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Investigation performed at the Departments of Orthopedic Surgery, Ogori Daiichi General Hospital, Ogori,
and Yamaguchi University School of Medicine, Ube, Yamaguchi-ken, Japan
TABLE I
DEMOGRAPHIC AND OPERATIVE DATA*
*ICN = intercostal nerve, SCN = supraclavicular nerve, MN = median nerve, MCN = musculocutaneous nerve, SSN = suprascapular nerve, fx = fracture, AX = axillary
nerve, and UN = ulnar nerve.
†– sign = no wave, ± sign = lower amplitude but recordable, and + sign = same wave as from normal fourth cervical nerve root.
‡The spinal accessory nerve was used as the donor motor nerve for all of the first free muscle transfer procedures and the fifth and sixth intercostal nerves, for all of
the VOL.
second 82-A, NO. transfer
free muscle 5, MAY 2000
procedures.
654 KAZUTERU DOI ET AL.
FIG. 1
Treatment algorithm. BP = brachial plexus, SSN = suprascapular nerve, MCN = musculocutaneous nerve, SAN = spinal accessory nerve,
MN = median nerve, SCN = supraclavicular nerve, ICN = intercostal nerve, UN = ulnar nerve, CMJ = carpometacarpal joint, and GH = gle-
nohumeral joint.
ergistic action16 was troublesome and inconvenient for Three patients had had an unsuccessful intercostal-to-
patients with a brachial plexus injury who had a normal musculocutaneous nerve transfer done by other sur-
contralateral upper limb. Furthermore, those authors geons. Two patients had had an injury of the subclavian
did not restore elbow extension and their patients had artery, which had been repaired but the artery had be-
to use the contralateral hand for positioning the hand in come thrombosed. One patient had had an associated
space while moving the fingers. spinal cord and spinal accessory nerve injury on the ip-
One of us (K. D.) and colleagues6,7,9 reported the in- silateral side but had recovered by the time of the oper-
terim results of double free muscle and multiple nerve ation. The interval between the injury and the first free
transfers (the so-called double free muscle technique) muscle transfer ranged from two to 113 months (mean,
to restore prehension. Although the powerful grip that 8.8 months).
was achieved was associated with clawing of the fingers, Myelography was performed preoperatively with use
grip, together with good prehension, are the most es- of metrizamide (Amipaque). During the operation, the
sential and useful functions for such patients. In the brachial plexus was exposed and the involved root was
current report, we describe the long-term results of the identified and electrically stimulated. The spinal evoked
double free muscle technique that was originally de- potentials were recorded from an epidural electrode,
scribed by one of us (K. D.) and colleagues and was which was placed preoperatively, to assess the quality of
subsequently modified6,7,9. the continuity of the root with the spinal cord.
Myelography and intraoperative monitoring of spi-
Materials and Methods
nal evoked potentials established that nine patients had
Patients a postganglionic rupture of the fifth cervical nerve root
The results in a consecutive series of patients who and a preganglionic avulsion of the sixth cervical to the
had undergone the double free muscle transfer proce- first thoracic nerve root. The remaining seventeen pa-
dure for the restoration of prehension following com- tients were classified as having a complete preganglionic
plete avulsion of the brachial plexus between August 1, avulsion of the fifth cervical to the first thoracic nerve
1990, and October 31, 1996, were reviewed retrospec- root, although five showed low but positive spinal
tively. The patients had given informed consent after evoked potential waves.
discussions concerning the procedure, the rehabilitation
program, and the prognosis before the initial operation. Operative Procedures
There were thirty-two patients, thirty of whom were The double free muscle technique described previ-
male and two of whom were female (Table I). At the ously by one of us (K. D.) and colleagues6,7,9 consisted of
time of the operation, the patients’ ages ranged from five established but modified reconstructive procedures
fifteen to forty-five years (mean, twenty-two years). (Fig. 1): (1) surgical exploration of the brachial plexus,
TABLE
RESULTS OF THEFREE
Long-Term
Early Results Elbow Function
Secondary Reconstruction Isokinetic
Time to EMG
Reinnerv. Arthrod., Other Durat Flexion Measurements Extension
(1st Transfer/ Gleno- Arthrod., Secondary of (Degrees/ (Concen./Eccen.) (Degrees/
Vasc. 2nd Transfer/ humeral Thumb Proce- Follow- MMT6 (Nm) MMT6
Case Comp.† Triceps Brachii) Joint Tenolysis CMJ dures up† Grade) Involved Normal Outcome Grade)
(mos.) (mos.)
1 No/no 4/6.5/8 Yes No Yes No 58/54 100/5 9/13 48/63 Exc. –30/3
2 No/no 4/5/no Yes No No No 27/25 100/5 — — Exc. –40/0
3 No/no 3/3/4 No No Yes No 65/60 110/5 — — Exc. –15/3
15 No/no 4/5/13 Yes EDC No No 45/43 125/5 5/8 40/49 Exc. –35/2
(splint)
16 No/no 3/4/6 No No No No 30/27 100/4 6/9 33/40 Good –45/2
22 No/no 5/4/did not test No No No No 27/24 100/3 2/6 40/53 Good –45/0
23 No/no 5/7/7 No No No No 26/24 120/5 8/12 40/53 Exc. –50/2
(splint)
*EMG = electromyographic, CMJ = carpometacarpal joint, MMT = manual muscle-testing, fx = fracture, TAM = total active motion, EDC = extensor digitorum com-
munis, ACC = spinal accessory nerve, FDP = flexor digitorum profundus, PIP = proximal interphalangeal joint, DIP = distal interphalangeal joint, IS = infraspinatus, BB =
biceps brachii, and D = deltoid.
†Values are given for the first transfer/second transfer.
‡Revision of the anastomosed vessel was successful, but the muscle became necrotic and a second free muscle transfer was performed.
§Patients who had an unstable glenohumeral joint were excluded from this calculation.
II
MUSCLE TRANSFER PROCEDURES*
Results
Shoulder Function
metacarpophalangeal joints were then started. During proximal and distal interphalangeal joints in extension
the early postoperative period, a plastic static splint was to allow these joints to stiffen in these positions.
used to maintain the wrist in a neutral position and the Following electromyographic documentation of rein-
Secondary Reconstruction
Tenolysis was done on the first free muscle (finger ex-
tensor) in nine patients and on the second free muscle
(finger flexor) in six (Table II). Arthrodesis of the gleno-
humeral joint was done with use of four large cancellous
FIG. 4
screws and iliac-crest bone graft in nine patients, and ar-
Illustration showing transfer of the third and fourth intercostal
throdesis of the carpometacarpal joint of the thumb was nerves to the motor branch of the triceps brachii muscle, performed
performed in eight. Three patients had arthrodesis of the to restore elbow extension and stability. This procedure is done at the
proximal and distal interphalangeal joints with percuta- time of the second free muscle transfer. a = third and fourth intercos-
tal nerves, b = motor branch of triceps brachii, and c = triceps brachii.
neous Kirschner wires. The reinnervated infraspinatus
muscle was transferred to the triceps brachii in two pa-
tients when the latter muscle failed to recover sufficiently. gers, with 60 degrees or more classified as excellent; 30
One patient had neurolysis of the spinal accessory nerve to 55 degrees, as good; 5 to 25 degrees, as fair; and 0 de-
because reinnervation was delayed. grees, as poor. The final outcome of prehension follow-
ing double free muscle transfer depends not only on
Assessment of Results finger motion but also on more proximal function, such
Early results: All thirty-two patients were evaluated as elbow flexion and dynamic elbow stability, which
for survival of the transferred muscles and electromy- were assessed according to the patient’s ability to posi-
ographic evidence of reinnervation of the transferred tion the hand in space while moving the fingers.
muscles and the triceps brachii (Table II). Sensory evaluation: Tinel’s sign was checked period-
Long-term results: Twenty-six of the thirty-two pa- ically in all patients, and sensibility in the corresponding
tients had long-term evaluation at least twenty-four distribution of the repaired nerve in the hand was eval-
months after the second free muscle transfer (Tables II uated. Sensation of vibration was tested with a tuning
and III). The parameters that were evaluated included fork; pain, with pin-prick; sensation of moving touch,
the strength of the transferred muscles and the triceps with cotton wool; and cutaneous pressure thresholds,
brachii, the range of active motion of the elbow and with Semmes-Weinstein monofilaments. All tests were
finger joints, sensory recovery, the ability to perform ac- performed by an experienced hand therapist, and the
tivities of daily living, and restoration of prehension. results of sensory recovery were classified according to
the modified Highet scale (Table IV)4,14.
Functional Outcome Pain (causalgia): Ten-point visual analog scales were
Motor evaluation: The modified grading system of used to define the severity of pain, with 5 points or less
Highet4,14 and that of one of us (K. D.) and colleagues6 indicating mild pain and more than 5 points, severe
were used to evaluate the results of elbow flexion (Table pain.
IV). Elbow-flexion power of more than grade 5 (accord- Functional ability: Functional ability was assessed
ing to the modified Highet scale) was classified as ex- with use of patient-based outcome measures, including
cellent; grade 3 or 4, as good; grade 1 or 2, as fair; and the weight of a book that could be held between the arm
grade 0, as poor. The final outcome of finger motion was and the trunk, the weight of a bag that could be lifted
graded according to the total active motion of the fin- with the forearm, the weight of a bottle that could be
TABLE III
LONG-TERM RESULTS: ACTIVITIES OF DAILY LIVING AND WORK*
Lifting Object with Lifting Object with Durat. Until
Lifting Pulp Pinch Hook Grip Both Hands Vocation Return to
Object with (Light [50-g] Holding Can Height Can Height Before/After Work or
Case Forearm (kg) Object) 300-g Bottle Lift (kg) Lifted† Lift (kg) Lifted† Reconstruct. School
(level) (level) (mos.)
1 Yes (6) Yes Yes Yes (5) 2 Yes (13) 2 Auto. builder/ 36
farmer.
2 Yes (5) No No No — No — Auto. builder/ 14
salesperson
3 Yes (5) Yes Yes Yes (3) 2 Yes (5) 2 Homemaker/ 6
homemaker
4 Yes (3) No No Yes (0.5) 1 Yes (2) 1 Student/ 12
salesperson
5 Yes (5) No No No — No — Construct./ 10
carpenter
6 Yes (5) No No Yes (2) 2 Yes (5) 2 Construct./ 50
construct.
7 Yes (5) No No Yes (0.5) 1 Yes (3) 1 Public officer/ 30
manager
8 Yes (5) No No Yes (0.5) 1 Yes (2) 1 Police officer/ 14
manager
9 No No No No — No — Masseur/ 24
masseur
10 Yes (6) Yes Yes Yes (1) 2 Yes (3) 2 Auto. builder/ 41
clerk
11 Yes (6) Yes Yes Yes (0.5) 1 Yes (2) 1 Student/student 35
12 Yes (6) No No No — No — Student/student 47
13 Yes (8) Yes Yes Yes (0.5) 1 Yes (2) 1 Student/officer 10
14 Yes (5) No No No — No — Designer/ 15
computer
programmer
15 Yes (5) Yes Yes Yes (1) 1 Yes (2.5) 1 Student/clerk 27
16 Yes (5) Yes Yes Yes (0.5) 1 Yes (2) 1 Designer/clerk 14
17 Yes (6) No No No — No — Student/ —
unemployed
18 Yes (6) Yes Yes Yes (1) 2 Yes (5) 2 Student/ 23
salesperson
19 Yes (5) No No Yes (1) 2 Yes (5) 2 Auto. builder/ 38
contruct.
20 Yes (1.5) Yes No Yes (0.5) 1 Yes (3) 1 Student/student 10
21 Yes (4) No No Yes (0.5) 1 Yes (3) 1 Student/computer 12
programmer
22 Yes (2) No No No — No — Student/student 24
23 Yes (5) Yes Yes Yes (1.5) 1 Yes (3) 1 Guard/guard 21
24 Yes (3) Yes Yes Yes (0.5) 1 Yes (2) 1 Student/student 12
25 Yes (3) Yes Yes Yes (0.5) 1 Yes (3) 1 Auto. builder/ —
unemployed
26 Yes (3) No No Yes (2) 2 Yes (5) 2 Student/student 12
Mean ± 4.8 ± 2.7 22 ± 2.6
s.d.
*All patients were able to lift a book weighing from one to three kilograms.
†Level 1 = to middle of thigh, and level 2 = to pubic symphysis.
held, the weight of a box that could be lifted, and the ables. The level of significance was set at p < 0.05.
height to which the box could be lifted with use of a
Results
hook grip and with both hands.
Statistical analysis: The paired t test for paired con- Early Results
tinuous variables was used. Spearman rank correlations Three free muscles had a thrombosis postoperatively
were calculated for the comparison of two-scaled vari- (Table II). Two of them were revised successfully after
Long-Term Results
Twenty-six patients were followed for at least twenty-
four months (maximum, eighty-one months; mean, thirty-
nine months) after the second transfer. The mean age at
the time of the operation was twenty-two years (range,
fifteen to forty-five years) (Table I). The mean interval
from the time of the injury to the first operation was 9.8
months (range, two to 113 months).
Elbow Function
FIG. 5-D
Active elbow flexion ranged from 50 to 145 de- Finger flexion (Fig. 5-C) and extension (Fig. 5-D) with the elbow in
grees (mean, 112 degrees). The strength of elbow flexion.
FIG. 5-E
The patient is shown unscrewing a bottle cap with both hands.
meters per day (range, 0.5 to 2.0 millimeters per day) in light objects with one hand and heavy objects with
twenty-one patients. In two patients who had inter- both hands (Fig. 5-F). Eleven of these patients also
costal nerve-crossing, the Tinel sign never progressed could hold a bottle with the reconstructed hand while
beyond the forearm. The mean interval between the opening its cap with the contralateral, normal hand
surgery and the initial recovery of sensibility in the (Fig. 5-E).
palm was twenty-two months (range, fourteen to thirty-
two months). Prehensile Recovery
Limited sensibility in the cutaneous distribution of A satisfactory (excellent or good) result was ob-
the repaired median or ulnar nerve was achieved in tained in seventeen (65 percent) of the twenty-six pa-
twenty-one patients. The recovered sensibility was the tients, according to our evaluation system. Fourteen
most sensitive in the palm, whereas only five patients patients (54 percent) could achieve more than 90 de-
felt sensation in the fingertips. All twenty-one patients grees of elbow flexion, position the hand in space while
had referred sensibility only to the clavicle or the chest moving the fingers more than 30 degrees voluntarily,
after supraclavicular or intercostal nerve reconstruc- and use the reconstructed hand for two-handed activi-
tion, respectively. Six patients had double sensation in ties such as holding a bottle while opening a cap and lift-
the cutaneous distribution of both the repaired nerve ing a heavy object. All of these patients were thirty-two
of the hand in situ and that of the recipient sensory years old or less and had had a short interval (eight
nerve. months or less) between the injury and the surgery, a
According to the modified Highet scale4,14, sensation long duration (more than fifty-five months) of follow-
recovered to S2+ in seven patients, to S2 in nine, and to up, and no associated injuries of the subclavian artery,
S1 in four; in the two remaining patients, there was no the spinal accessory nerve, or the spinal cord.
recovery of sensibility (S0). There was no significant
difference in the recovery of sensibility between the Donor-Site Sequelae
supraclavicular nerve and the intercostal nerve. There were no functional complications related to
the donor site, although some patients complained about
Pain the presence of a long scar that they considered to be
During the follow-up period, sixteen patients had cosmetically unacceptable.
causalgia. Five of these patients had complained of
causalgia preoperatively, but in the other patients the Discussion
pain developed during the postoperative rehabilita- The double free muscle procedure after complete
tion. At the time of the final follow-up examination, avulsion of the brachial plexus reliably provided pre-
according to the visual analog scales only two patients hension involving the basic grasping function of the
complained of moderate pain that interfered with their hand, as well as voluntary motion and stability of the
activities; the other fourteen patients had mild, inter- shoulder and elbow, in more than half of the twenty-six
mittent pain, which was relieved with medication and patients who had long-term follow-up. Nineteen pa-
did not seriously interfere with activities. The remain- tients could use the reconstructed hand for two-handed
ing ten patients did not have causalgia at any time. activities such as holding or lifting an object, despite
having a limited total range of active finger motion.
Ability to Hook or Hold Objects Fourteen patients with excellent or good prehension
All twenty-six patients could hold an object such as had a mean total range of active finger motion of 52
a book weighing more than one kilogram between the degrees (range, 30 to 110 degrees). Approximately half
arm and the trunk with use of the reinnervated second of the patients failed to obtain useful prehension, due
free muscle and the triceps brachii and assisted by the mainly to lack of active elbow extension as well as adhe-
rhomboid muscles. All but one patient could lift an ob- sion of the transferred muscles. However, they achieved
ject such as a bag weighing a mean of 4.8 kilograms good elbow function. Hence, even though prehension
with the forearm. No patient had key pinch since the was not achieved, the elbow flexion that was restored was
carpometacarpal joint of the thumb had been immobi- more reliable than that achieved with conventional
lized in opposition either with an arthrodesis or a nerve-transfer procedures, which have yielded a higher
splint. However, eleven patients were able to grasp a grade of elbow flexion than M3 in 80 percent of patients17.
light object such as a bottle weighing 300 grams. Nine- In the current series, the latissimus dorsi, gracilis,
teen patients were able to lift a bag weighing between and rectus femoris muscles were used as donor muscles.
0.5 and five kilograms with a hook grip and to lift a box The latissimus dorsi did not provide satisfactory finger
weighing two to thirteen kilograms with use of both function because of adhesion of the muscle to the pulley
hands up to the level of the middle of the thigh (twelve system and also because of rupture of its tendon due to
patients) or to the pubic symphysis (seven patients). ischemic necrosis of the portion distal to the pulley. The
These nineteen patients could use the reconstructed rectus femoris muscle was also unsatisfactory due to
hand well in daily activities for lifting and carrying poor muscle excursion with resulting poor finger func-
tion. The gracilis is the donor muscle of choice. free muscle reinnervated by the intercostal nerves. The
Tenolysis was indicated when active finger function final power that was achieved was weaker and the results
was not achieved despite strong contraction of the were less reliable than those of conventional nerve-
transferred muscle. Nine finger extensors and six finger crossing to the biceps brachi. This may be due to the dif-
flexors had tenolysis from the proximal musculotendi- ficulty in identifying the motor fascicles in the nerve
nous junction to the fingers. However, in four patients stump and the delay between the time of injury and the
with a latissimus dorsi transfer and in one with a rectus procedure. However, even if the power of the triceps
femoris transfer, tenolysis failed to improve the range of brachii was weak (M2), it could contribute to stability of
motion postoperatively as there was recurrence of ad- the elbow with the aid of gravity. If reinnervation of the
hesion. Nine patients who had a gracilis transfer had an triceps brachii fails, secondary reconstruction (for exam-
improved range of finger motion, ranging from 20 to 60 ple, transfer of the reinnervated infraspinatus to the tri-
degrees, postoperatively. ceps brachii) may be an option for restoring elbow
The spinal accessory nerve and the third to sixth in- stability8. Two patients obtained elbow extension power-
tercostal nerves were used in our series. There were sig- ful enough to negate the simultaneous elbow flexion
nificant differences between the two sources of donor while moving the fingers.
nerves with regard to the time that it took for reinner- Stability of the glenohumeral joint can be achieved
vation of the transferred muscle (p < 0.05)22; however, the by the reinnervated free muscle, the triceps brachii, and
final muscle power was not significantly different. The the shoulder-girdle muscles without arthrodesis. During
phrenic nerve and the contralateral seventh cervical exploration of the brachial plexus, if the fifth cervical
nerve root also may be used as donor nerves3,11,18,21, but we nerve root is available8 it should be crossed to the supra-
did not use these nerves because of the possible risks. scapular nerve with use of nerve-grafting, not only to
The double free muscle technique utilizes the simul- improve shoulder function but also to reinnervate para-
taneous movement of multiple joints with a limited lyzed muscles for use as possible donor muscles for
number of donor motor nerves; for example, the first transfer if the triceps brachii does not recover. If the gle-
free muscle reinnervated by the spinal accessory nerve nohumeral joint remains unstable even after recovery
works to extend the fingers and flex the elbow simulta- of these muscles, glenohumeral arthrodesis can be done,
neously. After recovery of the triceps brachii as an an- although this will limit several activities, such as turning
tagonist of the elbow flexor, the patients could position over during sleep. Care must be taken to prevent frac-
the hand in space while extending the fingers. ture of the proximal part of the humerus; in the current
Multiple intercostal nerve-crossing from the ipsilat- series, one humeral fracture occurred postoperatively.
eral side, such as crossing of the second free muscle with Restoration of basic functions such as protective
the fifth and sixth intercostal nerves and crossing of the sensation and position sense is imperative when pre-
triceps brachii with the third and fourth intercostal hensile function is restored after irreparable brachial
nerves, might have produced paradoxical movements, plexus injury. Sixteen patients achieved sensibility of the
such as simultaneous contraction of the elbow flexor hand that was at least S2, had adequate position sense,
(the second free muscle transfer) and the elbow exten- and never had a minor injury, such as a burn, in the re-
sor (the triceps brachii). Electromyography with use of constructed hand. Intercostal nerve-crossing has been
multichannel electrodes showed that the second free reported to provide a better outcome with regard to
muscle and the triceps brachii were contracting at the sensory restoration12. However, in the current series,
same time, although the amplitude of the compound there were no significant differences in sensibility be-
motor-action potential was different depending on the tween the patients in whom the suprascapular nerve had
phase of elbow and finger movement. However, the sec- been used as the donor nerve and those in whom the in-
ond free muscle acted as a supplemental elbow flexor tercostal nerves had been used.
since it was not placed in the flexion-extension plane of In contrast to series reported in the literature13,19, we
the elbow. The first free muscle acted as the main elbow had no patients with severe postoperative causalgia that
flexor. Subsequently, the patients could flex the elbow could not be relieved with the usual analgesics. Ten pa-
to overcome the antagonist. tients had never had causalgia. This finding is difficult to
The most powerful finger flexion was obtained with explain, but perhaps these patients had some inborn ge-
the elbow in extension while finger extension was not netic means of inhibiting pain. Parry19 noted that Orien-
operative, and the power of finger flexion decreased tal patients rarely reported pain in association with
slightly when the elbow was flexed. traction lesions of the brachial plexus. Sensory restora-
In nineteen patients, the triceps brachii was reinner- tion with transfer of the intercostal or supraclavicular
vated as demonstrated electromyographically, but only nerves to the median or ulnar nerve might have modu-
sixteen patients could voluntary stabilize the elbow joint lated pathogenesis of the deafferentation pathway of
when they moved the fingers. The time until the triceps causalgia, and the patients’ high motivation for surgical
brachii was reinnervated following nerve-crossing was reconstruction and rehabilitation might have helped
longer than the time until reinnervation of the second them to tolerate the pain better.
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