Skull Vibration-Induced Nystagmus in Superior Semicircular Canal Dehiscence: A New Insight into Vestibular Exploration—A Review

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

This review clarifies many obscure points of a phenomenon such as Skull Vibration-Induced Nystagmus in Superior Semicircular Canal Dehiscence observed by many authors but not always physiologically understood.

The aim of the review proposed by authors was to collect in literature the insights given by a skull-vibration-induced-nystagmus test performed with bone conducted stimulations in superior semicircular canal dehiscence (SCD). The argument is original and the point of view relevant beucause this bedside test is a recent useful insight among other bedside examination tests for the diagnosis of SCD in clinic. The conclusions are consistent with the text and careful reading of the text will allow an easier diagnosis of dehiscence, allowing the correct interpretation of difficult nystagmic signs. The proposed bibliography is excellent and recent.

Author Response

Comments and Suggestions for Authors

This review clarifies many obscure points of a phenomenon such as Skull Vibration-Induced Nystagmus in Superior Semicircular Canal Dehiscence observed by many authors but not always physiologically understood.

The aim of the review proposed by authors was to collect in literature the insights given by a skull-vibration-induced-nystagmus test performed with bone conducted stimulations in superior semicircular canal dehiscence (SCD). The argument is original and the point of view relevant beucause this bedside test is a recent useful insight among other bedside examination tests for the diagnosis of SCD in clinic. The conclusions are consistent with the text and careful reading of the text will allow an easier diagnosis of dehiscence, allowing the correct interpretation of difficult nystagmic signs. The proposed bibliography is excellent and recent.

Answer

 Dear Reviewer,

Many thanks for having reviewed our manuscript.

We are grateful for the recognition of our efforts and appreciate your comments.

Submission Date

15 November 2023

Date of this review

27 Nov 2023 10:12:52

Author Response File: Author Response.pdf

Reviewer 2 Report

Comments and Suggestions for Authors

My congratulations to the authors for putting this review together.  This is a topic that needs much more exploration and discussion.  This paper needs to be published but I have a few suggestions for consideration to include.

1. The studies discussed were all small but also the technical aspects of the vibration utilized varied.  One would suspect vision allowed vs vision denied scenarios may produce a different result if only simply the magnitude of the response.  The vibrators utilized could certainly impart differing degrees of energy and could be a significant factor in differing outcomes, even when the same frequency is used.  For example, I have been using SVIN testing for 20 years, and I have two different vibrators.  Although they are both 100 Hz, I am sure the displacement between the two is different, making the one with greater magnitude of displacement a “more sensitive” test.  Further, one is battery operated and the other is a plug-in.  When the batteries are getting low, the vibration reduces in magnitude and the magnitude of the nystagmus drops off.  Whereas the plug-in device gives much more stable output.

2. One explanation for different outcomes in SCD patients is the concomitant existence of vestibular loss/weakness.  This would obviously result in a look that is a combination of SCD and uVL results from the SVIN test.  This is not an academic concern.  Most studies on SCD fail to report a thorough vestibular evaluation.  Many of the SCD patients have caloric weaknesses or deficits noted on rotational chair or higher frequency studies.  These are not accounted for in the paper.  The paper discusses SCD and uVL as if they are mutually exclusive entities – they are not.

3. Another possible explanation is individual patient anatomic variability.  A recent paper of a large group of SCD patients demonstrated that 18% had a concomitant additional ipsilateral dehiscence.  Some of these dehiscences may not have a significant impact on SVIN but some certainly would.

4. The authors touched on the subject of test order.  Has anyone specifically studied this?  If so, or not, please state such.

5. Lastly, on Line 574, the authors state that SCD is a rare disorder.  It is not rare.  Rare disorders have a specific definition – those that affect less than 0.06% (U.S.) or 0.05% (EU) of the population.  We know from temporal bone studies that at least 0.5% have SCD and 1.5% have extreme bony thinning (<0.1 mm thickness).  When one looks at just the chronically dizzy population, the percentage of patients with SCD is certainly higher than that.  A better way to state Line 574 would be that it is “rarely diagnosed.”

Author Response

Reviewer 2.

My congratulations to the authors for putting this review together.  This is a topic that needs much more exploration and discussion.  This paper needs to be published but I have a few suggestions for consideration to include.

Answer:

Dear Reviewer,

Many thanks for having reviewed our manuscript and for your suggestions to improve it.

We modified the paper accordingly. Here follow our answers to each of your comments. The modifications are highlighted in yellow in the revised MS.

• The studies discussed were all small but also the technical aspects of the vibration utilized varied.  One would suspect vision allowed vs vision denied scenarios may produce a different result if only simply the magnitude of the response.  The vibrators utilized could certainly impart differing degrees of energy and could be a significant factor in differing outcomes, even when the same frequency is used.  For example, I have been using SVIN testing for 20 years, and I have two different vibrators.  Although they are both 100 Hz, I am sure the displacement between the two is different, making the one with greater magnitude of displacement a “more sensitive” test.  Further, one is battery operated and the other is a plug-in.  When the batteries are getting low, the vibration reduces in magnitude and the magnitude of the nystagmus drops off.  Whereas the plug-in device gives much more stable output.

Answer:

Thank you for your remarks. This is a real concern. I have a very similar experience : there is a patent difference of efficiency between a mechanic off axis rotating vibrator (masselotte) ( Synapsys or Inventis device) and an electromagnetic device particularly depending on a battery . There are numerous commercialized vibrator using frequencies at 100Hz but small amplitudes of vibrations < 0.2 mm. They are very well tolerated and cheap but not much efficient. We have experienced it with the Synapsys- Inventis vibrator  vs a cheap 100 Hz battery vibrator whose amplitude was small. This was the object of a medicine thesis report in the course of a French DIU. The commercial device showed false negative response in 30 % of UVL patients  tested positively with the Synapsys-Avantis device at equal frequencies of 100Hz. Moreover the SVIN slow phase velocity was significantly lower with the commercial battery device. This may be interpreted in the light of a minimal energy needed to stimulate the inner ear hair cells bundle. IS. Curthoys et al. (2013-2015) have already mentioned that these type 1 vestibular inner ear hair cells  respond to “jerks” as tectonic or seismic sensors. Dlugaiczik et al. have already mentioned suitable head accelerations between 0.1 to 0.4g and for tolerance accelerations < 2g. We have published in 2000 in a clinical work the need of minimal amplitude of vibration > 0.1 mm. Dumas G, Michel J, Lavieille JP, Ouedraogo E. [Semiologic value and optimum stimuli trial during the vibratory test: results of a 3D analysis of nystagmus]. Ann Otolaryngol Chir Cervicofac. 2000 Nov;117(5):299-312. PMID: 11084404.

These references have not been added in this paper since this review paper is limited  for the number of self-citations.

The technical conditions of SVIN concerning vision denied are as you mention an essential point. The fixation denied is needed to improve the response. For example in Aw’s experience (19) the horizontal component is negligible possibly because of a target fixation and inhibition of the hor. component.

This is now briefly commented in the chapter “limitations”.

Vibrators using adequate frequencies from 100 to 800 Hz may miss the nystagmus mainly when the vibrator amplitude is too small to provoke a jerk effect on the inner ear hair cell bundles which work as seismic receptors as already described by IS. Curthoys. Dlugaiczyk et al. (27) showed that the vibration needs accelerations of the head between 0.1 and 0.4 g to elicit a neural response, which are values below 2 g, non invasive  in human. Otherwise, it has been showed that for a constant frequency vibrators delivering amplitudes of vibrations lower than 0.1mm were inefficient to reveal a nystagmus. The series using frequencies only around 100 Hz may miss the nystagmus which is sometimes visible at 400 Hz or at higher frequency vibrations. The SVIN is sometimes very poor with small SPV at 100 Hz (9). 

Some publication (18) using eye fixation  minimizes or suppresses by inhibition  the horizontal component. Thus, it is mandatory when using SVINT to mask the not recorded eye to improve the response and suppress this bias (24).

• One explanation for different outcomes in SCD patients is the concomitant existence of vestibular loss/weakness.  This would obviously result in a look that is a combination of SCD and uVL results from the SVIN test.  This is not an academic concern.  Most studies on SCD fail to report a thorough vestibular evaluation.  Many of the SCD patients have caloric weaknesses or deficits noted on rotational chair or higher frequency studies.  These are not accounted for in the paper.  The paper discusses SCD and uVL as if they are mutually exclusive entities – they are not.

Answer:

This could be the case and a prior VHIT testing or Caloric testing before SVIN is useful or recommanded to allow a better interpretation of the different SVIN components in SCD.

In our experiencee the implication of  lateral SCC is  seldom concomitantly observed

The caloric test and HVHIT results are often normal. We have more frequently observed VHIT modifications for the sup SCC which we have mentioned in table 1&2 Dumas  et al. Eur Ann Otorhinolaryngol Head Neck Dis. (2019) (reference 9).

In this paper concerning 40 patients (27 uSCD and 13 bSCD) the caloric test (CaT) and VHIT were systematically performed in most patients.The caloric test was modified in 3/ 23 patients and the Hor SCC VHIT was modified in 1/22 patients . The Sup SCC VHIT  gain % asymmetry  was modified in 5/22 patients.The VHIT was performed in 22 of 27 uSCD  and the CaT in 23 of 27 uSCD.

This is now corrected  in the MS in the  discussion concerning the SVIN horizontal component.

The SVIN horizontal component frequently observed in SCD cannot be attributed to an unlikely concomitant horizontal SCC pathology since a caloric test modification in SCD is seldom observed (3 cases of 23 SCD) and a HVHIT function % of asymmetry in 1/22 cases in Dumas series (9). However this interaction remains possible in some cases. An anterior SCC VHIT gain asymmetry was more frequently observed in 5/ 22 patients.

• Another possible explanation is individual patient anatomic variability.  A recent paper of a large group of SCD patients demonstrated that 18% had a concomitant additional ipsilateral dehiscence.  Some of these dehiscences may not have a significant impact on SVIN but some certainly would.

Answer

This is a pertinent remark. We acknowledge the reviewer for this observation. This condition is possibly underestimated. In our experience we observed a bilateral condition in 13 of our 40 SCD patients (ref 19) and more seldom ipsilateral other topographical associated dehiscence  . However  this observation in our experience is not frequent enough to give conclusions. Aw (19) mentioned in bilateral  SCD condition a possible enhancement of the vertical component..

This is now briefly reported in the discussion and a reference 47 has been added.

There is otherwise individual patient anatomic variability in SCD and recent papers (47) showed that 18% had a concomitant additional ipsilateral dehiscence.  Some of these dehiscences may have  a significant impact on SVIN components.

• The authors touched on the subject of test order.  Has anyone specifically studied this?  If so, or not, please state such.

Answer:

To my knowledge I have not noticed a published systematic study on this topic. We have a current oncoming study about it. What is  mentioned in this paper is what the initial observations suggested.

• Lastly, on Line 574, the authors state that SCD is a rare disorder.  It is not rare.  Rare disorders have a specific definition – those that affect less than 0.06% (U.S.) or 0.05% (EU) of the population.  We know from temporal bone studies that at least 0.5% have SCD and 1.5% have extreme bony thinning (<0.1 mm thickness).  When one looks at just the chronically dizzy population, the percentage of patients with SCD is certainly higher than that.  A better way to state Line 574 would be that it is “rarely diagnosed.”

Answer:

Thank you for this remark. Carey et al. 2000 have signaled in a systematic analysis of 1000 temporal bones from archives that 0.5% had an anatomic patent SCD. This is now notified in the discussion  line 580 – 582 and a reference has been added.

SCD is an infrequent pathology (0.5% in Carey’s series of temporal bones from archives)(56). This pathology  is possibly otherwise frequently misrecognized in the clinic (49-51).

Submission Date

15 November 2023

Date of this review

10 Dec 2023 19:07:49

Author Response File: Author Response.pdf

Reviewer 3 Report

Comments and Suggestions for Authors

This is a very interesting study with a detailed review of published experience with vibration-induced nystagmus in SCD patients.  The work is of high practical value and the underlying explanation of the pathophysiological principles of SVIN variability is valuable.

I recommend it for publication after correction of several typos and clarification of the following few ambiguities:

The paragraph between lines 84 to 92 is unclear, probably the phrase "the full list of references" was swapped from line 88 after "..., USA)" on line 92. The sentence does not make sense in its present form.

The sentence on line 91 should end "...systematic review."

The paragraph between lines 84 to 92 is unclear, probably the phrase "the full list of references" was swapped from line 88 after "..., USA)" on line 92. The sentence does not make sense in its present form.

The sentence on line 91 should end "...systematic review."

Table 1 : the abbreviation Se (Sensitivity) is explained only after page 7 and is missing from the table legend.

In the legend to Table 1, line 117, there should be no comma after "follows,:".

On line 120, on the other hand, there is no period after "...side)".

Line 128 5- missing "s" in the word "videocopy"

Table 2 :

The abbreviation "GD" is not explained.

It is not clear what "Size estimate" is

„Dw“ abbreviation for Down-beating nystagmus is non-standard, it is aquestion whether to replace the word Down with the abbreviation at all, it fits comfortably in the table.

line 288 - misplaced space after the abbreviation "SPV :slow phase..." = should be

"SPV: slow phase…"

line 532 missing period after "deflection"

line 545 missing "o" in "endlymph"

line 711, References , the title of paper 43 is all capitalized.

Author Response

Comments reviewer 3

Comments and Suggestions for Authors

This is a very interesting study with a detailed review of published experience with vibration-induced nystagmus in SCD patients.  The work is of high practical value and the underlying explanation of the pathophysiological principles of SVIN variability is valuable.

I recommend it for publication after correction of several typos and clarification of the following few ambiguities:

Answer:

Many thanks for having reviewed our manuscript and for your suggestions to improve it. We modified the paper accordingly. Here follow our answers to each of your comments. The modifications are highlighted in yellow in the revised MS.

1-The paragraph between lines 84 to 92 is unclear, probably the phrase "the full list of references" was swapped from line 88 after "..., USA)" on line 92. The sentence does not make sense in its present form.The sentence on line 91 should end "...systematic review."

Answer:

This is now corrected in the revised MS. The end of the last sentence of the paragraph has been deleted.

The PRISMA guidelines were followed to conduct the systematic review. and the full list of references

2 - Table 1 : the abbreviation Se (Sensitivity) is explained only after page 7 and is missing from the table legend.

Answer:

The explanation of “Se”: “sensitivity of the test” is now included in the legend of table 1

It is now mentioned as follows in the legend line 114: “Se: sensitivity of the test. ViVOR: vibration-induced Vestibulo Ocular Reflex. The directions… »

3,- In the legend to Table 1, line 117, there should be no comma after "follows,:".

On line 120, on the other hand, there is no period after "...side)".

Line 128 5- missing "s" in the word "videocopy"

Answer:

These typing errors are now corrected in the lines 117,120 and 128

4- Table 2 :

The abbreviation "GD" is not explained.

Answer:

This means Protocol proposed by GD : (G. Dumas) : order 1 of stimulation= Stimulations of mastoids before vertex.

This is now mentioned as follows in the legend of the table 2 lines 257 , 258::

1. GD. (G.Dumas protocol)= Order 1 in 12 patients: Mastoid stimulation before vertex (Vx) stimulatio AC. (A.Castellucci protocol)= Order 2 in 27 patients: Vertex stimulation before mastoid stimulation.

The abbreviation AC means order 2 of stimulation= stimulation of vertex before the mastoids. Protocol proposed by AC (A. Castellucci)

This is now also explained in the text of the MS line 210 and 211

5 - It is not clear what "Size estimate" is

Answer:

The word “estimate” has been  deleted since the size was measured by neuroradiologists

6 -„Dw“ abbreviation for Down-beating nystagmus is non-standard, it is aquestion whether to replace the word Down with the abbreviation at all, it fits comfortably in the table.

Answer:

It is now modified in table 1 & Table 2: “Dw” has been replaced by “Down”.

7- line 288 - misplaced space after the abbreviation "SPV :slow phase..." = should be

"SPV: slow phase…"

line 532 missing period after "deflection"

line 545 missing "o" in "endlymph"

Answer:

The Typing errors lines 288, 532 and 545 are now corrected in the revised version of the MS

• line 711, References , the title of paper 43 is all capitalized.

Answer:

This is now corrected in the revised version of the references of the MS .

Cohen B, Suzuki JI, Bender MB. Eye movements from semicircular canal nerve stimulation in the cat. Ann Otol Rhinol Laryngol. (1964);73:153‑69.

Author Response File: Author Response.pdf