Classification of Choroiditis Based on Inflammatory Lesion Process rather than Fundus Appearance: Enhanced Comprehension through the ICGA Concepts of the Iceberg and Jellyfish Effects

Abstract

Choroidal inflammatory diseases have been classically grouped under the term of white dot syndromes (WDS), a term only based on the appearance (white-yellow dots) of inflammatory fundus lesions. This purely descriptive and vague terminology, regrouping a pot-pourri of posterior inflammatory conditions, probably came into use because the precise exploration of the choroid was not possible, and also because many of the diseases were rare and not well understood. Since the availability of indocyanine green angiography (ICGA) that allows one to explore the choroidal compartment, it became possible to understand the lesion mechanism of choroiditides and to classify this group of diseases according to their pathophysiological behaviour. It was our aim to show here that the term WDS is applied to and encompasses inflammatory conditions that are characterized by completely different lesion mechanisms and should therefore be classified separately from each other. ICGA made it possible to differentiate two types of choroiditides, including on the one hand inflammatory diseases of the choroidal stroma and on the other hand inflammatory diseases of the choriocapillaris. Unfortunately, twenty years after its advent, ICGA is still not used routinely in uveitis centres and the traditional inappropriate but overall useless term of WDS is still used, maintaining the confusion about these diseases. The aim of this work was (i) to illustrate that meaningful exploration of choroidal inflammation, mostly occult and inaccessible to usual investigations, has to be performed using ICGA, (ii) to insist on the crucial importance of ICGA in the management of choroiditis and (iii) to enhance the comprehension of the ICGA-based classification of choroiditis, by using the demonstrative and striking analogue concepts of iceberg and jellyfish effects.

Zusammenfassung

Entzündliche Aderhauterkrankungen (Choroiditiden) werden traditionell unter dem Begriff „White dot syndromes“ (WDS) zusammengefasst. Diese Terminologie basiert einzig und allein auf dem Fundusaspekt (weiße Fundus-Flecken) der Läsionen und versammelt Krankheitsbilder, die nichts miteinander zu tun haben. Durch die Indozyanin-Grün-Angiografie (ICGA) kann heutzutage die Aderhaut präzise untersucht werden. Dies erlaubt, die Pathogenese der Choroiditiden zu verstehen und macht es möglich, diese Krankheiten nach deren Mechanismus neu einzuteilen. Unser Ziel war es, zu zeigen, dass die Terminologie „WDS“ wenig Sinn macht und nichts als Konfusion erzeugt, da sie Krankheiten mit diverser Pathogenese in einen Topf wirft. Besser ist es, diese Krankheiten nach den 2 wichtigsten pathophysiologischen Mechanismen einzuteilen: nämlich 1. entzündliche Krankheiten des choroidalen Stromas und 2. Choriocapillaris-Entzündungen. Obwohl ICGA seit fast 20 Jahren praktiziert wird, ist die Methode leider noch nicht weit und breit in allen Uveitis-Zentren angenommen worden. Deswegen wollten wir in dieser Übersichtsarbeit durch anschauliche Konzepte wie „Eisberg oder Quallen Effekt“ den Kliniker auf die Wichtigkeit der ICGA-Abklärung aufmerksam machen, ohne die eine umsichtige Behandlung des Uveitispatienten mit Aderhautentzündung nicht denkbar ist.

Key words

choroiditis - indocyanine green angiography (ICGA) - stromal choroiditis - choriocapillaritis - iceberg effect - jellyfish effect - white dot syndromes

Schlüsselwörter

Choroiditis - Indozyanin-Grün-Angiografie (ICGA) - stromale Choroiditis - Choriocapillaritis - Eisbergkonzept - Quallenkonzept - Weiße Flecken Syndrome

• References

• 1 Forster DJ, Cano MR, Green RL et al. Echographic features of Vogt-Koyanagi-Harada syndrome. Arch Ophthalmol 1990; 108: 1421-1426
• 2 Matsumoto Y, Haen SP, Spaide RF. The white dot syndromes. Compr Ophthalmol Update 2007; 8: 179-200
• 3 Garg SP, Tewari HK, Khosla PK. Role of fluorescein angiography in choroiditis. Indian J Ophthalmol 1983; 31: 552-553
• 4 Ben Ezra D, Forrester JV. Fundal white dots: the spectrum of a similar pathological process. Br J Ophthalmol 1995; 856-860
• 5 The Foundation of the American Academy (ed.) Basic and Clinical Science Course 2000–2001, Section 9: Intraocular inflammation and uveitis. ISBN: 1-56055-208-5
• 6 Guyer DR, Yannuzzi LA, Slakter JS et al. The status of indocyanine green videoangiography. Curr Opin Ophthalmol 1993; 4: 3-6
• 7 Howe L, Stanford M, Graham E et al. Indocyanine green angiography in inflammatory eye diseases. Eye 1998; 12: 761-767
• 8 Papadia M, Herbort CP. Unilateral papillitis, the tip of the iceberg of bilateral ICGA-detected tuberculous choroiditis. Ocul Immunol Inflamm 2011; 19: 124-126
• 9 Yanuzzi LA. Indocyanine green angiography: a perspective on use in the clinical setting. Am J Ophthalmol 2011; 151: 745-751
• 10 Imamura Y, Engelbert M, Iida M et al. Polypoidal vasculopathy: a review. Surv Ophthalmol 2010; 55: 501-515
• 11 Regillo CD, Blade KA, Custis PH et al. Evaluating persistent and recurrent choroidal neovascularization. The role of indocyanine green angiography. Ophthalmology 1998; 105: 1821-1826
• 12 Herbort CP. Posterior uveitis: new insights given by indocyanine green angiography. Eye 1998; 12: 757-759
• 13 Herbort CP, Guex-Crosier Y, LeHoang P. Schematic interpretation of indocyanine green angiography. Ophthalmology 1994; 2: 169-176
• 14 Herbort CP, Mantovani A, Bouchenaki N. Indocyanine green angiography in Vogt-Koyanagi-Harada disease: angiographic signs and utility in patient follow-up. Int Ophthalmol 2007; 27: 173-182
• 15 Bouchenaki N, Cimino L, Auer C et al. Assessement and classification of choroidal vasculitis in posterior uveitis using indocyanine green angiography. Klin Monatsbl Augenheilkd 2002; 19: 243-249
• 16 Herbort CP. Choroiditis, general considerations and classification. In: Pleyer U, Mondino B, (eds.) Essentials in Ophthalmology: Uveitis and Immunological Disorders. Berlin, Heidelberg, New York: Springer; 2004: 202-208
• 17 Gass JDM. Acute posterior multifocal placoid pigment epitheliopathy. Arch Ophthalmol 1968; 80: 177-185
• 18 Nozik RA, Dorsch W. A new chorioretinopathy associated with anterior uveitis. Am J Ophthalmol 1973; 76: 758-762
• 19 Dreyer RF, Gass DJ. Multifocal choroiditis and panuveitis. A syndrome that mimics ocular histoplasmosis. Arch Ophthalmol 1984; 102: 1776-1784
• 20 Ryan SJ, Maumenee AE. Birdshot retinochoroidopathy. Am J Ophthalmol 1980; 89: 31-45
• 21 Gass JDM. Vitiliginous chorioretinitis. Arch Ophthalmol 1981; 99: 1778-1787
• 22 Jampol LM, Sieving PA, Pugh D et al. Multiple evanescent white dot syndrome. 1. Clinical findings. Arch Ophthalmol 1984; 102: 671-674
• 23 Sieving PA, Fishman GA, Jampol LM et al. Multiple evanescent white dot syndrome. 2. Electrophysiology of the photoreceptors during retinal pigment epithelial disease. Arch Ophthalmol 1984; 102: 675-679
• 24 Lewis H, Jampol LM. White dot syndromes. In: Pepose J, Holland GN, Wilhelmus KR, (eds) Ocular Infection and Immunity. St. Louis: Mosby; 1996: 560-570
• 25 Gaudio PA, Kaye DB, Brooks Crawford J. Histopathology of birdshot retinochoroidopathy. Br J Ophthalmol 2002; 86: 1439-1441
• 26 Yeh S, Forooghian F, Wong WT et al. Fundus autofluorescence imaging of the white dot syndromes. Arch Ophthalmol 2010; 128: 45-56
• 27 Herbort CP, Bodaghi B, LeHoang P. Angiographie au vert d’indocyanine au cours des maladies inflammatoires: principes, interpretation schématique, sémiologie et intérêt clinique. J Fr Ophtalmol 2001; 24: 423-447
• 28 Fardeau C, Herbort CP, Kullman N et al. Indocyanine green angiography in birdshot chorioretinopathy. Ophthalmology 1999; 106: 1928-1934
• 29 Herbort CP, Probst K, Cimino L et al. Differential inflammatory involvement in retina and choroïd in birdshot chorioretinopathy. Klin Monatsbl Augenheilkd 2004; 221: 351-356
• 30 Bouchenaki N, Herbort CP. The contribution of indocyanine green angiography to the appraisal and management of Vogt-Koyanagi-Harada disease. Ophthalmology 2001; 108: 54-64
• 31 Miyanaga M, Kawaguchi T, Miyata K et al. Indocyanine green findings in initial acute pretreatment Vogt-Koyanagi-Harada disease in Japanese patients. Jpn J Ophthalmol 2010; 54: 377-382
• 32 Bernasconi O, Auer C, Zografos L et al. Indocyanine green findings in sympathetic ophthalmia. Graefe’s Arch Clin Exp Ophthalmol 1998; 236: 350-353
• 33 Wolfensberger TJ, Herbort CP. Indocyanine green angiographic features in ocular sarcoidosis. Ophthalmology 1999; 106: 285-289
• 34 Wolfensberger TJ, Piguet B, Herbort CP. Indocyanine green angiographic features in tuberculous chorioretinitis. Am J Ophthalmol 1999; 127: 350-353
• 35 Papadia M, Herbort CP. Unilateral papillitis: the tip of the iceberg of bilateral ICGA detected tuberculous choroiditis. Ocul Immunol Inflamm 2011; 19: 124-126
• 36 Cimino L, Auer C, Herbort CP. Sensitivity of indocyanine green angiography for the follow-up of active inflammatory choriocapillaropathies. Ocul Immunol Inflamm 2000; 8: 275-283
• 37 Deutman AF. Acute multifocal ischaemic choroidopathy and the choriocapillaris. Int Ophthalmol 1983; 6: 155-160
• 38 Deutman AF, Lion F. Choriocapillaris nonperfusion in acute multifocal placoid pigment epitheliopathy. Am J Ophtalmol 1977; 84: 652-657
• 39 Howe LJ, Woon H, Graham EM et al. Choroidal hypoperfusion in acute posterior multifocal placoid pigment epitheliopathy. Ophthalmology 1995; 102: 790-798
• 40 Dhalival RS, Maguirre AM, Flower RW et al. Acute posterior multifocal placoid pigment epitheliopathy, an indocyanine green angiographic study. Retina 1993; 13: 317-325
• 41 Borruat FX, Auer C, Piguet B. Choroidopathy in multiple evanescent white dot syndrome. Arch Ophthalmol 1995; 113: 1569-1571
• 42 Papadi M, Herbort CP. Idiopathic choroiodal neovascularization as the inaugural sign of multiple evanescent white dot syndrome. Middle East Afr J Ophthalmol 2010; 17: 270-274
• 43 Herbort CP. Choroiditis: general considerations and classification. In: Pleyer U, Mondino B, (eds.) Essentials in Ophthalmology: Uveitis and Immunological Disorders. Berlin, Heidelberg, New York: Springer; 2004: 201-208
• 44 Bouchenaki N, Herbort CP. Stromal choroiditis. In: Pleyer U, Mondino B, (eds.) Essentials in Ophthalmology: Uveitis and Immunological Disorders. Berlin, Heidelberg, New York: Springer; 2004: 234-253
• 45 Herbort CP. Inflammatory choriocapillaropathies. In: et al. Gupta A, Gupta V, Herbort CP, (eds) Uveitis, Text and Imaging. New Dehli: Jaypee; 2009: 430-499
• 46 Fletcher WA, Imes RK, Goodman D et al. Acute idiopathic blind spot enlargement. A big blind spot syndrome without optic disc edema. Arch Ophthalmol 1988; 106: 44-49
• 47 Hamed LA, Schatz NJ, Glaser JS et al. Acute idiopathic blind spot enlargement without optic disc edema. Arch Ophthalmol 1988; 106: 1030-1031
• 48 Saito A, Saito W, Furudate N et al. Indocyanine green angiography in a case of punctate inner choroidopathy associated with acute zonal occult outer retinopathy. Jpn J ophthalmol 2007; 51: 295-300
• 49 Kuznik-Borkowska A, Cohen SY, Broïdo-Hooreman O et al. Acute macular neuroretinopathy. J Fr Ophtalmol 2006; 29: 319-322
• 50 Moshirfar M, Zimmermann PL. A case of AMPPiginous choroidopathy. In: American Uveitis Society Annual Meeting Abstracts. Meisler DM, Chern KC. (eds) Ocular Immunol Inflamm 1998; 6: 135-138
• 51 Jones BE, Jampol LM, Yannuzzi LA et al. Relentless placoid chorioretinitis. Arch Ophthalmol 2000; 118: 931-938
• 52 Cimino L, Mantovani A, Herbort CP. Primary inflammatory choriocapillaropathies. In: Pleyer U, Mondino B, (eds.) Essentials in Ophthalmology: Uveitis and Immunological Disorders. Berlin, Heidelberg, New York: Springer; 2004: 209-231
• 53 Inomata H, Sakamoto T. Immunohistochemical studies of Vogt-Koyanagi-Harada disease with sunset sky fundus. Curr Eye Res 1990; 9 (Suppl) 35-40
• 54 Rao NA, Marak GE. Sympathetic ophthalmia simulating Vogt-Koyanagi-Harada disease: a clinico-pathologic study of four cases. Jpn J Ophthalmol 1983; 27: 506-511
• 55 Gaudio PA, Kaye DB, Crawford JB. Histopathology of birdshot retinochoroidopathy. Br J Ophthalmol 2002; 86: 1439-1441