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Effect of submuscular versus intramuscular placement of ulnar nerve: Experimental model in the primate
Effect of Submuscular Versus Intramuscular Placement of Ulnar Nerve: Experimental Model in the Primate. A. L. DELLON, S. E. MACKINNON, A. R. HUDSON and D. A. HUNTER From Johns Hopkins University and Curtis Hand Center, Baltimore, Maryland and University of Toronto A primate model was developed to study the effect of submuscular versus intramuscular placement upon the development of ulnar nerve fibrosis. No significant adherence was found in either location between the ulnar nerve and the flexor-pronator muscle mass. There was no significant difference in the mean nerve fibre diameter or in the percent neural tissue between the ulnar nerves in the two different locations. It is suggested that it is the interaction of the transposed ulnar nerve with other fibrous anatomical structures proximal to, across, and distal to the elbow that causes failure in ulnar nerve transposition procedures, rather than an adverse reaction between the incised flexor-pronator muscle mass and the ulnar nerve.
Among the causes for failure of the operation of anterior transposition of the ulnar nerve at the elbow is said to be scar formation between the muscle of the incised flexor-pronator muscle mass and the ulnar nerve, when the nerve is transposed to either a submuscular or intramuscular position (Broudy, 1978). At present, none of the reports of results of treatment of ulnar nerve compression at the elbow is clearly superior to any others (Leffert, 1982; Wilson, 1973; Gay, 1947; Levy, 1072; Osborne, 1957; Harrison, 1970; King, 1970; Wadsworth, 1977; Macnicol, 1979; Foster, 1981). Indeed, most reported results of the surgical treatment of this problem are mediocre. If the operative technique required to transpose the ulnar nerve into an 1918) or submuscular intramuscular (Adson, (Learmonth, 1942) position were known to produce sufficient scar tissue about the ulnar nerve to risk recurrent entrapment, a basis would exist to select an alternate operative technique. To investigate the nature relationship, the present of this muscle-nerve experimental model was designed in the monkey. Materials
and Methods
Six adult baboons (Papio anubis) weighing lo-14 kg, were anaesthetized with a combination of ketalar and acepromazine. Each animal received 1.2 million units of Bicillin, its arm hairs were clipped, and then the arms scrubbed with betadine. Using sterile technique and 3.5 power loupe magnification, one ulnar nerve was transposed into a submuscular location as described by Learmonth (1942) and the other transposed into an intramuscular position. The medial intermuscular septum was resected in both arms, regardless of which technique was utilized. transposition For the intramuscular location, the scalpel blade was used to incise the flexor-pronator muscle mass to a depth approximately to the juncture between the middle and deepest third. Great care was taken to ensure that in its new transposed position there were no points of tetbering of the ulnar nerve either proximally or distally Receked for publication February, 1985. A. Lee Dellon, M.D., The Hampton Plaza 300 East Poppa Road Baltimore, Maryland
VOL.
11-B No. 1 FEBRUARY
1986
2.1204.
Fig. 1
Intraoperative photograph of a submuscular transposition of the ulnar nerve. At three months after surgery, the block of nerve and muscle specimen have been resected for analysis.
and the deep fascial bands orginating from the anterior surface of the elbow joint capsule were released. For both techniques, the flexor-pronator muscle fascia was closed with three horizontal mattress sutures of 3-O nylon. For both operative techniques, the branches of the flexor carpi ulnaris were preserved and dissected distally for the same distance. Each arm was closed with continuous 4-O nylon sutures and both elbows were immobilized in 90 degrees flexion in a protective orthoplast splint (Rose, 1983) for two weeks. Then, each arm was allowed unrestricted movement. There were no wound healing problems. Three months after surgery, the monkeys were anaesthetized again and specimens excised. Identical specimens were taken bilaterally to include a two cm. length of ulnar nerve proximal and distal to the flexorpronator muscle mass, the entire length or width of the flexor-pronator muscle mass through which the nerve travelled and a depth down to the anterior capsule of the elbow joint (Figure 1). The excised specimen was fixed in Karnovsky’s fixative and then post-fixed in osmium tetroxide. Sections for light microscopy were stained with toluidine blue. 117
A. L. DELLON,
Fig. 2
S. E. MACKINNON,
Photomicrograph of ulnar nerve in flexor-pronator muscle mass, an intramuscular transposition. Note muscle surrounds nerve and there is no fibrosis between the muscle-epineurium interface (top). Close-up of fascicle (bottom)
A. R. HUDSON
Fig .3
Photomicrograph of ulnar nerve beneath muscle mass, a submuscular transposition. fibrosis between the muscle-epineurium Close-up of fascicle (bottom).
118
flexor-pronator Note there is no interface (top).
TABLE 1 Morphometric analysis.
Results
At exploration three months after ulnar nerve transposition, the ulnar nerve in each of the twelve arms could be pulled proximally or distally and in each case did glide through the bed of its new location. The histological evaluation of the interface between muscle and the epineurium of the ulnar nerve demonstrated no fibrosis and, in particular, no difference between the intramuscular and the submuscular placements in terms of scar tissue formation. Morphometric analysis of the ulnar nerves transposed demonstrated no difference between fibre histograms and densities of the ulnar nerves placed intramuscular versus those placed submuscular (Table 1). The morphometric analysis demonstrated no difference in fibre histology between the region of these nerves within the muscle and the regions proximal to the muscle.
AND D. A. HUNTER
Locatton of Ulnar Nerve Submuscular Intramuscular
Mean Nerve Fibre Diameter (JA) 6.8 i 0.9* 5.9 f 0.4*
Pet-cm t Neural Tissue 33.2 zk 5.9* 28.8 i 3.4*
*not significant
During these dissections, it was noted that there was an anatomical species difference between the baboon and the human related to the cubital tunnel. Each of these baboons had an epitrochleoanconaeus muscle going from olecranon to medial humeral epicondyle innervated by a branch from the ulnar nerve just as it entered the cubital tunnel. Also, in each animal, the triceps insertion included a small muscular attachment to the floor of the cubital tunnel. There was not a prominent Osborne’s band. THE JOURNAL
OF HAND SURGERY
EFFECT
OF PLACEMENT
Discussion
The results of this study demonstrate that placement of a primate nerve along or into a length of freshly cut muscle does not result, in and of itself, in fibrosis at the muscle/epineurial interface, nor does it result in chronic compression within or beneath the resutured muscle. Thus, if one believes ulnar transposition to be indicated either technique can be chosen. Probably the most important factor in obtaining a successful result after an ulnar nerve transposition is not the method of transposition (submuscular vs. intramuscular) per se, but rather the attention which is given to the nerve proximal and distal to the region of the transfer. Traction on the nerve or new regions of impingement either proximally (medial intermuscular septum) or distally (Osborne’s band or periosteal origin of flexor carpi ulnaris head) to the transposition site may result in a failed-result in spite of careful attention to a detailed transposition itself. What factors may be responsible for the results obtained in this study and those observed clinically with respect to muscle/nerve relationships? One of the factors we believe is essential to developing the smooth interface between muscle and epineurium is movement. After allowing two weeks for the reattached muscle to heal, especially on the side where the flexor-pronator muscle mass is detached for submuscular placement, unrestricted arm movement was allowed to facilitate this gliding at the interface. It is possible, clinically, to immobilize the elbow too long. Another factor relates to the specific anatomical arrangement of the various muscles arising from medial humeral epicondyle. In humans, a thick and wide fibrous band stretches from this, condyle. where it will lay across the pathway and beneath the transposed ulnar nerve, as it gives origin to portions of the flexor-pronator muscle mass. This band is small or not present in the baboon. If this band is allowed to remain intact during ulnar nerve intra- or submuscular placement in the human, the nerve will become entrapped beneath the overlying sutured muscle fascia and this underlying fibrous ridge. Once entrapped in this area, any gliding movement would be impaired, leading to recurrent entrapment. The results of this study confirm our clinical impression that the major reason for failure of ulnar transposition
VOL. 11-B No. 1 FEBRUARY
1986
OF ULNAR
NERVE:
procedures is not the relationship of the nerve to the muscle, but the failure to eliminate adequately new sites for compression off the transposed nerve. These new sites are the fascia from the triceps to the medial intermuscular system and the medial intermuscular system proximal to the elbow, the deep fascial bands within the flexor-pronator muscle mass across the elbow, and the tethering effect of small ulnar nerve branches and periosteal origins of the ulnar head of the flexor carpi ulnaris distal to the elbow. Futhermore, it is suggested that the tenderness often attributed to the ulnar nerve in or beneath the muscle mass may be due to injury to the medial antebrachial cutaneous nerve (Dellon, 1985), rather than to scarring beneath the nerve and the muscle. References ADSON, A. W. (1918). The surgical treatment of progressive ulnar paralysis. Minnesota Medicine, I: 455-460. BROUDY, A. S., LEFFERT, R. D. and SMITH, R. _I. (1978). Technical problems with ulnar nerve transposition at the elbow: Findings and results of reoueration. The Journal of Hand Surgery. 3: 1:85-89. DELLON,& A. L. and MACKINNON, S. E (1985). Injury to the Medial Antebrachial Cutaneous Nerve During Cubital Tunnel Surgery. The Journal of Hand Surgery, 10B: 1: 33-36. FOSTER, R. J. and EDSHAGE, S. (1981). Factors related to the outcome of surgically managed compressive ulnar neuropathy at the elbow level. The Journal of Hand Surgery, 6: 2: 181-192. GAY, J. R. and LOVE, J. G. (1947). Diagnosis and Treatment of Tardy Paralvsis of the Ulnar Nerve. Based on a Studv of 100 Cases. The Journal of Bone-and Joint Surgery, 29: 4: 10X7-1097. I HARRISON, M. J. G. and NURICK, S. (1970). Results of Anterior Transposition of the Ulnar Nerve for Ulnar Neuritis. British Medical Journal. 1: 27-29. KING, T. and MORGAN, F. P. (1959). Late Results of Removing the Medial Humeral Epicondyle for Traumatic Ulnar Neuritis. The Journal of Bone and Joint Surgery, 410: 1: 51-55. LEARMONTH, J. R. (1942). A Technique for Transplanting the Ulnar Nerve. Surgery, Gynecology and Obstetrics, 75: 792-793. LEFFERT, R. D. (1982). Anterior submuscular transposition of the ulnar nerve by the Learmonth technique. The Journal of Hand Surgery, 7: 2: 147-155. LEVY, D. M. and APFELBERG, D. B. (1972). Results of Anterior Transposition for Ulnar Neuropathy at the Elbow. The American Journal of Surgery, 123: 304-308. MACNICOL, M. F. (1979). The Results of Operation for Ulnar Neuritis. The Journal of Bone and Joint Surgery, 61B: 2: 159-164. OSBORNE, G. (1957). The surgical treatment of tardy ulnar neuritis. The Journal of Bone and Joint Surgery, 39B: 4: 782 ROSE, B. W., MACKINNON, S. E., DELLON, A. L. and SNYDER, R. A. (1983). Design of a protective splint for the non-human primate extremity. Laboratory Animal Science, 33: 306-308. WADSWORTH, T. G. (1977). The External Compression Syndrome of the Ulnar Nerve at the Cubital Tunnel. Clinical Orthopaedics and Related Research, 124: 189-204. WILSON, D. H. and KROUT, R. (1973). Surgery of ulnar neuropathy at the elbow: 16 cases treated by decompression without transposition. Journal of Neurosurgery, 38: 6: 780.785.
119
Among the causes for failure of the operation of anterior transposition of the ulnar nerve at the elbow is said to be scar formation between the muscle of the incised flexor-pronator muscle mass and the ulnar nerve, when the nerve is transposed to either a submuscular or intramuscular position (Broudy, 1978). At present, none of the reports of results of treatment of ulnar nerve compression at the elbow is clearly superior to any others (Leffert, 1982; Wilson, 1973; Gay, 1947; Levy, 1072; Osborne, 1957; Harrison, 1970; King, 1970; Wadsworth, 1977; Macnicol, 1979; Foster, 1981). Indeed, most reported results of the surgical treatment of this problem are mediocre. If the operative technique required to transpose the ulnar nerve into an 1918) or submuscular intramuscular (Adson, (Learmonth, 1942) position were known to produce sufficient scar tissue about the ulnar nerve to risk recurrent entrapment, a basis would exist to select an alternate operative technique. To investigate the nature relationship, the present of this muscle-nerve experimental model was designed in the monkey. Materials
and Methods
Six adult baboons (Papio anubis) weighing lo-14 kg, were anaesthetized with a combination of ketalar and acepromazine. Each animal received 1.2 million units of Bicillin, its arm hairs were clipped, and then the arms scrubbed with betadine. Using sterile technique and 3.5 power loupe magnification, one ulnar nerve was transposed into a submuscular location as described by Learmonth (1942) and the other transposed into an intramuscular position. The medial intermuscular septum was resected in both arms, regardless of which technique was utilized. transposition For the intramuscular location, the scalpel blade was used to incise the flexor-pronator muscle mass to a depth approximately to the juncture between the middle and deepest third. Great care was taken to ensure that in its new transposed position there were no points of tetbering of the ulnar nerve either proximally or distally Receked for publication February, 1985. A. Lee Dellon, M.D., The Hampton Plaza 300 East Poppa Road Baltimore, Maryland
VOL.
11-B No. 1 FEBRUARY
1986
2.1204.
Fig. 1
Intraoperative photograph of a submuscular transposition of the ulnar nerve. At three months after surgery, the block of nerve and muscle specimen have been resected for analysis.
and the deep fascial bands orginating from the anterior surface of the elbow joint capsule were released. For both techniques, the flexor-pronator muscle fascia was closed with three horizontal mattress sutures of 3-O nylon. For both operative techniques, the branches of the flexor carpi ulnaris were preserved and dissected distally for the same distance. Each arm was closed with continuous 4-O nylon sutures and both elbows were immobilized in 90 degrees flexion in a protective orthoplast splint (Rose, 1983) for two weeks. Then, each arm was allowed unrestricted movement. There were no wound healing problems. Three months after surgery, the monkeys were anaesthetized again and specimens excised. Identical specimens were taken bilaterally to include a two cm. length of ulnar nerve proximal and distal to the flexorpronator muscle mass, the entire length or width of the flexor-pronator muscle mass through which the nerve travelled and a depth down to the anterior capsule of the elbow joint (Figure 1). The excised specimen was fixed in Karnovsky’s fixative and then post-fixed in osmium tetroxide. Sections for light microscopy were stained with toluidine blue. 117
A. L. DELLON,
Fig. 2
S. E. MACKINNON,
Photomicrograph of ulnar nerve in flexor-pronator muscle mass, an intramuscular transposition. Note muscle surrounds nerve and there is no fibrosis between the muscle-epineurium interface (top). Close-up of fascicle (bottom)
A. R. HUDSON
Fig .3
Photomicrograph of ulnar nerve beneath muscle mass, a submuscular transposition. fibrosis between the muscle-epineurium Close-up of fascicle (bottom).
118
flexor-pronator Note there is no interface (top).
TABLE 1 Morphometric analysis.
Results
At exploration three months after ulnar nerve transposition, the ulnar nerve in each of the twelve arms could be pulled proximally or distally and in each case did glide through the bed of its new location. The histological evaluation of the interface between muscle and the epineurium of the ulnar nerve demonstrated no fibrosis and, in particular, no difference between the intramuscular and the submuscular placements in terms of scar tissue formation. Morphometric analysis of the ulnar nerves transposed demonstrated no difference between fibre histograms and densities of the ulnar nerves placed intramuscular versus those placed submuscular (Table 1). The morphometric analysis demonstrated no difference in fibre histology between the region of these nerves within the muscle and the regions proximal to the muscle.
AND D. A. HUNTER
Locatton of Ulnar Nerve Submuscular Intramuscular
Mean Nerve Fibre Diameter (JA) 6.8 i 0.9* 5.9 f 0.4*
Pet-cm t Neural Tissue 33.2 zk 5.9* 28.8 i 3.4*
*not significant
During these dissections, it was noted that there was an anatomical species difference between the baboon and the human related to the cubital tunnel. Each of these baboons had an epitrochleoanconaeus muscle going from olecranon to medial humeral epicondyle innervated by a branch from the ulnar nerve just as it entered the cubital tunnel. Also, in each animal, the triceps insertion included a small muscular attachment to the floor of the cubital tunnel. There was not a prominent Osborne’s band. THE JOURNAL
OF HAND SURGERY
EFFECT
OF PLACEMENT
Discussion
The results of this study demonstrate that placement of a primate nerve along or into a length of freshly cut muscle does not result, in and of itself, in fibrosis at the muscle/epineurial interface, nor does it result in chronic compression within or beneath the resutured muscle. Thus, if one believes ulnar transposition to be indicated either technique can be chosen. Probably the most important factor in obtaining a successful result after an ulnar nerve transposition is not the method of transposition (submuscular vs. intramuscular) per se, but rather the attention which is given to the nerve proximal and distal to the region of the transfer. Traction on the nerve or new regions of impingement either proximally (medial intermuscular septum) or distally (Osborne’s band or periosteal origin of flexor carpi ulnaris head) to the transposition site may result in a failed-result in spite of careful attention to a detailed transposition itself. What factors may be responsible for the results obtained in this study and those observed clinically with respect to muscle/nerve relationships? One of the factors we believe is essential to developing the smooth interface between muscle and epineurium is movement. After allowing two weeks for the reattached muscle to heal, especially on the side where the flexor-pronator muscle mass is detached for submuscular placement, unrestricted arm movement was allowed to facilitate this gliding at the interface. It is possible, clinically, to immobilize the elbow too long. Another factor relates to the specific anatomical arrangement of the various muscles arising from medial humeral epicondyle. In humans, a thick and wide fibrous band stretches from this, condyle. where it will lay across the pathway and beneath the transposed ulnar nerve, as it gives origin to portions of the flexor-pronator muscle mass. This band is small or not present in the baboon. If this band is allowed to remain intact during ulnar nerve intra- or submuscular placement in the human, the nerve will become entrapped beneath the overlying sutured muscle fascia and this underlying fibrous ridge. Once entrapped in this area, any gliding movement would be impaired, leading to recurrent entrapment. The results of this study confirm our clinical impression that the major reason for failure of ulnar transposition
VOL. 11-B No. 1 FEBRUARY
1986
OF ULNAR
NERVE:
procedures is not the relationship of the nerve to the muscle, but the failure to eliminate adequately new sites for compression off the transposed nerve. These new sites are the fascia from the triceps to the medial intermuscular system and the medial intermuscular system proximal to the elbow, the deep fascial bands within the flexor-pronator muscle mass across the elbow, and the tethering effect of small ulnar nerve branches and periosteal origins of the ulnar head of the flexor carpi ulnaris distal to the elbow. Futhermore, it is suggested that the tenderness often attributed to the ulnar nerve in or beneath the muscle mass may be due to injury to the medial antebrachial cutaneous nerve (Dellon, 1985), rather than to scarring beneath the nerve and the muscle. References ADSON, A. W. (1918). The surgical treatment of progressive ulnar paralysis. Minnesota Medicine, I: 455-460. BROUDY, A. S., LEFFERT, R. D. and SMITH, R. _I. (1978). Technical problems with ulnar nerve transposition at the elbow: Findings and results of reoueration. The Journal of Hand Surgery. 3: 1:85-89. DELLON,& A. L. and MACKINNON, S. E (1985). Injury to the Medial Antebrachial Cutaneous Nerve During Cubital Tunnel Surgery. The Journal of Hand Surgery, 10B: 1: 33-36. FOSTER, R. J. and EDSHAGE, S. (1981). Factors related to the outcome of surgically managed compressive ulnar neuropathy at the elbow level. The Journal of Hand Surgery, 6: 2: 181-192. GAY, J. R. and LOVE, J. G. (1947). Diagnosis and Treatment of Tardy Paralvsis of the Ulnar Nerve. Based on a Studv of 100 Cases. The Journal of Bone-and Joint Surgery, 29: 4: 10X7-1097. I HARRISON, M. J. G. and NURICK, S. (1970). Results of Anterior Transposition of the Ulnar Nerve for Ulnar Neuritis. British Medical Journal. 1: 27-29. KING, T. and MORGAN, F. P. (1959). Late Results of Removing the Medial Humeral Epicondyle for Traumatic Ulnar Neuritis. The Journal of Bone and Joint Surgery, 410: 1: 51-55. LEARMONTH, J. R. (1942). A Technique for Transplanting the Ulnar Nerve. Surgery, Gynecology and Obstetrics, 75: 792-793. LEFFERT, R. D. (1982). Anterior submuscular transposition of the ulnar nerve by the Learmonth technique. The Journal of Hand Surgery, 7: 2: 147-155. LEVY, D. M. and APFELBERG, D. B. (1972). Results of Anterior Transposition for Ulnar Neuropathy at the Elbow. The American Journal of Surgery, 123: 304-308. MACNICOL, M. F. (1979). The Results of Operation for Ulnar Neuritis. The Journal of Bone and Joint Surgery, 61B: 2: 159-164. OSBORNE, G. (1957). The surgical treatment of tardy ulnar neuritis. The Journal of Bone and Joint Surgery, 39B: 4: 782 ROSE, B. W., MACKINNON, S. E., DELLON, A. L. and SNYDER, R. A. (1983). Design of a protective splint for the non-human primate extremity. Laboratory Animal Science, 33: 306-308. WADSWORTH, T. G. (1977). The External Compression Syndrome of the Ulnar Nerve at the Cubital Tunnel. Clinical Orthopaedics and Related Research, 124: 189-204. WILSON, D. H. and KROUT, R. (1973). Surgery of ulnar neuropathy at the elbow: 16 cases treated by decompression without transposition. Journal of Neurosurgery, 38: 6: 780.785.
119