Oral Lesions in Autoimmune Bullous Diseases: An Overview of Clinical Characteristics and Diagnostic Algorithm

Hanan Rashid, Aniek Lamberts, Gilles F H Diercks, Hendri H Pas, Joost M Meijer, Maria C Bolling, Barbara Horváth, Hanan Rashid, Aniek Lamberts, Gilles F H Diercks, Hendri H Pas, Joost M Meijer, Maria C Bolling, Barbara Horváth

Abstract

Autoimmune bullous diseases are a group of chronic inflammatory disorders caused by autoantibodies targeted against structural proteins of the desmosomal and hemidesmosomal plaques in the skin and mucosa, leading to intra-epithelial or subepithelial blistering. The oral mucosa is frequently affected in these diseases, in particular, in mucous membrane pemphigoid, pemphigus vulgaris, and paraneoplastic pemphigus. The clinical symptoms are heterogeneous and may present with erythema, blisters, erosions, and ulcers localized anywhere on the oral mucosa, and lead to severe complaints for the patients including pain, dysphagia, and foetor. Therefore, a quick and proper diagnosis with adequate treatment is needed. Clinical presentations of autoimmune bullous diseases often overlap and diagnosis cannot be made based on clinical features alone. Immunodiagnostic tests are of great importance in differentiating between the different diseases. Direct immunofluorescence microscopy shows depositions of autoantibodies along the epithelial basement membrane zone in mucous membrane pemphigoid subtypes, or depositions on the epithelial cell surface in pemphigus variants. Additional immunoserological tests are useful to discriminate between the different subtypes of pemphigoid, and are essential to differentiate between pemphigus and paraneoplastic pemphigus. This review gives an overview of the clinical characteristics of oral lesions and the diagnostic procedures in autoimmune blistering diseases, and provides a diagnostic algorithm for daily practice.

Conflict of interest statement

Barbara Horvath has received grants from AbbVIe, Janssen-Cilag, Solenne B.V., and Celgene; consulting fees from AbbVie, Janssen-Cilag, Novartis, UCB Pharma, Akari Pharmaceutics, Philips, and Roche and support for travel from AbbVie, Janssen-Cilag, and Novartis. Hanan Rashid, Aniek Lamberts, Gilles F.H. Diercks, Hendri H. Pas, Joost M. Meijer, and Maria C. Bollin have no conflicts of interest that are directly relevant to the content of this article.

Figures

Fig. 1
Fig. 1
Overlapping features in autoimmune bullous diseases, Stevens–Johnson syndrome, and oral lichen planus demonstrate that oral blistering diseases cannot be differentiated based on clinical presentation. Lesions include desquamative gingivitis (a, d, m), cheilitis (e, f, g, h, j, k), erythema and erosions and blistering of the buccal mucosa (b, i, l, n), palatum (c), and tongue (e, o)
Fig. 2
Fig. 2
Flowchart of the diagnostic pathway in patients with oral blistering, with the focus on autoimmune bullous diseases affecting the oral mucosa
Fig. 3
Fig. 3
Immunofluorescence results compatible with the diagnosis of pemphigoid diseases. a Direct immunofluorescence microscopy shows linear IgG along the epithelial basement membrane zone in an n-serrated pattern. b Direct immunofluorescence microscopy shows linear IgG along the epithelial basement membrane zone in a u-serrated pattern. c Indirect immunofluorescence microscopy on a substrate of salt-split skin (indirect immunofluorescence on salt-split skin), showing IgG bound to the epithelial side of the artificial split, wherein BP180 and BP230 are located. d Indirect immunofluorescence on salt-split skin showing IgG bound to the dermal side of the artificial split, wherein laminin-332, p200, and type VII collagen are located
Fig. 4
Fig. 4
Direct immunofluorescence microscopy staining of a pemphigus patient. a IgG staining in a smooth epithelial cell surface pattern. b IgG staining in a granular epithelial cell surface pattern
Fig. 5
Fig. 5
Diagnostic results in paraneoplastic pemphigus. a Direct immunofluorescence microscopy with an epithelial cell surface and anti-basement membrane zone pattern. b Indirect immunofluorescence microscopy on a rat bladder with IgG staining in an epithelial cell surface pattern, compatible with the diagnosis of paraneoplastic pemphigus. c Serum analyzed for IgG against paraneoplastic pemphigus antigens by immunoblotting (1) and immunoprecipitation (2). A2ML1 alpha-2-macroglobulin-like 1, EPL epiplakin, PPL periplakin

References

    1. Jonkman MF. Autoimmune bullous diseases. London: Springer; 2016.
    1. Schmidt E, Zillikens D. Pemphigoid diseases. Lancet. 2013;381:320–332. doi: 10.1016/S0140-6736(12)61140-4.
    1. Bystryn J-C, Rudolph JL. Pemphigus. Lancet. 2005;366:61–73. doi: 10.1016/S0140-6736(05)66829-8.
    1. Murrell DF, Pena S, Joly P, Marinovic B, Hashimoto T, Diaz LA, et al. Diagnosis and management of pemphigus: recommendations by an international panel of experts. J Am Acad Dermatol. 2018 doi: 10.1016/j.jaad.2018.02.021.
    1. Feliciani C, Joly P, Jonkman MF, Zambruno G, Zillikens D, Ioannides D, et al. Management of bullous pemphigoid: the European Dermatology Forum consensus in collaboration with the European Academy of Dermatology and Venereology. Br J Dermatol. 2015;172:867–877. doi: 10.1111/bjd.13717.
    1. Hertl M, Jedlickova H, Karpati S, Marinovic B, Uzun S, Yayli S, et al. Pemphigus: S2 guideline for diagnosis and treatment—guided by the European Dermatology Forum (EDF) in cooperation with the European Academy of Dermatology and Venereology (EADV) J Eur Acad Dermatol Venereol. 2015;29:405–414. doi: 10.1111/jdv.12772.
    1. Chan LS, Ahmed AR, Anhalt GJ, Bernauer W, Cooper KD, Elder MJ, et al. The first international consensus on mucous membrane pemphigoid: definition, diagnostic criteria, pathogenic factors, medical treatment, and prognostic indicators. Arch Dermatol. 2002;138:370–379.
    1. Meijer JM, Diercks GFH, Schmidt E, Pas HH, Jonkman MF. Laboratory diagnosis and clinical profile of anti-p200 pemphigoid. JAMA Dermatol. 2016;152:897–904. doi: 10.1001/jamadermatol.2016.1099.
    1. Frew JW, Murrell DF. Paraneoplastic pemphigus (paraneoplastic autoimmune multiorgan syndrome): clinical presentations and pathogenesis. Dermatol Clin. 2011;29(3):419–425. doi: 10.1016/j.det.2011.03.018.
    1. Suliman NM, Johannessen AC, Ali RW, Salman H, Astrom AN. Influence of oral mucosal lesions and oral symptoms on oral health related quality of life in dermatological patients: a cross sectional study in Sudan. BMC Oral Health. 2012;12:19. doi: 10.1186/1472-6831-12-19.
    1. Jascholt I, Lai O, Zillikens D, Kasperkiewicz M. Periodontitis in oral pemphigus and pemphigoid: a systematic review of published studies. J Am Acad Dermatol. 2017;76(975–978):e3.
    1. Chan LS, Wojnarowska F, Fine J-D, Zone JJ, Kirtschig G, Lozada-Nur F, et al. The first international consensus on mucous membrane pemphigoid. Arch Dermatol. 2004;138:370–379.
    1. Bertram F, Bröcker EB, Zillikens D, Schmidt E. Prospektive Untersuchung der Inzidenz blasenbildender Autoimmundermatosen in Unterfranken. J Dtsch Dermatol Ges. 2009;7:434–440.
    1. Arduino PG, Broccoletti R, Carbone M, Conrotto D, Pettigiani E, Giacometti S, et al. Describing the gingival involvement in a sample of 182 Italian predominantly oral mucous membrane pemphigoid patients: a retrospective series. Med Oral Patol Oral Cir Bucal. 2017;22:e149–e152.
    1. Bagan J, Jiménez Y, Murillo J, Bagan L. Oral mucous membrane pemphigoid: a clinical study of 100 low-risk cases. Oral Dis. 2018;24:132–134. doi: 10.1111/odi.12744.
    1. Welsh KI, Challacombe SJ, Black MM, Theron J, Setterfield J, Wojnarowska F, et al. Mucous membrane pemphigoid: HLA-DQB1*0301 is associated with all clinical sites of involvement and may be linked to antibasement membrane IgG production. Br J Dermatol. 2010;145:406–414.
    1. Carrozzo M, Fasano ME, Broccoletti R, Carbone M, Cozzani E, Rendine S, et al. HLA-DQB1 alleles in Italian patients with mucous membrane pemphigoid predominantly affecting the oral cavity. Br J Dermatol. 2003;145:805–808. doi: 10.1046/j.1365-2133.2001.04448.x.
    1. Delgado JC, Turbay D, Yunis EJ, Yunis JJ, Morton ED, Bhol K, et al. A common major histocompatibility complex class II allele HLA-DQB1*0301 is present in clinical variants of pemphigoid. Proc Natl Acad Sci USA. 1996;93:8569–8571. doi: 10.1073/pnas.93.16.8569.
    1. Mustafa MB, Porter SR, Smoller BR, Sitaru C. Oral mucosal manifestations of autoimmune skin diseases. Autoimmun Rev. 2015;14:930–951. doi: 10.1016/j.autrev.2015.06.005.
    1. Balding SD, Prost C, Diaz LA, Bernard P, Bedane C, Aberdam D, et al. Cicatricial pemphigoid auto antibodies react with multiple sites on the BP180 extracellular domain. J Investig Dermatol. 1996;106:141–146. doi: 10.1111/1523-1747.ep12329728.
    1. Oyama N, Setterfield JF, Powell AM, Sakuma-Oyama Y, Albert S, Bhogal BS, et al. Bullous pemphigoid antigen II (BP180) and its soluble extracellular domains are major autoantigens in mucous membrane pemphigoid: the pathogenic relevance to HLA class II alleles and disease severity. Br J Dermatol. 2006;154:90–98. doi: 10.1111/j.1365-2133.2005.06998.x.
    1. Lee JB, Liu Y, Hashimoto T. Cicatricial pemphigoid sera specifically react with the most C-terminal portion of BP180. J Dermatol Sci. 2003;32:59–64. doi: 10.1016/S0923-1811(03)00035-5.
    1. Calabresi V, Arduino P, Tirone F, Parodi A, Zambruno G, Bertolusso G, et al. Oral pemphigoid autoantibodies preferentially target BP180 ectodomain. Clin Immunol. 2006;122:207–213. doi: 10.1016/j.clim.2006.10.007.
    1. Setterfield J, Shirlaw PJ, Kerr-Muir M, Neill S, Bhogal BS, Morgan P, et al. Mucous membrane pemphigoid: a dual circulating antibody response with IgG and IgA signifies a more severe and persistent disease. Br J Dermatol. 1998;138:602–610. doi: 10.1046/j.1365-2133.1998.02168.x.
    1. Buonavoglia A, Leone P, Dammacco R, Di Lernia G, Petruzzi M, Bonamonte D, et al. Pemphigus and mucous membrane pemphigoid: an update from diagnosis to therapy. Autoimmun Rev. 2019;18(4):349–358. doi: 10.1016/j.autrev.2019.02.005.
    1. Scully C, Lo Muzio L. Oral mucosal diseases: mucous membrane pemphigoid. Br J Oral Maxillofac Surg. 2008;46:358–366. doi: 10.1016/j.bjoms.2007.07.200.
    1. Petruzzi M. Mucous membrane pemphigoid affecting the oral cavity: short review on etiopathogenesis, diagnosis and treatment. Immunopharmacol Immunotoxicol. 2012;34:363–367. doi: 10.3109/08923973.2011.608684.
    1. Villa A, Treister N, Woo S-B, Saavedra A, Sultan A. Oral mucous membrane pemphigoid and pemphigus vulgaris: a retrospective two-center cohort study. Oral Dis. 2017;23:498–504. doi: 10.1111/odi.12639.
    1. Ramos-e-Silva M, de-Moura-Ferreira A, Castro Jacques C. Oral involvement in autoimmune bullous diseases. Clin Dermatol. 2011;29:443–454. doi: 10.1016/j.clindermatol.2011.01.015.
    1. Perschbacher K. Mucocutaneous diseases of the oral cavity. Diagn Histopathol. 2018;24:166–171. doi: 10.1016/j.mpdhp.2018.03.004.
    1. Baglama Š, Trčko K, Rebol J, Miljković J. Oral manifestations of autoinflammatory and autoimmune diseases. Acta Dermatovenerol Alp Pannonica Adriat. 2018;27:9–16.
    1. Chin-Che Hsu R, Lazarova Z, Lee HG, Tung YC, Yu HS. Antiepiligrin cicatricial pemphigoid. J Am Acad Dermatol. 2000;42:841–844. doi: 10.1067/mjd.2000.104790.
    1. Egan CA, Lazarova Z, Darling TN, Yee C, Coté T, Yancey KB. Anti-epiligrin cicatricial pemphigoid and relative risk for cancer. Lancet. 2001;357:1850–1851. doi: 10.1016/S0140-6736(00)04971-0.
    1. Bernard P, Antonicelli F, Bedane C, Joly P, Le Roux-Villet C, Duvert-Lehembre S, et al. Prevalence and clinical significance of anti-laminin 332 autoantibodies detected by a novel enzyme-linked immunosorbent assay in mucous membrane pemphigoid. JAMA Dermatol. 2013;149:533–540. doi: 10.1001/jamadermatol.2013.1434.
    1. Benzaquen M, Suter VGA, Borradori L, Gschwend M, Feldmeyer L. Mucous membrane pemphigoid of the oral lichen type: a retrospective analysis of 16 cases. J Eur Acad Dermatol Venereol. 2019;33:e205–e207. doi: 10.1111/jdv.15473.
    1. Fukuda A, Himejima A, Tsuruta D, Koga H, Ohyama B, Morita S, et al. Four cases of mucous membrane pemphigoid with clinical features of oral lichen planus. Int J Dermatol. 2016;55:657–665. doi: 10.1111/ijd.12884.
    1. Chen M, Kim GH, Prakash L, Woodley DT. Epidermolysis bullosa acquisita: autoimmunity to anchoring fibril collagen. Autoimmunity. 2012;45:91–101. doi: 10.3109/08916934.2011.606450.
    1. Buijsrogge JJA, Diercks GFH, Pas HH, Jonkman MF. The many faces of epidermolysis bullosa acquisita after serration pattern analysis by direct immunofluorescence microscopy. Br J Dermatol. 2011;165:92–98. doi: 10.1111/j.1365-2133.2011.10346.x.
    1. Bascones-Martínez A, García-García V, Meurman JH, Requena-Caballero L. Immune-mediated diseases: what can be found in the oral cavity? Int J Dermatol. 2015;54:258–270. doi: 10.1111/ijd.12681.
    1. Lings K, Bygum A. Linear IgA bullous dermatosis: a retrospective study of 23 patients in Denmark. Acta Derm Venereol. 2015;95:466–471. doi: 10.2340/00015555-1990.
    1. Wojnarowska F, Marsden RA, Bhogal B, Black MM. Chronic bullous disease of childhood, childhood cicatricial pemphigoid, and linear IgA disease of adults: a comparative study demonstrating clinical and immunopathologic overlap. J Am Acad Dermatol. 1988;19:792–805. doi: 10.1016/S0190-9622(88)70236-4.
    1. Sánchez AR, Rogers RS, Kupp LI, Sheridan PJ. Desquamative gingivitis associated with IgG/IgA pemphigoid presents a challenging diagnosis and treatment: a case report. J Periodontol. 2005;75:1714–1719. doi: 10.1902/jop.2004.75.12.1714.
    1. Chen KR, Shimizu S, Miyakawa S, Ishiko A, Shimizu H, Hashimoto T. Coexistence of psoriasis and an unusual IgG-mediated subepidermal bullous dermatosis: identification of a novel 200-kDa lower lamina lucida target antigen. Br J Dermatol. 1996;134:340–346. doi: 10.1111/j.1365-2133.1996.tb07625.x.
    1. Zillikens D, Kawahara Y, Ishiko A, Shimizu H, Mayer J, Rank CV, et al. A novel subepidermal blistering disease with autoantibodies to a 200-kDa antigen of the basement membrane zone. J Investig Dermatol. 1996;106:1333–1338. doi: 10.1111/1523-1747.ep12349283.
    1. Goletz S, Hashimoto T, Zillikens D, Schmidt E. Anti-p200 pemphigoid. J Am Acad Dermatol. 2014;71:185–191. doi: 10.1016/j.jaad.2014.02.036.
    1. Hubner F, Recke A, Zillikens D, Linder R, Schmidt E. Prevalence and age distribution of pemphigus and pemphigoid diseases in Germany. J Investig Dermatol. 2016;136(12):2495–2498. doi: 10.1016/j.jid.2016.07.013.
    1. Tsankov N, Vassileva S, Kamarashev J, Kazandjieva J, Kuzeva V. Epidemiology of pemphigus in Sofia, Bulgaria: a 16-year retrospective study (1980–1995) Int J Dermatol. 2000;39:104–108. doi: 10.1046/j.1365-4362.2000.00864.x.
    1. Hahn-Ristic K, Rzany B, Amagai M, Brocker EB, Zillikens D. Increased incidence of pemphigus vulgaris in southern Europeans living in Germany compared with native Germans. J Eur Acad Dermatol Venereol. 2002;16:68–71. doi: 10.1046/j.1468-3083.2002.00384.x.
    1. V’lckova-Laskoska MT, Laskoski DS, Kamberova S, Caca-Biljanovska N, Volckova N. Epidemiology of pemphigus in Macedonia: a 15-year retrospective study (1990–2004) Int J Dermatol. 2007;46:253–258. doi: 10.1111/j.1365-4632.2006.03010.x.
    1. Micali G, Musumeci ML, Nasca MR. Epidemiologic analysis and clinical course of 84 consecutive cases of pemphigus in eastern Sicily. Int J Dermatol. 1998;37:197–200. doi: 10.1046/j.1365-4362.1998.00428.x.
    1. Baican A, Baican C, Chiriac G, Chiriac MT, Macovei V, Zillikens D, et al. Pemphigus vulgaris is the most common autoimmune bullous disease in Northwestern Romania. Int J Dermatol. 2010;49:768–774. doi: 10.1111/j.1365-4632.2009.04345.x.
    1. Michailidou EZ, Belazi MA, Markopoulos AK, Tsatsos MI, Mourellou ON, Antoniades DZ. Epidemiologic survey of pemphigus vulgaris with oral manifestations in northern Greece: retrospective study of 129 patients. Int J Dermatol. 2007;46:356–361. doi: 10.1111/j.1365-4632.2006.03044.x.
    1. Serwin AB, Koper M, Flisiak I. Incidence of pemphigus vulgaris and pemphigus foliaceus in North-East Poland (Podlaskie Province): a 15-year (2001–2015) bicentric retrospective study. Int J Dermatol. 2018;57:933–937. doi: 10.1111/ijd.14078.
    1. Marazza G, Pham HC, Scharer L, Pedrazzetti PP, Hunziker T, Trueb RM, et al. Incidence of bullous pemphigoid and pemphigus in Switzerland: a 2-year prospective study. Br J Dermatol. 2009;161:861–868. doi: 10.1111/j.1365-2133.2009.09300.x.
    1. Langan SM, Smeeth L, Hubbard R, Fleming KM, Smith CJP, West J. Bullous pemphigoid and pemphigus vulgaris: incidence and mortality in the UK: population based cohort study. BMJ. 2008;337:a180. doi: 10.1136/bmj.a180.
    1. Kridin K, Sagi SZ, Bergman R. Mortality and cause of death in patients with pemphigus. Acta Derm Venereol. 2017;97:607–611. doi: 10.2340/00015555-2611.
    1. Huang Y-H, Kuo C-F, Chen Y-H, Yang Y-W. Incidence, mortality, and causes of death of patients with pemphigus in Taiwan: a nationwide population-based study. J Investig Dermatol. 2012;132:92–97. doi: 10.1038/jid.2011.249.
    1. Kridin K. Pemphigus group: overview, epidemiology, mortality, and comorbidities. Immunol Res. 2018;66:255–270. doi: 10.1007/s12026-018-8986-7.
    1. Kridin K, Zelber-Sagi S, Bergman R. Pemphigus vulgaris and pemphigus foliaceus: differences in epidemiology and mortality. Acta Derm Venereol. 2017;97:1095–1099. doi: 10.2340/00015555-2706.
    1. Hammers CM, Stanley JR. Mechanisms of disease: pemphigus and bullous pemphigoid. Annu Rev Pathol. 2016;11:175–197. doi: 10.1146/annurev-pathol-012615-044313.
    1. Vodo D, Sarig O, Sprecher E. The genetics of pemphigus vulgaris. Front Med (Lausanne). 2018;5:226. doi: 10.3389/fmed.2018.00226.
    1. Sinha AA. The genetics of pemphigus. Dermatol Clin. 2011;29(381–91):vii.
    1. Mahoney MG, Wang Z, Rothenberger K, Koch PJ, Amagai M, Stanley JR. Explanations for the clinical and microscopic localization of lesions in pemphigus foliaceus and vulgaris. J Clin Investig. 1999;103:461–468. doi: 10.1172/JCI5252.
    1. Hanakawa Y, Matsuyoshi N, Stanley JR. Expression of desmoglein 1 compensates for genetic loss of desmoglein 3 in keratinocyte adhesion. J Investig Dermatol. 2002;119:27–31. doi: 10.1046/j.1523-1747.2002.01780.x.
    1. Heupel W-M, Zillikens D, Drenckhahn D, Waschke J. Pemphigus vulgaris IgG directly inhibit desmoglein 3-mediated transinteraction. J Immunol. 2008;181:1825–1834. doi: 10.4049/jimmunol.181.3.1825.
    1. 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;167:5439–5448. doi: 10.4049/jimmunol.167.9.5439.
    1. Oktarina DAM, van der Wier G, Diercks GFH, Jonkman MF, Pas HH. IgG-induced clustering of desmogleins 1 and 3 in skin of patients with pemphigus fits with the desmoglein nonassembly depletion hypothesis. Br J Dermatol. 2011;165:552–562. doi: 10.1111/j.1365-2133.2011.10463.x.
    1. van der Wier G, Pas HH, Kramer D, Diercks GFH, Jonkman MF. Smaller desmosomes are seen in the skin of pemphigus patients with anti-desmoglein 1 antibodies but not in patients with anti-desmoglein 3 antibodies. J Investig Dermatol. 2014;134(8):2287–2290. doi: 10.1038/jid.2014.140.
    1. Aoyama Y, Kitajima Y. Pemphigus vulgaris-IgG causes a rapid depletion of desmoglein 3 (Dsg3) from the Triton X-100 soluble pools, leading to the formation of Dsg3-depleted desmosomes in a human squamous carcinoma cell line, DJM-1 cells. J Investig Dermatol. 1999;112:67–71. doi: 10.1046/j.1523-1747.1999.00463.x.
    1. Li X, Ishii N, Ohata C, Furumura M, Hashimoto T. Signalling pathways in pemphigus vulgaris. Exp Dermatol. 2014;23:155–156. doi: 10.1111/exd.12317.
    1. Saito M, Stahley SN, Caughman CY, Mao X, Tucker DK, Payne AS, et al. Signaling dependent and independent mechanisms in pemphigus vulgaris blister formation. PLoS One. 2012;7:e50696. doi: 10.1371/journal.pone.0050696.
    1. Grando SA. Pemphigus autoimmunity: hypotheses and realities. Autoimmunity. 2012;45:7–35. doi: 10.3109/08916934.2011.606444.
    1. Bystryn J-C, Grando SA. A novel explanation for acantholysis in pemphigus vulgaris: the basal cell shrinkage hypothesis. J Am Acad Dermatol. 2006;54:513–516. doi: 10.1016/j.jaad.2005.12.003.
    1. Rock B, Labib RS, Diaz LA. Monovalent Fab’ immunoglobulin fragments from endemic pemphigus foliaceus autoantibodies reproduce the human disease in neonatal Balb/c mice. J Clin Investig. 1990;85:296–299. doi: 10.1172/JCI114426.
    1. Yamagami J, Payne AS, Kacir S, Ishii K, Siegel DL, Stanley JR. Homologous regions of autoantibody heavy chain complementarity-determining region 3 (H-CDR3) in patients with pemphigus cause pathogenicity. J Clin Investig. 2010;120:4111–4117. doi: 10.1172/JCI44425.
    1. Laskaris G, Sklavounou A, Stratigos J. Bullous pemphigoid, cicatricial pemphigoid, and pemphigus vulgaris: a comparative clinical survey of 278 cases. Oral Surg Oral Med Oral Pathol. 1982;54:656–662. doi: 10.1016/0030-4220(82)90080-9.
    1. Ahmed AR, Blose DA. Pemphigus vegetans: Neumann type and Hallopeau type. Int J Dermatol. 1984;23:135–141. doi: 10.1111/j.1365-4362.1984.tb05688.x.
    1. Anhalt GJ, Kim SC, Stanley JR, Korman NJ, Jabs DA, Kory M, et al. Paraneoplastic pemphigus: an autoimmune mucocutaneous disease associated with neoplasia. N Engl J Med. 1990;323:1729–1735. doi: 10.1056/NEJM199012203232503.
    1. Amber KT, Valdebran M, Grando SA. Paraneoplastic autoimmune multiorgan syndrome (PAMS): beyond the single phenotype of paraneoplastic pemphigus. Autoimmun Rev. 2018;17:1002–1010. doi: 10.1016/j.autrev.2018.04.008.
    1. Ohzono A, Sogame R, Li X, Teye K, Tsuchisaka A, Numata S, et al. Clinical and immunological findings in 104 cases of paraneoplastic pemphigus. Br J Dermatol. 2015;173:1447–1452. doi: 10.1111/bjd.14162.
    1. Czernik A, Camilleri M, Pittelkow MR, Grando SA. Paraneoplastic autoimmune multiorgan syndrome: 20 years after. Int J Dermatol. 2011;50(8):905–914. doi: 10.1111/j.1365-4632.2011.04868.x.
    1. Nousari HC, Kimyai-Asadi A, Anhalt GJ. Elevated serum levels of interleukin-6 in paraneoplastic pemphigus. J Investig Dermatol. 1999;112(3):396–398. doi: 10.1046/j.1523-1747.1999.00520.x.
    1. Nguyen VT, Ndoye A, Bassler KD, Shultz LD, Shields MC, Ruben BS, et al. Classification, clinical manifestations, and immunopathological mechanisms of the epithelial variant of paraneoplastic autoimmune multiorgan syndrome: a reappraisal of paraneoplastic pemphigus. Arch Dermatol. 2001;137:193–206.
    1. Leger S, Picard D, Ingen-Housz-Oro S, Arnault JP, Aubin F, Carsuzaa F, et al. Prognostic factors of paraneoplastic pemphigus. Arch Dermatol. 2012;148:1165–1172. doi: 10.1001/archdermatol.2012.1830.
    1. Lee J, Bloom R, Amber KT. A systematic review of patients with mucocutaneous and respiratory complications in paraneoplastic autoimmune Mmltiorgan syndrome: Castleman’s disease is the predominant malignancy. Lung. 2015;193(4):593–596. doi: 10.1007/s00408-015-9732-8.
    1. Liu Q, Bu D-F, Li D, Zhu X-J. Genotyping of HLA-I and HLA-II alleles in Chinese patients with paraneoplastic pemphigus. Br J Dermatol. 2008;158:587–591. doi: 10.1111/j.1365-2133.2007.08361.x.
    1. Martel P, Loiseau P, Joly P, Busson M, Lepage V, Mouquet H, et al. Paraneoplastic pemphigus is associated with the DRB1*03 allele. J Autoimmun. 2003;20(1):91–95. doi: 10.1016/S0896-8411(02)00092-6.
    1. Zhu X, Zhang B. Paraneoplastic pemphigus. J Dermatol. 2007;34(8):503–511. doi: 10.1111/j.1346-8138.2007.00322.x.
    1. Reich K, Brinck U, Letschert M, Blaschke V, Dames K, Braess J, et al. Graft-versus-host disease-like immunophenotype and apoptotic keratinocyte death in paraneoplastic pemphigus. Br J Dermatol. 1999;141(4):739–746. doi: 10.1046/j.1365-2133.1999.03123.x.
    1. Wang L, Bu D, Yang Y, Chen X, Zhu X. Mechanisms of disease Castleman’s tumours and production of autoantibody in paraneoplastic pemphigus. Lancet. 2004;363(9408):525–531. doi: 10.1016/S0140-6736(04)15539-6.
    1. Vezzoli P, Berti E, Marzano AV. Rationale and efficacy for the use of rituximab in paraneoplastic pemphigus. Expert Rev Clin Immunol. 2008;4(3):351–363. doi: 10.1586/1744666X.4.3.351.
    1. Tsuchisaka A, Numata S, Teye K, Natsuaki Y, Kawakami T, Takeda Y, et al. Epiplakin is a paraneoplastic pemphigus autoantigen and related to bronchiolitis obliterans in Japanese patients. J Investig Dermatol. 2016;136(2):399–408. doi: 10.1038/JID.2015.408.
    1. Poot AM, Diercks GFH, Kramer D, Schepens I, Klunder G, Hashimoto T, et al. Laboratory diagnosis of paraneoplastic pemphigus. Br J Dermatol. 2013;169:1016–1024. doi: 10.1111/bjd.12479.
    1. Numata S, Teye K, Tsuruta D, Sogame R, Ishii N, Koga H, et al. Anti-alpha-2-macroglobulin-like-1 autoantibodies are detected frequently and may be pathogenic in paraneoplastic pemphigus. J Investig Dermatol. 2013;133:1785–1793. doi: 10.1038/jid.2013.65.
    1. Lambert J, Bracke S, Van Roy F, Pas HH, Bonné S, De Schepper S. Serum plakophilin-3 autoreactivity in paraneoplastic pemphigus. Br J Dermatol. 2010;163:630–632. doi: 10.1111/j.1365-2133.2010.09845.x.
    1. Wang R, Li J, Wang M, Hao H, Chen X, Li R, et al. Prevalence of myasthenia gravis and associated autoantibodies in paraneoplastic pemphigus and their correlations with symptoms and prognosis. Br J Dermatol. 2015;172:968–975. doi: 10.1111/bjd.13525.
    1. Futei Y, Amagai M, Hashimoto T, Nishikawa T. Conformational epitope mapping and IgG subclass distribution of desmoglein 3 in paraneoplastic pemphigus. J Am Acad Dermatol. 2003;49(6):1023–1028. doi: 10.1016/S0190-9622(03)02160-1.
    1. Silva JA, de Mesquita KC, Igreja AC, Lucas IC, Freitas AF, Oliveira SM, et al. Paraneoplastic cutaneous manifestations: concepts and updates. An Bras Dermatol. 2013;88(1):9–22. doi: 10.1590/S0365-05962013000100001.
    1. Broussard KC, Leung TG, Moradi A, Thorne JE, Fine J. Autoimmune bullous diseases with skin and eye involvement: cicatricial pemphigoid, pemphigus vulgaris, and pemphigus paraneoplastica. Clin Dermatol. 2016;34:205–213. doi: 10.1016/j.clindermatol.2015.11.006.
    1. Sehgal VN, Srivastava G. Paraneoplastic pemphigus/paraneoplastic autoimmune multiorgan syndrome. Int J Dermatol. 2009;48(2):162–169. doi: 10.1111/j.1365-4632.2009.03995.x.
    1. Nguyen VT, Ndoye A, Basseler KD, Shultz LD, Shields MC, Ruben BS, et al. Classification, clinical manifestations, and immunopathological mechanisms of the epithelial variant of paraneoplastic autoimmune multiorgan syndrome: a reappraisal of paraneoplastic pemphigus. Arch Dermatol. 2001;137(2):193–206.
    1. Hashimoto T, Ohzono A, Ishii N. “Reply to: clinical and immunological findings in 104 cases of paraneoplastic pemphigus”: reply from the authors. Br J Dermatol. 2016;174:461–462. doi: 10.1111/bjd.14381.
    1. Siu A, Landon K, Ramos DM. Differential diagnosis and management of oral ulcers. Semin Cutan Med Surg. 2015;34:171–177. doi: 10.12788/j.sder.2015.0170.
    1. Kardaun SH, Jonkman MF. Stevens-Johnson syndrome/toxic epidermal necrolysis and erythema exsudativum multiforme. Autoimmune bullous diseases. London: Springer; 2016. pp. 183–193.
    1. Nikolskiy P. Trois nouveaux cas de pemphigus foliacé étudiés au point de vue de la symptomatologie. Ann Derm Syph. 1898;13:1026–1031.
    1. van Gijn J, Gijselhart JP. Nikolsky and his sign. Ned Tijdschr Geneeskd. 2011;155:A2846.
    1. Uzun S, Durdu M. The specificity and sensitivity of Nikolskiy sign in the diagnosis of pemphigus. J Am Acad Dermatol. 2006;54:411–415. doi: 10.1016/j.jaad.2005.10.019.
    1. Mignogna MD, Fortuna G, Leuci S, Ruoppo E, Marasca F, Matarasso S. Nikolsky’s sign on the gingival mucosa: a clinical tool for oral health practitioners. J Periodontol. 2008;79:2241–2246. doi: 10.1902/jop.2008.080217.
    1. Fortuna G, Marinkovich MP. Linear immunoglobulin A bullous dermatosis. Clin Dermatol. 2012;30:38–50. doi: 10.1016/j.clindermatol.2011.03.008.
    1. Rose C, Weyers W, Denisjuk N, Hillen U, Zillikens D, Shimanovich I. Histopathology of anti-p200 pemphigoid. Am J Dermatopathol. 2007;29:119–124. doi: 10.1097/DAD.0b013e31803326e6.
    1. Hrabovska Z, Jautova J, Hrabovsky V. A study of clinical, histopathological and direct immunofluorescence diagnosis in pemphigus group: utility of direct immunofluorescence. Bratisl Lek Listy. 2017;118:243–249.
    1. Horn TD, Anhalt GJ. Histologic features of paraneoplastic pemphigus. Arch Dermatol. 1992;128(8):1091–1095. doi: 10.1001/archderm.1992.01680180085011.
    1. Jordon RE, Beutner EH, Witebsky E, Blumental G, Hale WL, Lever WF. Basement zone antibodies in bullous pemphigoid. JAMA. 1967;200:751–756. doi: 10.1001/jama.1967.03120220053008.
    1. Giurdanella F, Diercks GFH, Jonkman MF, Pas HH. Laboratory diagnosis of pemphigus: direct immunofluorescence remains the gold standard. Br J Dermatol. 2016;175(1):185–186. doi: 10.1111/bjd.14408.
    1. Meijer JM, Diercks GFH, de Lang EWG, Pas HH, Jonkman MF. Assessment of diagnostic strategy for early recognition of bullous and nonbullous variants of pemphigoid. JAMA Dermatol. 2019 doi: 10.1001/jamadermatol.2018.4390.
    1. Diercks GF, Pas HH, Jonkman MF. Immunofluorescence of autoimmune bullous diseases. Surg Pathol Clin. 2017;10(2):505–512. doi: 10.1016/j.path.2017.01.011.
    1. Jonkman MF, Diercks GFH. How to take a biopsy. Autoimmune bullous diseases. London: Springer; 2016. pp. 33–37.
    1. Kamaguchi M, Iwata H, Ujiie I, Ujiie H, Sato J, Kitagawa Y, et al. Direct immunofluorescence using non-lesional buccal mucosa in mucous membrane pemphigoid. Front Med (Lausanne). 2018;5:20. doi: 10.3389/fmed.2018.00020.
    1. Carey B, Joshi S, Abdelghani A, Mee J, Andiappan M, Setterfield J. The optimal oral biopsy site for diagnosis of mucous membrane pemphigoid and pemphigus vulgaris. Br J Dermatol. 2019 doi: 10.1111/bjd.18032.
    1. Vodegel RM, de Jong MCJM, Meijer HJ, Weytingh MB, Pas HH, Jonkman MF. Enhanced diagnostic immunofluorescence using biopsies transported in saline. BMC Dermatol. 2004;4:10. doi: 10.1186/1471-5945-4-10.
    1. Meijer JM, Atefi I, Diercks GFH, Vorobyev A, Zuiderveen J, Meijer HJ, et al. Serration pattern analysis for differentiating epidermolysis bullosa acquisita from other pemphigoid diseases. J Am Acad Dermatol. 2018;78(754–9):e6.
    1. Thorne JE, Anhalt GJ, Jabs DA. Mucous membrane pemphigoid and pseudopemphigoid. Ophthalmology. 2004;111:45–52. doi: 10.1016/j.ophtha.2003.03.001.
    1. Shimanovich I, Nitz JM, Zillikens D. Multiple and repeated sampling increases the sensitivity of direct immunofluorescence testing for the diagnosis of mucous membrane pemphigoid. J Am Acad Dermatol. 2017;77(700–5):e3.
    1. Bean SF. Cicatricial pemphigoid: immunofluorescent studies. Arch Dermatol. 1974;110:552–555. doi: 10.1001/archderm.1974.01630100012002.
    1. Rogers RS, Perry HO, Bean SF, Jordon RE. Immunopathology of cicatricial pemphigoid: studies of complement deposition. J Investig Dermatol. 1977;68:39–43. doi: 10.1111/1523-1747.ep12485162.
    1. Rogers RS, Van Hale HM. Immunopathologic diagnosis of oral mucosal inflammatory diseases. Australas J Dermatol. 1986;27:51–57. doi: 10.1111/j.1440-0960.1986.tb00288.x.
    1. Terra JB, Jonkman MF, Diercks GFH, Pas HH. Low sensitivity of type VII collagen enzyme-linked immunosorbent assay in epidermolysis bullosa acquisita: serration pattern analysis on skin biopsy is required for diagnosis. Br J Dermatol. 2013;169:164–167. doi: 10.1111/bjd.12300.
    1. Vodegel RM, De Jong MCJM, Pas HH, Jonkman MF. IgA-mediated epidermolysis bullosa acquisita: two cases and review of the literature. J Am Acad Dermatol. 2002;47:919–925. doi: 10.1067/mjd.2002.125079.
    1. Joly P, Richard C, Gilbert D, Chosidow O, Roujeau JC, et al. Sensitivity and specificity of clinical, histologic, and immunologic features in the diagnosis of paraneoplastic pemphigus. J Am Acad Dermatol. 2000;43(4):619–626. doi: 10.1067/mjd.2000.107488.
    1. Poot AM, Siland J, Jonkman MF, Pas HH, Diercks GFH. Direct and indirect immunofluorescence staining patterns in the diagnosis of paraneoplastic pemphigus. Br J Dermatol. 2016;174:912–915. doi: 10.1111/bjd.14282.
    1. Feibelman C, Stolzner G, Provost TT. Pemphigus vulgaris: superior sensitivity of monkey esophagus in the determination of pemphigus antibody. Arch Dermatol. 1981;117:561–562. doi: 10.1001/archderm.1981.01650090043023.
    1. Pas H. Immunoassays. In: Jonkman M, editor. Autoimmune bullous diseases. London: Springer; 2016. pp. 57–62.
    1. Pas HH. Immunoblot assay in differential diagnosis of autoimmune blistering skin diseases. Clin Dermatol. 2001;19:622–630. doi: 10.1016/S0738-081X(00)00176-0.
    1. Izumi K, Nishie W, Mai Y, Ujiie H, Iwata H, Natsuga K, et al. Detection of mucous membrane pemphigoid autoantibodies by full-length BP180 enzyme-linked immunosorbent assay. J Dermatol Sci. 2017;88:247–248. doi: 10.1016/j.jdermsci.2017.07.005.
    1. Charneux J, Lorin J, Vitry F, Antonicelli F, Reguiai Z, Barbe C, et al. Usefulness of BP230 and BP180-NC16a enzyme-linked immunosorbent assays in the initial diagnosis of bullous pemphigoid: a retrospective study of 138 patients. Arch Dermatol. 2011;147:286–291. doi: 10.1001/archdermatol.2011.23.
    1. Schmidt E, Dahnrich C, Rosemann A, Probst C, Komorowski L, Saschenbrecker S, et al. Novel ELISA systems for antibodies to desmoglein 1 and 3: correlation of disease activity with serum autoantibody levels in individual pemphigus patients. Exp Dermatol. 2010;19:458–463. doi: 10.1111/j.1600-0625.2010.01069.x.
    1. Abasq C, Mouquet H, Gilbert D, Tron F, Grassi V, Musette P, et al. ELISA testing of anti-desmoglein 1 and 3 antibodies in the management of pemphigus. Arch Dermatol. 2009;145:529–535. doi: 10.1001/archdermatol.2009.9.
    1. Ishii K, Harada R, Matsuo I, Shirakata Y, Hashimoto K, Amagai M. In vitro keratinocyte dissociation assay for evaluation of the pathogenicity of anti-desmoglein 3 IgG autoantibodies in pemphigus vulgaris. J Investig Dermatol. 2005;124:939–946. doi: 10.1111/j.0022-202X.2005.23714.x.

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