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Caloric Testing
Kamran Barin
OVERVIEW
The function of the vestibulo-ocular reflex (VOR) can be evaluated by stimulating the vestibular system and measuring the eye movement responses. Head move­ments provide the natural and physiologic stimulation for the vestibular system but under most conditions, it is not possible to restrict such stimuli to one labyrinth at a time. As a result, caloric irrigations have been used historically as a more practical method for testing ves­tibular function in clinical settings. In the caloric test, the external auditory canal is irrigated by a medium that has a significantly different temperature compared with body temperature. The temperature gradient eventually reaches the labyrinth and under the appro­priate conditions can result in cupular deflections that produce vestibular responses.
Despite a number of limitations, caloric irriga­tions offer a major advantage over other types of ves­tibular stimulation. Unlike head movements, which always stimulate both labyrinths simultaneously, caloric irrigations allow each labyrinth to be evaluated independently (Baloh & Honrubia, 2001). Also, caloric stimulation can be generated by relatively small-sized and inexpensive equipment.
This chapter describes how to perform and inter­pret the caloric test. The underlying principles of the caloric test are also discussed so that the examiner can recognize the limitations and artifacts when they occur.
BACKGROUND
Mechanism of Caloric Stimulation
The first detailed description of the caloric test and its underlying mechanism is attributed to Robert Bárány (Baloh, 2002). In his now well-known book published almost a century ago, Bárány (1907) described caloric irrigations administered in the supine position with the head placed at an angle of 30 degrees with respect to the horizontal plane (Figure 12–1A). In this head position, known as the caloric test position, the lateral (horizontal) semicircular canals become aligned with the plane of gravity. In the absence of caloric stimula­tion, no responses are evoked from the lateral canals because the cupula and the surrounding endolymph have the same densities and are not affected by grav­ity. When the external auditory canal is irrigated with a medium that is considerably cooler or warmer than the body temperature, a temperature gradient is generated across the lateral canal of the irrigated ear. According to Bárány, the temperature gradient changes the density of the endolymph on the side of the canal closest to the site of irrigation. If that explanation is correct, warm irrigations in the standard caloric test position should cause the endolymph to become lighter and rise, thus generating an ampullopetal deflection of the cupula. Such a deflection should cause an excitatory response from the lateral canal and generate nystagmus with its fast phases beating toward the irrigated ear (see
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figure 12–1. Effects of caloric stimulation on the neural firing and the eye movement responses with the patient: supine with the head tilted up 30º (A), or prone with the head tilted down 30º (B). irrigation. Based on Barin, K. (2009). Clinical Neurophysiology of the Vestibular System. In J. Katz, L. Medwetsky, R. Bur­khart, and L. Hood, (Eds.), Handbook of Clinical Audiology (6th ed.). Philadelphia, PA: Lippincott Williams & Wilkins.
Figure 12–1A). Conversely, cool irrigations should cause the endolymph to become heavier and sink, thus generating an inhibitory response from the irrigated ear. The nystagmus fast phases should beat away from the side of irrigation. The relationship between the temperature in the irrigated ear and the direction of the evoked nystagmus fast phases is summarized by the acronym COWS — cold opposite, warm, same.
For many years, experimental findings were consistent with the above explanation and supported Bárány’s predictions regarding the mechanism of
Solid arrows indicate the onset of
caloric irrigations. The first serious challenge to this hypothesis came from one of the Spacelab I experi­ments in which caloric responses were observed in the absence of gravity (Scherer et al., 1986). This finding could not be explained based on Bárány’s hypothesis because the change of the endolymph density depends on the presence of gravity. Alternative hypotheses have since emerged, including the direct effect of tempera­ture on the vestibular nerve (Hood, 1989) and gravity­independent changes in the volume or pressure of the endolymph (Gentine, Eichhorn, Kopp, & Conraux,
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1991). However, there are a number of compelling experimental findings that cannot be explained by any mechanism other than the one proposed by Bárány. For example, Figure 12–1B shows what happens when caloric irrigations are administered with the patient in the prone position with the head tilted 30 degrees downward. The lateral canals are still in the vertical plane but their orientation with respect to gravity is the reverse of that in the standard caloric position. If the caloric stimulations are mediated entirely by grav­ity-independent mechanisms, the nystagmus direction should be the same in the supine and prone posi­tions. However, the exact opposite is expected under Bárány’s hypothesis. That is, warm irrigations in the prone position should generate nystagmus with the fast phases beating away from the irrigated ear. The reason is that the rise of lighter endolymph should now cause an ampullofugal flow of the endolymph, which should result in the inhibition of the irrigated lateral canal. Similarly, cool irrigations in the prone position should generate nystagmus with the fast phases beat­ing toward the irrigated ear, indicating excitation of the irrigated lateral canal.
Coats and Smith (1967) demonstrated that the direction of nystagmus was indeed different in the supine and prone positions. Furthermore, the intensity of the nystagmus was slightly higher for the supine position. They concluded that the primary component of caloric stimulation was the change in the endo­lymph density. Additionally, they proposed that there was a secondary component involving direct stimu­lation of the vestibular nerve. The first component is gravity dependent as postulated by Bárány, whereas the second component is gravity independent. Coats and Smith (1967) attributed the difference in nystag­mus intensity in different head positions to the fact that in the supine position, the two components are added but in the prone position, the two components are subtracted. This explains why caloric responses in the supine position are slightly larger than those in the prone position. Today, the general consensus on the mechanism of caloric stimulation is very similar to the views expressed by Coats and Smith (1967). That is, caloric stimulation consists of two components, one gravity dependent and the other gravity indepen­dent. Hood (1989) suggested that the contribution of the gravity-independent component was very small (~10%) and the change in the endolymph density was the dominant mechanism underlying caloric responses.
It is well known that caloric stimuli are highly variable and depend on characteristics that are dif­ferent from one individual to another. The effect of some of these differences, such as a perforated tym-
panic membrane (TM), is obvious. Other differences, such as the dimensions of the internal meatus, have a less obvious and more puzzling effect on the caloric stimulus (O’Neill, 1995). It is fair to say that the pre­cise mechanisms of caloric stimulation are still not fully understood.
Limitations of the Caloric Test
The caloric test suffers from a number of shortcom­ings. First, caloric stimuli are not calibrated (Stockwell,
1997). Even though the external stimulus is the same, the effect on the labyrinth differs from one patient to another and sometimes from one ear to the other in the same patient. Therefore, one cannot compare the sen­sitivity of the labyrinths in different patients by com­paring the absolute responses to caloric stimuli. The variability in the caloric stimulus can be reduced to a manageable level by comparing the responses of the right and left ears of the same patient. In such a case, one has to make a key assumption that both labyrinths receive equal stimulation. Therefore, caloric responses from the right and left ears are expected to be equal in an individual with normal vestibular function. In prac­tice, the difference between right and left responses of a normal person can be relatively large due to the variability of the caloric stimulus. Furthermore, the assumption of both labyrinths receiving equal stimula­tion is not valid when perforations or other anatomic anomalies are present.
The second limitation of the caloric test is that it is primarily a test of the lateral semicircular canals and their afferent neural pathways. Although caloric responses from the anterior and posterior semicircu­lar canals are possible (Fetter, Aw, Haslwanter, Heim­berger, & Dichgans, 1998), the distance from the external auditory canal makes it impractical for the temperature gradient to effectively reach the vertical canals. In some individuals, caloric irrigations do provoke small verti­cal and torsional nystagmus from the anterior and pos­terior canals, but horizontal nystagmus from the lateral canal dominates the overall response (Aw, Haslwanter, Fetter, Heimberger, & Todd, 1998).
The third limitation of the caloric test is that it generates extremely low-frequency stimulation of the vestibular system. The vestibular receptors respond best to brief head movements within the frequency range of about 0.1 to 3 Hz. The caloric stimulus is estimated to be equivalent to head movements with the frequency of approximately 0.003 Hz (Hamid, Hughes, & Kinney, 1987). As a result, some compare testing the vestibular system with the caloric stimulus
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to testing the auditory system at frequencies that are not commonly included in audiometric testing.
Finally, caloric irrigations are distressing and poorly tolerated by some patients. If the patient expe­riences severe vertigo and nausea before completing the caloric test, the results are rarely useful. The exam­iner should try to predict when the patient is likely to become ill and discontinue the irrigation before the onset of severe symptoms.
Given the limitations of the caloric test and the introduction of newer vestibular tests such as vestib­ular-evoked myogenic potentials (VEMPs) and video head impulse testing (vHIT), some have advocated abandoning the caloric test as a routine part of evalua­tion for dizzy patients. However, it is important to rec­ognize that despite these limitations, the caloric test has withstood the test of time and has been the single most useful test of the labyrinth and its afferent pathways. This is especially true in view of recent findings show­ing discrepancies in the caloric test and vHIT findings in different vestibular patient groups (Jung, Suh, & Kim, 2017; McCaslin, Rivas, Jacobson, & Bennett, 2015; Redondo-Martinez et al., 2016). Therefore, it seems that other vestibular tests can help in reducing the reliance on the caloric test, but it is premature to assume that they can replace the caloric test.
CALORIC IRRIGATORS
Two types of caloric irrigators are in clinical use today: water (open-loop) and air. A third type, the closed­loop water irrigator, is no longer manufactured com­mercially and will not be discussed further. Both water and air irrigator types are capable of delivering caloric stimulation at precise temperatures. Almost all com-
mercially available irrigators today have a built-in timer and a flow meter to regulate the duration and volume of irrigation. Furthermore, for computerized electronystagmography (ENG) and videonystagmog­raphy (VNG) systems, the irrigation temperature can be controlled by the computer to minimize the need for operator intervention.
There is controversy about the clinical use of air irrigators. The American National Standards Institute (ANSI) does not include them as a standard irrigation method in its latest recommendations for caloric test­ing (ANSI, 2009). The decision to exclude air in the ANSI standard is explained based on the lack of pub­lished data “to establish response variability equivalent to water calorics.” On the other hand, the British Soci­ety of Audiology (BSA), which has also published a set of standards for caloric testing, considers air irrigators acceptable for clinical use (BSA, 2010).
Given the controversy about air irrigators, it is worthwhile to consider the differences between the two irrigation methods. Table 12–1 summarizes the standard parameters recommended by ANSI and BSA for water and air irrigators. As is obvious from temper­ature, duration, and flow rate requirements, the heat capacity of air is far less than that of water (Fleming, Proctor, Dix, & Metz, 1978). That means that regulat­ing the temperature at the irrigator tip is crucial to the success of air irrigations. In addition, the actual tem­perature in the ear canal depends on the design of the delivery tip. The recommended temperatures in Table 12–1 are for irrigator tips where the air flows freely in and out of the ear canal. Some air irrigators seal the ear canal during the irrigation and cause the temperature at the TM to be significantly different compared with the temperature at the irrigator tip. Using the standard temperatures, especially for warm irrigations, can pose safety issues because the excess temperature can cause
Table 12–1. Irrigation Parameters Recommended by Different Organizations
Volume 200
Duration 40
Temperature (warm/cool)
Recommended by ANSI
(2009)
Water Air Water Air
± 20 mL/min
± 1 sec
44ºC/30ºC
± 0.5ºC
X
X 30 sec 60 sec
X
Recommended by BSA
(2010)
250
± 10 mL
44ºC/30ºC
± 0.4ºC
8
± 0.4 liters
50ºC/24ºC
± 0.4ºC
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a burning sensation in the ear canal. Therefore, any facility that uses this type of irrigator must follow the manufacturer’s temperature settings and establish its own normative values.
Another concern with some air irrigators is that they can heat air but they do not cool it. Instead, these irrigators use the air at the ambient temperature. These irrigators should be avoided for clinical use.
There are two papers that have addressed ANSI’s concerns regarding air irrigators. Zapala, Olsholt, and Lundy (2008) in a large-scale retrospective study showed that the sensitivity and specificity of both air and water calorics were similar for differentiating between normal and abnormal patients. In addition, they showed that the differences between warm and cool irrigation responses were higher for water calorics and that air calorics produced more uniform responses. Zapala et al. (2008) used slightly different tempera­tures for air calorics than those listed in Table 12–1 and they have advocated a similar procedure to calibrate caloric parameters as they did for their study. Similarly, Marques Perrella de Barros and Caovilla (2012) showed that there were no significant differences in unilateral weakness and directional preponderance for air ver­sus water calorics in 40 healthy individuals. They did report higher nystagmus intensities for individual irri­gations for water calorics compared with those for air calorics. This may explain the anecdotal reports that patients generally experience more discomfort during water calorics.
The exclusion of air in the ANSI standard has been largely ignored by the clinical community. Today, air irrigators are the most widely used method for generat­ing caloric stimuli, and their sales continue to outpace the sale of water irrigators by a large margin (personal communication with MicroMedical/Interacoustics and Otometrics/Natus).
Review of water and air irrigators show that both have advantages and limitations. The main advantage of water irrigators is that they are relatively simple and do not require a great deal of technical skill. The main disadvantage is the inconvenience. The returned water from the ear must be collected and some patients find water irrigations unpleasant because they produce strong caloric responses. Also, water irrigators cannot be used in patients with TM perforations. The main advantage of air is the convenience. There is no water to collect and it can be used in patients with TM per­forations. The main disadvantage of air irrigators is that they require more technical skill and a longer learning process.
In summary, both irrigation methods provide acceptable caloric stimulation. However, the examiner
must acquire the necessary skill to perform appropriate irrigations using whichever method he or she chooses. Furthermore, it should be noted that design differences for different irrigator models, especially for air irriga­tors, can influence the strength of the caloric stimula­tion. As a result, each clinic must either establish its own normative values or calibrate the caloric stimuli using methods similar to those described by Zapala et al. (2008).
PERFORMING THE CALORIC TEST
The most common form of caloric testing is the bither­mal caloric test. In this test, each ear is irrigated twice — once with a warm temperature and once with a cool temperature. This generates both excitatory and inhibitory responses from both ears. The validity of the caloric test is based on the assumption that both ears receive adequate and approximately equal stimulation. Some of the factors that affect the strength of caloric stimulation can be controlled by the examiner, such as the temperature and the duration of irrigations. It is the responsibility of the examiner to ensure that the controllable test parameters remain constant from one irrigation to another. Other factors are not controllable, such as the ear anatomy. The examiner must make a note of those uncontrolled factors that may affect the validity of the caloric test.
Preliminary Procedures
A few preliminary tasks should be performed before the caloric test. The ears should be inspected otoscopi­cally before the test. If there is cerumen blocking the ear canal, it should be removed before the irrigations. Even when the cerumen is not completely blocking the TM, the examiner may want to remove it because the irri­gation medium can push the cerumen deeper into the ear canal and impede the heat transfer. When removing the cerumen, it is best to suction or spoon it out instead of washing the ear canal with water. This is especially important for the users of air caloric systems because the remaining moisture in the ear canal may produce a cooling effect during warm irrigations and result in nystagmus initially beating in the opposite direction of what is expected for warm irrigations.
During the ear inspection, the examiner must make a note of any anatomic anomalies, such as those caused by surgery or trauma. Even when the ears look normal, anatomic changes may affect the heat transfer
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and interfere with caloric testing. Therefore, differences in the caloric responses from different ears should be interpreted cautiously when there is a history of ear surgery. Similarly, ear inspection should note any evi­dence of TM perforation, middle ear fluid, or otitis externa.
Before the test, the examiner should explain the procedure to the patient in an honest but nonthreat­ening manner. Developing good rapport is important because many patients are apprehensive about the caloric test. It is best to reassure the patient that the sen­sation of motion during caloric irrigations is expected and will not last long.
Standard Bithermal Caloric Test Procedure
First, the patient should be placed in the supine posi­tion with the head raised about 30 degrees. Eye move­ments must be calibrated at the beginning of the caloric test (see the next section about calibrations between irrigations). Next, visual fixation should be eliminated. At this time, the examiner should start the eye move­ment recording system and begin alerting the patient. The presence of any pre-existing nystagmus should be noted. The irrigation should begin promptly and should last anywhere from 30 to 60 seconds depending on the irrigation system (see Table 12–1). Once the irri­gation ends, the examiner should continue alerting the patient. The caloric response continues to get stronger and usually reaches its peak around 30 seconds after the end of the irrigation (about 60 to 90 seconds from the onset of the irrigation). Shortly after the response reaches its peak and begins to decline, the examiner should ask the patient to fixate on a stationary target. The fixation period is usually 5 to 10 seconds, after which the fixation should be eliminated again. The tracings should be marked to identify the beginning and the end of fixation. Eye movement recordings should continue until the caloric response subsides (usually two or three minutes from the onset of irriga­tion). After a waiting period, the remaining irrigations should be performed in the same manner.
Recalibration Before Each Irrigation
The ANSI (2009) standard as well as an earlier report by the Committee on Hearing, Bioacoustics, and Bio­mechanics (CHABA, 1992) recommend recalibration of eye movements before each irrigation. However, the most recent BSA recommendation has reversed the earlier standard and no longer requires it (BSA 2010). The concept of recalibration before each irrigation was a reasonable one for the users of older noncomputer­ized ENG equipment. However, for more modern com­puterized ENG and VNG systems, recalibration before each irrigation is an outdated recommendation that should be reconsidered.
Unlike ENG, in which eye movements are esti­mated indirectly by measuring the corneoretinal potential (CRP), eye movements in VNG are estimated directly by measuring the movements of the pupils. Therefore, recalibrations are unnecessary as long as the orientation of the cameras does not change with respect to the patient’s eyes. Even routine removal and replace­ment of the goggles have been shown to have minimal effect on the calibration (Andrew & Meredith, 2009).
Alerting Tasks
In any vestibular test that is performed in the absence of fixation, including the caloric test, it is necessary to keep the patient alert during the test (Jacobson & New­man, 1993). The purpose of alerting tasks is to maintain a steady stimulation of the higher cortical level brain activity that is most likely needed to generate the fast phases of nystagmus (Barin, 2009). As a result, the requirement for alerting tasks is independent of the eye movement measurement method.
A number of studies have examined the effect of different alerting tasks on the caloric response parame­ters (e.g., Davis & Mann, 1987; Formby et al., 1992). The most effective alerting tasks are those requiring inter­action of the patient with the examiner in which the patient is required to recall items from memory, such as names of states, cities, and so forth. The alerting tasks should be moderately challenging and on topics that are of interest to the patient.
Practical Considerations in Performing the Caloric Test
Although the above procedure is straightforward, there are many controversies and practical considerations that must be addressed.
Order of Irrigations
The ANSI and British standards recommend perform­ing irrigations in the bithermal caloric test in a specific order (ANSI, 2009; BSA, 2010). Warm irrigations are to be performed first, followed by cool irrigations in both standards. The ANSI standard requires the right ear to
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be irrigated first for both warm and cool temperatures. The BSA standard allows either the right or the left ear to be irrigated first, as long as the same order is used for both temperatures.
The main reason for the recommended sequence in the ANSI standard is the systematic decline in the intensity of caloric responses from the first to the last irrigation. Furman and Jacob (1993) first described this phenomenon and attributed it to central adapta­tion mechanisms. To reduce this bias, they suggested modifying the formulas used for quantifying the caloric responses or changing the order of irrigations. However, it is now clear that the underlying premise of the order effect in bithermal caloric testing may have been inaccurate. Lightfoot (2004) demonstrated that the order effect was specific to ENG and was not present in VNG. That is, the order effect is unrelated to the adap­tation mechanisms and reflects the systematic change in CRP over time. As a result, careful verification of cal­ibration (but not necessarily recalibration) before each irrigation can minimize or eliminate the order effect regardless of what order the irrigations are performed.
The main advantage of performing warm irriga­tions first is that under certain conditions, the examiner can interpret the caloric results without performing the cool irrigations (BSA, 2010). See the discussion on monothermal caloric testing below. However, there may be a disadvantage to starting with warm irriga­tions. Noaksson, Schulin, Kovacsovics, and Ledin (1998) have shown that starting with warm irrigations results in significantly stronger responses for warm irrigations. On the other hand, starting with cool irriga­tions can reduce the typical difference between warm and cool responses.
Based on the above discussion, it is clear that the order of irrigations recommended by ANSI (2009) and BSA (2010) is appropriate but is not the only accept­able sequence. In fact, when bithermal caloric testing is planned from the outset, performing cool irrigations first may have the advantage of reducing the differ­ence between the intensity of responses for warm and cool temperatures (Noaksson et al., 1998). Therefore, the examiner is free to start with either warm or cool irrigations as long as the ears are irrigated in the same order for each temperature.
Waiting Period Between Irrigations
The ANSI standard recommends waiting five minutes from the end of the recording for one irrigation to the beginning of the next irrigation (ANSI, 2009). The pur­pose of the wait period is to reduce residual effects of
the previous irrigation. However, the ANSI standard does not specify what constitutes the end of record­ing after each irrigation. That is, it is not clear whether the recording should be stopped after a fixed period of time from the onset of the irrigation or should continue until the caloric nystagmus dissipates completely.
In most patients, caloric-induced nystagmus dissi­pates within 3 minutes after the onset of the irrigation. However, there is strong evidence that the temperature gradient across the labyrinth persists much longer and, depending on the strength of the caloric response, may require over 10 minutes to return to its pre-irrigation state (Barnes, 1995). The effect of this residual tempera­ture gradient varies from one patient to another and from one irrigation to another. Therefore, maintaining a fixed time interval between successive irrigations may actually increase the variability of the caloric test. The most recent version of the BSA standard has tried to address this issue by recommending a 7-minute interval between the start of two consecutive irriga­tions with consideration for extending the interval for patients who continue to exhibit caloric-induced nys­tagmus after the wait period (BSA, 2010).
Monothermal Caloric Testing
A number of studies have considered the use of mono­thermal caloric tests either as a replacement or as a screening test for bithermal caloric testing (for a review, see Enticott, Dowell, & O’Leary, 2003; Jacobson, Calder, Shepherd, Rupp, & Newman, 1995; Murnane, Akin, Lynn, & Cyr, 2009). The advantages of monothermal caloric testing include shorter test time and possibly reduced patient discomfort. However, previous stud­ies that have compared monothermal and bithermal caloric tests have resulted in contradictory findings. The inconsistencies are most likely due to differences in the irrigation parameters and test procedures.
Some studies have entirely dismissed the use of monothermal caloric testing in clinical settings due to its presumed low sensitivity and specificity (e.g., Keith, Pensak, & Katbamna, 1991; Shupak, Kaminer, Gilbey, & Tal, 2010). However, several other studies have dem­onstrated that under certain conditions, monothermal caloric testing can be used as a screening test for the bithermal caloric test (e.g., Lightfoot et al., 2009; Mur­nane et al., 2009; Bush, Bingcang, Chang, et al., 2013). Yet significant disagreements remain about the other aspects of monothermal caloric testing.
A few studies recommend using a cool tempera­ture for monothermal testing. However, the majority of studies have demonstrated that warm monothermal