The assessment of the balance system in cranial artery stenosis

Abstract Introduction Vertigo and balance disorders are a significant clinical problem, especially in elderly patients. The narrowing of cranial vessels may be asymptomatic or produce neurological symptoms. Very often nonspecific signs of ischemia occur, such as headache, vertigo, or dizziness. Objective The objective of the study was to assess the effect of carotid and vertebral arteries stenosis on the function of the equilibrium organ on the basis of electronystagmography and posturography. Material The study was conducted in 63 patients, presenting with carotid and vertebral arteries stenosis. The control group consisted of 32 healthy persons. Methods All patients were subjected to precise audiological and otoneurological diagnostic examinations. Prior to being qualified for the study, patients were subjected to the assessment of arteries by means of Doppler ultrasonography. The vestibular organ was assessed by means of physical examination as well as by electronystagmography and posturography testing. Results and conclusions The study revealed statistically significant reduction in the results of the equilibrium organ assessments in patients with carotid and vertebral arteries sclerosis as compared to the control group. Abnormal ENG records in the study group patients were observed particularly in the pendulum test, optokinetic test, and the assessment of positional nystagmus, possibly indicating disturbances within the central part of the equilibrium system. Disturbed blood flow in arteries had also an important impact on spinovestibular reflexes and resulted in disturbed postural stability control. On the basis of the conducted studies, it is concluded that diagnostic examinations for carotid and vertebral artery stenosis should be performed in patients with equilibrium system disorders.


| INTRODUC TI ON
Vertigo and balance disorders are a significant clinical problem, especially in elderly patients (Hannaford et al., 2005;Maarsingh et al., 2010;Yardley, Owen, Nazareth, & Luzon, 1998). They occur in around 30% of people over the age of 65 and in 50% of those over 80 (Hannaford et al., 2005). Diagnosis and treatment of patients with balance disorders require vast knowledge and experience as well as multidisciplinary and multidirectional diagnostic actions.
Emboli of the cerebral arteries, including internal carotid arteries and vertebral arteries, are the most frequent among the causes of dizziness of the central origin with the ischemic nature (Dietrich, 2002).
They may indicate clinically relevant stenosis of the cranial arteries, mainly in the area of the vertebral artery and internal carotid artery, as well as the risk of ischemic stroke. Dizziness may be the only symptom of TIA in the vertebral-basilar system, in the course of subclavian steal syndrome, chronic dysfunction of the vertebral-basilar system, ischemic brain stem and cerebellum syndrome, and cerebellar hemorrhage (Gutmann, Wollenberg, Krampert, & Mees, 1993;Mees, Gutmann, & Wollenberg, 1992).
The available scientific reports do not accurately explain the correlation between dizziness and stenosis of the cranial arteries.
The aim of the study was to assess the impact of cranial artery

| Control group
The control group consisted of 32 healthy persons (14 men, 18 women) aged from 48 to 75 years (mean age M = 61, standard deviation SD ± 7 years). People qualified to this group did not report any middle ear disorders, hearing problems, dizziness, or balance disturbances; no pathology was found on the otolaryngological examination; the tympanic membrane was normal in the otoscopic test.
In persons from this group, an ultrasound examination of the cranial arteries was performed, the result of which was normal. The medical history excluded cardiovascular diseases.
These were patients with stenosis of the cranial arteries, referred to the Department of Vascular Surgery of the University Clinical Hospital in Wrocław in the years 2014-2015. The patients were divided into two age groups (45-60 years, 61-75 years). The study excluded patients with previous cranial trauma, meningitis, and neurological disorders (including epilepsy, multiple sclerosis, and Parkinson's disease). The analysis did not take into account patients receiving ototoxic medications, with the history of hearing and balance problems, as well as subjects with ENT abnormalities. During the study, none of the patients received medications that could affect the nervous system. All subjects were a group homogeneous in terms of the degree of cranial artery stenosis. Patients with internal carotid artery stenosis between 70% and 90% or with a peak systolic velocity of the vertebral artery flow above 120 cm/s were qualified to the study group.
The examined patients were classified into the following groups: patients with unilateral vertebral artery stenosis (n = 23), patients with unilateral carotid artery stenosis (n = 28), and patients with bilateral internal carotid artery stenosis (n = 12).

| ME THOD
All patients were subjected to thorough otoneurological diagnostic procedures. In the first stage, a detailed medical history was taken.
It covered the main ailment, chronic and past diseases with particular emphasis on the pathology of the middle and inner ear and the presence of any complications of the main disease, as well as conditions that may affect the hearing and balance organs, dizziness, and balance disorders. Attention was paid to the presence of symptoms that could indicate vestibular-cochlear organ disorders, such as headache, unstable body posture, problems with daily activities, or the loss of independence in performing basic activities. The assessment also included the risk factors of damage to the hearing and balance organ by exposure to the noise at work or as a result of taking ototoxic drugs.
Each patient was consulted by a neurologist and ophthalmologist.
Prior to qualifying to the study, the cranial arteries were evaluated using Doppler ultrasonography.
The otolaryngological examination was performed in each patient.
The vestibular organ was assessed in the physical examination, including Romberg's, Unterberger's, and Babiński-Weill's tests. In the next stage, objective tests, such as posturographic and electronystagmographic (ENG) examinations, were carried out.
The ENG examination was carried out with the help of a Hartmann two-channel computer electronystagmograph. The study assessed the occurrence of nystagmus, which is an objective symptom of vestibular disorders. The registered eye movements were perceived by electrodes located on the forehead and temples.
Electronystigmographic examination recorded: were assessed as normal (I type), distorted (II type), and completely distorted (III type), • caloric tests were performed by the Fitzgerald-Hallpike method.
The test was carried out using water at 30 and 44°C. The irrigation time was 30 s. Nystagmus assessment was performed by analyzing by the computer system the frequency of nystagmus deflections in selected 30 s of the peak of reaction. The Jongkees formula was used to assess nystagmus symmetry.
The ENG record also evaluated the presence of square waves, dysrhythmia, and dysmetry.
Vestibulospinal reflex tests were performed using a VSR Basic Balance Master posturograph from NeuroCom International Inc.
The strength plate was calibrated to the height of the subject, and the patient's center of gravity was presented on the monitor screen.
The study was preceded by registration of the study age, weight, and height. During the tests, the patient stood upright, his arms along the torso. Body posture control was assessed by performing five tests: Each test was performed three times and each test lasted 10 s. The mean velocity of the center of gravity deflection was evaluated.

Unilateral Stance Test-US
The patient stood on the right, then on the left leg with eyes open and closed. The patient performed each of the trials three times. The mean velocity of the center of gravity deflections in degrees per second was analyzed.

Limits of Stability (LOS) test
During the test, the patient saw his marked center of gravity on the monitor screen, which he had to keep in the center. After the sound signal, the patient had to move his center of gravity to the target point in the shortest time and by the straightest way. Eight directions were studied-front, back, left, right, and four diagonals.
Recorded were as follows: • response time (RT)-time from the moment of visual and acoustic signal to the beginning of the movement, • center of gravity swivel speed (MVL) to first end point (EPE), • direction control (DCL), that is, the comparison of the number of moves toward the target compared with the number of incorrect moves in percentage, • final intended swing in percentage (MXE).

5.. Rhythmic center of gravity transfer test (RWS)
The patient shifted his center of gravity sideways (L-P) or forward-backward (P-T), the tilting rhythm imposed the cursor on the screen moving at a speed of 1/s, 2/s, 3/s. The mean velocity of the center of gravity movement in degrees per second and the direction control value (DCL) resulting from the comparison of the number of movements were evaluated toward the goal to uncoordinated movements in percentage.

All procedures performed in studies involving human participants
were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study was accepted by ethics committee in Wroclaw Medical University.

| The analysis of electronystagmographic examination results
The ENG showed many abnormalities in patients with cranial artery stenosis. Spontaneous nystagmus with closed eyes was reported in 20 (31.8%) patients from the study group, while none of the persons from the control group demonstrated nystagmus, this difference was significant (p < 0.05). In the study group, positional nystagmus was observed in 33 (52.4%) patients, with the majority of Nylen I (28.6%) and Nylen III type nystagmus (22.2%). Abnormal optokinetic nystagmus was significantly more frequently (p < 0.05) observed in the study group compared with the control group (32 patients-50.8% vs. two patients-6.3%). An abnormal record was also significantly more often (p < 0.05) observed in the pendulum test in patients from the study group compared with the control group (24 vs. two persons). Square waves were statistically significantly more frequently (p < 0.05) reported in the ENG record in patients with cranial artery stenosis compared the control group (19 vs. 0). These data are illustrated in Table 1.
The analysis of the ENG results in patients from the study group did not show statistically significant differences depending on the age and the type of narrowed artery.

| Analysis of posturography results
The analysis of posturographic parameters in the study group demonstrated many statistically significant differences in com-  Table 2.
In the study group, the analysis of posturography results did not show statistically significant differences depending on the age of patients.
Patients with internal carotid stenosis achieved statistically significantly (p < 0.05) worse results in the US test and the LOS test compared to patients with vertebral artery stenosis.
Patients from the study group with the positive history of vertigo achieved statistically significantly (p < 0.05) worse results in all tests compared with the patients from the study group without vertigo (Table 3).

| D ISCUSS I ON
Inner ear disorders are very often overlooked in the diagnosis in the elderly, both by patients and doctors. Dizziness or vertigo is usually due to minor causes; patients experience a decrease in the quality of life, but, there is no risk of complications that may lead to further loss of health or death.
Benign positional dizziness is the most common cause of vertigo and balance disturbances (Kroenke, Hoffman, & Einstadter, 2000).

Vertigo of the vascular origin is a very important clinical problem.
Even though it is the second most common cause of all cases of vertigo (10%), it is a threat to the health and life of the patient. Although hearing loss, tinnitus, and vertigo may be the only symptoms preceding stroke (Seemungal, 2007), the problem of the impact of flow disturbances in the cranial arteries on the inner ear has not been thoroughly examined so far.
In our study, the assessment of the balance system disorders was based on the examinations which are a gold standard in dealing with these conditions. The balance system was evaluated on the basis of ENG and posturography. These tests require experi-   Eckstein et al. (2008) and Melliere et al. (1992) which positional nystagmus develops could not be fully explained (Brandt, 1990). Abnormal optokinetic nystagmus was reported in 32 (50.8%) patients from the study group and in two subjects (6.3%) from the control group. Many authors have described the distortion of optokinetic nystagmus, also of the vascular origin, in damage to the central nervous system. The abnormal result of the pendulum test was recorded in 24 (38%) patients from the study group and in two (6.3%) subjects from the control group.
Square waves were also significantly statistically (p < 0.05) more frequently observed in patients from the study group; they were found in 19 (30.2%) patients with cranial artery stenosis. Square waves were not reported in the ENG in any patient from the control group. In addition, dysmetry (in one patient) and dysrhythmia (in three patients) were detected in patients with cranial artery stenosis. These test results indicate significantly more frequent disorders of the central origin in the ENG, which is associated with cerebral ischemia caused by atherosclerosis and clinically relevant stenosis of the cranial arteries. Similar observations were made by other researchers (Grad & Baloh, 1989). According to the authors quoted above, this proves multilevel damage to the balance system.
There were no statistically significant differences in ENG results between patients with vertebral artery stenosis compared to subjects with internal carotid artery stenosis, but spontaneous nystagmus was more common in patients with vertebral artery stenosis (39.1% vs. 27.5%). However, the presence of positional nystagmus was more frequently recorded in patients with internal carotid stenosis (type Nylen 1 32.5% vs. 21.7%; type Nylen 3 27.5% vs. 13%), but these were not statistically significant differences. In the group of patients with internal carotid artery stenosis, an abnormal record in the pendulum test and square waves were more frequent. These results suggest an advantage of balance disorders in the vestibular organ in patients with vertebral artery stenosis, while in subjects with internal carotid artery stenosis, abnormalities of the central-neurological origin are more often. It is significant the patients with internal carotid artery stenosis manifest Significance means that p is less than or equal to .05.

TA B L E 2 (Continued)
TA B L E 3 The comparison of posturography results obtained in patients from the study group with and without dizziness (number and proportion of abnormal results)  Broussard, DeRocher, and Kalkofen (1996), the load on the lower limbs is almost similar and the differences do not exceed 7%.
The abnormal mean speed of the center of gravity tilt in the   (Norre, 1993;Riach & Starkes, 1993). The correct result of the LOS test depended on properly functioning visual coupling.
The patient's reaction time to a command to move was an important element of the LOS test which depended mainly on higher nervous functions (Hirabayashi & Iwasaki, 1995). Although in patients from the study group, the reaction time was delayed compared with subjects from the control group, this difference was not statistically significant.
In the RWS test, in patients with cranial artery stenosis, significant

| LIMITATI ON S OF THE S TUDY
The study has not been randomized. The group of patients was relatively small. That was due to narrow study inclusion criteria. A full package of otoneurologic examinations comprised a study cycle lasting approximately 3 hr. A need for patients to focus on the study and to cooperate with a technician in charge of the examinations gave rise to the situation, in which some of the patients were not able to finish their study cycle. Therefore, they must have been excluded from the study group. Significance means that p is less than or equal to .05.

TA B L E 3 (Continued)
The following were indicated: follow-up examinations, a new series of examinations to check the repeatability of the results, and-on the oc-

Diagnostic examinations for carotid and vertebral artery stenosis
should be performed in patients with equilibrium system disorders.

ACK N OWLED G M ENT
We thank prof. Dariusz Janczak for useful discussions. We thank Wroclaw Medical University for support.

CO N FLI C T O F I NTE R E S T S
Authors declare that they have no conflict of interest. Zatonski. Tomasz Zatonski supervised the project. All authors discussed the results and contributed to the final manuscript.

DATA AVA I L A B I L I T Y S TAT E M E N T
All data analyzed during this study are included in this published article.