left seventy-eight patients, all of whom met several additional criteria. First, preoperative testing had shown that all of the muscles of the arm, forearm, and hand were grade 0 (a complete palsy) according to the muscle-grading system of Seddon20. A complete palsy was defined as total motor and sensory loss from the fifth cervical to the first thoracic nerve, although, in many patients, the muscles of the shoulder girdle, such as the trapezius, levator scapulae, rhomboids, and serratus anterior, remained partially or fully active, as did the diaphragm. Second, the operative report had confirmed the presence of all lesions. Third, preoperative electromyography had shown complete denervation of the muscles supplied by the fifth cervical to the first thoracic nerve root, on at least two occasions20.
The study group consisted of five female patients and seventy-three male patients. The mean age at the time of the operation was twenty-three years (range, ten to fifty-two years). All patients had been referred from other institutions.
A motor-vehicle accident had caused the palsy in seventy-five patients, fifty-eight of whom had been in a motorcycle accident. The remaining three patients had sustained a sports-related injury.
Seventy patients had associated injuries, including thirty-seven injuries of the shoulder girdle and thirty-eight of the ipsilateral upper limb. Fifty-seven patients had had cranial trauma with loss of consciousness, and seventeen had been in a coma. Twenty-one patients had a severe arterial lesion (rupture or thrombosis of the main arterial trunk). No patient had acute ischemic symptoms, even though eleven patients had had an emergency vascular repair before the referral. (Six of these procedures had been successful, with recovery of the distal pulse, and five had not.)
Motor function of each muscle of the upper limb, including the shoulder muscles, was graded from 0 to 5 according to the muscle-grading system of Seddon20.
Sensitivity to light touch and to hot and cold was tested, as was stereognosis. The passive range of movement of each joint was noted. At the time of the preoperative clinical examination, all patients had an anesthetic hand. Eighteen patients had some evidence of sympathetic dystrophy, including edema, cyanosis, and skin problems. Fifty-seven patients had a Horner sign, and seventy-three had a positive Tinel sign in the supraclavicular area.
Pain was described in terms of its time of onset, site, radiation, and relief with use of drugs7,11. Grade 0 indicated no pain; grade 1, intermittent pain that often was related to the weather or the patient's emotional state; grade 2, severe pain; and grade 3, intolerable pain that was sufficient to awaken the patient from sleep and was not relieved by major analgesics21.
Each patient had electromyography on at least two occasions: at approximately the same time as the first consultation but at least three weeks after the injury, and before the operation. All patients had a cervical myelogram, postmyelographic computerized tomography, or magnetic resonance imaging, or a combination of these studies.
All patients had an operative procedure to assess and repair nerve lesions.
The mean delay (and standard deviation) between the injury and the operation was 5.4 ± 2.73 months (range, one to fifteen months). This delay was related to the time that had elapsed before the patient was referred to us.
Operative Technique
The details of the operative procedure have already been described elsewhere21,23. The operation was performed with the patient under general anesthesia; neuromuscular blocking agents such as curare, which would have prevented the stimulated muscles from contracting, were not used.
The incision must be large. Proximal to the clavicle it is L-shaped, with one limb parallel to the sternocleidomastoid muscle and the other parallel to the clavicle. The skin flap is raised carefully, and the external jugular vein is ligated. The sternocleidomastoid is retracted, and the dissection is continued into the prescalene area, where lymph nodes and fat are removed. The phrenic nerve is identified on the surface of the scalenus anterior and is followed proximally until it crosses the lateral aspect of that muscle. The fifth cervical nerve root is located precisely behind this point; the sixth cervical nerve root is more distal and medial, and its direction is less vertical; the seventh cervical nerve root is even more horizontal and is more posterior; and the eighth cervical and first thoracic nerve roots, which are more difficult to find, are situated even more posteriorly and medially.
The scalenus anterior is isolated and divided. The subclavian artery is retracted forward, and the dome of the pleura is retracted backward. The infraclavicular part of the incision follows the deltopectoral groove, dividing the pectoral muscles if necessary; sometimes the incision must be extended down the arm. The axillary artery is dissected, followed by the lateral, posterior, and medial cords of the brachial plexus, which may be difficult to identify. If the lesion is located immediately behind the clavicle, this bone may need to be divided (as was done in fifteen procedures); the clavicle is repaired with use of an AO plate at the end of the operation. Since the time of the initial series21, the operating time has decreased considerably, from eight to ten hours to four to six hours.
We used a supraclavicular and infraclavicular approach in seventy-five patients and a supraclavicular approach in three.
Types of Lesions
The lesions that were identified during the operative exploration were classified into seven types according to a modification of the criteria described by one of us (L. S.)21 (Table I). Our classification included only types I, IIA, IIB, IIC, IID, VA, and VI because they represent all types encountered in patients who have a total palsy.
With type-I lesions, five nerve roots are avulsed from the medulla; with type-IIA, four roots are avulsed and there is one postganglionic rupture; with type-IIB, three roots are avulsed and there are two postganglionic ruptures; with type-IIC, two roots are avulsed and there are three postganglionic ruptures; with type-IID, one root is avulsed and there are four postganglionic ruptures; with type-VA, there is rupture of the lateral, medial, and posterior cords; and with type-VI, the distal branches (the radial, axillary, median, ulnar, and musculocutaneous nerves) are involved.
Goals of the Operation
We believe that repair of the suprascapularis nerve is ineffective, and we prefer to use this nerve as a graft to repair a more distal branch. After good distal recovery has been achieved, a shoulder arthrodesis may be performed to restore stability. As stated previously, the first goal is to restore elbow flexion; the second, to restore wrist extension; the third, to restore finger flexion; and the fourth, to restore shoulder abduction23. Therefore, the first priority was to attach the graft to the musculocutaneous nerve or the lateral cord; the second, to attach the graft to the radial nerve after dissection and removal of the branch to the triceps or the posterior cord; the third, to attach the graft to the median nerve; and the fourth, to attach the graft to the axillary nerve. The operative strategy that was chosen was related to the type and extent of the lesion; the aspect of the proximal neuroma; and the number, quality, and length of the available grafts. The strategy also varied according to the time-period: initially, we attached more grafts to the distal nerves, and later, we connected more grafts to the cords.
When there was a complete avulsion of the nerve roots from the fifth cervical to the first thoracic level, a transfer of the spinal accessory nerve to the anterolateral aspect of the musculocutaneous nerve was carried out, either alone or in conjunction with a transfer of two or three intercostal nerves.
When there was a complete avulsion of all nerve roots except one (usually the fifth cervical nerve root, ruptured proximal to the clavicle), the nerve root with a postganglionic rupture was attached to the musculocutaneous nerve or the lateral cord. If the stump of the fifth cervical nerve root was of poor quality, a nerve transfer was carried out with use of the spinal accessory nerve to the musculocutaneous nerve, in order to reinforce the previous graft.
When there were three avulsed nerve roots and two ruptured ones (often the fifth and sixth cervical nerve roots), the fifth cervical nerve root was attached to the radial nerve after removal of the branch to the triceps or the posterior cord and the sixth cervical nerve root was attached to the musculocutaneous nerve or the lateral cord, depending on the lesion. If the proximal stump of the sixth cervical nerve root was of good quality, it was attached to the lateral cord; if it was of poor quality and the fifth cervical nerve root provided a stronger base, the latter was used for the same purpose.
An avulsion of two roots with three stumps available for grafting was rare. Finding a sufficient number of grafts to bridge the defects was the major problem in these patients. An osteotomy of the clavicle often made it possible to decrease the length of the graft as the sutures could be placed in immediate proximity to the proximal limit of the nerve lesion after section of the nerve in a zone of healthy tissue. The denervated ulnar nerve sometimes was used as a donor nerve.
Types of Nerve Repair
Three types of nerve repair were performed.
One hundred and thirteen nerve grafts were performed with use of the sural nerve, usually obtained from both sides by stripping between three or four incisions. Eleven other grafts included denervated ulnar nerve because a long defect had to be bridged. All grafting procedures were performed under the operating microscope with a magnification of between six and ten times. One or two 10-0 sutures ensured the fixation of both ends. Fibrin glue was not used.
Twenty-seven nerve transfers were performed with use of the spinal accessory nerve, with interposition of an interfascicular nerve graft. Four transfers were carried out with use of the intercostal nerves, but always in association with a transfer of the spinal accessory nerve.
Neurolysis was performed seven times, on stretched but apparently continuous nerve trunks.
Assessment of the Outcomes
There are many methods with which the results of brachial plexus repair can be assessed. In an effort to standardize the assessment, we evaluated the function of the muscles and the sensation in the areas supplied by the recipient nerve.
Motor function was evaluated on a scale ranging from 0 to 5 points, sensitivity was evaluated on a scale ranging from 0 to 3 points, and the active and passive ranges of motion were recorded. The patient's satisfaction with the result was rated on a 5-point scale (as very satisfied, satisfied, fairly satisfied, dissatisfied, or would not have the procedure again), and pain was rated on a scale ranging from 0 to 3 points.
Six types of grafts were used: those sutured to the musculocutaneous, radial, median, and axillary nerves, and those sutured to the lateral and posterior cords. A good result meant that at least one muscle supplied by the nerve graft was graded as 3+; a fair result, that recovery of muscular function was grade 3 or less; and a poor result, that there was no recovery.
The delay between the injury and the operative intervention, the length of the graft, the number of strands in the graft, the age of the patient at the time of the operation, the presence of vascular lesions, the type of nerve lesions, the presence of a proximal neuroma, and the origin of the graft were evaluated as prognostic factors. Quantitative data were evaluated with use of a Student t test, and qualitative data were evaluated with use of a chi-square test. A difference was considered to be significant if p was less than 0.05.
Pain and the functional outcome also were evaluated with respect to work activity. Because some patients had not only nerve repair but also palliative procedures, we included the results of both in the assessment. We also assessed the results with respect to three categories: satisfied (very pleased or pleased), fairly satisfied, and dissatisfied.
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Results
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Of the original seventy-eight patients, two had died, two had had an amputation, and eleven had been lost to follow-up. (Of the latter group, nine were from foreign countries or the French West Indies and were unable to return for examination.) The remaining sixty-three patients were examined by an independent observer (V. B.) who had not participated in the initial operative procedure. Of these patients, six had had a neurolysis only and fifty-seven had had a reconstructive procedure. Eighteen grafts were sutured onto the musculocutaneous nerve; eighteen, onto the radial nerve; twenty-six, onto the lateral cord; thirteen, onto the posterior cord; five, onto the median nerve; and three, onto the axillary nerve. The mean duration (and standard deviation) of follow-up was 10 ± 4 years (range, three to fifteen years).
As our repair strategy was based on the function that we chose to restore and not on the proximal stump that was available, the results of the grafting procedures will be discussed according to the recipient nerve.
Grafts to the Musculocutaneous Nerve
Of the eighteen grafts that were attached to the musculocutaneous nerve, eleven were obtained from a nerve root; two, from the lateral cord; and five, from a nerve root associated with a transfer of the spinal accessory nerve to the musculocutaneous nerve.
Ten grafts led to good recovery of the function of the biceps (a grade of 3+ or more) and eight, to poor recovery (a grade of 3 or less).
The delay between the accident and the intervention was the only significant prognostic factor that we could detect with the numbers available (p = 0.006); the longer the delay, the poorer the result (mean delay, 4.0 ± 1.52 months for the good results compared with 6.4 ± 1.81 months for the poor ones).
Grafts to the Lateral Cord
Of the twenty-six grafts that were attached to the lateral cord, twenty-two were obtained from a nerve root and four were obtained from a nerve root associated with a transfer of the spinal accessory nerve to the lateral cord.
Eighteen grafts resulted in good recovery of the function of the biceps and eight, in poor recovery. Five grafts led to good recovery of the function of the flexor carpi radialis and twenty, to poor recovery; the remaining graft was in a patient who had had a wrist arthrodesis elsewhere, before being included in this study. Four grafts led to good recovery of the function of the flexor digitorum and twenty-two, to poor recovery.
In this group, two prognostic factors were significant: the length of the graft (mean, 7.2 centimeters for the grafts associated with the good results compared with 9.6 centimeters for those associated with the poor ones; p = 0.04) and the delay between the accident and the intervention (mean, 4.2 months for the grafts associated with the good results compared with 6.5 months for those associated with the poor ones; p = 0.003).
Grafts to the Radial Nerve
Eighteen grafts were attached to the radial nerve. Five grafts led to good recovery of the function of the triceps and thirteen, to poor recovery. Two grafts resulted in good recovery of the function of the extensor carpi radialis and fifteen, in poor recovery; the remaining graft was in a patient who had had an arthrodesis of the wrist elsewhere. All grafting procedures had a poor result with respect to recovery of the function of the extensor digitorum.
The number of strands that were used for the graft was a significant factor (mean, 3.8 ± 0.9 strands for the grafts associated with the good results compared with 2 ± 0.73 for those associated with the poor ones; p = 0.002).
Grafts to the Posterior Cord
Thirteen grafts were attached to the posterior cord. Six of the procedures had a good result with respect to recovery of the function of the triceps and seven, a poor result. Three grafts led to good recovery of the function of the extensor carpi radialis and ten, to poor recovery. With respect to recovery of the function of the extensor digitorum, one grafting procedure had a good result and twelve, a poor result. With respect to shoulder abduction, two grafting procedures had a good result and nine, a poor result; the two remaining grafts were in patients who had had a shoulder arthrodesis.
With the numbers available for study, we could not detect a significant prognostic factor for the success of this type of graft.
Grafts to the Median Nerve
Five grafts were attached to the median nerve. One graft resulted in good recovery of the function of the flexor carpi radialis and four, in poor recovery. No grafting procedure yielded a good result with respect to recovery of the function of the flexor digitorum.
Grafts to the Axillary Nerve
Three grafts were attached to the axillary nerve. Two resulted in good recovery of the function of the deltoid, and one was a failure.
Nerve Transfer
Nineteen transfers of the spinal accessory nerve to the musculocutaneous nerve were performed, either as an isolated operation (six) or in association with transfer of the intercostal nerves (four) or with a graft (nine), usually from the fifth cervical nerve root.
Five of the six isolated nerve transfers resulted in good recovery of the function of the biceps (a grade of 3+ or more). Of the four transfers associated with an intercostal nerve transfer, two yielded a good result and two did not. Of the nine nerve transfers that were reinforced by a graft from the fifth cervical nerve root, four were successful and five were not. In total, these nineteen transfers led to eleven good results and eight fair or poor results.
We performed two transfers of the spinal accessory nerve to the lateral cord, attempting to select the fibers that form the musculocutaneous nerve as the recipient fibers; this type of transfer was reinforced with a graft from the fifth cervical nerve root. The results of both procedures were good. Two other nerve transfers, performed on the upper trunk and the radial nerve, yielded a poor result.
Prognostic Factors for Recovery of Biceps Function
Flexion of the elbow was always the first function that we attempted to restore. In order to determine the prognostic factors with respect to recovery of the function of the biceps, we analyzed the results for fifty-seven patients; the remaining six had had a neurolysis only. All fifty-seven patients had had either a graft or a nerve transfer to the musculocutaneous nerve or the lateral cord. At the time of the most recent follow-up examination, there were thirty-six good results and twenty-one poor ones.
Using statistical analysis, we identified four significant prognostic factors: the delay between the accident and the intervention (mean, 4.3 months for the better results compared with 6.3 months for the unfavorable outcomes; p = 0.003), a previous operation on a vascular lesion (all patients who had had such an operation had a poor result, whereas all who had not had such an operation had a good result; p = 0.0007), the presence of vasomotor problems (p = 0.008) and a Horner sign (p = 0.05) at the time of the preoperative clinical examination (these factors were directly related to a poor result), and the presence of a neuroma on the proximal stump (this factor was directly related to a good result; p = 0.001).
With the number of patients available for study, we could not detect a significant relationship between the clinical outcome and the age of the patient, the side of the injury, a comatose state, the type of lesion, the presence of a lesion in the shoulder girdle, a lesion of the nerve supplying the serratus anterior, or an osteotomy of the clavicle performed as part of the operative intervention.
Sensitivity
All patients reported anesthesia of the hand before the operation. Thirty-six patients reported protective sensation in the thumb and the index and long fingers at the time of the most recent follow-up. Grafts that were attached to the lateral cord were associated with the highest rate of recovery (fifteen of twenty-six procedures) and were directly related to a favorable outcome with regard to recovery of the function of the biceps (p = 0.02). Therefore, protective sensation usually was restored if motor function was recovered; however, sensory discrimination was never achieved.
Pain
Before the operation, nine of the sixty-three patients had had no pain (grade 0); sixteen, grade-1 pain; twenty-two, grade-2 pain; and sixteen, grade-3 pain. After the operation, twelve patients had grade-0 pain, twenty-eight had grade-1 pain, twenty had grade-2 pain, and only three had grade-3 pain; these differences represent a significant improvement (p = 0.0005) and suggest that the operation produces an analgesic effect5. Moreover, the presence of vasomotor problems before the operation was directly related to the subsequent occurrence of pain (p = 0.04). Four patients had a Nashold procedure (a dorsal-nerve-root-entry rhizotomy) with use of microcoagulation18; two of these patients had a good result, and two had a result that was only temporarily good, with recurrence of the pain after six and twelve months.
Palliative Procedures
Recovery from a total palsy after the procedure requires an interval of two to three years. Palliative procedures should be undertaken only after this time-period has elapsed. When palliative intervention is being planned, considerations should include the overall result of the operation, the patient's needs and motivations, the degree of pain, and the condition of the upper limb.
For patients who have a complete palsy, the best ancillary procedures are arthrodesis, osteotomy, and tenodesis. Muscle transfer is ineffective because a muscle that has recovered after denervation is poor material for a transfer.
Six patients had a shoulder arthrodesis. All six had had an unstable shoulder, with grade-3 or 4 biceps function, after reinnervation. Before the arthrodesis, the serratus anterior and the trapezius were grade 5 and the deltoid, infraspinatus, and supraspinatus were grade 0. None of the patients had grade-3 pain. The mean delay between the nerve repair and the arthrodesis was 4.6 ± 2.24 years (range, 2.3 to 7.7 years). The mean duration of follow-up after the arthrodesis was 4.5 ± 2.63 years (range, two to ten years). The site of the arthrodesis healed in all six patients, at a mean of 3.5 months.
At the time of the most recent follow-up, all six patients had a good result, with grade-0 or 1 pain. The strength of elbow flexion showed a mean improvement of 0.75 grade, with five patients having grade-4+ biceps function and one having grade-5. All six patients could lift ten pounds (4.5 kilograms) and were satisfied with the result.
Three of the six patients had more than one palliative procedure. Two patients had a transfer of the triceps onto the biceps because of co-contractions. Before the transfer, both had had grade-4 triceps function and one had had grade-3 and the other had had grade-4 biceps function. At the most recent follow-up evaluation, both patients had a good result, with grade-4 biceps function. The third patient had four ancillary procedures, including an osteotomy of the radius to achieve pronation, an arthrodesis of the interphalangeal joint of the thumb, a tenodesis of the extensor digitorum, and a wrist arthrodesis (performed elsewhere). This patient had the best result in this study (grade-5 biceps function, palmar grasp, and the ability to lift thirty pounds [13.6 kilograms]).
Two patients had a rotational osteotomy of the humerus; both were satisfied with the result.
One patient had a transfer of the pectoralis major and another, a transfer of the latissimus dorsi to reinforce elbow flexion. Both transfers failed.
Work Activity
Of the sixty-three patients, forty-nine were able to return to work at a mean of two and a half years after the injury, although most had been assigned to a new job. As others have noted9, it is difficult to assess whether work activity is related to functional improvement.
Subjective Assessment
Twenty-five patients were satisfied with the result of the procedure, sixteen were fairly satisfied, and twenty-two were dissatisfied. Even those who were dissatisfied believed that every available measure had been taken to treat the lesion. However, four patients stated that they would not have the operation again.
Relationship Between the Type of Lesion and the Functional Outcome
We evaluated five types of lesions in relation to one objective criterion (recovery of the function of the biceps) and one subjective criterion (satisfaction of the patient) (Tables II and III). There was a tendency for both the level of satisfaction and the grade of biceps function to be higher in association with type-IIB lesions, although this association could not be shown to be significant with the numbers available.
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Discussion
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The delay between the accident and the intervention was clearly one of the most significant prognostic factors with regard to the result of grafting (p = 0.006 for grafts attached to the musculocutaneous nerve, p = 0.003 for those attached to the lateral cord, and p = 0.003 for recovery of biceps function). To achieve an optimum result, the delay should be less than four months. No procedure, with any type of graft, that was performed after a delay of more than seven months had a successful result. After six months, as has been mentioned by many authors4,6,12, muscular atrophy, fibrosis, and joint stiffness are so severe that even if the grafting is a success function will not be restored. However, we do not consider an emergency operation to be a good solution, either. A delay in the procedure allows time for spontaneous recovery, resulting in healthier tissue. Perioperative assessment of the lesion is more accurate after wallerian degeneration has occurred; in addition, formation of a proximal neuroma allows definition of the exact limits for resection.
Many authors, ourselves included, have insisted on the need to apply grafts to more distal branches to improve the outcome; however, on the basis of the current study, the benefits of doing this are not clear. The results associated with attaching the graft to the lateral or posterior cord were better (although not significantly so; p = 0.08) than those associated with attaching it to individual peripheral nerves (the musculocutaneous or radial nerve). This is difficult to understand. The greater length of graft that is required to reach the distal nerves appears to be a more negative factor than the loss of axons that occurs as a result of the graft being proximally attached. However, the length of the graft should not be a factor that limits the trimming of the distal stump back to a zone of healthy tissue. The better results of proximal attachment of the graft also may be related to the fact that use of a shorter graft leaves more material available for grafting. Alternately, the better results may be related to reasons that are unclear at the present time.
The presence of a neuroma on the proximal stump was directly related to a good result (p = 0.001), confirming the findings of a previous study21. It was difficult to assess, during the operation, the quality of the nerve root that was being treated with the graft if there was no neuroma. We did not find any association between the surgeon's subjective assessment of the quality of the proximal stump and the result of the graft. Intraoperative monitoring of cortical somatosensory evoked potentials24 was not performed; this would have allowed us to define more precisely the proximal nerve-root lesion in patients who had no abnormalities on magnetic resonance imaging or myelography and no visible neuroma at the time of the operation. We consider these occurrences to be very rare.
The number of strands that were used for the grafts attached to the posterior part of the brachial plexus (the radial nerve) was a significant factor for distal recovery (p = 0.002); a minimum of four strands was necessary to achieve a good result.
On the basis of our findings in the current study, vascular lesions should not be treated operatively except in patients who have acute ischemic symptoms. None of our patients had such symptoms because the collateral circulation was always adequate. This issue is very controversial, but we believe that avoiding repair of the vessels during an emergency nerve repair leads to a better outcome. This may be related to the damage produced during the repair of the vessels, which decreases the viability of the nerve being repaired and makes the second operation much more difficult. In some patients who have no associated injuries, nerves and vessels can be repaired simultaneously by two operative teams; however, we have had limited experience with this procedure.
One of the main problems associated with brachial plexus palsy is pain7,11,19,22. According to the patients' subjective evaluation, the pain was sometimes so intense that the paralysis became a secondary concern7,18. The intensity of the pain was not related to the number of avulsed roots. Some drugs, including antidepressants and tranquilizers, were partially effective, but their undesirable side effects, such as sleepiness, were not well tolerated by the patients. Amputation has been totally ineffective in combating the pain20 because the cause of the pain depends on the central nervous system. The Nashold procedure18 (a dorsal-nerve-root-entry rhizotomy) may be effective for some patients who have very severe pain, as was shown in the current study.
Nerve transfer was described by Allieu et al.1,2, who used the spinal accessory nerve; by Tsuyama and Hara15,24,25, who used direct branching of two or three intercostal nerves; and by Millesi12-14, who used intercostal nerves bridged by a nerve graft. For reasons that we cannot explain, we found that isolated transfer of the spinal accessory nerve was more successful than transfer done in conjunction with an intercostal nerve transfer. We performed few nerve transfers compared with other authors16,17,24,25, but we always explored the proximal aspect of the brachial plexus and tried to repair the lesions primarily by grafting. This has not always been done by others, who have sometimes performed nerve transfers primarily19. Thus, it is difficult to compare our results with those of other studies.
With respect to the relationship between the result and the type of lesion, only type-IIB lesions were associated with a better outcome and, with the numbers available, we could not show this association to be significant. Interestingly, no relationship was observed between the other types of lesions and the outcome. Even among the patients who had the worst lesions (type I), more than half had recovery of the function of the biceps and half were satisfied with the result. The satisfaction index consists of a number of variables and could be related to improvements in motor function and relief of pain, whereas dissatisfaction could be related to the patients' personal problems or their psychological profile. This was the case for one patient who recovered function of the biceps and some function of the hand but asked for an amputation.
The results of the current study were compared with those of the study reported by one of us (L. S.) in 198221. That study consisted of thirty-two patients who had a complete palsy, and the learning curve for the operative procedure was taken into consideration. The mean delay between the injury and the operation was 7.2 months. Ten of twenty-one patients had good recovery of biceps function, and only two had recovery of hand function21. One purpose of the current study was to assess whether the results of this procedure have improved since the time of the earlier study and to try to determine the best site for the graft. The overall rate of recovery of biceps function, regardless of the type of repair, was thirty-six of fifty-seven. The rate of recovery of the extensor carpi radialis was two of eighteen for grafts attached to the radial nerve and three of thirteen for grafts attached to the posterior cord. We believe that good recovery of the extensor carpi radialis is important because, with an elbow that flexes, sensation in the fingers, and strong extensors, the fingers can be expected to regain their gripping function after a flexor tenodesis. Four of our patients had recovery of the flexors of the fingers, giving a good grasp.
Unlike other authors, we have never repaired the suprascapularis nerve with a graft as this may stabilize the shoulder and sometimes provide weak abduction but it has never succeeded in restoring both abduction and external rotation. Two of our patients had to be managed subsequently with a derotational osteotomy of the humerus, and six others had an arthrodesis of the shoulder. We prefer either to attach a graft to the axillary nerve, which gives a strong deltoid with active abduction, or to stabilize the shoulder with an arthrodesis while simultaneously correcting the excessive medial rotation that is often present. As reported by Allieu et al., the recovery of a strong biceps usually ensures excellent stability of the shoulder1.
Our data allow us to recommend this operation to patients who have a complete brachial plexus palsy. In the current series, some patients had good motor recovery; in two-thirds, the biceps became functional. Many patients recovered the function of two muscles, and some recovered that of three. The procedure also reduced pain. Sixteen patients had what they termed intolerable pain before the procedure compared with three patients at the time of the latest follow-up.
Unfortunately, even when the procedure leads to an improvement, the overall usefulness of the upper limb remains disappointing. The main problem with complete lesions is the lack of recovery in the distal muscles, especially the intrinsic muscles of the hand. If the patient can obtain even a primitive hand grip, good elbow flexion, and a stable shoulder, then the level of satisfaction is high. It is necessary to explain both the best possible outcome and the possibility of complete failure to each patient. The prognostic factors for success include a short delay between the injury and the operation, vessels that have not been ruptured or repaired in an emergency procedure, the presence of large neuromas at the ends of the nerves, a short graft, and a graft with many strands.
Over the previous two decades, techniques for the repair of injuries of the brachial plexus have evolved steadily; however, the procedure currently seems to have reached a plateau. It appears that additional advances can be made through scientific research on the pathophysiology of nerve tissue, pharmaceutical research on chemical agents that facilitate nerve growth, and biological research on synthetic nerve grafts and the repair of avulsed nerve roots at the level of the medulla8,10.
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Footnotes
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*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.
Service de Chirurgie Orthopédique et Traumatologique, Hôpital Lariboisière, 2, rue Ambroise-Paré, 75475 Paris CEDEX 10, France.
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References
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