This is the published version of a paper published in Journal of Oral Rehabilitation.
Citation for the original published paper (version of record):
Eklund, A., Wiesinger, B., Lampa, E., Österlund, C., Wänman, A. et al. (2020) Jaw-neck motor function in the acute stage after whiplash trauma
Journal of Oral Rehabilitation, 47(7): 834-842 https://doi.org/10.1111/joor.12981
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834 | wileyonlinelibrary.com/journal/joor J Oral Rehabil. 2020;47:834–842.
Received: 22 December 2019
|Revised: 29 March 2020
|Accepted: 2 April 2020 DOI: 10.1111/joor.12981
O R I G I N A L A R T I C L E
Jaw-neck motor function in the acute stage after whiplash trauma
| Birgitta Wiesinger1,2
| Ewa Lampa1
| Catharina Österlund1
| Anders Wänman1
| Birgitta Häggman-Henrikson1,3
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2020 The Authors. Journal of Oral Rehabilitation published by John Wiley & Sons Ltd The peer review history for this article is available at https://publo ns.com/publo n/10.1111/joor.12981 1Department of Odontology, Clinical Oral
Physiology, Faculty of Medicine, Umeå University, Umeå, Sweden
2Department of Research and Development, Umeå University, Sundsvall, Sweden
3Department of Orofacial Pain and Jaw Function, Faculty of Odontology, Malmö University, Malmö, Sweden
Anton Eklund, Department of Odontology, Clinical Oral Physiology, Umeå University, Umeå SE-901 87, Sweden.
Email: email@example.com Funding information
Västerbotten County Council (TUA);
Swedish Dental Society
Background: Jaw-neck motor function is affected in the chronic stage following whiplash trauma. It is not known whether motor function is affected also in the early stage after neck trauma.
Objectives: To determine how jaw and head movement amplitudes and movement cycle times correlate with jaw and neck pain, and neck disability in the acute stage after whiplash trauma.
Methods: Jaw and head movements during jaw opening-closing were recorded with an optoelectronic system in 23 cases (4 men, 19 women, 18-66 years) within 1 month after whiplash trauma and compared with 27 controls without neck trauma (15 men, 12 women, 20-66 years). Jaw and head movement amplitudes, head/jaw ratio (quotient of head and jaw movement amplitude) and movement cycle times were evaluated in relation to jaw and neck pain (Numeric Rating Scale) and neck disability (Neck Disability Index). Analyses were performed with Mann-Whitney U test and Spearman's correlation.
Results: Compared with controls, cases showed smaller jaw movement amplitudes (P = .006) but no difference in head movement amplitudes, head/jaw ratios or move- ment cycle times. There were no significant correlations between movement ampli- tudes or cycle times and jaw and neck pain, and neck disability. Cases with high neck pain intensity had smaller jaw movement amplitudes compared to cases with low neck pain intensity (P = .024).
Conclusion: The results suggest that jaw-neck motor function may be affected in the acute stage after whiplash trauma and more so in cases with higher neck pain intensity.
K E Y W O R D S
jaw, motor activity, movements, neck, pain, whiplash injury
1 | INTRODUCTION
It is well known that normal jaw function is composed of coordinated movements of the jaw and head-neck.1-3 In individuals without pain and dysfunction in the jaw and neck regions, jaw movements are facilitated by concomitant head movements during natural jaw func- tion. When performing a sequence of continuous maximum jaw opening-closing cycles, the head remains in a slightly extended po- sition after the end of the first movement cycle.1 Subsequent head movements originate from this extended head position, with addi- tional head extension during jaw opening and head flexion during jaw closing. Furthermore, this interrelationship between the jaw and head movements is affected by the magnitude and speed of jaw movements. Thus, head movements increase with larger jaw opening and head movements decrease with smaller jaw opening and with faster jaw movement cycles, demonstrating a strong func- tional coupling between the jaw and neck motor systems during jaw function.1,2 This functional connection is modified not only by the type of motor task performed, but also by peripheral input,3 which underlines the sensorimotor integration between the jaw and neck regions.
The term whiplash describes a consequence of a collision or other trauma that incorporates a sudden change in velocity of the head and neck from acceleration to deceleration.4 The incidence of whiplash trauma is about 2 per 1000 individuals per year,5 and the trauma can result in a range of symptoms. These various symptoms are embraced by the term whiplash-associated disorders (WAD), with neck pain and neck disability as the cardinal symptoms.6 Although many individuals will recover from a whiplash trauma, one in two will also report symptoms 1 year after trauma.7 According to the International Association for the Study of Pain (IASP), pain can be divided into acute and chronic, with pain persisting longer than 3 months defined as chronic8—this time limit can be applied also to pain after whiplash trauma. Several reviews identify higher levels of neck pain and neck disability shortly after the trauma as risk factors for a poor outcome.7,9,10
In addition to lingering neck pain and neck disability following whiplash trauma, effects on the jaw-neck motor function have been reported. Thus, changes in the amplitude and coordination between jaw and head movements during jaw opening-closing have been observed in individuals with chronic WAD. Compared to individ- uals without pain in the jaw or neck regions, patients with chronic WAD displayed smaller head and jaw movement amplitudes during a repeated jaw opening-closing task and with a smaller relative con- tribution of head movement. Moreover, compared to individuals without a history of neck trauma, head extension for chronic WAD patients was initiated later relative to jaw opening, thus indicating a disturbed coordination.11 In addition, the movement velocity was slower,11,12 and endurance during chewing was reduced,13 which indicates a lower capacity of the jaw-neck motor system. Taken to- gether, a range of differences in the jaw and neck motor function has been reported in individuals with chronic WAD compared to individuals without a history of neck trauma.
As described above, the motor function of the jaw and neck during jaw function has been studied in patients with chronic pain and disability after whiplash trauma,11,12 but it has not been examined in the acute stage. It is therefore not known whether the changes in jaw-neck motor function demonstrated in chronic WAD are absent, developing or are already evident in the acute stage after whiplash trauma. Given that recent studies have sug- gested early symptoms from the oro-facial region such as jaw pain14 and fatigue and pain during chewing,15 it is reasonable to assume that the integrated jaw-neck motor function could be af- fected in the acute stage after whiplash trauma. Therefore, the hypothesis of the present study was that jaw-neck motor function during jaw activities is affected already in the acute stage after whiplash trauma.
The aims of the present study were to determine how jaw and head movement amplitudes and movement cycle times correlate with jaw and neck pain, and neck disability in the acute stage after whiplash trauma.
2 | MATERIALS AND METHODS 2.1 | Study population
The study population was a subsample from a larger cohort that compared individuals after a recent whiplash trauma (cases) to a control group (controls). Cases were recruited through the Injury Data Base at Umeå University Hospital (Umeå, Sweden), and controls were recruited from the general population by advertis- ing.14,15 Participants in the present study were examined between 21 December 2010 and 5 February 2016. Inclusion criteria for both cases and controls were as follows: being a resident in the municipality of Umeå; age 18-70 years, and understanding of the spoken and written Swedish language. For cases, an additional in- clusion criterion was a diagnosis of neck distortion (ICD-10 S134) by a physician within 72 hours after a whiplash trauma from a car accident. Exclusion criterion for cases was WAD classified as grade IV (fracture) according to the Quebec Task Force classification sys- tem4 and for controls was a history of neck trauma. The availability of the subsample in the present study was based on access to the movement recording facilities on the day of the clinical examina- tion in the main study. The researcher was blinded to group alloca- tion (case or control) and the scheduling of the examination was carried out by a dental nurse. The final subsample consisted of 23 cases (4 men, 19 women, 18-66 years) and 27 controls (15 men, 12 women, 20-66 years) (Table 1).
All participants were examined at the Department of Clinical Oral Physiology, University Hospital of Umeå. Cases were examined within 1 month after being diagnosed at the Emergency Department at Umeå University Hospital, and controls were evaluated at avail- able examination times. The study was conducted according to the Declaration of Helsinki and approved by the Regional Ethical Review Board in Umeå (Dnr 2010-156-31M). Participation was voluntary,
and written informed consent was obtained. The subjects were given written and oral information and they could withdraw their participation at any time.
2.2 | Questionnaires
Before the movement recordings, all participants filled in the follow- ing questionnaires:
The Numeric Rating Scale (NRS) for assessing current pain in- tensity separately in the neck and the jaw regions. The NRS is an 11-graded scale with endpoints 0 denoting no pain and 10 denoting worst possible pain.
From the 3Q/TMD,16 two screening questions for assessing pain in the oro-facial area.17 Question 1 (Q1): Do you have pain in your temple, face, jaw or jaw joint once a week or more? Question 2 (Q2):
Do you have pain when you open your mouth wide or chew once a week or more?
Neck Disability Index (NDI) to quantify how daily life is affected by neck pain and impaired neck function. The NDI score ranges be- tween 0 and 50 and is presented as percentages (0%-100%), with this earlier proposed division: 0-8 = no disability, 10-28 = mild, 30-48 = moderate, 50-68 = severe and 70-100 = complete disability.18
The Symptom Checklist-90-Revised (SCL-90-R) from axis II of Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD) to evaluate psychosocial symptoms.19 The SCL-90-R standardised questionnaire is constructed as a 5-point Likert type- scale with a total of 32 questions that include non-specific physi- cal symptoms (12 items), non-pain physical symptoms (7 remaining items after removing the 5 pain-related questions) and the depres- sion scale (20 items). SCL-90-R scales provide cut-off values for nor- mal, moderate and severe symptoms, based on normative values of the general population.19
2.3 | Test procedure
Participants performed a jaw opening-closing task where jaw and head movements were recorded with an optoelectronic movement recording system. During the recordings, the participants were seated with back support but without a headrest. The back of the chair was vertically aligned and reached approximately the upper two-thirds of the thoracic spine, thus providing support for the lower part of the back. Information about this experimental set-up is provided in previous studies.1,2,11
Standardised verbal information about the jaw opening-closing task was provided to all participants prior to the movement record- ings by one of two researchers (EL or CÖ) who were blinded to the group allocation. The task was to perform self-paced continuous maximum jaw opening-closing movements from a starting position with the teeth in light contact (intercuspal position). Verbal com- mands were used to indicate the start and the stop of the task. Each recording lasted 25 seconds and was repeated once after a 2-minute resting period. Only the second movement recording was analysed since the first recording was intended as a learning trial.
In this double-blind study, the researchers responsible for the movement recordings (EL and CÖ) and movement analysis (AE) were blinded to group allocation. Before the start of the analysis of the movement recordings, the researcher responsible for the movement analysis (AE) was calibrated with another researcher that was expe- rienced in movement analysis (BH-H).
2.4 | Movement recordings
Head and jaw movements were recorded using a wireless opto- electronic movement recording system (MacReflex®; Qualisys, Gothenburg, Sweden) constructed for tracking changes in spatial 3D-positions of retroreflective markers (Ø 5 mm). The system has a high resolution,20 and the performance of the system's two cameras TA B L E 1 Demographic characteristics, neck disability, neck
pain, jaw pain, and psychosocial symptoms
Cases vs Controls P-value
Total n 23 27
Age (y) mean (SD) 36 (15) 32 (12) .482
Neck disability, NDI median (IQR)
16 (20) 2 (4) <.001
Neck pain, NRS median (IQR)
2 (3) 0 (1) <.001
Jaw pain, NRS median (IQR)
1 (1) 0 (0) <.001
Q1 positive n (%) 11 (48%) 2 (7%) .003
Q2 positive n (%) 5 (22%) 1 (4%) .082
Physical symptoms median (IQR)a
0.83 (1.17) 0.25 (0.42) <.001
median (IQR)b 0.71 (1.14) 0.14 (0.43) .006 Depression median
0.75 (1.02) 0.45 (0.65) .099
Note: Bold values indicate significant difference between groups.
SD = standard deviation; IQR = interquartile range; NDI = Neck Disability Index (0%-100%). NRS = Numerical Rating Scale (0-10);
Screening questions for oro-facial pain 3Q/TMD. Q1: Do you have pain in your temple, face, jaw or jaw joint once a week or more? Q2: Do you have pain when you open your mouth wide or chew once a week or more? SCL-90-R = Symptom Checklist-90-Revised
aCut-off values: normal < 0.500, moderate 0.500 to < 1.000, severe ≥ 1.000.
bCut-off values: normal < 0.428, moderate 0.428 to < 0.857, severe ≥ 0.857.
cCut-off values: normal < 0.535, moderate 0.535 to < 1.105, severe ≥ 1.105.
at 50 Hz provides an accuracy in spatial resolution of 0.02 mm with a recording dimension of 45 cm * 55 cm * 50 cm. A tripod with three markers was attached to the skin with double-sided adhesive tape on the bridge of the nose and a single marker to the tip of the chin.
This marker placement on the facial skin can provide adequate reg- istration of the relative movements of the head and the jaw dur- ing natural jaw function.1,11,21 The data of the individual markers' 3D-positions were extracted and controlled for correct marker identification and intact recordings of 3D-positions, according to the same procedure as in previous studies.1,21 Further analysis was carried out using dedicated software.
In April 2016, a camera failure was detected which meant that all movement recordings from 13 November 2015 until 5 February 2016 could not be used for analysis. During this time period, movement re- cordings of 4 cases and 7 controls were performed; therefore, these data were excluded. Recordings from two additional controls carried out in April 2012 and June 2012 were excluded due to missing marker information. Thus, the original subsample that consisted of 27 cases (8 men, 19 women, mean 36 years, 18-66 years) and 36 controls (20 men, 16 women, mean 31 years, 20-66 years) resulted in a final sub- sample of 23 cases (4 men, 19 women, mean 36 years, 18-66 years) and 27 controls (15 men, 12 women, mean 32 years, 20-66 years).
2.5 | Definitions
The start of a mandibular movement cycle was defined as the time point at which the mandible began the downward jaw-opening move- ment. The peak was defined as the time point for the most inferior position of the mandible, that is, at the shift from jaw-opening phase to the jaw-closing phase (Figure 1). The end of the closing phase was defined as the time point at the end of the upwards movement of the mandible.1 The corresponding head movement amplitude was defined as the distance between the most inferior and superior posi- tion of the head within the jaw opening-closing phase. The move- ment cycle time was defined as the time (s) elapsed between the start of two subsequent jaw opening-closing cycles. Head/jaw ratio was defined as the quotient of head and jaw movement amplitudes.
2.6 | Analyses
To determine the absolute movements of the lower jaw in relation to the head, mathematical adjustments were made for positional changes of the lower jaw marker as a result of concomitant head movements, with a procedure used in earlier studies.2,22 Spatial vec- tors were calculated between the 3D-positions at the start and peak of each movement cycle and were presented as head and jaw move- ment amplitudes.
Two movement recordings were performed for each subject;
the first recording was a learning trial not used for analysis, and the second recording was used for analyses and calculation of the arithmetic mean values of jaw and head movement amplitudes of
the first eight movement cycles and cycle time for the first seven jaw movement cycles. Fewer than eight jaw and head movement amplitudes and seven movement cycles were registered within the 25-second time frame for 12 subjects, 6 cases (26%) and 6 controls (22%). For these recordings, the arithmetic mean was calculated for the recorded number of cycles.
2.7 | Statistics
Descriptive data are presented as median and interquartile range.
For comparison of group differences with respect to distribu- tion of men and women and for the two questions from 3Q/TMD Fischer's exact test was performed. Mann-Whitney U test was used for evaluation of group differences in jaw and head move- ment amplitudes, head/jaw ratio, jaw opening-closing movement cycle times, neck disability (NDI), neck and jaw pain (NRS), age and the subscales from the SCL-90-R. Correlations were analysed separately within groups with Spearman´s correlation for move- ment amplitude and movement cycle time in relation to jaw pain (NRS), neck pain (NRS) and neck disability (NDI). For the case F I G U R E 1 A, Schematic illustration of maximum jaw opening- closing movements. B, Definitions of head and jaw movement amplitudes and movement cycle time. Jaw movements were mathematically compensated for concurrent head movements [Colour figure can be viewed at wileyonlinelibrary.com]
group, a post hoc subgroup analysis was conducted with the Mann-Whitney U test for individuals with higher neck pain inten- sity (NRS ≥ 4) compared to those with lower neck pain intensity (NRS < 4) with regard to movement amplitudes. For all statistical tests, the probability level was set to P < .05.
3 | RESULTS
3.1 | Demographic characteristics, pain ratings and psychosocial symptoms
The demographic characteristics and pain ratings were con- ducted before the movement recordings and are presented in Table 1. There was no age difference between groups (P = .482), but there was a higher proportion of women among cases and a higher proportion of men among controls (P = .008). More cases than controls reported pain in the temple, face, jaw or jaw joint once a week or more (Q1; 48% vs 7%, P = .003); however, there was no significant difference between the groups for pain during jaw function (Q2; cases 22% vs controls 4%, P = .082). Cases re- ported higher jaw and neck pain intensity and higher neck disabil- ity scores (all P < .001). The proportion of individuals reporting no neck pain (NRS = 0) was 13% for cases and 74% for controls. The corresponding percentages for no jaw pain (NRS = 0) were 43% for cases and 96% for controls. The cases also reported higher scores for non-specific physical symptoms (P < .001) and non-pain physi- cal symptoms (P = .006) compared to controls. There was no sig- nificant difference between the groups for depression symptoms (P = .099) (Table 1).
3.2 | Movement amplitudes and head/jaw ratio
Cases had significantly smaller jaw movement amplitudes (50.8 mm, IQR 18.3) during maximum jaw opening-closing com- pared to controls (62.6 mm, IQR 13.4, P = .006). There was no significant difference between cases and controls for head move- ment amplitudes (4.3 mm, IQR 4.2 vs 6.6 mm, IQR 5.9, respec- tively, P = .136) (Figure 2).
When men and women were analysed separately, male cases had smaller jaw movement amplitudes (50.0 mm, IQR 20.9) compared to male controls (63.7 mm, IQR 7.7, P = .02), whereas there was no significant difference in jaw movement amplitudes between female cases (51.5 mm, IQR 18.3) and female controls (56.5 mm, IQR 19.7, P = .484). For head movement amplitudes, there were no significant differences between male cases (5.3 mm, IQR 10.7) and male con- trols (7.7 mm, IQR 15.8, P = .885) or between female cases (4.2 mm, IQR 4.3) and female controls (6.3 mm, IQR 3.8, P = .326).
There was no significant difference in the head/jaw ratio be- tween cases and controls (0.11, IQR 0.07 vs 0.11, IQR 0.08, P = .690).
Post hoc tests showed that cases with higher neck pain intensity (NRS ≥ 4, n = 6) had significantly smaller jaw movement amplitudes
(39.6 mm, IQR 26.7) compared to cases with low neck pain intensity (NRS < 4, n = 17) (53.5 mm, IQR 14.6, P = .024) (Figure 3). For head movement amplitudes, there was no significant difference between cases with high versus low neck pain intensity (3.1 mm, IQR 3.6, vs 6.2 mm, IQR 3.9; P = .101) (Figure 3).
Male controls showed significantly larger jaw movement ampli- tudes (63.7 mm, IQR 7.7) compared to female controls (56.5 mm, IQR 19.7, P = .025), while male cases (50.0 mm, IQR 20.9) and fe- male cases (51.5 mm IQR 18.3, P = .907) showed no difference in jaw movement amplitudes. There were no differences in head move- ment amplitudes between male controls (7.7 mm, IQR 15.8) and fe- male controls (6.3 mm, IQR 3.8, P = .399), or between male cases (5.3 mm, IQR 10.7) and female cases (4.2 mm, IQR 4.3, P = .366).
F I G U R E 2 Jaw and head movement amplitudes (mm) for cases (n = 23) and controls (n = 27) during maximal jaw opening-closing movements. The box plots illustrate the medians, interquartile ranges and the 10th and 90th percentiles. Dots represent values outside the 10th and 90th percentiles [Colour figure can be viewed at wileyonlinelibrary.com]
F I G U R E 3 Jaw and head movement amplitudes (mm) for cases (n = 23) in relation to neck pain intensity on the numeric rating scale (NRS) during maximal jaw opening-closing movements. Pain intensity of <4 was reported by n = 17 and ≥4 by n = 6. The box plots illustrate the medians, interquartile ranges and the 10th and 90th percentiles. Dots represent values outside 10th and 90th percentiles [Colour figure can be viewed at wileyonlinelibrary.com]
3.3 | Movement cycle time
There was no significant difference between cases and controls for the jaw opening-closing movement cycle time; the median cycle time for cases was 2.44 s (IQR 1.63) and for controls was 2.13 s (IQR 1.35) (Figure 4).
3.4 | Correlation
There were no significant correlations between jaw or head move- ment amplitudes and cycle times and jaw pain, neck pain or neck disability (Table 2).
4 | DISCUSSION
This study indicates that jaw opening-closing movements are affected in the acute stage after whiplash trauma, and more so in individuals with a high intensity of neck pain. These interpretations are based on smaller jaw opening amplitudes in cases with whiplash trauma compared to in- dividuals with no history of neck trauma and that cases with higher neck pain intensity had significantly smaller jaw movement amplitudes com- pared to cases with low neck pain intensity. On a group level, however, no correlations between movement amplitudes of the jaw and head in relation to jaw or neck pain intensity, or to neck disability, were observed.
Pain can alter muscle activity and the coordination of synergist and antagonist muscles and thereby interfere with normal move- ment patterns.23 With regard to the effect from pain in the cervical area on motor control, experimentally induced pain in the splenius capitis and the sternocleidomastoid muscle was shown to affect the activity of neck muscles during isometric flexion and extension.24 During head-neck flexion, injection of hypertonic saline in splenius capitis led to decreased activity of the injected muscle as well as of
the sternocleidomastoid muscle bilaterally; furthermore, pain induc- tion in the sternocleidomastoid muscle resulted in decreased muscle activity bilaterally of the sternocleidomastoid, splenius capitis and trapezius muscles. During head-neck extension, hypertonic saline injection in the splenius capitis resulted in decreased activity of the injected muscle and increased activity of the trapezius bilaterally, whereas pain induction in the sternocleidomastoid only reduced muscle activity of the injected muscle.24 Experimental pain induc- tion in the masseter muscle affected both masseter and temporal muscle activity during chewing, with a higher activity during jaw opening and reduced activity during the jaw closing.25 In a natural head position, experimental pain induction in the masseter was as- sociated with ipsilateral increase in muscle activity of the masseter, sternocleidomastoid and splenius capitis muscles, while maximal jaw clenching resulted in decreased muscle activity of the masseter bi- laterally and the ipsilateral sternocleidomastoid muscle.26 In previ- ous studies, we have investigated the motor function of the jaw and neck during a jaw opening-closing task following experimental pain induction in the masseter muscle. The movements of the neck were affected, resulting in increased head movement amplitudes, thus in- dicating that masseter pain can affect the strategy for the integrated jaw-neck motor behaviour.27,28 Taken together, painful stimuli in the trigeminal and cervical areas can affect the muscle activity of both the jaw and neck motor systems.
For patients with chronic pain and dysfunction following whip- lash trauma, a range of differences with regard to motor function has been reported, compared to individuals without a neck trauma.
Individuals with chronic WAD had smaller maximal neck move- ments compared to individuals with idiopathic neck pain, and in- dividuals without neck pain.29 Furthermore, compared to healthy individuals, individuals with chronic WAD showed disturbed
F I G U R E 4 Movement cycle time (s) for cases (n = 23) and controls (n = 27) during maximal jaw opening-closing movements. The box plots illustrate the medians, interquartile ranges, and the 10th and 90th percentiles. Dots represent values outside 10th and 90th percentiles [Colour figure can be viewed at wileyonlinelibrary.com]
TA B L E 2 Correlation between jaw and head movement amplitudes, movement cycle time and neck pain (NRS), jaw pain (NRS) and neck disability (NDI) for cases (n = 23) and controls (n = 27), respectively
ra P-value ra P-value Jaw amplitude vs neck pain −.377 .076 −.112 .578 Jaw amplitude vs jaw pain −.225 .301 −.277 .162 Jaw amplitude vs neck
disability −.326 .129 −.027 .895
Head amplitude vs neck pain −.379 .075 −.150 .454 Head amplitude vs jaw pain −.368 .084 −.277 .162 Head amplitude vs neck
−.311 .148 −.072 .722
Cycle time vs neck pain .309 .151 −.136 .500
Cycle time vs jaw pain .326 .129 .000 1.000
Cycle time vs neck disability .313 .145 −.190 .342 Note: NRS = numeric rating scale (0-10); NDI = Neck Disability Index (0%-100%).
sensorimotor control during neck movements,30,31 disturbed head- eye coordination,32,33 reduced neck muscle strength34,35 and central hyperexcitability.36
Reduced jaw movement amplitudes after whiplash trauma could be related to pain. This is paralleled by experimental studies showing smaller maximal jaw opening after pain induction in the trapezius muscle,37 altered jaw movements after pain induction in the mas- seter muscle38 and altered jaw and neck muscle activity after pain induction in the masseter and splenius capitis muscles.25,26 It was also demonstrated in animal studies that the trigeminal subnucleus caudalis receives nociceptive input from different trigeminally and spinally innervated areas.39 The close neural interaction between the neck and jaw area is exemplified by findings that the jaw open- ing reflex was easier to trigger in mice under noxious stimuli of the semispinal muscle40 and that the sensitivity of muscle spindles in the neck was altered after noxious injection in the temporomandibular joint in cats.41 Furthermore, noxious stimuli of paraspinal tissues increased electromyography (EMG) activity of neck muscles in rats and the increase was positively associated with muscle length.42 Injection of nerve growth factor (NGF) has been shown to induce sensitisation of nociceptors in rats thereby lowering the threshold for signalling upon mechanical stimuli. The sensitisation process is thought to be associated with effects on the N-methyl-d-aspartate (NMDA) receptor through NGF receptor signalling.43 Therefore, the mechanical stimuli by movements could possibly increase action po- tentials from sensitised nociceptors.
The smaller jaw movements found in the present study could also be related to avoidance behaviour and fear of movement; these are known psychosocial factors that can affect motor function.44 Even in the absence of pain, or when pain is of low intensity, re- duced mobility of the head-neck can affect the capacity of the jaw motor system. We previously reported that fixation of the head in healthy individuals without neck pain reduced the amplitude of jaw movements during a maximum jaw opening-closing task.45 In indi- viduals with chronic WAD, we previously demonstrated decreased head and jaw movement amplitudes and decreased head-jaw ratio during maximal jaw opening-closing in comparison to pain-free in- dividuals.11,12 In the present study, male cases, compared to men without a neck trauma, showed smaller jaw movement amplitudes already in the acute stage after whiplash trauma. This is in line with impaired chewing function reported in the acute stage after whip- lash trauma15; furthermore, the chewing capacity was related to the degree of neck disability. Thus, individuals with a higher degree of neck disability reported more fatigue and pain during chewing.15 Taken together, these findings suggest early changes in motor func- tion following whiplash trauma that affect the capacity of the jaw motor system.
For head-neck movements, it has been shown that whiplash trauma can affect neck motor function already in the acute stage, as evidenced by a smaller cervical range of motion,46,47 altered EMG ac- tivity of the sternocleidomastoid muscle and impaired positioning of the neck compared to a control group.47,48 It has also been reported that reduced neck movements in the acute stage after whiplash
trauma is related to higher neck pain intensity49 and higher levels of neck disability.46,49 In the present study of jaw-neck function, the findings of smaller jaw amplitudes but no change in head amplitudes may seem contradictory. However, during natural jaw function, al- though the head movement is proportional to the jaw movement, head movement is considerably smaller, normally with a ratio be- tween head and jaw movements of about 10%-20% during maximal jaw opening.1,50 This means, that during the jaw opening-closing task performed in our study, the magnitude of head movements is con- siderably smaller than the movements performed during the max- imal range of cervical movements examined by Sterling et al47 and Fernandez-Perez et al46 in acute whiplash populations.
In the acute stage after whiplash trauma, a moderate correla- tion between the pain intensity in the jaw and neck regions was reported.14 Intensity of neck pain in the acute stage after whiplash trauma has also been identified as one risk factor for poor recovery.10 The findings in patients with chronic WAD, as reported above, with significantly reduced amplitudes of both jaw and head movements and head-jaw ratio compared to controls,11,12 were not evident in the present study in the acute stage after whiplash trauma. Higher neck pain ratings in patients with chronic WAD11,12 may contribute to the differences compared to the present study. This interpretation is sup- ported by our present finding in the acute phase of a difference in jaw movement amplitudes between cases with high vs. low neck pain in- tensity. The relatively low median neck pain intensity (NRS = 2) for the case group in the present study may be one explanation for the lack of difference in head movement amplitudes between cases and controls, albeit with a tendency for smaller head movement amplitudes in the six individuals with higher neck pain intensity.
Another contributing factor to the lack of difference between cases and controls may be that since the cases in the present study were examined in the acute stage after trauma, approximately half of them are expected to recover completely.7 Our previous reports of reduced head and jaw movement amplitudes during jaw function in patients with chronic WAD were based on a more selected patient group and are therefore not representative of all individuals after a whiplash trauma. Although the present study was based on a more representative case group, the fact that the original study popula- tion was reduced due to a camera failure resulted in a loss of data that may have affected the results.
There was no significant difference for the movement cycle time between cases and controls. Considering that the speed of the movement is related to the movement amplitude during a given time period, the smaller jaw movement amplitudes in the case group, to- gether with no difference in cycle time, indicate a slower jaw move- ment for cases compared to controls. Thus, the indication of a lower speed of jaw movements in chronic WAD11 is found also in the acute stage after whiplash trauma.
The unequal proportion of men and women in the case and con- trol groups impacts interpretation of the results. The significantly lower jaw movement amplitudes observed in male cases compared to male controls should be interpreted with some caution. EMG measurements of activity in jaw and neck muscles could have
provided additional information for evaluating neuromuscular ac- tivity during the recordings. Information about the subject's former medical health status and utilisation of healthcare prior and after the whiplash trauma is not known. The severity of the neck injury according to the grade of Quebec Task Force classification system was WAD I-III, but the specific classification grade is not available for the individual subjects. The possible relationship between WAD classification grade and jaw-neck motor function warrants further studies.
The clinical implication from the present study is that clinicians should be aware that patients with a recent whiplash trauma may also show impaired jaw motor function, especially if they report a high intensity of neck pain. In this context, it is worthwhile to also consider that high intensity of neck pain in the early stage after whiplash trauma is a negative prognostic factor for recovery.10 Furthermore, individuals with jaw pain in the acute stage after whip- lash trauma have a high risk of reporting jaw pain also in the chronic stage.51 Therefore, examination of the jaw system should be consid- ered by health and dental care providers in conjunction with a whip- lash trauma for early identification and management of individuals at risk for long-term jaw pain and dysfunction.
5 | CONCLUSION
In the present study, the results suggest jaw-neck motor function may be affected in the acute stage after a whiplash trauma although the effects were minor. Cases with higher neck pain intensity showed smaller maximal jaw opening amplitudes, which may indi- cate pain-related fear of movement that could be a risk factor for developing long-lasting pain and disability. However, the magnitude of jaw and head movement amplitudes was not correlated to jaw pain, neck pain or neck disability. Further research with prospec- tive study designs on a larger study population is warranted for un- derstanding the long-term effects of whiplash trauma on jaw-neck motor function.
The authors thank Erling Englund for statistical advice. The study was approved by the Regional Ethical Review Board in Umeå, Sweden (Dnr 201015631M). The study was supported by grants from Västerbotten County Council (TUA) and the Swedish Dental Society.
CONFLIC T OF INTEREST
The authors declare no conflict of interest.
BH-H, BW and AW contributed to the concept and design of the study. EL, BH-H and CÖ conducted the data collection. AE, BW and BH-H performed the data analysis and interpretation of results. AE wrote the first draft of the manuscript. All authors contributed to the manuscript revision and approved the final version.
Anton Eklund https://orcid.org/0000-0001-8904-8892 Birgitta Wiesinger https://orcid.org/0000-0003-1194-8975 Ewa Lampa https://orcid.org/0000-0002-7431-9618 Catharina Österlund https://orcid.org/0000-0002-8986-9401 Anders Wänman https://orcid.org/0000-0002-8346-5289 Birgitta Häggman-Henrikson https://orcid.
1. Eriksson PO, Häggman-Henrikson B, Nordh E, Zafar H. Co- ordinated mandibular and head-neck movements during rhythmic jaw activities in man. J Dent Res. 2000;79:1378-1384.
2. Eriksson PO, Zafar H, Nordh E. Concomitant mandibular and head- neck movements during jaw opening-closing in man. J Oral Rehabil.
3. Häggman-Henrikson B, Eriksson PO. Head movements during chewing: relation to size and texture of bolus. J Dent Res.
4. Spitzer WO, Skovron ML, Salmi LR, et al. Scientific monograph of the Quebec Task Force on Whiplash-Associated Disorders: redefining
"whiplash" and its management. Spine (Phila Pa. 1976). 1995;20:1s-73s.
5. Styrke J, Stålnacke BM, Bylund PO, Sojka P, Björnstig U. A 10-year incidence of acute whiplash injuries after road traffic crashes in a defined population in northern Sweden. PM&R. 2012;4:739-747.
6. Sterner Y, Gerdle B. Acute and chronic whiplash disorders–a review.
J Rehabil Med. 2004;36:193-209; quiz 210.
7. Carroll LJ, Holm LW, Hogg-Johnson S, et al. Course and prognos- tic factors for neck pain in whiplash-associated disorders (WAD):
results of the Bone and Joint Decade 2000–2010 Task Force on Neck Pain and Its Associated Disorders. Spine (Phila Pa. 1976).
8. Treede R-D, Rief W, Barke A, et al. A classification of chronic pain for ICD-11. Pain. 2015;156:1003-1007.
9. Sarrami P, Armstrong E, Naylor JM, Harris IA. Factors predicting outcome in whiplash injury: a systematic meta-review of prognostic factors. J Orthop Traumatol. 2017;18:9-16.
10. Walton DM, Macdermid JC, Giorgianni AA, Mascarenhas JC, West SC, Zammit CA. Risk factors for persistent problems following acute whiplash injury: update of a systematic review and meta-analysis.
J Orthop Sports Phys Ther. 2013;43:31-43.
11. Häggman-Henrikson B, Zafar H, Eriksson PO. Disturbed jaw be- havior in whiplash-associated disorders during rhythmic jaw move- ments. J Dent Res. 2002;81:747-751.
12. Eriksson PO, Häggman-Henrikson B, Zafar H. Jaw-neck dysfunction in whiplash-associated disorders. Arch Oral Biol. 2007;52:404-408.
13. Häggman-Henrikson B, Österlund C, Eriksson PO. Endurance during chewing in whiplash-associated disorders and TMD. J Dent Res. 2004;83:946-950.
14. Häggman-Henrikson B, Lampa E, Marklund S, Wänman A. Pain and disability in the jaw and neck region following whiplash trauma.
J Dent Res. 2016;95:1155-1160.
15. Lampa E, Wänman A, Nordh E, Häggman-Henrikson B. Effects on jaw function shortly after whiplash trauma. J Oral Rehabil.
16. Lövgren A, Häggman-Henrikson B, Visscher CM, Lobbezoo F, Marklund S, Wänman A. Temporomandibular pain and jaw dys- function at different ages covering the lifespan–a population based study. Eur J Pain. 2016;20:532-540.
17. Nilsson IM, List T, Drangsholt M. The reliability and validity of self-reported temporomandibular disorder pain in adolescents.
J Orofac Pain. 2006;20:138-144.
18. Vernon H, Mior S. The Neck Disability Index: a study of reliability and validity. J Manipulative Physiol Ther. 1991;14:409-415.
19. Dworkin SF, LeResche L. Research diagnostic criteria for temporo- mandibular disorders: review, criteria, examinations and specifica- tions, critique. J Craniomandib Disord. 1992;6:301-355.
20. Josefsson T, Nordh E, Eriksson PO. A flexible high-precision video system for digital recording of motor acts through lightweight re- flex markers. Comput Methods Programs Biomed. 1996;49:119-129.
21. Häggman-Henrikson B, Eriksson PO, Nordh E, Zafar H. Evaluation of skin- versus teeth-attached markers in wireless optoelec- tronic recordings of chewing movements in man. J Oral Rehabil.
22. Zafar H, Eriksson PO, Nordh E, Häggman-Henrikson B. Wireless optoelectronic recordings of mandibular and associated head- neck movements in man: a methodological study. J Oral Rehabil.
23. Hodges PW. Pain and motor control: from the laboratory to rehabil- itation. J Electromyogr Kinesiol. 2011;21:220-228.
24. Falla D, Farina D, Dahl MK, Graven-Nielsen T. Muscle pain induces task-dependent changes in cervical agonist/antagonist activity. J Appl Physiol. 1985;2007(102):601-609.
25. Svensson P, Houe L, Arendt-Nielsen L. Bilateral experimental mus- cle pain changes electromyographic activity of human jaw-closing muscles during mastication. Exp Brain Res. 1997;116:182-185.
26. Svensson P, Wang K, Sessle BJ, Arendt-Nielsen L. Associations be- tween pain and neuromuscular activity in the human jaw and neck muscles. Pain. 2004;109:225-232.
27. Wiesinger B, Häggman-Henrikson B, Hellström F, Wänman A.
Experimental masseter muscle pain alters jaw-neck motor strategy.
Eur J Pain. 2013;17:995-1004.
28. Wiesinger B, Häggman-Henrikson B, Hellström F, Englund E, Wänman A. Does induced masseter muscle pain affect integrated jaw-neck movements similarly in men and women? Eur J Oral Sci.
29. Stenneberg MS, Rood M, de Bie R, Schmitt MA, Cattrysse E, Scholten-Peeters GG. To what degree does active cervical range of motion differ between patients with neck pain, patients with whiplash, and those without neck pain? A systematic review and meta-analysis. Arch Phys Med Rehabil. 2017;98:1407-1434.
30. Woodhouse A, Vasseljen O. Altered motor control patterns in whip- lash and chronic neck pain. BMC Musculoskelet Disord. 2008;9:90.
31. Woodhouse A, Stavdahl Ø, Vasseljen O. Irregular head movement patterns in whiplash patients during a trajectory task. Exp Brain Res.
32. Treleaven J, Jull G, Grip H. Head eye co-ordination and gaze stabil- ity in subjects with persistent whiplash associated disorders. Man Ther. 2011;16:252-257.
33. Grip H, Jull G, Treleaven J. Head eye co-ordination using simulta- neous measurement of eye in head and head in space movements:
potential for use in subjects with a whiplash injury. J Clin Monit Comput. 2009;23:31-40.
34. Pearson I, Reichert A, De Serres SJ, Dumas JP, Cote JN. Maximal voluntary isometric neck strength deficits in adults with whip- lash-associated disorders and association with pain and fear of movement. J Orthop Sports Phys Ther. 2009;39:179-187.
35. Krogh S, Kasch H. Whiplash injury results in sustained impairments of cervical muscle function: a one-year prospective, controlled study. J Rehabil Med. 2018;50:548-555.
36. Stone AM, Vicenzino B, Lim EC, Sterling M. Measures of central hy- perexcitability in chronic whiplash associated disorder–a systematic review and meta-analysis. Man Ther. 2013;18:111-117.
37. Komiyama O, Arai M, Kawara M, Kobayashi K, De Laat A. Pain pat- terns and mandibular dysfunction following experimental trapezius muscle pain. J Orofac Pain. 2005;19:119-126.
38. Sae-Lee D, Whittle T, Peck CC, Forte AR, Klineberg IJ, Murray GM.
Experimental jaw-muscle pain has a differential effect on different jaw movement tasks. J Orofac Pain. 2008;22:15-29.
39. Sessle BJ, Hu JW, Amano N, Zhong G. Convergence of cutaneous, tooth pulp, visceral, neck and muscle afferents onto nociceptive and non-nociceptive neurones in trigeminal subnucleus caudalis (medullary dorsal horn) and its implications for referred pain. Pain.
40. Makowska A, Panfil C, Ellrich J. Nerve growth factor injection into semispinal neck muscle evokes sustained facilitation of the jaw-opening reflex in anesthetized mice – possible implications for tension-type headache. Exp Neurol. 2005;191:301-309.
41. Hellström F, Thunberg J, Bergenheim M, Sjölander P, Djupsjöbacka M, Johansson H. Increased intra-articular concentration of bra- dykinin in the temporomandibular joint changes the sensitivity of muscle spindles in dorsal neck muscles in the cat. Neurosci Res.
42. Shin P, Vernon H, Sessle BJ, Hu JW. Neck muscle length modulates nociceptive reflex evoked by noxious irritant application to rat neck tissues. Exp Brain Res. 2005;163:314-323.
43. Svensson P, Wang MW, Dong XD, Kumar U, Cairns BE. Human nerve growth factor sensitizes masseter muscle nociceptors in fe- male rats. Pain. 2010;148:473-480.
44. Vlaeyen JW, Linton SJ. Fear-avoidance and its consequences in chronic musculoskeletal pain: a state of the art. Pain. 2000;85:317-332.
45. Häggman-Henrikson B, Nordh E, Zafar H, Eriksson PO. Head immo- bilization can impair jaw function. J Dent Res. 2006;85:1001-1005.
46. Fernandez-Perez AM, Villaverde-Gutierrez C, Mora-Sanchez A, Alonso-Blanco C, Sterling M, Fernandez-de-Las-Penas C. Muscle trigger points, pressure pain threshold, and cervical range of mo- tion in patients with high level of disability related to acute whiplash injury. J Orthop Sports Phys Ther. 2012;42:634-641.
47. Sterling M, Jull G, Vicenzino B, Kenardy J, Darnell R. Development of motor system dysfunction following whiplash injury. Pain.
48. Sterling M, Jull G, Vicenzino B, Kenardy J. Characterization of acute whiplash-associated disorders. Spine (Phila Pa 1976). 2004;29:182-188.
49. De Rosario H, Vivas MJ, Sinovas MI, Page A. Relationship between neck motion and self-reported pain in patients with whiplash as- sociated disorders during the acute phase. Musculoskelet Sci Pract.
50. Österlund C, Nilsson E, Hellström F, Häger CK, Häggman-Henrikson B. Jaw-neck movement integration in 6-year-old children differs from that of adults. J Oral Rehabil. 2020;47(1):27-35.
51. Lampa E, Wänman A, PhD EN, Stålnacke B-M, Häggman-Henrikson B. The course of orofacial pain and jaw disability after whip- lash trauma: a 2-year prospective study. Spine (Phila Pa 1976).
How to cite this article: Eklund A, Wiesinger B, Lampa E, Österlund C, Wänman A, Häggman-Henrikson B. Jaw-neck motor function in the acute stage after whiplash trauma. J Oral Rehabil. 2020;47:834–842. https://doi.org/10.1111/joor.12981