Cervical kinematics in patients with vestibular pathology vs. patients with neck pain: A pilot study

2.1 Design overview

This cross-sectional, observational study, sought asymptomatic control subjects, subjects with VP and subjects with persistent NP for the study. Participants were matched in accordance to similar age andgender.

2.2 Setting and participants

The study was conducted at the Neck pain and Whiplash Research Unit at the XXXXX. Recruitment was through general advertising in the greater XXX area, through vestibular pathology support groups and through University and private practice treatment clinics.

Asymptomatic control subjects were excluded if they had any existing vestibular or cervical pathology, neck Disability Index (NDI) of greater than 10%. A score less than 8% indicates no neck pain and disability [31].

Inclusion criteria for subjects with NP included NP for greater than three months, and a NDI score greater than 10% [31]. A score above 10% indicates the patient has some degree of neck pain and disability [31]. Further they were required to have a reduction of mean velocity with VR testing of at least one SD from control values [17].

Exclusion criteria were as listed above.

Inclusion criteria for subjects with VP included diagnosed acoustic neuroma or Meniere’s disease by a Medical specialist and current active VP deficits confirmed by a physical examination, which included clinical tests of tandem gait (TG), visual vertical and clinical test of dynamic visual acuity (DVA). Exclusion criteria for this group also included other vestibular disorders such as Benign Paroxysmal Positional Vertigo, and a NDI of greater than 10%,

Further exclusion criteria for all groups included cervical fracture/dislocation, history of traumatic head injury, systemic diseases, neurological/res-piratory/cardiovascular disorders affecting physical performance, or were pregnant.

2.3 Self-reported measures

Neck disability index (NDI) was used to quantify self-perceived disability associated with neck pain. The NDI is both valid and reliable with higher percentage scores indicating greater disability [5, 30].

Visual symptoms scale (VSS) was used to characterise how a participant’s vision was being affected. Scored out of 48, it rated the frequency and severity of four factors including: needing to concentrate to focus, eye strain, visual fatigue and sensitivity to light, with higher scores indicating greater severity and frequency [28] these factors were based on common visual complaints in those with NP [28].

A Visual Analogue Scale (VAS) was used for participants to rate both their neck pain and dizziness on separate 100 mm scales. Greater scores indicate greater disability.

Pain on movement questionnaire (POM) was used to determine pain on each of the six cervical movements and also whether the VR system settings needed to be altered prior to testing. Participants were asked to rate the pain on a 100 mm VAS for each of the six neck movements with a greater sum of scores /600 mm indicating greater disability [14].

2.4 Cervical kinematics outcome measures

Cervical kinematics were measured using a customised neck VR system that used the same software (developed using Unity-pro software, version 3.5 Unity Technologies, San Francisco) as described previously [2] which created the interactive virtual environment. The upgraded hardware system used in this study included a head mounted display unit (HMD) (Oculus rift) with built in three-dimensional motion tracker. Calibration and tracking data tools were also used from the Oculus Rift DK2 Software kit (https://www.oculus.com/en-us/dk2/) with real-time tracking data analysis.

The neck VR system has three modules- ROM, velocity and accuracy, which aim to elicit cervical motion in response to visual stimuli. The participant controls an aeroplane using neck movements to reach a target. At the end of the module a full report regarding the participant’s kinematics is automatically generated. The ROM module measured ROM, the velocity module collected data to calculate velocity peak and mean, time to peak percentage (TTP%), and number of velocity peaks (NVP) and the accuracy module measured accuracy. For each of the separate velocity kinematic measures the value was calculated as the mean of the three best scores (out of 4 trials in each direction). Motion initiation was determined as the occasion when 5% of peak velocity was reached, and all kinematic measures were calculated in the timeframe between motion initiations to target hit. The tracker’s angular displacement were used to calculate the cervical movement kinematic variables: flexion (F) and extension (E) angular displacement was retrieved from pitch data, and rotation left (LR) and right (RR)- from Yaw data. The F+E and LR+RR values were then added together and divided by two to calculate a mean for each of the following variables for each movement plane. Information regarding these calculations has been given in the following publications [17, 20]. The default settings for velocity and accuracy were 50 degrees in each direction. The range of motion starting point was also 50 degrees and with each successful attempt the range was increased by 3 degrees until such time that the participant failed to reach the target in that particular direction on 3 attempts. The default settings were altered based on the POM testing. None of the vestibular or control subjects had this altered and about 10% of the neck pain subjects had the above default settings reduced to as little as 30 degrees in one or more of the directions.

Cervical ROM (degrees): Maximal ROM This has previously shown good repeatability and sensitivity [2].

2.5 Clinical vestibular measures

In order to determine eligibility and further describe the demographics of the vestibular population, clinical tests of tandem gait (TG), visual vertical and clinical dynamic visual acuity (DVA) were carried out in the vestibular patients.

Tandem Gait (TG) consisted of two parallel lines 5 cm thick, placed 10 cm apart along the floor. The participant walked 15 steps heel-toe between the lines [24]. The time it took to walk the middle 10steps was recorded along with the number of errors [8].

In addition, the Dizziness Handicap Inventory (DHI) and Activities-Specific Confidence Balance Scale (ABC) were used in vestibular patients to determine the severity of dizziness and confidence loss. DHI is a self-reported measure consisting of 25 items that cover the functional, emotional and physical aspects of dizziness. It has been shown to have good reliability with scores ranging from 0–100 and higher scores indicating greater handicap [11]. The ABC was used to measure confidence in functional tasks [15]. It consists of 16 items in which the participant rates how self-assured they feel in doing each item. Lower scores indicate lower levels of mobility.

All subjects completed a questionnaire, which included demographic questions, and all other questionnaires as above, including POM. Vestibular subjects then completed the physical tests consisting of the TG and visual vertical. All subjects were asked to execute the three modules of the kinematic assessment in the order of velocity, accuracy and ROM. Vestibular subjects then performed the clinical DVA test last to minimise adverse effects. Randomisation of the order of assessments was not appropriate as some tests had potential to elicit symptoms of dizziness and or motion sickness. Participants were given one brief practice trial of each module to reduce the learning effect. Between each module a rest break of approximately one minute was given and a subjective report of nausea was collected. The rest period was extended if any nausea or fatigue was reported and testing continued once they subsided [26]. Total time for testing was 45 minutes to one hour including rests.

Sample size was calculated based on previous studies comparing subjects with NP to controls [17]. The accuracy measures’ standard deviation were used to calculate sample size, as these were associated with the smallest significant effect size (–0.75). With a significance value of 0.05 and power of 0.8, a sample size of 12 NP subjects was needed. Since there is limited evidence surrounding the VP population in this setting, we aimed to recruit 20 participants in each group to account for this uncertainty.

Twenty-six VP subjects volunteered, 9 had NDI% >10 and were excluded, one subject did not have a specific vestibular diagnosis and 2 subjects were in their 80’s making it difficult to age match to our NP and control group. Thus 14 participated in the study. Six subjects in the VP group had been diagnosed with an acoustic neuroma that had been either surgically removed (3) or was still in situ (3), 8 had Meniere’s disease. All 14 of these subjects had clinical VP deficits confirmed by the clinical examination. Results of the demographic data and clinical examination of the VP subjects to confirm eligibility are presented in Table 1. Twenty controls and 20 neck pain subjects of similar age and gender were recruited to participate in the study.

Data was explored for normality and outliers. All demographic measures presented in Table 1 were checked before further analysis using a one-way ANOVA.

Group difference analysis between all kinematic measures was conducted using a one-way ANOVA. A post hoc Bonferroni analysis was then conducted to examine where the differences existed between the three groups.

Bivariate correlation analysis was calculated for both the NP and VP groups between variables of pain (POM, VAS pain and NDI), dizziness VAS, and visual symptoms (VSS) compared to selected kinematic measures using a two-tailed Spearman calculation. Interpretation of the strength of correlation was set at 0–0.25 little or no relationship, 0.25–0.5 fair to moderate, 0.5–0.75 moderate to good, >0.75 good to excellent [4].

Significance was determined at p < 0.05. IBM SPSS Statistics 22 software was used for all analyses (www.ibm.com/au/en).

This study had ethical approval from the Human Medical Research Ethics committee at the XXXX with written informed consent provided by eachparticipant.

4.1 Kinematics

The results of this study support the existing literature on kinematic impairments in people with NP and add to the scant literature on cervical kinematics in VP vestibular patients. Specifically, the NP group moved with less speed and altered acceleration/deceleration symmetry compared to controls. There were no significant differences seen in the VP group (Table 3). This could be due to the small sample size and heterogeneous nature of the VP group. However, in VP subjects, cervical kinematics appeared to be associated with dizziness (Table 2).

4.2 Neck pain kinematics

The results concerning the NP subjects are similar to previous studies between NP and control subjects using the VR system [17]. However, the symmetry between acceleration and deceleration phases findings have been inconsistent across previous research with TTP% found to be significantly altered in NP subjects in some [16, 17], but not other studies [21]. It is possible that this is due to the current study having NP participants with higher pain VAS and NDI and thus increased levels of asymmetry between groups [16, 17]. The current study found no differences in ROM or in accuracy between groups. This is also in accordance with previous literature on ROM with similar sample characteristics in regards to NDI (37±11) and pain VAS (52±16), using different methodology [22]. However, other studies using the VR system have shown significant differences in ROM between groups [21]. Previous research using different methodologies has found accuracy to be impaired in NP patients [12, 32] and studies using the same VR system software have also shown significantly decreased accuracy in patients with NP in comparison to controls [17]. Again, differences in population and/or updated hardware might be reasons for the discrepancy. Nevertheless, the most consistent kinematic finding, in agreement with existing evidence [17], was that neck motion velocity was reduced in patients with NP, accordingly this functional impairment should be studied further searching for effective management strategies.

4.3 Vestibular pathology kinematics

This study was the first of its kind to examine cervical kinematics in subjects with VP. There were no significant kinematic differences found between VP subjects and other groups, but mean kinematic values in VP subjects showed less speed and altered symmetry of velocity profile (TTP%) in comparison to controls, but faster and more symmetrical than NP subjects (Table 2). The vestibular organs are sensitive to fast head movement and changes in position, and therefore impaired kinematics seems very relevant to their physiological function [8]. A possible reason behind insignificant results could be that subject’s diagnosed with either Meniere’s or Acoustic Neuroma were both included within the VP sample. These VP populations were specifically targeted due to their discreet unilateral vestibular pathology and known deficits. However, these disorders are and were quite different in presentation (Table 1), which could explain the large SD across all measures in this group. This could also have been due to the lower sample size of this group with difficulty recruiting relatively young VP subjects without neck pain. This finding in itself may be important to consider as 9 potential subjects with VP were excluded from this study as they had concomitant neck pain. This would support other studies that suggest that neck pain is often associated with VP [29]. Further the post hoc analysis between the acoustic neuroma and Meniere’s subjects demonstrated generally poorer mean scores for cervical kinematics in the Meniere’s group. This is likely due to higher levels of dizziness and visual symptoms in this group (Table 1) and concurs with the correlation findings (Table 5). Future research should thus consider a larger group of those with VP, consider those with concomitant neck pain and or higher levels of dizziness and visual disturbances. Given the results of the current study it would seem that those with vestibular pathology and neck pain and those with higher levels of dizziness would have greater kinematic deficits.

In addition, it is yet unknown whether interventions aimed at improving cervical kinematics may be found effective in reducing vestibular symptoms. Clinically, cervical kinematic training using a VR system or a laser and target for people suffering NP has shown improvements in dynamic balance, neck disability and cervical motion kinematics [2]. It is possible that this approach may also benefit those with VP and demonstrated cervical kinematic impairment. Future research should explore this.

Interestingly in the current study, in nearly all measures, all groups including asymptomatic controls reached faster peak and mean velocities [17], higher ROM [21] and more symmetrical TTP% than our previous studies [17]. The reason behind the higher values are most likely due to the updated Oculus rift hardware used here, which has better tracking and motion sensors than previous hardware (Vuzix, www.vuzix,com).

4.4 Correlations

There were some significant correlations between dizziness to selected kinematics in both the neck pain and the vestibular pathology groups. These are interesting findings yet is a logical conclusion. Stimulation of the vestibular or cervical afferent system via head and neck movement can cause symptoms of dizziness and loss of balance [3]. Similarly, avoidance of activity and stiffness of the neck, seen in some VP patients to prevent episodes of dizziness, could potentially impact on cervical kinematics. The results of this study suggest that it is reasonable that anyone who experiences neck pain and or dizziness, as a result of head movements, may have altered cervical kinematics. Further, when considering VP subjects specifically it is possible that kinematics are primarily affected only those who have dizziness. There was large variability in these factors in the VP group, which may have affected the results and future studies looking at cervical kinematics in VP should consider those with moderate levels of dizziness as inclusion criteria for the vestibular group.

A surprising finding was a significant moderate negative correlation between accuracy in the sagittal plane and dizziness intensity in VP group. This was not seen in the NP group. It is possible that sensory reweighting from vestibular to cervical input in those with VP may have caused improved accuracy in this group.

4.5 Limitations

There were three main limitations to this study. Firstly, fear of motion and anxiety were not measured. This would have been interesting to examine and compare between groups as other studies have found inconsistent findings regarding the relationship between fear of motion and ROM in all directions [19, 27]. It is recommended that this be examined in future research.

Another limitation was the older sample size due to VP population being diagnosed more commonly over 40 years. All groups needed to be generally age and gender matched which limits the ability to compare between other studies with a younger population and limits the generalisation of the study.

The sample size for the VP was small. Future research may need to recruit more VP participants to further investigate the findings presented in this paper. As mentioned above, of particular interest would be to include a larger VP group and or VP subjects who experience moderate levels of dizziness and visual disturbances as well as those with secondary neck pain.