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Sex Differences in Masticatory Muscle Pain after Chewing

¹ Center for Orofacial Pain,
² Center for Orofacial Pain,
³ NIH Pain Center, Department of Oral and Maxillofacial Surgery-Box 0440, University of California, San Francisco, CA 94143-0440;
⁴ current address, Department of Orthodontics & Pediatric Dentistry, Nippon Dental University Hospital at Tokyo, 2-3-16 Fujimi, Chiyoda-ku, Tokyo 102-8158, Japan;

*corresponding author, rwg{at}itsa.ucsf.edu

	ABSTRACT

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Neither the etiology of muscle-related temporomandibular disorders (TMD) nor the reason for the disproportionate number of women suffering from these disorders is well-established. We tested the hypothesis that physiologically relevant exercise (i.e., chewing bubble gum for 6 min) increases masticatory muscle pain in patients, but not in asymptomatic control subjects, and that female patients experience a significantly greater increase than males. Chewing increased pain in both female and male patients and, unexpectedly, also in female control subjects. One hour after chewing, the pain remained above pre-test levels for female patients but not for the other groups. Thus, sex differences in chewing-induced pain were found in control subjects but not as hypothesized in patients. Because chewing-induced masticatory muscle pain was significantly greater in female control subjects than in males, and persisted longer in female patients than in males, these results suggest greater susceptibility in women.

KEY WORDS: muscle pain • exercise • chewing • sex differences • mastication • TMD

	INTRODUCTION

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Most clinicians who treat patients complaining of chronic pain involving the muscles of mastication accept the notion that such pain is exacerbated by exercise and that treatment should include recommendations for self-care aimed at reducing activity in these muscles. Patients are advised to eat only soft foods and to decrease parafunctional activities such as clenching (American Academy of Orofacial Pain, 1996). Several studies have found that a significant proportion of patients with temporomandibular disorders (TMD) report pain associated with chewing (Zarb and Thompson, 1970; Fricton et al., 1985; Bush et al., 1989; Dworkin et al., 1990; Gavish et al., 2000; Winocur et al., 2001). Other studies have documented increases in muscle pain in response to specific experimental exercise regimens (Molin, 1972; Christensen, 1976; Scott and Lundeen, 1980; Christensen and Radue, 1985; Bowley and Gale, 1987; Dao et al., 1994; Plesh et al., 1998; Gavish et al., 2002). Of these, only two studies (Dao et al., 1994; Gavish et al., 2002) examined the effects of physiologically relevant exercise, chewing, on masticatory muscle pain in patients with diagnosed TMD and in normal control subjects. Both studies used the same chewing bolus, a half-leaf of green casting wax, but the duration of the chewing test was different. Using a three-minute protocol, Dao and colleagues found that about 70% of the patients experienced increased pain, while the other 30% experienced decreased pain. In contrast, Gavish and colleagues found that virtually all patients experienced increased pain after chewing for 9 min, indicating that the duration of chewing is important in eliciting pain. There were no changes in pain in normal control subjects in either study. However, a pilot study conducted at the University of California, San Francisco (L. Centore and O. Plesh, unpublished observations), which did not include control subjects, found that chewing bubble gum for 6 min increased the pain in all but one of their subjects. Since the duration of chewing in this study was intermediate between those of the other two studies, but the chewing bolus was different (i.e., bubble gum vs. wax), the physical characteristics of the bolus could also play a role.

It is well-established that women outnumber men 3:1 to 9:1 as patients seeking care for TMD (Dworkin et al., 1990; Howard, 1991; Bush et al., 1993; Lipton et al., 1993). Although at least one study has reported sex differences in clenching-induced pain in normal volunteers (Plesh et al., 1998), no studies to date have examined for sex differences in masticatory muscle pain response to chewing exercise in either patients or normal control subjects. Therefore, the present study was designed to test the effect of chewing on masseter muscle pain in patients and in asymptomatic control subjects and to determine whether there are significant sex differences in pain responses. Some of these results have been reported in abstract form.

	MATERIALS & METHODS

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Seventy-one individuals participated in this study (Table). Patients were recruited at the University of California San Francisco Center for Orofacial Pain; control subjects were recruited from among university employees and students. Patients met the criteria for Axis I, Group I.a. or I.b. (i.e., myofascial pain with or without limited opening), of the Research Diagnostic Criteria (RDC) (Dworkin and LeResche, 1992). Their symptoms must have been present at least three months prior to the experiment. Patients with TM-joint-related conditions (RDC Axis I, Groups II or III) or other chronic pain conditions (e.g., fibromyalgia) were excluded from the study. Control participants were examined and were included in the study only if they had no history of TMD pain and had been free of any other pain during the previous three months. This study was approved by the Committee on Human Research at the University of California, San Francisco. Informed consent was obtained from each research subject.

Outcome Variables
    Pain
Participants were instructed in the area of interest (i.e., the masticatory muscles, particularly the masseter and/or temporalis) and were asked to rate their spontaneous (i.e., unevoked by palpation) pain by marking a 100-mm visual analog scale (VAS) anchored on the left with the words "No Pain" and on the right with the words "Worst Pain Imaginable". VAS pain ratings were recorded immediately prior to the chewing test, at one-minute intervals during the test, and at 1, 6, and 24 hrs after the test.

    Range of Motion
Maximal active (i.e., unassisted) mandibular range of motion was measured before and after the chewing test. For this measurement, patients were asked to open as far as possible, even if they experienced discomfort.

    Rate of Mastication
We assessed the rate of mastication during the test by counting the number of chewing cycles in a 10-second period during each of the 6 min.

Data Analysis
ANOVAs were used to test for significant differences (p 0.05) between the groups (i.e., patients and control subjects), between the sexes, and/or over time as described in RESULTS. For repeated-measures ANOVAs (Winer, 1971), the Mauchly criterion was used to determine if the assumption of sphericity for the within-subjects effects was met (Mauchly, 1940); if the Mauchly criterion was not satisfied, Greenhouse-Geisser adjusted p values (Greenhouse and Geisser, 1959) are presented. Post hoc tests are described in RESULTS.

	RESULTS

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Characteristics of study participants are shown in the Table. A two-way ANOVA (sex x group) showed no significant differences in age between the sexes or between the groups (i.e., patients and control volunteers) and no significant sex x group interaction.

Pre-test Pain
Pre-test pain levels (Table) were significantly greater in patients than in controls (F(1, 67) = 36.496, p < 0.001), but neither main effect of sex nor the sex x group interaction was significant, indicating that pre-test pain did not differ significantly between females and males in either group.

Chewing-induced Pain
To determine if there were significant changes in pain during chewing (Figs. 1A, 1B), we conducted a three-way repeated-measures ANOVA (sex x group x time with 7 levels, including the pre-test VAS score) that showed a significant sex x group x time interaction (F (6.402) = 3.05, p = 0.05), a significant main effect of time (F (6.402) = 31.4, p < 0.001), and a significant main effect of group (F (1.67) = 23.4, p < 0.001), but no other significant interactions or main effects. To determine the basis of the significant three-way interaction, we performed two-way repeated-measures ANOVAs (sex x time) separately for control subjects and for patients.

View larger version (15K): [in this window] [in a new window]   Figure 1. Effect of chewing on masticatory muscle pain. (A) Control subjects. Women (n = 19) experienced significantly greater increases in pain than did men (n = 17). (B) Patients. The change in pain during chewing was similar in both sexes. Although men (n = 7) demonstrated a higher overall level of pain than did women (n = 28), this difference was not significant. Asterisks denote time points at which the differences in pain between men and women were significant. Abbreviation: "P/T" refers to pre-test pain rating. Data are represented as mean ± SEM.

    Patients
Although patients as a group experienced increased pain during chewing (Fig. 1B; main effect of time, F (6.198) = 15.9, p < 0.001), there were no significant sex differences either overall or over time (i.e., neither the main effect of sex nor the sex x time interaction was significant).

Post-chewing Pain
To assess the longer-term effect of chewing exercise on pain, we gave participants a diary and asked them to complete VAS pain scores at 1, 6, and 24 hrs after the chewing test (Figs. 2A-2D). All diaries were returned except two from female patients and two from male patients. A one-way repeated-measures ANOVA (time with 4 levels) was performed for each of the four group samples. If there was a significant effect of time, post hoc pairwise contrasts were performed in which the VAS scores at each of the post-test time points were compared with the pre-test score to determine when the differences occurred. For these contrasts, a Bonferroni-type correction was applied such that the alpha level was set at p = 0.0167 (i.e., 0.05 ÷ 3).

View larger version (14K): [in this window] [in a new window]   Figure 2. Effect of chewing on pain over a 24-hour period. Participants completed and returned pain diaries in which they rated their pain levels at 1, 6, and 24 hrs after the test. These scores (mean ± SEM) are shown along with the pre-test ("P/T") scores (note that the times indicated on the x-axis are not spaced to scale). (A) Female control subjects (n = 19) and (B) male control subjects (n = 17) returned to pre-test pain levels within 1 hr after the test. (C) Female patients (n = 26) reported significantly elevated pain with respect to their pre-test pain levels 1 hr after the test (indicated by the asterisk) but returned to pre-test levels thereafter. (D) Male patients (n = 5), like control subjects, returned to pre-test pain levels within 1 hr. Note that the mean baseline VAS score for male patients in Fig. 2D is different from that shown in the Table and Fig. 1B, because the sample size is different.

    Patients
For female patients (Fig. 2C), but not male patients (Fig. 2D), pain levels after chewing were significantly different from pre-test levels (F (3.75) = 4.548, p = 0.006). The post hoc pairwise contrasts showed that only the one-hour post-test time point was significantly different from pre-test scores (F (1.25) = 12.827, p = 0.001).

Effect of Chewing on Range of Motion
To determine if chewing affected range of motion (Table), we performed a three-way repeated-measures ANOVA (sex x group x time with two levels). This analysis showed a significant main effect of time (F (1.67) = 6.453, p = 0.013), indicating that chewing resulted in a statistically significant reduction in active range of motion ( 1 mm), and a significant main effect of sex (F (1.67) = 10.043, p = 0.002), indicating that the range of motion for men was significantly greater than that for women ( 6 mm). There was no significant overall difference between patients and controls (main effect of group), nor were there any significant interactions.

Rate of Mastication
A two-way repeated-measures ANOVA (group x time) demonstrated that the rate of mastication differed significantly among the four group samples (Fig. 3; F (3.67) = 10.902, p < 0.001), but there was no significant main effect of time or group x time interaction. Scheffé’s post hoc analysis revealed that the lower rate of chewing in female patients was significantly different from that in each of the other three groups (p = 0.005, 0.005, and 0.043). To assess the relationship between chewing rate and pain, we correlated the VAS score and chewing rate at minute six (when pain was highest) for each of the four groups. This analysis failed to show significant correlation for any of the groups; for female patients, the result was r² = 0.044, p = 0.284, indicating that chewing rate did not correlate significantly with pain. However, a further analysis in which the pre-test baseline VAS scores were correlated with average chewing rates for all study participants revealed a significant correlation (r² = 0.126, p = 0.002), indicating that pre-existing pain significantly affected chewing rate during the test; that is, participants with higher pre-test pain levels tended to chew more slowly.

View larger version (22K): [in this window] [in a new window]   Figure 3. Rate of mastication during the test. Although female patients chewed significantly more slowly than the other three groups, there were no changes in the rate of chewing during the test in any of the groups. Rate of chewing is represented as number of chewing cycles/10 sec (mean ± SEM) during each minute of the test. Sample sizes are the same as in Fig. 1.

	DISCUSSION

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To determine the persistence of the increase in pain, we compared post-test VAS scores with pre-test VAS scores for each of the four group samples and found that the post-test pain levels for male and female control subjects and male patients did not differ from pre-test scores at any point, but that female patients recorded significantly higher pain levels compared with pre-test scores 1 hr after the test. Thus, the induction of pain in masticatory muscles by physiologically relevant exercise, chewing, depends on the presence of pre-existing pain and also on sex. That is, chewing resulted in increased pain in women regardless of the presence or absence of pre-existing pain but only in men with pre-existing pain. Furthermore, the increased pain persisted longer in female patients.

The differences in the results of the present study compared with those of previous studies are probably due to differences in the duration of the test as well as to differences in the physical characteristics of the chewing bolus. The present study used bubble gum and tested for 6 min. Dao and colleagues (1994) used casting wax and tested for 3 min and found increased pain in 70% of the patients but no increase in control subjects. Gavish and colleagues (2002) also used casting wax but tested for 9 min and found increased pain in virtually all patients but not in control subjects. Based on this significant separation between patients and control subjects, the authors of this latter study suggested that a chewing test might be developed as a diagnostic aid to identify myofascial pain patients. Our results, showing that female control subjects experienced increased pain, indicate that such a test would have to be carefully calibrated.

There was a statistically significant overall decrease in range of motion in participants after the test, but this change was small ( 1 mm) and was not significantly different among any of the four sample groups. Thus, the decrease in range of motion after the test did not reflect an effect of sex or of pre-existing pain. In any case, the clinical significance of such a small change is questionable. Not surprisingly, range of motion was greater for men than for women.

Although the rate of mastication for female patients was significantly lower than that in the other three groups, this did not appear to result from increasing pain during the test, because their rate was constant throughout the test despite the increasing pain over time, and their VAS pain scores at minute six did not correlate significantly with their chewing rate at minute six, which would presumably be the case if intra-test pain caused chewing rate to decrease. However, when average chewing rate was compared with pre-test VAS pain scores for all study participants, there was a significant negative correlation. Thus, the rate of mastication appears to be influenced by chronic pre-existing pain but is not sensitive to acute increases in pain, which raises the possibility that masticatory rate could contribute to the maintenance of chronic masticatory muscle pain. If so, recommendations to slow the rate of chewing in TMD patients might be of benefit.

In summary, we found that chewing significantly increased pain in patients with a history of chronic masticatory muscle pain as well as in women with no such history. Moreover, the increased pain persists significantly longer in female patients. These sex differences may be related to the as-yet-largely-unknown factors that result in the disproportionate number of women seeking treatment for chronic facial pain.

	ACKNOWLEDGMENTS

 
We thank Dr. Charles McNeill and Patricia Rudd, PT, for their suggestions and help in the recruitment of patients; Drs. Octavia Plesh and Linda Centore for many helpful suggestions in the design of this study; and Drs. Soh Nakahara, Sen Nakahara, Kazuhiko Ogihara, and Nippon Dental University School of Dentistry at Tokyo for their support of HK. This work was also supported by the Center for Orofacial Pain and the NIH Pain Center (UCSF) at the University of California, San Francisco, California. A preliminary report was presented at the IADR General Session in Chiba, Japan, in 2001 (J Dent Res 80[Spec Iss]:597 [abstract]).

Received February 27, 2002; Last revision October 3, 2002; Accepted October 29, 2002

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