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 �3�#�#�#�#���$������������������Pharyngolaryngeal manifestation of pemphigus vulgaris

Masafumi Ohki, MD; Shigeru Kikuchi, MD, PhD

Department of Otolaryngology, Saitama Medical Center, Saitama Medical University, 1981 Kamoda, Kawagoe-shi, Saitama 350-8550, Japan

Corresponding author: Masafumi Ohki
Department of Otolaryngology, Saitama Medical Center, Saitama Medical University, 1981 Kamoda, Kawagoe-shi, Saitama 350-8550, Japan
E-mail: m-ohki@umin.ac.jp
Tel: +81-49-228-3685
Fax: +81-49-225-6312

Financial Disclosure: None, Conflict of Interest: None



Abstract
Background: Pemphigus vulgaris is an autoimmune blister disorder targeting the skin and mucous membrane. Its initial symptoms are often intractable oral or pharyngolaryngeal lesions; therefore, patients usually consult an otorhinolaryngologist or physician first before consulting a dermatologist.
Objective: We aimed to investigate the clinical features of mucous membrane lesions in the oral and pharyngolaryngeal regions of patients with pemphigus vulgaris.
Methods: A retrospective chart review of the symptoms, lesion sites, features of lesions, and treatment was performed for patients with pemphigus vulgaris diagnosed between 2001 and 2012.
Results: Eight consecutive patients with pemphigus vulgaris who consulted an otorhinolaryngologist were enrolled in this study, only 3 of whom presented with eroded or eruptive skin lesions. Their mucous symptoms were sore throat, oral pain, odynophagia, hoarseness, and gingival bleeding. The mucous lesions were located in the palate, gingiva, tongue, epiglottis, pharynx, vocal cord, and nasal cavity and usually featured erosion, erosion with white coating, and erythematous patches. The patients were treated with systemic and/or topical steroid administration. Seven patients were treated with oral prednisolone (10�60 mg) administration. After the lesions were controlled, the prednisolone dose was tapered to lower than 0.2mg/kg. Some patients were given topical steroids in the form of nasal sprays or inhalants. The erosive nasal or vocal cord lesions improved thereafter.
Conclusion: Pemphigus vulgaris involves both the oral cavity and the pharyngolaryngeal and nasal cavities. Therefore, a patient with pemphigus vulgaris should undergo pharyngolaryngeal optic fiberscopic examination.

Key words: pemphigus vulgaris, desmoglein 1, desmoglein 3, autoimmune blistering disease, pharyngolaryngeal, nasal
Introduction
Pemphigus vulgaris is one of the various disorders that cause intractable oral or pharyngolaryngeal lesions. Pemphigus vulgaris is an autoimmune blister disorder that targets the skin and mucous membrane. Desmosomes form the adhesive core of intercellular junctions, which are made up of desmosomal cadherins, desmogleins (Dsgs), and desmocollins. When desmosomes are impaired by autoantibodies, the keratinocytes in the epidermis become dissociated. The currently known target antigens are Dsg1, Dsg3, and plakin protein, which act as adhesion molecules between keratinocytes in the epidermis [1-3]. Pemphigus diseases are classified into pemphigus vulgaris, pemphigus foliaceus, paraneoplastic pemphigus, pemphigus vegetans, pemphigus erythematosus, herpetiform pemphigus, or drug-induced pemphigus [1, 2, 4]. Pemphigus vulgaris is subclassified into mucosal-dominant pemphigus vulgaris and mucocutaneous-dominant pemphigus vulgaris [1, 5]. The mucosal-dominant type shows predominant oral erosions with limited 5 or 6 scattered skin lesions or isolated erosion or blisters not >5 cm in diameter [5]. The mucocutaneous-dominant type demonstrates extensive skin lesions in addition to oral lesions [5]. Serological examination was performed using sera samples from patients with mucosal-dominant pemphigus vulgaris, which usually tests negative for Dsg1 but positive for Dsg3. On the contrary, the mucocutaneous-dominant type usually tests positive for Dsg 1 and 3. Pemphigus vulgaris is generally treated by a dermatologist; however, because its initial symptoms are often oral lesions, patients usually consult an otorhinolaryngologist or physician first. From the standpoint of otorhinolaryngology, it is important to know the clinical characteristics of pemphigus vulgaris. Therefore, in the present study, we investigated the clinical features of mucous membrane lesions in the oral and pharyngolaryngeal regions of patients with pemphigus vulgaris.

Materials and Methods
This study involved 8 consecutive outpatients with pemphigus vulgaris who presented with pharyngolaryngeal lesions between 2001 and 2012. The clinical records of the patients were reviewed. These were especially focusing on the nasal, laryngeal, pharyngeal, and esopharyngeal involvement in pemphigus vulgaris. These areas were examined using an optic fiberscope in all patients. Tissue samples obtained by biopsy were examined by routine histological examination, including hematoxylin-eosin staining and direct immunofluorescence examination. Pemphigus vulgaris was clinically, histologically, and immunopathologically diagnosed in all the patients by their dermatologist. The sites and features of the lesions on the pharyngolarynx are shown. Laboratory data were expressed as mean � standard error values. This study was approved by the local ethics committee and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. Informed consent was obtained from all the patients.

Results
Clinical data
The 8 patients included 5 men and 3 women. Six patients had mucosal-dominant pemphigus vulgaris, whereas 2 patients had mucocutaneous-dominant pemphigus vulgaris. The patients enrolled in the study were aged 28�91 years (mean age, 59.8 years) at the time of diagnosis. The duration of symptoms was from 1 to 6 months (mean, 2.4 months; median, 1 month). Only 3 of the 8 patients presented with skin lesions either on the trunk (1/8, 13%), back (1/8, 13%), or upper and lower limbs (1/8, 13%). The skin lesions appeared erosive or eruptive. The symptoms at presentation were sore throat (5/8, 63%), oral pain (3/8, 38%), odynophagia (3/8, 38%), gingival bleeding (1/8, 13%), and rash (1/8, 13%). The sites of the membranous lesions were the oral cavity (8/8, 100%), palate (7/8, 88%), gingiva (4/8, 50%), tongue (1/8, 13%), epiglottis (4/8, 50%), pharynx (2/8, 25%), vocal cord (3/8, 38%), and nasal cavity (4/8, 50%) (Fig. 1). The membranous lesions usually featured erosion, erosion with white coating, and erythematous patches. The mucous membrane lesions were observed before the skin lesions appeared in 2 patients and after the skin lesions appeared in 1 patient. The other 5 patients showed no skin lesion.

Laboratory data
	The white blood cell counts were usually within the reference range, ranging from 4300 to 13200 cells/�L (7638 � 922 cells/�L). The C-reactive protein levels were 0.04 0.31 mg/dL (0.14 � 0.03 mg/dL). The serum levels of the diagnostic autoantibodies, Dsg1 or Dsg2, were measured (cutoff indices: Dsg1, 13 index; Dsg3, 6 index). The Dsg1 levels were elevated in 3 of the 8 patients (38%), whereas the Dsg3 levels were elevated in all the 8 patients (100%). Four patients with mucosal-dominant pemphigus vulgaris showed elevated Dsg3 levels alone, whereas 2 patients had elevated Dsg1 and Dsg3 levels. Of the patients with mucocutaneous-dominant pemphigus vulgaris, 1 showed elevated Dsg1 and Dsg3 levels and another showed an elevated Dsg3 level.

Histopathological findings
The histopathological findings revealed a suprabasilar slit over the intact basal layer with acantholytic cells in all the patients (Fig. 2a). The results of the direct immunofluorescence or immunohistochemical microscopic studies indicated positive deposition of immunoglobulin G (IgG) and/or C3 in the epidermal intracellular space in all the patients (Fig. 2b).

Treatments
	The patients were treated with systemic and/or topical steroid administration. Seven patients were treated with oral prednisolone (10�60 mg) administration. After the lesion was controlled, the prednisolone dose was tapered to lower than 0.2mg/kg. In 1 patient with nasal lesions, topical steroid or nasal spray containing mometasone furoate hydrate was administrated at 200 �g/day, but no systemic steroid was administered. The erosive nasal lesions disappeared thereafter. For the laryngeal lesions, we administered a fluticasone propionate inhalant at 200 �g/day, which improved the vocal cord lesions. In another patient with oral lesions alone, a topical steroid ointment containing dexamethasone controlled the oral lesions.

Discussion
The difference between mucosal- and mucocutaneous-dominant pemphigus vulgaris is defined by their phenotypes [5]. Typically, the target antigen of mucosal-dominant pemphigus vulgaris is Dsg3, whereas those of mucocutaneous-dominant pemphigus vulgaris are Dsg1 and Dsg3 [1]. Dsg1 and Dsg3 are distributed throughout the skin and mucosae but differ in distribution pattern [6, 7]. In the skin, Dsg1 is observed mainly in the upper layer of the epidermis, whereas Dsg3 is observed in the basal and parabasal cell layers. In the mucosae, Dsg1 and Dsg3 are distributed in all the layers, but the expression of Dsg3 is higher than that of Dsg1. Dsg1 and Dsg3 compensate the impaired adhesive function of the other. However, when expression in the tissue is reduced, neither is able to sufficiently compensate for the other and practical impairment of the tissue occurs [1]. However, in many cases in our study, the subtypes of the phenotypes were mismatched. Clinically, the subclasses differentiated by the target antigens (i.e., Dsg1 and Dsg3) are not always identical to practical phenotypes. Mucosal-dominant pemphigus vulgaris sometimes shows slight skin lesions, and mucocutaneous-dominant pemphigus vulgaris does not always show skin lesions. In the long term, skin lesions usually appear in many cases [3].
Because the epidermis detaches at the basal and prickle cell layers, the mucosal lesion usually appears erosive and covered with a white coating. When the white coating peels off, the mucosal lesion becomes eroded with or without bleeding. The sites of mucosal lesion are the oral cavity, pharynx, larynx, esophagus, nasal cavity, ear, vagina, and conjunctivae [1, 6-9]. The lesions in the oral cavity are usually observed in the buccal mucosae, palate, tongue, lips, gingivae, and floor of the mouth. The most frequent site is the oral cavity, and approximately half of the initial symptoms are related to oral lesions [3]. During the course of the disease, oral symptoms appear at the rate of almost 100% [6]. The symptoms are dependent on the impaired sites and mostly vary in presentation, such as oral pain, stinging, sore throat, pain on swallowing, hoarseness, dysphonia, dysphagia, odynophagia, epistaxis, stuffiness, blood-tinged mucus, earache, ear canal obstruction, vaginal discharge and pain, ocular pain, and excessive tearing [1, 6-9].
Even if lesions appear, the patient may be asymptomatic. In patients with only mucosal lesions without skin lesion, the diagnosis is often delayed or overlooked. Optical laryngeal fiberscopy or upper gastrointestinal endoscopy results often reveal pharyngolaryngeal or esopharyngeal lesions. Otorhinolaryngologists and gastroenterologists, who perform these examinations, must be aware of the features of the mucosal lesions in pemphigus vulgaris. However, these mucosal features (i.e., erosion with or without white coating) are not unique to pemphigus vulgaris. These are similar to the mucosal lesions of pemphigoid; therefore, it is impossible to make a diagnosis based only on the appearance of the mucosae. Therefore, diagnostic pathological and serological examinations are required. Occasionally, it is difficult to discriminate pemphigus vulgaris from the common pharyngolaryngitis at an acute stage. White blood cell counts and C-reactive protein levels are usually within the reference range in pemphigus vulgaris. These routine blood tests are probably useful, unless the patient�s condition is complicated by other infections.
The first-line treatment is steroid administration (prednisolone, 0.5�1.0 mg/kg daily). For skin lesions, an antibiotic or steroid ointment is used in combination with oral steroid administration. For mucosal lesions, a steroid ointment or nasal spray may be effective. We administered fluticasone propionate as an inhalant at 200 �g/day for the laryngeal lesions and mometasone furoate hydrate nasal spray at 200 �g/day for the nasal lesions. Good control of the lesions was demonstrated in all our patients. Therefore, these topical steroids may be effective, safe, and useful for nasal and pharyngolaryngeal lesions. With regard to other combination therapies, immunosuppressive therapy, plasma pheresis, and intravenous gamma globulin are sometimes performed [1]. After the disease is controlled, the daily prednisolone dose should be gradually tapered to lower than 0.2 mg/kg. The activity of the disease was associated with antibody titers of Dsg1 and Dsg3 [10]. Hence, monitoring of Dsg1 and Dsg3 levels is useful to determine disease activity and modulate the steroid dose.

Conclusion
Pemphigus vulgaris most frequently involves the oral cavity, followed by the epiglottis and nasal cavity. The lesions appear erosive, with or without white exudative coating. Pharyngolaryngeal optic fiberscopic examination is important in making a definitive diagnosis.

Acknowledgment: None

Reference
Amagai M (2010) Autoimmune and infectious skin diseases that target desmogleins. Proc Jpn Acad Ser B Phys Biol Sci 86:524-537.
Koulu L, Kusumi A, Steinberg MS, Klaus-Kovtun V, Stanley JR (1983) Human autoantibodies against a desmosomal core protein in pemphigus foliaceus. J Exp Med 160: 1509-1518.
Amagai M, Klaus-Kovtun V, Stanley JR (1991) Autoantibodies against a novel epithelial cadherin in pemphigus vulgaris, a disease of cell adhesion. Cell 67:869-877.
Amagai M, Hashimoto T, Green KJ, Shimizu N, Nishikawa T (1995) Antigen-specific immunoadsorption of pathogenic autoantibodies in pemphigus foliaceus. J Invest Dermatol 104: 895-901.
Amagai M, Tsunoda K, Zillikens D, Nagai T, Nishikawa T (1999) The clinical phenotype of pemphigus is defined by the anti-desmoglein autoantibody profile. J Am Acad Dermatol 40:167-170.
Su O, Onsun N, Meric Teker A, Cinkaya A, Yasemin Korkut A, et al (2010) Upper airway tract and upper gastrointestinal tract involvement in patients with pemphigus vulgaris. Eur J Dermatol 20:792-796.
Espana A, Fernandez S, del Olmo J, Marquina M, Pretel M, et al (2007) Ear, nose, and throat manifestations in pemphigus vulgaris. Br J Dermatol 156:733-737.
Kavala M, Altintas S, Kocaturk E, Zindanci I, Can B, Ruhi C (2011) Ear, nose and throat involvement in patients with pemphigus vulgaris: correlation with severity, phenotype and disease activity. J Eur Acad Dermatol Venereol 25:1324-1327.
Zagorodniuk I, Weltfriend S, Shtruminger L, Sprecher E, Kogan O, et al (2005) A comparison of anti-desmoglein antibodies and indirect immunofluorescence in the serodiagnosis of pemphigus vulgaris. Int J Dermatol 44: 541-544.
 HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed?term=Cheng%20SW%5BAuthor%5D&cauthor=true&cauthor_uid=12174096" Cheng SW,  HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed?term=Kobayashi%20M%5BAuthor%5D&cauthor=true&cauthor_uid=12174096" Kobayashi M, Kinoshita-Kuroda K,  HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed?term=Tanikawa%20A%5BAuthor%5D&cauthor=true&cauthor_uid=12174096" Tanikawa A, Amagai M, et al (2002) Monitoring disease activity in pemphigus with enzyme-linked immunosorbent assay using recombinant desmoglein 1 and 3. Br J Dermatol 147: 261-265.













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Clinical findings in pemphigus vulgaris: (a) erosive epiglottis with white coating (arrow), (b) erosion with white coating (arrow) on the palatoglossal arch, (c) erosion with a white fibrinous exudative lesion (arrow) on the arytenoid, and (d) erosion with white coating (arrow) on the uvula.

Fig. 2
Pathological findings. (a) Histopathological feature of a skin lesion biopsy sample showing a suprabasilar slit over the intact basal layer with acantholytic cells (hematoxylin-eosin staining; bar, 100 �m). (b) Direct immunofluorescence staining pattern demonstrating C3 deposition in the epidermal intracellular space. The bar indicates 100 �m.
PAGE   \* MERGEFORMAT2




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