Method for removing glial tumors by subpial dissection with preservation of cortical vessels

Abstract

FIELD: neurosurgery and neurology.SUBSTANCE: after surgical access, a vessel located on the surface of the tumor tissue and extending into adjacent areas of the cortex is visualized. On both sides of the vessel, a bipolar electrode is used to coagulate the areas of the cortex affected by the tumor. Then, using microscissors, the arachnoid membrane is opened in the area of coagulation zones. An encephalotomy is performed. Next, subpial resection of the tumor in these areas is performed using an ultrasonic destroyer-aspirator, preserving the arachnoid membrane in which the preserved vessel passes. When visualizing a vessel located deep in the groove, dissection of the groove is performed while preserving the arachnoid membrane in which the vessel passes. The tumor around the vessel is resected using an ultrasonic destroyer-aspirator. In this case, first the part of the tumor on one side of the vessel is resected, then the part on the other side. These resection areas are connected to each other under the vessel. Then the residual tumor fragments on the vessel are removed. When visualizing a vessel passing through a tumor to healthy areas of the brain, this vessel is preserved, and the tumor tissue is separated from it along the periphery using an ultrasonic destroyer-aspirator. During the isolation of cortical and subcortical vessels, they are irrigated with saline solution. Then, through the resulting “intervascular windows,” deeply located tumor fragments are removed.EFFECT: method allows for the preservation of blood flow in cortical vessels during the removal of glial brain tumors, reducing the risk of developing ischemic complications in functionally significant areas of the cortex adjacent to the tumor resection zone, as well as in the subcortical structures of the brain, which, as a consequence, is associated with lower risks of developing postoperative neurological deficit.1 cl, 3 ex

Description

[0001] The invention relates to the field of medicine, namely to neurosurgery, neurology, and can be used in microsurgical removal of glial tumors of the brain during neurosurgical operations.

[0002] Surgical treatment of patients with glial brain tumors is associated with the risk of postoperative neurological deficit, one of the most common causes of which is the development of ischemia in functionally significant areas of the brain. According to the literature, the risk of developing acute cerebrovascular accident in areas of the cortex and white matter of the brain adjacent to the tumor resection area is 64.6% [van der Boog A., Rados M., Akkermans A. et al. Occurrence, Risk Factors, and Consequences of Postoperative Ischemia After Glioma Resection: A Retrospective Study. Neurosurgery 92(1):p 125-136, January 2023. | DOI: 10.1227 / neu.0000000000002149]. The problem of searching for and studying methods that can reduce the likelihood of ischemia during surgery for glial brain tumors is relevant.

[0003] The authors conducted a literature search in PubMed, Google Scholar, and Elibrary, as well as a patent search in Google Patents and Yandex. Patents were found using the keywords "vascular preservation," "ischemia prevention," "arterial preservation," "glial tumors," and "gliomas." Over 500 papers were analyzed, but only 60 were selected during the initial analysis (paper title, abstract, or summary). A detailed review of the papers resulted in the final analysis including 15 articles and one patent.

[0004] We reviewed studies to determine if they described methods for preserving cerebral vessels during removal of glial tumors in order to prevent the development of ischemic complications. The only patent for an invention in our sample was devoted to the surgical treatment of patients with drug-resistant temporal lobe epilepsy, and the method for preserving the vessels consisted of opening the temporal horn of the lateral ventricle, dissecting the brain matter of the basal wall of the lateral ventricle to the pia mater while preserving the vessels that feed the isolated parts of the temporal lobe [Patent of the Russian Federation 2637858. Method for treating drug-resistant temporal lobe epilepsy / Khachatryan V.A., Nikolaenko M.S., Mamatkhanov M.R., Lebedev K.E., Abramov K.B., Khachatryan R.G. Claimed 16.09.2016. Published. [07.12.2017].This technique, firstly, does not apply to the surgical treatment of patients with glial brain tumors, and, secondly, is not universal in terms of preserving cerebral vessels, since it can only be used in the surgical treatment of pathologies localized in the temporal lobe.

[0005] In most articles devoted to the surgical treatment of patients with glial tumors of the brain, the described methods of preventing the development of ischemic complications by methods of preserving cortical and subcortical vessels concerned exclusively specific clinical situations, surgical approaches and certain localizations of tumors [Oertel J, Wagner W, Piek J, Schroeder H, Gaab M. Waterjet dissection of gliomas ~ experience with 51 procedures. Minim Invasive Neurosurg. 2004 Jun;47(3): 154-9. doi: 10.1055 / s-2004-818512. PMID: 15343431]. For example, the most frequently described methods in the works were the preservation of cortical vessels and vessels of the Sylvian fissure during the removal of low-grade paralimbic gliomas, in particular, glial tumors of the insular lobe [Hou Z, Huang Z, Li Z, Deng Z, Li G, Xu Y, Wang M, Sun S, Zhang Y, Qiao H and Xie J (2022) Incidence of ischemic complications and technical nuances of arteries preservation for insular gliomas resection.Front. Surg. 9:956872. doi: 10.3389 / fsurg.2022.95687; Isolan GR, Buffon V, Maldonado I, Monteiro JM, Yagmurlu K, Ribas CAPM, Roesler R and Malafaia O (2022) Avoiding vascular complications in insular glioma surgery - A microsurgical anatomy study and critical reflections regarding intraoperative findings. Front. Surg. 9:906466. doi: 10.3389 / fsurg.2022.906466; Moshel YA, Marcus JD, Parker EC, Kelly PJ. Resection of insular gliomas: the importance of lenticulostriate artery position. J Neurosurg. 2008 Nov; 109(5):825-34. doi: 10.3171 / JNS / 2008 / 109 / 11 / 0825. PMID: 18976071]. For example, a transopercular method for resecting insular and paralimbic gliomas with preservation of cortical vessels has been described [Michaud K, Duffau H. Surgery of insular and paralimbic diffuse low-grade gliomas: technical considerations. J Neurooncol. 2016 Nov; 130(2):289-298. doi: 10.1007 / sll060-016-2120-2. Epub 2016 May 9. PMID: 27161250].This method allows for the preservation of all cortical arteries and veins, as well as vessels within the Sylvian fissure, which is impossible with the conventional transsylvian approach. The transopercular approach avoids direct contact with the arteries of the Sylvian fissure, significantly reducing the incidence of postoperative complications and adverse outcomes. The technique involves performing an encephalotomy in the superior temporal or inferior frontal gyrus in a location free from major cortical vessels, thereby avoiding the involvement of the Sylvian fissure vessels during tumor removal. This method is considered an alternative, but it is only applicable to the removal of paralimbic tumors. A method for preserving vessels passing through the tumor tissue to other areas of the cortex or white matter has not been described.

[0006] Another similar method of preserving cortical vessels during the removal of glial tumors is the method of preserving the vessels of the Sylvian fissure and lenticulostriate arteries during the removal of insular gliomas [Sanai N, Polley MY, Berger MS (2010) Insular glioma resection: assessment of patient morbidity, survival, and tumor progression. J Neurosurg 112(1):1-9. doi: 10.3171 / 2009.6.JNS0952]. The technique involves the removal of insular glial tumors with preservation of the large vessels of the Sylvian fissure at the stage of surgical access, with subsequent removal of gliomas through the spaces located between the large vessels. The medial border of the resection is the lenticulostriate arteries, since damage to them is associated with a high risk of developing permanent postoperative neurological deficit. This method is accepted as an analogue.The advantage of the method is the ability to preserve both superficial and deep arteries; however, a technique for preserving vessels passing through tumor tissue to other areas of the cerebral cortex has not been described, nor have methods for preserving vessels during the removal of glial tumors in other locations been described.

[0007] The closest to the claimed method is the removal of low-grade gliomas with preservation of cortical vessels located superficially on the tumor using bipolar coagulation of the cerebral cortex on both sides of the vessel [Duffau H. A new concept of diffuse (low-grade) glioma surgery. Adv Tech Stand Neurosurg. 2012; 38:3-27. doi: 10.1007 / 978-3-7091-0676-1_1. PMID: 22592409]. The technique involves the removal of glial tumors with preservation of large cortical vessels passing along the surface of the tumor to functionally significant areas of the brain. The vessel is preserved by coagulation of the cerebral cortex affected by the tumor on both sides of the artery or vein, followed by encephalotomy and separation of brain tissue from the membranes using subpial dissection. This method is adopted as a prototype.The advantage of this method is the ability to preserve blood vessels not only during insular surgery but also during the removal of glial tumors in other locations. However, the prototype method does not preserve deep-seated brain vessels and is not suitable for use in the removal of deep-seated glial tumors.

[0008] Thus, preventing ischemic complications during surgical treatment of patients with gliomas of the brain remains a pressing issue and requires the search for universal methods to preserve the integrity and patency of cerebral vessels. We have developed such a method, the distinguishing features of which include the preservation of arteries and veins not only at the border between the tumor and healthy brain tissue but also those passing through the tumor tissue, as well as the preservation of both superficial and deep vessels. This method preserves the anatomical integrity of the vessels, as well as blood flow within them, reducing the risk of ischemia in the white and gray matter of the brain and, consequently, the incidence of adverse neurological outcomes. At the same time, the completeness of tumor resection is not compromised, nor is the time to glioma recurrence shortened.

[0009] The objective of the invention is to create a method for preserving both superficial and deep-seated cortical vessels, preventing the development of ischemic complications in areas of the cortex adjacent to the resection zone, as well as in the subcortical structures of the brain in order to improve the safety of surgical treatment of patients with gliomas, especially when they are localized near functionally significant areas of the brain.

[0010] The technical result achieved by using the invention consists in reducing the incidence of ischemic complications near the tumor resection zone and, as a consequence, in reducing the incidence of neurological deficit in patients after resection of glial tumors using this method.

[0011] The technique involves preserving the anatomical integrity and functional preservation of both superficial and deep-seated cortical arteries and veins during microsurgical removal of glial tumors of the brain using the subpial dissection method.

[0012] The proposed method for microsurgical removal of glial brain tumors with preservation of cortical vessels is performed as follows. After intubation, positioning the patient on the operating table under total anesthesia, and establishing surgical access, a corticotomy is performed in the projection of the tumor tissue. Upon visualization of a vessel located on the surface of the tumor tissue and extending into adjacent areas of the cortex, in order to preserve the vessel, coagulation of the tumor-affected areas of the cortex on both sides of the vessel is performed using a bipolar electrode at a coagulation power of 10-15 W. Then, the arachnoid membrane is opened with microscissors in the area of ​​the coagulation zones, and an encephalotomy is performed.Next, subpial resection of the tumor in these areas is performed using an ultrasonic destructor-aspirator with the parameters of minimal aspiration force (10-20%) and amplitude (40-50%), with the highest tissue selectivity mode (on / off time 10 / 10 ms or 20 / 10 ms) preserving the arachnoid membrane in which the preserved vessel passes. If a vessel located deep in the sulcus is visualized, it is also preserved by dissection of the sulcus with preservation of the arachnoid membrane in which it passes. The tumor around the vessel is resected using an ultrasonic destructor-aspirator with the above-mentioned parameters: first, a part of the tumor on one side of the vessel is resected, then on the other, these resection areas are connected to each other under the vessel; the final stage is the removal of residual tumor fragments that may remain on the vessel, using highly selective ultrasonic destruction modes.If a vessel passing through the glioma to healthy areas of the brain was visualized, this vessel was also preserved, and the tumor tissue was separated from its periphery using an ultrasonic aspirator-destructor. Throughout the procedure to isolate and preserve the cortical and subcortical vessels, they were liberally irrigated with warm saline using a syringe. The tumor was then removed deep within the glioma through the "intervascular windows" formed by the preserved superficial arteries and veins.

[0013] The scientific novelty of the proposed method lies in its preservation of arteries and veins, not only those located at the border between the tumor and healthy brain tissue but also those passing through the tumor tissue, as well as the main vessels and their small branches. This method preserves the anatomical integrity of the vessels, as well as blood flow within them, reducing the risk of ischemia in the white and gray matter of the brain and, consequently, the incidence of adverse neurological outcomes.The effectiveness of the proposed method for preserving blood flow in the vessels and minimizing the risk of developing ischemic complications in areas adjacent to the tumor resection zone is confirmed by postoperative neuroimaging data: preservation of blood flow in the vessels and their patency in most cases is confirmed by CT / MR angiography or MRI in T1-WI mode with contrast, the absence of ischemic complications in the postoperative period was confirmed using MRI in DWI and ADC modes.

[0014] The proposed method was developed and underwent clinical trials at the Department of Neurosurgery of the N.I. Pirogov National Medical and Surgical Center of the Russian Ministry of Healthcare in the treatment of 96 patients with glial brain tumors. Following surgical treatment using the proposed method of microsurgical removal of glial tumors with preservation of cortical and subcortical vessels, ischemic zones near the tumor resection zone developed in 12 patients (12.5%). Moreover, the radicality of tumor resection did not decrease compared to the extent of glioma resection in patients without the use of this technique (96.4 and 95.7%, respectively). Also, the 5-year relapse-free survival rate in patients with high- and low-grade gliomas did not change (approximately 20% in both groups).

[0015] The method is illustrated by the following clinical examples.

[0016] 1. Patient G., 43, was admitted to the Neurosurgical Department of the Pirogov National Medical and Surgical Center with a diagnosis of a space-occupying lesion in the supplementary motor area of ​​the left frontal lobe. His neurological status included intermittent weakness in the right arm, grade 3-4. The patient underwent surgery using the proposed microsurgical tumor removal technique with preservation of the superficial and deep cortical vessels. Following standard surgical access and mapping of the precentral gyrus with a bipolar electrode at a stimulus strength of 10 mA using the Taniguchi method, an encephalotomy was performed in the posterior third of the superior frontal gyrus, and removal of the space-occupying lesion was initiated using a destructor-aspirator. All vessels passing through the tumor tissue, especially the branches of the pericallous artery passing through the tumor superiorly and posteriorly and supplying the medial surface of the left precentral gyrus, were preserved.During posterior tumor resection using dynamic intraoperative direct monopolar neurostimulation using the Taniguchi method, the tumor was removed until it approached the left corticospinal tract at a minimum stimulus strength of 1 mA, after which resection was stopped. Standard wound closure procedures were performed. Upon examination 2 hours after surgery, the patient developed a neurological deficit in the form of akinetic mutism, which on the second day transformed into impaired speech initiation and movement in the right limbs. By the time of discharge (5 days after surgery), the neurological deficit had completely regressed, consistent with the classic course of supplementary motor area syndrome. MRI monitoring 24 hours after surgery, with reconstruction of white matter pathways, revealed no residual tumor tissue or intracranial hematomas. There were also no ischemic areas in the precentral gyrus or in the white matter where the corticospinal tract is located.MR angiography and contrast-enhanced T1-weighted imaging clearly visualized intact cortical vessels and branches from the pericallosal artery extending through the resection cavity to the precentral gyrus. The histological diagnosis was anaplastic astrocytoma (WHO grade 3). A 3-month follow-up examination revealed no neurological deficit. Thus, in this case, the proposed method of microsurgical tumor removal with preservation of cortical vessels demonstrated that the patency of the cortical and subcortical arteries was completely preserved according to neuroimaging data. No ischemic zones were detected in functionally significant areas adjacent to the resection zone (precentral gyrus and left corticospinal tract). The neurological deficit that developed after surgery was associated with the resection zone itself (supplementary motor area).

[0017] 2. Patient K, 55, was admitted to the neurosurgical department of the Pirogov National Medical and Surgical Center with a diagnosis of a space-occupying lesion in the left temporal and parietal lobes of the brain. Preoperative neurological status included periodic speech impairments similar to sensory aphasia. Preoperative diffusion tensor imaging revealed that the left speech tracts (arcuate and inferior fronto-occipital fasciculi) were located close to the tumor along its medial border. The patient underwent surgery using the proposed microsurgical tumor removal technique with preservation of the superficial and deep cortical vessels. After surgical access and intraoperative awakening of the patient (according to the “sleep-awakening-sedation” protocol), speech testing was performed against the background of direct cortical stimulation with a bipolar electrode using the Penfield method at a stimulus strength of 10 mA.Speech mapping revealed a speech zone (Wernicke's area) in the posterior middle temporal gyrus (direct stimulation resulted in speech errors, such as anomia and paraphasia). Subsequently, using bipolar coagulation at 15 W, an encephalotomy was performed in the posterior third of the superior temporal gyrus outside the identified speech zones. Removal of the tumor mass was initiated using a destructor-aspirator. All vessels running through the tumor tissue were preserved. During tumor resection in the medial regions, dynamic intraoperative direct monopolar subcortical stimulation using the Penfield method was performed alongside continuous speech testing. Speech impairments, such as speech arrest and paraphasia, were detected during white matter stimulation at a stimulus intensity of 4 mA. According to neuronavigation data, this corresponded to the area of ​​the speech tracts (arcuate and inferior fronto-occipital fasciculi). In this direction, the resection was stopped.Standard wound closure procedures were performed. Postoperatively, the patient experienced no worsening neurological deficits, including speech impairment. An MRI scan performed 24 hours after surgery, with reconstruction of the white matter pathways, revealed no signs of residual tumor tissue or intracranial hematomas, and no areas of ischemia in the white matter region where the speech tracts were located. Magnetic resonance angiography and contrast-enhanced T1-weighted imaging clearly visualized intact cortical and subcortical vessels. The histological diagnosis was anaplastic oligodendroglioma (WHO grade 3).Thus, in the presented example, using the proposed method of microsurgical removal of a tumor with preservation of cortical vessels, it was shown that the patency of the cortical and subcortical arteries, according to neuroimaging data, was completely preserved; no ischemic zones were detected in functionally significant areas adjacent to the resection zone (Wernicke's area and speech tracts of the white matter), which prevented the development of postoperative neurological deficit.

[0018] 3. Patient L., 34, was admitted to the Neurosurgical Department of the Pirogov National Medical and Surgical Center with a diagnosis of a space-occupying lesion in the supplementary motor area of ​​the right frontal lobe extending into the cingulate gyrus. Her neurological status included left-sided hemiparesis (grade 4) and periodic seizures with loss of consciousness. The patient underwent surgical treatment using the proposed microsurgical tumor removal technique with preservation of the superficial and deep cortical vessels. After surgical access and identification of the precentral gyrus using direct cortical stimulation with a bipolar electrode according to the Taniguchi method at a stimulus strength of 10 mA, a corticotomy was performed, and removal of the space-occupying lesion was initiated using a destructor-aspirator. All vessels passing through the tumor tissue were also preserved.Particular attention was paid to the branches of the pericallosal artery, which passed through the tumor superiorly and posteriorly, supplying the medial surface of the right precentral gyrus. The tumor was completely resected based on neuronavigation, intraoperative fluorescence, and ultrasonography. Based on intraoperative direct monopolar subcortical stimulation using the Taniguchi method in the posterior regions, resection was completed at a distance of 5 mA from the right corticospinal tract. Standard wound closure procedures were performed. No new neurological deficits were observed in the patient postoperatively, and the left-sided deficit completely regressed by the time of discharge (6 days postoperatively). During MRI monitoring 24 hours after surgery with reconstruction of the white matter pathways, no residual tumor tissue or intracranial hematomas were detected, and there were no ischemic zones in the precentral gyrus and in the white matter where the corticospinal tract is located.MR angiography and contrast-enhanced T1-weighted imaging clearly visualized intact cortical vessels and branches from the pericallosal artery extending through the resection cavity to the precentral gyrus. The histological diagnosis was diffuse astrocytoma (WHO grade 2). Thus, in this case, using the proposed method of microsurgical tumor removal with preservation of cortical vessels, neuroimaging data demonstrated that the patency of the cortical and subcortical arteries was completely preserved. No ischemic zones were detected in functionally significant areas adjacent to the resection zone (precentral gyrus and right corticospinal tract), which prevented the development of postoperative neurological deficit.

[0019] Sources of information:

[0020] 1) van der Boog A., Rados M., Akkermans A. et al. Occurrence, Risk Factors, and Consequences of Postoperative Ischemia After Glioma Resection: A Retrospective Study. Neurosurgery 92(1):p 125-136, January 2023.

[0021] 2) Russian Federation Patent 2637858. Method for treating drug-resistant temporal lobe epilepsy! Khachatryan V.A., Nikolaenko M.S., Mamatkhanov M.R., Lebedev K.E., Abramov K.B., Khachatryan R.G. Claimed 16.09.2016. Published 07.12.2017.

[0022] 3) Oertel J, Wagner W, Piek J, Schroeder H, Gaab M. Waterjet dissection of gliomas - experience with 51 procedures. Minimum Invasive Neurosurg. 2004 Jun; 47(3). T54-9.

[0023] 4) Hou Z, Huang Z, Li Z, Deng Z, Li G, Xu Y, Wang M, Sun S, Zhang Y, Qiao H and Xie J (2022) Incidence of ischemic complications and technical nuances of arteries preservation for insular gliomas resection. Front. Surg. 9:956872.

[0024] 5) Isolan GR, Buffon V, Maldonado I, Monteiro JM, Yagmurlu K, Ribas CAPM, Roesler R and Malafaia О (2022) Avoiding vascular complications in insular glioma surgery - A microsurgical anatomy study and critical reflections regarding intraoperative findings. Front. Surg. 9:906466.

[0025] 6) Moshel YA, Marcus JD, Parker EC, Kelly PJ. Resection of insular gliomas: the importance of lenticulostriate artery position. J Neurosurg. 2008 Nov; 109(5):825-34.

[0026] 7) Michaud K, Duffau H. Surgery of insular and paralimbic diffuse low-grade gliomas: technical considerations. J Neurooncol. 2016 Nov; 130(2):289-298.

[0027] 8) Sanai N, Polley MY, Berger MS (2010) Insular glioma resection: assessment of patient morbidity, survival, and tumor progression. J Neurosurg 112(1): 1-9.

[0028] 9) Duffau H. A new concept of diffuse (low-grade) glioma surgery. Adv Tech Stand Neurosurg. 2012; 38:3-27.

Claims

A method for microsurgical removal of glial tumors of the brain by subpial dissection, including removal of the tumor with an ultrasonic destroyer-aspirator, characterized in that after surgical access is achieved, a vessel located on the surface of the tumor tissue and extending to adjacent areas of the cortex is visualized, coagulation of the areas of the cortex affected by the tumor is performed on both sides of the vessel with a bipolar electrode, then the arachnoid membrane is opened in the area of ​​coagulation zones with microscissors, an encephalotomy is performed, and then subpial resection of the tumor in these zones is performed with an ultrasonic destroyer-aspirator with preservation of the arachnoid membrane in which the preserved vessel passes;When visualizing a vessel located deep in a sulcus, dissection of the sulcus is performed while preserving the arachnoid membrane in which the vessel passes, the tumor around the vessel is resected with an ultrasonic destroyer-aspirator, while first a part of the tumor on one side of the vessel is resected, then on the other side, these resection sites are connected to each other under the vessel, then the residual fragments of the tumor on the vessel are removed; when visualizing a vessel passing through the tumor to healthy areas of the brain, this vessel is preserved, and the tumor tissue is separated from it along the periphery with an ultrasonic destroyer-aspirator; during isolation of cortical and subcortical vessels, they are irrigated with saline; then, through the formed "intervascular windows", deep-seated fragments of the tumor are removed.