A comparison of stimulated bite force after mandibular advancement using rigid and nonrigid fixation

SCIENTIFIC AMBLES J Oral Maxillofac 46:26-32.

Surg

1966

A Comparison of Stimulated Bite Force After Mandibular Advancement Using Rigid and Nonrigid Fixation EDWARD ELLIS III, DDS, MS,* PAUL C. DECHOW, PHD,t AND DAVID S. CARLSON, PHDS This study evaluated maximum stimulated molar bite force following advancement of the mandible in 17 adult Macaca mulatta using rigid and nonrigid fixation techniques. Cephalometric analysis was also performed to determine the amount of proximal segment rotation. Analysis of the bite force showed the animals whose mandibles were advanced using rigid fixation to have significantly greater bite force at six weeks postsurgery when compared to those animals who underwent mandibular advancement and six weeks of maxillomandibular fixation. By the ninth postoperative week, there was no longer any significant difference between the two groups, indicating a rapid recovery of muscle function in the animals whose mandibles were immobilized following advancement. Both groups, however, had significant decreases in bite force at 12 weeks postsurgery when compared to preoperative values. Neither group had a significant amount of proximal segment rotation from the surgery.

Skeletal muscle is one of the most adaptable tissues to changes in morphology or function. Immobilization of a muscle and the resultant decrease in activity has been well studied in recent years. One result of immobilization, muscle atrophy, is an obvious finding and is associated with weakness of the involved muscle for several weeks or even months following immobilization. The exact mechanisms that are responsible for the atrophic response seen when immobilization is

employed remain elusive. It has been documented, however, that the atrophic response involves a loss of both contractile and metabolic proteins.‘,* The amount of myofibriliar protein loss during immobilization (disuse) has been shown to have some dependency on the position (or length) of the muscle during immobilization. Jokl and Konstadt* found that stretching a muscle during the immobilization period caused a compensatory production of protein that can balance what is usually lost. Conversely, immobilization of shortened muscle caused a marked loss of myotibrillar protein content, more so than would be expected from the effects of immobilization alone. Contractile properties of the involved muscles reflected the same findings as protein content, where a severe loss of contractile force was found with a shortened muscle. These findings on the effect of muscle immobilization and change in length are particularly important when one considers the sagittal ramus osteotomy procedure to alter mandibular length. If the proximal segment is allowed to rotate upward and forward as a result of this procedure, shortening of the masseter, temporalis, and medial pterygoid muscles will occur. This not only diminishes the mechanical advantage of these muscles, but immobilization of these shortened muscles during the pe-

* Assistant Professor, Department of Oral and Maxillofacial Surgery; Research Investigator, Center for Human Growth and Development, The University of Michigan, Ann Arbor, Michigan. t Assistant Professor, Department of Anatomy, Baylor College of Dentistry. $ Associate Professor, Departments of Orthodontics and Anatomy and Cell Biology;. Associate Research Scientist, Center for Human Growth and Development, The University of Michigan, Ann Arbor, Michigan. Supported by NIH-NIDR Grants nos. DE06874, DE05232 and erants from the Universitv of Michigan School of Dentistry and The Chalmers J. Lyons Academy of-Oral Surgeons-J. R.-Hayward Research Fund. Address correspondence and reprint requests to Dr. Ellis: Department of Oral and Maxillofacial Surgery, School of Dentistry, The University of Michigan, Ann Arbor, MI 48109-1078. 0 1988 American geons 0278-2391187

Association

of Oral and Maxillofacial

Sur-

$0.00 + .25

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ELLIS ETAL.

riod of maxillomandibular fixation may cause significant changes within the muscle fibers. The majority of investigations performed to evaluate disuse myoatrophy have been performed in muscles of the extremities, both in humans and animals. There is very little information available concerning disuse atrophy of the muscles of mastication. However, a recent study of the muscles of mastication in rhesus monkeys following mandibular advancement and maxillomandibular fixation3 revealed a long-term loss in maximal muscle force above that which could be explained by biomechanical changes in the craniofacial skeleton resulting from altered mandibular position. It was unclear from that study what the specific impact of immobilization (fixation) had on long-term recovery of muscle function. It has been shown in extremity injuries that the earlier a patient can resume active motion of the joint following surgery, the more rapid will be the recovery of muscle function.4-s Avoiding or decreasing the immobilization period,9*i0 electrical stimulation,“*‘* active motion, and/or exercising isometricallyi have been found to prevent or diminish the atrophic changes associated with immobilization. The use of rigid internal fixation following orthognathic surgical procedures has the advantage of allowing the surgeon to place the proximal segment in a position that prevents shortening of the muscles of mastication, and of reliably securing it there. Additionally, when the mandible is allowed to function throughout the period of osseous healing, less myoatrophy may occur. This should be manifest clinically as a smaller reduction in bite force. The purpose of this investigation was to evaluate the effect of mandibular osteotomy with and without maxillomandibular fixation on the function of the muscles of mastication using the adult rhesus monkey as an experimental model. Specifically, this study tested the related hypotheses that: 1) mandibular osteotomy with the use of maxillomandibular fixation for postsurgical immobilization of the proximal and distal segments results in a significant functional deficit of the muscles of mastication, and 2) resumption of jaw function immediately after mandibular osteotomy through use of rigid internal fixation reduces the functional loss in the jaw elevator muscles. Materials and Methods EXPERIMENTALDESIGN

Seventeen adult female rhesus monkeys (Mucaca mufutta) were used in this experiment. All animals had full dentitions with third molars in occlusion.

The total sample of monkeys was randomly divided into two groups. Animals in Group MMF (n = 6) had mandibular advancement surgery of approximately 4-6 mm and were placed in maxillomandibular fixation (MMF) for six weeks. Animals in Group RF (n = 11) had a similar surgical procedure except that the proximal and distal segments were secured with bicortical bone screws (rigid tixation; RF) and the animals were not placed into MMF. The six Group MMF animals and five of the Group RF animals were followed over a 12-week period postsurgery, at which time they were killed for later histolologic analysis of osseous and TMJ adaptations. Six of the animals in Group RF were killed six weeks after surgery for histologic analysis. Presurgical bite force readings and cephalograms were taken on all animals. Each animal was radiographed immediately postsurgically, and at weekly intervals up to 12 weeks. Stimulated bite force measurements were taken following osseous union of the osteotomized segments at six weeks postsurgery. These measurements were repeated at weekly intervals until the animal was killed. Surgical Procedure Four weeks prior to surgery, all animals began a mash diet on which they were maintained throughout the experimental period. Ten days prior to surgery, dental impressions were taken of all animals. Models were prepared and articulated to effect mandibular advancements of approximately 4-6 mm; an acrylic interocclusal wafer was fabricated that would lock the teeth into this new relationship. The surgical procedure used has been described previously14+*5 and involved a sagittal ramus osteotomy with slight modifications for use in the rhesus monkey. Once the mandible was split bilaterally, one of two types of fixation was employed. In Group MMF animals, the maxillary and mandibular teeth were bonded into the interocclusal splint using orthodontic composite resin after pumicing and acid-etching the teeth. In addition, three of the Group MMF animals had skeletal suspension wires placed (circummandibular to pyriform aperture). The proximal and distal segments were joined with a wire placed at the inferior border. In Group RF animals, rigid internal fixation was applied. The technique consisted of the application of temporuly MMF by wiring together the maxillary and mandibular dentition with the interoccusal splint in place, followed by the application of three 2-mm bone screws bilaterally. The procedure used was exactly as described by Jeter and co-workers.i6 The tempo-

28

STIMULATEDBITE FORCEAFTER MANDIBULARADVANCEMENT

rary MMF was released and the position of the mandible checked. The acrylic splint was then bonded to the maxillary dentition to provide a stable bite-plane on which the mandibular teeth could occlude in the postsurgical period. No postoperative MMF was used. Postsurgically, each animal received, the same standard mash diet and fresh fruit, Tang and water ad libitum. CEPHALOMETBICPROCEDURESAND ANALYSIS Prior to the surgical phase of the experiment, each monkey had radiopaque tantalum bone markers placed in prescribed locations throughout the craniofacial region. I’J* The implantation procedure allowed study of changes in position of osseous and dental structures through implant superimposition in serial cephalograms. Cephalograms were taken of each animal prior to surgery and at weekly intervals postsurgically until it was killed. The serial cephalograms were traced and digitized with a Summagraphics digitizer and Zenith microcomputer. The digitizer is accurate to the nearest 0.1 mm. Analysis of change in the position of the mandibular ramus was performed by measuring the angle between two bone markers in the mandibular ramus and the cranial reference line (CRL). The CRL is a line parallel to the preoperative occlusal plane drawn through a sphenoidal (cranial base) bone marker in the preoperative radiograph. This line was transferred to subsequent tracings by the computer. Student’s t-test was used to determine if there were any significant differences in the amount of proximal segment rotation between the two experimental groups in the presurgery to immediately postsurgery interval, and in the intervals from immediate postsurgery up to six weeks postsurgery, at which time the proximal and distal segments had healed. Pearson’s correlation coefficients were calculated to determine if the amount of proximal segment rotation and bite force measures were correlated. BITE FORCE MEASUREMENTAND ANALYSIS Stimulated bite force measurements were used in this experiment to determine recovery of muscle function following mandibular advancement in the postsurgical period and to compare differences in muscle recovery between groups. The bite force transducer and stimulation techniques have been described in detail elsewhere.19 The specific application of the technique to adult monkeys following mandibular advancement was similar to that re-

ported by Dechow and Carlson3y20 with several differences as described below. Bite force measurements were conducted on each animal prior to surgery and at weekly intervals following osseous healing (six weeks postsurgery) until it was killed. For each set of measurements, monkeys were anesthetized with a combination of Ketamine HCl (7-15 mg/kg) and Rompun (Xylazine; 1-2 mg/kg). Two Grass platinum unipolar needle electrodes were inserted into the masseter muscle through the skin, with one electrode positioned in the anteroinferior portion of the muscle and the other electrode in the posterosuperior portion of the muscle. Unilateral isometric bite force was measured at the most posterior cusp of the upper third molars, following two different stimulation procedures. Single pulses of 0.8 ms duration and sufficient voltage for maximal unilateral masticator-y muscle contraction (25-45 V)r9 were generated with a Grass Model 48 Square Pulse Stimulator. Readings from the transducer were amplified with a Vishay 2100 strain gage amplifier and displayed and photographed on a Tektronics 5 113 dual-beam storage oscilloscope (Fig. 1). Contractile speed was assessed through

C

0

1

2

P 8

1

FIGURE 1. Examples of stimulated molar bite force recordings (traced from oscilloscope photographs). The upper figure represents a tetanic contraction of the masticatory muscles in a rhesus monkey. The lower figure represents a single pulse (twitch) contraction. The x-axis is given as time in milliseconds (ms) and the y-axis is given as force in newtons (n).

ELLIS ET AL.

Table 1.

29

Bite Force Data Week

Group

Preop

Time-to-peak MMF Mean SD RF Mean SD Stimulated MMF Mean SD RF Mean SD

6

7

8

9

10

II

I?

tension (MS) 44.0 5.5 42.4 3.4

molar bite force

42.0 2.5 38.8 3.7

41.3 2.1 39.6 2.2

40.0 7.7 40.0 3.7

39.3 4.3 38.4 2.6

39.7 6.1 38.0 2.0

39.0 3.5 38.6 2.4

39.5 4.2 38.2 2.3

89.8 49.6 183.5 52.7

96.9 48.8 187.0 71.1

115.8 64.4 201.2 70.1

128.9 61.7 192.3 63.2

152.9 64.5 189.6 22.7

153.8 50.0 198.2 53.6

165.0 49.7 201.3 20.8

38.2 14.2 68.5 18.7

45.3 17.5 73.5 14.0

51.3 19.8 70.5 10.9

60.6 15.8 71.3 7.1

62.0 14.1 73.5 11.1

66.3 10.8 76.4 12.5

(newtons)

245.0 39.5 271.6 43.3

Relative molar bite force (7%of preop value) MMF Mean 100.0 36.1 SD 18.6 RF Mean 100.0 68.6 SD 22.4

Sample size for Group MMF = 6. Preop and week 6 sample size for Group RF =

measurements of time-to-peak tension, which were taken from the photographs of muscle twitches. Fused tetanus (maximal muscle contraction) was obtained by stimulating with pulses of 0.8 ms duration at frequencies of greater than 80 Hz for 400 ms at 25-45 V. Measurement of maxima1 unilateral masticatory muscle force were calculated from the oscilloscope tracing. Following these procedures, the animal was placed back in its cage and allowed to recover. Analysis of the bite force data consisted of twoway analysis of variance with repeated measures on one factor (time). T-tests were used in a posthoc analysis to differentiate further between the individual groups at different time periods and to differentiate between the two groups at single time periods. This analysis was performed on time-to-peak tension and on maximal force measurements. In addition, relative data of the maxima1 bite force of each animal as a percentage of its presurgical reading were calculated and statistical analysis was performed. In order to balance the designs, the six animals killed at week six in the RF group were excluded from the ANOVA. However, data from these animals were included in posthoc t-tests where appropriate. Results

All 17 animals withstood the surgical procedure well. There were no major infections or postoperative complications in any of the experimental animals. The MMF was stable throughout the followup period in Group MMF; no animals broke the composite bond between the splint and the teeth.

1I. Group RF sample size for weeks 7- I2 = 5.

PROXIMAL

SEGMENT

ROTATION

During the surgery, there was a mean anterior rotation of the mandibular ramus of 0.4” in Group MME Group RF had a mean posterior rotation of 1.4” with surgery. This was not a statistically signiticant difference. Over the next six weeks, the position of the proximal segment in Group RF was very stable. In Group MMF, the proximal segment rotated anteriorly by an insignificant amount (mean = 1.4”). There was no significant change in the position of the mandibular ramus between the two experimental groups at any time postsurgically. The correlation between the amount of proximal segment rotation and change in bite force was not significant . STIMULATED

BITE FORCE

(TABLE

1)

For time-to-peak tension (TPT), the ANOVA revealed no significant differences between Groups MMF and RF at any interval. However, significant differences were found over time (F = 2.38, P < 0.05). There was a gradual mean decrease in TPT for both Group RF and Group MMF from the preoperative measurement until week nine (Fig. 2). Ttests revealed significant differences in both groups between both the preoperative and week six measurements compared to measurements from weeks nine to 12. For molar bite force (MBF), there were significant differences between groups (F = 8.76, P < 0.01) and over time (F = 5.66, P < O.OOl>,but no significant interactive effects (Fig. 3). MBF for Group MMF animals at six weeks postsurgery (the

30

STIMULATED BITE FORCE AFTER MANDIBULAR

ADVANCEMENT

42

I

1

Preop

6

80

IA

60

8

9

10

11

12

FIGURE 3 (bortom). Change in occlusal force over the course of the experiment for both groups. Occlusal force is given as a percentage of the bite force that was measured preoperatively. Standard error bars for the mean of each time period are given for Group MMF. These estimates of variance are similar for both groups.

Postoperative Weeks

0

ii!! ti

7

FIGURE 2 (top). Change in time-to-peak twitch tension (TPT) over the course of the experiment for the combined RF and MMF groups. TPT is given in milliseconds (ms). The confidence bars are standard errors of the mean for each time period.

b

Q

3 8

40

0

20

Preop

0

7

8

9

10

11

12

Postoperative Weeks time of release of fixation) was 36.1% of the preoperative bite force (P < 0.001). Over the next six weeks, there was a progressive increase in bite force, so that at 12 weeks postsurgery the mean bite force had returned to 66.3% of the predperative value, which was still a significant decrease (P < 0.001). MBF for Group RF animals at six weeks was 68.6% of the preoperative bite force (P < 0.001). Over the next six weeks, there was a slight increase in MBF, so that at 12 weeks postsurgery MBF was 76.4% of the preoperative value, which was also still a significant decrease from the preoperative reading (Z’ < 0.001). Comparison between Groups MMF and RF showed that at six weeks postsurgery there was a

significant difference between them, with Group MMF having a greater reduction in MBF (P < 0.01). This significant difference between the two groups remained until the ninth postsurgical week. Discussion The results of this study suggest several possible adaptations in the muscles of mastication associated with mandibular advancement osteotomy and method of fixation. First, the reduction in TPT may imply a relative decrease in fatigue resistant muscle fibers. Close (1964) demonstrated in the rat that type IIa fibers (fast-fatigue resistant) have a slower TPT than type IIb (fast-fatiguable). Thus, a slight reduction in contractile speed might corre-

31

ELLIS ET AL.

spond with a differential atrophy of fatigue-resistant fibers compared to fatiguable fibers. The opposite effect has recently been found in the superficial temporalis muscle of rabbits following masseter myectomy,*l where the temporalis exhibited a relative hypertrophy in type IIa fibers, a corresponding increase in TPT and an increase in overall resistance to fatigue. This opposite effect was also found in monkey masticatory muscles after the placement of a bite-opening appliance, where the proportion of the relative cross-sectional areas of types IIa and IIb fibers corresponded with a prolongation of contraction time.** It is interesting that there were no significant differences between RF and MMF monkeys in TPT and that the reduction of TPT continued until the ninth week in both groups before leveling out with no recovery. This suggests that the surgery and subsequent postoperative care had a general effect on the masticatory muscles regardless of differences in fixation technique. One possible explanation is that the reduction in TPT (and the supposed reduction in resistance to fatigue) may not be an effect of the surgery at all but rather the result of the soft diet on which the both groups of animals were maintained throughout the postoperative period. This possibility corresponds well with the rabbit study previously discussed*i where an opposite but congruent result was found, namely a loss of masticatory tissue with a maintenance of the usual diet led to an increase in TPT and fatigue resistant properties. Both experimental groups demonstrated an initial decrease in maximal stimulated bite force. However, maintenance of function in the RF group led to much less of a decrease in force and probably less muscle atrophy than in the MMF group. However, this difference was only temporary. The lack of function in Group MMF did not affect long-term recovery of maximal muscle force. At the end of the experiment, both groups still showed a loss in muscle force compared to preoperative readings. This result is not surprising in light of the findings reported by Dechow and Carlson that adult monkeys showed loss in maximal muscle force a year or more following mandibular advancement,3 and that juvenile monkeys have reduced maximal masticatory muscle forces compared to controls as much as two years following mandibular surgery.*O IMPLICATIONS FOR

OnAL AND

MAXILLOFACIALSURGERY

It is clear that when a muscle is immobilized, atrophic changes will occur; this will be especially evident if the muscle has undergone any surgical insult. Moreover, previous studies indicate that im-

mobilizing a shortened muscle causes more severe changes than immobilization alone.* Thus, surgeons should strive to maintain the preoperative position of the proximal segment when performing the sagittal ramus osteotomy since any upward and forward proximal segment rotation will shorten the elevator muscles of mastication. This not only diminishes the mechanical advantage of these muscles, but also the immobilization of these shortened muscles during the period of maxillomandibular fixation may cause significant changes within the muscle fibers possibly leading to some permanent loss of bite force. Rigid fixation is the best way to prevent rotation of the proximal segment. When wires are used, it has been demonstrated that the use of a lower border wire between the proximal and distal segments is a more reliable way to secure these segments in the preoperative position than the use of an upper border wire.23 It is thought that the earlier a patient can resume active motion of the joint following surgery, the more rapid will be the recovery of muscle function. Avoiding or decreasing the immobilization period. electrical stimulation, active motion, and/or exercising isometrically have been found to prevent or diminish these changes. The use of rigid internal fixation not only has the advantage of allowing the surgeon to place the proximal segment in any position desired and of reliably securing it there, but also when the mandible is allowed to function throughout the period of osseous healing, less myoatrophy will occur. This should be manifest clinically as a smaller reduction in bite force. Perhaps the greatest advantage of rigid internal fixation is that it permits the initiation of physiotherapy earlier postsurgically than when maxillomandibular fixation is used and leads to a more rapid regain of bulk and strength. This study found that both experimental groups showed a significant functional deficit in the muscles of mastication following advancement of the mandible. Although this deficit was significantly greater in Group MMF at six weeks postsurgery, indicating greater myoatrophy, by the ninth postoperative week, this difference was no longer significant. It can be assumed, therefore, that the use of rigid internal fixation has no appreciable long-term benefit on the muscles of mastication, when compared to the use of maxillomandibular fixation, as long as the mandibular ramus is prevented from rotating in a counterclockwise direction. References 1. Edgetton VR: Neuromuscular adaptation to power and endurance work. Can J Appl Sport Sci 1:49, 1976

32

STIMULATED

2. Jokl P, Konstadt S: The effect of limb immobilization on muscle function and protein composition. Clin Orthop 174:222, 1983 3. Dechow PC, Carlson DS: Occlusal force after mandibular advancement in adult rhesus monkey. J Oral Maxillofac Surg 44:887, 1986 4. Stoboy J, Fredebold G, Strand FL: Evaluation of the effect of isometric training in fundamental and organic muscle atrophy. Arch Phys Med Rehab 49:508, 1968 5. Muller EA: Influence of training and of inactivity on muscle strength. Arch Phys Med Rehab 511449, 1970 6. Sargeant AJ, Davies CTM: The effect of disuse muscular atrophy on the forces generated in dynamic exercise. Clin Sci Mol Med 53: 183, 1977b 7. Allbrook D: Skeletal muscle regeneration. Muscle Nerve 4~234, 1981 8. Salmous S, Juricksson J: The adaptive response of skeletal muscles to increased use. Muscle Nerve 4:94, 1981 9. Haggmark T, Eriksson E: Hypotrophy of the soleus muscle in man after achilles tendon rupture: discussion of findings by computed tomography and morphological studies, Am J Sports Med 7:121, 1979 10. Sherman WM, Plyley MJ, Pearson DR, et al: Isokinetic rehabilitation following meniscectomy: comparison of two methods of training describing strength changes during and following release from rehabilitation. Am J Sports Med 10:155, 1983 11. Eriksson E, Haggmark T: A comparison of isometric muscle training and electrical stimulation in the recovery after knee ligament surgery. Am J Sports Med 7:48, 1979 12. Gould N, Donnermeyer D, Gammon GG, et al: Transcutaneous muscle stimulation to retard disuse atrophy after open meniscectomy. Clin Orthod 178: 190, 1983 13. Wolf E, Magora A, Gonen B: Disuse atrophy of the quadriceps muscle. Electromyography 11:479, 1971 14. Mayo KH, Ellis E: Stability following mandibular advance-

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BITE FORCE AFTER MANDIBULAR

ADVANCEMENT

ment using dental plus skeletal maxillomandibular fixation-an experimental investigation in Mucaca mulatta. J Oral Maxillofac Surg 45:243, 1987 Ellis E, Reynolds S, Carlson DS: Stability of the mandible following advancement: A comparison of three postsurgical fixation techniques in Macaca mulatta. Am J Orthod 1987 (in press) Jeter TS, Van Sickels JE, Dolwick MF: Rigid internal fixation of ramus osteotomies. A technique. J Oral Maxillofac Surg 42~270, 1984 Carlson DS, Ellis E, Schneiderman ED, et al: Experimental models of surgical intervention in the growing face. 1. Cephalometric analysis of facial growth and relapse. In: Effect of Surgical Intervention in Craniofacial Growth. Craniofacial Growth Series, Monograph No. 12, Center for Human Growth and Development. J.A. McNamara, Jr., D.S. Carlson, and K. Ribbens (eds.) pp. 1l-72, 1982. McNamara JA, Riolo ML, Enlow DH: The growth of the maxillary complex in the rhesus monkey (Macaca mulam). Am J Phys Anthrop 44:15, 1976 Dechow PC, Carlson DS: A method of bite force measurement in primates. J Biomechanics 16:797, 1983 Dechow PC, Carlson DS: Recovery of occlusal force after mandibular advancement in growing rhesus monkeys. J Dent Res 64:349, 1985 Guelinckx P, Dechow PC, Vanrusselt R, et al: Adaptations in craniofacial muscles after masseter muscle removal. J Dent Res 65: 1294, 1986 Faulkner JA, McCully KK, Carlson DS, et al: Contractile properties of the muscles of mastication of rhesus monkeys (Macaca mulattn) following increase in muscle length. Arch Oral Biol 27:841, 1982 Singer RS, Bays RA: A comparison between superior and inferior border wiring techniques in saggital split ramus osteotomy. J Oral Maxillofac Surg 43444, 1985