Head-Eye movement control tests in patients with chronic neck pain; Inter-observer reliability and discriminative validity

Neck pain is a common problem, with lifetime prevalence in the general population worldwide of up to 71%[1, 2]. Impaired head-eye movement control is an identified problem in patients with chronic neck pain, particularly in patients with whiplash associated disorders (WAD). Symptoms associated with head-eye movement control impairment are dizziness, headache, light-headedness and visual disorders[3]. Movements requiring the coordination of neck, head and eyes are known to provoke those symptoms. A well-known example is driving a car after whiplash trauma, where Gimse found changed eye movements during car driving[4]. He also found altered eye movements during reading and differences in smooth pursuit eye movements with the head in the neutral position[5]. In patient anamnesis, symptom provocation was found during walking, fast head rotations and observation of moving objects. Oculomotor dysfunctions after cervical trauma were described by Hildingssons and colleagues[6‐8]. Yahia and colleagues found abnormal dynamic and static balance in patients with chronic neck pain and dizziness[9]. Humphreys and colleagues[10] investigated neck pain in 180 patients: one third reported dizziness.

Following Treleaven and colleagues[3], dizziness is a frequent symptom in patients with neck pain and WAD. They assumed the underlying mechanism to be a convergence dysfunction of the sensorimotor input from the cervical spine, the vestibulum and the visual postural system. This theory is also supported by other authors[11‐14]. Heikkilä et al.[11], found a reduced range of cervical motion and decreased upper cervical proprioception, which affects the voluntary eye movement. Peterson[13] postulated the head-neck motor system as an ideal model for understanding issues of complex motor control and Armstrong[14], mentioned that sensory information from neck proprioceptors is processed in tandem with information from the vestibulum, cerebellum and cortex.

Following diagnosis of a dysfunction of convergence, the management of an intervention is based on the clinical presentation and the functional impairment. The following assessments are recommended to measure the functional impairment and are used in clinical practice: joint position error (JPE)[12], "The Fly" movement method[15], smooth pursuit neck torsion test (SPNT)[16], postural stability and balance, as well as oculomotory and head-eye coordination tests[17, 18].

In this study, the selection of our tests was influenced by some of the research tests outlined above. The test battery had to meet the following criteria: have the ability to transfer the research results into practice; be simple; performed without high-tech equipment; easy to learn; and, preferably, be low cost. The test battery of five tests was performed in the sitting position and the standing position. The latter, with feet together to achieve a more challenging balance position[19].

Eye movement was tested according to Jull and colleagues[19]. They tested eye-follow in both neutral and in relative 45°neck rotation, using the elements of the smooth pursuit neck torsion test from Tjell[16]. Tjell compared eye movements performed with the head in neutral position to a position in 45° relative head rotation. He reported significant differences between these two positions in patients with whiplash trauma compared to patients with vestibular pathology. Because of the unavailablity of equipment for standardizing eye movement velocity, in the present study the eye movement tests were performed differently to Tjell et al.[16]. The participants were asked to move their eyes horizontally from side to side as quickly as possible, while actively maintaining their initial fixed head position.

Treleaven and colleagues[3] showed that patients with WAD have decreased velocity of movement in the sequential head and eye movement test and in the gaze stability task, compared to healthy controls. Furthermore, patients with WAD have a reduced active range of motion of the cervical spine in the gaze stability test. These altered movement patterns were associated with a higher score in the Neck Disability Index (NDI)[3]. However, this data was collected using sophisticated laboratory equipment to measure eye movement in association with head movement. A physiotherapeutic diagnosis, is based on visual observation of the patients’ impaired head-eye movement. According to Treleaven[20] visual clinical observation of the quality of head and eye movement, in conjunction with symptom provocation, is the suggested method for assessment of oculomotory dysfunction. Qualitative and quantitative aspects of movement, as well as symptom provocation, are references for physiotherapeutic intervention[10, 19]. Range of motion and velocity of movement is difficult to measure without technical equipment but the quality of movement control can be visually inferred[21]. To date, the reliability of visual observation of head-eye coordination tests has not been investigated.

The main objectives of the present study were to:

Our hypothesis was that, "Visual assessments by physiotherapists of head-eye movement control deficit are reliable and that these tests are able to discriminate between controls and patients".

We also hypothesized a greater head-eye control deficit in the standing position compared to sitting, since the latter is a more challenging balance position and requires increased coordination.

Visual rating by physiotherapists of head-eye movement control tests is reliable. Predefined criteria for inter-tester reliability were fulfilled. Similar results for inter-tester reliability were reported by Luomajoki et al.[21], when videos of movement control tests of the lumbar spine were visually evaluated.

In the present study, the discriminative validity was supported with DOR values above 13 to 18, for persons with 2 or more positive tests out of 5. This means that patients with chronic neck pain and associated symptoms, such as dizziness, visual disorders, etc., are up to 13–18 times more likely to have 2 or more tests positive than healthy controls. For the clinical diagnosis of head-eye movement control impairment, a cut-off point of 2 positive results out of 5 tests in sitting or standing position is recommended.

Results showed there was no significant difference between the numbers of positive tests in the sitting and standing positions. Therefore, the hypothesis of an observable increase in head-eye movement control impairment in the standing with feet together position was not confirmed. Since all participants were first tested in sitting and then in standing position, the results also imply that there was no relevant accumulation of fatigue or learning adaptation. The test battery can, therefore, be reduced to five tests. We recommend the tests to be performed in the sitting position in order to minimise the risk of falling in patients with dizziness.

Visible differences between controls and patients were identified in the tests performed: patients with chronic neck pain showed a decelerated velocity of head and eye movements and distinctive movement quality. These results are in line with previous research[3].

The strength of these tests is that they can be performed by all subjects and do not require technical equipment, such as an oculograph. Results showed that quality differences were visually identifiable during the10 seconds performance per test. This is important for general clinical use, since assessment is fast and requires little installation. These tests could be of assistance in the daily clinical practice of physiotherapists, in deciding whether rehabilitation for eye-head movement control impairment is necessary.

Based on the results from previous research, methodological adaptations to the tests were made in order to adapt them to a clinical environment. The measurement of quantities, such as velocity and range of motion, is impossible without technical equipment; therefore, our tests were rated on the quality of movements. In the present study, impaired quality of movement control was characterized by a short interruption during the change of direction and irregular or uncoordinated, decelerated eye movements. Decreased active stabilization of the head position during the eye movements test was also a positive rating criterion. Difficulty in keeping a fixed gaze during the gaze stability test was a regular occurrence in the patient group and was a criterion for a positive rating. Difficulty in dissociating head and eye movements in the sequential test was typical and clearly visible for a positive rating in this test.

The rating of the head-eye movement control tests used in this study can be easily learned from a short instruction video.

The methodology had to be adapted so that the tests could be videotaped. The chosen videotaping method meant that we were only able to measure horizontal eye movement. Other movement directions would have resulted in the pupil being covering by the eye-lid on the tape. This limitation would not be present in daily clinical practice, where vertical and diagonal movements could also be assessed".

To exclude the impact of pain avoidance strategies[28] and mimic reactions from the videos, an inclusion criterion was a symptom-free active range of 45° head rotation to both sides.

There are certain limitations in the present study that need to be addressed. The intake of drugs was not considered. Since medication may have an influence on the velocity of head-eye movements, this information should be provided. The incidence of light was not standardized but, as there was no direct light from any side, it did not disturb the participants.

Contrary to clinical practice, raters were allowed to watch the videos several times. This may have improved inter-observer reliability. In clinical practice however, the physiotherapist is also able to repeat testing and, in addition, use symptom provocations and other assessments for clinical diagnostics. Unexpectedly, no male patients were included in the study because of recruitment problems. However, neck pain and WAD are more common in women[2, 29].

Contrary to Treleaven and colleagues[3], the study also included patients with no neck acceleration trauma. The reason for including these subjects was that research has shown that head-eye coordination impairment is also prevalent in neck pain patients without trauma[29, 30]. Two participants of the controls reported minor historical neck trauma but, since they had had no neck pain problems for many years, they were also included in the control group.

Further research should evaluate test-retest reliability in patients with stable symptoms. A correlation between head-eye coordination and NDI scores was not evaluated in this study, nor were differences in the performance of the trauma and non-trauma patient groups. These could be of further interest.

Moreover, following diagnosis and treatment, changes in head-eye coordination tests should be evaluated in relation to changes in patients’ limitations in daily life.

Visual assessment by physiotherapists of head-eye movement control tests is reliable. No differences between test performance in the sitting and standing positions were identified: the test battery can be reduced to five tests. Our subsequent recommendation was that tests be performed in the sitting position. The test battery can discriminate between patients with chronic neck pain and healthy controls. Two or more positive tests out of five can be interpreted as impaired head-eye movement control. Further research is needed to determine test-retest stability and responsiveness.

EDC: physiotherapist FH MAS ZHAW, PT OMT IFOMT, CRAFTA®, owner of a physiotherapy practice in the -Zentrum für Manuelle Therapie- Zurich, instructor at the University of Zurich, Department of Chiropractic Medicine, CH-8008 Zurich. JAH: physiotherapist FH MAS ZHAW, PT, OMT IFOMT, owner of a physiotherapy practice in CH-8132 Egg, instructor Kaltenborn- Evjenth-Conzept®. AM: physiotherapist, MSc Statistics, Institute of Physiotherapy, School of Health Professions, ZHAW Zurich University of Applied Sciences, CH-8401 Winterthur. HL: physiotherapist, MSc, PhD, Researcher and Lecturer, Institute of Physiotherapy, School of Health Professions, ZHAW Zurich University of Applied Sciences, CH-8401 Winterthur. JK: physiotherapist, MSc, PhD, Head of Research and Development, Institute of Physiotherapy, School of Health Professions, ZHAW Zurich University of Applied Sciences, CH-8401 Winterthur.