Jaw-neck motor function in the acute stage after whiplash trauma.

MR. ANTON EKLUND (Orcid ID : 0000-0001-8904-8892) DR. EWA LAMPA (Orcid ID : 0000-0002-7431-9618)

DR. CATHARINA ÖSTERLUND (Orcid ID : 0000-0002-8986-9401) PROF. ANDERS WÄNMAN (Orcid ID : 0000-0002-8346-5289)

DR. BIRGITTA HÄGGMAN-HENRIKSON (Orcid ID : 0000-0001-6088-3739)

Article type : Original Article

JAW-NECK MOTOR FUNCTION IN THE ACUTE STAGE AFTER WHIPLASH TRAUMA

Short title: JAW MOTOR FUNCTION AFTER WHIPLASH TRAUMA

Anton Eklund¹ | Birgitta Wiesinger^1,2 | Ewa Lampa¹ | Catharina Österlund¹ | Anders Wänman¹ | Birgitta Häggman-Henrikson^1,3

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

Corresponding Author:

Dr. A. Eklund

Department of Odontology/Clinical Oral Physiology, Umeå University, Umeå, SE-901 87 Sweden.

E-mail address; anton.eklund@umu.se

Accepted Article

Category: Original Research

ABSTRACT 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 whiplash 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 yrs) within one month after whiplash trauma and compared with 27 controls without neck trauma (15 men, 12 women, 20-66 yrs). 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=0.006) but no difference in head movement amplitudes, head/jaw ratios, or movement cycle times. There were no significant correlations between movement amplitudes 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=0.024).

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.

KEY WORDS

Whiplash injury, neck, jaw, motor activity, movements, pain

1 | INTRODUCTION

Accepted Article

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 function. When performing a sequence of continuous

maximum jaw opening-closing cycles, the head remains in a slightly extended position after the end of the first movement cycle.¹ Subsequent head movements originate from this extended head position, with additional 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 whereas head movements decrease with smaller jaw opening and with faster jaw movement cycles, demonstrating a strong functional 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 year⁵ 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 one 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 of the amplitude and coordination between jaw and head movements during jaw opening-closing have been observed in individuals with chronic WAD. Compared to individuals 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 contribution 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 together, 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.

Accepted Article

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 suggested early symptoms from the orofacial region after whiplash trauma, 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 affected 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 advertising.^14,

15 Participants in the present study were examined between December 21, 2010 and February 5, 2016.

Inclusion criteria for both cases and controls were: 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 inclusion criterion was a diagnosis of neck distortion (ICD-10 S134) by a physician within 72 hours after a whiplash trauma from a car accident. An exclusion criterion for cases was WAD classified as grade IV (fracture) according to the Quebec Task Force classification system⁴ 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 examination in the main study. The researcher was blinded to group allocation (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 yrs) and 27 controls (15 men, 12 women, 20-66 yrs) (Table 1).

All participants were examined at the Department of Clinical Oral Physiology, University Hospital of Umeå.

Cases were examined within one month after being diagnosed at the Emergency Department at Umeå University Hospital, and controls were evaluated at available examination times. The study was conducted according to the Declaration of Helsinki and approved by the Regional Ethical Review Board in Umeå (Dnr

Accepted Article

2010-156-31M). Participation was voluntary and written informed consent was obtained. The subjects were given written and oral information that they could withdraw their participation at any time.

2.2 | Questionnaires

Before the movement recordings, all participants filled in the following questionnaires:

 The Numeric Rating Scale (NRS) for assessing current pain intensity 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 orofacial 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 between 0-50, 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 standardized questionnaire is constructed as a 5-point Likert type-scale with a total of 32 questions that include the non-specific physical symptoms (12 items), the non-pain physical symptoms (7 remaining items after removing the 5 pain-related questions) and the depression scale (20 items).

SCL-90-R scales provide cut-off values for normal, 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 and 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}

Standardized verbal information about the jaw opening-closing task was provided to all participants prior to the movement recordings 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 commands were used to indicate the start and the stop of

Accepted Article

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 experienced in movement analysis (BH-H).

2.4 | Movement recordings

Head and jaw movements were recorded using a wireless optoelectronic movement recording system (MacReflex®; Qualisys, Gothenburg, Sweden) constructed for tracking changes in spatial 3D-positions of retroreflective markers (Ø 5mm). The system has a high resolution²⁰ and the performance of the system’s two cameras 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 registration of the relative movements of the head and the jaw during 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 November 13, 2015 until February 5, 2016 could not be used for analysis. During this time period movement recordings 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 yrs, 18-66 yrs) and 36 controls (20 men, 16 women, mean 31 yrs, 20-66 yrs) resulted in the final subsample of 23 cases (4 men, 19 women, mean 36 yrs, 18-66 yrs) and 27 controls (15 men, 12 women, mean 32 yrs, 20-66 yrs).

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 movement. The peak was defined as the time point for the most inferior position of the mandible, i.e., at the shift from jaw-opening phase to the jaw-closing phase (Fig. 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 position of the

Accepted Article

head within the jaw opening-closing phase. The movement cycle time was defined as the time (s) elapsed between the start of two subsequent jaw opening-closing cycles.

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 vectors were calculated between the 3D-positions at the start and peak of each movement cycle, and were presented as head and jaw movement 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 complete cycle time for the first seven jaw movement cycles. For 12 subjects, 6 cases (26%) and 6 controls (22%), fewer than eight jaw and head movement amplitudes were recorded within the 25-second time frame. For the calculation of movement cycle times, 12 subjects, 6 cases (26%) and 6 controls (22%), did not reach seven full movement cycles. 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 distribution 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 movement amplitudes, head/jaw ratio (quotient of head and jaw movement amplitudes), jaw opening-closing movement cycle times, neck disability (NDI), neck and jaw pain (NRS), age and the sub-scales from the SCL-90-R.

Correlations were analyzed separately within groups with Spearman´s correlation for movement amplitude and movement cycle time in relation to jaw pain (NRS), neck pain (NRS) and neck disability (NDI). For the case group, a posthoc subgroup analysis the with Mann-Whitney U test was conducted for individuals with higher neck pain intensity (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 <0.05.

3 |
 RESULTS

3.1 |
 Demographic characteristics, pain ratings and psychosocial symptoms

The demographic characteristics and pain ratings were done before the movement recordings and are presented in Table 1. There was no age difference between groups (p=0.482) but there was a higher

proportion of women among cases and a higher proportion of men among controls (p=0.008). More cases than controls reported pain in the temple, face, jaw or jaw joint once a week or more (Q1; 48% vs. 7%, p=0.003);

Accepted Article

however, there was no significant difference between the groups for pain during jaw function (Q2; cases 22%

vs controls 4%, p=0.082). Cases reported higher jaw and neck pain intensity and higher neck disability scores (all p<0.001). 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) was 43% for cases and 96% for controls.

The cases reported higher scores for non-specific physical symptoms (p<0.001) and non-pain physical symptoms (p=0.006) compared to controls. There was no significant difference between the groups for depression symptoms (p=0.099) (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 compared to controls (62.6 mm, IQR 13.4, p=0.006). There was no significant difference between cases and controls for head movement amplitudes (4.3 mm, IQR 4.2 vs. 6.6 mm, IQR 5.9, respectively, p=0.136) (Fig. 2).

When men and women were analyzed 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=0.02), 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, IQR19.7, p=0.484). For head movement amplitudes, there were no significant differences between male cases (5.3 mm, IQR 10.7) and male controls (7.7mm, IQR 15.8, p=0.885) or between female cases (4.2 mm, IQR 4.3) and female controls (6.3 mm, IQR 3.8, p=0.326).

There was no significant difference in the ratio between head and jaw movement amplitudes between cases and controls (0.11, IQR 0.07 vs. 0.11, IQR 0.08, p=0.690, respectively). 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=0.024) (Fig. 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=0.101), respectively (Fig. 3).

Male controls showed significantly larger jaw movement amplitudes (63.7 mm, IQR 7.7) compared to female controls (56.5 mm, IQR 19.7, p=0.025), while male cases (50.0 mm, IQR 20.9) and female cases (51.5 mm IQR 18.3, p=0.907) showed no difference in jaw movement amplitudes. There were no differences in head movement amplitudes between male controls (7.7 mm, IQR 15.8) and female controls (6.3 mm, IQR 3.8, p=0.399), or between male cases (5.3 mm, IQR 10.7) and female cases (4.2 mm, IQR 4.3, p=0.366).

3.3 | 
Movement cycle time

Accepted Article

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) (Fig. 4).

3.4 |
 Correlation

There were no significant correlations between jaw or head movement 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 individuals with no history of neck trauma and that cases with higher neck pain intensity had significantly smaller jaw movement amplitudes compared 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 movement 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 in the

sternocleidomastoid muscle bilaterally; furthermore, pain induction in the sternocleidomastoid muscle resulted in decreased muscle activity bilaterally in 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 in the injected muscle.²⁴ Experimental pain induction 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 associated with ipsilateral increases in muscle activity in the masseter,

sternocleidomastoid and splenius capitis muscles, while maximal jaw clenching resulted in decreased muscle activity from the masseter bilaterally and the ipsilateral sternocleidomastoid muscle.²⁶ In previous 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 indicating 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.

Accepted Article

For patients with chronic pain and dysfunction following whiplash trauma, a range of differences with regard to motor function has been reported. Individuals with chronic WAD had smaller maximal neck movements compared to individuals with idiopathic neck pain, and individuals without neck pain.²⁹ Furthermore, compared to healthy individuals, individuals with chronic WAD showed disturbed sensorimotor control during neck movements,^{30, 31} disturbed head-eye coordination,^{32, 33} reduced neck muscle strength^{34, 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 masseter 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 opening 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 to 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 to effects on the N-methyl-D-aspartate (NMDA) receptor through NGF receptor signalling.⁴³

Therefore, the mechanical stimuli by movements could possibly increase action potentials from a sensitised nociceptor.

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, reduced 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 individuals 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 individuals.^{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. In the acute stage, individuals with a recent whiplash trauma also showed impaired chewing function;¹⁵ 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

Accepted Article

Taken together, these findings suggest early changes in motor function 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 control already in the acute stage, as evidenced by a smaller cervical range of motion,^{46, 47} altered EMG-activity 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, although the head movement is proportional to the jaw movement, head movement is

considerably smaller, normally with a ratio between 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 considerably smaller than the movements performed during the maximal range of cervical movements examined by Sterling et al.⁴⁷ and Fernandez-Perez et al.⁴⁶ in acute whiplash populations.

In the acute stage after whiplash trauma, a moderate correlation 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 WAD^{11, 12} may contribute to the differences compared to the present study. This interpretation is supported by our present finding in the acute phase of a difference in jaw movement

amplitudes between cases with high vs. low neck pain intensity. 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, 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 population was reduced due to a camera failure resulted in a loss of data that may have affected the results.

Accepted Article

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, together with no difference in cycle time, indicates a slower jaw movement for cases compared to controls. Thus, the indication of a lower speed of jaw movements in chronic WAD¹¹ is also found in the acute stage after whiplash trauma.

The unequal proportion of men and women in the case and control 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 activity during the recordings. Information about the subject’s former medical health status and utilization of health care 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 whiplash trauma have a high risk of reporting jaw pain also in the chronic stage.⁵¹ Therefore, examination of the jaw system should be considered by health and dental care providers in conjunction with a whiplash 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 indicate 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 prospective study designs on a larger study population is warranted for understanding the long term effects of whiplash trauma on jaw-neck motor function.

AUTHOR CONTRIBUTION STATEMENT

BH-H, BW and AW contributed to the concept and design of the study. EL, BH-H and CÖ conducted the data

Accepted Article

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.

ACKNOWLEDGEMENTS

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.

CONFLICT OF INTEREST

The authors declare no conflict of interest.

REFERENCES

1. Eriksson PO, Haggman-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 1998;25:859-870.

3. Haggman-Henrikson B, Eriksson PO. Head movements during chewing: relation to size and texture of bolus. J Dent Res 2004;83:864-868.

4. Spitzer WO, Skovron ML, Salmi LR, Cassidy JD, Duranceau J, Suissa S, 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, Stalnacke BM, Bylund PO, Sojka P, Bjornstig 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, Cote P, Cassidy JD, Haldeman S, et al. Course and prognostic 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) 2008;33:S83-92.

8. Treede RD, Rief W, Barke A, Aziz Q, Bennett MI, Benoliel R, 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.

Accepted Article

11. Haggman-Henrikson B, Zafar H, Eriksson PO. Disturbed jaw behavior in whiplash-associated disorders during rhythmic jaw movements. J Dent Res 2002;81:747-751.

12. Eriksson PO, Haggman-Henrikson B, Zafar H. Jaw-neck dysfunction in whiplash-associated disorders.

Arch Oral Biol 2007;52:404-408.

13. Haggman-Henrikson B, Osterlund C, Eriksson PO. Endurance during chewing in whiplash-associated disorders and TMD. J Dent Res 2004;83:946-950.

14. Haggman-Henrikson B, Lampa E, Marklund S, Wanman A. Pain and Disability in the Jaw and Neck Region following Whiplash Trauma. J Dent Res 2016;95:1155-1160.

15. Lampa E, Wanman A, Nordh E, Haggman-Henrikson B. Effects on jaw function shortly after whiplash trauma. J Oral Rehabil 2017;44:941-947.

16. Lovgren A, Haggman-Henrikson B, Visscher CM, Lobbezoo F, Marklund S, Wanman A.

Temporomandibular pain and jaw dysfunction 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 temporomandibular disorders: review, criteria, examinations and specifications, 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 reflex markers. Comput Methods Programs Biomed 1996;49:119-129.

21. Haggman-Henrikson B, Eriksson PO, Nordh E, Zafar H. Evaluation of skin- versus teeth-attached markers in wireless optoelectronic recordings of chewing movements in man. J Oral Rehabil 1998;25:527-534.

22. Zafar H, Eriksson PO, Nordh E, Haggman-Henrikson B. Wireless optoelectronic recordings of mandibular and associated head-neck movements in man: a methodological study. J Oral Rehabil 2000;27:227-238.

23. Hodges PW. Pain and motor control: From the laboratory to rehabilitation. 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 muscle 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 between pain and neuromuscular activity in the human jaw and neck muscles. Pain 2004;109:225-232.

Accepted Article

27. Wiesinger B, Haggman-Henrikson B, Hellstrom F, Wanman A. Experimental masseter muscle pain alters jaw-neck motor strategy. Eur J Pain 2013;17:995-1004.

28. Wiesinger B, Haggman-Henrikson B, Hellstrom F, Englund E, Wanman A. Does induced masseter muscle pain affect integrated jaw-neck movements similarly in men and women? Eur J Oral Sci 2016;124:546- 553.

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 whiplash and chronic neck pain. BMC Musculoskelet Disord 2008;9:90.

31. Woodhouse A, Stavdahl O, Vasseljen O. Irregular head movement patterns in whiplash patients during a trajectory task. Exp Brain Res 2010;201:261-270.

32. Treleaven J, Jull G, Grip H. Head eye co-ordination and gaze stability 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 simultaneous 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 whiplash-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 hyperexcitability 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 patterns 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 1986;27:219-235.

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.

Accepted Article

41. Hellstrom F, Thunberg J, Bergenheim M, Sjolander P, Djupsjobacka M, Johansson H. Increased intra- articular concentration of bradykinin in the temporomandibular joint changes the sensitivity of muscle spindles in dorsal neck muscles in the cat. Neurosci Res 2002;42:91-99.

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 female 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. Haggman-Henrikson B, Nordh E, Zafar H, Eriksson PO. Head immobilization 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 motion 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 2003;103:65-73.

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 associated disorders during the acute phase. Musculoskelet Sci Pract 2018;38:23-29.

50. Osterlund C, Nilsson E, Hellstrom F, Hager CK, Haggman-Henrikson B. Jaw-neck movement integration in 6-year-old children differs from that of adults. J Oral Rehabil 2019.

51. Lampa E, Wanman A, Ph DE, Stalnacke BM, Haggman-Henrikson B. The Course of Orofacial Pain and Jaw Disability After Whiplash Trauma: A 2-year Prospective Study. Spine (Phila Pa 1976) 2020;45:E140- e147.

Accepted Article

FIGURE LEGENDS

FIGURE 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.

FIGURE 2 Jaw and head maximal movement amplitudes (mm) for cases (n=23) and controls (n=27) during jaw opening-closing movements. The box plots illustrate the medians, interquartile ranges, and the 10^th and 90^th percentiles. Dots represent values outside the 10^th and 90^th percentiles.

FIGURE 3 Jaw and head maximal movement amplitudes (mm) for cases (n=23) in relation to neck pain intensity on the numeric rating scale (NRS) during 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 10^th and 90^th percentiles. Dots represent values outside 10^th and 90^th percentiles.

FIGURE 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 10^th and 90^th percentiles. Dots represent values outside 10^th and 90^th percentiles.

Accepted Article

TABLE 1 Demographic characteristics, Neck Disability Index (NDI), jaw and neck pain, and psychosocial symptoms

Cases Controls Cases vs Controls p-value

Total n 23 27

Age (yr) mean (SD) 36 (15) 32 (12) 0.482

Neck disability, NDI median (IQR) 16 (20) 2 (4) <0.001

Neck pain, NRS median (IQR) 2 (3) 0 (1) <0.001

Jaw pain, NRS median (IQR) 1 (1) 0 (0) <0.001

Q1 positive n (%) 11 (48%) 2 (7%) 0.003

Q2 positive n (%) 5 (22%) 1 (4%) 0.082

SCL-90-R

Physical symptoms median (IQR)^† 0.83 (1.17) 0.25 (0.42) <0.001 Non pain symptomsmedian (IQR)^‡ 0.71 (1.14) 0.14 (0.43) 0.006 Depression median (IQR)^§ 0.75 (1.02) 0.45 (0.65) 0.099 Bold values indicate significant difference between groups. SD = Standard deviation; IQR = Interquartile range; NDI = Neck Disability Index (0-100 %).

Accepted Article

NRS = Numerical Rating Scale (0-10); Screening questions for orofacial 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

†Cut-off values: normal <0.500, moderate 0.500 to <1.000, severe ≥1.000

‡Cut-off values: normal <0.428, moderate 0.428 to <0.857, severe ≥0.857

§Cut-off values: normal <0.535, moderate 0.535 to <1.105, severe ≥1.105

TABLE 2 Correlation between jaw and head movement amplitudes, movement cycle time and jaw pain (NRS), neck pain (NRS) and neck disability (NDI) for cases (n=23) and controls (n=27), respectively

Cases Controls

r^† p-value r^† p-value

Jaw amplitude vs neck pain -0.377 0.076 -0.112 0.578

Jaw amplitude vs jaw pain -0.225 0.301 -0.277 0.162

Jaw amplitude vs neck disability -0.326 0.129 -0.027 0.895

Head amplitude vs neck pain -0.379 0.075 -0.150 0.454

Head amplitude vs jaw pain -0.368 0.084 -0.277 0.162

Head amplitude vs neck disability -0.311 0.148 -0.072 0.722

Cycle time vs neck pain 0.309 0.151 -0.136 0.500

Cycle time vs jaw pain 0.326 0.129 0.000 1.000

Cycle time vs neck disability 0.313 0.145 -0.190 0.342

NRS = Numeric Rating Scale (0-10); NDI=Neck Disability Index (0-100 %);

†Spearman´s correlation.

Accepted Article

TABLE 1 Demographic characteristics, Neck Disability Index (NDI), jaw and neck pain, and psychosocial symptoms

Cases Controls Cases vs Controls

p-value

Total n 23 27

Age (yr) mean (SD) 36 (15) 32 (12) 0.482

Neck disability, NDI median (IQR) 16 (20) 2 (4) <0.001

Neck pain, NRS median (IQR) 2 (3) 0 (1) <0.001

Jaw pain, NRS median (IQR) 1 (1) 0 (0) <0.001

Q1 positive n (%) 11 (48%) 2 (7%) 0.003

Q2 positive n (%) 5 (22%) 1 (4%) 0.082

SCL-90-R

Physical symptoms median (IQR)^† 0.83 (1.17) 0.25 (0.42) <0.001 Non pain symptomsmedian (IQR)^‡ 0.71 (1.14) 0.14 (0.43) 0.006 Depression median (IQR)^§ 0.75 (1.02) 0.45 (0.65) 0.099 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 orofacial 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

†Cut-off values: normal <0.500, moderate 0.500 to <1.000, severe ≥1.000

‡Cut-off values: normal <0.428, moderate 0.428 to <0.857, severe ≥0.857

§Cut-off values: normal <0.535, moderate 0.535 to <1.105, severe ≥1.105

Accepted Article

TABLE 2 Correlation between jaw and head movement amplitudes, movement cycle time and jaw pain (NRS), neck pain (NRS) and neck disability (NDI)

for cases (n=23) and controls (n=27), respectively

Cases Controls

r^† p-value r^† p-value

Jaw amplitude vs neck pain -0.377 0.076 -0.112 0.578

Jaw amplitude vs jaw pain -0.225 0.301 -0.277 0.162

Jaw amplitude vs neck disability -0.326 0.129 -0.027 0.895

Head amplitude vs neck pain -0.379 0.075 -0.150 0.454

Head amplitude vs jaw pain -0.368 0.084 -0.277 0.162

Head amplitude vs neck disability -0.311 0.148 -0.072 0.722

Cycle time vs neck pain 0.309 0.151 -0.136 0.500

Cycle time vs jaw pain 0.326 0.129 0.000 1.000

Cycle time vs neck disability 0.313 0.145 -0.190 0.342

NRS = Numeric Rating Scale (0-10); NDI=Neck Disability Index (0-100 %);

†Spearman´s correlation.

Accepted Article

Accepted Article

joor_12981_f2.tiff

Accepted Article

joor_12981_f3.tiff

Accepted Article

joor_12981_f4.tiff

Accepted Article