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. 2021 Dec 6;28(6):687–694. doi: 10.1177/15910199211062025

Study on the correlation between hemodynamic status of the transverse sinus-sigmoid sinus and the clinical efficacy of sigmoid sinus wall reconstruction

Zhenfeng Li 1, Long Jin 1,✉
PMCID: PMC9706262  PMID: 34866445

Abstract

Background and Purpose

For patients with pulsatile tinnitus who have both transverse sinus stenosis and sigmoid sinus wall anomalies, sigmoid sinus wall reconstruction surgery is the first-choice treatment when the trans-stenotic pressure gradient less than 10 mmHg. However, not all patients are cured by surgery. We hypothesized the abnormal hemodynamics caused by transverse sinus stenosis is associated with the clinical efficacy of surgery.

Methods

Eight pulsatile tinnitus patients treated with surgery were retrospectively reviewed (4 rehabilitated, 4 nonrehabilitated). All patients had radiologically diagnosed transverse sinus stenosis and sigmoid sinus wall anomalies. A numerical simulation of the hemodynamics of the transverse sinus-sigmoid sinus was performed using computational fluid dynamics technology. Changes in the blood flow patterns before and after surgery were observed. The blood flow velocity at the stenosis, vorticity of blood flow in the sigmoid sinus and wall pressure distribution in the sigmoid sinus wall anomalies area were compared.

Results

The blood flow velocity in the stenosis (preoperative P = 0.04, postoperative P = 0.004) and vorticity in the sigmoid sinus (preoperative P = 0.02, postoperative P = 0.007) pre- and post-surgery were significantly higher in the non-rehabilitation group than in the rehabilitation group. No significant difference was found in the wall pressure distribution in the sigmoid sinus wall anomalies area (preoperative P = 0.12, postoperative P = 0.24).

Conclusions

There is a clear correlation between the abnormal hemodynamic status caused by transverse sinus stenosis and the clinical efficacy of surgery. The blood flow velocity at the stenosis and vorticity of blood flow in the sigmoid sinus are factors influencing the clinical efficacy of surgery.

Keywords: Pulsatile tinnitus, computational fluid dynamics, transverse sinus stenosis, sigmoid sinus wall reconstruction, hemodynamic

Introduction

Pulsatile tinnitus (PT) is a form of objective tinnitus that is synchronized with the individual's heartbeat1–3 and accounts for 4%–10% of all cases of tinnitus.4,5 Persistent PT often affects patients’ mental health and can even lead to suicide. 6 Transverse sinus stenosis (TSS)7–9 and sigmoid sinus wall anomalies (SSWA)1,2,10–12 are the most common causes of venous PT; because the two often coexist, it is difficult to determine the role of the two possible causes of PT in individual PT patients, which presents many difficulties in the formulation of clinical treatment plans.2,9,13 It is also know that treating TSS with venous sinus stenting is extremely effective at treating PT with or without SSWA.14–16 However, owing to the rich collateral circulation leads to blood flow redistribution,17,18 not all radiologically TSS is pathologic and need to be treated.8,19 Trans-stenotic pressure gradient (TSG) of 10 mmHg traditionally used as indication of pathological TSS and patient selection criteria of for venous sinus stenting in PT patients.9,18,20 At present, for PT patients whose TSG is less than 10 mmHg, sigmoid sinus wall reconstruction (SSWR) is the first-choice treatment10,21,22 without the treatment of TSS. However, a study showed that only 75% (91/121) of patients experienced the disappear of PT after the SSWA was eliminated, 23 which suggests that TSS and the abnormal hemodynamic status of the transverse sinus-sigmoid sinus may be important factors affecting the clinical efficacy of SSWR. Previous study7,9 found that for patients with both TSS and SSWA, simply eliminating TSS by endovascular stenting can make the tinnitus symptoms disappear and even prompt the self-repair of the sigmoid sinus wall dehiscence (SSWD).

To further clarify the correlation between the hemodynamic status in the transverse sinus-sigmoid sinus and the clinical efficacy of SSWR for the treatment of PT, eight PT patients treated with SSWR (4 rehabilitated and 4 non-rehabilitated) were retrospectively reviewed. All patients had radiologically diagnosed TSS and SSWA; other causes of PT were excluded. Based on computational fluid dynamics (CFD) numerical simulation technology, using the patients’ real transverse sinus-sigmoid sinus anatomical structures and blood flow velocity data, the patient-specific transverse sinus-sigmoid sinus hemodynamic model was constructed, and the numerical simulation of the hemodynamics in the transverse sinus-sigmoid sinus was carried out. Changes in blood flow patterns in the transverse sinus-sigmoid sinus before and after SSWR were observed. The blood flow velocity (BFV) in the stenosis, vorticity of blood flow in the sigmoid sinus and wall pressure distribution on the SSWA area were compared between the two groups.

Materials and methods

Patient information

From January 2017 to December 2019, eight PT patients treated with SSWR were retrospectively reviewed. According to subjective reports of relief of PT symptoms at least 6 months after surgery, we divided the patients into a postoperative rehabilitation group (patients whose PT disappeared) and a postoperative non-rehabilitation group (patients whose PT recurred or did not change). The criteria for inclusion were as follows: 1) Tinnitus was synchronized to the patient's heartbeat, and its loudness could be reduced by pressing the internal jugular vein. Preoperative CTA/CTV and brain DSA confirmed the existence of SSWA (SSWD and/or sigmoid sinus diverticulum(SSD)) and TSS; 2) before the operation, the pressure gradient across the TSS was less than 10 mmHg, and the TSS was not previously treated; 3) no idiopathic intracranial hypertension, i.e., not fulfilling the modified Dandy criteria of ICP >25 cm H2O; 4) external and middle ear issues were excluded based on otoscopy and audiometric evaluation; and 5) two seasoned radiologists who were blinded to the prognosis compared the preoperative and postoperative CTA/V images and confirmed that the SSWA was completely eliminated.

3D geometry vascular model construction

Based on the 8 patients’ preoperative and postoperative CTA images (using a 256-slice spiral CT scanner (Philips), 512 × 512 pixels with 0.625 mm pixel size), we used MIMICS software (Version 17.0; Materialise, Belgium) to reconstruct 16 patient-specific 3D vascular models (Figure 1). The outlet and inlet of the model were located at the end of the intracranial segment of the internal jugular vein and the distal 1/3 of the TS, respectively. The SSWA was the extra region of the transverse sinus-sigmoid sinus junction from along the usual arc of the transverse sinus to the part of the arc that usually occurs below the sigmoid sinus. 10 We excluded all branches of the sinus system.

Figure 1.

Figure 1.

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Patient-specific 3D vascular models. (A) Position of inlet, outlet, TSS and SSWA. (B) 3D vascular models of rehabilitation group. (C) 3D vascular models of non-rehabilitation group.

Meshing

ANSYS 2020 R2 (ANSYS, Inc., Cecil Township, Pennsylvania, USA) was used for the meshing of the vascular models. We used the deviation of the BFV in the stenosis and vorticity in the sigmoid sinus as the criterion for the grid-independence test and found that using 0.3 million tetrahedral elements was sufficient for this experiment.

Computational models and simulations

ANSYS/CFX (2020 R2, ANSYS, Inc., USA) software was used for the CFD simulations. We used the Navier-Stokes formula as the governing equation for the calculations. Blood was presumed to be a Newtonian fluid that is incompressible and has a density of 1050 kg/m3 and a viscosity of 0.0035 Pa/s. The venous wall was presumed to be rigid and to have a nonslip boundary state. The steady flow state was set at the inlet, and the pressure state (0 pa) was set at the outlet. To obtain patient-specific blood flow data and improve the reliability of the study, inlet flow velocity was acquired from phase contrast MRA, in accordance with Amans’ work. 24 To obtain the BFV in the TSS, we cut a cross-section along the vertical diameter of the TSS (Figure 1) and extracted the velocity of the streamline through the plane.

Statistical analysis

Statistical analyses were conducted using GraphPad Prism 8.0 (GraphPad Software Corp, USA). The statistical significance of differences between the two subject groups was determined using Student's t test, and the Mann-Whitney U test was used when the data did not follow a normal distribution. P values less than 0.05 were considered significant.

Results

Eight female patients (4 in each group) were included in this study. There was no significant difference in age, BMI, duration, pressure gradient, inlet area, outlet area or model volume between the two groups (Tables 1 and 2). Table 3 describes the meaning of each hemodynamic parameter.

Table 1.

Case information.

Cases Age (years) Sex Duration (years) BMI (kg/m2) Slide Diagnosis TSG (mmHg) Change of PT
1 27 Female 6 22.51 Left SSD and SSWD 2.00 Disappearance
2 45 Female 6 27.14 Right SSD and SSWD 1.33 Disappearance
3 53 Female 3 27.06 Right SSWD 4.10 Disappearance
4 30 Female 5 19.83 Right SSWD 7.03 Disappearance
5 54 Female 2 26.39 Right SSD and SSWD 5.01 Recurrence
6 30 Female 2 23.24 Left SSD and SSWD 3.03 Recurrence
7 36 Female 7 21.56 Left SSWD 7.03 No change
8 59 Female 7 28.23 Right SSWD 5.03 No change
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PT = Pulsatile tinnitus, SSD = Sigmoid sinus diverticulum.

SSWD = Sigmoid sinus wall dehiscence, TSG = Trans-stenotic pressure gradient.

Table 2.

3D Vascular model and hemodynamic characteristics.

Rehabilitation group Non-rehabilitation group p value
Preoperative inlet area (mm2) 37.78 ± 7.61 44.67 ± 8.77 0.280
Postoperative inlet area (mm2) 39.19 ± 7.75 44.19 ± 9.45 0.440
Preoperative outlet area (mm2) 75.15 ± 29.74 71.74 ± 25.31 >0.990
Postoperative outlet area (mm2) 74.52 ± 27.90 57.36 ± 17.69 0.340
Preoperative model volume (mm3) 5267 ± 1513 4931 ± 716 0.700
Postoperative model volume (mm3) 5366 ± 1497 4582 ± 1003 0.420
Preoperative BFV in the inlet (cm/s) 22.84 ± 1.88 24.93 ± 1.86 0.170
Postoperative BFV in the inlet (cm/s) 22.50 ± 3.10 24.70 ± 2.31 0.290
Preoperative BFV in the TSS (cm/s) 92.45 ± 15.40 176.8 ± 64.61 0.040
Postoperative BFV in the TSS (cm/s) 84.97 ± 19.09 156.9 ± 25.27 0.004
Preoperative vorticity in SS (s−1) 34.72 ± 10.63 92.53 ± 30.77 0.020
Postoperative vorticity in SS (s−1) 32.25 ± 11.96 101.6 ± 29.81 0.007
Preoperative wall pressure in SSWA (Pa) 262.9 ± 147.0 534.1 ± 266.0 0.120
Postoperative wall pressure in SSWA (Pa) 246.7 ± 163.6 394.7 ± 161.0 0.240
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BFV = Blood flow velocity, SSWA = Sigmoid sinus wall anomalies.

TSS = Transverse sinus stenosis, SS = Sigmoid sinus.

Table 3.

Meaning of hemodynamic parameters.

Hemodynamic parameter Meaning
Blood flow velocity Blood flow velocity refers to the distance that a particle in the blood moves in the blood vessel per unit time. It is the most basic blood flow index, closely related to many indexes.
Blood flow patterns The blood flow patterns mainly include laminar flow and turbulent flow. Turbulent flow is the main source of blood flow murmurs, manifested as the flow direction of each particle in the blood stream is inconsistent, resulting in a vortex.
Turbulent Flow The formation of turbulence is related to the Reynold's number (Re), Re = ρvd/μ (where ρ and μ are blood flow density and viscosity coefficient, respectively, and v and d represent blood flow velocity and blood vessel diameter respectively), Re increases, The blood flow is prone to turbulence. The blood flow density and viscosity coefficient in an individual are usually unchanged, so Re is directly proportional to the blood flow velocity and the inner diameter of the blood vessel.
Vorticity Vorticity is one of the most important physical quantities describing turbulent motion. Turbulent flow usually uses vorticity to measure its strength and direction.
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Table 2 summarizes the pre- and postoperative hemodynamic characteristics. The BFV in the TSS was increased dramatically in all patients. The BFV in the TSS before and after the operation in the non-rehabilitation group was significantly higher than that in the rehabilitation group (Figure 2). Moreover, high-speed blood flow occurred in the same direction as the overall SSD growth. The SSD disappeared post-surgery, but the high-velocity blood flow caused by the TSS still impacted the anterolateral wall of the sigmoid sinus (Figure 3). Compared with the upstream area of the TSS, the velocity streamlines showed increased twisting and curling downstream of the TSS and an evident turbulent flow, which appeared as disorderly distributed streamlines and discontinuous velocity vectors in the SSD and the corresponding medial area of the SSWA (Figures 2 and 3). The vorticity of blood flow in the sigmoid sinus pre- and post-surgery was significantly higher in the non-rehabilitation group than in the rehabilitation group (Figure 4). The SSD disappeared post-surgery, but the turbulent flow in the corresponding medial area of the SSWA remained. In terms of wall pressure, no significant difference in wall pressure at the areas of the SSWA, wall pressure changes before and after surgery was found between the two groups (Figure 5).

Figure 2.

Figure 2.

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Velocity streamlines. (A)Velocity streamlines of rehabilitation group. (B) Velocity streamlines of non-rehabilitation group.

Figure 3.

Figure 3.

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Velocity vector map of the sigmoid sinus. (A) Velocity vector map of the sigmoid sinus of rehabilitation group (Case 1 and Case2). (B) Velocity vector map of the sigmoid sinus of non-rehabilitation group (Case 5 and Case 6).

Figure 4.

Figure 4.

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Preoperative vorticity cloud map of the sigmoid sinus (A) Preoperative vorticity cloud map of the sigmoid sinus of rehabilitation group. (B) Preoperative vorticity cloud map of the sigmoid sinus of non-rehabilitation group.

Figure 5.

Figure 5.

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Wall pressure distribution in the transverse sinus-sigmoid sinus. (A) Wall pressure distribution in the transverse sinus-sigmoid sinus of rehabilitation group. (B) Wall pressure distribution in the transverse sinus-sigmoid sinus of non-rehabilitation group.

Discussion

Although several researches speculated that abnormal hemodynamics caused by TSS may affect surgical effect in some patients who have undergone SSWR surgery alone.2,9,13 However, there is no hemodynamic study on this topic. In the current study, we found BFV in the TSS and vorticity of blood flow in the sigmoid sinus pre- and post-surgery in the non-rehabilitation group was significantly higher than that in the rehabilitation group.

TSS and SSWA frequently co-occur in patients with PT.2,13 TSS-related PT is usually treated by stent implantation,2,8,12,15,20 and SSWA are usually treated with SSWR.2,23 Although SSWR has achieved good results in the treatment of PT, not all PT patients with SSWA can be cured by surgery, even if the SSWA have been completely eliminated.2,25 The reasons for difference in surgical efficacy are unclear. Given that SSWA are usually accompanied by TSS, a previous study speculated that both TSS and SSWA play a role in the development of PT, which would explain the unrelieved tinnitus in some patients who have undergone SSWR surgery alone.2,8,9,13 However, it remains unclear whether and how TSS is related to surgical efficacy due to a lack of relevant hemodynamic evidence. Therefore, it is of great significance to clarify the relationship between abnormal hemodynamics caused by TSS and surgical efficacy, so as to formulate personalized treatment strategies for the next treatment of patients with poor prognosis. Our results suggested BFV in the TSS and vorticity of blood flow in the sigmoid sinus pre- and post-surgery were strongly related to the surgical effect. Compared with preoperative observations, the SSD disappeared post-surgery, but the turbulent flow in the corresponding medial area of the SSWA and the high-speed blood flow in the TSS remained (Figure 2). Therefore, treating SSWA alone cannot completely eliminate abnormal hemodynamic status, which resulting in poor surgical efficacy. By comparing the blood flow pattern in the transverse sinus-sigmoid sinus before and after surgery, we found that the velocity streamlines of the rehabilitation group became smoother and more regular (cases 2 and 4) or showed no change (cases 1 and 3) after surgery, while those of the non-rehabilitation group showed increased twisting and curling. This finding is consistent with a previous study9,10 and indicates that the treatment of venous PT should focus on eliminating blood flow disorders. In summary, for the non-rehabilitated patients, it is necessary to further perform venous sinus stent implantation to eliminate TSS and high-speed blood flow and turbulence at the stenosis, so as to eliminate tinnitus.

Previous hemodynamic studies aimed to explore the pathophysiological mechanism of PT. To our knowledge, there is only one hemodynamic study to explore the influencing factors of surgical efficacy. The present study is the first to investigate the relationship between hemodynamic abnormalities caused by TSS and surgical efficacy. Moreover, previous hemodynamic studies used the transverse sinus inlet BFV of healthy people as the model inlet BFV, while the transverse sinus BFV of PT patients was higher than that of healthy people. Therefore, the hemodynamic data obtained in previous studies were inevitably different from the actual situation. Different from previous hemodynamic studies, our CFD simulations were performed using patient-specific inlet velocity data acquired from phase contrast MRA, and using these data could produce more realistic simulations and improve the reliability of the results.

Although the pathogenesis of venous PT is not yet fully understood, it is generally believed that venous PT is caused by abnormal anatomical structures of the venous sinuses and the hemodynamic status of the transverse sinus-sigmoid sinus.1,10–12,24 Amans’ group previously identified turbulent flow patterns in patients with venous PT that was absent in control groups. 24 Li et al. 12 used 4D flow MRI technology to study the hemodynamics of the transverse sinus-sigmoid sinus in 21 patients with venous PT and 11 healthy controls. They found the BFV in the patients with PT was significantly higher than that in the healthy control group. There was an obvious turbulent flow in the patients with PT, but there was no disordered blood flow pattern in the healthy control group. In our study, increased BFV in TSS was observed in all patients, and an evident turbulent flow occurred in the SSD and the corresponding medial area of the SSWA before and after the operation (Figure 2), which is consistent with previous studies1,9,12,14,18 and suggests that the high-velocity blood flow in the TSS and the turbulent flow in the sigmoid sinus are important hemodynamic mechanisms of venous PT. A recent CFD study proposed that changes in wall pressure in SSWA pre- and post-operation are the cause of differences in surgical effects. 10 However, no significant difference was found in pre- and postoperative wall pressure changes between the two groups in our study. Previous research found that the increase in BFV due to TSS significantly increased the mean wall pressure of SSWA.7,9 Therefore, wall pressure is affected by both TSS and SSWA in our study, whereas previous studies did not show TSS interference, so the conclusion is not contradictory.

There are some limitations of this study. First, although the application of patient-specific models and real inlet velocity data means that the CFD numerical simulation results obtained in this study are more similar than previous hemodynamic studies to the real hemodynamics of the human body, the accuracy of the simulation results still needs to be verified by in vitro particle image velocimetry (PIV) and other experiments. Second, although our study is based on the theory that PT is caused by turbulence in the sigmoid sinus, we did not directly prove the hypothesis that turbulence is the source of the sound. In the future, it will be necessary to establish an animal model of PT and carry out relevant hemodynamic simulations to confirm this theory. Last, the assumption of steady state flow limits the ability to detect pressure fluctuations with the cardiac cycle that may be related to sound generation. 26

Conclusion

There is a clear correlation between the abnormal hemodynamic status caused by TSS and the clinical efficacy of surgery. The increased BFV in the TSS and higher vorticity of blood flow in the sigmoid sinus induced unrelieved PT in some patients who have undergone SSWR surgery alone. The present study provides a theoretical basis for further clinical treatment of patients with TSS and SSWA who have no remission of PT after SSWR: The key to eliminating PT is to eliminate TSS, thereby eliminating the abnormal blood flow state caused by TSS, and then eliminating tinnitus.

Footnotes

Authors’ contribution: All authors gave final approval of the published version and agreed to be 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. Zhenfeng Li, collected the data and performed CFD simulations. Long Jin helped to analyze the data. Zhenfeng Li and Long Jin wrote the manuscript.

Ethical approval statement: Ethical approval was obtained from the institution's review board of Beijing Friendship Hospital, Capital Medical University of China. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding: The author(s) received no financial support for the research, authorship and/or publication of this article.

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