Feasibility, Clinical Potential, and Limitations of Trans-Burr Hole Ultrasound for Postoperative Evaluation of Chronic Subdural Hematoma: A Prospective Pilot Study

Neurosurgery 95:924–931, 2024

Chronic subdural hematoma (CSDH) is commonly managed through burr hole surgery. Routine follow-up using computed tomography (CT) imaging is frequently used at many institutions, contributing to significant radiation exposure. This study evaluates the feasibility, safety, and reliability of trans-burr hole sonography as an alternative postoperative imaging modality, aiming to reduce radiation exposure by decreasing the frequency of CT scans.

METHODS: We conducted a prospective pilot study on 20 patients who underwent burr hole surgery for CSDH. Postoperative imaging included both CT and sonographic examinations through the burr hole. We assessed the ability to measure residual subdural fluid thickness under the burr hole sonographically compared with CT, the occurrence of complications, and the potential factors affecting sonographic image quality. The Pearson correlation coefficient was used to demonstrate relationships between CT and ultrasound and axial and coronal ultrasound.

RESULTS: Sonography through the burr hole was feasible in 73.5% of cases, providing measurements of residual fluid that closely paralleled CT findings, with an average discrepancy of 1.2 mm for axial and 1.4 mm for coronal sonographic views. A strong positive correlation was found between axial and coronal ultrasound (r = 0.955), CT and axial ultrasound (r = 0.936), and CT and coronal ultrasound (r = 0.920). The primary obstacle for sonographic imaging was the presence of air within the burr hole or the subdural space, which typically resolved over time after surgery.

CONCLUSION: Trans-burr hole sonography emerges as a promising technique for postoperative monitoring of CSDH, with the potential to safely reduce reliance on CT scans and associated radiation exposure in selected patients. Our results support further investigation into the extended use of sonography during the follow-up phase. Prospective multicenter studies are recommended to establish the method’s efficacy and to explore strategies for minimizing air presence postsurgery.

First Experience With Postoperative Transcranial Ultrasound Through Sonolucent Burr Hole Covers in Adult Hydrocephalus Patients

Neurosurgery 92:382–390, 2023

Managing patients with hydrocephalus and cerebrospinal fluid (CSF) disorders requires repeated head imaging. In adults, it is typically computed tomography (CT) or less commonly magnetic resonance imaging (MRI). However, CT poses cumulative radiation risks and MRI is costly. Ultrasound is a radiation-free, relatively inexpensive, and optionally point-of-care alternative, but is prohibited by very limited windows through an intact skull.

OBJECTIVE: To describe our initial experience with transcutaneous transcranial ultrasound through sonolucent burr hole covers in postoperative hydrocephalus and CSF disorder patients.

METHODS: Using cohort study design, infection and revision rates were compared between patients who underwent sonolucent burr hole cover placement during new ventriculoperitoneal shunt placement and endoscopic third ventriculostomy over the 1-year study time period and controls from the period 1 year before. Postoperatively, trans-burr hole ultrasound was performed in the clinic, at bedside inpatient, and in the radiology suite to assess ventricular anatomy.

RESULTS: Thirty-seven patients with sonolucent burr hole cover were compared with 57 historical control patients. There was no statistically significant difference in infection rates between the sonolucent burr hole cover group (1/37, 2.7%) and the control group (0/57, P = .394). Revision rates were 13.5% vs 15.8% (P = 1.000), but no revisions were related to the burr hole or cranial hardware.

CONCLUSION: Trans-burr hole ultrasound is feasible for gross evaluation of ventricular caliber postoperatively in patients with sonolucent burr hole covers. There was no increase in infection rate or revision rate. This imaging technique may serve as an alternative to CT and MRI in the management of select patients with hydrocephalus and CSF disorders.

5-Aminolevulinic Acid and Contrast-Enhanced Ultrasound: The Combination of the 2 Techniques to Optimize the Extent of Resection in Glioblastoma Surgery

Neurosurgery 86:E529–E540, 2020

The survival benefit in maximizing resection in glioblastomas (GBMs) has been demonstrated by numerous studies. The true limit of infiltration of GBMs has been an overwhelming obstacle, and several technological advances have been introduced to improve the identification of residual tumors.

OBJECTIVE: To evaluate whether the integration of 5-aminolevulinic acid (5-ALA) with microbubble contrast-enhanced ultrasound (CEUS) improves residual tumor identification and has an impact on the extent of resection (EOR), overall survival (OS), and progressionfree survival (PFS).

METHODS: A total of 230 GBM procedures were retrospectively studied. Cases were stratified according to the surgical procedure into 4 groups: 5-ALA- and CEUS-guided surgeries, 5-ALA-guided surgeries, CEUS-guided surgeries, and conventional microsurgical procedures.

RESULTS: Patients undergoing conventional microsurgical procedures showed the worst EORs compared to the assisted techniques (5-ALA and CEUS procedures). Both 5-ALA and CEUS techniques improved the EOR compared to conventional microsurgical procedures. However, their combination gave the best results in terms of the EOR (P = .0003). The median EOR% and the number of supramarginal resections are hence superior in the 5-ALA + CEUS + group compared to the others; this observation had consequences on PFS and OS in our series.

CONCLUSION: In terms of the EOR, the best results can be achieved through a combination of both techniques,where the 5-ALA-guided procedure is followed by a final survey with CEUS. Compared with other intraoperative imaging techniques, CEUS is a real-time, readily repeatable, safe, and inexpensive technique that provides valuable information to the surgeon before, during, and after resection.

Intraoperative 3D ultrasound–guided resection of diffuse low-grade gliomas

J Neurosurg 132:518–529, 2020

Extent of resection (EOR) and residual tumor volume are linked to prognosis in low-grade glioma (LGG) and there are various methods for facilitating safe maximal resection in such patients. In this prospective study the authors assess radiological and clinical results in consecutive patients with LGG treated with 3D ultrasound (US)–guided resection under general anesthesia.

METHODS Consecutive LGGs undergoing primary surgery guided with 3D US between 2008 and 2015 were included. All LGGs were classified according to the WHO 2016 classification system. Pre- and postoperative volumetric assessments were performed, and volumetric results were linked to overall and malignant-free survival. Pre- and postoperative health-related quality of life (HRQoL) was evaluated.

RESULTS Forty-seven consecutive patients were included. Twenty LGGs (43%) were isocitrate dehydrogenase (IDH)– mutated, 7 (14%) were IDH wild-type, 19 (40%) had both IDH mutation and 1p/19q codeletion, and 1 had IDH mutation and inconclusive 1p/19q status. Median resection grade was 93.4%, with gross-total resection achieved in 14 patients (30%). An additional 24 patients (51%) had small tumor remnants < 10 ml. A more conspicuous tumor border (p = 0.02) and lower University of California San Francisco prognostic score (p = 0.01) were associated with less remnant tumor tissue, and overall survival was significantly better with remnants < 10 ml (p = 0.03). HRQoL was maintained or improved in 86% of patients at 1 month. In both cases with severe permanent deficits, relevant ischemia was present on diffusionweighted postoperative MRI.

CONCLUSIONS Three-dimensional US–guided LGG resections under general anesthesia are safe and HRQoL is preserved in most patients. Effectiveness in terms of EOR appears to be consistent with published studies using other advanced neurosurgical tools. Avoiding intraoperative vascular injury is a key factor for achieving good functional outcome.

Differentiating brain radionecrosis from tumour recurrence: a role for contrast-enhanced ultrasound?

Acta Neurochir (2017) 159:2405–2408

Differentiating radionecrosis from tumour recurrence is a major issue in neuro-oncology. Conventional imaging is far from being validated as an alternative to histologicalassessment.

We report the case of a patient operated on for suspected recurrence of brain metastasis 9 months after cyberknife radiosurgery. While magnetic resonance imaging showed strong enhancement of the lesion, intraoperative contrast-enhanced ultrasonography (CEUS) surprisingly did
not—different from what is expected for brain metastases.

Histopathological examination documented radionecrosis. For the first time, we describe radionecrosis with CEUS; further investigation is needed; however, the lack of enhancement could represent an important hallmark in differential diagnosis with neoplastic tissue.

Linear array ultrasound in low-grade glioma surgery: histology-based assessment of accuracy in comparison to conventional intraoperative ultrasound and intraoperative MRI

Linear array ultrasound in low-grade glioma surgery

Acta Neurochir (2015) 157:195–206

In low-grade glioma (LGG) surgery, intraoperative differentiation between tumor and most likely tumor-free brain tissue can be challenging. Intraoperative ultrasound can facilitate tumor resection. The aim of this study is to evaluate the accuracy of linear array ultrasound in comparison to conventional intraoperative ultrasound (cioUS) and intraoperative high-field MRI (iMRI).

Methods We prospectively enrolled 13 patients harboring a LGG of WHO Grade II. After assumed near total removal, a resection control was performed using navigated cioUS, navigated lioUS, and iMRI. We harvested 30 navigated biopsies from the resection cavity and compared the histopathological findings with the respective imaging results. Spearman’s rho was calculated to test for significant correlations. Sensitivity and specificity as well as receiver operating characteristics (ROC) were calculated to assess test performance of each imaging modality.

Results Imaging results of lioUS correlated significantly (p<0.009) with iMRI. Both iMRI and lioUS correlated significantly with final histopathological diagnosis (p<0.006, p<0.014). cioUS did not correlate with other imaging findings or with final diagnosis. The highest sensitivity for residual tumor detection was found in iMRI (83 %), followed by lioUS (79 %). The sensitivity of cioUS was only 21 %. Specificity was highest in cioUS (100 %), whereas iMRI and lioUS both achieved 67 %. ROC curves showed fair results for iMRI and lioUS and a poor result for cioUS.

Conclusions Intraoperative resection control in LGGs using lioUS reaches a degree of accuracy close to iMRI. Test results of lioUS are superior to cioUS. cioUS often fails to discriminate solid tumors from “normal” brain tissue during resection control. Only in lesions <10 cc cioUS does show good accuracy.

Intra-operative correction of brain-shift

Intra-operative correction brain-shift

Acta Neurochir (2014) 156:1301–1310

Brain-shift is a major source of error in neuronavigation systems based on pre-operative images. In this paper, we present intra-operative correction of brain-shift using 3D ultrasound.

Methods The method is based on image registration of vessels extracted from pre-operative MRA and intra-operative power Doppler-based ultrasound and is fully integrated in the neuronavigation software.

Results We have performed correction of brain-shift in the operating room during surgery and provided the surgeon with updated information. Here, we present data from seven clinical cases with qualitative and quantitative error measures.

Conclusion The registration algorithm is fast enough to provide the surgeon with updated information within minutes and accounts for large portions of the experienced shift. Correction of brain-shift can make pre-operative data like fMRI and DTI reliable for a longer period of time and increase the usefulness of the MR data as a supplement to intra-operative 3D ultrasound in terms of overview and interpretation.

Intraoperative Contrast-Enhanced Ultrasound for Brain Tumor Surgery

INTRAOPERATIVE CEUS FOR BRAIN SURGERY

Neurosurgery 74:542–552, 2014 

Contrast-enhanced ultrasound (CEUS) is a dynamic and continuous modality that offers a real-time, direct view of vascularization patterns and tissue resistance for many organs. Thanks to newer ultrasound contrast agents, CEUS has become a wellestablished, live-imaging technique in many contexts, but it has never been used extensively for brain imaging. The use of intraoperative CEUS (iCEUS) imaging in neurosurgery is limited.

OBJECTIVE: To provide the first dynamic and continuous iCEUS evaluation of a variety of brain lesions.

METHODS: We evaluated 71 patients undergoing iCEUS imaging in an off-label setting while being operated on for different brain lesions; iCEUS imaging was obtained before resecting each lesion, after intravenous injection of ultrasound contrast agent. A semiquantitative, offline interobserver analysis was performed to visualize each brain lesion and to characterize its perfusion features, correlated with histopathology.

RESULTS: In all cases, the brain lesion was visualized intraoperatively with iCEUS. The afferent and efferent blood vessels were identified, allowing evaluation of the time and features of the arterial and venous phases and facilitating the surgical strategy. iCEUS also proved to be useful in highlighting the lesion compared with standard B-mode imaging and showing its perfusion patterns. No adverse effects were observed.

CONCLUSION: Our study is the first large-scale implementation of iCEUS in neurosurgery as a dynamic and continuous real-time imaging tool for brain surgery and provides the first iCEUS characterization of different brain neoplasms. The ability of CEUS to highlight and characterize brain tumor will possibly provide the neurosurgeon with important information anytime during a surgical procedure.

Surgical strategy in grade II astrocytoma

Surgical strategy in grade II astrocytoma

Acta Neurochir (2013) 155:2227–2235

We recently demonstrated a survival benefit of early resection in unselected diffuse low-grade gliomas (LGG). However, heterogeneity within the LGG entity warrants investigation in a homogenous subgroup. Astrocytoma represents the largest subgroup of LGG, and is characterized by diffuse growth and inferior prognosis. We aimed to study the effects of early resection compared to biopsy and watchful waiting in this subgroup.

Methods Patient data was retrospectively reviewed in two neurosurgical departments with regional referral practice. In one hospital, initial diagnostic biopsies and watchful waiting was favored, while early resections guided with three-dimensional (3D) ultrasound were advocated in the other hospital. This created a natural experiment with patient management heavy influenced by residential address. In the hospitals’ histopathology databases, all adult patients diagnosed with supratentorial LGG from 1998 through 2009 were screened (n =169) and underwent blinded histopathological review. Histopathological review concluded with 117 patients with grade II astrocytomas that were included in the present study. The primary end-point was overall survival assessed by a regional comparison.

Results Early resections were performed in 51 (82 %) versus 12 (22 %) patients in the respective hospitals (p <0.001). The two patient populations were otherwise similar. Median survival was 9.7 years (95 % CI 7.5–11.9) if treated in the hospital favoring early resections compared to 5.6 years (95 % CI 3.5– 7.6) if treated at the hospital favoring biopsy and watchful waiting (p =0.047). No difference in surgical-related neurological morbidity was seen (p =0.843).

Conclusions Early 3D ultrasound guided resections improve survival, apparently without increasedmorbidity, compared to biopsy and watchful waiting in patients with diffuse World Health Organization (WHO) grade II astrocytomas.

Modern intraoperative imaging modalities for the vascular neurosurgeon treating intracerebral hemorrhage

modern OR

Neurosurg Focus 34 (5):E2, 2013

This paper reviews the current intraoperative imaging tools that are available to assist neurosurgeons in the treatment of intracerebral hemorrhage (ICH). This review shares the authors’ experience with each modality and discusses the advantages, potential limitations, and disadvantages of each.

Surgery for ICH is directed at blood clot removal, reduction of intracranial pressure, and minimization of secondary damage associated with hematoma breakdown products. For effective occlusion and safe obliteration of vascular anomalies associated with ICH, vascular neurosurgeons today require a thorough understanding of the various intraoperative imaging modalities available for obtaining real-time information. Use of one or more of these modalities may improve the surgeon’s confidence during the procedure, the patient’s safety during surgery, and surgical outcome.

The modern techniques discussed include 1) indocyanine green–based video angiography, which provides realtime information based on high-quality images showing the residual filling of vascular pathological entities and the patency of blood vessels of any size in the surgical field; and 2) intraoperative angiography, which remains the gold standard intraoperative diagnostic test in the surgical management of cerebral aneurysms and arteriovenous malformations. Hybrid procedures, providing multimodality image-guided surgeries and combining endovascular with microsurgical strategies within the same surgical session, have become feasible and safe. Microdoppler is a safe, noninvasive, and reliable technique for evaluation of hemodynamics of vessels in the surgical field, with the advantage of ease of use. Intraoperative MRI provides an effective navigation tool for cavernoma surgery, in addition to assessing the extent of resection during the procedure. Intraoperative CT scanning has the advantage of very high sensitivity to acute bleeding, thereby assisting in the confirmation of the extent of hematoma evacuation and the extent of vascular anomaly resection. Intraoperative ultrasound aids navigation and evacuation assessment during intracerebral hematoma evacuation surgeries. It supports the concept of minimally invasive surgery and has undergone extensive development in recent years, with the quality of ultrasound imaging having improved considerably.

Image-guided therapy, combined with modern intraoperative imaging modalities, has changed the fundamentals of conventional vascular neurosurgery by presenting real-time visualization of both normal tissue and pathological entities. These imaging techniques are important adjuncts to the surgeon’s standard surgical armamentarium. Familiarity with these imaging modalities may help the surgeon complete procedures with improved safety, efficiency, and clinical outcome

Minimally invasive evacuation of spontaneous intracerebral hemorrhage using sonothrombolysis

J Neurosurg 115:592–601, 2011. DOI: 10.3171/2011.5.JNS10505

Catheter-based evacuation is a novel surgical approach for the treatment of brain hemorrhage. The object of this study was to evaluate the safety and efficacy of ultrasound in combination with recombinant tissue plasminogen activator (rt-PA) delivered through a microcatheter directly into spontaneous intraventricular (IVH) or intracerebral (ICH) hemorrhage in humans.

Methods. Thirty-three patients presenting to the Swedish Medical Center in Seattle, Washington, with ICH and IVH were screened between November 21, 2008, and July 13, 2009, for entry into this study. Entry criteria included the spontaneous onset of intracranial hemorrhage ≥ 25 ml and/or IVH producing ventricular obstruction. Nine patients (6 males and 3 females, with an average age of 63 years [range 38–83 years]) who met the entry criteria consented to participate and were entered into the trial. A ventricular drainage catheter and an ultrasound microcatheter were stereotactically delivered together, directly into the IVH or ICH. Recombinant tissue plasminogen activator and 24 hours of continuous ultrasound were delivered to the clot. Gravity drainage was performed. In patients with IVHs, 3 mg of rt-PA was injected; in patients with intraparenchymal hemorrhages, 0.9 mg of rt-PA was injected. The rt-PA was delivered in 3 doses over 24 hours.

Results. All patients had significant volume reductions in the treated hemorrhage. The mean percentage volume reduction after 24 hours of therapy, as determined on CT and compared with pretreatment stability scans, was 59 ± 5% (mean ± SEM) for ICH and 45.1 ± 13% for IVH (1 patient with ICH was excluded from analysis because of catheter breakage). There were no intracranial infections and no significant episodes of rebleeding according to clinical or CT assessment. One death occurred by 30 days after admission. Clinical improvements as determined by a decrease in the National Institutes of Health Stroke Scale score were demonstrated at 30 days after treatment in 7 of 9 patients. The rate of hemorrhage lysis was compared between 8 patients who completed treatment, and patient cohorts treated for IVH and ICH using identical doses of rt-PA and catheter drainage but without the ultrasound (courtesy of the MISTIE [Minimally Invasive Surgery plus T-PA for Intracerebral Hemorrhage Evacuation] and CLEAR II [Clot Lysis Evaluating Accelerated Resolution of Intraventricular Hemorrhage II] studies). Compared with the MISTIE and CLEAR data, the authors observed a faster rate of lysis during treatment for IVH and ICH in the patients treated with sonolysis plus rt-PA versus rt-PA alone.

Conclusions. Lysis and drainage of spontaneous ICH and IVH with a reduction in mass effect can be accomplished rapidly and safely through sonothrombolysis using stereotactically delivered drainage and ultrasound catheters via a bur hole. A larger clinical trial with catheters specifically designed for brain blood clot removal is warranted.

Intrasellar Ultrasound in Transsphenoidal Surgery: A Novel Technique

Neurosurgery 66:173-186, 2010. doi: 10.1227/01.NEU.0000360571.11582.4F

OBJECTIVE: Residual tumor masses are common after transsphenoidal surgery. The risk of a residual mass increases with tumor size and parasellar or suprasellar growth. Transsphenoidal surgery is usually performed without image guidance. We aimed to investigate a new technical solution developed for intraoperative ultrasound imaging during transsphenoidal surgery, with respect to potential clinical use and the ability to identify neuroanatomy and tumor.

METHODS: In 9 patients with pituitary macroadenomas, intrasphenoidal and intrasellar ultrasound was assessed during transsphenoidal operations. Ultrasound B-mode, power-Doppler and color-Doppler images were acquired using a small prototype linear array, side-looking probe. The long probe tip measures only 3 × 4 mm. We present images and discuss the potential of intrasphenoidal and intrasellar and ultrasound in transsphenoidal surgery.

RESULTS: We present 2-dimensional, high-resolution ultrasound images. A small side-looking, high-frequency ultrasound probe can be used to ensure orientation in the midline for the surgical approach to identify important neurovascular structures to be avoided during surgery and for resection control and identification of normal pituitary tissue. The image resolution is far better than what can be achieved with current clinical magnetic resonance imaging technology.

CONCLUSION: We believe that the concept of intrasellar ultrasound can be further developed to become a flexible and useful tool in transsphenoidal surgery.