Pemphigoid gestationis: new insights into the pathogenesis lead to novel diagnostic tools
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1 BJOG: an International Journal of Obstetrics and Gynaecology September 2002, Vol. 109, pp Pemphigoid gestationis: new insights into the pathogenesis lead to novel diagnostic tools Introduction Pemphigoid gestationis (PG), previously referred to as herpes gestationis, is an autoimmune disease of pregnancy and the early postpartum period. It is not related to herpes virus infection; the old term rather reflects the occurence of herpetiform lesions as a part of the clinical picture 1. Table 1 summarises the major autoimmune blistering diseases subdivided into those with intra- and subepidermal split formation. PG belongs to the group of autoimmune subepidermal blistering diseases. Reports on the incidence of the disease range from 1:1700 to 1:50,000 pregnancies 2,3. More recent studies tend to provide higher estimates; this is most probably due to the development of more sensitive techniques for the diagnosis of PG 3,4. The disease tends to improve spontaneously during the later stages of pregnancy and exacerbate immediately after delivery 1. Subsequent flareups may occur with menstruation or with the use of oestrogen- and/or progesteronebased oral contraceptives 5,6,13. Skin lesions usually clear within three months after delivery without scarring or milia formation 1. Nursing may affect the duration of the disease postpartum. It was reported that breastfeeding patients had a significantly shorter duration of eruption than bottlefeeding ones 13. Provided the paternity remains the same, PG generally recurs with subsequent pregnancies, and when it does, the disease begins earlier and lasts longer 1,5. However, several pregancies skipped by PG despite unchanged paternity have been described 7,13,14. The explanation for this phenomenon remains uncertain. Methods The Medline database from 1966 onwards was searched using the key words pemphigoid gestationis and herpes gestationis. The Cochrane database and Excerpta Medica were searched from 1980 until to date present using the same key words. All English and German language abstracts were reviewed and relevant studies were retrieved. Clinical features Most commonly, the onset of PG is in the second or third trimester, but the disease may also develop in the first trimester or in the first month postpartum 5 7. In rare cases, PG may be associated with hydatiform mole and choriocarcinoma 8,9. Intense pruritus is a characteristic feature and may precede the skin lesions by days and weeks 1. The clinical presentation of PG is polymorphic. Initially, one may see erythematous papules, plaques or targetoid lesions, similar to those observed in erythema multiforme (Fig. 1A). Subsequently, small vesicles and larger bullae may develop on either normal skin or on urticarial plaques 5 7 (Fig. 1B). However, blister formation can be absent during the entire course of the disease Lesions typically first arise in the periumbilical area and then spread to buttocks, trunk and extremeties 11. The face and mucous membranes are usually spared 6, although PG has also been described with primary and predominant involvement of the oral mucosa 12. D RCOG 2002 BJOG: an International Journal of Obstetrics and Gynaecology PII: S (02) Histopathology Histopathologic findings in PG show some characteristic features but are insufficient to differentiate it from other autoimmune subepidermal blistering diseases such as bullous pemphigoid. Biopsy specimens from early urticarial lesions demonstrate epidermal and papillary dermal oedema with occasional foci of eosinophilic spongiosis. In the dermis, there is a perivascular infiltrate composed of lymphocytes, histiocytes and eosinophils. If blisters are found, they are localised subepidermally and the dermal papillae are usually preserved. Basal cell necrosis has also been observed 15. Immunogenetics There is a certain genetic predisposition towards the development of PG. HLA-DR3 was found in 61 85% of patients with PG and the combined presence of both HLA- DR3 and DR4 was reported in 43 45% of cases 13,16. Equally important are paternal histocompatibility antigens. HLA-DR2 was found in 50% of the husbands of patients with PG 17. Interestingly, 85% of patients with history of PG (as compared with 25% of normal multiparous women) demonstrated the presence of anti-hla antibodies, at least some of which were directed against paternal HLA expressed in their placentae. The significance of this phenomenon is
2 971 Table 1. Autoimmune blistering diseases and their antigens*. Disease Autoantigens Intraepidermal blisters Pemphigus foliaceus desmolglein 1 Pemphigus vulgaris desmolglein 3 Paraneoplastic pemphigus desmolglein 1, 3, and plakin proteins IgA pemphigus desmocollin 1, desmolglein 3 Subepidermal blisters Bullous pemphigoid BP180, BP230 Pemphigoid gestationis BP180, BP230 Lichen planus pemphigoides BP180, BP230 Linear IgA disease BP180, BP230, 285 kda antigen, type VII collagen, 255 kda antigen Cicatricial pemphigoid BP180, a 6 h 4 integrin, laminin 5 and laminin 6, type VII collagen Epidermolysis bullosa acquisita type VII collagen Dermatitis herpetiformis Duhring tissue transglutaminase (?) * The most important autoantigens of subepidermal blistering diseases are printed in bold type. unknown 17. In addition, patients with PG may be at increased risk for the development of other autoimmune diseases associated with HLA-DR3 and DR4, especially of Graves disease 7,18. Immunopathology and diagnosis The immunopathologic hallmark of PG is linear deposition of C3 along the dermal epidermal junction as detected by direct immunofluorescence microscopy in biopsy specimens from urticarial lesions or from skin adjacent to blisters. Concomitant deposition of IgG may be demonstrated in about one-third of cases 1. If blisters are present, perilesional normal appearing skin is the best site for biopsy, as inflammation within the lesions may result in destruction of immunoreactants. By conventional indirect immunofluorescence microscopy, only 25% of patients with PG show circulating IgG antibodies against the dermal epidermal junction. However, using a special indirect complement fixation immunofluorescence technique, the majority of patients sera demonstrate complement-fixing IgG directed against an antigen of the dermal epidermal junction, the so-called herpes gestationis factor 19,20. If 1 M NaCl-split human skin is used as a substrate, PG autoantibodies bind to the epidermal side of the artificial blister 21 (Fig. 2). Immunoblotting studies demonstrated that 90% of PG sera recognise the 180-kDa bullous pemphigoid antigen (BP180), a major constituent of the dermal epidermal junction 22 (Fig. 3). Fig. 1. (A) Urticarial papules and plaques on the left trunk. (B) Herpetiform vesicles on the right trunk.
3 972 Fig. 2. Indirect immunofluorescence microscopy on 1 M NaCl-split skin. Linear deposition of C3 along the epidermal side of the split (250). Bullous pemphigoid is another subepidermal blistering disease that predominantly affects the elderly (mean age 76 years) 23, and shows close immunopathologic resemblance to PG. In addition to autoantibodies against BP180, about 10% of PG sera recognise the 230-kDa bullous pemphigoid antigen (BP230) The pathogenic relevance of autoantibodies directed against BP180, but not against BP230, has been demonstrated using a passive transfer animal model. Rabbit antibodies were raised against murine BP180 and passively transferred into neonatal mice. Intraperitoneal or subepidermal injection of these autoantibodies reproduced the clinical, histologic and immunopathologic features of PG and bullous pemphigoid in the animals 27. Interestingly, blister formation in this experimental model is dependent on complement activation and the recruitment of neutrophils 28,29. BP180 is a transmembrane protein associated with hemidesmosomes of basal keratinocytes (Fig. 4). Hemidesmosomes form the central portion of the dermal epidermal anchoring complex that functions by establishing a stable link between the keratin cytoskeleton of basal keratinocytes and structures of the upper dermis 33,34. This complex is of critical importance for maintaining dermal epidermal adhesion. It is hypothesised that binding of autoantibodies to BP180 initiates an inflammatory cascade, finally leading to blister formation within the lamina lucida of the dermal epidermal junction 35. BP180 is a transmembrane molecule consisting of an N-terminal intracellular domain and a C-terminal ectodomain. The ectodomain of BP180 is composed of 15 collagenous sequences [(X-Y-Glycine) x ] interrupted by 16 non-collagenous (NC) domains 31,36,37. The 16th non-collagenous (NC16A) and the 15th collagenous (C15) domain constitute a rigid rod spanning the lamina lucida of the dermal epidermal junction, whereas the remaining portion of BP180 forms a flexible C-terminal tail extending into the lamina densa 32. The NC16A domain has been identified as an immunodominant region of BP180 and is targeted by the majority of PG autoantibodies (Fig. 3). Within this membraneproximal stretch of 76 amino acids, PG autoantibodies bind to five well-defined epitopes (designated NC16A1, NC16A2, NC16A2.5, NC16A3 and NC16A5) 42,43 (Fig. 4). Four of these epitopes (NC16A1 through NC16A3) are also recognised by sera from patients with bullous pemphigoid and linear IgA disease 44,45. In contrast, PG sera do not react with epitope NC16A4, which is a major target of autoantibodies in lichen planus pemphigoides 46,47. Analysis of immunoglobulin subclasses in PG sera demonstrated that antibodies to BP180 NC16A mainly belong to IgG1 and IgG3 isotypes 42. This is in contrast to findings in bullous pemphigoid, where IgG4 is the major subclass of anti-bp180 NC16A autoantibodies 48. As IgG1 and IgG3 are the subclasses with the strongest complement-fixing properties, these findings may well explain complement deposition at the dermal epidermal junction, which is the most important immunopathologic finding in the skin of patients with PG. Elucidation of the target antigen and fine specificity of autoantibodies in PG and bullous pemphigoid has prompted the development of novel tools for the diagnosis of these diseases. An ELISA system utilising recombinant BP180 NC16A as the target antigen demonstrated high specificity (99%) and sensitivity (94%) for the detection of autoantibodies in sera from patients with bullous pemphigoid 49. Levels of autoantibodies to BP180 as detected by this ELISA correlated with disease activity (in contrast to titres of indirect immunofluorescence microscopy on salt-split skin) and may be Fig. 3. Serum from rabbit 8009 (R8009), raised against recombinant human NC16A, and from patients with PG and bullous pemphigoid (BP) recognise native BP180 in extracts of cultured human keratinocytes (KC-E) and a recombinant form of the immunodominant BP180 NC16A domain (NC16A) by immunoblotting. NHS ¼ normal human serum. Migration positions of molecular weight markers are indicated to the left of the blots.
4 973 Fig. 4. Schematic diagram of BP180 and recombinant forms of the NC16A domain. BP180 is a transmembrane hemidesmosomal protein of basal keratinocytes with type II orientation (i.e. the NH 2 terminus localises to the cytoplasm while the COOH terminus projects into the extracellular space). The BP180 molecule consists of a series of alternating collagenous (C, light grey) and non-collagenous (NC, dark grey) domains. The extracellular portion of the 16th non-collagenous domain (NC16A) is the major target of autoantibodies in patients with PG. NC16A has been subdivided into six fragments (NC16A1 through NC16A5) each approx. 15 amino acids in length (boxes). Amino acid residue numbers are shown above the boxes. C15 ¼ 15th collagenous domain of BP180; HP ¼ hemidesmosomal plaque. helpful in guiding treatment decisions in this disease 50. Another sensitive and specific ELISA utilising the entire BP180 ectodomain as the target antigen has been described 51. Recent data from our laboratory suggest that the BP180 NC16A ELISA is also a suitable tool for the diagnosis of PG and monitoring disease activity in patients with this disease 41. The cause for the production of autoantibodies to BP180 in patients with PG is still unclear. Several lines of evidence suggest an important role of placental antigens for initiation of the autoimmune response: (1) PG occurs only during pregnancy or in patients with choriocarcinoma and hydatiform mole 8,9 ; (2) No case of vesiculobullous eruption similar to PG has been reported in men with choriocarcinoma (unlike the tumour in women, which develops from gestational tissue with both maternal and paternal antigens represented, choriocarcinoma in men is totally derived from syngeneic tissue) 6 ; (3) Circulating autoantibodies in patients with PG bind to the dermal epidermal junction of skin and amnion 52,53 ; (4) BP180 is present not only in the epidermis but also in the amnion 54 ; (5) Abnormal expression of MHC class II molecules by cells of the amniochorionic stroma has been demonstrated in patients with PG 55,56 ; (6) In cases, in which by chance or altered paternity the mother and the fetus have identical HLA-D phenotypes, unaffected or skipped pregnancies occur 13. Based on these data, two possible mechanisms for the initiation of an autoimmune response in PG have been proposed. It is conceivable that placental BP180 is presented to the maternal immune system in association with abnormal MHC molecules, thus triggering the production of autoantibodies that cross react with the skin.
5 974 Alternatively, the placental stromal cells may evoke an allogeneic reaction to the BP180 antigen presented in the context of paternal MHC molecules of the placental stroma 57. However, the exact mechanism leading to the breakdown of protective tolerance to the fetoplacental unit remains to be determined. Differential diagnosis The most important differential diagnosis is between the prebullous stage of PG and polymorphic eruption of pregnancy (PEP) 11. PEP is an ill-defined group of nonautoimmune pregnancy-associated dermatoses including pruritic urticarial papules and plaques of pregnancy (PUPPP), erythema multiforme of pregnancy, prurigo anularis, toxaemic rash of pregnancy, prurigo gestationis Besnier, papular dermatitis of pregnancy, pruritic folliculitis of pregnancy and prurigo of pregnancy. Clinically and histologically, it is impossible to distinguish these conditions from each other and as long as there is no blister formation from PG 58. Differentiation between PEP and PG is possible by immunofluorescence microscopy or by immunoblot and ELISA analyses using recombinant forms of BP180. These studies will not demonstrate tissue bound or circulating autoantibodies in PEP. Pruritus in association with elevated levels of serum bile acids is the dominant symptom of intrahepatic cholestasis of pregnancy (ICP), another pregnancy-related disorder that must be distinguished from PG ICP may be associated with risk of fetal distress 3,61. No cutaneous lesions except for excoriations secondary to scratching are present, and no autoantibodies are detected 61. In addition to pregnancy-specific disorders, the differential diagnosis of PG has to consider other dermatoses, which coincidentally occur during pregnancy, including urticaria, insect bites, erythema multiforme, contact dermatitis, dermatitis herpetiformis and linear IgA disease. Most of these diseases can be differentiated from PG by routine histology; none shows IgG autoantibodies to BP Fetal risks Autoantibodies in PG belong to the IgG class of immunoglobulins and as such are able to cross the placental barrier. As a result, 5 10% of the newborns show urticarial, vesicular or bullous lesions. In the skin of uninvolved infants, deposition of C3 and IgG along the dermal epidermal junction may be demonstrated by direct immunofluorescence microscopy 5,6. The lesions invariably resolve during the first few weeks after delivery and usually do not require any treatment 11. Other aspects of fetal prognosis in PG are controversial. Lawley et al. 5 found PG to be associated with an increased risk of preterm delivery and fetal death. This study was criticised for its heavy reliance on cases described in the literature that tends to exaggerate complications 6. Later series did not find an increased fetal morbidity or mortality in PG 2,6. However, subsequent studies confirmed that PG is associated with an increased incidence of premature deliveries and both of small for date and low birthweight babies. The latter finding may be due to a mild placental failure induced by PG autoantibodies 18,62,63. If the mother has been treated with high dose corticosteroids, delivery should take place in a hospital with facilities for intensive care of the infant. The newborn should be monitored for signs of adrenal suppression, although this is a rare event 11. Treatment The treatment of PG is aimed at suppression of new blister formation and relief of the intense pruritus. In milder cases, this can be achieved by the use of topical corticosteroids in combination with oral antihistamines. In more severe cases, the administration initially of mg prednisolone per kilogram body weight daily is generally sufficient. This dose can usually be decreased during the course of the disease 1,5,15. Flareups postpartum may require a temporary increase of the corticosteroid dose 11. Treatment with systemic corticosteroids was not found to be a factor in increasing or decreasing fetal risks in PG 18. Conclusion The clinical diagnosis of PG can be difficult, as most patients do not develop the characteristic vesiculobullous lesions. The duration of pregnancy is probably too brief to result in autoantibody levels high enough to achieve dermal epidermal separation. The observation that in bullous pemphigoid, a disease closely related to PG, blister formation is usually preceded by a long premonitory phase characterised by itchy papules, urticarial plaques and other non-bullous lesions, supports this hypothesis. Detection of circulating autoantibodies to BP180 by immunoblotting or ELISA facilitates the diagnosis of PG with the help of serologic tests, even in the absence of blisters. Both techniques are sensitive and specific and, therefore, can be used for differentiating PG from other pruritic dermatoses of pregnancy. Assaying serum levels of autoantibodies to BP180 is also useful in monitoring disease activity and its response to treatment. Acknowledgements This work was supported by grant from the Wilhelm Sander-Stiftung, Munich, Germany.
6 975 Iakov Shimanovich, Eva B. Bröcker, Detlef Zillikens Department of Dermatology, University of Würzburg, Würzburg, Germany References 1. Shornick JK. Herpes gestationis. J Am Acad Dermatol 1987;17: Holmes RC, Black MM, Dann J, James DC, Bhogal B. A comparative study of toxic erythema of pregnancy and herpes gestationis. Br J Dermatol 1982;106: Roger D, Vaillant L, Fignon A, et al. Specific pruritic diseases of pregnancy. A prospective study of 3192 women. Arch Dermatol 1994;130: Zurn A, Celebi CR, Bernard P, Didierjean L, Saurat JH. A prospective study of 111 cases of pruritic dermatoses of pregnancy: IgM anti-basement membrane zone antibodies as a novel finding. Br J Dermatol 1992;126: Lawley TJ, Stingl G, Katz SI. Fetal and maternal risk factors in herpes gestationis. Arch Dermatol 1978;114: Shornick JK, Bangert JL, Freeman RG, Gilliam JN. Herpes gestationis: clinical and histological features of twenty-eight cases. JAmAcad Dermatol 1983;8: Jenkins RE, Hern S, Black MM. 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Molecular heterogeneity of the bullous pemphigoid antigens as detected by immunoblotting. J Immunol 1986;136: Liu Z, Diaz LA, Troy JL, et al. A passive transfer model of the organspecific autoimmune disease, bullous pemphigoid, using antibodies generated against the hemidesmosomal antigen, BP180. J Clin Invest 1993;92: Liu Z, Giudice GJ, Swartz SJ, et al. The role of complement in experimental bulluos pemphigoid. J Clin Invest 1995;95: Liu Z, Giudice GJ, Zhou X, et al. A major role for neutrophils in experimental bullous pemphigoid. J Clin Invest 1997;100: Diaz LA, Ratrie III H, Saunders WS, et al. Isolation of a human epidermal cdna corresponding to the 180-kD autoantigen recognized by bullous pemphigoid and herpes gestationis sera. Immunolocalization of this protein to the hemidesmosome. J Clin Invest 1990; 86: Giudice GJ, Emery DJ, Diaz LA. Cloning and primary structural analysis of the bullous pemphigoid autoantigen BP180. J Invest Dermatol 1992;99: Zillikens D, Giudice GJ. 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J Immunol 1993;151: Murakami H, Amagai M, Higashiyama M, et al. Analysis of antigens recognized by autoantibodies in herpes gestationis. Usefulness of immunoblotting using a fusion protein representing an extracellular domain of the 180 kd bullous pemphigoid antigen. J Dermatol Sci 1996;13: Perriard J, Janin F, Favre B, et al. IgG autoantibodies from bullous pemphigoid (BP) patients bind antigenic sites on both the extracellular and the intracellular domains of the BP antigen 180. J Invest Dermatol 1999;112: Jainta S, Powell J, Chimanovitch I, et al. Autoantibodies in patients with pemphigoid gestationis do not recognize the 120 kda soluble ectodomain of BP180/type XVII collagen. Arch Dermatol Res 2001; 293:95 [abstract].
7 Chimanovitch I, Schmidt E, Messer G, et al. IgG1 and IgG3 are the major immunoglobulin subclasses targeting epitopes within BP180 NC16A in pemphigoid gestationis. J Invest Dermatol 1999;113: Lin MS, Gharia M, Fu CL, et al. Molecular mapping of the major epitopes of BP180 recognized by herpes gestationis autoantibodies. Clin Immunol 1999;92: Zillikens D, Rose PA, Balding SD, et al. Tight clustering of extracellular BP180 epitopes recognized by bullous pemphigoid antibodies. J Invest Dermatol 1997;109: Zillikens D, Herzele K, Georgi M, et al. Autoantibodies in a subgroup of patients with linear IgA disease react with the NC16A domain of BP180. J Invest Dermatol 1999;113: Zillikens D, Caux F, Mascaro JM, et al. Autoantibodies in lichen planus pemphigoides react with a novel epitope within the C-terminal NC16A domain of BP180. J Invest Dermatol 1999;113: Kromminga A, Sitaru C, Meyer J, et al. Cicatricial pemphigoid differs from bullous pemphigoid and pemphigoid gestationis regarding the fine specificity of autoantibodies to the BP180 NC16A domain. J Dermatol Sci 2002;28: Döpp R, Schmidt E, Chimanovitch I, Leverkus M, Bröcker EB, Zillikens D. IgG4 and IgE are the major immunoglobulins targeting the NC16A domain of BP180 in bullous pemphigoid: serum levels of these immunoglobulins reflect disease activity. J Am Acad Dermatol 2000;42: Zillikens D, Mascaro JM, Rose PA, et al. A highly sensitive enzymelinked immunosorbent assay for the detection of circulating anti-bp180 autoantibodies in patients with bullous pemphigoid. J Invest Dermatol 1997;109: Schmidt E, Obe K, Bröcker EB, Zillikens D. Serum levels of antibodies to BP180 correlate with disease activity in patients with bullous pemphigoid. Arch Dermatol 2000;136: Haase C, Büdinger L, Borradori L, et al. Detection of IgG autoantibodies in the sera of patients with bullous and gestational pemphigoid: ELISA studies utilizing baculovirus-encoded form of bullous pemphigoid antigen 2. J Invest Dermatol 1998;110: Ortonne JP, Hsi BL, Verrando P, et al. Herpes gestationis factor reacts with the amniotic epithelial basement membrane. Br J Dermatol 1987;117: Kelly SE, Bhogal BS, Wojnarowska F, Black MM. Expression of a pemphigoid gestationis-related antigen by human placenta. Br J Dermatol 1988;118: Fairley JA, Heintz PW, Neuburg M, Diaz LA, Giudice GJ. Expression pattern of the bullous pemphigoid-180 antigen in normal and neoplastic epithelia. Br J Dermatol 1995;133: Kelly SE, Black MM, Fleming S. Antigen-presenting cells in the skin and placenta in pemphigoid gestationis. Br J Dermatol 1990;122: Borthwick GM, Holmes RC, Stirrat GM. Abnormal expression of class II MHC antigens in placentae from patients with pemphigoid gestationis. Placenta 1988;9: Kelly SE, Black MM, Fleming S. Pemphigoid gestationis: a unique mechanism of initiation of an autoimmune response by MHC class II molecules? J Pathol 1989;158: Borradori L, Saurat JH. Specific dermatoses of pregnancy. Toward a comprehensive view? Arch Dermatol 1994;130: Laatikainen TJ. Post-prandial serum bile acids in cholestasis of pregnancy. Ann Clin Res 1978;10: Berg B, Helm G, Petersohn L, Tryding N. Cholestasis of pregnancy: clinical and laboratory studies. Acta Obstet Gynecol Scand 1986;65: Reyes H. The spectrum of liver and gastrointestinal disease seen in cholestatis of pregnancy. Gastroenterol Clin North Am 1992;21: Holmes RC, Black MM. The fetal prognosis in pemphigoid gestationis. Br J Dermatol 1984;110: Mascaro Jr JM, Lecha M, Mascaro JM. Fetal morbidity in herpes gestationis. Arch Dermatol 1995;131:
Egyptian Dermatology Online Journal Vol. 8 No 2: 6, December Yasmeen J Bhat*, Iffat Hasan*, Atiya Yaseen*, Hina Altaf*, Shylla Mir**
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