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Sex Differences in Masticatory Muscle Pain after Chewing
1 Center for Orofacial Pain, Correspondence: *corresponding author, rwg{at}itsa.ucsf.edu
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
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.
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.
Chewing Test The chewing test consisted of 6 min of unilateral chewing of one piece of bubble gum (8 g, Bazooka, Topps Company, New York, NY, USA).
Outcome Variables
Range of Motion
Rate of Mastication
Data Analysis
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
Chewing-induced Pain
Control Subjects Females experienced a significantly greater increase in pain during chewing than did males (Fig. 1A ; sex x time interaction, F (6.204) = 5.5, p = 0.01). The main effect of time was also significant (F (6.204) = 18.0, p < 0.001). Post hoc simple main effects were used to determine at which time points the significant differences occurred; for these analyses, a Bonferroni-type correction was applied such that the alpha level was set at p = 0.008 (i.e., 0.05 ÷ 6). Pain for females was significantly greater than for males after the fifth and sixth minutes of chewing (DF 1.83; F = 8.1, p = 0.006; and F = 14.5, p < 0.001, respectively).
Patients
Post-chewing Pain
Control Subjects Post-chewing pain scores did not differ significantly from pre-test scores at any time point, indicating recovery within 1 hr for both females (Fig. 1A ) and males (Fig. 1B).
Patients
Effect of Chewing on Range of Motion
Rate of Mastication
In this study, we confirmed that chewing exercise can increase masticatory muscle pain in patients as previously shown (Dao et al., 1994; Gavish et al., 2002); however, in contrast to previous studies, we found a similar result in female control subjects. While there was no sex difference in patients, there was a highly significant sex difference in control subjects. 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 ( 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.
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 for publication February 27, 2002. Revision received October 3, 2002. Accepted for publication October 29, 2002.
Journal of Dental Research, Vol. 82, No. 2,
112-116 (2003) This article has been cited by other articles:
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ABSTRACT
INTRODUCTION
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 (
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 (
