http://informahealthcare.com/dre ISSN 0963-8288 print/ISSN 1464-5165 online Disabil Rehabil, 2015; 37(11): 958–962 ! 2014 Informa UK Ltd. DOI: 10.3109/09638288.2014.948141
RESEARCH PAPER
Visual disability rates in a ten-year cohort of patients with anterior visual pathway meningiomas Elite Bor-Shavit1,2, Naama Hammel1,2, Yoav Nahum1,2, Zvi Harry Rappaport3, and Hadas Stiebel-Kalish1,2,3 1
Department of Ophthalmology, Rabin Medical Center – Beilinson Campus, Petach Tikva, Israel, 2Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel, and 3Department of Neurosurgery and 4Department of Neuro-Ophthalmology Unit, Rabin Medical Center – Beilinson Campus, Petach Tikva, Israel Abstract
Keywords
Purpose: To examine the visual outcome of anterior visual pathway meningioma (AVPM) patients followed for at least one year. Methods: Data were collected on demographics, clinical course and management. Visual disability was classified at the first and last examination as follows: I – no visual disability; II – mild visual defect in one eye; III – mild visual defect in both eyes; IV – loss of driver’s license; V – legally blind. Results: Eight-one AVPM patients had their tumor originate in the clinoid process in 23 (28%), sphenoid-wing area in 18 (22%), cavernous sinus in 15 (19%), tuberculum sellae in 8 (10%), and mixed in 17 (21%). On last examination, 46 patients (57%) had good visual acuity in one or both eyes (Class I or II) and 17 (21%) were mildly affected in both eyes. The rate of Class IV disability was 16%, and Class V disability was 6%. Conclusions: Attention needs to be addressed to the considerable proportion of patients with AVPM (22% in this study) who may lose their driver’s license or become legally blind. Occupational therapists should play an important role in the multidisciplinary management of those patients to help them adapt to their new physical and social situation.
Blindness, loss of driver’s license, optic nerve, tumor, vision History Received 7 December 2013 Revised 20 July 2014 Accepted 21 July 2014 Published online 18 August 2014
ä Implications for Rehabilitation
Anterior visual pathway meningiomas (AVPMs) are commonly not life-threatening but they can lead to profound visual disability, especially when the tumor originates in the tuberculum sellae and cavernous sinus. Particular attention should be paid to visual acuity and visual field deficits, as these can profoundly affect the patient’s quality of life including ability to drive and activities of daily living. The interdisciplinary management of patients with AVPM should include the neurosurgeon, neuro-ophthalmologist and occupational therapist. Also, early intervention by the occupational therapist can help patients adapt to their current physical and social situation and return to everyday tasks more rapidly.
Introduction Meningiomas located adjacent to the anterior visual pathway apparatus (clinoid process, tuberculum sellae, suprasellar cistern, sphenoid ridge, cavernous sinus or planum sphenoidale) are rarely life-threatening. However, they may lead to chronic progressive visual disability [1] with a consequent reduction in quality of life and increase in health-care costs and social burden [2]. Current treatment options of anterior visual pathway meningioma (AVPM) include fractionated stereotactic radiotherapy (FSRT) and surgery. However, more data on expected vision disability outcome are needed to assist resource planning and rehabilitation.
Address for correspondence: Elite Bor-Shavit, MD, Department of Ophthalmology, Rabin Medical Center – Beilinson Campus, Petach Tikva 49100, Israel. Tel: 972-3-937-6100. Fax: 972-3-937-6104. E-mail: [email protected]
The aim of this study was to determine long-term visual disability rates in a large cohort of patients with AVPM attending a major medical center. Patients and methods The electronic files of a tertiary, university-affiliated medical center were reviewed for all patients who were admitted with a diagnosis of AVPM in 2001–2011 and followed for at least 12 months. The study was approved by the local Institutional Review Board. According to our hospital protocol, patients with AVPM are carefully followed by a multidisciplinary team of medical specialists in neurosurgery, neuro-ophthalmology, radiation oncology and neuroradiology. The team holds weekly meetings to review new cases, monitor tumor progression in existing cases by revising magnetic resonance imaging scans and neuroophthalmological examinations, and recommend interventions on the basis of these findings.
Visual disability in meningiomas of visual pathway
DOI: 10.3109/09638288.2014.948141
For purposes of the present study, three sets of data were collected: patient demographics, disease-related parameters and vision-related parameters. Patient demographics included age at presentation and sex, prior history of radiation exposure and duration of follow-up (in years). Disease-related parameters included site of origin of the primary tumor, number and types of interventions, namely surgery with or without complementary FSRT, radiosurgery alone, or conservative follow-up with serial brain magnetic resonance imaging (in stable or asymptomatic patients), and clinical course (progression/recurrence) according to available surgical reports and neuroimaging studies. Visionrelated parameters included best corrected visual acuity (BCVA) in each eye using the Snellen chart, presence of a relative afferent pupillary defect, color vision using Ishihara color plates, visual fields measured by the automated Humphrey analyzer (24-2 or 30-2), presence of any other ocular pathology that could affect visual function and presence of optic atrophy. A worsening or improvement of two or more Snellen lines was recorded as a change in BCVA. On the basis of these findings, visual disability was classified for each patient at presentation and at most recent follow-up/final examination according to the method of Goel et al. [3]: Class I – no visual disability in either eye, Class II – mild visual defect, defined as best corrected visual acuity (BCVA) in the better eye of 6/12 or more and visual field at least 200, in one eye only, Class III – mild visual defect in both eyes, Class IV – permanent loss of driver’s license, as defined by the Driver’s Guide of the Canadian Medical Association, the accepted standard for the Israel Bureau of Transportation, Class V – legally blind.
of complications of aggressive meningioma, such as acute hydrocephalus and repeated shunting procedures (two patients) or non-neurological causes (eight patients). However, all had adequate visual follow-up for more than 12 months and were therefore eligible for inclusion in the study. Thus, the final study cohort consisted of 81 patients, 64 women (79%) and 17 men (21%) of mean age 63.7 ± 10.7 years (range: 45–94 years). Twelve patients (15%) had a prior history of exposure to radiation treatment for oncological, dermatological or other diseases. The tumor originated in the clinoid process in 23 patients (28%), sphenoid-wing area in 18 (22%), cavernous sinus in 15 (19%) and tuberculum sellae in 8 (10%); the remaining 17 patients (21%) had AVPM of mixed origin. Visual disability rates at presentation At presentation, 53 patients (66%) had good visual function in one or both eyes (Class I or II) (Figure 1). Thirteen patients (16%) had a mild bilateral defect (Class III), 14 (17%) had already lost their driver’s license (Class IV), and one patient (1.2%) with sphenoidwing AVPM was legally blind in both eyes (Class V). Analysis by tumor origin yielded the highest rate of visual disability at presentation in the patients with tuberculum sellae meningiomas, of whom half (4/8) were designated Class IV. The visual disability was the result of visual field defects in 31 patients (37%) and of optic neuropathy/atrophy in 40 (49%). In 53 patients (65%), additional ophthalmological conditions, such as cataract, glaucoma and retinal disease, contributed to the visual disability. The incidence of these additional conditions was compatible with the expected incidence in the age-matched general population. Visual disability rates at last follow-up
Results Patient demographics and tumor location A total of 1553 patients were diagnosed with intracranial meningiomas during the 10-year study period. In 107 patients, the meningioma was located close to or involved the optic pathway warranting neuro-ophthalmological consultation and follow-up. Of this group, 26 patients were excluded from the study because of incomplete ophthalmological data or less than 12 months’ follow-up. Ten patients (12%) died during follow-up,
Figure 1. Visual disability classification at presentation (top row) and last-follow-up (bottom row) by anatomic location of the AVPM. Class I – no visual disability in either eye; Class II – mild visual defect in one eye only; Class III – mild visual defect in both eyes (BCVA in the better eye of 6/12 or better with a visual field of at least 20 degrees); Class IV – loss of driver’s license (as defined by the Driver’s Guide of the Canadian Medical Association, the accepted standard in the Israel Bureau of Transportation); Class V – legally blind.
959
Mean duration of follow-up was 4.3 ± 1.8 years (range 1.0–7.9 years). At the end of follow-up, 46 patients (57%) had good visual acuity (6/12 or better), in one or both eyes (Class I or II), 17 (21%) had a mild bilateral defect (Class III), 13 (16%) had lost their ability to drive (Class IV), and five (6%) were legally blind in both eyes (Class V). Analysis by tumor origin again yielded the worst visual disability in the patients with tubercullum sella AVPM, of whom 25% were designated Class V, followed by patients with
Class I 100% 90%
4
9
6
Class II
6
80%
Class IV 13
13 13
Class III
22
13
6
7 18
25 22
Class V
50 24 17 57 50%
25 33
48
6 17
27
70% 60%
12
1 17
18
16 28
13
38 13
40%
13
20
29
40 47
39
29
30% 17
25
25
20% 10% 0%
40 26
30 17
17
13
13
33
29
26 18
20
960
E. Bor-Shavit et al. Improvement
Disabil Rehabil, 2015; 37(11): 958–962
Stability
Table 1. Visual disability classification at presentation and last examination in patients with AVPM by treatment strategy.
Deterioraon
100 90
20
11 27
33
80 70 60
25
12 40
56
30
20
50 40 63
30 20
40
47
43 33
10 0 Mixed AVPM Sphenoid (n=17) wing (n=18)
Clinoid (n=23)
Cavernous Tubercullum sinus (n=15) Sella (n=8)
Figure 2. Graphic representation of progression of visual disability from presentation to last follow-up in patients with AVPM.
Treatment Visual disability classa Class I, n (%) First examination Last examination Class II, n (%) First examination Last examination Class III, n (%) First examination Last examination Class IV, n (%) First examination Last examination Class V, n (%) First examination Last examination
Conservative Surgery Radiotherapy Radiotherapy + (n ¼ 14) (n ¼ 32) (n ¼ 27) surgery (n ¼ 8) 36 36
22 22
26 19
25 25
42 29
38 31
41 41
38 25
7 14
22 22
15 19
13 25
14 14
16 19
19 15
25 25
0 7
3 6
0 7
0 0
a
cavernous sinus meningioma, of whom 27% were designated Class IV and 7%, Class V. None of the patients with clinoid meningioma was declared legally blind throughout the 10-year study period. Visual disability progression Visual function deteriorated in 34 patients (42%), remained stable throughout follow-up in 28 (35%), and improved in 19 (23%). By tumor origin, anterior cavernous sinus AVPM was associated with the highest rate of improvement in visual function (5/15 patients, 33%), and tuberculum sellae meningioma with the highest rate of deterioration in visual function (3/8 patients, 37%) (Figure 2). Sphenoid-wing meningioma with associated with the highest rate of stable function during follow-up (10/18 patients, 56%). Tumor management and visual disability As different neurosurgeons were involved in the operative treatment, the approach was not uniform. However, in most cases of clinoid, parasellar and suprasellar tumors, lateral supraorbital craniotomy was performed, followed when necessary by extradural clinoidectomy and optic canal unroofing. For more laterally placed tumors, pterional craniotomy with sphenoid wing resection was the method of choice. Surgical resection or tumor debulking without adjuvant radiotherapy was performed in 32 patients (40%), FSRT alone in eight patients (10%), and combined surgery and FSRT in 27 patients (33%); the remaining 14 patients (17%) were followed conservatively. Mean number of surgical interventions per patient was 1.2 ± 1.8 (range, 0–5); most patients (28/81, 35%) had only one surgical procedure, and one patient (1.2%) with aggressive sphenoid-wing meningioma required five surgeries because of tumor recurrence. Additional procedures were performed when tumor progression was detected on radiological follow-up. At the end of the last visit, an improvement in visual function was noted in 12 patients (37%) in the surgery-only group, six patients (75%) in the radiation-only group, and three patients (12%) in the combined surgery-radiation group. Conservative management was associated with no change in visual function in five5 patients (36%) and improved function in one patient (7%). Deterioration in vision was found in eight of the 27 patients treated by combined surgery and radiation: one had concomitant ocular disease causing the deterioration, one following surgery, and six had tumor re-growth before referral to radiotherapy. There was no change in the remaining patients, including 5/14 patients
Class I – no visual disability in either eye; Class II – mild visual defect in one eye only (mild visual defect defined as best corrected visual acuity (BCVA) of 6/12 or better and a visual field of at least 20 degrees); Class III – mild visual defect in both eyes; Class IV – loss of driver’s license; Class V – legally blind.
(36%) treated conservatively. The visual disability rates by treatment strategies are summarized in Table 1.
Discussion Meningiomas of the anterior visual pathway are neither lifethreatening nor do they commonly lead to neurological disability [4]. Therefore, we believe particular attention should be addressed to their effect on vision, separately from other neurological outcomes, because of the impact of visual disability on vocational capacity, mobility and quality of life. In a unique report, NeilDwyer et al. [2] shed light on an additional aspect of disability, namely, the burden placed on care givers. The authors concluded that existing outcome scales focus on neurological status with or without mental health and pain components. Therefore, they might not be adequate for patients with AVPM-induced visual disability. The present study describes the visual outcome of a cohort of 81 patients with AVPM attending a single tertiary medical center over a 10-year period. Prior outcome studies of AVPM focused mainly on the success rates of treatment (surgical and radiotherapy), defined tumor control or visual stabilization [5–9]. To our knowledge, this is the first study to address final visual disability. We found that only 67% of patients had good visual acuity (6/12 or better in at least one eye) (Class I–III [3]), at the end of followup (mean, 4.3 years). A substantial proportion of the cohort (22%) were either unable to drive (Class IV) or legally blind (Class V), and consequently are expected to require a high level of care. Thus, these findings have important implications not only for neurosurgeons and neuro-ophthalmologists, but also for occupational and vocational therapists. We defined fitness to drive according Israeli law, which follows the recommendations of the Canadian Medical Association [10]. Immediate and permanent visual contraindications to driving are as follows: BCVA less than 6/15 (20/50) in both eyes, with the worse eye less than 6/120 (20/400); visual field less than 120 along the horizontal meridian and 15 continuous above and below fixation in both eyes; diplopia within the central 40 of the visual field (that is, 20 to the left and right, above and below fixation); and need for telescopic spectacles,
DOI: 10.3109/09638288.2014.948141
hemianopia aids and other low-vision aids. Visual conditions/ diseases that may lead to temporary loss of a driver’s license are recent functional change from binocular to monocular vision, including temporary patching of an eye; decrease in other visual functions, such as color vision, contrast sensitivity, depth perception, dark adaptation and glare recovery, and; other ophthalmic conditions, such as cataract, glaucoma and ptosis. In this study, we applied only the criteria pertaining to permanent loss of one’s license. Statutory blindness is defined as total loss of visual acuity to no light perception, maximal BCVA 6/120 (20/400) in the better eye or loss of 200o or more of the visual field in the better eye. Another important finding of the study was the difference in visual outcome by origin of the meningioma. Clinoid meningiomas are usually associated with a relatively good prognosis because they occur unilaterally. Tobias et al. [11] found that resection of clinoid meningiomas led to significant vision improvement in 77% of cases. However, Pompili et al. [12] reported an equal distribution of improvement, worsening and post-operative stabilization (32% each). In our cohort, 79% of patients with clinoid tumors had good to excellent visual ability at the end of follow-up. Sphenoid-ridge meningiomas account for approximately 20% of all supratentorial meningiomas. They have been associated with higher morbidity, mortality and recurrence rates than meningiomas in other locations [12–14], and with higher recurrence rates than other intracranial meningiomas [15]. However, Nakamura et al. [16] reported a large series of sphenoid-ridge meningiomas with a better outcome; vision improved or stabilized in 30% of patients, compared to 56% for cavernous-sinus tumors that did not involve the sphenoid ridge. Our study supports the latter study, with a 56% rate of vision stabilization and 11% improvement in patients with sphenoid-ridge meningiomas. Cavernous sinus meningiomas were found in one study to be associated with a relatively good visual outcome, but only small tumors without anterior optic nerve extension were included [6]. By contrast, in the present study, the cavernous sinus meningiomas were large and extended anteriorly to the visual apparatus. They led to visual deterioration in 33% of patients; the final outcome was Class IV in 20% and Class V in 7%. Tuberculum sellae meningiomas may extend into both optic canals and share their vascular supply with the optic chiasm and prechiasmic optic nerves. Accordingly, they pose a high risk of severely reduced monocular or binocular vision. The surgical treatment of tuberculum sella and suprasellar meningioma has been widely reported in the literature [16–22]. Recovery after any type of treatment, however, is generally poor [23]. Jen and Lee [24] reported an 87.5% rate of visual loss in 32 patients with suprasellar meningiomas, and Odebode et al. [25] reported an 86% rate. In our cohort, patients with tuberculum sellae meningioma had the most dramatic decline in visual function (63%), including 3/5 patients treated surgically. Half the group had either lost their driver’s license or was legally blind at the last follow-up visit. Mixed-type AVPM accounts for 9% of all intracranial meningiomas [26]. Often referred to as ‘‘hyperostotic meningiomas of the sphenoid wing", mixed-type AVPMs are clinically and pathologically distinct from routine sphenoid-wing meningiomas. They may remain undiagnosed until they become significantly large and involve adjacent structures, such as the planum sphenoidale, tuberculum sellae, anterior clinoid process, diaphragm sellae and medial sphenoid wing, making them difficult to treat. Studies report insidious visual loss from optic nerve or tract compression [15]. In a cohort of patients with mixed-type AVPM, Zevgaridis et al. [22] found that visual prognosis was favorably affected by younger age (554 years), early diagnosis, and an intact arachnoid
Visual disability in meningiomas of visual pathway
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membrane around the lesion. Severe pre-operative visual loss of BCVA appeared to be an unfavorable prognostic factor (p50.047). It is noteworthy that early diagnosis of visual compromise in AVPM is hampered by the lack of patient awareness of visual loss because of second-eye compensation or attribution of the visual loss to other known, co-existing ophthalmologic conditions. In many cases, the visual symptoms go unnoticed until the anterior visual system is irreversibly damaged [27]. Functional outcomes are gradually improving, thanks to the availability of improved surgical and radiosurgical treatment options (FSRT) and increasing clinician education on the need for early neuro-ophthalmological screening [9,28–30]. In conclusion, although AVPM meningiomas are commonly not life-threatening, they may lead to profound visual disability. In our cohort, nearly one-fourth of the patients with AVPM either lost their ability to drive or became legally blind in both eyes. The worst prognosis was associated with tuberculum sellae and larger cavernous-sinus meningiomas. These findings emphasize the need for the involvement of neurosurgeons and neuro-ophthalmologists in the interdisciplinary management of patients with AVPM, to limit visual acuity and visual field damage, and importantly, occupational therapists, to aid patients in adapting to their new physical and social situation and rapidly returning to everyday activities.
Declaration of interest The authors report no declarations of interest. No funding or financial support was received for this study.
References 1. Andrews B, Wilson CB. Suprasellar meningiomas: the effect of tumor location on postoperative visual outcome. J Neurosurg 1988; 69:523–8. 2. Neil-Dwyer G, Lang D, Garfield J. The realities of postoperative disability and the carer’s burden. Ann R Coll Surg Engl 2001;83: 215–18. 3. Goel A, Gupta S, Desai K. New grading system to predict resectability of anterior clinoid meningiomas. Neurol Med Chir (Tokyo) 2000;40:610–17. 4. Scheitzach J, Schebesch KM, Brawanski A, Proescholdt MA. Skull base meningiomas: neurological outcome after microsurgical resection. J Neurooncol 2014;116:381–6. 5. Chicani CF, Miller NR. Visual outcome in surgically treated suprasellar meningiomas. J Neuroophthalmol 2003;23:3–10. 6. Klink DF, Sampath P, Miller NR, et al. Long-term visual outcome after nonradical microsurgery patients with parasellar and cavernous sinus meningiomas. Neurosurgery 2000;47:24–32. 7. Nakamura M, Roser F, Jacobs C, et al. Medial sphenoid wing meningiomas: clinical outcome and recurrence rate. Neurosurgery 2006;58:626–39. 8. Park CK, Jung HW, Yang SY, et al. Surgically treated tuberculum sellae and diaphragm sellae meningiomas: the importance of shortterm visual outcome. Neurosurgery 2006;59:238–43. 9. Stiebel-Kalish H, Reich E, Gal L, et al. Visual outcome in meningiomas around anterior visual pathways treated with linear accelerator fractionated stereotactic radiotherapy. Int J Radiat Oncol Biol Phys 2012;82:779–88. 10. Canadian Medical Association. Determining Medical Fitness to Operate Motor Vehicles - CMA driver’s guide, 7th ed., Section 11 – Vision. Ottawa, ON: Canadian Medical Association; 2006:45–50. 11. Tobias S, Kim CH, Kosmorsky G, Lee JH. Management of surgical clinoidal meningiomas. Neurosurg Focus 2003;14:e5. 12. Pompili A, Derome PJ, Visot A, Guiot G. Hyperostosing meningiomas of the sphenoid ridge – clinical features, surgical therapy, and long-term observations: Review of 49 cases. Surg Neurol 1982;17: 411–16. 13. Mirone G, Chibbaro S, Schiabello L, et al. En plaque sphenoid wing meningiomas: recurrence factors and surgical strategy in a series of 71 patients. Neurosurgery 2009;65:100–9.
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14. Russell SM, Benjamin V. Medial sphenoid ridge meningiomas: classification, microsurgical anatomy, operative nuances, and longterm surgical outcome in 35 consecutive patients. Neurosurgery 2008;62:38–50. 15. Mathiesen T, Kihlstrom L. Visual outcome of tuberculum sellae meningiomas after extradural optic nerve decompression. Neurosurgery 2006;59:570–6. 16. Nakamura M, Roser F, Struck M, et al. Tuberculum sellae meningiomas: clinical outcome considering different surgical approaches. Neurosurgery 2006;59:1019–29. 17. Bassiouni H, Asgari S, Stolke D. Tuberculum sellae meningiomas: functional outcome in a consecutive series treated microsurgically. Surg Neurol 2006;66:37–45. 18. Fahlbusch R, Schott W. Pterional surgery of meningiomas of the tuberculum sellae and planum sphenoidale: surgical results with special consideration of ophthalmological and endocrinological outcomes. J Neurosurg 2002;96:235–43. 19. Galal A, Faisal A, Al-Werdany M, et al. Determinants of postoperative visual recovery in suprasellar meningiomas. Acta Neurochir (Wien) 2010;152:69–77. 20. Margalit N, Kesler A, Ezer H, et al. Tuberculum and diaphragma sella meningioma – surgical technique and visual outcome in a series of 20 cases operated over a 2.5-year period. Acta Neurochir (Wien) 2007;149:1199–204. 21. Otani N, Muroi C, Yano H, et al. Surgical management of tuberculum sellae meningioma: role of selective extradural anterior clinoidectomy. Br J Neurosurg 2006;20:129–38. 22. Zevgaridis D, Medele RJ, Muller A, et al. Meningiomas of the sellar region presenting with visual impairment: impact of various
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prognostic factors on surgical outcome in 62 patients. Acta Neurochirurgica 2001;143:471–6. Jallu A, Kanaan I, Rahm B, Siqueira E. Suprasellar meningioma and blindness: a unique experience in Saudi Arabia. Surg Neurol 1996; 45:320–3. Jen SL, Lee LS. Suprasellar meningiomas: analysis of 32 cases. Zhonghua Yi Xue Za Zhi (Taipei) 1997;59:7–14. Odebode TO, Akang EE, Shokunbi MT, et al. Factors influencing visual and clinical outcome in Nigerian patients with cranial meningioma. J Clin Neurosci 2006;13:649–54. Shrivastava RK, Sen C, Costantino PD, Della Rocca R. Sphenoorbital meningiomas: surgical limitations and lessons learned in their long-term management. J Neurosurg 2005;103: 491–7. Rosenberg LF, Miller NR. Visual results after microsurgical removal of meningiomas involving the anterior visual system. Arch Ophthalmol 1984;102:1019–23. Baumert BG, Villa S, Studer G, et al. Early improvements in vision after fractionated stereotactic radiotherapy for primary optic nerve sheath meningioma. Radiother Oncol 2004;72: 169–74. Milker-Zabel S, Zabel A, Schulz-Ertner D, et al. Fractionated stereotactic radiotherapy in patients with benign or atypical intracranial meningioma: long-term experience and prognostic factors. Int J Radiat Oncol Biol Phys 2005;61:809–16. Milker-Zabel S, Zabel-du Bois A, Huber P, et al. Fractionated stereotactic radiation therapy in the management of benign cavernous sinus meningiomas: long-term experience and review of the literature. Strahlenther Onkol 2006;182:635–40.
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RESEARCH PAPER
Visual disability rates in a ten-year cohort of patients with anterior visual pathway meningiomas Elite Bor-Shavit1,2, Naama Hammel1,2, Yoav Nahum1,2, Zvi Harry Rappaport3, and Hadas Stiebel-Kalish1,2,3 1
Department of Ophthalmology, Rabin Medical Center – Beilinson Campus, Petach Tikva, Israel, 2Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel, and 3Department of Neurosurgery and 4Department of Neuro-Ophthalmology Unit, Rabin Medical Center – Beilinson Campus, Petach Tikva, Israel Abstract
Keywords
Purpose: To examine the visual outcome of anterior visual pathway meningioma (AVPM) patients followed for at least one year. Methods: Data were collected on demographics, clinical course and management. Visual disability was classified at the first and last examination as follows: I – no visual disability; II – mild visual defect in one eye; III – mild visual defect in both eyes; IV – loss of driver’s license; V – legally blind. Results: Eight-one AVPM patients had their tumor originate in the clinoid process in 23 (28%), sphenoid-wing area in 18 (22%), cavernous sinus in 15 (19%), tuberculum sellae in 8 (10%), and mixed in 17 (21%). On last examination, 46 patients (57%) had good visual acuity in one or both eyes (Class I or II) and 17 (21%) were mildly affected in both eyes. The rate of Class IV disability was 16%, and Class V disability was 6%. Conclusions: Attention needs to be addressed to the considerable proportion of patients with AVPM (22% in this study) who may lose their driver’s license or become legally blind. Occupational therapists should play an important role in the multidisciplinary management of those patients to help them adapt to their new physical and social situation.
Blindness, loss of driver’s license, optic nerve, tumor, vision History Received 7 December 2013 Revised 20 July 2014 Accepted 21 July 2014 Published online 18 August 2014
ä Implications for Rehabilitation
Anterior visual pathway meningiomas (AVPMs) are commonly not life-threatening but they can lead to profound visual disability, especially when the tumor originates in the tuberculum sellae and cavernous sinus. Particular attention should be paid to visual acuity and visual field deficits, as these can profoundly affect the patient’s quality of life including ability to drive and activities of daily living. The interdisciplinary management of patients with AVPM should include the neurosurgeon, neuro-ophthalmologist and occupational therapist. Also, early intervention by the occupational therapist can help patients adapt to their current physical and social situation and return to everyday tasks more rapidly.
Introduction Meningiomas located adjacent to the anterior visual pathway apparatus (clinoid process, tuberculum sellae, suprasellar cistern, sphenoid ridge, cavernous sinus or planum sphenoidale) are rarely life-threatening. However, they may lead to chronic progressive visual disability [1] with a consequent reduction in quality of life and increase in health-care costs and social burden [2]. Current treatment options of anterior visual pathway meningioma (AVPM) include fractionated stereotactic radiotherapy (FSRT) and surgery. However, more data on expected vision disability outcome are needed to assist resource planning and rehabilitation.
Address for correspondence: Elite Bor-Shavit, MD, Department of Ophthalmology, Rabin Medical Center – Beilinson Campus, Petach Tikva 49100, Israel. Tel: 972-3-937-6100. Fax: 972-3-937-6104. E-mail: [email protected]
The aim of this study was to determine long-term visual disability rates in a large cohort of patients with AVPM attending a major medical center. Patients and methods The electronic files of a tertiary, university-affiliated medical center were reviewed for all patients who were admitted with a diagnosis of AVPM in 2001–2011 and followed for at least 12 months. The study was approved by the local Institutional Review Board. According to our hospital protocol, patients with AVPM are carefully followed by a multidisciplinary team of medical specialists in neurosurgery, neuro-ophthalmology, radiation oncology and neuroradiology. The team holds weekly meetings to review new cases, monitor tumor progression in existing cases by revising magnetic resonance imaging scans and neuroophthalmological examinations, and recommend interventions on the basis of these findings.
Visual disability in meningiomas of visual pathway
DOI: 10.3109/09638288.2014.948141
For purposes of the present study, three sets of data were collected: patient demographics, disease-related parameters and vision-related parameters. Patient demographics included age at presentation and sex, prior history of radiation exposure and duration of follow-up (in years). Disease-related parameters included site of origin of the primary tumor, number and types of interventions, namely surgery with or without complementary FSRT, radiosurgery alone, or conservative follow-up with serial brain magnetic resonance imaging (in stable or asymptomatic patients), and clinical course (progression/recurrence) according to available surgical reports and neuroimaging studies. Visionrelated parameters included best corrected visual acuity (BCVA) in each eye using the Snellen chart, presence of a relative afferent pupillary defect, color vision using Ishihara color plates, visual fields measured by the automated Humphrey analyzer (24-2 or 30-2), presence of any other ocular pathology that could affect visual function and presence of optic atrophy. A worsening or improvement of two or more Snellen lines was recorded as a change in BCVA. On the basis of these findings, visual disability was classified for each patient at presentation and at most recent follow-up/final examination according to the method of Goel et al. [3]: Class I – no visual disability in either eye, Class II – mild visual defect, defined as best corrected visual acuity (BCVA) in the better eye of 6/12 or more and visual field at least 200, in one eye only, Class III – mild visual defect in both eyes, Class IV – permanent loss of driver’s license, as defined by the Driver’s Guide of the Canadian Medical Association, the accepted standard for the Israel Bureau of Transportation, Class V – legally blind.
of complications of aggressive meningioma, such as acute hydrocephalus and repeated shunting procedures (two patients) or non-neurological causes (eight patients). However, all had adequate visual follow-up for more than 12 months and were therefore eligible for inclusion in the study. Thus, the final study cohort consisted of 81 patients, 64 women (79%) and 17 men (21%) of mean age 63.7 ± 10.7 years (range: 45–94 years). Twelve patients (15%) had a prior history of exposure to radiation treatment for oncological, dermatological or other diseases. The tumor originated in the clinoid process in 23 patients (28%), sphenoid-wing area in 18 (22%), cavernous sinus in 15 (19%) and tuberculum sellae in 8 (10%); the remaining 17 patients (21%) had AVPM of mixed origin. Visual disability rates at presentation At presentation, 53 patients (66%) had good visual function in one or both eyes (Class I or II) (Figure 1). Thirteen patients (16%) had a mild bilateral defect (Class III), 14 (17%) had already lost their driver’s license (Class IV), and one patient (1.2%) with sphenoidwing AVPM was legally blind in both eyes (Class V). Analysis by tumor origin yielded the highest rate of visual disability at presentation in the patients with tuberculum sellae meningiomas, of whom half (4/8) were designated Class IV. The visual disability was the result of visual field defects in 31 patients (37%) and of optic neuropathy/atrophy in 40 (49%). In 53 patients (65%), additional ophthalmological conditions, such as cataract, glaucoma and retinal disease, contributed to the visual disability. The incidence of these additional conditions was compatible with the expected incidence in the age-matched general population. Visual disability rates at last follow-up
Results Patient demographics and tumor location A total of 1553 patients were diagnosed with intracranial meningiomas during the 10-year study period. In 107 patients, the meningioma was located close to or involved the optic pathway warranting neuro-ophthalmological consultation and follow-up. Of this group, 26 patients were excluded from the study because of incomplete ophthalmological data or less than 12 months’ follow-up. Ten patients (12%) died during follow-up,
Figure 1. Visual disability classification at presentation (top row) and last-follow-up (bottom row) by anatomic location of the AVPM. Class I – no visual disability in either eye; Class II – mild visual defect in one eye only; Class III – mild visual defect in both eyes (BCVA in the better eye of 6/12 or better with a visual field of at least 20 degrees); Class IV – loss of driver’s license (as defined by the Driver’s Guide of the Canadian Medical Association, the accepted standard in the Israel Bureau of Transportation); Class V – legally blind.
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Mean duration of follow-up was 4.3 ± 1.8 years (range 1.0–7.9 years). At the end of follow-up, 46 patients (57%) had good visual acuity (6/12 or better), in one or both eyes (Class I or II), 17 (21%) had a mild bilateral defect (Class III), 13 (16%) had lost their ability to drive (Class IV), and five (6%) were legally blind in both eyes (Class V). Analysis by tumor origin again yielded the worst visual disability in the patients with tubercullum sella AVPM, of whom 25% were designated Class V, followed by patients with
Class I 100% 90%
4
9
6
Class II
6
80%
Class IV 13
13 13
Class III
22
13
6
7 18
25 22
Class V
50 24 17 57 50%
25 33
48
6 17
27
70% 60%
12
1 17
18
16 28
13
38 13
40%
13
20
29
40 47
39
29
30% 17
25
25
20% 10% 0%
40 26
30 17
17
13
13
33
29
26 18
20
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Stability
Table 1. Visual disability classification at presentation and last examination in patients with AVPM by treatment strategy.
Deterioraon
100 90
20
11 27
33
80 70 60
25
12 40
56
30
20
50 40 63
30 20
40
47
43 33
10 0 Mixed AVPM Sphenoid (n=17) wing (n=18)
Clinoid (n=23)
Cavernous Tubercullum sinus (n=15) Sella (n=8)
Figure 2. Graphic representation of progression of visual disability from presentation to last follow-up in patients with AVPM.
Treatment Visual disability classa Class I, n (%) First examination Last examination Class II, n (%) First examination Last examination Class III, n (%) First examination Last examination Class IV, n (%) First examination Last examination Class V, n (%) First examination Last examination
Conservative Surgery Radiotherapy Radiotherapy + (n ¼ 14) (n ¼ 32) (n ¼ 27) surgery (n ¼ 8) 36 36
22 22
26 19
25 25
42 29
38 31
41 41
38 25
7 14
22 22
15 19
13 25
14 14
16 19
19 15
25 25
0 7
3 6
0 7
0 0
a
cavernous sinus meningioma, of whom 27% were designated Class IV and 7%, Class V. None of the patients with clinoid meningioma was declared legally blind throughout the 10-year study period. Visual disability progression Visual function deteriorated in 34 patients (42%), remained stable throughout follow-up in 28 (35%), and improved in 19 (23%). By tumor origin, anterior cavernous sinus AVPM was associated with the highest rate of improvement in visual function (5/15 patients, 33%), and tuberculum sellae meningioma with the highest rate of deterioration in visual function (3/8 patients, 37%) (Figure 2). Sphenoid-wing meningioma with associated with the highest rate of stable function during follow-up (10/18 patients, 56%). Tumor management and visual disability As different neurosurgeons were involved in the operative treatment, the approach was not uniform. However, in most cases of clinoid, parasellar and suprasellar tumors, lateral supraorbital craniotomy was performed, followed when necessary by extradural clinoidectomy and optic canal unroofing. For more laterally placed tumors, pterional craniotomy with sphenoid wing resection was the method of choice. Surgical resection or tumor debulking without adjuvant radiotherapy was performed in 32 patients (40%), FSRT alone in eight patients (10%), and combined surgery and FSRT in 27 patients (33%); the remaining 14 patients (17%) were followed conservatively. Mean number of surgical interventions per patient was 1.2 ± 1.8 (range, 0–5); most patients (28/81, 35%) had only one surgical procedure, and one patient (1.2%) with aggressive sphenoid-wing meningioma required five surgeries because of tumor recurrence. Additional procedures were performed when tumor progression was detected on radiological follow-up. At the end of the last visit, an improvement in visual function was noted in 12 patients (37%) in the surgery-only group, six patients (75%) in the radiation-only group, and three patients (12%) in the combined surgery-radiation group. Conservative management was associated with no change in visual function in five5 patients (36%) and improved function in one patient (7%). Deterioration in vision was found in eight of the 27 patients treated by combined surgery and radiation: one had concomitant ocular disease causing the deterioration, one following surgery, and six had tumor re-growth before referral to radiotherapy. There was no change in the remaining patients, including 5/14 patients
Class I – no visual disability in either eye; Class II – mild visual defect in one eye only (mild visual defect defined as best corrected visual acuity (BCVA) of 6/12 or better and a visual field of at least 20 degrees); Class III – mild visual defect in both eyes; Class IV – loss of driver’s license; Class V – legally blind.
(36%) treated conservatively. The visual disability rates by treatment strategies are summarized in Table 1.
Discussion Meningiomas of the anterior visual pathway are neither lifethreatening nor do they commonly lead to neurological disability [4]. Therefore, we believe particular attention should be addressed to their effect on vision, separately from other neurological outcomes, because of the impact of visual disability on vocational capacity, mobility and quality of life. In a unique report, NeilDwyer et al. [2] shed light on an additional aspect of disability, namely, the burden placed on care givers. The authors concluded that existing outcome scales focus on neurological status with or without mental health and pain components. Therefore, they might not be adequate for patients with AVPM-induced visual disability. The present study describes the visual outcome of a cohort of 81 patients with AVPM attending a single tertiary medical center over a 10-year period. Prior outcome studies of AVPM focused mainly on the success rates of treatment (surgical and radiotherapy), defined tumor control or visual stabilization [5–9]. To our knowledge, this is the first study to address final visual disability. We found that only 67% of patients had good visual acuity (6/12 or better in at least one eye) (Class I–III [3]), at the end of followup (mean, 4.3 years). A substantial proportion of the cohort (22%) were either unable to drive (Class IV) or legally blind (Class V), and consequently are expected to require a high level of care. Thus, these findings have important implications not only for neurosurgeons and neuro-ophthalmologists, but also for occupational and vocational therapists. We defined fitness to drive according Israeli law, which follows the recommendations of the Canadian Medical Association [10]. Immediate and permanent visual contraindications to driving are as follows: BCVA less than 6/15 (20/50) in both eyes, with the worse eye less than 6/120 (20/400); visual field less than 120 along the horizontal meridian and 15 continuous above and below fixation in both eyes; diplopia within the central 40 of the visual field (that is, 20 to the left and right, above and below fixation); and need for telescopic spectacles,
DOI: 10.3109/09638288.2014.948141
hemianopia aids and other low-vision aids. Visual conditions/ diseases that may lead to temporary loss of a driver’s license are recent functional change from binocular to monocular vision, including temporary patching of an eye; decrease in other visual functions, such as color vision, contrast sensitivity, depth perception, dark adaptation and glare recovery, and; other ophthalmic conditions, such as cataract, glaucoma and ptosis. In this study, we applied only the criteria pertaining to permanent loss of one’s license. Statutory blindness is defined as total loss of visual acuity to no light perception, maximal BCVA 6/120 (20/400) in the better eye or loss of 200o or more of the visual field in the better eye. Another important finding of the study was the difference in visual outcome by origin of the meningioma. Clinoid meningiomas are usually associated with a relatively good prognosis because they occur unilaterally. Tobias et al. [11] found that resection of clinoid meningiomas led to significant vision improvement in 77% of cases. However, Pompili et al. [12] reported an equal distribution of improvement, worsening and post-operative stabilization (32% each). In our cohort, 79% of patients with clinoid tumors had good to excellent visual ability at the end of follow-up. Sphenoid-ridge meningiomas account for approximately 20% of all supratentorial meningiomas. They have been associated with higher morbidity, mortality and recurrence rates than meningiomas in other locations [12–14], and with higher recurrence rates than other intracranial meningiomas [15]. However, Nakamura et al. [16] reported a large series of sphenoid-ridge meningiomas with a better outcome; vision improved or stabilized in 30% of patients, compared to 56% for cavernous-sinus tumors that did not involve the sphenoid ridge. Our study supports the latter study, with a 56% rate of vision stabilization and 11% improvement in patients with sphenoid-ridge meningiomas. Cavernous sinus meningiomas were found in one study to be associated with a relatively good visual outcome, but only small tumors without anterior optic nerve extension were included [6]. By contrast, in the present study, the cavernous sinus meningiomas were large and extended anteriorly to the visual apparatus. They led to visual deterioration in 33% of patients; the final outcome was Class IV in 20% and Class V in 7%. Tuberculum sellae meningiomas may extend into both optic canals and share their vascular supply with the optic chiasm and prechiasmic optic nerves. Accordingly, they pose a high risk of severely reduced monocular or binocular vision. The surgical treatment of tuberculum sella and suprasellar meningioma has been widely reported in the literature [16–22]. Recovery after any type of treatment, however, is generally poor [23]. Jen and Lee [24] reported an 87.5% rate of visual loss in 32 patients with suprasellar meningiomas, and Odebode et al. [25] reported an 86% rate. In our cohort, patients with tuberculum sellae meningioma had the most dramatic decline in visual function (63%), including 3/5 patients treated surgically. Half the group had either lost their driver’s license or was legally blind at the last follow-up visit. Mixed-type AVPM accounts for 9% of all intracranial meningiomas [26]. Often referred to as ‘‘hyperostotic meningiomas of the sphenoid wing", mixed-type AVPMs are clinically and pathologically distinct from routine sphenoid-wing meningiomas. They may remain undiagnosed until they become significantly large and involve adjacent structures, such as the planum sphenoidale, tuberculum sellae, anterior clinoid process, diaphragm sellae and medial sphenoid wing, making them difficult to treat. Studies report insidious visual loss from optic nerve or tract compression [15]. In a cohort of patients with mixed-type AVPM, Zevgaridis et al. [22] found that visual prognosis was favorably affected by younger age (554 years), early diagnosis, and an intact arachnoid
Visual disability in meningiomas of visual pathway
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membrane around the lesion. Severe pre-operative visual loss of BCVA appeared to be an unfavorable prognostic factor (p50.047). It is noteworthy that early diagnosis of visual compromise in AVPM is hampered by the lack of patient awareness of visual loss because of second-eye compensation or attribution of the visual loss to other known, co-existing ophthalmologic conditions. In many cases, the visual symptoms go unnoticed until the anterior visual system is irreversibly damaged [27]. Functional outcomes are gradually improving, thanks to the availability of improved surgical and radiosurgical treatment options (FSRT) and increasing clinician education on the need for early neuro-ophthalmological screening [9,28–30]. In conclusion, although AVPM meningiomas are commonly not life-threatening, they may lead to profound visual disability. In our cohort, nearly one-fourth of the patients with AVPM either lost their ability to drive or became legally blind in both eyes. The worst prognosis was associated with tuberculum sellae and larger cavernous-sinus meningiomas. These findings emphasize the need for the involvement of neurosurgeons and neuro-ophthalmologists in the interdisciplinary management of patients with AVPM, to limit visual acuity and visual field damage, and importantly, occupational therapists, to aid patients in adapting to their new physical and social situation and rapidly returning to everyday activities.
Declaration of interest The authors report no declarations of interest. No funding or financial support was received for this study.
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