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Intraoperative ultrasound assistance in the resection of small, deep-seated, or ill-defined intracerebral lesions

WANG, Yi-da; WANG, Yi; MAO, Ying; WANG, Yong; ZEE, Chi-Shing

doi: 10.3760/cma.j.issn.0366-6999.2011.20.018
Original article

Background Intraoperative ultrasound (IOUS) has been increasingly used as a guiding tool during neurosurgical procedures. In this study, we aimed to evaluate the potential application of intraoperative ultrasound assisted surgery in the resection of small, deep-seated, or ill-defined lesions.

Methods Eighty-six consecutive patients with small, deep-seated, or ill-defined intracerebral lesions were studied prospectively. An improved intraoperative imaging technique and surgical setup were practiced during the surgery. IOUS was performed in three orthogonal imaging planes (horizontal, coronal and sagittal).

Results Histopathological diagnoses of these 86 cases included cavernomas, metastases, hemangioblastomas, gliomas, and radiation necrosis. Forty-seven of the 86 lesions (54.7%) were small and deep-seated, 34/86 (39.5%) were ill-defined, and 5/86 (5.8%) were small, deep-seated, and ill-defined. Sonograms in the horizontal plane were obtained in all 86 cases. Sonograms in the sagittal plane and in the coronal plane were obtained only in 52 cases and in 46 cases, respectively, due to technical limitation. In 13 cases, sonograms in all three orthogonal planes were available. All lesions were successfully identified and localized by IOUS. Total resection was performed in 67 lesions (77.9%) and partial resection was performed in 19 lesions (22.1%).

Conclusions We propose IOUS to be performed in three orthogonal planes when surgery is planned for small, deep-seated, or ill-defined brain lesions. By applying this simple, improved technique, surgeons can perform resection of these lesions precisely.

Department of Ultrasound (Wang YD, Wang Y and Wang Y), Department of Neurosurgery (Mao Y), Huashan Hospital Affiliated to Fudan University, Shanghai 200040, China

Department of Radiology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90089, USA (Zee CS)

Correspondence to: WANG Yi, Department of Ultrasound, Huashan Hospital Affiliated to Fudan University, No. 12, Middle Urumqi Road, Shanghai 200040, China (Email:

(Received December 26, 2010)

Edited by Wang De

It is generally accepted that in the management of brain lesions the optimal results may be obtained when maximal surgical resection is achieved with minimal disturbance of neurological function.1-9 To achieve this goal, accurate localization and precise delineation of tumor margins are required. Computerized tomography (CT) and magnetic resonance (MR) imaging can readily localize and delineate these lesions at the preoperative stage. However, the use of intraoperative CT or MR during brain tumor resection is not always feasible. Although intraoperative MR (iMR) imaging has been proven to be more precise than 2D ultrasound, especially in detecting small tumor remnants, this modality is expensive and available in only a few centers. These factors likely contribute to their lack of routine use.10-16 Frame-based and frameless stereotactic preoperative data-based techniques, also called neuronavigation systems, are routinely used to help surgeons plan the site of craniotomy and identify critical structures, but these systems have inherent problems related to loss of accuracy resulting from unpredictable distortions, shifts and deformations after craniotomy and tissue removal.17-20

Ultrasonography (US) has been employed as a guide and diagnostic tool in neurosurgery practice in its present form since 1980s.21 As US can offer real-time imaging and the transducer itself always serves as a frame of reference, intraoperative ultrasound (IOUS) has been frequently reported to be successful in assisting tumor localization, resection control, image-guided biopsies, vascular imaging, and spinal procedures.21-29 Despite these advantages, however, IOUS still has its limitations. Surgeons complain that the ultrasonograms are hard to interpret, and the inability to demonstrate precise spatial localization can be confusing during surgery. Perhaps these problems are not remarkable when we are dealing with superficial subcortical tumors. When the resection of small, deep-seated, or ill-defined lesions is contemplated, these limitations appear to be drastically magnified. According to our neurosurgical practice experience, we find that high quality ultrasound images in orthogonal imaging planes may be the appropriate approach to solve this problem. Proper procedure in performing IOUS appears to be important in maintaining good image quality. The value of IOUS in guiding lesion resection may be enhanced when preoperative imaging data are available for comparison. In this prospective study, we intended to describe our experience of IOUS in the treatment of small, deep-seated, or ill defined lesions.

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We prospectively studied patients with intracerebral lesions scheduled for surgical treatment in our neurosurgery centers from July 2006 to June 2008. Intracerebral lesions must meet one or both of the following criteria to be selected into this study: A. small in size and deep in depth, i.e. lesion's depth-size index value more than 1.0. In order to preset objective eligible criteria, we define the ratio of tumor depth from the cortical surface (measure by US in millimeters, mm) to tumor maximal diameter (measure by US in mm) as “depth-size index”, which is sensitive and convenient in selecting valid cases. B. ill-defined tumor margins in US imaging and/or in MR imaging, namely tumor margins could not be visualized or separated from the surrounding tissue. Patients who harbored more than one brain lesion were excluded from our study.

CT and MR imaging was preformed in all cases at the preoperative stage. All patients had MR imaging with intravenous administration of gadolinium contrast agent performed within 5 days of the operation.

This study was approved by the Human Investigation Committee at our university and hospital, and written informed consent to use IOUS was obtained from all patients or their guardians in advance.

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During surgery, all IOUS were done with the same machine (ALOKA SSD-4000 scanner and a 3.5-7.5 MHz convex intraoperative probe with surface dimensions of nearly 20 mm × 12 mm). Visual images of the entire examination were continuously recorded on a hard disk in a Digital Imaging and Communication in Medicine (DICOM) movie format. For sterile usage, the transducer and its cord were covered with a sterile, translucent, disposable plastic sheath.

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Standard plane sonogram

The patient's position and operative field were tailored to make it possible to obtain IOUS in three orthogonal planes (horizontal, sagittal, and coronal). The site of the craniotomy was planned according to preoperative CT and MR data or with the assistance of neuronavigation if necessary. However, alternative techniques for improving quality of ultrasound images, including enlarging craniotomy size or making a second craniotomy site for US probe, were not adopted.

Immediately following craniotomy and before opening of the dura, an IOUS was performed in two or three orthogonal planes to obtain an overall view of the brain and skull. A low-MHz frequency preset was used, usually 3.5 MHz. Depending on the tumor site and operative field, not all three orthogonal planes were obtained in all cases, but at least two perpendicular standard planes were acquired. Intracranial normal anatomic structures, such as the lateral ventricles, corpus callosum, choroid plexus, and brain stem could be clearly identified in these images.

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Tumor localization and resection control

After identifying readily visible important structures, probe frequency was changed to maximize tumor resolution and margin identification. Tumor localization was determined by two perpendicular projection sections. After dural opening, IOUS was performed again to confirm localization. Tumor size, shape and its relationship to normal structures were compared with preoperative MR images. For some lesions which were located deeply in the eloquent area of the brain, a surgical approach was designed to avoid damage to surrounding important structures, thus the direction and depth of the surgical approach was guided by the placement of a Fogarthy catheter under IOUS. Reverberation caused by the catheter tip could be used as a target.

During surgery, IOUS was used repeatedly when needed. A final IOUS assessment was made when surgeons felt that the tumor was completely excised to exclude the presence of residual tumor.

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During July 2007 and June 2008, a total of 86 patients (between 7 and 78 years of age, 42.0±16.4 years) from among 586 consecutive patients who had undergone surgery for removal of brain lesions at our institution were eligible to be selected for our study. There were 52 males (60.5%) and 34 females (39.5%). Seizures, motor deficits, loss of the visual field and cranial nerve dysfunctions were the most common clinical symptoms. Histopathological diagnoses included 26 cavernomas, 11 metastases (including primary lung, breast, colon cancer and lymphoma), 2 hemangioblastomas, 43 gliomas, and 4 radiation necrosis. Baseline data of these patients are listed in Table 1. Of the 86 lesions, 47 lesions (54.7%) met criterion A, 34 lesions (39.5%) met criterion B, and 5 lesions (5.8%) met both two criteria to be selected for this study.

Table 1

Table 1

Over a 1-year-follow-up period, no death or intracranial hematoma or intracranial infection cases were reported in any of the 86 cases. Other adverse effects, including pulmonary infection, gastrointestinal hemorrhage, seizure disorder which had no relation to IOUS application, were not summarized in this study.

All lesions were hyperechoic in relation to normal brain. Low grade gliomas and cavernomas usually exhibited homogenous hyperechoic pattern, while high grade gliomas and metastases exhibited a non-homogenous hyperechoic pattern with hypoechoic areas of necrosis and cystic degeneration. There was no specific echogenic patterns identified that correlated with histopathological types. Satisfactory localization was achieved by IOUS in 75 lesions. The remaining 11 lesions, including 4 radiation necrosis lesions, 5 glioblastomas, and 2 low grade gliomas, were poorly localized; the location of the tumor was not well visualized by IOUS (Table 2).

Table 2

Table 2

For lesions fulfilling criterion A, a total resection was achieved in 42 cases, 36 of which were confirmed by intraoperative microscopic examination, and a subtotal resection was achieved in the remaining 6 cases. Among them, two were decided by surgeons before the operation because the lesions were located adjacent to or had invaded into the eloquent area. And in the other four cases, small unexpected remnants of lesions were detected by postoperative MR imaging one day after surgery. For tumors fulfilling criterion B, total resection was achieved in 21 cases, 15 of which were confirmed by microscopic examination, and subtotal resection was achieved in the remaining 13 cases; 8 residual lesions were intended by surgeons and in the other 7 cases remnants were revealed at follow-up MRI performed one day after surgery. For tumors fulfilling both criteria, total resection was achieved in 4 cases, 3 of which were confirmed by microscopic examination, and subtotal resection was achieved in the remaining case as planned by the neurosurgeon.

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Results of IOUS

Transverse plane sonograms were obtained in all 86 cases, sagittal plane sonograms were obtained in 52 cases, and coronal plane sonograms were obtained in 46 cases. In 13 cases, images were available in all three orthogonal planes. We found the ability of IOUS to obtain orthogonal plane sonograms was largely dependent on the location of the lesion.

As our study results showed, the transverse or horizontal plane was the most useful in IOUS practice. In order to get the transverse plane sonogram, the probe should be placed directly on the dura or cortical surface parallel to the patient's transverse plane. A series of images at different levels of the brain could be obtained (Figure 1). Hyperechoic skull, linear hyperechoic cerebral falx and anechoic lateral ventricle were prominent features and readily visible on these images.

Figure 1. A:

Figure 1. A:

After obtaining transverse plane images, the probe was rotated 90 degrees to obtain sagittal or coronal plane images. Median sagittal plane images were seldom obtained because craniotomy sites were rarely at the midline. Parasagittal images in the sagittal plane were frequently obtained. In these images, corpus callosum, choroid plexus, ventricles and cingulate gyrus were readily visible (Figure 2). Coronal images were also featured by the ventricular system, and the base of skull can be seen in sonograms (Figure 3).

Figure 2.

Figure 2.

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Illustrative cases

Case 1

This case involved a 32 years old man who complained of twitching of the extremities for one month and altered consciousness. MR imaging demonstrated a small T2 hypointense mass in the left hippocampus (Figure 4).

The patient subsequently underwent a left temporal craniotomy. Because of its small size, deep-location and ill-defined features, the neuronavigator system was employed to assist in the planning of the craniotomy site. After craniotomy, a transverse plane sonogram at the level of the brain stem was quickly obtained. Surgeons and radiologists had difficulty in localizing the tumor on the US monitor, and because of the brain shift and distortion following dura opening, the neuronavigation system based on preoperative data was not reliable. Fortunately, after referring to preoperative MR images, we realized that this hippocampal tumor was located approximately 1.5 cm to the left of the brainstem (Figure 2). Using this information and real-time standard transverse plane images, we were able to locate the slightly hyperechoic mass on ultrasound. Its maximal diameter was just 7 mm, and depth from cortical surface 32 mm, so the depth-size index was nearly 4.6. Subsequently, with real-time IOUS, surgeons completed the resection of tumor within 30 minutes. Pathological examination confirmed resection of a grade II astrocytoma.

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Case 2

A 35 years old man experienced headache for two months and an MRI examination demonstrated a T2 abnormal signal lesion with ill-defined margins in the left frontal lobe, near the cerebral falx. The patient subsequently underwent a left frontoparietal craniotomy. IOUS localized the lesion after the craniotomy. As shown in Figure 5, this mass appeared hyperechoic with similar echogenicity as the surrounding edema and normal tissue, so IOUS imaging could not precisely outline the tumor margin. However, IOUS provided higher resolution images when compared to MR images. More details were identified on sonogram; such as callosal sulcus, cingulate sulcus and cingulate gyrus. In addition, IOUS confirmed this lesion had invaded the cingulate gyrus which could not be identified by MR.

Both MR and US demonstrated this lesion just beneath the motor area, which made surgeons choose an indirect approach in order to avoid unnecessary damage to the precentral gyrus. The extent of tumor resection was determined by surgeons and guided by IOUS with the preservation of the cingulate gyrus. Histopathological diagnosis showed a grade II astrocytoma. Postoperative MR proved residual tumor in the cingulate gyrus as determined by IOUS.

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Small, deep-seated, ill-defined brain lesions pose enormous challenges to neurosurgeons. The extent of surgical resection of these lesions is largely limited by the surgeon's ability to localize tumors not seen on the surface, define their margins and differentiate residual tumors from normal brain. Maximal resection of tumor and minimal damage to normal tissue offer the patient an improved quality of life, prolonged survival, and improved control of neurological problems. In this prospective study of 86 patients, we propose to use a novel IOUS technique to obtain orthogonal plane images of high quality and investigate the benefit it will bring to brain surgery.

IOUS application in neurosurgery practice can be traced back to 1966, when Dyck et al4 reported that A-mode echoencephalography was useful in delineation of intracerebral mass lesions. Its application in its present form began with the preliminary report of Rubin et al21 in 1980. Since then, IOUS has become an important tool in brain surgery. Many investigators have demonstrated its benefits during neurosurgical procedures. Among these studies, some stressed the usefulness of IOUS in tumor localization, margin detection, tumor resection control, and residual tumor identification.4,21,23-25,27-29,32 Others emphasized comparing IOUS findings with pre- or post-operative imaging results.2,14,16,22,26,30,31 Although all these studies have confirmed the definite advantages of IOUS in brain surgery, many surgeons were frustrated when employing IOUS as a guidance tool during surgery: insufficient image quality and difficulty in interpreting oblique plane images, especially when dealing with small and deep-seated brain tumors. As far as we know, there are few articles dealing with improving IOUS image quality and setting standard IOUS orthogonal planes in guiding the procedures.4,35-37 Our study was intended to deal with this issue.

As this study results show, we can plan the patient position and craniotomy site before surgery, and IOUS imaging plane directions should be considered in the planning. Subsequent IOUS can easily be obtained in orthogonal planes after craniotomy by placing the probe directly on the dura or cortex. A low frequency probe, usually 3.5 MHz, is ideal to get a full view of brain and skull images. This scanning approach is feasible because at least two perpendicular imaging planes were performed in all 86 patients in our study. Once the US scanner is adjusted in the proper settings, even second-line devices (ALOKA, SSD-4000 in this study) can provide high quality sonograms in the operating room. It is true that most operating rooms are using second-line, often out-of-date machines that have been discarded by radiology department. Although the use of out-of-dated equipment is not to be encouraged, our study results show the feasibility and usefulness of such machines for IOUS in neurosurgery.

The high quality of orthogonal plane sonograms obtained during brain surgery proves that IOUS can provide useful information for surgeons during the operation. Considering that all images are in real time and US probes are inherently stereotactic, IOUS also has some definite advantages over intraoperative MR imaging. The ability to depict real-time anatomical data during a surgical procedure can affect surgical decision making and allow one to localize and characterize brain lesions just as Case 1 shows.

Some anatomic structures are easy to recognize in standard plane sonograms; such as cerebral and cerebellar falx, lateral ventricles, corpus callosum, choroid plexus, brain stem, and bones of the skull. Using these anatomic structures as a “beacon” and with a little practice, neurosurgeons will find it easy to interpret US images even if they have limited knowledge of ultrasound. Furthermore, as Case 2 shows, IOUS may have better resolution than MR imaging in some cases. The more details IOUS can provide, the better the surgeons can precisely determine the extent of resection, avoiding damage to eloquent areas of the brain.

This study was designed to evaluate the potential of IOUS utilization in small, deep-seated, or ill-defined lesions. Our results show that these two kinds of lesions represent nearly one seventh (86/586) of neurosurgery daily operative patients. Cavernomas and metastases were usually small (24/26, 92%) and deep-seated (11/11, 100%) in this study that made the operation difficult to perform even with intraoperative guidance tools. Trying combined use of IOUS with preoperative MR imaging may be a feasible solution in this situation, just as Case 1 shows. This method may be useful not only in tumor localization, but also very helpful whenever surgeons or radiologists feel unsure about tumor margins, extent of resection, or residual tumor.

Ill-defined tumor is another challenging brain lesion for surgeons. Glioblastomas, low grade gliomas, and radiation related necrosis in this study, 17/17 (100%), 11/17 (64.1%) and 4/4 (100%), respectively, tended to exhibit such characteristic. We did not strictly compare the IOUS characteristics of these lesions with preoperative imaging, thus the correlation between these different imaging techniques is not quite clear. But reportedly, IOUS delineates both gilomas and their transition toward normal tissue regardless of their CT or MR imaging patterns.30-32 IOUS can also differentiate edema from solid tumor and normal brain, while CT and MR imaging cannot.33,34 In this study, we also found that IOUS can provide higher resolution images than MR and thus delineate more anatomical details; as shown in Case 2. With IOUS, surgeons can control their resection of tumor in a more precise manner, which is more helpful when they deal with some unresectable or ill-defined tumors.

While our study shows a promising result of the IOUS application in neurosurgery before lesion resection, we acknowledge that there are still some limitations to this imaging modality for the detection of residual tumor. Most studies have reported that IOUS imaging for the detection of residual tumor towards the end of the operation was unreliable. The main problem is that surgeons or radiologists may interpret blood clots, which appear as hyperechoic band on US images, as residual tumor. During our study, we also confronted such a situation in some cases. Among the four unexpected subtotal resection cases, three were caused by the radiologists misinterpreting remnants as blood clots, accounting for 3.4% of the 86 cases. We argue that currently this problem has no suitable solution by IOUS itself. Differentiation between remnants and blood clots on sonogram may be experience-dependent and its difficulty varies in different cases. Another fact is that sound waves traversing a cyst cavity have less attenuation than those traversing solid tissue, which may cause so-called a “posterior enhancement” phenomenon. Therefore, a hyperechoic rim presents on the far side of the cystic cavity. This complication may contribute to the false positive result of IOUS in determining residual tumor. We also confronted this problem when we conducted this study. We tried to solve this problem as Cases 1 and 2 showed, by using standard orthogonal plane sonograms obtained intraoperatively and comparing these with preoperative imaging data. The relationship and spatial orientation of brain lesions to normal structures can be defined, thus the extent and margin of the lesion can be determined. However, this solution is not precise for it is dependent on preoperative data, and the surgical procedure may cause unpredictable distortions, shifts and deformations of brain tissues. At present, the optimal method of estimating residual tumor is intraoperative MR imaging. But it is not always feasible because of its huge expense and extensive requirement for operating room. We predict that some newly developed techniques in US imaging, such as contrast agent or elastosonography, may improve the ability of IOUS in determining the residual tumor when resection is under way.

Another limitation of our study is that there is no control group in our study. However, it seems clear that the surgical results from the current study are better when compared to the results obtained prior to applying IOUS.

In conclusion, by applying this improved technique for IOUS, high quality US images in two or more orthogonal planes obtained intraoperatively are useful in guiding resection of small, deep-seated, or ill defined brain lesions.

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brain neoplasms; neurosurgery; intraoperative ultrasound; magnetic resonance imaging

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