Subscribe to RSS
DOI: 10.1055/s-0034-1390393
Ocular Inflammation in Neurorheumatic Disease
Publication History
Publication Date:
04 November 2014 (online)
Abstract
Neuroimmunologic and systemic rheumatic diseases are frequently accompanied by inflammation of the eye, ocular adnexa, and orbital tissues. An understanding of the diverse forms of ophthalmic pathology in these conditions aids the clinician in making appropriate preventative, diagnostic, therapeutic, and prognostic decisions. In this review, the authors address ocular inflammation in neurorheumatic disease in three sections: first, they highlight current perspectives on immune mechanisms in the development of these disorders; next, they provide a framework for the recognition and evaluation of ophthalmologic inflammatory entities; finally, they discuss in detail several inflammatory conditions that affect the nervous system and the eye, emphasizing the features that should alert neurologists to initiate ophthalmologic evaluation. The conditions discussed include multiple sclerosis, neuromyelitis optica, chronic relapsing inflammatory optic neuropathy, Susac syndrome, Cogan syndrome, acute posterior multifocal placoid pigment epitheliopathy, Vogt-Koyanagi-Harada disease, Behçet disease, sarcoidosis, systemic lupus erythematosus, granulomatosis with polyangiitis (Wegener granulomatosis), polyarteritis nodosa, giant cell arteritis, IgG4-related disease, and Sjögren syndrome.
-
References
- 1 Medawar PB. Immunity to homologous grafted skin; the fate of skin homografts transplanted to the brain, to subcutaneous tissue, and to the anterior chamber of the eye. Br J Exp Pathol 1948; 29 (1) 58-69
- 2 Streilein JW. Ocular immune privilege: therapeutic opportunities from an experiment of nature. Nat Rev Immunol 2003; 3 (11) 879-889
- 3 Taylor AW. Ocular immune privilege. Eye (Lond) 2009; 23 (10) 1885-1889
- 4 Caspi RR. A look at autoimmunity and inflammation in the eye. J Clin Invest 2010; 120 (9) 3073-3083
- 5 Aviv RI, Miszkiel K. Orbital imaging: Part 2. Intraorbital pathology. Clin Radiol 2005; 60 (3) 288-307
- 6 Huang JJ, Gaudio PA. Ocular Inflammatory Disease and Uveitis Manual: Diagnosis and Treatment. 1st ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2010
- 7 Magro CM, Poe JC, Lubow M, Susac JO. Susac syndrome: an organ-specific autoimmune endotheliopathy syndrome associated with anti-endothelial cell antibodies. Am J Clin Pathol 2011; 136 (6) 903-912
- 8 Goverdhan SV, Lotery AJ, Howell WM. HLA and eye disease: a synopsis. Int J Immunogenet 2005; 32 (6) 333-342
- 9 Weyand CM, Fulbright JW, Hunder GG, Evans JM, Goronzy JJ. Treatment of giant cell arteritis: interleukin-6 as a biologic marker of disease activity. Arthritis Rheum 2000; 43 (5) 1041-1048
- 10 Toosy AT, Mason DF, Miller DH. Optic neuritis. Lancet Neurol 2014; 13 (1) 83-99
- 11 Chen L, Gordon LK. Ocular manifestations of multiple sclerosis. Curr Opin Ophthalmol 2005; 16 (5) 315-320
- 12 Biousse V, Trichet C, Bloch-Michel E, Roullet E. Multiple sclerosis associated with uveitis in two large clinic-based series. Neurology 1999; 52 (1) 179-181
- 13 Malinowski SM, Pulido JS, Folk JC. Long-term visual outcome and complications associated with pars planitis. Ophthalmology 1993; 100 (6) 818-824 , discussion 825
- 14 Donaldson MJ, Pulido JS, Herman DC, Diehl N, Hodge D. Pars planitis: a 20-year study of incidence, clinical features, and outcomes. Am J Ophthalmol 2007; 144 (6) 812-817
- 15 Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG. The spectrum of neuromyelitis optica. Lancet Neurol 2007; 6 (9) 805-815
- 16 Jarius S, Jacobi C, de Seze J , et al. Frequency and syndrome specificity of antibodies to aquaporin-4 in neurological patients with rheumatic disorders. Mult Scler 2011; 17 (9) 1067-1073
- 17 Pittock SJ, Lennon VA, de Seze J , et al. Neuromyelitis optica and non organ-specific autoimmunity. Arch Neurol 2008; 65 (1) 78-83
- 18 Wingerchuk DM, Weinshenker BG. The emerging relationship between neuromyelitis optica and systemic rheumatologic autoimmune disease. Mult Scler 2012; 18 (1) 5-10
- 19 Hinson SR, Pittock SJ, Lucchinetti CF , et al. Pathogenic potential of IgG binding to water channel extracellular domain in neuromyelitis optica. Neurology 2007; 69 (24) 2221-2231
- 20 Bradl M, Misu T, Takahashi T , et al. Neuromyelitis optica: pathogenicity of patient immunoglobulin in vivo. Ann Neurol 2009; 66 (5) 630-643
- 21 Kidd D, Burton B, Plant GT, Graham EM. Chronic relapsing inflammatory optic neuropathy (CRION). Brain 2003; 126 (Pt 2) 276-284
- 22 Petzold A, Plant GT. Chronic relapsing inflammatory optic neuropathy: a systematic review of 122 cases reported. J Neurol 2014; 261 (1) 17-26
- 23 Koczman JJ, Rouleau J, Gaunt M, Kardon RH, Wall M, Lee AG. Neuro-ophthalmic sarcoidosis: the University of Iowa experience. Semin Ophthalmol 2008; 23 (3) 157-168
- 24 Dörr J, Krautwald S, Wildemann B , et al. Characteristics of Susac syndrome: a review of all reported cases. Nat Rev Neurol 2013; 9 (6) 307-316
- 25 Susac JO, Hardman JM, Selhorst JB. Microangiopathy of the brain and retina. Neurology 1979; 29 (3) 313-316
- 26 Gross M, Banin E, Eliashar R, Ben-Hur T. Susac syndrome. Otol Neurotol 2004; 25 (4) 470-473
- 27 Haynes BF, Kaiser-Kupfer MI, Mason P, Fauci AS. Cogan syndrome: studies in thirteen patients, long-term follow-up, and a review of the literature. Medicine (Baltimore) 1980; 59 (6) 426-441
- 28 Bicknell JM, Holland JV. Neurologic manifestations of Cogan syndrome. Neurology 1978; 28 (3) 278-281
- 29 Albayram MS, Wityk R, Yousem DM, Zinreich SJ. The cerebral angiographic findings in Cogan syndrome. AJNR Am J Neuroradiol 2001; 22 (4) 751-754
- 30 Grasland A, Pouchot J, Hachulla E, Blétry O, Papo T, Vinceneux P ; Study Group for Cogan's Syndrome. Typical and atypical Cogan's syndrome: 32 cases and review of the literature. Rheumatology (Oxford) 2004; 43 (8) 1007-1015
- 31 de Vries JJ, den Dunnen WF, Timmerman EA, Kruithof IG, De Keyser J. Acute posterior multifocal placoid pigment epitheliopathy with cerebral vasculitis: a multisystem granulomatous disease. Arch Ophthalmol 2006; 124 (6) 910-913
- 32 Wolf MD, Alward WL, Folk JC. Long-term visual function in acute posterior multifocal placoid pigment epitheliopathy. Arch Ophthalmol 1991; 109 (6) 800-803
- 33 Mrejen S, Gallego-Pinazo R, Wald KJ, Freund KB. Acute posterior multifocal placoid pigment epitheliopathy as a choroidopathy: what we learned from adaptive optics imaging. JAMA Ophthalmol 2013; 131 (10) 1363-1364
- 34 Comu S, Verstraeten T, Rinkoff JS, Busis NA. Neurological manifestations of acute posterior multifocal placoid pigment epitheliopathy. Stroke 1996; 27 (5) 996-1001
- 35 Wilson CA, Choromokos EA, Sheppard R. Acute posterior multifocal placoid pigment epitheliopathy and cerebral vasculitis. Arch Ophthalmol 1988; 106 (6) 796-800
- 36 Sakata VM, da Silva FT, Hirata CE, de Carvalho JF, Yamamoto JH. Diagnosis and classification of Vogt-Koyanagi-Harada disease. Autoimmun Rev 2014; 13 (4-5) 550-555
- 37 Read RW, Rechodouni A, Butani N , et al. Complications and prognostic factors in Vogt-Koyanagi-Harada disease. Am J Ophthalmol 2001; 131 (5) 599-606
- 38 Read RW, Holland GN, Rao NA , et al. Revised diagnostic criteria for Vogt-Koyanagi-Harada disease: report of an international committee on nomenclature. Am J Ophthalmol 2001; 131 (5) 647-652
- 39 International Team for the Revision of the International Criteria for Behçet's Disease (ITR-ICBD). The International Criteria for Behçet's Disease (ICBD): a collaborative study of 27 countries on the sensitivity and specificity of the new criteria. J Eur Acad Dermatol Venereol 2014; 28 (3) 338-347
- 40 Al-Araji A, Kidd DP. Neuro-Behçet's disease: epidemiology, clinical characteristics, and management. Lancet Neurol 2009; 8 (2) 192-204
- 41 Tugal-Tutkun I, Onal S, Altan-Yaycioglu R, Huseyin Altunbas H, Urgancioglu M. Uveitis in Behçet disease: an analysis of 880 patients. Am J Ophthalmol 2004; 138 (3) 373-380
- 42 Hoitsma E, Faber CG, Drent M, Sharma OP. Neurosarcoidosis: a clinical dilemma. Lancet Neurol 2004; 3 (7) 397-407
- 43 Constantino T, Digre K, Zimmerman P. Neuro-ophthalmic complications of sarcoidosis. Semin Neurol 2000; 20 (1) 123-137
- 44 Birnbaum AD, Oh FS, Chakrabarti A, Tessler HH, Goldstein DA. Clinical features and diagnostic evaluation of biopsy-proven ocular sarcoidosis. Arch Ophthalmol 2011; 129 (4) 409-413
- 45 Cervera R, Piette JC, Font J , et al; Euro-Phospholipid Project Group. Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis Rheum 2002; 46 (4) 1019-1027
- 46 Ainiala H, Loukkola J, Peltola J, Korpela M, Hietaharju A. The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology 2001; 57 (3) 496-500
- 47 Sanna G, Bertolaccini ML, Cuadrado MJ , et al. Neuropsychiatric manifestations in systemic lupus erythematosus: prevalence and association with antiphospholipid antibodies. J Rheumatol 2003; 30 (5) 985-992
- 48 Bertsias GK, Boumpas DT. Pathogenesis, diagnosis and management of neuropsychiatric SLE manifestations. Nat Rev Rheumatol 2010; 6 (6) 358-367
- 49 DeGiorgio LA, Konstantinov KN, Lee SC, Hardin JA, Volpe BT, Diamond B. A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat Med 2001; 7 (11) 1189-1193
- 50 Tsuchiya H, Haga S, Takahashi Y, Kano T, Ishizaka Y, Mimori A. Identification of novel autoantibodies to GABAB receptors in patients with neuropsychiatric systemic lupus erythematosus. Rheumatology (Oxford) 2014; 53 (7) 1219-1228
- 51 Závada J, Nytrová P, Wandinger KP , et al. Seroprevalence and specificity of NMO-IgG (anti-aquaporin 4 antibodies) in patients with neuropsychiatric systemic lupus erythematosus. Rheumatol Int 2013; 33 (1) 259-263
- 52 Sivaraj RR, Durrani OM, Denniston AK, Murray PI, Gordon C. Ocular manifestations of systemic lupus erythematosus. Rheumatology (Oxford) 2007; 46 (12) 1757-1762
- 53 Palejwala NV, Walia HS, Yeh S. Ocular manifestations of systemic lupus erythematosus: a review of the literature. Autoimmune Dis 2012; 2012: 290898
- 54 Ushiyama O, Ushiyama K, Koarada S , et al. Retinal disease in patients with systemic lupus erythematosus. Ann Rheum Dis 2000; 59 (9) 705-708
- 55 Holle JU, Gross WL. Neurological involvement in Wegener's granulomatosis. Curr Opin Rheumatol 2011; 23 (1) 7-11
- 56 Nishino H, Rubino FA, DeRemee RA, Swanson JW, Parisi JE. Neurological involvement in Wegener's granulomatosis: an analysis of 324 consecutive patients at the Mayo Clinic. Ann Neurol 1993; 33 (1) 4-9
- 57 Sadiq SA, Jennings CR, Jones NS, Downes RN. Wegener's granulomatosis: the ocular manifestations revisited. Orbit 2000; 19 (4) 253-261
- 58 Pakrou N, Selva D, Leibovitch I. Wegener's granulomatosis: ophthalmic manifestations and management. Semin Arthritis Rheum 2006; 35 (5) 284-292
- 59 Provenzale JM, Mukherji S, Allen NB, Castillo M, Weber AW. Orbital involvement by Wegener's granulomatosis: imaging findings. AJR Am J Roentgenol 1996; 166 (4) 929-934
- 60 Bullen CL, Liesegang TJ, McDonald TJ, DeRemee RA. Ocular complications of Wegener's granulomatosis. Ophthalmology 1983; 90 (3) 279-290
- 61 Vischio JA, McCrary CT. Orbital Wegener's granulomatosis: a case report and review of the literature. Clin Rheumatol 2008; 27 (10) 1333-1336
- 62 Pagnoux C, Seror R, Henegar C , et al; French Vasculitis Study Group. Clinical features and outcomes in 348 patients with polyarteritis nodosa: a systematic retrospective study of patients diagnosed between 1963 and 2005 and entered into the French Vasculitis Study Group Database. Arthritis Rheum 2010; 62 (2) 616-626
- 63 Provenzale JM, Allen NB. Neuroradiologic findings in polyarteritis nodosa. AJNR Am J Neuroradiol 1996; 17 (6) 1119-1126
- 64 McCluskey P, Powell RJ. The eye in systemic inflammatory diseases. Lancet 2004; 364 (9451) 2125-2133
- 65 Akova YA, Jabbur NS, Foster CS. Ocular presentation of polyarteritis nodosa. Clinical course and management with steroid and cytotoxic therapy. Ophthalmology 1993; 100 (12) 1775-1781
- 66 Weyand CM, Goronzy JJ. Immune mechanisms in medium and large-vessel vasculitis. Nat Rev Rheumatol 2013; 9 (12) 731-740
- 67 Wilkinson IM, Russell RW. Arteries of the head and neck in giant cell arteritis. A pathological study to show the pattern of arterial involvement. Arch Neurol 1972; 27 (5) 378-391
- 68 Smetana GW, Shmerling RH. Does this patient have temporal arteritis?. JAMA 2002; 287 (1) 92-101
- 69 Goodman Jr BW. Temporal arteritis. Am J Med 1979; 67 (5) 839-852
- 70 Salvarani C, Cimino L, Macchioni P , et al. Risk factors for visual loss in an Italian population-based cohort of patients with giant cell arteritis. Arthritis Rheum 2005; 53 (2) 293-297
- 71 Liu GT, Glaser JS, Schatz NJ, Smith JL. Visual morbidity in giant cell arteritis. Clinical characteristics and prognosis for vision. Ophthalmology 1994; 101 (11) 1779-1785
- 72 Danesh-Meyer H, Savino PJ, Gamble GG. Poor prognosis of visual outcome after visual loss from giant cell arteritis. Ophthalmology 2005; 112 (6) 1098-1103
- 73 Stone JH, Zen Y, Deshpande V. IgG4-related disease. N Engl J Med 2012; 366 (6) 539-551
- 74 Yamamoto M, Takahashi H, Shinomura Y. Mechanisms and assessment of IgG4-related disease: lessons for the rheumatologist. Nat Rev Rheumatol 2014; 10 (3) 148-159
- 75 Wallace ZS, Khosroshahi A, Jakobiec FA , et al. IgG4-related systemic disease as a cause of “idiopathic” orbital inflammation, including orbital myositis, and trigeminal nerve involvement. Surv Ophthalmol 2012; 57 (1) 26-33
- 76 Wallace ZS, Deshpande V, Stone JH. Ophthalmic manifestations of IgG4-related disease: Single-center experience and literature review. Semin Arthritis Rheum 2014; 43 (6) 806-817
- 77 Mikulicz J. Ueber eine eigenartige symmetrische Erkrankung der Thränen- und Mundspeicheldrüsen. In: Beiträge zur Chirurgie. Festschrift gewidmet Theodor Billroth. Stuttgart: Ferdinand Enke; 1892: 610-630
- 78 Berkowitz AL, Samuels MA. The neurology of Sjogren's syndrome and the rheumatology of peripheral neuropathy and myelitis. Pract Neurol 2014; 14 (1) 14-22
- 79 Shiboski SC, Shiboski CH, Criswell L , et al; Sjögren's International Collaborative Clinical Alliance (SICCA) Research Groups. American College of Rheumatology classification criteria for Sjögren's syndrome: a data-driven, expert consensus approach in the Sjögren's International Collaborative Clinical Alliance cohort. Arthritis Care Res (Hoboken) 2012; 64 (4) 475-487