Role of intraoperative ultrasonography as a method of neuro-navigation in surgical treatment of intracranial hemorrhage

Abstract

Background:

Spontaneous intracranial hemorrhage (ICH), the second most common type of stroke, can be fatal or cause severe disability. A key technical goal while studying the surgical therapy of ICH should be the amount of hematoma evacuation. Multiple challenges are encountered while dealing with ICH cases, including the removal of a sufficient part of the hematoma with the least residual volume that can be considered acceptable for optimal functional outcome. Minimizing cortical damage and choosing the safest approach that can achieve maximal evacuation of the hematoma must be top priorities. For all the foregoing, intraoperative ultrasound (IOUS) has been proposed as a capable technique for the purpose of localizing the bleeding and tracking its evacuation in real-time.

Methods:

This is a retrospective study, including thirty patients with ICH treated in Neurosurgery departments in Fayoum and Cairo University hospitals from July 2017 to June 2024. Patients were operated upon with the help of IOUS. The benefit of using IOUS for achieving maximal evacuation was assessed according to the presence of residual hemorrhage in postoperative computed tomography (CT) or magnetic resonance imaging (MRI) compared to the preoperative radiological studies.

Results:

Regarding the epidemiological characteristics of the study group, the patients’ mean age of 44.86 ± 19.5 years was observed, with ages ranging from 13 to 75 years. 60% of the participants were males, while 40% were females. Considering the site of the hematoma, clots were observed in 33% of the subjects within the parietal lobe. In 30%, they were in the frontal lobe. 17% of bleeds were temporal, 13% were in the basal ganglia, and 7% were seen in the posterior fossa. With a standard deviation of 15.4 cc and a range of 13–80 cc, the average hematoma size as determined by CT/MRI was 34.5 cc. Furthermore, according to the US, the average size of the hematoma was 34.62 cc, with a standard deviation of 15.5 cc, and a range of 12–81 cc. Ultrasound (US) findings: when compared to control CTs, US had a sensitivity of 91.6% and a specificity of 100% for detecting residual hematoma following surgery, for a total accuracy of 96%.

Conclusion:

Neuro-navigation using US is a simple, quick, and risk-free method of real-time imaging for a variety of neurosurgical operations. It reduces the amount of brain exploration, the extent of dural incisions, and, hopefully, surgical morbidity while accurately identifying and localizing intracranial hematomas. In the absence of sophisticated radiological equipment, it provides generally agreed guidelines for maximizing evacuation.

INTRODUCTION

With a 30-day mortality rate higher than 50% and lasting neurological deficits in over 75% of patients, spontaneous intracranial hemorrhage (ICH) is a devastating and sometimes fatal kind of stroke.[4]

Seizures, vomiting, nausea, and headaches are the most common symptoms that patients report, and they tend to worsen quickly. More than half of patients may have a short prodrome, and specific neurological disorders and changes in awareness are prevalent.[1]

Although the most significant modifiable risk factor for spontaneous ICH is uncontrolled chronic arterial hypertension, there are other risk factors, such as being over the age of fifty-five, being male, smoking, and using anticoagulation and sympathomimetic medications.[16]

For ICH, noncontrast computed tomography (CT) is the goto first diagnostic imaging since it’s cheap, easy to interpret, readily available, and very sensitive to acute blood products and herniation. Magnetic resonance imaging (MRI) is less sensitive for acute blood product detection, but it is far more costly and better at aging ICH, identifying subacute or chronic hemorrhage, underlying vascular lesions, and neoplasms. It also better delineates involved anatomical structures. To identify vascular disease or active arterial extravasation, CT arteriography is helpful in secondary surveys. The basal ganglia and thalamus are the most frequent sites of spontaneous ICH, followed by lobar regions, pons, cerebellum, as well as at the very bottom of the list, other brainstem structures.[16]

Class 1 evidence-based guidelines for neurocritical care unit management of patients with spontaneous ICH have been issued by the American Heart Association and the American Stroke Association for the medical treatment of ICH. In brief, these suggestions include basic critical care monitoring, decreasing the control of arterial blood pressure to 140 mm Hg, treating coagulopathy, preventing deep vein thrombosis, managing glucose levels, treating seizures, and managing medical consequences.[9]

The 2019 Chinese recommendations regarding the diagnosis and therapy of hypertensive ICH rank surgery high among the therapeutic options because it quickly removes mechanical compression, clears the hematoma, and reduces intracranial pressure adequately.[7]

A key technical goal while studying the surgical therapy of ICH should be the amount of hematoma evacuation. For the best functional result, how much of the hematoma must be removed, or what amount of residual volume is considered acceptable? Because excessive evacuation might harm nearby (healthy) tissue and deep perforating arteries, determining the extent of the leftover hematoma is crucial.[3]

Particularly in cases of severe bleeding, open surgery carries the risk of damaging normal brain tissue, which may impact functional results.[21] Intraoperative ultrasonography has been suggested to detect bleeding and track its clearance in real-time, which may help reduce cortical damage and choose the safest strategy for radical hematoma evacuation.[7]

Our goal in this research was to evaluate intraoperative US as a neuro-navigation tool aiding in the radical evacuation process by detecting and evaluating the amount of the ICH and the extent of the remaining hematoma.

Aim of the study

By comparing its accuracy with that of the postoperative CT picture, we may determine the usefulness of intraoperative ultrasound (IOUS), or “Intraoperative Ultrasonography,” as an intraoperative guide for the complete evacuation of ICH and the identification of any residual.

MATERIALS AND METHODS

Study design

This is a retrospective study, including thirty patients with ICH treated in Neurosurgery departments in Fayoum and Cairo University hospitals from July 2017 to June 2024. Patients were operated upon using the help of IOUS. The benefit of using IOUS for achieving maximal evacuation was assessed according to the presence of residual hemorrhage in postoperative CT or MRI compared to the preoperative radiological studies.

Ultrasound (US) equipment

A Philips ClearVue 350 ultrasonography system was used to do intraoperative US scans with active probes C5-2 convex and L12-4 linear.

Inclusion criteria

1. Surgical intracranial hematoma

2. All age groups

3. No specific gender.

Exclusion criteria

1. Previous brain surgery

2. Evident Pneumocephaly in CT brain

3. Any patient treated by any modality of radiation or chemotherapy.

Clinical presentation

Patients presented with headache, neurological deficits, seizures, or disturbed conscious level.

Investigations

Laboratory investigations

Routine laboratories were done as complete blood picture, coagulation profile, and blood chemistry.

Imaging studies

MRI and CT scans of the brain were performed on occasion, with or without intravenous contrast.

Volume measurement: For lesions (ellipsoid formula)

Utilizing the modified McDonald’s standards, the volume of the lesion was determined from the CT and MRI brain scans.

Volume = ABC/2

Indications for surgery

CT brain and MRI with the following criteria: 1. Significant mass effect by lesion (on CT or MRI) 2. Midline shift more than 5 mm 3. Doubtful diagnosis (especially in adults) 4. Evidence of significantly increased intracranial pressure.

Management

Counseling and consent

The patient was educated about the neurological condition that necessitated surgery, the purpose of the procedure, the surgical approach, what to expect after the operation, and the anticipated risks, including the percentages of mortality and morbidity. The written permission must be comprehensive.

Preoperative medications

In supratentorial lesions, the anticonvulsant phenytoin was administered at a loading dosage of 15–18 mg/kg followed by a maintenance dose of 5–8 mg/kg.

The patients who were a part of this trial were all given third-generation cephalosporin antibiotics (2 g) when the anesthesia was induced and continued to take them for a minimum of 7 days after surgery (1 g every 12 h).

Operative technique

Utilizing the L12-4 linear and C5-2 convex active probes, the operator conducted an intraoperative US utilizing a Philips ClearVue 350 ultrasonography system. The purpose of the US was to check the dimensions, relations, and echogenicity differentiation of the hematoma based on its position and depth. To ensure optimal transmission of the acoustic beam within the encased scan head and the dura mater, the transducer and cable were put in a clear plastic surgical sterile sheath. The operation region was then irrigated with sterile saline.

We determined the distance between the pathology and the dura, the precise position and dimension of the pathology, and compared them with preoperative available MRI and CT images. The sheathed scan head was positioned on the outer layer of the dura mater over the scanning before opening the dura mater. This allowed us to identify the site and size of the hematoma before any brain shift could occur as a consequence of cerebrospinal fluid drainage after dural opening.

After opening the dura, the probe tip was positioned directly on top of the brain tissue for further scanning while saline irrigation was carried out continuously.

First, the hematoma’s location, consistency, and boundaries were analyzed. Then, colored mode scanning was used to detect any surrounding vascular structures. After that, the B-mode scan was used to check for any association with nearby anatomical landmarks, such as the ventricles and the tent.

We began hematoma evacuation from the closest safe area once we collected these statistics. While the evacuation was underway, thorough scanning was carried out to assess any leftover clots and its evolving relationship to nearby structures. Once the cavity was filled with sterile saline, another scan was done to determine its size relative to the original one, following which any leftover clots were carefully removed. This was done to ensure complete evacuation.

Postoperative care

• The drains were removed 1–2 days after the operation.

• The patient was given an intravenous antibiotic course that lasted for 3 days. Following discharge, they were instructed to take an oral antibiotic for about 7 days until the sutures were removed.

• The sutures were removed 10–14 days after the procedure, and the postoperative dressings were replaced every 48 h as per routine.

Follow-up and evaluation after operation

• CT and MRI scans were performed 24–48 h after the operation as a follow-up

• The size of the pathology before and after the operation was compared

• Every patient had their evacuation recorded along with the presence or absence of residue.

CASE PRESENTATION

A 55-year-old hypertensive male patient who had received medical treatment for hepatitis C virus. He presented with a disturbed level of consciousness and right-sided heaviness for 6 h. His neurological examination showed a Glasgow Coma Scale of 12/15, left hemiparesis (motor power was grade II) associated with left facial nerve palsy of lower motor neuron lesion in nature. Urgent CT brain revealed a large left parietal hyperdense mass compressing the brain parenchyma, causing a 5 mm mid-line [Figure 1]. The patient was operated upon by urgent evacuation using the aid of IOUS, which gave a negative residue result [Figures 2 and 3]. Postoperatively, the patient’s condition improved to be fully conscious with right-sided hemiparesis, the same as preoperative motor power. Follow up CT brain revealed complete evacuation of the hematoma [Figure 4].

Figure 1:

Preoperative computed tomography of the brain showed a sizable intracranial hemorrhage with significant midline shift; its estimated volume: 80 cc.

Figure 2:

Preevacuation intraoperative ultrasonography (IOUS) image showed a hyper-echoic mass (arrows), estimated volume by IOUS 81 cc.

Figure 3:

Postevacuation i n t r a o p e r a t i v e ultrasonography image showed no residuals (arrow).

Figure 4:

Postoperative computed tomography after 24 h.

RESULTS

According to the data in the table, the participants’ ages varied from 13 to 75, and the mean age was 44. Sixty percent of the people who took part were men, and 40% were women [Table 1].

Table 1:

Summary of demographic information from the research population.

According to the data in the table, hematomas were found in the following areas: the parietal, frontal, temporal, basal ganglia, and posterior fossa in 33%, 30%, 17%, 13%, and 7% of the study group, respectively [Table 2].

Table 2:

Frequency of different hematoma sites among the study group.

The table shows that hematoma sizes ranged from 13 to 80 cc, with a standard deviation of 15.4 cc, and an average of 34.5 cc, as determined by CT/MRI. On the other hand, the US revealed an average hematoma size of 34.62 cc, with a standard deviation of 15.5 cc, falling between 12 and 81 cc [Table 3].

Table 3:

Frequency of different intraoperative hematoma sizes by CT/MRI and US among study groups.

The data in the table show that there is a notable disparity between the two radiological diagnoses of brain lesions, with a p < 0.05. The total number of negative US findings was 26, of which 8 (31%) were false negatives confirmed by postoperative CT, and 18 (69%) were true negatives [Table 4].

Table 4:

Evaluation of remaining hematoma using various radiological methods in relation to the research group.

The table illustrates that most of the patients had a good hematoma evacuation rate [Table 5].

Table 5:

Postoperative hematoma evacuation rate.

The sensitivity and specificity of US, as compared to CT, in detecting residual hematoma during surgery were found to be 91.6% and 100%, respectively, with an overall accuracy of 96% [Table 6].

Table 6:

Ultrasound sensitivity and specificity for postoperative hematoma diagnosis compared to computed tomography.

Statistical analysis

• Data were input twice into Microsoft Access after collection and coding to make manipulating information easier. Analysis was carried out utilizing the Statistical Package for the Social Sciences program version 18 on Windows 7. Paired categorical data comparing CT and ultrasound residual detection were analyzed using McNemar’s test.

• Mathematical means as a measure of central tendency and standard deviations as a measurement of dispersion for quantitative parametric data and simple percentage- and number-based descriptive analysis for qualitative information.

For qualitative data

• To contrast over two qualitative groups, the Chi-square test is used

• A novel test’s sensitivity and specificity were evaluated using the “Receiver Operating Characteristic” curve [Figure 5].

• The threshold for significance was set at a p ≤ 0.05.

Figure 5:

Receiver operating characteristic (ROC) curve for ultrasound. Blue line: ROC curve of intraoperative ultrasound, Green line: Diagonal reference line.

DISCUSSION

There has been a tremendous deal of progress in neurological imaging and surgical procedures since the beginning of neurosurgery. These days, image-guided surgery is the gold standard for neurosurgery. Operating intracranially without damaging healthy brain tissue is the goal of brain surgery. Recognizing that we are just at the beginning of the history of image guiding is critical when looking back over the past 100 years. In terms of progress toward perfect brain surgery, we have not yet arrived at the pinnacle. Much may be accomplished and understood in the years to come to improve upon the present.

Spontaneous supratentorial ICH is highly debilitating and linked to a high risk of death. The primary approach for managing this condition involves optimal medical care, focusing on controlling blood pressure and addressing clotting disorders. Many clinical studies conducted during the past decade have shed light on the benefits of surgical intervention for cerebral bleeding. The optimal surgical strategy is still up in the air, despite significant developments in emergency patient care. Surgical hematoma removal has many potential advantages, such as decreasing intracranial pressure, avoiding brain herniation and mass effect, and minimizing the excitotoxic and neurotoxic consequences of blood products. Neuroendoscopy, open craniotomy, decompressive craniectomy, and minimally invasive catheter evacuation with thrombolysis are some of the surgical techniques that have been investigated.[4]

For neurosurgical guiding, intraoperative US has been useful for over 20 years, and it continues to have many appealing features. Finding the lesion’s location and its superficial part, as well as differentiating solid tumors from cystic components, are all tasks well-suited to US.

US imaging’s pinpoint localization reduces surgical time and improves patient safety. To better localize lesions intraoperatively, delineate edges, guarantee good resection, and reduce the influence of brain shift intraoperatively, US- guided neurosurgery is used globally. In our opinion, the most significant benefit of using intraoperative sonography is the reduction of dissection and intraoperative localization times.

Neurosurgeons have enthusiastically embraced the method because of its influence, which is difficult to quantify. As a result of this acceptance, they eventually insisted on using sonographic guidance in many circumstances. Confidence in craniotomy and durotomy placement and reduction of worry about iatrogenic harm may be achieved with rapid and precise identification of impalpable disease in crucial anatomic locations. The method also helped in determining if there were any ICH residuals at the expected end of dissection; by comparing the patient’s appearance before and after evacuation, we discovered echogenic material that was compatible with residual hematoma.

To shed light on this matter, we compared the efficacy of IOUS with that of postoperative CT and MRI to determine its usefulness in directing the complete evacuation of brain hematomas and detecting any residual intraoperatively. Our research comprised 30 patients with cerebral hematomas of varying sizes that were diagnosed between July 2017 and June 2024. On average, our patients were 44.86 years old. In addition, our investigation did not encounter any instances of IOUS being used in pediatric populations. Unmyelinated, ischemic newborn brain tissue is difficult to distinguish from an acute hematoma in terms of echogenicity by ultrasonography, according to LoPresti et al., 2020, who conducted surgery on an 8-week-old neonate.[13]

We found that 33% of the instances occurred in the parietal area, 30% in the frontal area, 17% in the temporal area, 13% in the basal ganglia, and 7% in the posterior fossa, when we looked at the locations of the hemorrhages in our research group. In a study conducted by Sadahiro et al. (2015), US was found to be useful in examining the basal ganglion and other deep regions of the brain.[17]

Similarly, Liu et al., 2020, documented the use of US in the surgical management of a rare case of idiopathic spontaneous intramedullary hemorrhage, which was successfully treated with the help of US during the operation. The patient’s prognosis was positive. They also thought that surgically treating intramedullary hemorrhage might benefit from using intraoperative ultrasonography.[12]

In our series, CT scans or MRIs were done for patients. The preoperative volume was calculated according to ellipsoid formula and was documented for each patient requiring surgery and confirmed by IOUS before evacuation, Obana et al., 1991, also performed transcranial US preoperative in his study and then comparing it by intraoperative imaging which give more realistic comparison intraoperative but they did their study on neonatal brain abscesses which can be easily appreciated and assessed preoperatively by transcranial ultrasonography in this age group.[15]

In every instance of our investigation, we inserted the probe directly into the dura by a craniotomy and irrigated it continuously with saline. Results showed that intracerebral hematomas were easily visible using US-guided localization through a bayonet-shaped US probe through burr holes in the 2015 study by Shimizu et al.[19] and in the operation performed by Strowitzki et al., by US-guided burr hole aspiration. However, in two patients, aspiration was not possible due to the presence of clots.[20] We were also unable to get these probes at our institution. In contrast to the MISTIE trials, which evaluated passive evacuation methods for intracerebral hemorrhage after minimally invasive surgery with recombinant tissue plasminogen activator, we actively evacuated all patients in our series. Musa et al., 2022, noted that some devices examined thus far involve the Nico BrainPath system (Nico, Indiana, USA), the Penumbra Apollo and Artemis aspiration systems (Penumbra Inc., California, USA), and the Aurora Surgiscope (Integra LifeSciences Corp., New Jersey, USA). On the other hand, active evacuation methods entail the quick removal of the hematoma using handheld aspiration devices, endoscopic tools, or retractor systems – sometimes with imaging guidance. The bigger size of the instruments used for active evacuation makes it somewhat more invasive than the passive technique; a tiny craniotomy is typically necessary. However, this method makes the hematoma easier to see and access.[14] In their article titled “Term of Endoscopic Craniotomy,” Du et al., 2022, noted that endoscopic craniotomy with a small bone window saves money on hospitalization because it does not involve artificial materials (like artificial dura mater) that are required for the operation and does not require secondary cranioplasty.[5] While Hayashi et al., 2019, found that endoscopic surgery can improve patient prognosis, narrow window surgery can occasionally lead to a low removal rate,[8] and this may provide neurosurgeons with a constructive guideline for choosing the surgical procedure to treat ICH.

In our study, we evaluated using of IOUS during spontaneous ICH evacuation and it revealed to achieve better hematoma evacuation rate with sensitivity and specificity of US, as compared to CT, in detecting residual hematoma during surgery were found to be 91.6% and 100%, respectively, with an overall accuracy of 96%, which theoretically good for preventing the secondary ICH sequences and this consistent with the findings of the study by Sam et al. (2023), that examined the use of intraoperative US during surgery to monitor the progression and treatment of intracranial traumatic hematomas, the researchers observed that in a comparative study involving 14 patients (or 25.93%), intraoperative US was utilized to aid in hematoma removal and/or ventriculostomy. They concluded that, under the guidance of skilled surgeons, intraoperative US is an effective tool for reducing mortality rates associated with ventriculostomy and intracranial hematoma removal.[18]

While Lee and Lee, 2005, utilized IOUS in instances with basal ganglia hematoma despite brain herniation under local anesthesia, they used the IOUS guidance and urokinase irrigation, they were able to drain the hematoma through a single temporal burr hole but they aimed to hematoma reduction by 50–70% of its volume rather than radical evacuation of clots to prevent potential secondary neuronal injury and concluded that it is simple, rapid, and safe.[11] A combination of US (IOUS) through a temporal burr hole and endoscopic evacuation through a second burr hole was used by Sadahiro et al., 2015.[17] On average, 96% of the hematoma was drained during the procedure, and the volume of the hematoma before surgery was 65.2 ± 37.1 cc. The endoscope location in the core of the hematoma was identified using real-time IOUS, which allowed them to avoid brain injury and detect any remaining hematoma. Chartrain et al., 2018, used intracavitary IOUS. With an evacuation rate of 98.2%, the average preoperative hematoma volume in this research was 68.5 ± 30.5.[2] With an average residual volume of 9.72%, Kiran Kumar et al., 2020, were able to achieve full BG hematoma evacuation in 41.2% of instances with IOUS.[10]

At El Beltagy et al., 2010, in which they evaluated the use of IOUS in posterior fossa pediatric tumor excision, they had a radiologist to perform intraoperative ultrasonography before and after tumor excision.[6] Although this might improve the interpretation of echogenic pictures, it did not in our investigation; the neurosurgeon conducted the US scans independently.

This study had some limitations, such as the small sample size, the short follow-up period, and the unicentric study. Furthermore, our study lacks updated equipment and facilities. Hence, increasing the sample size, performing a multicentric study, increasing follow-up period, asking for radiologist assistance intraoperative, and widening the scope of our study to US-guided surgery would be a great nucleus for further studies in this field.

CONCLUSION

Neuro-navigation using US offers a simple, quick, and safe method of real-time imaging for a variety of neurosurgical operations. In addition to reducing the amount of brain exploration and the size of dural incisions, it also accurately localizes intracranial hematomas, which should lead to less surgical morbidity. It provides widely acknowledged instructions for conducting a radical evacuation without the need for complicated radiological equipment. With its user-friendly interface, real-time guidance, and pinpoint placement, intraoperative ultrasonography may enhance patients’ overall prognosis, boost surgical effectiveness, and reduce operation time.

Ethical approval:

The research/study was approved by the Institutional Review Board at the Faculty of Medicine, Fayoum University, number R-323, dated September 17, 2024.

Declaration of patient consent:

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient has given consent for their images and other clinical information to be reported in the journal. The patient understands that the patient’s names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship:

Nil.

Conflicts of interest:

There are no conflicts of interest.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation:

The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.

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