VASCULARISED
NERVE
GRAFTS
M. MERLE and G. DAUTEL Service de Chirurgie Plastique et Reconstructrice de l’Apparei1 Locomoteur, Centre Hospitalo- Universitaire de Nancy, H6pital Jeanne &Arc, Toul, and Institut EuropCen de Biomatkriaux et de Microchirurgie, Universitk de Nancy I, France
Since Taylor (1976) successfully performed the first vascularised free nerve graft, experimental and clinical data have not provided conclusive support for the superiority of this method of repairing loss of nerve substance. Experimental work yields conflicting results. Histologic results are in favour of vascularised grafts but non-vascularised fascicular grafts placed in a healthy bed recover sufficient neovascularisation within a short period of time (four to six days). In the field of bra&al plexus repair, vascularised grafts give consistent results. However, if thrombosis of the anastomoses occurs, the grafts fail completely. In our experience, vascularised nerve grafts used for repairing digital nerves and arteries, have a high rate of thrombosis. There are few potential donor sites. A nerve graft cannot be considered to be physiologically vacularised if it relies only on an artery or on an arterialised vein. Given the present state of immunosuppressant treatments, vascularised allografts are not yet appropriate. Therefore, vascularised nerve grafts have limited applications. In general it is preferable to repair the tissue bed so as to promote revascularisation of conventional nerve grafts. Journal of Hand Surgery (British Volume, 1991) 16B: 483-488
Cases of extensive loss of nerve substance, i.e. more than 10 cm., have an uncertain outcome when they are repaired by conventional fascicular free grafting techniques. Therefore, great interest was aroused in 1976 when Taylor described the use of a radial nerve to graft an extensive loss of substance in a median nerve (Taylor and Ham, 1976). During the following decade, many experimental studies and clinical applications of this new technique were undertaken. As it appeared that the results were actually no better than those of conventional grafts and that there were few donor sites, enthusiasm and interest subsided. Allografts with immunosuppressants have remained at the experimental stage. Here we review both experimental works and clinical results in an attempt to summarise current opinions on this subject. The principle of vascularised nerve grafts goes back to Strange (1947) who described the possibility of grafting the median nerve by staged transposition of the ulnar nerve; he obtained his first success in 1948 (Strange, 1947 and 1948). The same principle of pedicled grafting was applied by MacCarty to repair the internal popliteal nerve using a pedicled graft taken from the external popliteal nerve (MacCarty, 1951). Vascular microsurgery revived interest in the technique of nerve repair by vascularised grafting. Taylor used the superficial branch of the radial nerve, 24 cm. long, vascularised by the radial artery to repair a defect of the median nerve. This technique is acceptable in patients presenting multiple traumas of the limbs, because sequelae at the donor site are minimal. However, the VOL. 168 No. 5 DECEMBER
1991
sensory loss would be unacceptable in the usual patient presenting with only a single injury. In 1978, Taylor classified vascularisation of peripheral nerves into five types, the first three of which could be used for free vascularised transfers. Taylor’s work in the field of donor sites was taken up by others. Bonney and Birch (1977) suggested using the ante-brachial portion of the ulnar nerve. Comtet (1981) described the vascularisation of the internal cutaneous nerve. Fachinelli et al. (1981) described the superficial sural artery which vascularises the external saphenous nerve. Lebreton and Merle (1983) described the vascularisation of the ulnar nerve in the arm. Oberlin (1985) described the pedicled external popliteal nerve. In 1983, Rose repaired loss of substance of digital nerves using the internal branch of the deep peroneal nerve lifted with the dorsalis pedis artery; later, he came to use only a vena comitans which he arterialised. This arterialisation technique was described by Townsend and Taylor (1976) for the external saphenous nerve and was also developed by Gu et al. (1985). Recently, Dautel(l991) used the anterior inter-osseous nerve taken with the anterior inter-osseous artery. Our clinical experience summarises the problems encountered in the upper limb, i.e., avulsions of the brachial plexus, extensive loss of substance with poor tissue environment (Volkmann, crush), and loss of substance of digital nerves. Vascularised grafts for extensive bra&al plexus
loss of substance of the
In cases of intra-spinal avulsion of C8 and Tl roots, it is 483
M. MERLE AND G. DAUTEL
legitimate to use the brachial or ante-brachial portion of the ulnar nerve to bridge an extensive gap, from C5/C6 to the upper trunk or even to the posterior cord. We used the brachial portion of the ulnar nerve in nine cases, five times as a free vascularised transfer and four times as a pedicled graft. By the use of free vascularised grafts measuring about 16.5 cm., itwaspossible to bridgegaps averaging 14.4 cm. in length. Usually, vascular anastomoses of the proximal ulnar pedicle were made with one of the cervical or thoracic branches of the sub-clavian artery. Four out of the five vascularised transfers remained viable. The Tine1 sign progressed distally at an average of 3 mm. per day during the first six months after operation. Contractions of the biceps were first observed clinically and electromyographically in the ninth month after operation whereas the same result would be observed only 12 months after non-vascularised fascicular grafts. The one observed failure was caused by early thrombosis of arterial and venous anastomoses; since extrinsic neovascularisation of whole nerve trunks is poor or delayed, the grafted nerve underwent ischemic necrosis. Functional failure was complete in this case. In the four cases where we used the pedicled brachial segment of the ulnar nerve, we observed recovery of the biceps graded M3+ (three patients) and M4 (one patient). In this situation, there is no risk of thrombosis but the length of the graft is a major concern. It is imperative to dissect the ulnar nerve as far as 6 cm. distal to the internal condyle of the humerus. This is necessary in order to mobilise the ulnar nerve upwards and suture it to the C5 or C6 root without tension. In this short series, it is worth noting the consistency of results of biceps function when the vascular anastomoses remain patent. Yet, when the patients are examined after three years or more, functional results are no better than those obtained with successful conventional fascicular grafts; progress of the Tine1 sign, which occurred through the vascularised graft at above average speed during the first six months (3 mm. per day), later stabilised at 1.5 mm. per day. Our results were similar to those obtained by Bonney et al. (1984) (two failures out of 12 cases), and Alnot (1988) (one failure out of ten), who used the ulnar nerve with its artery. We avoided using the ante-brachial portion of the ulnar nerve so as not to sacrifice the dominant artery of the hand. Vascularised nerve grafts for extensive loss of substance iu the forearm
Severe trauma to the forearm (crush, avulsion, Volkmann’s contracture) necessitates the restoration of at least sensory function of the median nerve. The tissue environment is usually poor and cannot support free fascicular grafts. Grafting the median nerve with the 484
vascularised brachial segment of the ulnar nerve seems to be a good choice. We have used this technique on three occasions, two of these for Volkmann’s ischaemic contracture. These two cases failed: early thrombosis of the vascular anastomoses resulted in necrosis of the grafts and no functional recovery was observed. This underlines the uncertainty of microsurgical techniques applied to recipient vessels severely damaged by the initial trauma.
Grafts of digital nerves
The published results of conventional digital nerve grafts vary widely. One can only admire the results of MacKinnon et al. (1988) who report 31 cases of discriminating sensitivity out of 33 operations, i.e. a 93% success rate. Tenny and Lewis (1984) obtained discriminating sensitivity in 32 cases out of 42. In our experience, Dumontier et al. (1990) observed discriminating sensitivity in three out of 16 patients. These disappointing results led us to investigate vascularised grafts. At first, we used Rose’s (1985) technique : the internal branch of the deep peroneal nerve is lifted with a vena comitans that is used to bridge the digital artery. Later, we switched to the technique of Dautel using the anterior inter-osseous nerve and its artery (Dautel et al., 1990). Our prospective study included nine patients. Seven patients suffered an immediate loss of substance on both artery and nerve caused by the initial trauma. Continuity was restored in two of these patients by an immediate vascularised nerve graft and in the other five by secondary vascularised nerve grafting. The eighth patient had been treated by primary repair of artery and nerve, but the nerve suture was done under excessive tension; a secondary graft was performed without waiting for nerve regrowth. The last patient had had a neglected wound; repair had been attempted by suture and after this failed, we did a vascularised graft. At that time, the artery was found to be thrombosed. Thus, surgical exploration at the time of grafting showed that in all cases there were defects of both artery and nerve. In no case was it necessary to interrupt the continuity of a normal digital artery in order to do the nerve graft. The average length of the graft was 35 mm. In the first five cases, the donor site used was the one described by Rose, i.e. the internal branch of the deep peroneal nerve and the vena comitants adjacent to the dorsalis pedis artery. In the last four cases, the segment of the anterior inter-osseous nerve distal to the origin of the flexor policis longus nerve was used as a donor site. The vascular sutures were end-to-end anastomoses except in two cases THE JOURNAL OF HAND SURGERY
Ulnar,
Ulnar,
Ulnar,
Ulnar,
Ulnar,
Radial,
Ulnar,
22
29
35
30
52
17
27
middle
index
middle
index
index
little
thumb
Ulnar, index
20
middle
Ulnar,
Collateral nerve involved
19
(years)
Age
Table 1
Nine months
Two months
Emergency
Emergency
Five months
Seven weeks
15 months
15 weeks
Ten weeks
Delay
Anterior nerve Anterior nerve Anterior nerve Anterior nerve
Negative Positive Negative Negative
End-to-end End-to-end End-to-end End-to-end
End-to-end End-to-end End-to-end End-to-end
35 35 35 35
inter-osseous inter-osseous inter-osseous inter-osseous
Deep peroneal
nerve
nerve
Negative
End-to-end
End-to-end
30
None
None
Patent
None
Thromb.
Thromb
Negative
End-to-end
Patent
Positive
End-to-end
Patent
Positive
20
Deep peroneal
End-to-end
End-to-end
End-to-side
nerve
nerve 35
Deep peroneal
Deep peroneal
End-to-side
Thromb
Arteriogram
Negative
Digital Allen test
40
End-to-end
Proximl vascular Distal vascular anastomosis anastomosis
End-to-end
nerve
length of the graft (mm) 50
Deep peroneal
Donor site
9
6
1%
8
13
15
16
18
22
Follow-up (months)
s: 11 M: 10 s: 12 M: 11 s: 13 M: 12 s: 10 M:8 S&15 MaI5 S&l5 Ma15 s>15 M: 12 s: 11 M: 11 s: 12 M: 11
Static and moving 2P.D.
M. MERLE AND G. DAUTEL
where the proximal anastomosis was an end-to-side suture. Immediate patency was judged at tourniquet release with a patency test done distal to both proximal and distal vascular anastomoses. All our grafts were found to be patent. No further monitoring was done in the first days after operation. Long-term vascular results were judged using the Allen test; in the first six cases, the results of the Allen test were compared with arteriographic data obtained in the third month after operation. Since the results consistently concurred, no arteriography was done in the last three cases. Thrombosis was observed in six of the grafts at the time of control; out of the three remaining patent grafts, two were the cases where proximal vascular anastomosis was end-to-side. Assessment of sensory results was done with the static and dynamic two-point discrimination tests. No selective block of the healthy contra-lateral nerve was used to study the sensory result. However, care was taken to test precisely the area of the pulp that was innervated solely by the grafted nerve. Sensory results observed in these nine clinical cases were as follows: three cases were considered as failures since static discrimination was equal to, or worse than 15 mm. No patient had a static two-point discrimination better than 10 mm. (Table 1). Even though this series was too small for statistical analysis, it seems that long-term sensation was not influenced by graft patency. The vascular results obtained in this series demonstrated the difficulties of late reconstructions of digital vascular axes when the contralateral axis is patent. Since there was no long-term postoperative monitoring, the exact time at which thrombosis occurred is not known. In the seven cases of secondary grafting, the vascular graft-either artery or vein-had to be as long or longer than the nerve graft. In order to place the anastomosis on normal vascular territory, it was necessary to extend the dissection proximally and distally along the arterial axis until the first healthy collateral branch was found, i.e. until reaching the first arterial branch fed by the contra-lateral artery through the anastomotic system. However, careful placement of the anastomosis on healthy territory did not prevent thrombosis in six out of nine cases. In order to document the vascular results of these grafts, it is necessary to use tests that relate directly to graft patency, i.e. arteriography and/or Allen test. The six cases with long-term thrombosis did not have sensory results different from those of the three cases where vessels remained patent. Thus, there is an important difference between vascularised nerve grafts involving small nerves, such as digital nerves, and those involving large nerve trunks. When secondary thrombosis occurs, small calibre nerves, such as the internal 486
branch of the deep peroneal nerve or the anterior interosseous nerve, are probably revascularised from their tissue environment as conventional non-vascularised nerve grafts would be. Our results are not in agreement with those of Rose (1989). It is therefore necessary to study the question by further clinical studies with assessment of post-operative vascular patency. Discussion
Our clinical experience of vascularised grafts indicate that the results, i.e. sensory and motor functional recovery, were not significantly enhanced. This was true for both the brachial portion of the ulnar nerve and small nerve trunks. The only guaranteed benefit, observed in cases of brachial plexus lesion, was the consistent recovery of biceps function at M3+ or M4 when the graft remained patent. However, when there was thrombosis of the anastomoses, necrosis of the graft ensued and functional failure was complete. This risk is not negligible in surgery of the brachial plexus and must be weighed against the relative safety of conventional fascicular grafts. The experimental work of Daly and Wood (1985) and of Lux et al. (1988) on the dog, demonstrated that blood supply to conventional non-vascularised grafts was superior to that of vascularised grafts on day four to day six, provided the tissue bed was healthy. This is the case with brachial plexus lesions, where the tissue bed is usually satisfactory and conducive to revascularisation of free nerve grafts. Claims of superiority of vascularised nerve grafts have been based mostly on optimistic forecasts during the first months after operation, when the Tine1 sign progresses through the graft at a rate of 3 mm. per day. This may be due to rapid phagocytosis of myelin sheaths and enhanced activity of Schwann cells. The fact remains that vascularised grafts have less tendency to sclerose than conventional grafts. The latter are submitted to ischaemia for several days; although Penkert et al. (1988) have shown that rabbit Schwann cells can survive ischaemia for six or seven days, there is little doubt that ischaemia hinders Schwann cell activity. Axonal regrowth seems to be optimal in the vascularised graft. However, at the proximal and distal suture sites and when the nerve divides into collateral branches, sprouts meet with the same obstacles as in conventional grafts. This may explain why the final results are similar with both techniques. These clinical results are not as good as the results of animal experimentation. Restrepo et al. (1985), and Shibata et al. (1988) demonstrated in the rabbit that the number and diameter of fibres, along with the thickness of myelin sheaths, were greater in vascularised than in non-vascularised grafts. Pho et al. (1985), found no THE JOURNAL OF HAND SURGERY
VASCULARISED
histological difference between vascularised and nonvascularised grafts in the rat. Koshima (1985), found that histologic and electromyographic results were better after vascularised grafts. However, de Medinaceli (1963), has shown that histological and electromyographic data are not good indicators of functional recovery; therefore, he proposed an index of function to assess nerve recovery in the rat. All donor sites are not equally good. The trunk of the ulnar nerve is good because it has both arterial supply and venous return. This is not the case with grafts of the internal branch of the deep peroneal nerve or of the anterior inter-osseous nerve, where a vena comitans’ is arterialised but no venous return is reconstructed. In these conditions, the nerve cannot be considered to be physiologically vascularised. It is probable that the nerve soon suffers from venous stasis, leading to oedema or even thrombosis. This insufficiency of venous return probably explains the disappointing sensory results we have observed after grafting digital nerves with Rose’s technique. The donor sites that we have listed in Table 2 are few in number. Even when nerves are of sufficient diameter and vessels are of appropriate calibre, these sites are rarely useful; the avulsions of C8 and Tl roots that justify their use are not a frequent occurrence. This paucity of donor sites has led several authors to study the possibility of using allografts with immunosuppressant drugs (Zalewski et al., 1981; MacKinnon et al., 1984; Bour and Merle, 1989). Experimental works done on primates, rabbits and rats showed that regenerating fibres grew in the allografts as long as the animals received cyclosporin but that functional results deteriorated greatly as soon as the immunosuppressant treatment
Table 2-Review
of vascuhrised
Authors
Year
Strange
1947
MacCarthy nerve
popliteal
1951
Taylor and Ham Bonney and Birch Townsend and Taylor Fachinelli et al.
1976 1977 1978
Comet Lebreton
1981 1983
Oberlin Rose Dautel
VOL.
and Merle et al.
1981
1985 1985 1991
16B No. 5 DECEMBER
graft techniques Technique Reconstruction of the median by the pedicled ulnar in two procedures Reconstruction of the internal popliteal nerve by the pedicled external popliteal Superficial radial-median Ulnar in the forearm External saphenous nerve with its arterialised vein External saphenous nerve and superficial sural artery Internal cutaneous nerve Ulnar nerve in the arm and proximal ulnar collateral artery Pedicled external popliteal nerve Internal branch of the anterior tibia1 nerve and dorsalis pedis artery Anterior inter-osseous nerve and anterior inter-osseous artery
1991
NERVE
GRAFTS
was stopped. Bour and Merle (1989) showed in rabbits that functional results of vascularised allografts are actually less satisfactory than those of vascularised autografts. At present, there is no possibility of using vascularised allografts in clinical practice until the immunological problem has been resolved with an ethically acceptable treatment. These technical obstacles might be overcome in the future; at present, they restrict the surgeon’s choices. We consider that it is preferable to ameliorate the quality of the tissue bed rather than to continue transplanting rare vascularised grafts. Giving a new surface to sclerosed tissue beds through the use of free or pedicled flaps will guarantee rapid revascularisation of conventional fascicular grafts. This option is all the more justifiable in cases of complex trauma: the associated procedures on bone and tendons also benefit from a satisfactory tissue bed.
References ALNOT, J. Y. (1988). The use of ulnar nerve as a vascularised nerve graft in some pecular conditions and particularly in total palsies of the brachial plexusC7, C8, Dl avulsions. In: Bmnelli, G. (Ed.) TextbookofMicrosurgery, Masson, Milan, 637439. BONNEY, G., BIRCH, R., JAMIESON, A. M. and EAMES, R. A. (1984). Experience with vascularized nerve grafts. Clinical Plastic Surgery, 11: 137142. BOUR, C. and MERLE, M. (1989). Les allogreffes nerveuses et les probl&nes immunologiques. Annales de Chimrgie de la Main, 8: 334-335. COMTET, J. J., BERTRAND, H. G., MOYEN B. and CONDAMINE, J. L. (1981). Greffe nerveuse vascularisee utilisant le brachial cutan& internee transplant6 avec un pCdicule vasculaire. Lyon Chirurgical, 77: 62-63. DALY, P. J. and WOOD, M. B. (1985). Endoneural and Epineural blood flow evaluation with free vascularized and conventional nerve grafts in the canine. Journal of Reconstructive Microsurgery, 2: 45-49. DAUTEL, G., NOEL, D., VOCHE, Ph. and MERLE, M. (1990). Greffes nerveuses vascularisCes des collat&aux digitaux. XXVI&e r&union du GEM, 15 dkcembre, PARIS. DE MEDINACELI, L., FREED, W. J. and WYATT, R. J. (1982). An indexof the functional condition of rat sciatic nerve based on measurements made from walking tracks. Experimental Neurology, 77: 634-643. DUMONTIER, C., KLOOS, M., DAP, F. and MERLE, M. (1990). Greffes nerveuses des collatlraux digitaux. Revue de Chirurgie Orthoptdique, 76: 311-316. FACHINELLI, A., MASQUELET, A., RESTREPO, Y. and GILBERT, A. (1981). The vascularized sural nerve. International Journal of Microsurgery, 3: 5742. GU, Y., ZHENG, Y., LI, H. and ZU, Y. (1985). Arterialized venous free sural nerve grafting. Journal of Plastic Surgery, 15 : 332-338. KOSHIMA, I. and HARII, K. (1985). Experimental study of vascularized nerve grafts: multifactorial analysis of axonal regeneration of nerves transplanted into an acute born wound. Journal of Hand Surgery, 10A: 64-72. KOSHIMA, I. and KIYONORI H. (1985). Experimental study of vascularized nerve grafts. Multifunctional analyses of axonal regeneration of nerves transplanted into an acute burn wound. Journal of Hand Surgery, lOA, 1: 64-72. LEBRETON, E., BOURGEON, Y., LASCOMBES, P., MERLE, M. and FOUCHER, G. (1983). Syst6matisation de la vascularisation de la portion brachiale de nerf ulnaire. Annales de Chururgie de la main, 2: 211-218. LUX, P., BREIDENBACH, W. and FIRRELL, J. (1988). Determination of temporal changes in blood flow in vascularized and vascularized nerve grafts in the dog. Plastic and Reconstructive Surgery, 82: 133-144. MACKINNON, S. E. and DELLON, A. C. (1988). Surgery of the peripheral nerve. Thieme medical Publishers, New York, 89-130. MACKINNON, S. E., HUDSON, A. R., FALK, R. E., KLINE, D. and HUNTER, D. (1984). Peripheral nerve allografts: an immunological assessment of pre-treatment methods. Journal of Neurosurgery, 14: 167-171. MCCARTY, C. (1951) Two stage autograft for repair of extensive damage to sciatic nerve. Journal of Neurosurgery, 8: 318-322.
M. MERLE
AND
OBERLIN, Ch. and ALNOT, J. Y. (1985). Utilisation du nerf sciatique poplitb externe comma greffe vascularisk. Revue de Chimrgie OrthopMique, 71 supplement II: 94-98. PENKERT, G., BINI, W. and SAMII, M. (1988). Revascularization of Nerve grafts: An experimental study. Journal of Reconstructive Microsurgery, 4: 319-325. PHO, R. W. H., LEE, Y. S., RUJIWETPONGSTORN, V. and PANG, M. (1985). Histological studies of vascularized Nerve graft and conventional Nerve graft. Journal of Hand Surgery, 10B: 45-48. RESTREPO, Y., MERLE, M., MICHON, J., FOLIGUET, B. and BARRAT, E. (1985). Free vascularized nerve grafts: An experimental study in the rabbit. Microsurgery, 6: 78-84. ROSE, E. H. (1985). Restoration of sensibility to anesthetic scarred digits with free vascularized nerve grafts from the dorsum of the foot. Journal of Hand Surgery, 10A: 514-521. ROSE, E. H., KOWALSKI, T. A. and NORRIS, M. S. (1989). The reversed venous arterialized nerve graft in digital nerve reconstruction across scarred beds. Plastic and Reconstructive Surgery, 83 : 593-602. SHIBATA, M., TSAI, T. M., FIRRELL, 3. andBREIDENBACH, W. C. (1988). Experimental comparison of vascularized and nonvascularized nerve grafting. Journal of Hand Surgery, 13A: 358-365. STRANGE, F. G. S. (1947). An operation for nerve pedicle grafting. British Journal of Surgery, 34: 423-425.
488
G. DAUTEL STRANGE, F. G. S. (1948). The pedicle nerve graft. British Journal of Surgery, 35: 331-333. TAYLOR, G. I. and HAM, F. (1976). The free vascularized nerve graft. Plastic and Reconstructive Surgery, 57: 413426. TAYLOR, G. I. (1978). Nerve grafting with simultaneous microvascular reconstruction. Clinical Octhopaedics and Related Research, 133; 5c-70. TENNY, J. R. and LEWIS, R. C. (1984). Digital nerve grafting for traumatic defects. Journal of Bone and Joint Surgery (Am), 66: 1375-l 379. TOWNSEND, P. L. G. and TAYLOR, G. I. (1984). Vascularized nerve grafts using composite arterialized neuro-venous system. British Journal of Surgery,37: 1-17. ZALEWSKI, A. A., GULATI, A. K. and SILVERS, W. K. (1981). Loss of host axons in nerve allografts after abolishing immunologic tolerance in rats. Experimental Neurology, 72: 502-506
M. Merle, Service de Chimrgie Plastique et Reconstructive de 1’Appareil Locomoteur, Centre Hospitalo-Universitaire de Nancy, HBpital Jeanne d’Arc, 54201 Toul, France. 0 1991 The British Society for Surgery of the Hand
THE
JOURNAL
OF HAND
SURGERY
NERVE
GRAFTS
M. MERLE and G. DAUTEL Service de Chirurgie Plastique et Reconstructrice de l’Apparei1 Locomoteur, Centre Hospitalo- Universitaire de Nancy, H6pital Jeanne &Arc, Toul, and Institut EuropCen de Biomatkriaux et de Microchirurgie, Universitk de Nancy I, France
Since Taylor (1976) successfully performed the first vascularised free nerve graft, experimental and clinical data have not provided conclusive support for the superiority of this method of repairing loss of nerve substance. Experimental work yields conflicting results. Histologic results are in favour of vascularised grafts but non-vascularised fascicular grafts placed in a healthy bed recover sufficient neovascularisation within a short period of time (four to six days). In the field of bra&al plexus repair, vascularised grafts give consistent results. However, if thrombosis of the anastomoses occurs, the grafts fail completely. In our experience, vascularised nerve grafts used for repairing digital nerves and arteries, have a high rate of thrombosis. There are few potential donor sites. A nerve graft cannot be considered to be physiologically vacularised if it relies only on an artery or on an arterialised vein. Given the present state of immunosuppressant treatments, vascularised allografts are not yet appropriate. Therefore, vascularised nerve grafts have limited applications. In general it is preferable to repair the tissue bed so as to promote revascularisation of conventional nerve grafts. Journal of Hand Surgery (British Volume, 1991) 16B: 483-488
Cases of extensive loss of nerve substance, i.e. more than 10 cm., have an uncertain outcome when they are repaired by conventional fascicular free grafting techniques. Therefore, great interest was aroused in 1976 when Taylor described the use of a radial nerve to graft an extensive loss of substance in a median nerve (Taylor and Ham, 1976). During the following decade, many experimental studies and clinical applications of this new technique were undertaken. As it appeared that the results were actually no better than those of conventional grafts and that there were few donor sites, enthusiasm and interest subsided. Allografts with immunosuppressants have remained at the experimental stage. Here we review both experimental works and clinical results in an attempt to summarise current opinions on this subject. The principle of vascularised nerve grafts goes back to Strange (1947) who described the possibility of grafting the median nerve by staged transposition of the ulnar nerve; he obtained his first success in 1948 (Strange, 1947 and 1948). The same principle of pedicled grafting was applied by MacCarty to repair the internal popliteal nerve using a pedicled graft taken from the external popliteal nerve (MacCarty, 1951). Vascular microsurgery revived interest in the technique of nerve repair by vascularised grafting. Taylor used the superficial branch of the radial nerve, 24 cm. long, vascularised by the radial artery to repair a defect of the median nerve. This technique is acceptable in patients presenting multiple traumas of the limbs, because sequelae at the donor site are minimal. However, the VOL. 168 No. 5 DECEMBER
1991
sensory loss would be unacceptable in the usual patient presenting with only a single injury. In 1978, Taylor classified vascularisation of peripheral nerves into five types, the first three of which could be used for free vascularised transfers. Taylor’s work in the field of donor sites was taken up by others. Bonney and Birch (1977) suggested using the ante-brachial portion of the ulnar nerve. Comtet (1981) described the vascularisation of the internal cutaneous nerve. Fachinelli et al. (1981) described the superficial sural artery which vascularises the external saphenous nerve. Lebreton and Merle (1983) described the vascularisation of the ulnar nerve in the arm. Oberlin (1985) described the pedicled external popliteal nerve. In 1983, Rose repaired loss of substance of digital nerves using the internal branch of the deep peroneal nerve lifted with the dorsalis pedis artery; later, he came to use only a vena comitans which he arterialised. This arterialisation technique was described by Townsend and Taylor (1976) for the external saphenous nerve and was also developed by Gu et al. (1985). Recently, Dautel(l991) used the anterior inter-osseous nerve taken with the anterior inter-osseous artery. Our clinical experience summarises the problems encountered in the upper limb, i.e., avulsions of the brachial plexus, extensive loss of substance with poor tissue environment (Volkmann, crush), and loss of substance of digital nerves. Vascularised grafts for extensive bra&al plexus
loss of substance of the
In cases of intra-spinal avulsion of C8 and Tl roots, it is 483
M. MERLE AND G. DAUTEL
legitimate to use the brachial or ante-brachial portion of the ulnar nerve to bridge an extensive gap, from C5/C6 to the upper trunk or even to the posterior cord. We used the brachial portion of the ulnar nerve in nine cases, five times as a free vascularised transfer and four times as a pedicled graft. By the use of free vascularised grafts measuring about 16.5 cm., itwaspossible to bridgegaps averaging 14.4 cm. in length. Usually, vascular anastomoses of the proximal ulnar pedicle were made with one of the cervical or thoracic branches of the sub-clavian artery. Four out of the five vascularised transfers remained viable. The Tine1 sign progressed distally at an average of 3 mm. per day during the first six months after operation. Contractions of the biceps were first observed clinically and electromyographically in the ninth month after operation whereas the same result would be observed only 12 months after non-vascularised fascicular grafts. The one observed failure was caused by early thrombosis of arterial and venous anastomoses; since extrinsic neovascularisation of whole nerve trunks is poor or delayed, the grafted nerve underwent ischemic necrosis. Functional failure was complete in this case. In the four cases where we used the pedicled brachial segment of the ulnar nerve, we observed recovery of the biceps graded M3+ (three patients) and M4 (one patient). In this situation, there is no risk of thrombosis but the length of the graft is a major concern. It is imperative to dissect the ulnar nerve as far as 6 cm. distal to the internal condyle of the humerus. This is necessary in order to mobilise the ulnar nerve upwards and suture it to the C5 or C6 root without tension. In this short series, it is worth noting the consistency of results of biceps function when the vascular anastomoses remain patent. Yet, when the patients are examined after three years or more, functional results are no better than those obtained with successful conventional fascicular grafts; progress of the Tine1 sign, which occurred through the vascularised graft at above average speed during the first six months (3 mm. per day), later stabilised at 1.5 mm. per day. Our results were similar to those obtained by Bonney et al. (1984) (two failures out of 12 cases), and Alnot (1988) (one failure out of ten), who used the ulnar nerve with its artery. We avoided using the ante-brachial portion of the ulnar nerve so as not to sacrifice the dominant artery of the hand. Vascularised nerve grafts for extensive loss of substance iu the forearm
Severe trauma to the forearm (crush, avulsion, Volkmann’s contracture) necessitates the restoration of at least sensory function of the median nerve. The tissue environment is usually poor and cannot support free fascicular grafts. Grafting the median nerve with the 484
vascularised brachial segment of the ulnar nerve seems to be a good choice. We have used this technique on three occasions, two of these for Volkmann’s ischaemic contracture. These two cases failed: early thrombosis of the vascular anastomoses resulted in necrosis of the grafts and no functional recovery was observed. This underlines the uncertainty of microsurgical techniques applied to recipient vessels severely damaged by the initial trauma.
Grafts of digital nerves
The published results of conventional digital nerve grafts vary widely. One can only admire the results of MacKinnon et al. (1988) who report 31 cases of discriminating sensitivity out of 33 operations, i.e. a 93% success rate. Tenny and Lewis (1984) obtained discriminating sensitivity in 32 cases out of 42. In our experience, Dumontier et al. (1990) observed discriminating sensitivity in three out of 16 patients. These disappointing results led us to investigate vascularised grafts. At first, we used Rose’s (1985) technique : the internal branch of the deep peroneal nerve is lifted with a vena comitans that is used to bridge the digital artery. Later, we switched to the technique of Dautel using the anterior inter-osseous nerve and its artery (Dautel et al., 1990). Our prospective study included nine patients. Seven patients suffered an immediate loss of substance on both artery and nerve caused by the initial trauma. Continuity was restored in two of these patients by an immediate vascularised nerve graft and in the other five by secondary vascularised nerve grafting. The eighth patient had been treated by primary repair of artery and nerve, but the nerve suture was done under excessive tension; a secondary graft was performed without waiting for nerve regrowth. The last patient had had a neglected wound; repair had been attempted by suture and after this failed, we did a vascularised graft. At that time, the artery was found to be thrombosed. Thus, surgical exploration at the time of grafting showed that in all cases there were defects of both artery and nerve. In no case was it necessary to interrupt the continuity of a normal digital artery in order to do the nerve graft. The average length of the graft was 35 mm. In the first five cases, the donor site used was the one described by Rose, i.e. the internal branch of the deep peroneal nerve and the vena comitants adjacent to the dorsalis pedis artery. In the last four cases, the segment of the anterior inter-osseous nerve distal to the origin of the flexor policis longus nerve was used as a donor site. The vascular sutures were end-to-end anastomoses except in two cases THE JOURNAL OF HAND SURGERY
Ulnar,
Ulnar,
Ulnar,
Ulnar,
Ulnar,
Radial,
Ulnar,
22
29
35
30
52
17
27
middle
index
middle
index
index
little
thumb
Ulnar, index
20
middle
Ulnar,
Collateral nerve involved
19
(years)
Age
Table 1
Nine months
Two months
Emergency
Emergency
Five months
Seven weeks
15 months
15 weeks
Ten weeks
Delay
Anterior nerve Anterior nerve Anterior nerve Anterior nerve
Negative Positive Negative Negative
End-to-end End-to-end End-to-end End-to-end
End-to-end End-to-end End-to-end End-to-end
35 35 35 35
inter-osseous inter-osseous inter-osseous inter-osseous
Deep peroneal
nerve
nerve
Negative
End-to-end
End-to-end
30
None
None
Patent
None
Thromb.
Thromb
Negative
End-to-end
Patent
Positive
End-to-end
Patent
Positive
20
Deep peroneal
End-to-end
End-to-end
End-to-side
nerve
nerve 35
Deep peroneal
Deep peroneal
End-to-side
Thromb
Arteriogram
Negative
Digital Allen test
40
End-to-end
Proximl vascular Distal vascular anastomosis anastomosis
End-to-end
nerve
length of the graft (mm) 50
Deep peroneal
Donor site
9
6
1%
8
13
15
16
18
22
Follow-up (months)
s: 11 M: 10 s: 12 M: 11 s: 13 M: 12 s: 10 M:8 S&15 MaI5 S&l5 Ma15 s>15 M: 12 s: 11 M: 11 s: 12 M: 11
Static and moving 2P.D.
M. MERLE AND G. DAUTEL
where the proximal anastomosis was an end-to-side suture. Immediate patency was judged at tourniquet release with a patency test done distal to both proximal and distal vascular anastomoses. All our grafts were found to be patent. No further monitoring was done in the first days after operation. Long-term vascular results were judged using the Allen test; in the first six cases, the results of the Allen test were compared with arteriographic data obtained in the third month after operation. Since the results consistently concurred, no arteriography was done in the last three cases. Thrombosis was observed in six of the grafts at the time of control; out of the three remaining patent grafts, two were the cases where proximal vascular anastomosis was end-to-side. Assessment of sensory results was done with the static and dynamic two-point discrimination tests. No selective block of the healthy contra-lateral nerve was used to study the sensory result. However, care was taken to test precisely the area of the pulp that was innervated solely by the grafted nerve. Sensory results observed in these nine clinical cases were as follows: three cases were considered as failures since static discrimination was equal to, or worse than 15 mm. No patient had a static two-point discrimination better than 10 mm. (Table 1). Even though this series was too small for statistical analysis, it seems that long-term sensation was not influenced by graft patency. The vascular results obtained in this series demonstrated the difficulties of late reconstructions of digital vascular axes when the contralateral axis is patent. Since there was no long-term postoperative monitoring, the exact time at which thrombosis occurred is not known. In the seven cases of secondary grafting, the vascular graft-either artery or vein-had to be as long or longer than the nerve graft. In order to place the anastomosis on normal vascular territory, it was necessary to extend the dissection proximally and distally along the arterial axis until the first healthy collateral branch was found, i.e. until reaching the first arterial branch fed by the contra-lateral artery through the anastomotic system. However, careful placement of the anastomosis on healthy territory did not prevent thrombosis in six out of nine cases. In order to document the vascular results of these grafts, it is necessary to use tests that relate directly to graft patency, i.e. arteriography and/or Allen test. The six cases with long-term thrombosis did not have sensory results different from those of the three cases where vessels remained patent. Thus, there is an important difference between vascularised nerve grafts involving small nerves, such as digital nerves, and those involving large nerve trunks. When secondary thrombosis occurs, small calibre nerves, such as the internal 486
branch of the deep peroneal nerve or the anterior interosseous nerve, are probably revascularised from their tissue environment as conventional non-vascularised nerve grafts would be. Our results are not in agreement with those of Rose (1989). It is therefore necessary to study the question by further clinical studies with assessment of post-operative vascular patency. Discussion
Our clinical experience of vascularised grafts indicate that the results, i.e. sensory and motor functional recovery, were not significantly enhanced. This was true for both the brachial portion of the ulnar nerve and small nerve trunks. The only guaranteed benefit, observed in cases of brachial plexus lesion, was the consistent recovery of biceps function at M3+ or M4 when the graft remained patent. However, when there was thrombosis of the anastomoses, necrosis of the graft ensued and functional failure was complete. This risk is not negligible in surgery of the brachial plexus and must be weighed against the relative safety of conventional fascicular grafts. The experimental work of Daly and Wood (1985) and of Lux et al. (1988) on the dog, demonstrated that blood supply to conventional non-vascularised grafts was superior to that of vascularised grafts on day four to day six, provided the tissue bed was healthy. This is the case with brachial plexus lesions, where the tissue bed is usually satisfactory and conducive to revascularisation of free nerve grafts. Claims of superiority of vascularised nerve grafts have been based mostly on optimistic forecasts during the first months after operation, when the Tine1 sign progresses through the graft at a rate of 3 mm. per day. This may be due to rapid phagocytosis of myelin sheaths and enhanced activity of Schwann cells. The fact remains that vascularised grafts have less tendency to sclerose than conventional grafts. The latter are submitted to ischaemia for several days; although Penkert et al. (1988) have shown that rabbit Schwann cells can survive ischaemia for six or seven days, there is little doubt that ischaemia hinders Schwann cell activity. Axonal regrowth seems to be optimal in the vascularised graft. However, at the proximal and distal suture sites and when the nerve divides into collateral branches, sprouts meet with the same obstacles as in conventional grafts. This may explain why the final results are similar with both techniques. These clinical results are not as good as the results of animal experimentation. Restrepo et al. (1985), and Shibata et al. (1988) demonstrated in the rabbit that the number and diameter of fibres, along with the thickness of myelin sheaths, were greater in vascularised than in non-vascularised grafts. Pho et al. (1985), found no THE JOURNAL OF HAND SURGERY
VASCULARISED
histological difference between vascularised and nonvascularised grafts in the rat. Koshima (1985), found that histologic and electromyographic results were better after vascularised grafts. However, de Medinaceli (1963), has shown that histological and electromyographic data are not good indicators of functional recovery; therefore, he proposed an index of function to assess nerve recovery in the rat. All donor sites are not equally good. The trunk of the ulnar nerve is good because it has both arterial supply and venous return. This is not the case with grafts of the internal branch of the deep peroneal nerve or of the anterior inter-osseous nerve, where a vena comitans’ is arterialised but no venous return is reconstructed. In these conditions, the nerve cannot be considered to be physiologically vascularised. It is probable that the nerve soon suffers from venous stasis, leading to oedema or even thrombosis. This insufficiency of venous return probably explains the disappointing sensory results we have observed after grafting digital nerves with Rose’s technique. The donor sites that we have listed in Table 2 are few in number. Even when nerves are of sufficient diameter and vessels are of appropriate calibre, these sites are rarely useful; the avulsions of C8 and Tl roots that justify their use are not a frequent occurrence. This paucity of donor sites has led several authors to study the possibility of using allografts with immunosuppressant drugs (Zalewski et al., 1981; MacKinnon et al., 1984; Bour and Merle, 1989). Experimental works done on primates, rabbits and rats showed that regenerating fibres grew in the allografts as long as the animals received cyclosporin but that functional results deteriorated greatly as soon as the immunosuppressant treatment
Table 2-Review
of vascuhrised
Authors
Year
Strange
1947
MacCarthy nerve
popliteal
1951
Taylor and Ham Bonney and Birch Townsend and Taylor Fachinelli et al.
1976 1977 1978
Comet Lebreton
1981 1983
Oberlin Rose Dautel
VOL.
and Merle et al.
1981
1985 1985 1991
16B No. 5 DECEMBER
graft techniques Technique Reconstruction of the median by the pedicled ulnar in two procedures Reconstruction of the internal popliteal nerve by the pedicled external popliteal Superficial radial-median Ulnar in the forearm External saphenous nerve with its arterialised vein External saphenous nerve and superficial sural artery Internal cutaneous nerve Ulnar nerve in the arm and proximal ulnar collateral artery Pedicled external popliteal nerve Internal branch of the anterior tibia1 nerve and dorsalis pedis artery Anterior inter-osseous nerve and anterior inter-osseous artery
1991
NERVE
GRAFTS
was stopped. Bour and Merle (1989) showed in rabbits that functional results of vascularised allografts are actually less satisfactory than those of vascularised autografts. At present, there is no possibility of using vascularised allografts in clinical practice until the immunological problem has been resolved with an ethically acceptable treatment. These technical obstacles might be overcome in the future; at present, they restrict the surgeon’s choices. We consider that it is preferable to ameliorate the quality of the tissue bed rather than to continue transplanting rare vascularised grafts. Giving a new surface to sclerosed tissue beds through the use of free or pedicled flaps will guarantee rapid revascularisation of conventional fascicular grafts. This option is all the more justifiable in cases of complex trauma: the associated procedures on bone and tendons also benefit from a satisfactory tissue bed.
References ALNOT, J. Y. (1988). The use of ulnar nerve as a vascularised nerve graft in some pecular conditions and particularly in total palsies of the brachial plexusC7, C8, Dl avulsions. In: Bmnelli, G. (Ed.) TextbookofMicrosurgery, Masson, Milan, 637439. BONNEY, G., BIRCH, R., JAMIESON, A. M. and EAMES, R. A. (1984). Experience with vascularized nerve grafts. Clinical Plastic Surgery, 11: 137142. BOUR, C. and MERLE, M. (1989). Les allogreffes nerveuses et les probl&nes immunologiques. Annales de Chimrgie de la Main, 8: 334-335. COMTET, J. J., BERTRAND, H. G., MOYEN B. and CONDAMINE, J. L. (1981). Greffe nerveuse vascularisee utilisant le brachial cutan& internee transplant6 avec un pCdicule vasculaire. Lyon Chirurgical, 77: 62-63. DALY, P. J. and WOOD, M. B. (1985). Endoneural and Epineural blood flow evaluation with free vascularized and conventional nerve grafts in the canine. Journal of Reconstructive Microsurgery, 2: 45-49. DAUTEL, G., NOEL, D., VOCHE, Ph. and MERLE, M. (1990). Greffes nerveuses vascularisCes des collat&aux digitaux. XXVI&e r&union du GEM, 15 dkcembre, PARIS. DE MEDINACELI, L., FREED, W. J. and WYATT, R. J. (1982). An indexof the functional condition of rat sciatic nerve based on measurements made from walking tracks. Experimental Neurology, 77: 634-643. DUMONTIER, C., KLOOS, M., DAP, F. and MERLE, M. (1990). Greffes nerveuses des collatlraux digitaux. Revue de Chirurgie Orthoptdique, 76: 311-316. FACHINELLI, A., MASQUELET, A., RESTREPO, Y. and GILBERT, A. (1981). The vascularized sural nerve. International Journal of Microsurgery, 3: 5742. GU, Y., ZHENG, Y., LI, H. and ZU, Y. (1985). Arterialized venous free sural nerve grafting. Journal of Plastic Surgery, 15 : 332-338. KOSHIMA, I. and HARII, K. (1985). Experimental study of vascularized nerve grafts: multifactorial analysis of axonal regeneration of nerves transplanted into an acute born wound. Journal of Hand Surgery, 10A: 64-72. KOSHIMA, I. and KIYONORI H. (1985). Experimental study of vascularized nerve grafts. Multifunctional analyses of axonal regeneration of nerves transplanted into an acute burn wound. Journal of Hand Surgery, lOA, 1: 64-72. LEBRETON, E., BOURGEON, Y., LASCOMBES, P., MERLE, M. and FOUCHER, G. (1983). Syst6matisation de la vascularisation de la portion brachiale de nerf ulnaire. Annales de Chururgie de la main, 2: 211-218. LUX, P., BREIDENBACH, W. and FIRRELL, J. (1988). Determination of temporal changes in blood flow in vascularized and vascularized nerve grafts in the dog. Plastic and Reconstructive Surgery, 82: 133-144. MACKINNON, S. E. and DELLON, A. C. (1988). Surgery of the peripheral nerve. Thieme medical Publishers, New York, 89-130. MACKINNON, S. E., HUDSON, A. R., FALK, R. E., KLINE, D. and HUNTER, D. (1984). Peripheral nerve allografts: an immunological assessment of pre-treatment methods. Journal of Neurosurgery, 14: 167-171. MCCARTY, C. (1951) Two stage autograft for repair of extensive damage to sciatic nerve. Journal of Neurosurgery, 8: 318-322.
M. MERLE
AND
OBERLIN, Ch. and ALNOT, J. Y. (1985). Utilisation du nerf sciatique poplitb externe comma greffe vascularisk. Revue de Chimrgie OrthopMique, 71 supplement II: 94-98. PENKERT, G., BINI, W. and SAMII, M. (1988). Revascularization of Nerve grafts: An experimental study. Journal of Reconstructive Microsurgery, 4: 319-325. PHO, R. W. H., LEE, Y. S., RUJIWETPONGSTORN, V. and PANG, M. (1985). Histological studies of vascularized Nerve graft and conventional Nerve graft. Journal of Hand Surgery, 10B: 45-48. RESTREPO, Y., MERLE, M., MICHON, J., FOLIGUET, B. and BARRAT, E. (1985). Free vascularized nerve grafts: An experimental study in the rabbit. Microsurgery, 6: 78-84. ROSE, E. H. (1985). Restoration of sensibility to anesthetic scarred digits with free vascularized nerve grafts from the dorsum of the foot. Journal of Hand Surgery, 10A: 514-521. ROSE, E. H., KOWALSKI, T. A. and NORRIS, M. S. (1989). The reversed venous arterialized nerve graft in digital nerve reconstruction across scarred beds. Plastic and Reconstructive Surgery, 83 : 593-602. SHIBATA, M., TSAI, T. M., FIRRELL, 3. andBREIDENBACH, W. C. (1988). Experimental comparison of vascularized and nonvascularized nerve grafting. Journal of Hand Surgery, 13A: 358-365. STRANGE, F. G. S. (1947). An operation for nerve pedicle grafting. British Journal of Surgery, 34: 423-425.
488
G. DAUTEL STRANGE, F. G. S. (1948). The pedicle nerve graft. British Journal of Surgery, 35: 331-333. TAYLOR, G. I. and HAM, F. (1976). The free vascularized nerve graft. Plastic and Reconstructive Surgery, 57: 413426. TAYLOR, G. I. (1978). Nerve grafting with simultaneous microvascular reconstruction. Clinical Octhopaedics and Related Research, 133; 5c-70. TENNY, J. R. and LEWIS, R. C. (1984). Digital nerve grafting for traumatic defects. Journal of Bone and Joint Surgery (Am), 66: 1375-l 379. TOWNSEND, P. L. G. and TAYLOR, G. I. (1984). Vascularized nerve grafts using composite arterialized neuro-venous system. British Journal of Surgery,37: 1-17. ZALEWSKI, A. A., GULATI, A. K. and SILVERS, W. K. (1981). Loss of host axons in nerve allografts after abolishing immunologic tolerance in rats. Experimental Neurology, 72: 502-506
M. Merle, Service de Chimrgie Plastique et Reconstructive de 1’Appareil Locomoteur, Centre Hospitalo-Universitaire de Nancy, HBpital Jeanne d’Arc, 54201 Toul, France. 0 1991 The British Society for Surgery of the Hand
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