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Microsurgical resection of tumors of the lateral and third ventricles: operative corridors for difficult-to-reach lesions Ulas Cikla1· Kyle I. Swanson1· Abdulfettah Tumturk1· Nese Keser1· Kutluay Uluc1 ·Aaron Cohen-Gadol2· Mustafa K. Baskaya J Neurooncol (2016) 130:331–340 DOI 10.1007/s11060-016-2126-9 Abstract 摘要 Tumors of the lateral and third ventricles are cradled on all sides by vital vascular and eloquent neural structures. Microsurgical resection, which always requires attentive planning, plays a critical role in the contemporary management of these lesions. This article provides an overview of the open microsurgical approaches to the region highlighting key clinical perspectives. 侧脑室和三脑室肿瘤全方位被重要的血管、神经结构包绕，显微外科切除是当前治疗此类病变的主要手段，术前需要详尽的计划。本文回顾分析侧脑室和三脑室的显微外科手术入路，突出关键的临床观点。
Introduction 前言 The surgical management of tumors of the lateral ventricles (LV) and the third ventricle (TV) remains a distinct challenge for neurosurgeons due to the deep and difficult-toreach location and frequent involvement of adjacent critical neurovascular structures. An appropriate surgical approach should provide adequate operative working space with minimal brain retraction or brain transgression [1–3]. To accomplish these goals, neurosurgeons may choose an approach that necessitates a longer distance to reach the tumor if it minimizes the amount of brain tissue that is resected or placed at risk by the approach. Furthermore, selection of the optimal approach to ventricular tumors depends on multiple other factors including the size of the ventricles and the tumor, the location of the arterial supply, pathological features of the tumor, and the surgeon’s experience. This paper provides an overview of the open surgical operative corridors to the lateral and TV tumors, highlighting the key surgical principles. 侧脑室（LV）和三脑室肿瘤（TV）由于位置深、显露困难并且常常累计毗邻重要的血管神经结构，对于神经外科医生手术治疗仍具挑战。理想的手术入路应该最轻柔地牵拉脑组织，并且能提供良好的手术视野。为了达到目的，神经外科医师选择的入路应该对脑组织的损伤最轻。此外，要根据多种因素选择脑室肿瘤最佳的手术入路，例如脑室和肿瘤的大小，供血动脉部位，肿瘤的病理学特征和外科医生的经验。本文回顾分析侧脑室和三脑室的显微外科手术入路，突出关键的临床要点。 Lateral ventricles 侧脑室 The LV are anatomically divided into five parts: the body, atrium, frontal horn, temporal horn, and occipital horn [4]. Tumors of the LV can also be grouped into primary and secondary tumors. Primary tumors are those arising from the structures within the ventricle, whereas secondary tumors are the larger group of tumors derived from adjacent structures and expanding into the ventricular cavity. Overall, tumors of the LV comprise between 0.8 and 1.6 % of all brain tumors [5, 6]. As many of the tumors arising in the LV are benign and slow growing, they are often not detected until they reach a considerable size that causes obstructive hydrocephalus or mass effect. Headaches and visual changes, often related to hydrocephalus, are the most common presenting symptoms. Other symptoms include endocrine disturbance, motor and sensory deficits, nausea and vomiting, and cognitive impairment [5, 7–9]. 侧脑室解剖上分为5部分，分别是体部、房部、额角、颞角和枕角。侧脑室肿瘤分为原发和继发。原发性肿瘤起源于脑室结构，继发性脑室肿瘤来自邻近结构向脑室内生长，比原发性脑室肿瘤更常见。侧脑室肿瘤占颅内肿瘤的0.8-1.6%，源自侧脑室的许多肿瘤是良性并生长缓慢，因此它们常常长到相当大引起脑积水和占位效应时才被发现。头痛和视力改变是最常见的主诉症状，可能与脑积水相关。其他的症状包括内分泌紊乱，运动和感觉障碍，恶心、呕吐，认知损害。 Multiple surgical approaches have been described for each location in the LV system (Fig. 1). The aim of each of these approaches is to provide an adequate corridor to the tumor while preserving eloquent overlying neurovascular structures [5]. A careful review of the pathoanatomy from multiple planes on imaging studies, including MRI, MR angiography or venography, and occasionally digital subtraction angiography, is essential for selecting the appropriate surgical strategy [10–12]. The neurovascular anatomy may be distorted by the tumor, or the patient may have an anatomical variation that makes a particular route unsafe. A thorough knowledge of the anatomy and available alternative surgical routes allows the neurosurgeon to accommodate to any change in the operative agenda and provides alternative contingency plans to deal with any unforeseen difficulty. 侧脑室每个部位的多个手术入路被描述（Fig.1）。要求每个手术入路能提供充分的操作空间并能保护肿瘤表面的神经血管结构。神经血管结构可能被肿瘤推移，或者病人可能有解剖变异，这种变异可能使常规手术路径变得不安全。因此选择恰当的手术方案前必须根据MRI、MRA、MRV的多个平面仔细复习病理解剖，偶尔需要DSA检查。详尽的解剖知识和可替代的手术入路可以使神经外科医生适应手术日程中的任何变化，制定应急计划能应对任何不可预见的困难。 Fig. 1 The surgical approaches to the lateral ventricle (LV) are shown on a lateral view of a cadaveric dissection of the brain. LV and third ventricle (TV) are shown in blue. Anatomical portions of the LV are depicted with gray ellipses. Red arrows show the direction of the approaches and the parts of the LV that can be reached by that individual approach。 Fig.1 脑解剖图侧位观显示的侧脑室(LV)手术入路。蓝色部分是LV和三脑室（TV），LV解剖结构用灰色椭圆形描记。红色箭头表示入路方向以及每个入路能到达侧脑室的部分。 Open surgical approaches to LV 侧脑室的手术入路 Frontal horn and body of LV 侧脑室额角和体部 Tumors in and around the anterior two-thirds of the LV can be accessed via either the interhemispheric anterior transcallosal approach (IATcA) (Fig. 2) or the frontal transcortical approach (FTA) [13–15]. AITcA and FTA both allow for excellent visualization of LV anatomical landmarks, including the thalamostriatal, anterior-septal and caudate veins, foramen of Monro and choroid plexus (CP) [4]. 侧脑室前2/3肿瘤可以选择大脑半球间经胼胝体前入路（IATcA）（Fig.2）或经额叶皮层入路（FTA）。IATcA和FTA都能很好的观察到侧脑室解剖标志，包括丘纹静脉、前隔静脉、尾状核静脉，Monro孔和脉络丛（CP）。 FTA may provide better access to larger tumors than the IATcA in the frontal horn, but it has a limited exposure of the contralateral LV and may pose an increased risk of postoperative seizures [1, 5]. FTA requires transection of the cortex and therefore potentially carries a higher risk of postoperative neurologic decline, such as attention deficits, as compared to the limited callosotomy during the IATcA. A corticotomy in the middle frontal gyrus or dissection through the superior frontal sulcus well anterior to the motor cortex decreases the likelihood of significant neurological deficit, but either a corticotomy or retraction of the supplemental motor or premotor area may cause at least a temporary hemiparesis. Furthermore, FTA is usually not advised for tumors within the mid-body of the LV because this approach would require an extension of the cortical incision into the motor cortex [13]. The most frequent complications following FTA are epilepsy (26 % of patients) followed by transient mutism (11 % of patients), hemiparesis (7 % of patients), and short-term memory disturbance [15]. FTA比IATcA更容易显露额角的大肿瘤，但对对侧脑室显露有限，而且增加术后发生癫痫的风险。FTA需要横断皮层，与IATcA中局限的胼胝体切开相比术后神经功能受损的风险更高，例如注意力下降。额中回皮层切开或经额上沟切开能减少严重的神经功能缺损发生，但是无论皮层切开还是补充运动区或运动前区的牵拉都可能引起暂时的轻偏瘫。此外，通常不推荐FTA应用在LV体部中段的肿瘤，因为可能会将皮层切口延长到皮质运动区。FTA后最常发生的并发症是癫痫（26%），短暂性缄默（11%），轻偏瘫（7%），短时记忆障碍。 AITcA remains the most commonly preferred microsurgical approach for exposure of ventricular tumors. The head is often positioned so the superior sagittal sinus (SSS) is parallel to the floor, exploiting gravity retraction on the ipsilateral hemisphere away from the falx and SSS. Some colleagues position the head in a neutral position to maintain basic anatomical orientation during microsurgery. A horseshoe or a linear parasagittal skin incision allows a parasagittal craniotomy located two-thirds anterior and one-third posterior to the coronal suture guided by intraoperative image-based neuronavigation. AITcA是目前脑室肿瘤最常推荐的显微外科入路。头部摆放位置使上矢状窦平行地面，一侧大脑半球在重力作用下可以与大脑镰和上矢状窦（SSS）自然分离。也有人将头部摆至矢状位，术中保持基本解剖位置。头皮切口采用马蹄形或矢状窦旁直切口，神经导航定位冠状缝，2/3位于冠状缝前，1/3位于冠状缝后。 The craniotomy is usually eccentric to one side but extends across the midline to allow for gentle mobilization of the SSS and falx cerebri. The dura is opened in a semilunar fashion with the SSS serving as the base of the dural flap. The dural incisions are tailored according to the drainage pattern of the parasagittal bridging veins. Every effort should be made to preserve the cortical draining veins and minimize the risk of venous infarction. Next, the interhemispheric fissure is dissected using meticulous sharp arachnoid dissection to free the cortex of the medial surface of the superior frontal gyrus from the falx cerebri. At the depth of the interhemispheric fissure, the corpus callosum (CC) is encountered and is differentiated from the cingulate gyri by a pearly white appearance. The cingulate gyri can be very adherent, requiring operator’s patience and adherence to microsurgical principles for their separation. The pericallosal arteries (PeCas) coursing over the CC are identified and carefully separated. Classically, the callosotomy involves an incision no larger than 2 cm, located in the midline between the two PeCas [16]. The exact location of the callosotomy can also be determined by neuronavigation. The target LV is entered after the callosotomy and anatomic landmarks are used to ensure that the correct LV has been entered. 骨瓣位于一侧越过中线以利于SSS和大脑镰轻微移动。根据矢状窦旁桥静脉剪开硬脑膜，硬脑膜半月形切开翻向上矢状窦。尽可能保护皮层引流静脉减少静脉梗死的风险。然后经纵裂锐性分离从大脑镰上松解额上回内侧面。在纵裂深部，胼胝体（CC）为珍珠白色与扣带回相区别。扣带回粘连紧密，需要术者耐心采用显微技术分离。胼周动脉跨过胼胝体上方，需要仔细分离，在胼周动脉之间切开胼胝体，切口不超过2cm。通过神经导航定位胼胝体切开的确切位置，胼胝体切开进入脑室后辨别解剖标志再次确认。
The surgical technique of the AITcA is demonstrated in videos presenting the resection of a LV subependymoma [Movie 1] and the resection of a LV gangliocytoma [Movie 2] (Fig. 3). Fig. 2 a–f Cadaveric dissection demonstrating the steps of interhemispheric transcallosal approach. a A C-shaped incision for the interhemispheric approach. b After craniotomy, the superior sagittal sinus (SSS) is seen at the midline. c After elevation of the dura, vasculature of the region, including cortical veins draining into the SSS, is seen more clearly. d The corpus callosum (CC), cingulate gyrus (CG), and the pericallosal arteries are seen in the interhemispheric fissure. e Dissection demonstrating the anatomical relationships of the LVs. Corpus callosum (CC), column of fornix (cf), foramen of Monro (FM), thalamus (T), genu of CC (G), body of fornix (bf), choroid plexus (chp). f Superior view of the LV over the FM (arrow) demonstrating the close relationship of the third ventricle with the optic nerve and the lamina terminalis. Optic nerve (II), septum pellucidum (sp), choroid plexus (chp), thalamus (T), thalamostriate vein (tsv), lamina terminalis (LT), column of the fornix (CF)。 Fig 2 a-f 尸体解剖演示大脑半球间经胼胝体入路步骤。a 切口。b 骨瓣去除后，上矢状窦位于中线。c 硬脑膜去除后局部血管清晰可见，包括皮层静脉引流到上矢状窦。d 大脑半球间裂内可见胼胝体、扣带回和胼周动脉。e 侧脑室内解剖关系，胼胝体、穹隆柱、Monro孔、丘脑、胼胝体膝部、穹隆体、脉络丛。f 越过Monro孔（箭头）侧脑室上面观显示三脑室和视神经、透明隔脉络丛、丘脑、丘纹静脉、终板、穹隆柱。 During the interhemispheric dissection, the cortices of the superior frontal and cingulate gyri, as well as the PeCas and their branches, are at risk of injury. Other potential major complications of this approach include disconnection syndrome from the callosotomy and transient or permanent memory deficits from injury to the forniceal bodies [3, 4, 13]. 分离纵裂过程可能会损伤额上回、扣带回、胼周动脉及其分支。该入路其它潜在的主要并发症包括胼胝体切开的分离综合征、短暂或永久的记忆缺失。
Atrium of the LV 侧脑室房部 Multiple surgical corridors have been described to approach the atrium of the LV via various operative trajectories [17]. The interhemispheric posterior transcallosal approach (IPTcA) is preferred for lesions involving the atrium of the LV and the splenium of the CC. The surgical technique for this approach is demonstrated in a video of the resection of a grade IV astrocytoma involving the thalamus, both the LV and the splenium of the CC [Movie 3] (Fig. 3). 进入侧脑室房部有多个手术入路。大脑半球间后方经胼胝体入路（IPTcA）被认为更适合累及侧脑室房部和胼胝体压部的病变。该手术入路的外科技术在一例累及丘脑、双侧LV和胼胝体压部的4级星形细胞瘤的手术录像中得以展现（Fig 3）。
Fig. 3 Preoperative and postoperative MR images of the cases which are presented in the complementary videos of the article. Case 1 Sagittal and axial MRI with contrast show non-enhancing right LV tumor. Post-operative sagittal flair imaging shows the minimal callosotomy and axial post-contrast T1 imaging confirms gross total resection through interhemispheric transcallosal approach. [Please see the video 1]. Case 2 Sagittal flair MRI and axial post-contrast T1 MRI shows a heterogeneously enhancing cystic tumor in the posterior TV. Post-operative sagittal cube MRI and post-contrast axial T1 MRI confirms gross total removal through this approach. [Please see the video 2]. Case 3 Sagittal and axial flair MRI show a tumor occupying the frontal horn, body and atrium of the LV. Post-operative sagittal flair MRI show the extent of the callosotomy and axial T1 MRI confirms the gross total removal. [Please see the video 3]. Case 4 The extent of heterogeneously enhancing tumor originating from the thalamus and the peripheral edema due to mass effect are shown in the contrasted sagittal and axial MRI. Postoperative sagittal flair MRI and post-contrast axial MRI confirm the gross total resection via posterior interhemispheric approach. [Please see the video 4] Fig 3 文章附加的影音资料中病例的术前、术后MRI。Case 1 矢状位和轴位增强MRI提示右侧LV肿瘤无增强。术后矢状位flair提示很小的胼胝体切口，术后轴位T1增强扫描证实通过半球间经胼胝体入路肿瘤全切。Case 2 矢状位MRI flair序列和术后轴位T1增强提示三脑室后部不均质强化囊变肿瘤。术后MRI提示肿瘤全切。Case 3 矢状位和轴位MRI flair序列显示肿瘤侵犯侧脑室前角、体部和房部。术后MRI flair 显示胼胝体切开长度和T1轴位证实肿瘤全切。Case 4 矢状位和轴位增强MRI显示肿瘤起源于丘脑，不均质强化伴占位效应引起的瘤周水肿。术后矢状位MRI flair和增强MRI证实通过半球间后方入路肿瘤全切。
Yasargil described another key route to the ventricular trigone, the ipsilateral interhemispheric posterior parietooccipital approach (IPPoA) [7, 13, 14]. Lesions of the medial wall of the ventricular trigone and the TV posterior to the massa intermedia of the thalamus can be tackled by this approach [18]. Although this approach requires transection of a small area of the precuneus gyrus, it provides a safe route that minimizes the risk of injury to the optic radiations and visual cortex [14]. Yasargil描述了另一个进入脑室三角部的重要入路是同侧大脑半球后部经顶枕入路（IPPoA），侧脑室三角区内侧壁和三脑室后部到丘脑中间块的病变可以通过此入路处理。尽管该入路需要切断楔前叶很小一部分，但它提供一个安全的手术路径，可以降低视辐射和视皮质的损伤。 Izci et al. studied the microsurgical anatomy and topographical relation of the surgical corridor provided by the supracerebellar transtentorial transcollateral sulcus approach to the atrium [17]. This approach provides a long working distance to reach tumors located in the inferior part of the atrium and posterior parahippocampal gyrus; however, tumors with a notable extension above the tentorium, significant lateral extension or tumors growing into the TV are not usually amenable to this approach. Izci 等在显微解剖基础上图示小脑上经天幕经旁沟入路到房部的关系。该入路通过较长的工作距离到达房部下方和海马旁回后方的肿瘤；但是，如果肿瘤向小脑幕上，横向扩展显著或向三脑室生长，通常不适用该入路。 The transcortical approaches to the atrium risk traversing important white matter tracts such as the internal capsule, optic radiations, and the striate cortex [7]. The parietal transcortical approach (also called the superior parietal lobule (SPL) approach) is a traditional transcortical approach for access to both medial and lateral walls of the atrium by traversing less eloquent cortex [1, 12, 19–24]. After a cortical incision through the SPL, the atrium, posterior body of LV, posterior half of the TV, and the quadrigeminal cistern can be reached [4]. Of note, this route is usually employed when there is ventricular enlargement [13]. One potential disadvantage of the SPL approach is the inability to gain early control of the vascular supply to the tumor, which usually enters into the inferior aspect of the tumor [25]. The most common complication of this approach is a homonymous visual field deficit from injury to the optic radiations [26]. Injury to the adjacent eloquent dominant inferior parietal lobule, which includes the supramarginal and angular gyri, can result in Gerstmann syndrome (apraxia, acalculia, finger agnosia, and right-left confusion) [7, 12, 27]. To avoid these complications, the relation of the tumor to eloquent cortex should be carefully delineated on preoperative imaging and both anatomic landmarks and neuronavigation utilized intraoperatively to ensure protection of eloquent cortices. 经皮层到房部可能损害重要的白质纤维束，例如内囊，视辐射和视皮质。顶部经皮质入路（也称作顶上小叶SPL入路）是经典的经皮质入路，此入路能到达房部内侧壁和外侧壁且很少涉及语言皮质。顶上小叶经皮层入路，可以暴露房部、侧脑室体后部、三脑室后部和四叠体池。此入路在有脑室扩大的时候经常会用到。SPL入路的一个潜在缺点是不能早期控制肿瘤的供血动脉，应为供血动脉常在肿瘤下方。最常见的并发症是视辐射损伤导致同向视野缺损。损伤临近的优势半球顶下小叶，包括缘上回和角回，会导致古茨曼（Gerstmann)综合征（失用，失算，手指失认，左右失认）。为了避免发生这样的并发症，肿瘤和语言中枢的关系在术前影像上要仔细描画，术中要结合解剖标志和神经导航确保语言中枢不被损害。 The subtemporal approach is a very useful lateral route for removal of tumors localized in the atrium since this approach provides immediate access to the anterior choroidal artery, which often gives vascular supply to the tumor, and has a decreased incidence of visual field defects as compared to the transtemporal approach [28]. This approach is preferable when the ipsilateral temporal horn is large, and the tumor is relatively small. In larger tumors, the subtemporal approach may require excessive retraction on the temporal lobe to complete tumor resection [25]. Kawashima et al. demonstrated the efficacy of the subtemporal approach in which an incision is made in the inferior temporal gyrus, occipitotemporal gyrus, or collateral sulcus to avoid transgression of the optic radiations and speech centers located in the dominant hemisphere [18]. 对于切除位于房部的肿瘤，颞下入路是非常有用的一个外侧入路。因为脉络膜前动脉常为肿瘤主要供血动脉，颞下入路能较早见到脉前动脉，而且与经颞叶入路相比视野缺损发生率较低。当病变同侧颞角扩大，肿瘤相对较小，采用颞下入路更理想。如果肿瘤很大，颞下入路需要过度牵拉颞叶。Kawashima等证实切口在颞下回、枕颞回或邻近脑沟的颞下入路可避免损伤视辐射和优势半球语言中枢。 A less commonly used approach is the transtemporal approach, which utilizes a cortical incision through a portion of the middle or inferior temporal gyri [4, 7, 20–22, 26, 29, 30]. This approach risks homonymous quadrantanopia due to injury to the optic radiations, as well as limited or impaired recognition of emotions from injury to the non-dominant temporal lobe or receptive aphasia from injury to the dominant temporal lobe [31, 32]. 经颞叶入路不太常用，皮层切口在颞下回或颞中回。该入路可能损伤视辐射导致同向性偏盲，同时非优势半球颞叶损伤会引起情感障碍，优势半球损害导致感觉性失语。
Temporal horn of LV 侧脑室颞角 The temporal horn can be accessed via lateral transcortical trajectories, also called the transtemporal approaches, through the middle temporal gyrus, and less commonly the inferior temporal gyrus [7]. The transtemporal approach often provides the shortest trajectory to the lesions in the temporal horn and is greatly facilitated by dilated ventricles [13]. The transtemporal approach usually affords early access to the choroidal arterial pedicle, which is often the vascular supply of tumors in the temporal horn; early occlusion of these vascular feeders facilitates debulking of the tumor [33]. The inferior temporal gyrus route, though not as direct as the middle temporal gyrus route, can be used to provide a safe distance from the language area of the dominant temporal lobe and also to avoid the anterior fibers of the optic radiations. Care must be taken to prevent injury to the vein of Labbe, the primary drainage system of the lateral temporal lobe. The transtemporal approach can result in a partial upper-quadrantanopia though patients do not often perceive this deficit in daily activities [34]. Furthermore, choroidal artery territory infarcts can occur if the anterior choroidal artery is sacrificed while interrupting the vascular supply of the tumor [13]. 外侧经皮层可以进入颞角，也叫经颞叶皮层入路，通常通过颞中回，少数情况切开颞下回。颞叶入路提供最短路径到达颞角病变，脑室扩大更容易操作。颞叶入路通常不会过早接近脉络膜动脉根部，该动脉通常为颞角内肿瘤供血，早期阻断肿瘤血供利于切除肿瘤。切开颞下回不如切开颞中回容易到达病变，但常用来提供距优势半球语言区的安全距离并且躲避视辐射前部纤维。避免损伤Labbe静脉，颞叶外侧的主要引流静脉。颞叶经皮层入路可能导致象限盲，但病人可能在日常生活中不会觉察。此外，为阻断肿瘤血供牺牲了脉络膜前动脉可能导致脉前动脉供血区梗死。 For anterior temporal horn tumors, we advocate the transsylvian trajectory via the pterional approach as originally described by Yasargil. This approach allows entrance into the anterior temporal horn while minimizing the risk to the anterior loop of Meyer’s optic radiation fibers as long as rigid retraction is not applied to the temporal lobe [13, 14, 35, 36]. This approach requires a wide opening of the Sylvian fissure, which is technically more demanding than the transtemporal approach. The former also harbors the potential for injury to the arterial branches of the middle cerebral artery and the sylvian veins. 治疗侧脑室颞角前方肿瘤，我们主张翼点入路分离外侧裂。该入路能到达颞角前面，而且只要不用力牵拉颞叶，视辐射前袢很少损伤。该入路需要广泛打开侧裂，技术要求比颞叶入路高，有可能损伤大脑中动脉分支和侧裂静脉。
侧脑室枕角 Occipital horn of LV For tumors that are located in the occipital horn of the LV, the posterior interhemispheric parieto-occipital transprecuneal trajectory provides an ideal corridor to achieve resection while minimizing the risks to the relevant subcortical tracts. For tumors that are isolated to the occipital horn and extend posteriorly or laterally toward the cortical surface, an occipital or posterior parietal transsulcal approach may be selected, depending on the superficial component of the tumor [7]. 对于侧脑室枕角的肿瘤，后纵裂顶枕部经楔前入路对相关的皮层下纤维损伤较小，是切除该部位肿瘤的理想入路。对孤立于枕角的肿瘤和那些向后、向外侧生长累及皮层的肿瘤，根据肿瘤最浅表的位置可以选择枕部或顶后部经脑沟入路。 附带视频如下： 未完待续---- 原著作者:Ulas Cikla，--- Aaron Cohen 编译者： 云强，内蒙古自治区人民医院,神经外科,主任医师, 博士，硕导。发表文章10余篇，SCI收录1篇。获内蒙古自治区医学会科学技术二等奖两项、三等奖一项，内蒙古科技进步三等奖一项。平台审稿团成员。 |
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