- Email: [email protected]
Muscle-nerve-muscle neurotization of the orbicularis oris muscle
Journal of Cranio-Maxillofacial Surgery (2001) 29, 302–306 # 2001 European Association for Cranio-Maxillofacial Surgery doi:10.1054/jcms.2001.0233, available online at http://www.idealibrary.com on
Muscle-nerve-muscle neurotization of the orbicularis oris muscle Ch. Kermer,1 W. Millesi,1 T. Paternostro,2 M. Nuhr2 1
Department of Maxillofacial Surgery (Head: Prof. DDr. R. Ewers); 2Department of Physical Medicine and Rehabilitation (Head: Prof. Dr. Veronika Fialka), University of Vienna, Austria SUMMARY. Introduction: A denervated half of the orbicularis oris muscle is not reinnervated spontaneously by axon sprouting from the intact contralateral side. The borderline between the facial nerve territories seems to act as a barrier. The muscle-nerve-muscle technique was advocated as a technique to reneurotize a denervated half of the orbicularis oris muscle in cases of marginal mandibular paralysis. Material and methods: This muscle-nervemuscle neurotization was tried to induce reinnervation of a denervated angle of the mouth in four patients. Grafts were harvested from the sural nerve. Functional recovery was assessed by measurement of facial movements and by electrophysiological examination. Results: In three of the four cases presented, this technique helped to improve function of the lower lip. The clinical relevance of the results is discussed. # 2001 European Association for Cranio-Maxillofacial Surgery orbicularis muscle is exposed on both sides. Between these incisions a submucosal tunnel is prepared. A segment of the sural nerve is harvested and divided into several grafts with a length of 40–50 mm each. Three to four nerve grafts are introduced into the tunnel (Fig. 1). After incision of the perimysium pockets are dissected into the muscle on both sides by small incisions. Then the grafts are implanted into these pockets and fixed with one epineural 10/0 suture each to prevent dislocation. One graft is buried into the depressor labii inferioris muscle of the affected side in addition. The mucous membrane is sutured.
INTRODUCTION Partial denervation of a muscle stimulates sprouting from the remaining axons and gradually the muscle becomes reinnervated totally or partially (Hoffman, 1950, 1951; Brown et al., 1980, 1981). A good example of this phenomenon is the pectoralis major muscle in which transection of one or the other of the several branches supplying the muscle is overcome by axon sprouting. Another example is the regeneration of the trapezius muscle after transection of the accessory nerve, provided that the muscular branch of the cervical plexus remains intact (Millesi and Walzer, 1985). In contrast, the orbicularis oris muscle, bilaterally innervated by both facial nerves, does not show internal sprouting from one side (intact) to the other side, if the latter has been denervated. This is surprising as from the anatomical point of view this muscle represents a single unit within the upper and within the lower lip with fibres crossing the midline (Langer and Toldt, 1902; Eisler, 1912). One might expect that by axon sprouting the paralyzed half of the muscle might be reinnervated after transection of the facial nerve on one side. In fact there is some sprouting across the midline, but from the clinical point of view the function of the paralyzed half of the muscle remains unsatisfactory. Apparently, the centreline acts as a relative barrier between the facial nerve territories. It was this particular situation which provoked the development of muscle-nerve-muscle neurotization by Millesi and Walzer (1985).
Patients Four patients with unilateral paralysis of the marginal mandibular branch of the facial nerve were operated on by this technique. In two patients the nerve has been sacrificed during radical resection of a squamous cell carcinoma of the floor of the mouth infiltrating the mandible; in one patient the nerve was transsected during mandibular resection and reconstruction in a case of osteoradionecrosis with external fistula. In the fourth case the marginal mandibular branch was cut during parotidectomy. The period of time between denervation and operation was within 6 months in two patients, in one patient 2 years and in another, 9 years (Table 1). Paresis of the mandibular branch of the facial nerve was confirmed by preoperative EMG recordings and measurement of nerve conduction velocity.
MATERIAL AND METHODS Assessment of recovery Operative procedure Functional recovery was assessed one year after the operation by clinical investigation and electromyographic studies.
The mucous membrane of the lower lip is incised vertically near the angle of the mouth, and the 302
Muscle-nerve-muscle neurotization of the orbicularis oris muscle
To describe objectively the resting appearance of the lower lip and the mimic function as well, each patient was evaluated by measuring distance using a caliper. According to Frey et al. (1994) three static and five dynamic points were chosen (Fig. 2). The static points are the central nose point in the midline of the dorsum of the nose and the right and left tragus point at the upper border of the cartilage of the tragus. The dynamic points are the right and left mouth corner point, the philtrum point at the vermilion border of the upper lip and the right and left midlateral point of the lower lip. The midlateral lip points are defined as the centre point between the median groove at the vermilion border of the upper lip and the mouth corner point at the vermilion border of the upper lip, with vertical projection of these to the lower lip at the vermilion border. The distances between the tragus and the corner of the mouth and the distances between the central nose point and the midlateral point of the lower lip were measured in resting position and in excursions such as maximal showing of the teeth and pursing of the lips. These exercises require maximal muscle activation and therefore are highly reliable for muscular activity. Three measurements were obtained for each parameter with the arithmetic means calculated. These were then compared with those of the nonaffected side (postoperatively only). The complex functional anatomy of the perioral musculature does not allow for accurate assessment and comparison of preoperative function with postoperative in an isolated marginal mandibular paralysis. This is due to the variability of presentation of symptoms. For example, in cases of total facial paralysis the philtrum
Fig. 1 – Positioning of sural nerve grafts with both ends buried between the muscle fibres.
will always deviate to the non-affected side with pursing of the lips, allowing for objective assessment. But with an isolated marginal mandibular paralysis, the philtrum may deviate either towards or away from the affected side, not allowing for accurate comparison. For electrophysiological assessment a Nicolet Viking II EMG machine (Nicolet Biomedical Inc., Madison, Wisconsin) was used. Needle EMG examination was performed for the orbicularis oris muscle and the depressor muscles as well. Resting and voluntary activity were recorded from three sites with a concentric needle electrode of 0.46 mm diameter and 0.07 mm sq. recording area. Occurrence of pathological spontaneous activity was assessed. For recording of voluntary activity the patient was asked to purse the lips or to depress the angle of the mouth downward.
Fig. 2 – Static and dynamic points in the face.
Table 1 – Cases treated for unilateral paralysis Case no. 1 2 3 4
303
Cause for lesion Tumour resection of mandible Tumour resection of mandible Resection due to fistula and osteoradionecrosis of the mandible Parotidectomy
Time between denervation and surgery (months) 24 108 6 6
304 Journal of Cranio-Maxillofacial Surgery
Stimulation of the nerve grafts at the nonparalyzed side with recording at the affected side was not possible as the distance between the two sites was too small. Only volume-conducted electrical potentials would have been recorded. Nerve conduction studies across the nerve grafts by stimulation of the facial nerve of the unaffected side were performed in three patients. The facial nerve was stimulated by a surface electrode in front of the ear, slightly inferior to the tragus. Supramaximal rectangular pulses of 200 msec were used. Recordings by needle electrode were made from the orbicularis oris muscle of the affected side. The presence or absence of an electrically induced needle action potential was described. RESULTS The follow-up demonstrated a sufficient reinnervation of the orbicularis oris muscle in the cases 1, 3 and 4. In two patients the cosmetic result regarding symmetry was good, in one case it was satisfactory (patient 3). Reneurotization, even after such a long period as 2 years after loss of function, led to sufficient contraction and mouth closure in these patients. The results of the measurements made with the caliper are shown in Table 2. The most important distances for evaluation of the function of the
orbicularis oris muscle are those between the central nose point and the midlateral point of the lower lip in resting position and with pursing of the lips as well. In cases 1, 3 and 4, almost identical distances could be measured on both sides, proving a symmetrical appearance of the patients (Fig. 3). In patient 2 reneurotization of the orbicularis oris muscle could not be achieved. In this case the relevant distances differed by up to 8 mm. Due to lack of function of the depressor muscles, the distance between the central nose point and the midlateral point of the lower lip with maximal tooth show was restricted on the affected side in all patients. Before surgery, needle EMG examination of the orbicularis oris muscle of the affected side revealed pathological spontaneous activity and no voluntary activity in the patients. One year after surgery, as a clear sign of reinnervation, pathological spontaneous activity disappeared and voluntary activity was recorded for the patients 1, 3 and 4 (Fig. 4). Persisting pathological spontaneous activity and no voluntary activity was recorded for patient 2. For nerve conduction studies across the nerve grafts by stimulation of the facial nerve of the unaffected side, no electrically induced muscle action potential was recorded. These findings, however, cannot be attributed solely to failed axonal regrowth, but may also represent insufficient myelination of nerve fibres. The latter can completely block impulse propagation.
Table 2 – Measurements with the caliper
Tragus point – corner of mouth Distance (resting position) Distance (excursion) Smiling, showing teeth Pursing of lips Central nose – midlateral point of lower lip Distance (resting position) Distance (excursion) Smiling, showing teeth Pursing of lips Tragus point – philtrum Distance (resting position) Distance (excursion) Smiling, showing teeth Corner of mouth – philtrum Distance (resting position) Distance (excursion) Pursing of lips
Patient 1 Patient 2 Patient 3 mean range, mean range, mean range, mm (n¼3) mm (n¼3) mm (n¼3)
Patient 4 mean range, mm (n¼3)
Affected side Non-affected side
121 120
107 108
112 112
111 114
Affected side Non-affected side Affected side Non-affected side
112 109 128 125
101 95 111 113
97 98 120 123
97 100 124 128
Affected side Non-affected side
75 77
62 66
70 74
72 73
Affected side Non-affected side Affected side Non-affected side
71 76 80 80
57 64 63 71
73 77 72 73
75 76 81 83
Affected side Non-affected side
145 144
136 139
139 139
141 143
Affected side Non-affected side
145 144
131 135
134 138
139 141
Affected side Non-affected side
36 37
38 40
39 41
40 40
Affected side Non-affected side
30 32
34 34
33 32
29 29
Muscle-nerve-muscle neurotization of the orbicularis oris muscle
305
Fig. 4 – Electromyography of voluntary activity of the orbicularis oris muscle; motor unit action potential typically found by reinnervation process.
Fig. 3 – Patient with unilateral marginal mandibular paralysis (A) preoperatively; (B) same patient one year after successful reinnervation of the orbicularis oris muscle by muscle-nerve-muscle grafting.
DISCUSSION Reinnervation from the non-paralyzed side to the paralyzed half of the orbicularis oris muscle has taken place in three of the patients presented. Thus it has been demonstrated that in addition to the three classical ways of neurotization – nerve suture, nerve implantation and muscular neurotization (Rubin and McCoy, 1978; Frey et al., 1982; Brunelli and Brunelli, 1993) – it is possible to encourage axonal growth from an innervated muscle via a nerve graft to another muscle. However, in the two cases with less than 2 years after denervation, new stimuli might have also reached the paralyzed side from the resected ipsilateral nerves. But our own preoperative examinations led us to believe that regeneration had already reached a final stage. In patient no. 1 neurotization of the denervated part of the orbicularis oris muscle could be achieved even after a denervation period of 2 years. However, minimal innervation treatment clinically evident might have prevented muscular atrophy. It can be assumed that the operation itself has stimulated axonal regeneration from the non-paralyzed side to the paralyzed side. Millesi had reported on another case of successful reinnervation of the orbicularis oris muscle by the muscle-nerve-muscle technique in 1985. Six years after this operation; he
harvested a biopsy from one of the nerve grafts with adjacent muscle. The biopsy revealed myelinated axons running from the nerve graft to the muscle. Since the axons transplanted originally must have undergone Wallerian degeneration, the biopsy demonstrated that the nerve grafts were neurotisized from the innervated part of the muscle. The basic mechanism, as in muscular neurotization, is regeneration rather than sprouting of axon (Must, 1987; Carlson, 1990). The innervated part of the orbicularis oris muscle and its supplying nerves are damaged by dissecting the muscle pockets. This surgically created injury apparently caused a regenerative response from the nerves. It is difficult to determine whether the regenerative response is due directly to nerve damage or to damage of the surrounding muscle fibres. However, it seems that some of the regenerating axons could enter the nerve grafts, grow along the grafts across the midline and neurotize the denervated muscle segment. The clinical applications of this technique seem to be limited. Muscle-nerve-muscle neurotization seems to occur only in synergistic, closely related muscles, but reinnervation of the (antagonistic) depressor muscles has not been achieved in our patients. CONCLUSION In special cases of partial denervation of the orbicularis oris muscle and weakness of lip closure, this technique, the muscle-nerve-muscle neurotization, helps to improve function of the lower lip. References Brown MC, Holland LR, Ironton R: Nodal and terminal sprouting from motor nerves in fast and slow muscles of the mouse. J Physiol London 306: 493–510, 1980 Brown MC, Holland LR, Hopkins WG: Motor nerve sprouting. Ann Rev Neurosci 4: 17–42, 1981 Brunelli GA, Brunelli R: Direct Muscle neurotization. J Reconstr Microsurg 9: 81–90, 1993 Carlson B: Personal communication at the 3rd Vienna Muscle Symposium, 1990 Eisler P: Die Muskeln des Stammes. Gustav Fischer, Jena: 134–139, 1912
306 Journal of Cranio-Maxillofacial Surgery Frey M, Gruber H, Holle J, Freilinger G: An experimental comparison of the different kinds of muscle reinnervation: nerve suture, nerve implantation, and muscular neurotization. Plast Reconstr Surg 93: 1334–1349, 1994 Frey M, Jenny A, Giovanoli P, Stu¨ssi E: Development of a new documentation system for facial movements as a basis for the international registry for neuromuscular reconstruction in the face. Plast Reconstr Surg 93: 1334–1349, 1994 Hoffman H: Local reinnervation in partially denervated muscle: a histophysiological study. Aust J Exp Biol Med Sci 28: 383–397, 1950 Hoffman H: Fate of interrupted nerve fibers regenerating into partially denervated muscles. Aust J Exper Biol Med Sci 28: 211–219, 1951 Langer C von, Toldt C: Lehrbuch der systematischen und topographischen Anatomie. Braumu¨ller, Wien und Leipzig: 211–217, 1902 Millesi H, Walzer LR: Muscular neurotization. In Freilinger G (ed.): 2nd Vienna muscle symposium. Facultas Wien: 149–154, 1985
Must R: Experimental investigation of muscular neurotisation in the rat. Muscle and nerve 10: 530–536, 1987 Rubin LR, McCoy W: Neural neutrotization. Ann Plast Surg 1: 562–567, 1978
Christian Kermer Department of Maxillofacial Surgery Medical School, University of Vienna Wa¨hringer Gu¨rtel 18-20 A-1090 Vienna Austria Tel: +43 1 40400 4252 Fax: +43 1 40400 4253 Paper received 8 August 2000 Accepted 30 May 2001 Published online 31 August 2001
Muscle-nerve-muscle neurotization of the orbicularis oris muscle Ch. Kermer,1 W. Millesi,1 T. Paternostro,2 M. Nuhr2 1
Department of Maxillofacial Surgery (Head: Prof. DDr. R. Ewers); 2Department of Physical Medicine and Rehabilitation (Head: Prof. Dr. Veronika Fialka), University of Vienna, Austria SUMMARY. Introduction: A denervated half of the orbicularis oris muscle is not reinnervated spontaneously by axon sprouting from the intact contralateral side. The borderline between the facial nerve territories seems to act as a barrier. The muscle-nerve-muscle technique was advocated as a technique to reneurotize a denervated half of the orbicularis oris muscle in cases of marginal mandibular paralysis. Material and methods: This muscle-nervemuscle neurotization was tried to induce reinnervation of a denervated angle of the mouth in four patients. Grafts were harvested from the sural nerve. Functional recovery was assessed by measurement of facial movements and by electrophysiological examination. Results: In three of the four cases presented, this technique helped to improve function of the lower lip. The clinical relevance of the results is discussed. # 2001 European Association for Cranio-Maxillofacial Surgery orbicularis muscle is exposed on both sides. Between these incisions a submucosal tunnel is prepared. A segment of the sural nerve is harvested and divided into several grafts with a length of 40–50 mm each. Three to four nerve grafts are introduced into the tunnel (Fig. 1). After incision of the perimysium pockets are dissected into the muscle on both sides by small incisions. Then the grafts are implanted into these pockets and fixed with one epineural 10/0 suture each to prevent dislocation. One graft is buried into the depressor labii inferioris muscle of the affected side in addition. The mucous membrane is sutured.
INTRODUCTION Partial denervation of a muscle stimulates sprouting from the remaining axons and gradually the muscle becomes reinnervated totally or partially (Hoffman, 1950, 1951; Brown et al., 1980, 1981). A good example of this phenomenon is the pectoralis major muscle in which transection of one or the other of the several branches supplying the muscle is overcome by axon sprouting. Another example is the regeneration of the trapezius muscle after transection of the accessory nerve, provided that the muscular branch of the cervical plexus remains intact (Millesi and Walzer, 1985). In contrast, the orbicularis oris muscle, bilaterally innervated by both facial nerves, does not show internal sprouting from one side (intact) to the other side, if the latter has been denervated. This is surprising as from the anatomical point of view this muscle represents a single unit within the upper and within the lower lip with fibres crossing the midline (Langer and Toldt, 1902; Eisler, 1912). One might expect that by axon sprouting the paralyzed half of the muscle might be reinnervated after transection of the facial nerve on one side. In fact there is some sprouting across the midline, but from the clinical point of view the function of the paralyzed half of the muscle remains unsatisfactory. Apparently, the centreline acts as a relative barrier between the facial nerve territories. It was this particular situation which provoked the development of muscle-nerve-muscle neurotization by Millesi and Walzer (1985).
Patients Four patients with unilateral paralysis of the marginal mandibular branch of the facial nerve were operated on by this technique. In two patients the nerve has been sacrificed during radical resection of a squamous cell carcinoma of the floor of the mouth infiltrating the mandible; in one patient the nerve was transsected during mandibular resection and reconstruction in a case of osteoradionecrosis with external fistula. In the fourth case the marginal mandibular branch was cut during parotidectomy. The period of time between denervation and operation was within 6 months in two patients, in one patient 2 years and in another, 9 years (Table 1). Paresis of the mandibular branch of the facial nerve was confirmed by preoperative EMG recordings and measurement of nerve conduction velocity.
MATERIAL AND METHODS Assessment of recovery Operative procedure Functional recovery was assessed one year after the operation by clinical investigation and electromyographic studies.
The mucous membrane of the lower lip is incised vertically near the angle of the mouth, and the 302
Muscle-nerve-muscle neurotization of the orbicularis oris muscle
To describe objectively the resting appearance of the lower lip and the mimic function as well, each patient was evaluated by measuring distance using a caliper. According to Frey et al. (1994) three static and five dynamic points were chosen (Fig. 2). The static points are the central nose point in the midline of the dorsum of the nose and the right and left tragus point at the upper border of the cartilage of the tragus. The dynamic points are the right and left mouth corner point, the philtrum point at the vermilion border of the upper lip and the right and left midlateral point of the lower lip. The midlateral lip points are defined as the centre point between the median groove at the vermilion border of the upper lip and the mouth corner point at the vermilion border of the upper lip, with vertical projection of these to the lower lip at the vermilion border. The distances between the tragus and the corner of the mouth and the distances between the central nose point and the midlateral point of the lower lip were measured in resting position and in excursions such as maximal showing of the teeth and pursing of the lips. These exercises require maximal muscle activation and therefore are highly reliable for muscular activity. Three measurements were obtained for each parameter with the arithmetic means calculated. These were then compared with those of the nonaffected side (postoperatively only). The complex functional anatomy of the perioral musculature does not allow for accurate assessment and comparison of preoperative function with postoperative in an isolated marginal mandibular paralysis. This is due to the variability of presentation of symptoms. For example, in cases of total facial paralysis the philtrum
Fig. 1 – Positioning of sural nerve grafts with both ends buried between the muscle fibres.
will always deviate to the non-affected side with pursing of the lips, allowing for objective assessment. But with an isolated marginal mandibular paralysis, the philtrum may deviate either towards or away from the affected side, not allowing for accurate comparison. For electrophysiological assessment a Nicolet Viking II EMG machine (Nicolet Biomedical Inc., Madison, Wisconsin) was used. Needle EMG examination was performed for the orbicularis oris muscle and the depressor muscles as well. Resting and voluntary activity were recorded from three sites with a concentric needle electrode of 0.46 mm diameter and 0.07 mm sq. recording area. Occurrence of pathological spontaneous activity was assessed. For recording of voluntary activity the patient was asked to purse the lips or to depress the angle of the mouth downward.
Fig. 2 – Static and dynamic points in the face.
Table 1 – Cases treated for unilateral paralysis Case no. 1 2 3 4
303
Cause for lesion Tumour resection of mandible Tumour resection of mandible Resection due to fistula and osteoradionecrosis of the mandible Parotidectomy
Time between denervation and surgery (months) 24 108 6 6
304 Journal of Cranio-Maxillofacial Surgery
Stimulation of the nerve grafts at the nonparalyzed side with recording at the affected side was not possible as the distance between the two sites was too small. Only volume-conducted electrical potentials would have been recorded. Nerve conduction studies across the nerve grafts by stimulation of the facial nerve of the unaffected side were performed in three patients. The facial nerve was stimulated by a surface electrode in front of the ear, slightly inferior to the tragus. Supramaximal rectangular pulses of 200 msec were used. Recordings by needle electrode were made from the orbicularis oris muscle of the affected side. The presence or absence of an electrically induced needle action potential was described. RESULTS The follow-up demonstrated a sufficient reinnervation of the orbicularis oris muscle in the cases 1, 3 and 4. In two patients the cosmetic result regarding symmetry was good, in one case it was satisfactory (patient 3). Reneurotization, even after such a long period as 2 years after loss of function, led to sufficient contraction and mouth closure in these patients. The results of the measurements made with the caliper are shown in Table 2. The most important distances for evaluation of the function of the
orbicularis oris muscle are those between the central nose point and the midlateral point of the lower lip in resting position and with pursing of the lips as well. In cases 1, 3 and 4, almost identical distances could be measured on both sides, proving a symmetrical appearance of the patients (Fig. 3). In patient 2 reneurotization of the orbicularis oris muscle could not be achieved. In this case the relevant distances differed by up to 8 mm. Due to lack of function of the depressor muscles, the distance between the central nose point and the midlateral point of the lower lip with maximal tooth show was restricted on the affected side in all patients. Before surgery, needle EMG examination of the orbicularis oris muscle of the affected side revealed pathological spontaneous activity and no voluntary activity in the patients. One year after surgery, as a clear sign of reinnervation, pathological spontaneous activity disappeared and voluntary activity was recorded for the patients 1, 3 and 4 (Fig. 4). Persisting pathological spontaneous activity and no voluntary activity was recorded for patient 2. For nerve conduction studies across the nerve grafts by stimulation of the facial nerve of the unaffected side, no electrically induced muscle action potential was recorded. These findings, however, cannot be attributed solely to failed axonal regrowth, but may also represent insufficient myelination of nerve fibres. The latter can completely block impulse propagation.
Table 2 – Measurements with the caliper
Tragus point – corner of mouth Distance (resting position) Distance (excursion) Smiling, showing teeth Pursing of lips Central nose – midlateral point of lower lip Distance (resting position) Distance (excursion) Smiling, showing teeth Pursing of lips Tragus point – philtrum Distance (resting position) Distance (excursion) Smiling, showing teeth Corner of mouth – philtrum Distance (resting position) Distance (excursion) Pursing of lips
Patient 1 Patient 2 Patient 3 mean range, mean range, mean range, mm (n¼3) mm (n¼3) mm (n¼3)
Patient 4 mean range, mm (n¼3)
Affected side Non-affected side
121 120
107 108
112 112
111 114
Affected side Non-affected side Affected side Non-affected side
112 109 128 125
101 95 111 113
97 98 120 123
97 100 124 128
Affected side Non-affected side
75 77
62 66
70 74
72 73
Affected side Non-affected side Affected side Non-affected side
71 76 80 80
57 64 63 71
73 77 72 73
75 76 81 83
Affected side Non-affected side
145 144
136 139
139 139
141 143
Affected side Non-affected side
145 144
131 135
134 138
139 141
Affected side Non-affected side
36 37
38 40
39 41
40 40
Affected side Non-affected side
30 32
34 34
33 32
29 29
Muscle-nerve-muscle neurotization of the orbicularis oris muscle
305
Fig. 4 – Electromyography of voluntary activity of the orbicularis oris muscle; motor unit action potential typically found by reinnervation process.
Fig. 3 – Patient with unilateral marginal mandibular paralysis (A) preoperatively; (B) same patient one year after successful reinnervation of the orbicularis oris muscle by muscle-nerve-muscle grafting.
DISCUSSION Reinnervation from the non-paralyzed side to the paralyzed half of the orbicularis oris muscle has taken place in three of the patients presented. Thus it has been demonstrated that in addition to the three classical ways of neurotization – nerve suture, nerve implantation and muscular neurotization (Rubin and McCoy, 1978; Frey et al., 1982; Brunelli and Brunelli, 1993) – it is possible to encourage axonal growth from an innervated muscle via a nerve graft to another muscle. However, in the two cases with less than 2 years after denervation, new stimuli might have also reached the paralyzed side from the resected ipsilateral nerves. But our own preoperative examinations led us to believe that regeneration had already reached a final stage. In patient no. 1 neurotization of the denervated part of the orbicularis oris muscle could be achieved even after a denervation period of 2 years. However, minimal innervation treatment clinically evident might have prevented muscular atrophy. It can be assumed that the operation itself has stimulated axonal regeneration from the non-paralyzed side to the paralyzed side. Millesi had reported on another case of successful reinnervation of the orbicularis oris muscle by the muscle-nerve-muscle technique in 1985. Six years after this operation; he
harvested a biopsy from one of the nerve grafts with adjacent muscle. The biopsy revealed myelinated axons running from the nerve graft to the muscle. Since the axons transplanted originally must have undergone Wallerian degeneration, the biopsy demonstrated that the nerve grafts were neurotisized from the innervated part of the muscle. The basic mechanism, as in muscular neurotization, is regeneration rather than sprouting of axon (Must, 1987; Carlson, 1990). The innervated part of the orbicularis oris muscle and its supplying nerves are damaged by dissecting the muscle pockets. This surgically created injury apparently caused a regenerative response from the nerves. It is difficult to determine whether the regenerative response is due directly to nerve damage or to damage of the surrounding muscle fibres. However, it seems that some of the regenerating axons could enter the nerve grafts, grow along the grafts across the midline and neurotize the denervated muscle segment. The clinical applications of this technique seem to be limited. Muscle-nerve-muscle neurotization seems to occur only in synergistic, closely related muscles, but reinnervation of the (antagonistic) depressor muscles has not been achieved in our patients. CONCLUSION In special cases of partial denervation of the orbicularis oris muscle and weakness of lip closure, this technique, the muscle-nerve-muscle neurotization, helps to improve function of the lower lip. References Brown MC, Holland LR, Ironton R: Nodal and terminal sprouting from motor nerves in fast and slow muscles of the mouse. J Physiol London 306: 493–510, 1980 Brown MC, Holland LR, Hopkins WG: Motor nerve sprouting. Ann Rev Neurosci 4: 17–42, 1981 Brunelli GA, Brunelli R: Direct Muscle neurotization. J Reconstr Microsurg 9: 81–90, 1993 Carlson B: Personal communication at the 3rd Vienna Muscle Symposium, 1990 Eisler P: Die Muskeln des Stammes. Gustav Fischer, Jena: 134–139, 1912
306 Journal of Cranio-Maxillofacial Surgery Frey M, Gruber H, Holle J, Freilinger G: An experimental comparison of the different kinds of muscle reinnervation: nerve suture, nerve implantation, and muscular neurotization. Plast Reconstr Surg 93: 1334–1349, 1994 Frey M, Jenny A, Giovanoli P, Stu¨ssi E: Development of a new documentation system for facial movements as a basis for the international registry for neuromuscular reconstruction in the face. Plast Reconstr Surg 93: 1334–1349, 1994 Hoffman H: Local reinnervation in partially denervated muscle: a histophysiological study. Aust J Exp Biol Med Sci 28: 383–397, 1950 Hoffman H: Fate of interrupted nerve fibers regenerating into partially denervated muscles. Aust J Exper Biol Med Sci 28: 211–219, 1951 Langer C von, Toldt C: Lehrbuch der systematischen und topographischen Anatomie. Braumu¨ller, Wien und Leipzig: 211–217, 1902 Millesi H, Walzer LR: Muscular neurotization. In Freilinger G (ed.): 2nd Vienna muscle symposium. Facultas Wien: 149–154, 1985
Must R: Experimental investigation of muscular neurotisation in the rat. Muscle and nerve 10: 530–536, 1987 Rubin LR, McCoy W: Neural neutrotization. Ann Plast Surg 1: 562–567, 1978
Christian Kermer Department of Maxillofacial Surgery Medical School, University of Vienna Wa¨hringer Gu¨rtel 18-20 A-1090 Vienna Austria Tel: +43 1 40400 4252 Fax: +43 1 40400 4253 Paper received 8 August 2000 Accepted 30 May 2001 Published online 31 August 2001