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Table of Contents
ORIGINAL ARTICLE
Year : 2020  |  Volume : 17  |  Issue : 4  |  Page : 246-251

Intraoperative ultrasound in neurosurgical procedures


1 Department of Neurosurgery, Narayana Medical College, Nellore, Andhra Pradesh, India
2 Department of Anaethesia and Critical Care, Balaji Institute of Orthopedic Research and Rehabilitation for the Disabled, BIRRD (T) Hospital, Tirupati, Andhra Pradesh, India
3 Department of Community Medicine, MGM Medical College and LSK Hospital, Kishanganj, Bihar, India
4 Department of Radiology, Narayana Medical College, Nellore, Andhra Pradesh, India

Date of Submission06-Jun-2020
Date of Acceptance05-Oct-2020
Date of Web Publication24-Nov-2020

Correspondence Address:
Dr. N A Sai Kiran
Department of Neurosurgery, Narayana Medical College, Nellore, Andhra Pradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/am.am_49_20

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  Abstract 


Introduction: The objective of the present study was to study the utility and the effectiveness of intraoperative ultrasound in neurosurgical procedures and to assess the outcome. Material and Methods: In this prospective study, operative procedures by a single surgeon under intraoperative ultrasound localization for basal ganglia/thalamic haematoma or traumatic brain contusions or brain tumours were included. Ultrasound scanning of the brain was performed before and after the excision of the lesion and during the procedure to verify the extent of removal of the lesion. Results: 74 patients underwent surgery for brain tumor/basal ganglia bleed/head injury with hemorrhagic contusion with the help of intraoperative ultrasound. Gross tumor resection was noted in 25 out of 36 cases of brain tumors (69.44%), complete evacuation of hematoma was noted in 14 out of 34 cases(41.2%) of basal ganglia bleed and in 2 out of 4 cases (50%) of intracerebral contusion. As per Modified Rankin scale (MRS)score, among the brain tumor cases, all patients had fared well in recovery and had better MRS scores except in one patient who expired during postoperative period. Conclusions: IoUS is a widely accessible, cheap, portable and less space occupying and reliable imaging tool to follow and modify the surgical plan in real time, and is more accurate and helpful in complete tumor resection, evacuation of intracerebral bleeds and contusions, and biopsy of deep seated lesions. It is easy and safe to handle with no risk of radiation.

Keywords: Basal ganglia bleed, brain tumor, head injury with brain contusion, intraoperative ultrasound, modified Rankin scale


How to cite this article:
Kumar V A, Kiran N A, Kumari B G, Pal R, Reddy V U, Agrawal A. Intraoperative ultrasound in neurosurgical procedures. Apollo Med 2020;17:246-51

How to cite this URL:
Kumar V A, Kiran N A, Kumari B G, Pal R, Reddy V U, Agrawal A. Intraoperative ultrasound in neurosurgical procedures. Apollo Med [serial online] 2020 [cited 2021 May 14];17:246-51. Available from: https://www.apollomedicine.org/text.asp?2020/17/4/246/301473




  Introduction Top


Intraoperative ultrasound (IoUS) has significant consequences on the outcome of both adult and pediatric neurosurgical patients. It is a great boon to the neurosurgeons as it is useful to localize and precisely excise the pathological lesions during intraoperative period in intracranial surgeries. It helps in foreseeing of surgical path for precise excision of pathological lesions and allows a real-time localization and visualization of any residual tumor mass while operating on any kind of central nervous system (CNS) lesions, even after brain shift and deformation have occurred, and where traditional navigation systems such as computed tomography (CT) scan and magnetic resonance imaging (MRI) have lost accuracy.[1],[2] It helps follow and/or plan the progression of tumor excision with accuracy and ease of use.[3],[4],[5],[6],[7],[8] The objective of the study is to study the utility and the effectiveness of IoUS in neurosurgical procedures and to assess the outcome.


  Materials and Methods Top


This prospective study was conducted from September 2016 to November 2018 in the Department of Neurosurgery in a tertiary care hospital after approval from the institutional ethical committee. All the participants consenting for operative procedures under IoUS localization for basal ganglia/thalamic hematoma, traumatic brain injury (TBI) with contusions, and brain tumors were included in the study. All the patients fitting into the criteria included in the study were operated by a single surgeon with the use of IoUS localization (Hitachi Healthcare's Aloka Prosound Alpha 7 IoUS using standard abdominal convex phased-array probe and with 5 MHz, 7.5 MHz transducer frequencies). B-mode (grey scale) ultrasound is used for the localization of the site, extent, depth, and structure of the lesion.[9] The data were collected with the help of a pretested, structured interview schedule, which contained the demographic and clinical features including age, gender, diagnosis, surgical procedure, and details of vital parameters, Glasgow coma scale (GCS) at admission and discharge, noninvasive investigations including imaging such as preoperative CT/MRI volume and postoperative CT/MRI volume, and outcome using modified Rankin scale (MRS) at discharge. Management and outcome details for all the patients were noted. During surgery after the craniotomy, the probe was placed gently above the dura after pouring of normal saline over the brain surface and the lesion is localized by IoUS for its location, anatomical margins, depth, and extent by sterile ultrasound probe, and it is intermittently checked for the extent of surgical removal of lesion till the maximum possible/complete removal of lesion is done.

Postoperatively, each patient was taken for CT brain as early as possible and assessed for residual lesion or any new evolved bleed in the scan. The volume of the lesion/bleed is noted from both preoperative CT/MRI and postoperative CT by measuring its length (l), breadth (b), and height (h) and calculated by the formula (lxbxh)/2. The clinical outcome of the patient after the proposed intervention was assessed by comparing the MRS at admission and at discharge which measures the degree of disability/dependence. Following approval from the institutional ethics committee, written informed consent was obtained from all the participants. Standard surgical procedure was followed, including patient positioning, localization, and surgical approach were identical as per standard operative procedures practiced in our center. The data were entered into MS Excel and interpretation was done using statistical software SPSS Statistics Version 24.0 (IBM SPSS Statistics for Windows, Version 24.0. Armonk, NY: IBM Corp). The data were expressed using descriptive statistics such as mean and standard deviation for continuous variables and frequency and percentage for categorical variables. Chi-square test was used for significance of categorical data at 5% level of statistical significance.


  Results Top


Out of a total of 74 patients who were admitted and underwent surgery for brain tumor/basal ganglia bleed/head injury with hemorrhagic contusion, there were 25 females and 49 males. Among these, 34 patients had basal ganglia bleed, 36 patients had brain tumor, and 4 had TBI with contusion. MR scale at admission was 5 in 40 patients, 4 in 8 patients, 3 in 2 patients, 2 in 2 patients, and 1 in 20 patients. At the time of discharge, twenty seven patients had MRS score 1, twelve patients had MRS 6, eleven patients had MRS 5, fifteen had MRS 4, four patients had MRS 3, and five patients had MRS 2. Among the subtypes, in basal ganglia bleed cases, ten patients had MRS 6, eight patients had MRS 5, twelve had MRS 4, one had MRS 3, one had MRS 2, and one had MRS 1. Among the brain tumor cases, one had MRS 6, two patients had MRS 5, three had MRS 4, three had MRS 3, four had MRS 2, and twenty three had MRS 1. Among the head injury with contusion cases, one had MRS 6, one had MRS 5, and two had MRS 1.

As per MR scale, among the brain tumor cases, all patients had fared well in recovery and had better MRS scores except in one patient who expired during postoperative period. In basal ganglia bleed cases, 16 patients had fared well and had better MRS score and 10 patients with poor GCS at admission expired and others had same MRS. Among the traumatic contusion cases, one patient had expired and others had same MRS score. Residual tumor/bleed was seen in 35 patients and no tumor or bleed was seen in 39 postoperative patients. Among the subtype, gross tumor resection was noted in 25 out of 36 cases of brain tumors (69.44%) and residual tumor was noted in 11 cases (30.56%) and the percentage of residual tumor volume ranged from 0% to 48.5% and the mean of the percentage of the residual volume was 8.52. Among the basal ganglia bleed cases, complete evacuation of hematoma was noted in 14 cases (41.2%) and residual bleed in 20 cases (58.8%), and the percentage of residual volume ranged from 0% to 44.3% and the mean of the percentage of the residual volume was 9.72. Among the four patients with head injury with intracerebral contusion, complete removal of contusion was done in 2 cases (50%) and residual contusion was noted in 2 cases (50%); the percentage of residual volume of contusion ranged from 0% to 26.6% and the mean of the percentage of the residual volume was 10.5%.


  Discussion Top


IoUS is useful in providing real-time intraoperative information such as the location, size of tumor/bleed, and residual tumor/bleed during cranial surgeries. The exact identification of anatomical landmarks and their variants, localization and portrayal of the extent of lesions, and foreseeing of surgical procedures to optimize surgical access and enhanced dexterity are critical in the planning and execution of any surgical procedure.[10] IoUS effectively detects deeply or superficially placed brain and spinal cord lesions.[11],[12] It had recently gained popularity in neurosurgery, after a series of publications have demonstrated that this method is safe and effective, especially when used with contrast medium (contrast-enhanced ultrasound (CEUS).[11],[12],[13],[14],[15]

IoUS is cost-effective and gives precise location of a lesion when compared to other imaging modalities, but it requires training for orientation. For this limitation, clubbing it with preoperative MRI was proposed.[16] Though preoperative MRI and/or CT gives accurate preoperative localization of the lesion, intraoperative MRI or USG is required for correct localization during surgery to avoid the brain shift. Among all the three, IOUS is cost-effective, but it does not match the routine orthogonal planes of MRI or CT images, and therefore less impressive to the neurosurgeon.[3],[17],[18] Due to these problems, IoUS was connected with other navigation modalities and is used during surgery with commercially available systems.[19] In this, an arbitrary ultrasound system is connected to a navigation system via a calibration procedure of the ultrasonography probe or scan plane.[20],[21],[22] Many imaging techniques are available to acquire baseline images; the frequently used are CT and MRI, but nowadays, other modalities are also being used, from preoperatively acquired metabolic imaging, as in the case of positron emission tomography, to intraoperatively acquired ultrasound (IoUS) and immunofluorescence, based on 5-aminolevulinic acid or indocyanine green.[23],[24],[25],[26],[27]

The microsurgical treatment of hypertensive basal ganglia hemorrhage [Figure 1] assisted by IoUS localization improved the precision of the operation, better evacuation of the hemorrhage, and decreased number of reoccurrences, as well as improved the quality of life of patients after the operation.[28] Few articles had mentioned regarding the detection of intracerebral hematomas and contusions causing mass effect and midline shifts with the help of a low frequency ultrasound probe through the temporal bone of an intact skull.[29],[30],[31],[32],[33] This can also be used bedside in decompressive craniectomy patients.[34],[35],[36] The quality of the image is good, and the accuracy is not reduced by dural grafts. A better knowledge of the brain parenchyma can be obtained, and specially, when massive intraoperative brain herniation is encountered, IoUS can be useful for differentiating various ipsilateral pathologies requiring surgery, such as intracerebral hematoma or sub dural hematoma with severe brain swelling. This also lessens the time and effort needed for imaging compared to the time required for surgical wound closure, transporting to CT room for a postoperative CT scan, and thus lessens the decision-making time and also the risk of patient getting worse during shifting.[37]
Figure 1: (a) The T2-weighted axial and (b) T2-weighted sagittal postgadolinium magnetic resonance imaging scan of left parasagittal high grade glioma, showing mixed intensity lesion with central moderate intense solid lesion (small arrow) and peripheral hyperintense cystic component (large arrow) and (c) intraoperative ultrasound done after opening the dura, showing hyperechoic solid component (s) with surrouding hypoechoic cystic (cy) collection

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The applications of IoUS related to intracranial space-occupying lesions were due to the ability to demonstrate several aspects of solid and cystic lesions, including septated fluid collections, areas of thick septations, nodularity, and solid components.[10] IoUS imaging using navigated intraoperative three-dimensional–ultrasound (3DUS) for brain glioma surgeries is well documented in the literature[38] Best results in the treatment of CNS tumors is possible only by gross total resection (GTR) with postoperative adjuvant chemoradiation, which depends on the surgeon's capacity to accurately delineate intraoperative tumor margins and its characteristics[3],[5],[7] This reduces further neurological damage leading to better outcomes in these patients.[7],[8],[39] Safe resection of CNS tumors have good clinical outcomes in both adults and children.

When attempting GTR, we demonstrated a 69.44% GTR rate (25 out of 36 cases of brain tumors) in our study. In our study, awake craniotomy and excision of the lesion with IoUS localization was done in 5 out of 34 brain tumor cases and IOUS helped in early localization and speedy removal of the tumor. IOUS usefulness in both adult and pediatric CNS tumor surgery in achieving a successful GTR, and in improving surgical outcomes is well supported in many articles. However, further studies are a need of the hour to showcase the existing limitations in order to improve the efficacy and its definitive role as an intraoperative imaging modality.[40] For still better results, other modalities such as intraoperative fluorescein imaging can be used simultaneously, mainly in high-grade gliomas. Šteňo et al. suggested an additional benefit of 3DUS over conventional navigation, especially in resections of eloquent low-grade glioma.[41] Metastatic tumors often have well-demarcated borders with the surrounding brain parenchyma, and this helps in en bloc resection with good outcomes.[42] Cerebral lesions appear hyperechoic and homogeneous with well-defined borders on IOUS as compared with normal brain parenchyma. High-grade lesions (i.e., gliomas) show a nonhomogenous hyperechoic pattern consistent with necrotic areas and hypo-echoic areas consistent with cystic degeneration [Figure 2]. Hemorrhagic areas within the lesions appear intensely hyperechoic, and low-grade tumors appear hyperechoic and more homogenous.[5] Several studies had mentioned that the margins of parenchymal brain tumors can be readily differentiated from surrounding brain.[6],[7] As per few studies. ultrasound can help differentiate cerebral oedema from solid tumor. which is difficult on both CT and MRI.[43] Hammoud et al. stated that the IoUS could clearly define tumor margins in majority except in cases where the patient received radiotherapy.[3]
Figure 2: (a) The T2-weighted sagittal and (b) T2-weighted sagittal postgadolinium magnetic resonance imaging scan of cerebellar hemangioblastoma, showing mixed intensity lesion with central hyperintensity and peripheral hypointensity (c) Intraoperative ultrasound done after opening the dura, showing hyperechoic mural nodule (m) with hypoechoic cystic (cy) collection surrounding the mural nodule. Well defined tumor margin is seen (arrow head)

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At present, the gold standard to estimate the residual tumor is MRI; however, Hammoud et al.[3] showed that post tumor excision volumes can be defined in many tumors with intraoperative ultrasound as well. However, intraoperative ultrasound in patients who had radiation-induced lesions.[3] As per our study using postoperative CT scan for measuring post excision tumor values, we were successful in complete excision of 24 out of 36 cases (66.6%) of cases, and there was a gross reduction in tumor volumes postoperatively even in remaining cases. In our study, IoUS was able to define the extent of resection quite well in 14 patients with gliomas, three patients with tuberculoms, four patients with metastasis, seven patients with meningioma, 4 cases of cerebellopontine angle schwannomas, and 1 case each of cerebellar hemangioblastoma [Figure 3] and cavernoma. However, the extent of resection was poorly defined in a case of recurrent glioma which had undergone radiotherapy after the first surgery and in a case of thalamic primitive neurectodermal tumor, where the tumor was diffuse.
Figure 3: (a) Computed tomography axial image showing acute left basal ganglia bleed (h) with mass effect and midline shift (large arrow) (b) Intraoperative ultrasound image showing hyperechoic bleed (h)

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Advantages

IoUS clearly defines the tumor margins and facilitates the tumor resection in both adult and pediatric patient populations.[3],[5],[44],[45] It improves the extent of resection of intraparenchymal brain tumors.[5] Furthermore, early tumor-bed hematomas can be recognizes as these have a characteristic appearance on ultrasound.[46],[47] It does not require any changes in patient positioning or the intraoperative setting, while at the same time offers significant spatial and temporal resolution.[48] Although conventional USG machines have limited role in planning the craniotomy, transcranial ultrasound can help identify brain tumors through areas of thin skull bones.[49],[50] Being a real-time imaging modality, IoUS has the advantage over other preoperative imaging modalities, to take into account intraoperative changes, therefore it appears to be a reliable tool for image-guided spine surgery as well (for intradural pathologies and to localize and visualize nonintradural pathologies). As a diagnostic tool, IoUS can provide relatively sensitive images of the brain. Accurate descriptions of sonographic features of cerebral anatomy are available in the literature.[37] The IoUS is a real-time modality, that facilitates immediate real-time correction of the trajectory to deep-seated lesions. This simplifies guidance towards the lesions and biopsy relatively biopsy and obviates the need for additional frame of reference relatively redundant.[47]

In summary, IOUS is a real-time, relatively cheap tool for localizing and defining the margins of the deep seated and can help determine the extent of maximal surgical resection, and for assessing the tumor volumes, and for detecting residual tumor[3],[5],[7],[51] In intracerebral hematomas, IoUS provides accurate information about the location, volume, and distance of the hematoma from the cortex, through the use of high echogenic area ultrasonic imaging[28] As it was possible to select the optimal route of approach to the hematoma, and identify the responsible artery for the hematoma, hemostasis has become more reliable, allowing the hematoma to be almost entirely evacuated.[28] It also proved effective at locating irregular hematomas, which otherwise become difficult to locate, with the procedure causing minimal brain damage, along with an increased rate of evacuation compared with the traditional method.[52] This is portable and not operation theatre specific. There is no radiation as compared to intraoperative CT Scan and it saves time when compared to Intraoperative MRI. During IOUS, there will be less patient fatigue. This is less space-occupying and easier to incorporate into existing operation theatres.

Limitations

IoUS overcomes several limitations of conventional intraoperative navigation systems, which rely upon preoperatively acquired imaging data sets. The major factors that limit the usage of IoUS are the efficiency of the performing surgeon (operator dependent) which in turn depends on one's learning curve, which enhances its utility in various neurosurgical procedures.[9] Though 3DUS along with neuronavigation is an useful intraoperative modality in awake procedures, the limitations are the increased cost of surgery and the patient fatigue, at times due to the duration of surgery.[53],[54],[55] In operations with greater surgical difficulty when the risk-cost comparison is performed, the surgical resection results have greatly increased. Due to quick access to the pathology, the dangers of cortical and vascular injuries can be reduced.[54],[55],[56] The study design and interpretation was subject to several limitations. This was a relatively small study, with all the patients attending a single center, and operated by a single surgeon (to avoid bias). Further studies with larger study populations are required to make better conclusions.

Future

The optimization of neuronavigation systems and the introduction of IoUS for both cranial and spine surgeries have been fostered by numerous advancements in several scientific fields (including biomedical engineering, imaging, electronics, and nanotechnology). Those technological aids serve now as an excellent tool for surgical planning and help surgeons to preserve vital structures encountered intraoperatively. Training and fellowship programs on IoUS may help many surgeons in a great way. As such, many spine surgeons all over the world are now utilizing IoUS in their practice, and this trend should foster the incorporation of IoUS in both intracranial and intraspinal surgical training and fellowship programs; in fact, the use of IoUS is likely to further increase in the coming decade when the use of ultrasonic contrast agents will further enhance the definition of images acquired intraoperatively.[10]

IoUS (with CEUS) has been useful in evaluating blood perfusion in a real-time fashion, as it helps neurosurgeons establish in advance the fine vascular pattern of any brain tumor, as well as the larger arterial/venous blood supplies of brain, similar to intraoperative angiography.[1],[2] Integration of an external ultrasonography system into the Brain lab navigation is accurate and precise. By modifying registration (and measurement conditions) via software modification, the in vitro accuracy and precision is improved and requirements for a clinical application are fully met.[19] To prevent errors in neuronavigation associated with potential changes in aneurysm localization following draining of cerebral-spinal-fluid or hematoma, confirmation with intraoperative ultrasonography imaging reduces the risk to a minimum.


  Conclusions Top


Real-time intraoperative imaging technologies have shown utility in providing assistance to resection in a dynamic surgical field. Increasing attention has been paid to IoUS technologies, with IoUS being reported as a widely accessible, portable and less space-occupying and reliable imaging tool to follow and modify the surgical plan in real time. Our study provides a prospective cohort analysis of the efficacy of IoUS in brain tumor resections, basal ganglia hematomas and other traumatic intracerebral contusions/hematomas. Our results support previously reported findings on the practicality and efficacy of IoUS, while also supporting current limitations to its use. IOUS is a cheap and effective alternative to MRI and CT that helps in real-time decision-making, and more accurate and complete tumor resection, thus rendering the best possible outcomes for both pediatric and adult neurosurgical patients.[40] This is useful for identification of solid and cystic components of a tumor, lessens the duration of surgery. This guides in planning the shortest pathway for the removal of the lesion, biopsy of deep seated lesions and also it is easy and safe to handle with no risk of radiation exposure.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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