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.
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.
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.
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
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.
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).
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.
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.
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.
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.
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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©2006American Society of Plastic Surgeons
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