J Oral Maxillofac 48:49-53.

Surg

1990

Electromyography of the Suprahyoid Musculature Following Mandibular Advancement With and Without Rigid Fixation EDWARD

ELLIS

III, DDS, MS,* PAUL C. DECHOW, PHD,t DAVID S. CAM-SON, PHD,$ AND VICTORIA LAROCHE, MS5

The purpose of this investigation was to determine if the activity of the suprahyoid musculature changes following advancement of the mandible and the use of rigid or nonrigid fixation. Ten monkeys underwent mandibular advancement; six underwent 6 weeks of maxillomandibular fixation (MMF), and four had rigid fixation without MMF. Electromyography (EMG) of the suprahyoid musculature was performed preoperatively, and at 3, 7, and 10 weeks postoperatively. The results of this study fail to demonstrate an increase in suprahyoid EMG activity following mandibular advancement. Furthermore, there were no differences between the groups with different types of fixation.

The suprahyoid musculature has been incriminated as a major cause of relapse following advancement of the mandible.‘-” It is thought that this group of muscles is stretched with mandibular advancement, producing posteriorly directed forces on the advanced distal segment. However, the nature of these forces remains undetermined. Lengthening of the suprahyoid muscle complex has been experimentally demonstrated in monkeys following mandibular advancement.‘33’4 It can therefore be

assumed that some tension is generated within the suprahyoid tissues, because soft tissue lengthening in a nongrowing tissue usually comes about only by means of stretching, at least in the short term. However, it has been assumed by many clinicians that there is also an active component within the suprahyoid musculature, ie, muscular contraction, causing posteriorly directed forces on the advanced distal segment. The mechanism by which this is thought to occur is via increased motor output to the muscles in response to lengthening. However, this has never been demonstrated. Should an active component exist, the posteriorly directed forces on the advanced mandible would be greater than if only passive soft tissue forces were acting. The purpose of this investigation was to determine if the activity of the suprahyoid musculature changes following advancement of the mandible and use of rigid or nonrigid fixation. The animals used in this investigation were the same as those used in the analysis of skeletal relapse by Ellis et alI5 and of adaptations in suprahyoid muscle length by Reynolds et a1.l4 Our hypothesis was that the electromyography (EMG) activity within the suprahyoid musculature is increased following large mandibular advancements in an attempt to reduce the amount of muscle stretch, ie, to reapproximate the preoperative muscle length. A secondary hypothe-

* Associate Professor, The University of Texas Southwestern Medical School, Dallas: Research Investigator, The Center for Human Growth and Development. The University of Michigan, Ann Arbor. * Assistant Professor of Anatomy, Baylor College of Dentistry, Dallas. $ Professor, Department of Orthodontics; Research Scientist, Center for Human Growth and Development, The University of Michigan, Ann Arbor. 8 Formerly, Research Associate. Craniofacial Biology Laboratory, The University of Michigan School of Dentistry. Supported in part by NIH-NIDR grants No. DE06874, DEO5232, DE07761. and a grant from the Chalmers J. Lyons Academy-James R. Hayward Research Fund. Address correspondence and reprint requests to Dr Ellis: University of Texas Southwest Medical Center, Division Oral and Maxillofacial Surgery. 5323 Harry Hines Blvd. Dallas, TX 75235. 0 1990 American Association of Oral and Maxillofacial geons 0278-2391190/4801-0009$3.OOJO

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EMG OF THE SUPRAHYOIDMUSCULATURE

sis was that the animals placed into maxillomandibular fixation (MMF) would have more resting suprahyoid EMG activity after surgery than those placed into rigid fixation without MMF, because their mandibles were constrained by MMF, making them unable to assume a “rest” posture. Materials and Methods EXPERIMENTALGROUPS Ten adult female Macaca mulatta were used in this experiment. All animals had full dentitions with third molars in occlusion. The monkeys were divided randomly into two experimental groups based on the method of postsurgical fixation used following mandibular advancement surgery. Animals in group MMF (n = 6) underwent advancement of the mandible followed by 6 weeks of MMF. Group RF animals (n = 4) underwent advancement of the mandible using bicortical bone screws to secure the proximal and distal segments. Animals in group RF were not placed into MMF. SURGICALTECHNIQUE The surgical procedure, which was described previously,15T16 involved a standard sagittal ramus advancement osteotomy of 4 to 6 mm with slight modifications for use in the rhesus monkey. In group MMF, the maxillary and mandibular teeth were bonded into a thin interocclusal splint with orthodontic composite resin after pumicing and acid etching the teeth, Maxillomandibular fixation was released 6 weeks after surgery. In group RF, three bicortical 2-mm bone screws were placed on each side as described by Jeter, Van Sickels, and Dolwick.” These animals did not undergo MMF following surgery.

thetic agent that has only a minor and transient effect on the neuromusculature.18 The animal was then placed into a restraining chair which permitted unrestricted movement and function of the head (Fig 1). The skin of the submental area was shaved, and the area of the skin for electrode placement was roughened by lightly pricking with a 27-gauge needle. Two 4-mm recessed surface electrodes (No. E210, In Vivo Metric Systems, Healdsburg, CA) were secured to the skin using adhesive after an ionic conductive media was placed in the electrodes (Fig 2). Input wires were connected to a Grass amplifier (model No. 7PSl1, Grass Medical Instruments, Quincy, MA), and output was recorded using a chart recorder (Grass Model 7 Polygraph) and an eight-channel Hewlett-Packard (Sunnyvale, CA) FM instrument tape recorder. Filtering of EMG signals excluded signals below 60 Hz and above 10,000 Hz. At the time of recording, EMG signals were integrated and rectified with a Grass integrator circuit (Model 7P3) with a time constant of 200 milliseconds. Mean maximum amplitudes of the integrated EMG curves were measured for 50 EMG samples for each activity at each time interval and used in subsequent computations. Mean integrated EMG values for all postoperative recordings were standardized relative to the preoperative mean for each activity. Two-way ANOVA with repeating factors was used to determine if there was any significant difference between groups or over time (between postoperative recording sessions).

EMG ANALYSIS Each animal underwent several training sessions before surgery to acquaint them with the EMG procedure. Electromyography recordings were obtained preoperatively and at 3, 7, and 10 weeks postsurgery. The 3-week recordings in group MMF animals were obtained while the mandible was still immobilized. The ‘I-week recording was 1 week, and the lo-week recording was 4 weeks following release of MMF in these animals. EMG TECHNIQUE Immediately following release from quarantine, each animal was lightly anesthetized by injecting 2 to 5 mg/kg ketamine hydrochloride intramuscularly. Ketamine HCl is a short-acting, dissociative anes-

FIGURE 1. Illustration of restraining chair. Free movement of the head was assured to avoid interference with function.

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FIGURE 2. Illustration showing placement of two electrodes (arrow) in the area of the suprahyoid musculature (skin removed for illustrative purposes). Note the fanshaped nature of suprahyoid muscle-there is no sharp distinction between anterior digastric, geniohyoid, and mylohyoid muscles in M mulatta.

After the effects of the ketamine had dissipated for 1 to 2 hours, the recording session began. Recordings were made continuously, and the activities of drinking and eating were made between periods of inactivity. For drinking, 1 mL of orange-flavored water was given via a catheter placed on the dorsum of the tongue at three separate times to induce deglutition. The animal was then given small bits of apple for consumption. These activities were repeated at least 50 times during each session. A sample of the data is shown in Fig 3. Each recording session lasted approximately 1 to 2 hours after the effect of the anesthetic had dissipated. The animal was then returned to its cage following removal of the EMG electrodes.

commonly noted in the first 6 postoperative weeks, the period when the patient’s mandible is immobilized.‘0*‘5~‘9*‘0 It has been hypothesized that the soft tissues exert posteriorly directed forces on the advanced mandibular segment, causing this relapse. ‘*2*8*11.‘2The nature of these forces is presumed to be either passive, from the stretched connective tissues, or active, from muscular contraction.

Results Results of the relative integrated EMG data for postural activity, drinking, and eating are presented in Figs 4-6. The results of the two-way ANOVA demonstrated no significant difference between experimental groups for any activity (P > .OS). However, there was a trend toward statistical significance for differences in relative integrated EMG activity over time within each group. The P values for drinking was significant (P = .015), whereas the P values for no activity (.143) and eating (.144) were low but not significant at the .05 level. Discussion Relapse following mandibular advancement surgery and use of the dentition to secure MMF is

FIGURE 3. Sample of EMG tracing for suprahyoid complex during eating. Upper figure is integrated tracing of raw EMG data (below) using 200-millisecond time constant.

EMG OF THE SUPRAHYOID

v-

Pre&ery

1 Time

:

:o

in Weeks

FIGURE 4. Relative integrated EMG activity during periods of inactivity, ie, between drinking and/or eating, for groups MMF and RF. Confidence bars are in standard error units.

In an experimental study of mandibular advancement, Carlson and coworkers demonstrated lengthening of the suprahyoid complex with mandibular lengthening.” However, they found lengthening to occur at the muscle-bone and muscle-tendon interfaces of the digastric muscle complex; no lengthening was noted in the muscle belly. The conclusion drawn from that study was that adaptations within the connective tissue attachments of the suprahyoid muscle complex occurred to accommodate the lengthened mandible and to preserve the presurgical length of the musculature. However, a study by the same group when larger mandibular advancements were performed showed some lengthening of the muscle belly in addition to lengthening of the connective tissue attachments of the muscle.14 Whether this lengthening of the muscle belly induced a central nervous system-mediated reactive contraction to try and maintain the presurgical

0’

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Premrgery

I

I

I

I

s Time

7

;

Time

I I

10

in Weeks

FIGURE 5. Relative integrated EMG activity during periods of drinking for groups MMF and RF. Confidence bars are in standard error units.

MUSCULATURE

J

:0

in Weeks

FIGURE 6. Relative integrated EMG activity during periods of eating for groups MMF and RF. Confidence bars are in standard error units.

length was not clear, as electromyography was not reported. When whole muscle is stretched, two specific morphologic changes may take place.” First, the connective tissue within the muscle, in the interstitial spaces, and at the terminal ends of each fiber becomes stretched. Second, once the connective tissue has reached the limit of its extensibility, the muscle fibers themselves become stretched. The net effect is an increase in tension due to both passive elastic properties of the connective tissue and the potential of active contraction of muscle.*‘*** If muscle fibers become stretched, reestablishment of the original sarcomere length is attempted. Although there are several mechanisms by which this can occur, the most common method by which muscle fibers can adapt to their altered length is by shortening, either by exerting tension on the altered skeletal segments and moving them until they reapproximate their original position (ie, relapse), or by migrating to a new site of attachment, but at a length approximating their original length. Both of these possibilities involving actual contraction of muscle fibers have been shown to occur after muscle lengthening. However, one might not expect this with the suprahyoid musculature because the stretch response is usually mediated through stretch receptors within muscle, and they are not present in the suprahyoids.23 The results showed no significant intergroup differences in suprahyoid EMG activity for any functional parameter studied. This indicates that neither mandibular lengthening nor the method of postsurgicai fixation is important in determining patterns of postsurgical suprahyoid EMG activity. There was no significant increase in EMG activity in the 3weeks postsurgery group MMF animals, as hypoth-

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esized, relative to preoperative or 3-week group RF values. In fact, for the activities of drinking and eating, group MMF animals displayed a trend toward a decrease in suprahyoid EMG activity over both their preoperative state and group RF values. This indicates a reduction of activity while in MMF. Group RF animals had almost no change in EMG activity at 3 weeks relative to their preoperative recordings. Interestingly, they had more activity than group MMF animals at this time, although not significantly so. Thus, the results of the EMG data do not support the contention that increased activity of the suprahyoid musculature following mandibular lengthening contributes to relapse, since group MMF, who had decreased EMG values at 3 weeks postsurgery, had a significant amount of skeletal relapse. I5 Of interest was the trend toward a significant difference of suprahyoid EMG activity in both groups over time. Three weeks following surgery, both groups showed decreased activity from the preoperative recording in at least one function, such as drinking in group RF and both drinking and eating in group MMF. The surgical inflammatory and wound healing phases may explain these findings. In the subsequent recordings, both groups tended to show increases in activity, resulting in greater values than recorded preoperatively. However, when the recordings are subjected to statistical analysis, only trends could be inferred. Thus, based on this study, one cannot implicate active contraction of the suprahyoid musculature as a causative factor in relapse following surgically lengthening the mandible. References I. Poulton DR. Ware WH: Surgical-orthodontic treatment of severe mandibular retrusion. Am J Orthod 59:244, 1971 2. Poulton DR, Ware WH: Surgical-orthodontic treatment of severe mandibular retrusion. II. Am J Orthod 63:237, 1973 3. McNeil1 RW, Hooley JR, Sundberg RJ: Skeletal relapse during intermaxillary fixation. J Oral Surg 31:212, 1973 4. Steinhauser EW: Advancement of the mandible by sagittal split and suprahyoid myotomy. J Oral Surg 31:212. 1973 5. Ive J, McNeil1 RW, West RA: Mandibular advancement:

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Skeletal and dental changes during fixation. J Oral Surg 35881. 1977 Epker BN, Wolford LM, Fish LC: Mandibular deficiency syndrome. Surgical considerations for mandibular advancement. Oral Surg 45:349, 1978 Kohn MW: Analysis of relapse after mandibular advancement surgery. J Oral Surg 36:676, 1978 Poulton DR. Ware WH, Baumrind S, et al: Surgical mandibular advancement studied with computer-aided cephalometrics. Am J Orthod 76:121, 1979 Schendel SA, Epker BN: Results after mandibular advancement surgery: An analysis of 87 cases. J Oral Surg 38:265, 1980 Lake SL, McNeil1 RE. Little RM, et al: Surgical mandibular advancement: A cephalometric analysis of treatment responses. Am J Orthod 80:376, 1981 Carlson DS. Ellis E, Schneiderman ED, et al: Experimental models of surgical intervention in the growing face: Cephalometric analysis of facial growth and relapse, in McNamara JA, Carlson DS, Ribbens KA (eds): The Effect of Surgical Intervention on Craniofacial Growth. Monograph No. 12, Craniofacial Growth Series, Center for Human Growth and Development, The University of Michigan, Ann Arbor Ellis E. Carlson DS: Stability two years following mandibular advancement with and without suprahyoid myotomy: An experimental investigation. J Oral Maxillofac Surg 41:426. 1983 Carlson DS, Ellis E, Dechow PC: Adaptation of the suprahyoid muscle complex to mandibular advancement surgery. Am J Orthod 92:134, 1987 Reynolds ST, Ellis E, Carlson DS: Adaptation of the suprahyoid muscle complex to large mandibular advancements. J Oral Maxillofac Surg 46: 1077, 1988 Ellis E, Reynolds S. Carlson DS: Stability of the mandible following advancement: A comparison of three postsurgical fixation techniques. Am J Orthod 94:38. 1988 Mayo KH, Ellis E: Stability of the mandible after advancement and use of dental plus skeletal maxillomandibular fixation: An experimental investigation in Macacu mulatta. J Oral Maxillofac Surg 45:243, 1987 Jeter TS. Van Sickels JE, Dolwick MF: Rigid internal fixation of ramus osteotomies. J Oral Maxillofac Surg 42:270. 1984 Kuroda T, McNamara JA: The effect of ketamine and phencyclidine on muscle activity in nonhuman primates. Anesth Analg 51:710. 1972 Will LA, Joondeph R, West RA, et al: Condylar position following mandibular advancement: Its relationship to relapse. J Oral Maxillofac Surg 42:578. 1984 Smith GC. Moloney FB, West RA: Mandibular advancement surgery. A study of the lower border wiring technique for osteosynthesis. Oral Surg 60:467, 1985 Carlson FD. Wilkie DR: Muscle Physiology. Englewood Cliffs, NJ, Prentice-Hall, 1974 Taylor A: Fiber types of the muscles of mastication, in Anderson DJ, Matthews B (eds): Mastication. Bristol, Wright, 1976 Dymytruk RJ: Neuromuscular spindles and depressor masticatory muscles of monkey. Am J Anat 141:147. 1974