Blood flow changes in the transverse-sigmoid sinus junction following effective surgical reconstruction for unilateral pulsatile tinnitus with sigmoid sinus wall anomalies: a four-dimensional flow magnetic resonance imaging analysis

Introduction

Pulsatile tinnitus (PT), which is mainly caused by vascular lesions, may have serious consequences for patients. PT can be arterial or venous in origin. Sigmoid sinus wall anomalies (SSWAs) are the most common causes of venous PT, accounting for up to 86.4% of cases (1). SSWAs mainly consist of sigmoid sinus wall dehiscence (SSWD; a localized defect of the sigmoid sinus bone wall, ranging from 0.1 to 10 mm), a sigmoid sinus diverticulum (SSD; the venous wall shows a localized pouch-like protrusion, similar in shape to an arterial aneurysm), and sigmoid sinus enlargement (2), and are often accompanied by an upstream transverse sinus stenosis (TSS) (3-5). SSWAs are often located in the transverse-sigmoid sinus junction (TSSJ), which is the location of sinus angulation (2). SSWA and PT occurrence is associated with the long-term effects of a large and high-speed blood flow, and vortex patterns (6-8).

Surgical reconstruction is often used to treat PT with SSWAs. SSWAs are filled with a new sigmoid sinus wall formed by autologous temporalis fascia, a periosteal flap, and temporal bone powder (9). The success rate of the procedure is high (approximately 70–90%) (9-12). However, a considerable number of patients complain of different degrees of recurrence during the long-term follow-up, which is suspected to be related to SSWD. It is not yet clear whether SSWD formation is related to the repair material, the blood flow effect, or a combination of multiple factors.

Traditional computed tomography (CT) and magnetic resonance imaging (MRI) examinations can only detect routine morphological abnormalities of venous PT (13); however, the development of morphological abnormalities and long-term recurrence of PT may be due to abnormalities in blood flow properties. Currently, no research has investigated the blood flow properties before and after surgical reconstruction based on real-world data.

Previous imaging studies after surgical reconstruction have reported the morphological characteristics of wall repair (14), but multiparameter blood flow characteristics have not been reported. Four-dimensional (4D) flow MRI is a phase contrast (PC) MRI that combines time-resolved and three directional flow velocity encoding. It can quantitatively obtain blood flow data of any node, section, or entire area within a reasonable scanning time and achieve dynamic visualization. We previously used 4D flow MRI to evaluate the differences in blood flow properties between SSWAs in normal individuals and PT patients (15).

This study used 4D flow MRI to explore the changes in blood flow properties in the TSSJ of patients with unilateral venous PT after effective surgical reconstruction to determine the effect of the surgical procedure on the PT-related blood flow. We present this article in accordance with the STROCSS reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-426/rc).

Methods

Participants

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Institutional Ethics Board of the Beijing Friendship Hospital, Capital Medical University (No. 2020-P2-202-01), and the requirement of individual consent for this retrospective analysis was waived. All the patients were recruited from the Beijing Friendship Hospital. To be eligible for inclusion in the study, the patients had to meet the following inclusion criteria: (I) have a clinical diagnosis of unilateral venous PT, with a tinnitus frequency consistent with that of the heartbeat/pulse, and tinnitus symptoms that were significantly relieved or completely disappeared after the affected internal jugular vein was pressed; (II) have undergone preoperative computed tomographic angiography/venography (CTA/V); (III) have SSWAs identified by preoperative CTA/V, and further confirmed by the complete resolution or significant alleviation of PT following standard surgical reconstruction as mentioned in our previous study (9,10); and (IV) have undergone 4D flow MRI within 2 days before surgery and after surgery, with PT elimination or significant alleviation after at least 6 months of follow-up. Significant alleviation of PT after surgery was defined as a reduction in the noise intensity by more than 70% as assessed by the Tinnitus Handicap Inventory scale and patient subjective perceived tinnitus loudness score, or as an occasional occurrence. Patients were excluded from the study if they met any of the following exclusion criteria: (I) had undergone an imaging examination indicating vascular tumor, non-vascular tumor, atherosclerosis (>50%), dura mater arteriovenous fistula, or other arterial vascular variations; and/or (II) had poor-quality images. The poor image quality was due to the shaking experienced by some patients during scanning, which resulted in images with heavy motion artifacts that could not be used and analyzed (3 cases).

After screening, 19 patients (18 females and 1 male) with unilateral venous PT caused by an SSWA were included in this study. The SSWAs of these patients were identified by preoperative CTA/V, and further confirmed by the complete resolution or significant alleviation of PT following standard surgical reconstruction as mentioned in our previous study (9).

Surgical procedure

All the patients underwent surgical reconstruction under general anesthesia. A postauricular incision was made, and the fascia of the temporalis muscle was removed and collected for later use. The mastoid cortex was separated and exposed, and the mastoid cortical bone powder was collected for use. If an SSD was present, the mastoid cavity was ground open to expose the SSD, and the diverticulum was contorted, softened, removed, and then repaired with the above-mentioned temporalis fascia. The cavity and fissure were filled with the bone powder and fixed with medical aural and encephalic glue. The mucoperiosteal flap was backfilled and bandaged after suturing.

MRI protocol

A 3.0T magnetic resonance (MR) scanner (Ingenia, Philips Healthcare, Amsterdam, the Netherlands) and a commercial head coil were used for cerebral 4D flow MRI. The scanning range ran from the torculum to the jugular bulb, allowing for complete observation of blood flow characteristics within the transverse sinus and sigmoid sinus. All images were acquired retrospectively via electrocardiogram gating, multiple turbo field echo sequences, and three-directional velocity encoding. Before scanning two-dimensional (2D) phase contrast (PC) and 4D flow sequences, MR venography scans were performed to obtain a more accurate venous morphology and determine the extent of localization. The velocity encoding of 4D flow MRI was flexibly determined according to 2D PC MRI with one-direction velocity encoding. The velocity encoding of 2D PC MRI was first set to 80 cm/s. If images demonstrated velocity aliasing, the encoding was increased by 20 cm/s, and the final velocity encoding of 2D PC MRI without velocity aliasing was set to that of 4D flow MRI. The position was fixed on the luminal section of the TSS. Because the blood flow velocity was greatest at the TSS, this velocity encoding setting prevented velocity aliasing. The detailed acquisition parameters used for 2D PC MR were as follows: repetition time/echo time (TR/TE): 10 ms/5.8 ms; flip angle (FA): 10°; field of view (FOV): 161 mm × 161 mm; matrix size (MS): 160 mm × 160 mm; reconstructed voxel size: 0.305 mm × 0.305 mm; slice orientation: the luminal section of the TSS; bandwidth: 192.4 Hz/pixel; cardiac phases: 13; and scan time: 1’23”. The acquisition parameters for 4D flow MRI were as follows: TR/TE: 8.5 ms/3.9 ms; FA: 20°; FOV: 161 mm × 161 mm × 40 mm; MS: 160 mm × 160 mm × 40 mm; reconstructed voxel size: 0.459 mm × 0.459 mm × 1 mm; slice orientation: transverse; bandwidth: 193.4 Hz/pixel; cardiac phases: 13; and scan time: 5’24”.

4D flow data analysis

GTFlow software (version 3.2.10, GyroTools, Zurich, Switzerland) was used to preprocess, visualize and quantify the 4D flow MRI data. Before the data visualization and quantification, region mask application, eddy current correction, velocity aliasing correction, and vessel segmentation were performed for preprocessing. The blood flow pattern was represented by the color streamline generated by the software to reflect the velocity and morphology. Two independent radiologists with at least 5 years of experience each, who were double-blinded to the clinical data, assessed the jets or vortices in the TSSJ. A vortex was defined as the closed formation of a concentric circular flow. If the outcomes differed, the final decision was made by a senior radiologist with 8 years of experience. Some indicators, including the maximum velocity (V_max, cm/s), average velocity (V_avg, cm/s), net flow (Flow, mL/s), and heart rate (HR), were also measured quantitatively. To ensure a fair comparison, whether on the ipsilateral or contralateral side, all the preoperative upstream TSSJ measurements were performed at the location where the peak velocity occurred; the downstream TSSJ measurements were performed at the beginning of the vertical segment of the sigmoid sinus, and the corresponding postoperative measurements were performed at the same level. The purpose of scan positioning was to evaluate whether surgery would alter the blood flow status upstream of the stenosis and downstream of the sigmoid sinus, which was adjacent to the surgical area. The contour was manually drawn along the vessel wall in the sectioned planes, and the V_max, V_avg, Flow, and HR were automatically defined in all 13 phases of one cardiac cycle.

Statistical analysis

The statistical analysis was conducted using SPSS (version 26.0, IBM Corp., Armonk, NY, USA). Differences between the pre- and postoperative up/downstream hemodynamic data were analyzed. The normality of the measurement data was assessed by the Shapiro-Wilk test. The paired-sample t-test was used if the data followed a normal distribution; otherwise, the Wilcoxon signed-rank test was used. A P value less than 0.05 was considered statistically significant.

Results

Patient demographics

The patients had an average age of 36.05±8.90 [23–52] years, and an average body mass index (BMI) of 22.99±2.87 kg/m² (range, 17.31–27.18 kg/m²). All the patients had unilateral PT (right: 13, left: 6). Of the 19 patients, 13 underwent surgery for an SSD, and 6 underwent surgery for SSWD; additionally, 84% (16/19) of the patients had a stenosis in the upstream TSSJ (Table 1).

Ipsilateral blood flow assessment

At the upstream TSSJ, only the V_avg differed significantly before and after treatment (P=0.01), while the V_max and Flow did not differ. At the downstream TSSJ, there were no significant differences in all indicators of any group.

At the TSSJ, 17 of the 19 patients had vortices (closed concentric circular flow) on the surgical side before surgery. Of these 19 patients, 14 had vortices on the surgical side only, and 3 had vortices on both sides (Table 1). Of the 13 patients with SSDs, 11 had accompanying vortices. In addition, the blood flow velocity of all the patients was relatively fast, and all patients with the TSS demonstrated high-speed jet flow streamlines (a sudden acceleration and a jet-like shaped blood flow as it passed through the TSS position). Of the 17 patients with vortices before surgery, the vortices disappeared completely in 8 patients, and slowed in 9 patients after surgery. Among the 11 SSD patients with vortices before surgery, the vortices disappeared completely in 8 patients, and slowed in 3 patients after surgery (Table 1). Vortex slowing was defined as a significant reduction in the number of streamlines of the vortex, and the flow velocity was observed visually after surgery under the same settings in the 3D color rendering. However, high-speed jets from the upstream TSSJ were still observed in all the patients with a TSS. The changes in blood flow patterns are shown in Figure 1.

Figure 1 Pre- and postoperative streamlines in a patient with a sigmoid sinus wall anomaly. (A) Preoperative streamline showing vortices in the sigmoid sinus wall anomaly and upstream jets generated at a transverse sinus stenosis. (B) Postoperative streamline showing the disappearance of vortices following the elimination of the diverticulum, and the presence of a remnant jet flow similar to the preoperative blood flow. The vortex is a localized concentric circular flow along the inner wall of the diverticulum. Jet flow refers to the jet-like shape of suddenly accelerated blood flow when it passes through the position of the transverse sinus stenosis.

Contralateral blood flow assessment

Only the downstream V_max of the entire patient group and the SSD group differed significantly before and after treatment (P=0.01, P=0.04, respectively), and no significant changes were observed in the other indicators.

Bilateral blood flow assessment and the HR

Bilateral flow was defined as the total flow on the surgical and nonsurgical sides. The bilateral flow and HR did not significantly differ among the groups.

All the quantitative results before and after treatment are presented in Tables 2,3.

Discussion

In this study, we applied 4D flow MRI to evaluate the blood flow properties in the TSSJ in patients with unilateral PT due to SSWAs, and clarified the qualitative and quantitative changes before and after surgery. The qualitative analysis revealed vortices inside the TSSJ and SSD, and a jet flow in the patients with the upstream TSS, as well as a high-speed blood flow in all the patients. After surgery, the vortices were eliminated or slowed, but the jet flow was unaffected. The quantitative analysis examined the high-speed blood flow in these patients, and revealed that this blood flow state did not change significantly after surgery. These findings suggest that: (I) high-speed blood flow is an important and common feature of SSWAs and is not significantly affected by surgery, but may be a potential risk factor for PT recurrence; (II) it is important to reconstruct a solid bony wall for the sigmoid sinus with multilayer and multimaterial structures; and (III) vortices are possibly a result rather than the cause of diverticulum formation.

In this study, most of the quantitative indices did not differ in the patients before and after surgery. However, the velocities at the upstream TSSJ, such as the V_max and V_avg, were obviously greater in the patients than the healthy subjects who had been subjected to the same MRI protocol in previous studies (15-17), confirming the importance of the high-speed blood flow in SSWA patients. In addition, cerebral blood flow affects intracranial pressure. In this study, there were no significant differences in the ipsilateral, contralateral, or bilateral (total cerebral) Flow before and after treatment, which did not cause changes in intracranial pressure, thus confirming the safety of the surgery.

According to the qualitative analysis, the streamlines showed vortices in most TSSJs and in all patients with SSDs, and the vortices disappeared after the extravascular operation was performed to eliminate the SSD and repair the sigmoid sinus wall. These results suggest that these vortices are secondary to local morphological changes caused by the formation of the SSD and TSSJ, and that vortices at the TSSJ can be used as indicators when evaluating the efficacy of surgery. According to a previous study, vortices are not found in all patients with SSDs (15). Similarly, in this study, vortices were not found in all the TSSJs. This might be related to the local morphology and the size of the SSD and TSSJ. The blood flow is not affected until it increases to a certain level; in this study, most patients with SSDs had obvious vortices, and all the TSSJs with vortices on the surgical side were located on the dominant side of the venous return, which may be related to the enlarged shape of the TSSJ. The vortices were eliminated or slowed by surgical reconstruction; however, the upstream jet flow and downstream flow patterns were not altered. The upstream jet flow remained at the preoperative level because the TSS was not modified. These findings also showed the safety of this surgery, which did not affect the blood flow upstream or downstream of the TSSJ.

Additionally, our findings suggest that the efficacy of the surgery may be attributed to the severing of the blood flow noise transmission pathway following surgical reconstruction. However, the speed of the jet flow at the upstream stenosis near the surgical area remained high postoperatively. The literature (6,7) has shown that PT resolves, and bone wall remodeling occurs around the sigmoid sinus once stenosis is alleviated, highlighting the critical role of high-speed blood flow in the development of SSWAs at stenotic sites. Consequently, our findings suggest that persistent high-speed jet flow may continue to exert pressure on the sigmoid sinus bone wall, potentially leading to PT recurrence. These findings indicate a clinical need to reinforce the bone wall to prevent or delay the recurrence of PT, and also indirectly confirm the high recurrence rate of PT after surgical reconstruction as reported in previous studies (9,10).

Limitations

This study had several limitations. First, the hemodynamic parameters were incomplete. Because 4D flow MRI is not a specialized vessel wall imaging technique, the irregular edge of the venous sinus can lead to the imprecise delineation of vessel walls, making the data on wall pressure and wall shear stress unreliable; hence, these parameters were not used. Computational fluid dynamics (CFD) will be used for further evaluation in the future, as it can provide more comprehensive hemodynamic parameters. Second, the postoperative MRI follow-up time was not uniform among the patients, and there was no CT, which reflects diagnosis and treatment practices in clinical settings. In addition, we speculate that there is a risk of recurrence after surgery, but there is currently no practical basis for this risk. We intend to conduct follow-up CT scans to compare and evaluate the changes in the bone wall at the repair site before and after surgery. Third, this study was conducted at a single center. Different institutions use different methods for surgical reconstruction. Some simply repair the bone wall, while others further compress the venous sinus to narrow it. This center performs only simple repair. The differences in surgical procedures can affect the outcomes, and selection bias for single-center patients might also have affected the results.

Conclusions

4D flow MRI is an effective method for qualitatively and quantitatively studying the blood flow in the sigmoid sinus in patients with SSWAs. Two characteristic flow patterns were found in the SSWA patients; that is, the vortex flow (in the patients with SSDs and TSSJs), and the jet flow (in the patients with a TSS). Additionally, all the SSWA patients had a high-speed blood flow. Surgical reconstruction is a safe and effective surgical procedure, but it cannot change the high-speed blood flow state, which represents a significant potential risk for PT recurrence. Thus, the solid bone wall of the sigmoid sinus needs to be reconstructed with multilayer and multimaterial structures.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROCSS reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-426/rc

Funding: This work was supported by the National Natural Science Foundation of China (Nos. 82302333, 61931013, 82171886, and 62171297); the Natural Science Foundation of Beijing Municipality (No. 7222301); the Beijing Key Clinical Discipline Funding (No. 2021-135); Beijing Scholar 2015 (No. [2015] 160); Capital’s Funds for Health Improvement and Research (No. 2022-1-1111); and Beijing Friendship Hospital, Capital Medical University (No. YYZZ202244).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-426/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Institutional Ethics Board of the Beijing Friendship Hospital, Capital Medical University (No. 2020-P2-202-01), and the requirement of individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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