Flow patterns in the jugular veins of pulsatile tinnitus patients
Introduction
A variety of imaging modalities are available to evaluate abnormalities of the intracranial venous circulation including CT Angiography, MR Angiography, and catheter-based diagnostic cerebral angiography. These methods afford detailed images of the geometric morphology of veins that are frequently tortuous with highly varying caliber. However, these anatomic studies provide little insight into the flow patterns of blood within these veins. Understanding flow patterns in the cerebral veins could provide important information about the pathophysiology of many clinical conditions. This report focuses on the venous flow patterns in patients with pulsatile tinnitus (PT).
Tinnitus is the auditory perception of sound in the absence of an external source. It affects more than 50 million Americans, often severely (Krishnan et al., 2006). It is not uncommon for patients to suffer from insomnia, depression, or even suicidal ideations (Jacques et al., 2013, Pridmore et al., 2012). A small subset of tinnitus (5–10%), termed PT, is pulsatile and is often described as a “whooshing” sound (Harvey et al., 2014, Liyanage et al., 2006). PT is often related to abnormal flow in vascular structures near the cochlea (Krishnan et al., 2006, Madani and Connor, 2009). PT etiologies can be venous (40%), arterial (35%), or undetermined (25%) (Mattox and Hudgins, 2008).
While controversial, abnormal internal jugular vein (IJV) geometries, such as enlarged or high-riding jugular bulbs (HJB), have been suggested as a source of PT in a subset of patients. A cohort study (Sonmez et al., 2007) found that subset to be roughly 30% of PT patients, though we note their study did not correlate symptom laterality with the side of the venous abnormality. Case studies (Adler and Ropper, 1986, Buckwalter et al., 1983, Chandler, 1983) proposed that the blood flow through the anatomic aberration may contribute to PT. Patients reported changes in PT with changes in flow through the jugular vein; for example, decreased flow with ipsilateral neck compression led to decreased symptoms, while increased flow in high-flow states (e.g. exercise or pregnancy) have been linked to increased pulsatile tinnitus strength (Buckwalter et al., 1983).
Despite those observations, we emphasize that an association between PT and abnormal jugular bulbs is only tentative. Both Buckwalter et al. (1983) and Chandler (1983) promoted jugular vein ligation as a treatment for PT, which has since been determined ineffective (Jin and Wang, 2015). Additionally, the presence of a HJB alone is not itself predictive of PT; Marsot-Dupuch (2001) determined that only 4.5% of patients with an enlarged jugular bulb ever develop PT, while Park et al. (2015) found a 35% prevalence of HJB in patients with hearing loss. The ambiguity of the role of abnormal jugular vein geometries and flow rate in PT pathology suggests the link between flow, shape, and sound, if it exists, must be complex; simply observing the flow rate and bulb shape is not enough to identify the origin of venous PT.
This study was motivated by our preliminary observations of complex flow within the jugular vein (Acevedo-Bolton et al., 2015, Kefayati et al., 2016). Those studies reveal a pronounced vortex core surrounded by a peripheral circulating flow pattern. Similar geometries and flow patterns have been noted by others as a source of sound (Vonnegut, 1954). We believe more detailed and subcategorized analyses are needed to define the relationship between the structure of the cerebral venous system and the flow patterns, which in turn may help elucidate the source of PT.
Bony structures overlying the draining veins limit the use of Doppler Ultrasound, the conventional in vivo approach for measuring velocities. MR velocimetry overcomes this limitation through its ability to define the full velocity vector in three-dimensional space throughout the pulsatile cycle – a method referred to as 4D MR Velocimetry (4D-MRV) (Markl et al., 2012, Nayak et al., 2015). 4D-MRV has been explored in application to the cerebral venous sinuses for both in vivo and in vitro models (Acevedo-Bolton et al., 2015, Kefayati et al., 2016). However, 4D-MRV is restricted in both spatial and temporal resolution. Furthermore, in vivo measurement only evaluates the specific physiologic condition presented at time of examination, and cannot readily explore flow field variations in response to different physiological conditions, such as heart rate or exercise, that might alter total volume flow.
Compared to in vivo MRV, Computational Fluid Dynamics (CFD) provides higher spatial and temporal resolution, and parameters can be adjusted to explore physiologic limits. We therefore employed CFD to provide controlled simulations in the complex anatomic geometries of the transverse sinus (TS), sigmoid sinus (SS), and internal jugular vein (IJV). This work utilized subject-specific CFD based on lumenal geometries from contrast-enhanced MR Venography (MRV), and inlet flow waveforms from 2D through-plane MR velocimetry measured for each individual. As a starting point, we investigated the relationship between jugular geometry and flow by comparing the velocity fields in “elevated” jugular bulbs, which were prevalent in our symptomatic population, to those in “rounded” bulbs, which were prevalent in our asymptomatic subjects.
Section snippets
Subject recruitment
Subjects were recruited from the UCSF Pulsatile Tinnitus Clinic and provided informed consent for participation in accordance with the procedures approved by our Institutional Review Board. Subjects with unrelated pathology known to cause PT were excluded from analysis (Table 1).
Image acquisition
Imaging was performed on a 3T Siemens Skyra (Siemens Medical Systems, Erlangen, Germany) and consisted of a high-resolution MR venogram to define the venous lumenal geometry, and MR flow studies to define the inlet flow
Results
16 individuals were recruited: 12 subjects who reported symptoms of PT and 4 controls (for summary, see Table 1). Of the symptomatic subjects, two were excluded due to underlying pathology known to cause PT (namely fistulas and SS diverticulum). One PT patient reported congenital unilateral deafness, and was excluded from further analysis due to inability to reliably lateralize the symptomatic side. Of the remaining nine PT patients, six were classified as having "neither" geometry, three had
Image-based velocity field evaluation
This study expands on findings from an in vivo imaging study of the velocity field patterns in the jugular veins of patients with PT (Acevedo-Bolton et al., 2015), but the current work includes a greater number of patients and utilizes CFD. Similar to the work of Acevedo-Bolton and colleagues, we also found the velocity field in subjects with elevated jugular bulbs to be extremely complex with pronounced vortical components. We demonstrate differences in the vortical component of flow between
Conclusions
Our study identifies a strong correlation between anatomic morphology of the jugular bulb and resulting flow patterns. Elevated jugular bulbs present with a pronounced vortex. A possible connection between conditions that promote the type of vortical flow and the generation of sound is postulated, but a definitive causal mechanism remains to be established.
Conflict of interest
There are no conflicts of interest to declare.
Acknowledgments
Financial support for this project was provided by Department of Radiology and Biomedical Imaging, UCSF. Grant support was provided by NIH, HL114118 (DS) and NS059944 (DS).
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