Retinal vasculitis - Postgraduate Medical Journal · 2008-12-18 · Postgraduate Medical Journal (1988) 64, 488-496 Retinal vasculitis M.D. Sanders and E.M. Graham Medical Ophthalmology

Postgraduate Medical Journal (1988) 64, 488-496

Retinal vasculitis

M.D. Sanders and E.M. Graham

Medical Ophthalmology Unit, St Thomas' Hospital, London SE] 7EH, UK.

Summary: Evidence is now accumulating on both clinical and experimental grounds that theretina is an a priori source of inflammatory activity. Reactive inflammation in the retina mayproduce many of the clinical signs previously ascribed to uveal inflammation. Autoimmunemechanisms are probably responsible for the majority of cases of retinal vasculitis. Autoimmuneretinal vasculitis occurs without other classical signs of inflammatory response in any other parts ofthe body. When associated systemic manifestations occur they may reflect different underlyingimmunopathogenic abnormalities.Thus in diseases with predominantly arterial involvement (e.g. systemic lupus erythematosus,

polyarteritis nodosa) the retinal arteries bear the brunt of this disease. In Beheet's disease thesystemic involvement is usually venous and ocular involvement produces diffuse capillary and venousinflammation with areas of retinal necrosis and major vascular occlusion. The retinal appearancesdiffer from sarcoidosis in which a granulomatous response produces characteristic periphlebitis.Finally, autoimmune retinal vasculitis produces diffuse capillary and venous damage, without anysystemic signs.

In the next decade the search will be for the identification of the specific antigens initiating thesedisparate retinal features. Retinal S antigen is a potent antigen, but rhodopsin, interphotoreceptorbinding protein, and transducin all need further experimental investigation. Precise documentationwill herald the dawn of new therapeutic measures based on a sound immunological fabric.

IntroductionNowhere else in the body can a microcirculation beobserved with such precision as in the retinalcirculation. The vessels are distributed on the flatsurface of the retina allowing accurate photo-graphic documentation, and clear differentiation canbe made between arteries, capillaries and veins. Inaddition, the integrity of endothelial cells can bedocumented by the use of fluorescein angiography,and monitored by fluorophotometry. Over the past20 years experimental studies have shown that theretina contains several potent antigens, the mostimportant being retinal S antigen.1 An animalmodel of retinal vasculitis has been producedfollowing the injection of retinal S antigen, and thisdisease produces several features in common withthe posterior uveitis in humans.2 Thus retinal vas-culitis may be a more accurate and preferentialterm reflecting inflammatory disease of the retinarather than the conventional term of uveitis.3

This review will therefore consider the mostfrequent causes of retinal vasculitis studied by theMedical Ophthalmology Unit at St Thomas' Hos-pital over the past decade. A group was formed(Figure 1) in which Dr Geraint James acted as bothinspirator and catalyst. The study consists of 150cases in which infective, ischaemic, degenerative

and metastatic diseases have been actively excluded(Figure 2). Rare causes of retinal vasculitis includedemyelinating disease, HLA B27 related disease anda few other eponymous conditions but the mainsub-groups that will be considered in this revieware:

1. Retinal arteritis2. Retinal vasculitis in: (a) Behqet's disease; (b)

sarcoidosis3. Autoimmune retinal vasculitis

Retinal arterial involvement: retinal arteritis

Retinal arterial occlusion without detectable embol-ism has been noted for many years, but an increasein the number of reports has occurred over the pastfew years (Figure 3). An idiopathic group hasemerged under a number of terms, including: reti-nal arteriolitis,4 retinal periarteritis,5 segmental reti-nal periarteritis,6 recurrent artery occlusion.7Microangiopathy of the brain and retina8 indicatesconcurrent cerebral involvement, and deafness hasalso been associated.9 In all these reports there wasmajor involvement of retinal arteries and arteriolesbut with preserved central vision and an absence ofinflammatory response in the eye (i.e. absence ofcells in the anterior chamber or vitreous). Debatetherefore exists as to whether these changes repre-

©) The Fellowship of Postgraduate Medicine, 1988

Correspondence: M.D. Sanders, F.R.C.P., F.R.C.S.

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RETINAL VASCULITIS 489

Figure 1 Retinal Vasculitis Study Group, St Thomas' Hospital 1986.

Figure 2 Diagnostic dartboard for retinal vasculitis.Outer circle represents condition that might simulateimmune mediated retinal vasculitis. Second circlerepresents rare causes of retinal vasculitis. Inner circle- common causes of retinal vasculitis with systemicinflammatory disease. Bull's eye - autoimmune retinalvasculitis.

sent immune complex deposition, an immune com-plex-mediated vasculitis or simply deposition ofantigen in the vessel with secondary antibody reac-tion. Interactions between platelets and endothelialcells may be altered and recently antibodies toendothelial cells and platelets have been detected.These patients present a clinical diagnostic problem,and examples will now be given with discussion ofthe mechanism. In addition, arteriolar occlusionshave been described in association with systemicdisease of proven autoimmune nature and these willalso be considered.

Idiopathic retinal arteritis

The combination of multiple retinal artery occlu-sions in young patients often with additional neuro-logical involvement has been repeatedly describedover the past decade.4'7'8 This syndrome has notevolved into a nosological or aetiological entity. Atypical case is illustrated below:A 40 year old cigarette smoking surgeon was

admitted to the National Hospital under Dr W.Goody. He had multiple peripheral non-embolicretinal artery occlusions in both eyes, and centralvision was spared. There was no evidence of inflam-

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490 M.D. SANDERS & E.M. GRAHAM

Figure 3 Retinal arteritis. (a) Multiple focal arterialabnormalities in a young man who had vision of 6/60in each eye. No systemic disease was found. (b)Peripheral nonperfusion of the retina due to ischaemia.

mation and cotton wool spots were not seen.Extensive investigations haematologically andimmunologically were normal, though lipid levelswere slightly increased. Macroangiography of thecerebral vessels showed no occlusive arterial dis-ease, no angiitis and no source for embolisation inthe carotid arteries. Similarly, echocardiographyshowed no source for cardiac embolisation.The patient over the next year developed areas of

neovascularisation at the border of non-perfusedand perfused retina, which gave rise to vitreoushaemorrhages. These areas of neovascularisationwere treated by laser photocoagulation. No sys-

temic disease evolved over 5 years of follow-upexamination.

Wegener's granulomatosis-polyarteritis nodosa

It is probable that these two conditions representdifferent clinical spectrums of the same disease. In1866 Kussmaul and Maier defined the gross andmicroscopic pathway of the disease that theyappropriately named periarteritis nodosa. The termnperiarteritis nodosa described the nodules in themedia or adventitia of small arteries. The findingsof epithelioid and giant cells and propensity toallergic manifestations such as asthma led Churgand Strauss°1 to introduce the term allergic granu-loma. Zeek"1 suggested the term necrotising angiitisfor this group and suggested five subgroups: (1)hypersensitivity angiitis; (2) allergic granulomatousangiitis; (3) rheumatic arteritis; (4) periarteritisnodosa; (5) temporal arteritis.Wegener in 1936 defined a disease characterized

by necrotising granulomatous vasculitis of theupper and lower respiratory tract progressing torenal involvement with glomerulonephritis. Thiscondition has been further subdivided in severaldifferent subgroups, one of which has granuloma-tous features, e.g. sarcoidal Wegener's, and anotherwith lymphoreticular features, e.g. lymphomatoidgranulomatosis. 1 2

The proximity of the orbit to the upper nasaltract may account for the high incidence of ocularinvolvement which occurred in 47% of the patientsdescribed by Haynes et al.,13 with orbital involve-ment being most common, and only one patienthaving optic disc vasculitis. A review of eightpatients with ocular involvement at St Thomas'Hospital showed retinal involvement in only onecase and this case represented the rare group ofsarcoidal Wegener's. The patient was a 12 year oldboy presenting with transverse myelitis, pneumoniaand uveitis. The retinal veins showed perivasculitisin the periphery and there was no arterial involve-ment.14 The retinal involvement in this caseresembles the retinopathy of sarcoidosis and this isconsistent with the histological similarity to sarcoi-dosis. Ocular involvement in periarteritis nodosa isextremely rare and our experience extends to onlytwo cases which are included in this group. In onepatient bilateral sixth nerve palsy was accompaniedby branch arteriolar occlusions. In the other patienta central vein occlusion was the only ocularmanifestation.

Churg-Strauss syndrome

Allergic angiitis and granulomatosis forms part ofthe spectrum of disseminated systemic necrotising

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vasculitis and pathological examination shows fibri-noid necrosis of small and medium sized arteries.Churg-Strauss differs from polyarteritis nodosa inthe degree of inflammatory involvement of smallvessels including capillaries and veins. There areseveral reports of ocular involvement in this syn-drome, and retinal arterial occlusions have been afeature.15 16 It is interesting that there is a markedperipheral and tissue eosinophilia in the Churg-Strauss syndrome which is also a feature of thehypereosinophilic syndrome.

Loeffler's eosinophilic syndromeAn interesting young patient with endocarditis,eosinophilia and renal disease was referred by DrGuy Neild. Fundus examination showed numerousretinal arterial occlusions in both eyes without signsof retinal infarction. Fluorescein angiography con-firmed arteriolar occlusion, and there was no evi-dence of choroidal involvement. Autopsy wasperformed which showed occlusion of arterioles byfibrinoid material but without perivascular inflam-mation. The patient was diagnosed as Loeffler'sfibroblastic endocarditis which represents one endof the spectrum of the hypereosinophilicsyndrome. 7

Systemic lupus erythematosus

Systemic lupus erythematosus (SLE) is a well-established non-organ-specific autoimmune diseaseand both human and animal studies suggest thatgenetic, endocrine and environmental factors areinvolved.

Retinal involvement occurs in 5 to 10% of casesand this association provides strong evidence tosupport the concept of autoimmune disease produc-ing a retinopathy. SLE produces multisystem in-volvement and definitive diagnostic criteriaare available with the detection of extractable anti-nuclear antibodies, and in particular anti-DNAantibodies.The retinal features are due to arterial occlusion

and the characteristic findings are cotton woolspots (Figure 4), larger retinal infarcts and opticdisc infarction. Embolic occlusion from cardiacvegetations may occur, but the retinal changes areusually manifest without clinical or post-mortemchanges of Libman-Sachs endocarditis, and withoutvisible calcific retinal emboli.A particular feature of the retinopathy of SLE is

that the veins are not involved, and there are noinflammatory changes in the anterior chamber orvitreous. Pathological examination shows occlusionof arterioles by fibrinoid material without vasculitis,though vasculitis or immunoglobulin deposition

Figure 4 Systemic lupus erythematosus. (a) Multiplecotton wool spots. (b) Attenuated arterioles withreduced retinal perfusion.

may be found in other vessels. In cerebral SLEmicrovascular damage is a characteristic neuropath-ological finding and speculation suggests twoimmunopathogenic mechanisms. Firstly, immunecomplex-mediated vascular injury and secondly,direct autoantibody-mediated attack on the vascu-lar endothelium. The cross reactivity of anti-cardio-lipid antibodies with cell membrane phospholipidsmay suggest an explanation for the endothelial celldamage, as high levels of anticardiolipid antibodiesare a feature of some cases of SLE.18A third and particularly interesting aspect is the

finding of antibodies to neuronal membrane anti-gens, which may be shared with lymphocyte anti-gens. In one patient in this series pathologicalexamination of the eyes was obtained of a youngboy with cerebral and ocular SLE. Fibrinoid occlu-sion of retinal arteries occurred without arteritis,but extensive cellular infiltration and vasculitisoccurred in choroidal vessels. The choroidal inflam-matory signs may reflect the increased permeabilityof the choroid vessels, as a result of immunecomplex disease involvement, and cerebral arteriesshowed occlusion though an arteritis was found inthe meningeal vessels.14

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Goodpasture's syndrome

Goodpasture in 1919 described a patient withhaemoptysis, anaemia and proteinuria, and post-mortem examination showed pulmonary alveolarhaemorrhages and glomerulonephritis. Immunologi-cal studies have shown the deposition of immuno-globulin G (IgG) in a linear pattern in basementmembrane of the kidney and lung. Similar changeswere reported in the eye by Jampol et al.20 withlinear deposition of IgG in Bruchs membrane andthe basement membranes of the choroidal vessels.Clinical examination of the two patients hereported showed ischaemic areas in the choroid inone, and both had non-rhegmatogenous retinaldetachments. We have seen one case of Goodpas-ture's syndrome who was normotensive but hadmultiple cotton wool spots and occasional haemorr-hages.21 There were no signs of retinal detachmentor choroidal disease. Histological examination of arenal biopsy showed IgG deposition in a linearfashion in the basement membrane. It is possiblethat the retinopathy in this condition also is relatedto antibodies to endothelial cells or constituents ofthe cell membrane.

Pathogenesis of retinal arteritis

A group of conditions therefore exists presenting innormotensive patients without a source for emboli-sation in which retinal and cerebral infarctionoccurs. The conditions include SLE, polyarteritisnodosa, Churg-Strauss syndrome, Goodpasture'ssyndrome and Loeffler's eosinophilic syndrome,with an additional idiopathic group. The clinicalfeatures of this group are: (1) cotton wool spotsindicating precapillary arteriolar involvement; (2)retinal branch arteriolar occlusions (a) with infarc-tion, (b) without signs of infarction, suggesting thatpatients were not examined during the acute phaseor that evolution of occlusion was chronic innature; (3) no signs of ocular inflammation.

It is interesting to speculate that this group mayexhibit antibodies or autoantibodies against endoth-elial cells or constituents of their cell membraneswith immune complex deposition. It is establishedthat retinal and cerebral endothelial cells havesimilar anatomical and physiological characteristicsand this may extend to their immunological proper-ties. In addition, the finding of antineuronal anti-bodies in cerebral SLE raises the question ofwhether shared antigens occur in the retina andbrain. The assumed autoimmune nature of theassociated disease lends credence to the view thatthis is an immunological process and though a true

vasculitis has not yet been recorded on histologicalexamination the mechanism is presumablyinflammatory.

Retinal vasculitis

Retinal vasculitis is defined as inflammation of theeye (cells in the anterior chamber and/or vitreous)in association with retinal vascular disease; this maybe ophthalmoscopically evident or demonstrableonly by fluorescein angiography. Classically theinflammation involves the retinal veins and post-capillary vessels but rarely the arterioles. Retinalvasculitis occurs in three clinical situations either asan isolated clinical manifestation or in associationwith either sarcoidosis or Behcet's disease. Theaetiology is unknown but autoimmune processesare deemed responsible even when retinal vasculitisoccurs without other systemic manifestations.Autoimmunity represents an immune response

directed against the host which may become apathological factor if it exceeds a certain threshold.Certain criteria are necessary for establishing anautoimmune disease:

1. Autoreactive antibodies or lymphocytes can bedetected.

2. The autoimmune reaction can be shown todamage target cells directly or by secondary immu-nological and inflammatory reactions.

3. The disease can be transmitted byauto-antibodies.

4. Immunomanipulation ameliorates the disease.Many of these criteria are established in retinal

vasculitis and in addition we have developed ananimal model of the disease which closely simulatesthe disease in man on immunological, clinical andpathological grounds.

The clinical features of retinal vasculitis withsystemic disease

Sarcoidosis

Sarcoidosis is a multisystemic granulomatous dis-order of unknown aetiology with pulmonary, cuta-neous and ocular manifestations. Ocularinvolvement occurs in approximately 25% ofcases.22'23 The ophthalmologist by detecting ocularinvolvement may aid the diagnosis of a multisystemdisease, but furthermore the retinal findings may bepathognomonic.24 In the present series there were17 biopsy proven cases of sarcoidosis. In this groupin addition to pulmonary and ocular involvementthe following systems were involved: arthritis 7,cutaneous 2, central nervous system 3, Kveim +ve10 and biopsy lung/skin 7.

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Retinal involvement was characterized by focalperiphlebitis and this is a characteristic feature ofsarcoidosis (Figure 5). Predominant changes occuraround the veins and arterial involvement is vir-tually never seen. Clinical and fluorescein angio-graphic features include: focal periphlebitis (78%),diffuse capillary leakage (44%), new vessel forma-tion (5%) and acute retinopathy.

Iritis occurred in 41% of cases and retinal andoptic disc involvement may occur without involve-ment of the anterior chamber. Retinal vein occlu-sion and infiltration of the retina are not seen insarcoidosis and serve to differentiate sarcoidosisfrom Behqet's disease. There were no cases of theacute retinopathy of sarcoidosis in this seriesthough this rare presentation has been seen in twoother cases and included in other reports.24'25 Theacute retinopathy usually progresses to capillaryclosure and neovascularisation.

Behfet's syndrome

Behqet's syndrome is a multisystem disease affectingyoung adults with a classical triad of mouth ulcers,genital ulcers and iritis. Recognized in the writingof Hippocrates but eventually named after a Tur-kish dermatologist, Professor Halusi Behcet, thiscondition provides a major challenge to ophthalmo-logy because of the ocular devastation it produces.Clinically patients give a long history of mouthulcers, usually from childhood, and often with upto 12 ulcers occurring simultaneously. Ocular

Figure 5 Sarcoidosis. Peripheral retinal periphlebitis,a pathognomonic feature of retinal sarcoidosis.

features present in the second and third decadesand in addition to ocular features there are muco-cutaneous, intestinal, vascular, urological and neur-ological manifestations. Death from Behcet'ssyndrome is rare (3 to 4%) and the disease usuallyburns itself out, leaving a blind or partially blindpatient. The underlying histopathological lesion inall organ systems is vasculitis. This includes perivas-cular infiltrates of monocular cells, swelling andproliferation of endothelial cells leading to partialobliteration of small vessels and fibrinoid degener-ation.26 Despite a wide variety of immunologicalabnormalities, there is no specific diagnostic testand the clinician rather than the immunologistholds the key to diagnosis. The high incidence ofthe haplotype HLA B5 has been described in allepidemiological studies of ocular Behqet's, includingthose in both Japan and Europe. HLA B27 how-ever may be found in the arthritis type of Behcet'ssyndrome and HLA B12 in the mucocutaneoustype.27 There may be a disequilibrium linkagebetween HLA B5 and HLA A2 in the ocular groupwith retinal vein occlusion.28 Immune complexesare found in patients and in exacerbations ofdisease an increase in IgG complexes.27

Ocular involvement has certain specific and diag-nostic features, and occurs in 80% of patients.Behqet's syndrome produces the most aggressivepattern of vasculitis and in the last decade visionwas deemed to be lost within 3.36 years after onsetof ocular involvement.29 However, the prognosishas been improved by early recognition andaggressive treatment by steroids, immunosuppres-sives and cyclosporins. Excellent reviews are avail-able26'30 so that this discussion will concentrate onthe retinal features.Emphasis must first be placed on the fact that

this is a retinal and not a choroidal disease, onboth clinical and pathological evidence. Hypopyonis a rare feature occurring in our series in 13% ofcases, and iritis (48%) is mild and does not usuallyproduce visual loss. Retinal involvement has char-acteristic features first indicated in 197928 but sup-ported by the present series. Our present seriescomprises 39 patients and 65% were under the ageof 40 years. The general features include: mouthulcers 100%, genital ulcers 66%, skin lesions 51%,arthritis 46%, thrombophlebitis 43% and centralnervous system involvement.The ocular features could be subdivided into four

distinct groups: diffuse capillary leakage 100%,branch vein occlusion 62%, infiltrations 40%, andterminal stage with optic atrophy and maculardegeneration. Diffuse capillary leakage occurred inall cases, as observed by fluorescein angiographyand affected the posterior pole (Figure 6). Maximalinvolvement occurred at the disc, the arcuate capil-

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Figure 6 Behget's disease. (a) Severe retinal vascularleakage on fluorescein angiography of this left eye withfocal infiltration. (b) One month after prednisolonetreatment there is marked resolution of the leakage ofdye.

laries and the macular capillaries. A peripheralperiphlebitis or focal periphlebitis was not seen.Extensive areas of retinal non-perfusion were notseen without venous occlusion, and neither wasneovascularisation a feature. These factors serve todistinguish the retinopathy of Behcet's syndromefrom other types of vasculitis.Branch vein occlusion occurred in 62% of cases

and could involve small macular vessels or hemi-sphere vein occlusion. Central retinal vein occlusionwas not seen. Factors contributing to the patho-genesis include inflammation of the vessel wall butin addition elevated blood viscosity was found intwo patients. Branch vein occlusion, particularlywhen the macular vessels are involved, provides amajor source of the visual disability associated withBeh,et's syndrome.

Figure 7 Autoimmune retinal vasculitis. Severe bi-lateral visual loss was seen in this 18 year old girl.There was disc oedema on the left with diffuse capill-ary leakage on fluorescein angiography (a), extensioninto the periphery with marked perivenous leakage (b).

Retinal infiltrations present deep pale areas, oftensurrounded by haemorrhages. They resolvepromptly on steroid treatment suggesting they aremanifestations of inflammation rather than ischae-mia and may be seen as a retinal manifestation ofthe hypopyon.

Retinal infiltrations and branch vein occlusionsare specific and pathognomonic features of theretinopathy of Behcet's disease and are not seen inany other condition. Despite modern therapeuticmeasures and the use of cyclosporin in ourpatients31 the visual prognosis was bad: 46% - 6/18in both eyes, 80% - 6/18 in one eye. Immunologi-cal tests were not of diagnostic value, though HLAB5 occurred in 65% of cases and in 27% of casesthe combination HLA A2 and B5 was associatedwith branch vein occlusions.

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The clinical features of autoimmune retinalvasculitis

Sixty-seven patients had retinal inflammatory dis-ease without other systemic features. The finding ofautoimmune features and the establishment of ananimal model justifies the appellation for this groupof 'autoimmune retinal vasculitis' (ARV).There were 67 patients in this group with a

female predominance (27 males, 40 females). Themajority (72%) of patients were under 40 years ofage: under age 20 - 21%, 20-29 - 21%, and 30-39- 30%, 15% were 40-49 years of age and 13% over50. Examination showed no evidence of cutaneous,neurological or pulmonary disease and specific testswere negative. Immunological tests were similar tothose patients with retinal vasculitis and a systemicdisease, though the incidence of retinal autoanti-

bodies (measured by indirect immunofluorescence)was lower in those with systemic disease only.Two subgroups could be demonstrated, one with

positive retinal antibodies (34 patients) and theother with negative retinal antibodies (36 patients).There were no clinical differences between thesegroups and one may speculate that in the negativegroup tests may have been directed at the wrongepitope of retinal S antigen, or indeed the wrongantigen.There are two characteristic retinal features of

autoimmune retinal vasculitis (Figure 7): diffusecapillary leakage (83%) and capillary closure andnew vessels (23%). In particular there were noinfiltrations or branch vein occlusions in contrast toBehcet's disease, no evidence of peripheral peri-phlebitis as seen in sarcoidosis, and no signs ofarterial occlusion.

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3. Sanders, M.D. Retinal arteritis, retinal vasculitis andautoimmune retinal vasculitis. Eye 1987, 1: 441-465.

4. Jampol, L.M., Isenberg, S.J. & Goldberg, M.F.Occlusive retinal arteriolitis with neovascularization.Am J Ophthalmol 1976, 81: 583-589.

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Retinal vasculitis - Postgraduate Medical Journal · 2008-12-18 · Postgraduate Medical Journal (1988) 64, 488-496 Retinal vasculitis M.D. Sanders and E.M. Graham Medical Ophthalmology