Autoimmune bullous disorders 1)
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1 Clin Chem Lab Med 2006;44(2): by Walter de Gruyter Berlin New York. DOI /CCLM /39 Review Autoimmune bullous disorders 1) Rüdiger Eming* and Michael Hertl for the members of the Autoimmune Diagnostics Working Group Klinik für Dermatologie und Allergologie, Philipps- Universität Marburg, Marburg, Germany Abstract Bullous skin diseases represent a group of organ-specific autoimmune disorders characterised by binding of circulating autoantibodies to adhesion molecules of the epidermis and the dermo-epidermal basement membrane zone. Binding of these autoantibodies to their antigenic targets results in loss of adhesion between epidermal keratinocytes and at the level of the basement membrane zone. Chronic blisters and secondary painful erosions are the clinical hallmark of autoimmune bullous disorders. Histopathology reveals the location of blister formation and helps to classify the subtype of the bullous skin disorder. Immunofluorescence is crucial for diagnosing autoimmune bullous skin disorders. Tissue-bound autoantibodies are detected by direct immunofluorescence of perilesional skin. Circulating autoantibodies can be visualised by indirect immunofluorescence using tissue substrates such as monkey oesophagus and sodium chloride-split human skin. Most of the autoantigens are available as recombinant proteins, which allows for autoantibody screening by ELISA or immunoblot analysis to confirm the primary diagnosis and, importantly, for immunoserological follow-up of patients. Keywords: adhesion molecules; autoantibodies; basement membrane zone; bullous skin diseases; desmosomes; ELISA; immunofluorescence; sodium chloride-split skin. Introduction Bullous autoimmune skin disorders, including some life-threatening diseases, are manifest in the skin and mucous membranes and are clinically characterised by the appearance of blisters and secondary erosions. 1) The German version of this article has been published in LaboratoriumsMedizin 2005;29(4): The English version of the article contains additional figures and is published in Clin Chem Lab Med with kind permission from the authors. *Corresponding author: Dr. med. Rüdiger Eming, Klinik für Dermatologie und Allergologie, Philipps-Universität Marburg, Deutschhausstraße 9, Marburg, Germany Phone: q , Fax: q , eming@med.uni-marburg.de Bullous autoimmune dermatoses have a common pathogenic mechanism involving binding of autoantibodies to specific adhesion molecules in epidermal desmosomes, and in some cases in the area of the dermo-epidermal basement membrane zone. The binding of circulating autoantibodies and the induction of an inflammatory reaction in the area of target structures lead to loss of adhesion with subsequent intra- or subepidermal blister formation (1). The clinical appearance is heterogeneous and secondary eruptions such as erosions, encrustation, impetiginisation, and scarred secondary erosions can dominate the clinical picture. Diagnosis of this organ-specific chronic autoimmune disease is frequently a problem. Therefore, a diagnostic concept to allow standardisation of the available examination methods (Figure 1) was developed by the autoimmune diagnostic working group of the United German Society for Clinical Chemistry and Laboratory Medicine (DGKL). History and clinical findings For the most part, bullous autoimmune dermatoses exhibit a chronic progression, in which the principal clinical symptoms are blisters and painful secondary erosions on the skin and mucous membranes that lack a tendency to heal. The most frequent adult bullous skin disease, the bullous pemphigoid (BP), demonstrates taut blisters on the torso and extremities. A prodromal phase with pruritus and papulovesicular or urticarial plaques can precede the occurrence of blisters. In diseases of the pemphigus group, loose fragile blisters are often no longer detectable and erosions with a crusty surface are frequently prominent. Table 1 shows the clinical characteristics of different bullous autoimmune dermatoses. Clinical differential diagnosis The most important differential diagnoses of bullous autoimmune dermatoses include: a) infectious diseases in connection with bacterial and viral infections; b) immunological causes, such as bullous druginduced skin rashes or erythema exsudativum multiforme (EEM); and c) the group of hereditary blister-forming dermatoses. Table 2 summarises these differential diagnoses. Classification of bullous autoimmune dermatoses Classification of the blister-forming autoimmune skin diseases is based on the localisation of the blister formation (2). The diseases are categorised into three groups: those that exhibit an intra-epidermal loss of
2 Eming and Hertl: Autoimmune bullous disorders 145 Figure 1 Diagnosis of bullous autoimmune skin diseases. Table 1 Disease Clinical characteristics of bullous autoimmune skin diseases. Clinical characteristics Pemphigus vulgaris (PV)/foliaceus (PF) Paraneoplastic pemphigus (PNP) IgA-pemphigus Bullous pemphigoid (BP) Pemphigoid gestationis (PG) Mucous membrane pemphigoid (MMP, formerly cicatricial pemphigoid, CP) Linear IgA bullous dermatosis (LABD/CBDC) Epidermolysis bullosa acquisita (EBA) Dermatitis herpetiformis (DH) Loose blisters/erosions on mucous membranes (PV) and skin (PF, PV); PF predominantly in seborrheic skin areas Haemorrhagic stomatitis, polymorph exanthema; lichenoid efflorescences palmoplantar; frequent associations: haematologic malignoma, thymoma, Castleman tumour Fragile, annular, rim-accentuated blisters or pustules, or crusty erosions on the skin; rarely affection of mucous membranes Urticarial, pruriginous plaques with taut blisters or erosions; intertriginous areas on the flexor side of the extremities; 10 30% involvement of the mucous membranes Erythematous papules and plaques, eczema, pruritus; often 2nd or 3rd trimester Erosions and ulcerations with atrophy of the mucous membranes (beware conjunctivitis, symblephara), involvement of skin in ;25% of cases, capillitium, head, upper trunk Most frequent form in childhood; polymorph, often centrifugally grouped, pearl string-like arranged taut blisters, often mucous membrane involvement; associations: colitis ulcerosa; primary sclerosing cholangitis Mechanobullous, inflammatory and atrophic variant, frequent involvement of mucous membranes; scarring and formation of milia Accentuated excoriated papule vesicles at extensor side or small blisters; pruriginous papulae, erythematous plaques, intense pruritus; coeliac disease does not have to be clinically manifest
3 146 Eming and Hertl: Autoimmune bullous disorders Article in press - uncorrected proof Table 2 Differential diagnoses of bullous skin diseases. Disease groups Disease Clinical/diagnostic characteristics Hereditary bullous Epidermolysis bullosa simplex Occurrence at birth or early childhood; diseases group, basal membrane bullous clinical findings according to genetic defect; epidermolysis group, dystrophic DIF and IIF negative bullous epidermolysis group Infectious diseases Impetigo contagiosa Microbiology, other signs of inflammation; IF and serology negative Staphylococcal scalded-skin Most widely described epidermolysis, syndrome histology; IF and serology negative Bullous erysipelas Clinical and serological inflammation parameters; IF and serology negative Herpes simplex HSV evidence in blister fluid; IF and serology negative Varicella zoster virus Clinical picture, general symptoms; IF and serology negative Immunological Bullous systemic lupus IF and serology positive (anti-collagen VII-Ak), diseases erythematosus (SLE) ANA positive; other SLE criteria positive Erosive lichen ruber planus IF: subepidermal cytoid bodies, IIF negative; cutaneous involvement, hepatopathy Erythema exsudativum multiforme History; IF and serology with majus form (EEM) sometimes positive, ICS pattern (anti-desmoplakin-ak) Bullous drug-induced exanthema EEM-like picture or laminar epidermolysis, (SJS, TEN) histology; IF and serology negative Subcorneal pustulosis (Sneddon- Leukocytosis, serologic signs of inflammation, Wilkinson) DIF and serology negative Other diseases Porphyria cutanea tarda Porphyrins in serum and urine, IF and serology negative, light-exposed areas Bullosis diabeticorum Glucose in serum/urine, IF and serology negative Traumatic/toxic blister formation History; DIF and serology negative IF, immunofluorescence; DIF, direct immunofluorescence; IIF, indirect immunofluorescence. adhesion (acantholysis); those with skin-splitting in the area of the basement membrane zone; and dermatoses with damaged sublaminal adherence. An Table 3 Classification of bullous autoimmune skin diseases. I. Intraepidermal loss of adhesion (desmosome) 1. Pemphigus vulgaris 1.1. Pemphigus vegetans (Neumann type, Hallopeau type) 1.2. Pemphigus herpetiformis 2. Pemphigus foliaceus 2.1. Fogo selvagem (endemic type) 2.2. Pemphigus erythematosus (Senear-Usher) 2.3. Pemphigus sebhorrhoicus 3. Paraneoplastic pemphigus 4. Drug-induced pemphigus 5. IgA pemphigus 5.1. Subcorneal pustulous dermatosis 5.2. Intraepidermal neutrophile dermatosis II. Subepidermal loss of adhesion (lamina lucida/ densa) 1.1. Bullous pemphigoid 1.2. Pemphigoid gestationis 1.3. Mucous membrane pemphigoid 1.4. Other pemphigoid types 2. Linear IgA- bullous dermatosis 2.1. Chronic bullous dermatosis of childhood 2.2. Adult forms 3. Epidermolysis bullosa acquisita III. Subepidermal loss of adhesion (dermal) 1. Dermatitis herpetiformis Duhring overview of this classification is given in Table 3. In diagnosing bullous autoimmune skin diseases, histological examination of diseased skin allows differentiation between intra- and subepidermal blister formation. Thus, histology plays a major role in differentiating intra-epidermal (desmosomal) from subepidermal loss of adhesion. However, definitive classification is not possible from histological findings alone. Direct and indirect immunofluorescence Direct immunofluorescence The diagnosis of bullous autoimmune skin diseases involves immunohistological and immunoserological tests (3). Using direct immunofluorescence (DIF) of perilesional skin tissue-bound autoantibodies, mostly classified as IgG, but also including IgA (linear IgA dermatosis, IgA pemphigus, IgA-type Epidermolysis bullosa acqusita), as well as the complement factor C3, can be verified. The localisation of tissue-bound autoantibodies leads to characteristic fluorescent patterns, which allow allocation to specific entities (Figure 2). Intercellular reticulate (desmosomal) deposits of IgG (or IgA in IgA pemphigus) and complement factors (frequently C3) are obvious in all pemphigus diseases. Linear deposits of IgG and C3 in the area of the dermo-epidermal basement membrane zone can be found in the pemphigoid group and Epidermolysis bullosa acqusita. Linear deposits of IgA at the basal membrane are
4 Eming and Hertl: Autoimmune bullous disorders 147 Figure 2 Characteristic immunofluorescent pattern of tissue-bound autoantibodies with direct immunofluorescence. (A) Intercellular (desmosomal) deposits of IgG in diseases of the pemphigus type. (B) Linear deposits of IgG (and IgA) in the area of the basement membrane zone in pemphigoid, epidermolysis bullosa acquisita, and linear IgA dermatosis. (C) Dermatitis herpetiformis Duhring shows granular IgA deposits in the dermal papillae. characteristic of linear IgA dermatosis and are also found in IgA-type Epidermolysis bullosa acqusita. The DIF of Dermatitis herpetiformis Duhring shows granular IgA deposits in the dermal papillae and occasionally in the basement membrane area. Indirect immunofluorescence Indirect immunofluorescence (IIF) detects circulating serum autoantibodies in patients (Figure 3A, B). In this test, monkey oesophagus is used as a substrate for pemphigus diseases. In certain cases, plakin-rich tissue, such as Figure 3 (A, B) Proof of circulating autoantibodies with indirect immunofluorescence. (A) Intercellular, intraepidermal IgG (and rarely IgA) binding in pemphigus on monkey oesophagus. (B) IgA reactivity in the endomysium of smooth muscle in dermatitis herpetiformis Duhring. (C E) Three characteristic fluorescence patterns in the so-called NaCl-split skin test. Human skin shows an artificial splitting in the area of the lamina lucida of the basement membrane zone after incubation with 1 M NaCl. (C) Pemphigoid-type IgG reactivity to autoantigens in the epidermal part (blister roof) can be seen. (D) Binding of circulating IgG autoantibodies with reactivity to the dermal area in epidermolysis bullosa acquisita. (E) Staining in the epidermal and dermal areas of the NaCl-split skin in scarred mucous membrane pemphigoid (anti-laminin-5-antibody). In linear IgA dermatosis, IgA reactivity occurs in the epidermal area (blister roof).
5 148 Eming and Hertl: Autoimmune bullous disorders Article in press - uncorrected proof Table 4 Immunofluorescence in bullous autoimmune skin diseases. Disease Direct Indirect Target antigens immunofluorescence immunofluorescence Pemphigus vulgaris (PV), Intercellular IgG and C3 Intercellular IgG Dsg3 (PV), Dsg1 (PF, PV), pemphigus foliaceus (monkey oesophagus) Dsg4 (assoc. with anti- (PF) Dsg1) (seldom plakins) Paraneoplastic Intercellular IgG and C3; linear Intercellular IgG (rat bladder) Dsg1/Dsg3, plakins pemphigus IgG and C3 at the BMZ (desmoplakin, envoplakin, periplakin), BP230, 170 kda-antigen IgA-pemphigus Intercellular IgA and C3 Intercellular IgA (monkey Desmocollin 1, Dsg1/Dsg3 oesophagus) in 50% Bullous pemphigoid Linear IgG (IgA) and C3 at the IgG epidermal (SSS) BP180, BP230 BMZ Pemphigoid gestationis Linear IgG -C3 at the BMZ IgG epidermal (SSS) BP180 (BP230) Mucous membrane Linear IgG and/or IgA and/or IgG or IgA epidermal BP180 (BP230), pemphigoid C3 at the BMZ "dermal (SSS) laminin-5, 6b4-integrin Linear IgA-bullous Linear IgA (and C3) at the IgA epidermal, where applicable LAD-1, BP180, BP230 dermatosis BMZ dermal (SSS) Epidermolysis bullosa Linear IgG and C3 at the BMZ; IgG (or IgA) and C3 dermal Collagen VII acquisita (EBA) linear IgA and C3 at the BMZ (SSS) (IgA-type EBA) Dermatitis herpetiformis Granular IgA deposits at IgA against endomysium of Epidermal dermal papillae smooth muscle cells transglutaminase (monkey oesophagus) BMZ, basement membrane zone; SSS, sodium chloride-split skin. guinea pig oesophagus or rat bladder epithelia, is used. The different DIF and IIF tests with their respective target antigens are summarised in Table 4. An additional substrate for IIF is sodium chloridesplit skin. This test is used to further differentiate pemphigoid, linear IgA dermatosis, and EBA (Figure 3C E). Pemphigoid disease and EBA demonstrate immunohistologically linear deposits of IgG and C3 in the area of the dermo-epidermal basement membrane zone. In addition, linear IgA deposits in the area of the basement membrane zone are characteristic of linear IgA dermatosis, but can also be found in the IgA variant of EBA. For the sodium chloride split-skin test, human skin is incubated in 1 M NaCl solution, so that an artificial split is induced in the area of the lamina lucida of the basement membrane zone. This splitting separates pemphigoid autoantigens from those of EBA. Sera of pemphigoid patients typically show IgG binding to target antigens in the area of the blister roof (epidermal part), whereas sera of patients with EBA show IgG reactivity at the base of the blister (dermal part). IgA autoantibodies can be verified in 60 70% of patients with linear IgA dermatosis, with a reactivity to autoantigens in the epidermal area of the NaCl-split skin. A specific characteristic of sera from patients with mucous membrane pemphigoid is that laminin-5 (epiligrin)- reactive sera show reactivity to the epidermal and dermal parts of the NaCl-split skin, where the IgG reactivity shows a typical pattern at the blister base. Immunoserological tests with recombinant autoantigens or autoantigen extracts ELISA and immunoblot tests with recombinant and purified native autoantigens are an important addition to the diagnosis of bullous autoimmune dermatoses. The identification of autoantigens of most autoimmune blistering skin diseases has allowed their use in immunoserological procedures in the last few years (4 8). These antigens are either prepared by recombination or from epidermal extracts or cultured keratinocytes. Commercial test systems are currently only available for the autoantigens Dsg1/Dsg3 (pemphigus group) for the NC16A region of BP (bullous pemphigoid) and for tissue transglutaminase (dermatitis herpetiformis). A type VII-collagen has been described for EBA, but is not commercially available (9). Therefore, dermal protein extracts for immunoblot analysis are used for proof of autoantibodies in EBA. Furthermore, specialised laboratories, including the Departments of Dermatology in Marburg, Freiburg, and Lübeck, carry out additional serological tests in the form of ELISAs, immunoblots, and immunoprecipitation with recombinant and native varieties of the autoantigens Dsg1/Dsg3, BP180/BP230 and laminin-5 (10 12). Diagnostic course The current immunoserologic course of tests commonly used is based on recent developments in the diagnostic field of bullous autoimmune skin diseases. ELISA tests are at present the most important method for diagnosis. A correlation between disease activity and antibody titres was verified, especially for pemphigus and pemphigoid diseases (13). The frequency of serological controls during the disease course mainly depends on the clinical picture. In phases of active disease, monitoring of autoantibodies is recommended every 4 weeks. With stable skin conditions, quarterly check-ups seem reasonable.
6 Eming and Hertl: Autoimmune bullous disorders 149 Fundamentally there are three goals. In the first instance, ELISA tests, as well as semi-quantitative immunoblots and immunoprecipitation, allow a correlation between the clinical picture and the extent of the antibody titre. Secondly, these examination methods allow characterisation of the autoantibody subclasses. In the acute stages of pemphigus disease there is already evidence that besides IgG 4, desmoglein-reactive autoantibodies of the class IgG 1 can be detected, as well as sporadic detection of IgE (7). Thirdly, characterisation of the epitope specificity of autoantibodies is possible (14, 15). Therefore, immunoserology not only confirms diagnosis, but also provides a better understanding of the immunopathogenesis of these diseases. References 1. Sitaru C, Zillikens D. Mechanisms of blister induction by autoantibodies. Exp Dermatol 2005;14: Hertl M. Humoral and cellular autoimmunity in autoimmune bullous skin disorders. Int Arch Allergy Immumol 2000;122: Hertl M, Schuler G. Bullous autoimmune dermatoses. 3: Diagnosis and therapy Hautarzt 2002;53: Chorzelski TP, Sulej J, Tchorzewska H, Jablonska S, Beutner EH, Kumar V. IgA class endomysium antibodies in dermatitis herpetiformis and coeliac disease. Ann NY Acad Sci 1983;4: Zillikens D, Rose PA, Balding SD, Liu Z, Olague-Marchan M, Diaz L, et al. Tight clustering of extracellular BP180 epitopes recognized by bullous pemphigoid autoantibodies. J Invest Dermatol 1997;109: Dieterich W, Laag E, Bruckner-Tuderman L, Reunala T, Karpati S, Zagoni T, et al. Antibodies to tissue transglutaminase as serologic markers in patients with dermatitis herpetiformis. J Invest Dermatol 1999;113: Späth S, Riechers R, Borradori L, Zillikens D, Büdinger L, Hertl M. Detection of autoantibodies of various subclasses (IgG1, IgG4, IgA, IgE) against desmoglein 3 in patients with acute onset and chronic pemphigus vulgaris. Br J Dermatol 2001;144: Thoma-Uszynski S, Uter W, Schwietzke S, Hofmann SC, Hunziker T, Bernard P, et al. BP230 and BP180 autoantibodies in bullous pemphigoid. J Invest Dermatol 2004;122: Chen M, Chan LS, Cai X, O Toole EA, Sample JC, Woodley DT. Development of an ELISA for rapid detection of anti-type VII collagen autoantibodies in epidermolysis bullosa acquisita. J Invest Dermatol 1997;108: Haase C, Büdinger L, Borradori L, Yee C, Merk HF, Yancey K, et al. Detection of IgG autoantibodies in the sera of patients with bullous and gestational pemphigoid: ELISA studies utilizing a baculovirus-encoded form of bullous pemphigoid antigen 2. J Invest Dermatol 1998; 110: Hofmann SC, Thoma-Uszynski S, Hunziker T, Bernard P, Koebnick C, Stauber A, et al. Severity and phenotype of bullous pemphigoid relate to autoantibody profile against the NH2- und COOH-terminal regions of BP180 ectodomain. J Invest Dermatol 2002;119: Bekou V, Thoma-Uszynski S, Wendler O, Uter W, Schwietzke S, Hunziker T, et al. Detection of laminin 5- specific auto-antibodies in mucous membrane and bullous pemphigoid sera by ELISA. J Invest Dermatol 2005;124: Amagai M, Komai A, Hashimoto T, Shirakata Y, Hashimito K, Yamada T, et al. Usefulness of enzyme-linked immunosorbent assay using recombinant desmogleins 1 and 3 for serodiagnosis of pemphigus. Br J Dermatol 1999;140: Sekiguchi M, Futei Y, Fujii Y, Iwasaki T, Nishikawa T, Amagai M. Dominant autoimmune epitopes recognized by pemphigus antibodies map to the N-terminal adhesive region of desmogleins. J Immunol 2001;167: Hacker-Foegen MK, Janson M, Amagai M, Fairley JA, Lin MS. Pathogenicity and epitope characteristics of antidesmoglein-1 from pemphigus foliaceus patients expressing only IgG1 autoantibodies. J Invest Dermatol 2003;121:
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