- Email: [email protected]
Significance of the Tentorial Alignment in Protecting the Occipital Lobe with the Poppen Approach for Tentorial or Pineal Area Meningiomas
Accepted Manuscript Significance of the tentorial alignment in protecting the occipital lobe through the Poppen approach for tentorial or pineal area meningiomas Deling Li, MD, Haoyu Zhang, MD, Wang Jia, MD, Liwei Zhang, MD, Junting Zhang, MD, Weiming Liu, MD, Ming Ni, MD, Guijun Jia, MD PII:
S1878-8750(17)31310-4
DOI:
10.1016/j.wneu.2017.08.013
Reference:
WNEU 6263
To appear in:
World Neurosurgery
Received Date: 18 March 2017 Revised Date:
29 July 2017
Accepted Date: 1 August 2017
Please cite this article as: Li D, Zhang H, Jia W, Zhang L, Zhang J, Liu W, Ni M, Jia G, Significance of the tentorial alignment in protecting the occipital lobe through the Poppen approach for tentorial or pineal area meningiomas, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.08.013. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Significance of the tentorial alignment in protecting the occipital lobe through the Poppen approach for tentorial or pineal area meningiomas Deling Li
1*
, MD, Haoyu Zhang 1,
MD, Weiming Liu
MD,
Wang Jia 1,
MD, Liwei
Zhang 1,
MD, Junting
Zhang 1,
1
, MD, Ming Ni 1, MD, Guijun Jia 1#, MD
1 Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University; Beijing Key
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Laboratory of Brain Tumor, Beijing, China. China National Clinical Research Center for Neurological Diseases (NCRC-ND)
#Corresponding author: Guijun Jia
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Phone: 96-10-67098431 Fax: 86-10-67051377
tentorium, tentorial angle, meningiomas, Poppen
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Key words:
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Email:[email protected]
ACCEPTED MANUSCRIPT Abstract Object. We aimed to identify the factors that can predict the risk of occipital lobe damage preoperatively when resecting tumors located at the tentorial or pineal regions through the occipital-transtentorial approach (Poppen approach).
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Methods. In 27 consecutive patients who underwent tumor resection through the Poppen approach for tentorial or pineal region meningiomas, the following morphologic parameters were assessed on a preoperative MRI: 1) tentorial angle; 2) tentorial length; 3) the shortest distance from the confluence of sinus to the tumor. All these parameters, together with tumor size,
test, chi-square test, or Fisher’s exact test.
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texture, and resection extent, were correlated with occipital lobe damage by using the ANOVA
Results. The mean value was 55.3±5.6° (range 45-66°) for the tentorial angle, which was
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significantly associated with the occipital lobe damage grades (p=0.008), but this was not the case for the tentorial length (p=0.802) and the shortest distance from the confluence of sinus to the tumor (p=0.695). Interestingly, age was also strongly associated with occipital lobe damage risk (p=0.020). The patients in the subgroup with no occipital damage (Grade 4) were the youngest (aged 47.3 years), compared with other grades, with age of 58.0 years for Grade 1, 54.3 years for Grade 2, and 58.6 years for Grade 3. These two parameters were also significant after multivariate analysis. No correlation was observed between either tumor nature or the extent of
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resection and damage grades.
Conclusions. The risk of occipital lobe damage increases in the presence of a steep tentorial angle during the Poppen approach for tentorial or pineal area tumors. Awareness of such anatomical features preoperatively is important for minimizing operative complications. tentorium, tentorial angle, meningiomas, Poppen.
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Key words:
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Abbreviations used in this paper:
TM = Tentorial meningiomas; TA = Tentorial angle; MRI = magnetic resonance imaging; ANOVA = one-way analysis of variance; CSF = cerebrospinal fluid.
ACCEPTED MANUSCRIPT Introduction Tentorial meningiomas (TM) are complex entities that require multiple surgical approaches, according to the tumor position and its relationship with the surrounding structures12,16. Based on the tumor’s location and direction of growth, there could be several surgical approaches for removing the tumor safely 8. The POPPEN approach, or occipital interhemispheric transtentorial approach, is often undertaken if the tumor is located at the posteromedial or anteromedial
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tentorium, or even along the tentorial notch2,7,12. Similarly, the pineal region meningiomas, especially falcotentorial meningiomas, are usually surgically resected through the POPPEN approach, which usually causes occipital lobe damage
10,15
. Occipital lobe damage may cause
hematoma, which has to be evacuated by a secondary operation and may lead to vision problems
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such as hemianopia 6,9,13.
Thus far, there has been no research on the factors associated with this severe surgical complication and how to decrease the risk. In resecting tumors through the POPPEN approach,
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one of the most important procedures is lifting up the occipital lobe on the retractor, which can cause local hyperperfusion of the retracted occipital region and even visual field defect without obvious occipital lobe damage seen on a CT 18. In our experience, whether the tentorium is steep or flat can be associated with the difficulty of lifting up the occipital lobe, and this might be one factor that correlates to the extent of occipital lobe damage. The tentorial angle (TA) was used to quantify the slope of the tentorium with several calculation methods 11,14,17.
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In addition to the TA, there might be other factors associated with occipital lobe damage, including tumor characteristics such as the direction of growth (superior or inferior), the texture (soft or hard), and the tumor size; and intraoperative parameters such as blood loss volume, length of operation, and the tumor resection grade. All these parameters should be analyzed
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together to determine which factors are independent factors that should be given more attention to decrease the occipital lobe damage complication during surgery.
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This research summarizes our retrospectively analyzed data of 27 patients with tentorial or pineal region meningiomas. We aimed to identify the factors that can predict the risk of occipital lobe damage, so that patients can be informed possible complications before resection of tumors located at the tentorium or pineal region through the Poppen approach. Our observations provided the basis for analyzing the relationship between the morphology of the tentorium, especially the tentorial angle, and the risk of damage to the occipital lobe in resecting tentorial or falcotentorial meningiomas through the POPPEN approach, and provide further insight into how to lower the risk with appropriate surgical skills.
Materials and Methods By scanning the clinical data in Beijing Tiantan Hospital, we found a total of 112 cases of tentorial
ACCEPTED MANUSCRIPT meningiomas (TM) admitted to the neurosurgical department between 2012 and 2015. Only the TM cases treated with the POPPEN approach were included in the research. Two patients in whom tumors involved the occipital pole were excluded, and two other patients with tumors larger than 6 cm that were accompanied with hydrocephalus were also excluded. The research flowchart is shown in Fig. 1. The records of all 23 TM cases, plus another four cases with pineal falcotentorial meningiomas on which tumor resection through the POPPEN approach was
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performed, were retrospectively reviewed for clinical presentation, radiological imaging, surgical record, and outcome. TA was measured as the angle between the tentorium and the line drawn from the hard palate (indicated in Fig. 2E) according to the criteria by Burak Sade and Joung H. Lee
11
. The extents of occipital lobe damage were divided into four categories: hematoma
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(Grade 1), punctate hemorrhage (Grade 2), brain edema (Grade 3), and normal (Grade 4), based on the postoperative CT scan or magnetic resonance imaging (MRI) (indicated in Fig. 2).
system for tumor removal 5.
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The extent of tumor resection for meningiomas was classified according to the Simpson grading
Intergroup frequencies among the four grades of occipital lobe damage were compared using the one-way analysis of variance (ANOVA) for continuous variables such as patient age, maximum diameter of tumor, tentorial angle, and tentorial length, and using theχ2 /Fisher exact test method for categorical variables such as sex, tumor location, tumor texture, and extent of the
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resection. We divided the occipital lobe damage to binary data including having occipital lobe damage (Grade 1, 2, and 3) and not having occipital lobe damage （Grade 4） ，and then analyzed the significant factors from univariate analysis with multivariate logistic regression analysis to see whether this parameter could be an independent factor. Statistical analysis was performed using
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commercial statistical software (SPSS 23.0, SPSS Inc., Chicago, IL, USA). A P value less than 0.05 was considered statistically significant.
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Results
There was no operative mortality. All patients were positioned prone laterally intraoperatively. A 58-year-old patient who had the most severe occipital lobe damage had an occipital lobe hematoma, which was found 6 h after tumor resection and emergency hematoma evacuation was performed immediately (Fig. 3). Homonymous hemianopia appeared in this patient, and was not resolved 6 months postoperatively. Another tentorial meningioma patient with Grade 2 occipital lobe damage, with punctate hemorrhage at the occipital lobe on the postoperative CT scan which did not need to be evacuated by secondary operation, was also shown (Fig. 4). The radiologic parameters, including the tumor extension, tumor texture, maximum diameter of tumor, TA, tentorial length, and the shortest distance from the confluence of sinus to the tumor, did not correlate significantly with the occipital lobe damage (Table 1).
ACCEPTED MANUSCRIPT However, age was strongly associated with occipital lobe damage risk (p=0.020). The patients in the subgroup with no occipital damage (Grade 4) were the youngest (aged 47.3 years), compared with the patients in other subgroups, with ages of 58.0 years for Grade 1, 54.3 years for Grade 2, and 58.6 years for Grade 3, respectively. The mean values of the TA were 55.3±5.6° (range 45-66°) and were significantly associated with occipital lobe damage grade (p=0.008). The most severe occipital lobe damage occurred in a 58-year-old male patient who had the steepest tentorium
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(TA=66°) and required a secondary hematoma evacuation rescue surgery. The mean values of TA were (58.9±5.8) ° for Grade 2, (55.6±2.3) ° for Grade 3, and (52.2±4.8) ° for Grade 4.
For blood loss in the operation, we found that a tendency to lose more blood may lead to more severe occipital lobe damage, although this finding was not significant.
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For the multivariate analysis of age and tentorial angle parameters, considering the group 1, 2 and 3 as damage group , we found that TA and age were both independent factors that correlated with occipital lobe damage after removal of tentorial tumors through the POPPEN
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approach (respectively p=0.024 and p=0.029) (Table 2). The cutoff point was identified as tentorial angle≥53° to predict more likely of occipital damage, with sensitivity of 87% and specificity of 67%.
Discussion
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This is the first research project to study the relationship of prognostic factors, including radiologic feature of the tumor itself, such as the texture, size, and location;. and the intraoperative factors such as the length of surgery, the blood loss volume, and resection grade of the tumor, with the grade of occipital lobe damage in the tumor at the tentorial and pineal
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regions resected through the POPPEN approach.
We found that the patients' age and TA were statistically significant factors leading to an
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increased chance of postoperative occipital lobe injury, but this was not the case for the other parameters. First, the older the patients, the more likely they were to suffer occipital lobe damage during surgery. One reason could be that brain compliance usually decreases with aging. The textures were usually different in the brains of patients of different ages. The brains of elderly patients were more prone to be contused with head accidents, and age was proven to be one of important prediction factors of hemorrhagic progression of contusions in traumatic brain injury 3. It was the similar case in the TMs removal operation while lifting up the occipital lobe. Second, we found that the TA was the significant radiologic parameter related to the extent of occipital lobe damage. In the patients with a larger tentorial angle, it was much more difficult for neurosurgeons in the course of retracting the occipital lobe upward to release cerebrospinal fluid (CSF) and then resect the tumor. Hence, this parameter found in preoperative radiologic features
ACCEPTED MANUSCRIPT can be used as a prognostic factor for intraoperative occipital lobe damage complications in operating on tumors at the tentorial region via the POPPEN approach. Before this study, we thought about that longer time in surgery might be associated with more severe occipital lobe damage, because the occipital lobe had to be lifted up and retracted in the course of the operation. However, the length of surgery did not prove to be significantly associated with the extent of occipital lobe damage in our study. The reason for this might be
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that after sufficient CSF was released from the ambient cistern or quadrigeminal cistern, the pressure on the occipital lobe by the retractor was minimal, and to some extent, it was different from other retraction operations. Releasing CSF as soon as possible after a craniotomy was almost our routine procedure in surgery for these patients.
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The blood loss might be associated with occipital lobe damage. One reason was that occipital lobe damage, especially hematoma, could be one origin of intraoperative bleeding, and the second reason was that more blood loss could be attributed to the sacrifice of venous bleeding,
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which might increase the hyperperfusion condition after tumor removal. However, we discovered that more blood loss tends to accompany more severe occipital lobe damage. This indicates that when abundant blood was lost that contributed to other factors such as the tumor itself, occipital lobe damage could be avoided.
Our study excluded the huge tentorial meningiomas larger than 6 cm in diameter. We also excluded tumors with hydrocephalus, because if hydrocephalus existed, it was more difficult to
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release CSF by retracting the occipital lobe; sometimes we preferred CSF external drainage through the frontal or occipital horn of the lateral ventricles to decrease intracranial pressure before opening the dura mater.
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Practical Implications
Patient position and cervical vertebra flexure were important in the occipital interhemispheric
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transtentorial approach. Compared with the patients in a prone position, those positioned laterally had lower blood loss, shorter operations, decreased cerebral edema, and better visual outcomes. The researchers concluded that gravity retracted the occipital lobe when the patients were positioned laterally with enhanced operative exposure 4. We always positioned the patients laterally, and slightly rotated the head to make the medial one-third of the transverse sinus highest, while at the same time flexing the cervical vertebra and retracting the lower mandible. The side used for the craniotomy was based on gravity aiding occipital retraction. All these requirements for positioning were used to make the posterior occipitalis sufficiently exposed, retract the occipital lobe more easily, and take advantage of gravity to retract the occipital lobe. If the TA is large, we recommend making the best of this position to lower retraction pressure and the likelihood of occipital lobe edema and damage.
ACCEPTED MANUSCRIPT The craniotomy flap edges were just lateral to the superior sagittal sinus and superior to the transverse sinus. It was especially important to expose the inferior edge adequately, and no bone eaves were left to prevent direct visualization of the tentorium. The retracting pressure and direction were important for protecting the occipital lobe. First, the pressure against the occipital lobe had to be as low as possible after sufficient CSF was released. Intermittently releasing the retractor, as well as using a broader retractor, were important key
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points for decreasing the likelihood of occipital lobe damage intraoperatively. Second, the direction of retracting the occipital lobe was important for protecting it during resection of tumors in the tentorial region. If the patients had a relatively large TA, we preferred to choose the optimal surgical corridor of the posterior interhemispheric approach, which could lower
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retraction pressure to the occipital lobe compared with directly lifting up or retracting the occipital lobe. This also could decrease the probability of sacrificing multiple occipitobasal veins, which drain into the tentorial sinuses and are located just medial to the transverse sinus 1 in the
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course of exposing the tumor along the tentorium. The draining veins damage could cause local hyperperfusion of the occipital region and made it more prone to the retracting pressure. It was important to release CSF before beginning to remove a tumor, especially for small tumors. If enough CSF is released, it might not be necessary to retract the occipital lobe if patient positing is adequate and intraoperative hyperosmolar agents are administered. The position for CSF release was also important for protecting the surrounding normal brain tissue, including the
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occipital lobe. The ambient cistern or quadrigeminal cistern was usually where we chose to release CSF. If the patient had a relatively large TA and enlarged lateral ventricles, we could make CSF external drainage and decrease intracranial pressure. If the tumor was relatively large and obstructed the cerebrospinal fluid flowing channel, we predicted that CSF leakage might be
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difficult, and chose external drainage from the lateral ventricle. Like the core spirits of microsurgical neurosurgery, how to achieve tumor removal through small
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exposure is also critical for TMs or other tumors at tentorial region. As the intracapsular contents are removed, the tumor collapses, thus making it possible to remove more tumor through the small exposure. If the tumor is relatively large and the TA is big, we recommend that this operative technique should be applied thoroughly.
Conclusions The tentorial angle, which could depict the steep extent of the tentorium, was significantly associated with occipital lobe damage, while resecting the tentorial meningiomas and other tumors located at tentorial or pineal region through the POPPEN approach. Awareness of such anatomical features at the time of preoperative planning is of paramount importance in selecting the optimum surgical approach and minimizing operative complications.
ACCEPTED MANUSCRIPT Acknowledgments The authors are grateful to Pinan Liu, Jisheng Wang, and other relevant staff members of Beijing Tiantan Hospital, who helped perform surgery for patients. In addition, we would like to thank Junmei Wang for providing pathological determinations. This work was supported in part by the National Key Technology Research and Development Program of the Ministry of Science and
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Technology of China (2013BAI09B03, 2014BAI04B01, 2015BAI12B04), the National Natural Science Foundation of China Projects (81502156), the Beijing Municipal Administration of Hospitals’ Youth Program (QML20150502), and the Capital Health Research and Development of
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Special Expert(2016-4-2049).
Disclosure
or the findings specified in this paper.
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The authors report no conflict of interest concerning the materials or methods used in this study
Table 1. Demographic, radiologic parameter and operation characteristics of patients with tentorial meningiomas, pineal region meningiomas, and hemangioblastomas at vermis cerebellum operated through the Poppen approach.
angles).
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Table 2. The multivariate analysis of significant factors from univariate analysis (age and tentorial
Fig. 1. The research flowchart.
Fig. 2. Assessment of occipital lobe damage by postoperative CT scan and magnetic resonance imaging (MRI) compared with preoperative MRI. A: Grade 1, postoperative occipital lobe
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hematoma with secondary operation; B: Grade 2, punctate hemorrhage; C: Grade 3, more severe occipital edema than preoperatively；D：Grade 4, none; E: MRI showing the measurements of the
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tentorial angle; F: The tentorial angles significantly correlated to occipital lobe damage grades (p=0.011).
Fig. 3. A tentorial meningioma patient with Grade 1 occipital lobe damage. A-B: Preoperative axonal and coronal enhancement MRI scan showed a meningioma inferior to the tentorium; C: The tentorial angle was 66 degrees; D: The CT scan at 6 hours postoperatively showed a hematoma at occipital lobe, and the patient received the second operation; E: The CT scan after the second operation; F: The MRI scanning 1 week postoperatively. Fig. 4. A tentorial meningioma patient with Grade 2 occipital lobe damage. A-C: Preoperative MRI scanning showed tentorial meningioma, and the tentorial angle was 63 degrees. D: The CT scan on the night after the operation showed punctate hemorrhage at the occipital lobe with conservative therapy. E: The first day postoperative CT showed a little absorption. F: 1 week
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Sade B, Lee JH: Significance of the tentorial alignment in approaching the trigeminal nerve and the ventral petrous region through the suboccipital retrosigmoid technique. J Neurosurg 107:932-936, 2007
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transtentorial approach. Clin Neurol Neurosurg 115:1250-1256, 2013
ACCEPTED MANUSCRIPT Table 1. Demographic, radiologic parameter and operation characteristics of patients with tentorial meningiomas, pineal region meningiomas operated via Poppen approach. Occipital lobe damage Grade 1(n=1)
Occipital lobe damage Grade 2(n=7)
Occipital lobe damage Grade 3(n=7)
Occipital lobe damage Grade 4(n=12)
P value
Sex distribution, no. of male Age (yrs) Tumor location#
1
2
1
6
0.228
58.0 B(1)
Tumor texture
Soft(1)
54.3±9.2 B(4) I(3) S(0) Hard (2) Medium (5)
58.6±7.8 B(2) I(2) S(3) Hard (2) Medium (5)
Maximum diameter (mm) Tentorial angle (degrees) Tentorial length (mm) The least distance from confluence of sinus to tumor （mm） ） Operation duration (min) Blood loss (ml)* Resection grade
32.2
37.5±11.9
35.4±13.5
66.0
58.9±5.8
50.7 13.1
0.020 0.100
55.6±2.3
52.2±4.8
0.008
43.6±8.0
46.5±7.8
45.2±7.7
0.802
24.1±19.8
22.0±11.9
28.4±14.5
0.695
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47.3±5.6 B(6) I(6) S(0) Hard (3) Medium (8) Soft(1) 30.9±7.1
0.287
0.584
330±68.4
290.0±72.4
313.3±72.0
0.583
1700 Grade 4(1)
650±500 Grade 2(4) Grade 4(3)
329±95 Grade 2 (6) Grade 3(1) Grade 4(0)
350±145 Grade 1(3) Grade 2(7) Grade 3(1) Grade 4(1)
0.184 0.089
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240.0
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#
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Parameter
I：Inferiorly of tentorium; S: superiorly of tentorium; B: grew both inferiorly and superiorly of tentorium. *Analyzed by nonparameteric analysis.
ACCEPTED MANUSCRIPT Table 2. The multivariate analysis of significant factors from univariate analysis ( age and tentorial angles). Yes（ （n=15） ）
No（ （n=12） ）
P value
Angle Age
57.8±5.0 56.5±8.2
52.2±4.8 47.3±5.6
0.024 0.029
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ACCEPTED MANUSCRIPT Highlights The tentorial angle was first used to correlate the risk of occipital lobe damage in the series of tentorial meningioma with POPPEN approach and found to be the most important factor compared to the tumor itself characters and other anatomical features.
According to our finding, some important skills for lowering operative complications were figured out.
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S1878-8750(17)31310-4
DOI:
10.1016/j.wneu.2017.08.013
Reference:
WNEU 6263
To appear in:
World Neurosurgery
Received Date: 18 March 2017 Revised Date:
29 July 2017
Accepted Date: 1 August 2017
Please cite this article as: Li D, Zhang H, Jia W, Zhang L, Zhang J, Liu W, Ni M, Jia G, Significance of the tentorial alignment in protecting the occipital lobe through the Poppen approach for tentorial or pineal area meningiomas, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.08.013. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Significance of the tentorial alignment in protecting the occipital lobe through the Poppen approach for tentorial or pineal area meningiomas Deling Li
1*
, MD, Haoyu Zhang 1,
MD, Weiming Liu
MD,
Wang Jia 1,
MD, Liwei
Zhang 1,
MD, Junting
Zhang 1,
1
, MD, Ming Ni 1, MD, Guijun Jia 1#, MD
1 Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University; Beijing Key
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Laboratory of Brain Tumor, Beijing, China. China National Clinical Research Center for Neurological Diseases (NCRC-ND)
#Corresponding author: Guijun Jia
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Phone: 96-10-67098431 Fax: 86-10-67051377
tentorium, tentorial angle, meningiomas, Poppen
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Key words:
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Email:[email protected]
ACCEPTED MANUSCRIPT Abstract Object. We aimed to identify the factors that can predict the risk of occipital lobe damage preoperatively when resecting tumors located at the tentorial or pineal regions through the occipital-transtentorial approach (Poppen approach).
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Methods. In 27 consecutive patients who underwent tumor resection through the Poppen approach for tentorial or pineal region meningiomas, the following morphologic parameters were assessed on a preoperative MRI: 1) tentorial angle; 2) tentorial length; 3) the shortest distance from the confluence of sinus to the tumor. All these parameters, together with tumor size,
test, chi-square test, or Fisher’s exact test.
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texture, and resection extent, were correlated with occipital lobe damage by using the ANOVA
Results. The mean value was 55.3±5.6° (range 45-66°) for the tentorial angle, which was
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significantly associated with the occipital lobe damage grades (p=0.008), but this was not the case for the tentorial length (p=0.802) and the shortest distance from the confluence of sinus to the tumor (p=0.695). Interestingly, age was also strongly associated with occipital lobe damage risk (p=0.020). The patients in the subgroup with no occipital damage (Grade 4) were the youngest (aged 47.3 years), compared with other grades, with age of 58.0 years for Grade 1, 54.3 years for Grade 2, and 58.6 years for Grade 3. These two parameters were also significant after multivariate analysis. No correlation was observed between either tumor nature or the extent of
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resection and damage grades.
Conclusions. The risk of occipital lobe damage increases in the presence of a steep tentorial angle during the Poppen approach for tentorial or pineal area tumors. Awareness of such anatomical features preoperatively is important for minimizing operative complications. tentorium, tentorial angle, meningiomas, Poppen.
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Key words:
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Abbreviations used in this paper:
TM = Tentorial meningiomas; TA = Tentorial angle; MRI = magnetic resonance imaging; ANOVA = one-way analysis of variance; CSF = cerebrospinal fluid.
ACCEPTED MANUSCRIPT Introduction Tentorial meningiomas (TM) are complex entities that require multiple surgical approaches, according to the tumor position and its relationship with the surrounding structures12,16. Based on the tumor’s location and direction of growth, there could be several surgical approaches for removing the tumor safely 8. The POPPEN approach, or occipital interhemispheric transtentorial approach, is often undertaken if the tumor is located at the posteromedial or anteromedial
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tentorium, or even along the tentorial notch2,7,12. Similarly, the pineal region meningiomas, especially falcotentorial meningiomas, are usually surgically resected through the POPPEN approach, which usually causes occipital lobe damage
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. Occipital lobe damage may cause
hematoma, which has to be evacuated by a secondary operation and may lead to vision problems
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such as hemianopia 6,9,13.
Thus far, there has been no research on the factors associated with this severe surgical complication and how to decrease the risk. In resecting tumors through the POPPEN approach,
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one of the most important procedures is lifting up the occipital lobe on the retractor, which can cause local hyperperfusion of the retracted occipital region and even visual field defect without obvious occipital lobe damage seen on a CT 18. In our experience, whether the tentorium is steep or flat can be associated with the difficulty of lifting up the occipital lobe, and this might be one factor that correlates to the extent of occipital lobe damage. The tentorial angle (TA) was used to quantify the slope of the tentorium with several calculation methods 11,14,17.
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In addition to the TA, there might be other factors associated with occipital lobe damage, including tumor characteristics such as the direction of growth (superior or inferior), the texture (soft or hard), and the tumor size; and intraoperative parameters such as blood loss volume, length of operation, and the tumor resection grade. All these parameters should be analyzed
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together to determine which factors are independent factors that should be given more attention to decrease the occipital lobe damage complication during surgery.
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This research summarizes our retrospectively analyzed data of 27 patients with tentorial or pineal region meningiomas. We aimed to identify the factors that can predict the risk of occipital lobe damage, so that patients can be informed possible complications before resection of tumors located at the tentorium or pineal region through the Poppen approach. Our observations provided the basis for analyzing the relationship between the morphology of the tentorium, especially the tentorial angle, and the risk of damage to the occipital lobe in resecting tentorial or falcotentorial meningiomas through the POPPEN approach, and provide further insight into how to lower the risk with appropriate surgical skills.
Materials and Methods By scanning the clinical data in Beijing Tiantan Hospital, we found a total of 112 cases of tentorial
ACCEPTED MANUSCRIPT meningiomas (TM) admitted to the neurosurgical department between 2012 and 2015. Only the TM cases treated with the POPPEN approach were included in the research. Two patients in whom tumors involved the occipital pole were excluded, and two other patients with tumors larger than 6 cm that were accompanied with hydrocephalus were also excluded. The research flowchart is shown in Fig. 1. The records of all 23 TM cases, plus another four cases with pineal falcotentorial meningiomas on which tumor resection through the POPPEN approach was
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performed, were retrospectively reviewed for clinical presentation, radiological imaging, surgical record, and outcome. TA was measured as the angle between the tentorium and the line drawn from the hard palate (indicated in Fig. 2E) according to the criteria by Burak Sade and Joung H. Lee
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. The extents of occipital lobe damage were divided into four categories: hematoma
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(Grade 1), punctate hemorrhage (Grade 2), brain edema (Grade 3), and normal (Grade 4), based on the postoperative CT scan or magnetic resonance imaging (MRI) (indicated in Fig. 2).
system for tumor removal 5.
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The extent of tumor resection for meningiomas was classified according to the Simpson grading
Intergroup frequencies among the four grades of occipital lobe damage were compared using the one-way analysis of variance (ANOVA) for continuous variables such as patient age, maximum diameter of tumor, tentorial angle, and tentorial length, and using theχ2 /Fisher exact test method for categorical variables such as sex, tumor location, tumor texture, and extent of the
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resection. We divided the occipital lobe damage to binary data including having occipital lobe damage (Grade 1, 2, and 3) and not having occipital lobe damage （Grade 4） ，and then analyzed the significant factors from univariate analysis with multivariate logistic regression analysis to see whether this parameter could be an independent factor. Statistical analysis was performed using
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commercial statistical software (SPSS 23.0, SPSS Inc., Chicago, IL, USA). A P value less than 0.05 was considered statistically significant.
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Results
There was no operative mortality. All patients were positioned prone laterally intraoperatively. A 58-year-old patient who had the most severe occipital lobe damage had an occipital lobe hematoma, which was found 6 h after tumor resection and emergency hematoma evacuation was performed immediately (Fig. 3). Homonymous hemianopia appeared in this patient, and was not resolved 6 months postoperatively. Another tentorial meningioma patient with Grade 2 occipital lobe damage, with punctate hemorrhage at the occipital lobe on the postoperative CT scan which did not need to be evacuated by secondary operation, was also shown (Fig. 4). The radiologic parameters, including the tumor extension, tumor texture, maximum diameter of tumor, TA, tentorial length, and the shortest distance from the confluence of sinus to the tumor, did not correlate significantly with the occipital lobe damage (Table 1).
ACCEPTED MANUSCRIPT However, age was strongly associated with occipital lobe damage risk (p=0.020). The patients in the subgroup with no occipital damage (Grade 4) were the youngest (aged 47.3 years), compared with the patients in other subgroups, with ages of 58.0 years for Grade 1, 54.3 years for Grade 2, and 58.6 years for Grade 3, respectively. The mean values of the TA were 55.3±5.6° (range 45-66°) and were significantly associated with occipital lobe damage grade (p=0.008). The most severe occipital lobe damage occurred in a 58-year-old male patient who had the steepest tentorium
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(TA=66°) and required a secondary hematoma evacuation rescue surgery. The mean values of TA were (58.9±5.8) ° for Grade 2, (55.6±2.3) ° for Grade 3, and (52.2±4.8) ° for Grade 4.
For blood loss in the operation, we found that a tendency to lose more blood may lead to more severe occipital lobe damage, although this finding was not significant.
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For the multivariate analysis of age and tentorial angle parameters, considering the group 1, 2 and 3 as damage group , we found that TA and age were both independent factors that correlated with occipital lobe damage after removal of tentorial tumors through the POPPEN
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approach (respectively p=0.024 and p=0.029) (Table 2). The cutoff point was identified as tentorial angle≥53° to predict more likely of occipital damage, with sensitivity of 87% and specificity of 67%.
Discussion
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This is the first research project to study the relationship of prognostic factors, including radiologic feature of the tumor itself, such as the texture, size, and location;. and the intraoperative factors such as the length of surgery, the blood loss volume, and resection grade of the tumor, with the grade of occipital lobe damage in the tumor at the tentorial and pineal
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regions resected through the POPPEN approach.
We found that the patients' age and TA were statistically significant factors leading to an
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increased chance of postoperative occipital lobe injury, but this was not the case for the other parameters. First, the older the patients, the more likely they were to suffer occipital lobe damage during surgery. One reason could be that brain compliance usually decreases with aging. The textures were usually different in the brains of patients of different ages. The brains of elderly patients were more prone to be contused with head accidents, and age was proven to be one of important prediction factors of hemorrhagic progression of contusions in traumatic brain injury 3. It was the similar case in the TMs removal operation while lifting up the occipital lobe. Second, we found that the TA was the significant radiologic parameter related to the extent of occipital lobe damage. In the patients with a larger tentorial angle, it was much more difficult for neurosurgeons in the course of retracting the occipital lobe upward to release cerebrospinal fluid (CSF) and then resect the tumor. Hence, this parameter found in preoperative radiologic features
ACCEPTED MANUSCRIPT can be used as a prognostic factor for intraoperative occipital lobe damage complications in operating on tumors at the tentorial region via the POPPEN approach. Before this study, we thought about that longer time in surgery might be associated with more severe occipital lobe damage, because the occipital lobe had to be lifted up and retracted in the course of the operation. However, the length of surgery did not prove to be significantly associated with the extent of occipital lobe damage in our study. The reason for this might be
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that after sufficient CSF was released from the ambient cistern or quadrigeminal cistern, the pressure on the occipital lobe by the retractor was minimal, and to some extent, it was different from other retraction operations. Releasing CSF as soon as possible after a craniotomy was almost our routine procedure in surgery for these patients.
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The blood loss might be associated with occipital lobe damage. One reason was that occipital lobe damage, especially hematoma, could be one origin of intraoperative bleeding, and the second reason was that more blood loss could be attributed to the sacrifice of venous bleeding,
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which might increase the hyperperfusion condition after tumor removal. However, we discovered that more blood loss tends to accompany more severe occipital lobe damage. This indicates that when abundant blood was lost that contributed to other factors such as the tumor itself, occipital lobe damage could be avoided.
Our study excluded the huge tentorial meningiomas larger than 6 cm in diameter. We also excluded tumors with hydrocephalus, because if hydrocephalus existed, it was more difficult to
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release CSF by retracting the occipital lobe; sometimes we preferred CSF external drainage through the frontal or occipital horn of the lateral ventricles to decrease intracranial pressure before opening the dura mater.
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Practical Implications
Patient position and cervical vertebra flexure were important in the occipital interhemispheric
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transtentorial approach. Compared with the patients in a prone position, those positioned laterally had lower blood loss, shorter operations, decreased cerebral edema, and better visual outcomes. The researchers concluded that gravity retracted the occipital lobe when the patients were positioned laterally with enhanced operative exposure 4. We always positioned the patients laterally, and slightly rotated the head to make the medial one-third of the transverse sinus highest, while at the same time flexing the cervical vertebra and retracting the lower mandible. The side used for the craniotomy was based on gravity aiding occipital retraction. All these requirements for positioning were used to make the posterior occipitalis sufficiently exposed, retract the occipital lobe more easily, and take advantage of gravity to retract the occipital lobe. If the TA is large, we recommend making the best of this position to lower retraction pressure and the likelihood of occipital lobe edema and damage.
ACCEPTED MANUSCRIPT The craniotomy flap edges were just lateral to the superior sagittal sinus and superior to the transverse sinus. It was especially important to expose the inferior edge adequately, and no bone eaves were left to prevent direct visualization of the tentorium. The retracting pressure and direction were important for protecting the occipital lobe. First, the pressure against the occipital lobe had to be as low as possible after sufficient CSF was released. Intermittently releasing the retractor, as well as using a broader retractor, were important key
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points for decreasing the likelihood of occipital lobe damage intraoperatively. Second, the direction of retracting the occipital lobe was important for protecting it during resection of tumors in the tentorial region. If the patients had a relatively large TA, we preferred to choose the optimal surgical corridor of the posterior interhemispheric approach, which could lower
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retraction pressure to the occipital lobe compared with directly lifting up or retracting the occipital lobe. This also could decrease the probability of sacrificing multiple occipitobasal veins, which drain into the tentorial sinuses and are located just medial to the transverse sinus 1 in the
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course of exposing the tumor along the tentorium. The draining veins damage could cause local hyperperfusion of the occipital region and made it more prone to the retracting pressure. It was important to release CSF before beginning to remove a tumor, especially for small tumors. If enough CSF is released, it might not be necessary to retract the occipital lobe if patient positing is adequate and intraoperative hyperosmolar agents are administered. The position for CSF release was also important for protecting the surrounding normal brain tissue, including the
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occipital lobe. The ambient cistern or quadrigeminal cistern was usually where we chose to release CSF. If the patient had a relatively large TA and enlarged lateral ventricles, we could make CSF external drainage and decrease intracranial pressure. If the tumor was relatively large and obstructed the cerebrospinal fluid flowing channel, we predicted that CSF leakage might be
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difficult, and chose external drainage from the lateral ventricle. Like the core spirits of microsurgical neurosurgery, how to achieve tumor removal through small
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exposure is also critical for TMs or other tumors at tentorial region. As the intracapsular contents are removed, the tumor collapses, thus making it possible to remove more tumor through the small exposure. If the tumor is relatively large and the TA is big, we recommend that this operative technique should be applied thoroughly.
Conclusions The tentorial angle, which could depict the steep extent of the tentorium, was significantly associated with occipital lobe damage, while resecting the tentorial meningiomas and other tumors located at tentorial or pineal region through the POPPEN approach. Awareness of such anatomical features at the time of preoperative planning is of paramount importance in selecting the optimum surgical approach and minimizing operative complications.
ACCEPTED MANUSCRIPT Acknowledgments The authors are grateful to Pinan Liu, Jisheng Wang, and other relevant staff members of Beijing Tiantan Hospital, who helped perform surgery for patients. In addition, we would like to thank Junmei Wang for providing pathological determinations. This work was supported in part by the National Key Technology Research and Development Program of the Ministry of Science and
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Technology of China (2013BAI09B03, 2014BAI04B01, 2015BAI12B04), the National Natural Science Foundation of China Projects (81502156), the Beijing Municipal Administration of Hospitals’ Youth Program (QML20150502), and the Capital Health Research and Development of
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Special Expert(2016-4-2049).
Disclosure
or the findings specified in this paper.
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The authors report no conflict of interest concerning the materials or methods used in this study
Table 1. Demographic, radiologic parameter and operation characteristics of patients with tentorial meningiomas, pineal region meningiomas, and hemangioblastomas at vermis cerebellum operated through the Poppen approach.
angles).
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Table 2. The multivariate analysis of significant factors from univariate analysis (age and tentorial
Fig. 1. The research flowchart.
Fig. 2. Assessment of occipital lobe damage by postoperative CT scan and magnetic resonance imaging (MRI) compared with preoperative MRI. A: Grade 1, postoperative occipital lobe
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hematoma with secondary operation; B: Grade 2, punctate hemorrhage; C: Grade 3, more severe occipital edema than preoperatively；D：Grade 4, none; E: MRI showing the measurements of the
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tentorial angle; F: The tentorial angles significantly correlated to occipital lobe damage grades (p=0.011).
Fig. 3. A tentorial meningioma patient with Grade 1 occipital lobe damage. A-B: Preoperative axonal and coronal enhancement MRI scan showed a meningioma inferior to the tentorium; C: The tentorial angle was 66 degrees; D: The CT scan at 6 hours postoperatively showed a hematoma at occipital lobe, and the patient received the second operation; E: The CT scan after the second operation; F: The MRI scanning 1 week postoperatively. Fig. 4. A tentorial meningioma patient with Grade 2 occipital lobe damage. A-C: Preoperative MRI scanning showed tentorial meningioma, and the tentorial angle was 63 degrees. D: The CT scan on the night after the operation showed punctate hemorrhage at the occipital lobe with conservative therapy. E: The first day postoperative CT showed a little absorption. F: 1 week
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ACCEPTED MANUSCRIPT Table 1. Demographic, radiologic parameter and operation characteristics of patients with tentorial meningiomas, pineal region meningiomas operated via Poppen approach. Occipital lobe damage Grade 1(n=1)
Occipital lobe damage Grade 2(n=7)
Occipital lobe damage Grade 3(n=7)
Occipital lobe damage Grade 4(n=12)
P value
Sex distribution, no. of male Age (yrs) Tumor location#
1
2
1
6
0.228
58.0 B(1)
Tumor texture
Soft(1)
54.3±9.2 B(4) I(3) S(0) Hard (2) Medium (5)
58.6±7.8 B(2) I(2) S(3) Hard (2) Medium (5)
Maximum diameter (mm) Tentorial angle (degrees) Tentorial length (mm) The least distance from confluence of sinus to tumor （mm） ） Operation duration (min) Blood loss (ml)* Resection grade
32.2
37.5±11.9
35.4±13.5
66.0
58.9±5.8
50.7 13.1
0.020 0.100
55.6±2.3
52.2±4.8
0.008
43.6±8.0
46.5±7.8
45.2±7.7
0.802
24.1±19.8
22.0±11.9
28.4±14.5
0.695
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47.3±5.6 B(6) I(6) S(0) Hard (3) Medium (8) Soft(1) 30.9±7.1
0.287
0.584
330±68.4
290.0±72.4
313.3±72.0
0.583
1700 Grade 4(1)
650±500 Grade 2(4) Grade 4(3)
329±95 Grade 2 (6) Grade 3(1) Grade 4(0)
350±145 Grade 1(3) Grade 2(7) Grade 3(1) Grade 4(1)
0.184 0.089
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Parameter
I：Inferiorly of tentorium; S: superiorly of tentorium; B: grew both inferiorly and superiorly of tentorium. *Analyzed by nonparameteric analysis.
ACCEPTED MANUSCRIPT Table 2. The multivariate analysis of significant factors from univariate analysis ( age and tentorial angles). Yes（ （n=15） ）
No（ （n=12） ）
P value
Angle Age
57.8±5.0 56.5±8.2
52.2±4.8 47.3±5.6
0.024 0.029
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ACCEPTED MANUSCRIPT Highlights The tentorial angle was first used to correlate the risk of occipital lobe damage in the series of tentorial meningioma with POPPEN approach and found to be the most important factor compared to the tumor itself characters and other anatomical features.
According to our finding, some important skills for lowering operative complications were figured out.
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