Fluid-fluid level in cystic vestibular schwannoma: a predictor of peritumoral adhesion

Clinical article

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Object

The aim of this study was to evaluate the clinical results and surgical outcomes of cystic vestibular schwannomas (VSs) with fluid-fluid levels.

Methods

Forty-five patients with cystic VSs and 86 with solid VSs were enrolled in the study. The patients in the cystic VSs were further divided into those with and without fluid-fluid levels. The clinical and neuroimaging features, intraoperative findings, and surgical outcomes of the 3 groups were retrospectively compared.

Results

Peritumoral adhesion was significantly greater in the fluid-level group (70.8%) than in the nonfluid-level group (28.6%) and the solid group (25.6%; p < 0.0001). Complete removal of the VS occurred significantly less in the fluid-level group (45.8%, 11/24) than in the nonfluid-level group (76.2%, 16/21) and the solid group (75.6%, 65/86; p = 0.015). Postoperative facial nerve function in the fluid-level group was less favorable than in the other 2 groups; good/satisfactory facial nerve function 1 year after surgery was noted in 50.0% cases in the fluid-level group compared with 83.3% cases in the nonfluid-level group (p = 0.038).

Conclusions

Cystic VSs with fluid-fluid levels more frequently adhered to surrounding neurovascular structures and had a less favorable surgical outcome. A possible mechanism of peritumoral adhesion is intratumoral hemorrhage and consequent inflammatory reactions that lead to destruction of the tumor-nerve barrier. These findings may be useful in predicting surgical outcome and planning surgical strategy preoperatively.

Abbreviations used in this paper:DRIVE = driven equilibrium; PICA = posterior inferior cerebellar artery; TSE = turbo spin echo; VS = vestibular schwannoma.

Abstract

Object

The aim of this study was to evaluate the clinical results and surgical outcomes of cystic vestibular schwannomas (VSs) with fluid-fluid levels.

Methods

Forty-five patients with cystic VSs and 86 with solid VSs were enrolled in the study. The patients in the cystic VSs were further divided into those with and without fluid-fluid levels. The clinical and neuroimaging features, intraoperative findings, and surgical outcomes of the 3 groups were retrospectively compared.

Results

Peritumoral adhesion was significantly greater in the fluid-level group (70.8%) than in the nonfluid-level group (28.6%) and the solid group (25.6%; p < 0.0001). Complete removal of the VS occurred significantly less in the fluid-level group (45.8%, 11/24) than in the nonfluid-level group (76.2%, 16/21) and the solid group (75.6%, 65/86; p = 0.015). Postoperative facial nerve function in the fluid-level group was less favorable than in the other 2 groups; good/satisfactory facial nerve function 1 year after surgery was noted in 50.0% cases in the fluid-level group compared with 83.3% cases in the nonfluid-level group (p = 0.038).

Conclusions

Cystic VSs with fluid-fluid levels more frequently adhered to surrounding neurovascular structures and had a less favorable surgical outcome. A possible mechanism of peritumoral adhesion is intratumoral hemorrhage and consequent inflammatory reactions that lead to destruction of the tumor-nerve barrier. These findings may be useful in predicting surgical outcome and planning surgical strategy preoperatively.

Cystic VSs are described as behaving more aggressively than solid VSs, with atypical initial symptoms, preoperative facial palsy, short clinical history, large size, unenlarged internal auditory canal, and sudden deterioration because of rapid growth, unpredictable expansion of the cystic component, or hemorrhage.15,27 Cystic VS also presents a therapeutic dilemma. Observation alone is not recommended for these tumors because the cystic component expands rapidly, resulting in severe mass effect and hydrocephalus.6 Apart from the large tumor size at diagnosis and the cystic component, sudden deterioration resulting from expansion of the cystic component or hemorrhage after radiosurgery does not support radiation therapy as a treatment option.9,11

Regarding surgical treatment, cystic VS also has a worse prognosis because of the difficulty in preserving an adequate subarachnoid dissection plane, hypervascularity of the solid components, frequent engulfment of neurovascular structures, unusual cranial nerve displacement, substantially increased risk of accidental lesioning of the facial nerve,2,21,27 and a greater tendency for postoperative bleeding19,26 as compared with solid VSs. But the results of some recent studies have not supported these conclusions.12,14,23 Thus, we hypothesized that not all cystic VSs may have worse surgical outcomes, and some undefined factors originating from cystic VSs might be responsible for these different clinical and surgical courses. Interestingly, we found a subset of cystic VSs presented with fluid-fluid levels, indicating intratumoral hemorrhage, as previously reported.7,24 The aim of this study was to evaluate the clinical results of cystic VSs with fluid-fluid levels, and to investigate whether the presence of fluid-fluid levels in cystic VSs may be relevant and important for predicting surgical outcome. We also discuss the possible mechanism of peritumoral adhesion and formation of fluid-fluid levels and its implication for surgical strategy.

Methods

Patient Population

From April 2008 to March 2012, 224 cases of VS were admitted to Beijing Sanbo Brain Hospital. The clinical data of all cases were reviewed retrospectively. The tumors were defined as cystic when the radiological evidence of cyst formation presented and the intraoperative findings revealed significant cystic components. The cases that were considered neurofibromatosis Type 2, treated previously by radiosurgery, or had recurrent VS were excluded from this study. Eventually, 45 cases of cystic VS and 86 cases of solid VS were included in the study population.

Preoperative Investigation

All routine preoperative investigations were performed. Special investigations included pure tone audiometry, speech discrimination tests, and auditory evoked potential recordings. Neuroradiological investigations included bone window CT and MRI with contrast enhancement. The 45 cases of cystic VS were further divided into 2 groups according to whether fluid-fluid levels had been noted on preoperative MRI. To detect small fluid-fluid levels in cystic VSs, we used thin-slice, T2-weighted, 3D TSE pulse sequences with DRIVE. The tumor size was defined as the largest diameter in the cerebellopontine angle without considering the intracanalicular component of the tumor, which was measured and recorded by the operators (M.W.Z. and D.J.Z.) on the radiological workstation.

Surgical Procedure

All cases were operated on via a suboccipital retrosigmoid approach by the senior author (C.J.Y.), who has performed more than 1000 cases of VS resection. Standard microneurosurgical techniques were used, with intraoperative neuroelectrophysiological monitoring performed with Medelec Synergy (Oxford Instruments Medical, Inc.) in all cases.

A complete resection was attempted in all cases. The facial nerve runs along the surface of the tumor and usually becomes elongated and thin. We try to identify this nerve and dissect it along the arachnoidal plane. Sometimes it is difficult to preserve the arachnoidal plane due to a stronger peritumoral adhesion. Moreover, the facial nerves may be displaced in a different position, which may depend on the pattern of the cyst in VS. The presence of multiple cysts made it more difficult to identify the course of the facial nerve and protect it during tumor dissection. The characteristics of the adhesion of the tumor were carefully noted by reviewing the surgery and surgical video records. The senior author (C.J.Y.) considered a tumor to be adhesive if a subarachnoid plane of dissection did not exist between the tumor capsule and peritumoral neurovascular structures (such as the facial nerve, brainstem, or PICA), which resulted in discontinuity of the facial nerve or deliberately leaving small pieces of tumor remnant adhering to these important neurovascular structures. Otherwise, a tumor was considered nonadhesive if the subarachnoid plane of dissection did exist and could be used to bluntly or sharply dissect the tumor capsule completely from the facial nerve, brainstem, or PICA.

Postoperative Outcome and Follow-Up

Postoperative facial nerve function was assessed according to the House-Brackmann grading scale at discharge (about 2 weeks postoperatively) and 1 year postoperatively. All cases were analyzed for complications and postoperative course and followed-up by repeated MRI and neurological examinations, with a specific focus on facial nerve function.

Statistical Analysis

Using the statistical software SPSS (version 12.0), 1-way ANOVA was used to determine statistical differences in the duration of symptoms and tumor size between cystic VS with or without fluid-fluid levels and solid VS. The chi-square test was used to determine differences in the number of multiple cysts, peritumoral adhesions, total resections, and facial nerve outcomes between cystic VSs with or without fluid-fluid levels, and solid VSs. A probability level < 0.05 was considered statistically significant.

Results

Clinical Features

The 3 groups consisted of 66 male and 65 female patients, who ranged in age from 13 to 79 years old (mean 44.86 years old). As determined by preoperative MRI, 24 cases of cystic VSs with fluid-fluid levels were considered the fluid-level group, whereas 21 cases without fluid-fluid levels were regarded as the nonfluid-level group (Fig. 1). It is noteworthy that the thin-slice, T2-weighted, 3D TSE pulse sequence with DRIVE detected some small fluid-fluid levels in 7 cases, which had not been found using conventional MRI (Fig. 2). Moreover, obvious multiple cysts were observed in 19 (79.2%) of the 24 cases in the fluid-level group compared with 10 (47.6%) of the 21 cases in the nonfluid-level group (p = 0.027; Fig. 3; Table 1).

Fig. 1.
Fig. 1.

Axial T1-weighted (A), T2-weighted (B), and T1-enhanced (C) MR images showing cystic VS with (Case 16, Table 1; upper row) and without (Case 37, Table 1; lower row) fluid-fluid levels.

Fig. 2.
Fig. 2.

Axial T2-weighted MR images of Case 35. Thin-slice T2-weighted 3D TSE pulse sequence with DRIVE detected some small fluid-fluid levels (arrow) within a cystic VS (left), whereas a conventional T2-weighted MR image did not (right).

Fig. 3.
Fig. 3.

Case 19. Axial T1-weighted (A), T2-weighted (B), and T1-enhanced (C) MR images showing a typical multicystic VS with fluid-fluid level.

TABLE 1:

Clinical summary of 45 cases of cystic VS*

Case No.Age (yrs), SexChief Symptom/SignSymptom Duration (mos)Fluid LevelMultiple CystPreop Tumor Size (mm)Periop FindingsHouse-Brackmann Grade (discharge/1 yr)FU (mos)Recurrence
137, Mtinnitus, hearing impairment24yesyes35nonadhesive, total resection, facial nerve preservedIV/IV51none
227, Ftinnitus, hearing impairment, visual impairment, lower CN impairment, facial numbness, gait disturbance48nono68nonadhesive, total resection, facial nerve preservedII/I51none, blindness
341, Mtinnitus, hearing impairment, facial numbness48noyes52nonadhesive, total resection, facial nerve preservedII/I46none
446, Ftinnitus, hearing impairment, facial numbness12nono40adhesive, near-total resection, facial nerve preservedIIIlostlost
560, Mhearing impairment, facial numbness12yesyes22adhesive, near-total resection, facial nerve preservedII/I42none, tinnitus
637, Ftinnitus, hearing impairment96yesyes45nonadhesive, total resection, facial nerve preservedIV/IV42none, tinnitus
752, Mhearing impairment, headache6nono34nonadhesive, total resection, facial nerve preservedIII/II40none
824, Mhearing impairment8noyes34nonadhesive, total resection, facial nerve preservedI/I39none
955, Ftinnitus, hearing impairment12nono19nonadhesive, total resection, facial nerve preservedII/I38none, tinnitus
1041, Mfacial numbness1yesyes31nonadhesive, total resection, facial nerve preservedIIlostlost
1152, Fhearing impairment24nono33nonadhesive, total resection, facial nerve preservedIII/II34none
1252, Mtinnitus, hearing impairment, facial palsy, gait disturbance, facial numbness72noyes38nonadhesive, total resection, facial nerve preservedII/II32none
1339, Ftinnitus, hearing impairment, visual impairment24yesyes47nonadhesive, total resection, facial nerve preservedII/I31none, light perception
1452, Mhearing impairment, visual impairment, facial numbness24yesno37adhesive, total resection, facial nerve broken & anastomosedVI/VI30none
1534, Mtinnitus, hearing impairment18noyes26nonadhesive, total resection, facial nerve preservedIV/III30none
1650, Ftinnitus, hearing impairment, dizziness, facial palsy, gait disturbance, nausea/vomiting36yesno33adhesive, near-total resection, facial nerve preservedIV/IV30none
1753, Mhearing impairment, facial numbness1yesyes28nonadhesive, total resection, facial nerve preservedIII/II29none
1858, Fhearing impairment, facial numbness24nono40adhesive, near-total resection, facial nerve preserved, post-op cerebellar hemorrhageIII/V29none, gait disturbance, corneal ulcer
1934, Mtinnitus, hearing impairment12yesyes46adhesive, near-total resection, facial nerve preservedIII/III28none
2055, Fhearing impairment, facial numbness & pain48noyes35adhesive, near-total resection, facial nerve preservedIV/III27none, gait disturbance
2145, Mhearing impairment, facial numbness6yesyes31adhesive, total resection, facial nerve brokenVI/VI27none
2249, Mhearing impairment, tinnitus, facial numbness, ataxia252yesyes50adhesive, total resection, facial nerve brokenVI/VI26none
2339, Mhearing impairment, facial pain60noyes40adhesive, total resection, facial nerve brokenVI/VI24none
2439, Mtinnitus, hearing impairment, facial palsy36yesyes50adhesive, total resection, facial nerve broken & anastomosedVI/VI25none
2517, Mtinnitus, hearing impairment, ataxia12nono62nonadhesive, total resection, facial nerve preservedIII/IV25none
2645, Mtinnitus, facial numbness48nono28nonadhesive, total resection, facial nerve preservedII/I24none, tinnitus
2727, Fdizziness20 (days)yesyes38nonadhesive, near-total resection, facial nerve preservedIII/V22none, small tumor remnant, masseteric–facial nerve anastomosis
2832, Mhearing impairment, facial numbness, ataxia36noyes40nonadhesive, total resection, facial nerve preservedIII/II18none
2943, Mhearing impairment, facial numbness, ataxia24yesno45adhesive (brain stem), near-total resection, facial nerve preservedIVlostlost
3033, Mhearing impairment, HA72yesyes34adhesive, near-total resection, facial nerve preservedIII/III16none, tinnitus
3170, Mhearing impairment, tinnitus, dizziness120yesyes51adhesive (brain stem), near-total resection, facial nerve preservedII/I16none, facial numbness
3258, Mtinnitus, hearing impairment240nono35nonadhesive, total resection, facial nerve preservedIII/III15none
3329, Mhearing impairment, HA, dizziness, facial numbness12noyes44nonadhesive, total resection, facial nerve preservedIII/I14none
3467, Fhearing impairment, ataxia, facial numbness, lower extremity weakness48yesno24adhesive (PICA), near-total resection, facial nerve preservedIII/I13none
3553, Mhearing impairment, tinnitus, ageusia, ataxia, dizziness60yesyes39adhesive, near-total resection, facial nerve preservedII/I12none
3666, Mhearing impairment, HA48nono38nonadhesive, total resection, facial nerve preservedII/I12none
3740, Fdizziness, facial numbness, hearing impairment24nono42nonadhesive, total resection, facial nerve preservedIV/II12none
3835, Mhearing impairment, tinnitus, facial numbness3noyes32adhesive, near-total resection, facial nerve preservedIII9none
3973, Mhearing impairment, tinnitus, HA, facial numbness, facial palsy, ataxia24noyes42adhesive (PICA), near-total resection, facial nerve preservedIII8none
4027, Mhearing impairment, HA, facial numbness, facial palsy, ataxia3yesno56adhesive, total resection, facial nerve broken & anastomosedVI7none
4137, Mfacial numbness, hearing impairment, facial palsy6yesyes40nonadhesive, total resection, facial nerve preservedII7none
4279, Mhearing impairment, facial numbness6yesyes36adhesive, near-total resection, facial nerve preservedII5none
4351, Fhearing impairment, dizziness, ataxia60yesyes47adhesive, near-total resection, facial nerve preservedIII5none
4457, Mhearing impairment36yesyes25adhesive, near-total resection, facial nerve preservedII4none
4543, Mhearing impairment36yesyes37adhesive, near-total resection, facial nerve preservedII4none

* CN = cranial nerve; FU = follow up; HA = headache.

† With hemorrhage.

The clinical records of cystic VSs are summarized in Table 1. The mean duration of symptoms (± SEM) was 41.49 ± 11.13 months in the fluid-level group, 39.38 ± 10.90 months in the nonfluid-level group, and 51.92 ± 7.83 months in the solid group (p = 0.644). The mean tumor size was 38.63 ± 1.89 mm in the fluid-level group, and 39.14 ± 2.41 mm in the nonfluid-level group (p = 0.955). The mean tumor size was 32.42 ± 1.11 mm in the solid group, significantly smaller than the mean size in the cystic VS group (p = 0.004).

Surgical Outcome

In the fluid-level group, 17 (70.8%) of 24 VSs were considered to be adhesive—of which 14 adhered to the facial nerve (Fig. 4), 2 adhered to the brainstem, and 1 adhered to the PICA. In the nonfluid-level group, 6 (28.6%) of 21 were considered to be adhesive—5 of which adhered to the facial nerve and 1 adhered to the PICA. In the solid VS group, 22 (25.6%) of 86 were considered to be adhesive—of which 15 adhered to the facial nerve, 5 adhered to the brainstem, and 2 adhered to both of them simultaneously. Peritumoral adhesion was significantly greater in the fluid-level group (70.8%) than in the nonfluid-level group (28.6%) or solid group (25.6%; p < 0.0001). Complete tumor removal was achieved in 45.8% of the patients (11/24) in the fluid-level group, which was significantly lower than in the nonfluid-level group (76.2%, 16/21) and the solid group (75.6%, 65/86; p = 0.015). Five (20.8%) of 24 patients in the fluid-level group, 1 (4.8%) of 21 in the nonfluid-level group, and 4 (4.7%) of 86 in the solid group had a broken facial nerve due to surgery, but these values were not significantly different (p = 0.058). However, in the case of a broken facial nerve in the nonfluid-level group, although MRI did not find any fluid-fluid level, there were other obvious hemorrhage appearances (Fig. 5).

Fig. 4.
Fig. 4.

Intraoperative photograph showing a tumor remnant adhering to the facial nerve. V N. = trigeminal nerve; VI N. = abducent nerve; VII N. = facial nerve.

Fig. 5.
Fig. 5.

Axial T1-weighted (A), T2-weighted (B), and FLAIR (C) MR images showing hemorrhage appearance in the case with a broken facial nerve in the nonfluid-level group.

Postoperative Course and Follow-Up

At discharge, facial nerve function was evaluated in all cases. Reconstruction of the facial nerve was attempted in 5 cases with a broken facial nerve, and all of these cases were graded as House-Brackmann Grade VI, even if they achieved some nerve function. Facial nerve grades at discharge are compared between the 3 groups in Fig. 6 upper. Favorable facial nerve function (House-Brackmann grades ranging from I to III) was noted in 62.5% of cases (15/24) in the fluid-level group, 81% of cases (17/21) in the nonfluid-level group, and 62.8% of cases (54/86) in the solid group (p = 0.273). The surgery-related significant complications included cerebellar hemorrhage in 1 case (Case 18, Table 1) of the nonfluid-level group and 1 case in the solid group, which were reexplored in the immediate postoperative period. The follow-up period of the entire group ranged from 4 to 54 months, with a mean follow-up of 26.2 months. Ninety-three cases underwent follow-up examination up to 1 year to evaluate the postoperative 1-year facial nerve function. Long-term facial nerve grades are compared between the 3 groups in Fig. 6 lower. Favorable facial nerve function was observed in 50% of cases (8/16) in the fluid-level group compared with 83.3% of cases (15/18) in the nonfluid-level group (p = 0.038) and in 67.8% of cases (40/59) in the solid group (p = 0.116). One case with House-Brackmann Grade V in the fluid-level group underwent masseteric–facial nerve anastomosis (Case 27, Table 1). Another patient in the solid VS group underwent hypoglossal-facial nerve anastomosis. One case (Case 27, Table 1) in the fluid-level group had demonstrable lesions on follow-up MRI; because of the very small tumor size and no symptoms, this patient was followed up for 19 months. Another case in the solid VS group had a remnant lesion noted on repeated MRI and underwent stereotactic radiosurgery twice. In the other cases, no recurrence was found.

Fig. 6.
Fig. 6.

Bar graphs showing 2-week (upper) and 1-year (lower) postoperative House-Brackmann facial nerve grades of the 3 groups.

Discussion

The result of this study show that cystic VSs with fluid-fluid levels more frequently adhere tightly to surrounding neurovascular structures and have a less favorable surgical outcome.

Criterion of Cystic VS

The incidence of cystic VS varies from 5.7% to 48%, with rates of approximately 10% in more recent studies.23 However, the true incidence is debatable and is dependent on the criteria used. Most recent studies defined the tumors as cystic when the intraoperative findings revealed the presence of significant cystic elements, in addition to the preoperative radiological evidence of cyst formation.21,23,27 But the studies of Charabi et al.4,10 presented stricter criteria for cystic VSs that also included histological verification of the presence of an S100-positive membrane. In our series, we did not include any histological criteria. Histological verification of an S100-positive membrane is used to differentiate a peritumoral arachnoid cyst from cystic VS. When experienced neurosurgeons dissect the tumor capsule in the subarachnoid plane, it is not difficult to differentiate the cystic wall from an arachnoid cyst. Furthermore, enhancement of the cyst wall is an imaging characteristic that can be used to differentiate a cystic wall from arachnoid cysts.

Facial Nerve Outcome of Cystic VS

There continue to be debates regarding the correlation between cystic VS and postoperative facial nerve outcome. In most studies, reported facial nerve outcomes after cystic VS resection were worse than the results with solid tumors of comparable size.5,10,18,19,21,26,27,30 This difference may be due to a tight adhesion of the nerve to the tumor surface, with difficulties in preserving the arachnoidal plane, unusual position of displacement dependent on the pattern of development and growth of the cyst, and the low resistance to traction after cyst evacuation.2,21,27 However, other studies have not found any significant differences in facial nerve outcomes between cystic and solid tumors or different cystic tumor types.2,12,14,23 Lunardi et al.17 believed that aspiration of the cyst content facilitated recognition and preservation of the facial nerve and removal of the solid component, thus ensuring a very good prognosis in all patients. Mehrotra et al.20 found that in cystic VS, facial nerve preservation was higher due to the faster and earlier decompression of the lesion that facilitated its earlier identification. However, in those patients in whom the cystic component was in excess of 90%, preservation of the anatomical continuity of the facial nerve was difficult.

Peritumoral Adhesion of Cystic VS

Because there have been conflicting views on whether postoperative facial nerve outcomes of cystic VSs were significantly different from solid VSs, we believe that apart from tumor size, cystic component, and surgeon experience, some other factors must affect the tumor's adhesion to the surrounding neurovascular structures. The results of our study showed that not all cystic VSs adhered to surrounding neurovascular structures, but cystic VSs with fluid-fluid levels, indicating intratumoral hemorrhage, more frequently adhered to the facial nerve, brainstem, or PICA, and had a worse prognosis.

Certainly, the degree of adhesion of the tumor to surrounding neurovascular structures is unable to be measured because this is very subjective,16 and is judged by the neurosurgeon while dissecting the arachnoidal plane. The rate of complete resection is also affected by a neurosurgeon's experience. The senior neurosurgeon of this study has performed more than 1000 cases of VS resection over 20 years. Deliberate subtotal tumor removal was performed only in cases of adherence of the tumor to important neurovascular structures, not for hypervascular tumors with a risk of bleeding or intraoperative cerebellar swelling.27 Thus, the criterion of adhesion in this study was as follows: deliberate subtotal tumor removal or discontinuity of the facial nerve resulting from disappearance of the arachnoidal plane. Therefore, in this study, a tumor's adhesion to surrounding neurovascular structures, judged by the same experienced neurosurgeon, is relatively objective.

Possible Mechanism of Peritumoral Adhesion

Given the results of this study, we hypothesize that repeated intratumoral hemorrhages significantly increase the risk of peritumoral adhesion in cystic VS. At the beginning of the procedure, some degenerative changes occurred in VS, which included fatty and hyaline degeneration.8,15 These changes probably result in or are accompanied by vascular abnormalities such as hypervascularity, malformed vessels, hyalinized vessels, and thrombosis,3,8,15,20 and then hemorrhages and hemosiderin deposition.13,22,29 Because of the vascular abnormalities, the incidence of intratumoral hemorrhage and multiple cyst formation in VS increased as the tumor grew.28 Intratumoral hemorrhage introduces massive inflammatory cell infiltration,20 especially macrophages2–4 and releases proteinase,26 including matrix metalloproteinase–2, which destructs the tumor–nerve barrier proteolytically and increases peritumoral adhesion.21 In this study, extensive lymphocytes, lipophages (foamy macrophages), and hemosiderin-laden macrophages were observed in the samples of the fluid-level group (data not shown). Furthermore, we found that most cystic VSs with fluid-fluid levels were multicystic, with thin cystic walls on the surface of the tumors. We believe these multiple cysts were caused by repeated microhemorrhages, and then multiple cysts on the surface significantly increased the chance of peritumoral adhesion with surrounding neurovascular structures, especially the facial nerve, brainstem, and PICA.

Fluid-Fluid Level in Cystic VS

Fluid-fluid levels in tumors can be caused by hemorrhage from hypervascular neuromas or by collection of liquefacted necrotic material.7,24 However, necrosis is usually accompanied by hemorrhage, while microhemorrhage is common in VS.13,22,29 By histologically analyzing intracranial schwannomas with spontaneous hemorrhage, it was found that the majority were hypervascular with dilated thin-walled vessels, and this resulted in hemorrhage and fluid-fluid levels within the cystic tumor.1 Therefore, we believe that the formation of the fluid-fluid level in cystic VS was due to hemorrhage.

Computed tomography scans and MRI, if performed in a gravity-dependent plane, depict fluid–fluid levels by virtue of their high-contrast resolution. It is noteworthy that in our experience, thin-slice, T2-weighted, 3D TSE pulse sequence with DRIVE was more sensitive for detecting small fluid-fluid levels. Seven cases of the fluid-level group would have been missed without this technique.

Surgical Strategy

Although many important neurovascular structures may be found to adhere to VSs during resection, neurosurgeons usually focus their attention on the brainstem, the facial nerve, and the vessels in the posterior fossa. To protect these important neurovascular structures, we advocate the strategy of looking for subarachnoid planes that lend themselves to blunt or sharp dissection. If the arachnoid plane is not well developed, we use the onion skin technique of tumor removal,25 in which each layer of the VS is removed, from the inner layer to the outer layer, until the outermost layer is reached and removed piecemeal. Finally, only the thin capsule is lying over the facial nerve, the brainstem, or vessels of the posterior fossa. At that time, we advocate subtotal resection in these areas,23 leaving portions of the thin capsule, and reducing the vitality of tumor remnant to delay or prevent its relapse using low-power coagulation; this will decrease the risk of neurovascular damage, but not increase recurrence rate as shown in our follow-up data.

Limitations of the Study

The retrospective collection of data might have introduced a selection bias. The tumors that initially received radiotherapy were solid, and therefore many solid tumors were excluded. It is not possible to blind the surgeon to the fluid-fluid group. For cases with a cosmetic requirement, a more conservative strategy was adopted during tumor resection to protect the facial nerve. Regarding surgical assessments, the judgment of peritumoral adhesion is subjective; this source of bias was minimized by using data from a single neurosurgeon who could apply a relatively consistent philosophy. However, single-surgeon experience also limits the generalizability of results. As to follow-up assessments, the 1-year follow-up is not long enough, and some facial nerve functions were found to improve after 1-year.

Conclusions

The cystic VSs with fluid-fluid levels more frequently adhered tightly to surrounding neurovascular structures, and had a less favorable surgical outcome. A possible mechanism of peritumoral adhesion is intratumoral hemorrhage and consequent inflammatory reactions that lead to destruction of the tumor-nerve barrier. Magnetic resonance imaging, especially thin-slice, T2-weighted, 3D TSE pulse sequence with DRIVE, is more sensitive for detecting small fluid-fluid levels. These findings may be useful in predicting surgical outcome and determining preoperative surgical strategy.

Disclosure

Funding for this study was provided by the Beijing Municipal Science & Technology Commission (grant no. Z111107058811015) to Dr. Hongwei Zhang, and the Sanbo Research Fund to Dr. Lei Xia.

Author contributions to the study and manuscript preparation include the following. Conception and design: H Zhang, Xia, Yu, Qi. Acquisition of data: Xia, M Zhang, Ren, Qu, Wang, Zhu, Zhao, Qi, Yao. Analysis and interpretation of data: all authors. Drafting the article: Xia. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: H Zhang. Statistical analysis: Xia, Qu, Wang. Administrative/technical/material support: H Zhang, Yu, M Zhang, Ren, Qu, Wang, Zhu, Zhao, Qi, Yao. Study supervision: H Zhang, Yu, Zhu, Zhao, Qi, Yao.

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  • 16

    Kanzaki JTos MSanna MMoffat DAMonsell EMBerliner KI: New and modified reporting systems from the consensus meeting on systems for reporting results in vestibular schwannoma. Otol Neurotol 24:6426492003

  • 17

    Lunardi PMissori PMastronardi LFortuna A: Cystic acoustic schwannomas. Acta Neurochir (Wien) 110:1201231991

  • 18

    Matthies CSamii M: Management of 1000 vestibular schwannomas (acoustic neuromas): clinical presentation. Neurosurgery 40:1101997

  • 19

    Matthies CSamii MKrebs S: Management of vestibular schwannomas (acoustic neuromas): radiological features in 202 cases—their value for diagnosis and their predictive importance. Neurosurgery 40:4694821997

  • 20

    Mehrotra NBehari SPal LBanerji DSahu RNJain VK: Giant vestibular schwannomas: focusing on the differences between the solid and the cystic variants. Br J Neurosurg 22:5505562008

  • 21

    Moon KSJung SSeo SKJung TYKim IYRyu HH: Cystic vestibular schwannomas: a possible role of matrix metalloproteinase-2 in cyst development and unfavorable surgical outcome. J Neurosurg 106:8668712007

  • 22

    Park CKKim DCPark SHKim JEPaek SHKim DG: Microhemorrhage, a possible mechanism for cyst formation in vestibular schwannomas. J Neurosurg 105:5765802006

  • 23

    Piccirillo EWiet MRFlanagan SDispenza FGiannuzzi AMancini F: Cystic vestibular schwannoma: classification, management, and facial nerve outcomes. Otol Neurotol 30:8268342009

  • 24

    Prasad SGupta SPatankar TGoel A: Fluid-fluid levels in intracranial schwannomas. Australas Radiol 43:5295311999

  • 25

    Samii MGerganov VSamii A: Improved preservation of hearing and facial nerve function in vestibular schwannoma surgery via the retrosigmoid approach in a series of 200 patients. J Neurosurg 105:5275352006

  • 26

    Samii MMatthies C: Management of 1000 vestibular schwannomas (acoustic neuromas): surgical management and results with an emphasis on complications and how to avoid them. Neurosurgery 40:11231997

  • 27

    Sinha SSharma BS: Cystic acoustic neuromas: surgical outcome in a series of 58 patients. J Clin Neurosci 15:5115152008

  • 28

    Sugihara SKinoshita TMatsusue EFujii SOgawa T: Multicystic acoustic schwannoma with intratumoral hemorrhage: a report of two cases. Magn Reson Med Sci 3:1011042004

  • 29

    Thamburaj KRadhakrishnan VVThomas BNair SMenon G: Intratumoral microhemorrhages on T2*-weighted gradientecho imaging helps differentiate vestibular schwannoma from meningioma. AJNR Am J Neuroradiol 29:5525572008

  • 30

    Zaouche SIonescu EDubreuil CFerber-Viart C: Pre- and intraoperative predictive factors of facial palsy in vestibular schwannoma surgery. Acta Otolaryngol 125:3633692005

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Article Information

Address correspondence to: Hongwei Zhang, M.D., Ph.D., Department of Neurosurgery, Beijing Sanbo Brain Hospital, Capital Medical University, No. 50, Yi-Ke-Song Road, Haidian District, 100093 Beijing, China. email: zhanghw23@sohu.com.

Please include this information when citing this paper: published online July 19, 2013; DOI: 10.3171/2013.6.JNS121630.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Axial T1-weighted (A), T2-weighted (B), and T1-enhanced (C) MR images showing cystic VS with (Case 16, Table 1; upper row) and without (Case 37, Table 1; lower row) fluid-fluid levels.

  • View in gallery

    Axial T2-weighted MR images of Case 35. Thin-slice T2-weighted 3D TSE pulse sequence with DRIVE detected some small fluid-fluid levels (arrow) within a cystic VS (left), whereas a conventional T2-weighted MR image did not (right).

  • View in gallery

    Case 19. Axial T1-weighted (A), T2-weighted (B), and T1-enhanced (C) MR images showing a typical multicystic VS with fluid-fluid level.

  • View in gallery

    Intraoperative photograph showing a tumor remnant adhering to the facial nerve. V N. = trigeminal nerve; VI N. = abducent nerve; VII N. = facial nerve.

  • View in gallery

    Axial T1-weighted (A), T2-weighted (B), and FLAIR (C) MR images showing hemorrhage appearance in the case with a broken facial nerve in the nonfluid-level group.

  • View in gallery

    Bar graphs showing 2-week (upper) and 1-year (lower) postoperative House-Brackmann facial nerve grades of the 3 groups.

References

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Charabi SKlinken LTos MThomsen J: Histopathology and growth pattern of cystic acoustic neuromas. Laryngoscope 104:134813521994

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Charabi STos MBørgesen SEThomsen J: Cystic acoustic neuromas. Results of translabyrinthine surgery. Arch Otolaryngol Head Neck Surg 120:133313381994

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Charabi STos MThomsen JRygaard JFundova PCharabi B: Cystic vestibular schwannoma—clinical and experimental studies. Acta Otolaryngol Suppl 543:11132000

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Chin KFBabar JTzifa KChavda SVIrving RM: Vestibular schwannomas with fluid-fluid level. J Laryngol Otol 121:9029062007

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Couloigner VGervaz EKalamarides MFerrary ERey ASterkers O: Clinical and histologic parameters correlated with facial nerve function after vestibular schwannoma surgery. Skull Base 13:13192003

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de Ipolyi ARYang IBuckley ABarbaro NMCheung SWParsa AT: Fluctuating response of a cystic vestibular schwannoma to radiosurgery: case report. Neurosurgery 62:E1164E11652008

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Fundová PCharabi STos MThomsen J: Cystic vestibular schwannoma: surgical outcome. J Laryngol Otol 114:9359392000

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Ganslandt OFahrig AStrauss C: Hemorrhage into cystic vestibular schwannoma following stereotactic radiation therapy. Zentralbl Neurochir 69:2042062008

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Gerganov VMKlinge PMNouri MStieglitz LSamii MSamii A: Prognostic clinical and radiological parameters for immediate facial nerve function following vestibular schwannoma surgery. Acta Neurochir (Wien) 151:5815872009

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Gomez-Brouchet ADelisle MBCognard CBonafe ACharlet JPDeguine O: Vestibular schwannomas: correlations between magnetic resonance imaging and histopathologic appearance. Otol Neurotol 22:79862001

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Jones SEBaguley DMMoffat DA: Are facial nerve outcomes worse following surgery for cystic vestibular schwannoma?. Skull Base 17:2812842007

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Kameyama STanaka RKawaguchi TFukuda MOyanagi K: Cystic acoustic neurinomas: studies of 14 cases. Acta Neurochir (Wien) 138:6956991996

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Kanzaki JTos MSanna MMoffat DAMonsell EMBerliner KI: New and modified reporting systems from the consensus meeting on systems for reporting results in vestibular schwannoma. Otol Neurotol 24:6426492003

17

Lunardi PMissori PMastronardi LFortuna A: Cystic acoustic schwannomas. Acta Neurochir (Wien) 110:1201231991

18

Matthies CSamii M: Management of 1000 vestibular schwannomas (acoustic neuromas): clinical presentation. Neurosurgery 40:1101997

19

Matthies CSamii MKrebs S: Management of vestibular schwannomas (acoustic neuromas): radiological features in 202 cases—their value for diagnosis and their predictive importance. Neurosurgery 40:4694821997

20

Mehrotra NBehari SPal LBanerji DSahu RNJain VK: Giant vestibular schwannomas: focusing on the differences between the solid and the cystic variants. Br J Neurosurg 22:5505562008

21

Moon KSJung SSeo SKJung TYKim IYRyu HH: Cystic vestibular schwannomas: a possible role of matrix metalloproteinase-2 in cyst development and unfavorable surgical outcome. J Neurosurg 106:8668712007

22

Park CKKim DCPark SHKim JEPaek SHKim DG: Microhemorrhage, a possible mechanism for cyst formation in vestibular schwannomas. J Neurosurg 105:5765802006

23

Piccirillo EWiet MRFlanagan SDispenza FGiannuzzi AMancini F: Cystic vestibular schwannoma: classification, management, and facial nerve outcomes. Otol Neurotol 30:8268342009

24

Prasad SGupta SPatankar TGoel A: Fluid-fluid levels in intracranial schwannomas. Australas Radiol 43:5295311999

25

Samii MGerganov VSamii A: Improved preservation of hearing and facial nerve function in vestibular schwannoma surgery via the retrosigmoid approach in a series of 200 patients. J Neurosurg 105:5275352006

26

Samii MMatthies C: Management of 1000 vestibular schwannomas (acoustic neuromas): surgical management and results with an emphasis on complications and how to avoid them. Neurosurgery 40:11231997

27

Sinha SSharma BS: Cystic acoustic neuromas: surgical outcome in a series of 58 patients. J Clin Neurosci 15:5115152008

28

Sugihara SKinoshita TMatsusue EFujii SOgawa T: Multicystic acoustic schwannoma with intratumoral hemorrhage: a report of two cases. Magn Reson Med Sci 3:1011042004

29

Thamburaj KRadhakrishnan VVThomas BNair SMenon G: Intratumoral microhemorrhages on T2*-weighted gradientecho imaging helps differentiate vestibular schwannoma from meningioma. AJNR Am J Neuroradiol 29:5525572008

30

Zaouche SIonescu EDubreuil CFerber-Viart C: Pre- and intraoperative predictive factors of facial palsy in vestibular schwannoma surgery. Acta Otolaryngol 125:3633692005

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