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microsurgery 'burr hole' for intracranial tumors and mesial temporal lobe epilepsy
Journal: Burdenko's Journal of Neurosurgery. 2019;83(6): 44‑57
Read: 4596 times
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It is generally accepted that optimal neurosurgical approach should be associated with minimum traction and/or resection of brain tissue. Considering this principle, minimally invasive methods including endoscopic and endovascular surgery have been recently introduced in neurosurgery. These approaches are accompanied by no contact or minimal interaction with brain structures. Minimally invasive approaches become more preferable in microneurosurgery. Philosophical basis of these tendencies is determined by the statement of the great surgeon Emil Theodor Kocher [1], who emphasized: “Approach should be as large as necessary and as small as possible”.
A gradual transition from extensive craniotomies performed by Walter Edward Dandy and other well-known neurosurgeons to less traumatic approaches has occurred over the last century. Undoubtedly, this was due to clinical introduction of operating microscope. Donald H. Wilson [2] was the first neurosurgeon who created the “Keyhole” concept in neurosurgery. He was able to reduce craniotomy dimension up to 5 cm and perform various intracranial procedures through this approach thanks to the use of operating microscope. Successful operations determined development of new approaches in surgical treatment of brain tumors and gradual prevalence of minimally invasive approaches. To date, a whole direction has already been formed in neurosurgery. It is the so-called “Keyhole” neurosurgery [2—6].
The main principle of “Keyhole” surgery is small craniotomy for minimized trauma and traction of brain tissue. A sufficient number of reports devoted to “Keyhole” surgery have been published. The authors demonstrate advisability of this technique for various neurosurgical diseases of the brain. Minimal dimension of craniotomy in Keyhole microneurosurgery is 2x3 cm [2—6].
It seemed that minimum dimensions of craniotomy were achieved for adequate neurosurgical procedures. Robert Reish [7] as one of the founders of Keyhole neurosurgery states that “the biggest mistake of surgeon following Keyhole surgery philosophy is a too small craniotomy”. He believes that craniotomy dimension less than 2x3 cm is not adequate for neurosurgical intervention.
The introduction of hands-free system for positioning of operating microscope (MARI) [8] made it possible to reduce craniotomy up to standard burr hole with a diameter of 14 mm. This approach was adequate to conduct microsurgical interventions for various intracranial tumors. We called this technique “Burr hole” microneurosurgery. The first author of this report has used this technique in more than 500 operations at the Burdenko Neurosurgery Center since 2016. Surgical outcomes of the first 200 operations are analyzed in this manuscript.
Inclusion criteria
There were patients with various intracranial tumors.
Exclusion criteria:
— meningeal tumors followed by advanced lesion of convexital dura mater;
— skull base tumors involving great arteries and/or characterized by intense blood supply;
— intracerebral tumors with advanced lesion of convexital cortex;
— intracerebral tumors of functionally important areas requiring intraoperative mapping of sensorimotor or speech cortical zones;
— advanced insular gliomas.
Distribution of patients
This sample of patients includes the results of 200 Burr hole microsurgical operations with a burr hole diameter of 14 mm. All interventions have been carried out for the period from February 15, 2016 to November 14, 2017. Age of patients ranged from 16 to 79 years (median 38 years). Females prevailed (1.6:1). Intracranial mass lesions (tumors, cysts, hematomas) were observed in 176 cases, pharmacoresistant hippocampal sclerosis — in 24 cases. The last patients underwent selective amygdalogippocampectomy.
Distribution of patients depending on histological diagnosis is shown in Table 1.
Distribution of tumors depending on localization, dimension and volume is shown in Table 2.
Dimensions and volume of tumor were calculated using MRI data. Tumor boundaries were determined considering the area of contrast agent accumulation in T1-weighted images for contrasted tumors and dimensions of changed MR signal area in T2-weighted and FLAIR images for non-contrasted tumors (Table 2).
Burr hole transcortical approaches prevailed among these 200 operations (n=81, 40.5%). There were also retrosigmoid (n=38, 19%), subtemporal (n=32, 16%), infratentorial supracerebellar (n=25, 12.5%), interhemispheric (n=17, 8.5%), telovelar (n=5, 2.5%) and supraorbital approaches (n=2, 1%) (Fig. 1).
Transcortical operations were mainly performed for tumors of the pineal area, third ventricle and midbrain (25 cases), tumors of the lateral ventricles (26 cases), subcortical nuclei (10 cases) and hemispheric tumors (20 cases).
Postoperative neurological outcomes were divided into three categories: improvement, deterioration, no change. Surgery-associated mortality was defined as death within 30 days after surgery. Preoperative and postoperative MRI data were analyzed to assess quality of resection. Complete resection (100%) was defined as the absence of visible contrast-enhanced residual tumor or hyperintense signals in T2-weighted and FLAIR images. Almost complete resection was defined as resection of more than 90% of tumor volume, subtotal — 75—90% of tumor, partial — less than 75% of tumor and open biopsy. MRI was performed in 173 patients within various dates after surgery (from 2 days to 3 months). In other cases, MRI was impossible to be carried out. In these patients, quality of resection was evaluated considering CT data and intraoperative findings in 18 cases. Quality of resection was not evaluated in 9 (4.5%) cases.
Total resection in patients with hippocampal sclerosis was determined by resection of amygdala, hippocampus and parahippocampal gyrus up to projection of the quadruple plate.
Postoperative in-hospital CT was performed in all patients to identify possible complications.
Surgical equipment
All operations were performed using standard microsurgical instruments without retractors, endoscopic techniques or navigation. All procedures were carried out using OPMI NC-4 microscope (in rare cases OPMI Pentero). MARI device [8] was installed on the microscope in all cases to control its function (Pitskhelauri D., 2014). This device is useful for hands-free positioning of the microscope in all directions and correction of optical parameters.
Position on the operating table
Surgeries were performed under general endotracheal anesthesia. The patient's head was fixed in a head-holder with three brackets. Patient’s position on the operating table was selected depending on surgical approach. Most of patients underwent surgery in a horizontal position. Supine position was in 161 (80%) patients, prone position – in 4 (2%) cases, lateral position – in 1 patient. Patient's sitting position was preferred in 34 (17%) cases.
Burr hole drilling and wound closure
A 4-cm linear incision of soft tissues was performed in layer-by-layer fashion including the periosteum. The edges of incision were extended using one retractor. Burr hole was superimposed using The Codman Neuro Disposable Perforator with a diameter of 14 mm. Inner bone plate was resected by bone cutters in such a way that the channel through the skull bones took the form of a truncated cone with upper diameter of 14 mm and inner diameter of 18 mm (Fig. 2).
Dura mater was opened in X-shaped fashion as a rule (in rare cases — U-shaped dissection). The flaps of the dura were retracted on the stay-sutures. Subsequent surgical stages were performed in accordance with standard microsurgical technique.
Completion of the main surgical stage and hemostasis was followed by dura mater closure using one of the following methods: a) closure with one interrupted suture so that all four flaps converged with each other in the center of the burr hole (Fig. 1c); b) dura closure with several sutures or continuous suture. The first method was applied in 110 cases, the second one — in 90 patients. Tachocomb patch 2x2 cm was superimposed in all cases in order to seal the sutures. Wax and medical glue (Evisel) were used in rare cases of retrosigmoid approach (Fig. 3)
Burr hole surgery for resection of vestibular schwannoma is shown in Fig. 3.
Quality of resection was evaluated in 167 patients considering MRI and CT data. However, 6 patients were excluded from the analysis since they underwent drainage of CSF cysts or dissection of adhesions in ventricular system. Moreover, those patients who underwent scheduled open biopsy were also excluded (n=18). Complete resection was achieved in 118 cases (71%), almost complete resection — in 27 (16%) cases, subtotal resection — in 15 (9%) cases and partial resection — in 7 (4%) cases. In general, complete and almost complete resection was achieved in 145 (87%) cases (Table 3).
Duration of surgery from incision of soft tissues and closure of the wound ranged from 35 to 300 min (median 80). Duration of operations depending on localization of tumors is shown in Table 3.
Resection of hemispheric tumors (gliomas, metastases), neoplasms of pineal area and third ventricle required minimal time (median 60 and 65 min, respectively). Maximum time was required for resection of advanced tumors of ventricular system involving several ventricles (median 210 min).
The median of surgery time was 65 min in the group of patients who underwent microsurgical ventriculostomy and simultaneous biopsy.
Time of weaning from ventilator in postoperative period ranged from 5 min to 5 days (median 70 min). Patients after selective subtemporal amygdalohippocampectomy were weaned from ventilator 40 min earlier compared with other patients.
Patients were verticalized at different terms after surgery (from the first day to 20 days). The vast majority of patients (n=195) were verticalized within the first 3 days.
Clinical improvement was observed in 126 (63%) patients, no significant postoperative changes were found in 62 (31%) cases, deterioration — in 11 (5.5%) cases.
One patient died on the 14th day after resection of parietal lobe metastasis from metastatic lesion of lungs, adrenal glands and femur followed by multiple organ failure.
Microsurgical ventriculostomy
Microsurgical third ventriculostomy was performed in 27 cases for correction or prevention of occlusive hydrocephalus. Stenting of cerebral aqueduct was made in 2 cases. Additional bypass of ventricular system was no required after these operations.
In the group of ventriculostomy, open biopsy of pineal or third ventricle tumor was performed in addition to perforation of third ventricle bottom in 13 cases. Biopsy was informative in all cases. In 5 cases, ventriculostomy was performed for adhesions in ventricular system, benign aqueduct obstruction and cerebrospinal fluid cyst (cavum vergae). In the other 10 cases, ventriculostomy was performed at the final stage of resection of deep median tumors.
Stenting of stoma was performed in 9 (33%) patients after ventriculostomy to prevent its occlusion. These operations were performed for tumors of pineal area, third and lateral ventricles, as well as lesion of the optic tubercle.
Subtemporal selective amygdalohippocampectomy
Selective subtemporal amygdalohippocampectomy (n=24) for pharmacoresistant hippocampal sclerosis resulted resection of amygdala, hippocampus and parahippocampal gyrus. Posterior boundary of resection reached the projection of lateral geniculate body or quadrigeminal plate. In 23 cases, postoperative CT confirmed scheduled quality of resection. Residual hippocampus body and tail were observed only in one case. Therefore, the patient underwent redo resection of hippocampus through the existing burr hole.
All patients were followed-up. Postoperative follow-up period ranged from 6 to 20 months (median 12). MRI performed within 2—6 months after surgery confirmed adequate resection of medial temporal lobe complex in all patients. Engel class 1 of seizure control was achieved in 77.2%, class 1a — in 72.7% of cases.
Complications
Intracerebral hemorrhage after resection of tumor occurred in 4 cases that required redo surgery and emergency removal of hematoma. Debridement of hematoma through the previous burr hole was performed in 3 cases. Additional osteoplastic craniotomy was required in 1 case. In one case, transcortical resection of large neurocytoma of the right lateral ventricle was followed by epidural hematoma. In this patient, redo osteoplastic craniotomy and removal of hematoma were urgently performed.
Postoperative CSF leakage after surgery of posterior cranial fossa was observed in 4 (2%) cases. This complication occurred in 3 cases of retrosigmoid approach (8% of all retrosigmoid accesses) and in 1 case of median suboccipital approach. There were no differences between dura mater closure with one interrupted suture and several or continuous sutures. Additional sutures on the wound and several lumbar punctures with drainage of cerebrospinal fluid were effective to stop CSF leakage.
A single epileptic seizure developed in 1 patient after transcortical transventricular subchoroidal approach to pineal tumor. Symptoms of short-term aseptic meningitis were revealed in another patient with vestibular nerve schwannoma. Cognitive impairment was noted in both cases.
Facial paresis occurred in 5 patients after resection of vestibular schwannoma (18.5% of all schwannomas) and 1 patient after resection of epidermoid cyst of the cerebellopontine angle.
In two cases, severe condition was due to lesion of the midbrain. Aphatic disorders developed in 3 cases. Bulbar syndrome was observed in 1 case, hemiparesis — in 4 cases.
Pre- and postoperative visual field assessment was performed in 14 patients who underwent selective amygdalohippocampectomy through subtemporal approach. Standard automated perimetry system was used for this purpose (Humphrey II-370 visual field analyzer). Visual field loss was absent in 4 out of 14 patients. Homonymous upper quadrant hemianopsia was detected in 10 patients (71%), and none of these patients had visual defect within 20° of visual field.
Minimally invasive microsurgical approaches are currently developed to all brain zones (pineal area [9–10], different meningiomas [11–13], ventricular tumors [14], chiasmal-sellar area [15—16], insula, medial temporal complex [17—21], hemispheric gliomas and various metastases [22—24], vestibular schwanoma [25—28], approaches for vascular surgery [6, 29—31], supraorbital area [4, 7, 13, 32—34], pediatric surgery [35], minipterional approach [5, 31, 36] for endoscopic ventriculostomy [37]).
Craniotomy up to 20x30 mm is sufficient for microsurgical manipulations in “keyhole” surgery.
Procedures through this small craniotomy are possible thanks to the achievements of modern microneurosurgery. Modern operating microscopes with powerful lighting and multiple magnification, microsurgical instruments, navigation systems, endoscopic equipment are valuable for successful minimally invasive surgery.
The difficulty of manipulations through a small craniotomy is determined by not only insufficient illumination of the object of interest in the depth of the wound. Smaller burr hole implies more intense interaction of surgeon with microscope for its reposition and optimal visualization (Fig. 4).
A device for control of operating microscope (“MARI”) was developed and introduced into clinical practice in 2006 at the Burdenko Neurosurgery Center [8]. This equipment allows hands-free positioning of operating microscope in any direction without distraction from surgical field. To date, the first author of this report has completed over 3,000 neurosurgical procedures using this device. Frequent and easy hands-free movements of microscope around surgical field contributed to gradual narrowing of craniotomy for deep tumors. The constant presence of two micro-tools within surgical wound allows adequate manipulations in the depth of the wound through a narrow craniotomy without the use of retractors. Our preliminary unpublished data confirm that MARI device is accompanied by at least 5 times higher frequency of movement of the microscope than overall frequency of movements (manual + mouth switch) reported by S. Eivazi et al [38].
It is clear that frequent hands-free movements of microscope are useful to visualize the target under different angles for a short period. Moreover, these movements are associated with continuous manipulations in surgical wound by both hands. At the same time, microsurgical tools are also used as retractors. Undoubtedly, complete visualization of the target increases surgical accuracy and safety.
We have not found literature data devoted to microsurgical resection of intracranial tumors through a burr hole in the skull with a diameter of 14 mm. Dimension of the smallest craniotomy in “keyhole” surgery is 2×3 cm.
Microsurgery using a tubular retractor with a diameter of 18 mm is more approximate option for “burr hole” surgery [39]. Deployment of this retractor requires burr hole with a diameter of 30 mm to determine the site of corticotomy and freely change the angle of attack.
Does it make sense to use small “entrance gate” inside the skull? In our opinion, it is advisable for the following reasons: 1) reduced surgery time and duration of anesthesia due to fast craniotomy and closure of the wound. Median of surgery time was 80 min in our sample; 2) “burr hole” surgery is associated with exposure of less area of the cortex, that protects the brain from the contact with external environment (air, surgical instruments, light beam of the microscope, etc.); in addition, burr hole edges protect the brain from unnecessary traction, which inadvertently occurs during standard craniotomy; 3) less area of burr hole craniotomy reduces the risk of air embolism in case of infratentorial supracerebellar approach in patient’s sitting position in comparison with “keyhole” craniotomy; 4) “burr hole” surgery is associated with reduced risk of dissection of mastoid or frontal sinuses (supraorbital, retrosigmoid approaches) or less length of sinus wall defect in case of dissection in comparison with “keyhole” surgery; 5) burr hole more effectively prevents brain traction in comparison with “keyhole” craniotomy; different brain surface areas exposed in “keyhole” and “burr hole” surgery are obvious. Keyhole craniotomy area is 600 mm2 (20x30 mm), while burr hole craniotomy area is 150 mm2 (S= χr2). Therefore, burr hole craniotomy area is 4 times smaller than keyhole craniotomy area.
Even minor brain tractions result indirect dislocation of adjacent and distant structures in addition to local effect [40–41]. In our opinion, this factor is very important since we do not yet know the consequences of even “small” brain tractions in different areas (for example, vein compression followed by impaired venous circulation). In general, we are guided by a simple truth that ideal neurosurgery should be accompanied by minimum resection and/or retraction of brain tissue during surgical approach. Our results confirm this concept, although there is yet no clear statistical evidence. Nevertheless, it is obvious that burr hole surgery is associated with reduced duration of operation and less brain injury. As a result, faster postoperative waking up of patients is observed (median time of weaning from ventilator — 70 min). Verticalization on the day of surgery or the next day was observed in 181 (90.5%) cases. In our opinion, fast postoperative recovery is due to not only precise and accurate manipulations in close proximity to the target, but also minimal incisions of brain matter and dynamic traction of neurovascular structures within surgical approach.
Postoperative hospital-stay is generally accepted indicator of recovery after surgery. In accordance with in-hospital protocol of the Burdenko Neurosurgery Center, patients are discharged after removal of sutures (the 6th—7 day). Therefore, it was impossible to evaluate recovery time depending on length of postoperative hospital-stay.
Postoperative clinical deterioration was noted in 12 cases (6%). This was mainly due to appearance or exacerbation of local brain damage around the target (hemiparesis, facial nerve paresis, oculomotor disorders, etc.) rather approach per se.
The main cause of craniotomy enlargement in 8 patients was wrong localization of the burr hole in relation to superior sagittal (2 cases) and sigmoid sinuses (4 cases) in anterior hemispheric and retrosigmoid approaches. In other two cases, craniotomy was enlarged due to large epidural hematoma and extremely dense structure of large meningioma of inferior sagittal sinus with its close contact with pericallous arteries.
Inaccurate choice of localization of the burr hole in retrosigmoid approach determines the need for active use of navigation system. It is necessary to determine the correct trajectory of approach and localization of the burr hole.
Burr hole surgery with preliminary planning of surgical intervention was successful in other 200 cases. Thus, complete or almost complete resection was performed in 145 out of 167 patients who were scheduled for maximum possible resection of tumor or excision of medial temporal complex for hippocampal sclerosis.
“Burr hole” vs “Keyhole”
We compared effectiveness of “keyhole” and “burr hole” surgery for intracranial tumors and hippocampal sclerosis. It should be noted that certain essential data including duration of surgery, tumor dimensions, quality of resection, etc. are absent in most of available reports devoted to “keyhole” surgery. We summarized the main results of minimally invasive interventions for various intracranial tumors and hippocampal sclerosis reported by various authors (Table 4).
Thus, tumor dimensions or volumes are reported only in 4 reports devoted to vestibular schwannomas and hemispheric gliomas.
In our sample, complete and almost complete resection was achieved in 86% of patients (70% and 16%, respectively) who were scheduled for maximum possible resection of tumor. According to the data in the Table 4, the percentage of complete resection of various intracranial neoplasms is 59—100% in case of “keyhole” microsurgery.
Keyhole subtemporal or transtemporal amygdalohippocampectomy results postoperative seizure control (Engel class I) in 78—87% of patients with hippocampal sclerosis followed by epilepsy [17, 19, 20]. This value was 77% in our sample that is acceptable for surgery of hippocampal sclerosis.
According to the Table 3, burr hole surgery is associated with significantly less duration of intervention while other parameters of burr hole and keyhole approaches are similar. According to the literature data, median duration of “keyhole” surgery is 193 min, while this value was 80 min in our sample. Moreover, median duration of surgery was 90 min in those patients who were scheduled for maximum possible resection of tumor or standard selective amygdalohippocampectomy. This value is 2 times less compared with literature data.
Postoperative complications and recovery
Complications occurred in 5 patients (hemorrhage within the bed of excised tumor in 4 patients and epidural hematoma in 1 patient). Emergency operations were required in all these cases. Interventions were successful as a rule. However, 1 patient died after resection of hemispheric metastasis and debridement of hematoma in the bed of excised tumor. Death occurred due to somatic complications caused by multiple metastases in other organs.
CSF leakage was observed only in 4 (2%) patients despite leaky closure of the dura mater. It was found that all these events were recorded after operations on posterior cranial fossa through infratentorial or median suboccipital burr hole approach. Accordingly, there were no cases of CSF leakage among patients with supratentorial tumors.
Incidence of CSF leakage in retrosigmoid approach was 5%, among patients with schwannoma — 3.7%. M. Renovanz et al. (2015) found this complication in 16 cases (12%) including 9 patients after supratentorial approach and 7 patients after infratentorial approach [35].
H. Shahinian [27] reported CSF leakage in 3% of patients with schwannoma. B. Mostafa [26] revealed this complication in 15% of patients with various lesions of cerebellopontine angle after retrosigmoid surgery.
Burr hole surgery: further development
We would like to emphasize certain negative aspects despite favorable outcomes reported in our research. In our opinion, these aspects are not directly disadvantages of burr hole surgery. However, these drawbacks do not currently allow placing this method as an alternative to conventional approaches along with keyhole surgery.
These are retrospective analysis, absence of follow-up data, control group of patients and pre- and postoperative neuropsychological analysis. However, we are convinced that further development of burr hole technology in neurosurgical practice will contribute to development of minimally invasive burr hole microneurosurgery as a new surgical direction. These interventions will be associated with minimal injury of brain matter, reduced time of anesthesia and surgery.
We repeat the words of Donald H. Wilson, who emphasized the need for large craniotomy in some cases. He noted that “we do not make a fetish from keyhole surgery. Large arteriovenous malformations, hemispherectomy and some cases of epilepsy definitely require standard craniotomy”.
Burr hole microneurosurgery is valuable for surgical treatment of various intracranial lesions through a smaller craniotomy compared with keyhole surgery. In our opinion, this approach reduces injury of not only superficial tissues but, most importantly, brain itself.
Our preliminary results confirm the promising nature of burr hole microneurosurgery. Further prospective study is required to understand the capabilities of this method.
Authors’ participation
Concept and design of the study: D.P., A.B., K.E.
Collection and analysis of data: K.E., A.B., G.N., M.T.
Statistical analysis: D.P., K.E., A.B., G.N., S.A., M.T.
Writing the text: D.P.
Editing: D.P., P.I.
The authors declare no conflict of interest.
In my opinion, the research of D.I. Pitskhelauri et al. is an outstanding achievement of modern neurosurgery.
Resection of brain tumor or other lesion through burr hole approach is not an end in itself. Dimension of craniotomy should provide successful complete resection with minimal risk for a patient.
Nevertheless, miniaturization of approach is justified, since it not only reduces soft tissue trauma, but also protects the brain from damage to some extent due to limited surgical area.
Resection of various brain tumors or other interventions on the deep brain structures through burr hole approach became possible and justified only thanks to invention and widespread use of MARI device in everyday practice. This equipment was developed by D.I. Pitskhelauri and represented by a special helmet connected with operating microscope. This device allows positioning of the microscope, changing magnification and illumination so that surgical object is always in focus. These features ensure safe manipulations. This equipment fundamentally changes the possibility of operations under the microscope and facilitates surgery without spatulas.
I want to congratulate D.I. Pitskhelauri and his assistants with an outstanding achievement, which has no equal in modern neurosurgical literature.
However, I would like to emphasize certain aspect. It concerns the desire of D.I. Pitskhelauri, perhaps subconsciously, to prove that most tumors may be successfully resected through a burr hole. This is true even for those lesions with well-developed technique of resection, for example, auditory neurinoma. Resection of these tumors implies trepanation of auditory meatus, that is hardly feasible through a burr hole.
The author’s desire to set a record in surgical capabilities is guessed in this ambition. This desire is laudable, but the records are good in sports while in medicine their role is doubtful. Neurosurgeon must measure his capabilities and choose an approach for adequate surgery with minimal risk for a patient.
This report cannot be regarded as a call to resect brain tumors and perform other complex interventions only through a burr hole approach.
The main goal is to show that microsurgery is developing and its capabilities are far from exhausted. The use of these opportunities will contribute to successful treatment of the most complex brain and spinal cord diseases.
A.N. Konovalov (Moscow, Russia)
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