Factors Associated With Abducens Nerve Palsy in Patients Undergoing Surgery for Petroclival Meningiomas

Background: During the surgical resection of petroclival meningiomas, preserving the cranial nerves is crucial. The abducens nerve is particularly vulnerable during surgery. However, the preoperative risk factors and postoperative prognosis of abducens nerve palsy (ANP) are poorly understood. Methods: We retrospectively analyzed 70 patients who underwent surgery for petroclival meningiomas between May 2010 and December 2019, divided into gross-total resection (GTR) and subtotal resection (STR) groups. The relationship of preoperative clinical factors with the incidence and recovery of postoperative ANP was analyzed. Results: Postoperative ANP was observed in 23 patients (32.9%). Multivariable logistic regression revealed that the tumor-to-cerebellar peduncle T2 imaging intensity index (TCTI) (P < 0.001) and internal auditory canal invasion (P = 0.033) contributed to postoperative ANP. GTR was achieved in 37 patients (52.9%), and 10 (27.0%) of them showed ANP. STR was achieved in 33 patients (47.1%), and 13 (39.4%) of them showed ANP. Recovery from ANP took a median of 6.6 months (range, 4.5-20.3 months). At 6 months after the operation, recovery of the abducens nerve function was observed in 16 patients (69.0%); of whom, 4 (40.0%) were in the GTR group and 12 (92.3%) were in the STR group (P = 0.025). Conclusions: TCTI and internal auditory canal invasion were the risk factors for postoperative ANP. Although intentional STR did not prevent ANP immediately after the operation, recovery of the abducens nerve function after surgery was observed more frequently in the STR group than in the GTR group.

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Factors Associated With Abducens Nerve Palsy in Patients Undergoing Surgery for Petroclival Meningiomas Jihwan Yoo, MD, Seung Hun Lim, MD, In-Ho Jung, MD, Hun Ho Park, MD, Jinu Han, MD, PhD, Chang-Ki Hong, MD, PhD Background: During the surgical resection of petroclival meningiomas, preserving the cranial nerves is crucial. The abducens nerve is particularly vulnerable during surgery. However, the preoperative risk factors and postoperative prognosis of abducens nerve palsy (ANP) are poorly understood. Methods: We retrospectively analyzed 70 patients who underwent surgery for petroclival meningiomas between May 2010 and December 2019, divided into gross-total resection (GTR) and subtotal resection (STR) groups. The relationship of preoperative clinical factors with the incidence and recovery of postoperative ANP was analyzed. Results: Postoperative ANP was observed in 23 patients (32.9%). Multivariable logistic regression revealed that the tumor-to-cerebellar peduncle T2 imaging intensity index (TCTI) (P , 0.001) and internal auditory canal invasion (P = 0.033) contributed to postoperative ANP. GTR was achieved in 37 patients (52.9%), and 10 (27.0%) of them showed ANP. STR was achieved in 33 patients (47.1%), and 13 (39.4%) of them showed ANP. Recovery from ANP took a median of 6.6 months (range, 4.5–20.3 months). At 6 months after the operation, recovery of the abducens nerve function was observed in 16 patients (69.0%); of whom, 4 (40.0%) were in the GTR group and 12 (92.3%) were in the STR group (P = 0.025). Conclusions: TCTI and internal auditory canal invasion were the risk factors for postoperative ANP. Although intentional STR did not prevent ANP immediately after the operation, Department of Neurosurgery (JY, SHL, IHJ, HHP), Brain Tumor Center, Gangnam Severance Hospital, Yonsei University, Seoul, Korea; Yonsei University College of Medicine (JY), Seoul, Republic of Korea; Department of Ophthalmology (JH), Gangnam Severance Hospital, Yonsei University, Seoul, Republic of Korea; and Department of Neurosurgery (CKH), Asan Medical Center, University of Ulsan, College of Medicine, Seoul, Republic of Korea. The authors report no conflicts of interest. The data that support the findings of this study are available from the corresponding author (C.K.H.) upon reasonable request. Informed consent was obtained from the patients under relevant guidelines and regulations. Patients signed informed consent regarding publishing their data and photographs. Address correspondence to Chang-Ki Hong, MD, PhD, Department of Neurosurgery, Brain Tumor Center, Gangnam Severance Hospital, Yonsei University, 20, Eonju-ro-63-gil, Gangnam-gu, Seoul 06229, Korea; E-mail: [e-mail] Yoo et al: J Neuro-Ophthalmol 2022; 42: e209-e216 recovery of the abducens nerve function after surgery was observed more frequently in the STR group than in the GTR group. Journal of Neuro-Ophthalmology 2022;42:e209–e216 doi: 10.1097/WNO.0000000000001473 © 2021 by North American Neuro-Ophthalmology Society O perative treatment of petroclival meningiomas (PCMs) is a neurosurgical challenge. It involves the gross-total resection of the tumor along with the preservation of complex neurovascular structures at the skull base (1–4). Proximity to the brainstem, adhesion to cranial nerves (CNs) and major vessels, and narrow surgical corridors can cause high postoperative morbidity and mortality (5,6). Advances in surgical equipment and techniques have led to a gradual improvement in the postoperative outcome in patients with PCM, but it is still difficult to overcome these challenges completely. Among the various CN injuries that can occur during PCM surgery, abducens nerve palsy (ANP) is the most frequently observed extraocular muscle disorder, and it occurs in approximately 6.9%–38.7% of all PCM surgeries (7–13). Because the abducens nerve has a long intracranial portion, it is easily damaged by a subtle injury mechanism involving stretching during PCM surgery (13). This injury consequently limits the abduction function of the patient’s eye, causing strabismus and diplopia (14). Reports indicate that some anatomical sites are more prone to these injuries, and the risk may vary depending on the histology of the tumor (15). Thus, preoperative tumor histology, size, location, and relative relationship to the adjacent neurovascular structures may be important in predicting the risk of postoperative nerve deficits. Few studies have analyzed the preoperative prognostic factors for ANP (14,16). These studies have reported risk factors including whether the tumor exceeded the midline, whether the infratrigeminal area was exposed, and whether e209 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution adhesion between the tumor and nerves persisted (14). However, previous investigations of various bone structures and radiologic parameters observed in MRI have been insufficient, and the number of patients enrolled in these studies was very small; thus, the application of statistical analysis in these studies was limited. Accordingly, in this study, we attempted to elucidate the factors associated with ANP during PCM surgeries and observe the natural history of ANP recovery. METHODS In this retrospective study, we included consecutive patients newly diagnosed with World Health Organization Grade I petroclival meningiomas at the Gangnam Severance hospital between May 2010 and December 2019. Petroclival meningioma was defined as a tumor that originates in the petroclival junction medial to the fifth CN. Procedures were conducted in our hospital by 2, senior, highly experienced surgeons using neuronavigation (Stealth S8 system, Medtronic, Dublin, Ireland, and Navigation system II, Stryker, MI). Seventy patients were identified, and their data, including demographics, clinical presentation, pathological diagnosis, radiological features, and intraoperative findings, were collected from electronic medical records. Radical resections were performed to minimize brainstem and CN injury. If the adhesion was too severe or the risk of CN injury was too high, a deliberate subtotal resection (STR) was performed. We excluded patients with preoperative diplopia or strabismus, a history of brain surgery, those who had not undergone surgery, those with a follow-up period of ,1 year, and those lost to follow-up. We recorded the status of ANP in all patients. The degree of ANP was documented preoperatively and postoperatively with the aid of ophthalmologists. The ophthalmic examination was performed immediately after the operation and again at 3 and 6 months after the operation. Ethical Approval This retrospective study conformed to the ethical guidelines of the 1975 Declaration of Helsinki and its later amendments and was approved by the Institutional Review Board of Severance Hospital, Yonsei University College of Medicine, Seoul, Republic of Korea (3-2021-0007). The patients’ information was anonymized and deidentified before analysis. Radiologic Parameter Analysis We measured the signal density of a region-of-interest in T2 image using an apparent diffusion coefficient map to determine tumor consistency (17,18). The signal density is a relative value; thus, the comparison of T2 values between patients was based on the tumor-to-cerebellar peduncle T2 imaging intensity (TCTI) ratio as described by Smith et al. (17) Additionally, we retrospectively reviewed images from all patients and determined cavernous e210 sinus invasion, brainstem compression (confirmed by shape), brainstem edema (confirmed by a high signal in the brainstem on T2 image), and internal auditory canal (IAC) invasion. The location of the tumor was classified into either petrous dominant (. 50% lateral to the trigeminal nerve) or clivus dominant (. 50% medial to the trigeminal nerve) (Fig. 1) (2,19,20). The extent of resection was evaluated based on postoperative MRI, and gross-total resection (GTR) was defined as no residual enhancing lesion on the postoperative MRI. STR was confirmed based on operative findings and postoperative MRI as a remnant contrast-enhancing tumor. Measurement of Abducens Nerve Palsy The functional evaluation of ANP was measured according to the Scott–Kraft score by an independent ophthalmologist (J.H.) (Fig. 2) (21). The score is an integer from 1 to 6, depending on the extraocular muscle, where 6 is normal, 3–5 indicates partial palsy (strabismus), and 1–2 indicates complete palsy. Each patient’s score was evaluated preoperatively, immediately post operation, and 3 and 6 months postoperatively. Ophthalmic surgery was performed if diplopia persisted without any improvement at 6 months postoperatively. Statistical Analysis Fisher exact test and the x2 test were used to compare demographics between the STR and GTR groups. To assess the risk factors for ANP, a logistic regression test was performed. Variables showing a P value of ,0.2 in the univariable logistic regression test were included in a multivariable logistic regression test. Two methods were used to represent the recovery pattern. We first compared the degree of strabismus between the GTR group and the STR group in preoperative, postoperative, postoperative 3 months, and postoperative 6 months by chi-squared test. Second, reverse Kaplan–Meier curve was used to observe continuous time and recovery, and recovery was defined as no grossly observed strabismus (Scott–Kraft score 6). All tests were conducted using SPSS version 23 (IBM, Armonk, NY), and P , 0.05 was considered statistically significant. RESULTS Demographics of the patients are shown in Table 1. In total, 70 patients were included; of whom, 37 (52.9%) were from the GTR group and 33 (47.1%) were from the STR group. Sixty-one patients were female. Eighty percent of the patients demonstrated preoperative symptoms. Radiological features, including the tumor diameter, TCTI index, midline crossing, cavernous sinus invasion, brainstem compression, brainstem edema, and IAC invasion, are documented in Table 1. IAC invasion was observed in 35 patients (50.0%), and brainstem compression was observed in .80% of the patients; however, signal changes in the brainstem were only observed in 10 patients (14.3%). The overwhelming majority of tumors were Yoo et al: J Neuro-Ophthalmol 2022; 42: e209-e216 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 1. Comparative examples representing each variable, including the extent of resection, internal auditory canal invasion, brainstem edema, cavernous sinus invasion, and brainstem compression. White arrowheads indicate that these variables are observed on MRI. The white arrow indicates remnant tumor postoperatively. FIG. 2. Schematic illustration indicating the degree of abducens nerve palsy. Scott–Kraft score 1–2: complete abducens nerve palsy, 3–5: incomplete (partial) abducens nerve palsy, and 6: normal. Yoo et al: J Neuro-Ophthalmol 2022; 42: e209-e216 e211 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution diagnosed as meningothelial meningiomas on pathology, followed by transitional, secretory, and fibrous meningiomas. TABLE 2. Univariate logistic regression analysis of factors associated with abducens nerve palsy Univariate Logistic Regression Model of Factors Associated with Abducens Nerve Palsy Univariable analysis was performed using a logistic regression model for all the measured continuous and categorical variables. Sex, TCTI index, diameter, and IAC invasion showed statistical significance (P , 0.2) (Table 2). These factors were then entered into a multivariable analysis, and the TCTI index and IAC invasion retained statistical significance. The odds ratios (ORs) of the variables are shown in Table 3. The TCTI index was a continuous variable with an OR of 0.001. The higher the T2 intensity of the tumor compared with the T2 intensity of the cerebellar peduncle, the lower the risk. Prognosis of Abducens Palsy After Surgery Twenty-three patients showed ANP immediately after surgery; of whom, 10 patients underwent GTR, and the remaining underwent STR (Fig. 3). The median time to full TABLE 1. Patient demographics N = 70 Age (yr) (mean, range) Sex (n, %) Female Male Follow-up period (months) (mean, range) Preoperative symptoms (n, %) Headache Facial sensory change Hearing impairment Duration of symptoms (months) (mean, range) Postoperative abducens nerve palsy (n, %) Tumor size* (mm) (mean, range) TCTI index Crossing the midline (n, %) Cavernous sinus invasion (n, %) IAC invasion (n, %) Brainstem compression (n, %) Brainstem edema (n, %) EOR (n, %) Subtotal Gross total Pathology (n, %) Meningothelial Secretory Transitional Fibrous 52.5 (32–84) 61 (87.1%) 9 (12.9%) 42.9 (12.4–118.3) 56 33 19 11 7.4 (80.0%) (54.1%) (31.1%) (18.0%) (0.4–60.0) 23 (32.9%) 35.6 1.11 18 21 35 58 10 (9–68) (0.29–1.99) (25.7%) (30.0%) (50.0%) (82.9%) (14.3%) 33 (47.1%) 37 (52.9%) 63 4 2 1 (90.0%) (5.0%) (2.8%) (1.2%) *Tumor size was defined as the largest diameter. EOR, extent of resection; IAC, internal auditory canal; TCTI, tumor-to-cerebellar peduncle T2 imaging intensity. e212 Age Sex Male Female Symptom No Yes Duration TCTI index ADC (s/mm2) Diameter (mm) EOR GTR STR CS invasion No Yes Stem compression No Yes Stem edema No Yes IAC invasion No Yes OR 95% CI 1.002 0.951–1.056 1.000 0.222 0.023–1.890 P 0.926 0.168 0.376 1.000 1.721 1.008 0.001 1.001 1.034 0.517–5.724 0.970–1.048 0.000–0.020 0.997–1.005 0.992–1.077 1.000 1.755 0.641–4.804 0.685 , 0.001 0.731 0.113 0.274 0.542 1.000 1.395 0.478–4.066 0.527 1.000 1.579 0.384–6.496 0.836 1.000 0.857 0.200–3.673 0.025 1.000 3.368 1.164–9.744 ADC, apparent diffusion coefficient; CI, confidence interval; CS, cavernous sinus; IAC, internal auditory canal; OR, odds ratio; TCTI, tumor-to-cerebellar peduncle T2 imaging intensity. recovery without surgical assistance was 6.6 months (range, 4.5–20.3 months). Immediately after the operation, complete palsy was observed in 10 patients (76.9%) in the STR group and 8 patients (80.0%) in the GTR group (P . 0.999). At 3 months after the operation, complete palsy was observed in 7 patients (53.8%) in the STR group TABLE 3. Multivariate logistic regression analysis of factors associated with abducens nerve palsy Multivariate OR Sex M F TCTI index Diameter (cm) IAC invasion No Yes 95% CI P 0.219 1.000 0.219 0.001 0.969 0.006–3.183 0.000–0.012 0.893–1.051 1.000 10.436 1.205–90.349 ,0.001 0.450 0.033 CI, confidence interval; IAC, internal auditory canal; OR, odds ratio; TCTI, tumor-to-cerebellar peduncle T2 imaging intensity. Yoo et al: J Neuro-Ophthalmol 2022; 42: e209-e216 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution and 6 patients (60.0%) in the GTR group. At 6 months after surgery, complete palsy was observed in 5 patients (38.5%) in the STR group and 6 patients (60.0%) in the GTR group. Functional recovery of the abducens nerve based on Scott–Kraft scores was observed in 12 patients (92.3%) in the STR group and 4 patients (40.0%) in the GTR group at 6 months after surgery (P = 0.025). We found a statistically significant tendency to observe the functional recovery of the abducens nerve more often in the STR group than in the GTR group (Fig. 4A). However, statistical significance was not reached in the reverse Kaplan–Meier curve, which recorded recovery incidence over time (P = 0.296) (Fig. 4B). CONCLUSIONS In this study, we focused on the abducens nerve, which is involved in eye movement and is most easily damaged during PCM surgery (8), and we investigated the factors related to such damage and the natural course of ANP. We found that preoperative MRI revealed an increased risk of injury with low TCTI index or IAC invasion of the tumor. Spontaneous recovery was more likely if the patient showed partial palsy immediately or 6 months after surgery, or if they showed a tendency to recover within 6 months. For spontaneous recovery, the median period was 6.6 months (maximum, 20.3 months). When STR was attempted due to adhesion between the tumor and adjacent structures, the incidence of ANP did not decrease immediately after surgery. However, recovery at 6 months was observed more frequently in the STR group than in the GTR group. Tumor consistency is well known to be an important factor that can cause CN deficit in PCM surgery, and fibrous consistency is known to increase postoperative morbidity (22–25). Therefore, various analyzes were attempted to predict tumor consistency before surgery using MRI (26). According to Yao et al, T1 image did not provide diagnostic or prognostic value, and 11 of the 14 references suggest that there was a strong correlation between T2 signal intensity and tumor consistency (26). However, the limitation of most studies is that tumor consistency is classified as firm or soft in a dichotomous manner (27). The results of this study show that the lower the TCTI index, that is, the lower the relative T2 intensity of the tumor, the higher the risk of CN injury. These results, consistent with existing studies, show that the TCTI index well reflects the tumor consistency and that the firm consistency increases the CN injury during PCM surgery. IAC Invasion is not reported to be associated with postoperative cranial journalism in general meningioma surgeries (28,29). Agarwal et al reported that there was no association between IAC invasion and CN deficit in 34 cerebellopontine angle meningioma surgeries (29). In addition, Peraio et al reported that tumor removal with intracranial IAC drilling did not increase the risk of CN injury in a study reporting the surgical results of posterior fossa FIG. 3. Functional recovery in patients with petroclival meningioma and postoperative abducens nerve palsy. White, light blue, and blue represent the severity of abducens nerve palsy in the gross-total resection group. Light red and red represent the severity of abducens nerve palsy in the subtotal resection group. The white, light blue, and blue columns represent normal, partial palsy, and complete palsy, respectively. Yoo et al: J Neuro-Ophthalmol 2022; 42: e209-e216 e213 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 4. Recovery patterns by the extent of resection. A. Recovery patterns at each follow-up period by gross-total resection (GTR) group and subtotal resection (STR) group. Functional recovery of the abducens nerve was observed in 12 patients (92.3%) in the STR group and 4 patients (40.0%) in the GTR group (P = 0.025). There was a statistically significant tendency to observe the functional recovery of the abducens nerve more often in the STR group than in the GTR group. B. Reverse Kaplan–Meier curve by GTR group and STR group. Recovery with continuous time variables was recorded, and no statistical significance was found between the 2 groups (P = 0.296). meningioma in 174 patients (28). Therefore, in this study, we found an increased risk of ANP in PCM surgery, probably because the IAC is very close to the Dorellos canal and the risk of nerve damage during tumor manipulation is increased rather than the IAC invasion itself is dangerous (30–32). Thin-slice MRI is required to observe the anatomical relationship between the tumor, IAC, and Dorellos canal. Fast imaging employing steady-state acquisition or proton density-weighted MRI could be helpful as a representative imaging protocol (33,34). Thin-slice MRI allows good observation of the interdural segment of Dorello canal (34). If the tumor invades this structure, abducens nerve injury is likely to occur during surgery. Such neural damage is mainly observed at the point where the nerve enters the dura; it is often difficult to find the nerve endings and requires great care, as it is not possible to use the suture technique. The dural insertion point is hypothetically the most vulnerable because the neural angle is made acute by the tumor (Fig. 5). During PCM surgery, damage to the abducens nerve is virtually inevitable, but there are very few reports on the recovery stages of abducens nerve injury. Sekhar et al reported reconstruction experiences after the transection of the abducens nerve in 7 patients (35). One of the 2 patients who underwent suturing and 1 of the 5 patients who underwent nerve grafting had a good prognosis (2/7 patients; 28.6%), but the remaining patients reported no clinical improvement. Sawamura et al also reported that they experienced abducens nerve transection in the prepontine cistern and reported a good prognosis after reconnection (36). However, if PCM is present, the abducens nerve is degenerated, thinned, and fragile, and if invaded by the tumor, reconnection per se may be difficult posttransection. ANP can occur without transection, caused by demyelination, axoplasmic flow worsening, and vascular insufficiency of e214 the nerve (37). Paradoxically, these processes may be the basis for late recovery, even if nerve continuity is maintained after the surgical removal of the intracranial lesion causing the ANP. Moreover, even when transection does not occur during surgery, demyelination and vascular insufficiency caused by microinjury may be the cause. This theory can be supported clinically by the fact that even after STR in this study, the incidence of ANP did not decrease immediately, but it recovered more frequently. Borghei-Razavi et al, in a study analyzing tumors located in 40 petroclival areas, suggested that CN damage frequency differs according to tumor pathology (38). However, when analyzing the relationship between tumor origin and the abducens nerve, no statistical significance was found. According to a report by Shono et al, ANP was found in 9 of 240 patients (3.75%) with tumors in the skull base. The prognosis was poor when the pathological finding was FIG. 5. Schematic illustration of abducens nerve transposition by the tumor. The dural insertion point is shown to be the most vulnerable point. Yoo et al: J Neuro-Ophthalmol 2022; 42: e209-e216 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution meningioma (16). Additionally, a systematic review by Di Carlo et al reported that approximately 8% of patients experienced early ANP, and 3.6% experienced late ANP (8). Among CNs, the most common palsy was that of the facial nerve (13.9%). Among the 3 nerves related to eye movement, ANP was the most common, and results differed according to the surgical technique. In particular, when the petrosal approach (including anterior and posterior approaches) was implemented, ANP was highly frequent. Additionally, according to Schneider et al, if the postoperative Mib-1 score was $5, the possibility of a new CN deficit was marked (39). Even if surgical preparation considers the physical relationship between the tumor and the nerve, the risk may vary depending on the nature of the approach or the tumor itself. This study had some limitations. First, it was a retrospective review. Second, considering that PCM is a rare disease, the small sample size in this study may not provide statistically significant differences. Third, the analysis of the recovery of ANP based on a 6-month follow-up period may not be enough; longer-term follow-up of ophthalmic data may be necessary. Finally, because we did not analyze pathological supplementary data, such as the data regarding Ki-67, no associations of this type were investigated. Nevertheless, no previous study has attempted to predict ANP based on MRI before surgery, and this study is among those with the largest number of such patients and may provide a comprehensive representation of the relevant information to patients and neurosurgeons dealing with PCM. In closing, managing ANP is crucial concerning the quality of life of patients with PCM. When treating PCMs, it is recommended that surgeons carefully review radiological factors, such as the TCTI index and IAC invasion, before surgery. Although intentional STR does not appear to prevent the occurrence of ANP immediately after surgery, it could be attempted for late recovery. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: J. Yoo, S. H. Lim, and C. K. Hong; b. Acquisition of data: J. Yoo, S. H. Lim, I. H. Jung, and J. Han; c. Analysis and Interpretation of Data: J. Yoo, S. H. Lim, and I. H. Jung. Category 2: a. Drafting the manuscript: J. Yoo, S. H. Lim, and C. K. Hong; b. Revising it for intellectual content: H. H. Park. Category 3: Final approval of the completed manuscript: J. Yoo and C. K. Hong. ACKNOWLEDGMENTS The authors thank MID (Medical Illustration & Design) for providing excellent support with the medical illustration. The authors also thank Editage (www.editage.co.kr) for English language editing. The results of this study were Yoo et al: J Neuro-Ophthalmol 2022; 42: e209-e216 presented at the annual meeting of the Korean Skull Base Society in November 2020. REFERENCES 1. 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