Electromyographic activity of the jaw-closing muscles in patients with osseointegrated implant fixed partial dentures Randall C. Duncan, DDS, MS,a Arthur T. Storey, DDS, MS, PhD,b John D. Rugh, PhD,C and Stephen M. Parel, DDSd Ehrling Bergquist Strategic Hospital, Offutt Air Force Base, Neb.; and University Science Center, Dental School, San Antonio, Tex.
of Texas Health
The control of postural and synergistic jaw reflexes involves interrelated sensory input from receptors in the jaw muscles, temporomandihular joint, periodontal ligament, and mucosa. This investigation was done to determine whether a decrease in intraoral sensory aiferent discharge significantly altered the onset of the jaw-unloading reflex. The subject population consisted of three groups with 10 subjects in each group. Group 1 had maxillary and mandibular natural teeth and group 2 consisted of edentulous subjects with complete dentures. Group 3 consisted of edentulous subjects with maxillary complete dentures and mandibular complete implant-supported prostheses. The unloading reflex was initiated with a muscleunloading device and recorded with a storage oscilloscope. A one-way analysis of variance found no significant differences in the unloading-reflex latency for the masseter or temporal muscles among the three experimental groups (p < 0.05). (J PROSTHET DENT 1992;67:544-9.)
P
resent evidence indicates that patients with an osseointegrated implant fixed partial denture (FPD) approach the masticatory function of patients with equivalent natural teeth.lmgIt is believed that this success is primarily because the rigid connection between implant and bone allows stress transmission without appreciable motion in the prosthesis.1° The masticatory system, however, has the potential to develop large impact forces during function that, if inadequately unloaded, could compromise the integrity of this bone-implant interface. I1 For this reason, Skalakl’ recommended the use of acrylic resin between the occluding surface and the fixture to provide adequate shock protection. Clinical evidence for the lasting integration of loaded fixtures, however, has not revealed a problem with excessive occlusal forces.r2 However, Lundgren et a1.r3studied the occlusal force pattern in patients with complete dentures
The opinions expressed herein are those of the authors and are not to be construed as official or reflecting the views of the U.S. Air Force or the Department of Defense. Supported in part by the Education and Research Foundation of Prosthodontics. Third place, John J. Sharry Prosthodontic Research Competition, American College of Prosthodontists, Tucson, Ark., 1990. aMajor, U.S. Air Force, Dental Corps; Assistant Chairman, Department of Prosthodontics, Ehrling Bergquist Strategic Hospital. bProfessor and Chairman, Department of Orthodontics, University of Texas Health Science Center, Dental School. cProfessor, Department of Oral and Maxillofacial Surgery, University of Texas Health Science Center, Dental School. dProfessor and Head, Division of Maxillofacial Prosthetics, University of Texas Health Science Center, Dental School.
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opposing mandibular implant FPDs and found that patients chewed with 60% of their maximal closing force. This force can be compared with 26% of maximal closing force in patients with unilateral posterior two-unit cantilevers, 37% in patients with bilateral end abutments, and 45% reported in natural teeth.14-16 In an electromyographic study of masticatory muscle activity, Haraldson17 reported that patients with implant FPDs chewed with consistent muscle activity during the whole chewing sequence, compared with dentate patients who had a decrease in muscle activity at the end of the chewing act.‘s Haraldson17 theorized that this change in the chewing pattern might be due to a decrease in oral tactile sensibility that could cause a change in neurophysiological feedback mechanisms. He suggested that a masticatory training program may be indicated for patients undergoing implant fixed partial denture rehabilitation. The unloading reflex, or “Entlastung” reflex, was first described in limb muscles by Hansen and Hoffmann,lg and in masticatory muscles by Hannam et akzOand Beaudreau et a1.21The reflex has been defined as the sudden or unexpected removal of an isometric load from the jaw-closing muscles.20-24Most investigators generally believe that this is a protective masticatory reflex in that it arrests jaw movements before tooth contact occurs.20,21,24,25When a hard object is encountered between the teeth, large isometric forces are generated that can result in the teeth crashing together when the object suddenly breaks. The sensory input for this reflex has not been fully established, although several possible sources of receptors have been proposed including muscle receptors,26-28periodontal ligament receptors,20g21 mucosal receptors,2g joint receptors,20,26and tendon receptors20 as well as reciprocal inhi-
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Table I. Identification Receptors stimulated
stimulated stimulated
MUSCLES
of receptors stimulated
Group 1 (Control)
Group 2 (Control)
+
0
0
0 +
+* +
+T +
Periodontal ligament Mucosa All others *Receptors tReceptors
IN JAW
in maxilla in maxilla
Group 3 (Experimental)
and mandible. only.
bition of jaw muscles. 24,3oProviding that the unloading reflex involves interrelated input from several afferent pathways, a decrease in sensory input may affect reflex latency. In other words, the latency could be altered if a decrease in stimulus intensity significantly affected the threshold potential for this reflex. Although the incorporation of a mechanical damping system in the prosthesis design has been recommended to eliminate potentially harmful forces, it may only be necessary if the physiologic load-compensating mechanism were compromised. However, the jaw unloading reflex in patients with implant-supported prostheses has not yet been investigated. This investigation was done to determine whether a decrease in intraoral sensory afferent discharge significantly altered the onset of the jaw-unloading reflex. This study tested the null hypothesis that there is no statistically significant difference in the latency of the unloading reflex when experimental subjects are compared with the control subjects. METHODS
AND
MATERIAL
The experimental design called for a comparison of unilateral electromyographic activity of the masseter and temporal muscles during isometric loading among three population groups. A group size of 10 subjects was statistically determined by power analysis of a pilot study. The subjects were all selected from The University of Texas, Dental School at San Antonio, and were fully informed of the procedures and risks before their consent was obtained. An even gender distribution was selected with an average age of 57.5 years. Patients were not selected if they had a history of temporomandibular, auricular, or neuromuscular pain or dysfunction. Most of the patients with implantsupported prostheses had a mandibular implant-supported fixed prosthesis opposing a maxillary removable complete denture. For this reason, two control groups were used in this study to identify the role of mucosal receptors under the complete dentures of the experimental group (Table I). Control group 1 consisted of 10 subjects with natural maxillary and mandibular teeth surrounded by mechanoreceptors in the periodontal ligament in both dental arches. Control group 2 consisted of 10 completely edentulous subjects restored with maxillary and mandibular
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Fig. 1. Unloading apparatus. (A) Stationary upper jaw bar, (B) piezoelectric cartridge transducer, (C) lower jaw bar with hole for glass tube that provides resistance to jaw closing, (0) trigger arm mechanically linking transducer to lower jaw bar, (E) polypropylene pad secured to jaw bar. Dental impression material placed on this pad allowed reproducible positioning of apparatus in mouth, (F) axis of rotation for lower jaw bar.
complete dentures. These subjects were totally missing periodontal ligament receptors in both arches, but had mucosal receptors stimulated by the prostheses. The experimental group (group 3) consisted of 10 completely edentulous subjects restored with a maxillary complete denture and a mandibular implant-supported prosthesis. Implant-supported prostheses were of a hybrid design constructed on four to five threaded cylindrical fixtures (Nobelpharma USA Inc., Waltham, Mass.), which were surgically placed by procedures outlined by Branemark et a1.31and Albrektsson et al.‘O Artificial teeth used in all prostheses were made of acrylic resin (Bioblend, Dentsply International, Inc., York, Pa.) processed to a high-impact acrylic resin denture base (Lucitone 199, Dentsply International, Inc., Milford, Del.). This group of subjects had mucosal receptors stimulated only in the maxillary arch. The apparatus used for muscle unloading allowed the subjects to develop an isometric loading force with jawclosing muscles until the resistance to jaw closure was suddenly overcome, initiating the unloading reflex. The apparatus was a modified version of the device used by Miles and Wilkinson24 and consisted of two cast chromium alloy (Ticonium 100, Ticonium Co., New York, N.Y.) jaw bars mounted on a stainless steel plate measuring 112 mm x 60 mm x 2 mm (Fig. 1). The upper bar was fixed at a constant position in relation to the lower bar, which was hinged and allowed to rotate. The lower bar was positioned 19 mm from the upper bar and stabilized temporarily by a 35 mm sec545
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ET AL
3. Descriptive representation of reflex latency and duration. EMG trace was adjusted to begin at second vertical line on graticule the instant glass tube broke. Latency demonstrated in this drawing is 10 msec and duration is 47 msec. Fig.
Fig. 2. Electrode placement. Bipolar surface electrode placement parallel to muscle fibers with interelectrode distance of 2 cm. Line connecting outer canthus of eye and angle of mandible was used as guide in placing electrodes on masseter muscle, with most inferior electrode 1 cm from mandibular inferior border. Electrodes were placed on temporal muscle as close to hairline as possible. ,Ground electrode was placed at mastoid region on ipsilateral side.
tion of glass tubing (4 mm diameter, Pyrex, American Scientific Products, Houston, Tex.) which was placed through the jaw bar and the stainless steel plate. The glass tube was positioned away from the rotational center of the bar to allow it to break consistently at a resistance of 59N (Instron Universal testing machine, Model 1125, Instron Corp., Canton, Mass.). Breakage of the glass tube was detected by a piezoelectric cartridge transducer that was mechanically linked to the lower bar. This bar was connected to the external trigger input of a single trace storage oscilloscope (Model 7623A, Tektronix, Inc., Beaverton, Ore.) that was calibrated to begin a sweep at the exact instant the glass tubing broke. The entire apparatus was covered with plastic film (Anchor Industries, St. Louis, MO.) to contain the glass tubing after breakage. Each jaw bar had a biteplate covered with polypropylene material (Buffalo Dental Mfg., Co., Syosset, N.Y.) secured with cyanoacrylate cement (Rapid Bonding Adhesive, Toagosei Chemical, Tokyo, Japan). A polyether registration material (Ramitek, Premier, Norristown, Pa.) was used to consistently position the jaw bars in the maxillary first premolar region for three recordings in each muscle group. The activity of the temporal and masseter muscles was recorded with silver-silver chloride surface electrodes (Model SE-40, 8.5 mm diameter, J & J, Poulsbo, Wash.) using double-backed adhesive disks (Med Associates, Inc., East Fairfield, Ver.) and electrode paste (type 651-1022,
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Hewlett Packard Redux Creme, Waltham, Mass.). Electrodes were positioned on the skin parallel to the direction of the muscle fibers (Fig. 2). Interelectrode impedance was measured with an impedance meter (Model EZM, Gross Instrument Co., Quincy, Mass.) and was kept below 10 kilo-ohms. Unilateral EMG activity was recorded at a constant temperature of 75’ C on subjects seated in an upright position so that the Frankfort plane was parallel to the floor. The oscilloscope vertical mode was connected to a DC coupled differential amplifier (Model 7A22, Tektronix, Inc.), and the band width was set with a high-frequency cutoff (-3 dB) at 10 kHz and a low frequency cutoff (-3 dB) at 0.1 kHz. The volts per graticule division used was at 50 pV. Amplitude was measured from the horizontal midline of the graticule (Fig. 3). The time per displayed division was set at 20 milliseconds and was adjusted to begin at the second vertical graticule line. All trace recordings were photographed with a camera (Model C-5A, Tektronix, Inc.) using black and white instant pack film (type 667, Polaroid Corp., Cambridge, Mass.). The term “silent period” as used by previous investigators represents a period of inhibition of muscle activity upon sudden decrease of isometric closure.20,‘& 28This period will be referred to in this investigation as the silent period of the unloading reflex or SPUR. Reflex latency was used as the dependent variable based on the hypothesis that the mechanism for the SPUR is due to a difference in decay of excitation and inhibition on levator muscle motor neurons. Criteria for reflex measurements were based on the following definition of latency. The latency of the un-
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Table II. Means and standard deviations for SPUR latencies (msec) for masseter muscle
Table III. Summary of single-factor ANOVA for masseter muscle SPUR latency df
Mean square
Group SOWCI?
Subject
2 4 5 6 8 9 10
Total Mean SD
1 9.33 9.00 9.33 10.66 9.00 13.33 10.00 11.33 10.33 10.33 102.64 10.26 rt 1.32
2
3
10.00 10.00 9.66 10.00 10.00 10.00 11.66 10.00 9.66 9.66 100.64 10.06 kO.58
9.33 10.00 11.33 10.00 10.00 10.66 10.00 10.00 9.00 11.00 101.32 10.13 LO.71
loading reflex was defined as the duration of EMG activity that is present after the break of the glass tube and before the start of the SPUR. This latency was measured in the photograph starting at the second vertical graticule line and extending to the last positive or negative peak, which was twice the baseline value of the decreased EMG period. The adequacy of the definition was tested with doubleblind investigators using only the definition as a guide. Calculations using the paired sample t-test were made and it was determined that no difference existed between the two raters for latency (p < 0.05). The correlation coefficient between the two raters was +0.93. Therefore, all data in this study were measured by a single-blind investigator. RESULTS A single-factor ANOVA was performed to investigate the effects of decreased intraoral sensory receptor discharge on the onset of the unloading reflex. The dependent measure was latency (in milliseconds) of masseter and temporal muscle unloading as measured from the storage oscilloscope. The mean latencies for the masseter muscle in all three groups are shown in Table II. Group 1, subjects with natural teeth, had a mean latency of 10.26 msec (+ 1.32) with a range of 7 to 15 msec. In group 2, complete denture subjects, the masseter muscle demonstrated a mean latency of 10.06 msec (kO.58) with a range of 8 to 11 msec. In group 3, the implant fixed partial denture population, demonstrated a mean latency of 10.13 msec (+0.71) with a range of 7 to 14 msec. In Table III, the calculated value (Fcalc = 0.12) did not exceed the critical value (Fcr = 3.35). Therefore, the times of onset for the unloading reflex were not significantly different among the three groups in the masseter muscle. The mean latencies for the temporal muscle in all three groups are listed in Table IV. Group 1 had a mean latency of 9.30 msec (ir 1.70) with a range of 5 to 14 msec. In group
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Among groups
0.20
2
0.10
Within groups Total
23.25 23.45
27 tG
0.86
F
0.12
Calculated value 0.12; critical value 3.35 at p < 0.05. Conclusion: Unable to reject null hypothesis.
2, the mean latency was 9.83 msec (kO.39) and a range of 8 to 11 msec. Group 3 demonstrated a mean latency of 10.30 msec ( -t 1.04) with a range of 8 to 14 msec. The calculated value (Fcalc = 1.89) listed in Table V did not exceed the critical value (Fcr = 3.35); therefore, the times of onset for the unloading reflex were not significantly different among the three groups in the temporal muscle either. Comparative results for both muscles are shown in Fig. 4. According to these findings, there is no basis for rejecting the null hypothesis at a significance level of 0.05. DISCUSSION The latencies of the unloading reflex recorded in this investigation occurred at approximately 10 msec. This corresponds with the results of Lamarre and Lund26 who described monosynaptic “features” in the load-compensating mechanism of jaw-closing muscles. The latencies of dentate subjects recorded by Hannam et a1.,20Beaudreau et a1.,21and Miles and Wilkinson,24 however, were approximately 20 msec, 35 msec, and 10 to 15 msec, respectively. Their data varied significantly within each study, possibly because of their recording techniques. Standard deviations reported by Beaudreau et a1.21ranged from 2 9 msec in the masseter muscles to +16 msec in the temporal muscle, whereas Miles and Wilkinson’* reported a range of 10 to 20 msec. The standard deviations were lower in this investigation with t 1.32, 2 0.58, and + 0.71 respectively in groups 1, 2, and 3. This small deviation may be attributed to the accuracy of the position of the unloading apparatus in the subject’s mouth by an occlusal registration. Most investigations point to the muscle receptors as the primary source for jaw unloading except for the study of Goodwin and Luschei.32 They reported that a complete bilateral destruction of levator spindle afferent cell bodies in the mesencephalic trigeminal nucleus did not abolish the SPUR. In this situation one would expect the latency of the SPUR to be longer.26 However, because of the measuring techniques used by Goodwin and Luschei,32 it was not possible for them to measure the exact latency of the SPUR. The stimulation of oral mucosa has also been demonstrated to inhibit jaw-closing muscles.33s34Therefore, the SPUR recorded in this situation could have been produced by afferents located elsewhere. Because the oral mucosa receives 547
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Table IV. Means and standard deviations for SPUR latencies (msec) for temporal muscle
MASSETER TEMPORALIS
Group Subject
1
2
12
3 11.66
0.00
9.33
9.00
10.00
10.00
0.00
10.00
9.33
8.33
10.00
10.00
9.33
9.00
9.33
10.00
12.33
10
6
6.66 1 2.66
10.33
8
10.00
10.00
10.00
9
9.66
10.00
10.00
g
11.00
ii
10
Total Mean SD
7.33
9.66
92.97 9.30
98.32 9.83
k1.70
20.39
ET AL
9.33
6
102.98
4
10.30 zk1.04
2
its innervation from the same fibers as the periodontal ligament, these findings should not be surprising. Little research, however, has been conducted in this area. The short latencies reported in this investigation attest to the existence of a simplistic mechanism for jaw-muscle load compensation, thereby supporting the autogenic inhibition theory proposed by Angel et a1.F8Murphy,27 and Lamarre and Lund.26 The weakness of the reciprocal inhibition theory as proposed by Barnet et a1.30and Miles and Wilkinsonz4 lies in the polysynaptic onset of antagonist activity. Most investigators report this activity occurring well after agonist inhibition.26, 28 Miles and Wilkinson24 reported the occurrence of simultaneous agonist and antagonist activity and concluded that the mechanism for limiting jaw movement during the reflex was antagonist stiffness. However, in a subsequent study they found this stiffness to be dependent on whether the subject consciously anticipated an unloading event.25 This would certainly include antagonist coactivation as a component of the unloading reflex, but does not explain the mechanism of reflex initiation when jaw unloading occurs unexpectedly. The use of reflex latency in this investigation was based on the hypothesis that the mechanism for the SPUR is due to a difference in decay of excitation and inhibition on levator-muscle motor neurons. A larger time course for excitation by periodontal receptors versus mandibular levator receptors could lead to a shorter latency on the loss of the periodontal afferents. The rationale is as follows: clenching before fracture of the glass tube and initiation of the SPUR would activate levator muscle spindles (through alpha-gamma coactivation35) and periodontal afferents with monosynaptic excitatory connections to the levator motor neurons. At the same time, Golgi tendon organs (in the levator muscles) and periodontal afferents have polysynaptic inhibitory connections to the same motor neurons. With breakage of 548
0
GROUPS 4. Mean EMG latencies of masseter and temporal muscles. Comparative results demonstrate no statistically significant differences observed in unloading reflex latency for masseter or temporal muscles.
Fig.
Table V. Summary of single-factor ANOVA for temporal muscle SPUR latency source
Sum of squares
df
Mean square
2
2.51 1.33
Among groups
5.02
Within groups Total
35.81
27
40.83
iii
F
1.89
Calculated value 1.89; critical reject null hypothesis.
value 3.35 at p < 0.05. Conclusion:
Unable to
the glass tube, the monosynaptic facilitation would delay more rapidly than the polysynaptic inhibition on these motor neurons. Since the fiber size of the muscle afferents are larger than that of the periodontal afferents, and the conduction distances are shorter, the latency of the SPUR should be longer with the presence of the periodontal innervation. That is, loss of the periodontal innervation would lead to a shortening of the SPUR. The absence of any change in latency found in these experiments favors a muscle spindle origin for the SPUR. Physiologic properties of the mandible and mechanical properties of the prosthesis have a major influence on the functional deformation of a fixed prosthesis.36 Since jawmuscle unloading has been demonstrated to occur normally APRIL
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in patients with implant-supported prostheses, the occurrence of the large impact loads described by Skalakll remains questionable. Therefore, the placement of shock absorbing materials between occlusal surfaces and the bone-implant interface may not be indicated in this type of prosthesis design. CLINICAL
11. 12.
13.
IMPLICATIONS
Controlled initial loading of the implant fixtures has been an important function of acrylic resin materials in implant prostheses. Because bone remineralization occurs up to 1 year after implant placement in the mandible and up to 18 months in the maxillae, it is advisable that the shock absorption qualities of acrylic resin be used initially to protect the bone-implant interface from harmful loading forces. The final restoration can then be made on a stronger, denser bone-implant interface, with greater assurance that the implant fixtures are capable of withstanding masticatory loading forces.
14.
15.
16.
17.
18. 19.
SUMMARY The present investigation found that the mean latencies for the masseter and temporal muscles did not differ significantly among three groups of subjects with different oral sensory conditions. This provides evidence that the unloading reflex latency does not significantly change because of a decrease in sensory input from periodontal ligament receptors around natural teeth. These results do not exclude these receptors from participating in the inhibitory mechanism of the jaw-closing muscles, but instead suggest that other receptors play a more important role in the SPUR. Alternatively, other afferents may sufficiently compensate for their loss, provided that mechanisms for functional reorganization exist for this reflex.
20. 21. 22. 23.
24.
25.
26. 27.
REFERENCES 1. Jemt T, Carlsson GE. Aspects of mastication with bridges on osseointegrated implants. Stand J Dent Res 1986;94:66-71. 2. Jemt T, Lindquist L, Hedegard B. Changes in chewing patterns of patients with complete dentures after placement of osseointegrated implants in the mandible. J PROSTHET DENT 1985;53:578-83. 3. Haraldson T, Ingervall B. Silent period and jaw jerk reflex in patients with osseointegrated oral implant bridges. Stand J Dent Res 197987: 365.72. 4. Haraldson T, Ingervall B. Muscle function during chewing and swallowing in patients with osseointegrated oral implant bridges. An electromyographic study. Acta Odontol Stand 1979;37:207-16. 5. Haraldson T, Carlsson GE. Bite force and oral function in patients with osseointegrated oral implants. Stand J Dent Res 1977;85:200-8. 6. Haraldson T, Carlsson GE, Ingervall B. Functional state, bite force and postural muscle activity in patients with osseointegrated oral implant bridges. Acta Odontol Stand 1979;3’7:195-206. 7. Lindquist LW, Carlsson GE. Long-term effects on chewing with mandibular fixed prostheses on osseointegrated implants. Acta Odontol Stand 1985;43:39-45. 8. Haraldson T, Carlsson GE. Chewing efficiency in patients with osseointegrated oral implant bridges. Swed Dent J 1979;3:183-91. 9. Haraldson T. A lo-year functional follow-up of patients with osseointegrated implant bridges. In: van Steenberge 0, ed. Tissue integration in oral and maxillo-facial reconstruction. Proceedings of an International Congress. Amsterdam: Excerpta Medica, 1986320.5. 10. Albrektsson T, Branemark P-I, Hansson HA, Lindstrom J. Osseointegrated titanium implants. Requirements for ensuring a long-lasting, diTHE
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rectbone-to-implantanchorageinman.ActaOrthopScand 1981;52:15570. Skalak R. Biomechanical considerations in osseointegrated prostheses. J PROSTHET DENT 1983;49:843-8. Adell R, Lekholm U, Rockier B, Branemark P-I. A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 1981;10:387-416. Lundgren D, Laurel1 L, FaIk H, Bergendal T. Occlusal force pattern during mastication in dentitions with mandibular fixed partial dentures supported on osseointegrated implants. J PROSTHET DENT 1987;58: 197.203. Lundgren D, Laurel1 L. Occlusal force pattern during chewing and biting in dentitions restored with fixed bridges of cross-arch extension. II. Unilateral posterior two-unit cantilevers. J Oral Rehabil 1986;13:191203. Lundgren D, Laurel1 L. Occlusal force pattern during chewing and biting in dentitions restored with fixed bridges of cross-arch extension. I. Bilateral end abutments, J Oral Rehabil 1986;13:57-71. Moller E, Scheikholeslam B, Lous I. Response of elevator activity during mastication to treatment of functional disorders. Stand Dent J 1984;92:64-83. Haraldson T. Comparisons of chewing patterns in patients with bridges supported on osseointegrated implants and subjects with natural dentitions. Acta Odontol Stand 1983;41:203-8. Jemt T. Chewing patterns in dentate and complete denture wearersrecorded by light-emitting diodes. Swed Dent J 1981;5:199-205. Hansen K, Hoffmann P. Weitere Untersuchungen uher die Bedeutung der Eigenreflexe fur unsere Bewegungen. I. Anspannungs-und Entspannungsreflexe. Z Biol 1922;75:293-304. Hannam AG, Matthews B, Yemm R. The unloading reflex in masticatory muscles of man. Arch Oral Biol 1968;13:361-4. Beaudreau DE, Daugherty WR Jr, Masland WS. Two types of motor pause in masticatory muscles. Am J Physiol 1969;216:16-21. Duhner R, Sessle BJ, Storey AT. The neural basis of oral and facial function. New York: Plenum, 1978. Greenwood LC. The neuromuscular system. In: Mohl ND, Zarb GA, Carlsson GE, Rugh JD, eds. A textbook of occlusion. Chicago: Quintessence, 1988. Miles TS, Wilkinson TM. Limitation of jaw movement by antagonist muscle stiffness during unloading of human jaw closing muscles. Exp Brain Res 1982;46:305-10. Miles TS, Madigan ML. Programming of antagonist muscle stiffness during masticatory muscle unloading in man. Arch Oral Biol 1983;28: 947-51. Lamarre Y, Lund JP. Load compensation in human masseter muscles. J Physiol 1975;253:21-35. Murphy TR. Shortening inhibition of prime movers. A safety factor in mastication. Br Dent J 1967;123:578-84. Angel RW, Eppler W, Iannone A. Silent period produced by unloading of muscle during voluntary contraction. d Physiol 1965;180:864-70. Gill HI. Unloading reflex of the jaw muscles. J Dent Res 1970;49:649. Barnet CH, Davies DV, MacCoraill MA. Synovial joints: their structure and mechanics. London: Longmans, Green, 1961. Branemark P-I, Hansson BO, Adell R, Breine U, Lindstrom J, Hallen 0, Ohman A. Osseointegrated implants in the treatment of the edentulous jaw. Experience from a lo-year period. Stand J Plast Reconstr Surg 1977;11(Suppl 161:1-132. Goodwin GM, Luschei ES. Effects of destroying spindle afferents from jaw muscles on mastication in monkeys. J Neurophysiol1974;37:967-81. Yemm R. The response of the masseter and temporal muscles following electrical stimulation of the oral mucous membrane in man. Arch Oral Biol 1972;17:23-33. Yemm R. ReAex jaw opening following electrical stimulation of oral mucous membrane in man. Arch Oral Biol 1972;17:513-23. Cody FWJ, Taylor A. Behaviour of spindles in the jaw-closing muscles during eating and drinking in the cat. J Physiol 1961;231: 49.50. Glantz P-O, Strandman E, Svensson SA, Randow K. On functional strain in fixed mandibular reconstructions. I. An in vitro study. Acta Odontol Stand 1984;42:241-9.
Reprint requests to: DR. RANDALL C. DUNCAN 2137 ELLSWORTH AVE. OMAHA. NE 68123
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of Texas Health
The control of postural and synergistic jaw reflexes involves interrelated sensory input from receptors in the jaw muscles, temporomandihular joint, periodontal ligament, and mucosa. This investigation was done to determine whether a decrease in intraoral sensory aiferent discharge significantly altered the onset of the jaw-unloading reflex. The subject population consisted of three groups with 10 subjects in each group. Group 1 had maxillary and mandibular natural teeth and group 2 consisted of edentulous subjects with complete dentures. Group 3 consisted of edentulous subjects with maxillary complete dentures and mandibular complete implant-supported prostheses. The unloading reflex was initiated with a muscleunloading device and recorded with a storage oscilloscope. A one-way analysis of variance found no significant differences in the unloading-reflex latency for the masseter or temporal muscles among the three experimental groups (p < 0.05). (J PROSTHET DENT 1992;67:544-9.)
P
resent evidence indicates that patients with an osseointegrated implant fixed partial denture (FPD) approach the masticatory function of patients with equivalent natural teeth.lmgIt is believed that this success is primarily because the rigid connection between implant and bone allows stress transmission without appreciable motion in the prosthesis.1° The masticatory system, however, has the potential to develop large impact forces during function that, if inadequately unloaded, could compromise the integrity of this bone-implant interface. I1 For this reason, Skalakl’ recommended the use of acrylic resin between the occluding surface and the fixture to provide adequate shock protection. Clinical evidence for the lasting integration of loaded fixtures, however, has not revealed a problem with excessive occlusal forces.r2 However, Lundgren et a1.r3studied the occlusal force pattern in patients with complete dentures
The opinions expressed herein are those of the authors and are not to be construed as official or reflecting the views of the U.S. Air Force or the Department of Defense. Supported in part by the Education and Research Foundation of Prosthodontics. Third place, John J. Sharry Prosthodontic Research Competition, American College of Prosthodontists, Tucson, Ark., 1990. aMajor, U.S. Air Force, Dental Corps; Assistant Chairman, Department of Prosthodontics, Ehrling Bergquist Strategic Hospital. bProfessor and Chairman, Department of Orthodontics, University of Texas Health Science Center, Dental School. cProfessor, Department of Oral and Maxillofacial Surgery, University of Texas Health Science Center, Dental School. dProfessor and Head, Division of Maxillofacial Prosthetics, University of Texas Health Science Center, Dental School.
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opposing mandibular implant FPDs and found that patients chewed with 60% of their maximal closing force. This force can be compared with 26% of maximal closing force in patients with unilateral posterior two-unit cantilevers, 37% in patients with bilateral end abutments, and 45% reported in natural teeth.14-16 In an electromyographic study of masticatory muscle activity, Haraldson17 reported that patients with implant FPDs chewed with consistent muscle activity during the whole chewing sequence, compared with dentate patients who had a decrease in muscle activity at the end of the chewing act.‘s Haraldson17 theorized that this change in the chewing pattern might be due to a decrease in oral tactile sensibility that could cause a change in neurophysiological feedback mechanisms. He suggested that a masticatory training program may be indicated for patients undergoing implant fixed partial denture rehabilitation. The unloading reflex, or “Entlastung” reflex, was first described in limb muscles by Hansen and Hoffmann,lg and in masticatory muscles by Hannam et akzOand Beaudreau et a1.21The reflex has been defined as the sudden or unexpected removal of an isometric load from the jaw-closing muscles.20-24Most investigators generally believe that this is a protective masticatory reflex in that it arrests jaw movements before tooth contact occurs.20,21,24,25When a hard object is encountered between the teeth, large isometric forces are generated that can result in the teeth crashing together when the object suddenly breaks. The sensory input for this reflex has not been fully established, although several possible sources of receptors have been proposed including muscle receptors,26-28periodontal ligament receptors,20g21 mucosal receptors,2g joint receptors,20,26and tendon receptors20 as well as reciprocal inhi-
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Table I. Identification Receptors stimulated
stimulated stimulated
MUSCLES
of receptors stimulated
Group 1 (Control)
Group 2 (Control)
+
0
0
0 +
+* +
+T +
Periodontal ligament Mucosa All others *Receptors tReceptors
IN JAW
in maxilla in maxilla
Group 3 (Experimental)
and mandible. only.
bition of jaw muscles. 24,3oProviding that the unloading reflex involves interrelated input from several afferent pathways, a decrease in sensory input may affect reflex latency. In other words, the latency could be altered if a decrease in stimulus intensity significantly affected the threshold potential for this reflex. Although the incorporation of a mechanical damping system in the prosthesis design has been recommended to eliminate potentially harmful forces, it may only be necessary if the physiologic load-compensating mechanism were compromised. However, the jaw unloading reflex in patients with implant-supported prostheses has not yet been investigated. This investigation was done to determine whether a decrease in intraoral sensory afferent discharge significantly altered the onset of the jaw-unloading reflex. This study tested the null hypothesis that there is no statistically significant difference in the latency of the unloading reflex when experimental subjects are compared with the control subjects. METHODS
AND
MATERIAL
The experimental design called for a comparison of unilateral electromyographic activity of the masseter and temporal muscles during isometric loading among three population groups. A group size of 10 subjects was statistically determined by power analysis of a pilot study. The subjects were all selected from The University of Texas, Dental School at San Antonio, and were fully informed of the procedures and risks before their consent was obtained. An even gender distribution was selected with an average age of 57.5 years. Patients were not selected if they had a history of temporomandibular, auricular, or neuromuscular pain or dysfunction. Most of the patients with implantsupported prostheses had a mandibular implant-supported fixed prosthesis opposing a maxillary removable complete denture. For this reason, two control groups were used in this study to identify the role of mucosal receptors under the complete dentures of the experimental group (Table I). Control group 1 consisted of 10 subjects with natural maxillary and mandibular teeth surrounded by mechanoreceptors in the periodontal ligament in both dental arches. Control group 2 consisted of 10 completely edentulous subjects restored with maxillary and mandibular
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Fig. 1. Unloading apparatus. (A) Stationary upper jaw bar, (B) piezoelectric cartridge transducer, (C) lower jaw bar with hole for glass tube that provides resistance to jaw closing, (0) trigger arm mechanically linking transducer to lower jaw bar, (E) polypropylene pad secured to jaw bar. Dental impression material placed on this pad allowed reproducible positioning of apparatus in mouth, (F) axis of rotation for lower jaw bar.
complete dentures. These subjects were totally missing periodontal ligament receptors in both arches, but had mucosal receptors stimulated by the prostheses. The experimental group (group 3) consisted of 10 completely edentulous subjects restored with a maxillary complete denture and a mandibular implant-supported prosthesis. Implant-supported prostheses were of a hybrid design constructed on four to five threaded cylindrical fixtures (Nobelpharma USA Inc., Waltham, Mass.), which were surgically placed by procedures outlined by Branemark et a1.31and Albrektsson et al.‘O Artificial teeth used in all prostheses were made of acrylic resin (Bioblend, Dentsply International, Inc., York, Pa.) processed to a high-impact acrylic resin denture base (Lucitone 199, Dentsply International, Inc., Milford, Del.). This group of subjects had mucosal receptors stimulated only in the maxillary arch. The apparatus used for muscle unloading allowed the subjects to develop an isometric loading force with jawclosing muscles until the resistance to jaw closure was suddenly overcome, initiating the unloading reflex. The apparatus was a modified version of the device used by Miles and Wilkinson24 and consisted of two cast chromium alloy (Ticonium 100, Ticonium Co., New York, N.Y.) jaw bars mounted on a stainless steel plate measuring 112 mm x 60 mm x 2 mm (Fig. 1). The upper bar was fixed at a constant position in relation to the lower bar, which was hinged and allowed to rotate. The lower bar was positioned 19 mm from the upper bar and stabilized temporarily by a 35 mm sec545
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ET AL
3. Descriptive representation of reflex latency and duration. EMG trace was adjusted to begin at second vertical line on graticule the instant glass tube broke. Latency demonstrated in this drawing is 10 msec and duration is 47 msec. Fig.
Fig. 2. Electrode placement. Bipolar surface electrode placement parallel to muscle fibers with interelectrode distance of 2 cm. Line connecting outer canthus of eye and angle of mandible was used as guide in placing electrodes on masseter muscle, with most inferior electrode 1 cm from mandibular inferior border. Electrodes were placed on temporal muscle as close to hairline as possible. ,Ground electrode was placed at mastoid region on ipsilateral side.
tion of glass tubing (4 mm diameter, Pyrex, American Scientific Products, Houston, Tex.) which was placed through the jaw bar and the stainless steel plate. The glass tube was positioned away from the rotational center of the bar to allow it to break consistently at a resistance of 59N (Instron Universal testing machine, Model 1125, Instron Corp., Canton, Mass.). Breakage of the glass tube was detected by a piezoelectric cartridge transducer that was mechanically linked to the lower bar. This bar was connected to the external trigger input of a single trace storage oscilloscope (Model 7623A, Tektronix, Inc., Beaverton, Ore.) that was calibrated to begin a sweep at the exact instant the glass tubing broke. The entire apparatus was covered with plastic film (Anchor Industries, St. Louis, MO.) to contain the glass tubing after breakage. Each jaw bar had a biteplate covered with polypropylene material (Buffalo Dental Mfg., Co., Syosset, N.Y.) secured with cyanoacrylate cement (Rapid Bonding Adhesive, Toagosei Chemical, Tokyo, Japan). A polyether registration material (Ramitek, Premier, Norristown, Pa.) was used to consistently position the jaw bars in the maxillary first premolar region for three recordings in each muscle group. The activity of the temporal and masseter muscles was recorded with silver-silver chloride surface electrodes (Model SE-40, 8.5 mm diameter, J & J, Poulsbo, Wash.) using double-backed adhesive disks (Med Associates, Inc., East Fairfield, Ver.) and electrode paste (type 651-1022,
546
Hewlett Packard Redux Creme, Waltham, Mass.). Electrodes were positioned on the skin parallel to the direction of the muscle fibers (Fig. 2). Interelectrode impedance was measured with an impedance meter (Model EZM, Gross Instrument Co., Quincy, Mass.) and was kept below 10 kilo-ohms. Unilateral EMG activity was recorded at a constant temperature of 75’ C on subjects seated in an upright position so that the Frankfort plane was parallel to the floor. The oscilloscope vertical mode was connected to a DC coupled differential amplifier (Model 7A22, Tektronix, Inc.), and the band width was set with a high-frequency cutoff (-3 dB) at 10 kHz and a low frequency cutoff (-3 dB) at 0.1 kHz. The volts per graticule division used was at 50 pV. Amplitude was measured from the horizontal midline of the graticule (Fig. 3). The time per displayed division was set at 20 milliseconds and was adjusted to begin at the second vertical graticule line. All trace recordings were photographed with a camera (Model C-5A, Tektronix, Inc.) using black and white instant pack film (type 667, Polaroid Corp., Cambridge, Mass.). The term “silent period” as used by previous investigators represents a period of inhibition of muscle activity upon sudden decrease of isometric closure.20,‘& 28This period will be referred to in this investigation as the silent period of the unloading reflex or SPUR. Reflex latency was used as the dependent variable based on the hypothesis that the mechanism for the SPUR is due to a difference in decay of excitation and inhibition on levator muscle motor neurons. Criteria for reflex measurements were based on the following definition of latency. The latency of the un-
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Table II. Means and standard deviations for SPUR latencies (msec) for masseter muscle
Table III. Summary of single-factor ANOVA for masseter muscle SPUR latency df
Mean square
Group SOWCI?
Subject
2 4 5 6 8 9 10
Total Mean SD
1 9.33 9.00 9.33 10.66 9.00 13.33 10.00 11.33 10.33 10.33 102.64 10.26 rt 1.32
2
3
10.00 10.00 9.66 10.00 10.00 10.00 11.66 10.00 9.66 9.66 100.64 10.06 kO.58
9.33 10.00 11.33 10.00 10.00 10.66 10.00 10.00 9.00 11.00 101.32 10.13 LO.71
loading reflex was defined as the duration of EMG activity that is present after the break of the glass tube and before the start of the SPUR. This latency was measured in the photograph starting at the second vertical graticule line and extending to the last positive or negative peak, which was twice the baseline value of the decreased EMG period. The adequacy of the definition was tested with doubleblind investigators using only the definition as a guide. Calculations using the paired sample t-test were made and it was determined that no difference existed between the two raters for latency (p < 0.05). The correlation coefficient between the two raters was +0.93. Therefore, all data in this study were measured by a single-blind investigator. RESULTS A single-factor ANOVA was performed to investigate the effects of decreased intraoral sensory receptor discharge on the onset of the unloading reflex. The dependent measure was latency (in milliseconds) of masseter and temporal muscle unloading as measured from the storage oscilloscope. The mean latencies for the masseter muscle in all three groups are shown in Table II. Group 1, subjects with natural teeth, had a mean latency of 10.26 msec (+ 1.32) with a range of 7 to 15 msec. In group 2, complete denture subjects, the masseter muscle demonstrated a mean latency of 10.06 msec (kO.58) with a range of 8 to 11 msec. In group 3, the implant fixed partial denture population, demonstrated a mean latency of 10.13 msec (+0.71) with a range of 7 to 14 msec. In Table III, the calculated value (Fcalc = 0.12) did not exceed the critical value (Fcr = 3.35). Therefore, the times of onset for the unloading reflex were not significantly different among the three groups in the masseter muscle. The mean latencies for the temporal muscle in all three groups are listed in Table IV. Group 1 had a mean latency of 9.30 msec (ir 1.70) with a range of 5 to 14 msec. In group
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Among groups
0.20
2
0.10
Within groups Total
23.25 23.45
27 tG
0.86
F
0.12
Calculated value 0.12; critical value 3.35 at p < 0.05. Conclusion: Unable to reject null hypothesis.
2, the mean latency was 9.83 msec (kO.39) and a range of 8 to 11 msec. Group 3 demonstrated a mean latency of 10.30 msec ( -t 1.04) with a range of 8 to 14 msec. The calculated value (Fcalc = 1.89) listed in Table V did not exceed the critical value (Fcr = 3.35); therefore, the times of onset for the unloading reflex were not significantly different among the three groups in the temporal muscle either. Comparative results for both muscles are shown in Fig. 4. According to these findings, there is no basis for rejecting the null hypothesis at a significance level of 0.05. DISCUSSION The latencies of the unloading reflex recorded in this investigation occurred at approximately 10 msec. This corresponds with the results of Lamarre and Lund26 who described monosynaptic “features” in the load-compensating mechanism of jaw-closing muscles. The latencies of dentate subjects recorded by Hannam et a1.,20Beaudreau et a1.,21and Miles and Wilkinson,24 however, were approximately 20 msec, 35 msec, and 10 to 15 msec, respectively. Their data varied significantly within each study, possibly because of their recording techniques. Standard deviations reported by Beaudreau et a1.21ranged from 2 9 msec in the masseter muscles to +16 msec in the temporal muscle, whereas Miles and Wilkinson’* reported a range of 10 to 20 msec. The standard deviations were lower in this investigation with t 1.32, 2 0.58, and + 0.71 respectively in groups 1, 2, and 3. This small deviation may be attributed to the accuracy of the position of the unloading apparatus in the subject’s mouth by an occlusal registration. Most investigations point to the muscle receptors as the primary source for jaw unloading except for the study of Goodwin and Luschei.32 They reported that a complete bilateral destruction of levator spindle afferent cell bodies in the mesencephalic trigeminal nucleus did not abolish the SPUR. In this situation one would expect the latency of the SPUR to be longer.26 However, because of the measuring techniques used by Goodwin and Luschei,32 it was not possible for them to measure the exact latency of the SPUR. The stimulation of oral mucosa has also been demonstrated to inhibit jaw-closing muscles.33s34Therefore, the SPUR recorded in this situation could have been produced by afferents located elsewhere. Because the oral mucosa receives 547
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Table IV. Means and standard deviations for SPUR latencies (msec) for temporal muscle
MASSETER TEMPORALIS
Group Subject
1
2
12
3 11.66
0.00
9.33
9.00
10.00
10.00
0.00
10.00
9.33
8.33
10.00
10.00
9.33
9.00
9.33
10.00
12.33
10
6
6.66 1 2.66
10.33
8
10.00
10.00
10.00
9
9.66
10.00
10.00
g
11.00
ii
10
Total Mean SD
7.33
9.66
92.97 9.30
98.32 9.83
k1.70
20.39
ET AL
9.33
6
102.98
4
10.30 zk1.04
2
its innervation from the same fibers as the periodontal ligament, these findings should not be surprising. Little research, however, has been conducted in this area. The short latencies reported in this investigation attest to the existence of a simplistic mechanism for jaw-muscle load compensation, thereby supporting the autogenic inhibition theory proposed by Angel et a1.F8Murphy,27 and Lamarre and Lund.26 The weakness of the reciprocal inhibition theory as proposed by Barnet et a1.30and Miles and Wilkinsonz4 lies in the polysynaptic onset of antagonist activity. Most investigators report this activity occurring well after agonist inhibition.26, 28 Miles and Wilkinson24 reported the occurrence of simultaneous agonist and antagonist activity and concluded that the mechanism for limiting jaw movement during the reflex was antagonist stiffness. However, in a subsequent study they found this stiffness to be dependent on whether the subject consciously anticipated an unloading event.25 This would certainly include antagonist coactivation as a component of the unloading reflex, but does not explain the mechanism of reflex initiation when jaw unloading occurs unexpectedly. The use of reflex latency in this investigation was based on the hypothesis that the mechanism for the SPUR is due to a difference in decay of excitation and inhibition on levator-muscle motor neurons. A larger time course for excitation by periodontal receptors versus mandibular levator receptors could lead to a shorter latency on the loss of the periodontal afferents. The rationale is as follows: clenching before fracture of the glass tube and initiation of the SPUR would activate levator muscle spindles (through alpha-gamma coactivation35) and periodontal afferents with monosynaptic excitatory connections to the levator motor neurons. At the same time, Golgi tendon organs (in the levator muscles) and periodontal afferents have polysynaptic inhibitory connections to the same motor neurons. With breakage of 548
0
GROUPS 4. Mean EMG latencies of masseter and temporal muscles. Comparative results demonstrate no statistically significant differences observed in unloading reflex latency for masseter or temporal muscles.
Fig.
Table V. Summary of single-factor ANOVA for temporal muscle SPUR latency source
Sum of squares
df
Mean square
2
2.51 1.33
Among groups
5.02
Within groups Total
35.81
27
40.83
iii
F
1.89
Calculated value 1.89; critical reject null hypothesis.
value 3.35 at p < 0.05. Conclusion:
Unable to
the glass tube, the monosynaptic facilitation would delay more rapidly than the polysynaptic inhibition on these motor neurons. Since the fiber size of the muscle afferents are larger than that of the periodontal afferents, and the conduction distances are shorter, the latency of the SPUR should be longer with the presence of the periodontal innervation. That is, loss of the periodontal innervation would lead to a shortening of the SPUR. The absence of any change in latency found in these experiments favors a muscle spindle origin for the SPUR. Physiologic properties of the mandible and mechanical properties of the prosthesis have a major influence on the functional deformation of a fixed prosthesis.36 Since jawmuscle unloading has been demonstrated to occur normally APRIL
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in patients with implant-supported prostheses, the occurrence of the large impact loads described by Skalakll remains questionable. Therefore, the placement of shock absorbing materials between occlusal surfaces and the bone-implant interface may not be indicated in this type of prosthesis design. CLINICAL
11. 12.
13.
IMPLICATIONS
Controlled initial loading of the implant fixtures has been an important function of acrylic resin materials in implant prostheses. Because bone remineralization occurs up to 1 year after implant placement in the mandible and up to 18 months in the maxillae, it is advisable that the shock absorption qualities of acrylic resin be used initially to protect the bone-implant interface from harmful loading forces. The final restoration can then be made on a stronger, denser bone-implant interface, with greater assurance that the implant fixtures are capable of withstanding masticatory loading forces.
14.
15.
16.
17.
18. 19.
SUMMARY The present investigation found that the mean latencies for the masseter and temporal muscles did not differ significantly among three groups of subjects with different oral sensory conditions. This provides evidence that the unloading reflex latency does not significantly change because of a decrease in sensory input from periodontal ligament receptors around natural teeth. These results do not exclude these receptors from participating in the inhibitory mechanism of the jaw-closing muscles, but instead suggest that other receptors play a more important role in the SPUR. Alternatively, other afferents may sufficiently compensate for their loss, provided that mechanisms for functional reorganization exist for this reflex.
20. 21. 22. 23.
24.
25.
26. 27.
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