Advances in Medical Sciences 60 (2015) 25–30
Contents lists available at ScienceDirect
Advances in Medical Sciences journal homepage: www.elsevier.com/locate/advms
Original Research Article
Usefulness of intraoperative monitoring of oculomotor and abducens nerves during surgical treatment of the cavernous sinus meningiomas Wojciech Kaspera a,*, Piotr Adamczyk a, Aleksandra S´laska-Kaspera b, Piotr Ładzin´ski a a b
Department of Neurosurgery, Medical University of Silesia, Regional Hospital, Sosnowiec, Poland Department of Laryngology, Medical University of Silesia, University Hospital, Katowice, Poland
A R T I C L E I N F O
A B S T R A C T
Article history: Received 26 May 2014 Accepted 28 August 2014 Available online 6 September 2014
Purpose: We analyzed the usefulness and prognostic value of intraoperative monitoring for identification of the oculomotor (III) and the abducens (VI) nerve in patients with cavernous sinus meningiomas. Material/methods: 43 patients diagnosed with cavernous sinus meningiomas were divided according to their topography. Function of the nerves was scored on original clinical and neurophysiological scales. Results: The percentage of nerves identified correctly with the monitoring was significantly higher (91% vs. 53% for nerve III and 70% vs. 23% for nerve VI, p < 0.001). The fractions of nerves III and VI identified correctly by means of the monitoring were significantly higher in the case of tumors with intra- and extracavernous location (89% vs. 32%, p < 0.01) and intracavernous tumors (80% vs. 20%, p < 0.05), respectively. The quality of post-resection recording correlated with functional status of both the nerves determined 9 months after the surgery (R = 0.51, p < 0.001 for nerve III and R = 0.57, p < 0.01 for nerve VI). Even a trace or pathological response to the post-resection stimulation was associated with improved functional status (90% vs. 50%, p < 0.05 for nerve III and 93% vs. 38%, p < 0.01 for nerve VI). Conclusions: Neurophysiological monitoring of ocular motor nerves enables their intraoperative identification during resections of the cavernous sinus meningiomas. Intraoperative monitoring of nerve III is particularly important in the case of tumors with extra- and intracavernous location, and the monitoring of nerve VI in the case of intracavernous tumors. The outcome of the post-resection monitoring has prognostic value with regard to the clinical status of the nerves on long-term follow-up. ß 2014 Medical University of Bialystok. Published by Elsevier Urban & Partner Sp. z o.o. All rights reserved.
Keywords: Cavernous sinus meningiomas Neurophysiological intraoperative monitoring Oculomotor nerve Abducens nerve
1. Introduction Progress in surgical technique resulted in increased radicality of skull base procedures. One example is surgical treatment of meningiomas located in the cavernous sinus and its surroundings. However, these procedures are still associated with the risk of injury to cranial nerves related to the cavernous sinus. Intraoperative neurophysiological monitoring, supporting visual identification of ocular motor nerves, constitutes one way of preventing such complications [1–4]. While the usefulness of the neurophysiological monitoring in facial nerve sparing was unambiguously confirmed in the case of resections of the cerebellopontine angle
* Corresponding author at: Department of Neurosurgery, Medical University of Silesia, Regional Hospital, Plac Medykow 1, 41-200 Sosnowiec, Poland. Tel.: +48 32 368 2551; fax: +48 32 368 2550. E-mail address: [email protected] (W. Kaspera).
tumors, there is no similar evidence with regard to tumors located in the cavernous sinus. Most of the sparse papers dealing with the problem in question [5,6] centered around the description of the methodology of monitoring itself. Moreover, the few available opinions in this matter are highly inconclusive [4,7,8]. For example, Weisz et al. [8] claimed that intraoperative monitoring is not associated with additional benefits due to specific anatomical relationships between the ocular motor nerves and tumor. However, Sekiya et al. [4] showed that the intraoperative monitoring facilitates identification of oculomotor (III) nerve, especially if the tumor alters normal anatomical relationships within the cavernous sinus. The results of this latter study might be confounded by the lack of statistical analysis [4]. The aim of this prospective study was to use statistical analysis in order to objectively verify the usefulness of neurophysiological monitoring for intraoperative identification of nerve III and abducens (VI) nerve. Moreover, having access to a relatively large (as for this type of tumors) sample of 43 operated patients, we
http://dx.doi.org/10.1016/j.advms.2014.08.009 1896-1126/ß 2014 Medical University of Bialystok. Published by Elsevier Urban & Partner Sp. z o.o. All rights reserved.
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W. Kaspera et al. / Advances in Medical Sciences 60 (2015) 25–30
analyzed the usefulness of this method in various topographic variants of the cavernous sinus tumors. Finally, we verified if the use of intraoperative monitoring influences clinically determined function of the nerves during long-term follow-up. 2. Patients and methods 2.1. Patients The study included the group of 43 consecutive patients (33 women and 10 men) aged between 22 and 74 years (mean age: 49.8 years), who were diagnosed with meningiomas located in the cavernous sinus or its surroundings. All the patients were treated at the Department of Neurosurgery, Medical University of Silesia in Sosnowiec between 2001 and 2011. Five topographic types of the tumors were identified on the basis of their localization documented on MRI: (1) intracavernous tumors (type A, Fig. 1a and b), (2) extracavernous tumors surrounding the cavernous sinus (type B, Fig. 1c and d), (3) tumors with both extra- and intracavernous location, penetrating into the anterior part of the cavernous sinus (type C, Fig. 1e and f), (4) tumors with both extraand intracavernous location, penetrating into the posterior part of the cavernous sinus (type D, Fig. 1 g and h), and (5) tumors with both extra- and intracavernous location, invading the entire cavernous sinus (type E, Fig. 1i and j). Functional status of nerves III and VI was determined one day prior to the surgery, at discharge from hospital, and during control visit 9 months after the surgery. The functional impairment of the nerves was graded on a 4-item scale: (I) normal status, (II) discrete paresis or subjectively reported impression of double vision without evident impairment of the eye globe motility, (III) severe paresis, and (IV) palsy. Although none of the patients showed isolated trochlear (IV) nerve palsy, functional deficits of this nerve accompanied disorders of nerve III and VI in some cases. 2.2. Intraoperative monitoring of nerves III and VI Monitoring was conducted with a 16/32 channel amplifier ISIS (Inomed Medizintechnik, Germany) exporting data to NeuroExplorer software. Recording needle electrodes were applied to muscles innervated by the monitored nerves: levator palpebrae superioris muscle or superior rectus muscle to monitor nerve III, and lateral rectus muscle for the purpose of nerve VI monitoring. A reference electrode was applied to the temporal muscle [9]. We eventually examined two nerves: nerve III located in the cavernous sinus wall, and nerve VI passing through the cavernous sinus. After several unsuccessful attempts we resigned from nerve IV monitoring. This decision was associated with difficulties in clinical interpretation of neurological deficits resulting from functional impairment of this nerve, as well as with problems with proper insertion of recording electrode into a small superior oblique muscle, or with selective stimulation of nerve IV located in close proximity of nerve III in the cavernous sinus wall. The nerves were stimulated with a 1.5–1.8 V direct current delivered via parallel or concentric electrodes. The amplitude of recording was considered as a principal criterion of muscular response. The result of identification was classified using a 4-item scale (from a to d): (a) both visual and electromyographic identification, (b) visual identification without electromyographic response,
Fig. 1. Topographic types of 43 analyzed meningiomas of the cavernous sinus. (a, b) Type A tumor, fibrosus meningioma located inside the left cavernous sinus; (c, d) type B tumor, mixed meningioma of the right large sphenoid wing, infiltrating layers of the lateral wall of the cavernous sinus; (e, f) type C tumor, syncytial meningioma involving the orbital cone, sphenoid sinus and anterior part of the right
cavernous sinus; (g, h) type D tumor, psammomatous meningioma involving the apex of the left temporal bone pyramid and superior part of the clivus, penetrating through the Meckel’s cavity toward the posterior part of the cavernous sinus; (i, j) type E tumor, psammomatous meningioma of the left cavernous sinus, penetrating toward the sella turcica, ethmoid sinus, medial parts of the temporal lobe, clivus and apex of the temporal bone pyramid.
W. Kaspera et al. / Advances in Medical Sciences 60 (2015) 25–30
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Fig. 2. (a, b) Normal recording of oculomotor (a) and abducens (b) nerve function with more than 1 mV amplitude; (c, d) abnormal, multiphasic recording of oculomotor nerve function (c) with amplitude below 0.5 mV, abnormal recording of abducens nerve function (d) with amplitude of about 0.6 mV, baseline amplitude of both nerves markedly exceeded 1 mV with subsequent more than a 50% decrease; (e, f) lack of response to stimulation: lack of response to oculomotor nerve stimulation other than stimulatory artifact (e), lack of recording of abducens nerve function (f) numerous artifacts that should not be interpreted as a recording of the nerve function.
(c) impossibility of visual identification with positive result of electromyographic testing, and (d) neither visual nor electromyographic identification. The functional neurophysiological impairment of nerves III and VI was assessed on a 3-item scale: (1) normal recording, i.e. evident spike with at least 0.5 mV baseline amplitude, (2) abnormal recording, i.e. a trace of response or evident (more than 50%) decrease in the amplitude as compared to the baseline level, and (3) lack of response to stimulation (Fig. 2). The postoperative examination was not conducted in one patient who died immediately after the surgery due to injury of internal carotid artery. Furthermore, we resigned from identification of nerve VI in three patients whose tumors infiltrated lateral walls of the cavernous sinus without penetration of its cavity (which corresponded to type B tumors). 2.3. Statistical analysis The results were analyzed with Statistica 5.5 package (StatSoft, United States) and Excel spreadsheet. Relationships between studied variables were analyzed with the Spearman’s rank correlation coefficients as well as with the McNemar’s test and Fisher’s exact test. The results of the testing were considered significant at p 0.05. 3. Results The proportions of nerves III identified accurately with and without an aid of neurophysiological monitoring were 39:43 and 23:43, respectively (91% vs. 53% correct identifications), and the analogous proportions of correctly identified nerves VI amounted to 28:40 and 9:40, respectively (70% vs. 23% correct identifications). The analysis for nerve VI did not include three patients in
whom this nerve was not identified intraoperatively. The fractions of oculomotor and abducens nerves that were identified correctly with an aid of neurophysiological monitoring turned out to be significantly higher than in the case of visual inspection (McNemar’s test, p < 0.001). Moreover, our analysis revealed that the percentage of oculomotor nerves that were identified correctly without the neurophysiological monitoring differed significantly depending on a topography of the tumor; the fraction of the correctly identified nerves was the highest in the case of intracavernous tumors (type A) and the lowest for both intra- and extracavernous tumors, that involved the whole cavernous sinus (type E) (Fisher’s exact test, p < 0.01; Table 1). In contrast, the percentage of oculomotor nerves Table 1 Number of oculomotor nerves that were correctly identified without an aid of neurophysiological monitoring in patients with various topographical types of the cavernous sinus tumor (Fisher’s exact test, p < 0.01). Visual identification (variant)
Topographic type of analyzed tumor A
B
C
D
E
Yes (a + b) No (c + d) Total
11 4 15
2 1 3
0 2 2
4 0 4
6 13 19
Total
23 20 43
A – intracavernous tumor, B – extracavernous tumor surrounding the cavernous sinus, C – tumor with both extra- and intracavernous location, penetrating into the anterior part of the cavernous sinus, D – tumor with both extra- and intracavernous location, penetrating into the posterior part of the cavernous sinus, E – tumor with both extra- and intracavernous location, invading the entire cavernous sinus; a – visual identification by an operator confirmed with electromyography, b – visual identification without electromyographic response, c – impossibility of visual identification with positive result of electromyographic testing, d – neither visual nor electromyographic identification.
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that were identified correctly on the basis of neurophysiological monitoring did not differ significantly between various topographic types of the tumors (Fisher’s exact test, p = 0.7). The topography of the tumor did not exert significant effect on the percentage of correctly identified nerves VI, either on neurophysiological monitoring or on visual inspection (Fisher’s exact test, p = 0.6 and p = 0.3, respectively). As type A and type E tumors predominated in our material, we analyzed possibility of identifying nerves III and VI in these two topographic variants. The use of monitoring was not reflected by an increase in the percentage of nerves III that were identified correctly in patients with type A tumors (McNemar’s test, p = 0.7). In the case of type E tumors, the proportions of nerves III that were identified correctly with and without an aid of neurophysiological monitoring amounted to 17:19 and 6:19, respectively (89% vs. 32% correct identifications). The percentage of nerves III that were identified correctly by means of monitoring turned out to be significantly higher than in the case of visual inspection (McNemar’s test, p < 0.01). The proportions of nerves VI that were identified correctly with and without monitoring in patients with type A tumors amounted to 12:15 and 3:15, respectively (80% vs. 20% correct identifications). The percentage of abducens nerves identified correctly with an aid of neurophysiological monitoring turned out to be significantly higher than in the case of visual inspection (McNemar’s test, p < 0.05). In contrast, the use of monitoring was not reflected by a significant increase in the percentage of correctly identified nerves VI in patients with type E tumors (McNemar’s test, p = 0.5). During the last stage of our analysis we verified a prognostic value of muscular response to stimulation of the ocular motor nerves. Using the 3-item scale of neurophysiological functional impairment, we analyzed a relationship between the outcome of postoperative nerve III stimulation and functional status of this nerve determined 9 months after the surgery (Table 2). One patient who died during perioperative period and two individuals in whom the nerve could not be identified, either visually or by means of monitoring (type d of identification), were excluded from the analysis. We showed that better postoperative recording was associated with better functional status of nerve III at control visit (Spearman’s rank correlation coefficient, R = 0.51, p < 0.001). Moreover, we verified if retaining any potential to transmission (the presence of either normal or abnormal postoperative recording) has any impact on improvement in functional status of nerve III between discharge from hospital and control examination 9 months after the surgery. The improvement in functional status of nerve III was defined as at least one point increase in the 4-item functional impairment scale. The analysis did not include patients without any functional deficits of nerve III
Table 2 Relationship between the outcome of postoperative neurophysiological recording of oculomotor nerve and functional status of this nerve determined 9 months after the surgery (Spearman’s rank correlation coefficient, R = 0.51, p < 0.001). Postoperative recording (variant)
Normal (1) Abnormal (2) Lacking (3) Total
Functional status of oculomotor nerve I
II
III
IV
12 7 5 24
3 1 3 7
0 0 1 1
0 1 7 8
Total
15 9 16 40a
a The analysis did not include one patient who died during perioperative period and two individuals in whom the nerve could not be identified, either visually or by means of monitoring (type d of identification); 1 – normal recording, i.e. evident spike with at least 0.5 mV baseline amplitude, 2 – abnormal recording, i.e. a trace of response or evident (more than 50%) decrease in the amplitude as compared to the baseline level, 3 – lack of response to stimulation.
Table 3 Relationship between the outcome of postoperative neurophysiological recording of abducens nerve and functional status of this nerve determined 9 months after the surgery (Spearman’s rank correlation coefficient, R = 0.57, p < 0.01). Postoperative recording (variant)
Normal (1) Abnormal (2) Lacking (3) Total
Functional status of abducens nerve
Total
I
II
III
IV
5 6 2 13
1 3 2 6
0 2 4 6
0 1 4 5
6 12 12 30a
a The analysis did not include one patient who died during perioperative period, three individuals who were not subjected to nerve VI identification, and nine persons in whom identification of this nerve was not possible (type d of identification). Legend as in Table 2.
at the time of discharge (n = 4) and one individual who died during perioperative period. The proportion of patients showing the improvement in the nerve function was 18:20 for the group with at least minimum response (either normal or abnormal one) to the stimulation, and 9:18 in those whose nerves did not respond to the postoperative stimulation or could not be identified (90% vs. 50% of patients with long-term improvement of the functional status of nerve III, Fisher’s exact test, p < 0.05). Also in the case of nerve VI, better postoperative recording was associated with better functional status determined 9 months after the surgery (Spearman’s rank correlation coefficient, R = 0.57, p < 0.01; Table 3). The analysis did not include one patient who died during perioperative period, three individuals who were not subjected to nerve VI identification, and nine persons in whom identification of this nerve was not possible (type d of identification). The proportion of patients who showed an improvement in the functional status of nerve VI during control examination taking place 9 months after the surgery was 14:15 for the group with retained normal or pathological response to stimulation, and 8:21 in persons whose nerves did not respond to the postoperative stimulation or could not be identified (93% vs. 38% of patients with improved functional status of nerve VI, Fisher’s exact test, p < 0.01). The analysis did not include one patient who died during perioperative period, three individuals who were not subjected to nerve VI identification, and another three persons who did not show any functional deficits of this nerve at the time of discharge. 4. Discussion Our findings suggest that neurophysiological monitoring plays an important role in the identification of ocular motor nerves during resection of tumors located in the cavernous sinus. Moreover, we showed that the outcome of nerve III and VI identification differs depending on a topographic type of the cavernous sinus meningioma. The tumors included in our analysis represented five topographic types (A–E). The type A tumors were intracavernous lesions, directly contacting or forming adhesions with nerve VI, but without involvement of nerve III. The type B–E tumors were located in the lateral wall of the cavernous sinus, contacted nerve III and invaded various compartments of the cavernous sinus; this group included type E tumors with both intra- and extracavernous location. We showed that correct visual identification of nerve III is possible in the case of tumors that penetrate inside the cavernous sinus (type A). Consequently, neurophysiological monitoring does not play an important role during identification of the nerve in patients with tumors of this type. The usefulness of nerve III monitoring is limited to tumors that are located outside the cavernous sinus and obstruct the view of the nerve (type E). Furthermore, the intraoperative monitoring
W. Kaspera et al. / Advances in Medical Sciences 60 (2015) 25–30
turned out to be particularly important for identification of nerve VI in patients with tumors growing inside the cavernous sinus (type A). In contrast, the use of monitoring was not reflected by a significant increase in the percentage of nerves VI that were identified correctly in patients with type E meningiomas. Consequently, nerve III is more likely to be correctly identified in patients with intracavernous tumors due to possibility of its visual identification, additionally supported by neurophysiological monitoring. In contrast, the use of monitoring significantly increases probability of identifying this nerve in patients with tumors having both intra- and extracavernous location. In the case of nerve VI, the efficacy of monitoring is limited solely to the intracavernous masses. Moreover, we revealed that outcome of the monitoring is a prognostic factor of functional status of ocular motor nerves on long-term follow-up. Better outcome of the postoperative monitoring turned out to be associated with better functional status of the nerves determined 9 months after the surgery. Moreover, we showed that retaining even a trace potential to transmission is associated with significant improvement of the nerve function during control examination. The abovementioned findings are consistent with the data published by De Jesus et al. [7], according to whom implementation of cranial nerve monitoring constitutes one reason behind recently observed improvement in the outcomes of surgical treatment of the cavernous sinus meningiomas. Monitoring of response from ocular motor nerves, as well as monitoring of other motor cranial nerves, turned out to be efficient during brain stem tumors operations and other cranial base tumors resections, and as such is used for many years in a number of centers [10–13]. Also the benefits of facial nerve monitoring during resections for tumors of the cerebellopontine angle do not raise any controversies. However, the usefulness of neurophysiological monitoring of ocular motor nerves during resections of the cavernous sinus tumors is still put into question [4,8,12]. Resections of the cavernous sinus tumors do not belong to ‘‘standard’’ neurosurgical procedures and as such are performed in a small number centers, only few of which use intraoperative monitoring. Probably this represents the reason behind a paucity of published papers dealing with monitoring of ocular motor nerves during resections of the cavernous sinus tumors. Weisz et al. [8] questioned the benefits of intraoperative monitoring of ocular motor nerves. According to these authors, in the case of the cerebellopontine angle tumor resection (during which the efficacy of monitoring is unquestioned), the nerve is usually located outside the mass, rather than being surrounded by the latter, and its form can vary from a single unaltered trunk to a bunch of minute fibers. However, the situation is frequently different in the case of nerves located within the cavernous sinus. They can be dislocated, infiltrated or invaded by the tumor or, conversely, are completely independent from the mass. Therefore, the abovementioned authors concluded that while the nerves that are invaded or infiltrated by the tumor cannot be spared, those being visible for an operator do not require any neurophysiological monitoring [8]. To the best of our knowledge the paper published by Sekiya et al. [4] is the only one dedicated solely to the monitoring of ocular motor nerves. According to the authors of this paper, monitoring of ocular motor nerves is very useful, similar to the monitoring of facial nerve during resections for the vestibular schwannomas. Not only the authors emphasized the role of the monitoring in the identification of the nerve, but also highlighted its importance in confirming the result of visual inspection [4]. Consequently, the two contradictory opinions exist in literature; while some authors equal the usefulness of the ocular motor nerve monitoring during the operations for the cavernous sinus
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tumors to that of the facial nerve monitoring during resection of the cerebellopontine angle tumors, the others put it into question. In our opinion, however, both these attitudes are too radical. Monitoring of the ocular motor nerves is useful and as such should be recommended, but one should not expect the similar outcomes as in the case of facial nerve monitoring during resections of the cerebellopontine angle tumors. The benefits of monitoring are evident in patients whose tumors alter local topographic relationships, form adhesions with surrounding nerves, and show enhanced texture and rich vasculature. Potential limitations of the hereby presented analysis include the use of our own systems for topographic classification of operated tumors, functional and neurophysiological assessment of the analyzed nerves and outcome of their identification. Therefore, comparison of our findings (albeit objective) with the results from other centers which do not use the intraoperative monitoring, can be inaccurate. Furthermore, comparison between our results and the data published by other authors can be hindered due to differences in technical skills of operators, resection strategies used and histopathological characteristics of analyzed tumors. 5. Conclusions (1) Neurophysiological monitoring of both oculomotor and abducens nerves is reflected by their successful intraoperative identification in most of the cases. (2) The use of neurophysiological monitoring for intraoperative identification of oculomotor nerve seems particularly important in the case of tumors with both extra- and intracavernous location, penetrating into the entire cavernous sinus. Moreover, the monitoring plays an important role in the identification of nerve VI in patients with intracavernous tumors. (3) Postoperative assessment of nerve III and VI based on neurophysiological monitoring has prognostic value with regard to the clinical status of these nerves on longterm follow-up. Conflict of interests The authors declare no conflict of interests. Financial disclosure The authors have no financing to disclose. References [1] Sekhar LN, Moller AR. Operative management of tumors involving the cavernous sinus. J Neurosurg 1986;64(June (6)):879–89. [2] Sekhar LN, Pomeranz S, Sen CN. Management of tumours involving the cavernous sinus. Acta Neurochir Suppl (Wien) 1991;53:101–12. [3] Sekhar LN, Sen CN, Jho HD, Janecka IP. Surgical treatment of intracavernous neoplasms: a four-year experience. Neurosurgery 1989;24(January (1)): 18–30. [4] Sekiya T, Hatayama T, Iwabuchi T, Maeda S. Intraoperative recordings of evoked extraocular muscle activities to monitor ocular motor nerve function. Neurosurgery 1993;32(February (2)):227–35. [5] Møller AR. Evoked potentials in intraoperative monitoring. Baltimore: Williams & Wilkins; 1988. [6] Møller AR. Intraoperative neurophysiological monitoring. Totowa, NJ: Humana Press; 2006. [7] De Jesus O, Sekhar LN, Parikh HK, Wright DC, Wagner DP. Long-term followup of patients with meningiomas involving the cavernous sinus: recurrence, progression, and quality of life. Neurosurgery 1996;39(November (5)): 915–20. [8] Weisz DJ, Sen C, Yang B. Neurophysiological monitoring during cavernous sinus surgery. In: Eisenberg MB, Al-Mefty O, editors. The cavernous sinus – a comprehensive text. Philadelphia: Lippincott Williams & Wilkins; 2000. p. 123–36. [9] Alberti O, Sure U, Riegel T, Bertalanffy H. Image-guided placement of eye muscle electrodes for intraoperative cranial nerve monitoring. Neurosurgery 2001;49(September (3)):660–4.
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[10] Grabb PA, Albright AL, Sclabassi RJ, Pollack IF. Continuous intraoperative electromyographic monitoring of cranial nerves during resection of fourth ventricular tumors in children. J Neurosurg 1997;86(January (1)):1–4. [11] Husain AM, Wright DR, Stolp BW, Friedman AH, Keifer JC. Neurophysiological intraoperative monitoring of the glossopharyngeal nerve: technical case report. Neurosurgery 2008;63(October (4 Suppl. 2)):277–8.
[12] Maurer J, Pelster H, Amedee RG, Mann WJ. Intraoperative monitoring of motor cranial nerves in skull base surgery. Skull Base Surg 1995;5(3): 169–75. [13] Sekiya T, Hatayama T, Shimamura N, Suzuki S. Intraoperative electrophysiological monitoring of oculomotor nuclei and their intramedullary tracts during midbrain tumor surgery. Neurosurgery 2000;47(November (5)):1170–7.
Contents lists available at ScienceDirect
Advances in Medical Sciences journal homepage: www.elsevier.com/locate/advms
Original Research Article
Usefulness of intraoperative monitoring of oculomotor and abducens nerves during surgical treatment of the cavernous sinus meningiomas Wojciech Kaspera a,*, Piotr Adamczyk a, Aleksandra S´laska-Kaspera b, Piotr Ładzin´ski a a b
Department of Neurosurgery, Medical University of Silesia, Regional Hospital, Sosnowiec, Poland Department of Laryngology, Medical University of Silesia, University Hospital, Katowice, Poland
A R T I C L E I N F O
A B S T R A C T
Article history: Received 26 May 2014 Accepted 28 August 2014 Available online 6 September 2014
Purpose: We analyzed the usefulness and prognostic value of intraoperative monitoring for identification of the oculomotor (III) and the abducens (VI) nerve in patients with cavernous sinus meningiomas. Material/methods: 43 patients diagnosed with cavernous sinus meningiomas were divided according to their topography. Function of the nerves was scored on original clinical and neurophysiological scales. Results: The percentage of nerves identified correctly with the monitoring was significantly higher (91% vs. 53% for nerve III and 70% vs. 23% for nerve VI, p < 0.001). The fractions of nerves III and VI identified correctly by means of the monitoring were significantly higher in the case of tumors with intra- and extracavernous location (89% vs. 32%, p < 0.01) and intracavernous tumors (80% vs. 20%, p < 0.05), respectively. The quality of post-resection recording correlated with functional status of both the nerves determined 9 months after the surgery (R = 0.51, p < 0.001 for nerve III and R = 0.57, p < 0.01 for nerve VI). Even a trace or pathological response to the post-resection stimulation was associated with improved functional status (90% vs. 50%, p < 0.05 for nerve III and 93% vs. 38%, p < 0.01 for nerve VI). Conclusions: Neurophysiological monitoring of ocular motor nerves enables their intraoperative identification during resections of the cavernous sinus meningiomas. Intraoperative monitoring of nerve III is particularly important in the case of tumors with extra- and intracavernous location, and the monitoring of nerve VI in the case of intracavernous tumors. The outcome of the post-resection monitoring has prognostic value with regard to the clinical status of the nerves on long-term follow-up. ß 2014 Medical University of Bialystok. Published by Elsevier Urban & Partner Sp. z o.o. All rights reserved.
Keywords: Cavernous sinus meningiomas Neurophysiological intraoperative monitoring Oculomotor nerve Abducens nerve
1. Introduction Progress in surgical technique resulted in increased radicality of skull base procedures. One example is surgical treatment of meningiomas located in the cavernous sinus and its surroundings. However, these procedures are still associated with the risk of injury to cranial nerves related to the cavernous sinus. Intraoperative neurophysiological monitoring, supporting visual identification of ocular motor nerves, constitutes one way of preventing such complications [1–4]. While the usefulness of the neurophysiological monitoring in facial nerve sparing was unambiguously confirmed in the case of resections of the cerebellopontine angle
* Corresponding author at: Department of Neurosurgery, Medical University of Silesia, Regional Hospital, Plac Medykow 1, 41-200 Sosnowiec, Poland. Tel.: +48 32 368 2551; fax: +48 32 368 2550. E-mail address: [email protected] (W. Kaspera).
tumors, there is no similar evidence with regard to tumors located in the cavernous sinus. Most of the sparse papers dealing with the problem in question [5,6] centered around the description of the methodology of monitoring itself. Moreover, the few available opinions in this matter are highly inconclusive [4,7,8]. For example, Weisz et al. [8] claimed that intraoperative monitoring is not associated with additional benefits due to specific anatomical relationships between the ocular motor nerves and tumor. However, Sekiya et al. [4] showed that the intraoperative monitoring facilitates identification of oculomotor (III) nerve, especially if the tumor alters normal anatomical relationships within the cavernous sinus. The results of this latter study might be confounded by the lack of statistical analysis [4]. The aim of this prospective study was to use statistical analysis in order to objectively verify the usefulness of neurophysiological monitoring for intraoperative identification of nerve III and abducens (VI) nerve. Moreover, having access to a relatively large (as for this type of tumors) sample of 43 operated patients, we
http://dx.doi.org/10.1016/j.advms.2014.08.009 1896-1126/ß 2014 Medical University of Bialystok. Published by Elsevier Urban & Partner Sp. z o.o. All rights reserved.
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analyzed the usefulness of this method in various topographic variants of the cavernous sinus tumors. Finally, we verified if the use of intraoperative monitoring influences clinically determined function of the nerves during long-term follow-up. 2. Patients and methods 2.1. Patients The study included the group of 43 consecutive patients (33 women and 10 men) aged between 22 and 74 years (mean age: 49.8 years), who were diagnosed with meningiomas located in the cavernous sinus or its surroundings. All the patients were treated at the Department of Neurosurgery, Medical University of Silesia in Sosnowiec between 2001 and 2011. Five topographic types of the tumors were identified on the basis of their localization documented on MRI: (1) intracavernous tumors (type A, Fig. 1a and b), (2) extracavernous tumors surrounding the cavernous sinus (type B, Fig. 1c and d), (3) tumors with both extra- and intracavernous location, penetrating into the anterior part of the cavernous sinus (type C, Fig. 1e and f), (4) tumors with both extraand intracavernous location, penetrating into the posterior part of the cavernous sinus (type D, Fig. 1 g and h), and (5) tumors with both extra- and intracavernous location, invading the entire cavernous sinus (type E, Fig. 1i and j). Functional status of nerves III and VI was determined one day prior to the surgery, at discharge from hospital, and during control visit 9 months after the surgery. The functional impairment of the nerves was graded on a 4-item scale: (I) normal status, (II) discrete paresis or subjectively reported impression of double vision without evident impairment of the eye globe motility, (III) severe paresis, and (IV) palsy. Although none of the patients showed isolated trochlear (IV) nerve palsy, functional deficits of this nerve accompanied disorders of nerve III and VI in some cases. 2.2. Intraoperative monitoring of nerves III and VI Monitoring was conducted with a 16/32 channel amplifier ISIS (Inomed Medizintechnik, Germany) exporting data to NeuroExplorer software. Recording needle electrodes were applied to muscles innervated by the monitored nerves: levator palpebrae superioris muscle or superior rectus muscle to monitor nerve III, and lateral rectus muscle for the purpose of nerve VI monitoring. A reference electrode was applied to the temporal muscle [9]. We eventually examined two nerves: nerve III located in the cavernous sinus wall, and nerve VI passing through the cavernous sinus. After several unsuccessful attempts we resigned from nerve IV monitoring. This decision was associated with difficulties in clinical interpretation of neurological deficits resulting from functional impairment of this nerve, as well as with problems with proper insertion of recording electrode into a small superior oblique muscle, or with selective stimulation of nerve IV located in close proximity of nerve III in the cavernous sinus wall. The nerves were stimulated with a 1.5–1.8 V direct current delivered via parallel or concentric electrodes. The amplitude of recording was considered as a principal criterion of muscular response. The result of identification was classified using a 4-item scale (from a to d): (a) both visual and electromyographic identification, (b) visual identification without electromyographic response,
Fig. 1. Topographic types of 43 analyzed meningiomas of the cavernous sinus. (a, b) Type A tumor, fibrosus meningioma located inside the left cavernous sinus; (c, d) type B tumor, mixed meningioma of the right large sphenoid wing, infiltrating layers of the lateral wall of the cavernous sinus; (e, f) type C tumor, syncytial meningioma involving the orbital cone, sphenoid sinus and anterior part of the right
cavernous sinus; (g, h) type D tumor, psammomatous meningioma involving the apex of the left temporal bone pyramid and superior part of the clivus, penetrating through the Meckel’s cavity toward the posterior part of the cavernous sinus; (i, j) type E tumor, psammomatous meningioma of the left cavernous sinus, penetrating toward the sella turcica, ethmoid sinus, medial parts of the temporal lobe, clivus and apex of the temporal bone pyramid.
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Fig. 2. (a, b) Normal recording of oculomotor (a) and abducens (b) nerve function with more than 1 mV amplitude; (c, d) abnormal, multiphasic recording of oculomotor nerve function (c) with amplitude below 0.5 mV, abnormal recording of abducens nerve function (d) with amplitude of about 0.6 mV, baseline amplitude of both nerves markedly exceeded 1 mV with subsequent more than a 50% decrease; (e, f) lack of response to stimulation: lack of response to oculomotor nerve stimulation other than stimulatory artifact (e), lack of recording of abducens nerve function (f) numerous artifacts that should not be interpreted as a recording of the nerve function.
(c) impossibility of visual identification with positive result of electromyographic testing, and (d) neither visual nor electromyographic identification. The functional neurophysiological impairment of nerves III and VI was assessed on a 3-item scale: (1) normal recording, i.e. evident spike with at least 0.5 mV baseline amplitude, (2) abnormal recording, i.e. a trace of response or evident (more than 50%) decrease in the amplitude as compared to the baseline level, and (3) lack of response to stimulation (Fig. 2). The postoperative examination was not conducted in one patient who died immediately after the surgery due to injury of internal carotid artery. Furthermore, we resigned from identification of nerve VI in three patients whose tumors infiltrated lateral walls of the cavernous sinus without penetration of its cavity (which corresponded to type B tumors). 2.3. Statistical analysis The results were analyzed with Statistica 5.5 package (StatSoft, United States) and Excel spreadsheet. Relationships between studied variables were analyzed with the Spearman’s rank correlation coefficients as well as with the McNemar’s test and Fisher’s exact test. The results of the testing were considered significant at p 0.05. 3. Results The proportions of nerves III identified accurately with and without an aid of neurophysiological monitoring were 39:43 and 23:43, respectively (91% vs. 53% correct identifications), and the analogous proportions of correctly identified nerves VI amounted to 28:40 and 9:40, respectively (70% vs. 23% correct identifications). The analysis for nerve VI did not include three patients in
whom this nerve was not identified intraoperatively. The fractions of oculomotor and abducens nerves that were identified correctly with an aid of neurophysiological monitoring turned out to be significantly higher than in the case of visual inspection (McNemar’s test, p < 0.001). Moreover, our analysis revealed that the percentage of oculomotor nerves that were identified correctly without the neurophysiological monitoring differed significantly depending on a topography of the tumor; the fraction of the correctly identified nerves was the highest in the case of intracavernous tumors (type A) and the lowest for both intra- and extracavernous tumors, that involved the whole cavernous sinus (type E) (Fisher’s exact test, p < 0.01; Table 1). In contrast, the percentage of oculomotor nerves Table 1 Number of oculomotor nerves that were correctly identified without an aid of neurophysiological monitoring in patients with various topographical types of the cavernous sinus tumor (Fisher’s exact test, p < 0.01). Visual identification (variant)
Topographic type of analyzed tumor A
B
C
D
E
Yes (a + b) No (c + d) Total
11 4 15
2 1 3
0 2 2
4 0 4
6 13 19
Total
23 20 43
A – intracavernous tumor, B – extracavernous tumor surrounding the cavernous sinus, C – tumor with both extra- and intracavernous location, penetrating into the anterior part of the cavernous sinus, D – tumor with both extra- and intracavernous location, penetrating into the posterior part of the cavernous sinus, E – tumor with both extra- and intracavernous location, invading the entire cavernous sinus; a – visual identification by an operator confirmed with electromyography, b – visual identification without electromyographic response, c – impossibility of visual identification with positive result of electromyographic testing, d – neither visual nor electromyographic identification.
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that were identified correctly on the basis of neurophysiological monitoring did not differ significantly between various topographic types of the tumors (Fisher’s exact test, p = 0.7). The topography of the tumor did not exert significant effect on the percentage of correctly identified nerves VI, either on neurophysiological monitoring or on visual inspection (Fisher’s exact test, p = 0.6 and p = 0.3, respectively). As type A and type E tumors predominated in our material, we analyzed possibility of identifying nerves III and VI in these two topographic variants. The use of monitoring was not reflected by an increase in the percentage of nerves III that were identified correctly in patients with type A tumors (McNemar’s test, p = 0.7). In the case of type E tumors, the proportions of nerves III that were identified correctly with and without an aid of neurophysiological monitoring amounted to 17:19 and 6:19, respectively (89% vs. 32% correct identifications). The percentage of nerves III that were identified correctly by means of monitoring turned out to be significantly higher than in the case of visual inspection (McNemar’s test, p < 0.01). The proportions of nerves VI that were identified correctly with and without monitoring in patients with type A tumors amounted to 12:15 and 3:15, respectively (80% vs. 20% correct identifications). The percentage of abducens nerves identified correctly with an aid of neurophysiological monitoring turned out to be significantly higher than in the case of visual inspection (McNemar’s test, p < 0.05). In contrast, the use of monitoring was not reflected by a significant increase in the percentage of correctly identified nerves VI in patients with type E tumors (McNemar’s test, p = 0.5). During the last stage of our analysis we verified a prognostic value of muscular response to stimulation of the ocular motor nerves. Using the 3-item scale of neurophysiological functional impairment, we analyzed a relationship between the outcome of postoperative nerve III stimulation and functional status of this nerve determined 9 months after the surgery (Table 2). One patient who died during perioperative period and two individuals in whom the nerve could not be identified, either visually or by means of monitoring (type d of identification), were excluded from the analysis. We showed that better postoperative recording was associated with better functional status of nerve III at control visit (Spearman’s rank correlation coefficient, R = 0.51, p < 0.001). Moreover, we verified if retaining any potential to transmission (the presence of either normal or abnormal postoperative recording) has any impact on improvement in functional status of nerve III between discharge from hospital and control examination 9 months after the surgery. The improvement in functional status of nerve III was defined as at least one point increase in the 4-item functional impairment scale. The analysis did not include patients without any functional deficits of nerve III
Table 2 Relationship between the outcome of postoperative neurophysiological recording of oculomotor nerve and functional status of this nerve determined 9 months after the surgery (Spearman’s rank correlation coefficient, R = 0.51, p < 0.001). Postoperative recording (variant)
Normal (1) Abnormal (2) Lacking (3) Total
Functional status of oculomotor nerve I
II
III
IV
12 7 5 24
3 1 3 7
0 0 1 1
0 1 7 8
Total
15 9 16 40a
a The analysis did not include one patient who died during perioperative period and two individuals in whom the nerve could not be identified, either visually or by means of monitoring (type d of identification); 1 – normal recording, i.e. evident spike with at least 0.5 mV baseline amplitude, 2 – abnormal recording, i.e. a trace of response or evident (more than 50%) decrease in the amplitude as compared to the baseline level, 3 – lack of response to stimulation.
Table 3 Relationship between the outcome of postoperative neurophysiological recording of abducens nerve and functional status of this nerve determined 9 months after the surgery (Spearman’s rank correlation coefficient, R = 0.57, p < 0.01). Postoperative recording (variant)
Normal (1) Abnormal (2) Lacking (3) Total
Functional status of abducens nerve
Total
I
II
III
IV
5 6 2 13
1 3 2 6
0 2 4 6
0 1 4 5
6 12 12 30a
a The analysis did not include one patient who died during perioperative period, three individuals who were not subjected to nerve VI identification, and nine persons in whom identification of this nerve was not possible (type d of identification). Legend as in Table 2.
at the time of discharge (n = 4) and one individual who died during perioperative period. The proportion of patients showing the improvement in the nerve function was 18:20 for the group with at least minimum response (either normal or abnormal one) to the stimulation, and 9:18 in those whose nerves did not respond to the postoperative stimulation or could not be identified (90% vs. 50% of patients with long-term improvement of the functional status of nerve III, Fisher’s exact test, p < 0.05). Also in the case of nerve VI, better postoperative recording was associated with better functional status determined 9 months after the surgery (Spearman’s rank correlation coefficient, R = 0.57, p < 0.01; Table 3). The analysis did not include one patient who died during perioperative period, three individuals who were not subjected to nerve VI identification, and nine persons in whom identification of this nerve was not possible (type d of identification). The proportion of patients who showed an improvement in the functional status of nerve VI during control examination taking place 9 months after the surgery was 14:15 for the group with retained normal or pathological response to stimulation, and 8:21 in persons whose nerves did not respond to the postoperative stimulation or could not be identified (93% vs. 38% of patients with improved functional status of nerve VI, Fisher’s exact test, p < 0.01). The analysis did not include one patient who died during perioperative period, three individuals who were not subjected to nerve VI identification, and another three persons who did not show any functional deficits of this nerve at the time of discharge. 4. Discussion Our findings suggest that neurophysiological monitoring plays an important role in the identification of ocular motor nerves during resection of tumors located in the cavernous sinus. Moreover, we showed that the outcome of nerve III and VI identification differs depending on a topographic type of the cavernous sinus meningioma. The tumors included in our analysis represented five topographic types (A–E). The type A tumors were intracavernous lesions, directly contacting or forming adhesions with nerve VI, but without involvement of nerve III. The type B–E tumors were located in the lateral wall of the cavernous sinus, contacted nerve III and invaded various compartments of the cavernous sinus; this group included type E tumors with both intra- and extracavernous location. We showed that correct visual identification of nerve III is possible in the case of tumors that penetrate inside the cavernous sinus (type A). Consequently, neurophysiological monitoring does not play an important role during identification of the nerve in patients with tumors of this type. The usefulness of nerve III monitoring is limited to tumors that are located outside the cavernous sinus and obstruct the view of the nerve (type E). Furthermore, the intraoperative monitoring
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turned out to be particularly important for identification of nerve VI in patients with tumors growing inside the cavernous sinus (type A). In contrast, the use of monitoring was not reflected by a significant increase in the percentage of nerves VI that were identified correctly in patients with type E meningiomas. Consequently, nerve III is more likely to be correctly identified in patients with intracavernous tumors due to possibility of its visual identification, additionally supported by neurophysiological monitoring. In contrast, the use of monitoring significantly increases probability of identifying this nerve in patients with tumors having both intra- and extracavernous location. In the case of nerve VI, the efficacy of monitoring is limited solely to the intracavernous masses. Moreover, we revealed that outcome of the monitoring is a prognostic factor of functional status of ocular motor nerves on long-term follow-up. Better outcome of the postoperative monitoring turned out to be associated with better functional status of the nerves determined 9 months after the surgery. Moreover, we showed that retaining even a trace potential to transmission is associated with significant improvement of the nerve function during control examination. The abovementioned findings are consistent with the data published by De Jesus et al. [7], according to whom implementation of cranial nerve monitoring constitutes one reason behind recently observed improvement in the outcomes of surgical treatment of the cavernous sinus meningiomas. Monitoring of response from ocular motor nerves, as well as monitoring of other motor cranial nerves, turned out to be efficient during brain stem tumors operations and other cranial base tumors resections, and as such is used for many years in a number of centers [10–13]. Also the benefits of facial nerve monitoring during resections for tumors of the cerebellopontine angle do not raise any controversies. However, the usefulness of neurophysiological monitoring of ocular motor nerves during resections of the cavernous sinus tumors is still put into question [4,8,12]. Resections of the cavernous sinus tumors do not belong to ‘‘standard’’ neurosurgical procedures and as such are performed in a small number centers, only few of which use intraoperative monitoring. Probably this represents the reason behind a paucity of published papers dealing with monitoring of ocular motor nerves during resections of the cavernous sinus tumors. Weisz et al. [8] questioned the benefits of intraoperative monitoring of ocular motor nerves. According to these authors, in the case of the cerebellopontine angle tumor resection (during which the efficacy of monitoring is unquestioned), the nerve is usually located outside the mass, rather than being surrounded by the latter, and its form can vary from a single unaltered trunk to a bunch of minute fibers. However, the situation is frequently different in the case of nerves located within the cavernous sinus. They can be dislocated, infiltrated or invaded by the tumor or, conversely, are completely independent from the mass. Therefore, the abovementioned authors concluded that while the nerves that are invaded or infiltrated by the tumor cannot be spared, those being visible for an operator do not require any neurophysiological monitoring [8]. To the best of our knowledge the paper published by Sekiya et al. [4] is the only one dedicated solely to the monitoring of ocular motor nerves. According to the authors of this paper, monitoring of ocular motor nerves is very useful, similar to the monitoring of facial nerve during resections for the vestibular schwannomas. Not only the authors emphasized the role of the monitoring in the identification of the nerve, but also highlighted its importance in confirming the result of visual inspection [4]. Consequently, the two contradictory opinions exist in literature; while some authors equal the usefulness of the ocular motor nerve monitoring during the operations for the cavernous sinus
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tumors to that of the facial nerve monitoring during resection of the cerebellopontine angle tumors, the others put it into question. In our opinion, however, both these attitudes are too radical. Monitoring of the ocular motor nerves is useful and as such should be recommended, but one should not expect the similar outcomes as in the case of facial nerve monitoring during resections of the cerebellopontine angle tumors. The benefits of monitoring are evident in patients whose tumors alter local topographic relationships, form adhesions with surrounding nerves, and show enhanced texture and rich vasculature. Potential limitations of the hereby presented analysis include the use of our own systems for topographic classification of operated tumors, functional and neurophysiological assessment of the analyzed nerves and outcome of their identification. Therefore, comparison of our findings (albeit objective) with the results from other centers which do not use the intraoperative monitoring, can be inaccurate. Furthermore, comparison between our results and the data published by other authors can be hindered due to differences in technical skills of operators, resection strategies used and histopathological characteristics of analyzed tumors. 5. Conclusions (1) Neurophysiological monitoring of both oculomotor and abducens nerves is reflected by their successful intraoperative identification in most of the cases. (2) The use of neurophysiological monitoring for intraoperative identification of oculomotor nerve seems particularly important in the case of tumors with both extra- and intracavernous location, penetrating into the entire cavernous sinus. Moreover, the monitoring plays an important role in the identification of nerve VI in patients with intracavernous tumors. (3) Postoperative assessment of nerve III and VI based on neurophysiological monitoring has prognostic value with regard to the clinical status of these nerves on longterm follow-up. Conflict of interests The authors declare no conflict of interests. Financial disclosure The authors have no financing to disclose. References [1] Sekhar LN, Moller AR. Operative management of tumors involving the cavernous sinus. J Neurosurg 1986;64(June (6)):879–89. [2] Sekhar LN, Pomeranz S, Sen CN. Management of tumours involving the cavernous sinus. Acta Neurochir Suppl (Wien) 1991;53:101–12. [3] Sekhar LN, Sen CN, Jho HD, Janecka IP. Surgical treatment of intracavernous neoplasms: a four-year experience. Neurosurgery 1989;24(January (1)): 18–30. [4] Sekiya T, Hatayama T, Iwabuchi T, Maeda S. Intraoperative recordings of evoked extraocular muscle activities to monitor ocular motor nerve function. Neurosurgery 1993;32(February (2)):227–35. [5] Møller AR. Evoked potentials in intraoperative monitoring. Baltimore: Williams & Wilkins; 1988. [6] Møller AR. Intraoperative neurophysiological monitoring. Totowa, NJ: Humana Press; 2006. [7] De Jesus O, Sekhar LN, Parikh HK, Wright DC, Wagner DP. Long-term followup of patients with meningiomas involving the cavernous sinus: recurrence, progression, and quality of life. Neurosurgery 1996;39(November (5)): 915–20. [8] Weisz DJ, Sen C, Yang B. Neurophysiological monitoring during cavernous sinus surgery. In: Eisenberg MB, Al-Mefty O, editors. The cavernous sinus – a comprehensive text. Philadelphia: Lippincott Williams & Wilkins; 2000. p. 123–36. [9] Alberti O, Sure U, Riegel T, Bertalanffy H. Image-guided placement of eye muscle electrodes for intraoperative cranial nerve monitoring. Neurosurgery 2001;49(September (3)):660–4.
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[10] Grabb PA, Albright AL, Sclabassi RJ, Pollack IF. Continuous intraoperative electromyographic monitoring of cranial nerves during resection of fourth ventricular tumors in children. J Neurosurg 1997;86(January (1)):1–4. [11] Husain AM, Wright DR, Stolp BW, Friedman AH, Keifer JC. Neurophysiological intraoperative monitoring of the glossopharyngeal nerve: technical case report. Neurosurgery 2008;63(October (4 Suppl. 2)):277–8.
[12] Maurer J, Pelster H, Amedee RG, Mann WJ. Intraoperative monitoring of motor cranial nerves in skull base surgery. Skull Base Surg 1995;5(3): 169–75. [13] Sekiya T, Hatayama T, Shimamura N, Suzuki S. Intraoperative electrophysiological monitoring of oculomotor nuclei and their intramedullary tracts during midbrain tumor surgery. Neurosurgery 2000;47(November (5)):1170–7.
