Venous balloon test occlusion for pulsatile tinnitus assessment: A clinical feasibility study

Abstract

Background

Pulsatile tinnitus (PT) can have huge impact on the patients’ quality of life and can be associated with curable vascular anomalies. In the present study, we aim firstly to describe our protocol for venous BTO and secondly to report possible predictors for a positive BTO test.

Methods

All consecutive PT patients undergoing BTO for the purpose of determining eligibility for venous neuro-intervention were included. We recommend BTO for patients when there is uncertainty in the association of the venous pathology identified on non-invasive cross-sectional imaging (CTV or MRV) and the patient's symptoms.

Results

Between May 2016 and October 2022, we recorded 29 venous balloon test occlusions fulfilling our inclusions criteria. Over the 29 procedures scheduled, 8 finally did not lead to a successful balloon test occlusion. The main reason was that the patient did not hear the PT on the day the angiogram was performed. Two patients could not have the BTO due to difficulties in venous navigation. After BTO, only four patients of our cohort were scheduled for an endovascular treatment.

Conclusion

We describe a technique and present a single cohort of venous BTO in severe PT patients with unclear anatomical cause. This angiographic test was useful to exclude patients from endovascular surgery and discuss the most probable cause of the PT. Complexity of vascular PT should support a patient-based approach when discussing interventional treatment.

Introduction

Pulsatile tinnitus (PT) is the perception of a rhythmical sound in the absence of an external source. It is usually synchronous with the heartbeat. Tinnitus can have a significant impact on patients’ quality of life ¹ and is associated with sleep disorders ² and anxiety disorders. ³ PT can be caused by various vascular anomalies that can be treated surgically.^4–7. These include dural arterio-venous fistula, arteriovenous malformations, carotid stenosis, and glomus tumors. Anatomic anomalies in the cerebral venous circulation have also been associated with PT and more recently have been shown to be effectively treated using endovascular techniques^4,8–11. These anomalies include venous sinus stenosis at various levels between the torcula and brachiocephalic vein (i.e. extrinsic causes such as idiopathic intracranial hypertension (IIH) and Eagle's syndrome or intrinsic causes such as arachnoid granulation), sinus diverticula, and high riding jugular bulb.^4,5 Since these anatomic features may be commonly reported for asymptomatic patients, it is often difficult for a clinician to attribute one anatomical finding to the symptoms and establish the indication for surgery.

Balloon test occlusion (BTO) is a common technique to plan deconstructive therapy for arterial pathologies such as internal carotid occlusions for giant complex aneurysms. ¹² However, the technique has been poorly described on the venous pathologies. BTO on the venous side serves two main purposes: to determine if the occlusion of venous structure improves the patient's symptoms and to determine if the patient can tolerate the hemodynamic changes brought about by the occlusion. In the present study, we aim firstly to describe our protocol for venous BTO and secondly to report possible predictors for a positive BTO test.

Methods

Patient population

All consecutive patients who underwent a BTO for PT assessment between May 2016 and October 2022 from our tertiary center, specialized in treating vascular PT, were considered in our study. This study did not require ethics approval because of its retrospective design. We recommend BTO for patients when there is uncertainty in the association of the venous pathology identified on non-invasive cross-sectional imaging (CTV or MRV) and the patient's symptoms. For instance, shunting lesions such as dural arteriovenous fistulae ipsilateral to the PT that underwent venous BTO prior to planning a treatment were excluded. Moreover, patients presenting with IIH and transverse sinus stenosis were considered as straightforward cases for endovascular treatment and did not require BTO. Conversely, PT associated a high riding jugular bulb will undergo venous BTO prior deciding on any interventions.

Medical files were reviewed for clinical and radiologic data. Venous anatomy on cross-sectional imaging as well as presence of bone dehiscence and extracranial stenosis were studied. Angiograms were reviewed to assess: venous drainage patterns and dominance, presence of stenosis and exclusion of arteriovenous lesions. Technical aspects of the BTO were reviewed including devices used, presence of a pressure gradient, site of balloon inflation, test outcome on PT, anatomical anomalies discovered, and complications related to the procedure.

Balloon test occlusion

First, a complete diagnostic angiogram was performed to assess the venous anatomy and cerebral blood flow drainage. From the preoperative CT, we identified one or both hemispheres with a suspected anatomical anomaly causing the PT. All procedures were performed using systemic heparinization. An 8F shorth sheath was placed in the right femoral vein for venous access. A 5F arterial introducer was placed on the right radial artery, through which a diagnostic catheter was used to perform the complete arterial angiogram, including a cervical view of the internal jugular veins from both sides. The 5F arterial catheter was then placed to the common carotid artery, on the side where the anatomical anomaly was suspected. A 3D rotational venous phase angiogram was performed to rule out irregular transverse sinus stenoses, which can be missed on antero-posterior and lateral projections. The injection was given through the arterial 5F diagnostic catheter, and the delay was calculated from the previous DSA run. This 3D venogram allowed us to study the venous anatomy more accurately and detect or exclude the presence of a dural sinus stenosis, especially for those that are irregular and not easily visualized on either the standard AP or lateral projections. We then performed a 2D venous run which was used as a roadmap to navigate a 6F long introducer over a 6F diagnostic catheter and an 0.035” guidewire (Advantage Glidewire, Terumo, Tokyo, Japan). We performed a venous pressure measurement, using the diagnostic catheter or a microcatheter (2.3F Progreat, Terumo, Tokyo, Japan), measuring from right atrium and cervical IJV to intracranial sinuses. Each pressure was noted to describe a brain to heart gradient and a post/pre stenosis gradient if present. After this, we performed the BTO using the long sheath, with or without support of an intermediate catheter if required. We then chose a balloon depending on the anatomical site we wanted to occlude. For a complete transverse sinus occlusion, 10  ×  80 Copernic (Balt, Montmorency, France) or Mustang (Boston Scientific, Marlborough, Massachusetts) balloon were selected. For more selective occlusion, like some condylar emissary veins, we preferred Scepter XC (Microvention, Aliso Viejo, California) or Eclipse 2L (Balt, Montmorency, France). Before and after inflation, the patient was asked to describe their tinnitus, blinded to the actual inflation or deflation. The tinnitus was reported before and after each inflation/deflation. Complete flow arrest was confirmed during each inflation by an arterial contrast run. BTO test results were characterized into three groups: positive (sound improved after inflation), negative (sound was stable), inconclusive (answer inconsistent or patient was not certain of its state).

Statistics

We performed a statistical analysis on the subgroup of patients who had a successful inflation of a balloon contemporary to a clinical PT reported before the inflation. We looked for association between a positive result and baseline demographics. To increase statistical power, because of the small sample, positive BTO were compared to a merge group of inconclusive and negative BTO. Quantitative variables were presented as mean and standard deviations, and they were compared with Mann–Whitney test. Qualitative variables were presented as percentages and compared with Fisher test.

Results

Baseline characteristics

Between May 2016 and October 2022, we performed 29 venous BTOs fulfilling our inclusion criteria. Figure 1 presents the flow chart of these patients and Supplemental Table 1 presents their clinical characteristics, radiological findings, devices used and BTO results for each patient. Mean patient age was 55.5 (SD 14.1), 75% were female. 25/29 patients had pure PT, 4 patients had IIH associated with PT. Localization of the PT was as follows: 9 were present on the right side, 13 on the left side, 7 were bilateral. Main indications were: persistence of PT after stenting of a venous stenosis, presence of Eagle's syndrome and other venous anomalies (condylar emissary vein, high riding jugular bulb).

Figure 1.

Pulsatile tinnitus patient flow chart.

BTO: balloon test occlusion; PT: pulsatile tinnitus.

Technical results

Over the 29 procedures scheduled, 8 finally did not lead to a successful BTO. The main reason was that the patient did not hear the PT on the day the angiogram was performed (five patients). One patient could undergo the provocative maneuver by positioning their head, leading to a disappearance of the PT secondary to an Eagle syndrome, therefore a balloon was not needed. Two patients could not have the BTO due to difficulties in venous navigation.

In the population where the balloon navigation was initiated (23 patients), technical success was defined as complete venous balloon navigation and inflation and was achieved in 21 patients (91.3%). For one patient navigation of the balloon was not possible due to tortuous anatomy, using a Scepter XC 4  ×  11. One patient could not endure the end of the procedure, which was longer than usual due to tortuous anatomy. Figure 2 demonstrates an example of a long balloon inflated from the right transverse sinus to the jugular vein on digital subtraction angiography. Figure 3 is another example of a more selective BTO of a high-riding jugular bulb. Supplemental videos 1 and 2 demonstrate the complete flow arrest in a right transverse sinus with a digital subtracted angiography before and after balloon inflation. To achieve this result, a large bore guiding catheter was used in all cases: 20/23 cases used a BMX (Penumbra, Alameda, California); 1 Cerebase (Cerenovus, Irvine, California); 1 Benchmark (Penumbra, Alameda, California); and 1 Destination (Terumo, Tokyo, Japan). In addition, an intermediate catheter was used in four cases, a 6F Navien (Medtronic, Minneapolis, Minnesota) was preferred. Large balloons were necessary to have a complete flow arrest. We used mainly Copernic 10  ×  80 mm (Balt, Montmorency, France) in 12/23 patients. Other balloons were Mustang 10  ×  40 mm (Boston Scientific, Marlborough, Massachusets), Scepter XC 4  ×  11 mm (Microvention, Aliso Viejo, California), and Eclipse 2L (Balt, Montmorency, France).

Figure 2.

Balloon test occlusion of a left transverse sinus. Venous digital subtracted angiography with antero-posterior (A) and lateral views (B) showing a left posterior condylar emissary vein (black arrow). After balloon inflation, occlusion of the left transverse sinus on antero-posterior view (C) and lateral view (D). Inflated 10-80 Copernic balloon (Balt, Montmorency, France) is visible on C and D (white star).

Figure 3.

Selective balloon test occlusion of a right sigmoid sinus. Venous digital subtracted angiography in antero-posterior projection (A), showing a right high riding jugular bulb (arrowhead). Inflation of a 10–40 Mustang balloon (Boston Scientific, Marlborough, Massachusetts) in the right sigmoid sinus (white star), demonstrated on the non-subtracted venous angiography in AP (B) and lateral (C) projections. Venous subtracted angiography demonstrates the flow-arrest in the sigmoid sinus (D).

Clinical results

Over 21 successful inflations: 12 patients reported a stable PT during balloon inflation, validating a negative test; 4 patients had a positive test (3 partially improved and 1 complete improvement of PT); 4 had inconclusive changes after inflation. One of the patients had a disappearance of the PT during the catheterization, before balloon inflation, which reappeared after 24 h. In this case, we concluded that the change of flow caused by the catheterization was enough to temporarily stop the PT. One patient surprisingly described a slight increase of her PT (less than 50%). This patient had a left PT, hypoplastic left transverse sinus, a minimally prominent left condylar emissary vein and vertebral plexus vein, a right high riding jugular bulb and bilateral internal jugular vein compressions. The balloon inflation covered from the right transverse sigmoid junction to the distal internal jugular vein.

Variables associated with positive BTO

We performed an analysis to look for baseline demographics variable predictive of a positive BTO (Table 1). As described earlier, inconclusive and negative BTO were merged as a same group, compared to positive BTO. The only variable associated with BTO result was age: over 21 successful inflations, patients with a significant PT decrease were 39.0 years old (33.0; 46.8) whereas patients whose PT did not improve were 61.0 (60.0; 69.0), p < 0.01.

Table 1.

Association between patient characteristics, balloon test occlusion technique (BTO), and BTO clinical result.

		BTO negative or inconclusive (17)	BTO positive (4)	p
Patient age, median [Q25–75]		61.0 [60.0; 69.0]	39.0 [33.0; 46.8]	<0.01
Patient sex, n	Female	11 (65%)	3 (75%)	1
Pathology, n	PT	16 (94%)	3 (75%)	0.35
	IIH  +  PT	1 (5.9%)	1 (25%)
PT side, n	Left	5 (29%)	1 (25%)	1
Whooshing yn, n	Yes	9 (53%)	2 (50%)	1
	No	8 (47%)	2 (50%)
Venous DAC, n	No DAC	14 (82%)	4 (100%)	1
	DAC	3 (18%)	0 (0%)
Venous balloon, n	Copernic 10  ×  80	8 (47%)	4 (100%)	0.76
	Scepter XC 4  ×  11	4 (24%)	0 (0%)
	Mustang 10  ×  40	2 (12%)	0 (0%)
	Mustang 10  ×  80	1 (5.9%)	0 (0%)
	Eclipse 2L	1 (5.9%)	0 (0%)
	Scepter 4  ×  11	1 (5.9%)	0 (0%)

After BTO, only four patients in our cohort were scheduled for an endovascular interventional treatment. Due to the small number, we did not perform statistical analysis on this subgroup. One patient with a positive BTO underwent transverse sinus stenting for stenosis with clinical success (complete improvement of PT). One patient who did not hear PT during the BTO underwent condylar emissary vein coiling with slight improvement post-operatively. One patient with an inconclusive BTO had a transverse sinus stenting and a coiling of a posterior emissary vein. This patient is currently being investigated for a CSF leak. One patient with a negative BTO had a condylar emissary vein coiling without efficacy. This patient is now being considered for transcranial stimulation. In addition, two patients with Eagle's syndrome were referred to an ENT surgeon after an attempted BTO: one had an inconclusive result, one a failed attempt.

Complication

One patient had a complication with a transient IV cranial nerve paresis after the BTO. An MRI was conducted at 1 week, showing rare punctate ischemic lesions. The post-operative CTA raised a doubt on an iatrogenic right V2 dissection, but a previous CTA showing the same anomaly was more in favor of an anatomic variant. To note this patient was treated temporarily with aspirin, without ischemic recurrence.

Discussion

This is the first study to demonstrate the use of BTO for PT assessment. From 29 attempted BTOs, the exam was successfully completed for 21 patients. The main reason for failure was that patients could not hear the PT sound the day of the exam. It could be because the PT was less present during the angio, there was difficulty to assess the symptoms in the supine position, or with the distraction of noises from the monitoring equipment inside the angiosuite. There were only two technical failures where the balloon could not be navigated through the tortuous venous anatomy. This study demonstrated the feasibility of the BTO technique for PT in everyday practice and its value to exclude or consider patients for endovascular surgery. The BTO was positive in only four patients, however, this number can be explained by our inclusion criteria which included a highly selected population from clinically unclear or doubtful cases from a tertiary PT center. For example, clear transverse sinus stenosis would not require BTO and was directly addressed for endovascular treatment.

Although BTO are widely used in INR to occlude arterial feeders before planning a deconstructive therapy, its use on the venous anatomy is less common. Firstly, it has been described to select patients for endovascular treatment of dural arteriovenous fistulas before sinus occlusion by coils. ¹³ A case report has also reported the use of venous balloon inflation to test the occlusion of the straight sinus in the pre-operative planning of a deconstructive therapy for meningioma surgical resection. ¹⁴ Another case report described a BTO of sigmoid sinuses before tumor resection. ¹⁵ Regarding PT, Park et al. ¹⁶ demonstrated the interest to use conscious sedation as they were filling a venous diverticulum with coils, where the patient reported an improvement immediately after the filling. Similarly, conscious sedation has been used to assess the efficacy of a transverse sinus stenosis by stenting. A Solitaire stent was deployed, non-detached, and the resolution of the clinical symptom led the team to detach the stent and treat the patient. ¹⁷ Apart from angiographic findings, clinical maneuvers have demonstrated to be very useful in patients’ selection. Eliezer et al. described different patterns after manual cervical compression: resolution of PT after carotid compression was defined as arterial; resolution of PT after jugular compression was defined as venous; no change was defined as neutral. The authors showed that the clinical pattern defined as “venous PT” after cervical compression was the only patient cluster in which embolization was a clinical success. ¹⁸ These observations support the idea that clinical and angiographic selection are feasible and crucial for PT treatment. A recent large series have been published, including 164 patients with PT undergoing DSA. ⁸ Among them, 66 patients (40%) underwent a BTO which was done at the discretion of the neurointerventionist. As expected, its use was associated with venous PT and non-vascular PT compared with PT caused by shunting lesion. Unfortunately, the results of the BTO tests were not described.

In our study, patients with a positive BTO were significantly younger. As vascular PT is a very complex and multicausal pathology, this result is difficult to interpret. Firstly, hearing loss is the most common factor for tinnitus. ¹ Advanced age could be the cause for non-vascular tinnitus, therefore not responding to BTO. In addition, we could raise the question that vascular causes at the origin of the PT could be more plastic at a younger age, therefore more able to BTO positive result and maybe treatment success. The low positivity of BTO in this series translates the complexity of then assessment of thesome of severe PT cases. Initially, these cases were not considered for treatment because there was no clinical/imaging correlation that could justify a primary indication for a treatment.

This study has some limitations. Firstly, this is a retrospective analysis of a prospective collected series of cases of patients presenting severe PT with significant impact on their quality of life with unclear or doubtful association with venous structures that were not considered for a treatment in a first assessment. Secondly, we present a relatively large cohort regarding this rare disease but 29 patients are not enough to conclude on statistical analysis, especially regarding the few treatments done. A larger cohort is necessary to confirm statistical associations with multivariate analysis and to repeat the analysis in the multiple venous pathologies subgroups.

Conclusion

Venous BTO is a useful exam for assessment of patients experiencing severe PT with unclear anatomical cause. This angiographic test was useful to exclude patients from endovascular surgery and discuss the most probable cause of the PT. Complexity of vascular PT should support a patient-based approach when discussing interventional treatment.