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Surgical Management of Brainstem Cavernous Malformation: Report of 67 Patients
Original Article
Surgical Management of Brainstem Cavernous Malformation: Report of 67 Patients Songbai Gui, Guolu Meng, Xinru Xiao, Zhen Wu, Junting Zhang
BACKGROUND: Brainstem cavernous malformations (CMs) are benign lesions, often show an acute onset, and result in a high rate of morbidity. Surgical resection could inhibit the progressive deterioration of neurologic function caused by repetitive hemorrhage. This study aimed to summarize timing, approaches, and techniques of surgery and to evaluate outcomes of treatment.
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METHODS: Between March 2011 and May 2013, 67 patients (32 male, 35 female; average age 40 years; range, 14e68 years) with brainstem CMs received surgical treatment. Clinical presentation, surgical approaches, and results of follow-up were retrospectively analyzed.
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RESULTS: Seven surgical approaches were used: orbitozygomatic approach (1 case), suboccipital transtentorial approach (Poppen approach; 3 cases), subtemporal transtentorial approach (32 cases), subtemporal transtentorial/ anterior petrosectomy approach (9 cases), suboccipital retrosigmoid approach (3 cases), midline suboccipital approach (16 cases), and far lateral approach (3 cases). Total resection of the brainstem CM was achieved in all cases (100%). No operative mortality was encountered. Nine patients had new symptoms after surgery: 3 had diplopia, 3 had facial numbness, 1 had numbness of contralateral limbs, 1 had transient aphasia, and 1 had reduced muscle strength of contralateral limbs. Symptoms significantly improved in 23 patients (34.3%), symptoms were unchanged in 36 patients (53.7%), and new postoperative symptoms occurred in 9 patients (13.4%).
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CONCLUSIONS: Choosing a proper surgical approach and using appropriate techniques are fundamental for favorable outcomes of patients with brainstem CMs.
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Key words Brainstem - Cavernous malformation - Surgical approach - Surgical technique -
Abbreviations and Acronyms CM: Cavernous malformation MRI: Magnetic resonance imaging
INTRODUCTION
C
ommonly seen brainstem lesions include cavernous malformations (CMs), gliomas, and hemangioblastomas. Among these lesions, CM has the highest incidence. Brainstem CMs are benign lesions, often have an acute onset, and result in a high rate of morbidity. Brainstem CMs can be cured through surgical resection, but it is difficult to determine a proper surgical approach to the brainstem.1,2 Choosing an optimal surgical approach based on the different anatomic sites of the various CM lesions is a prerequisite for favorable surgical outcomes. Furthermore, injury to normal peripheral brainstem tissues surrounding CM lesions can lead to serious disability, and so appropriate surgical techniques are extremely critical in such cases. Proper surgical techniques not only resect the lesion but also minimize surgical injury and determine patient prognosis after resection. In recent years, great advances in modern surgical methods and imaging, including intraoperative navigation and electrophysiologic monitoring, have occurred, further improving the outcome of brainstem CM surgery.1-6 The aim of the present study was to summarize the surgical approach rationale in 67 patients with differently located brainstem CMs treated at our hospital between March 2011 and May 2013.
MATERIALS AND METHODS Patients The study protocol was approved by the Ethics Committee of the Beijing Tiantan Hospital, Beijing, China. The study included 67 patients with brainstem CMs that were diagnosed by cranial magnetic resonance imaging (MRI) and computed tomography scanning who underwent surgical treatment at Beijing Tiantan Hospital from March 2011 to May 2013. Of the 67 patients, 32 were male (47.8%), and 35 were female (52.2%). The average age of patients was 40 years (range, 14e68 years), and the disease course ranged from 8 days to 10 years.
Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China To whom correspondence should be addressed: Junting Zhang M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.11.008 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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Surgical Approaches Surgical approaches were determined according to the location of CM lesions. The principal aim was to facilitate lesion resection and minimize surgical injury. The criteria to choose a safe entry zone to a brainstem CM are based on 3 principles: 1) avoiding injury to the underlying nuclei, 2) avoiding injury to the projection of all fibers, and 3) approaching lesions through the closest point to lesions. Midbrain. If the lesion was located in the dorsal midbrain, a suboccipital transtentorial approach (Poppen approach) was performed (Figure 1). If the lesion was located in the lateral midbrain, a lateral approach (subtemporal transtentorial approach) was
Figure 1. Cavernous malformation lesions located at the dorsal midbrain were approached using the Poppen approach. (A and B) Magnetic resonance imaging
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chosen. (3) For lesions in the ventral midbrain, if the lesion was located relatively high, a pterional approach was used, and if the lesion was low, an orbitozygomatic approach was performed. Pons. If the lesion was located at the lateral or ventrolateral side of the upper part of the pons, a lateral approach was chosen. If the lesion was located at a relatively high level, a straight incision was made for craniotomy followed by a subtemporal transtentorial approach (Figure 2). If the lesion was located at a relatively low level, a straight-incision craniotomy was made, followed by a subtemporal transtentorial/anterior petrosectomy approach. During this procedure, after craniotomy, the dura mater was cut open in an arcuate shape, and the cerebrospinal fluid was released by
before surgery. (C and D) Magnetic resonance imaging after surgery.
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Figure 2. For cavernous malformation lesions located at the ventrolateral part of the upper pons, a straight incision was made for craniotomy, followed by a subtemporal transtentorial approach. (AeC) Magnetic
lifting up the temporal lobe followed by resection of the tentorium and the dural surface of the petrous apex. At this point, preservation of the trigeminal nerve roots is vital, and the petrous apex bone can be smoothed if necessary to increase the downward field under the microscope. If the lesion was located at the upper part of the dorsolateral pons, an occipitotemporal horseshoe-shaped incision was made for craniotomy, and a lateral approach (subtemporal transtentorial approach) was performed (Figure 3). For lesions located at the lateral side of the lower pons, if the CM could be suitably approached by opening the brainstem behind the site where the acoustic nerve emerged from the brainstem, a suboccipital retrosigmoid approach was chosen (Figure 4). However, if the CM could be suitably approached by opening the brainstem via the anterior side where the acoustic nerve emerged from the brainstem, a far lateral approach was performed (Figure 5). If the lesion was located at the ventral side of the lower pons, again, a far lateral approach was used. If the lesion was located at the dorsal pons, a midline suboccipital transefourth ventricle approach was performed, and part of the cerebellar vermis could be cut if necessary.
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resonance imaging before surgery. (DeF) Magnetic resonance imaging after surgery.
Medulla. If the lesion was located at the dorsal medulla, a midline suboccipital approach was chosen (Figure 6). If the lesion was located at the lateral or ventrolateral medulla, a far lateral approach was performed. Surgical Techniques and Intraoperative Assistive Techniques Theoretically, the brainstem should be cut where the lesion is the nearest to the surface of the brainstem. Sometimes the surface of brainstem is yellow-colored, which can help indicate the location of lesions. When choosing the incision, the nucleus and the conduction bundles, such as the pyramidal tract or the nucleus at the bottom of the fourth ventricle, should be avoided. The old hemorrhage found in the lesion should be cleaned to achieve more space for surgery. Lesions should be resected as completely as possible, and if the lesion size is too large, it should be removed by piecemeal resection. During resection, electrocoagulation was used to shrink the surface of the lesion, facilitating its separation from the surrounding brainstem tissues. Intraoperative procedures were as follows: 1) Venous malformations near the lesions were retained. 2) During resection, the CM lesions were gently separated from the surrounding glial
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Figure 3. For cavernous malformation lesions located at the dorsolateral part of the upper pons, an occipitotemporal horseshoe-shaped incision was made, followed by the subtemporal transtentorial approach. (AeC)
tissues. 3) Lesions were removed thoroughly because residual lesions have a high incidence (62%) of hemorrhage.3 4) For deeply located CM lesions (absence of yellow-colored areas on the surface of brainstem or no thinned surface was suitable for incision) and for patients who had relatively small CMs, intraoperative navigation was performed. 5) Intraoperative electrophysiologic monitoring (e.g., brainstem evoked potential or cranial nerve monitoring) was used to avoid injuries of important tracts or nucleus in the brainstem. Pathologic Verification The resected tissues of all patients were sent for pathologic examination for accurate diagnosis. Follow-Up All patients underwent postoperative MRI and repeat MRI at 3 months after surgery. Afterward, patients underwent annual MRI.
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Magnetic resonance imaging before surgery. (DeF) Magnetic resonance imaging after surgery.
RESULTS Demographic and Clinical Characteristics of Patients CM was diagnosed in 67 patients (32 [47.8%] male and 35 [52.2%] female; median age 40 years; range, 14e68 years). Lesion locations included the midbrain in 12 (17.9%) patients, the pons in 42 (62.7%) patients, and the medulla in 13 (19.4%) patients (Table 1). Symptoms included headache, dizziness, and nausea in 41 (61.2%) patients; decreased limb muscle strength in 22 (32.8%) patients; ataxia in 27 (40.3%) patients; disturbance of limb sensation (including numbness and loss of superficial sensory phenomena) in 33 (49.3%) patients; cranial nerve dysfunction in 59 (88.1%) patients; and disturbance of consciousness in 4 (6.0%) patients. Surgical Approaches and Outcomes Seven approaches were included: orbitozygomatic approach (1 case), suboccipital transtentorial approach (Poppen approach; 3 cases), subtemporal transtentorial approach (32 cases),
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Figure 4. For cavernous malformation lesions located at the lateral sides of the lower pons (suitable for approach by opening the brainstem at the site behind where the acoustic nerve emerges from the
subtemporal transtentorial/anterior petrosectomy approach (9 cases), suboccipital-retrosigmoid approach (3 cases), midline suboccipital approach (16 cases), and far lateral approach (3 cases) (Table 2). For all patients, the lesions were completely resected, which was verified by postoperative imaging. None of the patients showed residual lesions or hemorrhage during the postoperative follow-up period, and the rate of total lesion resection was 100%. Pathologic examinations verified the diagnosis of CM. Complications No operative mortality was encountered. After surgery, 3 patients with medullary CMs developed lung infection. These patients presented with swallowing dysfunction accompanied by cough reflex dysfunction; all patients recovered after antibiotic therapy in combination with physiotherapy (back patting and walking).
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brainstem), a suboccipital postsigmoid approach was chosen. (A and B) Magnetic resonance imaging before surgery. (C and D) Magnetic resonance imaging after surgery.
Intracranial infection occurred in 2 patients, which was successfully treated with lumbar puncture to release the cerebrospinal fluid and antimicrobials. Nine patients experienced new symptoms after surgery, including diplopia in 3 patients, facial numbness in 3 patients, numbness of contralateral limbs in 1 patient, transient aphasia in 1 patient, and reduced muscle strength of contralateral limbs in 1 patient. The patients presenting with new symptoms of neurologic deficits recovered within approximately 6 months after surgery except for the 2 patients with diplopia and the 2 patients with facial numbness. The diplopia of the 2 patients had improved during follow-up, and the other 2 patients have remained facial numbness until the last post-operative examination. Follow-Up The average follow-up time was 51.7 months (range, 40e66 months). After lesion resection, 23 (34.3%) patients showed
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Figure 5. For cavernous malformation lesions located at the lateral sides of the lower pons (suitable for approach by opening the brainstem at the site in front of where the acoustic nerve emerges from the brainstem), a far
significantly improved symptoms, 35 (52.2%) patients showed no change in symptoms, and 9 (13.4%) patients had new postoperative symptoms. No patient mortality was encountered. MRI was performed postoperatively, 3 months after surgery, and annually thereafter. No recurrence or hemorrhage was found on follow-up MRI. DISCUSSION CMs are predisposed to develop within the brainstem. Approximately 18%e35% of intracranial CMs are located within the brainstem,7,8 and the pons has the highest incidence of CMs.9 CMs occurring at different sites manifest with different symptoms, and surgical resection is the treatment of choice for CMs occurring within the brainstem.1,2,10,11 Gross et al.3 summarized 68 surgical series comprising 1390 patients. The overall complete resection rate reported in the literature is 92%. Complication rates were 84% improved or the same and 16% worse or dead at long-term follow-up. In 61 series with 1291 patients, there was an overall 91% complete excision
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lateral approach was chosen. (AeC) Magnetic resonance imaging before surgery. (DeF) Magnetic resonance imaging after surgery.
rate. Of 105 partially resected CMs, 65 rebled (62%). The mortality rate from hemorrhage of a residual CM was 6% (4 of 65 cases). In our series, the rate of total lesion resection was 100%. After the operation, 23 (34.3%) patients showed significantly improved symptoms, 35 (52.2%) patients showed no change in symptoms, and 9 (13.4%) patients presented with new postoperative symptoms. No patients died, and no recurrence or hemorrhage was found during the follow-up period. Compared with historical case series, the data in our series seem to be better.
Indications of Surgery Compared with supratentorial CMs, a brainstem CM is more likely to manifest with major severe signs and symptoms. Surgical resection can inhibit the progressive deterioration of neurologic function caused by repetitive hemorrhage. When deciding whether to perform surgery, the following key factors should be considered: (1) If surgery is not performed, how great will the risk be for future CM rehemorrhage? (2) What are possible symptoms of neurologic impairment if rebleeding is encountered? (3) What is
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Figure 6. Cavernous malformation lesions located at the dorsal medulla were approached via the posterior midline suboccipital approach. (A and B) Magnetic
the patient’s overall clinical status (including age, present neurologic function, size and location of lesions)? (4) What are possible surgical injuries, and how severely can they result in neurologic deficit? (5) What is the skill level of the surgeon?8 Based on these factors, the surgical indication should be balanced between the surgical risk and the natural history of the brainstem CM. It has been reported that after the first hemorrhage, the incidence of rebleeding can be 21%e60% per year,12-14 and the incidence of rehemorrhage within 1 year after the first bleeding reported was 8% per month.13 Repetitive bleeding can significantly aggravate previous symptoms of neurologic deficits. Also, it will further increase the difficulty of surgical resection and cause greater trauma to the tissues at the periphery of CM lesions during surgical resection.15 Despite the patients having experienced brainstem lesion resection, surgery for CM may aggravate
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resonance imaging before surgery. (C and D) Magnetic resonance imaging after surgery.
existing neurologic deficits or cause new deficits. Most new symptoms are transient and resolve after surgery, and surgical treatment leads to relatively low rates of mortality and morbidity.8 A study with an 8-year follow-up of patients with brainstem CM found that patients who received conservative treatment or ventricular shunt (hydrocephalus) had a poorer prognosis compared with patients who received microsurgical resection.15 In this study, the indications of surgery were determined according to the principle that the risk and severity of rehemorrhageinduced neurologic damage exceeded those of surgery-induced neurologic damage. Thus, for patients who experienced a first hemorrhage with lesions <1 cm in diameter and located relatively far from the brainstem surface, we suggest only observation and follow-up. However, if a patient had a history of hemorrhage and
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Table 1. Baseline Demographic Data and Clinical Characteristics of Patients Characteristic
Value
Sex Male
32 (47.8%)
Female
35 (52.2%)
Average age Disease course
40 years 8 dayse10 years
Site of lesion Midbrain
12 (17.9%)
Pons
42 (62.7%)
Medulla Average follow-up time
13 (19.4%) 51.7 months
presented with obvious symptoms, and the lesion was >2 cm in diameter located near the surface of the brainstem, we suggest surgical resection. However, as bleeding of the CM inside the medulla may cause death, the indications of surgery should be adjusted for patients with medullary CM. Timing of Surgery We suggest performing surgery within 3 weeks to 1 month after hemorrhage for the following reasons. First, based on our observations, part of the hematoma can liquefy within this time period, and an area of gliosis can form surrounding the lesion, both of which will facilitate the isolation of lesions from the peripheral brainstem tissues. During this time period, the lesion will be loosely attached to the peripheral brainstem tissues, which helps to resect the lesion and reduce surgical injury. In this study, some patients had a delayed diagnosis or waited a long time for surgery (3e6 months after hemorrhage), and we noticed that these patients had solidified hematomas that were firmly adhered to the peripheral brainstem tissues, which increased the surgical difficulty as well as led to more surgical injury. Second, hematomas
Table 2. Types of Surgical Approaches Characteristic
Value
Number of cases
67
Surgical approach Orbitozygomatic Suboccipital transtentorial
3 (4.5%)
Subtemporal transtentorial
32 (47.8%)
Subtemporal transtentorial/anterior petrosectomy
9 (13.4%)
Suboccipital retrosigmoid Midline suboccipital Far lateral
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1 (1.5%)
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3 (4.5%) 16 (23.9%) 3 (4.5%)
and lesions can be clearly distinguished on MRI during this time period. Determining the defined location of lesions within the hematoma is key to choosing the appropriate surgical approach.16 In addition, we believe that disturbed consciousness, poor breath or heart rate, and hemiplegia are not surgical contraindications. In contrast, the presence of these symptoms suggests surgery should be performed as soon as possible so that further neurologic deficits can be alleviated. In this study, 4 patients showed varying degrees of disturbance of consciousness (drowsiness or light coma), but after surgery and supportive treatment, they all regained consciousness gradually. For patients with lesions located inside the medulla who demonstrate obvious symptoms, surgery should be considered as early as possible, as these lesions may cause changes in breath and heart rate, which may result in sudden death of patients. Surgical Approaches When the lesion reaches the surface of the brainstem, it creates a natural corridor to the lesion. In the case of a lesion that does not reach the surface, the safe entry zones are used to avoid damage to important structures. Because the nuclei and corticospinal fibers are mainly located at the dorsal and ventral brainstem, we choose lateral approaches in many cases. Brown et al.17 suggested the 2-point method for determining the optimal approach to brainstem lesions: the first point represents the center of the lesion, and the second point represents the site where the lesion is nearest to the brainstem surface or the site evaluated as the safest for brainstem incision. By connecting the 2 points and extending the line outward, the pointed location on the skull surface would be the optimal location of the craniotomy. However, in actual clinical practice, there are many other factors that need to be considered when determining a proper approach, such as the clinical manifestations, site of lesion, location where lesion was the nearest to the brainstem surface, peripheral brainstem function, type and distribution of hematoma, accompanying veins, surgeon’s familiarity with different approaches, and individual condition of patients.18 For example, for lesions located within the midbrain and pons, we suggest the lateral approach be used as much as possible because by approaching the lesion through the lateral dumb region rather than the midline suboccipital approach, the important nucleus at the dorsal medium region of brainstem can be avoided. Controversial Approaches and Our Experience Lesions Located at Dorsal Midline of Midbrain. We adopted the suboccipital transtentorial approach (Poppen approach) because it provides a wide field of vision, is easy to operate, and causes fewer complications. Some scholars suggest an infratentorial supracerebellar approach, which can be performed from 3 different angles (i.e., midline, paramidline, or lateral).18-20 Different angles correspond to different locations of the CM within the dorsal midbrain (midline corresponds to midline suboccipital craniotomy, paramidline corresponds to paramidline suboccipital craniotomy, and lateral corresponds to suboccipital retrosigmoid craniotomy). It is thought that this approach can avoid damaging the occipital cortex and thereby prevent any visual field defect after surgery. We believe that when using the Poppen approach, the cerebrospinal fluid can be removed sufficiently at first, and after
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the occipital lobe falls naturally, it can be gently flipped up to expose the surgical area. This will not damage the occipital lobe. We do not suggest the infratentorial supracerebellar approach because it may damage the bridging veins, which may result in cerebellar damage and swelling.21 Apart from that, the infratentorial supracerebellar approach requires a sitting position for surgery, and we do not use such a position during our surgeries.
For lesions located at the lateral midbrain or ventrolateral or lateral part of the upper pons, some scholars prefer the infratentorial supracerebellar approach.19,20 As we have described previously, we do not use this approach in our surgeries. For lesions at the ventrolateral and lateral part of the upper pons, we do not recommend the suboccipital retrosigmoid approach because it provides a poor angle to approach these CMs, which increases the risk of trigeminal nerve injury.
Lesions Located at Lateral Midbrain, Ventrolateral or Lateral Side of Midbrain-Pons Junction, and Upper Pons. For these lesions, we use the subtemporal transtentorial approach or the subtemporal transtentorial/anterior petrosectomy approach. This approach is advantageous for exposing lesions at the ventrolateral or lateral side of the midbrain and upper pons and is particularly suitable for lesions that are located close to the edge of the tentorium.22 For upper pons CMs located in the horizontal or upper part to the root of the trigeminal nerve, we use the subtemporal transtentorial approach. The petrous bone does not need to be ground, and the incision for brainstem opening is above the trigeminal nerve. For upper pons CMs located beneath the trigeminal nerve, we use the subtemporal transtentorial/anterior petrosectomy approach. Some of the petrous bone should be ground, and the brainstem is opened between the trigeminal and acoustic nerves to approach the lesion.23 For the previously described 2 types of approaches, a preauricular straight incision was made for craniotomy because this causes less trauma; requires shorter operative time; only slightly stretches the Labbé vein; and can avoid damage to the functions of the oculomotor, trochlear, and acoustic nerves as well as the bottom structures of the fourth ventricle.21
Lesions Located at Lateral Sides of Lower Pons. For lesions located at the lateral sides of the lower pons, when the site where the lesion located nearest to the brainstem surface is behind the acoustic nerve, we use the suboccipital retrosigmoid approach and open the brainstem behind where the acoustic nerve emerges from the brainstem. Otherwise, if the site of the lesion located nearest to the brainstem surface is anterior to the acoustic nerve, the far lateral approach is chosen, and the brainstem is opened anteriorly to where the acoustic nerve emerges from the brainstem. Furthermore, although the presigmoid approach can reach the lateral pons more directly, we do not recommend this approach because it requires a long time for craniotomy, causes greater trauma, and may damage the patient’s hearing and sigmoid sinus.
2. Li D, Hao SY, Tang J, Xiao XR, Jia GJ, Wu Z, et al. Surgical management of pediatric brainstem cavernous malformations. J Neurosurg Pediatr. 2014; 13:484-502. 3. Gross BA, Batjer HH, Awad IA, Bendok BR, Du R. Brainstem cavernous malformations: 1390 surgical cases from the literature. World Neurosurg. 2013;80: 89-93. 4. Kin T, Nakatomi H, Shojima M, Tanaka M, Ino K, Mori H, et al. A new strategic neurosurgical planning tool for brainstem cavernous malformations using interactive computer graphics with multimodal fusion images. J Neurosurg. 2012;117: 78-88.
Resection of brainstem CMs is indicated in symptomatic patients when the lesions can be accessed surgically. In most patients, new neurologic deficits may occur postoperatively, but they are transient and resolve during the follow-up period. The surgical approach is best determined according to the site of the lesion.
cavernous malformations: surgical approaches and clinical experiences with 38 patients. Clin Neurol Neurosurg. 2014;116:72-79.
REFERENCES 1. Li D, Yang Y, Hao SY, Wang L, Tang J, Xiao XR, et al. Hemorrhage risk, surgical management, and functional outcome of brainstem cavernous malformations. J Neurosurg. 2013;119:996-1008.
CONCLUSIONS
7. Porter RW, Detwiler PW, Spetzler RF, Lawton MT, Baskin JJ, Derksen PT, et al. Cavernous malformations of the brainstem: experience with 100 patients. J Neurosurg. 1999;90:50-58. 8. Samii M, Eghbal R, Carvalho GA, Matthies C. Surgical management of brainstem cavernomas. J Neurosurg. 2001;95:825-832. 9. Rigamonti D, Hadley MN, Drayer BP, Johnson PC, Hoenig-Rigamonti K, Knight JT, et al. Cerebral cavernous malformations. Incidence and familial occurrence. N Engl J Med. 1988;319:343-347. 10. Chen L, Zhao Y, Zhou L, Zhu W, Pan Z, Mao Y. Surgical strategies in treating brainstem cavernous malformations. Neurosurgery. 2011;68:609-620 [discussion: 620-621].
5. Pandey P, Westbroek EM, Gooderham PA, Steinberg GK. Cavernous malformation of brainstem, thalamus, and basal ganglia: a series of 176 patients. Neurosurgery. 2013;72:573-589 [discussion: 588-589].
11. Abla AA, Lekovic GP, Turner JD, de Oliveira JG, Porter R, Spetzler RF. Advances in the treatment and outcome of brainstem cavernous malformation surgery: a single-center case series of 300 surgically treated patients. Neurosurgery. 2011;68: 403-414 [discussion: 414-415].
6. Chen LH, Zhang HT, Chen L, Liu LX, Xu RX. Minimally invasive resection of brainstem
12. Fritschi JA, Reulen HJ, Spetzler RF, Zabramski JM. Cavernous malformations of the brain stem. A
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review of 139 cases. Acta Neurochir (Wien). 1994;130: 35-46. 13. Hauck EF, Barnett SL, White JA, Samson D. Symptomatic brainstem cavernomas. Neurosurgery. 2009;64:61-70 [discussion: 70-71]. 14. Wang CC, Liu A, Zhang JT, Sun B, Zhao YL. Surgical management of brain-stem cavernous malformations: report of 137 cases. Surg Neurol. 2003;59:444-454 [discussion: 454]. 15. Mathiesen T, Edner G, Kihlstrom L. Deep and brainstem cavernomas: a consecutive 8-year series. J Neurosurg. 2003;99:31-37. 16. Sandalcioglu IE, Wiedemayer H, Secer S, Asgari S, Stolke D. Surgical removal of brain stem cavernous malformations: surgical indications, technical considerations, and results. J Neurol Neurosurg Psychiatry. 2002;72:351-355. 17. Brown AP, Thompson BG, Spetzler RF. The twopoint method: evaluating brain stem lesions. BNI Q. 1996;12:20-24. 18. Giliberto G, Lanzino DJ, Diehn FE, Factor D, Flemming KD, Lanzino G. Brainstem cavernous malformations: anatomical, clinical, and surgical considerations. Neurosurg Focus. 2010;29:E9.
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19. Ramina R, Mattei TA, de Aguiar PH, Meneses MS, Ferraz VR, Aires R, et al. Surgical management of brainstem cavernous malformations. Neurol Sci. 2011;32:1013-1028. 20. Abla AA, Turner JD, Mitha AP, Lekovic G, Spetzler RF. Surgical approaches to brainstem cavernous malformations. Neurosurg Focus. 2010; 29:E8. 21. Sabatino G, Rigante L, Marchese E, Albanese A, Esposito G, Capone G, et al. Anterior subtemporal approach for posterolateral brainstem cavernomas: report of ten cases. Acta Neurochir (Wien). 2012;154:2009-2016.
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22. Steno J, Bizik I, Stenova J, Timarova G. Subtemporal transtentorial resection of cavernous malformations involving the pyramidal tract in the upper pons and mesencephalon. Acta Neurochir (Wien). 2011;153:1955-1962 [discussion: 1962]. 23. Francois P, Ben Ismail M, Hamel O, Bataille B, Jan M, Velut S. Anterior transpetrosal and subtemporal transtentorial approaches for pontine cavernomas. Acta Neurochir (Wien). 2010;152: 1321-1329 [discussion: 1329].
commercial or financial relationships that could be construed as a potential conflict of interest. Received 2 September 2018; accepted 2 November 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.11.008 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any
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Surgical Management of Brainstem Cavernous Malformation: Report of 67 Patients Songbai Gui, Guolu Meng, Xinru Xiao, Zhen Wu, Junting Zhang
BACKGROUND: Brainstem cavernous malformations (CMs) are benign lesions, often show an acute onset, and result in a high rate of morbidity. Surgical resection could inhibit the progressive deterioration of neurologic function caused by repetitive hemorrhage. This study aimed to summarize timing, approaches, and techniques of surgery and to evaluate outcomes of treatment.
-
METHODS: Between March 2011 and May 2013, 67 patients (32 male, 35 female; average age 40 years; range, 14e68 years) with brainstem CMs received surgical treatment. Clinical presentation, surgical approaches, and results of follow-up were retrospectively analyzed.
-
RESULTS: Seven surgical approaches were used: orbitozygomatic approach (1 case), suboccipital transtentorial approach (Poppen approach; 3 cases), subtemporal transtentorial approach (32 cases), subtemporal transtentorial/ anterior petrosectomy approach (9 cases), suboccipital retrosigmoid approach (3 cases), midline suboccipital approach (16 cases), and far lateral approach (3 cases). Total resection of the brainstem CM was achieved in all cases (100%). No operative mortality was encountered. Nine patients had new symptoms after surgery: 3 had diplopia, 3 had facial numbness, 1 had numbness of contralateral limbs, 1 had transient aphasia, and 1 had reduced muscle strength of contralateral limbs. Symptoms significantly improved in 23 patients (34.3%), symptoms were unchanged in 36 patients (53.7%), and new postoperative symptoms occurred in 9 patients (13.4%).
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CONCLUSIONS: Choosing a proper surgical approach and using appropriate techniques are fundamental for favorable outcomes of patients with brainstem CMs.
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Key words Brainstem - Cavernous malformation - Surgical approach - Surgical technique -
Abbreviations and Acronyms CM: Cavernous malformation MRI: Magnetic resonance imaging
INTRODUCTION
C
ommonly seen brainstem lesions include cavernous malformations (CMs), gliomas, and hemangioblastomas. Among these lesions, CM has the highest incidence. Brainstem CMs are benign lesions, often have an acute onset, and result in a high rate of morbidity. Brainstem CMs can be cured through surgical resection, but it is difficult to determine a proper surgical approach to the brainstem.1,2 Choosing an optimal surgical approach based on the different anatomic sites of the various CM lesions is a prerequisite for favorable surgical outcomes. Furthermore, injury to normal peripheral brainstem tissues surrounding CM lesions can lead to serious disability, and so appropriate surgical techniques are extremely critical in such cases. Proper surgical techniques not only resect the lesion but also minimize surgical injury and determine patient prognosis after resection. In recent years, great advances in modern surgical methods and imaging, including intraoperative navigation and electrophysiologic monitoring, have occurred, further improving the outcome of brainstem CM surgery.1-6 The aim of the present study was to summarize the surgical approach rationale in 67 patients with differently located brainstem CMs treated at our hospital between March 2011 and May 2013.
MATERIALS AND METHODS Patients The study protocol was approved by the Ethics Committee of the Beijing Tiantan Hospital, Beijing, China. The study included 67 patients with brainstem CMs that were diagnosed by cranial magnetic resonance imaging (MRI) and computed tomography scanning who underwent surgical treatment at Beijing Tiantan Hospital from March 2011 to May 2013. Of the 67 patients, 32 were male (47.8%), and 35 were female (52.2%). The average age of patients was 40 years (range, 14e68 years), and the disease course ranged from 8 days to 10 years.
Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China To whom correspondence should be addressed: Junting Zhang M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.11.008 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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Surgical Approaches Surgical approaches were determined according to the location of CM lesions. The principal aim was to facilitate lesion resection and minimize surgical injury. The criteria to choose a safe entry zone to a brainstem CM are based on 3 principles: 1) avoiding injury to the underlying nuclei, 2) avoiding injury to the projection of all fibers, and 3) approaching lesions through the closest point to lesions. Midbrain. If the lesion was located in the dorsal midbrain, a suboccipital transtentorial approach (Poppen approach) was performed (Figure 1). If the lesion was located in the lateral midbrain, a lateral approach (subtemporal transtentorial approach) was
Figure 1. Cavernous malformation lesions located at the dorsal midbrain were approached using the Poppen approach. (A and B) Magnetic resonance imaging
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chosen. (3) For lesions in the ventral midbrain, if the lesion was located relatively high, a pterional approach was used, and if the lesion was low, an orbitozygomatic approach was performed. Pons. If the lesion was located at the lateral or ventrolateral side of the upper part of the pons, a lateral approach was chosen. If the lesion was located at a relatively high level, a straight incision was made for craniotomy followed by a subtemporal transtentorial approach (Figure 2). If the lesion was located at a relatively low level, a straight-incision craniotomy was made, followed by a subtemporal transtentorial/anterior petrosectomy approach. During this procedure, after craniotomy, the dura mater was cut open in an arcuate shape, and the cerebrospinal fluid was released by
before surgery. (C and D) Magnetic resonance imaging after surgery.
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Figure 2. For cavernous malformation lesions located at the ventrolateral part of the upper pons, a straight incision was made for craniotomy, followed by a subtemporal transtentorial approach. (AeC) Magnetic
lifting up the temporal lobe followed by resection of the tentorium and the dural surface of the petrous apex. At this point, preservation of the trigeminal nerve roots is vital, and the petrous apex bone can be smoothed if necessary to increase the downward field under the microscope. If the lesion was located at the upper part of the dorsolateral pons, an occipitotemporal horseshoe-shaped incision was made for craniotomy, and a lateral approach (subtemporal transtentorial approach) was performed (Figure 3). For lesions located at the lateral side of the lower pons, if the CM could be suitably approached by opening the brainstem behind the site where the acoustic nerve emerged from the brainstem, a suboccipital retrosigmoid approach was chosen (Figure 4). However, if the CM could be suitably approached by opening the brainstem via the anterior side where the acoustic nerve emerged from the brainstem, a far lateral approach was performed (Figure 5). If the lesion was located at the ventral side of the lower pons, again, a far lateral approach was used. If the lesion was located at the dorsal pons, a midline suboccipital transefourth ventricle approach was performed, and part of the cerebellar vermis could be cut if necessary.
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resonance imaging before surgery. (DeF) Magnetic resonance imaging after surgery.
Medulla. If the lesion was located at the dorsal medulla, a midline suboccipital approach was chosen (Figure 6). If the lesion was located at the lateral or ventrolateral medulla, a far lateral approach was performed. Surgical Techniques and Intraoperative Assistive Techniques Theoretically, the brainstem should be cut where the lesion is the nearest to the surface of the brainstem. Sometimes the surface of brainstem is yellow-colored, which can help indicate the location of lesions. When choosing the incision, the nucleus and the conduction bundles, such as the pyramidal tract or the nucleus at the bottom of the fourth ventricle, should be avoided. The old hemorrhage found in the lesion should be cleaned to achieve more space for surgery. Lesions should be resected as completely as possible, and if the lesion size is too large, it should be removed by piecemeal resection. During resection, electrocoagulation was used to shrink the surface of the lesion, facilitating its separation from the surrounding brainstem tissues. Intraoperative procedures were as follows: 1) Venous malformations near the lesions were retained. 2) During resection, the CM lesions were gently separated from the surrounding glial
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Figure 3. For cavernous malformation lesions located at the dorsolateral part of the upper pons, an occipitotemporal horseshoe-shaped incision was made, followed by the subtemporal transtentorial approach. (AeC)
tissues. 3) Lesions were removed thoroughly because residual lesions have a high incidence (62%) of hemorrhage.3 4) For deeply located CM lesions (absence of yellow-colored areas on the surface of brainstem or no thinned surface was suitable for incision) and for patients who had relatively small CMs, intraoperative navigation was performed. 5) Intraoperative electrophysiologic monitoring (e.g., brainstem evoked potential or cranial nerve monitoring) was used to avoid injuries of important tracts or nucleus in the brainstem. Pathologic Verification The resected tissues of all patients were sent for pathologic examination for accurate diagnosis. Follow-Up All patients underwent postoperative MRI and repeat MRI at 3 months after surgery. Afterward, patients underwent annual MRI.
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Magnetic resonance imaging before surgery. (DeF) Magnetic resonance imaging after surgery.
RESULTS Demographic and Clinical Characteristics of Patients CM was diagnosed in 67 patients (32 [47.8%] male and 35 [52.2%] female; median age 40 years; range, 14e68 years). Lesion locations included the midbrain in 12 (17.9%) patients, the pons in 42 (62.7%) patients, and the medulla in 13 (19.4%) patients (Table 1). Symptoms included headache, dizziness, and nausea in 41 (61.2%) patients; decreased limb muscle strength in 22 (32.8%) patients; ataxia in 27 (40.3%) patients; disturbance of limb sensation (including numbness and loss of superficial sensory phenomena) in 33 (49.3%) patients; cranial nerve dysfunction in 59 (88.1%) patients; and disturbance of consciousness in 4 (6.0%) patients. Surgical Approaches and Outcomes Seven approaches were included: orbitozygomatic approach (1 case), suboccipital transtentorial approach (Poppen approach; 3 cases), subtemporal transtentorial approach (32 cases),
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Figure 4. For cavernous malformation lesions located at the lateral sides of the lower pons (suitable for approach by opening the brainstem at the site behind where the acoustic nerve emerges from the
subtemporal transtentorial/anterior petrosectomy approach (9 cases), suboccipital-retrosigmoid approach (3 cases), midline suboccipital approach (16 cases), and far lateral approach (3 cases) (Table 2). For all patients, the lesions were completely resected, which was verified by postoperative imaging. None of the patients showed residual lesions or hemorrhage during the postoperative follow-up period, and the rate of total lesion resection was 100%. Pathologic examinations verified the diagnosis of CM. Complications No operative mortality was encountered. After surgery, 3 patients with medullary CMs developed lung infection. These patients presented with swallowing dysfunction accompanied by cough reflex dysfunction; all patients recovered after antibiotic therapy in combination with physiotherapy (back patting and walking).
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brainstem), a suboccipital postsigmoid approach was chosen. (A and B) Magnetic resonance imaging before surgery. (C and D) Magnetic resonance imaging after surgery.
Intracranial infection occurred in 2 patients, which was successfully treated with lumbar puncture to release the cerebrospinal fluid and antimicrobials. Nine patients experienced new symptoms after surgery, including diplopia in 3 patients, facial numbness in 3 patients, numbness of contralateral limbs in 1 patient, transient aphasia in 1 patient, and reduced muscle strength of contralateral limbs in 1 patient. The patients presenting with new symptoms of neurologic deficits recovered within approximately 6 months after surgery except for the 2 patients with diplopia and the 2 patients with facial numbness. The diplopia of the 2 patients had improved during follow-up, and the other 2 patients have remained facial numbness until the last post-operative examination. Follow-Up The average follow-up time was 51.7 months (range, 40e66 months). After lesion resection, 23 (34.3%) patients showed
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Figure 5. For cavernous malformation lesions located at the lateral sides of the lower pons (suitable for approach by opening the brainstem at the site in front of where the acoustic nerve emerges from the brainstem), a far
significantly improved symptoms, 35 (52.2%) patients showed no change in symptoms, and 9 (13.4%) patients had new postoperative symptoms. No patient mortality was encountered. MRI was performed postoperatively, 3 months after surgery, and annually thereafter. No recurrence or hemorrhage was found on follow-up MRI. DISCUSSION CMs are predisposed to develop within the brainstem. Approximately 18%e35% of intracranial CMs are located within the brainstem,7,8 and the pons has the highest incidence of CMs.9 CMs occurring at different sites manifest with different symptoms, and surgical resection is the treatment of choice for CMs occurring within the brainstem.1,2,10,11 Gross et al.3 summarized 68 surgical series comprising 1390 patients. The overall complete resection rate reported in the literature is 92%. Complication rates were 84% improved or the same and 16% worse or dead at long-term follow-up. In 61 series with 1291 patients, there was an overall 91% complete excision
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lateral approach was chosen. (AeC) Magnetic resonance imaging before surgery. (DeF) Magnetic resonance imaging after surgery.
rate. Of 105 partially resected CMs, 65 rebled (62%). The mortality rate from hemorrhage of a residual CM was 6% (4 of 65 cases). In our series, the rate of total lesion resection was 100%. After the operation, 23 (34.3%) patients showed significantly improved symptoms, 35 (52.2%) patients showed no change in symptoms, and 9 (13.4%) patients presented with new postoperative symptoms. No patients died, and no recurrence or hemorrhage was found during the follow-up period. Compared with historical case series, the data in our series seem to be better.
Indications of Surgery Compared with supratentorial CMs, a brainstem CM is more likely to manifest with major severe signs and symptoms. Surgical resection can inhibit the progressive deterioration of neurologic function caused by repetitive hemorrhage. When deciding whether to perform surgery, the following key factors should be considered: (1) If surgery is not performed, how great will the risk be for future CM rehemorrhage? (2) What are possible symptoms of neurologic impairment if rebleeding is encountered? (3) What is
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Figure 6. Cavernous malformation lesions located at the dorsal medulla were approached via the posterior midline suboccipital approach. (A and B) Magnetic
the patient’s overall clinical status (including age, present neurologic function, size and location of lesions)? (4) What are possible surgical injuries, and how severely can they result in neurologic deficit? (5) What is the skill level of the surgeon?8 Based on these factors, the surgical indication should be balanced between the surgical risk and the natural history of the brainstem CM. It has been reported that after the first hemorrhage, the incidence of rebleeding can be 21%e60% per year,12-14 and the incidence of rehemorrhage within 1 year after the first bleeding reported was 8% per month.13 Repetitive bleeding can significantly aggravate previous symptoms of neurologic deficits. Also, it will further increase the difficulty of surgical resection and cause greater trauma to the tissues at the periphery of CM lesions during surgical resection.15 Despite the patients having experienced brainstem lesion resection, surgery for CM may aggravate
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resonance imaging before surgery. (C and D) Magnetic resonance imaging after surgery.
existing neurologic deficits or cause new deficits. Most new symptoms are transient and resolve after surgery, and surgical treatment leads to relatively low rates of mortality and morbidity.8 A study with an 8-year follow-up of patients with brainstem CM found that patients who received conservative treatment or ventricular shunt (hydrocephalus) had a poorer prognosis compared with patients who received microsurgical resection.15 In this study, the indications of surgery were determined according to the principle that the risk and severity of rehemorrhageinduced neurologic damage exceeded those of surgery-induced neurologic damage. Thus, for patients who experienced a first hemorrhage with lesions <1 cm in diameter and located relatively far from the brainstem surface, we suggest only observation and follow-up. However, if a patient had a history of hemorrhage and
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Table 1. Baseline Demographic Data and Clinical Characteristics of Patients Characteristic
Value
Sex Male
32 (47.8%)
Female
35 (52.2%)
Average age Disease course
40 years 8 dayse10 years
Site of lesion Midbrain
12 (17.9%)
Pons
42 (62.7%)
Medulla Average follow-up time
13 (19.4%) 51.7 months
presented with obvious symptoms, and the lesion was >2 cm in diameter located near the surface of the brainstem, we suggest surgical resection. However, as bleeding of the CM inside the medulla may cause death, the indications of surgery should be adjusted for patients with medullary CM. Timing of Surgery We suggest performing surgery within 3 weeks to 1 month after hemorrhage for the following reasons. First, based on our observations, part of the hematoma can liquefy within this time period, and an area of gliosis can form surrounding the lesion, both of which will facilitate the isolation of lesions from the peripheral brainstem tissues. During this time period, the lesion will be loosely attached to the peripheral brainstem tissues, which helps to resect the lesion and reduce surgical injury. In this study, some patients had a delayed diagnosis or waited a long time for surgery (3e6 months after hemorrhage), and we noticed that these patients had solidified hematomas that were firmly adhered to the peripheral brainstem tissues, which increased the surgical difficulty as well as led to more surgical injury. Second, hematomas
Table 2. Types of Surgical Approaches Characteristic
Value
Number of cases
67
Surgical approach Orbitozygomatic Suboccipital transtentorial
3 (4.5%)
Subtemporal transtentorial
32 (47.8%)
Subtemporal transtentorial/anterior petrosectomy
9 (13.4%)
Suboccipital retrosigmoid Midline suboccipital Far lateral
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1 (1.5%)
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3 (4.5%) 16 (23.9%) 3 (4.5%)
and lesions can be clearly distinguished on MRI during this time period. Determining the defined location of lesions within the hematoma is key to choosing the appropriate surgical approach.16 In addition, we believe that disturbed consciousness, poor breath or heart rate, and hemiplegia are not surgical contraindications. In contrast, the presence of these symptoms suggests surgery should be performed as soon as possible so that further neurologic deficits can be alleviated. In this study, 4 patients showed varying degrees of disturbance of consciousness (drowsiness or light coma), but after surgery and supportive treatment, they all regained consciousness gradually. For patients with lesions located inside the medulla who demonstrate obvious symptoms, surgery should be considered as early as possible, as these lesions may cause changes in breath and heart rate, which may result in sudden death of patients. Surgical Approaches When the lesion reaches the surface of the brainstem, it creates a natural corridor to the lesion. In the case of a lesion that does not reach the surface, the safe entry zones are used to avoid damage to important structures. Because the nuclei and corticospinal fibers are mainly located at the dorsal and ventral brainstem, we choose lateral approaches in many cases. Brown et al.17 suggested the 2-point method for determining the optimal approach to brainstem lesions: the first point represents the center of the lesion, and the second point represents the site where the lesion is nearest to the brainstem surface or the site evaluated as the safest for brainstem incision. By connecting the 2 points and extending the line outward, the pointed location on the skull surface would be the optimal location of the craniotomy. However, in actual clinical practice, there are many other factors that need to be considered when determining a proper approach, such as the clinical manifestations, site of lesion, location where lesion was the nearest to the brainstem surface, peripheral brainstem function, type and distribution of hematoma, accompanying veins, surgeon’s familiarity with different approaches, and individual condition of patients.18 For example, for lesions located within the midbrain and pons, we suggest the lateral approach be used as much as possible because by approaching the lesion through the lateral dumb region rather than the midline suboccipital approach, the important nucleus at the dorsal medium region of brainstem can be avoided. Controversial Approaches and Our Experience Lesions Located at Dorsal Midline of Midbrain. We adopted the suboccipital transtentorial approach (Poppen approach) because it provides a wide field of vision, is easy to operate, and causes fewer complications. Some scholars suggest an infratentorial supracerebellar approach, which can be performed from 3 different angles (i.e., midline, paramidline, or lateral).18-20 Different angles correspond to different locations of the CM within the dorsal midbrain (midline corresponds to midline suboccipital craniotomy, paramidline corresponds to paramidline suboccipital craniotomy, and lateral corresponds to suboccipital retrosigmoid craniotomy). It is thought that this approach can avoid damaging the occipital cortex and thereby prevent any visual field defect after surgery. We believe that when using the Poppen approach, the cerebrospinal fluid can be removed sufficiently at first, and after
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the occipital lobe falls naturally, it can be gently flipped up to expose the surgical area. This will not damage the occipital lobe. We do not suggest the infratentorial supracerebellar approach because it may damage the bridging veins, which may result in cerebellar damage and swelling.21 Apart from that, the infratentorial supracerebellar approach requires a sitting position for surgery, and we do not use such a position during our surgeries.
For lesions located at the lateral midbrain or ventrolateral or lateral part of the upper pons, some scholars prefer the infratentorial supracerebellar approach.19,20 As we have described previously, we do not use this approach in our surgeries. For lesions at the ventrolateral and lateral part of the upper pons, we do not recommend the suboccipital retrosigmoid approach because it provides a poor angle to approach these CMs, which increases the risk of trigeminal nerve injury.
Lesions Located at Lateral Midbrain, Ventrolateral or Lateral Side of Midbrain-Pons Junction, and Upper Pons. For these lesions, we use the subtemporal transtentorial approach or the subtemporal transtentorial/anterior petrosectomy approach. This approach is advantageous for exposing lesions at the ventrolateral or lateral side of the midbrain and upper pons and is particularly suitable for lesions that are located close to the edge of the tentorium.22 For upper pons CMs located in the horizontal or upper part to the root of the trigeminal nerve, we use the subtemporal transtentorial approach. The petrous bone does not need to be ground, and the incision for brainstem opening is above the trigeminal nerve. For upper pons CMs located beneath the trigeminal nerve, we use the subtemporal transtentorial/anterior petrosectomy approach. Some of the petrous bone should be ground, and the brainstem is opened between the trigeminal and acoustic nerves to approach the lesion.23 For the previously described 2 types of approaches, a preauricular straight incision was made for craniotomy because this causes less trauma; requires shorter operative time; only slightly stretches the Labbé vein; and can avoid damage to the functions of the oculomotor, trochlear, and acoustic nerves as well as the bottom structures of the fourth ventricle.21
Lesions Located at Lateral Sides of Lower Pons. For lesions located at the lateral sides of the lower pons, when the site where the lesion located nearest to the brainstem surface is behind the acoustic nerve, we use the suboccipital retrosigmoid approach and open the brainstem behind where the acoustic nerve emerges from the brainstem. Otherwise, if the site of the lesion located nearest to the brainstem surface is anterior to the acoustic nerve, the far lateral approach is chosen, and the brainstem is opened anteriorly to where the acoustic nerve emerges from the brainstem. Furthermore, although the presigmoid approach can reach the lateral pons more directly, we do not recommend this approach because it requires a long time for craniotomy, causes greater trauma, and may damage the patient’s hearing and sigmoid sinus.
2. Li D, Hao SY, Tang J, Xiao XR, Jia GJ, Wu Z, et al. Surgical management of pediatric brainstem cavernous malformations. J Neurosurg Pediatr. 2014; 13:484-502. 3. Gross BA, Batjer HH, Awad IA, Bendok BR, Du R. Brainstem cavernous malformations: 1390 surgical cases from the literature. World Neurosurg. 2013;80: 89-93. 4. Kin T, Nakatomi H, Shojima M, Tanaka M, Ino K, Mori H, et al. A new strategic neurosurgical planning tool for brainstem cavernous malformations using interactive computer graphics with multimodal fusion images. J Neurosurg. 2012;117: 78-88.
Resection of brainstem CMs is indicated in symptomatic patients when the lesions can be accessed surgically. In most patients, new neurologic deficits may occur postoperatively, but they are transient and resolve during the follow-up period. The surgical approach is best determined according to the site of the lesion.
cavernous malformations: surgical approaches and clinical experiences with 38 patients. Clin Neurol Neurosurg. 2014;116:72-79.
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CONCLUSIONS
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commercial or financial relationships that could be construed as a potential conflict of interest. Received 2 September 2018; accepted 2 November 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.11.008 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any
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