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J Dent Res 83(12):946-950, 2004
© 2004 International and American Associations for Dental Research


RESEARCH REPORTS
Clinical

Endurance during Chewing in Whiplash-associated Disorders and TMD

B. Häggman-Henrikson1,2, C. Österlund1,2, and P.-O. Eriksson1,2,*

1 Department of Odontology, Clinical Oral Physiology, Umeå University, S-901 87 Umeå, Sweden; and
2 Centre for Musculoskeletal Research, Gävle University, Sweden;

* corresponding author, per-olof.eriksson{at}odont.umu.se


   ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
We have previously shown an association between neck injury and disturbed jaw function. This study tested the hypothesis of a relationship between neck injury and impaired endurance during chewing. Fifty patients with whiplash-associated disorders (WAD) were compared with 50 temporomandibular disorders (TMD) patients and 50 healthy subjects. Endurance was evaluated during unilateral chewing of gum for 5 min when participants reported fatigue and pain. Whereas all healthy subjects completed the task, 1/4 of the TMD and a majority of the WAD patients discontinued the task. A majority of the WAD patients also reported fatigue and pain. These findings suggest an association between neck injury and reduced functional capacity of the jaw motor system. From the results, we propose that routine examination of WAD patients should include jaw function and that an endurance test as described in this study could also be a useful tool for non-dental professionals.

KEY WORDS: chewing • endurance • head • neck • whiplash injury


   INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Reduced endurance is one sign of motor dysfunction, and endurance tests can therefore be valuable in the assessment of deranged neuromuscular function. Most studies on the human jaw motor system have used static tests, such as tooth clenching, to evaluate endurance. A relationship has been demonstrated among the intensity of tooth clenching, the onset of fatigue and pain, and endurance time (Christensen et al., 1982; Naeije, 1984; Clark and Adler, 1987; Svensson et al., 2001). Compared with clenching, considerably longer endurance times have been found for chewing (Tzakis et al., 1992; Bakke et al., 1996; Christensen et al., 1996; Farella et al., 2001). Chewing soft chewing gum for 40 min provoked fatigue and pain in few or no healthy females (Bakke et al., 1996), whereas chewing of hard chewing gum for 30 min induced both fatigue and pain in healthy subjects (Tzakis et al., 1992; Farella et al., 2001).

Jaw movements are the result of coordinated activation of jaw and neck muscles, leading to simultaneous movements in the temporomandibular, atlanto-occipital, and cervical spine joints (Eriksson et al., 2000). Thus, jaw function involves integrative jaw and neck motor control. Given that natural jaw function requires a healthy state of both mandibular and neck motor systems, injury to any of the joints involved might derange jaw function. In fact, we have recently shown an association between neck injury and deranged jaw function, as reflected by reduced amplitude, speed, and disturbed coordination of head and mandibular movements (Häggman-Henrikson et al., 2002; Eriksson et al., 2004).

No previous study has evaluated if neck injury can impair endurance during chewing. The aim of the present study was to test the hypothesis of a relationship between neck injury and impaired endurance during chewing. A chewing test was designed to evaluate the endurance of the jaw system in individuals with whiplash-associated disorders (WAD) and, for comparison, in patients with pain and dysfunction and musculoskeletal disorders (i.e., temporomandibular disorders [TMD]) in the jaw-face, and in healthy subjects.


   MATERIALS & METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
Fifty WAD patients were compared with 50 TMD patients and 50 healthy subjects. The patients had been referred to the Department of Clinical Oral Physiology at Umeå University Hospital (Northern Sweden) for assessment and management of longstanding jaw-facial pain and dysfunction, present more than 3 mos. The patients were consecutively examined by one of the authors (POE). Symptoms and signs of jaw-face pain and dysfunction, i.e., TMD, were documented by clinical examination (Okeson and de Kanter, 1996).

For the TMD group, the inclusion criterion was jaw-face pain and dysfunction of muscular origin, Group 1, Axis I, according to Research Diagnostic Criteria (Dworkin and LeResche, 1992). Exclusion criteria were temporomandibular joint disorders and/or history of trauma to the head-neck regions.

The WAD patients were primarily diagnosed by a physician. Typically, after a neck injury, they had developed neck pain, impaired and painful head-neck movements, and tenderness to palpation in neck muscles. The traumas—consisting of motor vehicle accidents (29 females, 11 males) and falls (eight females, two males)—had resulted in a WAD grade II-III according to the Quebec Task Force classification (Spitzer et al., 1995). In this classification, grades 0 and I denote no neck pain, and neck pain but no signs, respectively. Grades II and III denote neck pain with musculoskeletal signs, and neurological signs, respectively, and grade IV denotes neck pain and fracture. For the WAD group, the inclusion criterion was pain and dysfunction in the jaw-face that had developed following the neck injury. The duration between trauma and examination of jaw function was from 1 to 9 yrs (median, 4 yrs) for females, and from 2 to 4 yrs (median, 3 yrs) for males. The exclusion criterion was reported jaw-face pain and dysfunction prior to the head-neck injury (Table 1Go).


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Table 1. Characteristics of Subjects
 
For the healthy group, inclusion criteria were the absence of jaw-face pain and dysfunction after clinical examination, as described above, and no history of head-neck injury. For all groups, the exclusion criterion was general joint or muscle diseases. All participants had given their informed consent according to the World Medical Association’s Declaration of Helsinki and were unaware of the underlying aim of the investigation. The investigation was approved by the Ethics Committee, Umeå University.

Test Procedure
The subjects were comfortably seated in an upright position, with back support up to the mid-scapular level, but without a headrest. They performed unilateral chewing of a standardized bolus (3 x 1 g) of chewing gum (V6®, Stimorol AB, Malmö, Sweden) for 5 min on their preferred chewing side. Subjects were free to discontinue the task at any time if fatigue/pain was intolerable, and this information was incorporated into the data analysis. The subjects were instructed not to talk during the chewing test and to point to the words "fatigue", "stiffness", "weakness", "exhaustion", "ache", and "pain", on a clipboard, if any of these symptoms was experienced. The time point during chewing at which a subject chose a symptom was at the discretion of the individual and was duly noted. The words "fatigue", "exhaustion", "stiffness", and "weakness" were pooled as "fatigue", and "pain" and "ache" were pooled as "pain".

Statistics
For continuous data, we used mean, range, and standard deviation for descriptive statistics. The hypothesis of no differences between groups in (i) fatigue, pain, and endurance and (ii) time for onset of symptoms and failure points was tested by means of (i) the 2x2 chi-square test, and (ii) the Mann-Whitney U test, with a probability level of 0.05.


   RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Participants
WAD and TMD patients were consecutively examined. In the healthy group, the ratio between males and females was 1:1, whereas for both patient groups the ratio for these consecutively examined patients was 1:3. For the healthy group, there was no relationship between age or gender and reported symptoms.

Fatigue and Pain
More subjects in the WAD group reported fatigue and pain compared with both the healthy and TMD groups. Furthermore, these WAD subjects reported an earlier onset of fatigue compared with both healthy (p < 0.001) and TMD subjects (p < 0.001), and an earlier onset of pain compared with TMD subjects (p = 0.034) (Fig.Go).



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Figure. Left panel shows time of onset of symptoms for the subjects in the healthy (n = 50), TMD (n= 50), and WAD (n = 50) groups who reported fatigue (A), or pain (B) and failure point (C) for the subjects who failed to complete the task. Numbers in parenthesis indicate the number of subjects in each group who reported symptoms, and vertical lines indicate median values. Right panel shows percentage of subjects in each group who reported fatigue (D) and pain (E) or who discontinued the task (F). P-values were calculated for group differences by the Chi-square test.

 
Discontinued Task
A majority of WAD subjects discontinued the task, whereas all healthy subjects completed the chewing test (Table 2Go). In addition to discontinuing the task more often than the TMD and healthy groups, the WAD subjects who failed did so at an earlier point in the task than did the TMD subjects who discontinued (p = 0.014) (Fig.Go).


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Table 2. Number of Subjects in Respective Groups Who Either Completed or Discontinued the Chewing Task, and Who Reported Fatigue and/or Pain
 
Gender Differences
Fatigue was reported more often by women than by men in the TMD group (p = 0.006). The women in the WAD group who reported fatigue or pain did so earlier in the task than did the men (p = 0.033 and p = 0.025, respectively). For both the TMD and WAD groups, the women who discontinued the task tended to do so at an earlier point than did the men (Table 3Go).


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Table 3. Group and Gender Differences for Fatigue, Pain, and Endurance
 

   DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In this study, we evaluated the endurance of the jaw motor system in WAD patients using a dynamic loading task. Compared with the healthy and TMD groups, the WAD individuals reported fatigue and pain more often and earlier, and a majority discontinued the chewing task. These results suggest an association between neck injury and impaired jaw function and add to previous data suggesting a tight functional coupling between the jaw and the head-neck motor systems.

The fact that all healthy subjects completed the task, and that very few reported fatigue or pain, is in line with previous reports of no symptoms (Farella et al., 2001), or low frequency of fatigue and pain (Bakke et al., 1996), during the chewing of soft gum. These observations—that the jaw system generally seems to be resistant to fatigue during dynamic loading—are in accord with the fact that jaw-closing muscles are composed of a high proportion of fatigue-resistant (Type I) fibers (Eriksson and Thornell, 1983) and a high density of capillaries (Stål et al., 1996). Moreover, our finding that the TMD patients reported fatigue and pain more often than did healthy subjects corroborates previous reports that fatigue and pain are common symptoms in TMD, and that chewing can increase these symptoms (Dao et al., 1994; Gavish et al., 2002).

It has been reported that almost 25% of TMD patients have a history of trauma to the head-neck, mainly whiplash trauma (De Boever and Keersmaekers, 1996). Compared with TMD patients without a history of trauma, patients with post-traumatic TMD seem to present with more severe jaw-facial pain and dysfunction (De Boever and Keersmaekers, 1996; Goldberg et al., 1996; Kolbinson et al., 1997a), and it has been suggested that the prognosis for recovery from jaw-face pain and dysfunction is lower in this group (Kolbinson et al., 1997b). Furthermore, it has been reported that post-traumatic TMD patients have more symptoms associated with affective disorders, e.g., sleep disturbances (Kolbinson et al., 1997a), respond more poorly in reaction time tests, and overall tire more easily (Goldberg et al., 1996) than do non-traumatic TMD patients. The fact that many of these symptoms are also associated with closed-head injuries indicates that the etiology of post-traumatic TMD differs from that of non-traumatic TMD. Our results corroborate the suggestion that patients with jaw-face pain and dysfunction and with a history of neck injury are unique and more complex with regard to the spread and severity of pain and dysfunction (Goldberg et al., 1996).

It is well-known that females outnumber males in pain clinics. The patients in this study were examined consecutively, and the predominance of females represents the sex difference for patients referred to our department during the study period. All healthy subjects completed the chewing task without age or sex differences for reported symptoms and endurance. However, in the TMD group, women reported fatigue more often than men, and women in the WAD group reported an earlier onset of both fatigue and pain. These results are consistent with indications that, compared with males, females seem to respond earlier to nociceptive input and have a lower pain threshold (Plesh et al., 1998; Wise et al., 2002) and lower pain tolerance (Bragdon et al., 2002; Wise et al., 2002). They also seem to report more pain after tooth-clenching (Plesh et al., 1998) and chewing (Karibe et al., 2003). Our present finding of a reduced endurance indicates a lower functional capacity of the jaw motor system in females, which might contribute to a higher susceptibility for developing more and more severe pain, exhaustion, and dysfunction in the jaw motor system. No conclusive explanation for these sex differences has as yet been reported, either for TMD or for musculoskeletal disorders in other body regions. Thus, many persistent pain conditions have a higher prevalence in females (Unruh, 1996), but the neurobiological mechanisms underlying sex differences are unknown.

Recent studies have proposed that the fusimotor muscle spindle system plays an important role in the development of musculoskeletal pain conditions (Johansson et al., 1999). It has also been shown that reflex connections between chemosensitive muscle afferents and the fusimotor system exist intersegmentally, i.e., between the trigeminal (masseter muscle) and the cervical regions (Hellström et al., 2000). Furthermore, there is support for intersegmental nociceptive connections between the cervical spine and the trigeminal regions (Hu et al., 1993). Analysis of these data, taken together, suggests a tight coupling between the jaw and the neck sensory-motor systems in the onset and spread of pain and dysfunction in the jaw and head-neck regions. Our present results are consistent with these experimental data.

In conclusion, the present finding of a severely reduced endurance during chewing in WAD individuals suggests an association between neck injury and impaired functional capacity of the human jaw motor system. Based on present and previous results, examination of jaw function seems recommendable as part of the routine evaluation of WAD patients, and for this, the endurance test described in this study could be a useful tool. Finally, from data suggesting that jaw function involves simultaneous neuro-muscular activation of movements in the temporomandibular, atlanto-occipital, and cervical spine joints (Eriksson et al., 2000), and that neck injury can disturb natural jaw function (Häggman-Henrikson et al., 2002; Eriksson et al., 2004), we propose that a suitable term for the condition involving both neck and jaw disorders could be "Cervico-Cranio Mandibular Disorders" (CCMD).


   ACKNOWLEDGMENTS
 
This study was supported by the Faculty of Medicine and Odontology, Umeå University, by the Swedish Dental Society, and by The Public Dental Health Service, Västerbotten, Sweden.

Received May 13, 2003; Last revision September 16, 2004; Accepted September 23, 2004


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 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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