Surgical resection of upper-middle clivus chordomas via a modified anterior transpetrous approach

Clinical Neurology and Neurosurgery 130 (2015) 20–25

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Surgical resection of upper-middle clivus chordomas via a modified anterior transpetrous approach Ke Wang a,b,1 , Liang Wang a,b,1 , Kaibing Tian a,b , Xinru Xiao a,b , Zhen Wu a,b , Guijun Jia a,b , Liwei Zhang a,b , Junting Zhang a,b,∗ a Skull Base and Brainstem Tumor Division, Department of Neurosurgery, Beijing Tian Tan Hospital, Capital Medical University, Tiantan Xili 6, Dongcheng District, Beijing 100050, China b China National Clinical Research Center for Neurological Diseases, NCRC-ND, Tiantan Xili 6, Dongcheng District, Beijing 100050, China

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Article history: Received 26 June 2014 Received in revised form 6 December 2014 Accepted 20 December 2014 Available online 31 December 2014 Keywords: Clivus chordomas Modified ATPA approach Complication Survival

a b s t r a c t Background: Skull base chordomas are challenging and have a high rate of recurrence. Methods: A modified anterior transpetrous approach (ATPA) was performed in 17 upper clivus chordomas, and clinical data were retrospectively studied. Results: All 17 cases were radically treated via the modified ATPA, and the total removal and subtotal removal rates were 23.5% and 76.5%, respectively. The primary complaints were headaches and visual disturbances. The short-term postoperative complications were diplopia (12 cases, 70.6%) and facial numbness (7 cases, 41.2%). With a mean follow up of 44.5 months, 5 cases (29.4%) presented with tumor recurrence, and most cases had relatively good outcomes except for 2 patients who died because of rapid recurrence. The long-term complications were facial numbness (35.3%). Conclusions: The upper skull base chordomas could be radically removed via the modified ATPA under selected conditions, with limited complications and improved outcomes. The radical surgery treatment strategy was recommended for skull base chordomas. However, the present series included limited cases; therefore, post-operative follow-up, long-term outcomes and a larger number of cases of clivus chordomas should be observed to evaluate the effectiveness of the modified ATPA approach. © 2014 Elsevier B.V. All rights reserved.

1. Preface Chordomas are rare tumors that are derived from the remnants of the notochord, and approximately 32–49% of the tumors are found in the skull base region [1–3]. The prognosis of skull base chordomas is poor because of its invasive characteristics involving the bone, making total resection difficult, particularly when the tumor erodes into the clivus and brainstem [3–7]. Our previous report showed that the 5-year and 10-year survival rates were 79.4% and 67.6%, respectively, and the 5-year and 10-year recurrence rates were 34.7% and 52.9%, respectively [8]. Radical surgery

∗ Corresponding author at: Skull Base and Brainstem Tumor Division, Department of Neurosurgery, Beijing Tian Tan Hospital, Capital Medical University, Tiantan Xili 6, Dongcheng District, Beijing 100050, China. Tel.: +86 10 67098431; fax: +86 10 67091377. E-mail addresses: [email protected] (K. Wang), [email protected] (L. Wang), [email protected] (K. Tian), [email protected] (X. Xiao), [email protected] (Z. Wu), [email protected] (G. Jia), [email protected] (L. Zhang), [email protected] (J. Zhang). 1 These authors contributed equally to this work. http://dx.doi.org/10.1016/j.clineuro.2014.12.016 0303-8467/© 2014 Elsevier B.V. All rights reserved.

was the treatment of choice for skull base chordomas, and adjuvant radiotherapy may contribute to tumor control [8–10]. Tumors in the upper-middle clivus region are complicated by the involvement of the brainstem, cranial nerves and vasculature. Chordomas in this area are derived from epidural bones [11] and could be surgically removed via the an anterior approach by endoscopy [12–14]. In cases in which the tumor invaded the subdural spaces and expanded laterally, and, in particular, adhered to the brainstem and cavernous sinus, the risk for the anterior approach was high, and lateral approaches were more suitable [13]. Several lateral approaches, including the modified anterior transpetrous approach (ATPA), have been well illustrated for tumors of the upper-middle clivus by Xiao et al. [15]. Here, we present our series of 17 upper-middle clivus chordomas that were treated via the modified ATPA. 2. Materials and methods From June 2009 to June 2012, 17 patients with upper-middle clivus chordoma were surgically treated at the Department of Neurosurgery, Tian Tan Hospital, Capital Medical University. All of the

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Picture 1. The modified anterior transpetrous approach for upper-middle clivus chordomas. The basic surgical techniques of the modified ATPA approach. (A) The lateral decubitus position was used, a curved periauricular skin incision was started approximately 0.5 cm below the zygmatic arch (red arrow), approximately 11 cm in length. (B) After the skin flap, a pear-shaped bone flap was performed, and the dura mater was then excised. (C) The cerebellar tentorium and dura on the petrous apex were coagulated and incised to expose the petrous apex bone fully. (D) Drilling of the petrous apex bone (white arrow) was performed subdurally and began internally from the trigeminal impression. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

patients were treated via the modified ATPA approach. The maleto-female ratio was 1.125:1 (9:8), with a mean age of 43.9 ± 10 years. There were 4 recurrent patients, 3 of whom had received surgical treatment and gamma knife radiation before presenting to our department, and the remaining 1 case had only received surgical treatment 2 years before he came to our department. The primary complaints were visual disturbances (10 cases, 58.8%) and headaches (9 cases, 52.9%), and facial numbness was reported in 3 cases (17.6%). The period from the onset of the chief complaint to surgical treatment ranged from 1 month to 7 years, with a mean period of 14 months. After an evaluation of the magnetic resonance (MR) enhancement images and computed tomography (CT) bone window images, the modified ATPA approach was chosen as the surgical treatment for all of the patients based on the location of the tumor and on the erosion of the bone. Surgeries were performed under neurophysiologic monitoring (the motor evoked potential, oculomotor nerve, trigeminal nerve, and facial nerve). Details of the surgical approach of the modified ATPA have been illustrated by Xiao et al. [15], shown in Pictures 1 and 2. All of the patients underwent radical resection, which was confirmed by postoperative-enhanced MR images. During the modified anterior transpetrous approach, a curved periauricular skin incision was used, and the cerebellar tentorium and dura on the petrous apex were coagulated and incised

to expose the petrous apex bone fully. The drilling of the petrous apex bone was performed subdurally and began internally from the trigeminal impression [15]. Radical removal of the tumor was performed, and the infiltrated bones were removed. Fat transplants were used in order to avoid cerebrospinal fluid (CSF) leakage. The dura mater of the clivus was protected as much as possible. The treatment strategy was as follows: after a careful evaluation of all of the clinical details of the patients, radical resection of the tumor was performed under electrophysiological monitoring, and the neuronavigation system (Medtronic Inc., USA) was used in recurrent cases for the purpose of identifying possible difficult situations. Adjuvant radiotherapy was advised three months postoperatively after a thorough evaluation of the MR images. The surgical degree was confirmed by the senior surgeons and postoperative MR and CT images as follows: (1) gross total resection: no tumor residual detected on the postoperative MR and CT images, as well as during the surgeon’s observation under the microscope during the surgery; (2) subtotal resection: tumor residual less than 10% of the original volume; and (3) partial resection: tumor residual larger than 10% of the original volume. Gross total and subtotal removal were defined as radical resection. Tumor recurrence was defined as any newly identified enhancement after gross total resection or any increase in the tumor volume after subtotal resection. The tumor volume was calculated using the

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Picture 2. Surgical example of upper-middle clivus chordomas via a modified anterior transpetrous approach. (A, B) Preoperative contrast MR images. A diagnosis of a skull base chordoma was considered. (C) The postoperative CT scan bone window showed that the petrous apex was drilled (red arrow) and that the contralateral petrous apex was intact. The drilling area began internally from the trigeminal impression, usually not exceeding 1.5 cm laterally, not exceeding 6 mm forwardly from the posterior edge of the petrous ridge, and not exceeding 8 mm in depth from the surface of the petrous bone. (D–F) Post operative MR images (3 months later) showed the subtotal removal of the clivus chordoma (the suspected residual tumors are shown in the orange arrow) and the fat transplant (blue arrow) in the surgical area. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

following formula: (D1 × D2 × D3)/2; this calculation was performed by the same senior neurosurgeons when recording the surgery records using the image system. All of the cases were pathologically confirmed, and cases without pathological confirmation were excluded. All of the clinical data and MR and CT images were retrospectively studied in detail. Patient follow up was performed by postsurgical office visits and telephone interviews for those who could not visit the clinic. All of the patient data were compiled from the hospital and office records, imaging studies, and records provided by the patients themselves. All of the patients were volunteers under the protection of the Hospital Ethics Committee. Statistical analysis: the clinical and follow-up data were collected by database software (Epidata 3.02). Groups with or without postoperative radiation were compared. Kaplan–Meier survival analysis was performed using SPSS 12.0 (SPSS Version 12.0 software; SPSS Inc., Chicago, IL, USA).

cerebral artery territory, and the tumor growth rapidly led to death 8 months later. No CSF leakage was observed postoperatively. With a mean follow up of 44.5 months (8–64 months), 8 cases (47.1%) received radiation therapy, which consisted primarily of gamma knife radiation. Five cases (29.4%) had tumor recurrence. Of these, two patients (11.8%) died due to rapid tumor growth 8 months and 12 months after surgery. There were no significant differences between postoperative radiotherapy and recurrence (p = 0.671, Picture 3). All of the primary cases had a

3. Results All of the 17 patients underwent radical resection via the modified ATPA approach. Of these, 4 (23.5%) patients underwent gross total resection, and 13 patients (76.5%) underwent subtotal resection; there were no cases of partial resection. The tumor volume of the 17 cases ranged from 5 to 75 ml with a mean volume of 23 ml. Three cases were pathologically confirmed as chondroid chordomas; the remaining cases were classic chordomas; details are shown in Table 1. Short-term postoperative complications were diplopia (12 cases, 70.6%) and facial numbness (7 cases, 41.2%) (Table 2). One recurrent case had brain infarction in the middle

Picture 3. The relationship between postoperative radiation and tumor recurrence (p = 0.672).

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Table 1 Clinical data of the 17 clivus chordomas. No. Gender Age (year)

Previous history

Chief complain

Time of chief complain

Volume Surgical (ml) degree

short term complication

Follow up (months)

Radiation

Recurrence KPS

1

F

61

N

Headache, dizziness

1 month

6

Total

64

N

N

90

2

F

40

Operation

hoarseness

6 months

16

Subtotal

56

Y,␥-knife

N

90

3 4

M F

48 54

N N

10 days 3 months

9 19

Total Subtotal

54 48

Y,␥-knife Y, *

N N

90 90

5

M

55

N

diplopia Impaired vision, dizziness Headache

Blepharoptosis, diplopia Facioplegia, abducent paralysis Facial numbness Facial numbness

4 years

5

Total

48

N

N

90

6

M

50

75

Subtotal

53

Y,␥-knife

N

80

M

47

Bucking, right limb weakness Impaired vision, facial numbness

8 months

7

4 months

28

Subtotal

Cerebral infarction, limb weakness

8

N

Y

0

8

M

46

␥-knife and EEA Radiation* and operation N

3 months

13

Subtotal

abducent paralysis

36

N

N

100

9 10 11

M F F

46 34 31

N N N

Diplopia, facial numbness headache Headache, diplopia Medical test

12 months 2 years 2 months

9 13 12

Subtotal Total Subtotal

51 29 54

Y,* Y,␥-knife N

N Y N

90 70 90

12 13

M M

44 44

N N

Headache, diplopia Diplopia, headache, dizziness, numbness

4 months 3 years

9 50

Subtotal Subtotal

39 34

Y,␥-knife N

Y N

80 90

14 15

F M

53 19

N N

Headache, diplopia Headache, diplopia

6 months 7 years

28 11

Subtotal Subtotal

34 33

N N

N N

90 100

16 17

F F

34 41

N Radiation*

Diplopia Headache, impaired vision

3 months 4 months

72 15

Subtotal Subtotal

abducent paralysis abducent paralysis abducent paralysis, facial numbness abducent paralysis Epilepsy, abducent paralysis, facial numbness abducent paralysis Blepharoptosis, diplopia, facial numbness abducent paralysis Blepharoptosis, diplopia, facial numbness

31 12

N Y,*

Y Y

90 0

Facial numbness, right limb weakness right limb weakness

F, female; M, male; N, none; Y, yes; EEA, endoscopic endonasal approach. * , The radiation type was missing. Table 2 Clinical symptoms of patients. Pre-operation

Short term complication

Long term complication

Sign

Cases (%)

Sign

Cases (%)

Sign

Cases (%)

visual disturbance headache facial numbness

10 (58.8%) 9 (52.9%) 3 (17.6%)

diplopia facial numbness blepharoptosis

12 (70.6%) 7 (41.2%) 3 (17.6%)

facial numbness diplopia recurrence

6 (35.3%) 4 (23.6%) 5 (29.4%)

relatively good Karnofsky performance scale (KPS) score during the follow-up period; at the last follow up, most of the patients received a KPS score of 90 or 100 (11 cases, 64.7%), 2 cases (11.8%) received a KPS score of 80, while 1 case (5.9%) received a score of 70 due to tumor recurrences, twice re-surgeries and one radiation therapy. The diplopia was recovered in 8 cases; however, facial numbness was only recovered in 1 case. Except for one patient who had brain infarction and died, none of the other patients developed language abnormalities of any type. One patient had a seizure after the surgery that was controlled with sodium valproate, and the seizures disappeared, although he had quit the medical treatment during the 34-month follow up. 4. Discussion Skull base chordoma is of epidural origin [1,2], and the rationale to choose the most suitable approach, both in the short term and long term, was to achieve the best tumor control rate and reasonable quality of life [3–8]. Many approaches have been well illustrated in the literature, including the frontal and lateral approaches. Overall, most middle-line clivus chordomas could be treated via frontal approaches, such as endonasal transsphenoidal

surgery using endoscopy [12]. Such approaches could be ideally used when the tumors are limited to the middle line, without extensive lateral extension. However, due to the limited surgical exposure and because the tumors may infiltrate intradurally into areas such as the cavernous sinus and/or an area close to the internal carotid, the frontal approaches could be of high risk, and incomplete resection which could result in higher recurrence rates [13]. Additionally, the frontal approaches may be associated with other complications, including CSF leakage, tension pneumocephalus, and intracranial hematoma [12–14]. Our earlier experiences with upper and middle skull base chordomas mostly involved treatment through the presigmoidal approach [8]. This approach can provide sufficient surgical access to skull base tumors and results in high rates of complete resection. However, the disadvantages are a high rate of complications and a prolonged surgical time [16]. The anterior transpetrous approach (ATPA) was first introduced by Bochenek and Kukwa [17]. Subsequently, Kawase and colleagues modified this approach for petroclivus tumors [15,18]. While the ATPA approach involves drilling the petrous apex bone extradurally, the present modified ATPA involves drilling the petrous apex bone subdurally, using the trigeminal impression and posterior

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edge of the ridge as landmarks [15], this approach can be easily performed with adequate equipment. In our previous report by Xiao et al. [15], the modified ATPA provided sufficient exposure to the area of the middle and upper petroclivus and medial side of the internal acoustic meatus (IAM) through drilling of the apical bone, a procedure that was very important for the radical resection of upper-middle clivus chordomas because these tumors are usually located ventral to the midbrain and pons and infiltrate the clivus without clear margins. Therefore, the modified ATPA can provide a sufficient and safe exposure for procedures under the microscope for complete resection of the tumor. Using the modified ATPA, the present data showed that the 17 cases of upper clivus chordoma underwent radical resection, as the modified ATPA provided sufficient exposure of the upper clivus. Compared with the presigmoidal approach [8], the present modified ATPA can also provide a high rate of radical resection without CSF leakage [15]. In addition, the benefit of the modified ATPA approach was obvious in that the operation time may be much shorter and much safer than the presigmoidal approach [8,15] because the modified ATPA approach avoids treatment of the vital sigmoid sinus. Third, the modified ATPA approach, compared with the endonasal transsphenoidal approach, could provide better exposure to intradural tumors as well as to those parts extending laterally (unilaterally) and sufficient exposure for the tumors in the middle line. Thus, increased chances and safety exist for radical resection by protecting the brain stem directly under microscopic review, and the combination use of the navigation system may helpful considering the complicated anatomy relationship, particularly in recurrent cases. However, the present modified ATPA approach has its own shortcomings for skull base chordomas that the approach involved opening the dura mater of the skull base and manipulating it subdurally. Additionally, it was noticed that the dura mater may contribute to the prognosis [19]. Although the exact role of the dura mater for the prognosis is unknown presently, the clivus dura mater was carefully protected during the surgical procedure. Because the cases enrolled in the present series were all of dura mater breakthrough, a precise conclusion regarding the significance of the clivus dura mater for the prognosis of chordomas was difficult to make. Radical resection may result in a higher rate of complications, including CSF leakage, particularly in cases with extensive bone infiltration by the tumor [8–10]. Special attention was paid to CSF leakage, and in the present series, no such complications were noticed. During the surgery, the dura mater of the clivus was protected with careful resection, and the fat transplants adhering to the surgical area after the tumor was removed. Additionally, the drilled apical bones were carefully waxed. Although the surgeries were performed with special care to prevent injury to the cranial nerves under the surveillance of neurophysiologic monitoring (the motor evoked potential, oculomotor nerve, trigeminal nerve, and facial nerve), the major complications via the modified ATPA were cranial nerve palsies. The present series showed that the fifth cranial nerve was the most vulnerable nerve that could be easily injured and hard to recover, thereby causing permanent complications, which were higher than those reported in the literature. One possible reason was that when the tumors were infiltrating into the cavernous sinus area, they released the 5th cranial nerve and were manipulated just beneath it, which was of high risk. Tumors in this area present a challenge and should be manipulated carefully. The other common complications were visual disturbances (diplopia): up to 58.8% of patients had signs before surgery, and 70.6% had signs during the postoperative period; however, the symptoms were recovered during the postoperative period. Although the present series showed that the visual disturbances (diplopia) were recovered in most of the cases, special attention should be paid during the surgery to protect the 3rd, 4th, and 6th nerves, particularly when coagulating and

cutting the edge of the cerebellar tentorium for the 4th cranial nerve located just beneath it. It was reported in the literature that the 6th cranial nerve was also a major problem of postoperative diplopia via the endoscopic endonasal approach for centrally located clival chordomas [14], possibly suggesting that the 6th nerve may be impaired by the tumor; however, this nerve should be protected whenever possible. It was noted that during the modified ATPA or lateral approaches, there were risks of temporal lobe injuries [15] that may have resulted in epilepsy or language disorders. To avoid such complications, during the modified ATPA, the squamous part of the temporal bone was drilled by adjusting the angle, and the lower edge of the bone window was flattened to the button of the middle fossa. Next, the cerebrospinal fluid (CSF) was carefully released underneath the temporal lobe, and a lumbar puncture was performed at the very beginning of the surgery to prepare for difficult situations. In addition, during the entire surgical procedure, it was extremely critical to manipulate the tissue gently and correctly. In the present series of 17 cases, only one patient developed epilepsy and a language disorder. Both the present series and the series of Xiao et al. [15] showed that the temporal lobe could be well protected via the modified ATPA. Skull base chordomas have been shown to have a poor prognosis. Radical resection, tumor pathology indicating a chondroid chordoma, and postoperative radiation have been shown to indicate a relatively good prognosis [3–6]. The present series, compared with our previous report by Wu et al. [8], had a lower recurrence rate and a higher survival rate at 3 years after the surgery. There were several possible underlying reasons. First, all of the cases in the present series received radical surgical treatment. The radical strategy has been advocated and well illustrated by many authors. Sen et al. [20] reported their series of 71 clivus chordomas with 58% radical resection and a 5-year overall survival of 75%. Ito et al. [9] reported on their consecutive 19 clivus chordomas with initial aggressive resection and a mean follow up of 80.2 months. All of the cases in their series survived, and the 5-year progression-free survival rate was 47.9%. Our present data supported those results and radical resection for skull base chordomas. However, our study had an enrollment bias. Among the enrolled patients, only 4 cases (23.5%) had previously undergone treatment compared with 33.0% of previous surgical treatments in the report by Wu et al. [8]. The recurrent chordomas were more challenging for surgeries. In some circumstances, palliative surgeries were advocated to protect the function of the patients [21]. In the present series, 4 patients with treatment histories were surgically treated, and subtotal resections were achieved. During the follow-up time, two of the patients died because of the rapid progression of the tumor. However, due to the slow-growing character of the tumor, the other 2 cases were in good condition during the follow up at 53 months and 56 months (KPS 80 and 90 scores, respectively). These results indicate that recurrent chordomas may have a good prognosis after radical treatment. Tumor size was a prognostic factor for skull base chordomas [3]. A small tumor may contribute to the high rate of complete resection. In a retrospective analysis, the author revealed that a large tumor size with a diameter greater than 5 cm was associated with an increased rate of death [3]. The present series, with a mean tumor volume of 22.9 ml, supported the conclusion that the tumor size was an independent risk factor and that small chordomas have a better prognosis. There were 3 cases of chondroid chordomas in the present series, and all cases had a good prognosis and did not present with any recurrence. The better prognostic factor of the chondroid subtype supported data reported in the literature [1–6]. In the present series, which combined radical surgery with adjuvant radiotherapy, only 8 cases received postoperative

K. Wang et al. / Clinical Neurology and Neurosurgery 130 (2015) 20–25

radiation, mostly gamma knife radiation. There was no correlation between the postoperative radiation treatment and recurrence in the present limited case series. This result was in accordance with the systematic report by Dimiao et al. [4]. In their meta-analysis, 58 cases of complete resection were compared based on whether the patients had received adjuvant radiation. The results showed that there was no difference in the 5-year recurrence and survival rates. However, it has been reported that adjuvant radiotherapy could help in tumor control [9,22,23]. In their meta-analysis, Jian et al. [22] suggested that adjuvant radiotherapy may improve the rate of recurrence. Gamma knife radiation [23,24], proton beam radiation and photo beam radiation [25,26], particularly the heavy ion radiation of carbon therapy, have been reported to control chordomas effectively [27]. Although there is no consensus in the literature [3–6], the advocated treatment strategy for skull base chordomas is radical surgery, and adjuvant radiotherapy is advocated for 3 months postoperatively, particularly in patients with a residual tumor [8]. In summary, the present series of 17 skull base chordomas showed that in selected cases, the upper-middle skull base chordomas can be radically removed via the modified ATPA with limited complications and improved outcomes. For skull base chordomas, although challenging, a good understanding of different approaches and choosing the most suitable approaches for the purpose of radical surgery were advocated. However, the present series consisted of limited cases; therefore, post-operative follow ups, long-term outcomes and a large number of cases should be observed for the effectiveness of the modified ATPA approach regarding radical surgery for upper-middle clivus chordomas. Conflict of interest The authors declare no conflict of interest. Disclosure This work was supported in part by the National Natural Science Foundation of China (Grant No. 81101910), Natural Science Foundation of Beijing, China (Grant No. 7142052). Acknowledgments We are grateful to the study subjects for participating in the research. References [1] Chambers KJ, Lin DT, Meier J, Remenschneider A, Herr M, Gray ST. Incidence and survival patterns of cranial chordoma in the United States. Laryngoscope 2014;124(5):1097–102. [2] Hung GY, Horng JL, Yen HJ, Yen CC, Chen WM, Chen PC, et al. Incidence patterns of primary bone cancer in Taiwan (2003–2010): a population-based study. Ann Surg Oncol 2014;21(8):2490–8. [3] Lee J, Bhatia NN, Hoang BH, Ziogas A, Zell JA. Analysis of prognostic factors for patients with chordoma with use of the California Cancer Registry. J Bone Joint Surg Am 2012;94(4):356–63.

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