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Restoration of Prehension Using Double Free Muscle Technique After Complete Avulsion of Brachial Plexus in Children: A Report of Three Cases
Restoration of Prehension Using Double Free Muscle Technique After Complete Avulsion of Brachial Plexus in Children: A Report of Three Cases Yasunori Hattori, MD, PhD, Kazuteru Doi, MD, PhD, Keisuke Ikeda, MD, Jose Miguel Pagsaligan, MD, Masao Watanabe, Ogori, Yamaguchi, Japan
Purpose: Brachial plexus injury in children, excluding birth palsy, is relatively rare and seldom reported. We report our technique, the results of this procedure, and problems we encountered in treating children with brachial plexus injury. Methods: From 1999 through 2002, we treated 3 children with complete avulsion of the brachial plexus due to trauma by using double free muscle technique (DFMT) with a nerve transfer procedure using the contralateral seventh cervical nerve root transfer to reconstruct prehensile function. There were 2 boys aged 5 and 11 years and a girl aged 4 years. All patients were followed up for at least 3 years after the surgery. Results: All the transferred muscles survived without any vascular complications and were reinnervated successfully. The average active range of elbow flexion was 125° (range, 90°–145°). The average total active range of motion of the fingers was 69° (range, 40°–102°). All patients obtained voluntary prehensile function and could use the reconstructed hand for activities of daily living. They were able to lift and carry light objects with the reconstructed hand and heavy objects with both hands. Conclusions: The results of DFMT for reconstruction of BPI in children were encouraging. Appropriate postoperative rehabilitation under close supervision is important to obtain useful prehensile function. (J Hand Surg 2005;30A:812– 819. Copyright © 2005 by the American Society for Surgery of the Hand.) Key words: Traumatic brachial plexus injury, functioning free muscle transfer, contralateral seventh cervical root transfer, child, prehension.
From the Department of Orthopedic Surgery, Ogori Daiichi General Hospital and Yamaguchi University School of Medicine, Ogori, Yamaguchi, and Department of Rehabilitation, Ogori Daiichi General Hospital, Ogori, Yamaguchi, Japan. Received for publication April 28, 2004; accepted in revised form December 14, 2004. 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. Corresponding author: Yasunori Hattori, MD, PhD, Department of Orthopedic Surgery, Ogori Daiichi General Hospital, Shimogo, 862-3, Ogori, Yoshikigun, Yamaguchi, Japan; [email protected]. Copyright © 2005 by the American Society for Surgery of the Hand 0363-5023/05/30A04-0026$30.00/0 doi:10.1016/j.jhsa.2004.12.011
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Table 1. Patient Data Case
Affected Side
Gender/Age at Injury
Extent of Injury
1
L
M/5 y, 10 mo
C5-T1: pre
2
L
F/4 y, 9 mo
C5: post C6-T1: pre
3
L
M/11 y, 1 mo
C5,6: post C7-T1: pre
Surgical Procedures
Injury–Brachial Plexus Exploration
Follow-Up Period
4.5 mo
4 y, 6 mo
3.5 mo
4 y, 1 mo
1.5 mo
3 y, 3 mo
CC7–VUNG–Ra, Ss DFMT Volar Capsulodesis of MPj C5–VUNG–Ss, PC CC7–VUNG–Me DFMT Tenolysis C5,6–VUNG–UT CC7–VUNG–PC DFMT
Me, median nerve; PC, posterior cord; post, postganglionic injury; pre, preganglionic injury; Ra, radial nerve; Ss, suprascapular nerve; UT, upper trunk.
Recently the restoration of prehension after complete avulsion of the brachial plexus has been the focus in reconstruction of upper-limb function after brachial plexus injury (BPI). For this purpose several procedures—including nerve transfer to the median nerve using extraplexal nerves, such as the intercostal nerves, or the contralateral seventh cervical nerve root transfer (CC7)1– 4 and combined functioning free muscle transfer (FFMT)3,5— have been reported. We developed the double free muscle technique (DFMT) using 2 FFMTs to restore the prehensile function and reported the long-term results of this procedure in 26 cases.5 This technique yielded the most reliable prehensile function after irreparable injuries. We have performed DFMT in 50 patients with complete avulsion of the brachial plexus from 1990 through 2002. Among them 3 patients were children who were not included in our previous report.5 In this paper we report our technique, the results, and the problems in treating children with BPI.
Patients From 1999 to 2002, 3 children with BPI were treated surgically in our hospital. There were 2 boys aged 5 and 11 years and a girl aged 4 years. All the children were victims of motor vehicle accidents. Preoperative evaluation included a complete history, a detailed clinical examination, and cervical myelography. The intervals from injury to brachial plexus exploration were 4.5, 3.5, and 1.5 months in patients 1, 2, and 3, respectively. Final diagnosis was confirmed intraoperatively on surgical exploration of the brachial plexus combined with electrophysiologic testing and measurement of choline acetyltransferase activity.6,7 All patients had complete injury of the
brachial plexus. In patient 1 all roots had preganglionic injury. In patient 2 the C5 root was diagnosed as postganglionic injury and the C6 to T1 roots as preganglionic injury. In patient 3 the C5 and C6 roots had postganglionic injury and the C7 to T1 roots had preganglionic injury. Overall patient data are summarized in Table 1.
Surgical Procedures The original technique of DFMT consisted of 5 established reconstructive procedures5: (1) surgical exploration of the brachial plexus, intraoperative diagnosis using electrophysiologic testing, and repair of the disrupted cervical roots when possible; (2) the first FFMT supplied by spinal accessory nerve transfer to restore elbow flexion and finger extension; (3) the second FFMT supplied by the fifth and sixth intercostal nerves to restore finger flexion; (4) transfer of the third and fourth intercostal nerves to the motor branch of the triceps brachii muscle (done concomitantly with the second FFMT) to restore elbow extension; and (5) transfer of the supraclavicular nerve or the intercostal sensory rami to the median nerve or the ulnar nerve component of the medial cord of the brachial plexus (done concomitantly with the second FFMT) to restore hand sensibility. The surgical technique in pediatric cases was basically the same as in adults except for some modification. Brachial plexus exploration was performed in the usual manner. After the completion of intraoperative diagnosis nerve reconstruction was performed. In patient 1, CC7 was transferred to supply of the radial nerve and suprascapular nerve via a 22-cm free vascularized ulnar nerve graft (VUNG) based on the superior ulnar collateral artery (SUCA)
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along with its venae comitantes. In patient 2 ipsilateral C5 root was used to supply the suprascapular nerve and posterior cord via a 10-cm free VUNG based on the SUCA and CC7 was used to supply the median nerve via a 22-cm free VUNG based on the ulnar artery (UA) and its venae comitantes. In patient 3 ipsilateral C5 and C6 roots were used to supply the upper trunk via the 10-cm free VUNG based on the SUCA and CC7 was transferred to the posterior cord via the 25-cm free VUNG based on the UA. In patients 2 and 3 the whole length of the ulnar nerve was harvested from its division at the medial cord down to the palm along with the SUCA and the UA as its vascular pedicle. The ulnar nerve then was divided into 2 segments. In the use of ipsilateral C5 or C6 the vascular pedicle of VUNG was anastomosed to the ipsilateral transverse cervical artery and vein, whereas in the use of CC7 anastomosis was done to the contralateral transverse cervical artery and vein. The first FFMT was performed 2 or 3 months after the exploration of the brachial plexus and nerve reconstruction. For restoration of elbow flexion and finger extension contralateral gracilis muscle was transferred and supplied by the spinal accessory nerve. Three months after the first FFMT the second FFMT was carried out. For restoration of finger flexion ipsilateral gracilis muscle was transferred and supplied by the third and fourth intercostal nerves. In patients 1 and 3 the second intercostal nerve and sensory branch of third intercostal nerve were transferred to the median nerve for sensory restoration of the hand.
Postoperative Management The upper limb was immobilized without tension on the transferred muscles, the motor nerves, and the anastomosed vessels for 4 weeks after each FFMT. Gentle passive exercises for the elbow and the metacarpophalangeal joints then were started. After electromyographic (EMG) documentation of reinnervation of the transferred muscle EMG biofeedback technique was started to train the transferred muscles. After recovery of active elbow and finger movements EMG biofeedback technique was started to train for independent finger extension and flexion.
Secondary Reconstruction In patient 1 volar capsulodesis of the metacarpophalangeal joints of the index to small fingers was done to correct the intrinsic minus deformity 3 years after the first FFMT. In patient 2 tenolysis was done on the
first FFMT (finger extensor) 1.5 years after the first FFMT.
Assessment of Results Early results. Survival of transferred muscles was evaluated by monitoring the skin flap of the gracilis muscles. Reinnervation of transferred muscles was evaluated by needle electromyograms.
Long-term results. All patients had long-term evaluation at least 3 years after the first surgery (exploration of the brachial plexus and nerve reconstruction). The parameters that were evaluated included the range of active motion of the shoulder, elbow, and finger joints, and sensory recovery. Sensory recovery of the median nerve territory of the hand was tested with Semmes-Weinstein monofilament test. Results All the transferred muscles survived without any vascular complications and were reinnervated successfully as detected electromyographically 2 to 4 months after surgery. Voluntary contraction was noted 1 to 2 months later. Regarding the neurologic deficits of the contralateral upper limb after CC7 transection all patients complained of numbness over the palmar side of the thumb, index, and middle fingers; however, it was improved completely within 3 months after surgery. None of the patients experienced any muscle weakness of the limb even on the first day after surgery. None of the patients had any complications related to the surgery or needed blood transfusion. At the final follow-up examination active abduction of the shoulder was 30°, 60°, and 30° in patients 1, 2, and 3, respectively. Active external rotation of shoulder was 60°, 60°, and ⫺60° in patients 1, 2, and 3, respectively. In patient 1 recovery of suprasupinatus and infrasupinatus muscles was good; however, active abduction and flexion were not excellent because of residual long thoracic nerve palsy (winging scapula).8 In patient 3 good recovery of suprascapular nerve and no winging scapula were noted but the shoulder function was limited by joint contracture. Active range of elbow flexion was 140°, 145°, and 90° in patients 1, 2, and 3, respectively. Although active range of elbow flexion was not full the strength of elbow flexion was equivalent to M4 in all patients. Voluntary extension of the elbow was limited by postoperative contracture of the elbow joint. The mean range of elbow extension was ⫺30°. In
Middle
abd, abduction; DIPJ, distal interphalangeal joint; Ext, extension; Ext Ro, external rotation; Flex, flexion; in ro, internal rotation; MPJ, metacarpophalangeal joint; PIPJ, proximal interphalangeal joint; ROM, range of motion; SWT, Semmes-Weinstein Test. *Average active ROM of 4 fingers.
4.31 (⫹) 4.31 (⫹) 4.56 (⫹)
Index Thumb
4.31 (⫹) 4.31 (⫹) 4.56 (⫹) 102 66 40 –10/42 –5/10 None
DIPJ PIPJ
–20/75 –35/80 –40/65 –20/35 –20/36 –10/25 (⫹) (⫹) (⫹)
MPJ Flex
140 145 90 –35 –25 –30
Ext In Ro
60 60 80 60 60 –60
Ext Ro
10 50 0 1 2 3
Abd Flex Patient
ROM of Shoulder (°)
Table 2. Overall Results
A 5-year-old boy who had sustained left complete BPI was referred to our hospital 4 months after the injury. Clinical examination showed that his left brachial plexus was paralyzed completely. A preoperative myelogram showed traumatic meningoceles from the C5 to T1 roots. Exploration of the brachial plexus was performed 4.5 months after the injury. Intraoperative electrophysiologic testing and measurement of choline acetyltransferase activity confirmed preganglionic injury of all 5 roots. The CC7 was transferred to the radial and suprascapular nerve via a VUNG for restoration of shoulder function and elbow extension. Two months after the exploration the first FFMT was performed; three months after the first FFMT the second FFMT was performed. The second intercostal nerve and the sensory branch of the third intercostal nerve were transferred to the median nerve for sensory restoration of the hand. The postoperative course was uneventful. Electromyography showed evidence of reinnervation of the suprasupinatus muscle at 4.5 months and of the triceps brachii muscle at 7 months after CC7 neurotization to the suprascapular and radial nerves. Electromyographic reinnervation of the first FFMT was
ROM of Elbow (°)
Representative Case (Patient 1)
30 50 30
Dynamic Elbow Stability
Active ROM of Fingers*(°)
TAM of Fingers (°)
Sensory Recovery (SWT)
DFMT, because 2 FFMTs work for elbow flexion and finger function, triceps brachii muscle function is imperative to negate the tendency of elbow flexion while moving fingers and voluntarily positioning the hand in space.5,9 We defined such antagonist function of triceps brachii as dynamic elbow stability.5,9 Although power of elbow extension was equivalent to M2 all patients obtained dynamic elbow stability and were able to stabilize the elbow joint while activating the transferred muscles for finger functions with the aid of gravity. The average total active range of motion (TAM) of the 4 fingers was 102°, 66°, and 40° in patients 1, 2, and 3, respectively. In patient 2, in addition to the voluntary movement of 4 fingers flexion and opposition of the thumb were restored by good recovery of CC7 neurotization to the median nerve. Thumb motion was visible 1 year after the procedure. Clinically the thumb motion was independent from the contralateral side. All patients obtained protective sensation (at least 4.56 on Semmes-Weinstein test) in the median nerve territory of the hand 1.5 to 2 years after the sensory reconstructive procedure. During the follow-up period none of the patients had causalgia or any skin ulcers on the reconstructed limb. Overall results are summarized in Table 2.
4.31 (⫹) 4.31 (⫹) 4.56 (⫹)
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obtained at 3 months and voluntary contraction of transferred muscle was visible at 4.5 months after surgery. Electromyographic reinneravtion of the second FFMT was confirmed 3.5 months after surgery. The power of reinnervated muscles increased gradually. Two years after the exploration of the brachial plexus volar capsulodesis of the metacarpophalangeal joints of the index to small fingers was performed to correct the intrinsic minus deformity. At the final follow-up examination 4.5 years after initial surgery active range of elbow motion was ⫺35° in extension and 140° in flexion. The patient was able to flex and extend his fingers independent of the position of the elbow. Although the strength of elbow extension was equivalent to M2 recovery of triceps brachii muscle was adequate enough to obtain the dynamic elbow stability. The total active motion (TAM) was 102°. He could use the reconstructed hand well in activities of daily living. He could control the movement of the reconstructed limb in any position and was able to lift and carry light objects with the involved hand and heavy objects with both hands. Postoperative function of the reconstructed upper extremity is shown in Figure 1.
Discussion Brachial plexus injury in children— excluding birth palsy—is relatively rare and is seldom reported. To the best of our knowledge only 3 reports have focused on the results of surgical reconstruction of BPI in children. Boome10 reported on 16 children seen over 14 years; however, he did not describe fully the type and extent of injury, detailed surgical procedures, or functional outcome. Dumontier and Gilbert11 reported 25 children seen over 15 years. Sixteen had surgical repair of the brachial plexus, including 8 who had total BPI. Reconstruction of the median nerve (n ⫽ 5) using either intercostal nerves transfer (3 patients) or nerve grafting (2 patients) did not provide useful motor recovery of the hand. Recently, El-Gammal et al12 reported on 11 children who had reconstruction using nerve graft and transfer. Restoration of finger flexion was attempted in 4 patients with total BPI. In 2 patients CC7 was transferred to the median nerve via a VUNG, in 1 patient ipsilateral C5 root was used for transfer to the median nerve, and in 1 patient intercostal nerves were transferred to the median nerve. Satisfactory function with M4 strength of finger and wrist flexion was achieved only in 1 patient, in whom the median nerve was supplied by intercostal nerves. The DFMT provides the most reliable prehensile
function after complete avulsion of the brachial plexus. In our previous article5 we reported that satisfactory prehensile function (voluntary finger motion with more than 30° of TAM and more than 90° of active elbow flexion with dynamic elbow stability) was restored in 17 (65%) of the 26 adult patients. We modified this reconstructive procedure in our pediatric cases by using the CC7 transfer. The use of CC7 was first reported by Gu et al in 19921 and subsequently by Chuang et al in 1993.3 Recently there were some reports on the use of CC7 for brachial plexus reconstruction.2,4,13,14 Contralateral seventh cervical nerve root transfer is relatively new and may be a valuable transfer; however, its efficacy, safety, and selection of recipient nerve remains controversial. In the previous reports CC7 was used mainly to supply the median nerve. Gu et al2 had excellent results in 5 of 8 cases (63%) and their patients achieved motor recovery of the wrist and finger flexion up to M3 to M4. In the report of Waikakul et al,13 however, only 20 of 96 cases (21%) achieved M3 or M4 strength of wrist and finger flexion. In the series of Songcharoen et al4 6 of the 21 patients (29%) achieved the satisfactory result of finger flexion. They also performed multiple nerve transfer, including the use of phrenic nerve and spinal accessory nerve for restoration of shoulder and elbow function. They concluded that even though the result of CC7 to the median nerve was better than the other donor nerve the success rate of this procedure was still far too low. In addition to these unreliable results of transfer to the median nerve using CC7 there is a major disadvantage regarding their strategy to reconstruct hand function of a completely paralyzed upper extremity after BPI. Because they did not reconstruct the finger extension as an antagonist function of finger flexion the dynamic splint for finger extension must be worn permanently to use the reconstructed hand in activities of daily living. It should be emphasized that such a splint is troublesome and inconvenient for patients with a BPI who have a normal contralateral upper limb. For these reasons we believe that the independent function of finger extension and flexion reconstructed by DFMT has superior results compared with the median nerve reconstruction (finger flexion) using CC7 alone. With DFMT the importance of elbow stability for useful prehension is well recognized.5,9 To improve the adaptability of the reconstructed hand for activities of daily living stability and voluntary movement of the shoulder should be considered.8 For these reasons we used mainly CC7 for reconstruction of
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Figure 1. Postoperative function of patient 1 at final follow-up evaluation. (A) Extension of elbow. (B) Flexion of elbow. (C) Finger extension in elbow flexion. (D) Finger flexion in elbow flexion.
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elbow extension and shoulder function.14 In patient 1, CC7 was transferred to the radial nerve and suprascapular nerve. The patient could extend the wrist joint against gravity and had enough triceps brachii strength to obtain dynamic elbow stability with the aid of gravity. Despite good recovery of the suprascapular nerve, however, active abduction of the shoulder was 30° because of the winging scapula (long thoracic nerve palsy).8 In patient 3, CC7 was used to transfer to the posterior cord. The patient obtained M2 strength of the triceps brachii muscle and dynamic elbow stability. In the original DFMT procedure elbow extension was reconstructed using intercostal nerve transfer to the triceps branch of the radial nerve, and dynamic elbow stability was obtained in 14 of 24 patients (58%).9 The results of CC7 for reconstruction of elbow stability might be superior to the intercostal nerve transfer. In patient 2, C5 root was available and was used to supply the suprascapular nerve and posterior cord. This patient was the youngest in this series and had great potential of nerve recovery. Thus, we used CC7 to supply the median nerve for recovery of thumb function. The patient obtained satisfactory function of the thumb, with M3 strength of the flexor pollicis longus and opposition, and good sensory recovery of the hand. In the second FFMT the tendon of the transferred muscle was connected to the flexor digitorum profundus tendons in end-to-side fashion. Although the result of the second FFMT was strong enough strength of finger flexion could be further augmented by restored flexor digitorum profundus supplied by CC7. Function of the restored flexor digitorum profundus was clinically independent from the contralateral side, and it coordinated well with function of the second FFMT. Postoperative rehabilitation is very important to achieve useful prehensile function after DFMT. The detailed rehabilitation program has been reported previously.5 We used the same program in children. Compared with our adult patients postoperative reeducation of transferred muscles was easier and children could adjust well with the new function without need for a special program. After the EMG reinnervation of transferred muscles, an EMG biofeedback technique was useful to increase the muscle strength and train for independent finger extension and flexion. Motivation and understanding for postoperative rehabilitation, however, were more important in children. The close supervision from a hand therapist and parents’ cooperation are mandatory for a successful rehabilitation. Two of our patients (1, 2) had strict
postoperative rehabilitation in our rehabilitation center with excellent outcome of prehensile function. The other child (patient 3) had rehabilitation at another rehabilitation center; we could not follow this patient closely after surgery. He lacked motivation for and understanding of postoperative rehabilitation. Despite the good motor recovery of FFMT his functional result was not excellent because of joint contracture and adhesion of transferred muscles. The use of FFMT in the reconstruction of a severely paralyzed upper extremity is well documented; it is now accepted and considered valuable for extremity reconstruction not only in the adults but also in children.15–17 We performed 208 FFMTs in 147 patients for reconstruction of a severely paralyzed extremity from 1982 through 2002. Among them there were 18 FFMTs in 13 children (age range, 2–12 years).17 There were no statistical differences between FFMTs performed in children and in adults regarding the rate of postoperative vascular complications and survival. Although microvascular anastomosis of smaller vessels was mandatory for FFMT in children we did not experience any difficulties in microsurgical procedures. The diameter of the vessels in children is large in proportion to their body size.18 From our experiences the diameter of the nutrient vessel of gracilis muscle in a 2-year-old girl was approximately 1 mm, which was large enough to perform a reliable microvascular anastomosis. There are, however, specific considerations regarding FFMT in children compared with adults. The possible serious complication after FFMT in children is its influence on skeletal growth. In DFMT 2 FFMTs act as the elbow flexor5; the first FFMT acts as the main elbow flexor and the second FFMT acts as a supplemental elbow flexor. If the transferred muscle is not able to grow flexion contracture of the elbow joint should worsen gradually in proportion to skeletal growth. Although elbow flexion contracture was evident in our 3 patients after DFMT with a long-term follow-up period, the contracture had not worsened gradually with time. Imbalance of power strength between elbow flexion and extension caused this contracture. We believe that transferred muscle can grow in proportion to skeletal growth. The results of DFMT for reconstruction of traumatic BPI in children were encouraging and superior to those achieved in adults. Because of the great potential of nerve recovery a child with a BPI is a good candidate for reconstruction with DFMT. Appropriate postoperative management and a close re-
Hattori et al / Brachial Plexus Injury in Children
lationship between patient and hand therapist are important to complete the rehabilitation and obtain useful prehensile function.
9.
References 1. Gu Y-D, Zhang G-M, Chen D-S, Yan J-G, Cheng X-M, Chen L. Seventh cervical nerve root transfer from the contralateral healthy side for treatment of brachial plexus root avulsion. J Hand Surg 1992;17B:518 –521. 2. Gu Y-D, Chen D-S, Zhang G-M, Cheng X-M, Xu J-G, Zhang L-Y, et al. Long-term functional results of contralateral C7 transfer. J Reconstr Microsurg 1998;14:57–59. 3. Chuang DC-C, Wei F-C, Noordhoff MS. Cross-chest C7 nerve grafting followed by free muscle transplantations for the treatment of total avulsed brachial plexus injuries: a preliminary report. Plast Reconstr Surg 1993;92:717–727. 4. Songcharoen P, Wongtrakul S, Mahaisavariya B, Spinner RJ. Hemi-contralateral C7 transfer to median nerve in the treatment of root avulsion brachial plexus injury. J Hand Surg 2001;26:1058 –1064. 5. Doi K, Muramatsu K, Hattori Y, Otsuka K, Tan S-H, Nanda V, Watanabe M. Restoration of prehension with the double free muscle technique following complete avulsion of the brachial plexus: Indication and long-term results. J Bone Joint Surg 2000;82A:652– 666. 6. Hattori Y, Doi K, Dhawan V, Ikeda K, Kaneko K, Ohi R. Choline acetyltransferase activity and evoked spinal cord potentials for diagnosis of brachial plexus injury. J Bone Joint Surg 2004;86B:70 –73. 7. Hattori Y, Doi K, Fukushima S, Kaneko K. The diagnostic value of intraoperative measurement of choline acetyltransferase activity during brachial plexus surgery. J Hand Surg 2000;25B:509 –511. 8. Doi K, Hattori Y, Ikeda K, Dhawan V. Significance of
10. 11. 12.
13.
14.
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17.
18.
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shoulder function in the reconstruction of prehension with double free- muscle transfer after complete paralysis of the brachial plexus. Plast Reconstr Surg 2003;112:1596 –1603. Doi K, Shigetomi M, Kaneko K, Tan S-H, Hiura Y, Hattori Y, Kawakami F. Significance of elbow extension in reconstruction of prehension with reinnervated free-muscle transfer following complete brachial plexus avulsion. Plast Reconstr Surg 1997;100:364 –372. Boome RS. Traumatic brachial plexus injury. In: Gupta A, ed. The growing hand. London: Mosby, 2000:653– 657. Dumontier C, Gilbert A. Traumatic brachial plexus palsy in children. Ann Hand Surg 1990;9:351–357. El-Gammal TA, El-Sayed A, Kotb MM. Surgical treatment of brachial plexus traction injuries in children, excluding obstetric palsy. Microsurgery 2003;23:14 –17. Waikakul S, Orapin S, Vanadurongwan V. Clinical results of contralateral C7 root neurotization to the median nerve in brachial plexus injuries with total root avulsions. J Hand Surg 1999;24B:556 –560. Hattori Y, Doi K, Toh S, Ohi R. Short-term results of contralateral C7 transfer for brachial plexus reconstruction. J Jpn Soc Surg Hand 2001;18:213–217. Zuker RM, Egerszegi EP, Manktelow RT, McLeod A, Candlish S. Volkmann’s ischemic contracture in children: the results of free vascularized muscle transplantation. Microsurgery 1991;12:341–345. Baliarsing AS, Doi K, Hattori Y. Bilateral elbow flexion reconstruction with functioning free muscle transfer for obstetric brachial plexus palsy. J Hand Surg 2002;27B:484 – 487. Doi K, Hattori Y, Ikeda K, Ejiri S. Free muscle transfer for reconstruction of extremities in children. J Jpn Soc Reconstr Microsurg 2003;16:238 –247. Hattori Y, Doi K, Ikeda K. Replantation in infants and young children. J Jpn Soc Surg Hand 2001;18:204 –210.
Purpose: Brachial plexus injury in children, excluding birth palsy, is relatively rare and seldom reported. We report our technique, the results of this procedure, and problems we encountered in treating children with brachial plexus injury. Methods: From 1999 through 2002, we treated 3 children with complete avulsion of the brachial plexus due to trauma by using double free muscle technique (DFMT) with a nerve transfer procedure using the contralateral seventh cervical nerve root transfer to reconstruct prehensile function. There were 2 boys aged 5 and 11 years and a girl aged 4 years. All patients were followed up for at least 3 years after the surgery. Results: All the transferred muscles survived without any vascular complications and were reinnervated successfully. The average active range of elbow flexion was 125° (range, 90°–145°). The average total active range of motion of the fingers was 69° (range, 40°–102°). All patients obtained voluntary prehensile function and could use the reconstructed hand for activities of daily living. They were able to lift and carry light objects with the reconstructed hand and heavy objects with both hands. Conclusions: The results of DFMT for reconstruction of BPI in children were encouraging. Appropriate postoperative rehabilitation under close supervision is important to obtain useful prehensile function. (J Hand Surg 2005;30A:812– 819. Copyright © 2005 by the American Society for Surgery of the Hand.) Key words: Traumatic brachial plexus injury, functioning free muscle transfer, contralateral seventh cervical root transfer, child, prehension.
From the Department of Orthopedic Surgery, Ogori Daiichi General Hospital and Yamaguchi University School of Medicine, Ogori, Yamaguchi, and Department of Rehabilitation, Ogori Daiichi General Hospital, Ogori, Yamaguchi, Japan. Received for publication April 28, 2004; accepted in revised form December 14, 2004. 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. Corresponding author: Yasunori Hattori, MD, PhD, Department of Orthopedic Surgery, Ogori Daiichi General Hospital, Shimogo, 862-3, Ogori, Yoshikigun, Yamaguchi, Japan; [email protected]. Copyright © 2005 by the American Society for Surgery of the Hand 0363-5023/05/30A04-0026$30.00/0 doi:10.1016/j.jhsa.2004.12.011
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Table 1. Patient Data Case
Affected Side
Gender/Age at Injury
Extent of Injury
1
L
M/5 y, 10 mo
C5-T1: pre
2
L
F/4 y, 9 mo
C5: post C6-T1: pre
3
L
M/11 y, 1 mo
C5,6: post C7-T1: pre
Surgical Procedures
Injury–Brachial Plexus Exploration
Follow-Up Period
4.5 mo
4 y, 6 mo
3.5 mo
4 y, 1 mo
1.5 mo
3 y, 3 mo
CC7–VUNG–Ra, Ss DFMT Volar Capsulodesis of MPj C5–VUNG–Ss, PC CC7–VUNG–Me DFMT Tenolysis C5,6–VUNG–UT CC7–VUNG–PC DFMT
Me, median nerve; PC, posterior cord; post, postganglionic injury; pre, preganglionic injury; Ra, radial nerve; Ss, suprascapular nerve; UT, upper trunk.
Recently the restoration of prehension after complete avulsion of the brachial plexus has been the focus in reconstruction of upper-limb function after brachial plexus injury (BPI). For this purpose several procedures—including nerve transfer to the median nerve using extraplexal nerves, such as the intercostal nerves, or the contralateral seventh cervical nerve root transfer (CC7)1– 4 and combined functioning free muscle transfer (FFMT)3,5— have been reported. We developed the double free muscle technique (DFMT) using 2 FFMTs to restore the prehensile function and reported the long-term results of this procedure in 26 cases.5 This technique yielded the most reliable prehensile function after irreparable injuries. We have performed DFMT in 50 patients with complete avulsion of the brachial plexus from 1990 through 2002. Among them 3 patients were children who were not included in our previous report.5 In this paper we report our technique, the results, and the problems in treating children with BPI.
Patients From 1999 to 2002, 3 children with BPI were treated surgically in our hospital. There were 2 boys aged 5 and 11 years and a girl aged 4 years. All the children were victims of motor vehicle accidents. Preoperative evaluation included a complete history, a detailed clinical examination, and cervical myelography. The intervals from injury to brachial plexus exploration were 4.5, 3.5, and 1.5 months in patients 1, 2, and 3, respectively. Final diagnosis was confirmed intraoperatively on surgical exploration of the brachial plexus combined with electrophysiologic testing and measurement of choline acetyltransferase activity.6,7 All patients had complete injury of the
brachial plexus. In patient 1 all roots had preganglionic injury. In patient 2 the C5 root was diagnosed as postganglionic injury and the C6 to T1 roots as preganglionic injury. In patient 3 the C5 and C6 roots had postganglionic injury and the C7 to T1 roots had preganglionic injury. Overall patient data are summarized in Table 1.
Surgical Procedures The original technique of DFMT consisted of 5 established reconstructive procedures5: (1) surgical exploration of the brachial plexus, intraoperative diagnosis using electrophysiologic testing, and repair of the disrupted cervical roots when possible; (2) the first FFMT supplied by spinal accessory nerve transfer to restore elbow flexion and finger extension; (3) the second FFMT supplied by the fifth and sixth intercostal nerves to restore finger flexion; (4) transfer of the third and fourth intercostal nerves to the motor branch of the triceps brachii muscle (done concomitantly with the second FFMT) to restore elbow extension; and (5) transfer of the supraclavicular nerve or the intercostal sensory rami to the median nerve or the ulnar nerve component of the medial cord of the brachial plexus (done concomitantly with the second FFMT) to restore hand sensibility. The surgical technique in pediatric cases was basically the same as in adults except for some modification. Brachial plexus exploration was performed in the usual manner. After the completion of intraoperative diagnosis nerve reconstruction was performed. In patient 1, CC7 was transferred to supply of the radial nerve and suprascapular nerve via a 22-cm free vascularized ulnar nerve graft (VUNG) based on the superior ulnar collateral artery (SUCA)
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along with its venae comitantes. In patient 2 ipsilateral C5 root was used to supply the suprascapular nerve and posterior cord via a 10-cm free VUNG based on the SUCA and CC7 was used to supply the median nerve via a 22-cm free VUNG based on the ulnar artery (UA) and its venae comitantes. In patient 3 ipsilateral C5 and C6 roots were used to supply the upper trunk via the 10-cm free VUNG based on the SUCA and CC7 was transferred to the posterior cord via the 25-cm free VUNG based on the UA. In patients 2 and 3 the whole length of the ulnar nerve was harvested from its division at the medial cord down to the palm along with the SUCA and the UA as its vascular pedicle. The ulnar nerve then was divided into 2 segments. In the use of ipsilateral C5 or C6 the vascular pedicle of VUNG was anastomosed to the ipsilateral transverse cervical artery and vein, whereas in the use of CC7 anastomosis was done to the contralateral transverse cervical artery and vein. The first FFMT was performed 2 or 3 months after the exploration of the brachial plexus and nerve reconstruction. For restoration of elbow flexion and finger extension contralateral gracilis muscle was transferred and supplied by the spinal accessory nerve. Three months after the first FFMT the second FFMT was carried out. For restoration of finger flexion ipsilateral gracilis muscle was transferred and supplied by the third and fourth intercostal nerves. In patients 1 and 3 the second intercostal nerve and sensory branch of third intercostal nerve were transferred to the median nerve for sensory restoration of the hand.
Postoperative Management The upper limb was immobilized without tension on the transferred muscles, the motor nerves, and the anastomosed vessels for 4 weeks after each FFMT. Gentle passive exercises for the elbow and the metacarpophalangeal joints then were started. After electromyographic (EMG) documentation of reinnervation of the transferred muscle EMG biofeedback technique was started to train the transferred muscles. After recovery of active elbow and finger movements EMG biofeedback technique was started to train for independent finger extension and flexion.
Secondary Reconstruction In patient 1 volar capsulodesis of the metacarpophalangeal joints of the index to small fingers was done to correct the intrinsic minus deformity 3 years after the first FFMT. In patient 2 tenolysis was done on the
first FFMT (finger extensor) 1.5 years after the first FFMT.
Assessment of Results Early results. Survival of transferred muscles was evaluated by monitoring the skin flap of the gracilis muscles. Reinnervation of transferred muscles was evaluated by needle electromyograms.
Long-term results. All patients had long-term evaluation at least 3 years after the first surgery (exploration of the brachial plexus and nerve reconstruction). The parameters that were evaluated included the range of active motion of the shoulder, elbow, and finger joints, and sensory recovery. Sensory recovery of the median nerve territory of the hand was tested with Semmes-Weinstein monofilament test. Results All the transferred muscles survived without any vascular complications and were reinnervated successfully as detected electromyographically 2 to 4 months after surgery. Voluntary contraction was noted 1 to 2 months later. Regarding the neurologic deficits of the contralateral upper limb after CC7 transection all patients complained of numbness over the palmar side of the thumb, index, and middle fingers; however, it was improved completely within 3 months after surgery. None of the patients experienced any muscle weakness of the limb even on the first day after surgery. None of the patients had any complications related to the surgery or needed blood transfusion. At the final follow-up examination active abduction of the shoulder was 30°, 60°, and 30° in patients 1, 2, and 3, respectively. Active external rotation of shoulder was 60°, 60°, and ⫺60° in patients 1, 2, and 3, respectively. In patient 1 recovery of suprasupinatus and infrasupinatus muscles was good; however, active abduction and flexion were not excellent because of residual long thoracic nerve palsy (winging scapula).8 In patient 3 good recovery of suprascapular nerve and no winging scapula were noted but the shoulder function was limited by joint contracture. Active range of elbow flexion was 140°, 145°, and 90° in patients 1, 2, and 3, respectively. Although active range of elbow flexion was not full the strength of elbow flexion was equivalent to M4 in all patients. Voluntary extension of the elbow was limited by postoperative contracture of the elbow joint. The mean range of elbow extension was ⫺30°. In
Middle
abd, abduction; DIPJ, distal interphalangeal joint; Ext, extension; Ext Ro, external rotation; Flex, flexion; in ro, internal rotation; MPJ, metacarpophalangeal joint; PIPJ, proximal interphalangeal joint; ROM, range of motion; SWT, Semmes-Weinstein Test. *Average active ROM of 4 fingers.
4.31 (⫹) 4.31 (⫹) 4.56 (⫹)
Index Thumb
4.31 (⫹) 4.31 (⫹) 4.56 (⫹) 102 66 40 –10/42 –5/10 None
DIPJ PIPJ
–20/75 –35/80 –40/65 –20/35 –20/36 –10/25 (⫹) (⫹) (⫹)
MPJ Flex
140 145 90 –35 –25 –30
Ext In Ro
60 60 80 60 60 –60
Ext Ro
10 50 0 1 2 3
Abd Flex Patient
ROM of Shoulder (°)
Table 2. Overall Results
A 5-year-old boy who had sustained left complete BPI was referred to our hospital 4 months after the injury. Clinical examination showed that his left brachial plexus was paralyzed completely. A preoperative myelogram showed traumatic meningoceles from the C5 to T1 roots. Exploration of the brachial plexus was performed 4.5 months after the injury. Intraoperative electrophysiologic testing and measurement of choline acetyltransferase activity confirmed preganglionic injury of all 5 roots. The CC7 was transferred to the radial and suprascapular nerve via a VUNG for restoration of shoulder function and elbow extension. Two months after the exploration the first FFMT was performed; three months after the first FFMT the second FFMT was performed. The second intercostal nerve and the sensory branch of the third intercostal nerve were transferred to the median nerve for sensory restoration of the hand. The postoperative course was uneventful. Electromyography showed evidence of reinnervation of the suprasupinatus muscle at 4.5 months and of the triceps brachii muscle at 7 months after CC7 neurotization to the suprascapular and radial nerves. Electromyographic reinnervation of the first FFMT was
ROM of Elbow (°)
Representative Case (Patient 1)
30 50 30
Dynamic Elbow Stability
Active ROM of Fingers*(°)
TAM of Fingers (°)
Sensory Recovery (SWT)
DFMT, because 2 FFMTs work for elbow flexion and finger function, triceps brachii muscle function is imperative to negate the tendency of elbow flexion while moving fingers and voluntarily positioning the hand in space.5,9 We defined such antagonist function of triceps brachii as dynamic elbow stability.5,9 Although power of elbow extension was equivalent to M2 all patients obtained dynamic elbow stability and were able to stabilize the elbow joint while activating the transferred muscles for finger functions with the aid of gravity. The average total active range of motion (TAM) of the 4 fingers was 102°, 66°, and 40° in patients 1, 2, and 3, respectively. In patient 2, in addition to the voluntary movement of 4 fingers flexion and opposition of the thumb were restored by good recovery of CC7 neurotization to the median nerve. Thumb motion was visible 1 year after the procedure. Clinically the thumb motion was independent from the contralateral side. All patients obtained protective sensation (at least 4.56 on Semmes-Weinstein test) in the median nerve territory of the hand 1.5 to 2 years after the sensory reconstructive procedure. During the follow-up period none of the patients had causalgia or any skin ulcers on the reconstructed limb. Overall results are summarized in Table 2.
4.31 (⫹) 4.31 (⫹) 4.56 (⫹)
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obtained at 3 months and voluntary contraction of transferred muscle was visible at 4.5 months after surgery. Electromyographic reinneravtion of the second FFMT was confirmed 3.5 months after surgery. The power of reinnervated muscles increased gradually. Two years after the exploration of the brachial plexus volar capsulodesis of the metacarpophalangeal joints of the index to small fingers was performed to correct the intrinsic minus deformity. At the final follow-up examination 4.5 years after initial surgery active range of elbow motion was ⫺35° in extension and 140° in flexion. The patient was able to flex and extend his fingers independent of the position of the elbow. Although the strength of elbow extension was equivalent to M2 recovery of triceps brachii muscle was adequate enough to obtain the dynamic elbow stability. The total active motion (TAM) was 102°. He could use the reconstructed hand well in activities of daily living. He could control the movement of the reconstructed limb in any position and was able to lift and carry light objects with the involved hand and heavy objects with both hands. Postoperative function of the reconstructed upper extremity is shown in Figure 1.
Discussion Brachial plexus injury in children— excluding birth palsy—is relatively rare and is seldom reported. To the best of our knowledge only 3 reports have focused on the results of surgical reconstruction of BPI in children. Boome10 reported on 16 children seen over 14 years; however, he did not describe fully the type and extent of injury, detailed surgical procedures, or functional outcome. Dumontier and Gilbert11 reported 25 children seen over 15 years. Sixteen had surgical repair of the brachial plexus, including 8 who had total BPI. Reconstruction of the median nerve (n ⫽ 5) using either intercostal nerves transfer (3 patients) or nerve grafting (2 patients) did not provide useful motor recovery of the hand. Recently, El-Gammal et al12 reported on 11 children who had reconstruction using nerve graft and transfer. Restoration of finger flexion was attempted in 4 patients with total BPI. In 2 patients CC7 was transferred to the median nerve via a VUNG, in 1 patient ipsilateral C5 root was used for transfer to the median nerve, and in 1 patient intercostal nerves were transferred to the median nerve. Satisfactory function with M4 strength of finger and wrist flexion was achieved only in 1 patient, in whom the median nerve was supplied by intercostal nerves. The DFMT provides the most reliable prehensile
function after complete avulsion of the brachial plexus. In our previous article5 we reported that satisfactory prehensile function (voluntary finger motion with more than 30° of TAM and more than 90° of active elbow flexion with dynamic elbow stability) was restored in 17 (65%) of the 26 adult patients. We modified this reconstructive procedure in our pediatric cases by using the CC7 transfer. The use of CC7 was first reported by Gu et al in 19921 and subsequently by Chuang et al in 1993.3 Recently there were some reports on the use of CC7 for brachial plexus reconstruction.2,4,13,14 Contralateral seventh cervical nerve root transfer is relatively new and may be a valuable transfer; however, its efficacy, safety, and selection of recipient nerve remains controversial. In the previous reports CC7 was used mainly to supply the median nerve. Gu et al2 had excellent results in 5 of 8 cases (63%) and their patients achieved motor recovery of the wrist and finger flexion up to M3 to M4. In the report of Waikakul et al,13 however, only 20 of 96 cases (21%) achieved M3 or M4 strength of wrist and finger flexion. In the series of Songcharoen et al4 6 of the 21 patients (29%) achieved the satisfactory result of finger flexion. They also performed multiple nerve transfer, including the use of phrenic nerve and spinal accessory nerve for restoration of shoulder and elbow function. They concluded that even though the result of CC7 to the median nerve was better than the other donor nerve the success rate of this procedure was still far too low. In addition to these unreliable results of transfer to the median nerve using CC7 there is a major disadvantage regarding their strategy to reconstruct hand function of a completely paralyzed upper extremity after BPI. Because they did not reconstruct the finger extension as an antagonist function of finger flexion the dynamic splint for finger extension must be worn permanently to use the reconstructed hand in activities of daily living. It should be emphasized that such a splint is troublesome and inconvenient for patients with a BPI who have a normal contralateral upper limb. For these reasons we believe that the independent function of finger extension and flexion reconstructed by DFMT has superior results compared with the median nerve reconstruction (finger flexion) using CC7 alone. With DFMT the importance of elbow stability for useful prehension is well recognized.5,9 To improve the adaptability of the reconstructed hand for activities of daily living stability and voluntary movement of the shoulder should be considered.8 For these reasons we used mainly CC7 for reconstruction of
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Figure 1. Postoperative function of patient 1 at final follow-up evaluation. (A) Extension of elbow. (B) Flexion of elbow. (C) Finger extension in elbow flexion. (D) Finger flexion in elbow flexion.
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elbow extension and shoulder function.14 In patient 1, CC7 was transferred to the radial nerve and suprascapular nerve. The patient could extend the wrist joint against gravity and had enough triceps brachii strength to obtain dynamic elbow stability with the aid of gravity. Despite good recovery of the suprascapular nerve, however, active abduction of the shoulder was 30° because of the winging scapula (long thoracic nerve palsy).8 In patient 3, CC7 was used to transfer to the posterior cord. The patient obtained M2 strength of the triceps brachii muscle and dynamic elbow stability. In the original DFMT procedure elbow extension was reconstructed using intercostal nerve transfer to the triceps branch of the radial nerve, and dynamic elbow stability was obtained in 14 of 24 patients (58%).9 The results of CC7 for reconstruction of elbow stability might be superior to the intercostal nerve transfer. In patient 2, C5 root was available and was used to supply the suprascapular nerve and posterior cord. This patient was the youngest in this series and had great potential of nerve recovery. Thus, we used CC7 to supply the median nerve for recovery of thumb function. The patient obtained satisfactory function of the thumb, with M3 strength of the flexor pollicis longus and opposition, and good sensory recovery of the hand. In the second FFMT the tendon of the transferred muscle was connected to the flexor digitorum profundus tendons in end-to-side fashion. Although the result of the second FFMT was strong enough strength of finger flexion could be further augmented by restored flexor digitorum profundus supplied by CC7. Function of the restored flexor digitorum profundus was clinically independent from the contralateral side, and it coordinated well with function of the second FFMT. Postoperative rehabilitation is very important to achieve useful prehensile function after DFMT. The detailed rehabilitation program has been reported previously.5 We used the same program in children. Compared with our adult patients postoperative reeducation of transferred muscles was easier and children could adjust well with the new function without need for a special program. After the EMG reinnervation of transferred muscles, an EMG biofeedback technique was useful to increase the muscle strength and train for independent finger extension and flexion. Motivation and understanding for postoperative rehabilitation, however, were more important in children. The close supervision from a hand therapist and parents’ cooperation are mandatory for a successful rehabilitation. Two of our patients (1, 2) had strict
postoperative rehabilitation in our rehabilitation center with excellent outcome of prehensile function. The other child (patient 3) had rehabilitation at another rehabilitation center; we could not follow this patient closely after surgery. He lacked motivation for and understanding of postoperative rehabilitation. Despite the good motor recovery of FFMT his functional result was not excellent because of joint contracture and adhesion of transferred muscles. The use of FFMT in the reconstruction of a severely paralyzed upper extremity is well documented; it is now accepted and considered valuable for extremity reconstruction not only in the adults but also in children.15–17 We performed 208 FFMTs in 147 patients for reconstruction of a severely paralyzed extremity from 1982 through 2002. Among them there were 18 FFMTs in 13 children (age range, 2–12 years).17 There were no statistical differences between FFMTs performed in children and in adults regarding the rate of postoperative vascular complications and survival. Although microvascular anastomosis of smaller vessels was mandatory for FFMT in children we did not experience any difficulties in microsurgical procedures. The diameter of the vessels in children is large in proportion to their body size.18 From our experiences the diameter of the nutrient vessel of gracilis muscle in a 2-year-old girl was approximately 1 mm, which was large enough to perform a reliable microvascular anastomosis. There are, however, specific considerations regarding FFMT in children compared with adults. The possible serious complication after FFMT in children is its influence on skeletal growth. In DFMT 2 FFMTs act as the elbow flexor5; the first FFMT acts as the main elbow flexor and the second FFMT acts as a supplemental elbow flexor. If the transferred muscle is not able to grow flexion contracture of the elbow joint should worsen gradually in proportion to skeletal growth. Although elbow flexion contracture was evident in our 3 patients after DFMT with a long-term follow-up period, the contracture had not worsened gradually with time. Imbalance of power strength between elbow flexion and extension caused this contracture. We believe that transferred muscle can grow in proportion to skeletal growth. The results of DFMT for reconstruction of traumatic BPI in children were encouraging and superior to those achieved in adults. Because of the great potential of nerve recovery a child with a BPI is a good candidate for reconstruction with DFMT. Appropriate postoperative management and a close re-
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lationship between patient and hand therapist are important to complete the rehabilitation and obtain useful prehensile function.
9.
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shoulder function in the reconstruction of prehension with double free- muscle transfer after complete paralysis of the brachial plexus. Plast Reconstr Surg 2003;112:1596 –1603. Doi K, Shigetomi M, Kaneko K, Tan S-H, Hiura Y, Hattori Y, Kawakami F. Significance of elbow extension in reconstruction of prehension with reinnervated free-muscle transfer following complete brachial plexus avulsion. Plast Reconstr Surg 1997;100:364 –372. Boome RS. Traumatic brachial plexus injury. In: Gupta A, ed. The growing hand. London: Mosby, 2000:653– 657. Dumontier C, Gilbert A. Traumatic brachial plexus palsy in children. Ann Hand Surg 1990;9:351–357. El-Gammal TA, El-Sayed A, Kotb MM. Surgical treatment of brachial plexus traction injuries in children, excluding obstetric palsy. Microsurgery 2003;23:14 –17. Waikakul S, Orapin S, Vanadurongwan V. Clinical results of contralateral C7 root neurotization to the median nerve in brachial plexus injuries with total root avulsions. J Hand Surg 1999;24B:556 –560. Hattori Y, Doi K, Toh S, Ohi R. Short-term results of contralateral C7 transfer for brachial plexus reconstruction. J Jpn Soc Surg Hand 2001;18:213–217. Zuker RM, Egerszegi EP, Manktelow RT, McLeod A, Candlish S. Volkmann’s ischemic contracture in children: the results of free vascularized muscle transplantation. Microsurgery 1991;12:341–345. Baliarsing AS, Doi K, Hattori Y. Bilateral elbow flexion reconstruction with functioning free muscle transfer for obstetric brachial plexus palsy. J Hand Surg 2002;27B:484 – 487. Doi K, Hattori Y, Ikeda K, Ejiri S. Free muscle transfer for reconstruction of extremities in children. J Jpn Soc Reconstr Microsurg 2003;16:238 –247. Hattori Y, Doi K, Ikeda K. Replantation in infants and young children. J Jpn Soc Surg Hand 2001;18:204 –210.