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J Neurosurg 107:666–671, 2007
Median to radial nerve transfer for treatment of radial
nerve palsy
Case report
SUSAN E. MACKINNON, M.D., BRANDON ROQUE, B.S., AND THOMAS H. TUNG, M.D.
Division of Plastic and Reconstructive Surgery, Washington University School of Medicine,
St. Louis, Missouri
PThe purpose of this study is to report a surgical technique of nerve transfer to restore radial nerve function after a
complete palsy due to a proximal injury to the radial nerve. The authors report the case of a patient who underwent
direct nerve transfer of redundant or expendable motor branches of the median nerve in the proximal forearm to the
extensor carpi radialis brevis and the posterior interosseous branches of the radial nerve. Assessment included degree
of recovery of wrist and finger extension, and median nerve function including pinch and grip strength.
Clinical evidence of reinnervation was noted at 6 months postoperatively. The follow-up period was 18 months. Recovery of finger and wrist extension was almost complete with Grade 4/5 strength. Pinch and grip strength were improved postoperatively. No motor or sensory deficits related to the median nerve were noted, and the patient is very
satisfied with her degree of functional restoration.
Transfer of redundant synergistic motor branches of the median nerve can successfully reinnervate the finger and
wrist extensor muscles to restore radial nerve function. This median to radial nerve transfer offers an alternative to nerve
repair, graft, or tendon transfer for the treatment of radial nerve palsy. (DOI: 10.3171/JNS-07/09/0666)
KEY WORDS • median nerve • nerve transfer • radial nerve injury
to the radial nerve in the upper extremity is common2 and can result from orthopedic injuries or their
surgical management,17,31,45 direct nerve trauma,3,18,37 as
part of a brachial plexus injury,26,32,54 or nerve compression.1,29,36,41,47 Radial nerve palsy may also be caused by
nerve tumors,26 local inflammation,30,44,61 or idiopathic neuritis.46,50 The most appropriate management will depend on
the cause, the level and extent of the injury or lesion, the
degree of functional impairment, and the duration of the
problem. Injury to the radial nerve in the lower arm or forearm can usually be managed by direct repair or reconstruction with nerve grafts, offering restoration of function.
Proximal radial nerve injury near the axilla or higher is especially problematic because the distance and time required for reinnervation of the extensor muscles in the forearm often preclude significant recovery of function, with
any delays in treatment further worsening the outcome.9,10,
21,28,33–35
In such cases or in cases of long-standing palsy,
reconstruction with tendon transfers has been the mainstay
of treatment.5,6,22,51
I
NJURY
Abbreviations used in this paper: AIN = anterior interosseous
nerve; ECRB = extensor carpi radialis brevis; ECRL = extensor carpi radialis longus; FCR = flexor carpi radialis; FDS = flexor digitorum sublimis; PIN = posterior interosseous nerve; PL = palmaris
longus.
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The technique of nerve transfer has been used with increasing frequency for motor and sensory reconstruction of
proximal upper-extremity nerve and brachial plexus injuries.27,38,60 Nerve transfers at the level of the upper arm and
shoulder have conventionally been used to restore shoulder
and elbow function after brachial plexus root avulsion injury.26,54,56 In the forearm, nerve transfers from redundant or
expendable motor branches of the median nerve have been
reported with good outcomes.24,25,55 In the lower extremity,
motor and sensory nerve transfers have also been described
in the management of extensive injuries where few alternative options exist.57 In this study we report a case of complete radial nerve palsy in the forearm treated successfully
with nerve transfer of redundant motor branches of the
median nerve to the PIN and ECRB branch of the radial
nerve with specific nerve transfer of the synergistic FDS
to the wrist extensor (ECRB) and FCR to finger extensors
(PIN) (Fig. 1).
Case Report
History and Examination. This 32-year-old right-handdominant woman was involved in a motor vehicle accident
and suffered multiple injuries including fractures of her left
tibia, right humerus, and lumbar spine. Because of nonJ. Neurosurg. / Volume 107 / September, 2007
Nerve transfer for radial nerve function
FIG. 1. Illustration of transfer of redundant FDS and FCR/PL
branches of the median nerve in the proximal forearm to the ECRB
and posterior interosseous branches of the radial nerve through a
single proximal volar forearm incision.
union of her humeral fracture, she underwent intramedullary rod placement in the right humerus 2 months after the
accident through standard incisions at the anterior aspect of
the acromion and laterally just above the elbow joint (Fig.
2). Postoperatively she awakened with a complete radial
nerve palsy. No improvement in radial nerve function was
seen after 7 months, and surgical exploration was undertaken, which revealed a disruption of the right radial nerve at
the level of the distal screw just above the elbow joint. She
had been treated at an outlying hospital and was referred at
that time for treatment of her radial nerve palsy. The initial
physical examination demonstrated no radial nerve function and a pinch/grip strength of 6/20 lbs on the right and
11/42 lbs on the left. Multiple treatment options and their
risks and benefits were reviewed. The patient was concerned about the morbidity of nerve grafting, the likelihood
of poor recovery given the time since injury, and the numerous scars required for tendon transfers as well as nerve graft
harvest. She was informed that although a median to radial
nerve transfer was a new option,11,12 it was the best chance
for her wrist and finger extensors to be reinnervated in a
timely fashion. It was decided to proceed with a median to
radial nerve transfer.
Operation. An incision was made in the proximal volar
forearm just below the antecubital crease. The median nerve
and its branches were identified with intraoperative stimulation of the FDS, FCR, and PL, the AIN, and the main
median nerve. A disposable nerve stimulator with a current
of 1 to 2 mA (Varistim III, Medtronic) was used to stimulate
the various branches of the median nerve. The ground needle was inserted into the soft tissue near the branches to
facilitate specific stimulation and identification of each of
the branches. Nerve action potentials were not measured because special equipment and personnel are needed, and the
quality of the donor motor nerve can be evaluated by direct
stimulation and target muscle response. It is important to
note that no intrafascicular dissection of the median nerve
was performed. By contrast, just the branches of the median nerve itself were dissected and identified. Stimulation of
the FDS branch will cause finger flexion, and stimulation of
the FCR/PL branch will cause wrist flexion. If the FCR and
PL branches are separate, then stimulation of the PL branch
J. Neurosurg. / Volume 107 / September, 2007
FIG. 2. Radiograph of the patient’s right upper extremity following placement of an intramuscular rod for the humeral fracture.
will cause visible contraction of its tendon in the distal volar
forearm just proximal to the wrist, and possibly in the proximal palm because of its insertion as the palmar aponeurosis with very weak wrist flexion. Through the same incision
the radial sensory nerve was identified and followed proximally to identify the PIN and the branch to the ECRB. In
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S. E. Mackinnon, B. Roque, and T. H. Tung
preparation for nerve transfer, the radial nerve branches to
the ECRB and the PIN were divided as proximally as possible to maximize length for the transfer (Fig. 3). The branch
to the FDS and the FCR/PL branch of the median nerve
were then divided as distally as possible to allow a direct
tension-free end-to-end coaptation to the ECRB branch and
the PIN, respectively, using standard microneurosurgical
technique.
The lateral incision from the previous surgery in the distal upper arm just above the elbow was also explored prior
to the microsurgical repairs to see if it was possible to reconstruct the nerve to the ECRL. Transection of the radial
nerve was confirmed. There was a large proximal neuroma
distal to the branches to the ECRL and brachioradialis muscles. Although the branches to the ECRL and brachioradialis were found to be physically intact, no muscular contraction was seen with electrical stimulation of the nerve
branches. The radial nerve at this level was scarred even to
the spiral groove. Nerve graft reconstruction was thus not
possible because of the lack of a healthy proximal stump.
The proximal radial neuroma was mobilized and transposed
proximally into the triceps muscle to minimize chronic neuroma pain.
Postoperative Course. The elbow was immobilized at 90˚
flexion for 10 days, and then passive range of motion exercises were initiated. Four months postoperatively, the patient had a pinch/grip strength of 8/20 lbs on the right (compared with 6/20 lbs preoperatively) and 12/55 lbs on the
left. The first evidence of reinnervation was noted 6 months
postoperatively when she first noted some wrist extension
with flexion of her fingers. At 10 months postoperatively
pinch/grip was 10/20 lbs on the right and 14/40 lbs on the
left. At the last follow-up visit 18 months after surgery, her
pinch/grip was 12/40 lbs on the right and 11/55 lbs on the
left (Table 1). She now has almost complete active extension of her wrist and fingers with just a slight lag in extension of her index finger (Fig. 4). Strength was deemed as
Medical Research Council Grade 4/5. This function spontaneously recovered with no motor reeducation. Pinch and
grip strength on the right was improved postoperatively. No
motor or sensory deficits related to the median nerve were
noted, and the patient is very satisfied with her degree of
functional restoration.
Discussion
Treatment of nerve injury has relied on primary nerve
repair and grafting or tendon transfers.27 Advances in peripheral nerve surgery including improvements in surgical
technique and instrumentation, and knowledge of injury
patterns, nerve regeneration, and internal topography have
all contributed to improvement in outcomes. Transection
injuries are appropriately treated with primary nerve repair
when possible,7,26,43,48 and short nerve gaps are managed with
nerve grafts or more recently, nerve conduits have become
a viable option for nerve gaps less than or equal to 3 cm in
length.4,16,19,20 However, there is a subset of nerve injuries that
are not amenable to primary repair and for which grafting
is not consistently successful. These injuries include very
proximal nerve injury, those in which the zone of injury is
FIG. 3. Intraoperative photographs. Upper: Dissection of motor branches of the right median nerve through the proximal volar
forearm incision (elbow to the right, and hand to the left). A indicates the FCR/PL branch; B, the median nerve (proximal to the
AIN branch); C, the FDS branch; and D, the pronator teres branch.
Lower: The FDS and FCR/PL branches (black arrow) of the median nerve are divided distally and transposed laterally toward the
ECRB, and posterior interosseous branches of the radial nerve
(white arrow) are divided proximally prior to direct end-to-end coaptation.
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TABLE 1
Preoperative and postoperative measurements
of the patient’s pinch and grip strength
Pinch/Grip (lbs)
Time Point
Rt
Lt
preop
4 mos postop
10 mos postop
18 mos postop
6/20
8/20
10/20
12/40
11/42
12/55
14/40
11/55
J. Neurosurg. / Volume 107 / September, 2007
Nerve transfer for radial nerve function
FIG. 4. Photographs taken at 1-year follow-up demonstrating restoration of finger and wrist extension of the right hand.
extensive, resulting in a long nerve gap, and idiopathic nerve
palsies or neuritis in which no proximal healthy nerve segment exists.9,28,33–35 For these problems, nerve transfer provides an alternative surgical option.27,57,60
The recovery of motor function following nerve repair
depends on both a sufficient number of motor axons reaching the target muscle, and reinnervation prior to degeneration of the neuromuscular junction.8,10,21 In the case of proximal injury or long nerve gaps, there may not be sufficient
time for regenerating axons to reach the motor endplates of
target muscles before they become permanently resistant to
reinnervation. Transfer of a distal nerve in proximity to the
target muscle eliminates the need for nerve grafts and reduces the time required for motor axons to reach the motor
endplates. A nerve transfer essentially converts a high proximal level injury to a low or distal nerve injury. As such,
even a patient whose treatment is delayed remains a good
candidate for distal nerve transfer reconstruction. Because
the reinnervated target muscle maintains its anatomical location and attachments, a nerve transfer does not alter biomechanical factors that affect muscle function such as vector and tension.13,14 There is minimal dissection and scarring
of the muscle bed that can limit muscle excursion and altogether may negatively influence the strength of a muscle
or tendon transfer. Experimentally, functional deficits have
been associated with the tendon repair component of a muscle transfer with no significant effect noted when a nerve
repair or vascular anastomosis was performed.15
Nerve transfers are used commonly for the reconstruction of elbow and shoulder function in brachial plexus injuries.26,54 Because of the proximal level of the lesion in
such injuries, especially brachial plexus root avulsions, reconstruction with long nerve grafts often restore function
poorly and excellent results can be achieved with distal
nerve transfers close to the target muscle(s).27,42,56 High ulnar
and median nerve injuries also result in loss of critical hand
functions and are also associated with suboptimal outcomes
following nerve graft reconstruction because of the long
distance required for nerve regeneration.26 The results of
distal nerve transfers for such injuries have been very good
and include transfer of the distal AIN to the deep motor
branch of the ulnar nerve27,39,59 or the recurrent motor branch
of the median nerve at the level of the wrist,58 and the use of
redundant motor branches of the median or ulnar nerves to
restore pronation55 and radial nerve function.24,25 The functional outcomes have been as good or better than alternative
methods such as tendon or muscle transfers, and in many
cases offer a reconstructive option in cases in which none
otherwise exists. In our experience, the results from motor
nerve transfers have been remarkably good and we hypothJ. Neurosurg. / Volume 107 / September, 2007
esize that an additional reason for this is the elimination of
the need for a sensory nerve graft. There has been suggestion in the recent experimental literature that nerve regeneration is superior if the sensory environment can be excluded from the regenerative equation.40,49
The selection of a donor nerve branch to a muscle that is
synergistic to the target muscle will facilitate postoperative
therapy and motor reeducation. However, a nerve supplying
a muscle that is nonsynergistic or even antagonistic to the
target muscle can be used. Motor reeducation may be more
complicated, however, and the use of additional therapies
such as audio and/or visual biofeedback may be necessary
to correctly recruit the target muscles and to minimize simultaneous contraction of the antagonistic muscles. Nevertheless, excellent functional outcome can still be achieved
with a compliant patient who understands the motor reeducation strategies and appropriate hand therapy.24,25 In the
case reported here, a redundant FDS branch (finger flexion)
of the median nerve was used to reinnervate the ECRB
(wrist extension), and the FCR/PL branch (wrist flexion) of
the median nerve was transferred to the PIN (finger extension). Although median and radial nerve functions are nonsynergistic, certain movements are complementary based
on the tenodesis effect (Fig. 5). This refers to the length–
tension relationship between wrist position and the extrinsic
flexors of the fingers. Wrist extension increases the passive
tension of the flexor tendons and thereby passively causes
finger flexion and increases flexion strength, whereas wrist
flexion has the opposite effect. As such, the use of a donor
nerve branch that contributes to finger flexion (FDS) rather
than wrist flexion (FCR/PL) is better suited to restore wrist
extension (ECRB). Similarly, a donor nerve branch that innervates a muscle for wrist flexion (FCR) is more appropriately used for finger extension (PIN). From a motor reeducation point of view this will facilitate the relearning process
as these movements are synergistic.
Wrist extension has greater force requirements than finger extension. The excellent functional results seen with this
nerve transfer likely also relate to the relatively greater number of motor axons directed to the ECRB compared with the
PIN branches. With this transfer, there is a slight size match
discrepancy between the two nerve repairs with the PIN being larger than the ECRB. By contrast, the two donor nerves
are of similar size. Thus the wrist extensor receives a relatively greater ratio of motor axons. Although we have reported good results in two other patients with this median to
radial nerve transfer,24,25 we did not recognize the nuances of
the transfer as well as we now do as discussed in this report.
The concern of donor morbidity and downgrading of
function in the donor muscle group following nerve trans669
S. E. Mackinnon, B. Roque, and T. H. Tung
branches of the median nerve in the forearm very close to
the finger and wrist extensor muscles are used to reinnervate
those muscles by transfer without the need for nerve grafts,
and with a minimal distance required for nerve regeneration
and therefore faster reinnervation. Synergistic nerve transfer
techniques can result in excellent function recovery without
the need for significant motor reeducation and with no donor morbidity.
References
FIG. 5. Illustrations. The tenodesis effect refers to the length–
tension relationship between wrist position and the extrinsic flexors
of the fingers. Wrist extension increases the passive tension of the
flexor tendons and thereby passively causes finger flexion and increases flexion strength, whereas wrist flexion has the opposite effect and allows the digits to passively extend.
fer has not been clinically substantiated.23,27,38,52,53 To minimize this risk, it is therefore important that redundant or
expendable motor branches are used for transfer and that
adequate function remaining in the donor muscle group is
verified by electrical stimulation prior to transfer. Study of
the motor branches of the median nerve in the forearm has
demonstrated redundancies in the majority of patients in the
branches to the pronator teres and FDS, in addition to the
functionally redundant PL.55 The branches of the median
nerve to the pronator teres, FDS, and PL are in an ideal position for use in transfer to distal branches of the radial
nerve, although consideration can be given to sparing the
PL for use as a tendon transfer such as an opponensplasty
in patients with more complex palsies.
Conclusions
Until recently, the treatment for proximal or extensive radial nerve injury has been reconstruction with tendon transfers or nerve repair. We have presented an alternative method for treatment of radial nerve injury. Redundant motor
670
1. Barber KW, Bianco AJ, Soule EH, MacCarty CS: Benign extraneural soft-tissue tumors of the extremities causing compression of nerves. J Bone Joint Surg Am 44:98, 1962
2. Barton NJ: Radial nerve lesions. Hand 5:200–208, 1973
3. Bateman JE: Trauma to Nerves in Limbs. Philadelphia: Saunders, 1962
4. Belkas JS, Shoichet MS, Midha R: Peripheral nerve regeneration through guidance tubes. Neurol Res 26:151–160, 2004
5. Bevin AG: Early tendon transfer for radial nerve transection.
Hand 8:134–136, 1976
6. Burkhalter WE: Early tendon transfer in upper extremity peripheral nerve injury. Clin Orthop Relat Res 104:68–79, 1974
7. Calder JS, Green CJ: Nerve-muscle sandwich grafts: the importance of Schwann cells in peripheral nerve regeneration through
muscle basal lamina conduits. J Hand Surg [Br] 20:423–428,
1995
8. Cederna PS, Youssef MK, Asato H, Urbanchek MG, Kuzon
WM Jr: Skeletal muscle reinnervation by reduced axonal numbers results in whole muscle force deficits. Plast Reconstr Surg
105:2003–2011, 2000
9. Dellon AL: The moving two-point discrimination test: clinical
evaluation of the quickly adapting fiber/receptor system. J Hand
Surg [Am] 3:474–481, 1978
10. Fu SY, Gordon T: Contributing factors to poor functional recovery after delayed nerve repair: prolonged axotomy. J Neurosci
15:3876–3885, 1995
11. Gawande A: Complications: A Surgeon’s Notes on an Imperfect Science. New York: Picador, 2002
12. Gawande A: Desperate measures. The New Yorker, May 5, 2003
13. Guelinckx PJ, Carlson BM, Faulkner JA: Morphologic characteristics of muscles grafted in rabbits with neurovascular repair.
J Reconstr Microsurg 8:481–489, 1992
14. Guelinckx PJ, Faulkner JA: Parallel-fibered muscles transplanted with neurovascular repair into bipennate muscle site in rabbits. Plast Reconstr Surg 89:290–298, 1992
15. Guelinckx PJ, Faulkner JA, Essig DA: Neurovascular-anastomosed muscle grafts in rabbits: functional deficits result from
tendon repair. Muscle Nerve 11:745–751, 1988
16. Hazari A, Wiberg M, Johansson-Ruden G, Green C, Terenghi G:
A resorbable nerve conduit as an alternative to nerve autograft
in nerve gap repair. Br J Plast Surg 52:653–657, 1999
17. Holstein A, Lewis GM: Fractures of the humerus with radialnerve paralysis. J Bone Joint Surg Am 45:1382–1388, 1963
18. Kettelkamp DB, Alexander H: Clinical review of radial nerve
injury. J Trauma 7:424–432, 1967
19. Kim J, Dellon AL: Reconstruction of a painful post-traumatic
medial plantar neuroma with a bioabsorbable nerve conduit: a
case report. J Foot Ankle Surg 40:318–323, 2001
20. Kitahara AK, Nishimura Y, Shimizu K, Endo K: Facial nerve
repair accomplished by the interposition of a collagen nerve
guide. J Neurosurg 93:113–120, 2000
21. Kobayashi J, Mackinnon SE, Watanabe O, Ball DJ, Gu XM,
Hunter DA, et al: The effect of duration of muscle denervation on
functional recovery in the rat model. Muscle Nerve 20:858–866,
1997
22. Kruft S, von Heimburg D, Reill P: Treatment of irreversible lesion of the radial nerve by tendon transfer: indication and long-
J. Neurosurg. / Volume 107 / September, 2007
Nerve transfer for radial nerve function
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
term results of the Merle d’Aubigne procedure. Plast Reconstr
Surg 100:610–618, 1997
Leechavengvongs S, Witoonchart K, Uerpairojkit C, Thuvasethakul P, Ketmalasiri W: Nerve transfer to biceps muscle using a
part of the ulnar nerve in brachial plexus injury (upper arm type):
a report of 32 cases. J Hand Surg [Am] 23:711–716, 1998
Lowe JB III, Sen SK, Mackinnon SE: Current approach to radial nerve paralysis. Plast Reconstr Surg 110:1099–1113, 2002
Lowe JB III, Tung TR, Mackinnon SE: New surgical option for
radial nerve paralysis. Plast Reconstr Surg 110:836–843, 2002
Mackinnon SE, Dellon AL (eds): Surgery of the Peripheral
Nerve. New York: Thieme, 1988
Mackinnon SE, Novak CB: Nerve transfers. New options for reconstruction following nerve injury. Hand Clin 15:643–666,
1999
Mailander P, Berger A, Schaller E, Ruhe K: Results of primary
nerve repair in the upper extremity. Microsurgery 10:147–150,
1989
Manske PR: Compression of the radial nerve by the triceps muscle: a case report. J Bone Joint Surg Am 59:835–836, 1977
Marmor L, Lawrence JF, Dubois EL: Posterior interosseous nerve
palsy due to rheumatoid arthritis. J Bone Joint Surg Am 49:
381–383, 1967
Mast JW, Spiegel PG, Harvey JP Jr, Harrison C: Fractures of the
humeral shaft: a retrospective study of 240 adult fractures. Clin
Orthop Relat Res 112:254–262, 1975
Midha R: Epidemiology of brachial plexus injuries in a multitrauma population. Neurosurgery 40:1182–1189, 1997
Millesi H: Progress in peripheral nerve reconstruction. World J
Surg 14:733–747, 1990
Millesi H, Meissl G, Berger A: Further experience with interfascicular grafting of the median, ulnar, and radial nerves. J
Bone Joint Surg Am 58:209–218, 1976
Moberg E: Criticism and study of methods of examining sensibility of the hand. Neurology 12:8–19, 1962
Moon N, Marmor L: Parostal lipoma of the proximal part of the
radius. A clinical entity with frequent radial-nerve injury. J Bone
Joint Surg Am 46:608–614, 1964
Morris AH: Irreducible Monteggia lesion with radial-nerve entrapment. A case report. J Bone Joint Surg Am 56:1744–1746, 1974
Nath RK, Mackinnon SE: Nerve transfers in the upper extremity. Hand Clin 16:131–139, 2000
Nath RK, Mackinnon SE, Shenaq SM: New nerve transfers following peripheral nerve injuries. Oper Techn Plast Reconstr
Surg 4:2–11, 1997
Nichols CM, Brenner MJ, Fox IK, Tung TH, Hunter DA, Rickman SR, et al: Effect of motor versus sensory nerve grafts on
peripheral nerve regeneration. Exp Neurol 190:347–355, 2004
Nielsen HO: Posterior interosseous nerve paralysis caused by fibrous band compression at the supinator muscle. A report of
four cases. Acta Orthop Scand 47:304–307, 1976
Novak CB, Mackinnon SE, Tung TH: Patient outcome following
a thoracodorsal to musculocutaneous nerve transfer for reconstruction of elbow flexion. Br J Plast Surg 55:416–419, 2002
Omer GE Jr: The prognosis for untreated traumatic injuries, in
Omer GE Jr, Spinner M, Van Beek AL (eds): Management of
Peripheral Nerve Problems. Philadelphia: WB Saunders, 1998,
pp 365–370
Popelka S, Vainio K: Entrapment of the posterior interosseous
J. Neurosurg. / Volume 107 / September, 2007
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
56.
57.
58.
59.
60.
61.
branch of the radial nerve in rheumatoid arthritis. Acta Orthop
Scand 45:370–372, 1974
Samardzic M, Grujicic D, Milinkovic ZB: Radial nerve lesions associated with fractures of the humeral shaft. Injury 21:220–222,
1990
Sharrard WJ: Posterior interosseous neuritis. J Bone Joint Surg
Br 48:777–780, 1966
Spinner M: The arcade of Frohse and its relationship to posterior
interosseous nerve paralysis. J Bone Joint Surg Br 50:809–812,
1968
Spinner M: Injuries to the Major Branches of Peripheral
Nerves of the Forearm. Philadelphia: WB Saunders, 1972
Sulaiman OAR, Midha R, Munro CA, Matsuyama T, Al-Majed
A, Gordon T: Chronic Schwann cell denervation and the presence of a sensory nerve reduce motor axonal regeneration. Exp
Neurol 176:342–354, 2002
Sunderland S: Nerve and Nerve Injuries. Edinburgh: Churchill Livingstone, 1968
Sunderland S: Traumatic injuries of the peripheral nerves: I.
Simple compression of the radial nerve. Brain 68:56, 1945
Sungpet A, Suphachatwong C, Kawinwonggowit V: One-fascicle
median nerve transfer to biceps muscle in C5 and C6 root avulsions of brachial plexus injury. Microsurgery 23:10–13, 2003
Teboul F, Kakkar R, Ameur N, Beaulieu JY, Oberlin C: Transfer of fascicles from the ulnar nerve to the nerve to the biceps in
the treatment of upper brachial plexus palsy. J Bone Joint Surg
Am 86:1485–1490, 2004
Terzis JK, Papakonstantinou KC: The surgical treatment of
brachial plexus injuries in adults. Plast Reconstr Surg 106:
1097–1124, 2000
Tung TH, Mackinnon SE: Flexor digitorum superficialis nerve
transfer to restore pronation: two case reports and anatomic
study. J Hand Surg [Am] 26:1065–1072, 2001
Tung TH, Novak CB, Mackinnon SE: Nerve transfers to the biceps and brachialis branches to improve elbow flexion strength
after brachial plexus injuries. J Neurosurg 98:313–318, 2003
Tung TH, Weber RV, Mackinnon SE: Nerve transfers for the
upper and lower extremities. Oper Tech Orthop 14:213–222,
2004
Vernadakis AJ, Humphreys DB, Mackinnon SE: Distal anterior
interosseous nerve in the recurrent motor branch graft for reconstruction of a median nerve neuroma-in-continuity. J Reconstr
Microsurg 20:7–11, 2004
Wang Y, Zhu S: Transfer of a branch of the anterior interosseous nerve to the motor branch of the median nerve and ulnar
nerve. Chin Med J 110:216–219, 1997
Weber RV, Mackinnon SE: Nerve transfers in the upper extremity. J Am Soc Surg Hand 4:200–213, 2004
Weinberger LM: Non-traumatic paralysis of the dorsal interosseous nerve. Surg Gynecol Obstet 69:358, 1939
Manuscript submitted April 14, 2005.
Accepted February 14, 2007.
Address reprint requests to: Susan E. Mackinnon, M.D., Division
of Plastic and Reconstructive Surgery, Washington University School
of Medicine, Suite 5401, 660 South Euclid Avenue, St. Louis, Missouri 63110. email: [email protected].
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