Veterans with dizziness recruit compensatory saccades in each semicircular canal plane although VOR gain is normal

Abstract

BACKGROUND:

Exposure to brain injury via blast or blunt mechanisms disrupts multiple sensorimotor systems simultaneously. Large numbers of US Gulf War era and Operation Iraqi/Enduring Freedom veterans with traumatic brain injury (TBI) are suffering the symptom of dizziness – presumed due to “Multi-Sensory Impairment”, a clinical pattern of damage to the auditory, visual and vestibular sensorimotor systems.

OBJECTIVE:

To describe the oculomotor response to rapid head rotation in a population of veterans with dizziness. We also describe the reliability of using the video head impulse test (vHIT) in a veteran population.

METHODS:

We used the vHIT to evaluate the vestibular-ocular reflex (VOR) gain and presence of compensatory saccades (CS) in each semicircular canal of 81 veterans (31% TBI) with dizziness. Data was collected using the ICS Otometric™ vHIT. Data was processed using both the Otometric™ software and custom software written in MATLAB™. This data was evaluated through Kruskal-Wallis rank-sum test and analysis of regression.

RESULTS:

Veterans with dizziness recruit CS in all semicircular canal planes even though their VOR gain is normal. The vHIT is a reliable clinical test to quantify the metrics of the VOR and CS in veterans.

CONCLUSION:

Veterans with dizziness symptoms use compensatory saccades in all planes of semicircular canal rotation, despite having normal peripheral VOR gain during rapid head rotation. The video head impulse test is a stable measure of vestibular slow phase and metrics of compensatory saccades in veterans with dizziness.

Keywords

Traumatic brain injury compensatory saccade vestibular-ocular reflex video head impulse test

1 Introduction

Exposure to brain injury via blast or blunt mechanisms disrupts multiple sensorimotor systems simultaneously and veterans from both the Gulf War and Operation Iraqi/Enduring Freedom (OIF/OEF) campaigns report physical, sensory, cognitive, and behavioral/emotional changes [7 , 34]. Typically, symptoms related to these damaged systems recover within weeks and significant improvement often occurs after 3 months. However, a significant population of our wounded veterans suffer long-term functional consequences of visual deficits, postural and locomotor instabilities, disorientation, dizziness, sensitivity to visual and body motion, and an impaired ability to read. Recent evidence has emerged that within the population of these veterans exposed to traumatic brain injury (TBI), a clinical pattern of damage to the auditory, visual, and vestibular sensorimotor systems has emerged, which has collectively been given the name multi-sensory impairment (MSI) [15, 22].

Large numbers of US Gulf War era and OIF/OEF veterans with mild Traumatic Brain Injury (mTBI) (>350K) are suffering MSI [33] with the inner ear commonly involved when symptoms of MSI are experienced. In fact, it has been estimated that 50% of service members with conductive sensorineural, or mixed hearing loss will have evidence for vestibular damage [8, 22]. Other studies report that vestibular symptoms (dizziness, imbalance, vertigo, gaze instability, motion intolerance) after TBI are as high as 80% [17 , 24]. The standard of care for dizziness symptoms in patients with TBI includes gaze stability exercises [25], yet little is known on how these exercises reduce symptoms in the TBI population. There is therefore, a need to better understand the oculomotor physiology related to head motion in TBI.

The video head impulse test (vHIT) has become an increasingly popular means of evaluating the gain of the vestibular-ocular reflex (VOR). The vHIT measures semicircular canal function using high-speed (250 Hz) video cameras embedded in lightweight goggles. The vHIT method has been validated against the gold standard scleral search coil method [2 , 26]. During a head movement, the VOR helps maintain stabilization of images on the fovea of the retina [10]. In healthy function, a normal VOR keeps the eyes on the target of interest by moving the eyes with an equal velocity but opposite direction of the head movement. The gain of the VOR is a ratio of eye to head velocity and is typically – 1.

An indicator of a peripheral vestibular hypofunction is a reduced VOR gain, due to the eye velocity being slower than the head velocity. As a result, images move off the fovea of the retina, causing gaze instability. Another oculomotor signature of gaze instability is the presence of a compensatory saccade – a saccade that improves gaze stability [29, 31]. Compensatory saccades occur in the same direction as the deficient VOR and are known as “covert” when occurring during the head rotation, or ‘overt’ when occurring after the head has stopped moving [4, 32]. The presence of these compensatory saccades suggests gaze instability and may be a useful metric to identify vestibular impairments (central or peripheral) to head rotation [33]. Therefore, evidence for vestibular impairment may be characterized by a reduced VOR gain or the presence of compensatory saccades. It remains unclear whether compensatory saccade characteristics such as frequency, latency, and amplitude differ between veterans with and without TBI. Furthermore, given CS are known to change with rehabilitative efforts in patients with peripheral vestibular hypofunction, it is critical to know how stable their metrics are to repeated impulse rotation in TBI. The characteristics of the head impulse are also important given the non-linearity of the VOR [10].

To date, no study has examined the VOR in the vertical semicircular canal planes (i.e. right anterior/left posterior) in veterans exposed to TBI. The purpose of this study was to investigate the relationship of VOR gain and compensatory saccades in all six semicircular canals of veterans with and without TBI. Additionally, we describe the reliability of using vHIT outcomes in a veteran population.

2 Materials and methods

2.1 Participants

Eighty-one veterans aged 26–70 with reports of dizziness participated in two studies of vestibular function (“Treatment of Vestibular Dysfunction using a Portable Stimulator” DOD Grant Award number W81XWH-14-2-0012) and (“Sensorimotor Assessment and Rehabilitative Apparatus” DOD Grant Award W81XWH-15-1-0442) in the years 2015 - 2017. Dizziness was captured using the Dizziness Handicap Inventory, The Vertigo Symptom Scale, and the Vestibular Disorders Activities of Daily Living Scale questionnaires in attempt to capture the broad manifestations of the symptom. All participants provided written informed consent as approved by the Institutional Review Board at the VA NJ Health Care Systems and the Human Research Protection Office of the Department of Defense.

For the reliability portion of the study, two vHIT sessions were applied in n = 23 of the 81 study participants. The time gap between these two test vHIT sessions was at least 2 hours.

2.2 TBI Assessment

To evaluate for the history of TBI, we performed the Polytrauma Interview. This format uses a semi-structured interview to determine the lifetime incidence of TBI. This assessment is the standard TBI evaluation used at the VA NJ Health Care systems, known as the “comprehensive 2nd level TBI evaluation Part 1”. This standard evaluation uses self-report questionnaires to identify the types of head injuries sustained (i.e. blast, bullet, vehicular, or other). The ‘Other’ category includes injuries related to “assault, blunt force, sports-related, or object hitting head”.

2.3 Video head impulse testing

vHIT data was collected using a commercial device that records the head and right eye velocity at a frame rate of 250 Hz (ICS Otometrics, Natus Medical Incorporated, Denmark). In brief, veterans wore the vHIT lightweight goggle frame with a built-in camera to record the right eye and head velocity. Participants sat on a stationary chair 1 meter from a visual fixation target on the wall in a well-lit room. Trained examiners performed at least 20 head impulses in each pair of semicircular canal planes of horizontal, left anterior- right posterior (LARP) and right anterior- left posterior (RALP). We recorded VOR gain and the presence of compensatory saccades considering their frequency, amplitude, and latency.

2.4 Exclusion criteria

Subject’s data were excluded when the type of injury was not specified, or if less than 20 head impulses were collected for each of the three planes of head rotation (horizontal, LARP, RALP). As a result of these exclusion criteria, n = 11 data sets were excluded. Data presented below is therefore from n = 70 Veterans with complete datasets.

2.5 Data analysis

Mean VOR gains for each semicircular canal were calculated using the ICS Otometric software (Natus Medical Incorporated, Denmark). Custom software written in the MATLAB programming environment was used to then compare semicircular canal plane VOR gains (i.e. mean RALP) (The MathWorks, Inc., Natick, Massachusetts, United States). Both programs define VOR gain as the ratio of the area under the eye velocity curve to the head velocity curve from onset to offset (head velocity returned to zero) of the head impulse. VOR gain values were determined excluding the influence of any compensatory saccade. Trained personnel examined individual head impulse traces for quality and rejected those impulses for artifacts or when evidence of noise (i.e. loose goggle, wrong calibration, and head-overshoot) [18].

Compensatory saccade (CS) metrics were analyzed with custom software written in the MATLAB programming environment (The MathWorks, Inc., Natick, Massachusetts, United States). The software identifies the CS based on a priori determined eye acceleration greater than 4000 degrees/s² in attempt to ensure the eye traces were saccadic and not higher acceleration vestibular slow phases [5]. Overt saccades were defined as any saccade occurring after the head velocity returned to zero and in the direction of the VOR; covert saccades were defined as any saccade occurring during the head velocity (before head velocity returned to zero) and in the direction of the VOR. CS latency was defined as the difference in time between the onset of the head and the CS. CS amplitude was defined as the area under the curve of the saccade. Data also included mean head velocity, head acceleration, and the number of covert/overt saccades.

2.6 Statistical analysis

All statistical analyses were conducted using the custom software in RStudio version 1.1.419 (R Core Team, 2013). For the reliability test, metrics of the saccades from repeated vHIT sessions were compared using paired two sample t-test. For the comparison test between non-TBI and TBI veterans, Kruskal-Wallis rank-sum test compared the VOR gains of semicircular canals in the same plane. Kruskal-Wallis rank-sum test compared VOR gains, saccade parameters, mean head velocity, and mean head acceleration within each plane. Analysis of regression was conducted to examine the relationship between recruitment of CS and magnitude of VOR gain.

3 Results

3.1 Demographic

Our data captured n = 45 non-TBI veterans and n = 25 veterans with a history of TBI, of which 100% were male. Within these 25 veterans, five were classified as moderate TBI and 20 as mild TBI. All of the veterans with TBI were classified as chronic, ranging in year of injury between 1967 and 2016 (3–52 years). In the veteran cohort without TBI, 84% were male. We found no difference in mean age between the veterans with or without TBI (Table 1). The majority type of injury in the veterans was due to blunt force, though many of the veterans did have more than one type of injury.

Table 1
Demographics of veterans with and without TBI

TBI Non-TBI

Age mean [SD] 52±2 (N = 25) 53±1 (N = 45)

Age range 33–70 years 26–69 years

Type of injury % Blast: 26% N/A

% Bullet: 0%

% Vehicular: 18%

% Blunt and others: 56%

	TBI	Non-TBI
Age mean [SD]	52±2 (N = 25)	53±1 (N = 45)
Age range	33–70 years	26–69 years
Type of injury	% Blast: 26%	N/A
	% Bullet: 0%
	% Vehicular: 18%
	% Blunt and others: 56%

TBI – Traumatic Brain Injury.

3.2 VOR gain

Although we found statistical differences in VOR gain within similar semicircular canals (Table 2), each of the VOR gain values are within the normal range of variability as compared to healthy controls and are not likely to be clinically relevant [15]. Therefore, the VOR gains within each canal plane (i.e. right and left for Yaw, or RA and LP for RALP) were combined; we found no difference in mean peak head velocity or mean peak head acceleration during head impulses between veterans with TBI and those without TBI (Table 3).

Table 2
Mean and 1 SD VOR gain for veterans with dizziness

Horizontal SCC Anterior SCC Posterior SCC

Left Right Left Right Left Right

TBI 0.89±0.09 0.94±0.08 0.82±0.21 0.81±0.21 0.87±0.22 0.87±0.12

Non TBI 0.90±0.13 0.96±0.16 0.79±0.21 0.83±0.15 0.89±0.17 0.85±0.17

	Horizontal SCC	Anterior SCC	Posterior SCC
TBI	0.89±0.09	0.94±0.08	0.82±0.21	0.81±0.21	0.87±0.22	0.87±0.12
Non TBI	0.90±0.13	0.96±0.16	0.79±0.21	0.83±0.15	0.89±0.17	0.85±0.17

Italics denote a statistical difference (p≤0.05) in VOR gain between similar semicircular canals for right and left vestibular system. There was no difference in VOR gain within the anterior or posterior SCC for the TBI subjects. There was no difference in VOR gain between TBI and Non TBI patients. Each of these VOR gain values are within normal variability; though it has been established that a change score of 0.06 VOR gain represents a minimal clinically important difference as compared against fall risk [11]. SCC – semicircular canal.

Table 3

Mean [Interquartile Ratio] head velocity and acceleration in semicircular canal plane impulse testing in veterans with dizziness

Head Velocity (d/s)	TBI	Non-TBI	p value
Horizontal	171.37 [154.08, 201.41]	159.18 [146.66, 177.35]	0.286
RALP	126.63 [120.47, 136.26]	127.14 [117.40, 137.38]	0.672
LARP	126.99 [119.15, 140.95]	124.37 [116.64, 143.91]	0.602
Head Accel (d/s/s)	TBI	Non-TBI
Horizontal	3533 [2802, 4340]	3413 [2878, 3831]	0.764
RALP	2749 [2544, 3365]	2736 [2375, 3167]	0.481
LARP	2492 [2343, 2897]	2531 [2117, 3167]	0.755

There were no differences in head velocity or head acceleration across semicircular canal plane testing. Accel – acceleration; d/s – degrees/second; d/s/s/ - degrees/second/second.

3.3 Compensatory saccades

Within both groups of veterans (TBI and non-TBI), our data revealed that ∼25% of head impulses involved the recruitment of a CS. Both covert and overt CS subtypes were recruited, Fig. 1. The split between subtypes of overt and covert CS varied depending on canal plane. Seventy percent of the CS in the yaw plane were overt, while 60% were overt in the RALP plane and only 30% overt in the LARP plane (Table 4).

Fig. 1

Exemplar record of the presence of covert and overt saccades during the video head impulse test in veterans with dizziness.

Table 4

Comparisons of VOR and saccade metrics between two vHIT sessions

Canal Plane	Metric	Session 1 (median [IQR])	Session 2 (median [IQR])	p value
YAW	VOR Gain	0.89 [0.86, 0.93]	0.91 [0.85, 0.93]	0.92
	Peak Head Velocity (d/s)	155.3 [146.3, 167.21]	161.83 [149, 176.8]	0.448
	Peak Head Accel (d/s/s)	2838 [2662, 3346]	2886 [2516, 3349]	0.886
	Percent Overt	71.9 [57.14, 86.06]	72.73 [60.8, 87.3]	0.733
	CS Latency (ms)	232.8 [203.59, 297.1]	237.45 [191.9, 290.4]	0.684
	CS Amplitude (d/s)	167.1 [195.6, 84.0]	236.3 [313.2, 73.5]	0.249
LARP	VOR Gain	0.91 [0.79, 0.97]	0.89 [0.75, 0.92]	0.388
	Peak Head Velocity (d/s)	121.15 [117.6, 134.15]	121.31 [119.48, 130.67]	0.928
	Peak Head Accel (d/s/s)	2348 [2159, 2601]	2166 [2001, 2470]	0.256
	Percent Overt	33.33 [20, 50]	23.36 [0.0, 62.9]	0.539
	CS Latency (ms)	130.15 [96, 176]	125.68 [94.5, 181.4]	0.827
	CS Amplitude (d/s)	34.55 [116.1, 13.8]	38.58 [125.5, 20.61]	0.525
RALP	VOR Gain	0.81 [0.72, 0.9]	0.76 [0.69, 0.88]	0.56
	Peak Head Velocity (d/s)	128.68 [118.7, 139.3]	128.36 [119.1, 141.7]	0.939
	Peak Head Accel (d/s/s)	2736 [2279, 3355]	2724 [2332 3020]	0.92
	Percent Overt	60.26 [33.85, 90]	61.82 [22.22, 79.46]	0.647
	CS Latency (ms)	186.37 [135.9, 215.6]	184.91 [114.06, 240.4]	0.944
	CS Amplitude (d/s)	121.60 [218.2, 4.9]	75.11 [186.78, 17.5]	0.878

LARP – left anterior right posterior; RALP – right anterior left posterior; IQR – Interquartile Ratio; d/s – degrees/second; d/s/s/ - degrees/second/second; ms – millisecond. CS – compensatory saccade; Percent overt refers to the percentage of CS that occur after the head rotation has stopped.

3.4 Reliability

We measured test-retest reliability in n = 23 veterans; 87% were male and 13% were female. We found no significant difference between the vHIT test and retest sessions in terms of VOR gains or metrics of the CS (Table 4).

4 Discussion

The critical result of our study was that veterans show recruitment of CS in all semicircular canal planes. To date, the presence of CS in veterans has not been determined. Although their VOR gains (a ratio of eye and head velocity) are normal in each semicircular canal, the presence of the compensatory saccades in each canal plane suggests gaze instability based on an eye and head position asymmetry error. Saccades are recruited to change eye in orbit position and are modifiable when exposed to targets that vary their position [1]. The presence of these saccades implies eye and head position are dissimilar in position. Various studies have indicated that patients with vestibular deficit use compensatory saccades as a strategy to augment the deficient VOR [13 , 31]. Our data showed that every veteran with dizziness used compensatory saccades (covert or overt subtypes) even though the VOR gain was normal. Additionally, it is interesting that the distribution of overt: covert saccades varied across the plane of canal rotation (yaw, LARP, RALP). This difference may be functionally relevant, though we will need to measure final eye position to determine such significance. Since most of our participating veterans with TBI had head injuries prior to or during combat (service) many years before participating in this study, it remains possible that the VOR gain of those veterans with TBI recovered and only the CS remains as evidence for such damage. This seems unlikely given the VOR gain tends not to recover to high-velocity passive head rotation once injured [6]. It is difficult to know why CS were recruited in the presence of a normal VOR gain, though we are not the first to report such a result [4, 30]. CS are not an uncommon finding when performing yaw vHIT in subjects with a bilaterally intact VOR (4, 5). In fact, Anson, et al. (2016) identified at least one CS in 91% in a sample of healthy older adults [4, 5]. Our data adds to this literature by showing that veterans with dizziness recruit CS in the vertical semicircular canal planes as well, which is a novel finding and suggests that the mechanism responsible for generating the CS is similar for both vertical and horizontal semicircular canal afference. Prior up vs down head impulse data in active duty service members with TBI due to blast exposure report the presence of overt and covert CS with the VOR gain being lower during active compared with passive head impulse testing [27]. Typically, passive head rotation derived VOR gains are lower than active head rotation derived VOR gains [13]. This suggests the central processing of vestibular afference can be abnormal in TBI and that the signal to recruit CS is shared for active and passive rotation.

Our data show the vHIT is a reliable clinical test to quantify both VOR gain and compensatory saccade metrics in the veteran population with or without TBI, others have reported vHIT as being valid [17]. This is important to establish considering rehabilitative efforts to improve gaze stability are showing that the CS are modifiable [21 , 30]. We found no evidence for peripheral vestibular hypofunction based on vHIT in any of the subjects with TBI. This result is in accord with previous data presented by Alshehri et al. who reported civilians with mild TBI and dizziness had normal horizontal semicircular canal VOR gains during impulse testing [3]. Our result extends this finding to the vertical semicircular canals. Current evidence thus suggests VOR gain as measured by head-only impulse testing (i.e. vHIT) is not sensitive to identify TBI in civilians or veterans.

5 Limitations

The study findings should not be generalized beyond veterans who have dizziness. One limitation of the study is the self-report nature of the TBI evaluation process. It is possible some of the veterans were less accurate in reporting their injury. Additionally, we used different, though trained, examiners to conduct the vHIT that might introduce variability. Finally, although both genders are included in the total sample, only a few were female veterans.

6 Conclusion

Footnotes

Acknowledgment

We would like to thank Bishoy Samy for his help with Matlab code editing and troubleshooting, Justyna Michalik and Kamila Migdal for their help with data collection. We would like to thank all veterans who participated in this study. Drs Schubert and Serrador were funded by DOD Grant Awards W81XWH-15-1-0442 and W81XWH-14-2-0012, respectively.

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Veterans with dizziness recruit compensatory saccades in each semicircular canal plane although VOR gain is normal

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1 Introduction

2 Materials and methods

2.1 Participants

2.2 TBI Assessment

2.3 Video head impulse testing

2.4 Exclusion criteria

2.5 Data analysis

2.6 Statistical analysis

3 Results

3.1 Demographic

Table 1 Demographics of veterans with and without TBI TBI Non-TBI Age mean [SD] 52±2 (N = 25) 53±1 (N = 45) Age range 33–70 years 26–69 years Type of injury % Blast: 26% N/A % Bullet: 0% % Vehicular: 18% % Blunt and others: 56%

Table 2 Mean and 1 SD VOR gain for veterans with dizziness Horizontal SCC Anterior SCC Posterior SCC Left Right Left Right Left Right TBI 0.89±0.09 0.94±0.08 0.82±0.21 0.81±0.21 0.87±0.22 0.87±0.12 Non TBI 0.90±0.13 0.96±0.16 0.79±0.21 0.83±0.15 0.89±0.17 0.85±0.17

4 Discussion

5 Limitations

6 Conclusion

Footnotes

Acknowledgment

References

Table 1
Demographics of veterans with and without TBI

TBI Non-TBI

Age mean [SD] 52±2 (N = 25) 53±1 (N = 45)

Age range 33–70 years 26–69 years

Type of injury % Blast: 26% N/A

% Bullet: 0%

% Vehicular: 18%

% Blunt and others: 56%

Table 2
Mean and 1 SD VOR gain for veterans with dizziness

Horizontal SCC Anterior SCC Posterior SCC

Left Right Left Right Left Right

TBI 0.89±0.09 0.94±0.08 0.82±0.21 0.81±0.21 0.87±0.22 0.87±0.12

Non TBI 0.90±0.13 0.96±0.16 0.79±0.21 0.83±0.15 0.89±0.17 0.85±0.17