Title | Is Neuroretinitis Associated With Multiple Sclerosis? |
Creator | N. R. Miller; L. N. Johnson; T. Bakaeva; G. P. Van Stavern; A. G. Lee |
OCR Text | Show Point Counter-Point Section Editors: Andrew G. Lee, MD Gregory P. Van Stavern, MD Is Neuroretinitis Associated With Multiple Sclerosis? Neil R. Miller, MD, Lenworth N. Johnson, MD, Tatiana Bakaeva, MD, PhD, Gregory P. Van Stavern, MD, Andrew G. Lee, MD G. P. Van Stavern, MD and A. G. Lee, MD Although demyelinating optic neuritis (ON) is commonly associated with and often a presenting event for multiple sclerosis (MS), neuroretinitis has traditionally been believed to be unrelated. Recent literature has called this into question. Three experts debate whether neuroretinitis is causal or coincidental to MS. PRO: Neuroretinitis is Associated With Multiple Sclerosis—T. Bakaeva, MD, PhD and L. N. Johnson, MD, MA In the waning months of 2019, the novel severe acute respiratory syndrome coronavirus 2 disease (COVID-19) silently took the stage waiting its turn. And then one by one, it gripped and decimated the Kent (pseudonym) family, save one member. Sarah (pseudonym) had been hospitalized, but not for COVID-19. She seemed lucky, but in reality, good luck was not her friend. Sarah was accidently struck in the left leg by a baseball and that afternoon her right leg was hit by a passing car as she crossed the street. Although both legs had sustained trauma and both had the same yellowish hue with surrounding red discoloration, x-rays soon revealed Sarah had a compound fracture of the right leg. This time, Sarah’s doctors were optimistic about her recovery and ability to walk after stabilizing the bones in her leg. By contrast, almost 1 year ago, they were less sanguine when she had several months of inability to walk due to right leg weakness and simultaneous eye pain with near complete loss of vision in her right eye. “Wow! That’s awesome,” said the medical students as each got their turn to look deep into Sarah’s eyes with the light emanating from the instrument on their heads while holding a 20-diopter lens in their outstretched hands. The right optic nerve was pale from the past bout of ON. By contrast, the left optic nerve was very plump, and white linear residue could be seen Wilmer Eye Institute (NRM), Johns Hopkins University School of Medicine, Baltimore, Maryland; Neuro-Ophthalmology Unit (LNJ, TB), Warren Alpert Medical School of Brown University, Lifespan, Rhode Island Hospital, Providence, Rhode Island; Department of Ophthalmology and Visual Sciences (GPVS), Washington University in St. Louis School of Medicine, St. Louis, Missouri; and Chair, Blanton Eye Institute (AGL), Houston Methodist Hospital, Houston, Texas. The authors report no conflicts of interest. Address correspondence to Gregory P. Van Stavern, MD, Department of Ophthalmology and Visual Sciences, Washington University in St. Louis School of Medicine, 660 S. Euclid Avenue, St. Louis, MO 63110-1010; E-mail: vanstaverng@vision.wustl.edu 126 forming a star-shaped appearance in her macula. About a year ago, when the right eye was affected, there was only moderate swelling of the right optic nerve, with no evidence of stellate exudates in the macula. Her visual loss and inability to walk at that time resolved over 3 months. The medical team wondered out loud whether Sarah had now developed MS. MS is an inflammatory demyelinating disease of the central nervous system. Intraocular inflammation in association with MS can manifest as intermediate uveitis or pars planitis, diagnosed by the presence of retinal periphlebitis and inflammatory cellular aggregates in the anterior vitreous and pars plana (1). ON is an inflammatory demyelinating disorder in MS. ON can be a clinically isolated syndrome preceding the diagnosis of MS in up to 20% of patients. In addition, 38%–50% of patients with MS will develop ON at some point during the course of MS (2). Among individuals who have ON preceding the diagnosis of MS, most (67%) will have a normal appearing optic nerve—so-called retrobulbar ON— that affects the orbital, intracanalicular, or intracranial segments of the optic nerve. In the remaining one-third (33%) of ON cases, the inflammation will affect the anterior part of the optic nerve and will cause visible optic disc edema, also known as anterior ON or papillitis. Anterior ON can be further subdivided into cases with a normal-appearing macula and those with concomitant subretinal fluid and macular exudates. The latter condition, in which a partial or complete “macular star” forms from the lipoproteinaceous exudates in the Henle layer, is termed neuroretinitis (3,4). Neuroretinitis is a nonspecific finding however, just as fever is a sign of disease but not the etiology per se. A plethora of diseases and disorders are associated with neuroretinitis, principally infections caused by viral, bacterial (particularly cat-scratch disease), fungal, and helminthic agents (e.g., diffuse unilateral subacute neuroretinitis). In addition, neuroretinitis has occurred with inflammatory/immunologic disorders (e.g., Miller et al: J Neuro-Ophthalmol 2022; 42: 126-130 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Point Counter-Point sarcoidosis and systemic lupus erythematosus), idiopathic retinal vasculitis, retinal aneurysm, neuroretinitis, nonarteritic anterior ischemic optic neuropathy, idiopathic intracranial hypertension (pseudotumor cerebri), and ON. Notably, neuroretinitis was present in approximately 2% of 388 participants enrolled in the Optic Neuritis Treatment Trial (ONTT) (5–7). However, in the ONTT, participants were enrolled within 8 days from onset of vision loss, and macular exudates typically occur within 1–3 weeks of symptom onset. The design of ONTT did not include funduscopic photographs during follow-up visits. Consequently, the true incidence of neuroretinitis in ON could be greater than 2 percent. Parmley et al published a report in 1987 that combined and updated their previously published 1984 articles on neuroretinitis (3,8,9). Because none of their patients developed MS, Parmley et al (8) opined that neuroretinitis was not associated with MS. Subsequently, the ONTT authors— some of whom were coauthors of the Parmley’s articles—also declared that neuroretinitis is not associated with MS, when none of the 8 participants with neuroretinitis in the ONTT developed MS (6,7). It is important to recall the polemic, “Absence of evidence is not evidence of absence” (10). Parmley et al (8) had followed 23 patients prospectively, 10 of whom were physically examined between 1 and 2 years after symptom onset and 13 were evaluated only by telephone interviews over an average of 8 years. In the ONTT, a prospective randomized cohort study, 16% of participants who had no MRI lesions at the onset of ON developed MS within 5 years (approximately 3% per year conversion to MS between years 1 and 5) and a total of 22% had MS by 10 years (approximate conversion rate of 1% per year between years 6 and 10) (5–7). Based on the aforementioned data, we would expect possibly 3 patients (0.3–0.6 of 10 participants followed for 1–2 years and 2.4 of 13 participants followed for 8 years) to develop MS in the Parmley report. In addition, all 8 participants in the ONTT with neuroretinitis had normal MRI on initial examination. Consequently, we would expect possibly 2 (22%) of the 8 participants in the ONTT to convert to MS within 10 years. The absence of conversion to MS in these studies is limited by the small sample sizes of neuroretinitis cases. Nonetheless, Parmley et al did indicate that 3 of their retrospectively evaluated patients with neuroretinitis did have neurologic manifestations that resolved (2 had numbness of the left side of the body—one of whom had abnormal somatosensory evoked potential and one had urinary urgency and incontinence). We would argue that these 3 patients could have had MS. In 2004, Williams and Johnson (11) in a retrospective analysis of 35 consecutive patients with neuroretinitis identified 3 patients (8.6%) with a diagnosis of MS. All 3 patients had previous episodes of ON, and the episodes of neuroretinitis occurred 1, 4, and 10 years after the diagnosis of MS. Therefore, it is certainly possible that neuroretinitis could be associated with MS. It is also possible that neuroretinitis is more often a late finding in MS, rather than an initial presenting event. Williams and Johnson had noted a potential confounder that 2 of their 3 patients had previous use of b-interferon (Avonex [Biogen, Cambridge MA] or Betaseron [Bayer, Leverkusen, Germany]) and one patient had concurrent use of b-interferon when the neuroretinitis developed. Moura et al (12) and Lee and El-Dairi (13) described cases of neuroretinitis in myelin oligodendrocyte glycoprotein antibody–associated disease (MOGAD)— another demyelinating disorder of the central nervous system that has predilection for the optic pathways. An independent study of the serum of 177 participants in the ONTT identified 3 cases (1.7%) of MOGAD (14). All 3 cases had optic disc edema, normal initial MRI, and none developed MS over 15 years apart from one participant who had a recurrent bout of ON. None of those 3 participants had neuroretinitis with macular star formation. Regrettably, none of the patients in the Williams and Johnson or Parmley et al’s series were tested for MOG antibody because this test was not yet available. In summary, neuroretinitis is a sign of significant optic nerve inflammation with disc edema and leakage of lipoproteinaceous fluid from the peripapillary optic disc vessels to the macula causing a macular star formation. Although more often observed in infections such as catscratch disease, it is present in at least 2 percent of cases of ON. Because of the scarcity of patients with combined ON and macular star formation, the true relationship of neuroretinitis and MS remains uncertain. Nevertheless, neuroretinitis has been reported in association with MS, but it may be a later manifestation. A prospective study of patients with idiopathic neuroretinitis may provide further insights into the correlation of neuroretinitis and MS. Neuroretinitis is Not Associated With Multiple Sclerosis—Neil Miller, MD In 1916, T. Leber described a condition characterized by acute unilateral visual loss associated with an exudative maculopathy consisting of hard exudates arranged in a star figure around the fovea (15). Leber believed that the condition was a primary retinal process and called it a “stellate maculopathy.” The condition subsequently became known as Leber stellate maculopathy (16) until 1977, when Gass (17) reported that patients Miller et al: J Neuro-Ophthalmol 2022; 42: 126-130 with the condition showed swelling of the optic disc before and often concurrent with the appearance of the star figure. The optic disc swelling then resolved, leaving the maculopathy as the primary or sole ophthalmoscopic abnormality. Gass (17) also performed fluorescein angiography in several of the patients with this condition and showed that there was no leakage from retinal vessels surrounding the macula. He thus concluded that the 127 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Point Counter-Point condition was not a primary maculopathy, but rather a form of ON with the star figure occurring from spread of fluid from optic disc vessels. Because the condition affected both the optic nerve and the retina, he called it neuroretinitis and emphasized that it occurred commonly in children and young adults, up to 50% of whom had an antecedent viral illness, usually affecting the respiratory tract, a few weeks before the onset of visual symptoms. It subsequently has become clear that some cases of neuroretinitis are associated with infectious diseases, whereas others occur as apparently isolated phenomena (3,4,9,18,19). Neuroretinitis is believed to be an infectious or immunemediated process that may be precipitated by a number of different agents, including viruses. A common association is with an antecedent viral syndrome, suggesting a possible viral etiology for up to 50% of cases; however, viruses rarely are cultured from the cerebrospinal fluid of such patients, and serologic evidence of a concomitant viral infection usually is absent (3,9,17); however, one case of neuroretinitis associated with herpes simplex encephalitis was reported by Johnson and Wisotzkey (20), as was a case of bilateral neuroretinitis associated with serologic evidence of hepatitis B virus infection (21). Foster et al (22) reported a case of neuroretinitis that occurred in a young man with mumps. Neuroretinitis may occur in patients with evidence of infectious disease caused by organisms other than viruses (18,19,23). In my experience and that of others, cat-scratch disease is the most common infectious process associated with neuroretinitis (4,19). Neuroretinitis also can occur in association with Bartonella henselae and, less frequently, with B. quintana infections but without clinical evidence of cat-scratch disease (24). Other common infections include syphilis (25– 28) and Lyme disease (29). Patients with toxoplasmosis, toxocariasis, histoplasmosis, and even helminthic infections may develop an acute anterior ON that, in rare cases, is associated with a macular star figure (30–34). Whether such conditions truly are examples of neuroretinitis is unclear, but I believe that any presumed or known inflammatory or infectious optic neuropathy that is characterized by optic disc swelling and the eventual development of a macular star figure not caused by leakage from macular vessels should be defined as neuroretinitis; thus, these cases would fit that description as would cases of anterior ON with a macular star associated with antibodies to myelin oligodendrocyte glycoprotein (12,13). On the other hand, there are cases of optic disc swelling that should never be mistaken for neuroretinitis although they are characterized by optic disc swelling that, on occasion, is associated with the development of a macular star figure. These mimicking conditions include papilledema and anterior ischemic optic neuropathy (particularly in patients with diabetes mellitus). Systemic hypertension also may cause both optic disc swelling and a macular star figure (35), but fluorescein angiography in such cases shows leakage from macular vessels. 128 One condition that is not associated with neuroretinitis is MS. One might assume that because neuroretinitis is a form of anterior ON, the likelihood of developing MS after an attack of neuroretinitis would be as high as it is after an attack of straightforward ON. However, although the rate of development of MS after an attack of anterior or retrobulbar ON is substantial, there is no increased tendency for patients who experience an attack of neuroretinitis to develop MS. Parmley et al (8) reviewed the literature on the development of MS after an attack of ON and rarely found a comment on the presence of a macular star. They also calculated that the rate of development of MS in patients with neuroretinitis was the same as that in the normal population, about 6–80 per 100,000. Finally, they looked at 50 of their own patients with neuroretinitis and found that none of the 13 patients contacted retrospectively after a mean period of 8 years had developed MS nor had 10 patients followed prospectively for 1–2 years, although they stated that 3 of the patients had “other neurologic manifestations” that were insufficient to diagnose MS. In a letter to the editor regarding this article, Wilson and Smith (36) emphasized some limitations of the study, namely 1) the follow-up period for the 10 patients followed prospectively was somewhat short, 2) the authors’ series was small, and 3) the fact that 3 patients had “other neurologic manifestations” might suggest that the patients really did have MS or a similar process. Subsequently, Williams and Johnson (11) performed a retrospective review of 35 patients with neuroretinitis seen in a single university-based practice. In none of these patients had MS occurred after the occurrence of neuroretinitis, although 3 patients had already developed MS at the time of diagnosis. All 3 patients were taking b-interferon when the neuroretinitis occurred, and the authors suggested that this treatment might have influenced the permeability of disc vessels, thus affecting the funduscopic appearance. In a review of neuroretinitis, Purvin et al (4) stated that one of their patients developed relapsing-remitting MS after experiencing neuroretinitis; however, the neuroretinitis was attributed to cat-scratch disease, and the MS occurred 11 years after the neuroretinitis occurred. For these reasons, I agree with Purvin et al that neuroretinitis 1) is never the presenting sign of MS and 2) does not increase the risk of the subsequent development of MS. Thus, the designation of an acute anterior optic neuropathy associated with a macular star figure as neuroretinitis rather than a “typical” anterior ON substantially alters the systemic and neurological prognoses in the patient being evaluated, and the evaluation and management of patients with neuroretinitis should be very different from that of patients with anterior ON. Miller et al: J Neuro-Ophthalmol 2022; 42: 126-130 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Point Counter-Point Rebuttal—Drs. T. Bakaeva and L. N. Johnson As Gass (17) postulated in 1977, neuroretinitis is not a maculopathy, but rather a form of anterior optic neuropathy when edema from the optic nerve head spreads to the macula leaving lipoproteinaceous material in the Henle layer forming a star-shaped figure. It seems that Dr. Miller agrees that neuroretinitis is not a separate pathological entity but rather the extreme on the spectrum of neuroophthalmological inflammatory and infectious disorders, on one end of which there is a retrobulbar ON and on the other neuroretinitis with a macular star. Based on the available data, the more anterior the optic nerve inflammation occurs, the less likely it is to be related to MS, and more likely to be infectious or idiopathic: Although 31% of patients with retrobulbar ON in the ONTT series eventually developed MS, the anterior ON was related to MS in only 14% of patients (7). Likewise, although neuroretinitis is more commonly seen in infectious diseases or as an idiopathic entity, the likelihood of that to be related to MS is not zero: In Williams and Johnson’s (11), series 3 of 35 patients (8.6%) with neuroretinitis had a diagnosis of MS, which is much higher than the prevalence of MS in the US population, which is about 300 per 100,000 or 0.3% (37). Based on Williams and Johnson’s data, neuroretinitis seems to be a late symptom of MS rather than a presenting feature. On the other hand, the true incidence of neuroretinitis in the ONTT series is unknown: The study design included funduscopic examination only at the time of enrollment, within 8 days from onset of vision loss, but not during the follow-up visits. In early neuroretinitis, papillitis may present without a macular star, and typical macular exudates are observed up to 1–3 weeks later. More longitudinal studies are needed to characterize the true association of neuroretinitis and MS, as well as to determine the exact risk of development of MS in these patients. Rebuttal—Dr. Miller There is no question that patients with MS can develop neuroretinitis and that patients with neuroretinitis can develop MS. The issue for me is whether the 2 are related. To date, there is no convincing evidence that there is an association, particularly as MS is a common disorder. Indeed, it seems to me that evaluating a patient with neuroretinitis for MS is similar to evaluating a patient with a unilateral, insidious onset, slowly progressive optic neuropathy for MS. If you want to do it, fine, but just as the first patient should be considered to have a compressive process until proven otherwise, for a patient with neuroretinitis, first consider the “usual suspects,” that is, infectious or non-MS inflammatory causes! In addition, remember that the macular star figure usually develops a week or 2 after the patient becomes symptomatic and disc swelling is seen (although optical coherence tomography may show early macular exudates not obvious on clinical examination). A couple of other points require emphasis (or re-emphasis). First, I believe the term “neuroretinitis” should be reserved for cases of anterior optic neuropathy known or suspected to be caused by infection or inflammation (i.e., patients with an ON). It should not be used for patients with macular exudates associated with severe papilledema, anterior ischemic optic neuropathy, etc. Sec- Miller et al: J Neuro-Ophthalmol 2022; 42: 126-130 ond, the MRI performed in participants in the ONTT was done when the software used to obtain fluid-attenuated inversion recovery images was not yet available nor was there any paramagnetic contrast material used. Thus, the findings (or lack thereof) in the patients enrolled in the ONTT must be taken with a grain of salt. Finally, as my colleagues Bakaeva and Johnson contributed a patient anecdote, I will provide one of my own. One of the patients who was enrolled in the ONTT was a young woman—a professional ice skater—who presented with acute, monocular visual loss and was found to have a unilateral anterior optic neuropathy. She was told of the possible association of anterior ON and MS (she was devastated, particularly because if she developed MS, it might mean the end of her career), the treatment options available to her, and the option of participating in the ONTT. She agreed to be enrolled in the ONTT. She returned a few weeks later, at which time her disc swelling was resolving and she now had an obvious macular star. At this point, I asked her if she had any pets, and she told me she had 2 cats that occasionally scratched her. Subsequent Bartonella titers were positive. She made a complete recovery and over the next 15 years was well with no evidence of MS. 129 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Point Counter-Point Summary and Conclusion—Drs. A. G. Lee and G. P. Van Stavern Although it is clear that neuroretinitis can occur in the setting of MS, it is still uncertain whether it is causally related or coincidental. Importantly, whether an episode of neuroretinitis increases the risk for the future development of MS remains controversial. Similarly, the question of whether an episode of neuroretinitis counts as a demyelinating attack remains unanswered. Longitudinal studies are needed to better answer these questions about MS and neuroretinitis. REFERENCES 17. Gass JDM. Diseases of the optic nerve that may simulate macular disease. Trans Am Acad Ophthalmol Otolaryngol. 1977;83:766–769. 18. Brazis PW, Lee AG. Optic disk edema with a macular star. Mayo Clin Proc. 1996;71:1162–1166. 19. Abdelhakim A, Rasool N. Neuroretinitis: a review. Curr Opin Ophthalmol. 2018;29:514–519. 20. Johnson BL, Wisotzkey HM. Neuroretinitis associated with herpes simplex encephalitis in an adult. Am J Ophthalmol. 1977;83:481–489. 21. Farthing CF, Howard RS, Thin RN. Papillitis and hepatitis B. Br Med J. 1986;292:1712. 22. Foster RE, Lowder CY, Meisler DM, Kosmorsky GS, BaetzGreenwalt B. Mumps neuroretinitis in an adolescent. Am J Ophthalmol. 1990;110:91–93. 23. Fairbanks AM, Starr MR, Chen JJ, Bhatti MT. Treatment strategies for neuroretinitis: current options and emerging therapies. Curr Treat Options Neurol. 2019;21:36. 24. Celiker H, Kazokoglu H, Eraslan M, Cerman E, Karabas L. Bartonella henselae neuroretinitis in patinets without cat scratch. Jpn J Infect Dis. 2018;71:397–401. 25. Fewell AG. Unilateral neuroretinitis of syphilitic origin with a striate figure in the macula. Arch Ophthalmol. 1932;8:615. 26. Folk JC, Weingeist TA, Corbett JJ, Lobes LA, Watzke RC. Syphilitic neuroretinitis. Am J Ophthalmol. 1983;95:480–486. 27. Veldman E, Bos PJ. Neuroretinitis in secondary syphilis. Doc Ophthalmol. 1986;64:23–29. 28. Halperin LS. Neuroretinitis due to seronegative syphilis associated with human immunodeficiency virus. J Clin Neuroophthalmol. 1992;12:171–172. 29. Lesser RL, Kornmehl EW, Pachner AR, Kattah J, Hedges TR 3rd, Newman NM, Ecker PA, Glassman MI. Neuroophthalmologic manifestations of Lyme disease. Ophthalmology. 1990;97:699–706. 30. Manschot WA, Daamen CBF. Congenital ocular toxoplasmosis. Arch Ophthalmol. 1965;74:48–54. 31. Bird AC, Smith JL, Curtin VT. Neomatode optic neuritis. Am J Ophthalmol. 1970;69:72–77. 32. Brown GC, Tasman WS. Retinal arterial obstruction in association with presumed Toxocara canis neuroretinitis. Ann Ophthalmol. 1981;13:1385–1387. 33. Moreno RJ, Weisman J, Waller S. Neuroretinitis: an unusual presentation of ocular toxoplasmosis. Ann Ophthalmol. 1992;24:68–70. 34. MacGrory B, Cheng D, Fisayo A. Toxoplasma neuroretinitis. RI Med J. 2013;102:39–40. 35. Lee AG, Beaver HA. Acute bilateral optic disk edema with a macular star figure in a 12-year-old girl. Surv Ophthalmol. 2002;47:42–49. 36. Wilson WB, Smith DB. Does neuroretinitis rule out multiple sclerosis?. Arch Neurol. 1989;46:358. 37. Wallin MT, Culpepper WJ, Campbell JD, Nelson LM, LangerGould A, Marrie RA, Cutter GR, Kaye WE, Wagner L, Tremlett H, Buka SL, Dilokthornsakul P, Topol B, Chen LH, LaRocca NG. US Multiple Sclerosis Prevalence Workgroup. The prevalence of MS in the United States: a population-based estimate using health claims data. Neurology. 2019;92:e1029–e1040. 1. Prieto JF, Dios E, Gutierrez JM, Mayo A, Calonge M, Herreras JM. Pars planitis: epidemiology, treatment, and association with multiple sclerosis. Ocul Immunol Inflam. 2001;9:93–102. 2. Arnold AC. Evolving management of optic neuritis and multiple sclerosis. Am J Ophthalmol. 2005;139:1101–1108. 3. Dreyer RF, Hopen G, Gass JD, Smith JL. Leber’s idiopathic stellate neuroretinitis. Arch Ophthalmol. 1984;102:1140– 1145. 4. Purvin V, Sundaram S, Kawasaki A. Neuroretinitis: review of the literature and new observations. J Neuroophthalmol. 2011;31:58–68. 5. Beck RW, Trobe JD, Moke PS, Gal RL, Xing D, Bhatti MT, Brodsky MC, Buckley EG, Chrousos GA, Corbett J, Eggenberger E, Goodwin JA, Katz B, Kaufman DI, Keltner JL, Kupersmith MJ, Miller NR, Nazarian S, Orengo-Nania S, Savino PJ, Shults WT, Smith CH, Wall M. Optic Neuritis Study Group. High- and lowrisk profiles for the development of multiple sclerosis within 10 years after optic neuritis: experience of the optic neuritis treatment trial. Arch Ophthalmol. 2003;121:944–949. 6. Optic Neuritis Study Group. The 5-year risk of MS after optic neuritis. Experience of the optic neuritis treatment trial. Neurology. 1997;49:1404–1413. doi:10.1212/wnl.49.5.1404. 7. Optic Neuritis Study Group. Multiple sclerosis risk after optic neuritis: final optic neuritis treatment trial follow-up. Arch Neurol. 2008;65:727–732. doi:10.1001/archneur.65.6.727. 8. Parmley VC, Schiffman JS, Maitland CG, Miller NR, Dreyer RF, Hoyt WF. Does neuroretinitis rule out multiple sclerosis?. Arch Neurol. 1987;44:1045–1048. 9. Maitland CG, Miller NR. Neuroretinitis. Arch Ophthalmol. 1984;102:1146–1150. 10. Altman DG, Bland JM. Absence of evidence is not evidence of absence. Br Med J. 1995;311:485. 11. Williams KE, Johnson LN. Neuroretinitis in patients with multiple sclerosis. Ophthalmology. 2004;111:335–340; Discussion 340–341. 12. Moura FC, Sato DK, Rimkus CM, Apóstolos-Pereira SL, Michelli de Oliveira L, Leite CC, Fujihara K, Monteiro MLR, Callegaro D. Anti-MOG (myelin oligodendrocyte glycoprotein)positive severe optic neuritis with optic disc ischaemia and macular star. Neuroophthalmology. 2015;39:285–288. 13. Lee AR, El-Dairi MA. Anti–myelin oligodendrocyte glycoprotein optic neuritis or neuroretinitis?. JAMA Ophthalmol. 2018;136:e182928. 14. Chen JJ, Tobin WO, Majed M, Jitprapaikulsan J, Fryer JP, Leavitt JA, Flanagan EP, McKeon A, Pittock SJ. Prevalence of myelin oligodendrocyte glycoprotein and aquaporin-4-IgG in patients in the Optic Neuritis Treatment Trial. JAMA Ophthalmol. 2018;136:419–422. 15. Leber T. Pseudoneuritic retinal disease, stellate retinitis: the angiopathic retinal affections after severe skull injury. Graefe Saemisch Handb Ges Augenheilkd. 1916;7:1319. 16. François J, Verriest G, De Laey JJ. Leber’s idiopathic stellate retinopathy. Am J Ophthalmol. 1969;68:340–345. 130 Miller et al: J Neuro-Ophthalmol 2022; 42: 126-130 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. |
Date | 2022-03 |
Language | eng |
Format | application/pdf |
Type | Text |
Publication Type | Journal Article |
Source | Journal of Neuro-Ophthalmology, March 2022, Volume 42, Issue 1 |
Publisher | Lippincott, Williams & Wilkins |
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