Title | Neuro-Ophthalmic Manifestations of Sarcoidosis |
Creator | Amanda D. Henderson, MD; Jing Tian, MS; Andrew R. Carey, MD |
Affiliation | Wilmer Eye Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland |
Abstract | Sarcoidosis is an idiopathic, multisystem, inflammatory disease that has central nervous system involvement in 5%-15% of cases. The presentation of neurosarcoidosis is highly variable, and the MRI findings often mimic the appearance of other central nervous system diseases. Therefore, the diagnosis can be challenging. About one-third of neurosarcoidosis cases have neuro-ophthalmic manifestations and, thus, may be evaluated by a neuro-ophthalmologist early in the disease course |
Subject | Sarcoidosis; Neurosarcoidosis; CNS |
OCR Text | Show Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Neuro-Ophthalmic Manifestations of Sarcoidosis Amanda D. Henderson, MD, Jing Tian, MS, Andrew R. Carey, MD Background: Sarcoidosis is an idiopathic, multisystem, inflammatory disease that has central nervous system involvement in 5%–15% of cases. The presentation of neurosarcoidosis is highly variable, and the MRI findings often mimic the appearance of other central nervous system diseases. Therefore, the diagnosis can be challenging. About one-third of neurosarcoidosis cases have neuro-ophthalmic manifestations and, thus, may be evaluated by a neuroophthalmologist early in the disease course. Methods: We performed a retrospective review of 22 cases of biopsy-proven sarcoidosis with neuro-ophthalmic manifestations, seen at the Wilmer Eye Institute from January 2013 to September 2019, in which we described the demographic information, clinical presentations, neuroimaging findings, and diagnostic evaluations. Results: Twenty-two patients were included. Fifteen patients identified as black and 7 as white. Fifteen were women, and 7 men. Mean age at sarcoidosis diagnosis was 45.9 years (range 26–66). Neuro-ophthalmic findings included optic neuropathy in 11 (50%); proptosis/orbital inflammation in 5 (23%); abducens palsy in 5 (23%); trochlear palsy, trigeminal distribution numbness, and bitemporal hemianopia in 2 each (9%); and oculomotor palsy, facial palsy, optic perineuritis, dorsal midbrain syndrome, central vestibular nystagmus, and papilledema in 1 each (5%). Eight (36%) had a pre-existing diagnosis of sarcoidosis; however, in 14 (64%), the neuro-ophthalmic presentation led to the sarcoidosis diagnosis. Patients with a pre-existing sarcoidosis diagnosis were younger than those without this diagnosis (38.5 vs 50.1 years, P = 0.035). Brain MRI was abnormal in all but 1 case (95%). In patients without a pre-existing sarcoidosis diagnosis, all 7 tested for angiotensin converting enzyme (ACE) had normal values, and 75% of the 12 who had computed tomography (CT) chest had findings suggestive of sarcoidosis (86% of black patients vs 50% of white patients). Conclusions: Patients with neurosarcoidosis may present initially with a neuro-ophthalmic manifestation, and this presentation may be more common in older patients. MRI usually is abnormal, although findings may be nonspecific. Wilmer Eye Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland. Supported by Wilmer Biostatistics Core Grant EY01765. Serum testing for ACE is not helpful. Normal CT chest does not rule out underlying sarcoidosis, particularly in white patients. Journal of Neuro-Ophthalmology 2021;41:e591–e597 doi: 10.1097/WNO.0000000000001108 © 2020 by North American Neuro-Ophthalmology Society S arcoidosis is an idiopathic, multisystem disease, characterized pathologically by noncaseating granulomatous inflammation. Clinically, central nervous system involvement is present in about 5%–15% of patients with sarcoidosis, with about half of those patients initially presenting with a neurologic manifestation (1,2). The presentation of neurosarcoidosis is highly variable, and the MRI findings often mimic the appearance of other central nervous system diseases, including meningioma, infectious or carcinomatous meningitis, demyelinating disease, tuberculosis, granulomatosis with polyangiitis, lymphoma, or other neoplastic disease (3). Therefore, the diagnosis can be challenging. About one-third of neurosarcoidosis cases have neuroophthalmic manifestations (4). Therefore, patients may be evaluated by a neuro-ophthalmologist early in their disease course. Thorough knowledge of the neuro-ophthalmic findings that may be associated with neurosarcoidosis, their potential appearances on MRI, and the additional evaluations required to confirm the diagnosis, is helpful to avoid missing the diagnosis and to allow for appropriate treatment in a timely manner. As MRI technology improves, we now are able to characterize lesions neuroradiologically that may not have been visualized in the past (5). In this study, we describe the neuro-ophthalmic manifestations of neurosarcoidosis, including their neuroradiologic appearances, and we place particular emphasis on the imaging characteristics that should prompt further evaluation for sarcoidosis. The authors report no conflicts of interest. METHODS Address correspondence to Amanda D. Henderson, MD, Wilmer Eye Institute, Johns Hopkins University School of Medicine, 600 N. Wolfe Street, Wilmer 233, Baltimore, MD 21287; E-mail: ahende24@jhmi. edu This study was approved by the Institutional Review Board of the Johns Hopkins University School of Medicine before the initiation of data collection and complied with the Henderson et al: J Neuro-Ophthalmol 2021; 41: e591-e597 e591 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution Health Insurance Portability and Accountability Act. We performed a retrospective chart review of cases of biopsyproven sarcoidosis with neuro-ophthalmic manifestations seen at the Wilmer Eye Institute from January 2013 to September 2019. Forty cases were identified using search criteria of neurosarcoidosis diagnosis plus a documented ophthalmology encounter at our institution. Six were excluded because of lack of biopsy-proven sarcoidosis, and 12 because of lack of neuro-ophthalmic involvement. Twenty-two cases were included in the analyses. Collected data included demographics; presence and characteristics of ocular involvement; characterization of neuro-ophthalmic involvement; status of sarcoidosis diagnosis at the time of neuro-ophthalmic presentation; results of diagnostic testing including location of diagnostic biopsy, angiotensin converting enzyme (ACE) level, computed tomography (CT) chest findings, neuroimaging findings, positron emission tomography (PET) findings, and cerebrospinal fluid (CSF) analyses; and clinical course. Statistical analysis was performed using SAS 9.2 (SAS Institution, Cary, NC). For continuous variables, t test was used to compare the differences between 2 race groups. For categorical variables, Fisher exact test was used compare the percentage difference between 2 groups because of the small sample size. P , 0.05 was used to define statistical significance. RESULTS Twenty-two cases with biopsy-proven sarcoidosis and neuro-ophthalmic manifestations were included. Fifteen patients identified as black and 7 as white. Fifteen were women, and 7 men. Mean age at sarcoidosis diagnosis was 45.9 years (range 26–66, SD 12.7 years). Neuroophthalmic findings included optic neuropathy in 11 (50%); proptosis/orbital inflammation in 5 (23%); abducens nerve palsy in 5 (23%); trochlear nerve palsy (9%), trigeminal distribution numbness (9%), and bitemporal hemianopia (9%) in 2 each; and oculomotor nerve palsy (5%), facial palsy (5%), optic perineuritis (5%), dorsal midbrain syndrome (5%), central vestibular nystagmus (5%), and papilledema (5%) in 1 each. Among eyes with optic neuropathy, visual acuity nadir ranged from 20/20 to no light perception. In the eye with no light perception acuity, there was no improvement in vision with steroid treatment. However, there were some notable cases of marked visual improvement, including an eye with hand motion vision that improved to 20/20 with steroid therapy, although the ultimate visual outcome in this eye dropped to 20/30 after a relapse, and an eye with counting fingers vision that improved to 20/25 with steroid therapy. Clinical details of the optic neuropathy cases are shown in Table 1. Five patients had other ocular involvement, including 2 with anterior uveitis, 1 with conjunctival nodules, 1 with lacrimal gland involvement, and 1 with chorioretinitis, with 3 of these patients having no known sarcoidosis diagnosis at presentation. Eight patients (36%) had a pre-existing diagnosis of sarcoidosis at the time of presentation with a neuroophthalmic finding; however, in 14 cases (64%), the neuro-ophthalmic manifestation was the presenting feature that led to further evaluation and the sarcoidosis diagnosis. Patients who presented with a pre-existing sarcoidosis diagnosis were younger than those whose neuroophthalmic presentation led to the diagnosis (38.5 vs 50.1 years, P = 0.035). Diagnostic work up in patients without known sarcoidosis at the time of neuro-ophthalmic presentation demonstrated that all 7 tested for ACE had normal values, 9 of the 12 (75%) who had CT chest had findings suggestive of sarcoidosis (86% of black patients vs 50% of white patients), and 50% of the 10 who had lumbar TABLE 1. Clinical characteristics of sarcoidosis optic neuropathy Case Affected eye(s) Funduscopic Examination 1 OU Initially normal OU, developed disc pallor OU 3 5 6 7 OD OD OS OU 9 11 12 OS OS OU 14 16 17 OS OD OD Normal Disc pallor Initially normal, developed temporal disc pallor Initially normal OD, choroidal and optic nerve infiltration OS; developed disc pallor OU, chorioretinal atrophy OS Normal Normal Initially disc swelling OU with hemorrhage OS, developed disc pallor OU Initially mild disc edema, resolved with treatment Disc pallor Normal Visual Acuity Nadir Final Visual Acuity CF OD HM OS 20/60 20/150 CF 20/35 OD 20/50 OS 20/50 20/100 20/20 OD 20/125 OS 20/70 NLP 20/30 20/800 OD 20/30 OS 20/20 20/50 20/25 20/30 OD 20/50 OS 20/20 20/20 20/20 OD 20/20 OS 20/25 NLP No follow up CF, counting fingers; HM, hand motion; NLP, no light perception; OD, right eye; OS, left eye; OU, both eyes. e592 Henderson et al: J Neuro-Ophthalmol 2021; 41: e591-e597 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 1. Optic nerve enhancement. T1-weighted, postcontrast, fat-saturated axial MRI demonstrates left greater than right optic nerve enhancement in a patient with bilateral optic neuropathy. puncture had elevated monocytes and 60% had high protein. Among all included cases, of the 11 total patients who had PET scans performed, 8 (73%) showed findings consistent with sarcoidosis. Location of positive biopsy included 6 lymph nodes, 4 dura, 3 lung, 3 orbit, 2 skin, 2 brain, and 2 sinus. No statistically significant differences were found between the groups with and without a pre-existing sarcoidosis diagnosis in race, elevated ACE level, abnormal CT chest, location of positive biopsy, abnormal PET, and CSF composition. Among all included cases, 21 of the 22 patients had brain MRIs, and neuroimaging was abnormal in all but 1 case (95%). Notable abnormalities included optic pathway thickening and enhancement (Fig. 1), extraocular muscle enlargement (Fig. 2), enhancement of other cranial nerves (Fig. 3), suprasellar lesions (Fig. 4), and cavernous sinus enhancement (Fig. 5). Pachymeningeal enhancement, leptomeningeal enhancement, and periventricular white matter lesions also were common. Further characterization of the MRI findings is presented in Table 2, along with findings from previous series. All 22 patients were treated with systemic steroids. Eighteen received steroid sparing immunosuppressive treatment, including 12 treated with mycophenolate mofetil, 4 with infliximab, 4 with methotrexate, 3 with hydroxychloroquine, 3 with azathioprine, 3 with adalimumab, 1 with thalidomide, and 1 with rituximab. Twelve patients had relapsing disease, 9 improved, and 1 had no follow-up data available. Henderson et al: J Neuro-Ophthalmol 2021; 41: e591-e597 FIG. 2. Proptosis. T1-weighted, postcontrast, fat-saturated axial MRI demonstrates thickening and enhancement of the right orbital apex, lateral rectus, and temporalis muscle in a patient with right-sided proptosis and optic neuropathy. CONCLUSIONS In our study, nearly two-thirds of patients had no known sarcoidosis history at the time of their neuro-ophthalmic presentation. Prior studies of neuro-ophthalmic sarcoidosis have reported that a neuro-ophthalmic presentation led to the primary sarcoidosis diagnosis in 31%–88% of these cases (2,4,8,23,24,26). These data emphasize the importance of familiarity with possible neuro-ophthalmic presentations of sarcoidosis among neuro-ophthalmologists, and further diagnostic evaluations needed to heighten suspicion and to identify potential biopsy sites to confirm the diagnosis. Our study additionally showed that patients in whom sarcoidosis initially presented with a neuro-ophthalmic manifestation were older than those who already carried this diagnosis, suggesting that ophthalmologists may need to maintain higher suspicion for primary neuro-ophthalmic sarcoidosis in older patients. Optic neuropathy was the most common neuroophthalmic feature of neurosarcoidosis in our series. Our series agrees with previous reports that have shown that no light perception vision is not uncommon in these cases; interestingly, the presence of no light perception acuity does not preclude visual recovery in all cases (4,13,24). Although the patient with no light perception acuity in our study did not improve with steroid treatment, there were cases of hand motion and counting fingers vision that improved markedly with steroid treatment. Therefore, our data, along e593 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 4. Pituitary stalk thickening and enhancement. T1-weighted, post-contrast, coronal MRI demonstrates diffuse leptomeningeal enhancement with multiple areas of focal nodular enhancement and thickening and enhancement of the pituitary stalk. setting of a neuro-ophthalmic abnormality is unlikely with a completely normal MRI. Since a brain MRI with gadolinium enhancement often is ordered early in the work up of FIG. 3. Cranial nerve enhancement. T1-weighted, postcontrast, axial MRI demonstrates leptomeningeal enhancement with prominent enhancement of the left oculomotor nerve in a patient with diplopia. with previously published data on this topic, emphasize the importance of recognition of sarcoidosis in these cases of optic neuropathy, to allow for appropriate treatment, because this may result in substantial visual improvement for these patients. Other findings in our study included proptosis, orbital inflammation, cranial nerve palsies, bitemporal hemianopia, dorsal midbrain syndrome, nystagmus, and papilledema. The spectrum of neuro-ophthalmic findings in our patient series overlaps with that of previously reported findings, which have included cranial nerve palsies, tonic pupil, nystagmus, Parinaud syndrome, cavernous sinus syndrome, Horner syndrome, and homonymous visual field defects due to optic tract or occipital lobe involvement (2,4,8,23,24,26). Seventh nerve palsy is the most commonly reported manifestation of neurosarcoidosis in the literature, although this was not the case in our study (27). These data describe the most common neuroophthalmic presentations of sarcoidosis but also, perhaps more importantly, highlight the broad spectrum of neuroophthalmic presentations of sarcoidosis, thus emphasizing the importance of maintaining suspicion for sarcoidosis as work up of any of these neuro-ophthalmic issues is pursued. We found that 95% of patients had an abnormal brain MRI, suggesting that a diagnosis of neurosarcoidosis in the e594 FIG. 5. Orbital apex syndrome. T1-weighted, postcontrast, axial MRI demonstrates enhancing right cavernous sinus lesion, mimicking meningioma, which extends to the orbital apex, in a patient with right orbital apex syndrome. Henderson et al: J Neuro-Ophthalmol 2021; 41: e591-e597 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 2. Brain MRI appearance of neuro-ophthalmic sarcoidosis Study Anthony et al. (6) Carmody et al. (7) Christoforidis et al. (8) Dash et al. (9) Earle et al. (10) Elia et al. (11) Heuser and Kerty (2) Ing et al. (12) Kidd et al. (13) Koczman et al. (4) Maust et al. (14) Ng et al. (15) Pollock et al. (16) Reed et al. (17) Tadayonnejad et al. (18) Tanyildiz et al. (19) Verma and Praharaj (20) Wilson et al. (21) Zhang et al. (22) Our study Study Anthony et al. (6) Carmody et al. (7) Christoforidis et al. (8) Dash et al. (9) Earle et al. (10) Elia et al. (11) Heuser and Kerty (2) Ing et al. (12) Kidd et al. (13) Koczman et al. (4) Maust et al. (14) Ng et al. (15) Pollock et al. (16) Reed et al. (17) Tadayonnejad et al. (18) Tanyildiz et al. (19) Verma and Praharaj (20) Wilson et al. (21) Zhang et al. (22) Our study No. of Cases with MRI Brain Optic Pathway Thickening/Enhancement 4 15 82* 1 1 1 7 1 51 19 3 1 1 1 1 1 1 3 1 21 4 9 4 Extraocular Muscle Enlargement Enhancement of Other Cranial Nerves Sellar/Suprasellar Lesion Cavernous Sinus Enhancement 1 1 3 1 1 1 1 1 27 12 2 1 1 1 1 1 1 1 1 7 1 2 1 2 1 3 5 Lacrimal Gland Enlargement/Enhancement Periventricular White Matter Lesions Intraorbital/Intracranial Mass Lesion Leptomeningeal Enhancement 3 5 2 3 1 3 Pachymeningeal Enhancement 1 1 1 1 1 1 16 3 1 1 1 1 1 1 1 1 1 1 1 7 4 3 2 6 4 *Eighty-two scans from 34 patients with CNS sarcoidosis, patients included in this table had neuro-ophthalmic involvement. CNS, central nervous system. a patient with an unexplained neuro-ophthalmic problem, this finding provides valuable information to guide the work up of these patients. Findings including leptomeningeal and/or pachymeningeal enhancement, lacrimal gland enlargement, optic pathway thickening and enhancement, extraocular muscle enlargement, cranial nerve enhancement (particularly when involving multiple cranial nerves or occurring in association with leptomeningeal enhancement), and enhancing lesions of the cavernous sinus, orbit, or suprasellar region, should raise suspicion for neurosarcoidosis and prompt further diagnostic evaluation. Previously reported MRI findings in neuro-ophthalmic sarcoidosis mirror our findings and include pathologic enhancement of the optic nerves, optic nerve sheaths, Henderson et al: J Neuro-Ophthalmol 2021; 41: e591-e597 chiasm, optic radiations, cavernous sinus, pachymeninges, leptomeninges, and cortical parenchyma, and orbital masses that may mimic other neoplastic or inflammatory processes, including meningioma, glioma, and orbital pseudotumor (2,4,7,9,11–13,23,28). Although noncontrasted MRI may show optic nerve thickening in cases of anterior visual pathway involvement, the use of gadolinium greatly increases the sensitivity of MRI for neurosarcoidosis (7,29). Interestingly, in contrast to the findings of our study, only 43%– 85% of patients with neuro-ophthalmic findings attributed to neurosarcoidosis have been shown to have abnormal brain imaging in past reports (2,4,23–25). Specifically, it has been reported that 40% of cranial nerve palsies attributable to sarcoidosis do not show abnormalities on e595 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution gadolinium-enhanced MRI (8). Possible explanations for the discrepancy between our findings and those of prior reports reflect technical limitations of the imaging itself, inclusion of cases of peripheral facial nerve palsy attributable to parotid gland involvement (Heerfordt syndrome), or misdiagnosis in prior series, as only one of these studies used biopsy-proven disease as an inclusion criterion (4). However, as neuroimaging technology improves, specifically with higher resolution MRI capabilities, we are better able to characterize neuroinflammatory lesions, including those from neurosarcoidosis. Therefore, it is not surprising that our study found a higher rate of abnormal neuroimaging than prior reports. Because we only included cases that presented in 2013 or later, this higher rate of abnormal MRI likely is reflective of modern clinical practice. Suspicion for neurosarcoidosis should be heightened and further testing pursued if MRI findings could be consistent with this condition. If neurosarcoidosis is suspected, then further work up should be pursued with chest imaging, which can assess for characteristic findings of hilar lymphadenopathy and may allow for the pursuit of definitive pathologic diagnosis with a minimally-invasive bronchoscopy with biopsy of the involved lymph nodes (30). Interestingly, our study found that, among patients without a known history of sarcoidosis, 75% of those who had a CT chest performed as part of their diagnostic work up had findings suggestive of sarcoidosis. However, the rate of abnormal CT chest was much higher in black than in white patients, although this finding did not reach statistical significance. This suggests that a normal CT chest may not be adequate to “rule out” sarcoidosis in a white patient presenting with a neuro-ophthalmic manifestation. In this case, if CT chest is unremarkable, but suspicion for sarcoidosis remains high, then full body PET may be used to evaluate for sarcoidosis involvement elsewhere in the body and potentially locate an area in which biopsy may be pursued (31). Although ACE frequently is considered as a biomarker for sarcoidosis, we found that none of the patients initially presenting with neuro-ophthalmic manifestations had an elevated ACE, demonstrating that ACE is not useful in this setting. The low sensitivity of ACE for diagnosis of neuroophthalmic sarcoidosis, as well as for diagnosis of sarcoidosis in general, has been reported previously (4,23,28,31–35). Although the focus of this article is neuro-ophthalmic involvement, it is important to note that ophthalmic involvement also is common in sarcoidosis and has been reported in 22%–60% of cases (36). Because ophthalmologists have the tools and abilities to perform thorough ocular examinations, we have the unique opportunity to evaluate for ocular involvement, which, when present, may heighten our suspicion for an underlying diagnosis of sarcoidosis. Common eye findings in sarcoidosis include dry eye due to lacrimal gland involvement, conjunctival nodules, granulomatous anterior uveitis, cystoid macular edema, choroidopathy that can present with punched-out e596 lesions or with granuloma formation, and periphlebitis (36,37). Coexistence of classic ocular signs of sarcoidosis may increase suspicion for this underlying disease; however, absence of these findings does not exclude the possibility of sarcoidosis. In conclusion, although the neuro-ophthalmic presentations of sarcoidosis vary, optic neuropathy, not infrequently presenting with very poor acuity; proptosis; orbital inflammation; and cranial nerve palsies are common. MRI brain with gadolinium is appropriate for further evaluation of these issues in the setting of an unknown cause, and findings consistent with neurosarcoidosis, as described in detail in the Table 2 and the Figures, should raise suspicion for sarcoidosis and prompt further evaluation with CT chest in all patients, with need to proceed to PET if CT chest is unremarkable, particularly in white patients or older patients. In addition, in the setting of abnormal MRI, lumbar puncture findings of elevated protein and elevated monocyte count should raise suspicion for neurosarcoidosis. Coexisting ophthalmic findings, including conjunctival nodules, uveitis, and chorioretinopathy, are suggestive of sarcoidosis, as well. Unfortunately, serum ACE is not a helpful biomarker in ruling out neurosarcoidosis. Finally, if the diagnosis remains unclear despite extensive evaluation, a rapid and marked improvement in neuro-ophthalmic symptoms with initiation of steroid treatment is supportive of a diagnosis of neurosarcoidosis. Limitations of this study include its retrospective nature and relatively small sample size, which may have limited our ability to detect statistically significant differences between the groups of patients with and without a prior sarcoidosis diagnosis. Multicenter studies to obtain a larger number of cases could be helpful in further elucidating the differences between these groups. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: A. Henderson; b. Acquisition of data: A. Henderson; c. Analysis and interpretation of data: A. Henderson, J. Tian, and A. R. Carey. Category 2: a. Drafting the manuscript: A. Henderson; b. Revising it for intellectual content: A. Henderson, J. Tian, and A. R. Carey. Category 3: a. Final approval of the completed manuscript: A. 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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 |
Publisher | Lippincott, Williams & Wilkins |
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