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Smile Reconstruction in Adults with Free Muscle Transfer Innervated by the Masseter Motor Nerve: Effectiveness and Cerebral Adaptation

Manktelow, Ralph T. M.D.; Tomat, Laura R. M.Sc.; Zuker, Ron M. M.D.; Chang, Mary B.Sc., P.T.

doi: 10.1097/01.prs.0000232195.20293.bd
RECONSTRUCTIVE: HEAD AND NECK: ORIGINAL ARTICLES
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Background: This study assesses the ability of the masseter motor nerve–innervated microneurovascular muscle transfer to produce an effective smile in adult patients with bilateral and unilateral facial paralysis.

Methods: The operation consists of a one-stage microneurovascular transfer of a portion of the gracilis muscle that is innervated with the masseter motor nerve. The muscle is inserted into the cheek and attached to the mouth to produce a smile. The outcomes assessed were the amount of movement of the transferred muscle; the aesthetic quality of the smile; the control, use, and spontaneity of the smile; and the functional effects on eating, drinking, and speech. The study included 27 patients aged 16 to 61 years who received 45 muscle transfers.

Results: All 45 muscle transfers developed movement. The commissure movement averaged 13.0 ± 4.7 mm at an angle of 47 ± 15 degrees above the horizontal, and the mid upper lip movement averaged 8.3 ± 3.0 mm at 42 ± 17 degrees. Age did not affect the amount of movement. Patients older than 50 years had the same amount of movement as patients younger than 26 years (p = 0.605). Ninety-six percent of patients were satisfied with their smile.

Conclusions: A spontaneous smile, the ability to smile without thinking about it, occurred routinely in 59 percent and occasionally in 29 percent of patients. Eighty-five percent of patients learned to smile without biting. Age did not affect the degree of spontaneity of smiling or the patient's ability to smile without biting.

Toronto, Ontario, Canada

From the Division of Plastic Surgery, Toronto General Hospital, University Health Network; Division of Plastic Surgery, Hospital for Sick Children; and Toronto Western Hospital, University Health Network.

Received for publication December 9, 2004; accepted May 17, 2005.

Presented in part at the Ninth International Facial Nerve Symposium, in San Francisco, California, July 30, 2001; the Inaugural Congress of the World Society for Reconstructive Microsurgery, in Taipei, Taiwan, November of 2001; the American Association of Plastic Surgeons, in Seattle, Washington, April 29, 2002 (2002 Leonard R. Rubin AAPS Best Paper Award); the Canadian Society of Plastic Surgeons, in St. John, New Brunswick, May 13, 2002; and the 14th Annual Meeting of the European Association of Plastic Surgeons, in Vienna, Austria, June 5, 2003.

Readers may also refer to the online version of the article at the Journal's Web site (www.PRSJournal.com) for additional materials.

Ralph T. Manktelow, M.D., University Health Network, Toronto General Hospital, 200 Elizabeth Street, Eaton North 7-228, Toronto, Ontario M5G 2C4, Canada, rmanktelow@hotmail.com

Effective communication is very difficult in the presence of the asymmetric or absent facial expression that is found in facial paralysis. A smile or a laugh is at least as important as speech in communicating meaning and emotional feeling. Frequently, a smile is a spontaneous expression, and this spontaneity is an important capability. However, a normal smile can be produced by either conscious effort or as a spontaneous response to an emotional event.

In the past 20 years, the procedure of microneurovascular muscle transfer has had increasing acceptance as the preferred operation for reconstructing the paralyzed lower face. The contralateral seventh nerve, by means of a cross-facial nerve graft, provides the preferred innervation of a muscle transfer for unilateral facial paralysis reconstruction.1–6 The prospect of obtaining spontaneous smile movement by innervation from the contralateral seventh nerve has endeared this procedure to the surgeon. However, patients who have bilateral facial paralysis require a different nerve for innervation of the transfer. In addition, some patients with apparent unilateral paralysis have no nerves to spare on the uninvolved side with which to innervate a cross-facial nerve graft effectively. This clinical situation, where the seventh nerve is not available or inadequate, presents a significant innervation problem. In these situations, we have used either the hypoglossal nerve, the motor nerve to the masseter muscle, or the motor nerve to the trapezius.

The selected motor nerve must provide adequate innervation to produce strong muscle contraction and allow the patient to control the movement of the muscle. Patients want to have conscious control of their smile and also have a spontaneous smile. In our initial experience with the masseter motor nerve, we did not expect to obtain a spontaneous smile. We believed that, with innervation using any nerve other than the seventh, we would be unable to obtain a spontaneous smile. We expected that the patient would always have to bite to activate his or her smile.

The purpose of this article is to study the effectiveness of the masseter motor nerve in providing adequate innervation to a muscle transfer for lower facial reconstruction in adults. Does the masseter motor nerve produce a muscle contraction that provides a good simulation of a smile and does the patient incorporate this smile into normal social activities? We assessed the patient's use of their smile in social activities and evaluated the patient's ability to smile spontaneously, that is, without thinking of biting or closing the jaw and without conscious thought.

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PATIENTS AND METHODS

All 33 adult patients who received a gracilis muscle transfer innervated with the masseter motor nerve between 1983 and July 2003 were candidates for the study. Of the 33 patients who received one or more masseter innervated gracilis transfers, 27 agreed to participate in the study and complete the questionnaire.

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Operative Technique

The operation consisted of a microneurovascular transfer of a portion of the gracilis muscle to the paralyzed side of the face.7 The muscle was inserted into the perioral soft tissues using a no. 2 polyglycolic acid suture (Fig. 1). This thickness of suture is used to provide secure fixation that prevents the suture from cutting through the tissues while fibrous union is occurring. If muscle tissue was available, the insertion points were into the paralyzed orbicularis oris muscle at the site of the insertion of the zygomaticus major and the levator labii superioris. If no muscle tissue was available for insertion, the transfer was inserted into fibrofatty tissue of the lip at these same sites. To support the lower lip, the most inferior point of insertion was at the point on the lower lip where the depressor anguli oris is normally inserted. The temporal and preauricular parotid fascia was used as a fixation site for the muscle's new origin. For bilateral reconstructions, the muscle was inserted identically on each side, and the operation on the second side was performed 2 to 4 months after the first. If the reconstruction was unilateral, the origin and insertion were selected in a manner that was designed to mimic the shape of the smile on the other side. Each muscle was reinnervated with the motor nerve to the masseter muscle. This nerve was found on the deep surface of the deep head of the masseter muscle near its posterior superior margin. By detaching the posterior 2 to 3 cm of the origin of the masseter muscle from the arch of the zygoma, the nerve was identified as it passed inferiorly and anteriorly (Fig. 2). A 2-cm length of nerve was exposed, divided inferiorly, and transposed superficially for nerve coaptation. Muscle revascularization was performed with the facial artery and vein.

Fig. 1.

Fig. 1.

Fig. 2.

Fig. 2.

After the onset of muscle movement, which was usually 3 to 4 months after the final operation, a learning process was commenced. The patient began by practicing smile movement when looking in the mirror, making a biting motion, and observing the effect. This taught the patients how to create and control their smile and to develop confidence in the appearance of their smile. The patients then practiced their smile with family and friends and, after they had developed confidence, with strangers.

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Data Collection

Demographic information and preoperative and postoperative clinical data were collected from 10 patients from hospital and clinic charts. Data for the 17 most recent patients were collected from a database designed specifically for the muscle transfer operation.

Nineteen patients had postoperative smile movement measurements assessed by the FaceMS.8 The FaceMS is a validated movement measurement technique that uses a digital video camera, a computer, a video editing program, and Adobe Photoshop (Adobe Systems, Inc., San Jose, Calif.). The FaceMS technique was used to provide measurements of the amount and direction of movement of the commissure and mid upper lip. The handheld ruler measurement technique involves the use of a transparent ruler that is held against the lips in a standardized manner. This technique allows measurement of the relationships of selected points on the lips to each other and to the midline. The commissure was identified as the lateral point where the upper and lower lip vermilion margins meet. The mid upper lip point was on the vermilion margin of the upper lip halfway between the commissure and the central point of the Cupid's bow. Eight patients were unable to return for a follow-up examination and measurements because they lived too far away. For these eight patients, the presence of facial movement was verified either by standardized photographs or videos that were sent to us; however, measurements could not be obtained.

A questionnaire was mailed to study participants to assess the aesthetic quality of their reconstructed smile; the control, use, and spontaneity of their smile; and functional effects on eating, drinking, and speech (see appendix, Masseter Questionnaire, in the online version of the Journal at www.PRSJournal.com). A cover letter stated that the surgeon would not be allowed to see the returned questionnaire or individual results. The questionnaire is divided into eight sections: eating, drinking, and speech; comfort level with the use of one's smile; frequency of use of one's smile; enjoyment of one's smile; biting; overall satisfaction; learning techniques to smile; and appearance at rest. The section titled biting assessed the need to move the jaw to activate the smile and the development of spontaneous smiling.

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Statistical Analysis

All analysis was performed using SPSS software (SPSS, Inc., Chicago, Ill.). Two-tailed paired sample t tests were performed to evaluate the significance of preoperative versus postoperative events. Analysis of variance was used to evaluate the effect of age, gender, and muscle weight on commissure movement. Regression analysis was used to compare muscle movement, weight, and age. Because rest positions were categorized, chi-square tests were performed to compare preoperative versus postoperative measures. Statistically significant results were obtained for values of p < 0.05.9

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RESULTS

The study group of 27 patients included 18 women and nine men, with an average age of 34.4 years at the time of their first muscle transfer (range, 16 to 61 years). Eighteen patients received bilateral muscle transfers and nine received unilateral transfers. Thus, the study included 45 muscle transfers in 27 patients.

The average time between paralysis onset and date of first muscle operation was 20.3 years, with a range between 2 and 54 years. The follow-up from the time of the patient's first muscle operation to the time that this study was conducted ranged from 0.4 to 20.7 years, with an average of 4.7 years.

Of the 27 patients, nine had total bilateral, nine had partial bilateral, and nine had primarily a unilateral facial paralysis. Twelve patients had congenital palsies and 15 had acquired palsies. The causes of palsy in the 18 bilateral patients were Mobius syndrome in eight, other congenital in one, Bell's palsy in one, intracranial tumor in three, temporal bone fracture in one, and miscellaneous in four. The causes of the palsy in the unilateral patients were parotid tumor in one, acoustic neuroma in one, intracranial tumor in one, Bell's palsy in two, congenital in three, and basal skull fracture in one.

The average age of the nine unilateral patients at the time of their muscle operation was 36.0 years. The average duration from time of paralysis onset to time of surgery was 16.8 years, with a range of 4 to 38 years. Innervation by a cross-facial nerve graft was not used for these nine patients either because there were no nerves to spare on the apparently intact side (n = 7) or because there was a concern that innervation would not be strong enough with a cross-facial nerve graft because of advanced age and a particularly strong smile on the normal side (n = 2).

Each transfer consisted of a segment of the gracilis muscle that was centered on the dominant vascular pedicle. Forty to 60 percent of the width of the gracilis muscle was used. The segment of muscle weighed an average of 26.5 g (range, 12 to 41 g) and had an average length of 8.5 cm on the upper margin and 7.5 cm on the lower margin. During the muscle operation, two patients had rhytidectomies, one had a sling to the mouth using tendon, and two had fat removed from the cheek area. One or more years after the muscle operation, two patients returned to have fat removed from their cheek to decrease bulkiness. Two unilateral patients had a tendon sling inserted to replace the paralyzed orbicularis oris in one-half of their lower lip, one patient had the muscle repositioned, and two patients had a vermilion resection to their lower lip.

Postoperative complications included one hematoma that was removed in the operating room and one facial abscess that was drained at 8 days after muscle transfer. Five patients developed postoperative swelling with or without redness, two in the face and three in the thigh. They were assumed to have had early cellulitis and were treated with antibiotics. Their conditions resolved promptly without sequelae.

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Movement Analysis

All 45 muscles developed movement. Nineteen patients with 31 muscle transfers were available for measurement of commissure and mid upper movement. This included all patients who could travel to our center. The commissure movement of all 31 muscles transfers averaged 13.0 ± 4.7 mm at an angle of 47 ± 15 degrees above the horizontal. The mid upper lip point moved an average of 8.3 ± 3.0 mm at an angle of 42 ± 17 degrees (Fig. 3 and Table 1).

Fig. 3.

Fig. 3.

Table 1

Table 1

There was no significant difference in the amount of movement gained by unilateral and bilateral patients (p = 0.473; 95 percent confidence interval, –3.812 to 7.29). In the unilateral patients, the amount and direction of movement of the reconstructed side was compared with the other side to assess symmetry of the reconstruction. The commissure on the reconstructed side moved on average 85 percent as much as on the normal side. There was no significant difference between the reconstructed commissure and the normal commissure (p = 0.232, 95 percent confidence interval, –5.56 to 1.64). In unilateral patients, the commissure on the reconstructed mid upper lip moved 68 percent as much as on the normal upper lip. This difference was significant (p = 0.001; 95 percent confidence interval, 3.93 to 1.81). The direction of movement (angle above the horizontal) of the normal (p = 0.501; 95 percent confidence interval, –8.9 to 16.4) and reconstructed commissures and upper lips (p = 0.5, 95 percent confidence interval, –10.17 to 18.45) was not significantly different.

The possible factors affecting the amount of muscle excursion as revealed by commissure movement were analyzed. The factors assessed included age, gender, side of reconstruction, muscle weight, and coverage of motor nerve. An analysis of variance comparing gender and muscle excursion revealed that male patients had greater movement than female patients (mean,14.5 and 12.0 mm, respectively) (p = 0.249). An analysis of variance comparing gender and weight of muscle indicated a significant difference between male muscle weights (mean, 29.57 ± 6.9 g) and female muscle weights (mean, 21.75 ± 4.7 g) (p = 0.012). A linear regression indicated 24 percent of variation in commissure movement is explained by muscle weight (p = 0.045), with an increase in muscle weight producing increased excursion.

Regression analyses were performed to compare ages and amount of commissure movement. Age was not related to the amount of movement (p = 0.955). As we are particularly concerned about recommending surgery in the older age group, patients were divided into two equal groups. Analysis of variance was used to compare patients at the top half of our age group (range, 34 to 61 years) to patients at the lower half of the age group (range, 16 to 32 years). There was no significant difference in commissure movement between the groups (p = 0.289). The amount of commissure movement in patients at the extreme ends of the age range was also compared. The six patients older than 50 years were compared with the six patients younger than 26 years. There was no significant difference in the amount of commissure movement (p = 0.605). The oldest bilateral patient (61 years) had an average excursion of the commissure of 18.3 mm (Fig. 4), and our oldest unilateral patient (59 years) had an average excursion of the commissure of 14.6 mm (Fig. 5); both of these values are above the average range of excursion for the entire group.

Fig. 4.

Fig. 4.

Fig. 5.

Fig. 5.

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Assessment of Spontaneity and Biting

Eighty-nine percent of patients reported smiling spontaneously, which is without consciously thinking about it some of the time. Fifty-nine percent of patients reported routinely smiling spontaneously. These patients responded to the question regarding whether they must consciously think to smile that this was the case one-half of the time or rarely. Spontaneous smiling occurred all or most of the time in 37 percent of patients.

Eighty-five percent of patients learned to smile without biting. Sixty-nine percent of patients learned to smile without biting all or most of the time. Fifteen percent of patients needed to bite to smile at least half of the time. Fifteen percent always needed to bite to smile. Thirty percent of patients were uncomfortable with the appearance of their smile movements when eating with others and 70 percent were comfortable with their facial movements while eating.

We divided the patients into two groups, aged 16 to 32 years (14 patients) and 34 to 61 years (13 patients), and compared the two groups with respect to the frequency of a spontaneous smile and the ability to smile without biting. Smiling spontaneously occurred routinely 64 percent of the time in the younger group and 54 percent of the time in the older group. Smiling without biting occurred routinely 62 percent of the time in the younger group and 77 percent of the time in the older group. Three of six patients who were 50 years of age or older routinely had a spontaneous smile.

Within the cohort of patients, there were three with total bilateral congenital and one with total unilateral congenital facial paralysis. Thus, these patients had no previous smile experience either on both sides or on the side of the paralysis. After surgery, two patients were able to smile without biting all the time and two were able to smile without biting at least half the time. All four smiled spontaneously, with two patients smiling spontaneously almost all the time and two smiling spontaneously occasionally.

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Aesthetic Analysis

The preoperative and postoperative appearance of representative smile reconstructions is illustrated in Figures 4 through 8. Patients judged the aesthetic quality of their smile (Table 2) and their degree of comfort using their smile in various situations (Table 3).

Fig. 6.

Fig. 6.

Fig. 7.

Fig. 7.

Fig. 8.

Fig. 8.

Table 2

Table 2

Table 3

Table 3

All patients admitted using their smile at least some of the time when they are with family and friends, and 69 percent use it all or most of the time. There was no significant difference between the frequency of smile use when with family and friends versus and when with strangers (p = 1.0; 95 percent confidence interval, –0.2903 to 0.2903). Eighty-two percent of patients were sure that strangers recognized when they were smiling and 18 percent were unsure. Ninety-six percent of patients were satisfied with their smile. One patient said that even though she was not satisfied with her smile, she might undergo the surgery again. The only person who would not have the surgery again was a 54-year-old bilateral patient who indicated that, although she was very satisfied with the result of the surgery, the surgery had been too much effort for her.

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Eating, Drinking, and Speech

Fifty percent of patients who had difficulty eating and drinking were improved and 38 percent were unchanged after surgery. The incidence of difficulty eating and drinking was reduced from 75 percent to 38 percent for unilateral patients and from 50 percent to 22 percent for bilateral patients (p = 0.093).

There was a significant improvement in the ability of patients to pronounce words containing the labial sounds “b,” “p,” and “s.” Fifty-two percent of those having difficulty speaking were able speak more clearly and 48 percent were unchanged following surgery. The incidence of difficulty speaking was reduced from 67 percent to 11 percent for unilateral patients and from 87 percent to 53 percent for bilateral patients following surgery.

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DISCUSSION

Study Technique

A questionnaire was used to assess the patient's opinion of their smile, the spontaneity of their smile, and other functional effects of surgery (see appendix, Masseter Questionnaire, in the online version of the Journal at www.PRSJournal.com). For each question, there was a choice of four or five responses, such as very easy, easy, difficult, very difficult, and do not know. This choice provided the patients with the opportunity to grade their answer. As 82 percent of patients participated in the study and completed the questionnaire, the responses should be representative of the entire cohort. We resisted the temptation to assess and grade the smile ourselves because of potential bias caused by our involvement in the treatment. The judgment of the patient was felt to be a relevant assessment of aesthetics. However, this judgment is also subject to bias because of the doctor–patient relationship. To minimize doctor–patient relationship bias, the surgeons were blinded to the individual responses to the questionnaire, and the patients were so informed.

This questionnaire was an effective means of assessing whether patients incorporate their smile into interpersonal relationships. However, a useful opportunity to assess the nature and control of the patient's smile also occurred during informal conversations during postoperative visits in the clinic. The authors frequently observed spontaneous laughter and smiling at these visits.

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Muscle Excursion

Measurements of the amount of smile movement were obtained using the FaceMS technique.8 With this technique, we measured the amount of movement of the commissure, mid upper and mid lower lips, and central lip points. Of these measurements, the movements of commissure and mid upper lip points have been shown to be the most valid points for evaluating the smile movement.10 We have therefore reported the vectors of movement of these points. Recently published studies of microneurovascular muscle transfers,1–6 except for one,6 do not report the amount of movement produced by the transfer during smiling. We feel that quantitative assessments of lip movements are necessary to evaluate and compare results objectively.

There were 45 muscle transfers in 27 patients available for study. All 45 muscles contracted and 31 were available for measurement. The maximum smile in a normal nonparalyzed face has a commissure movement of 7 to 22 mm (average, 14 mm).10 The maximum smile excursion of our masseter-innervated gracilis muscle transfers was 6 to 22 mm (average, 13 mm), which is the normal range of movement for the normal smile.11 In fact, muscle contraction is so strong that we feel we can use smaller pieces of muscle, thus allowing us to obtain good movement and minimizing the potential bulk in the cheek.

We assessed factors that might have an effect on the amount of muscle excursion. We examined age, weight of muscle used, and length of transferred muscle. However, we were only able to show a modest direct relationship between the weight of muscle used and muscle excursion. Although men had a larger excursion than women, they also had, on average, larger muscles, and we suspect that muscle weight and not gender is the most important factor. Although there are few data on the quality of nerve recovery with respect to age, it is generally believed that the results of nerve repairs are poorer with increasing years.12 However, in this study of facial paralysis muscle transfer, we could not establish any significant difference in the range of movement with respect to age. Not only was there no difference in muscle excursion when the older half of the group was compared with the younger half, but when the extreme ends of the age scale were compared, there was no difference. On the basis of our prior experience with microneurovascular muscle transfer to the upper extremity, we had suspected that age might not be significant in determining the quality of motor nerve recovery in general.13,14

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Reliability of Movement

All 45 muscles survived, contracted, and gave a useful smile. Of the 31 muscles from which we obtained postoperative measurements, all gave a commissure excursion that was in the normal range (7 to 22 mm),10 except for four muscles. These muscles were in two bilateral patients whose commissure movements averaged only 6 mm, which is slightly less than the lower limit of normal. However, they still had a recognizable and useful smile. The effectiveness of this innervation should be compared with that of a cross-facial nerve graft. When a cross-facial nerve is used to innervate a muscle transfer, our experience is that there is a wide variation in the amount of movement that is obtained, the amount of movement is rarely as much as on the opposite normal side, and sometimes there is no movement. The reason for this variability of results and generally smaller excursion is related to the use of a nerve graft.

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Cerebral Adaptation

Our goal was to provide effective facial expression using the fifth cranial nerve rather than the seventh. Effective facial expression frequently involves smiling under voluntary control. This was our initial objective. However, with time, we became increasingly interested in the possibility of smiling without actually biting or consciously thinking about smiling (i.e., a spontaneous smile).

Although we have used masseter motor nerve–innervated transfers more frequently in children (146 muscles in 78 children) than in adults, we chose to study adults because the adult is more self-aware and can report the ability to smile spontaneously. We chose the questionnaire as an evaluation technique because it provides a patient's own assessment of the occurrence of a spontaneous smile and its frequency. We found that people who would like to smile become very aware of a smile that occurs without conscious effort, as do their friends and family—who give valuable feedback. Artificial settings such as a video studio, although useful for recording a smile, are unlikely to duplicate normal social interaction.

To assess whether there was spontaneity of movement when the fifth cranial nerve, a nerve used to bite, is used to produce a smile, we asked whether patients needed to consciously think to produce a smile and whether they actually had to bite to smile. We recognized that some of a nonparalyzed person's smiling is a response to conscious effort and some is unconscious and a response to emotional events. A spontaneous smile, which is the ability to smile without thinking about it, occurred in 89 percent of patients at least some of the time. In 59 percent of patients, it occurred routinely (i.e., half the time or more). These were the most surprising findings of this study and bring up the issue of cerebral plasticity, or cerebral cortical reorganization. This is the ability of the human brain to reorganize, adapt, and compensate for injury or changes in the environment. Even though the temporalis and masseter muscles have been used for facial paralysis reconstruction for at least 60 years15 and more recently have been popularized by Rubin, we were unable to find any studies that identified the effectiveness of cerebral adaptation when these muscles are used to reconstruct facial expression.

To facilitate the use of the muscle transfer, the patients were given a learning program. The goal was to develop facility in smiling at other persons and particularly to encourage spontaneous smiling presumably through cerebral cortical reorganization. After the muscle transfer, the patient initially learns to simulate a smile by biting. By practicing this in front of a mirror, the patient gains confidence in their ability to produce a smile. Different degrees and types of smiles are learned by observing the effect of making a weak or a forceful bite and of slowly or quickly developing biting pressure. The learning begins shortly after muscle movement has occurred and is done for short periods of time many times per day. As the principal learning stimuli for physical skills are repetition, reinforcement, and motivation,11,16 the patient is encouraged to use their smile as frequently as possible. When the patient smiles at another person who responds by smiling back, there is a powerful reinforcement both consciously and unconsciously that likely aids the learning process. The patient is encouraged to become a smiling person so that, through frequent repetition, they develop confidence in their smile and maximize the changes in the cerebral cortex.

The first accomplishment in the learning process is apparent when the patient is able to consciously contract their transferred gracilis muscle and smile without biting or closing their jaw. When asked how they developed this ability, patients can never explain it; they say that “it just happens.” The next step in the learning/adaptation process is to smile spontaneously (i.e., without conscious effort). Patients are also unable to explain how they accomplish this step in the process of incorporating the smile into their socialization. These capabilities are likely facilitated by the repetitive action of using their smile when interacting with other people. Using the new smile in appropriate social situations will usually result in another person returning a smile. The patient then realizes that the movement was indeed recognized as a smile. We feel that using the smile in social situations that prompt another person to return a smile is particularly beneficial in training the patient's cerebral cortex. A returned smile should reinforce the learning process.

Cerebral cortical reorganization is known to occur in many clinical situations, including Braille reading, following nerve injuries, and in limb amputations.17 One of the clearest examples of cerebral cortical reorganization occurs with nerve transfers in patients with brachial plexus injuries. Reconstruction of biceps function is done by attaching the intercostal nerves to the musculocutaneous nerve. After reinnervation, the patient initially activates the transfer by taking a deep breath and thus flexes the elbow. After 1 to 2 years, many patients begin to move their elbow independent of respirations and can maintain the biceps muscle contraction without disturbing respiration; they have learned to separate respiratory movements from elbow movements. To bend their elbow, they no longer think of breathing but think of bending their elbow.

This process has been studied using transcranial magnetic stimulation and functional magnetic resonance imaging. The control center for respiratory movement is in the medial aspect of the primary motor cortical area, and the center for elbow flexion is in the lateral aspect of the primary motor cortical area. Motor cortical reorganization has been shown by our group and reported by Chen et al.17,18 to occur when intercostal nerves are transferred to the musculocutaneous nerve or to the nerve of a functioning muscle transfer used for biceps reconstruction. Functional magnetic resonance imaging and transcranial magnetic stimulation studies demonstrated that, initially, the respiratory center controlled elbow flexion. After 6 months, the biceps cortical center appears to take control of elbow flexion. The biceps cortical center would appear to be controlling elbow flexion by way of the respiratory cortical center through the peripheral respiratory nerve pathway, which ends in the intercostal nerves.17,19

In our facial muscle transfers, we have not been able to use functional magnetic resonance imaging or transcranial magnetic stimulation to study the shifting of control from the “jaw muscle center” to the “facial movement center” because of the close proximity of the two centers. It is likely that there is a similar process, with the facial nerve center taking over control by activating connections to the fifth nerve center and through this center activating the motor axons of the masseter branch of the trigeminal nerve, causing gracilis muscle contraction and a smile. The mechanism of cerebral cortical reorganization is not well established. The changes in cortical motor reorganization are thought to be possible through the use of preexisting but latent horizontal connections in the cortex that become active. It is thought that these fibers, which are normally inactive, become functional conduits between the cortical centers in response to “learning” stimuli. The connections in these situations are between the biceps motor center and the respiratory center or, in our patients, the seventh nerve center and the fifth nerve center.20 This is considered to be a neurologic unmasking of horizontal connections20 and/or the development of new synaptic connections21–24 (Fig. 9).

Fig. 9.

Fig. 9.

It has been speculated that the adaptability of the cerebral cortex deteriorates with increasing age. This decrease in adaptability is apparent in sensory recovery.25 We expected that spontaneous smiling might not occur or be as common in the older patient. We do not have enough patients to draw a statistically significant conclusion about the older (>50 years) patient; however, we have been encouraged by finding that three of six patients older than 50 years routinely had a spontaneous smile.

We expected that cerebral cortical reorganization might not occur if there had never been any smiling activity, as in the congenital facial paralysis patient. It is believed that the primary neurologic defect in the Moebius syndrome patient is nuclear agenesis in the brain stem.26 It is not known whether there is a cerebral cortical “smile” center in these patients. It has been speculated that the cerebral cortical center for facial expression might not exist in this situation27 and therefore cortical reorganization might not be possible. This does not appear to be the case, as all four of our congenital patients with complete facial palsies had a spontaneous smile at least some of the time, with two patients routinely smiling spontaneously.

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Aesthetics

Evaluation of the aesthetics of smile reconstruction is challenging. At the most basic level of aesthetic appreciation is the recognition by the casual observer that the facial expression is indeed a smile. This is an essential test of the reconstruction. The patient is usually aware of this test because, when they smile in social situations, they will know whether they receive a smile in return. Our reconstructions passed this test fairly well as demonstrated by 82 percent of patients saying that they were sure strangers recognized when they were smiling. However, 18 percent were unsure, which suggests that there is room for improvement.

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Disadvantages of Using the Masseter Motor Nerve

Eleven percent of patients were rarely able to smile spontaneously and 15 percent were rarely able to smile with out making a biting motion. If the patient never develops a spontaneous smile or needs to use jaw movement to create a smile, it is a significant disadvantage. Nevertheless, in the bilateral facial paralysis patient, there is no alternative but to use a nerve other than the seventh nerve. Putting this in the perspective of the person who is unable to smile effectively at any time, it is a tremendous advantage to be able to smile when one so desires even though it is not spontaneous. Although there is a necessary learning process, most patients are so highly motivated that they consider this to be a minor issue. Although we did not specifically study the extent of each patient's practice, we suspect that the likelihood of developing a smile that is separate from fifth nerve activity is dependent on the intensity of early practice.

We were initially concerned that there would be a smiling movement whenever the patient was chewing and that this might be a visually distracting when eating with other persons. However, when questioned, no one felt that they could not eat in front of others, and 70 percent felt that there was not enough movement to be bothered by it.

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Unilateral Paralysis

Symmetry is an achievable goal in bilateral reconstructions, as the surgeon can perform identical transfers for each side. However, in unilateral paralysis, the surgeon is attempting to place a transfer in such a way as to match the shape of the normal side, and this is much more challenging.2

With the cross-facial nerve graft, there is usually less movement than on the normal side of the face, and sometimes there is very little movement. However, masseter motor innervation produces an amount of movement that is in the normal range, and the movement is consistently good. We speculate that there may be a larger role for the masseter motor nerve for innervation of patients with unilateral paralysis who would otherwise have been considered to be candidates for cross-facial nerve graft innervation of a muscle transfer. Subsequent to this study, we are offering this alternative to some unilateral patients. This may be particularly suitable for the older patient in whom cross-facial nerve graft reinnervation is difficult, for the patient who has a heavy face or a lot of rest asymmetry, for the patient who does not wish to undergo two operations, for the person whose primary need is to smile with conscious effort, or for the person who has a very powerful smile on their normal side.

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CONCLUSIONS

The masseter motor nerve provides a powerful and reliable innervation to a free muscle transfer when used for smile reconstruction. With this operation, the amount and direction of the upper lip and commissure movement are similar to those of a normal smile. Patients reported that their facial movement was a good representation of a smile and was usually recognized as such by strangers. With practice, the majority of patients developed the ability to smile spontaneously and without jaw movement. As unilateral patients developed good facial symmetry because of the large amount of movement obtained, this innervation may be a good alternative to cross-facial nerve graft innervation of a muscle transfer.

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