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The Stony Brook awake craniotomy protocol: A technical note
Journal of Clinical Neuroscience 67 (2019) 221–225
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Tools and techniques
The Stony Brook awake craniotomy protocol: A technical note Erica Shen a, Colleen Calandra b, Sofia Geralemou c, Christopher Page c, Raphael Davis b, Wesam Andraous c, Charles Mikell b,⇑ a
Stony Brook University School of Medicine, United States Department of Neurosurgery, Stony Brook University Hospital, United States c Department of Anesthesiology, Stony Brook University Hospital, United States b
a r t i c l e
i n f o
Article history: Received 16 December 2018 Accepted 21 June 2019
Keywords: Awake craniotomy Cortical mapping Functional testing Anesthesiology techniques
a b s t r a c t Most current awake craniotomy techniques utilize unnecessarily complicated airway management, and cause discomfort to the patients during the awake phase of the surgery. Our manuscript is written to discuss the neurosurgical and anesthetic techniques that we have developed to optimize awake craniotomy techniques at Stony Brook University Medical Center. We used the frameless BrainlabTM skull-mounted array for stereotactic navigation. Rigid fixation of the skull was avoided. General anesthesia with established airway was used during the ‘‘asleep” phase of the surgery. Following the removal of the bone flap and the opening of the dura, the patients were woken up, and the established airway was removed. Cortical mapping was performed to establish a safe entry zone for tumor removal. While the tumors were being removed, we continued motor examination and casual conversation with the patients to ensure safety. Patients were sedated during the remaining phase of the surgery until skin closure. No patient exhibited any neurological deficits or adverse anesthesia outcomes during the postoperative period. The protocol we developed avoids rigid skull fixation and emphasizes flexible intraoperative planning, thereby maximizing patient and physician comfort while allowing for successful tumor resection. Ó 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction Primary and metastatic brain tumors are a significant public health burden in the United States. Many gliomas and metastatic tumors are located within or near an eloquent region of the brain, such as functional areas involved in motor or speech processes. Awake craniotomy, a technique that allows for intraoperative cortical mapping and functional testing, has emerged as the current treatment of choice for resection of brain tumors that involve an eloquent region of the brain [6,13]. The technique, which allows for an interdisciplinary team’s interaction with an awake patient during the operation, has been shown to aid a larger extent of tumor resection while minimizing the risk of causing or worsening a new or a pre-existing neurological deficit during the surgery [7,18,24,25]. Most anesthetic and surgical methods that have been described in the literature separate the awake craniotomy procedure into three phases [1]. Craniotomy and opening of the dura under
⇑ Corresponding author at: Stony Brook Medicine, Department of Neurosurgery, 101 Nicolls Rd, Stony Brook, NY 11794, United States. E-mail address: [email protected] (C. Mikell).
general anesthesia take place during the first phase. During the second phase, patient is awakened and extubated, electrical stimulation of the cortex is performed to plan the corticectomy, and functional testing is conducted during resection of the tumor. During the third phase, closure of the cranium and scalp is performed. Among the published protocols, patients are uniformly awake during the second phase of the procedure to allow for interactions with the interdisciplinary team. Published protocols differ in anesthetic strategies applied during the first phase and the last phase of an awake craniotomy, with two types of protocols being the most well-known [21]. The ‘‘asleep-awake-asleep” protocol calls for the placement of the patient under general anesthesia with a supported airway during the first phase, has the patient awaken with removal of the supported airway in order to attend to functional testing during the second phase, and then has the patient reanesthetized with an re-established airway during the final phase [9,11,14,23]. The ‘‘conscious sedation” protocol calls for a deepened sedation with spontaneous respiration during the initial and final phase of the surgery, and has the patient awaken during the second phase to allow for functional testing [4,8,9]. A substantial minority of patients report moderate to severe discomfort during awake craniotomies, with some pain and
https://doi.org/10.1016/j.jocn.2019.06.042 0967-5868/Ó 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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anxiety that can be directly attributed to the rigid pinning of the head to a three-point Mayfield head frame, initial local anesthesia injection, and scalp opening [8,15,30]. Almost all published protocols employ the use of a Mayfield head frame. To reduce patientreported anxiety, we established a protocol to locate and resect the brain lesion without head pinning by carefully positioning a patient’s head at the start of an operation and by utilizing the Brainlab cranial navigation system. Airway management during different phases of surgery can be challenging, especially if different levels of arousal are required from the patient. Non-rigid positioning of the head on a donut or horseshoe headrest allows the patient to move his or her neck as needed to maximize comfort and allows the anesthesiologist extensive access to the airway during transitional phases of the surgery. General anesthesia offers a number of potential advantages over sedation for the initial phase of the surgery. Mechanical ventilation under general anesthesia helps to regulate brain volume to a certain extent, which can be helpful in a clinical situation where intracranial pressure may be increased due to a tumor mass [11]. Furthermore, because the airway is secured at the beginning of the surgery, our protocol allows us to make a ‘‘game-time” decision on whether the patient requires extubation and functional testing. The flexibility to make an impromptu decision intraoperatively can be beneficial, for instance, if the tumor clearly comes to the surface upon opening the dura. In that case, the step of extubation and functional testing is no longer essential and can be easily avoided, as it is safe to maintain the patient under general anesthesia with a protected airway. At Stony Brook University Hospital, we have developed a protocol that avoids rigid skull fixation and simplifies airway management. We believe that our protocol can help to maximize patient and physician comfort while allowing for successful tumor resection. 2. Methods 2.1. Patient selection and preoperative preparation Patients were in good general health to tolerate surgery and had reasonable airway mechanics. To minimize anxiety, we gave patients 2 mg of midazolam prior to departing for the operating room. 2.2. Operation room setup Each patient was positioned in the operation room with his or her head facing the instruments. We arranged the anesthesiologist, the vital sign monitors (indicating electrocardiography (ECG), noninvasive blood pressure, pulse oximetry and capnography), and the Brainlab cranial navigation apparatus (BrainLAB AG, Munich, Germany) to the side of the patient. We attached the Brainlab skull-mounted reference array (52121B/52129) to the patient’s forehead, away from the site of the planned craniotomy. The operating microscope was placed near the patient’s head, but the ultrasound, the Mayo stand, the Sonopet ultrasonic aspirator, and the ceiling-mounted boom containing cautery generators and suction were at the patient’s feet. The details of the operation setup are depicted in Fig. 1. 2.3. Patient positioning We positioned patients who underwent frontal craniotomy in the supine position. The head of the patient was placed on a Styrofoam donut, in a neutral position. We positioned patients who underwent temporal craniotomy in the lateral decubitus position. The head of the patient was elevated with either multiple blankets
Fig. 1. Operation Room Set-Up. Instruments have been labeled in the figure. The brown hexagon represents the patient’s head position. The two red circles represent the operating surgeon and his or her assistant. The two green triangles represent the anesthesiologists. The purple pentagon represents the circulating nurse.
or a Styrofoam donut. The patient’s ‘‘down” arm, which was wearing the blood pressure cuff, was extended towards the anesthesiologists (Fig. 2). Three-point rigid fixation of the skull was not used. We draped using a single ‘‘hip drape” from 3 M, which made a large space for the anesthesiologist and the patient to be face-to-face and to talk. 2.4. Surgical and anesthetic procedure After careful positioning of the patient and general monitoring, patients received IV propofol (2 mgkg 1), remifentanil infusion (0.05 lg 1kg 1min 1 in 5 min) and rocuronium (1 mgkg 1). We inserted a laryngeal mask airway (LMA) or endotracheal (ET) tube to secure the airway. Anesthesia was maintained with IV propofol (50–75 lg 1kg 1min 1) and remifentanil (0.05 lg 1kg 1min 1) infusions until awakening. For the awake portion of the surgeries, patients received dexmedetomidine infusions starting at 0.2 lg 1 kg 1h 1 with the dose titrated up 0.7 lg 1kg 1h 1, as needed for anxiolysis. The location of tumor(s) was confirmed with the Brainlab cranial navigation system prior to the planning of the incision site. We then shaved, prepped, and draped the surgical area in a sterile fashion. Our usual perioperative medications included 0.5–1 g of levetiracetam (anticonvulsant), 10 mg of dexamethasone (corticosteroid), 0.5 g/kg of mannitol, and 2 g of cefazolin IV for skin flora prophylaxis. We used a combination of sharp dissection and Bovie cautery to elevate the scalp. The neuronavigation system was again used to confirm that the surgical field provided enough exposure for tumor resection. We discontinued propofol and remifentanil fifteen minutes prior to the planned wakeup of the patient for cortical mapping and functional testing. IV sugammadex (2 mgkg 1) was given to the patient to reverse the effect of rocuronium. Once the patient began to follow commands, we removed the LMA or endotracheal tube. Dexmedetomidine was reduced to a level (0.2 lg 1 kg 1h 1) at which the patient was awake and conversational, with minimum achievable discomfort and anxiety. 2.5. General cortical mapping techniques We conducted cortical mapping and functional testing when the patient was awake and conversational. Specifically, we used a
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areas that were negative for language function were resected during corticectomy. 2.8. Tumor resection and skin closure We resected tumors using a combination of blunt dissection, bipolar electrocautery, and the Sonopet ultrasonic aspirator. The extent of tumor resection confirmed with intraoperative ultrasound. After meticulous hemostasis, we closed the dura, skull, and skin. During this phase of the surgery, we either re-intubated the patients or sedated them with a combination of remifentanil (0.05 lg 1kg 1min 1) and dexmedetomidine (0.2–0.7 lg 1 kg 1h 1). 3. Results & illustrative cases: 3.1. Case 1: awake motor mapping A 49-year-old man presented with focal seizures and was found to a frontal mass adjacent to the precentral gyrus measuring 2.5 cm 1.7 cm with moderate surrounding edema. He had some
Fig. 2. Lateral patient positioning for language mapping. Top Left: a patient who underwent temporal craniotomy was positioned in the lateral decubitus position. The patient’s head was elevated with blankets and a Styrofoam donut, with his ‘‘down” arm extended towards the anesthesiologist. Top Right: the incision site was marked for temporal craniotomy. Bottom Left: patient was draped with a single ‘‘hip drape” from 3 M, which allows for anethesiologists and neurologists to interact with the patient during the procedure. Bottom Right: the surgical site after the dura is opened.
hand-held bipolar stimulator for direct cortical electrical stimulation, and a six-contact recording electrode over the surface of the cortex close to the location of stimulation for electrocorticography (ECoG) recording. Prior to mapping, we administered a series of stimuli to the cortex, each for five seconds, increasing the amplitude by 1 mA each time, until an afterdischarge was obtained on ECoG recording [16,29]. 2.6. Motor mapping We obtained a baseline neurological exam of hand, arm, and leg strength prior to resection of the tumor. Areas that are near eloquent motor regions were stimulated, and a positive stimulation site was identified if a patient began to develop contralateral motor movement during stimulation. Only tumor-containing areas that were negative for motor function were resected during corticectomy. 2.7. Language mapping We established baseline language function prior to resection of the tumor. We used a series of tasks including word repetition, object identification, and comprehension during cortical mapping to identify critical sites. Areas that are near eloquent speech regions were mapped, and a positive stimulation site was identified if the stimulated patient began to develop difficulties in any of the language tests during stimulation. Only tumor-containing
Fig. 3. T2-weighted axial MRI images demonstrating pre-operative vs. postoperative changes a. Left frontal craniotomy with awake motor mapping; b. Left temporal craniotomy with awake language mapping; c. Left temporal craniotomy under general anesthesia where the tumor was easily identifiable.
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subtle hand weakness on neurological examination. During resection of tumor, the patient developed subjective hand weakness, tumor resection was halted as a result. Subtotal tumor resection was obtained (Fig. 3a). At the two-month follow-up visit, the patient was found to have full motor and sensory function in his hand. The patient stated that he was able to use his computer without difficulty. 3.2. Case 2: awake language mapping A 43-year-old woman with a history of breast cancer presented with a seizure and word-finding difficulties and was found to have a left posterior temporal lesion (measuring 1.7 cm 1.7 cm 1.4 cm, Fig. 3b). Left temporal craniotomy was performed with total tumor resection obtained. At the one-month follow-up visit, the patient’s language level was found to be near baseline. She was able to name objects without difficulty and to correctly interpret the meaning of a proverb (intact abstract reasoning). The patient stated that she had some subjective word-finding difficulty during speech, and when sending text messages, but was otherwise intact. 4. Discussion The protocol developed at Stony Brook departs from prior reported techniques in one primary aspect. We emphasize the careful initial positioning of the patient to avoid rigid head pinning during the initial phase of surgery. We believe that our avoidance of rigid head pinning in conjunction with the use of general anesthesia in Phase 1 of awake craniotomies may help to increase patients’ safety and comfort during the procedure. Avoidance of cranial pinning during the first phase of the surgery not only helps to alleviate feelings of discomfort and anxiety associated with the use of the Mayfield headholder [8,29], but also may help to prevent related complications from the procedure. Previous reports show that a substantial minority of patients express discomfort and anxiety, which we believe can be attributed partially to the first phase of the surgery, including rigid head pinning to the Mayfield stand [18,20]. Furthermore, seizure is a known possible complication in any craniotomy (occurring in 3– 18% cases) [26]. Complications such as dislocation of the head from the Mayfield headholder can occur as a result of patient agitation, uncoordinated movement, or seizure when emerging from general anesthesia to being awake or during cortical stimulation [5,12]. Although intraoperative seizures can generally be controlled with ice-cold saline, propofol, or midazolam [27], when such complications occur the operation is usually resumed under general anesthesia rather than in an awake setting [27]. Such intraoperative disruption can result in unnecessary distress on both the patient and the medical staff. With careful initial positioning of patients and with utilization of the Brainlab cranial navigation system, we were able to locate and resect the brain lesions without the rigid pinning of the patient’s head. We thus found that the use of a Mayfield head frame was unnecessary. The key to this flexible approach is having the airway fully secured and the head appropriately positioned without the use of rigid fixation. One potential disadvantage to our approach is that without rigid fixation of the head there is a theoretical risk that the patient’s head may move during tumor resection that may result in unwanted intraoperative complications. However, because the patient is awake during the tumor resection portion of the operation, continuous verbal communication with the patient has been enough to maintain the patient’s head in place during surgery. We are in support of placing patients under general anesthesia with a secured airway rather than sedating patients without a
secured airway during the first phase of the surgery for the following reasons. First, mechanical ventilation using an advanced airway in the asleep-awake protocol helps to avoid hypercapnia and regulate brain volume to a certain extent, which can be helpful and safer in a clinical situation where an increased intracranial pressure can often result from a tumor mass [11]. Mechanical ventilation under general anesthesia can also help to minimize alterations in intracranial pressure caused by compromised cerebral autoregulation or insufficient pain control [22]. Tight control of brain volume through respiratory regulation may be less crucial after tumor resection during the last phase of the surgery, when mass effects resulting from a tumor are no longer present. Second, general anesthesia used in the asleep-awake technique helps to better control for patients’ pain and anxiety. Third, it has been suggested the asleep-awake technique may help patients to be cooperate longer during the awake phase if they are unconscious during Phase 1 of surgery, especially when the procedure is expected to be long [17]. Last, optimal sedation is required in the monitored anesthesia care (MAC) technique to maintain the patient during surgery, which may be a delicate balance to accomplish. Too much sedation can lead to hypoxia, hypercarbia, respiratory depression, and noncooperation during intraoperative mapping. Too little sedation can result in patients experiencing significant anxiety and pain [10]. Because patients were under general anesthesia with an established airway during the first phase of the surgery, an impromptu decision regarding whether to wake up the patient for cortical mapping could be made based on the intraoperative appearance of the lesion. An established airway during the first phase allows for the patient to be maintained under general anesthesia in a relatively stress-free manner during tumor resection without the risk of respiratory desaturation that is sometimes associated with sedation without a secured airway [18,26]. We feel strongly that this flexible approach that provides options for intraoperative surgical decisions that can best suit a patient’s needs. For instance, in a patient where the tumor is in the margin of the cortex and can be easily identified and distinguished from the remaining cortex upon opening the dura, resecting the tumor while keeping the patient under general anesthesia helps to maximize the patient’s comfort and safety. One such situation occurred during one of our planned awake craniotomies. A patient with brain metastasis from lung adenocarcinoma required a left temporal craniotomy. Upon opening the dura, the patient’s tumor was bulging out in the surgical site. Because the tumor was easily identified, we elected to keep the patient under general anesthesia during tumor resection to minimize any unnecessary procedure and discomfort for the patient. In this case, we successfully achieved gross total resection of the tumor, as shown in Fig. 3c. Postoperatively and at the three-month follow-up visit, the patient revealed no notable cognitive dysfunction. Remifentanil, an opioid with a short half-life that is independent of rate of infusion allowing for rapid emergence from anesthesia, has been the drug of choice at many medical centers. However, the medication causes respiratory depression making it less ideal to use during sedation without respiratory support [28]. Dexmedetomidine, a highly specific a2-agonist with analgesic effects, has become popular in recent years [3]. Dexmedetomidine does not suppress ventilation and has been shown to decrease the amount of other sedative and opioid agents, thus reducing their adverse effects [2,19]. We have incorporated the recent development of co-usage of dexmedetomidine with remifentanil here at Stony Brook, which helps to decrease the amount of remifentanil used, thereby reducing remifentanil-induced respiratorydepressive effects during the third phase of awake craniotomy. A recently published article describes an ‘‘awake-awake-awake” craniotomy technique that does not require any sedation. The arti-
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cle emphasizes on a hand-in-hand/shoulder physical contact for emotional support from health providers to patients and on alternative relaxation techniques such listening to music and imaging mental images of vacationing elsewhere to reduce patients’ stress and anxiety that are evoked during the surgery [12]. Although this protocol took a very different approach from what we have described here at Stony Brook Medical Center, we may adopt some of methods described in their protocol such as increased physical contact between health providers and patients to further maximizing patient comfort during our awake craniotomy in the future. We did not include a large number of patients in our technical report. This is a limitation of the current protocol. A larger patient population should be included in a future study to allow a more detailed discussion of the benefits and drawbacks of our procedure compared to prior described procedures. 5. Conclusion At Stony Brook University Medical Center, we have developed a simple protocol for craniotomy under general anesthesia, with subsequent ‘‘wake-up” testing. The protocol avoids rigid skull fixation and emphasizes prompt intraoperative decisions based on clinical scenarios, helping to maximize patient and physician comfort while allowing for successful tumor resection. Ethics statement The current study received a formal exemption from the Stony Brook University Office of Research Compliance indicating that it did not require IRB approval. Activities included in the manuscript were conducted in compliance with applicable regulations. Informed written consent was obtained from the patient whose photos were used in the manuscript. Acknowledgement The authors would like to thank the Department of Neurosurgery at the Stony Brook University School of Medicine for the departmental funding that made the current project possible. References [1] Andersen JH, Olsen KS. Anesthesia for awake craniotomy is safe and welltolerated. Dan Med Bull 2010;10:A4194. [2] Ard Jr JL, Bekker AY, Doyle WK. Dexmedetomidine in awake craniotomy: a technical note. Surg Neurol 2005;63:114–7. [3] Bekker AY, Kaufman B, Samir H, Doyle W. The use of Dexmedetomidine infusion for awake craniotomy. Anesth Analog 2001;92:1251–3. [4] Berkenstadt H, Perel A, Hadani M, Unofrievich I, Ram Z. Monitored anesthesia care using remifentanil and propofol for awake craniotomy. J Neurosurg Anesthesiol 2001;13:246–9. [5] Bilotta F, Rosa G. ‘‘Anesthesia” for awake neurosurgery. Curr Opin Anaesthesiol 2009;22:560–5. [6] Brown T, Shah AH, Bregy A, Shah NH, Thambuswamy M, Barbarite E, et al. Awake or craniotomy for brain tumor resection: the rule rather than the exception? J Neurosurg Anesthesiol 2013;25:240–7.
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[7] Chacko AG, Thomas SG, Babu KS, Daniel RT, Chacko G, Prabhu K, et al. Awake craniotomy and electrophysiological mapping for eloquent area tumors. Clin Neurol Neurosurg 2013;115:329–34. [8] Danks RA, Rogers M, Aglio LS, Gugino LD, Black PM. Patient tolerance of craniotomy performed with the patient under local anesthesia and monitored conscious sedation. Neurosurgery 1998;42:28–36. [9] Dilmen OK, Akcil EF, Oguz A, Vehid H, Tunali Y. Comparison of conscious sedation and asleep-awake-asleep techniques for awake craniotomy. J Clin Neurosci 2017;35:30–4. [10] Frost EA, Booij LH. Anesthesia in the patient for awake craniotomy. Curr Opin Anaesthesiol 2007;20:331–5. [11] Fukaya C, Katayama Y, Yoshino A, Kobayashi K, Kasai M, Yamamoto T. Intraoperative wake-up procedure with propofol and laryngeal mask for optimal excision of brain tumor in eloquent areas. J Clin Neurosci 2001;8:253–5. [12] Hansen E, Seemann M, Zech N, Doenitz C, Luerding R, Brawanski A. Awake craniotomies without any sedation: the awake-awake-awake technique. Acta Neurochir 2013;155:1417–24. [13] Hervey-Jumper SL, Li J, Lau D, Molinaro AM, Perry DW, Meng L, et al. Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period. J Neurosurg 2015;123:325–9. [14] Huncke K, Van de Wiele B, Fried I, Rubinstein EH. The asleep-awake-asleep anesthetic technique for intraoperative language mapping. Neurosurgery 1998;42:1312–7. [15] Joswig H, Bratelj D, Brunner T, Jacomet A, Hildebrandt G, Surbeck W. Awake craniotomy: first-year experiences and patient perception. World Neurosurg 2016;90:588–96. [16] Kim SS, McCutcheon IE, Suki D, Weinberg JS, Sawaya R, Lang FF, et al. Awake craniotomy for brain tumors near eloquent cortex: correlation of intraoperative cortical mapping with neurological outcomes in 309 consecutive patients. Neurosurgery 2009;64:836–45. [17] Lobo FA, Wagemakers M, Absalom AR. Anaesthesia for awake craniotomy. Br J Anaesth 2016;116:740–4. [18] Manninen PH, Balki M, Lukitto K, Bernstein M. Patient satisfaction with awake craniotomy for tumor surgery: a comparison of remifentanil and fentanyl in conjunction with propofol. Anesth Analog 2006;102:237–42. [19] Mantz J, Josserand J, Hamada S. Dexmedetomidine: new insights. Eur J Anaesthesiol 2011;28:3–6. [20] Ostrom QT, Gittleman H, Farah P, Ondracek A, Chen Y, Wolinsky Y, et al. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United Sates in 2006-2010. Neuro Oncol 2013;15(Suppl. 2): ii1–ii56. [21] Paldor I, Drummond KJ, Awad M, Sufaro YZ, Kaye AH. Is a wake-up call in order? Review of the evidence for awake craniotomy. J Clin Neurosci 2016;23:1–7. [22] Quiney N, Cooper R, Stoneham M, Walters F. Pain after craniotomy. A time for reappraisal? Br J Neurosurg 1996;10:295–9. [23] Rajan S, Cata JP, Nada E, Weil R, Pal R, Avitsian R. Asleep-awake-asleep craniotomy: a comparison with general anesthesia for resection of supratentorial tumors. J Clin Neurosci 2013;20:1068–73. [24] Sacko O, Lauwers-Cances V, Brauge D, Sesay M, Brenner A, Roux FE. Awake craniotomy vs. surgery under general anesthesia for resection of supratentorial lesions. Neurosurgery 2011;68:1192–8. [25] Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping for glioma resection. N Engl J Med 2008;358:18–27. [26] Sarang A, Dinsmore J. Anesthesia for awake craniotomy-evolution of a technique that facilities awake neurological testing. Br J Anaesth 2003;90:161–5. [27] Sartorious CJ, Berger MS. Rapid termination of intraoperative stimulationevoked seizures with application of cold Ringer’s lactate to the cortex. Technical note. J Neurosurg 1988;88:349–51. [28] Sidaras G, Hunter JM. Is it safe to artificially ventilate a paralyzed patient through the laryngeal mask? The jury is still out. Br J Anaesth 2001;86:749–53. [29] Whittle IR, Borthwick S, Haq N. Brain dysfunction following ‘‘awake” craniotomy, brain mapping and resection of glioma. Br J Neurosurg 2003;17:130–7. [30] Whittle IR, Midgley S, Georges H, Pringle AM, Taylor R. Patient perceptions of ‘‘awake” brain tumor surgery. Acta Neurochir 2005;147:275–7.
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Tools and techniques
The Stony Brook awake craniotomy protocol: A technical note Erica Shen a, Colleen Calandra b, Sofia Geralemou c, Christopher Page c, Raphael Davis b, Wesam Andraous c, Charles Mikell b,⇑ a
Stony Brook University School of Medicine, United States Department of Neurosurgery, Stony Brook University Hospital, United States c Department of Anesthesiology, Stony Brook University Hospital, United States b
a r t i c l e
i n f o
Article history: Received 16 December 2018 Accepted 21 June 2019
Keywords: Awake craniotomy Cortical mapping Functional testing Anesthesiology techniques
a b s t r a c t Most current awake craniotomy techniques utilize unnecessarily complicated airway management, and cause discomfort to the patients during the awake phase of the surgery. Our manuscript is written to discuss the neurosurgical and anesthetic techniques that we have developed to optimize awake craniotomy techniques at Stony Brook University Medical Center. We used the frameless BrainlabTM skull-mounted array for stereotactic navigation. Rigid fixation of the skull was avoided. General anesthesia with established airway was used during the ‘‘asleep” phase of the surgery. Following the removal of the bone flap and the opening of the dura, the patients were woken up, and the established airway was removed. Cortical mapping was performed to establish a safe entry zone for tumor removal. While the tumors were being removed, we continued motor examination and casual conversation with the patients to ensure safety. Patients were sedated during the remaining phase of the surgery until skin closure. No patient exhibited any neurological deficits or adverse anesthesia outcomes during the postoperative period. The protocol we developed avoids rigid skull fixation and emphasizes flexible intraoperative planning, thereby maximizing patient and physician comfort while allowing for successful tumor resection. Ó 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction Primary and metastatic brain tumors are a significant public health burden in the United States. Many gliomas and metastatic tumors are located within or near an eloquent region of the brain, such as functional areas involved in motor or speech processes. Awake craniotomy, a technique that allows for intraoperative cortical mapping and functional testing, has emerged as the current treatment of choice for resection of brain tumors that involve an eloquent region of the brain [6,13]. The technique, which allows for an interdisciplinary team’s interaction with an awake patient during the operation, has been shown to aid a larger extent of tumor resection while minimizing the risk of causing or worsening a new or a pre-existing neurological deficit during the surgery [7,18,24,25]. Most anesthetic and surgical methods that have been described in the literature separate the awake craniotomy procedure into three phases [1]. Craniotomy and opening of the dura under
⇑ Corresponding author at: Stony Brook Medicine, Department of Neurosurgery, 101 Nicolls Rd, Stony Brook, NY 11794, United States. E-mail address: [email protected] (C. Mikell).
general anesthesia take place during the first phase. During the second phase, patient is awakened and extubated, electrical stimulation of the cortex is performed to plan the corticectomy, and functional testing is conducted during resection of the tumor. During the third phase, closure of the cranium and scalp is performed. Among the published protocols, patients are uniformly awake during the second phase of the procedure to allow for interactions with the interdisciplinary team. Published protocols differ in anesthetic strategies applied during the first phase and the last phase of an awake craniotomy, with two types of protocols being the most well-known [21]. The ‘‘asleep-awake-asleep” protocol calls for the placement of the patient under general anesthesia with a supported airway during the first phase, has the patient awaken with removal of the supported airway in order to attend to functional testing during the second phase, and then has the patient reanesthetized with an re-established airway during the final phase [9,11,14,23]. The ‘‘conscious sedation” protocol calls for a deepened sedation with spontaneous respiration during the initial and final phase of the surgery, and has the patient awaken during the second phase to allow for functional testing [4,8,9]. A substantial minority of patients report moderate to severe discomfort during awake craniotomies, with some pain and
https://doi.org/10.1016/j.jocn.2019.06.042 0967-5868/Ó 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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anxiety that can be directly attributed to the rigid pinning of the head to a three-point Mayfield head frame, initial local anesthesia injection, and scalp opening [8,15,30]. Almost all published protocols employ the use of a Mayfield head frame. To reduce patientreported anxiety, we established a protocol to locate and resect the brain lesion without head pinning by carefully positioning a patient’s head at the start of an operation and by utilizing the Brainlab cranial navigation system. Airway management during different phases of surgery can be challenging, especially if different levels of arousal are required from the patient. Non-rigid positioning of the head on a donut or horseshoe headrest allows the patient to move his or her neck as needed to maximize comfort and allows the anesthesiologist extensive access to the airway during transitional phases of the surgery. General anesthesia offers a number of potential advantages over sedation for the initial phase of the surgery. Mechanical ventilation under general anesthesia helps to regulate brain volume to a certain extent, which can be helpful in a clinical situation where intracranial pressure may be increased due to a tumor mass [11]. Furthermore, because the airway is secured at the beginning of the surgery, our protocol allows us to make a ‘‘game-time” decision on whether the patient requires extubation and functional testing. The flexibility to make an impromptu decision intraoperatively can be beneficial, for instance, if the tumor clearly comes to the surface upon opening the dura. In that case, the step of extubation and functional testing is no longer essential and can be easily avoided, as it is safe to maintain the patient under general anesthesia with a protected airway. At Stony Brook University Hospital, we have developed a protocol that avoids rigid skull fixation and simplifies airway management. We believe that our protocol can help to maximize patient and physician comfort while allowing for successful tumor resection. 2. Methods 2.1. Patient selection and preoperative preparation Patients were in good general health to tolerate surgery and had reasonable airway mechanics. To minimize anxiety, we gave patients 2 mg of midazolam prior to departing for the operating room. 2.2. Operation room setup Each patient was positioned in the operation room with his or her head facing the instruments. We arranged the anesthesiologist, the vital sign monitors (indicating electrocardiography (ECG), noninvasive blood pressure, pulse oximetry and capnography), and the Brainlab cranial navigation apparatus (BrainLAB AG, Munich, Germany) to the side of the patient. We attached the Brainlab skull-mounted reference array (52121B/52129) to the patient’s forehead, away from the site of the planned craniotomy. The operating microscope was placed near the patient’s head, but the ultrasound, the Mayo stand, the Sonopet ultrasonic aspirator, and the ceiling-mounted boom containing cautery generators and suction were at the patient’s feet. The details of the operation setup are depicted in Fig. 1. 2.3. Patient positioning We positioned patients who underwent frontal craniotomy in the supine position. The head of the patient was placed on a Styrofoam donut, in a neutral position. We positioned patients who underwent temporal craniotomy in the lateral decubitus position. The head of the patient was elevated with either multiple blankets
Fig. 1. Operation Room Set-Up. Instruments have been labeled in the figure. The brown hexagon represents the patient’s head position. The two red circles represent the operating surgeon and his or her assistant. The two green triangles represent the anesthesiologists. The purple pentagon represents the circulating nurse.
or a Styrofoam donut. The patient’s ‘‘down” arm, which was wearing the blood pressure cuff, was extended towards the anesthesiologists (Fig. 2). Three-point rigid fixation of the skull was not used. We draped using a single ‘‘hip drape” from 3 M, which made a large space for the anesthesiologist and the patient to be face-to-face and to talk. 2.4. Surgical and anesthetic procedure After careful positioning of the patient and general monitoring, patients received IV propofol (2 mgkg 1), remifentanil infusion (0.05 lg 1kg 1min 1 in 5 min) and rocuronium (1 mgkg 1). We inserted a laryngeal mask airway (LMA) or endotracheal (ET) tube to secure the airway. Anesthesia was maintained with IV propofol (50–75 lg 1kg 1min 1) and remifentanil (0.05 lg 1kg 1min 1) infusions until awakening. For the awake portion of the surgeries, patients received dexmedetomidine infusions starting at 0.2 lg 1 kg 1h 1 with the dose titrated up 0.7 lg 1kg 1h 1, as needed for anxiolysis. The location of tumor(s) was confirmed with the Brainlab cranial navigation system prior to the planning of the incision site. We then shaved, prepped, and draped the surgical area in a sterile fashion. Our usual perioperative medications included 0.5–1 g of levetiracetam (anticonvulsant), 10 mg of dexamethasone (corticosteroid), 0.5 g/kg of mannitol, and 2 g of cefazolin IV for skin flora prophylaxis. We used a combination of sharp dissection and Bovie cautery to elevate the scalp. The neuronavigation system was again used to confirm that the surgical field provided enough exposure for tumor resection. We discontinued propofol and remifentanil fifteen minutes prior to the planned wakeup of the patient for cortical mapping and functional testing. IV sugammadex (2 mgkg 1) was given to the patient to reverse the effect of rocuronium. Once the patient began to follow commands, we removed the LMA or endotracheal tube. Dexmedetomidine was reduced to a level (0.2 lg 1 kg 1h 1) at which the patient was awake and conversational, with minimum achievable discomfort and anxiety. 2.5. General cortical mapping techniques We conducted cortical mapping and functional testing when the patient was awake and conversational. Specifically, we used a
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areas that were negative for language function were resected during corticectomy. 2.8. Tumor resection and skin closure We resected tumors using a combination of blunt dissection, bipolar electrocautery, and the Sonopet ultrasonic aspirator. The extent of tumor resection confirmed with intraoperative ultrasound. After meticulous hemostasis, we closed the dura, skull, and skin. During this phase of the surgery, we either re-intubated the patients or sedated them with a combination of remifentanil (0.05 lg 1kg 1min 1) and dexmedetomidine (0.2–0.7 lg 1 kg 1h 1). 3. Results & illustrative cases: 3.1. Case 1: awake motor mapping A 49-year-old man presented with focal seizures and was found to a frontal mass adjacent to the precentral gyrus measuring 2.5 cm 1.7 cm with moderate surrounding edema. He had some
Fig. 2. Lateral patient positioning for language mapping. Top Left: a patient who underwent temporal craniotomy was positioned in the lateral decubitus position. The patient’s head was elevated with blankets and a Styrofoam donut, with his ‘‘down” arm extended towards the anesthesiologist. Top Right: the incision site was marked for temporal craniotomy. Bottom Left: patient was draped with a single ‘‘hip drape” from 3 M, which allows for anethesiologists and neurologists to interact with the patient during the procedure. Bottom Right: the surgical site after the dura is opened.
hand-held bipolar stimulator for direct cortical electrical stimulation, and a six-contact recording electrode over the surface of the cortex close to the location of stimulation for electrocorticography (ECoG) recording. Prior to mapping, we administered a series of stimuli to the cortex, each for five seconds, increasing the amplitude by 1 mA each time, until an afterdischarge was obtained on ECoG recording [16,29]. 2.6. Motor mapping We obtained a baseline neurological exam of hand, arm, and leg strength prior to resection of the tumor. Areas that are near eloquent motor regions were stimulated, and a positive stimulation site was identified if a patient began to develop contralateral motor movement during stimulation. Only tumor-containing areas that were negative for motor function were resected during corticectomy. 2.7. Language mapping We established baseline language function prior to resection of the tumor. We used a series of tasks including word repetition, object identification, and comprehension during cortical mapping to identify critical sites. Areas that are near eloquent speech regions were mapped, and a positive stimulation site was identified if the stimulated patient began to develop difficulties in any of the language tests during stimulation. Only tumor-containing
Fig. 3. T2-weighted axial MRI images demonstrating pre-operative vs. postoperative changes a. Left frontal craniotomy with awake motor mapping; b. Left temporal craniotomy with awake language mapping; c. Left temporal craniotomy under general anesthesia where the tumor was easily identifiable.
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subtle hand weakness on neurological examination. During resection of tumor, the patient developed subjective hand weakness, tumor resection was halted as a result. Subtotal tumor resection was obtained (Fig. 3a). At the two-month follow-up visit, the patient was found to have full motor and sensory function in his hand. The patient stated that he was able to use his computer without difficulty. 3.2. Case 2: awake language mapping A 43-year-old woman with a history of breast cancer presented with a seizure and word-finding difficulties and was found to have a left posterior temporal lesion (measuring 1.7 cm 1.7 cm 1.4 cm, Fig. 3b). Left temporal craniotomy was performed with total tumor resection obtained. At the one-month follow-up visit, the patient’s language level was found to be near baseline. She was able to name objects without difficulty and to correctly interpret the meaning of a proverb (intact abstract reasoning). The patient stated that she had some subjective word-finding difficulty during speech, and when sending text messages, but was otherwise intact. 4. Discussion The protocol developed at Stony Brook departs from prior reported techniques in one primary aspect. We emphasize the careful initial positioning of the patient to avoid rigid head pinning during the initial phase of surgery. We believe that our avoidance of rigid head pinning in conjunction with the use of general anesthesia in Phase 1 of awake craniotomies may help to increase patients’ safety and comfort during the procedure. Avoidance of cranial pinning during the first phase of the surgery not only helps to alleviate feelings of discomfort and anxiety associated with the use of the Mayfield headholder [8,29], but also may help to prevent related complications from the procedure. Previous reports show that a substantial minority of patients express discomfort and anxiety, which we believe can be attributed partially to the first phase of the surgery, including rigid head pinning to the Mayfield stand [18,20]. Furthermore, seizure is a known possible complication in any craniotomy (occurring in 3– 18% cases) [26]. Complications such as dislocation of the head from the Mayfield headholder can occur as a result of patient agitation, uncoordinated movement, or seizure when emerging from general anesthesia to being awake or during cortical stimulation [5,12]. Although intraoperative seizures can generally be controlled with ice-cold saline, propofol, or midazolam [27], when such complications occur the operation is usually resumed under general anesthesia rather than in an awake setting [27]. Such intraoperative disruption can result in unnecessary distress on both the patient and the medical staff. With careful initial positioning of patients and with utilization of the Brainlab cranial navigation system, we were able to locate and resect the brain lesions without the rigid pinning of the patient’s head. We thus found that the use of a Mayfield head frame was unnecessary. The key to this flexible approach is having the airway fully secured and the head appropriately positioned without the use of rigid fixation. One potential disadvantage to our approach is that without rigid fixation of the head there is a theoretical risk that the patient’s head may move during tumor resection that may result in unwanted intraoperative complications. However, because the patient is awake during the tumor resection portion of the operation, continuous verbal communication with the patient has been enough to maintain the patient’s head in place during surgery. We are in support of placing patients under general anesthesia with a secured airway rather than sedating patients without a
secured airway during the first phase of the surgery for the following reasons. First, mechanical ventilation using an advanced airway in the asleep-awake protocol helps to avoid hypercapnia and regulate brain volume to a certain extent, which can be helpful and safer in a clinical situation where an increased intracranial pressure can often result from a tumor mass [11]. Mechanical ventilation under general anesthesia can also help to minimize alterations in intracranial pressure caused by compromised cerebral autoregulation or insufficient pain control [22]. Tight control of brain volume through respiratory regulation may be less crucial after tumor resection during the last phase of the surgery, when mass effects resulting from a tumor are no longer present. Second, general anesthesia used in the asleep-awake technique helps to better control for patients’ pain and anxiety. Third, it has been suggested the asleep-awake technique may help patients to be cooperate longer during the awake phase if they are unconscious during Phase 1 of surgery, especially when the procedure is expected to be long [17]. Last, optimal sedation is required in the monitored anesthesia care (MAC) technique to maintain the patient during surgery, which may be a delicate balance to accomplish. Too much sedation can lead to hypoxia, hypercarbia, respiratory depression, and noncooperation during intraoperative mapping. Too little sedation can result in patients experiencing significant anxiety and pain [10]. Because patients were under general anesthesia with an established airway during the first phase of the surgery, an impromptu decision regarding whether to wake up the patient for cortical mapping could be made based on the intraoperative appearance of the lesion. An established airway during the first phase allows for the patient to be maintained under general anesthesia in a relatively stress-free manner during tumor resection without the risk of respiratory desaturation that is sometimes associated with sedation without a secured airway [18,26]. We feel strongly that this flexible approach that provides options for intraoperative surgical decisions that can best suit a patient’s needs. For instance, in a patient where the tumor is in the margin of the cortex and can be easily identified and distinguished from the remaining cortex upon opening the dura, resecting the tumor while keeping the patient under general anesthesia helps to maximize the patient’s comfort and safety. One such situation occurred during one of our planned awake craniotomies. A patient with brain metastasis from lung adenocarcinoma required a left temporal craniotomy. Upon opening the dura, the patient’s tumor was bulging out in the surgical site. Because the tumor was easily identified, we elected to keep the patient under general anesthesia during tumor resection to minimize any unnecessary procedure and discomfort for the patient. In this case, we successfully achieved gross total resection of the tumor, as shown in Fig. 3c. Postoperatively and at the three-month follow-up visit, the patient revealed no notable cognitive dysfunction. Remifentanil, an opioid with a short half-life that is independent of rate of infusion allowing for rapid emergence from anesthesia, has been the drug of choice at many medical centers. However, the medication causes respiratory depression making it less ideal to use during sedation without respiratory support [28]. Dexmedetomidine, a highly specific a2-agonist with analgesic effects, has become popular in recent years [3]. Dexmedetomidine does not suppress ventilation and has been shown to decrease the amount of other sedative and opioid agents, thus reducing their adverse effects [2,19]. We have incorporated the recent development of co-usage of dexmedetomidine with remifentanil here at Stony Brook, which helps to decrease the amount of remifentanil used, thereby reducing remifentanil-induced respiratorydepressive effects during the third phase of awake craniotomy. A recently published article describes an ‘‘awake-awake-awake” craniotomy technique that does not require any sedation. The arti-
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cle emphasizes on a hand-in-hand/shoulder physical contact for emotional support from health providers to patients and on alternative relaxation techniques such listening to music and imaging mental images of vacationing elsewhere to reduce patients’ stress and anxiety that are evoked during the surgery [12]. Although this protocol took a very different approach from what we have described here at Stony Brook Medical Center, we may adopt some of methods described in their protocol such as increased physical contact between health providers and patients to further maximizing patient comfort during our awake craniotomy in the future. We did not include a large number of patients in our technical report. This is a limitation of the current protocol. A larger patient population should be included in a future study to allow a more detailed discussion of the benefits and drawbacks of our procedure compared to prior described procedures. 5. Conclusion At Stony Brook University Medical Center, we have developed a simple protocol for craniotomy under general anesthesia, with subsequent ‘‘wake-up” testing. The protocol avoids rigid skull fixation and emphasizes prompt intraoperative decisions based on clinical scenarios, helping to maximize patient and physician comfort while allowing for successful tumor resection. Ethics statement The current study received a formal exemption from the Stony Brook University Office of Research Compliance indicating that it did not require IRB approval. Activities included in the manuscript were conducted in compliance with applicable regulations. Informed written consent was obtained from the patient whose photos were used in the manuscript. Acknowledgement The authors would like to thank the Department of Neurosurgery at the Stony Brook University School of Medicine for the departmental funding that made the current project possible. References [1] Andersen JH, Olsen KS. Anesthesia for awake craniotomy is safe and welltolerated. Dan Med Bull 2010;10:A4194. [2] Ard Jr JL, Bekker AY, Doyle WK. Dexmedetomidine in awake craniotomy: a technical note. Surg Neurol 2005;63:114–7. [3] Bekker AY, Kaufman B, Samir H, Doyle W. The use of Dexmedetomidine infusion for awake craniotomy. Anesth Analog 2001;92:1251–3. [4] Berkenstadt H, Perel A, Hadani M, Unofrievich I, Ram Z. Monitored anesthesia care using remifentanil and propofol for awake craniotomy. J Neurosurg Anesthesiol 2001;13:246–9. [5] Bilotta F, Rosa G. ‘‘Anesthesia” for awake neurosurgery. Curr Opin Anaesthesiol 2009;22:560–5. [6] Brown T, Shah AH, Bregy A, Shah NH, Thambuswamy M, Barbarite E, et al. Awake or craniotomy for brain tumor resection: the rule rather than the exception? J Neurosurg Anesthesiol 2013;25:240–7.
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