Usefulness of postural sway spectral analysis in the diagnostic route and clinical integration of cervicogenic and vestibular sources of dizziness: A cross-sectional preliminary study

Abstract

BACKGROUND:

Posturography power spectra (PS) implementation has been proven to discriminate between sensory inputs detriment of vestibular and proprioceptive origin.

OBJECTIVE:

To deepen the role of posturography testing in the diagnostic route of dizzy conditions, by comparing two groups of patients –93 affected by cervicogenic dizziness (CGD) and 72 by unilateral vestibular hypofunction (UVH) –with a group of 98 age- and gender-matched healthy subjects, serving as control group (CON).

METHODS:

All participants underwent otoneurological testing including video head impulse test (vHIT) and posturography testing with PS analysis. They also filled in Dizziness Handicap Inventory (DHI), Tampa Scale for Kinesiophobia and Hospital Anxiety and Depression Scale questionnaires.

RESULTS:

UVH and CGD patients were found to have significant increase in vestibular- and proprioceptive-related PS values when compared with CON. Receiver operating characteristic curves found PS values to reliably discriminate both groups from CON. Positive and negative correlations were respectively found between vestibular-/proprioceptive-related PS domain and DHI in both groups and between PS and vHIT scores in UVH patients.

CONCLUSIONS:

PS analysis demonstrated to be useful in differentiating CGD and UVH patients each other and when compared to CON, to objectively represent perceived symptoms filled along the DHI scale and to corroborate the rate of vestibular deficit in UVH patients.

Keywords

Posturography testing cervicogenic dizziness fast fourier transform video-head impulse test unilateral vestibular hypofunction

1 Introduction

The complaint of “dizziness” is a vague descriptor of a multitude of sensations that can be attributable to a variety of pathophysiological processes [49]. Apart from cardiovascular/metabolic explanations and central nervous system disorders, the main causes of dizziness include peripheral vestibular dysfunction (i.e. unilateral vestibular hypofunction, UVH) and conditions involving the cervical spine, referred to as cervicogenic dizziness (CGD) [12]. CGD is a motion sensation deriving from a proprioceptive disturbance of the neck [17], it is characterized by the presence of imbalance, unsteadiness, disorientation (i.e. the feeling of being “lost”), neck pain, limited cervical range of motion, and may be accompanied by headache [27, 57]. To be considered CGD, dizziness should be closely related to changes in cervical spine position or cervical joint movement [45]. Many cases of CGD have been diagnosed post-whiplash injury, or have been associated with inflammatory, degenerative, or mechanical dysfunctions of the cervical spine [37 , 48], possibly resulting in a disruption of the cervical proprioceptive inputs to the vestibular nuclei [22, 48].

Despite these aspects, CGD still remains a clinical condition achieved by exclusion criteria; that is, its diagnosis exists considering that no single test is able to definitely verify the condition, and it cannot be confirmed by outcome, imaging, laboratory values, or unique signs and/or symptoms [13, 48]. Diagnoses by exclusion are challenging for healthcare practitioners and patients because a strong understanding of the sequencing of proper tests and measures - reliable to rule out or rule in competing diagnoses - is needed. In particular, such uncertainties in diagnostic route reflect i) doubts regarding the causes underpinning the symptoms of imbalance, unsteadiness, and disorientation and ii) those neuropsychological disturbances which equally affect subjects suffering both from proprioceptive and/or peripheral vestibular conditions [16 , 54].

Given these aspects and recent evidences demonstrating vestibulo-ocular reflex (VOR) analysis, by means of diverse clinical tests, as not fully conclusive in the diagnostic route of patients complaining from dizziness-related symptoms [30, 56], previous experiences proposed to objectively assess postural instability by means of posturography measurements [16 , 59]. Indeed, this time-sparing technique and its implementations [16 , 59] have proven to be useful in detecting significant alterations in body sway during perturbating situations, as well as abnormalities in somatosensory and visual input ratio. This has been confirmed especially due to power spectra implementation, an analysis which has been largely used in postural assessment when handling both vestibular and proprioceptive deficits. [2 , 61].

Thus, considering that chronic vestibular hypofunction and spinal proprioceptive disorders represent frequent, often underdiagnosed causes of chronic dizziness in clinical practice, the aim of the present preliminary study is to further deepen the role of posturography testing in defining the diagnostic route and integrate the clinical aspects of these conditions, by means of a cross-sectional study comparing two groups of patients –affected by CGD and UVH –with a group of healthy subjects, serving as control group (CON).

2 Materials and methods

2.1 Participants selection

Participants were prospectively recruited from the ITER Center for Balance and Rehabilitation Research, a regional institutional interdisciplinary disorder clinic, and University of Rome Tor Vergata, after their enrolment in the local longitudinal cohort study. Considering the lack of specific tests recognized for the diagnosis of CGD, general accepted criteria supported by the literature were operationalized in order to achieve the clinical suspicion in right-handed subjects ranging from 18 to 65 years of age [24, 57], as following: 1. Exclusion of these differential diagnoses: a. Migrainous vertigo b. Vertigo of central origin c. Benign paroxysmal positional vertigo (BPPV) d. Meniere disease e. Vestibular neuritis f. Vertigo induced by drugs g. Psychogenic vertigo (anxiety and/or panic disorder and/or phobia) h. Orthostatic hypotension 2. Presence of a subjective feeling of dizziness associated with pain, movement, rigidity, or certain positions of the neck from at least 3 months; 3. Cervical pain, trauma, and/or disease 4. If from traumatic origin, there has to be a temporal proximity between the onset of dizziness and the neck injury. Diagnosis of CGD was considered if criteria 1 to 3 were fulfilled. As for criterion 2, dizziness had to occur during the same period than neck pain occurred and dizziness had to be proportional to the severity of the neck pain that generally fluctuates in time. Criterion 4 addresses cervicogenic dizziness occurring after a neck trauma [16, 59]. Specific exclusion criteria for this group were: presence of trauma or recent surgery in the head, face, neck, or chest; an otoneurological diagnosis of central or peripheral vertigo, and receiving physiotherapy during the study period.

Furthermore, in line with previous studies demonstrating functional correlations between vestibular dominance and side of vestibular lesion [6, 7], only right-handed patients affected by right chronic UVH participated in the study. According to accepted criteria [18], the diagnosis of chronic UVH was achieved by responses to bithermal water caloric irrigations, with at least 25%reduced vestibular response on one side when calculated by means of Jongkees’ formula after at least 3 months from the onset of symptoms [3, 18].

Finally, age- and gender-matched right-handed healthy subjects –with appropriate educational and cognitive level - were examined and included in the CON if they met the following criteria: (1) experiencing no neck pain or dizziness over the past 6 months, and (2) being 18 to 65 years old. Individuals belonging to all groups were required to report negative anamnesis for malignancy, head trauma, neuropsychiatric disorders, metabolic, cardiovascular, endocrine, infectious and other otoneurological diseases. A routine blood test was performed, in order to exclude subjects with undetected metabolic/endocrine conditions, while neurological disturbances were excluded using the Mini Mental State Examination (MMSE) and prescribing Magnetic Resonance Imaging in all participants in the study. Finally, no patient was pregnant or breastfeeding and all subjects taking drugs possibly affecting otoneurological/postural functions were excluded. The study was approved by the University Hospital Institutional Review Board, it adhered to the principles of the Declaration of Helsinki and all the participants provided written informed consent after receiving a detailed explanation of the study.

Evaluation criteria suggested in literature [35, 57] and including history, physical examination and a thorough clinical otoneurological examination (including pure tone audiometry and impedance, binocular electrooculography analysis with positional maneuvers, Head Shaking Test, clinical Head Impulse Test [cHIT] as well as limb coordination, gait observation and Romberg stance Test) were devised to exclude other causes of dizziness [28, 32] before the three groups of subjects underwent:

3 Objective testing

3.1 Video Head Impulse Testing (vHIT)

For vHIT measurements the EyeSeeCam System and the technique proposed in previous studies were used [9, 33]. The vHIT results were classified as abnormal if two conditions were met: abnormal gain according to the calculated normative data and presence of refixation saccades (revealed by visual inspection, according to Blodow et al. [9]). With the manufacturer’s software (OtoAccess), both side median (med) values recorded at 60 milliseconds were extracted on.xls files for raw analysis. In line with previous procedures [9 , 33], diagnosis of UVH was confirmed in the present cohort in case of gain below 0.85 and 0.82 for the right and left sides respectively. This was calculated as the lower cut-off value of the gain-reference range (mean_normal±2(standard deviations; SD) equal to 0.93±2(0.04) and 0.92±2(0.05) for right and left side respectively), incorporating 95%of healthy population, age- and gender matched with the current population of patients [9 , 32] and including the above-mentioned normal volunteers in our laboratory.

3.2 Static posturography testing

Each patient was instructed to keep an upright position on a standardized platform for static posturography (EDM Euroclinic). The recording period was 60 seconds for each test (eyes closed or open while standing on the stiff platform) and the sampling frequency in the time domain was 25 Hz [2, 33]. The center of pressure was monitored, while performing the test. The posturographic parameters considered in our study were the path length (length), the 95%confidence ellipse area (area) both calculated according to Prieto et al. [44], and the fast Fourier transform (FFT) elaboration of oscillations on both the X (right-left) and Y (forward-backwards) planes [2, 33]. Time-domain oscillation signals (X and Y) were extracted from the original manufacturer’s software into.txt format and the FFT elaborations were gained through a core function implemented on Matlab space (Appendix A) [32, 33]. Spectral values (power spectra, PS) of body oscillations were quantified on an.xls file, for every frequency from 0.0122 to 4.9927 Hz [33]. As in previous experiences [33], we subdivided the frequency spectrum into three groups: 0.0122 to 0.6958 Hz (low-frequency interval); 0.708 to 0.9888 Hz (middle-frequency interval); 1.001 to 4.9927 Hz (high-frequency interval). Following previous experiences accounting for the reliability of this method [1, 14], within each frequency spectrum group, the spectral intensity was determined by adding the PS recorded for each frequency and the mean PS of the same group.[2 , 33].

4 Self-report (SRM) and Performance Measure (PM)

The Italian Dizziness Handicap Inventory (DHI) version comprises 25 questions designed to assess a patient’s functional (DHI-F; 9 questions), emotional (DHI-E; 9 questions), and physical (DHI-P; 7 questions) limitations on a three-point scale [39].

Fear of movement was quantified with the Italian language version of the Tampa Scale for Kinesiophobia (TSK-17), a 17 item self-report questionnaire in which each question was scored using a 4-point Likert scale ranging from 1 (strongly disagree) to 4 (strongly agree); 4 items (4, 8, 12, and 16) were negatively worded and reverse scored. Total score ranges between 17 and 68 points, with higher scores indicating a higher degree of kinesiophobia [36].

Anxiety and depression were evaluated with the Hospital Anxiety and Depression Scale (HADS). This self-administered questionnaire contains 14 items, rated on a 4-point Likert type scale (from 0 to 3 points). The tool includes 2 subscales of 7 items that assess anxiety and depression. The Italian-language version of the HADS has good psychometric properties [10].

5 Data handling and statistical analysis

The X² test was carried out to define associations between categorical factors and groups. Mean and standard deviations (SDs) of objective testing and SRM/PM scores were calculated in all groups. To assess that data were of Gaussian distribution, D’Agostino K squared normality and Levene’s homoscedasticity test were applied (where the null hypothesis is that the data are normally and homogeneously distributed). A mixed analysis of variance was performed with the groups as between factors for each objective and SRM/PM variable. Gender, age, MMSE, educational level and time from CGD/UVH diagnosis (elapsing time, ET, in months), were treated—where possible—as categorical and continuous predictors. The significant cut-off level (α) was set at a p value of 0.05. Bonferroni correction for multiple comparisons was used for the post hoc test of the significant main effects. Then, a two-tailed Spearman’s rank correlation was performed between significant objective testing and SRM/PM scores in the CGD/UVH groups of subjects. Given the large sample size of this group and the two-tailed nature of the test, a significant cut-off level (a) was set at a p value of 0.05.

To assess the ability of posturography parameters to predict patients’ cause of dizziness, a receiver operating characteristic (ROC) area under the curve (AUC) analysis of the posturography parameters was undertaken, and values presented with their 95%confidence intervals (c.i.).

Sensitivities, specificities and likelihood ratios are reported for the optimal cut-off values (c), which have been determined by maximizing sensitivity and specificity for each ROC curve by means of the Youden Index (J), which defines the maximum potential effectiveness of a marker and is formally defined as J = maximum {Sensitivity (c) + Specificity (c) –1} (STATISTICA 7 package for Windows) [8, 20].

6 Results

6.1 Participants

Among 114 CGD and 81 UVH patients, 5 were found to take antidepressant drugs, 4 referred recent head/chest trauma, 4 were affected by BPPV, 3 demonstrated a VOR gain below the normative range and/or a mismatch between vHIT and caloric testing results, 5 were affected by diabetes, 5 were already undergoing rehabilitation treatment and 4 had history of alcohol abuse. Thus, after the exclusion of these individuals, 93 subjects (51 females, 42 males; mean age = 43.3±13.7 years) fulfilling inclusion criteria for CGD, 72 subjects diagnosed as suffering from UVH (39 females, 33 males; mean age = 45.3±14.1 years) and 98 age- and gender-matched healthy subjects (50 females, 46 males; mean age = 46±15.4 years) were enrolled in the study (Table 1). No statistical differences were found when comparing clinical and socio-demographic values of the three groups of subjects.

Table 1
Clinical and socio-demographic description of participants

CGD (n = 93) CON (n = 98) UVH (n = 72)

Age (years) 43.3±13.7 46±15.4 45.3±14.1

Male 42 48 33

Female 51 50 39

ET (months) 34.2±16.9 - 39.1±17.5

MMSE 29±0.82 29.1±0.76 29.2±0.8

vHIT

Left VOR gain 0.91±0.05 0.92±0.05 0.98±0.13

Right VOR gain 0.92±0.04 0.93±0.04 0.63±0.05

Level of education

< 4 years 21 23 16

5 –7 years 39 41 32

8 –13 years 22 21 14

> 14 years 11 13 10

UVH etiology

Neuritis - - 41

AN - - 11

Previous petrous - - 9

Previous cochlear - - 4

Ramsay-Hunt - - 7

	CGD (n = 93)	CON (n = 98)	UVH (n = 72)
Age (years)	43.3±13.7	46±15.4	45.3±14.1
Male	42	48	33
Female	51	50	39
ET (months)	34.2±16.9	-	39.1±17.5
MMSE	29±0.82	29.1±0.76	29.2±0.8
vHIT
Left VOR gain	0.91±0.05	0.92±0.05	0.98±0.13
Right VOR gain	0.92±0.04	0.93±0.04	0.63±0.05
Level of education
< 4 years	21	23	16
5 –7 years	39	41	32
8 –13 years	22	21	14
> 14 years	11	13	10
UVH etiology
Neuritis	-	-	41
AN	-	-	11
Previous petrous	-	-	9
Previous cochlear	-	-	4
Ramsay-Hunt	-	-	7

Clinical and socio-demographic aspects of cervicogenic (GCD), unilateral vestibular hypofunction (UVH) patients and helathy subjects serving as control group (CON). Time from diagnosis of UVH/CGD (elapsing time), ET; Mini-Mental State Exam, MMSE; video-head impulse test, vHIT; vestibulo-ocular reflex, VOR; acoustic neuroma, AN; petrous surgery, petrous; cochlear surgery, cochlear. Where required, mean± standard deviations are given.

According to the above-mentioned criteria for VOR gain deficit [9], UVH patients demonstrated significant reduction in the VOR gain in the affected ear (Table 1). The main symptom in UVH patients was dizziness, reported by 64 out of 72 patients (90%); 33 out of 72 patients (46%) reported vertigo, while 27 (37,5%) reported postural unsteadiness.

6.2 Posturography testing

Bonferroni correction found a significant increase in area and length parameters –in both eyes closed and open condition –when comparing UVH with CGD patients and when comparing those groups to CON subjects. The same post-hoc correction highlighted a significant increase in PS values within the low-frequency interval in eyes closed condition on X and Y plane when comparing UVH to both CGD and CON subjects. Furthermore, a significant increase in PS values within the middle-frequency interval in eyes closed condition on X and Y plane was found when comparing UVH and CGD patients to CON subjects. Finally, CGD patients were shown to have a significant increase in PS values within the high-frequency interval in eyes closed condition on X and Y planes when compared with UVH and CON subjects (Table 2, Fig. 1).

Table 2
Main effects of posturography measurements between CGD, UVH and CON subjects

CGD CON UVH

Posturography Mean SD Mean SD Mean SD Significance

Length EO (mm) 553.64^* 126.26 425.34l 124.44 634.96# 110.61 F(2, 260) = 64.962, p < 0.05

Length EC (mm) 904.89^* 148.64 595.98l 141.35 979.47# 177.06 F(2, 260) = 155.11, p < 0.05

Area EO (mm²) 547.35^* 192.06 401.76l 121.11 756.53# 252.26 F(2, 260) = 72.77, p < 0.05

Area EC (mm²) 949.97^* 303.04 599.58l 135.97 1649.66# 414.92 F(2, 260) = 267.93, p < 0.05

PS L EC X 4.73 1.7 4.74l 1.58 8.69# 1.77 F(2, 260) = 141.81, p < 0.05

PS L EC Y 2.74 1.05 2.71l 1.06 8.11# 1.73 F(2, 260) = 458.91, p < 0.05

PS L EO X 5.34 1.1 5.25 1.06 5.48 0.57 F(2, 260) = 1.089, p > 0.05

PS L EO Y 4.13 1.11 4.07 1.19 4.69 0.37 F(2, 260) = 11.95, p < 0.05

PS M EC X 0.56^* 0.03 0.29l 0.08 0.56 0.03 F(2, 260) = 642.78, p < 0.05

PS M EC Y 0.5^* 0.01 0.24l 0.06 0.5 0.02 F(2, 260) = 1109.4, p < 0.05

PS M EO X 0.35 0.1 0.33 0.08 0.32 0.02 F(2, 260) = 4.62, p > 0.05

PS M EO Y 0.23 0.06 0.21 0.05 0.22 0.02 F(2, 260) = 10.8, p < 0.05

PS H EC X 1.44^* 0.11 1.1 0.16 1.12# 0.12 F(2, 260) = 173.29, p < 0.05

PS H EC Y 1.24^* 0.09 1.03 0.14 1.07# 0.09 F(2, 260) = 81.46, p < 0.05

PS H EO X 1.05 0.14 1 0.12 1.01 0.12 F(2, 260) = 11.58, p < 0.05

PS H EO Y 0.79 0.1 0.76 0.13 0.81 0.17 F(2, 260) = 2.83, p > 0.05

	CGD	CON	UVH
Length EO (mm)	553.64^*	126.26	425.34l	124.44	634.96#	110.61	F(2, 260) = 64.962, p < 0.05
Length EC (mm)	904.89^*	148.64	595.98l	141.35	979.47#	177.06	F(2, 260) = 155.11, p < 0.05
Area EO (mm²)	547.35^*	192.06	401.76l	121.11	756.53#	252.26	F(2, 260) = 72.77, p < 0.05
Area EC (mm²)	949.97^*	303.04	599.58l	135.97	1649.66#	414.92	F(2, 260) = 267.93, p < 0.05
PS L EC X	4.73	1.7	4.74l	1.58	8.69#	1.77	F(2, 260) = 141.81, p < 0.05
PS L EC Y	2.74	1.05	2.71l	1.06	8.11#	1.73	F(2, 260) = 458.91, p < 0.05
PS L EO X	5.34	1.1	5.25	1.06	5.48	0.57	F(2, 260) = 1.089, p > 0.05
PS L EO Y	4.13	1.11	4.07	1.19	4.69	0.37	F(2, 260) = 11.95, p < 0.05
PS M EC X	0.56^*	0.03	0.29l	0.08	0.56	0.03	F(2, 260) = 642.78, p < 0.05
PS M EC Y	0.5^*	0.01	0.24l	0.06	0.5	0.02	F(2, 260) = 1109.4, p < 0.05
PS M EO X	0.35	0.1	0.33	0.08	0.32	0.02	F(2, 260) = 4.62, p > 0.05
PS M EO Y	0.23	0.06	0.21	0.05	0.22	0.02	F(2, 260) = 10.8, p < 0.05
PS H EC X	1.44^*	0.11	1.1	0.16	1.12#	0.12	F(2, 260) = 173.29, p < 0.05
PS H EC Y	1.24^*	0.09	1.03	0.14	1.07#	0.09	F(2, 260) = 81.46, p < 0.05
PS H EO X	1.05	0.14	1	0.12	1.01	0.12	F(2, 260) = 11.58, p < 0.05
PS H EO Y	0.79	0.1	0.76	0.13	0.81	0.17	F(2, 260) = 2.83, p > 0.05

Main effects of objective measurements in cervicogenic (CGD) and unilateral vestibular hypofunction (UVH) subjects when compared with control group (CON). Eyes closed, EC; eyes open, EO; power spectra, PS; low-frequency domain, L; middle-frequency domain, M; high-frequency-domain, H; X plane, X; Y plane, Y; standard deviation, SD. ^*, # and l, respectively indicate post-hoc significant comparisons between CGD and CON, CGD and UVH and UVH and CON.

Fig. 1

Mean and standard deviation of posturography power spectra analysis when comparing cervicogenic dizziness (CGD), unilateral vestibular hypofunction (UVH) and control group (CON) subjects. Eyes closed, EC; eyes open, EO; X plane, X; Y plane, Y. Brackets indicate significant comparisons.

6.3 SRM/PM

Post-hoc correction demonstrated a significant increase in all DHI subsets when comparing UVH patients to CON and CGD subjects, and the latter group significantly scored higher DHI subsets values when compared with CON. Finally, UVH and CGD patients were found to significantly score higher values in TSK-17 and both anxiety and depression subsets of HADS when respectively compared to CON subjects (Table 3)

Table 3
Significant differences in self-report and performance measures between CGD, UVH and CON subjects

CGD CON UVH

Mean SD Mean SD Mean SD Significance

DHI P 9.24^* 4.1 0.89l 1.28 16.4# 4.5 F(2, 260) = 475.27, p < 0.05

DHI F 5.44^* 3.15 0.51l 1.04 19.55# 4.04 F(2, 260) = 695.39, p < 0.05

DHI E 26.98^* 6.85 0.4 l 0.85 20.47# 3.01 F(2, 260) = 1389.7, p < 0.05

DHI total 15.41^* 4.59 1.81l 2.45 56.43# 6.94 F(2, 260) = 1937.1, p < 0.05

TSK-17 39.04^* 12.62 21.47l 3.76 40.12 9.59 F(2, 260) = 115.41, p < 0.05

HADS - anxiety 7.95^* 2.88 3.33l 2.28 7.73 2.18 F(2, 260) = 101.53, p < 0.05

HADS - depression 10.77^* 5.26 3.45l 2.05 9.25 3.54 F(2, 260) = 94.986, p < 0.05

	CGD	CON	UVH
DHI P	9.24^*	4.1	0.89l	1.28	16.4#	4.5	F(2, 260) = 475.27, p < 0.05
DHI F	5.44^*	3.15	0.51l	1.04	19.55#	4.04	F(2, 260) = 695.39, p < 0.05
DHI E	26.98^*	6.85	0.4 l	0.85	20.47#	3.01	F(2, 260) = 1389.7, p < 0.05
DHI total	15.41^*	4.59	1.81l	2.45	56.43#	6.94	F(2, 260) = 1937.1, p < 0.05
TSK-17	39.04^*	12.62	21.47l	3.76	40.12	9.59	F(2, 260) = 115.41, p < 0.05
HADS - anxiety	7.95^*	2.88	3.33l	2.28	7.73	2.18	F(2, 260) = 101.53, p < 0.05
HADS - depression	10.77^*	5.26	3.45l	2.05	9.25	3.54	F(2, 260) = 94.986, p < 0.05

Between-group effect of main self-report and performance measures when comparing cervicogenic (CGD), unilateral vestibular hypofunction (UVH) and healthy subjects serving as control group (CON). Dizziness Handicap Inventory, DHI; Physical, P; Functional, F; Emotional, E; Tampa Scale for Kinesiophobia, TSK-17; Hospital Anxiety and Depression Scale, HADS. ^*, # and l, respectively indicate post-hoc significant comparisons between CGD and CON, CGD and UVH and UVH and CON.

6.4 ROC analysis

PS values in eyes closed condition on X plane within low-frequency intervals were found to distinguish UVH patients from CON subjects, with an AUC of 0.94 (95%c.i. 0.91 to 0.97) and a cut-off value of 6.62 (sensitivity: 83.3%, 95%c.i. 72.7%to 91%; specificity: 88.7%, 95%c.i. 80.8%to 94.2%) (Fig. 2A). PS values in eyes closed condition on X plane within high-frequency interval were found to distinguish CGD patients from CON subjects with an AUC of 0.95 (95%c.i. 0.92 to 0.97) and a cut-off value of 1.25 (sensitivity: 96.7%, 95%c.i. 90.8%to 99.3%; specificity: 78.5%, 95%c.i. 69.1%to 86.2%) (Fig. 2B).

Fig. 2

Receiver operating characteristic (ROC) curve depicting sensitivity, specificity and cut-off values for power spectra analysis in A) eyes closed condition on X plane within low-frequency interval in unilateral vestibular hypofunction patients and in B) eyes closed condition on X plane within high-frequency interval in cervicogenic dizziness patients, respectively compared with control subjects. Cut-points (c) have been calculated according to the Youden Index (J) = maximum {Sensitivity (c) + Specificity (c) –1}.

Finally, a positive correlation was found between PS values –within both low- and high- frequency interval in eyes closed condition on X and Y planes - with total DHI scores in UVH (r = 0.84 and r = 0.77) (Fig. 3A) and CGD patients (r = 0.85 and r = 0.75) (Fig. 3B), respectively, and a negative correlation was demonstrated in UVH subjects between PS values within low-frequency interval in eyes closed condition on X and Y planes and VOR gain of the affected ear (r = –0.78 and r = –0.71) (Fig. 3C).

Fig. 3

Plotted scatterplots of positive correlations between total Dizziness Handicap Inventory scores and power spectra (PS) values in eyes closed condition on X and Y planes within A) low-frequency interval in unilateral vestibular hypofunction (UVH) and B) high-frequency interval in cervicogenic dizziness (CGD) patients. In C) negative correlation between PS values within low-frequency interval in eyes closed condition on X and Y planes and vestibulo-ocular reflex (VOR) gain of the affected ear in UVH subjects.

7 Discussion

Beyond the expected and significant postural sway differences in length and area parameters among the three study groups, the first interesting finding in the present study is the significant difference in power spectra analysis when comparing UVH and CGD subjects to controls, along different frequency domains (Table 2, Fig. 1). The implementation of such analysis, depicting postural rearrangement in CGD and UVH patients, demonstrated a significant increase in middle- and low-frequency intervals for UVH relative to CON, and in middle- and high-frequency intervals for CGD relative to CON (Fig. 1 2). Among the vast literature concerning this topic, several categorizations of frequency bands have been proposed and the main subdivision has been found between oscillations under or over the value of 1-2 Hz [2 , 42]. However, present findings reinforce those studies depicting different kind of oscillation rearrangement to correlate with different neural loops regulating balance: a longer loop associated with visuo-vestibular regulation (lower frequencies) and a shorter loop (i.e. ‘myotatic loop’), due to proprioceptive participation, producing higher frequency oscillations [2 , 42]. Oscillations in the range around and over 1 Hz and around and under 0.7 Hz have been respectively linked by previous studies to an increase in the proprio-spinal reflex [11], thus reflecting proprioceptive cues, and in the vestibulo-spinal reflex (VSR) [2, 32], reflecting vestibular inflows. In line with these assumptions, patients with vestibular and proprioceptive deficits have been previously found to increasingly sway within respective domains [2, 32] and previous studies found that an increase in PS within a frequency range is associated with weakness in the relative sensory cue [2 , 38]. Extending these aspects, ROC curves for the eyes closed condition on X plane demonstrated PS cut-off values of 6.62 (Fig. 2A) within low-frequency interval and 1.25 (Fig. 2B) within high-frequency interval, when contrasting PS values of each group with CON. This may indicate spectral analysis as a supportive tool in the diagnostic route of dizziness considering that neural networks of postural control are highly overlapping. Indeed, it has been proposed that a disruption of the normal afferent signals from the upper cervical proprioceptors –accounting for CGD - results in aberrant information being sent to the vestibular nuclei [47, 58]. This could result in an inaccurate depiction of head and neck orientation in space [23, 48], which would cause alteration of postural stability, and of head and eye movement control [23, 24].

Furthermore - from a clinical point of view - this kind of implementation assumes more relevance considering that PS –within both low- and high- frequency intervals in eyes closed condition on X and Y planes - positively correlated with total DHI values in UVH and CGD patients, respectively (Fig. 3A and 3B). If on one side PS values under vestibular control have been extensively correlated with cognitive and biological parameters in previous experiences [31, 34], the present study found, for the first time, a relationship between posturography implementation and a widely implemented tool for studying the impact of dizziness on individual performance [39], opening a further strategy to disentangle possible mismatching factors between the objective source and subjective perception of dizziness. In fact, since previous studies found that the severity of subjective symptoms, as assessed by the DHI, represents the strongest predictive factor for quality of life [16 , 46] in vestibular and cervicogenic disorders, dynamic posturography parameters were found to be independent predictors of DHI score [51, 60] indicating dynamic postural tests, rather than static posturography, as more associated to subjectively perceived dizziness [55]. Studies have shown that balance performance, when measured quantitatively using laboratory testing, does not necessarily correspond to the extent of handicap in patients with dizziness, with correlations ranging from weak to moderate [15 , 55]. Lack of synchrony between subjective complaints and objective findings, with respect to balance, is common in patients with dizziness and previous studies confirmed that quiet stance postural measurements weakly account for the perceived dizziness measured by means of DHI [15, 29], possibly due to the fact that diverse individual factors (e.g. cognitive resilience, visual influences, walking conditions, etc...) may play critical roles in the perception of impaired movement, stability, somatosensory processing, or chronic subjective dizziness, related to reciprocal effects between subcortical multisensory organization regions and cortical areas subserving cognitive and emotional processes [53, 60].

A negative correlation was found between PS values within low-frequency domain in eyes closed condition in both X and Y planes and VOR gain when measured by means of vHIT in UVH patients (Fig. 3C). Considering the multimodal sensory rearrangement involved in higher processes of vestibular recovery, some studies to now tried to correlate compensatory and adaptive processes for the VOR and the VSR, evaluated by means of different vestibular stimulation testing and posturography [40]. In the present study, such correlation appears to be of interest, considering that balance control for the stance task in eyes closed condition - studied for the first time by means of a spectral analysis sub-grouping frequencies related to the vestibular system and depending on these inputs for stability [19] - tends to parallel with VOR gain. Despite evidences positing VSR and VOR neural pathways to no longer follow a common route beyond the vestibular nuclei, present findings reinforce theories positing that functional relationships between the two exist [4]. Although these connections could open new strategies in the diagnostic/prognostic route of dizziness complaints due to UVH, caution should be applied when pairing VOR results and the vestibular-spinal status after UVH onset. This is due to the fact that: i) balance control is a result of vestibulo-spinal responses interacting with the proprioceptive system [4 , 19] and a product of vestibular neural pathways different than VOR ones and ii) VOR testing does not duplicate head velocity profiles necessary to characterize the vestibular component of the balance disability experienced by UVH patients during stance and gait tests [4].

In conclusion, the present study findings advocate posturography testing implementation in the diagnostic route of patients suffering from dizziness due to vestibular and cervicogenic sources. Especially, power spectral analysis demonstrated to be useful in differentiating –with appropriate cut-off values –CGD and UVH patients, to objectively represent perceived symptoms filled along the DHI scale and to finally corroborate the rate of VOR gain deficit in UVH patients, possibly suggesting a certain degree of mutual influence between this reflex and VSR.

8 Limitations of the study

The present study suffers from some limitations which have to be addressed when pointing attention to the results. These, indeed, have to be interpreted as an explorative attempt at depicting reliable cut-off values distinguishing PS outcomes between CGD/UVH patients and a control group. This choice, which should not be intended as a proof of differences between UVH and CGD, was adopted as a preliminary effort in order to depict possibly useful values for future studies aiming at detecting differences between the two groups of patients.

Declaration of interest

All authors certify that they have NO affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

Author contributions

Conceptualization MA, AM, AV; Data curation AM, MA, BM, GDF; Formal analysis AM, MA, AV; Funding acquisition MA, AM; Investigation AM, AV, MA; Methodology AM, AV, MA, BM, GDF; Project administration MA, AM; Resources AM, MA, AV, GDF, BM; Software AM, MA; Supervision MA, AM, BM; Validation AM, Ma; Visualization MA, AM; Roles/Writing - original draft AM, MA, AV, BM, GDF; Writing - review & editing MA, AM, AV, GDF, BM.

Footnotes

Appendix A

Core function implemented in Matlab in order to obtain fast Fourier transform of X and Y oscillations. The symbol ‘%’ and ‘s’ represent a Matlab comment and X or Y oscillations, respectively:

L = length(s) %s vector of signal values

Fs = 25; %Sampling frequency

NFFT = 2^∧nextpow2(L); %Next power of 2 from length of s

f = Fs/2^*linspace(0,1,NFFT/2 + 1);

S = fft(s,NFFT)/L; %FFT of a signal s

modS = 2^*abs(S(1:NFFT/2 + 1));

ms = max(modS);

S_norm = modS/ms;

References

Alessandrini

, D’Erme

, Bruno

, Napolitano

and Magrini

, Vestibular compensation: analysis of postural re-arrangement as a control index for unilateral vestibular deficit:, NeuroReport 14 (2003), 1075–1079.

Alessandrini

, Lanciani

, Bruno

, Napolitano

and Di Girolamo

, Posturography frequency analysis of sound-evoked body sway in normal subjects, Eur Arch Otorhinolaryngol 263 (2006), 248–252.

Alessandrini

, Micarelli

, Chiaravalloti

, Candidi

, Bruno

, Di Pietro

, Oberg

, Schillaci

and Pagani

, Cerebellar metabolic involvement and its correlations with clinical parameters in vestibular neuritis, J Neurol 261 (2014), 1976–1985.

Allum

J.H.

, Honegger

, Relation between head impulse tests, rotating chair tests, and stance and gait posturography after an acute unilateral peripheral vestibular deficit, Otol Neurotol 34 (2013), 980–989.

Allum

J.H.

, Oude Nijhuis

L.B.

and Carpenter

M.G.

, Differences in coding provided by proprioceptive and vestibular sensory signals may contribute to lateral instability in vestibular loss subjects, Exp Brain Res 184 (2008), 391–410.

Arshad

, Patel

, Goga

, Nigmatullina

and Bronstein

A.M.

, Role of handedness-related vestibular cortical dominance upon the vestibular-ocular reflex, J Neurol 262 (2015), 1069–1071.

Becker-Bense

, Dieterich

, Buchholz

H.G.

, Bartenstein

, Schreckenberger

and Brandt

, The differential effects of acute right- vs. left-sided vestibular failure on brain metabolism, Brain Struct Funct 219 (2014), 1355–1367.

Berrar

and Flach

, Caveats and pitfalls of ROC analysis in clinical microarray research (and how to avoid them), Brief Bioinform 13 (2012), 83–97.

Blodow

, Pannasch

and Walther

L.E.

, Detection of isolated covert saccades with the video head impulse test in peripheral vestibular disorders, Auris Nasus Larynx 40 (2013), 348–351.

10.

Costantini

, Musso

, Viterbori

, Bonci

, Del Mastro

, Garrone

, Venturini

and Morasso

, Detecting psychological distress in cancer patients: validity of the Italian version of the Hospital Anxiety and Depression Scale, Support Care Cancer 7 (1999), 121–127.

11.

Dichgans

and Brandt

, Visual-Vestibular Interaction: Effects on Self-Motion Perception and Postural Control, in: Perception, R. Held, H.W. Leibowitz and H.-L. Teuber (eds.), Springer Berlin Heidelberg, Berlin, Heidelberg, 1978, pp. 755–804.

12.

Fife

T.D.

, Positional dizziness, Continuum (Minneap Minn) 18 (2012), 1060–1085.

13.

Fred

H.L.

, The diagnosis of exclusion: an ongoing uncertainty, Tex Heart Inst J 40 (2013), 379–381.

14.

Giacomini

P.G.

, Alessandrini

and Magrini

, Long-term postural abnormalities in benign paroxysmal positional vertigo, ORL J Otorhinolaryngol Relat Spec 64 (2002), 237–241.

15.

Gill-Body

K.M.

, Beninato

and Krebs

D.E.

, Relationship among balance impairments, functional performance, and disability in people with peripheral vestibular hypofunction, Phys Ther 80 (2000), 748–758.

16.

Grande-Alonso

, Moral Saiz

, Minguez Zuazo

, Lerma Lara

and La Touche

, Biobehavioural analysis of the vestibular system and posture control in patients with cervicogenic dizziness. A cross-sectional study, Neurologia 33 (2018), 98–106.

17.

Hain

T.C.

, Cervicogenic causes of vertigo, Curr Opin Neurol 28 (2015), 69–73.

18.

Hall

C.D.

, Herdman

S.J.

, Whitney

S.L.

, Cass

S.P.

, Clendaniel

R.A.

, Fife

T.D.

, Furman

J.M.

, Getchius

T.S.

, Goebel

J.A.

, Shepard

N.T.

and Woodhouse

S.N.

, Vestibular Rehabilitation for Peripheral Vestibular Hypofunction: An Evidence-Based Clinical Practice Guideline: From The American Physical Therapy Association Neurology Section, J Neurol Phys Ther 40 (2016), 124–155.

19.

Horlings

C.G.

, Kung

U.M.

, Honegger

, Van Engelen

B.G.

, Van Alfen

, Bloem

B.R.

and Allum

J.H.

, Vestibular and proprioceptive influences on trunk movements during quiet standing, Neuroscience 161 (2009), 904–914.

20.

Joosten

, Boudart

, Vincent

J.L.

, Vanden Eynden

, Barvais

, Van Obbergh

, Rinehart

and Desebbe

, Ability of a New Smartphone Pulse Pressure Variation and Cardiac Output Application to Predict Fluid Responsiveness in Patients Undergoing Cardiac Surgery, Anesth Analg (2018).

21.

Karlberg

, Johansson

, Magnusson

and Fransson

P.A.

, Dizziness of suspected cervical origin distinguished by posturographic assessment of human postural dynamics, J Vestib Res 6 (1996), 37–47.

22.

Karlberg

, Magnusson

, Malmstrom

E.M.

, Melander

and Moritz

, Postural and symptomatic improvement after physiotherapy in patients with dizziness of suspected cervical origin, Arch Phys Med Rehabil 77 (1996), 874–882.

23.

Kristjansson

and Treleaven

, Sensorimotor function and dizziness in neck pain: implications for assessment and management, J Orthop Sports Phys Ther 39 (2009), 364–377.

24.

L’Heureux-Lebeau

, Godbout

, Berbiche

and Saliba

, Evaluation of paraclinical tests in the diagnosis of cervicogenic dizziness, Otol Neurotol 35 (2014), 1858–1865.

25.

Lloyd

S.K.

, Kasbekar

A.V.

, Baguley

D.M.

and Moffat

D.A.

, Audiovestibular factors influencing quality of life in patients with conservatively managed sporadic vestibular schwannoma, Otol Neurotol 31 (2010), 968–976.

26.

Loughran

, Gatehouse

, Kishore

and Swan

I.R.

, Does patient-perceived handicap correspond to the modified clinical test for the sensory interaction on balance? Otol Neurotol 27 (2006), 86–91.

27.

Lystad

R.P.

, Bell

, Bonnevie-Svendsen

and Carter

C.V.

, Manual therapy with and without vestibular rehabilitation for cervicogenic dizziness: a systematic review, Chiropr Man Therap 19 (2011), 21.

28.

Malmstrom

E.M.

, Karlberg

, Melander

, Magnusson

and Moritz

, Cervicogenic dizziness - musculoskeletal findings before and after treatment and long-term outcome, Disabil Rehabil 29 (2007), 1193–1205.

29.

Mbongo

, Tran Ba Huy

, Vidal

P.P.

and de Waele

, Relationship between dynamic balance and self-reported handicap in patients who have unilateral peripheral vestibular loss, Otol Neurotol 28 (2007), 905–910.

30.

McCaslin

D.L.

, Jacobson

G.P.

, Bennett

M.L.

, Gruenwald

J.M.

and Green

A.P.

, Predictive properties of the video head impulse test: measures of caloric symmetry and self-report dizziness handicap, Ear Hear 35 (2014), e185–191.

31.

Micarelli

, Liguori

, Viziano

, Izzi

, Placidi

and Alessandrini

, Integrating postural and vestibular dimensions to depict impairment in moderate-to-severe obstructive sleep apnea syndrome patients, J Sleep Res 26 (2017), 487–494.

32.

Micarelli

, Viziano

, Bruno

, Micarelli

and Alessandrini

, Vestibular impairment in Multiple Chemical Sensitivity: Component analysis findings, J Vestib Res 26 (2016), 459–468.

33.

Micarelli

, Viziano

, Della-Morte

, Augimeri

and Alessandrini

, Degree of Functional Impairment Associated With Vestibular Hypofunction Among Older Adults With Cognitive Decline, Otol Neurotol 39 (2018), e392–e400.

34.

Micarelli

, Viziano

, Della-Morte

, Augimeri

and Alessandrini

, Degree of Functional Impairment Associated With Vestibular Hypofunction Among Older Adults With Cognitive Decline:, Otology & Neurotology 39 (2018), e392–e400.

35.

Minguez-Zuazo

, Grande-Alonso

, Saiz

B.M.

, La Touche

and Lara

S.L.

, Therapeutic patient education and exercise therapy in patients with cervicogenic dizziness: a prospective case series clinical study, J Exerc Rehabil 12 (2016), 216–225.

36.

Monticone

, Giorgi

, Baiardi

, Barbieri

, Rocca

and Bonezzi

, Development of the Italian version of the Tampa Scale of Kinesiophobia (TSK-I): cross-cultural adaptation, factor analysis, reliability, and validity, Spine (Phila Pa 1976) 35 (2010), 1241–1246.

37.

Morinaka

, Musculoskeletal diseases as a causal factor of cervical vertigo, Auris Nasus Larynx 36 (2009), 649–654.

38.

Nagy

, Feher-Kiss

, Barnai

, Domjan-Preszner

, Angyan

and Horvath

, Postural control in elderly subjects participating in balance training, Eur J Appl Physiol 100 (2007), 97–104.

39.

Nola

, Mostardini

, Salvi

, Ercolani

A.P.

and Ralli

, Validity of Italian adaptation of the Dizziness Handicap Inventory (DHI) and evaluation of the quality of life in patients with acute dizziness, Acta Otorhinolaryngol Ital 30 (2010), 190.

40.

Norre

M.E.

, Forrez

G.H.

and Beckers

A.M.

, Vestibular compensation evaluated by rotation tests and posturography, Arch Otolaryngol Head Neck Surg 113 (1987), 533–535.

41.

Oppenheim

, Kohen-Raz

, Alex

, Kohen-Raz

and Azarya

, Postural characteristics of diabetic neuropathy, Diabetes Care 22 (1999), 328–332.

42.

Paillard

, Costes-Salon

, Lafont

and Dupui

, Are there differences in postural regulation according to the level of competition in judoists? Br J Sports Med 36 (2002), 304–305.

43.

Perez

, Martin

and Garcia-Tapia

, Dizziness: relating the severity of vertigo to the degree of handicap by measuring vestibular impairment, Otolaryngol Head Neck Surg 128 (2003), 372–381.

44.

Prieto

T.E.

, Myklebust

J.B.

, Hoffmann

R.G.

, Lovett

E.G.

and Myklebust

B.M.

, Measures of postural steadiness: differences between healthy young and elderly adults, IEEE Trans Biomed Eng 43 (1996), 956–966.

45.

Reid

S.A.

, Callister

, Katekar

M.G.

and Rivett

D.A.

, Effects of cervical spine manual therapy on range of motion, head repositioning, and balance in participants with cervicogenic dizziness: a randomized controlled trial, Arch Phys Med Rehabil 95 (2014), 1603–1612.

46.

Reid

S.A.

, Callister

, Snodgrass

S.J.

, Katekar

M.G.

and Rivett

D.A.

, Manual therapy for cervicogenic dizziness: Long-term outcomes of a randomised trial, Man Ther 20 (2015), 148–156.

47.

Reid

S.A.

and Rivett

D.A.

, Manual therapy treatment of cervicogenic dizziness: a systematic review, Man Ther 10 (2005), 4–13.

48.

Reiley

A.S.

, Vickory

F.M.

, Funderburg

S.E.

, Cesario

R.A.

and Clendaniel

R.A.

, How to diagnose cervicogenic dizziness, Arch Physiother 7 (2017), 12.

49.

Reneker

J.C.

, Cheruvu

V.K.

, Yang

, James

M.A.

and Cook

C.E.

, Physical examination of dizziness in athletes after a concussion: A descriptive study, Musculoskelet Sci Pract 34 (2018), 8–13.

50.

Robertson

D.D.

and Ireland

D.J.

, Dizziness Handicap Inventory correlates of computerized dynamic posturography, J Otolaryngol 24 (1995), 118–124.

51.

Row

, Chan

, Damiano

, Shenouda

, Collins

and Zampieri

, Balance Assessment in Traumatic Brain Injury: A Comparison of the Sensory Organization and Limits of Stability Tests, J Neurotrauma (2019).

52.

Smith

P.F.

, The vestibular system and cognition, Curr Opin Neurol 30 (2017), 84–89.

53.

Staab

J.P.

, Balaban

C.D.

and Furman

J.M.

, Threat assessment and locomotion: clinical applications of an integrated model of anxiety and postural control, Semin Neurol 33 (2013), 297–306.

54.

Sugaya

, Arai

and Goto

, Changes in cognitive function in patients with intractable dizziness following vestibular rehabilitation, Sci Rep 8 (2018), 9984.

55.

Vereeck

, Truijen

, Wuyts

F.L.

and Van de Heyning

P.H.

, The dizziness handicap inventory and its relationship with functional balance performance, Otol Neurotol 28 (2007), 87–93.

56.

Walther

L.E.

, Lohler

, Agrawal

, Motschall

, Schubach

, Meerpohl

J.J.

and Schmucker

, Evaluating the Diagnostic Accuracy of the Head-Impulse Test: A Scoping Review, JAMA Otolaryngol Head Neck Surg (2019).

57.

Wrisley

D.M.

, Sparto

P.J.

, Whitney

S.L.

and Furman

J.M.

, Cervicogenic dizziness: a review of diagnosis and treatment, J Orthop Sports Phys Ther 30 (2000), 755–766.

58.

Wyke

, Cervical articular contribution to posture and gait: their relation to senile disequilibrium, Age Ageing 8 (1979), 251–258.

59.

Yahia

, Ghroubi

, Jribi

, Malla

, Baklouti

, Ghorbel

and Elleuch

M.H.

, Chronic neck pain and vertigo: Is a true balance disorder present? Ann Phys Rehabil Med 52 (2009), 556–567.

60.

Yip

C.W.

and Strupp

, The Dizziness Handicap Inventory does not correlate with vestibular function tests: a prospective study, J Neurol 265 (2018), 1210–1218.

61.

Yoneda

and Tokumasu

, Frequency analysis of body sway in the upright posture. Statistical study in cases of peripheral vestibular disease, Acta Otolaryngol 102 (1986), 87–92.

	CGD		CON		UVH
Posturography	Mean	SD	Mean	SD	Mean	SD	Significance
Length EO (mm)	553.64^*	126.26	425.34l	124.44	634.96#	110.61	F(2, 260) = 64.962, p < 0.05
Length EC (mm)	904.89^*	148.64	595.98l	141.35	979.47#	177.06	F(2, 260) = 155.11, p < 0.05
Area EO (mm²)	547.35^*	192.06	401.76l	121.11	756.53#	252.26	F(2, 260) = 72.77, p < 0.05
Area EC (mm²)	949.97^*	303.04	599.58l	135.97	1649.66#	414.92	F(2, 260) = 267.93, p < 0.05
PS L EC X	4.73	1.7	4.74l	1.58	8.69#	1.77	F(2, 260) = 141.81, p < 0.05
PS L EC Y	2.74	1.05	2.71l	1.06	8.11#	1.73	F(2, 260) = 458.91, p < 0.05
PS L EO X	5.34	1.1	5.25	1.06	5.48	0.57	F(2, 260) = 1.089, p > 0.05
PS L EO Y	4.13	1.11	4.07	1.19	4.69	0.37	F(2, 260) = 11.95, p < 0.05
PS M EC X	0.56^*	0.03	0.29l	0.08	0.56	0.03	F(2, 260) = 642.78, p < 0.05
PS M EC Y	0.5^*	0.01	0.24l	0.06	0.5	0.02	F(2, 260) = 1109.4, p < 0.05
PS M EO X	0.35	0.1	0.33	0.08	0.32	0.02	F(2, 260) = 4.62, p > 0.05
PS M EO Y	0.23	0.06	0.21	0.05	0.22	0.02	F(2, 260) = 10.8, p < 0.05
PS H EC X	1.44^*	0.11	1.1	0.16	1.12#	0.12	F(2, 260) = 173.29, p < 0.05
PS H EC Y	1.24^*	0.09	1.03	0.14	1.07#	0.09	F(2, 260) = 81.46, p < 0.05
PS H EO X	1.05	0.14	1	0.12	1.01	0.12	F(2, 260) = 11.58, p < 0.05
PS H EO Y	0.79	0.1	0.76	0.13	0.81	0.17	F(2, 260) = 2.83, p > 0.05