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A comparison of vascularized and conventional sural nerve grafts
A comparison
of vascularized
and conventional
sural nerve grafts Long-term
results of a randomized
grafts in patients with comparable
series of 27 vascularized
and 22 conventional
sural nerve
upper extremity injuries are reported. Recovery speed and
outcome depended on (1) whether or not there was an overlying skin defect, (2) how the defect was closed, and (3) which nerve was injured and at what level. Generally, a vascularixed
nerve
graft is indicated when the nerve gap is more than 6 cm and is associated with a massive skin defect or the graft is performed after reimplantation. Otherwise, results achieved with a conventional graft are equally good. (J HAND SURG 1992;17A:670-6.)
Kazuteru
Doi,
Yoko Kurafuji,
MD, OTR,
Koichi
Tamaru,
and Shinya
MD, Kawai,
Kazuhiro MD,
Sakai,
MD,
Noriyuki
Kuwata,
MD,
Ube, Japan
T
he vascularized nerve graft is different from other vascularized composite tissue grafts, such as free skin flaps and toe transfers, in that it can survive without immediate revascularization. It also differs from the conventional nerve graft in being able to survive to some extent in an unfavorable environment.’ A number of experimental studies established definite indications for vascularized nerve grafts.2-9 However, it is not clear whether axonal regeneration in vascularized nerve grafts is superior to that in conventional nerve especially when small-caliber nerve grafts are grafts, ‘O placed in healthy beds.‘, ” Clinical studies have suggested that vascularized nerve graft may be indicated for nerve grafting in the poorly vascularized scarred beds,‘2-‘9 but these conditions are difficult to reproduce experimentally.*~ lo, *OA well-controlled clinical study is necessary to establish the indications for vascularized and conventional nerve grafts. No study to date has
From the Department of Otthopaedic Surgery, Yamaguchi School of Medicine, Ube, 755, Japan.
University
Presented at the Societe Intemationale de Orthopedique et de Traumatologie 90 (SICOT 90) Meeting in Montreal, Canada, September 8 through 15, 1990. Received for publication July 18, 1991.
Feb. 22, 1991; accepted
in revised form
No benefits in any form have heen received or will be received from a commercial party related directly or indirectly to the subject of
this article. Reprint requests: Kazuteru Doi, MD, Department of Orthopaedic Surgery, Japan.
Yamaguchi
University
School of Medicine,
311132567
670
THEJOURNALOFHANDSURGERY
Fig. 1. Vascularized sural nerve graft. a, The vascular pedicle is based on either the cutaneous branch of the peroneal artery or the musculocutaneous perforating branch of the posterior tibia1 artery. b, The nerve usually is sectioned into as many as four segments. c, A skin flap can be elevated with the nerve to monitor vascular patency. (Redrawn from Doi K. et al, J HAND SURG 1987;12A:677.)
Ube, 755,
been able to control the many factors that affect recovery from nerve injuries.L2-L9 We have previously described a reliable technique for free vascularized sural nerve grafting and have reported preliminary clinical results. 13,I7 Early follow-up has been encouraging. The present report compares the
Vol. 17A, No. 4 July 1992
long-term results of individual nerve repair in the upper extremity with free vascularized and nonvascularized sural nerve grafts. Materials
and methods
A description of the surgical techniques for vascularized and nonvascularized sural nerve grafting follows. ‘I. ” Vascularized sural nerve graft. The vascularized sural nerve graft is based on either the cutaneous branch of the peroneal artery or the muscular perforating branch of the posterior tibia1 artery. It is harvested and sectioned into as many as four segments to accommodate the discrepancy between the diameters of the injured nerve and the graft while safely maintaining each segment’s vascularity by preserving the fascia intact (Fig. 1). An island of skin can be elevated with the nerve to monitor vascular patency. After the recipient site has been prepared properly for interfascicular nerve grafting and microvascular anastomosis, the vascular pedicle of the graft is divided. The sural nerve is folded, and each nerve segment is approximated individually. The circulation is restored by microvascular anastomosis. Conventional sural nerve graft. A longitudinal incision is made over the sural nerve in the lower leg, and the sural nerve is harvested. Segments that are long enough to bridge the nerve gap and approximately the same diameter as the injured nerve are created. Interfascicular nerve grafting under an operating microscope is performed with 10-O nylon. Materials. Since 1984 the senior author has assigned patients at random to undergo vascularized nerve graft or conventional graft for repair of nerve defects of the upper extremity. Patients were included when (1) their age was between 17 and 50 years, (2) the senior author personally performed the nerve grafting, (3) a sural nerve graft was used, (4) postoperative rehabilitation was performed at our hospital and by the same hand therapist, and (5) the postoperative follow-up was at least 24 months. Twenty-seven vascularized sural nerve grafts and 22 conventional grafts met these criteria and are included in this study. The followup period ranged from 24 to 40 months (mean, 26 months). Neurologic evaluation. Postoperative recovery was assessed by the speed of advancement of Tinel’s sign 90 days postoperatively, time to sensory reinnervation in the correct anatomic distribution of the repaired nerve. time to electromyographic reinnervation, and final sensory recovery and motor recovery 24 months postoperatively, according to Highet’s scalez2 for as-
Vascularized and conventional free sural nerve grafts
671
sessment of the median, ulnar, and radial nerves. The axillary nerve was assessed only by the system for evaluating the strength of the deltoid muscle developed by the British Council.22 The digital nerves were assessed according to the sensory evaluation system of the British Council, Semmes-Weinstein’s monofilament test, and the moving two-point discrimination test. Results Axillary nerve. Five axillary nerves were repaired with the use of free vascularized sural nerve grafts and three with conventional grafts (Table I). Two vascularized nerve grafts were placed between the posterior cord of the brachial plexus and the axillary nerve, and three grafts were placed distal to the division of the posterior cord. The three conventional grafts were placed distal to the division of the posterior cord. No patient had any skin defect or scarring around the nerve defect. The mean time to electromyographic reinnervation of the deltoid muscle was 6 months in the vascularized group and 4 months in the conventional group; the mean muscle strength of the deltoid at 24 months was M4.2 in the vascularized group and M4.3 in the conventional group. Neither difference was statistically significant. Median nerve Ten median nerve lesions-three high and seven low-were repaired. Three vascularized nerve grafts used for high median nerve lesions were excluded because no conventional grafts were used in patients with injuries at this level. Four of seven patients with low median nerve injury underwent vascularized nerve grafts, and two of these had an accompanying skin flap to close a massive skin defect (Table II). Three patients underwent conventional grafts after closure of a large skin defect with a groin flap. The mean speed of advancement of Tinel’s sign 2 months postoperatively was 1.8 mm/day in the vascularized group and 0.5 mm/day in the conventional group. The mean time to S2 sensory reinnervation in the fingertip distal to the distal finger crease of the thumb, index, and long fingers was 16.8 weeks in the vascularized group and 30.7 weeks in the conventional group. Time to electromyographic reinnervation of the abductor pollicis brevis muscle ranged from 6 months to 8.5 months (mean, 7.4 months) in the vascularized group and from 11 months to 14 months (mean, 12.5 months) in the conventional group. One patient who underwent conventional grafting had failed to innervate this muscle 2 years postoperatively.
672
The Journal of HAND SURGERY
Doi et al.
Table I. Demographics Case No.
and results in patients with axillary nerve lesions undergoing Nerve gap
Age
W)
(cm)
Free vascularized sural nerve graft 1 19 2 19 3 24 4 21 5 17 Mean f SD 6.0
6 6 5 I 6
Conventional nerve graft 1 18 2 21 3 17 Mean -t SD
Survival of skin flap
Time to EMG innervation of deltoid (mo)
Yes Yes No flapt No flap No flap
4.7 f
Strength of shoulder ABD* 24 mo postoperatively
3 4 7 12 4 6.0 2 3.29-?
* 0.63$ 3 5 6
nerve grafting
_ _ -
4 4 5 3 5 4.2 + 0.75$
3 4 5 4.0 k 0.82$
1.25$
4 5 4 4.3 ? 0.47:
*ABD = °ree abduction. tNo skin flap to monitor graft circulation was elevated. SDifferences were not statistically significant.
Table II. Demographic nerve grafting
Case No.
Age fyr)
Free vascularized 1 18 2 50 3 45 4 50
Skin defect
and clinical results in patients with low median nerve lesions undergoing
Length of nerve gap (cm)
sural nerve graft + 5 + 6 _ 5 _ 5
Mean k SD
Yes Yes Yes Yes
5.3 k 0.43$
Conventional nerve graft 1 31 _ 2 21 + 3 50 + Mean 2 SD
Survival of skin flap
5 10 7 7.3 f
2.053:
Speed of Tinel’s sign* (mmi
Time to S2
Time to EMG
day)
@k)
(APB) (mo)
Motor
Sensory
2.2 1.5 2.0 1.6
14 18 17 18
6 8.5 7 8
M3 M2 M3 M2
s3 s3 s3 s3
1.8 2 0.2t -
0.5 0.5 0.5 0.5 *
Final results
16.8 ”
1.64t
24 26 42
ot
30.7 f
8.06t
7.4 2 0.96t
2.5 f 0.50$
11 14 None
M2 Ml MO
12.5 k 1.50t
1 k 0.81$
3 2
ot
s3 s2 s2 2.3 2 0.47t
APB = Abductor policis brevis. *Distance Tinel’s sign advancedduring the first 3 months. tp < 0.05. PNo statisfically significant difference.
The mean outcome scores 2 years postoperatively were M2.5, S3 in the vascularized group and M 1, S2.3 in the conventional group. This difference was statistically significant (p < 0.05). Ulnar nerve. Eight ulnar nerves were repaired with four vascularized nerve grafts and four conventional grafts; there were two high lesions and six low lesions. High ulner nerve lesions. One vascularized graft and one conventional graft were used (Table III). The speed of advancement of Tinel’s sign 3 months postopera-
tiveiy, time to S2 sensory reinnervation in the tip of the small finger, time to electromyographic reinnervation of the abductor digiti minimi muscle, and level of function at 2 years were better after the vascularized nerve graft. Low ulnar nerve lesions. Four vascularized nerve grafts and three conventional grafts were implanted (Table IV). One of four skin flaps monitoring circulation of the vascularized grafts became necrotic and was excised 1 week postoperatively. This case was excluded
Vol. 17A, No. 4 July 1992
613
Vascularized and conventional free sural nerve grafts
Table III. Demographics
and clinical results in patients with high ulnar nerve lesions undergoing
nerve grafting Length of nerve Age (yr)
Skin defect
30 18
7 8
-
Survival of
Kind of Graft
graft (cm)
Speed of Tinel’s sign (mm Iday)
flap Yes
FVNG Conventional
Final results
Time to s2
Time to EMG WM)
(mo) 14 None
2.2 0.5
(mo)
Motor
Sensory
M3 Ml
s2 Sl
20 39
ADM = Abductor digiti minimi. FVNG = Free vascularized sum1 nerve graft.
Table IV. Demographics
and clinical results in patients with low ulnar nerve lesions undergoing
nerve grafting Case No.
Skin defect
Age fyr)
Free vascularized
1
1 2 3
Tinel's sign
Time to S2
(cm)
Jlap
(mmlday)
fmo)
Yes Yes Yes No
2 2 2 0.5
4 5 4 None
-
Speed of
5 6 6 I
-
1.6 + 0.65t
5.7 * 0.47t
Mean 2 SD* Conventional
Survival of
Final results Time to EMG WM)
Motor
fmo)
Sensory
sural nerve graft
31 20 12 49
2 3 4
Length of nerve gap
4.3 t
0.47t
4 5 4 12
s3 s3 s3 Sl
M3 M3 M4 Ml
6.25 + 3.34t
M3.3
t
0.47t
s3 *
ot
nerve graft -
41 22 35
0.6 f 0.08t
4.3 f 0.47t
Mean a SD
0.7 0.5 0.6
-
5 4 4
8 9 None
M2 M2 MO
s2 s2 S2
8.5 + 0.5t
M2t
s2t
6 7 I 6.7 2 0.47t
ADM = Abductor digiti minimi. *Case 4 is excluded because of skin flap necrosis.
tp < 0.05.
Table V. Demographics
and clinical results in patients with high radial nerve lesions undergoing
nerve grafting Case No.
Age fyr)
Free vascular
Length of nerve gap (cm)
Survival of
None None
8 14 11.0 2 3.00$
Yes Yes
None None None
10 8 11
Pap
Speed of Tinel’s sign (mm I day)
Time to EMG (EDC) (mo)
Final results44otor
2 2 2t
4 8 6 ? 2t
M4 M3 M3.5 + 0.5t
None 0.5 0.6
None 12 10 11 * 1t
sural nerve graft
1
18 50 Mean f SD Conventional nerve graft 2
1 2 3
Skin defect
34 32 22 Mean 2 SD
EDC = Extensor digiti communis. *No significant difference. tp = < 0.05.
9.7 ?
1.24$
0.55 zk 0.05t
MO M2 Ml MI.0 t 0.8”F
614
The Journal of HAND SURGERY
Doi et al.
Table VI, Demographics grafting
and clinical results in patients with low radial nerve lesions undergoing
I
Case No.
Age (yr)
Free vascular 1 2
sural nerve graft 50 50
Conventional
I 2
Skin defect
I
Length of nerve
Time to EMG
gap (cm)
Survival of flap
5 5
Yes Yes
5 5.5 5.3 + 0.25*
M4 M4 M4*
-
5 6 5.5 2 0.5*
M4 M2 M3*
None None
Mean k SD nerve graft 37 None 45 None Mean k SD
nerve
5* 5 4 4.5 k 0.5*
(EPLJ fmo)
Final results-Motor
EPL = Extensor policis longus.
*Not statistically significant.
Table VII. Demographics nerve grafting
and clinical results of patients with digital nerve lesions undergoing
Final results Case No.
Age fvri
Skin defect
Length of nerve gap
Survival of
(emi
Pap
Speed of Tinel’s sign (mm/day)
6 6 6 6 5 5 5
Yes Yes Partial Yes Yes Yes Yes
2.0 1.2 0.8 1.2 3.0 2.0 2.0
3 3 6 4 3 4 4
5.6 k 0.49$
1.74 k 0.686
3.9 2 0.99§
5 4 7 6 6 6
0.5 0.7 0.4 0.6 0.5 0.5
13 12 8 8 None 16
Free vascular sural nerve graft 1 50 None 2 19 None 3 32 None 4 42 None 5 46 Yes 6 42 None 1 36 None Mean k SD Conventional 1 2 3 4 5 6
nerve graft 46 None 50 None 45 None 24 Yes 32 Yes 49 Yes
Mean -t SD
5.7 z!T0.94$
-
0.53
Time to S2 fmo)
+ 0.091
11.4 k 3.076
Moving 2PDt Sensory
Semmes-Weinstein*
Cmmi
s2 s3 s2 s4 s3 54 s3
4.17 3.61 4.17 2.83 3.61 2.83 3.61
None 8 None 4 10 6 10
3.35 k 0.53$ s2 s3 s2 s3 None s2
4.17 3.61 4.17 3.61
None 12 None 8
4.17
None
3.37 2 0.49$
*Semmes-Weinstein monofilament test. TMoving two-point discrimination. SNo significant difference. §p < 0.05.
from the evaluation. The mean advancement of the Tinel’s sign 2 months postoperatively, the mean time to S2 sensory recovery in the tip of the small finger, and the mean time to electromyographic reinnervation of the abductor digiti minimi muscle were shorter in the vascularized graft group (Table IV). Functional evaluation 2 years postoperatively was M3.3, S3 and M2, S2 for successful vascularized and conventional grafts, respectively. Differences in function between vascu-
larized and conventional grafts were significant (p < 0.05) (Table 4). Radial nerve. Nine radial nerves (five high lesions and four low lesions) were repaired with four vascularized nerve grafts and five conventional grafts (Table V). High lesions. Two high radial nerve injuries were repaired by vascularized grafts. Both skin flaps elevated to monitor circulation in the vascularized group sur-
Vol. 17A, No. 4 July 1992
vived. The mean advancement of Tinel’s sign 2 months postoperatively was faster in the vascularized graft. One conventional graft failed to regenerate through the proximal neurorrhaphy site. Sensory reinnervation to the dorsal skin over the first interosseous muscle was unreliable because some patients had cross-innervation from an adjacent nerve. The mean time to electromyographic reinnervation of the extensor digiti communis muscle in the vascularized group was quicker, and functionai evaluation 2 years postoperatively was M3.5 in the vascularized group and Ml in the conventional group. Low lesions. Two vascularized sural nerve grafts and two conventional grafts were used to repair 4 to 6 cm nerve gaps in the posterior interosseous nerve (Table VI). The mean time to electromyographic reinnervation to the extensor digiti communis muscle and the final motor evaluation were comparable in the vascularized and conventional groups. Digital nerves. Thirteen digital nerve defects in the palm were repaired with seven vascularized and six conventional grafts (Table VII). Three vascularized and five conventional grafts were used to repair a nerve defect after replantation of an amputated hand or digit. One vascularized graft accompanied a skin flap to close a skin defect of the palm. Three conventional grafts were applied secondarily after closure of a palmar skin defect by a pedicled groin flap. In one patient two vascularized nerve grafts in the index finger and one conventional nerve graft in the long finger were performed concomitantly. Six skin flaps to monitor circulation survived, and one developed partial necrosis. The mean advancement of Tinel’s sign in the vascularized group, excluding the patient with skin flap necrosis, was 1.7 mm/day. The speed in the conventional graft group was 0.5 mm/day. The final sensory recovery in the two groups was not different. Discussion Ideally, clinical studies comparing long-term results of nerve grafting should involve patients with similar injuries. No patients with axillary nerve and posterior interosseous nerve lesions had skin defects, and they had well-vascularized beds. The length of the nerve grafts was less than 6 cm in most cases. No differences in speed of recovery or final outcome between vascularized and conventional nerve grafts were detected for these two cases. Five of 8 patients with low median nerve lesions and 5 of 13 patients with digital nerve lesions also had large skin defects. Four patients in whom the skin defect and nerve gaps were repaired primarily with vascularized
Vascularized and conventional free sural nerve grafts
nerve
graft
with
accompanying
skin
675
flap showed
quicker recovery than patients with delayed conventional nerve grafting after skin closure by pedical groin skin flap. Half of the patients who underwent this twostage procedure showed no return of function. Five of six conventional nerve grafts for digital nerve lesions were done after replantation, and all did poorly. Inadequate vascularity after a pedicled skin flap and replantation has been reported23-25 by other authors, and revascularization of a conventional nerve graft transplanted in such cases often is delayed.15* l9 No patient with a high ulnar nerve and high radial nerve lesion had a massive skin defect or severe scarring, but vascularized nerve grafts showed earlier, more reliable, and more complete recovery than conventional grafts. The nerve gaps were relatively long, ranging between 7 and 14 cm (mean, 9 cm). Simple nerve repairs have been reported to regenerate at a rate of 1 mm per day. In this series, vascularized grafts recovered at approximately 1.8 mm per day and the conventional grafts at only 0.5 mm per day. The reason for this difference cannot be explained by the data in this study. The number of cases in this series is small, and the results may change as our experience grows. However, our preliminary conclusion is that vascularized sural nerve grafting is indicated when a nerve gap of more than 6 cm is associated with a large skin defect or amputation. REFERENCES 1.
Millesi H. Microsurgery of peripheral nerves: neurolysis, nerve grafts, brachial plexus injuries. In: Buncke HT,
Fumas DW, eds. Symposium on clinical frontiers in reconstructive microsurgery. St. Louis: CV Mosby, 1984:353-73. 2. Koshima I, Harii K. Experimental study of vascularized nerve graft: multifactorial analyses of axonal regeneration of nerves transplanted into an acute bum wound. J HAND SURG 1985;10A:64-72. 3. Pho RWH, Lee YS, Rujiwetpongstom U, Pang M. Histological studies of vascularized nerve graft and conventional nerve graft. J HAND SURG 1985;10B:45-8. 4. Restrepo Y, Merle M, Michon J, Folliguet B, Barrate E. Free vascularized nerve graft: an experimental study in the rabbit. Microsurgery 1985;6:78-84. 5. Daly PJ, Wood MB. Endoneural and epineural blood flow evaluation with free vascularized and conventional nerve grafts in the canine. J Reconstr Microsurg 1985;2:45-9. 6. Lind R, Wood MB. Comparison of the pattern of early revascularization of conventional versus vascularized nerve grafts in the canine. J Reconstr Microsurg 1986;2:229-34. 7. Seckel BR, Ryn SE, Simons JE. Gangne RG, Watkins
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The Journal of HAND SURGERY
Doi et al.
E. Vascularized versus nonvascularized nerve grafts: an experimental structural comparison. Plast Reconstr Surg 1986;78:21 l-20. Lux P, Breidenbach W, Firrell J. Determination of temporal changes in blood flow in vascularized and nonvascularized nerve grafts in the dog. Plast Reconstr Surg 1988;82:133-44. Shibata M, Tsai TM, Firrel J, Breidenbach WC. Experimental comparison of vascularized and nonvascularized nerve grafting. J HAND SURC 1988;13A:370-7. McCulough CJ, Gagey 0, Higginson DW, Sandin BM, Crow JC, Sebille A. Axon regeneration and vascularizaton of nerve grafts: an experimental study. J HAND SURG 1984;9B:323-7. Mackinnon SE. The blood supply of vascularized nerve grafts. Invited discussion of Breidenbach WC, Terzis JK. J Reconstr Microsurg 1986;3:57-8. Taylor GI, Ham FJ. The vascularized nerve graft: a further experimental and clinical application of microvascular techniques. Plast Reconstr Surg 1976;57:413-26. Doi K, Kuwata N, Kawakami F, Tamaru K, Kawai S. The free vascularized sural nerve graft. Microsurgery 1984;5:175-84. Bonney G, Birch R, Jamieson AM, Eames RA. Experience with vascularized nerve graft. Clin Plast Surg 1984;11:137-42. Rose EH, Kowalski TA. Restoration of sensibility to anesthetic scarred digits with free vascularized nerve graft from the dorsum of the foot. J HAND SURC 1985;lOA:514-21. Townsend PLG, Taylor GI. Vascularized nerve grafts using composite arterialized neuro-venous system. Br J Plast Surg 1984;37:1-17. Doi K, Kuwata N, Sakai K, Tamaru K, Kawai S. A
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
reliable technique of free vascularized sural nerve grafting and preliminary results of clinical applications. J HAND SURG 1987;12A:677-84. Boorman JG, Sykes PJ. Vascularized versus conventional nerve grafting: a case report. J HAND SURG 1987;12B:218-20. Rose EH, Kowalski T, Norris M. The reversed venous arterialized nerve graft in digital nerve reconstruction across scarred beds. Plast Reconstr Surg 1989;83:593604. Dellon AL. Invited discussion of Lind R, Wood MB. Comparison of the pattern of early revascularization of conventional versus vascularized nerve grafts in the canine. J Reconstr Microsurg 1986;2:229-34. Mackinnon SE, Kelly L, Hunter DA. Comparison of regeneration across a vascularized versus conventional nerve graft: case report. Microsurgery 1988;9:226-33. Omer GW. Report of the committee for evaluation of the clinical result in peripheral nerve injury. J HAND SURG 1983;8:754-8. Manke DA, Summer DS, Van Beek AL, Lambeth A. Hemodynamic studies of digital and extremity replants and revascularization. Surgery 1980;88:445-52:~. Freedlander E. The relationship between cold intolerance and cutaneous blood flow in digital replantation patients. J HAND SURG 1986;llB:15-9. Duran WN. Microcirculatory hemodynamics In: Serafin D, Buncke HJ, eds. Microsurgical composite tissue transplantation. St. Louis: CV Mosby, 1979:31-42. Sasaki GH, Pang CY. Hemodynamics and viability of acute neurovascular island skin flaps in rats. Plast Reconstr Surg 1980;65: 152-8. Sunderland S. Nerves and nerve injuries. London: Churchill Livingstone, 1972:687-719.
of vascularized
and conventional
sural nerve grafts Long-term
results of a randomized
grafts in patients with comparable
series of 27 vascularized
and 22 conventional
sural nerve
upper extremity injuries are reported. Recovery speed and
outcome depended on (1) whether or not there was an overlying skin defect, (2) how the defect was closed, and (3) which nerve was injured and at what level. Generally, a vascularixed
nerve
graft is indicated when the nerve gap is more than 6 cm and is associated with a massive skin defect or the graft is performed after reimplantation. Otherwise, results achieved with a conventional graft are equally good. (J HAND SURG 1992;17A:670-6.)
Kazuteru
Doi,
Yoko Kurafuji,
MD, OTR,
Koichi
Tamaru,
and Shinya
MD, Kawai,
Kazuhiro MD,
Sakai,
MD,
Noriyuki
Kuwata,
MD,
Ube, Japan
T
he vascularized nerve graft is different from other vascularized composite tissue grafts, such as free skin flaps and toe transfers, in that it can survive without immediate revascularization. It also differs from the conventional nerve graft in being able to survive to some extent in an unfavorable environment.’ A number of experimental studies established definite indications for vascularized nerve grafts.2-9 However, it is not clear whether axonal regeneration in vascularized nerve grafts is superior to that in conventional nerve especially when small-caliber nerve grafts are grafts, ‘O placed in healthy beds.‘, ” Clinical studies have suggested that vascularized nerve graft may be indicated for nerve grafting in the poorly vascularized scarred beds,‘2-‘9 but these conditions are difficult to reproduce experimentally.*~ lo, *OA well-controlled clinical study is necessary to establish the indications for vascularized and conventional nerve grafts. No study to date has
From the Department of Otthopaedic Surgery, Yamaguchi School of Medicine, Ube, 755, Japan.
University
Presented at the Societe Intemationale de Orthopedique et de Traumatologie 90 (SICOT 90) Meeting in Montreal, Canada, September 8 through 15, 1990. Received for publication July 18, 1991.
Feb. 22, 1991; accepted
in revised form
No benefits in any form have heen received or will be received from a commercial party related directly or indirectly to the subject of
this article. Reprint requests: Kazuteru Doi, MD, Department of Orthopaedic Surgery, Japan.
Yamaguchi
University
School of Medicine,
311132567
670
THEJOURNALOFHANDSURGERY
Fig. 1. Vascularized sural nerve graft. a, The vascular pedicle is based on either the cutaneous branch of the peroneal artery or the musculocutaneous perforating branch of the posterior tibia1 artery. b, The nerve usually is sectioned into as many as four segments. c, A skin flap can be elevated with the nerve to monitor vascular patency. (Redrawn from Doi K. et al, J HAND SURG 1987;12A:677.)
Ube, 755,
been able to control the many factors that affect recovery from nerve injuries.L2-L9 We have previously described a reliable technique for free vascularized sural nerve grafting and have reported preliminary clinical results. 13,I7 Early follow-up has been encouraging. The present report compares the
Vol. 17A, No. 4 July 1992
long-term results of individual nerve repair in the upper extremity with free vascularized and nonvascularized sural nerve grafts. Materials
and methods
A description of the surgical techniques for vascularized and nonvascularized sural nerve grafting follows. ‘I. ” Vascularized sural nerve graft. The vascularized sural nerve graft is based on either the cutaneous branch of the peroneal artery or the muscular perforating branch of the posterior tibia1 artery. It is harvested and sectioned into as many as four segments to accommodate the discrepancy between the diameters of the injured nerve and the graft while safely maintaining each segment’s vascularity by preserving the fascia intact (Fig. 1). An island of skin can be elevated with the nerve to monitor vascular patency. After the recipient site has been prepared properly for interfascicular nerve grafting and microvascular anastomosis, the vascular pedicle of the graft is divided. The sural nerve is folded, and each nerve segment is approximated individually. The circulation is restored by microvascular anastomosis. Conventional sural nerve graft. A longitudinal incision is made over the sural nerve in the lower leg, and the sural nerve is harvested. Segments that are long enough to bridge the nerve gap and approximately the same diameter as the injured nerve are created. Interfascicular nerve grafting under an operating microscope is performed with 10-O nylon. Materials. Since 1984 the senior author has assigned patients at random to undergo vascularized nerve graft or conventional graft for repair of nerve defects of the upper extremity. Patients were included when (1) their age was between 17 and 50 years, (2) the senior author personally performed the nerve grafting, (3) a sural nerve graft was used, (4) postoperative rehabilitation was performed at our hospital and by the same hand therapist, and (5) the postoperative follow-up was at least 24 months. Twenty-seven vascularized sural nerve grafts and 22 conventional grafts met these criteria and are included in this study. The followup period ranged from 24 to 40 months (mean, 26 months). Neurologic evaluation. Postoperative recovery was assessed by the speed of advancement of Tinel’s sign 90 days postoperatively, time to sensory reinnervation in the correct anatomic distribution of the repaired nerve. time to electromyographic reinnervation, and final sensory recovery and motor recovery 24 months postoperatively, according to Highet’s scalez2 for as-
Vascularized and conventional free sural nerve grafts
671
sessment of the median, ulnar, and radial nerves. The axillary nerve was assessed only by the system for evaluating the strength of the deltoid muscle developed by the British Council.22 The digital nerves were assessed according to the sensory evaluation system of the British Council, Semmes-Weinstein’s monofilament test, and the moving two-point discrimination test. Results Axillary nerve. Five axillary nerves were repaired with the use of free vascularized sural nerve grafts and three with conventional grafts (Table I). Two vascularized nerve grafts were placed between the posterior cord of the brachial plexus and the axillary nerve, and three grafts were placed distal to the division of the posterior cord. The three conventional grafts were placed distal to the division of the posterior cord. No patient had any skin defect or scarring around the nerve defect. The mean time to electromyographic reinnervation of the deltoid muscle was 6 months in the vascularized group and 4 months in the conventional group; the mean muscle strength of the deltoid at 24 months was M4.2 in the vascularized group and M4.3 in the conventional group. Neither difference was statistically significant. Median nerve Ten median nerve lesions-three high and seven low-were repaired. Three vascularized nerve grafts used for high median nerve lesions were excluded because no conventional grafts were used in patients with injuries at this level. Four of seven patients with low median nerve injury underwent vascularized nerve grafts, and two of these had an accompanying skin flap to close a massive skin defect (Table II). Three patients underwent conventional grafts after closure of a large skin defect with a groin flap. The mean speed of advancement of Tinel’s sign 2 months postoperatively was 1.8 mm/day in the vascularized group and 0.5 mm/day in the conventional group. The mean time to S2 sensory reinnervation in the fingertip distal to the distal finger crease of the thumb, index, and long fingers was 16.8 weeks in the vascularized group and 30.7 weeks in the conventional group. Time to electromyographic reinnervation of the abductor pollicis brevis muscle ranged from 6 months to 8.5 months (mean, 7.4 months) in the vascularized group and from 11 months to 14 months (mean, 12.5 months) in the conventional group. One patient who underwent conventional grafting had failed to innervate this muscle 2 years postoperatively.
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Doi et al.
Table I. Demographics Case No.
and results in patients with axillary nerve lesions undergoing Nerve gap
Age
W)
(cm)
Free vascularized sural nerve graft 1 19 2 19 3 24 4 21 5 17 Mean f SD 6.0
6 6 5 I 6
Conventional nerve graft 1 18 2 21 3 17 Mean -t SD
Survival of skin flap
Time to EMG innervation of deltoid (mo)
Yes Yes No flapt No flap No flap
4.7 f
Strength of shoulder ABD* 24 mo postoperatively
3 4 7 12 4 6.0 2 3.29-?
* 0.63$ 3 5 6
nerve grafting
_ _ -
4 4 5 3 5 4.2 + 0.75$
3 4 5 4.0 k 0.82$
1.25$
4 5 4 4.3 ? 0.47:
*ABD = °ree abduction. tNo skin flap to monitor graft circulation was elevated. SDifferences were not statistically significant.
Table II. Demographic nerve grafting
Case No.
Age fyr)
Free vascularized 1 18 2 50 3 45 4 50
Skin defect
and clinical results in patients with low median nerve lesions undergoing
Length of nerve gap (cm)
sural nerve graft + 5 + 6 _ 5 _ 5
Mean k SD
Yes Yes Yes Yes
5.3 k 0.43$
Conventional nerve graft 1 31 _ 2 21 + 3 50 + Mean 2 SD
Survival of skin flap
5 10 7 7.3 f
2.053:
Speed of Tinel’s sign* (mmi
Time to S2
Time to EMG
day)
@k)
(APB) (mo)
Motor
Sensory
2.2 1.5 2.0 1.6
14 18 17 18
6 8.5 7 8
M3 M2 M3 M2
s3 s3 s3 s3
1.8 2 0.2t -
0.5 0.5 0.5 0.5 *
Final results
16.8 ”
1.64t
24 26 42
ot
30.7 f
8.06t
7.4 2 0.96t
2.5 f 0.50$
11 14 None
M2 Ml MO
12.5 k 1.50t
1 k 0.81$
3 2
ot
s3 s2 s2 2.3 2 0.47t
APB = Abductor policis brevis. *Distance Tinel’s sign advancedduring the first 3 months. tp < 0.05. PNo statisfically significant difference.
The mean outcome scores 2 years postoperatively were M2.5, S3 in the vascularized group and M 1, S2.3 in the conventional group. This difference was statistically significant (p < 0.05). Ulnar nerve. Eight ulnar nerves were repaired with four vascularized nerve grafts and four conventional grafts; there were two high lesions and six low lesions. High ulner nerve lesions. One vascularized graft and one conventional graft were used (Table III). The speed of advancement of Tinel’s sign 3 months postopera-
tiveiy, time to S2 sensory reinnervation in the tip of the small finger, time to electromyographic reinnervation of the abductor digiti minimi muscle, and level of function at 2 years were better after the vascularized nerve graft. Low ulnar nerve lesions. Four vascularized nerve grafts and three conventional grafts were implanted (Table IV). One of four skin flaps monitoring circulation of the vascularized grafts became necrotic and was excised 1 week postoperatively. This case was excluded
Vol. 17A, No. 4 July 1992
613
Vascularized and conventional free sural nerve grafts
Table III. Demographics
and clinical results in patients with high ulnar nerve lesions undergoing
nerve grafting Length of nerve Age (yr)
Skin defect
30 18
7 8
-
Survival of
Kind of Graft
graft (cm)
Speed of Tinel’s sign (mm Iday)
flap Yes
FVNG Conventional
Final results
Time to s2
Time to EMG WM)
(mo) 14 None
2.2 0.5
(mo)
Motor
Sensory
M3 Ml
s2 Sl
20 39
ADM = Abductor digiti minimi. FVNG = Free vascularized sum1 nerve graft.
Table IV. Demographics
and clinical results in patients with low ulnar nerve lesions undergoing
nerve grafting Case No.
Skin defect
Age fyr)
Free vascularized
1
1 2 3
Tinel's sign
Time to S2
(cm)
Jlap
(mmlday)
fmo)
Yes Yes Yes No
2 2 2 0.5
4 5 4 None
-
Speed of
5 6 6 I
-
1.6 + 0.65t
5.7 * 0.47t
Mean 2 SD* Conventional
Survival of
Final results Time to EMG WM)
Motor
fmo)
Sensory
sural nerve graft
31 20 12 49
2 3 4
Length of nerve gap
4.3 t
0.47t
4 5 4 12
s3 s3 s3 Sl
M3 M3 M4 Ml
6.25 + 3.34t
M3.3
t
0.47t
s3 *
ot
nerve graft -
41 22 35
0.6 f 0.08t
4.3 f 0.47t
Mean a SD
0.7 0.5 0.6
-
5 4 4
8 9 None
M2 M2 MO
s2 s2 S2
8.5 + 0.5t
M2t
s2t
6 7 I 6.7 2 0.47t
ADM = Abductor digiti minimi. *Case 4 is excluded because of skin flap necrosis.
tp < 0.05.
Table V. Demographics
and clinical results in patients with high radial nerve lesions undergoing
nerve grafting Case No.
Age fyr)
Free vascular
Length of nerve gap (cm)
Survival of
None None
8 14 11.0 2 3.00$
Yes Yes
None None None
10 8 11
Pap
Speed of Tinel’s sign (mm I day)
Time to EMG (EDC) (mo)
Final results44otor
2 2 2t
4 8 6 ? 2t
M4 M3 M3.5 + 0.5t
None 0.5 0.6
None 12 10 11 * 1t
sural nerve graft
1
18 50 Mean f SD Conventional nerve graft 2
1 2 3
Skin defect
34 32 22 Mean 2 SD
EDC = Extensor digiti communis. *No significant difference. tp = < 0.05.
9.7 ?
1.24$
0.55 zk 0.05t
MO M2 Ml MI.0 t 0.8”F
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Doi et al.
Table VI, Demographics grafting
and clinical results in patients with low radial nerve lesions undergoing
I
Case No.
Age (yr)
Free vascular 1 2
sural nerve graft 50 50
Conventional
I 2
Skin defect
I
Length of nerve
Time to EMG
gap (cm)
Survival of flap
5 5
Yes Yes
5 5.5 5.3 + 0.25*
M4 M4 M4*
-
5 6 5.5 2 0.5*
M4 M2 M3*
None None
Mean k SD nerve graft 37 None 45 None Mean k SD
nerve
5* 5 4 4.5 k 0.5*
(EPLJ fmo)
Final results-Motor
EPL = Extensor policis longus.
*Not statistically significant.
Table VII. Demographics nerve grafting
and clinical results of patients with digital nerve lesions undergoing
Final results Case No.
Age fvri
Skin defect
Length of nerve gap
Survival of
(emi
Pap
Speed of Tinel’s sign (mm/day)
6 6 6 6 5 5 5
Yes Yes Partial Yes Yes Yes Yes
2.0 1.2 0.8 1.2 3.0 2.0 2.0
3 3 6 4 3 4 4
5.6 k 0.49$
1.74 k 0.686
3.9 2 0.99§
5 4 7 6 6 6
0.5 0.7 0.4 0.6 0.5 0.5
13 12 8 8 None 16
Free vascular sural nerve graft 1 50 None 2 19 None 3 32 None 4 42 None 5 46 Yes 6 42 None 1 36 None Mean k SD Conventional 1 2 3 4 5 6
nerve graft 46 None 50 None 45 None 24 Yes 32 Yes 49 Yes
Mean -t SD
5.7 z!T0.94$
-
0.53
Time to S2 fmo)
+ 0.091
11.4 k 3.076
Moving 2PDt Sensory
Semmes-Weinstein*
Cmmi
s2 s3 s2 s4 s3 54 s3
4.17 3.61 4.17 2.83 3.61 2.83 3.61
None 8 None 4 10 6 10
3.35 k 0.53$ s2 s3 s2 s3 None s2
4.17 3.61 4.17 3.61
None 12 None 8
4.17
None
3.37 2 0.49$
*Semmes-Weinstein monofilament test. TMoving two-point discrimination. SNo significant difference. §p < 0.05.
from the evaluation. The mean advancement of the Tinel’s sign 2 months postoperatively, the mean time to S2 sensory recovery in the tip of the small finger, and the mean time to electromyographic reinnervation of the abductor digiti minimi muscle were shorter in the vascularized graft group (Table IV). Functional evaluation 2 years postoperatively was M3.3, S3 and M2, S2 for successful vascularized and conventional grafts, respectively. Differences in function between vascu-
larized and conventional grafts were significant (p < 0.05) (Table 4). Radial nerve. Nine radial nerves (five high lesions and four low lesions) were repaired with four vascularized nerve grafts and five conventional grafts (Table V). High lesions. Two high radial nerve injuries were repaired by vascularized grafts. Both skin flaps elevated to monitor circulation in the vascularized group sur-
Vol. 17A, No. 4 July 1992
vived. The mean advancement of Tinel’s sign 2 months postoperatively was faster in the vascularized graft. One conventional graft failed to regenerate through the proximal neurorrhaphy site. Sensory reinnervation to the dorsal skin over the first interosseous muscle was unreliable because some patients had cross-innervation from an adjacent nerve. The mean time to electromyographic reinnervation of the extensor digiti communis muscle in the vascularized group was quicker, and functionai evaluation 2 years postoperatively was M3.5 in the vascularized group and Ml in the conventional group. Low lesions. Two vascularized sural nerve grafts and two conventional grafts were used to repair 4 to 6 cm nerve gaps in the posterior interosseous nerve (Table VI). The mean time to electromyographic reinnervation to the extensor digiti communis muscle and the final motor evaluation were comparable in the vascularized and conventional groups. Digital nerves. Thirteen digital nerve defects in the palm were repaired with seven vascularized and six conventional grafts (Table VII). Three vascularized and five conventional grafts were used to repair a nerve defect after replantation of an amputated hand or digit. One vascularized graft accompanied a skin flap to close a skin defect of the palm. Three conventional grafts were applied secondarily after closure of a palmar skin defect by a pedicled groin flap. In one patient two vascularized nerve grafts in the index finger and one conventional nerve graft in the long finger were performed concomitantly. Six skin flaps to monitor circulation survived, and one developed partial necrosis. The mean advancement of Tinel’s sign in the vascularized group, excluding the patient with skin flap necrosis, was 1.7 mm/day. The speed in the conventional graft group was 0.5 mm/day. The final sensory recovery in the two groups was not different. Discussion Ideally, clinical studies comparing long-term results of nerve grafting should involve patients with similar injuries. No patients with axillary nerve and posterior interosseous nerve lesions had skin defects, and they had well-vascularized beds. The length of the nerve grafts was less than 6 cm in most cases. No differences in speed of recovery or final outcome between vascularized and conventional nerve grafts were detected for these two cases. Five of 8 patients with low median nerve lesions and 5 of 13 patients with digital nerve lesions also had large skin defects. Four patients in whom the skin defect and nerve gaps were repaired primarily with vascularized
Vascularized and conventional free sural nerve grafts
nerve
graft
with
accompanying
skin
675
flap showed
quicker recovery than patients with delayed conventional nerve grafting after skin closure by pedical groin skin flap. Half of the patients who underwent this twostage procedure showed no return of function. Five of six conventional nerve grafts for digital nerve lesions were done after replantation, and all did poorly. Inadequate vascularity after a pedicled skin flap and replantation has been reported23-25 by other authors, and revascularization of a conventional nerve graft transplanted in such cases often is delayed.15* l9 No patient with a high ulnar nerve and high radial nerve lesion had a massive skin defect or severe scarring, but vascularized nerve grafts showed earlier, more reliable, and more complete recovery than conventional grafts. The nerve gaps were relatively long, ranging between 7 and 14 cm (mean, 9 cm). Simple nerve repairs have been reported to regenerate at a rate of 1 mm per day. In this series, vascularized grafts recovered at approximately 1.8 mm per day and the conventional grafts at only 0.5 mm per day. The reason for this difference cannot be explained by the data in this study. The number of cases in this series is small, and the results may change as our experience grows. However, our preliminary conclusion is that vascularized sural nerve grafting is indicated when a nerve gap of more than 6 cm is associated with a large skin defect or amputation. REFERENCES 1.
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