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Disturbed Jaw Behavior in Whiplash-associated Disorders during Rhythmic Jaw Movements

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

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

	ABSTRACT

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As shown previously, "functional jaw movements" are the result of coordinated activation of jaw as well as neck muscles, leading to simultaneous movements in the temporomandibular, atlanto-occipital, and cervical spine joints. In this study, the effect of neck trauma on natural jaw function was evaluated in 12 individuals suffering from whiplash-associated disorders (WAD). Spatiotemporal characteristics of mandibular and concomitant head movements were evaluated for three different modes of rhythmic jaw activities: self-paced continuous maximal jaw-opening/-closing movements, paced continuous maximal jaw-opening/-closing movements at 50 cycles/minute, and unilateral chewing. Compared with healthy subjects, the WAD group showed smaller magnitude and altered coordination pattern (a change in temporal relations) of mandibular and head movements. In conclusion, these results show that neck trauma can derange integrated jaw and neck behavior, and underline the functional coupling between the jaw and head-neck motor systems.

KEY WORDS: human • head • mandible • movements • neck • rhythmic • whiplash-associated disorders

	INTRODUCTION

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An overlap in the signs and symptoms of temporomandibular disorders with those of cervical spine disorders has been reported (Browne et al., 1998). Thus, patients with temporomandibular disorders may present with pain and dysfunction in the neck region (Clark et al., 1987; De Wijer et al., 1996b; De Laat et al., 1998; Visscher et al., 2001), and patients with cervical spine disorders with pain and dysfunction in the jaw-face region (Kirveskari et al., 1988; De Wijer et al., 1996a; Ciancaglini et al., 1999). Furthermore, pain and dysfunction in the jaw-face region have been reported in association with whiplash-associated disorders (WAD), i.e., cervical spine disorder following neck trauma (Burgess, 1991; Goldberg, 1999).

Our previous findings of concomitant mandibular and head-neck movements during natural jaw function have allowed us to propose a new concept for natural human jaw function. In this concept, "functional jaw movements" are the result of coordinated activation of jaw as well as neck muscles, leading to simultaneous movements in the temporomandibular, atlanto-occipital, and cervical spine joints (Eriksson et al., 1998, 2000; Zafar et al., 2000a). Given that natural jaw function requires a healthy state for both the mandibular and the head-neck motor systems, injury to any of the joints involved might derange jaw function. The present aim was to study whether neck trauma, leading to pain and dysfunction, can compromise natural jaw function. Using a 3-D wireless opto-electronic recording system (Josefsson et al., 1996), we analyzed spatiotemporal characteristics of mandibular and head movements for three different modes of rhythmic jaw activities in individuals suffering from WAD, and compared these data with data from healthy subjects (Eriksson et al., 2000).

	MATERIALS & METHODS

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Subjects
Ten females and two males (aged 28-50 yrs; median age, 32 yrs) participated in the study. All were referred to the Department of Clinical Oral Physiology, Umeå University Hospital, between 1993 and 1998, for pain and dysfunction in the jaw and neck regions that had developed following neck trauma. The traumas, consisting of motor vehicle accidents (seven females, two males) and falls (three females), had resulted in a WAD class II-III according to the Quebec classification (Spitzer et al., 1995). The duration between trauma and examination was 1 to 9 yrs (median, 2 yrs) for females, and 2 to 4 yrs (median, 3 yrs) for males. Jaw-facial pain and dysfunction were summarized by Helkimo’s anamnestic (Ai) and clinical dysfunction (Di) indices. Ai was II for all individuals and Di was 1 to 3 (median 3). All individuals were tender to palpation in neck muscles, and head movements were impaired and painful. Pain intensity was measured for the jaw-face and for the neck according to a visual analogue scale that was labeled from 0 (no pain) to 10 (worst pain). Pain intensity was rated for "present pain", "least pain", and "worst pain". On average, jaw-face pain was rated 4, 2, and 8, and neck pain 5, 3, and 9, respectively. Data from seven females and five males (aged 23-45 yrs; median age, 26 yrs), free from pain and dysfunction in the craniomandibular and neck regions, were used for comparison (Eriksson et al., 2000). All subjects 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 of the Umeå University.

General Procedure
The participants were seated comfortably in an upright position with back support up to the mid-scapular level but without headrest. Movements of the mandible and the head were simultaneously monitored in 3 dimensions (3D), by means of a wireless opto-electronic recording system with a sampling rate of 50 Hz (MacReflex^®, Sävedalen, Sweden). Movements were recorded by a tripod of markers attached firmly to the skin by trimmed double-sided adhesive tape at the midline of the face at the bridge of the nose (head) and by a single skin-attached marker at the center of the tip of the chin (mandible).

Details of the procedures for off-line data and conditioning were presented previously (Häggman-Henrikson et al., 1998; Eriksson et al., 2000; Zafar et al., 2000b).

Each subject was recorded in 3 standardized motor tasks according to a protocol previously used for healthy subjects (Eriksson et al., 2000): (i) self-paced continuous maximal jaw-opening/-closing movements, (ii) paced continuous maximal jaw-opening/-closing movements in time with a metronome set at 50 beats/min, and (iii) unilateral chewing of 3 pieces of pre-softened chewing gum (weight, 3 g) on the side chosen by the subject. Prior to the start of each recording, the subject was instructed to position the teeth in light contact in the intercuspal position, and this position was used as a reference. Each motor task was recorded twice, each during a 12-second period with an interval of 2 min between recordings.

Definitions
The start of a mandibular movement cycle was defined as the time point at which the mandible began the downward, jaw-opening, movement. The peak was defined as the time point for the most inferior position of the mandible, i.e., at the shift from the jaw-opening phase to the jaw-closing phase. The end of the closing phase was defined as the time point at the end of the upward movement of the mandible. The duration of each cycle (time/cycle) was defined as the time between 2 consecutive start points.

Analysis
The start and peak of each head and mandibular movement cycle were determined, and 3-D movement amplitudes were calculated. The data from the 2 repeated tests were pooled, and estimates were based on the data from 8 movement cycles (4 consecutive cycles from each test). The first cycle in all tests was also analyzed separately. For the 2 continuous maximal jaw-opening/-closing tasks, the start and the peak of each head movement cycle were analyzed with reference to the start and the peak of the corresponding mandibular movement cycle. The effects of the head movements on the recorded mandibular movements were compensated for mathematically. Details of analysis and calculations have been presented previously (Häggman-Henrikson et al., 1998; Eriksson et al., 2000; Zafar et al., 2000b).

Statistical Analysis
Intra-individual (cycle-to-cycle) variability was described by means of coefficient of variation for movement amplitudes, variance for time points, and also as a spatiotemporal index (Zafar et al., 2002). This index was calculated for mandibular movements in relation to the head, head movements, and mandibular movements in space (the combined movement of the mandible and the head). Low index values indicate high spatiotemporal consistency. Mean, range, and standard deviation were used for descriptive statistics. Differences between motor tasks and sessions and between the WAD group and the healthy group were tested with the Wilcoxon matched-pairs test and Mann-Whitney U-test, respectively, with a probability level of 0.05.

	RESULTS

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At the start of the first mandibular movement cycle, there was an initial change in head position, an "initial head extension". Compared with the healthy subjects, the WAD group had smaller initial head extension for the paced continuous jaw-opening/-closing task. In addition to the prevailing head extension, head extension-flexion movements were seen during the 2 maximal continuous jaw-opening/-closing tasks. Some WAD subjects showed very limited and irregular head movement patterns (Fig. 1).

View larger version (18K): [in this window] [in a new window]   Figure 1. 3-D mandibular (hatched line) and head (solid line) movement amplitudes during a sequence of paced continuous maximal jaw-opening/-closing cycles for a healthy subject (from Eriksson et al., 2000) and a WAD patient.

View larger version (23K): [in this window] [in a new window]   Figure 2. Box and whisker plots (median, quartiles, and range) of initial head extension, head movements, and mandibular movement amplitudes for healthy (unfilled boxes, from Eriksson et al., 2000) and WAD (hatched boxes) subjects for the different tasks; continuous maximal jaw-opening/-closing movements at self-paced rate (Cont), at a rate of 50 cycles per min (Cont 50), and during chewing (Chew).

For the 2 continuous jaw-opening/-closing tasks, the start and the peak of each head movement cycle were analyzed with reference to the start and the peak of the corresponding mandibular movement cycle. For the WAD group, at the first mandibular movement cycle, the head movement started after the mandible for both the self-paced (0.04 sec) and the paced (0.02 sec) movements. For the subsequent mandibular movement cycles, the head preceded the mandibular movement for both the self-paced (0.02 sec) and the paced (0.01 sec) movements. At the peak of the mandibular movement, the head lagged behind the mandible for both the self-paced (0.02 sec) and the paced (0.03 sec) movements. Thus, compared with the healthy group, the WAD group had a delayed start of the head movement in relation to mandibular movement (Fig. 3). Due to relatively small head movements during chewing, temporal relations between head and mandibular movements could not be systematically analyzed for this task.

View larger version (21K): [in this window] [in a new window]   Figure 3. Box and whisker plots (median, quartiles, and range) of time points of head movement in relation to reference mandibular time points (vertical hatched line on zero position of the x- axis) for healthy (unfilled boxes, from Eriksson et al., 2000) and WAD subjects (hatched boxes) for the defined time points: at the start of the mandibular movement cycle 1 (Start 1) and cycles 2-4 (Start 2-4), and at the peak of mandibular movement (Peak) for the self-paced (Cont) and paced (Cont50) continuous jaw movement cycles. Negative sign (-) on the x-axis indicates head movement before mandibular movement.

	DISCUSSION

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From previous studies, we have concluded that natural jaw function relies on simultaneous movements in the temporomandibular, atlanto-occipital, and cervical spine joints (Eriksson et al., 2000). Neck trauma, leading to pain and dysfunction, can therefore be expected to compromise jaw function. This suggestion is supported by the present finding of smaller amplitudes of both mandibular and head movements for the WAD group, compared with healthy subjects. Due to this marked reduction in head movement amplitudes, the ratio between head and mandibular movement amplitudes was smaller than for healthy subjects. This ratio reflects the positioning of the middle of the gape in space with reference to the start position. Therefore, the small ratio for the WAD group indicates a "faulty", too low, positioning of the gape after a neck trauma, which in turn may hamper optimal jaw activities. Another indication of impaired head movement during jaw function was the smaller initial head extension in the WAD group for the self-paced opening-closing movements. A sufficient head positioning will favor the biomechanical relations for jaw activities, and hence facilitate optimal mandibular movements and force production. This interpretation is corroborated by the finding in man that extension of the head will result in an increase in maximum bite force (Hellsing and Hagberg, 1990) and in stability of mandibular closing movements (Yamada et al., 1999).

Compared with healthy subjecs, the WAD group had smaller mandibular and head movement amplitudes for the continuous opening-closing tasks, but similar durations of total cycle time. This means that both mandibular and head movements were performed with a lower angular velocity, i.e., lower speed for the WAD group. Furthermore, the finding that the head lagged behind the mandible at the start of the first movement cycle reflects the fact that the anticipatory, "feed forward", positioning of the head seen in healthy subjects (Eriksson et al., 2000) was disturbed. In addition, compared with healthy subjects, the WAD group showed higher cycle-to-cycle variability of (i) head movement amplitudes and (ii) coordination of mandibular and head movement time points. This indicates an instability in the control of the integrated jaw-neck behavior in the WAD group. However, the spatiotemporal index for the mandibular movements in space, i.e., the combined movement of the mandible and the head, did not show any divergence as compared with that in healthy subjects. This notable finding may reflect an ability of the jaw-neck motor system to compensate for the instability in head-neck behavior to ensure an invariant, albeit "faulty", jaw function.

Pain is probably a significant explanatory factor of the present findings of disturbed jaw function in the WAD group. It is known that trigeminal nociceptive input to the brain stem can reduce amplitude and speed of mandibular movements (Lund et al., 1991; Stohler, 1999; Svensson and Graven-Nielsen, 2001). Moreover, the fusimotor muscle spindle system has been proposed to play an important role in the development of musculoskeletal pain conditions (Johansson et al., 1999), and such a mechanism seems to exist also in the jaw system (Capra and Ro, 2000; Ro and Capra, 2001). Notably, it has recently been shown that reflex connections between chemosensitive muscle afferents and the fusimotor system also exist intersegmentally, i.e., between the trigeminal and cervical regions (Hellström et al., 2000). Support for an intersegmental cervico-trigeminal pain connection has been reported previously (Hu et al., 1993). Taken together, these data suggest a tight coupling between the jaw and neck sensory-motor systems for onset and spread of pain and dysfunction in the jaw and head-neck regions.

In conclusion, our results suggest that trauma to the neck region, leading to whiplash-associated disorders, can disturb natural jaw activities. The results underline the concept of a functional integration between the mandibular and the head-neck motor systems during jaw function.

	ACKNOWLEDGMENTS

 
The skillful technical assistance of Mr. Jan Öberg and the programming assistance of Mr. Mattias Backén are gratefully acknowledged. This study was supported by the Umeå University Faculty of Odontology, the Swedish Dental Society, and Trygg-Hansa.

Received September 26, 2001; Last revision June 25, 2002; Accepted August 9, 2002

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