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Histology and Immunopathology of Systemic Lupus Erythematosus Affecting the Conjunctiva

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Histology and Immunopathology of Systemic Lupus Erythematosus Affecting the Conjunctiva HISTOLOGY AND IMMUNOPATHOLOGY OF SYSTEMIC LUPUS ERYTHEMATOSUS AFFECTING THE CONJUNCTIVA 1 2 l 1 ARND HEILIGENHAUS , , JAMES E. DUTI and C. STEPHEN FOSTER Boston, Massachusetts and Essen, Germany 1 SUMMARY factors. The disease is characterised by a great Systemic lupus erythematosus (SLE) is an autoimmune clinical diversity, including facial rash, discoid lupus, disease occasionally involving the conjunctiva, sclera or Raynaud's phenomenon, alopecia, photosensitivity, cornea. The immunopathology of the active epibulbar oral and nasopharyngeal ulcers, non-deforming lesions has not been studied in detail. Conjunctival arthritis, nephrotic syndrome, pleuritis, pericarditis, biopsies from 11 SLE patients with active epibulbar psychosis, convulsions, anaemia, leucopenia or 3 lesions and from 12 age-matched individuals under­ thrombocytopenia?, The course may be acute but going cataract surgery were analysed by light micro­ frequently is chronic with remissions. scopy, immunofluorescence and immunoperoxidase Ocular involvement in SLE is well documented, techniques. SLE patients presented with scleritis (3 but the prevalence of ocular manifestations varies in cases), peripheral ulcerative keratitis (5 cases) or unselected patients, depending on the exacerbations progressive cicatrising conjunctivitis (5 cases). Histolo­ and remissions of the condition.4,5 Intraocular gically, SLE specimens showed moderate subepithelial manifestations, which include uveitis, cotton wool and perivascular mononuclear cell infiltration or spots and intraretinal haemorrhages, perivasculitis, granuloma formation in the substantia propria, and vasculitis, �apilloedema and optic neuritis, are squamous metaplasia; thrombosis was not seen. common.4,6, The retinopathy may parallel the Immunoreactant deposition was present at the epithe­ activity of the systemic disease,8,9 being a marker lial basement membrane in 4 of 5 cases with cicatrising for poor prognosis for survival.lO Extraocular find­ conjunctivitis. Vascular immunodeposits were detected ings are keratoconjunctivis sicca (KCS),l1 superficial in 4 cases. The epithelium showed increased T helper punctate keratopathy,12 peripheral corneal infil­ cells (CD4+), granulocytes and natural killer cells 13 16 17 trates, interstitial keratitis,14,15 episcleritis , or (CD67+), dendritic cells (CD1+), and an increase in scleritis.18 Conjunctival involvement has been found ULA-DR expression compared with normal tissue. In 4. 5; 19,20 the substantia propria, B cells (CD22+), macrophages occasionally. (CD14+), dendritic cells, activated T cells (CD25+, Only limited data have been published on the histological or immunofluorescent characteristics of CD3+), the T helper (CD4+)ff suppressor (CD8+) 16 21 ratio and HLA-DR expression were all increased. conjunctival specimens in SLE patients; , there has These observations suggest that the rare epibulbar been no characterisation of the mononuclear cells manifestations in SLE result from immune-complex­ involved. Therefore, we investigated conjunctival mediated reactions. specimens from SLE patients by classical histo­ logical, immunofluorescent and immunoperoxidase Systemic lupus erythematosus (SLE) is an autoimune techniques. disease associated with severe alterations in immune regulation. The aetiology may be multifactorial, MATERIALS AND METHODS involving genetic predisposition and environmental Patients I Conjunctival biopsies from 11 patients with SLE From: Hilies Immunology Laboratory, Immunology and were taken. Twelve conjunctival specimen from Uveitis Service, Massachusetts Eye and Ear Infirmary, Harvard 2 Medical School, Boston, Massachusetts, USA; Department of healthy adults, obtained during cataract surgery, Ophthalmology, University of Essen, Essen, Germany. served as a control group. Correspondence to: A. Heiligenhaus, MD, Department of The diagnosis of SLE was based on a combination Ophthalmology, University, Hufelandstrasse 55, D-45122 Essen Germany. of clinical and laboratory parameters and met the Eye (1996) 10, 425-432 © 1996 Royal College of Ophthalmologists 426 A. HEILIGENHAUS ET AL. Table I. Primary monoclonal antibodies used and their specificities Antibody Dilution Vendor Specificity Anti-CDla 1140 Dako, Carpinteria, CA Langerhans cells Anti-CD3 1140 AMAC, Westbrook, ME T cells, thymocytes Anti-CD4 1/40 AMAC T helper/inducer cells Anti-CDS UD Becton Dickinson, Mountain View, CA T cytotoxic/suppressor cells Anti-CD14 1140 AMAC Monocytes/macrophages Anti-CD22 UD Becton Dickinson B cells Anti-CD25 UD Becton Dickinson Activated T cells Anti-CD67 1140 AMAC Granulocytes, natural killer cells Anti-HLA-DR 1/100 Becton Dickinson HLA-DR (class II histocompatibility antigen) UD, undiluted. criteria for the diagnosis of the disease accepted by buffered saline (PBS), pH 7.2 (except for goat anti­ the American Rheumatism Association?.3 Personal human albumin, which was diluted in PBS alone). data, symptoms and signs of ocular and systemic After air-drying the slides, one drop of conjugated problems, and previous and current treatment anti-serum was applied and incubated for 30 minutes modalities were recorded. Anterior segment and at room temperature in a moisture chamber. The external ocular photographs recorded the findings of slides were washed with PBS and coverslipped. site and degree of external eye inflammation. Slides were read by a fluorescence microscope (Zeiss Photomic III, Oberkochen, Germany). Biopsy After informed consent had been obtained from the Immunoperoxidase patient, the biopsies were taken by a technique The cryosections were air-dried, fixed in ?2 100% previously described Briefly, the tissue was har­ acetone, and incubated with 1% BSA in PBS, pH vested from the bulbar conjunctiva adjacent to the 7.2, for 30 minutes. Tissue sections were then limbus. In patients with SLE the area of obvious incubated with the primary antibodies for 45 minutes inflammation was chosen. The average size of the at room temperature followed by a 20 minute block specimen was 7 X 4 mm. Each specimen was divided with 3 % H202 for endogenous peroxidase. Anti­ into two equal pieces. bodies used in these studies are listed in Table 1. Following a series of PBS washes, the tissue was Histopathology incubated for 30 minutes with a 1:500 dilution of One piece of the specimen was placed in Karnovky's Biotin-SP-AffiniPure goat anti-mouse IgG (H+L) fixative (1 % paraformaldehyde, 1.25% glutaralde­ (Jackson ImmunoResearch Laboratories, West hyde, 0.13% sucrose, and 25 mM sodium phosphate Grove, PA). After washing in PBS, the sections in 150 mM sodium cacodylate buffer, pH 7.2) and were incubated for 20 minutes with a 1:1000 dilution stored overnight at 4 0c. After dehydration in of peroxidase-conjugated streptavidin (Jackson ascending ethanol concentrations, the tissue was ImmunoResearch Laboratories), and reacted with embedded in Historesin (LKB-Produkter AB, peroxidase substrate containing 3-amino-9-ethylcar­ Bromma, Sweden), sectioned at 2 /-Lm, and stained bazole and H202 in 0.1 M acetate buffer. Specimens by standard procedures with haematoxylin and eosin, were then post-fixedin formalin, counterstained with periodic acid-Schiff and alkaline Giemsa. Gill's No.3 haematoxylin, and coverslipped.Positive brown reactions on cell surfaces in the substantia Immunofluorescence propria were counted in two serial sections in The second piece of tissue was snap-frozen in liquid masked fashion in three representative high-power nitrogen, embedded in OCT compound (Tissue Tek, fields (x450) with a 10 X 10 mm square grid; a 10 X Miles Laboratories, Naperville, IL) and stored at 2 mm grid was used for counting epithelial cells. -70°C until sectioning. Four micrometre cryostat The mean number of stained cells of each cell sections were cut onto gelatin-coated 12-well slides subset and the standard error were calculated. The for immunofluorescence and immunoperoxidase significanceof differences of means between normals studies. and SLE patients was calculated by a two-tailed Direct immunofluorescentstaining was performed Student's t-test. using fluorescein (FITC)- or rhodamine (TRITC)­ labelled goat IgG directed against each human RESULTS immunoglobulin (IgA, IgD, IgE, IgG, IgM), comple­ Patients ment components C3 and C4, fibrin and albumin Table II summarises the clinical characteristics and (Organon Teknika-Cappel, Durham, NC), as pre­ the treatment modalities of our patients at the time 2 2 viously described? . 3 Briefly, antisera were diluted of biopsy. The mean age was 54.6 years (range 17-77 in 1% bovine serum albumin (BSA) in phosphate- years). Nine patients were female, 2 were male. Five IMMUNOPATHOLOGY OF EPIBULBAR SLE 427 Table II. Systemic lupus erythematosus: ocular manifestations inflammatory activIty of an underlying scleritis. and treatment at the time of biopsy Diminished numbers of goblet cells, as well as Case Sex/age squamous metaplasia, correlated clinically with no. (years) Manifestation Treatment progressive cicatrising conjunctivitis (cases 1, 5 and 1 F175 Cicatrising conjunctivitis, NSAID 9), sicca syndrome (case 11), both (case 8), or episcleritis, SPK, IK 2 F/52 Episcleritis, scleritis, PUK NSAID, DXC, TC peripheral ulcerative keratitis (case 6). Epithelial 3 F177 Sicca, PUK, optic neuritis None invasion by neutrophils appeared with peripheral 4 M/65 Scleritis NSAID ulcerative keratitis in 1 case, and leucocytic epithelial 5 F/39 Cicatrising conjunctivitis TC 6 M/62 PUK NSAID,DXC invasion correlated with interstitial keratitis in 7 F/57 Cicatrising conjunctivitis,
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