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ORIGINAL ARTICLE
Year : 2016  |  Volume : 64  |  Issue : 5  |  Page : 973-979

Role of surgery for small petrous apex meningiomas causing refractory trigeminal neuropathy in the minimally invasive era


1 Department of Neurosurgery, Faculty of Medicine, Cairo University, Cairo, Egypt
2 Department of Ear and Nose, Fayoum University, Egypt
3 Department of Neurosurgery, Nasser Institute, Cairo, Egypt
4 Department of Neurosurgery, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, New York, USA

Date of Web Publication12-Sep-2016

Correspondence Address:
Ahmed Hegazy
Department of Neurosurgery, Faculty of Medicine, Kasr Al-Ainy Medical College, Ahmed Orabist, Al-Mohandeseen, Giza, Greater Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.190230

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 » Abstract 


Background: Radiosurgery seems to be a very appealing option for patients having a small petrous apex meningioma and presenting with trigeminal neuralgia, presumably because of the lower risk and cost involved. The aim of this study was to analyze the results of our surgical series of petrous apex meningioma presenting with trigeminal neuralgia, and to determine the efficacy of neurosurgical treatment with regard to pain control. The procedure-related complication and morbidity rates were also evaluated.
Materials and Methods: This is a retrospective study of 17 patients with a small (<3 cm) petrous apex meningioma. The included patients were refractory to medical treatment for trigeminal neuralgia and were deemed as surgical candidates. Postoperatively, the patients were assessed for pain relief according to the Barrow Neurological Institute (BNI) scale. A P value of less than 0.05 was considered significant. Magnetic resonance imaging was also performed after 6 weeks to assess the radicality of resection.
Results: In a median follow-up of approximately 2 years, the study showed that 14 of the 17 (82.4%) patients had complete pain relief, with very low morbidity and no mortality, and 100% tumor control. According to the Barrow Neurological Institute (BNI) scale for the assessment of postoperative pain relief, 52.9, 23.5, 5.9, 11.8, and 5.9% of patients had grades I, II, IIIa, IIIb, and IV in terms of their pain relief, respectively.
Conclusions: In our population of patients, surgery proved to be successful in providing symptomatic relief, with low morbidity and no mortality, and was comparable with other studies involving the minimally invasive modalities. However, these results warrant further follow-up, with recruitment of more patients, to demonstrate whether or not, surgery should be the primary choice of treatment in this subgroup of patients.


Keywords: Petrous apex lesions; stereotactic radiosurgery; trigeminal neuralgia


How to cite this article:
Hegazy A, Alfiki A, Adel M F, Alsawy M F, Al-Dash M F, Zein M, Amin SM, Al-Shami H, Biswas A. Role of surgery for small petrous apex meningiomas causing refractory trigeminal neuropathy in the minimally invasive era. Neurol India 2016;64:973-9

How to cite this URL:
Hegazy A, Alfiki A, Adel M F, Alsawy M F, Al-Dash M F, Zein M, Amin SM, Al-Shami H, Biswas A. Role of surgery for small petrous apex meningiomas causing refractory trigeminal neuropathy in the minimally invasive era. Neurol India [serial online] 2016 [cited 2020 Apr 4];64:973-9. Available from: http://www.neurologyindia.com/text.asp?2016/64/5/973/190230





 » Introduction Top


Most patients with trigeminal neuralgia (TN) have severe morbidity due to pain in the distribution of the trigeminal nerve (TGN). When caused by tumors, the pain is even more severe, and often involves more than one division of the TGN distribution. It also responds poorly to medical treatment.[1],[2],[3],[4],[5],[6],[7] TN secondary to a tumor usually affects patients during the early course of the disease. The best modality of management of trigeminal neuralgic pain in the presence of smaller tumors in the vicinity of the TGN remains controversial.[5],[8] In this era, stereotactic radiation seems to be an appealing option.[6] However, the management of associated trigeminal neuralgia (TN) often requires the administration of higher doses of radiation than required in an isolated meningioma that does not present as TN. Eventually, many patients require surgery for the persistent clinical symptoms. Although there are many case reports addressing this clinical concern, there are no original studies referring to the management of TN as a result of a small petrous apex meningioma, due to the rarity of this finding. The aim of our study was to analyze the outcome of pain relief following surgical excision of the small petrous apex meningioma that was responsible for the causation of TN. This article also attempts to compare the results of pain relief obtained in our series with those presented in the relevant literature for different treatment modalities pertaining to petrous apex meningiomas.


 » Materials and Methods Top


Between January 2011 and October 2015, the data from 17 patients with a small (<3 cm in maximum diameter) petrous apex meningioma, who underwent surgery at Cairo University Hospitals was analysed. The surgery was performed in all of them in order to address their persistent trigeminal pain despite the administration of maximum medical treatment. Patients were included in the study only if they had a small petrous apex meningioma manifesting as TN and were fit for surgery. Of the total number of patients who fulfilled this criteria, there was one patient who had already undergone previous gamma knife treatment. All the patients were operated using either an anterior petrosal approach or a retrosigmoid approach. The techniques used for anesthesia, positioning, approach, and tumor resection have been described previously in the literature.[3],[5],[6],[7] All patients underwent a contrast enhanced magnetic resonance (MR) imaging scan to assess the extent of resection at 6 weeks. The extent of resection was described as gross total (Simpson Grade I or II), subtotal (>90% resection), or partial (<90% resection), as determined by the surgeon's intraoperative impression and the postoperative magnetic resonance (MR) image.

The improvement obtained in the TN was graded according to the Barrow Neurological Institute (BNI) pain scale.[9],[10] The outcome was classified as: Good (BNI grades I–IIIa) and poor (BNI grades IIIb, IV, and V).

Operative findings that were collated included: (a) The relationship of the tumor to the nerve, meninges, and bone; (b) the presence or absence of an offending loop of the superior cerebellar artery; and, (c) the condition of the trigeminal nerve. The relationship between the tumor and nerve was classified as 'in contact,' 'displaced,' or 'infiltrated.'[11] The study followed the set of ethical principles laid down in the Declaration of Helsinki.

Sample characteristics

Seventeen patients were included in this study with 14 (82.4%) female patients. The mean age in this patient population was 47.3 years with the standard deviation being 11.24 years. Patients were classified into two groups according to their age: <45 and >45 years. Frequency and percentage distribution for each age group were 8 and 47.1%; and, 9 and 52.9%, respectively. In addition, the mean and standard deviation with regard to the follow-up period calculated over the months, were 23.64 and 6.73, respectively, with a 95% CI (20.18, 27.11), and the median value being 22.0.

Statistical techniques

Among the parametric tests, the t-test and one-way analysis of variance (ANOVA) tests were employed. On the other hand, among the nonparametric tests, Kolmogorov–Smirnov test (KS test) was used to test for the sample homogeneity. For hypothesis testing, one sample test for proportions, the KS test for two independent samples, and regression analysis by backward elimination were used. All previously mentioned tests were carried out using α = 0.05 and β ≤ 0.2 level of significance. All statistical analysis was done using the Statistical Package for the Social Science [IBM SPSS statistics (20.0)] and Minitab® 16 Statistical Software (Minitab Inc.).

Variables in the study

Variables used in this study were divided into three groups:



  1. Demographic variables: Age and gender
  2. Tumor-related variables: Tumor volume in cubic centimeters (cm 3), tumor extension, vascularity, consistency, side, and pathology
  3. Variables related to the surgical outcome: Duration of pain before treatment; pain distribution; facial numbness before and after the treatment; clinical presentation; the surgical approach; surgery-related variables such as the plane of cleavage and relationship to the surrounding structures (bone, dura, vessels, brainstem, and trigeminal nerve, including a description of the condition of the nerve); postoperative BNI scale, and whether the patient needed treatment or not; complications; extent of resection, and, the follow up status.



 » Results Top


Sample homogeneity

The tumor size and preoperative pain distribution were compared with the demographic data. The tumor size was correlated with gender and age using t-test for two independent groups (P = 0.947 for gender and 0.950 for age groups). The pain distribution (composed of three dummy variables [V1, i.e., ophthalmic division, 0], [V2, i.e., maxillary division, 0], [V3, i.e., mandibular division, 0] was correlated with the demographic data (gender) using KS test (P value = 0.999, 0.972, 0.998). It was also correlated with additional demographic data that included patients in the age group less than or equal to 45 years, and those in the age goup greater than 45 years (P value = 0.734, 0.999, 0.998, respectively). Thus, the study design proved to be a one sample study (simple design).

Descriptive statistics

  1. Analysis of pain results following treatment:Fourteen of the 17 (82. 4%) patients were pain free at a median follow-up of 22 months. In addition, the percentage distribution (%) of results (the quality of BNI scale) specific to the group of patients in this study was 52.9, 23.5, 5.9, 11.8, 5.9 for grades I, II, IIIa, IIIb, and IV, respectively.

  2. Analysis of the distribution of postoperative pain improvement (based on the BNI scale) among various demographic variables (age groups and genders) and their pain distribution:In the present study, the authors tried to determine whether or not the degree of improvement (based on the BNI scale) was related to age, gender, or the preoperative clinical presentation (i.e., distribution of the neuralgic pain in the ophthalmic, maxillary, or mandibular divisions of the TGN). The results showed no significant difference with respect to these variables, with P = 0.395, 0.998 (P > 0.05) for age and gender, respectively, using the chi square test. However, with regard to the preoperative distribution of pain, it was found that patients with pain in the ophthalmic division of the TGN had the worst outcome (BNI grades IIIb or IV) with no significant improvement (P = 0.999), whereas the patients with pain in the maxillary and mandibular divisions of the TGN had a much better outcome with P = 0.035 and 0.058, respectively. Therefore, the most favorable outcome was noted for patients with maxillary pain followed by patients with mandibular pain (P < 0.05 and P < 0.1, respectively) using the Wilcoxon's signed ranks test

  3. Factors affecting postoperative BNI outcome:Backward regression analysis was used to determine the best group of homogenous variables affecting the postoperative BNI scale

    The most important variables which appeared in the model were:

    • V1 ophthalmic division pain (positive effect): The higher the incidence of ophthalmic division involvement during preoperative clinical presentation, the higher was the postoperative (worse) BNI scale;
    • Tumor volume (negative effect): A better BNI outcome was associated with a smaller tumor size;
    • Presence or absence of postoperative complications (dummy variable; positive effect): A worse BNI was associated with the increased incidence of postoperative complications;
    • TGN root visibility on preoperative imaging (dummy variable; negative effect): A worse BNI was obtained when the TGN root was not seen on preoperative imaging; and
    • Postoperative follow-up period in months (positive effect): There was a possibility that the BNI may worsen with time. In addition, because of the critical indication of this finding, a direct correlation analysis between this variable and the BNI scale was done, which proved to be significant with an r = 0.691, which is also considered significant at 0.01 level of significance The model showed that the five variables mentioned earlier contributed to influencing the BNI obtained with an R2 = 89.7% and that the model was significant at 0.01 level of significance.


  4. Analysis of complications following surgical treatment:Our findings indicate that 14 out of 17 patients (82.3%) included in the study showed a remarkable improvement after the surgery. Only 1 of them had a grade III outcome according to the BNI scale, whereas the remaining 13 patients were in grades I (9 cases, 52.9%) and II (4 cases, 23.5%). One patient in this group, who was diagnosed as a case of neurofibromatosis type II, showed tumor and pain recurrence 9 months after surgery, and also required the placement of a ventriculoperitoneal shunt for hydrocephalus. A total of 17.6% of our patients showed minor reversible cranial nerve deficits, and these included: A third nerve paralysis in one case, which resolved spontaneously in 3 months; a transient facial nerve paralysis in one case, which resolved spontaneously in 4.5 months; and a post-craniotomy syndrome, which improved gradually over 1.5 years but did not disappear. At the last follow up, no patients had neurological deficits.


Illustrative cases

Case 1

A 56-year-old female patient presented with TN, involving all three divisions of the TGN on the right side. She had frequent attacks of the neuralgic pain, approximately 5 to 10 times every hour. The patient was given a dose of 1600 mg of carbamazepine on a daily basis but failed to show any response. On examination, it was found that there were trigger zones all over the face; however, there was no sensory or motor deficit in the distribution of the TGN. An MRI showed a right petrous apex meningioma, which was about 2.7 × 1.8 × 2.2 cm in its maximum diameter [Figure 1]. The patient was operated through a right anterior-petrosal approach [Figure 2]. The greater superficial petrosal nerve (GSPN) was our reliable superficial landmark of the Kawase's triangle and served as the superficial lateral border of anterior petrosectomy on the middle fossa to avoid internal carotid artery (ICA) injury [Figure 3]. The TGN root was found to be severely distorted by the tumor, which was partly insinuated between the tumor and the bone. The nerve was found to be reddish and hyperemic [Figure 4]. The tumor was completely removed [Figure 5], and postoperatively, there was an immediate disappearance of pain. The patient was allowed to stop carbamazepine in the early postoperative period and remained pain free until the last available follow up visit. The postoperative MRI [Figure 6] showed complete tumor excision.
Figure 1: Preoperative axial T1-weighted contrast enhanced image at the level of pons shows the right petrous apex meningioma

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Figure 2: Intra-operative photograph showing extra-dural exposure of Kawase's triangle. Abbreviations used: GG: Gasserion ganglion; GSPN: Greater superficial petrosal nerve; TL: Temporal lobe; PA: Petrous apex

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Figure 3: Intra-operative photograph showing extra-dural drilling of the apex of the petrous bone

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Figure 4: Intra-operative photograph showing neurovascular dissection of the tumor

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Figure 5: Surgical view after complete tumor removal

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Figure 6: Postoperative MRI shows complete excision of the tumor. A hyperintense signal due to the presence of fat is seen

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Case 2

A 46-year-old female patient presented with a 2-year history of pain in the distribution of the left TGN. The attacks were occurring at a frequency of 2–3 times every hour. The pain was lancinating in nature and occurred in the distribution of maxillary and mandibular divisions of TGN; however, between the attacks, the patient was not pain free. Thus, the sharp shooting pain was replaced by a dull aching pain in the same distribution but of a lower intensity. This patient also had an associated myofascial spasm on the left side. On examination, there was no muscle wasting; however, there was hypoesthesia involving the left side of the face. The patient had been given medical treatment including, but not limited to, carbamazepine 1200 mg/day, gabapentin up to 3600 mg/day, steroids, and phenytoin 300 mg/day.

In spite of significant doses of medicines, the patient failed to respond to medical treatment, and the attacks became worse. Radiologically, there was an enhancing space occupying lesion at the apex of the petrous bone, which was encroaching on the brain stem and the mesial temporal lobe [Figure 7]. The patient was offered surgery, and was operated through a left-sided anterior-petrosal approach combined with a frontotemporal corridor. During surgery, the tumor was found to completely displace the TGN root and occupied the angle between the root and  Gasserian ganglion More Details; however, the tumor could be easily dissected from the nerve and the brain stem. The nerve was found to be healthy without considerable hyperemia or invasion. The postoperative recovery was unremarkable, and the pain disappeared completely; the attacks of myofascial spasm decreased in frequency but persisted. Postoperative radiology showed complete tumor resection [Figure 8]. The pathology report proved the tumor to be a meningothelial meningioma (World Health Organisation grade I).
Figure 7: MRI showing enhancing meningioma at the apex of petrous bone, which was encroaching on the brain stem and the mesial temporal lobe

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Figure 8: Postoperative MRI showing a complete tumor resection

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 » Discussion Top


Although there is agreement that the best treatment for tumor induced TN,[4] which represents up to 6% of all cases TN,[2] includes removal of the tumor and obtaining relief from neuralgic pain, there is no agreement, however, on the the ideal choice of treatment, particularly for tumors less than 3 cm in size. This is because a number of treatment options are available including medical treatment, glycerol rhizotomy, percutaneous Gasserian ganglion compression, radiofrequency trigeminal nerve ablation, alcohol injection, stereotactic radiosurgery, and microsurgery.[2]

The response to medical treatment is only short lived.[6] Glycerol rhizotomy, percutaneous Gasserian ganglion compression, radio frequency trigeminal ganglion ablation, and alcohol injection into the Meckel's cave are simple and repeatable; however, they have variable failure rates ranging between 29 and 56%, and do not address the primary pathology responsible for the neuralgic pain, that is, the existing tumor compressing the trigeminal nerve.[4]

Stereotactic radiosurgery is noninvasive, presumably costs less than surgery,[12],[13] produces a good tumor control,[14] requires no general anesthesia,[15],[16] and has a lower rate of complications. It does not, however, produce satisfactory quantitative as well as qualitative outcomes, as TN often persists.[2] Although surgery is expensive in many western countries, in a developing country like Egypt, because of the subsidy by the government, carryng out surgery for excising the tumor is often more economical than administering radiosurgery.

The most widely used approach in the present series was the anterior-petrosal approach utilizing a frontotemporal craniotomy in 15 cases, whereas the retrosigmoid approach was used in two cases. Other approaches which have been reported to be used in the resection of petrous apex meningiomas include the pterional, posterior petrosal, and the expanded endoscopic transpetrous transnasal approaches.[1],[17],[18],[19],[20]

Other reports have recorded similar success rates for the treatment of meningiomas with TN.[1],[5] The main drawbacks of surgery include the high incidence of surgical complications. Some of the reported complications, mainly in the prestereotactic radiosurgery era, particularly for larger tumors, have included cranial nerve deficits in up to 50% of cases, intracranial hemorrhage, cerebrospinal fluid leakage, and death, in addition to approach-related morbidities.[1] However, these problems were not encountered in the current study because most complications reported in literature are related to tumor size, its anatomical relationships, and the invasion of nearby structures.[21] Accordingly, the surgical resection of smaller tumors is less likely to produce major complications.[6],[22],[23]

On the other hand, a number of reports, including those specifically focusing on stereotactic radiosurgery, have indicated that tumor resection, whenever possible, produces the most effective pain relief in the presence of tumor induced TN.[1] In addition, stereotactic radiosurgery is not a complication free procedure. In spite of a lower incidence of complications, stereotactic radiosurgery has been shown to produce a new onset neuralgic pain or worsening of preexisting TN in approximately 10–12% of skull base meningiomas treated by stereotactic radiosurgery. Besides, radiation-induced meningiomas or cavernous malformations, peritumoral edema, cranial nerve damage, arteritis, and brain stem necrosis may result as a sequel to stereotacic radiosurgery.[24],[25],[26],[27],[28],[29] Unlike the transient effects of cranial nerve paresis seen following surgery, most of these complications induced by radiosurgery are usually permanent. Some reports have shown that the incidence of complications following radiosurgery reaches almost 7.6%.[22] In a recent report on the treatment of TN caused by a small petrous apex lesion where stereotactic radiosurgery was used as the primary treatment modality, tumor shrinkage was not associated with pain relief. Thus, it was found that apart from the 2 patients who showed no improvement initially, there were 3 additional patients who showed pain recurrence in the initial 12 months following the administration of stereotactic radiosurgery, 2 of whom required further surgical treatment.[2]

In this small pilot study of patients with a median follow-up of approximately 2 years, minimally invasive surgery provided a successful relief from TN. However, these results warrant further follow-up, with recruitment of more patients in a multicentric trial to demonstrate if surgical excision of petrous apex meningiomas for refractory TN should be the primary treatment of choice.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest

 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]

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