Abstract
BACKGROUND:
There is a prevailing opinion that spinning sensations signify a peripheral vestibular pathology while non-spinning sensations are not of vestibular origin.
OBJECTIVES:
1) Characterize the subjective sensations reported by patients during caloric testing. 2) Assess if the sensation was correlated with the peak slow phase velocity (SPV).
METHODS:
Retrospective chart review at a Canadian adult tertiary-quaternary care balance centre for patients undergoing diagnostic caloric testing between December 2014 and September 2015.
RESULTS:
Of 163 patients included, 122 had normal calorics and 41 demonstrated unilateral weakness. Spinning/rotatory movements were the most commonly reported sensations (55–70%). No sensation was reported among 10–20% of patients. Other non-rotatory sensations were reported 20–25% of the time. Both lack of sensation and other sensations were more likely to be correlated with SPVs that were significantly lower than those associated with spinning/rotating sensations. However, 18% of patients with normal calorics and robust SPVs with warm irrigation still reported non-spinning sensations.
CONCLUSIONS:
During caloric irrigation, subjective sensations other than spinning and rotating are reported 20–25% of the time and these tend to be associated with lower peak SPV. Non-spinning vertigo is not uncommon as a subjective description of vestibular sensation even in normal patients with strong SPVs.
Introduction
The evaluation of patients with balance disorders is challenging since dizziness, as an experience, is private and subjective. Clinical assessment relies heavily on the history provided by the patient and the verbal labeling of their experience. Patients often have difficulty describing their dizziness and use a wide variety of terms and comparisons often analogous to external actions or events to which other individuals can (hopefully) relate [1].
Classically, dizziness described as spinning of the visual environment is thought to originate from the inner ear and patients who do not report a spinning sensation could be dismissed as not having an inner ear problem. Although it is well known that patients can describe their dizziness with terms such as floating, swimming, walking on clouds or feeling disoriented [1], our limited knowledge on the nature and prevalence of these non-rotatory sensation could lead to overlooking a potential inner ear aetiology. For example, it was noted that only 53% of patients with diagnostic positioning evidence of benign positional vertigo reported a rotatory sensation while others complained of poor balance, light-headedness, nausea or an impression of tilting [2].
Caloric testing is part of the videonystagmography (VNG) battery of tests that assess vestibular function through its impact on eye movements and the induction of nystagmus, a repetitive jerky ocular movement with a slow and a fast phase. Caloric testing consists of warm and cold-water irrigation in the external ear canal. As it is believed to induce an imbalance in the vestibular signals from the inner ear, it has classically been considered as a model of peripheral vertigo, since such imbalance in signals from both ears is postulated as the aetiology of pathologic peripheral vertigo sensations. Despite the vestibular stimulation, a limited study of caloric-evoked sensations has reported that up to 20% of patients did not experience a rotatory sensation during caloric testing [3]. The full range of subjective descriptions was not elucidated in this study. A positive correlation has been found between the severity of the elicited eye movements and the sensation of movement and nausea elicited during caloric testing, but the authors did not expand this to other subjective experiences [4].
To our knowledge, no study has assessed the full range of symptoms and subjective descriptions reported by patients during vestibular function testing and correlated it with the magnitude of the resulting eye movements. Further characterizing the sensations experienced during these vestibular tests has the potential of expanding the range of symptoms and subjective descriptions that can be considered vestibular in nature, providing further evidence and nuance to the vast array of vestibular sensations. Increased awareness of the complex symptomatology could result in increased diagnostic accuracy and avoidance of delays in treatment.
In this context, the objectives of the present study were to characterize the range of subjective sensations reported by patients and to assess if this sensation could be correlated with the peak slow phase velocity (SPV) evaluated during caloric vestibular stimulation.
Materials and methods
Study design
Approval was obtained from the University of British Columbia Ethics Review Board ID H16-00444.
A retrospective chart review of consecutive patients who had undergone VNG testing between December 2014 and September 2015 at an adult tertiary-quaternary care academic institution was performed. All patients referred for vestibular testing had a full clinical assessment by a certified otolaryngologist. During the caloric testing, patients were routinely asked to describe the sensation induced by each caloric irrigation, using open-ended questions, and this information was prospectively documented in the caloric report. The sensation reported during each irrigation along with the corresponding peak SPV of the induced nystagmus were collected for data analysis. Patients with active insurance or medicolegal claims, those unable to tolerate caloric testing, or those without recording of subjective sensations in the report were excluded. Only the caloric report was reviewed; the clinical diagnosis prompting the testing was not recorded.
Caloric testing protocol
At our institution, caloric testing is routinely performed by three experienced vestibular audiologists using a standardized protocol of 30-seconds of water irrigation at a flow rate of 500 mL/min with a minimum five-minute delay between each irrigation. Irrigation temperatures of 30C and 44C were used for cool and warm calorics respectively as per recommended protocols (British Society of Audiology 2010). The peak slow phase velocity was quantified using pupil tracking video technology (Micromedical VisualEyes Four Channel VNG system utilizing the Spectrum 8 software suite). Monothermal warm calorics were used as a screen; if there was≥14% unilateral weakness then cool calorics were used to confirm the unilateral weakness based on the method published by Lightfoot et al. [5] Unilateral weakness at our center is defined an asymmetry >20% as per the Jongkee’s formula with bithermal calorics [6].
Analysis
The reported sensations experienced with each caloric irrigation were grouped into three broad categories (Spinning/rotating, Other, No sensation) and their prevalence was assessed. When more than one sensation was reported by the patient along with spinning or rotating, they were assigned to the spinning or rotating category. Sensations reported during warm and cold calorics were analysed separately and then compared. Subanalyses were performed to compare ears with normal calorics to those with caloric weakness. The mean peak SPV of each category were compared using the student t-Test. Given that a normal distribution could not be assumed in all subgroups, a Kruskal-Wallis test was also performed to compare the mean SPV across groups. Statistical analyses were performed using JMP 11 (Cary, NC). Given binaural testing for each patient, results from each ear were considered as separate data points.
Results
A total of 200 charts were reviewed with 161 adult patients fitting the inclusion criteria; 60 men and 101 women, mean age of 53.9 years old (+/–14.9). Thirty-nine patients were excluded; caloric testing was omitted from the VNG in 28 patients and the subjective sensation was not documented in 11 patients. All patients had warm calorics performed; cold calorics were also performed in 72 patients. Unilateral weakness was identified in 39 patients. No patients had bilateral vestibular hypofunction. Subjective sensations were not recorded in 19 of 144 ears (10 patients) that underwent cold caloric irrigation.
Many different descriptors of subjective sensations were reported by patients during caloric testing. These were grouped qualitatively into three categories to facilitate coherence and further analysis (Table 1). The prevalence of each category during warm and cold caloric testing with sub-analysis for patients with normal calorics versus unilateral weakness is visually depicted in Fig. 1.
Qualitative description of sensations reported during caloric testing and their regrouping into categories
Qualitative description of sensations reported during caloric testing and their regrouping into categories
Distribution of sensations based on irrigating temperature and caloric results.
Overall, spinning and rotating account for 70% of the subjective sensations experienced by patients during warm calorics and 55% during cold calorics. Other sensations are reported 19.6% of the time during warm calorics and 25% during cold calorics while no sensation at all is elicited in 10.2% of ears during warm caloric and 20% during cold calorics. Comparative analysis of sensation distribution with a Chi-Square goodness to fit model demonstrated that with cold irrigation the proportion of spinning/rotating sensations is significantly reduced as compared to warm irrigation and the rate of no reported sensation is increased (p < 0.001). These data suggest that warm and cold caloric vestibular stimuli generate a different profile of subjective sensations.
Impact of the status of the inner ear / caloric results
When the prevalence of sensations in patients with normal caloric results and those with unilateral weakness is analysed separately, a significantly different distribution of sensations is obtained (p < 0.001). During warm calorics, the rate of spinning/rotating sensations decreases from 76% to 51% in patients with normal results compared those with unilateral weakness. A similar result is obtained during cold calorics, where the rate of spinning/rotating drops from 67% to 46%, respectively. This suggests that when stimulated, patients with a unilateral weakness are less likely to report spinning/rotating sensations. While the rates of other sensations reported remain stable across settings, the rate of no reported sensation is significantly higher in patients’ ears with unilateral weakness as compared to those with normal caloric results.
Analysis of peak slow phase velocity
The relationship between peak slow phase velocity (SPV) and sensation was examined in each caloric group with separation of normal versus unilateral weakness (Figs. 2 and 3). Overall, during warm caloric irrigation, the mean peak SPV significantly decreased as we move from spinning/rotating to other sensations to no sensation at all (Fig. 2A). A similar trend is noted in the subgroup of patients with normal calorics but was not significant on the t-test as the SPV of spinning/rotating and other sensations were quite similar (Fig. 2B). The trend is strong and significant during warm irrigation of patients with unilateral weakness (Fig. 2C). During cold irrigation, this same trend was only significant on the student t-test for the subgroup of patients with normal calorics (Fig. 3B). Across all groups and irrigation settings, the mean peak SPV among those with no subjective sensation was significantly lower than when any sensation was reported. When non-parametric statistical analysis was done using the Kruskal-Wallis significant differences across all groups and settings were noted (p < 0.05) (Table 2).
Peak slow phase velocity distribution and its mean for each sensation reported during warm caloric irrigation divided according to caloric results.
Peak slow phase velocity distribution and its mean for each sensation reported during cold caloric irrigation divided according to caloric results.
Output of the Kruskal-Wallis tests assessing the difference in sensation associated slow phase velocities across settings and subgroups
DF: degrees of freedom.
Overall, there appears to be a link between the peak SPV and the sensation experienced with the tendency for higher SPV to be associated with spinning/rotating sensations.
Patients experience a vast range of subjective sensations during caloric testing thus contradicting the traditional teaching that vestibular sensations originating from the inner ear must feel like spinning. While spinning and rotating sensations remain the most frequently reported, non-rotatory sensations are not uncommon with both caloric vestibular stimuli in patients with both normal and asymmetric vestibular function. Subjective sensations other than spinning/rotating are elicited 18–25% of the time despite normal caloric testing and robust SPV responses. Higher peak SPV tends to be predictive of experiencing a spinning or rotatory sensation, and lower SPV cause increasingly weaker localization of symptoms, resulting in non-rotatory movement, vague spatial uncertainty and at the lowest end of the spectrum, no sensation at all.
A significant portion of patients did not experience a rotating motion but reported non-rotating motions, vague spatial disorientation and even bodily sensations despite objective observation of horizontal jerk nystagmus typical during caloric irrigation. Beyond the inherent human variability in describing our subjective experiences, there are several possible explanations for the reporting of sensations other than spinning during caloric irrigation. A number of patients reported sensations such as floating, falling and moving sideways which could be otolithic in nature. Despite the classic dogma that caloric responses are carried through the horizontal canal, some studies have suggested otolithic modulation of caloric responses [7, 8] while others have considered direct thermal influences on the vestibular end organs and their innervation [9, 10]. While direct thermal stimulation has been rejected as the primary aetiology of caloric nystagmus, it may influence the subjective sensation if the other organs and their innervation within the vestibular labyrinth are stimulated. Another explanation could lie in the complex interplay of vestibular inputs with other neurosensory functions. Caloric irrigation has been shown to modulate the sense of body schema and the mental representation of the various body parts in space [11] as well as impact our perception of pain and touch [12]. Therefore, disruption of the normal flow of vestibular input to these systems of body schema and somatosensory organization could be another possible contributor to the array of non-movement sensations described by patients in this study.
Regardless, the magnitude of the peak slow phase velocity correlates to the described sensation. A higher SPV more likely generated a spinning sensation; both lack of sensation and non-rotatory (other) sensations were more likely to be correlated with slower SPVs than those associated with spinning/rotating sensations. As would be expected, the lack of reported sensation with irrigation was more common in patients with vestibular hypofunction since a nonresponsive vestibular organ would not elicit any vestibular input centrally.
It was surprising to note that 18% of patients with normal caloric function reported non-rotatory sensations during warm irrigations despite robust SPV responses comparable to those obtained in patients who reported spinning sensations. We could hypothesise that a central mechanism of vestibular input interpretation could be at the source of both their symptoms that warranted the VNG as well as the non-rotatory sensation that they felt during the caloric. Unfortunately, the final diagnoses are not available to us to test this hypothesis. Significant heterogeneity existed among the non-rotatory sensations and attempts to analyse these separately yielded small numbers that lacked power to draw any significant conclusions. Future studies with larger numbers might consider decorticating the different subcategories and better classifying the nature of these non-rotatory sensations.
Presumably, included patients represent a wide range of vestibular functions and pathologies, which may inherently impact the sensations reported. We could not characterize our results with regards to the underlying diagnosis, which may impact the generalizability of our results to other populations. Further research is needed to better characterize the relationships between different sensations and various peripheral vestibular pathologies.
Conclusions
In the assessment of patients with balance disorders, traditional teaching states that the key to diagnosis lies in taking a thorough history, and great weight is placed on the patient’s subjective description of dizziness to guide diagnosis. Moreover, clinical teaching dogma has suggested that non-spinning dizziness is non-vestibular in nature. Many Otolaryngologists dismiss patients during initial assessment when non-spinning dizziness is reported; however, given that non-rotatory sensations are not uncommon they should not exclude patients from being placed into vestibular diagnostic categories.