Gamma knife radiosurgery for trigeminal schwannomas

Radiosurgery

Gamma Knife Radiosurgery for Trigeminal Schwannomas Barbara Nettel, M.D., Ajay Niranjan, MBBS, M.Ch., Juan J. Martin, M.D., Christopher J. Koebbe, M.D., Douglas Kondziolka, M.D., F.A.C.S., John C. Flickinger, M.D., F.A.C.R., and L. Dade Lunsford, M.D., F.A.C.S. Departments of Neurological Surgery, The University of Pittsburgh, and The Center for Image-Guided Neurosurgery, University of Pittsburgh Medical Center-Presbyterian, Pittsburgh, Pennsylvania

Nettel B, Niranjan A, Martin JJ, Koebbe CJ, Kondziolka D, Flickinger JC, Lunsford LD. Gamma knife radiosurgery for trigeminal schwannomas. Surg Neurol 2004;62:435– 446.

KEY WORDS

Trigeminal schwannomas, radiosurgery, Gamma Knife.

BACKGROUND

Trigeminal schwannomas are uncommon tumors that may be microsurgically removed in selected cases, albeit with significant risk for new neurological morbidity. We evaluated the role of stereotactic radiosurgery as an alternative for patients with newly diagnosed or residual trigeminal schwannomas. METHODS

The records of 23 patients who underwent radiosurgery for trigeminal schwannoma were reviewed. The most frequent presenting symptoms were facial numbness (11 patients), diplopia (6 patients), and facial pain (3 patients). One patient presented with partial complex seizures as the first symptom. Twelve patients had undergone one or more prior resections. Eleven underwent radiosurgery on the basis of imaging diagnosis only. The mean tumor volume was 4.5 mL (range 0.46 –11.2 cc). Radiosurgery was performed using a median marginal dose of 15 Gy (range, 13–20 Gy). RESULTS

At a median imaging follow-up of 40 months (range, 12– 146), 20 of 22 evaluable patients (91%) had tumor growth control (regression in 15 and no further tumor growth in 5). One 80-year-old patient died of unrelated cause 4 months after radiosurgery. Two patients with enlarged tumors were treated effectively with repeat radiosurgery. Twelve of 23 patients (52%) reported improvement and 9 (39%) had no change in their symptoms. Two patients noted new neurological complaints (transient facial weakness in 1 patient and worsening of the preradiosurgery facial numbness in another patient).

espite advances in skull base surgery techniques, complete resection of trigeminal schwannomas remains a challenge for neurosurgeons. Complete surgical removal has been associated with a significant risk of new neurological deficits and is not achieved in most cases [1,11,20,21,23]. Stereotactic radiosurgery, as an alternative or adjunct to microsurgery, has shown excellent long-term outcomes in the management of patients with vestibular schwannomas (acoustic neuromas), achieving a high rate of tumor growth control with low morbidity [2,4,5,13,19,22]. Based on the outcomes of stereotactic radiosurgery for other schwann cell neoplasms, radiosurgery has been performed for the treatment of trigeminal schwannomas [8,10,17,18]. Because trigeminal schwannomas comprise only 0.8 to 8% of all intracranial schwannomas, they are considered rare tumors [3,11,15,16,20,21,24]. Outcomes after radiosurgery management are as yet poorly documented [8,10,12,17,18,25]. We present an expanded analysis of our experience using Leksell Gamma Knife威 as the primary or secondary treatment strategy.

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CONCLUSIONS

Radiosurgery is an effective minimally invasive management option for patients with residual or newly diagnosed trigeminal schwannomas. © 2004 Elsevier Inc. All rights reserved. Address reprint requests to: Dr. L. Dade Lunsford, Department of Neurological Surgery, University of Pittsburgh, Suite B-400, 200 Lothrop St., Pittsburgh, PA 15213. Received September 24, 2003; accepted February 12, 2004. © 2004 Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010 –1710

Materials and Methods PATIENT DEMOGRAPHICS Between August 1987 and December 2001 a total of 829 patients with intracranial schwannomas underwent Gamma Knife威 radiosurgery at the University of Pittsburgh. Fifty-five patients had nonacoustic schwannomas; 23 of these 55 had trigeminal 0090-3019/04/$–see front matter doi:10.1016/j.surneu.2004.02.035

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Radiosurgery for Trigeminal Schwannomas: Presenting Symptoms and Signs (N ⫽ 23)

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CHARACTERISTICS Diagnostic method Histological (prior resection)a MR Imaging (no prior resection)b Symptoms Facial numbness Facial pain Double vision Headache Vertigo Imbalance Partial seizures Signs Trigeminal sensory disturbance Loss of corneal sensation Extraoccular movement deficit Facial weakness a

Nettel et al

NO. (%) 11 (48%) 12 (52%) 11 (48%) 3 (13%) 6 (26%) 2 (8.6%) 1 (4.3%) 4 (17%) 1 (4.3%) 21 (91%) 7 (30%) 9 (39%) 1 (4.3%)

Secondary radiosurgery group. Primary radiosurgery group.

b

schwannomas. The patient population consisted of 12 females and 11 males. The median age was 47 years (range, 15– 82 years). One patient had neurofibromatosis Type II. Presenting symptoms and signs are shown in Table 1. Initial symptoms included facial numbness (11 patients), diplopia (6 patients), and facial pain (3 patients). One patient presented with partial complex seizures. Twelve patients received radiosurgery as primary treatment with a diagnosis based on magnetic resonance imaging (MRI) (Figures 1 and 2). In these patients the tumor was confined to the course of the trigeminal nerve with extension into the cavernous sinus. These tumors did not have a broad dural base more typical of a petroclival meningioma. Two patients had tumor extension into the posterior fossa (petrous apex and petroclival region). Secondary radiosurgery was performed in 11 patients who had incomplete surgical resection. Typical trigeminal schwannomas were diagnosed in all 11 patients. Nine patients had partial removal and 2 had gross total resection but delayed recurrence. Such patients had tumors confined to Meckel’s cave; 2 patients had residual tumor that extended into the cavernous sinus, and 2 patients had tumor that extended to the tentorium and the petrous apex. RADIOSURGICAL TECHNIQUE The Leksell Model G Stereotactic frame (Elekta Instruments, Atlanta GA) was applied to the patients’ heads using local anesthesia and mild intravenous sedation. Spoiled Gradient Recalled MR sequences (SPGR) were performed to image the entire tumor volume and adjacent brain structures. A conformal

radiosurgery dose plan was designed using GammaPlan威 software. All patients underwent radiosurgery using either the model U, B, or C Leksell Gamma Knife威. Some centers outline the tumor volume first and then plan a treatment volume. Using various algorithms a theoretical conformity index can be calculated. While calculating a conformity index would be a good potential research tool, we do not calculate it, as we do not outline the tumor volume. Our practice, however, is to make a highly conformal dose plan by covering the entire tumor volume by the treatment isodose line (usually 50%) using multiple isocenters. Thus entire tumor gets a minimum marginal dose [14]. The median tumor volume was 4.5 mL (range 0.46 –11.2 cc). In 22 patients a median marginal dose of 15 Gy (range, 13–20 Gy) was delivered to the 50% isodose line using 1 to 13 isocenters of different beam diameters (median of 5 isocenters). In 1 patient a 55% isodose line conformed to the tumor margin. The median maximum radiation dose was 30 Gy (range, 26 – 40 Gy). After radiosurgery, the patients were instructed to have clinical and imaging follow-up every 6 months during the first year, then yearly for 2 years. If tumor growth was halted, additional imaging evaluations were requested at 4, 6, 8, and 12 years. Local control was defined as radiologically stable tumor with preserved neurological function. If a new symptom or any existing cranial nerve function worsened, the patient was suspected of having an adverse radiation effect. A new MRI was then obtained to assess tumor status and the effect of radiosurgery.

Results None of 23 patients were lost to follow-up. One patient died from congestive heart failure 4 months after radiosurgery. The FUP range in rest (22 patients) of the evaluable patients was 12 to 146 months (median 40 months, average 56 months). Of these, 19 had more than 26 months FUP and only 3 patients had less than 2-years FUP (1 patient each with 12, 19, and 23 months, respectively). Clinical and imaging results are summarized in Table 2. CLINICAL RESPONSE Twelve patients (52%) reported improvement and 9 (39%) had no change in their initial symptoms. The patient who died of congestive heart failure during follow-up had no change in symptoms. Two patients had suspected adverse radiation effects. One patient (who had facial numbness before radiosur-

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Axial and coronal MRI (A) of a 61-year-old male who presented with facial numbness and hypoesthesia involving V1 and V2 distribution. This patient with left sided trigeminal schwannoma was treated with radiosurgery using a margin dose of 15 Gy to the 50% isodose line. Follow-up MRI 6 months after radiosurgery (B) show loss of central contrast uptake. A slight decrease in tumor size is noted at 14 months (C) followup. Further tumor shrinkage is noted at 41 months (D) and 86 months (E) follow-ups.

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Axial MRI of a 49-year-old female who presented with headache, facial numbness, and ptosis. She underwent Gamma Knife radiosurgery for trigeminal schwannoma (A) using 15 Gy margin dose to the 50% isodose line. Follow-up MRI 3 months after radiosurgery (B) show loss of central contrast in the tumor with a slight increase in the tumor size. The patient also noted transient mild facial weakness. Follow-up MRI at 8 months (C) shows regression in the tumor size. The facial weakness had recovered by this time. Further imaging follow-ups at 15 (D), 21 (E), and 26 (F) months after radiosurgery show significant tumor regression.

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Imaging and Clinical Results of Radiosurgery for Trigeminal Schwannoma in 23 Patients

NO. OF PATIENTS PERCENT Imaging response Tumor regression Stable tumor Tumor growth Loss of central contrast uptake Delayed peritumoral T2 change Clinical response Improvement No change New symptoms

15 6 2 6 1

65% 26% 9% 26% 4.3%

12 9 2

52% 39% 9%

gery) noted worsening of trigeminal light touch sensory loss. Another patient noted temporary facial weakness (House-Brackmann Grade-2) [7] 3 months after radiosurgery. Facial nerve function normalized after a 6 weeks course of corticosteroids. Thereafter, the patient noted improvement in her preradiosurgery sensory symptoms; imaging documented tumor regression after radiosurgery. IMAGING RESPONSE While the goal of microsurgery is to remove or to decompress tumor, the goal of benign tumor radiosurgery is to control tumor growth. Tumor growth control is defined as freedom from further tumor growth, from new symptom related to growth and from the need of additional surgical treatment. Therefore, after radiosurgery, if a patient does not develop any new symptom and imaging shows no further growth, the tumor is considered controlled. Patients are given choice of tumor removal and tumor control. Patients willing to accept tumor control as successful outcome choose radiosurgery. Those patients who desire tumor removal or regression are managed by microsurgery. Twenty patients (91%) had tumor growth control. We observed tumor regression in 15 patients (65%) and growth arrest in additional 6 patients (26%) over a median follow-up of 40 months. In the secondary treatment group (radiosurgery used after tumor resection) tumor regressed in 9 (Figure 3), remained unchanged in 2 patients, and enlarged in 1 patient. In the primary treatment group (diagnosis based on imaging alone), the tumor regressed in 5 (Figures 1 and 2) and remained stable in 6 patients. Two patients had delayed tumor progression. A 15-year-old male developed V2 and V3 sensory loss after subtotal resection of a trigeminal schwannoma. The residual tumor was treated with radiosurgery. Although no symptom developed, his 24

TUMOR GROWTH CONTROL.

months follow-up MRI showed tumor enlargement. He was retreated with Gamma Knife radiosurgery 2 years after the first procedure. The tumor remained stable 23 months after the second procedure. In another patient, the tumor (10.1 mL volume at radiosurgery) remained stable for 4 years. At 52 months the patient developed facial weakness, and a repeat MRI showed tumor enlargement. To deliver a therapeutic dose, the patient was retreated in two-stages. During the first stage the portion of the tumor extending into the posterior fossa (treatment volume 8.5 mL) was irradiated and 3 months later the portion of the tumor invading the cavernous sinus (17.5 mL) was treated. The posterior portion treated in the first stage, showed signs of central necrosis when the new MRI for the second stage was performed. This radiologic characteristic has been documented before as a predictor of delayed tumor shrinkage [8,12]. The tumor has remained stable 12 months after the second procedures. A patient with neurofibromatosis Type 2 developed a new lesion involving the contralateral cavernous sinus 101 months after radiosurgery, consistent with a contralateral trigeminal schwannoma. Radiosurgery was recommended for this new lesion. MRI also showed an extramedulary-intradural spinal tumor at T2 level, consistent with a meningioma. Six patients in this series developed loss of paramagnetic contrast enhancement between 3 and 7 months after radiosurgery. Further follow-up imaging in these patients documented tumor regression between 8 and 101 months (Figure 3). Only 1 patient showed peritumoral enhanced long relaxation time (TR) signal changes at 18 months without any clinical consequences (Figure 4). Such changes are suspected of being transient peritumoral edema.

TUMOR APPEARANCE.

Discussion Our report describes 23 patients with trigeminal schwannomas treated by either primary or secondary (after surgery) radiosurgery. Although such schwannomas are relatively rare, various published series support the application of radiosurgery because of long-term tumor control and low operative morbidity [10,12,17,18]. SURGICAL RESECTION Various authors report excellent results after complete surgical removal [1,6,16,20,21,23]. However, surgical removal of trigeminal schwannomas is associated with the development of new neurological

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Axial MRI of an 82-year-old male who had prior surgical resection of a trigeminal nerve sheath tumor with postoperative III, V, and VI nerve palsies. He was treated with Gamma Knife radiosurgery for tumor regrowth (A). Follow-up images after 5 months (B) show significant loss of central contrast. Follow-up images at 24 months (C) show significant tumor shrinkage. Further tumor shrinkage is seen on images at 35 months follow-up (D).

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deficits in 13 to 86% of patients (Table 3). We reviewed in detail the published reports of surgical removal of trigeminal schwannomas. McCormick et al reported outcomes in 14 patients with trigeminal schwannomas using either subtemporal, transtentorial, or suboccipital approaches [11]. Samii et al performed trigeminal schwannoma surgery using either frontotemporal-transylvian, retrosigmoid, subtemporal-presigmoid, or infratemporalextradural approaches in 12 patients [20]. Al-Mefty et al reported their experience with zygomaticmiddle fossa, cranioorbital-zygomatic, extended

petrosal, pterional, or combined approaches in 25 patients [1]. Long-term permanent cranial nerve deficits were reported in 12 patients (86%) by McCormick et al, in 8 patients (33%) by Samii et al, and in 3 patients (13%) by Al-Mefty et al. Despite removal, recurrence is not uncommon. McCormick et al noted a 36% recurrence rate while Samii et al and Al-Mefty et al reported the need for additional surgery because of tumor regrowth in 17% and 12% of the patients, respectively. Recently, Goel et al reported their experience using lateral basal, retrosigmoid, infratemporal,

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Axial (A) and sagittal (B) MRI of a 57-year-old female with a right sided trigeminal schwannoma. She was treated with a margin dose of 15 Gy prescribed to the 50% isodose line. Follow-up MRI 18 months after radiosurgery (C and D) show enhanced signal on long-TR image (D) without brainstem distortion or compression of the fourth ventricle. She remained asymptomatic. The long-TR signal change persisted at 26 months imaging follow-up (E and F).

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Trigeminal Schwannoma Management

FOLLOW-UP (MONTHS) MEDIAN (RANGE)

AUTHORS

NO. OF PATIENTS

McCormick et al 1988

14

Subtemporal, transtentorial, suboccipital

47 (4–177)

Samii et al 1995

12

25 (12–60)

Al-Mefty et al 2002

25

Goel et al 2003

73

Frontotemporal transylvian, retrosigmoid, subtemporalpresigmoid, infratemporal extradural Zygomatic-middle fossa, cranioorbital zygomatic extended petrosal, pterional, combined Lateral basal, retrosigmoid, infratemporal, frontotemporal, petrosal, combined

Pollock et al 2002 Present series 2003

10 23

Gamma Knife radiosurgery Gamma Knife radiosurgery

43 (12–111) 40 (12–146)

SURGICAL APPROACH

33 (3–134) 38 (6–120)

RECURRENCE POSTOPERATIVE COMPLICATIONS Death 1 hydrocephalus 1 CSF leak 1 meningitis 1 CSF leak 2, sinus thrombosis 1 tetraparesis 1, mild facial weakness 2 CSF leak 1 transient nerve deficit 11 (44%) Death 2 CSF leak 1 meningitis 1 osteomylitis 1 hematoma 1 — —

OR

NEUROPATHY

RE-TREATMENTS

12 (86%)

5 (35.7%)

8 (33%) (4 complete and 4 partial neuropathy)

2 (16.7%)

3 (13%)

3 (12%)

New deficit 5 (6.8%) worsening of facial sensation 13 (17.7%)

1 (1.45)

3 (30%) Temporary facial weakness 1 (4.3%) worsening of facial sensation 1 (4.3%)

1 (10%) 2 (8.6%)

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frontotemporal, petrosal, or combined surgical approaches in the management of 73 patients [6]. Total tumor excision was achieved in 70% of the patients. Postoperative complications in this series included death (2 patients), CSF leak (1 patient), meningitis (1 patient), osteomyelitis (1 patient), and hematoma (1 patient). Five patients (7%) developed new neurological deficits and 13 (18%) experienced worsening of their facial sensation. The outcome of microsurgery depends upon many factors (e.g., tumor size, approach, and surgeon’s experience). Many patients in microsurgical series may not have been suitable for radiosurgery because of large tumor volume. These patients may suffer from additional complications after microsurgery. RADIOSURGERY While postoperative complications (CSF leak, meningitis, transient, or permanent neurological deficit) can occur after skull base surgery, radiosurgery has little acute postoperative morbidity. Pollock et al reported outcomes after Gamma Knife radiosurgery in 24 patients with nonvestibular schwannoma including 10 with trigeminal schwannomas [17]. These authors reported a 96% tumor control rate (90% for trigeminal schwannomas). One patient with malignant trigeminal schwannoma died of tumor progression. Three of 10 patients with trigeminal schwannomas suffered new or worsening trigeminal dysfunction after radiosurgery. Kida et al treated 19 patients with trigeminal schwannoma using Gamma Knife radiosurgery [9]. These authors reported a 100% tumor control rate. Two of their patients reported worsening facial pain after radiosurgery. Mabanta et al performed Linear accelerator based radiosurgery on 18 patients who had nonacoustic schwannomas and 7 of these had trigeminal schwannomas [10]. These investigators treated 56% of their patients using a single isocenter, 33% with 2 to 4 isocenters and 11% with more than 5 isocenters. Local control was 100% but overall 17% of patients developed adverse radiation effects. In the present series only two patients (8.6%) developed delayed new or worsening symptoms after radiosurgery. Both these patients were treated in our initial experience and received relatively higher marginal doses. As our experience grew with vestibular schwannomas, we gradually lowered the tumor margin dose to 13 Gy with still excellent tumor growth control. The lower tumor margin doses are associated with diminished risk of complications [2,4,5,13,19]. In our series, 8.6% patients needed additional radiosurgery to treat continued tumor growth. We noted tumor shrinkage in 65%

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and stable tumors without further growth in 26% of the patients. Even though a large number of patients with vestibular schwannomas are treated without histological proof of diagnosis, their radiological characteristics are diagnostic with a high degree of certainty. Because of the location of trigeminal Schwannomas, a differential diagnosis exists, making an imaging diagnosis less accurate. However, the imaging appearance of meningiomas, chondrosarcomas, lymphomas, and metastases usually can be differentiated from trigeminal Schwannomas using various MRI sequences. Because no patient in our primary treatment group had delayed surgery, we cannot verify that all had trigeminal nerve sheath tumors. Of interest, those 12 patients with a proven diagnosis of schwannoma have had tumor shrinkage in 9 (75%). Regression was noted in 5 of 11 primary treated patients. In view of the reported morbidities of subtotal resection or biopsy, we do not believe that a histologic diagnosis is necessary for patients with typical signs, symptoms, and imaging. COMBINED SURGERY AND RADIOSURGERY For larger symptomatic tumors with mass effect removal is the preferred initial management strategy. When the tumor cannot be excised completely, radiosurgery is an excellent secondary strategy. Goel et al reported excellent results after resection of large trigeminal schwannomas [6]. They performed surgery for residual and recurrent tumors also. We believe that residual or recurrent tumors are safely and effectively treated by radiosurgery. The goal of recurrent or residual schwannoma management should be tumor growth control (and neurologic preservation) rather than complete tumor removal at the expense of major neurological deficits. Radiosurgery seems ideal for small volume residual tumors that enter the cavernous sinus. We suggest that patients with residual or recurrent trigeminal schwannomas should be given the option of radiosurgery instead of another resection. THE OPTIMAL RADIOSURGERY PATIENT Patients with small to moderate sized tumors with intact cranial nerve function are optimal candidates for radiosurgery. Current methods (multi-isocenter conformal dose plan, stereotactic MR imaging, and 13 Gy tumor margin dose) are associated with a high tumor control rate and minimal risk of adverse radiation effects. For larger tumors initial resection followed by delayed radiosurgery for residual tumor is an effective option.

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COMMENTARIES

This paper reports on the largest series of patients with trigeminal schwannoma treated by Gamma Knife surgery, and it also gives the longest follow up. Clearly the paper demonstrates that Gamma Knife surgery is an attractive management alternative for tumors less than 10 mL in volume. Undoubtedly, tumors of this size can also be successfully removed by microsurgery. However, in my experience, some facial numbness after surgery is unavoidable. Gamma Knife surgery should, therefore, be seriously considered as a primary management alternative. I concur with the opinion that a low prescription dose can achieve a dramatic volume reduction. In 6 recent patients of mine, followed for more than 3 years, dramatic volume reductions were achieved with prescription doses of 10 Gy/D to 14 Gy. The dramatic volume reduction in the patient prescribed 10 Gy was, however, followed by a delayed recurrence necessitating re-treatment. Schwannomas of the trigeminal nerve seem for sundry reasons to be more radio responsive than vestibular schwannomas. Patients should be warned that exacerbation of de novo facial pain may occur transiently as a result of this treatment. A typical trigeminal schwannoma is usually correctly identified on an MRI scan. The differential diagnoses mainly include meningiomas and metastatic tumors. Considering the fact that these tumors are also well managed by Gamma Knife surgery, an inadvertent treatment of them by radiosurgery would not be a serious problem.