An update on the cutaneous manifestations of coeliac disease and non-coeliac gluten sensitivity

References

• Leonard MM, Sapone A, Catassi C, Fasano A. Celiac disease and nonceliac gluten sensitivity: a review. JAMA 2017;318(7):647–656.
   PubMed Web of Science ®Google Scholar
• Czaja-Bulsa G. Non coeliac gluten sensitivity – a new disease with gluten intolerance. Clin Nutr 2015;34(2):189–194. doi:10.1016/j.clnu.2014.08.012.
   PubMed Web of Science ®Google Scholar
• Humbert P, Pelletier F, Dreno B, et al. Gluten intolerance and skin diseases. Eur J Dermatol. 2006;16(1):4–11.
   PubMed Web of Science ®Google Scholar
• Reunala T, Salmi TT, Hervonen K, et al. Dermatitis herpetiformis: a common extraintestinal manifestation of coeliac disease. Nutrients 2018;10(5):602.
   Web of Science ®Google Scholar
• Griffiths C, Barker J, Bleiker T, et al. Rook's textbook of dermatology, 4vol., 9th ed. Hoboken, NJ: Wiley-Blackwell Press; 2016. p. 4696.
   Google Scholar
• Reunala T, Salmi TT, Hervonen K. Dermatitis herpetiformis: pathognomonic transglutaminase IgA deposits in the skin and excellent prognosis on a gluten-free diet. Acta Derm Venerol 2015;95(8):917–922. doi:10.2340/00015555-2162.
   PubMed Web of Science ®Google Scholar
• Kárpáti S, Sárdy M, Németh K, et al. Transglutaminases in autoimmune and inherited skin diseases: The phenomena of epitope spreading and functional compensation. Exp Dermatol 2017;27(8):807–814. doi:10.1111/exd.13449.
   Web of Science ®Google Scholar
• Collin P, Huhtala H, Virta L, et al. Diagnosis of celiac disease in clinical practice: physician's alertness to the condition essential. J Clin Gastroenterol 2007;41(2):152–156.
   PubMed Web of Science ®Google Scholar
• Salmi TT, Hervonen K, Kautiainen H, et al. Prevalence and incidence of dermatitis herpetiformis: a 40-year prospective study from Finland. Br J Dermatol 2011;165(2):354–359.
   PubMed Web of Science ®Google Scholar
• Virta LJ, Kaukinen K, Collin P. Incidence and prevalence of diagnosed coeliac disease in Finland: results of effective case finding in adults. Scand J Gastroenterol 2009;44(8):933–938.
   PubMed Web of Science ®Google Scholar
• West J, Fleming KM, Tata LJ, et al. Incidence and prevalence of celiac disease and dermatitis herpetiformis in the UK over two decades: population-based study. Am J Gastroenterol 2014;109(5):757–768.
   PubMed Web of Science ®Google Scholar
• Smith JB, Tulloch JE, Meyer LJ, Zone JJ. The incidence and prevalence of dermatitis herpetiformis in Utah. Arch Dermatol 1992;128(12):1608–1610.
   PubMedGoogle Scholar
• Askling J, Linet M, Gridley G, et al. Cancer incidence in a population-based cohort of individuals hospitalized with celiac disease or dermatitis herpetiformis. Gastroenterology 2002;123(5):1428–1435.
   PubMed Web of Science ®Google Scholar
• Zingone F, West J, Auricchio R, et al. Incidence and distribution of coeliac disease in Campania (Italy): 2011-2013. United European Gastroenterol J 2015;3(2):182–189. doi:10.1177/2050640615571021.
   PubMed Web of Science ®Google Scholar
• Losurdo G, Principi M, Iannone A, et al. Extra- intestinal manifestations of non-celiac gluten sensitivity: An expanding paradigm. World J Gastroenterol 2018;24(14):1521–1530. doi:10.3748/wjg.v24.i14.1521.
   PubMed Web of Science ®Google Scholar
• Antiga E, Verdelli A, Calabrò A, et al. Clinical and immunopathological features of 159 patients with dermatitis herpetiformis: an Italian experience. G Ital Dermatol Venereol 2013;148(2):163–169.
   PubMed Web of Science ®Google Scholar
• Macbeth AE, Lee KY, Levell NJ, et al. Photoletter to the editor: Dermatitis herpetiformis co-localised with vitiligo in a patient with autoimmune polyglandular syndrome. J Dermatol Case Rep 2013;7(3):101–102. doi:10.3315/jdcr.2013.1153.
   PubMedGoogle Scholar
• Mendes FB, Hissa-Elian A, Abreu MA, Gonçalves VS. Review: dermatitis herpetiformis. An Bras Dermatol 2013;88(4):594–599. doi:10.1590/abd1806-4841.20131775.
   PubMed Web of Science ®Google Scholar
• Sárdy M, Kárpáti S, Merkl B, Paulsson M, et al. Epidermal transglutaminase (TGase 3) is the autoantigen of dermatitis herpetiformis. J Exp Med 2002;195(6):747–757.
   PubMed Web of Science ®Google Scholar
• Zone JJ, Meyer LJ, Petersen MJ. Deposition of granular IgA relative to clinical lesions in dermatitis herpetiformis. Arch Dermatol 1996;132(8):912–918.
   PubMedGoogle Scholar
• Donaldson MR, Zone JJ, Schmidt LA, et al. Epidermal transglutaminase deposits in perilesional and uninvolved skin in patients with dermatitis herpetiformis. J Invest Dermatol 2007;127(5):1268–1271.
   PubMed Web of Science ®Google Scholar
• Kurosaki Y, Suga Y, Negi O, et al. Monitoring of immunoglobulin A antibodies to epidermal and tissue transglutaminases overan 18-month period in a Japanese patient with dermatitis herpetiformis. J Dermatol 2018;45(8):e211–e212. doi:10.1111/1346-8138.14264.
   PubMed Web of Science ®Google Scholar
• Kárpáti S. Dermatitis herpetiformis: close to unravelling a disease. J Dermatol Sci 2004;34(2):83–90.
   PubMed Web of Science ®Google Scholar
• Taylor TB, Zone JJ. Sensitivity of transglutaminase 3 in the IgA aggregates in dermatitis herpetiformis skin to potassium iodide. J Invest Dermatol 2018;138(9):2066–2068. doi:10.1016/j.jid.2018.03.1497.
   PubMed Web of Science ®Google Scholar
• Huelsz-Prince G, Belkin AM, VanBavel E, Bakker EN. Activation of extracellular transglutaminase 2 by mechanical force in the arterial wall. J Vasc Res 2013;50(5):383–395.
   PubMed Web of Science ®Google Scholar
• Gornowicz-Porowska J, Seraszek-Jaros A, Bowszyc-Dmochowska M, et al. Immunoexpression of IgA receptors (CD89, CD71) in dermatitis herpetiformis. Folia Histochem Cytobiol 2018;55(4):212–220.
   Web of Science ®Google Scholar
• Reitamo S, Reunala T, Konttinen YT, et al. Inflammatory cells, IgA, C3, fibrin and fibronectin in skin lesions in dermatitis herpetiformis. Br J Dermatol 1981;105(2):167–177.
   PubMed Web of Science ®Google Scholar
• Garioch JJ, Baker BS, Leonard JN, Fry L. T lymphocytes in lesional skin of patients with dermatitis herpetiformis. Br J Dermatol 1994;131(6):822–826.
   PubMed Web of Science ®Google Scholar
• Hall RP, 3rd, Benbenisty KM, Mickle C, et al. Serum IL-8 in patients with dermatitis herpetiformis is produced in response to dietary gluten. J Invest Dermatol 2007;127(9):2158–2165. Sep
   PubMed Web of Science ®Google Scholar
• Hall RP, 3rd, Takeuchi F, Benbenisty KM, Streilein RD. Cutaneous endothelial cell activation in normal skin of patients with dermatitis herpetiformis associated with increased serum levels of IL-8, sE-Selectin, and TNF-alpha. J Invest Dermatol 2006;126(6):1331–1337.
   PubMed Web of Science ®Google Scholar
• Zebrowska A, Waszczykowska E, Wagrowska-Danilewicz M, et al. Expression of selected adhesion molecules in dermatitis herpetiformis and bullous pemphigoid. Pol J Pathol 2009;60(1):26–34.
   PubMed Web of Science ®Google Scholar
• Garioch JJ, Lewis HM, Sargent SA, et al. 25 years' experience of a gluten-free diet in the treatment of dermatitis herpetiformis. Br J Dermatol 1994;131(4):541–545.
   PubMed Web of Science ®Google Scholar
• Hietikko M, Hervonen K, Salmi T, et al. Disappearance of epidermal transglutaminase and IgA deposits from the papillary dermis of patients with dermatitis herpetiformis after a long-term gluten-free diet. Br J Dermatol 2018;178(3):e198–e201. doi:10.1111/bjd.15995.
   PubMed Web of Science ®Google Scholar
• Kárpáti S, Meurer M, Stolz W, et al. Dermatitis herpetiformis bodies. Ultrastructural study on the skin of patients using direct preembedding immunogold labeling. Arch Dermatol 1990;126(11):1469–1474.
   PubMedGoogle Scholar
• Preisz K, Sárdy M, Horváth A, Kárpáti S. Immunoglobulin, complement and epidermal transglutaminase deposition in the cutaneous vessels in dermatitis herpetiformis. J Eur Acad Dermatol Venerol 2005;19(1):74–79.
   PubMed Web of Science ®Google Scholar
• Taylor TB, Schmidt LA, Meyer LJ, Zone JJ. Transglutaminase 3 present in the IgA aggregates in dermatitis herpetiformis skin is enzymatically active and binds soluble fibrinogen. J Invest Dermatol 2015;135(2):623–625.
   PubMed Web of Science ®Google Scholar
• Clarindo MV, Possebon AT, Soligo EM, et al. Dermatitis herpetiformis: pathophysiology, clinical presentation, diagnosis and treatment. An Bras Dermatol 2014;89(6):865–875.
   PubMed Web of Science ®Google Scholar
• Bonciolini V, Bonciani D, Verdelli A, et al. Newly described clinical and immunopathological feature of dermatitis herpetiformis. Clin. Dev Immunol 2012;2012:1.
   Google Scholar
• Bonciani D, Verdelli A, Bonciolini V, et al. Dermatitis herpetiformis: from the genetics to the development of skin lesions. Clin Dev Immunol 2012;2012:1.
   Google Scholar
• Hujoel IA, Van Dyke CT, Brantner T, et al. Natural history and clinical detection of undiagnosed coeliac disease in a North American community. Aliment Pharmacol Ther 2018;47(10):1358–1366.
   PubMed Web of Science ®Google Scholar
• Kneisel A, Hertl M. Autoimmune bullous skin diseases. Part 1: clinical manifestations. JDDG 2011;9(10):844–857.
   Google Scholar
• Caproni M, Antiga E, Melani L, Fabbri P. Italian Group for Cutaneous Immunopathology. Guidelines for the diagnosis and treatment of dermatitis herpetiformis. J Eur Acad Dermatol Venereol 2009;23(6):633–638.
   PubMed Web of Science ®Google Scholar
• Barnadas MA. Dermatitis herpetiformis: a review of direct immunofluorescence findings. Am J Dermatopathol 2016;38(4):283–288.
   PubMed Web of Science ®Google Scholar
• Wozel G, Blasum C. Dapsone in dermatology and beyond. Arch Dermatol Res 2014;306(2):103–124. doi:10.1007/s00403-013-1409-7.
   PubMed Web of Science ®Google Scholar
• Sunilkumar MN, Ajith TA, Parvathy VK. Acute dapsone poisoning in a 3-year-old child: case report with review of literature. World J Clin Cases 2015;3(10):911–914.
   PubMed Web of Science ®Google Scholar
• Bolotin D, Petronic-Rosic V. Dermatitis herpetiformis. Part II. Diagnosis, management, and prognosis. J Am Acad Dermatol 2011;64(6):1027–1033.
   PubMed Web of Science ®Google Scholar
• McFadden JP, Leonard JN, Powles AV, et al. Sulphamethoxypyridazine for dermatitis herpetiformis, linear IgA disease and cicatricial pemphigoid. Br J Dermatol 1989;121(6):759–762.
   PubMed Web of Science ®Google Scholar
• Kazmierowski JA, Ross JE, Peizner DS, Wuepper KD. Dermatitis herpetiformis: effects of sulfones and sulfonamides on neutrophil myeloperoxidase-mediated iodination and cytotoxicity. J Clin Immunol 1984;4(1):55–64.
   PubMed Web of Science ®Google Scholar
• Willsteed E, Lee M, Wong LC, Cooper A. Sulfasalazine and dermatitis herpetiformis. Australas J Dermatol 2005;46(2):101–103.
   PubMedGoogle Scholar
• Christophers E. Psoriasis-epidemiology and clinical spectrum. Clin Exp Dermatol 2001;26(4):314–320.
   PubMed Web of Science ®Google Scholar
• Raut AS, Prabhu RH, Patravale VB. Psoriasis clinical implications and treatment: a review. Crit Rev Ther Drug Carrier Syst 2013;30(3):183–216.
   PubMed Web of Science ®Google Scholar
• Ojetti V, Aguilar Sánchez J, Guerriero C, et al. High prevalence of celiac disease in psoriasis. Am J Gastroenterol 2003;98(11):2574–2575.
   PubMed Web of Science ®Google Scholar
• Lindqvist U, Rudsander Å, Boström Å, et al. IgA antibodies to gliadin and coeliac disease in psoriatic arthritis. Rheumatology 2002;41(1):31–37.
   PubMed Web of Science ®Google Scholar
• Egeberg A, Griffiths CEM, Mallbris L, et al. The association between psoriasis and coeliac disease. Br J Dermatol 2017;177(6):e329–e330.
   PubMed Web of Science ®Google Scholar
• Ungprasert P, Wijarnpreecha K, Kittanamongkolchai W. Psoriasis and risk of celiac disease: a systematic review and meta-analysis. Indian J Dermatol 2017;62(1):41–46.
   PubMed Web of Science ®Google Scholar
• Bhatia BK, Millsop JW, Debbaneh M, et al. Diet and psoriasis, part II: celiac disease and role of a gluten-free diet. J Am Acad Dermatol 2014;71(2):350–358.
   PubMed Web of Science ®Google Scholar
• Van Heel DA, Franke L, Hunt KA, et al. A genome-wide association study for celiac disease identifies risk variants in the region harboring IL2 and IL21. Nat Genet 2007;39(7):827–829.
   PubMed Web of Science ®Google Scholar
• Ventura A, Magazzu G, Greco L. Duration of exposure to gluten and risk for autoimmune disorders in patients with celiac disease. SIGEP study group for autoimmune disorders in celiac disease. Gastroenterology 1999;117(2):297–303.
   PubMed Web of Science ®Google Scholar
• Tortora R, Capone P, De Stefano G, et al. Metabolic syndrome in patients with coeliac disease on a gluten-free diet. Aliment Pharmacol Ther 2015;41(4):352–359. Feb
   PubMed Web of Science ®Google Scholar
• Imperatore N, Tortora R, Testa A, et al. Proton pump inhibitors as risk factor for metabolic syndrome and hepatic steatosis in coeliac disease patients on gluten-free diet. J Gastroenterol. 2018;53(4):507–516.
   PubMed Web of Science ®Google Scholar
• Greaves M. Chronic urticaria. J Allergy Clin Immunol 2000;105(4):664–672.
   PubMed Web of Science ®Google Scholar
• Ludvigsson JF, Lindelöf B, Rashtak S, et al. Does urticaria risk increase in patients with celiac disease? A large population-based cohort study. Eur J Dermatol 2013;23(5):681–687.
   PubMed Web of Science ®Google Scholar
• Kolkhir P, Borzova E, Grattan C, et al. Autoimmune comorbidity in chronic spontaneous urticaria: a systematic review. Autoimmun Rev 2017;16(12):1196–1208.
   PubMed Web of Science ®Google Scholar
• Caminiti L, Passalacqua G, Magazzu G, et al. Chronic urticaria and associated coeliac disease in children: a case-control study. Pediatr Allergy Immunol 2005;16(5):428–432.
   PubMed Web of Science ®Google Scholar
• Alkhalifah A. Alopecia areata update. Dermatol Clin 2013;31(1):93–108.
   PubMed Web of Science ®Google Scholar
• Alkhalifah A, Alsantali A, Wang E, et al. Alopecia areata update: Part I. Clinical picture, histopathology, and pathogenesis. J Am Acad Dermatol 2010;62(2):177–188.
   PubMed Web of Science ®Google Scholar
• Corazza GR, Andreani ML, Venturo N, et al. Celiac disease and alopecia areata: report of a new association. Gastroenterology 1995;109(4):1333–1337.
   PubMed Web of Science ®Google Scholar
• Volta U, Bardazzi F, Zauli D, et al. Serological screening for coeliac disease in vitiligo and alopecia areata. Br J Dermatol 1997;136(5):801–802.
   PubMed Web of Science ®Google Scholar
• Hallaji Z, Akhyani M, Ehsani AH, et al. Prevalence of anti-gliadin antibody in patients with alopecia areata: a case-control study. Tehran Univ. Med. J 2011;68:738–742.
   Google Scholar
• Collin P, Reunala T. Recognition and management of the cutaneous manifestations of celiac disease: a guide for dermatologists. Am J Clin Dermatol 2003;4(1):13–20.
   PubMed Web of Science ®Google Scholar
• Spritz RA. The genetics of generalized vitiligo and associated autoimmune diseases. J Dermatol Sci 2006;41(1):3–10.
   PubMed Web of Science ®Google Scholar
• Passeron T, Ortonne JP. Physiopathology and genetics of vitiligo. J Autoimmun 2005;25:63–68.
   PubMed Web of Science ®Google Scholar
• Zabihollah S, Jamshid N, Farahnaz FN, Farinaz F. Vitiligo and autoantibodies of celiac disease. Int J Prev Med 2013;4(2):200–203.
   PubMedGoogle Scholar
• Rodríguez-García C, González-Hernández S, Pérez-Robayna N, et al. Repigmentation of vitiligo lesions in a child with celiac disease after a gluten-free diet. Pediatr Dermatol 2011;28(2):209–210.
   PubMed Web of Science ®Google Scholar
• Scully C, Carrozzo M. Oral mucosal disease: lichen planus. Br J Oral Maxillofac Surg 2008;46(1):15–21.
   PubMed Web of Science ®Google Scholar
• Cigic L, Gavic L, Simunic M, et al. Increased prevalence of celiac disease in patients with oral lichen planus. Clin Oral Investig 2015;19(3):627–635.
   PubMed Web of Science ®Google Scholar
• Pastore L, Carroccio A, Compilato D, et al. Oral manifestations of celiac disease. J Clin Gastroenterol 2008;42(3):224–232.
   PubMed Web of Science ®Google Scholar
• Rodrigo L, Beteta-Gorriti V, Alvarez N, et al. Cutaneous and mucosal manifestations associated with celiac disease. Nutrients 2018;10(7):800.
   Web of Science ®Google Scholar
• Nieri M, Tofani E, Defraia E, et al. Enamel defects and aphthous stomatitis in celiac and healthy subjects: systematic review and meta-analysis of controlled studies. J Dent 2017;65:1–10.
   PubMed Web of Science ®Google Scholar
• Meyers S, Dikman S, Spiera H, et al. Cutaneous vasculitis complicating coeliac disease. Gut 1981;22(1):61–64.
   PubMed Web of Science ®Google Scholar
• Elli L, Branchi F, Tomba C, et al. Diagnosis of gluten related disorders: Celiac disease, wheat allergy and non-celiac gluten sensitivity. Wjg. 2015;21(23):7110–7119.
   PubMed Web of Science ®Google Scholar
• Faina V, Paolino G, Bavastrelli M, et al. Classification of cutaneous manifestations in patients with non-celiac gluten sensitivity (NCGS) and wheat allergy (WA). J Am Acad Dermatol 2017;S0190-9622(17):32811–32816.
   Google Scholar
• Shahbazkhani B, Sadeghi A, Malekzadeh R, et al. Non-celiac gluten sensitivity has narrowed the spectrum of irritable bowel syndrome: a double-blind randomized placebo-controlled trial. Nutrients 2015;7(6):4542–4554.
   PubMed Web of Science ®Google Scholar
• Sapone A, Lammers KM, Casolaro V, et al. Divergence of gut permeability and mucosal immune gene expression in two gluten-associated conditions: celiac disease and gluten sensitivity. BMC Med 2011;9(1):23.
   PubMedGoogle Scholar
• Sapone A, Lammers KM, Mazzarella G, et al. Differential mucosal IL-17 expression in two gliadin-induced disorders: gluten sensitivity and the autoimmune enteropathy celiac disease. Int Arch Allergy Immunol 2010;152(1):75–80.
   PubMed Web of Science ®Google Scholar
• Biesiekierski JR, Newnham ED, Irving PM, et al. Gluten causes gastrointestinal symptoms in subjects without celiac disease: a double-blind randomized placebo-controlled trial. Am J Gastroenterol 2011;106(3):508–514.
   PubMed Web of Science ®Google Scholar
• Di Sabatino A, Volta U, Salvatore C, et al. Small amounts of gluten in subjects with suspected nonceliac gluten sensitivity: a randomized, double-blind, placebo controlled, cross-over trial. Clin Gastroenterol Hepatol 2015;13(9):1604–1612.
   PubMed Web of Science ®Google Scholar
• Elli L, Tomba C, Branchi F, et al. Evidence for the presence of non-celiac gluten sensitivity in patients with functional gastrointestinal symptoms: results from a multicenter randomized double-blind placebo-controlled gluten challenge. Nutrients 2016;8(2):84.
   PubMed Web of Science ®Google Scholar
• Zanini B, Baschè R, Ferraresi A, et al. Randomised clinical study: gluten challenge induces symptom recurrence in only a minority of patients who meet clinical criteria for non-celiac gluten sensitivity. Aliment Pharmacol Ther 2015;42(8):968–976.
   PubMed Web of Science ®Google Scholar
• Junker Y, Zeissig S, Kim S-J, et al. Wheat amylase trypsin inhibitors drive intestinal inflammation via activation of toll-like receptor 4. J Exp Med 2012;209(13):2395–2408.
   PubMed Web of Science ®Google Scholar
• Halmos EP, Power VA, Shepherd SJ, et al. Diet low in FODMAPs reduces symptoms of irritable bowel syndrome. Gastroenterology 2014;146(1):67–75.
   PubMed Web of Science ®Google Scholar
• Skodje GI, Sarna VK, Minelle IH, et al. Fructan, rather than gluten, induces symptoms in patients with self-reported non-celiac gluten sensitivity. Gastroenterology 2018;154(3):529–539.e2. doi: 10.1053/j.gastro.2017.10.040.
   PubMed Web of Science ®Google Scholar
• Bonciolini V, Bianchi B, Del Bianco E, et al. Cutaneous manifestations of non-celiac gluten sensitivity: clinical histological and immunopathological features. Nutrients 2015;7(9):7798–7805.
   PubMed Web of Science ®Google Scholar
• Daulatzai MA. Non-celiac gluten sensitivity triggers gut dysbiosis, neuroinflammation, gut-brain axis dysfunction, and vulnerability for dementia. CNS Neurol Disord Drug Targets 2015;14(1):110–131.
   PubMed Web of Science ®Google Scholar
• Tonutti E, Bizzaro N. Diagnosis and classification of celiac disease and gluten sensitivity. Autoimmun Rev 2014;13(4–5):472–476.
   PubMed Web of Science ®Google Scholar
• Francavilla R, Cristofori F, Castellaneta S, et al. Clinical, serologic, and histologic features of gluten sensitivity in children. J Pediatr. 2014;164(3):463–467.
   PubMed Web of Science ®Google Scholar
• Volta U, Bardella MT, Calabrò A, et al. Study group for non-celiac gluten sensitivity. An Italian prospective multicenter survey on patients suspected of having non-celiac gluten sensitivity. BMC Med 2014;12:85.
   PubMed Web of Science ®Google Scholar
• Catassi C, Elli L, Bonaz B, et al. Diagnosis of non-celiac gluten sensitivity (NCGS): the Salerno experts' criteria. Nutrients 2015;7(6):4966–4977.
   PubMed Web of Science ®Google Scholar