Diagnostic ultrasound for rotational vertebral artery syndrome: indications, examination technique, diagnostic criteria, and algorithm (Russian expert consensus)

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INTRODUCTION

The relevance of diagnosing rotational vertebral artery (VA) compression is due to the demand among neurologists for ultrasound (US) examinations involving head rotation tests, as further patient management depends on their correct performance and the accurate interpretation of the results.

Rotational Vertebral Artery Compression Syndrome (RCS) is one of the causes of vertebrobasilar insufficiency (VBI) and is characterized by its transient, reversible, and dynamic mechanical compression (to the degree of hemodynamically significant stenosis or occlusion) by extravascular structures at the atlantoaxial or subaxial level during the neck and head rotation. In foreign sources, RCS is widely known as Bow Hunter's Syndrome (BHS) [1–3].

BHS is considered a rare pathology, usually diagnosed after clinical episodes of ischemia in the vertebrobasilar system (VBS) linked to head rotation or extension, or upon discovering vertebral artery (VA) dissection [4]. According to the data, the prevalence of BHS ranges from 5% to 17% among patients with VBI symptoms when changing head position and among clinically asymptomatic individuals [3, 5, 6].

In Russian clinical practice, we frequently encounter overdiagnosis of extravascular vertebral artery compression due to head and neck movements. This is due to the misinterpretation of patient complaints, the lack of a specific clinical presentation, no universal diagnostic criteria, and low awareness of alternative diagnoses. BHS is also called VA syndrome or vertebrogenic VA compression syndrome and is seen as a common cause of both acute and chronic vertebrobasilar insufficiency (VBI) [7]. VA syndrome is an umbrella term for a complex of cerebral, vascular, and vegetative syndromes caused by lumen narrowing, vessel wall deformation, and irritation of the VA autonomic plexus [8].

The risk of developing VBI symptoms in BHS increases if the dominant VA is compressed while the contralateral VA is narrowed (e.g., hypoplastic or stenosed) or occluded [1]. VA compression is often asymptomatic because the blood supply to the structures of the posterior cranial fossa is maintained by a system of collateral pathways, including:

• the contralateral VA;
• functionally patent posterior communicating arteries;
• P1 segments of the posterior cerebral arteries (from the bifurcation of the basilar artery to the posterior communicating artery).

These pathways can immediately compensate for a sudden stop in blood flow through one or both VAs [9].

Extravasal compression of the VA can occur at any level of the extracranial segment. According to published data, the most common anatomical site of rotational compression is the level of the second cervical (CII) vertebra and above [1, 3]. This is due to the leading role of the atlanto-occipital joint in enabling rotational movements of the head and neck, given the relative immobility of the VA in the area of its exit from the spinal canal at the CII level and entry into the atlanto-occipital membrane. Such anatomical features make the VA prone to stenosis, occlusion, or injury in this area. Compression of the VA occurs as a result of its excessive stretching and narrowing when turning the head to the contralateral side [10]. According to other authors, VA compression is more frequently found in the first two segments of the VA and is caused by an extravasal structure, typically in neurodegenerative spinal diseases [5, 11]. This type of VA compression is associated with turning the head to the ipsilateral side.

Causes of extravasal VA compression can be divided into four groups [1–3, 11]:

• congenital skeletal anomalies (e.g., bone spur, Kimmerle anomaly, anomalies of the odontoid process, hypertrophied or ossified atlanto-occipital membrane, dural fold in the foramen magnum, Klippel–Feil syndrome, anomalies of the transverse process, rotatory atlanto-axial subluxation, atlanto-axial instability);
• acquired skeletal deformities (e.g., osteophytes, spondylolisthesis, lateral disc herniations, exostosis, hypertrophy of the facet and uncovertebral joints, osteochondroma, etc.);
• cases of the neck muscles hypertrophy or spasm (anterior scalene muscle, longus colli muscle, inferior oblique muscle of the neck);
• compression by various space-occupying lesions (for example, tumor, trauma, thyroid cartilage, cervical sympathetic ganglia, etc.).

Currently, there are no universal guidelines for the BHS detection algorithm, so most authors use different criteria and methods for patient examination. Many authors consider dynamic cerebral angiography the "gold standard" for diagnosing compression, as it clearly shows a VA filling defect during head rotation [1–3, 7, 12]. Subsequent CT and/or MRI of the cervical spine with targeted slices at the compression level can help determine the pathogenesis of arterial compression [12]. However, at the diagnostic screening stage, ultrasound is the best method because of its informativeness, accessibility, non-invasiveness, and cost [1, 2, 7, 12].

ULTRASOUND WITH ROTATIONAL TESTS OF THE HEAD AND NECK

Ultrasound's uniqueness is in its ability for real-time dynamic monitoring of hemodynamic changes during rotation tests. The examination must be conducted as prescribed by a neurologist, alongside the study of the brachiocephalic arteries, with mandatory additional time allocated.

Arteries Examined

It is necessary to examine the VA, the basilar artery (BA), and the PCA. The level and degree of possible VA compression are determined by identifying direct and indirect Doppler signs at the level of the first, second, third, and fourth (V1–V4) segments. The regional significance of VA compression must be assessed based on changes in blood flow velocity parameters in the BA and PCA.

Type of Ultrasound Examination and Transducers

To evaluate the VA at the extracranial level (V1–V3 segments), a linear transducer for peripheral vessels (frequency 3–12 MHz) should be used. To evaluate the VA in the V3 segment and the proximal part of V1, micro-convex (frequency 3–8 MHz) and convex (frequency 2–5 MHz) transducers may be used if necessary.

To examine the VA in the V4 segment, the BA, and the PCA, a phased array sector transducer (frequency 2–5 MHz) should be used for transcranial duplex scanning, and a pulsed-wave (frequency 2 MHz) transducer for transcranial Doppler.

Patient and Physician Positioning

The examination of the VBS arteries can be performed in three patient positions:

• supine on the back (evaluation of the VA in the V1–V3 segments and the PCA);
• supine on the stomach (assessment of the VA in the V4 segment and the BA);
• sitting (assessment of the VA in the V4 segment and the BA).

According to literature data, when performing ultrasound with rotational tests, many researchers use the supine and sitting positions [13].

The supine position is convenient for both the physician and the patient. The prone position is convenient for the physician but has certain inconveniences for the patient, especially for elderly patients and individuals with increased body weight. During transcranial examination of the VA (V4 segment) and BA, for a more level horizontal head position on the couch and for patient comfort, the patient can be asked to place their hands (fists) under their forehead and a small pillow under their chest. The sitting position is convenient for the patient; however, it has certain inconveniences for the physician, as their arm is forced to remain tense and suspended. In some cases, it becomes almost fully extended, like when the patient sits back on a wide couch. Furthermore, the patient may involuntarily lean away due to the transducer's pressure, causing difficulties in consistently recording blood flow velocity from the examined vessels.

Types of Head and Neck Rotation

Ultrasound with head rotations is usually performed with the head turned to the sides and flexed and extended. L. Kimihira et al. [14] proposed using combined positions involving head rotations with simultaneous extension and flexion. There are 9 head positions in total: neutral, flexion, extension, right and left rotations, and combinations of side rotation with simultaneous extension or flexion (Fig. 1). It is also recommended to conduct the examination with the head in the position where VBI symptoms occur.

 

Fig. 1. Head positions during ultrasound investigation of the vertebral arteries with rotation tests: a, right rotation with extension; b, extension; c, left rotation with extension; d, right rotation; e, neutral position; f, left rotation; g, right rotation with flexion; h, flexion; i, left rotation with flexion; «+» — visualization is optimal; «+/−» — visualization is limited; «−» — visualization is impossible. V1 — first segment of the vertebral artery; V2 — second segment of the vertebral artery; V3 — third segment of the vertebral artery.

 

Topographic and Anatomical Limitations of Locating the Arteries of the Vertebrobasilar System During Head Rotation

Isolated rotation to the ipsilateral side of the examined VA significantly complicates the assessment of blood flow in the V2 segment (see Fig. 1, d) and makes it practically impossible during combined (see Fig. 1, g) or isolated forward head tilt (see Fig. 1, h), even if the transducer is placed on the side of the neck behind the sternocleidomastoid muscle.

Positions with maximum head tilt hinder visualization of the V4 segment of the VA and make clear visualization of the BA nearly impossible. This is due to the rigid and rather long tail part of the transducer, which, by resting against the patient's back, does not allow the ultrasound beam to be directed at the required angle into the region of the BA passage. Moreover, the challenges in obtaining a signal from these arteries are intensified by the absence of visualization of their walls in B-mode, requiring reliance solely on images in color or power Doppler mapping mode.

The main limitation for transcranial examination is the lack of adequate temporal ultrasound windows.

Ultrasound Criteria for Extravasal Compression of the Vertebral Artery

Formal analysis of published data revealed a lack of universal ultrasound criteria for diagnosing extravasal compression of the VA, impacting the detection frequency in various medical diagnostic centers both in Russia and internationally [7]. Published sources report the following considered indicators of hemodynamics:

• peak systolic velocity (PSV);
• end-diastolic velocity (EDV);
• mean velocity;
• peripheral resistance indices.

The following ultrasound Doppler criteria for extravasal compression of the VA during rotation tests are distinguished [3, 5, 6, 9, 15–19]:

• before the compression zone (pre-compression or pre-occlusive changes) — no changes or a decrease in PSV, a more pronounced decrease or absence of EDV, and an increase in peripheral resistance indices;
• in the compression zone (compression changes) — an increase in PSV ≥50% or absence of blood flow;
• after the compression zone (post-compression changes) in the V4 segment — a decrease in PSV ≥30% from baseline values, an increase in EDV, a decrease in peripheral resistance indices, blood flow turbulence (Fig. 2).

 

Fig. 2. Patterns of pre-stenotic (a), stenotic (b), post-stenotic (c) blood flow and pre-occlusive blood flow (d).

 

A decrease in blood flow with zero diastolic velocity during head rotation indicates occlusion (complete compression of the lumen) of the VA above the site of examination (see Fig. 2, d).

The regional significance of VA compression during head rotations is determined by decreased blood flow velocity in the BA and PCA. However, there is no published data on the threshold values for PSV reduction in the BA. In patients with rotational VBI, continuous transcranial Doppler monitoring shows a >50% decrease in mean blood flow velocity in the PCA during head turns. Returning to a neutral position results in a reactive hyperemic response with a >10% velocity increase [12, 20].

Blood flow monitoring in the BA during extravasal VA compression reveals the compensatory role of the second VA in VBS blood supply. Blood flow monitoring in the P1 segment of the PCA provides similar information and allows assessment of blood flow in the BA when adequate localization is impossible, such as during head rotations with maximum extension. Blood flow monitoring in the P2 segment of the PCA (from the origin of the posterior communicating artery around the midbrain) provides information about the blood supply to the VBS (occipital lobes and some other posterior regions of the brain), considering possible compensatory involvement of the carotid basin through the posterior communicating artery.

ALGORITHM FOR PERFORMING ROTATIONAL TESTS DURING ULTRASOUND EXAMINATION

Russian experts propose an algorithm for performing rotational tests during ultrasound to identify the level and significance of extravasal compression of the VA (Fig. 3).

 

Fig. 3. Diagram of the algorithm for ultrasound investigation with rotation tests.

 

Step 1 The patient is in the supine position, the head position is neutral. The blood flow in the V2 segment of the VA is assessed. It is necessary to select the artery section where blood flow is most accurately recorded in a neutral head position and during rotational tests.

Step 2 The patient is in the supine position. The blood flow in the V2 segment is assessed in each of the VAs during rotation of the head and neck:

• right turn + extension + flexion;
• left turn + extension + flexion.

In the absence of hemodynamic changes in the V2 segment, the study is completed. Negative test. No extravasal influence on the VA was identified.

Step 3 Several sequential actions must be performed depending on the identified blood flow changes.

• If pre-compression blood flow changes are identified in the V2 segment during head rotation to the side opposite the VA being examined, with or without simultaneous head extension, blood flow in the V3 segment of the VA is assessed in the neutral head position and during the movement causing these changes.
• If pre-compression blood flow changes are detected during head rotation to the ipsilateral side, with or without head flexion, blood flow is assessed in the V2 segment above the examination level in the same position. During ipsilateral head rotation, since visualization of the entire V2 segment is limited, blood flow is assessed in the V4 segment with the patient prone or sitting with their back to the physician.
• If post-compression blood flow changes are identified during head rotation to the ipsilateral side, with or without head flexion, blood flow is assessed in the V1 and V2 segments of the VA below the examination level to the origin from the subclavian artery in the same position.

Step 4 When identifying signs of extravasal impact on the VA at any level, we assess the regional significance of the changes in blood flow. No significant post-stenotic changes in hemodynamic parameters in the BA and PCA (a PSV decrease of less than 50% from neutral head position values) indicates no regional significance of rotational VA compression.

Blood flow is assessed in the P1 and P2 segments of the ipsilateral PCA with the patient being in the supine position and the head in a neutral position.

Blood flow is assessed in the P1 and P2 segments of the ipsilateral PCA in the head position causing maximum VA compression. In the case of complete or incomplete ipsilateral posterior trifurcation, blood flow is assessed in the contralateral PCA.

If it is impossible to obtain a signal from the PCA, the regional significance of VA compression is assessed by changes in blood flow in the BA with the patient in the prone or sitting position.

Key Points of the Ultrasound Examination Protocol and Conclusion When Performing Rotational Tests of the Head and Neck

Examination protocol. Description of the vertebral artery in the neutral head position, indicating the diameter, structural changes, level of entry into the bone canal, artery course, PSV, and resistance index (RI).

Description of the changes in PSV and RI in the V2 segment during head rotation to the right and left, as well as during head rotation in these directions combined with extension and flexion.

In case of detecting pre-compression changes of the VA in the V2 segment (see above), changes in PSV and RI in the V3 segment or the distal part of V2 must be described.

Upon detection of post-compression changes in the V2 segment (see above), changes in PSV and RI in the V1 segment or the proximal part of V2 must be described.

If signs of VA compression at the extracranial level are detected, changes in PSV and RI in the BA and/or PCA must be described.

Conclusion: Hemodynamic signs of VA compression stenosis or occlusion, indicating head position in which they occured, compression level, and regional significance.

Additional Information: It should be denoted whether the patient had complaints during the rotation tests.

The protocol form can be determined in each medical institution, considering the recommendations on methodology and data interpretation outlined in this article.

Example of Writing an Ultrasound Examination Protocol

For better understanding of the features of diagnosing vascular disorders, below there is an example of ultrasound image descriptions (Fig. 4) and a conclusion for a patient with extravasal rotational compression of the left VA at the V3 segment level.

 

Fig. 4. Blood flow recording in the arteries of the vertebrobasilar system in a patient with functional compression of the left vertebral artery in the V3 segment. Blood flow recording in the left vertebral artery: a, in the V2 segment in the neutral head position; b, in the V2 segment during right head rotation; c, in the V2 segment during right head rotation with extension; d, in the V3 segment in the neutral head position; e, in the V3 segment during right head rotation; f, in the V3 segment during right head rotation with extension. Blood flow recording in the right vertebral artery: g, in the V1 segment in the neutral head position; h, in the V1 segment during right head rotation with extension. Blood flow recording in the left posterior cerebral artery: i, in the P1 segment in the neutral head position; j, in the P1 segment during right head rotation with extension; k, in the P2 segment in the neutral head position; l, in the P2 segment during right head rotation with extension; m, a twofold increase in blood flow velocity in the P1 segment during compression of the ipsilateral common carotid artery (the yellow arrow indicates the moment of compression). PSV — peak systolic velocity; RI — resistance index; lPCA — left posterior cerebral artery.

 

Examination protocol. Left VA with a diameter of 3.6 mm. No structural changes detected. Enters the bony canal of the cervical vertebrae at the CVI level. It runs straight until entering the bony canal and between the transverse processes of the cervical vertebrae. Blood flow velocity (PSV in the V2 segment — 33 cm/s) and peripheral resistance (RI = 0.63) are normal (see Fig. 4, a).

When the head is turned to the right, PSV decreases to 27 cm/s with increased peripheral resistance (RI = 0.72) in the V2 segment (see Fig. 4, b). Meanwhile, in the V3 segment (above the CII vertebra), vessel lumen narrowing is seen in color Doppler mapping with an aliasing effect and a local PSV increase to 119 cm/s (see Fig. 4, e) [46 cm/s in the neutral position (see Fig. 4, d)]. Turning the head right with extension shows a significant decrease in PSV (to 8 cm/s), EDV to 0 cm/s, and RI = 1.0 in the V2 segment (see Fig. 4, c). In the same head position, blood flow is absent in the proximal V3 segment (see Fig. 4, f), whereas the PSV in the contralateral right VA in the V1 segment increases compensatorily compared to the neutral head position — from 41 cm/s (see Fig. 4, g) to 61 cm/s (see Fig. 4, h).

Technical difficulties prevented the assessment of blood flow patterns in the BA. The regional significance of rotational compression of the left VA was evaluated by the blood flow test in the left PCA. When the head is rotated to the right with simultaneous extension, PSV in the P1 segment of the PCA decreased from 51 cm/s in the neutral position (see Fig. 4, i) to 37 cm/s (see Fig. 4, j), a 27% reduction with a threshold value of >50%, and RI from 0.49 to 0.41. No decrease in PSV and RI was observed in the P2 segment of the PCA (see Fig. 4, l) compared to the values in the neutral head position (PSV — 58 and 60 cm/s; RI — 0.48 and 0.47, respectively) (see Fig. 4, k). The preservation of hemodynamic parameters in the P2 segment of the PCA is due to compensatory blood flow from the ipsilateral internal carotid artery via the left posterior communicating artery. This functioning was identified during compression of the ipsilateral common carotid artery, showing a 2-fold increase in PSV in the P1 segment of the PCA compared to the baseline (see Fig. 4, m).

Conclusion: Hemodynamic signs of compressional stenosis of the left vertebral artery in the V3 segment during rightward head rotation. Hemodynamic signs of compression occlusion of the left vertebral artery in the V3 segment during rightward rotation with head extension. Compensatory increase in blood flow velocity in the right vertebral artery. No regional significance of rotational compression of the left vertebral artery.

Additional Information: The patient had no complaints during rotation tests with the head.

Additional Methods of Investigation and Possible Causes of Vertebral Artery Compression

Compression of the left VA during head rotation was confirmed using CT angiography (Fig. 5, a). During this investigation, the patient's head rotation causing VA compression was established under ultrasound guidance. The cause of VA compression in the V3 segment was a rotational subluxation of the C2 vertebra (see Fig. 5, b).

 

Fig. 5. Results of functional angiography of the: a, left vertebral artery with a subtotal stenosis of the vertebral artery lumen above the second cervical vertebra (the site of compression is indicated by an arrow) during left head rotation with simultaneous extension; b, computed tomography of the cervical spine, rotational subluxation of the second cervical vertebra (indicated by a dashed square).

 

Thus, functional extravasal compression of the left vertebral artery was identified in a patient with periodic headaches and dizziness, causing stenosis in the V3 segment during right head rotation and occlusion during right head rotation with extension, confirmed by computed tomography angiography. The lack of patient complaints during rotation tests and the regional significance of left VA compression for the VBB is due to increased blood flow velocity in the right VA and the involvement of the ipsilateral internal carotid artery in supplying the left PCA via the posterior communicating artery. The cause of left VA compression in the V3 segment is a rotational subluxation of the C2 vertebra. A following consultation with a neurologist is recommended to determine further treatment.

CONCLUSION

Clinical manifestations of rotational compression are nonspecific but must be linked to head position changes and regress quickly after returning to a neutral position. Ultrasound of the VA with rotational tests should be performed as prescribed by a neurologist, with additional time allocated for the tests. The VA can experience compression (from stenosis to occlusion) at any point along the V1–V3 segments. The most common compression site is the CI–CII vertebrae for young and middle-aged patients, and CII–CVII for the elderly.

Relative to the direction of head rotation, the compressed VA is more often contralateral in cases of compression at the atlantoaxial level (V3 segment) and ipsilateral at the subaxial level (V1–V2 segments).

The main hemodynamic indicators of significant VA compression during rotational tests are: proximal to the compression site — decreased blood flow velocity (mainly end-diastolic velocity) and increased peripheral resistance; at the compression site — local increase in blood flow velocity; distal to the compression site — decreased blood flow velocity and peripheral resistance indices.

During rotation tests, evaluate the regional significance of VA compression by assessing blood flow in the BA or PCA. In turn, the ultrasound protocol must record information about the onset and patient complaints dynamics, as well as clinical manifestations during rotation tests.

ADDITIONAL INFORMATION

Author contributions: A.O. Chechetkin: data curation, writing — original draft, visualization, methodology; T.V. Balakhonova, L.E. Shulgina: data curation, writing — original draft, writing — review & editing, methodology; T.N. Enkina, V.P. Kulikov, I.E. Timina, M.V. Shumilina: writing — review & editing. All the authors approved the version of the manuscript to be published and agreed to be accountable for all aspects of the work, ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Ethics approval: Not applicable.

Consent for publication: No informed consent for publication of the patient's medical data was obtained, as contact with the patient could not be established (the used material was archival). All data presented are anonymized, and no photographs are published.

Funding sources: No funding.

Disclosure of interests: The authors have no relationships, activities, or interests for the last three years related to for-profit or not-for-profit third parties whose interests may be affected by the content of the article.

Statement of originality: No previously published material (text, images, or data) was used in this study or article.

Data availability statement: The editorial policy regarding data sharing does not apply to this work.

Generative AI: No generative artificial intelligence technologies were used to prepare this article.

Provenance and peer-review: This article was submitted unsolicited and reviewed following the standard procedure. The peer-review process involved two external reviewers and member of the Editorial Board.

About the authors

Andrey O. Chechetkin

Russian Сenter of Neurology and Neurosciences

Author for correspondence.
Email: andreychechetkin@gmail.com
ORCID iD: 0000-0002-8726-8928
SPIN-code: 9394-6995

MD, Dr. Sci. (Medicine)

Russian Federation, Moscow

Tatyana V. Balakhonova

National Medical Research Centre of Cardiology named after Academician E.I. Chazov

Email: tvbdoc@gmail.com
ORCID iD: 0000-0002-7273-6979
SPIN-code: 3738-3289

MD, Dr. Sci. (Medicine), Professor

Russian Federation, Moscow

Tatiana N. Enkina

North-Western District and Scientific Clinical Center named after L.G. Sokolov

Email: tatiana.enkina@yandex.ru
ORCID iD: 0009-0004-7739-1684
SPIN-code: 7594-1380

MD, Cand. Sci. (Medicine)

Russian Federation, Saint Petersburg

Vladimir P. Kulikov

Altai State Medical University

Email: kulikov57@mail.ru
ORCID iD: 0000-0003-4869-5465
SPIN-code: 9224-1959

MD, Dr. Sci. (Medicine), Professor

Russian Federation, Barnaul

Irina E. Timina

A.V. Vishnevsky National Medical Research Center of Surgery

Email: timina68@mail.ru
ORCID iD: 0000-0001-7026-9417
SPIN-code: 1100-8854

MD, Dr. Sci. (Medicine)

Russian Federation, Moscow

Ludmila E. Shulgina

Polyclinic No. 1 of the Presidential Administration of the Russian Federation

Email: ofd-shulgina@yandex.ru
ORCID iD: 0009-0009-6325-8766
SPIN-code: 7757-2071

MD, Dr. Sci. (Medicine)

Russian Federation, Moscow

Margarita V. Shumilina

National Medical Research Center for Cardiovascular Surgery named after A.N. Bakulev

Email: Shumilinamv@yandex.ru
ORCID iD: 0000-0001-9871-8173
SPIN-code: 8102-9042

MD, Dr. Sci. (Medicine)

Russian Federation, Moscow

References

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