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New devices and techniques
Original research
Novel endovascular transmural technique for pharmacological block of superior cervical ganglion prevents sympathetic-mediated cerebral vasospasm
  1. Wi Jin Kim1,
  2. Hasitha Milan Samarage1,
  3. Matiar Jafari1,
  4. David Zarrin2,
  5. Keshav Goel3,
  6. Xin Qi4,
  7. Anthony C Wang1,
  8. Jeremiah Johnson1,
  9. Geoffrey P Colby1
  1. 1 Department of Neurosurgery, University of California Los Angeles, Los Angeles, California, USA
  2. 2 David Geffen School of Medicine, University of California Los Angeles, Los Angeles, California, USA
  3. 3 University of California Los Angeles, Los Angeles, California, USA
  4. 4 School of Medicine, UCLA, Los Angeles, California, USA
  1. Correspondence to Dr Geoffrey P Colby; gcolby{at}mednet.ucla.edu

Abstract

Background Sympathetic-mediated vasoconstriction from the superior cervical ganglion (SCG) is a significant contributor to cerebral vasospasm. Inhibition of the SCG has been shown to improve cerebral blood flow and reverse cerebral vasospasm in swine models. We evaluated the efficacy of a novel minimally invasive endovascular approach to target and pharmacologically inhibit the SCG, using a Micro-Infusion Device for transmural drug delivery.

Methods Eight SCGs in four Yorkshire swine were surgically identified. After confirming appropriate sympathetic-mediated intracranial vasoconstriction response with SCG stimulation, an endovascular Micro-Infusion Device was used for transmural targeting of the SCG and delivery of 1.5–2 mL of 1% lidocaine-contrast mixture to the perivascular space. Digital subtraction angiography was obtained at: (1) baseline; (2) with SCG stimulation; and (3) after lidocaine delivery to the SCG using the Micro-Infusion Device with concurrent SCG stimulation. Vessel diameters were measured and compared.

Results Endovascular transmural delivery of lidocaine to the SCG and carotid perivascular tissue using the Micro-Infusion Device successfully inhibited sympathetic-mediated vasoconstriction response. Measured vessel diameters after lidocaine delivery were comparable to baseline despite SCG stimulation.

Conclusion A novel endovascular technique of transmural delivery of lidocaine to the SCG and carotid artery perivascular tissues successfully inhibits the sympathetic input to the cerebral vasculature and modulates sympathetic-mediated cerebral vasospasm. These results suggest promising steps towards translation to potential clinical use for patients suffering from cerebral vasospasm.

  • angiography
  • technique
  • neck
  • intervention
  • blood flow

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information.

https://doi.org/10.1136/jnis-2023-020636

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    WHAT IS ALREADY KNOWN ON THIS TOPIC

    • The superior cervical ganglion (SCG) innervates the cerebral vasculature to cause sympathetic-mediated vasoconstriction. Inhibition of the SCG has been shown to increase cerebral blood flow and reverse cerebral vasospasm in swine models.

    WHAT THIS STUDY ADDS

    • This study uses a novel endovascular approach to target and inhibit the sympathetic perivascular nerves of the carotid artery using a transmural drug delivery system.

    HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY

    • The results of this study open the possibility of a novel endovascular procedure to mitigate sympathetic-mediated vasoconstrictive response in patients suffering from cerebral vasospasm.

    Introduction

    Cerebral vasospasm remains the leading potentially treatable cause of death and disability in patients with subarachnoid hemorrhage, particularly in aneurysmal subarachnoid hemorrhage. Central to the adverse outcome of cerebral vasospasm is the narrowing of cerebral arteries and its related cerebral hypoperfusion, leading to delayed ischemic neurologic deficit.1 One-third of patients develop symptomatic ischemia from cerebral vasospasm following aneurysm rupture, and half of these patients develop permanent cerebral infarcts.2 The pathogenesis of cerebral vasospasm is multifactorial, involving nitric oxide scavenging,3 increased endothelin 1,4 and inflammatory remodeling of the intracranial vasculature.5 Regardless of the exact mechanism of cerebral vasospasm, reversal of the arterial narrowing and improvement of cerebral perfusion often results in rapid improvement of patients’ clinical condition.

    Sympathetic innervation to the cerebral vessels stems from the superior cervical ganglion (SCG), and the activation of such sympathetic activity is a significant contributor to the pathogenesis of cerebral vasospasm.6–11 Stimulation of the SCG causes potent cerebral perfusion deficit and vasoconstriction in a swine model, mimicking pathological cerebral vasospasm.12 13 In addition, inhibition of the SCG with local anesthetic blocks the effects of sympathetic stimulation and restores cerebral blood flow and vessel caliber.

    The Micro-Infusion Device (Mercator MedSystems) is a US Food and Drug Administration approved endovascular catheter intended for infusion of diagnostic and therapeutic agents into the vessel wall and perivascular areas of peripheral vasculature. Our group has adapted this technique for the cervical and cerebral vasculature. Repeated use of this device in swine carotid artery is safe and without complications of vessel injury, intravascular thrombus, extravascular hematoma, or stroke.14 We aimed to develop a minimally invasive, endovascular approach to target and inhibit the SCG as a novel treatment modality for cerebral vasospasm.

    In the present study, we assessed whether sympathetic-mediated vasoconstriction of cerebral vasculature can be inhibited by an endovascular transmural technique using the Micro-Infusion Device to block sympathetic output of the SCG.

    Methods

    Animal care

    Ethical use of animals, associated housing/handling and all related experiments were reviewed and approved by the institution’s Institutional Animal Care and Use Committee and Animal Research Committee and Division of Laboratory Animal Medicine. All procedures were conducted in accordance with the Association for Assessment and Accreditation of Laboratory Animal Care International guidelines.

    Anesthesia, neck dissection and digital subtraction angiography

    Four Yorkshire swine (Sus scrofa), representing eight carotid arteries, of either gender between 40–50 kg were used. The animals were anesthetized and bilateral carotid sheath contents were surgically exposed as previously described.12 The SCG was identified and electrically stimulated as established. Diagnostic angiography procedures were performed using a Siemens Artis Zeego C-Arm as described.13 Digital subtraction angiography of the neck and intracranial vasculature was obtained before and with SCG stimulation (figure 1). Following a rest period for the vasculature to return to baseline, the Micro-Infusion Device was navigated to the mid-common carotid artery (at the approximate location of the SCG) under fluoroscopy as previously described.14

    Figure 1
    Figure 1

    Representative AP view of swine cerebral angiogram projected onto axial view of MRI of swine brain. Red arrows: location of vessel diameter measurement. Black arrows: anatomic references. ACA, anterior cerebral artery; AP, anterior-posterior; APA, ascending pharyngeal artery; ICA, internal carotid artery; aMCA, anterior middle cerebral artery; PCA, posterior cerebral artery; pMCA, posterior middle cerebral artery;.

    Carotid transmural inhibition of the SCG

    The radio-opaque triangle markers of the Micro-Infusion Device were used to direct the needle in the postero-medial direction to target the SCG. The location of the SCG was identified by anatomic landmarks (posterior and medial to the common carotid artery, proximal to ascending pharyngeal artery branch point) and the electrode needles. Under fluoroscopy, the balloon was inflated to fill the width of the vessel, causing subsequent microneedle puncture of the vessel wall (figure 2A–D); 1.5–2 mL of 1% lidocaine with 50% Omnipaque (iohexol) 300 contrast solution was injected into the common carotid perivascular space (figure 2E–I). The balloon of the Micro-Infusion Device was subsequently deflated and the catheter was removed. Post-procedure diagnostic angiograms were obtained to evaluate for any complications, such as dissection or contrast extravasation. The SCG was again stimulated 90 s after transmural lidocaine injection, and another diagnostic angiogram was obtained 30 s after onset of stimulation to evaluate for inhibition of sympathetic-mediated intracranial vasoconstriction.

    Figure 2
    Figure 2

    AP view of right neck showing positioning and transmural lidocaine injection using the Micro-Infusion Device. (A) Fluoroscopy single shot showing Micro-Infusion Device positioned in the right common carotid artery with needle aimed towards the SCG. Electric needle stimulators placed in the right SCG (black arrow). Distal and proximal radio-opaque indicators of the Micro-Infusion Device (black arrowheads). Orientation marker for Micro-Infusion Device needle (white arrowhead). (B, C) DSA showing gradual inflation of the Micro-Infusion Device balloon. (D) X-ray showing fully inflated balloon of the Micro-Infusion Device. (E–H) DSA showing gradual transmural injection of 1% lidocaine in 50% contrast solution (2 mL) into the targeted SCG/perivascular space. (I) Fluoroscopy single shot image showing immediate post-injection image. AP, anterior-posterior; DSA, digital subtraction angiography; SCG, superior cervical ganglion.

    Vessel measurements

    Vessel diameters were measured using tools on the institution’s PACS (picture archiving and communication system). Location of the vessel diameter measurements for various arteries are shown in figure 1. Diameters of the ascending pharyngeal artery (APA), anterior cerebral artery (ACA), anterior middle cerebral artery (aMCA), posterior middle cerebral artery (pMCA), internal carotid artery (ICA) and posterior cerebral artery (PCA) were measured. All measurements were done under four times the original magnification to ensure accurate measurements of vessel diameter at the same location as previously described.13

    Statistics

    To account for normal variation in vessel diameter between animals and laterality, vessel diameters were represented as a percent of the diameters measured at baseline (no SCG stimulation) and compared between groups. Two-tailed Student’s t-test was used to determine statistical significance between groups. The significant level for all tests was set at P=0.05.

    Results

    Eight SCGs in four animals were targeted using the Micro-Infusion Device in our study. Stimulation of the SCG resulted in significant ipsilateral vasoconstriction response (figure 3B) in the cervico-cranial vasculature, as seen previously.13 Electrical stimulation of the SCG led to statistically significant reduction (P<0.05) in select ipsilateral vessel diameters. Compared with baseline, the APA diameter decreased by 40.0±16.7%, the ICA diameter decreased by 7.51±8.14%, the aMCA diameter decreased by 31.1±9.20%, and the ACA diameter decreased by 36.9±8.38% (figure 4). Changes in the pMCA diameter was not statistically significant.

    Figure 3
    Figure 3

    Swine cerebral angiograms (right common carotid injection) modeling cerebral vasospasm before and after novel endovascular treatment. (A) Baseline. (B) Right SCG stimulation. (C) Lidocaine administration using the Micro-Infusion Device with subsequent right SCG stimulation. SCG, superior cervical ganglion.

    Figure 4
    Figure 4

    Violin plots of Individual vessel diameters. Vessel diameters plotted as a percent of baseline (no SCG stimulation) vessel diameters (bandwidth=5). (A) Ascending pharyngeal artery (t-test P=4.7x10−4). (B) Internal carotid artery (t-test P=0.01). (C) Posterior middle cerebral artery (t-test P=0.11). (D) Internal carotid artery (t-test P=6.2x10−4). (E) Anterior cerebral artery (t-test P=3.1x10−4). Red: SCG stimulation. Green: SCG stimulation with prior 1% lidocaine administration using the Micro-Infusion Device. White dot in center of violin plot: median. Colored line across violin plot: mean. Vertical gray box: IQR. *P≤0.05; **P≤0.01; ***P≤0.001; ns, non-statistically significant. ACA, anterior cerebral artery; APA, ascending pharyngeal artery; ICA, internal carotid artery; MCA, middle cerebral artery; SCG, superior cervical ganglion.

    After allowing the SCG stimulation to wear off and the vasculature to return to baseline caliber, the Micro-Infusion Device was used to deliver 1.5 to 2 mL of 1% lidocaine with 50% contrast mixture to the SCG and/or perivascular efferent sympathetic fibers of the carotid artery without evidence of vascular injury, such as vessel dissection, contrast extravasation or hemorrhage in all eight SCG injections (figure 2). Lidocaine delivery using the Micro-Infusion Device was able to inhibit sympathetic-mediated intracranial vasoconstriction despite subsequent SCG stimulation (figures 3 and 4); all measured vessel diameter means were within 13% of, and non-statistically different from, baseline measurements (all P>0.05).

    Discussion

    This study builds on our prior studies to demonstrate the effectiveness of a novel minimally invasive endovascular therapy in mitigating sympathetic-mediated vasoconstriction response seen in cerebral vasospasm. We are the first group to show that endovascular transmural targeting and delivery of a pharmacological agent is possible in cervical and cerebral vasculature to modulate cerebral vessel diameters. Lidocaine was successfully delivered across the wall of the carotid artery, from intraluminal to extraluminal, to the SCG and perivascular tissue, and this blocked sympathetic-mediated vasoconstrictive effects.

    Inhibiting the sympathetic output to cerebral vessels has been proposed to treat cerebral vasospasm-related perfusion deficit.15 The effects of sympathetic blockade at the stellate ganglion and the SCG on cerebral blood flow have been documented in several cases to date. Gupta and colleagues blocked the stellate ganglion in 20 male patients without subarachnoid hemorrhage and measured cerebral hemodynamics via transcranial Doppler ultrasonography, showing that stellate ganglion blockade increased perfusion pressure and decreased cerebral vascular tone without disrupting vessel autoregulation.15 Treggiari and colleagues reported SCG blockade in nine patients who developed symptomatic cerebral vasospasm following open aneurysm surgery. Improvement in cerebral perfusion was found in all patients using angiography, and complete symptom resolution occurred in six conscious patients.16 More recently, Bombardieri et al outlined a review showing promising outcomes for cervical sympathetic blockade for treatment of vasospasm and delayed cerebral ischemia.17 These studies suggest that sympathetic blockade is a promising target for the treatment of cerebral vasospasm.

    Patients with moderate-to-severe cerebral vasospasm, especially when symptomatic, invariably obtain a cerebral angiogram, often with interventions such as calcium channel blocker infusions or balloon angioplasty. These procedures are performed by neuro-endovascular specialists with neurosurgery, radiology, or neurology backgrounds. Therefore, new endovascular techniques for the treatment of cerebral vasospasm can be added to the standard clinical workflow by the same specialists without the need for significant additional resources or coordination required for another procedure. This makes the endovascular technique described in this manuscript favorable compared to percutaneous approaches to the SCG, assuming the endovascular technique is safe and similar means of drug delivery and inhibition can be achieved. Towards this end, this technique using the Micro-Infusion Device was previously tested and deemed safe in the swine carotid artery,14 which has been described to be most similar,18 yet more fragile, compared with that of the human carotid artery.19 Furthermore, the vessel diameter changes with SCG stimulation and rescue after lidocaine injection using the Micro-Infusion Device seen in this study (figure 4) was comparable to the results in our prior study in which the SCG was blocked by a direct injection through an open surgical approach.13 These results suggests that the novel endovascular transmural technique for SCG inhibition is safe in use and equivalent in efficacy.

    While an aim of this study was to directly inject the SCG using the Micro-Infusion Device, it is unclear if the transmural injection reached into the ganglion itself. As seen in figure 2E–I, there was infiltration of the lidocaine-contrast mixture into the perivascular space, but we were unable to discern if it reached inside the ganglion tissue. Adding a staining agent (dye) into the lidocaine-contrast mixture did not help to discriminate if the agent was actively injected into the ganglion, as the mixture diffusely spread into and stained the surrounding structures. However, given that there was effective inhibition of the sympathetic-mediated vasoconstrictive effects in all our experiments, we hypothesized that our injection either involved the ganglion and/or may also be blocking the downstream perivascular efferent sympathetic fibers (third order sympathetic neurons) that reside in and surround the carotid artery adventitia. This hypothesis could be tested in the future by moving the Micro-Infusion Device more distal in the carotid artery before injecting the lidocaine to target the efferent sympathetic fibers further away from the SCG.

    Although a robust dose-response study, or multiple measures of duration of efficacy of lidocaine, would be interesting and add to our understanding of the utility of this technique, this was determined to be beyond the scope of this study. A prior experiment showed restoration of SCG stimulation approximately 60 to 90 min after lidocaine injection into the SCG (data not shown), consistent with restoration of normal SCG function. Durability of SCG inhibition can presumably be selected based on the half-life of the drug used. Numerous sodium channel blocking agents with varying duration of efficacy are available, such as bupivacaine or even liposomal bupivacaine, that are effective up to 24–48 hours.

    This study represents a novel paradigm for adjunct treatment of cerebral vasospasm and for approaching any condition that may benefit from delivery of agents (small molecule, biological, etc) to perivascular structures of the head or neck. We recognize there are limitations in the present study and these include the following. An established animal model was used for the current study; however, this is also a limitation, as human cerebral vasospasm is a complex pathophysiologic process that may not be properly replicated in an animal model. Our study also has a small sample size. Yet, given the striking and reproducible changes in vessel caliber, we were able to demonstrate statistical significance with this sample size. Use of further swine for more data points was deemed unnecessary. Another limitation includes the use of the Micro-Infusion Device in an area of open neck dissection. Because the design of this study requires an open surgical approach to identify and electrically stimulate the SCG, the Micro-Infusion Device was used to inject into an area that had been dissected and was free of the connective tissue that would normally surround the structures in the neck, including the SCG. This may have allowed more extensive infiltration of lidocaine into the surrounding perivascular tissue than in a clinical scenario in which the neck has not been surgically manipulated. However, in an alternate study when SCG inhibition was not tested (no prior neck dissection), a similar distribution of contrast dye into the carotid perivascular tissues was observed (data not shown). This suggests that drug distribution is similar regardless of prior neck dissection.

    Translatability to humans

    While carotid puncture may raise concern and alarm in some clinicians, it is a technique with a long history in the field of endovascular intervention. Percutaneous direct carotid punctures have been utilized frequently in the past for cervical and cerebral angiography.20 Furthermore, carotid punctures are still utilized in modern times for neurointervention21 and cardiac intervention22 when other approaches are not feasible. Finally, transcarotid artery revascularization is a technique that involves direct carotid puncture that has been determined to be safe and is commonly used for carotid atherosclerotic disease.23

    Interestingly, inadvertent carotid punctures occur in up to 9.3% of attempted internal jugular central venous line placements using an 18-guage introducer needle with little to no neurological vascular consequences.24 As such, we hypothesize that a carotid puncture in humans using the 34-guage microneedle from the Micro-Infusion Device will have minimal safety issues given the tiny size of the needle. Additionally, our prior work established the safety profile of the Micro-Infusion Device after extensive testing showed no evidence of post-procedural stroke, hematoma or dissection after repeated use in the swine carotid artery,14 which is determined to be the most similar to,18 yet more fragile than, the human carotid artery.19 We recognize that, despite a promising safety profile, the actual risk profile of using the Micro-Infusion Device in the carotid arteries of humans will need to be established. Caution and stringent protocols are required for translation of this technique into clinical practice as carotid intimal injury, dissection or hematoma could result in significant morbidity or mortality.

    Another aspect of our study that potentially limits translatability to clinical practice is our model of cerebral vasospasm. Our model only tests the autonomic vasoconstrictive components of vasospasm mediated by the sympathetic nervous system, which partially mimics cerebral vasospasm seen in clinical practice. Cerebral vasospasm is thought to be a complex disease involving neurogenic, metabolic and endothelial factors.25 Hence, developing a true cure for cerebral vasospasm may be difficult and involve several mechanisms of intervention. However, given the established understanding of sympathetic hyperactivity often seen with cerebral vasospasm,6–8 26 we believe that sympathetic blockade is an important component of a likely multi-pronged treatment paradigm for this disease.

    Conclusion

    The novel endovascular transmural technique demonstrated here can successfully deliver a pharmacological agent to the carotid artery perivascular tissues and SCG to inhibit the sympathetic input to the cerebral vasculature and prevent sympathetic-mediated cerebral vasospasm. The result of this study affirms feasibility of a novel adjunct treatment strategy for cerebral vasospasm that should be further explored.

    Data availability statement

    All data relevant to the study are included in the article or uploaded as supplementary information.

    Ethics statements

    Patient consent for publication

    Ethics approval

    Not applicable.

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    Footnotes

    • Contributors WJK, HMS, MJ, ACW, JJ and GPC had substantial contributions to the concept and design of the work and the interpretation of the data for the work. WJK, HMS, MJ, DZ, KG, XQ and GPC had substantial contributions to the acquisition, analysis and interpretation of the data for the work. All authors were significantly involved in drafting and revising the work. All authors reviewed and approved the final version of the work and agree to be accountable for aspects of the work. GPC is the author responsible for the overall content of the work as the guarantor. The guarantor accepts full responsibility for the work and/or the conduct of the study, had access to the data, and controlled the decision to publish.

    • Funding Casa Colina Foundation research grant, NIH Research Education Programs (R25).

    • Competing interests None declared.

    • Provenance and peer review Not commissioned; externally peer reviewed.