Title | Visual Outcomes in Surgically Treated Intracranial Meningiomas |
Creator | Yibing Zhang, BA; John Kim, MD; Chris Andrews, PhD; Erica Archer, MD; Lulu Bursztyn, MD; Hilary Grabe, MD; Edward Margolin, MD; Stephen Sullivan, MD; Jonathan Trobe, MD |
Affiliation | Department of Ophthalmology and Visual Sciences (Kellogg Eye Center) (YZ, CA, EA, LB, HG, EM, JT); Department of Radiology (Neuroradiology) (JK); Department of Neurosurgery (SS, JT); and Department of Neurology (JT), University of Michigan |
Abstract | Intracranial meningiomas that arise from the medial sphenoid ridge, anterior clinoid process, tuberculum sellae, or planum sphenoidale often impair vision by compressing the optic nerves and optic chiasm. Although many studies have reported visual outcome following surgery for these tumors, documentation has often been incomplete and not validated by patient self-report. |
Subject | Intracranial Meningiomas; Visual Impairment; Optic Nerve Compression |
OCR Text | Show Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Visual Outcomes in Surgically Treated Intracranial Meningiomas Yibing Zhang, BA, John Kim, MD, Chris Andrews, PhD, Erica Archer, MD, Lulu Bursztyn, MD, Hilary Grabe, MD, Edward Margolin, MD, Stephen Sullivan, MD, Jonathan Trobe, MD Background: Intracranial meningiomas that arise from the medial sphenoid ridge, anterior clinoid process, tuberculum sellae, or planum sphenoidale often impair vision by compressing the optic nerves and optic chiasm. Although many studies have reported visual outcome following surgery for these tumors, documentation has often been incomplete and not validated by patient self-report. Methods: Retrospective study of 40 patients drawn from a single, academic, medical center. We used a unique method of assessing visual outcome based on whether the change in visual function affected the preoperatively better-sighted or worse-sighted eye in the belief that this method would correlate with effects on activities of daily living (ADL). To elicit patient self-reports of those effects, we conducted telephone interviews of 25 patients with a standard questionnaire. We also assessed putative ophthalmic, imaging, and surgical predictors of visual outcome. Results: Visual improvement occurred in 61% of patients with preoperative monocular visual dysfunction, but only 22% of patients reported improvement in their ability to conduct ADL, and 17% lost vision. Visual outcomes were better in patients with preoperative binocular visual dysfunction, where visual improvement occurred in 73% and no patient lost vision in the preoperatively bettersighted eye. However, only 27% of patients with preoperative binocular visual dysfunction reported improvement in their ability to conduct ADL. Long duration of vision impairment, presence of optic disc pallor, large tumor size, and imaging-based preoperative optic canal involvement did not preclude a favorable visual outcome. Department of Ophthalmology and Visual Sciences (Kellogg Eye Center) (YZ, CA, EA, LB, HG, EM, JT); Department of Radiology (Neuroradiology) (JK); Department of Neurosurgery (SS, JT); and Department of Neurology (JT), University of Michigan. The authors report no conflicts of interest. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www. jneuro-ophthalmology.com). Address correspondence to Jonathan D. Trobe, MD, Department of Ophthalmology and Visual Science, Kellogg Eye Center, University of Michigan, 1000 Wall Street, Ann Arbor, MI 48105; E-mail: jdtrobe@ umich.edu. e548 Aggressive surgical reduction in displacement of the optic nerves was not necessary to obtain a favorable visual outcome and sometimes led to an unfavorable visual outcome. Conclusions: In this study, surgery often improved vision, especially in patients with preoperative binocular visual dysfunction. But patients indicated that the effect on their ability to perform ADL was more modest. Moreover, 17% of patients with preoperative monocular visual dysfunction lost vision in the only affected eye, often to a considerable degree. In those patients, surgery would be justified primarily to relieve the concern of having a large brain tumor and to prevent tumor growth. Preoperative ophthalmic and imaging features poorly predicted visual outcomes. Favorable visual outcomes occurred without aggressive surgical debulking of the tumors. Journal of Neuro-Ophthalmology 2021;41:e548–e559 doi: 10.1097/WNO.0000000000001205 © 2021 by North American Neuro-Ophthalmology Society I ntracranial sphenoid meningiomas, which account for 3%–10% of intracranial meningiomas (1), may impair vision by compressing the optic nerves or optic chiasm. Favorable postoperative visual outcomes have varied from 40% to 65% and unfavorable outcomes from 17% to 40% (2–9), but data on visual outcomes have been incomplete, nonuniform, and not validated by patient self-report (2–20). Although patient age and sex, duration of visual symptoms, preoperative visual function, optic disc pallor, preoperative tumor size, site of tumor origin, tumor involvement of the optic canal, imaging evidence of an intact arachnoid membrane, tumor adhesion to the vision pathway, and peritumoral edema have been suggested as predictors of visual outcome (2,3,5–9,11–19), none has been consistently verified. Studies have been limited by small patient cohorts (2,5,7–13,16,19,21), inadequate visual function data (2,3,7,11,12,14,15,17,22), lack of highresolution imaging, and lack of imaging-based confirmation of the extent of surgical extirpation. Zhang et al: J Neuro-Ophthalmol 2021; 41: e548-e559 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution This study was undertaken to provide more robust information about the effect of surgery on visual outcome. We used a novel system of determining visual outcome according to whether the patient had preoperative monocular or binocular visual dysfunction. We carried out telephone interviews of most of the patients to obtain their perceptions of the impact of surgery on their ability to perform activities of daily living (ADLs). We also investigated ophthalmic, imaging, and surgical predictors of visual outcome. METHODS The medical records of the Neuro-Ophthalmology Clinics of Michigan Medicine from 2006 to 2019 were searched for patients who had undergone surgery for meningiomas that caused compressive dysfunction of the optic nerves or optic chiasm. Patients were included only if they had undergone the surgery at our institution and had thorough preoperative ophthalmic records, high-quality preoperative and postoperative MRIs, complete operative notes, and clinical and imaging follow-up for at least 6 months after the surgery. We excluded 7 patients who had permanent postoperative complications (including 5 with stroke and 2 with operative site hemorrhage that required reoperation), postoperative radiation therapy, medical comorbidities that might affect vision, or brain abnormalities that might confound imaging interpretation. The assessments of visual acuity and visual field were drawn from the last neuro-ophthalmic encounter, which occurred at a minimum of 6 months after the surgery. Where patients had multiple assessments of postoperative visual function at least 6 months after the surgery, we did not find any meaningful changes. The following information was extracted from the electronic medical records: (1) patient demographics; (2) dates of diagnosis and surgery; (3) preoperative and postoperative best-corrected visual acuity and Humphrey visual field mean deviations, and presence of preoperative optic disc pallor; (4) preoperative imaging-based tumor size, site of origin, signal characteristics, degree of optic nerve or optic chiasm displacement by tumor, presence of tumor at the intracranial opening of the optic canal, and tumor invasion of the orbit; (5) postoperative imaging-based tumor size reduction, change in the amount of displacement of the optic nerves and optic chiasm, presence of tumor at the intracranial opening of the optic canal, and tumor invasion of the orbit; (6) date of surgery; (7) identity of the surgeon; (8) surgical approach; (9) operative notes regarding the surgeon’s approach to portions of the tumor extending into the intracranial opening of the optic canal; (10) intraoperative and postoperative complications. The study neuro-radiologist (J.K.), who was masked as to visual outcome, reviewed all preoperative and postoperative brain imaging studies. Preoperative and postoperative tumor size was measured in cubic centimeters. The degree of Zhang et al: J Neuro-Ophthalmol 2021; 41: e548-e559 preoperative and postoperative optic nerve or optic chiasm displacement was graded as 0 (no displacement), 1 (minimal displacement), or 2 (marked displacement). Preoperative and postoperative intracranial optic canal involvement by tumor was graded as 0 (no involvement), 1 (possible involvement), or 2 (definite involvement). Tumor extension into the orbital apex was graded as 0 (no extension), 1 (mild extension), or 2 (marked extension). The cohort was divided into 2 groups according to whether the preoperative visual dysfunction from tumor compression involved one eye (“monocular visual dysfunction”) or both eyes (“binocular visual dysfunction”). We defined postoperative improvement or decline in visual function as a change of at least 2 lines of Snellen visual acuity or at least 2 decibels (dB) of Humphrey visual field (24-2 protocol) mean deviation. This cutoff was selected because we predicted that it would reflect patient perception of a change in visual function. Among patients with preoperative monocular visual dysfunction, we used the following definitions of visual outcome: 1. Somewhat favorable visual outcome: postoperative improvement in visual function in the preoperatively affected eye without decline in visual function in the contralateral unaffected eye; the term “somewhat” was used here because patients never gained postoperative visual function in the affected eye that matched that of the unaffected eye. 2. Somewhat unfavorable visual outcome: postoperative decline in visual function in the preoperatively affected eye; the term “somewhat” was used here because patients never lost the normal visual function in the unaffected eye. 3. Neutral visual outcome: no postoperative change in visual acuity or visual field in either eye. In patients with preoperative binocular visual dysfunction, we used the following definitions of visual outcome: 1. Highly favorable visual outcome: postoperative improvement in visual function in the preoperatively bettersighted eye regardless of visual outcome in the preoperatively worse-sighted eye 2. Somewhat favorable visual outcome: postoperative improvement in visual function in the preoperatively worse-sighted eye without change in visual outcome in the preoperatively better-sighted eye. 3. Highly unfavorable visual outcome: postoperative decline in visual function in the preoperatively bettersighted eye regardless of visual outcome in the preoperatively worse-sighted eye. 4. Somewhat unfavorable visual outcome: postoperative decline in visual function in the preoperatively worsesighted eye without change in visual outcome in the preoperatively better-sighted eye. e549 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution 5. Neutral visual outcome: no postoperative change in visual function in either eye. Categorical variables were summarized by counts and percentages and cross-tabulated with visual outcome. Continuous variables were summarized by medians and ranges. They were partitioned into thirds for crosstabulation with visual outcome. Presence of associations was tested with likelihood ratio tests from multinomial logistic regression models. Statistical analyses were performed in R version 3.6.3 (R Core Team, Vienna, Austria). We conducted telephone interviews on 25 patients using a standard questionnaire (see Supplemental Digital Content, Appendix, http://links.lww.com/WNO/A457). The questions elicited the patients’ self-assessment of their visual outcome, the impact of that visual outcome on ADLs, including driving, their views on the experience of undergoing the surgery, and whether they would undergo such a surgical procedure again. We compared our assessment of visual outcome with that of the patients. Preoperative imaging features Meningiomas originated from the planum sphenoidale or tuberculum sellae (“midline tumors”) in 31 patients (78%) and from the anterior clinoid process or medial sphenoid ridge (“lateral tumors”) in 9 patients (22%). Of the 31 anatomically midline tumors, 9 (29%) affected visual function in only one eye; of the 9 anatomically lateral tumors, all affected visual function in only one eye. Based on the preoperative MRI studies, tumors ranged in volume between 1.82 and 381 cm3 (median, 19.4 cm3). Avid enhancement was present in 30 tumors (75%). T2weighted high-intensity signal was present in 21 tumors (53%). The tumor displaced one or both optic nerves or the optic chiasm in 33 patients (80%). Preoperative imaging disclosed that meningioma was present at the intracranial end of the optic canal in 32 patients (71%). Among those 32 patients, it was judged by imaging interpretation as definitely present in 20 patients and probably present in 12 patients. Only 5 tumors (13%) had invaded the orbit. Visual Outcomes RESULTS Cohort Characteristics Demographics Entry criteria were met by 40 patients, 30 (75%) of whom were women. Patients ranged in age between 30 and 74 years (median, 58 years). Surgical procedures Surgery was performed by 4 different surgeons: surgeon #1 performed 29 procedures; surgeon #2 performed 8 procedures; surgeon #3 performed 2 procedures; and surgeon #4 performed 1 procedure. Surgical approaches included 5 expanded endonasal resections and 35 pterional craniotomy variants with the addition of skull base osteotomies depending on tumor size and surgeon preference. Nine procedures were performed between 2006 and 2013 and 31 procedures between 2014 and 2019. There were no intraoperative complications. Preoperative ophthalmic features Patients reported preoperative vision loss with a duration that ranged from 1 to 144 months (median, 15 months), but this information was considered highly inaccurate because the vision loss was rarely acute and patients admitted that they were unable to recall precisely when symptoms began. Deficits in visual function attributable to tumor compression affected only one eye (“monocular visual dysfunction”) in 18 patients (45%) and both eyes (“binocular visual dysfunction”) in 22 patients (55%). Preoperative best-corrected visual acuity ranged from 20/20 to light perception (median 20/50). Preoperative Humphrey visual field mean deviations ranged from +0.16 dB to 233.1 dB (median, 216.5 dB). Optic disc pallor was recorded preoperatively in one eye or both in 28 patients (70%). e550 Preoperative monocular visual dysfunction Vision improved postoperatively in 11 of 18 patients (61%) (Tables 1–3). These outcomes were considered only “somewhat favorable” because patients never regained sight in the preoperatively affected eye that was as good as that of the preoperatively unaffected eye. Only 4 of 18 patients (22%) gained 4 or more Snellen lines. Three patients with “somewhat favorable” visual outcomes did not gain visual acuity postoperatively, but gained improvement of at least 6 dB in visual field mean deviation. Vision declined postoperatively in 3 patients (17%). These outcomes were considered only “somewhat unfavorable” because patients never lost vision in the preoperatively better-sighted eye. However, 1 patient sustained a decline of 8 Snellen lines and 219.55 dB, 1 patient sustained a decline of 2 Snellen lines and 28.8 dB, and 1 patient sustained a decline of 5 Snellen lines in the preoperatively affected eye. There was no change in visual function postoperatively in 4 patients (22%), considered a neutral visual outcome. Preoperative binocular visual dysfunction Vision improved in 16 patients (73%); 13 (59%) had a “highly favorable visual outcome” and 3 (14%) had a “somewhat favorable visual outcome.” Among the 13 patients who had a “highly favorable visual outcome,” 6 (27%) gained at least 4 Snellen lines of visual acuity or at least 5 dB in the visual field mean deviation in that eye (Tables 1, 3). Postoperative visual function in the preoperatively worse-sighted eye never surpassed the visual function in the preoperatively better-sighted eye. Three patients (14%) had a “somewhat unfavorable visual outcome” in that they lost vision in the preoperatively worse-sighted eye without a change in visual function in the preoperatively Zhang et al: J Neuro-Ophthalmol 2021; 41: e548-e559 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 1. Visual outcomes in patients with preoperative monocular and binocular visual dysfunction Visual Outcome Preoperative Monocular Visual Dysfunction (n = 18) Highly favorable Somewhat favorable Neutral Somewhat unfavorable Highly unfavorable N/A 11 (61%) 4 (22%) 3 (17%) N/A Preoperative Binocular Visual Dysfunction (n = 22) Total (N = 40) 13 (59%) 3 (14%) 3 (14%) 3 (14%) 0 (0%) 13 (33%) 14 (35%) 7 (18%) 6 (15%) 0 (0%) Percentages may not add to 100 due to rounding. N/A, not applicable. better-sighted eye. Among them was 1 patient who lost 5 Snellen lines of visual acuity and 3.15 dB in visual field mean deviation, 1 patient who lost 7 Snellen lines, and 1 patient who lost 9.77 dB in visual field mean deviation without a change in visual acuity in the preoperatively worse-sighted eye. No patients suffered a “highly unfavorable visual outcome,” indicated by loss of vision in the preoperatively better-sighted eye. Three patients (14%) had a neutral visual outcome. Patients’ Self-Assessment of Visual Outcome and Impact on Activities of Daily Living We conducted telephone interviews on 25 patients (11 with preoperative monocular dysfunction, 14 with preoperative binocular visual dysfunction), 76% of whom had been assessed as having had postoperative visual improvement, as compared with only 68% in the entire cohort, so our interview sample included slightly more patients with favorable outcomes. The correlation between our assessment and patients’ assessment of visual outcome was strong. Preoperative monocular visual dysfunction Among 11 interviewed patients, 9 (82%) agreed with our assessment of their visual outcome. However, of the 6 patients who agreed that visual outcome had improved, only 3 reported that ADLs, including driving, had improved. All 3 of those patients had gained at least 4 Snellen lines, reaching a postoperative visual acuity of at least 20/25. In the 3 patients who agreed that visual outcome had improved but denied that it had improved TABLE 2. Preoperative and postoperative visual acuities and visual fields in patients with preoperative monocular visual dysfunction Visual Acuity (Snellen Notation) Patient Somewhat favorable visual outcome 1 2 3 4 5 6 7 8 9 10 11 Somewhat unfavorable visual outcome 12 13 14 Neutral outcome 15 16 17 18 Visual Fields (Mean Deviation in Decibels) Preoperative Postoperative Preoperative Postoperative 20/20 20/50 Hand movements 20/25 20/50 20/80 20/80 20/30 20/150 20/40 20/40 20/25 20/30 Counts fingers 20/25 20/20 20/25 20/25 20/20 20/25 20/30 20/25 211.25 220.60 231.90 226.48 29.06 222.10 222.35 214.59 219.52 210.29 217.10 26.55 26.06 219.13 217.09 23.78 20.06 20.42 28.12 28.20 23.44 29.10 20/60 20/20 20/20 20/80 20/150 20/100 221.00 25.38 27.95 229.80 224.93 N/A 20/15 20/20 20/30 20/20 20/15 20/20 20/25 20/20 24.33 24.23 25.30 0.16 25.64 23.48 23.50 0.70 Zhang et al: J Neuro-Ophthalmol 2021; 41: e548-e559 e551 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 3. Preoperative and postoperative visual acuities and visual fields in patients with preoperative binocular visual dysfunction Preoperative Better-Sighted Eye Patient Number Favorable visual outcome 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 Unfavorable visual outcome 35 36 37 Neutral outcome 38 39 40 Visual Acuity (Snellen Notation) Preoperative Worse-Sighted Eye Visual Fields (Mean Deviation in Decibels) Visual Fields (Mean Deviation in Decibels) Preoperative Postoperative Preoperative Postoperative Preoperative Postoperative Preoperative Postoperative 20/100 20/50 233.11 231.26 N/A 20/20 Light perception 20/15 20/20 20/20 20/20 20/15 20/25 20/30 20/20 20/20 20/30 20/30 20/30 20/20 230.10 N/A 221.70 N/A Light perception 20/40 Count fingers 233.11 20/30 Hand movements 20/25 20/30 20/125 20/20 20/15 20/40 20/60 20/25 20/25 20/25 20/30 20/40 20/20 232.50 N/A 213.50 N/A 214.85 211.87 N/A 23.90 22.70 28.10 27.27 24.80 24.88 210.31 28.17 210.10 22.24 21.71 21.92 21.34 20.90 20.10 22.87 22.99 21.19 26.57 23.81 22.55 26.69 20.80 Hand movements 20/50 Light perception 20/30 Count fingers 20/800 20/800 20/20 20/125 20/1,000 20/50 20/70 20/40 20/150 Count fingers 20/40 20/60 20/40 20/20 20/400 20/20 20/60 20/20 20/25 20/25 20/30 20/500 20/400 20/20 220.91 N/A N/A 230.00 29.70 219.80 N/A 229.80 218.82 211.28 220.94 222.24 28.90 224.83 26.37 20.50 216.00 24.40 26.95 25.37 227.46 25.12 25.17 214.12 210.26 20.60 20/50 20/20 20/15 20/30 20/20 20/20 24.41 22.49 0.82 24.35 21.37 1.62 20/70 20/25 20/50 20/50 20/80 Light perception 216.73 24.90 215.79 226.50 28.05 N/A 20/50 20/20 20/25 20/60 20/15 20/20 221.64 25.24 20.44 N/A 25.67 21.06 Counting fingers 20/20 20/25 Hand motion 20/15 20/25 231 27.79 26.29 N/A 26.49 25.59 their ability to perform ADLs, visual acuity had risen from 20/50 to 20/30, 20/40 to 20/25, and 20/80 to 20/25. Thus, even a substantial improvement in visual acuity to near normal was not always enough to have an impact on ADLs, perhaps because the “controlling” unaffected eye retained normal visual function. Two patients disagreed with our assessment of a favorable visual outcome, telling us that there had been no change in their vision postoperatively. One patient had gained only 2 Snellen lines, and 1 patient had gained visual field but not visual acuity. Evidently, a small gain in visual acuity or a gain limited to the visual field was not enough to make an impact on ADLs in this group. The single interviewed patient whose visual acuity had fallen drastically, from 20/20 to 20/100 postoperatively, reported not being able to read or drive since the surgery but was grateful that the surgery had “saved my life.” Nine of the 11 interviewed patients reported that they would definitely undergo the surgery again; the 2 patients who reported that they would only “probably” undergo the surgery again had sustained only minor gains in visual acuity. e552 Visual Acuity (Snellen Notation) Preoperative binocular visual dysfunction Among 14 interviewed patients, 12 (86%) agreed with our assessment of their visual outcome. However, of the 10 patients who agreed that vision had improved, 6 denied that it had improved their ability to perform ADLs. Three of them had gained vision only in the preoperatively worse-sighted eye, and 2 had gained visual field but not visual acuity. One patient disagreed with our assessment that vision had improved, having gained visual field but not visual acuity. One patient, assessed as having had a neutral visual outcome, reported that his transient obscurations of vision in the better-sighted eye had disappeared completely after surgery, enabling him to function much better in ADLs. Putative Predictors of Visual Outcome Age and Sex The difference in visual outcome between men and women was not statistically significant (Table 5). Similarly, there was no statistical difference in visual outcome among 3 Zhang et al: J Neuro-Ophthalmol 2021; 41: e548-e559 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution age groups: 48 years or younger (n = 14), 49 years–62 years (n = 13), and 63 years or older (n = 13). Identity of the surgeon, surgical approach, and epoch of the surgical procedure Visual outcomes were unrelated to the identity of the surgeon, the surgical approach, or whether the surgery had been done in the first or second epoch of the study. Preoperative visual acuity Visual outcomes were significantly better in patients with preoperative visual acuity of 20/70 or worse than in those with 20/40 or better. This counterintuitive result was confounded by our criteria for visual improvement, which depended on a change in the number of Snellen lines on which patients correctly identified letters, so that patients with relatively good preoperative visual acuity had less room to improve than those with relatively poor visual acuity. Of the 27 patients who achieved a favorable postoperative visual outcome, 11 (41%) had a preoperative visual acuity of 20/80 or worse. Thus, poor preoperative visual function did not preclude a favorable visual outcome. Preoperative Humphrey visual field mean deviation This feature was a poor predictor of visual outcome. Among the 12 patients whose preoperative mean deviations were 220.9 dB or worse, 10 (83%) had a favorable outcome. By comparison, among the 12 patients whose preoperative mean deviations were 29.1 dB or better, only 3 (25%) had a favorable visual outcome. As with visual acuity, this counterintuitive result was confounded by our criteria for visual improvement. Of the 27 patients with favorable visual outcomes, 15 had preoperative visual field mean deviations of 210 dB or worse. Thus, a poor preoperative visual field did not preclude a favorable visual outcome. Duration of visual symptoms A longer self-reported duration of visual symptoms was slightly associated with a worse visual outcome. But patients with 17 or more months of vision loss were as likely to have a favorable visual outcome as those with a shorter duration of symptoms. Moreover, the duration of visual symptoms does not correlate with the level of preoperative visual acuity (Table 4). Preoperative optic disc pallor The presence of preoperative optic disc pallor was significantly related to a poor preoperative visual acuity (Table 4) but did not preclude a good visual outcome (Table 5). Thus, of the 28 patients (70%) who had optic disc pallor, 20 (71%) had a favorable visual outcome and only 4 (14%) had an unfavorable outcome. Preoperative tumor size, optic nerve displacement, and site of tumor origin None of these features affected visual outcome. Preoperative optic canal involvement by tumor The presence of optic canal involvement was not significantly associated with a greater chance of an unfavorable visual outcome, and it did not preclude a favorable visual outcome. Among 20 patients with definite imagining evidence of canal involvement, 13 (65%) had a favorable visual outcome and 5 (25%) had an unfavorable visual outcome. Among 8 patients who had no optic canal involvement, 6 (75%) had a favorable visual outcome and none had an unfavorable visual outcome. Postoperative reduction of tumor volume The amount of imaging reduction in tumor volume postoperatively did not significantly affect visual outcome. Among 24 patients with at least 70% tumor volume reduction, 17 (71%) sustained a favorable visual outcome (Fig. 1) and 3 (13%) sustained an unfavorable visual outcome. Among the 16 patients with less than 70% tumor volume reduction, 10 (63%) sustained a favorable visual outcome (Fig. 2) and 3 (18%) sustained an unfavorable visual outcome. TABLE 4. Association of preoperative duration of visual symptoms and visual dysfunction Preoperative Visual Dysfunction Covariate Duration of Preoperative visual symptoms (months) 0–6 7, 12 17, 144 Not documented Presence of preoperative optic disc pallor No Yes Not documented Number of Patients 20/15 to 20/30 20/40 to 20/70 20/80 to Light Perception P 0.467 18 9 8 5 7 3 2 2 (39%) (33%) (25%) (40%) 3 6 3 1 (17%) (67%) (38%) (20%) 8 (44%) 0 (0%) 3 (37%) 2 (40%) 0.008 11 28 1 Zhang et al: J Neuro-Ophthalmol 2021; 41: e548-e559 8 (73%) 6 (22%) 0 (0%) 1 (9%) 11 (39%) 0 (0%) 2 (18%) 11 (39%) 1 (100%) e553 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 5. Putative predictors of visual outcome Visual Outcome Covariate Sex Women Men Age (years) 30–48 49–62 63–74 Duration of preoperative visual symptoms (months) 0–6 7–12 17–144 Missing data Preoperative visual acuity (logMAR-converted Snellen notation) 20/15–20/30 20/40-20/70 20/80-LP Preoperative visual field (mean deviation, in decibels) 233.1 to 220.9 220.6 to 29.7 29.1 to 0.2 Missing data Preoperative optic disc pallor No Yes Missing data Site of tumor origin Lateral (medial sphenoid ridge, clinoid process) Midline (tuberculum sellae, planum sphenoidale) Preoperative tumor volume (cm3) 1.8–10.9 11.0–30.5 53–381 Percentage postoperative tumor volume reduction 100% 70%–99% 0%–69% Preoperative optic nerve displacement None Minimal Marked Preoperative optic canal involvement None Possible Definite Imaging change from preoperative to postoperative optic nerve displacement None-.None Possible-.None Possible-.Possible Definite-.None Definite-.Possible Definite-.Definite e554 n Favorable Neutral Unfavorable 30 10 18 (60%) 9 (90%) 6 (20%) 1 (10%) 6 (20%) 0 (0%) 14 13 13 8 (57%) 10 (77%) 9 (69%) 4 (29%) 0 (0%) 3 (23%) 2 (14%) 3 (23%) 1 (8%) 18 9 8 5 13 5 6 3 4 (22%) 2 (22%) 0 (0%) 1 (20%) 1 2 2 1 P 0.087 0.817 0.020 (72%) (56%) (75%) (60%) (5.7%) (22%) (25%) (20%) 0.027 14 14 12 5 (36%) 11 (79%) 11 (92%) 6 (43%) 0 (0%) 1 (8%) 3 (21%) 3 (21%) 0 (0%) 12 12 12 4 10 10 3 4 (84%) (83%) (25%) (100%) 1 (8%) 0 (0%) 6 (50%) 0 (0%) 1 (8%) 2 (17%) 3 (25%) 0 (0%) 11 28 1 6 (55%) 20 (72%) 1 (100%) 3 (27%) 4 (14%) 0 (0%) 2 (18%) 4 (14%) 0 (0%) 9 31 5 (56%) 22 (71%) 3 (33%) 4 (13%) 1 (11%) 5 (16%) 14 13 13 11 (79%) 8 (62%) 8 (61%) 1 (7%) 2 (15%) 4 (31%) 2 (14%) 3 (23%) 1 (8%) 13 11 16 10 (77%) 7 (64%) 10 (62%) 2 (15%) 2 (18%) 3 (19%) 1 (8%) 2 (18%) 3 (19%) 7 11 22 4 (57%) 6 (55%) 17 (77%) 2 (29%) 3 (27%) 2 (9%) 1 (14%) 2 (18%) 3 (14%) 8 12 20 6 (75%) 8 (67%) 13 (65%) 2 (25%) 3 (25%) 2 (10%) 0 (0%) 1 (8%) 5 (25%) 0.002 0.574 0.404 0.544 0.925 0.590 0.254 0.536–0.318 7 8 3 10 9 3 4 4 2 9 6 2 (57%) (50%) (67%) (90%) (67%) (67%) 2 (29%) 2 (25%) 1 (33%) 0 (0%) 1 (11%) 1 (33%) 1 (14%) 2 (25%) 0 (0%) 1 (10%) 2 (22%) 0 (0%) Zhang et al: J Neuro-Ophthalmol 2021; 41: e548-e559 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution (Continued ) Visual Outcome Covariate Imaging change from preoperative to postoperative optic canal tumor involvement None-.None Possible-.None Possible-.Possible Definite-.None Definite-.Possible Definite-.Definite n Favorable Neutral Unfavorable P 0.085–0.270 8 6 6 4 1 15 6 3 5 4 1 8 (75%) (50%) (83%) (100%) (100%) (54%) 2 (25%) 3 (50%) 0 (0%) 0 (0%) 0 (0%) 2 (13%) 0 (0%) 0 (0%) 1 (17%) 0 (0%) 0 (0%) 5 (33%) Each P-value is derived from a likelihood ratio test of a multinomial logistic regression model. Although continuous variables are categorized for display in the table, the P-values of continuous variables (age, duration, visual acuity, visual field, volume, % reduction) were derived using the continuous variable in the regression model. The 2 “imaging change” variables have 2 values each. The first is for the model using all patients. The second is for model built with only patients who had “definite” involvement at baseline. Postoperative reduction in optic nerve displacement Marked postoperative reduction in displacement of the optic nerves or optic chiasm by tumor did not benefit vision and actually appeared to cause more harm. Among the 27 patients who displayed postoperative reduction of at least 1 imaging grade, 19 (70%) sustained a favorable visual outcome (Fig. 3), but 5 (19%) sustained an unfavorable visual outcome (Fig. 4). These 5 patients were among the 6 patients in the entire cohort who had an unfavorable visual outcome. Of the 6 patients in whom surgery did not substantially alter displacement of the optic nerves or optic chiasm, 4 (66%) had a favorable outcome (Fig. 5) and none had an unfavorable visual outcome. Postoperative reduction in optic canal tumor Imaging reduction in optic canal tumor had mixed effects on visual outcome. Five of the 20 patients (25%) with definite preoperative imaging evidence of optic canal involvement and at least 1 imaging grade of postoperative reduction in optic canal tumor involvement sustained a favorable visual outcome (Fig. 6). But 8 of 15 patients (53%) in whom there was no postoperative imaging change in optic canal involvement also sustained a favorable visual outcome (Fig. 7) and 5 patients (33%) sustained an unfavorable visual outcome. rather than eyes. Its validity was largely affirmed by patient assessment. For example, 2 patients with preoperative binocular visual dysfunction who lost vision in the preoperatively worsesighted eye but gained vision in the preoperatively better-sighted eye reported that their improved vision had contributed to better execution of ADLs. Had visual outcomes been counted according to eyes that information would have been lost. The positive nature of visual outcomes in this study must be interpreted with qualifications. Among the 18 patients with preoperative monocular visual dysfunction, only 4 patients (22%) gained at least 4 Snellen lines, enough to make them appreciate an impact on ADLs. This result is not surprising, considering that nearly all ADLs, including driving, can be well executed with the normal vision retained in the unaffected eye. Only a major improvement in visual function in the affected eye would contribute to improved depth perception or the patient’s sense of a broader field of vision. Thus, in patients with preoperative monocular visual dysfunction, surgery is justified primarily to relieve the concern of having a large brain tumor and to prevent tumor growth that might cause further impairment in vision and other brain functions. One of DISCUSSION In this cohort of 40 first surgical procedures for anterior skull base meningiomas compressing the optic nerves or optic chiasm, visual outcomes were favorable in 61% of patients with preoperative monocular visual dysfunction, mostly from meningiomas seated in the medial sphenoid ridge or anterior clinoid process, and in 73% of patients with preoperative binocular visual dysfunction, mostly from meningiomas originating in the planum sphenoidale or tuberculum sellae. These results cannot be easily compared with those of previous publications (3,5–7,9,11,13–15,20) because we used a scoring system for visual outcomes that was based on patients Zhang et al: J Neuro-Ophthalmol 2021; 41: e548-e559 FIG. 1. Both optic nerves affected preoperatively (patient #30). Major tumor debulking with favorable visual outcome. A 52-year-old man with preoperative visual acuity of 20/25 in the right eye and 20/70 in the left eye, and postoperative visual acuity of 20/20 in the right eye and 20/25 in the left eye. Preoperative (left) and postoperative (right) postcontrast T1-weighted MRI. e555 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 2. Right optic nerve affected preoperatively (patient #6). Minor tumor debulking with favorable visual outcome. A 47-year-old woman with preoperative visual acuity of 20/80 in the affected right eye and postoperative visual acuity of 20/25 in that eye. Preoperative (left) and postoperative (right) postcontrast T1-weighted MRI. the patients we interviewed, who had actually sustained an unfavorable visual outcome, expressed relief at having a brain tumor removed. The decision to operate should consider tumor size, its proximity to the unaffected optic nerve and optic chiasm, and its pace of growth, which must be balanced against the risks of surgery, including loss of vision. In that regard, 3 of patients (17%) in this group suffered postoperative loss of vision in the affected eye, often to a considerable degree. The benefit of surgery among the 22 patients with preoperative binocular visual dysfunction was more evident. In that group, 73% attained improvement, and no patient lost sight in the preoperatively better-sighted eye. Yet even in this group, our assessment of a favorable visual outcome overestimated its contribution to improved ADLs. Surgery did not have a substantial impact if the gain in visual acuity was restricted to the worse-sighted eye or when there was a gain in visual field without a gain in visual acuity in the preoperatively better-sighted eye. Many of the touted predictors of visual outcome were not confirmed in this study. Patient age and gender did not influence visual outcome. Although a longer duration of visual symptoms was associated with an unfavorable visual outcome, it did not preclude a favorable visual outcome. Moreover, this feature is likely to be inaccurate because vision loss from these tumors usually proceeds slowly and because intact vision in one eye may prevent patients from noticing vision loss in the other eye until it is advanced. Notably, the duration of visual symptoms did not correlate with preoperative visual acuity. Preoperative optic disc pallor, a sign of optic nerve axonal loss often considered to presage an unfavorable visual outcome (21), did not do so in this study. As many as 70% of our patients had this sign preoperatively, yet they often benefited from surgery. Optical coherence tomography, a quantitative sign of retinal axonal loss reported to be predictive of visual outcome in surgery for pituitary tumors (23,24), and meningiomas (25), could not be used in this study because too few patients had undergone that test. e556 FIG. 3. Right optic nerve affected preoperatively (patient #7). Major postoperative reduction in optic nerve displacement with favorable visual outcome. A 56-year-old woman with preoperative visual acuity of 20/80 in the affected right eye and postoperative visual acuity of 20/25 in that eye. Preoperative (left) and postoperative (right) postcontrast T1-weighted MRI. Our study also differs from many previous studies (3,5,9,11,14,16,17) in failing to show that preoperative visual acuity and visual field are robust predictors of visual outcome. There was no cutoff of Snellen acuity or visual field mean deviation that precluded substantial postoperative improvement in vision. We acknowledge that our criteria for measuring visual outcome may have impaired a reasonable assessment of the impact of these factors in patients with good preoperative function, but many patients with very poor preoperative visual acuity or visual field sustained favorable visual outcomes. Our detailed imaging analysis surprisingly disclosed few unequivocal predictors of visual outcome. Previous authors have found that tumor size (2,5,16,17,26) and degree of visual pathway displacement (6,17) affect visual outcome. Yet many of our patients who had enormous tumors that obliterated the optic nerves and chiasm fared well postoperatively. Some authors have suggested that aggressive tumor resection is necessary to obtain favorable visual results (6,22), but there have been no robust data linking the amount of surgical resection to visual outcome, in part because of a lack of comparative preoperative and postoperative imaging data. In this study, marked reduction in tumor FIG. 4. Both optic nerves affected preoperatively (patient #37). Major postoperative reduction in optic nerve displacement with unfavorable visual outcome. A 58-year-old woman with preoperative visual acuity of 20/15 in the right eye and 20/50 in the left eye, and postoperative visual acuity of 20/20 in the right eye and light perception in the left eye. Preoperative (left) and postoperative (right) postcontrast T1-weighted MRI. Zhang et al: J Neuro-Ophthalmol 2021; 41: e548-e559 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 5. Both optic nerves affected preoperatively (patient #29). Minor postoperative reduction in optic nerve displacement with favorable visual outcome. A 46-year-old woman with preoperative visual acuity of 20/25 in the right eye and 20/50 in the left eye, and postoperative visual acuity of 20/20 in the right eye and 20/25 in the left eye. Preoperative (left) and postoperative (right) postcontrast T1weighted MRI. bulk by the surgeon, as confirmed by postoperative imaging, did not improve vision as compared with lesser reduction. Using a cutoff of 70% postoperative tumor volume reduction, nearly as many patients with less than that amount of tumor volume reduction had a favorable visual outcome as did those with 70% or more tumor volume reduction. Marked reduction in postoperative optic nerve or optic chiasm displacement by tumor appeared to adversely affect visual outcome. Among the 27 patients whose imaging studies disclosed marked or moderate reduction in displacement, 5 (19%) had an unfavorable visual outcome, and they were among only 6 patients in our cohort who had an unfavorable visual outcome. By contrast, of the 6 patients whose imaging showed minimal if any change in postoperative displacement of the optic nerves or optic chiasm, 4 (66%) had a favorable outcome and none had an unfavorable visual outcome. Thus, major reduction in optic nerve or chiasm displacement does not appear to be necessary to obtain a favorable visual outcome and may incur extra risks. Moreover, there are no reported data to suggest that major resection of these tumors provides a better safeguard against tumor recurrence than lesser resection. Preoperative evidence of tumor in the optic canal has been said to foretell a poor visual outcome (27–29). In this study, it did indicate a greater chance of an unfavorable visual outcome, but it did not preclude a favorable visual result. Several authors (12,30) have emphasized the importance of unroofing the optic canal or at least removing tumor embedded at its intracranial opening. However, the effect of surgical removal of optic canal tumor on visual outcome is confounded by the fact that past reports do not always indicate how much, if any, surgery was done on the optic canal (27–29). In this study, we used a postoperative imaging assessment, rather than the surgeon’s report, as a gauge of optic canal tumor removal. PostoperZhang et al: J Neuro-Ophthalmol 2021; 41: e548-e559 FIG. 6. Both optic nerves affected preoperatively (patient #24). Postoperative reduction in optic canal tumor with favorable visual outcome. A 30-year-old woman with preoperative visual acuity of 20/125 in the right eye and 20/ 800 in the left eye, and postoperative visual acuity of 20/ 20 in the right eye and 20/20 in the left eye. Preoperative (left) and postoperative (right) postcontrast T1-weighted MRI. ative imaging reduction in optic canal tumor was associated with a benefit to vision, but it also increased the risk of a poor visual outcome. The following decision-making guidelines have emerged from this study: 1. Preoperative demographic, ophthalmic, and imaging measures, including tumor size and involvement of the optic canal, are weak predictors of visual outcome and should not be used to preclude surgery. 2. Patients with preoperative monocular visual dysfunction should be aware that, although they have a better-thaneven chance of gaining improved vision in the affected eye, it is unlikely to reach the level of the unaffected eye. As a result, even a favorable visual outcome may not have a major impact on ADLs. The 22% chance for a substantial gain in vision, and some protection against tumor growth and progressive vision loss, must be balanced against the 17% chance of sustaining a postoperative decline in vision, often severe. FIG. 7. Both optic nerves affected preoperatively (patient #23). No postoperative reduction in optic canal tumor (arrow) with favorable visual outcome. A 65-year old woman with preoperative visual acuity of counting fingers in the right eye and 20/30 in the left eye, and postoperative visual acuity of 20/40 in the right eye and 20/20 in the left eye. Preoperative (left) and postoperative (right) postcontrast T1weighted MRI. e557 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution 3. Patients with preoperative binocular visual dysfunction are better candidates for surgery than those with monocular visual dysfunction. They can expect a better-thaneven chance of improved vision in the better-sighted eye, yet a lesser chance that improvement will translate into improved execution of ADLs. Even so, the risk of vision loss in the preoperatively better-sighted eye is low, whereas the risk of leaving behind a midline tumor that has already affected both optic nerves is high. 4. Aggressive debulking of the tumor in an attempt to reduce displacement of the optic nerves and chiasm does not appear to improve the chances of visual recovery and entails a risk of an adverse visual outcome. 5. Removal of optic canal tumor might improve vision but might also lead to a poor visual outcome. At that same time, lack of removal of optic canal tumor does not preclude a favorable visual outcome. Among the deficiencies of this study is a relatively small cohort size, although it is larger than that of most comparable studies. As such, it limits the power of assessing visual outcomes. As a retrospective study, it is weakened by incomplete and nonuniform clinical and surgical documentation. Conventional MRI studies do not always permit accurate assessment of optic canal tumor. Only 4 surgeons performed the procedures, the majority by a single surgeon, so many of our conclusions may depend on one surgeon’s skill. Also, the clinical outcomes presented in this study relate only to first intracranial procedures. There are no data about whether these patients later developed tumor recurrence that required reoperation or radiotherapy. The strong points of the study are detailed recording of visual information and correlation with imaging studies, the ability to judge the extent of surgery based on postoperative imaging, and an assessment of visual outcome validated by patient self-report. We acknowledge that the questionnaire used to interview patients was not validated, but we believe that it provided a real-world assessment of the impact of surgery on visual capabilities. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: Y. Zhang, J. Kim, C. Andrews, E. Archer, L. Bursztyn, H. Grabe, E. Margolin, S. Sullivan, and J. Trobe; b. Acquisition of data: Y. Zhang, J. Kim, E. Archer, L. Bursztyn, H. Grabe, E. Margolin, S. Sullivan, and J. Trobe; c. Analysis and interpretation of data: Y. Zhang, J. Kim, C. Andrews, E. Archer, L. Bursztyn, H. Grabe, E. Margolin, S. Sullivan, and J. Trobe. Category 2: a. Drafting the manuscript: Y. Zhang, J. Kim, C. Andrews, E. Archer, L. Bursztyn, H. Grabe, E. Margolin, S. Sullivan, and J. Trobe; b. Revising it for intellectual content: Y. Zhang, J. Kim, C. Andrews, E. Archer, L. Bursztyn, H. Grabe, E. Margolin, S. Sullivan, and J. Trobe. Category 3: a. Final approval of the completed manuscript: Y. Zhang, J. Kim, C. Andrews, E. Archer, L. Bursztyn, H. Grabe, E. Margolin, S. Sullivan, and J. Trobe. e558 REFERENCES 1. Demonte F, McDermott M, Al-Mefty O. Al-Mefty’s Meningiomas. 2nd edition. Vol 35–39. Thieme Medical 2011;206–213. 2. Jen SL, Lee LS. Suprasellar meningiomas: analysis of 32 cases. Chin Med J. 1997;59:7–14. 3. Zevgaridis D, Medele RJ, Müller A, Hischa AC, Steiger HJ. Meningiomas of the sellar region presenting with visual impairment: impact of various prognostic factors on surgical outcome in 62 patients. 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Date | 2021-12 |
Language | eng |
Format | application/pdf |
Type | Text |
Publication Type | Journal Article |
Source | Journal of Neuro-Ophthalmology, December 2021, Volume 41, Issue 4 |
Collection | Neuro-Ophthalmology Virtual Education Library: Journal of Neuro-Ophthalmology Archives: https://novel.utah.edu/jno/ |
Publisher | Lippincott, Williams & Wilkins |
Holding Institution | Spencer S. Eccles Health Sciences Library, University of Utah |
Rights Management | © North American Neuro-Ophthalmology Society |
ARK | ark:/87278/s6tv0g9x |
Setname | ehsl_novel_jno |
ID | 2116199 |
Reference URL | https://collections.lib.utah.edu/ark:/87278/s6tv0g9x |