Clinics in Dermatology (2012) 30, 1733

Autoimmune bullous diseases associations

Suzana Ljubojevic, MD, PhD , Jasna Lipozeni, MD, PhD
University Department of Dermatology and Venereology, University Hospital Center Zagreb, School of Medicine, University of Zagreb, Salata 4, 10000 Zagreb, Croatia

Abstract The presence of one autoimmune disorder helps lead to the discovery of other autoimmune conditions. It is thought that diseases in which autoimmunity is a feature tend to be associated together more often than one can ascribe to chance. A variety of diseases have been implicated in the onset of intraepidermal and subepidermal autoimmune diseases. The presence of one autoimmune disease should alert the physician to watch for a second immunologic disorder. A list of autoimmune bullous diseases associations includes autoimmune bullous diseases, pemphigus, pemphigoid, epidermolysis bullosa acquisita, dermatitis herpetiformis (Duhring), linear immunoglobulin A disease, and multiple autoimmune syndrome. 2012 Elsevier Inc. All rights reserved.

Introduction
The immunobullous diseases are characterized by pathogenic autoantibodies directed at target antigens whose function is cell-to-cell adhesion with the epidermis or adhesion of stratified squamous epithelium to dermis mesenchyme.1 Disorders of autoimmune pathogenesis occur with increased frequency in patients with a history of another autoimmune disease. The tendency to develop another disease occurs in about 25% of these patients.2 Overlapping sometimes occurs, but commonly, it is time that allows one syndrome to take on the features of another. The cutaneous autoimmune disorders can be divided into two categories: organ-specific and organ-nonspecific disorders.3 Organ-specific disorders, such as pemphigus vulgaris and bullous pemphigoid (BP), are characterized by autoimmune injury that is confined to the skin and mucosa. Organnonspecific disorders, such as systemic lupus erythematosus (SLE), are those where the immunologic injury occurs in skin
Corresponding author. Tel.: +385 1 4920 014. E-mail address: suzana.ljubojevic@zg.t-com.hr (S. Ljubojevic). 0738-081X/$ see front matter 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.clindermatol.2011.03.006

and also in internal organs.3,4 A list of intraepidermal and subepidermal autoimmune bullous disease associations and a detailed literature review is presented and summarized in Tables 1 and 2.

Pemphigus vulgaris
Pemphigus vulgaris occurs in patients with other disorders characterized by immunologic disturbances. Thymoma or myasthenia gravis (MG) have been reported in a number of patients with pemphigus vulgaris.5-18 MG is an autoimmune disease resulting from the production of antibodies against the acetylcholine receptors of the neuromuscular junction. It is frequently associated with morphologic abnormalities of the thymus. Thymoma is the most common primary mediastinal neoplasm and is known to give rise to autoimmune disorders. Approximately 40% of thymoma patients have parathymic syndromes, including MG and other autoimmune diseases.19 Abnormalities of the thymus may precede or follow the onset of pemphigus. Thymic abnormalities include benign or

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Table 1 The intraepidermal immunobullous disease associations Disease Pemphigus vulgaris Disease associations Alopecia areata Bullous pemphigoid Chronic lymphocytic leukemia Darier disease HIV Lichen planus Lupus erythematosus systemicus Myasthenia gravis Paget's disease of the nipple Pemphigus foliaceus Psoriasis vulgaris Thymoma Vitiligo Colonic cancer Gastric cancer HIV Lung cancer Lymphosarcoma Bullous pemphigoid Grave disease HIV IgA nephropathy Lupus erythematosus systemicus Myasthenia gravis Mycosis fungoides Oral lichen planus Psoriasis vulgaris Thymoma Acute polyarthritis B-cell lymphoma Crohn disease/ulcerative colitis Gluten sensitive enteropathy HIV IgA monoclonal gammopathy Lung cancer Myeloma Rheumatoid arthritis Sjgren's syndrome HIV Lung and prostate cancer Lupus erythematosus systemicus Psoriasis vulgaris Bronchiolitis obliterans Bullous pemphigoid Castleman tumor Chronic lymphocytic leukemia Gastrointestinal stromal tumor Lupus erythematosus systemicus Melanoma Myasthenia gravis Non-Hodgkin lymphoma Table 1 (continued) Disease

S. Ljubojevic, J. Lipozeni

Disease associations Pancreas carcinoma Polymyositis Renal carcinoma Sarcoma Thymoma Toxic epidermal necrolysis Uterine carcinoma Waldenstrm's macroglobulinemia

Pemphigus vegetans

Pemphigus foliaceus/ erythematosus

Intercellular IgA dermatosis (IgA pemphigus)

Pemphigus herpetiformis

Paraneoplastic pemphigus

malignant thymoma and thymic hyperplasia, and some patients can have all three diseases.16-18 Besides pemphigus vulgaris, MG and thymoma can also be associated with pemphigus foliaceus or pemphigus erythematosus.20-24 Pemphigus vulgaris may develop in patients with SLE,25-29 an autoimmune disease of unknown origin that may affect many parts of the body. Cutaneous manifestations are frequent and occasionally bullous or blistering lesions appear, such as bullous SLE (BSLE).25 In one of these patients, pemphigus vulgaris developed before SLE, and in another, SLE was presented before pemphigus vulgaris25-29; therefore, it seems that the order in which these conditions appear is not a conclusive factor in this association, nor that this association modifies the prognosis of these conditions or produces worsening of the SLE activity.25 BP and pemphigus vulgaris have coexisted,30-32 and the presence of two autoimmune diseases or a dual diagnosis should be considered in BP patients who are nonresponsive to conventional therapy. One patient was described with pemphigus foliaceus in whom pemphigus vulgaris subsequently developed.33 The transition of pemphigus vulgaris into pemphigus foliaceus is rare, and the immunologic changes underlying this event are not well understood.34-36 Autoimmune-mediated disorders tend to speed up human immunodeficiency virus (HIV) disease progression.37 Pemphigus vulgaris has been reported to be associated with HIV.37-41 The frequency and spectrum of mucocutaneous manifestation associated with HIV infection increases with clinical and immunologic deterioration.38 Treatment of pemphigus vulgaris with immunosuppressive drugs may cause HIV disease progression. Viral infections, in particular herpes virus infections, have been identified as a possible triggering factor for pemphigus.1,42-44 Viral DNA for herpes simplex, Epstein-Barr virus, and human herpes viruses 6 and 8 has been detected in some skin biopsy specimens or in peripheral blood mononuclear cells from pemphigus patients1,42-44; however, the inability to detect herpes virus DNA consistently suggests that viral infection may only be an occasional factor triggering the outbreak or exacerbation of the disease.44 An epidemiologic review suggested a positive correlation with pesticide exposure but a possibly protective effect from

Autoimmune bullous diseases associations

Table 2 The subepidermal immunobullous disease associations Disease Bullous pemphigoid Disease associations Alopecia Amyotrophic lateral sclerosis Acquired hemophilia Acquired thrombocytopenia Autoimmune neutropenia Autoimmune thrombocytopenia Castleman disease Dementia Dermatitis herpetiformis (Duhring) Dermatomyositis/polymyositis Diabetes mellitus Epilepsy Glomerulonephritis Grave diseases Hashimoto disease HIV Immune-complex glomerulonephritis Kaposi sarcoma Lichen planus Linear IgA dermatosis Malignances Multiple sclerosis Myasthenia gravis Nephropathia Parkinson disease Pemphigus foliaceus Pemphigus vulgaris Pernicious anemia Primary biliary cirrhosis Psoriasis Rheumatoid arthritis Shy-Dragger syndrome Thymoma Ulcerative colitis Vitiligo Autoimmune thrombocytopenia Choriocarcinoma Grave disease Hashimoto thyroiditis Hydatiform mole Pernicious anemia Trophoblastic tumors Vitiligo Amyloidosis Chron disease Chronic lymphocytic leukemia Diabetes Hashimoto thyroiditis IgM macroglobulinemia Linear IgA disease Lupus erythematosus systemicus Multiple endocrinopathy syndrome carcinoma Multiple myeloma Psoriasis Table 2 (continued) Disease Disease associations Pulmonary fibrosis Rheumatoid arthritis Thymoma Ulcerative colitis Addison disease Alopecia areata Ataxia Atrophic gastritis Bullous pemphigoid Cutaneous leiomyoma Dementia Diabetes Epilepsy Gluten sensitive enteropathy (Celiac disease) Hashimoto thyroiditis Hemodialysis IgA nephropathy Lichen planopilaris Lupus erythematosus systemicus Lymphoma (gastric and non-Hodgkin) Nephrotic syndrome Pernicious anemia Polycystic kidney disease Polymyositis/dermatomyositis Primary biliary cirrhosis Relapsing polychondritis Rheumatoid arthritis Sarcoidosis Sjgren syndrome Thyroid disease Ulcerative colitis Vitiligo Acquired hemophilia Bullous pemphigoid Celiac disease Chronic hepatitis Chronic lymphocytic leukemia Crohn disease Dermatomyositis Hemolytic anemia Hodgkin lymphoma Hydatidiform mole Hypothyroidism IgA nephropathy Immune-complex glomerulonephritis Malignancies Membranous glomerulonephropathy Monoclonal glomerulonephropathy Multiple sclerosis Non-Hodgkin lymphoma Pancreatic lipase deficiency

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Dermatitis herpetiformis (Duhring)

Linear IgA disease

Pemphigoid gestationis

Epidermolysis bullosa acquisita

(continued on next page)

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Table 2 (continued) Disease Disease associations Polycythemia rubra vera Polymyalgia rheumatica Psoriasis vulgaris Rheumatoid arthritis Sarcoidosis Spondyloarthropathy Lupus erythematosus systemicus Ulcerative colitis

S. Ljubojevic, J. Lipozeni regions. Although the coexistence of pemphigus vegetans and an internal neoplasm is rare, it has been described in coexistence with lung cancer, lymphosarcoma, colon, and gastric cancer.61-65 Pemphigus vegetans is described in association with HIV infection.66,67

Pemphigus foliaceus/erythematosus
Pemphigus erythematosus is a variant of pemphigus foliaceus. Pemphigus erythematosus and pemphigus foliaceus may be associated with MG or thymoma.20-24,68,69 There are few reports of the coexistence of pemphigus foliaceus with BP,70,71 psoriasis vulgaris,72-76 Grave disease,77 oral lichen planus,76 SLE,69 mycosis fungoides,78 HIV,79 and immunoglobulin (Ig) A nephropathy.74 There are also a few reports on radiotherapy-induced pemphigus foliaceus.80,81

cigarette smoking.45,46 The beneficial effect of smoking on pemphigus might be explained by its effect on the immune system.46 Smoking also has an antiestrogenic effect, whereas pesticides have an estrogenic effect.45,46 The lower numbers of smokers among patients, the higher exposure rates to pesticides, and the higher number of female patients who had been pregnant may point to the contribution of estrogens to the disease process.46 The most common environmental factors that might induce pemphigus are drugs and food, and are divided into three main groups according to their chemical structure: thiols (containing a sulfhydryl group), phenol, and nonthiol nonphenol.47 Thiol and phenol compounds can induce acantholysis in tissue cultures in vitro.47,48 The suggested mechanisms for thiol acantholysis include direct biochemical impairment of cell adhesion, protease activation, and immunologic reaction with the formation of a neoantigen.47,48 Possible mechanisms of phenol-induced pemphigus include the induction of interleukin (IL) 1 and tumor necrosis factor (TNF)- release by keratinocytes.47,48 Some plants, in particular those belonging to the Allium group, contain several active compounds with stable disulfide and thiol groups in their molecule.49 The Allium group includes many important vegetables, including like onion, leek, and garlic. Garlic is widely appreciated as a spice and as a vegetable as well as an over-the-counter phytotherapeutic. It is used medicinally, mainly for the treatment of hypercholesterolemia and prevention of arteriosclerosis.50,51 Case reports have highlighted the possibility that garlic use may cause pemphigus.52 Allyl compounds of garlic are able to provoke acantholysis in normal human skin cultured in vitro.52 There are only a few reports on coexistence of pemphigus vulgaris with psoriasis vulgaris,53 vitiligo,54,55 alopecia areata,54 lichen planus,56 Darier disease,57 Paget disease of the nipple, 58 radiotherapy,59 and chronic lymphocytic leukemia.60

Intercellular IgA dermatosis (IgA pemphigus)

IgA pemphigus is a rare disease marked by a vesiculopustular eruption characterized by intercellular IgA deposition in the epidermis.82 It encompasses two subgroups: subcorneal pustular dermatosis type and intraepidermal neutrophilic IgA dermatosis type. The most frequently reported association is with monoclonal IgA gammopathy (IgA- and IgA-) in the subcorneal type.83-88 IgA pemphigus is often associated with other disorders, including myeloma,84,89 B-cell lymphoma,90 gastrointestinal disorders (Crohn disease, colitis, ulcerative colitis, gluten-sensitive enteropathy),90-94 acute polyarthritis,95 rheumatoid arthritis,96,97 Sjgren syndrome,82,96 and HIV infection.88,98,99 HIV infection results in immunodeficiency and immune dysregulation with polyclonal B-cell activation, which has been associated with autoantibody formation and the development of autoimmune disease.82 A patient with subcorneal pustular dermatosis-type IgA pemphigus, which arose during a course of chrysotherapy for rheumatoid arthritis was reported.97 An association of IgA pemphigus and IgA gammopathy and lung cancer has been reported.100,101

Pemphigus herpetiformis
Pemphigus herpetiformis is a rare pemphigus variant. The clinical features of this form of pemphigus resemble dermatitis herpetiformis; however, histologic examination and immunofluorescence yield findings diagnostic for pemphigus.102 There are few reports of the coexistence of pemphigus herpetiformis with psoriasis vulgaris. 103,104 Pemphigus disease developed in one patient with a history of psoriasis shortly after a course of ultraviolet (UV) light treatment, raising a possible role of UV light in the induction of pemphigus herpetiformis.103 Pemphigus herpetiformis has been reported to occur in association with lung and prostate cancer.105-107 The coexistence of pemphigus herpetiformis

Pemphigus vegetans
Pemphigus vegetans is a rare variant of pemphigus vulgaris characterized by vegetating plaques in the flexural

Autoimmune bullous diseases associations with SLE108 and an HIV-positive man41 who developed pemphigus herpetiformis are described. A patient with pemphigus herpetiformis association with use of medication (thiopronine) has been reported.109

21 results in acantholysis, and drugs are postulated to induce acantholysis directly in the absence of antibody formation.165 Drugs that induce pemphigus may be categorized into three groups: thiol (containing a sulfhydryl group) phenol, and nonthiol nonphenol drugs.47 Thiol drugs are reported most frequently as the culprits of drug-induced pemphigus.165 Induction of IL-1 and TNF- release by keratinocytes can are possible mechanisms of phenolinduced pemphigus.47,48 Research has shown 61 drugs can induce pemphigus.166 Penicillamine and captopril are the thiol drugs most often associated with drug-induced pemphigus.53,62,165-173 Other thiol drugs are bucillamine, lisinopril, pyritinol, thiopronine, piroxicam, thiamazole, 5-thiopyridoxine, and gold sodium thiomalate.109,165,166,174-180 Nonthiol drugs include angiotensin-converting enzyme inhibitors, such as enalapril, ramipril, and fosinopril, and the angiotensin II receptor blockers, candesartan and telmisartan.53,62,165,166,175,176,181-186 Other drugs implicated in pemphigus are nifedipine, the penicillins, cephalosporins, quinolones, rifampicin, pyrazolone derivatives, chloroquine, hydroxychloroquine, montelukast, interferon, imiquimod, and heroin.165,166,176,187-194 An epidemiologic review of Iranian pemphigus vulgaris patients suggested a positive correlation with oral contraceptive use.45 Pemphigus vulgaris and foliaceus have been induced by radiotherapy and pemphigus vulgaris by thermal burns and electrical injury.59,195,196

Paraneoplastic pemphigus
Paraneoplastic pemphigus (PNP) is an autoimmune syndrome mostly seen in association with malignancy, although it can occur in association with a benign neoplasm. The most commonly associated are lymphoproliferative disorders.110 The most commonly associated neoplasms are hematologic neoplasms or disorders, which constitute nearly 84% of all tumor-related PNP.111-113 Included are non-Hodgkin lymphoma,114-117, chronic lymphocytic leukemia,118-120 Castleman disease,121-128 thymoma (malignant and benign),129-133 retroperitoneal sarcoma, 127,129,134-137 and Waldenstrm macroglobulinemia.138 PNP in children and adolescents is most often a presenting sign of occult Castleman disease.123-125 It presents with severe oral mucositis and cutaneous lichenoid lesions.124 A girl with PNP associated with Hodgkin lymphoma was described.139 Carcinomas constitute nearly 58% of the total nonhematologic malignancies.140,141 Underlying neoplasm malignancies can also be associated with PNP, including pancreas,142 uterine,143,144 hepatocellular,145,146 and renal malignancy.147 One report described PNP associated with a malignant gastrointestinal stromal tumor.148 With very rare exceptions, more common cancers, such as adenocarcinomas of breast, bowel, and lung, or basal cell and squamous cell carcinoma of the skin have not been associated with PNP.110 A few reports have connected PNP with tumors such as squamous cell carcinoma, but most of these diagnoses have not been confirmed by immunochemical testing, so the association remains unproven.110 Other associated disorders or triggering factors are MG,132,149 systemic mastocytosis,150 SLE,151 polymyositis,151 bronchiolitis obliterans,152-154 malignant melanoma,155 and toxic epidermal necrolysis.156 Some cases have been linked with the use of fludarabine chemotherapy,157-160 radiotherapy,161 and chemotherapy with interferon.162 PNP can coexist with BP,163 and one case associated with non-Hodgkin lymphoma evolved into typical pemphigus vulgaris after the patient experienced a 4-year disease-free interval.164 Underlying disorders and possible triggering factors may contribute to the development of a specific autoimmunity in PNP. 140 Clinicians should be highly suspicious when signs and symptoms suggestive of PNP are present in cancer patients of hematologic and nonhematologic origin.

Bullous pemphigoid
The potential occurrence of malignant diseases in patients with BP is most likely related to the old age of the patients. BP is an affliction of elderly people, with onset usually after age 60, with a mean of 80 years.1,197 BP can occur in people younger than 40 years and also in children.1,198-200 The etiology of childhood BP is also unknown; however, drug intake and vaccination have been incriminated in some cases.201,202 Some reports have suggested an increased frequency of certain cancers (such as of digestive tract, lung, urinary bladder, breast) and lymphoproliferative disorders.1,3,120,203-219 There is controversy about association between BP and malignancy. Most large series have concluded that there is no or only a very small increase in the incidence of malignancy in BP patients compared with ageand sex-matched controls, although the association may exist in individual patients.1,203 A study of 1113 Japanese patients with BP showed that an association in 64 patients (5.8%) between internal malignancies and BP.200 This association ratio was significantly higher than that of the controls aged older than 70 (0.61%).200 The carcinoma may express the BP antigens and evoke an immune response.1 BP has also been found in association with certain dermatoses, such as psoriasis and lichen planus.220-244 In these conditions, it has been speculated that the inflammatory process at the dermoepidermal junction is responsible for

Drug-induced pemphigus
A variety of drugs may exacerbate or induce pemphigus. Some of these drugs induce antibody formation, which

22 the exposure of antigens to autoreactive T lymphocytes leading to a secondary immune response.3 In 1929, the first case of a psoriatic patient who developed a bullous eruption was described.220 In 1976, the first association between the incidence of BP and antipsoriatic therapy was described.221 Some authors think that the concurrence of psoriasis vulgaris and bullous diseases is due to a combined action of diseased psoriatic epidermis and irritant effects of antipsoriatic therapy, which may initiate the production of basement membrane zone autoantibodies in susceptible individuals.222-224 The basal membrane zone can then precipitate the antigenic modification of proteins at the dermoepidermal junction. The breakdown of this zone by the treatments may facilitate the exposure of such antigens to the circulation. Most reported cases of BP with psoriasis literature occurred after antipsoriatic treatment, such as with tar, anthralin, psoralens, sun exposure, psoralen and UVA (PUVA) therapy, or UVA and UVB light.225-234 These therapies are widely used, and one would expect to find many more cases of psoriasis associated with bullous diseases. In some patients, no causative agent was found. The triggering factor remains unknown. The occurrence of bullous lesions in psoriasis patients receiving PUVA therapy is not uncommon. Those bullous lesions usually represent a phototoxic reaction (various drugs) or just accidental overdosage.233,234 It is explained as an expression of the preexisting subclinical bullous disease or as an immunologic response resulting in the formation of complement-binding basement membrane zone antibodies.235 Bullous lesions in such patients usually develop in erythematous areas and are histopathologically characterized by a large number of sunburn cells. Some psoriatic patients have developed bullous disease without any previous therapy.225,229,235,236 Coexistence of psoriasis vulgaris and BP has also been described in association with other diseases such as generalized scleroderma,237 Hashimoto thyroiditis,238 and vitiligo.239,240 The coexistence of BP and lichen planus may indicate a possible link between the pathology in the junctional zone in lichen planus and the appearance of antibasement membrane zone antibodies and bullous lesions.241-243 The coexistence of lichen planus and BP, referred to as lichen planus pemphigoides, shows typical clinical, histologic, and immunopathologic features of both diseases.244 BP is described in patients with other autoimmune disorders, such as SLE,245-248 rheumatoid arthritis,249-254 vitilligo,239,240,253,255,256 Hashimoto thyroiditis,238,254,257 Grave disease,258 dermatomyositis,210,259 polymyositis,260 autoimmune neutropenia,254 autoimmune thrombocytopenia,261 immune-complex glomerulonephritis,262 MG,263 and HIV.264-266 Although a case-control study did not find any increased risk for autoimmune disorders in BP, it is likely that these associations are not fortuitous but reflect a genetically determined susceptibility to develop autoimmune disease.267 Other diseases associated with BP are diabetes

S. Ljubojevic, J. Lipozeni mellitus,268-270 pernicious anemia,271,272 ulcerative colitis,273-277 hyperthyreosis and hypothyreosis,256,278 polymyalgia rheumatica,278 alopecia,254 mycosis fungoides,279 primary biliary cirrhosis,255,280,281 Castleman disease,282 Kaposi sarcoma,283 thymoma,263 nephritis and glomerulonephritis,280,284-290 morphea,291 and acquired hemophilia.253,292,293 The occurrence rate of primary diabetes mellitus before the administration of systemic corticosteroids was significantly higher in patients with BP (20%) than in the controls (2.5%, P = .004).268 Some authors have reported an association of BP with other autoimmune blistering diseases, including pemphigus vulgaris,30-32 pemphigus foliaceus,70,71 linear IgA dermatosis,294,295 and dermatitis herpetiformis (DH).296,297 Strong associations were observed between specific neurologic diseases and the later development of BP, supporting possible causal associations.3,244,268,298,299 Mechanisms for disease occurrence based on these findings include immobility or age-related autoimmunity.298 The association between BP, multiple sclerosis, and Parkinson disease, based on retrospective epidemiologic studies, is highly statistically significant.300-306 BP has also been described in patients with amyotrophic lateral sclerosis, 307,308 dementia,268,298,299,309 epilepsy,298,299 and Shy-Dragger syndrome.310 The significance of these associations is unclear, but it is intriguing to note that one of the two autoantigens of BP, the BP230, has several isoforms (such as BPAG1-a) that are expressed in the central and peripheral nervous system and in muscles.311 In certain cases, autoantibodies to BP230 may possibly cross-react with these isoforms and contribute to the neurologic manifestations.3 The etiopathogenic mechanisms and the causes that induce the loss of immunologic tolerance are not yet understood. BP in some patients may be induced by trauma,312 burns,313-317 or radiotherapy.318-321 It is not clear yet by which mechanisms drugs affect the development of BP, but it is likely that these patients have an underlying susceptibility for the development of BP and the drugs act as triggers.3,322 The results from a case-control study suggest that some drug therapies may be a risk factor for BP.323 Sulfur-containing drugs commonly cause drug-induced pemphigoid, with furosemide being the most common.324-330 Besides diuretics, nonsteroidal anti-inflammatory drugs, D-penicillamine, antibiotics (ampicillin, amoxicillin, and ciprofloxacin), -blockers, iodine, simvastatin and captopril are the most frequently implicated drugs.3,244,331-335

Pemphigoid gestationis
Pemphigoid gestationis is most commonly associated with pregnancy; however, it may also be associated with a hydatiform mole, trophoblastic tumors, or choriocarcinoma.336 Such pregnancies should be considered high-risk. Onset of pemphigoid gestationis is in the first or second

Autoimmune bullous diseases associations trimester, and presence of blisters may lead to adverse pregnancy outcomes, including decreased gestational age at delivery, preterm birth, and low birthweight neonates.336-339 Women with pemphigoid gestationis in their medical history are considered to have higher prevalence of autoimmune disease, including Grave disease (autoimmune thyrotoxicosis), Hashimoto thyroiditis, vitiligo, autoimmune thrombocytopenia, and pernicious anemia.336-340 Exacerbations may occur with oral contraceptives, and the severity may vary during the menstrual cycle.338 Patients with pemphigoid gestationis have an increased incidence of alleles of the human leukocyte antigens (HLA) HLA-B8 (class I) and HLA-DR3, and HLA-DR4 (class II) encoded on the short arm of chromosome 6.341,342

23 conditions have a 95% incidence of the HLA haplotypes DR3/DQ2. DH and gluten-sensitive enteropathy or, as it is more commonly called, celiac disease (CD), are glutensensitive diseases that have common immunopathologic and genetic mechanisms. Subsequently, the CD and DH were recognized as having the same gastrointestinal abnormalities.374 A recent report demonstrated that the likelihood in CD of an associated autoimmune disease is related to the duration of exposure to gluten and is higher in patients with CD diagnosed at a later stage.375 In most cases, the associated autoimmune disorder appeared before a glutenfree diet was initiated, suggesting that long-standing untreated CD predisposes to the occurrence of other autoimmune disorders in the same patient.375 In addition, longstanding CD is associated with increased frequency of lymphomas of the intestine.376 DH is associated with an additional autoimmune disorder in approximately 10% of patients,377-379 and may be a consequence of a common genetic background.377 Autoimmune disorders associated with DH and CD include autoimmune thyroiditis (Hashimoto thyroiditis),377,380 type I diabetes,381 SLE,377,382,383 Sjgren disease,377,384,385 dermatomyositis/ polymyositis,385,386 vitiligo,377,387-389 rheumatoid arthritis,390 and others. The most common malignancies associated with DH and CD are gastrointestinal lymphomas and non-Hodgkin lymphoma. 391-393 In a study of long-term risks of malignant diseases and mortality in patients with CD and DH, non-Hodgkin lymphoma emerged in patients with undiagnosed or poorly treated CD.391 The mortality rate in DH was even lower than in the population. The data from this study support the early diagnosis and dietary treatment of these conditions.391 In addition to CD, gastric disorders, such as atrophic gastritis are associated with DH.394,395 DH may exceptionally be associated with chronic ulcerative colitis.396 Neuropsychiatric complications have been reported in up to 26% of patients with CD.397 This is probably an overestimate because of the chance associations with some common neurologic conditions such as epilepsy. Gluten has been postulated to be neurotoxic, possibly via immune mechanisms. The frequency of neurologic dysfunction in patients with DH has not been characterized, 397 but these patients might be expected to be particularly susceptible to neuronal damage because some continue to consume gluten when their dermatologic symptoms are controlled by dapsone. 397 The most often described neurologic associations with DH and CD are ataxia, dementia, and epilepsy.397-399 There are few case report on DH coexistence with thyroid disease (hyperthyreosis and hypothyreosis, thyrotoxicosis),385,400 sarcoidosis,377 alopecia areata,377 lichen planopilaris,401 relapsing polychondritis,402 cutaneous leiomyoma,403 BP,296,297 primary biliary cirrhoisis,404 pernicious anemia,390 Addison disease,405 nephrotic syndrome,406 IgA nephropathy, 407 polycystic kidney disease, and hemodialysis.408

Epidermolysis bullosa acquisita

Epidermolysis bullosa acquisita (EBA) is characterized by IgG autoantibodies that target collagen VII, a major skin basement membrane component. Another autoimmune bullous skin disease that may exhibit autoantibodies against type VII collagen is BSLE. EBA and BSLE patients often have a common HLA major histocompatibility class II cell surface protein, HLA-DR2, suggesting EBA and BSLE are immunologically related diseases.343 Patients with both EBA and BSLE have been reported.344-346 The disease most frequently associated with EBA appears to be inflammatory bowel disease (IBD), occurring in an estimated of 25% to 50% of EBA patients,347-354 with Crohn disease350-354 the most frequently associated with EBA. An EBA association with ulcerative colitis is reported in only a few patients.347 Autoantibodies against type VII collagen have been detected in up to 68% of IBD patients.349 Although these findings suggest that chronic intestinal inflammation in IBD predisposes for autoimmunity against type VII collagen, their relevance for the pathogenesis of both IBD and EBA is still unclear.348 Patients with IBD, especially Crohn disease, have a high prevalence of circulating antibodies against type VII collagen.355 EBA has been reported in association with a number of other systemic diseases, such as multiple myeloma,356-360 amyloidosis,360 psoriasis vulgaris,361,362 chronic lymphocytic leukemia,363 IgM macroglobulinaemia,364 multiple endocrinopathy syndrome,365 carcinoma,366-370 rheumatoid arthritis, Hashimoto thyroiditis, diabetes, pulmonary fibrosis, and thymoma.3,348 One report has been published of mixed bullous disease of EBA and linear IgA bullous dermatosis.371 EBA was reported in a 73-year-old patient after a 2-week treatment of antibiotics, including vancomycin.372

Dermatitis herpetiformis
All patients with DH have evidence of gluten sensitivity in the small intestine, although only two-thirds showed villous atrophy on a single biopsy specimen.373 Both

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S. Ljubojevic, J. Lipozeni logic autoimmune disorders have been described in association with MAS.450 In MAS, patients often have at least one dermatologic condition. MAS can be classified into three groups that correspond with the prevalence of their being associated with one another. In patients with two autoimmune diseases, this classification is helpful when signs of a third disorder emerge;2,450-452 Type 1 MAS includes MG, thymoma, polymyositis, and giant cell myocarditis. Type 2 MAS includes Sjgren syndrome, rheumatoid arthritis, primary biliary cirrhosis, scleroderma, and autoimmune thyroid disease (Hashimoto thyroiditis, atrophic thyroiditis, Grave disease). Type 3 MAS groups autoimmune thyroid disease, MG, and/or thymoma, Sjgren syndrome, pernicious anemia, idiopathic thrombocytopenic purpura, Addison disease, insulin-dependent diabetes, vitiligo, autoimmune hemolytic anemia, SLE, and DH, and the immune system marker HLA-B8 and/or DR3 or DR5 seems to be an important factor.452 Other conditions found in various combinations in MAS are pemphigus and autoimmune thyroid disease in type 1 MAS; chronic active hepatitis, SLE, pemphigus, BP, autoimmune hemolytic anemia, idiopathic thrombocytopenic purpura, alopecia areata, and Addison disease in type 2 MAS; and acquired primary hypogonadism, hypophysitis, rheumatoid arthritis, primary biliary cirrhosis, relapsing polychondritis, multiple sclerosis, chronic active hepatitis, ulcerative colitis, and scleroderma in type 3 MAS.452

Linear IgA disease

Linear IgA disease (LAD) is itself an autoimmune disease, and an association with other such disorders is interesting, despite proven causality.409 Patients with LAD have been described in association with SLE,409,410 dermatomyositis,409,411 rheumatoid arthritis,412 psoriasis,413 BP,295 and polymyalgia rheumatica.409 These associations may be coincidental.409 LAD associated with malignancy has been reported in as many as 5% of patients.409 There is an increased incidence of lymphoproliferative disorders, specifically Hodgkin disease, non-Hodgkin lymphoma, and chronic lymphocytic leukemia.414-417 LAD has also been reported with other associated malignancies, such as bladder, breast, renal, uterine, thyroid, pancreatic, esophageal, colon, eccrine, retroperitoneal, and metastatic squamous cell carcinoma, metastatic hypernephroma, ocular melanoma, plasmacytoma, and multiple myeloma.409,418-426 The validity of the association between LAD and malignancy remains to be proven.409 There are few reports on a LAD association with pancreatic lipase deficiency,409 chronic hepatitis,427 Crohn disease,428 ulcerative colitis,429,430 CD,431 multiple sclerosis,432 acquired hemophilia,433 IgA nephropathy,434 spondyloathropathy,435 membranous glomerulonephropathy,436 monoclonal glomerulonephropathy,437 immune-complex glomerulonephritis,262 hemolytic anemia,434 hydatidiform mole,438 sarcoidosis,439 polycythemia rubra vera,409 and hypothyroism.409 Many precipitating factors are observed in association with LAD, namely preceding illnesses and drugs.440-449 Preceding illnesses that have been reported in association with LAD include varicella, herpes zoster, tuberculosis, Paecilomyces lung infection, gynecologic infections, typhoid, brucella, antibiotic-treated tetanus, and upper respiratory infections. 409,440,441 The significance of these associations is uncertain. Local skin trauma has initiated the disease in some patients.1,442 Among the various implicated causative drugs, vancomycin is the most commonly associated with LAD.440,443 Other potential triggers include amiodarone, amoxicillin, amoxicillin-clavulanate, ampicillin sodium, captopril, cefamandole nafate, cyclosporine, depot sulfonamide, diclofenac, furosemide, glibenclamide, interferon-, interferon-2a, IL 2, iodine contrast agent, lithium carbonate, moxifloxacin, naproxen penicillin sodium, phenytoin sodium, somatostatin, sulfamethoxazoletrimethoprim, sulfisoxazole, topical sodium hypochlorite, and vigabatrin.1,409,444-448 LAD development was reported in a 54-year-old woman after an influenza vaccination.449

Conclusions
The presence of one autoimmune disease increases the likelihood of additional autoimmune diseases. The occurrence of autoimmune disease coexistence indicates the need for continued surveillance for the development of new autoimmune disease in predisposed patients.

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Multiple autoimmune syndrome

Multiple autoimmune syndrome (MAS) is a condition in which patients have at least three distinct autoimmune conditions. Since the first report in 1988, various dermato-

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