Coeliac disease is often accompanied by extraintestinal manifestations, which can be the result of aberrant immune responses but also malabsorption
These concurrent conditions can affect various systems and organs, and include manifestations in the skin, musculoskeletal and central nervous system
Anaemia, osteoporosis, dermatitis herpetiformis and gluten ataxia are among the most commonly seen characteristics
In the paediatric population, coeliac disease can lead to severe growth disorders, such as short stature and delayed puberty due to hypogonadism
Coeliac disease is a common disorder that can arise at any age and typically presents with a broad spectrum of symptoms. The disease is thought to be underdiagnosed, in part owing to the fact that coeliac disease is often characterized by associated conditions and extraintestinal manifestations that can misdirect and impede diagnosis. Some of these manifestations are direct consequences of autoimmunity, such as dermatitis herpetiformis or gluten ataxia, whereas others are indirectly related to inflammation and/or malabsorption including anaemia, osteoporosis, short stature and delayed puberty. Any organ from the central nervous system to joints, liver or teeth can be affected. In some cases, extraintestinal symptoms are the only clinical manifestations of coeliac disease or occur in conjunction with diarrhoea and malabsorptive symptoms. An increased awareness among medical practitioners of the variety of extraintestinal manifestations of coeliac disease is essential to improve diagnosis and treatment.
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Fasano, A. & Catassi, C. Current approaches to diagnosis and treatment of celiac disease: an evolving spectrum. Gastroenterology 120, 636–651 (2001).
Green, P. H. & Cellier, C. Celiac disease. N. Engl. J. Med. 357, 1731–1743 (2007).
Reilly, N. R., Fasano, A. & Green, P. H. Presentation of celiac disease. Gastrointest. Endosc. Clin. N. Am. 22, 613–621 (2012).
Tersigni, C. et al. Celiac disease and reproductive disorders: meta-analysis of epidemiologic associations and potential pathogenic mechanisms. Hum. Reprod. Update 20, 582–593 (2014).
Castillo, N. E., Theethira, T. G. & Leffler, D. A. The present and the future in the diagnosis and management of celiac disease. Gastroenterol. Rep. (Oxf.) 3, 3–11 (2015).
Reilly, N. R. & Green, P. H. Epidemiology and clinical presentations of celiac disease. Semin. Immunopathol. 34, 473–478 (2012).
Bhattacharya, M., Kapoor, S. & Dubey, A. P. Celiac disease presentation in a tertiary referral centre in India: current scenario. Indian J. Gastroenterol. 32, 98–102 (2013).
Bai, J. C. et al. World Gastroenterology Organisation global guidelines on celiac disease. J. Clin. Gastroenterol. 47, 121–126 (2013).
Volta, U., Caio, G., Stanghellini, V. & De Giorgio, R. The changing clinical profile of celiac disease: a 15-year experience (1998–2012) in an Italian referral center. BMC Gastroenterol. 14, 194 (2014).
Fasano, A. Surprises from celiac disease. Sci. Am. 301, 54–61 (2009).
Lionetti, E. & Catassi, C. New clues in celiac disease epidemiology, pathogenesis, clinical manifestations, and treatment. Int. Rev. Immunol. 30, 219–231 (2011).
Abadie, V., Sollid, L. M., Barreiro, L. B. & Jabri, B. Integration of genetic and immunological insights into a model of celiac disease pathogenesis. Annu. Rev. Immunol. 29, 493–525 (2011).
Antvorskov, J. C., Josefsen, K., Engkilde, K., Funda, D. P. & Buschard, K. Dietary gluten and the development of type 1 diabetes. Diabetologia 57, 1770–1780 (2014).
Anjum, N., Baker, P. N., Robinson, N. J. & Aplin, J. D. Maternal celiac disease autoantibodies bind directly to syncytiotrophoblast and inhibit placental tissue transglutaminase activity. Reprod. Biol. Endocrinol. 7, 16 (2009).
Hadjivassiliou, M. et al. Autoantibodies in gluten ataxia recognize a novel neuronal transglutaminase. Ann. Neurol. 64, 332–343 (2008).
Halfdanarson, T. R., Litzow, M. R. & Murray, J. A. Hematologic manifestations of celiac disease. Blood 109, 412–421 (2007).
Rampertab, S. D., Pooran, N., Brar, P., Singh, P. & Green, P. H. Trends in the presentation of celiac disease. Am. J. Med. 119, 355.e9–e14 (2006).
Reilly, N. R. et al. Celiac disease in normal-weight and overweight children: clinical features and growth outcomes following a gluten-free diet. J. Pediatr. Gastroenterol. Nutr. 53, 528–531 (2011).
Harper, J. W., Holleran, S. F., Ramakrishnan, R., Bhagat, G. & Green, P. H. Anemia in celiac disease is multifactorial in etiology. Am. J. Hematol. 82, 996–1000 (2007).
Bergamaschi, G. et al. Anemia of chronic disease and defective erythropoietin production in patients with celiac disease. Haematologica 93, 1785–1791 (2008).
Abu Daya, H., Lebwohl, B., Lewis, S. K. & Green, P. H. Celiac disease patients presenting with anemia have more severe disease than those presenting with diarrhea. Clin. Gastroenterol. Hepatol. 11, 1472–1477 (2013).
Singh, P., Arora, S. & Makharia, G. K. Presence of anemia in patients with celiac disease suggests more severe disease. Indian J. Gastroenterol. 33, 161–164 (2014).
Kavimandan, A. et al. Prevalence of celiac disease in nutritional anemia at a tertiary care center. Indian J. Gastroenterol. 33, 114–118 (2014).
Grisolano, S. W. et al. The usefulness of routine small bowel biopsies in evaluation of iron deficiency anemia. J. Clin. Gastroenterol. 38, 756–760 (2004).
Karnam, U. S., Felder, L. R. & Raskin, J. B. Prevalence of occult celiac disease in patients with iron-deficiency anemia: a prospective study. South Med. J. 97, 30–34 (2004).
Murray, J. A. et al. Association between celiac disease and iron deficiency in Caucasians, but not non-Caucasians. Clin. Gastroenterol. Hepatol. 11, 808–814 (2013).
Goddard, A. F., James, M. W., McIntyre, A. S. & Scott, B. B. Guidelines for the management of iron deficiency anaemia. Gut 60, 1309–1316 (2011).
Rubio-Tapia, A. et al. ACG clinical guidelines: diagnosis and management of celiac disease. Am. J. Gastroenterol. 108, 656–676 (2013).
Smukalla, S., Lebwohl, B., Mears, J. G., Leslie, L. A. & Green, P. H. How often do hematologists consider celiac disease in iron-deficiency anemia? Results of a national survey. Clin. Adv. Hematol. Oncol. 12, 100–105 (2014).
Abu Daya, H., Lebwohl, B., Smukalla, S., Lewis, S. K. & Green, P. H. Utilizing HDL levels to improve detection of celiac disease in patients with iron deficiency anemia. Am. J. Gastroenterol. 109, 769–770 (2014).
Ciacci, C. et al. Low plasma cholesterol: a correlate of nondiagnosed celiac disease in adults with hypochromic anemia. Am. J. Gastroenterol. 94, 1888–1891 (1999).
Bianchi, M. L. & Bardella, M. T. Bone in celiac disease. Osteoporos. Int. 19, 1705–1716 (2008).
Mazure, R. et al. Bone mineral affection in asymptomatic adult patients with celiac disease. Am. J. Gastroenterol. 89, 2130–2134 (1994).
Valdimarsson, T., Toss, G., Ross, I., Lofman, O. & Strom, M. Bone mineral density in coeliac disease. Scand. J. Gastroenterol. 29, 457–461 (1994).
Lebwohl, B., Michaelsson, K., Green, P. H. & Ludvigsson, J. F. Persistent mucosal damage and risk of fracture in celiac disease. J. Clin. Endocrinol. Metab. 99, 609–616 (2014).
Thomason, K., West, J., Logan, R. F., Coupland, C. & Holmes, G. K. Fracture experience of patients with coeliac disease: a population based survey. Gut 52, 518–522 (2003).
Logan, R. & West, J. Risk of fracture in coeliac disease. Gut 52, 1532 (2003).
Jafri, M. R. et al. Long-term fracture risk in patients with celiac disease: a population-based study in Olmsted County, Minnesota. Dig. Dis. Sci. 53, 964–971 (2008).
Moreno, M. L. et al. Stratification of bone fracture risk in patients with celiac disease. Clin. Gastroenterol. Hepatol. 2, 127–134 (2004).
Gonzalez, D. et al. Is it necessary to screen for celiac disease in postmenopausal osteoporotic women? Calcif. Tissue Int. 71, 141–144 (2002).
Di Stefano, M. et al. Bone mass and metabolism in dermatitis herpetiformis. Dig. Dis. Sci. 44, 2139–2143 (1999).
Corazza, G. R. et al. Bone mass and metabolism in patients with celiac disease. Gastroenterology 109, 122–128 (1995).
Larussa, T. et al. Bone mineralization in celiac disease. Gastroenterol. Res. Pract. 2012, 198025 (2012).
Sugai, E. et al. Bone-specific antibodies in sera from patients with celiac disease: characterization and implications in osteoporosis. J. Clin. Immunol. 22, 353–362 (2002).
Riches, P. L. et al. Osteoporosis associated with neutralizing autoantibodies against osteoprotegerin. N. Engl. J. Med. 361, 1459–1465 (2009).
Meyer, D., Stavropolous, S., Diamond, B., Shane, E. & Green, P. H. Osteoporosis in a north american adult population with celiac disease. Am. J. Gastroenterol. 96, 112–119 (2001).
Kumar, M. et al. Effect of zoledronic acid on bone mineral density in patients of celiac disease: a prospective, randomized, pilot study. Indian J. Med. Res. 138, 882–887 (2013).
Ghozzi, M. et al. Screening for celiac disease, by endomysial antibodies, in patients with unexplained articular manifestations. Rheumatol. Int. 34, 637–642 (2014).
Bourne, J. T. et al. Arthritis and coeliac disease. Ann. Rheum. Dis. 44, 592–598 (1985).
Lepore, L. et al. Prevalence of celiac disease in patients with juvenile chronic arthritis. J. Pediatr. 129, 311–313 (1996).
Maki, M. et al. Reticulin antibody, arthritis, and coeliac disease in children. Lancet 1, 479–480 (1988).
George, E. K. et al. Juvenile chronic arthritis and coeliac disease in The Netherlands. Clin. Exp. Rheumatol. 14, 571–575 (1996).
Usai, P. et al. Adult celiac disease is frequently associated with sacroiliitis. Dig. Dis. Sci. 40, 1906–1908 (1995).
Lubrano, E. et al. The arthritis of coeliac disease: prevalence and pattern in 200 adult patients. Br. J. Rheumatol. 35, 1314–1318 (1996).
Marks, J., Shuster, S. & Watson, A. J. Small-bowel changes in dermatitis herpetiformis. Lancet 2, 1280–1282 (1966).
Zone, J. J. Skin manifestations of celiac disease. Gastroenterology 128, S87–S91 (2005).
Bolotin, D. & Petronic-Rosic, V. Dermatitis herpetiformis. Part, I. Epidemiology, pathogenesis, and clinical presentation. J. Am. Acad. Dermatol. 64, 1017–1024 (2011).
Bolotin, D. & Petronic-Rosic, V. Dermatitis herpetiformis. Part, I. I. Diagnosis, management, and prognosis. J. Am. Acad. Dermatol. 64, 1027–1033 (2011).
Jaskowski, T. D. et al. IgA anti-epidermal transglutaminase antibodies in dermatitis herpetiformis and pediatric celiac disease. J. Invest. Dermatol. 129, 2728–2730 (2009).
Leffler, D. A. et al. Etiologies and predictors of diagnosis in nonresponsive celiac disease. Clin. Gastroenterol. Hepatol. 5, 445–450 (2007).
Ludvigsson, J. F., Lindelof, B., Zingone, F. & Ciacci, C. Psoriasis in a nationwide cohort study of patients with celiac disease. J. Invest. Dermatol. 131, 2010–2016 (2011).
Michaelsson, G. et al. Psoriasis patients with antibodies to gliadin can be improved by a gluten-free diet. Br. J. Dermatol. 142, 44–51 (2000).
Woo, W. K. et al. Coeliac disease-associated antibodies correlate with psoriasis activity. Br. J. Dermatol. 151, 891–894 (2004).
Buxton, J. L. et al. Multiple measures of adiposity are associated with mean leukocyte telomere length in the northern Finland birth cohort 1966. PLoS One 9, e99133 (2014).
Collin, P. & Reunala, T. Recognition and management of the cutaneous manifestations of celiac disease: a guide for dermatologists. Am. J. Clin. Dermatol. 4, 13–20 (2003).
Theethira, T. G., Dennis, M. & Leffler, D. A. Nutritional consequences of celiac disease and the gluten-free diet. Expert Rev. Gastroenterol. Hepatol. 8, 123–129 (2014).
Corazza, G. R. et al. Celiac disease and alopecia areata: report of a new association. Gastroenterology 109, 1333–1337 (1995).
Bardella, M. T. et al. Alopecia areata and coeliac disease: no effect of a gluten-free diet on hair growth. Dermatology 200, 108–110 (2000).
Hadjivassiliou, M. et al. Gluten ataxia in perspective: epidemiology, genetic susceptibility and clinical characteristics. Brain 126, 685–691 (2003).
Hadjivassiliou, M. et al. Clinical, radiological, neurophysiological, and neuropathological characteristics of gluten ataxia. Lancet 352, 1582–1585 (1998).
Abele, M. et al. The aetiology of sporadic adult-onset ataxia. Brain 125, 961–968 (2002).
Cooke, W. T. & Smith, W. T. Neurological disorders associated with adult coeliac disease. Brain 89, 683–722 (1966).
Hadjivassiliou, M. et al. The humoral response in the pathogenesis of gluten ataxia. Neurology 58, 1221–1226 (2002).
Korponay-Szabo, I. R. et al. In vivo targeting of intestinal and extraintestinal transglutaminase 2 by coeliac autoantibodies. Gut 53, 641–648 (2004).
Hadjivassiliou, M. et al. Autoantibody targeting of brain and intestinal transglutaminase in gluten ataxia. Neurology 66, 373–377 (2006).
Boscolo, S. et al. Gluten ataxia: passive transfer in a mouse model. Ann. N. Y. Acad. Sci. 1107, 319–328 (2007).
Hadjivassiliou, M., Sanders, D. S., Woodroofe, N., Williamson, C. & Grunewald, R. A. Gluten ataxia. Cerebellum 7, 494–498 (2008).
Centers for Disease Control and Prevention. Autism Spectrum Disorder (ASD). Prevalence. [online], (2015).
Harrington, J. W. & Allen, K. The clinician's guide to autism. Pediatr. Rev. 35, 62–78; quiz 78 (2014).
Genuis, S. J. & Bouchard, T. P. Celiac disease presenting as autism. J. Child. Neurol. 25, 114–119 (2010).
Barcia, G., Posar, A., Santucci, M. & Parmeggiani, A. Autism and coeliac disease. J. Autism Dev. Disord. 38, 407–408 (2008).
Black, C., Kaye, J. A. & Jick, H. Relation of childhood gastrointestinal disorders to autism: nested case-control study using data from the UK General Practice Research Database. BMJ 325, 419–421 (2002).
Pavone, L., Fiumara, A., Bottaro, G., Mazzone, D. & Coleman, M. Autism and celiac disease: failure to validate the hypothesis that a link might exist. Biol. Psychiatry 42, 72–75 (1997).
Batista, I. C. et al. Autism spectrum disorder and celiac disease: no evidence for a link. Arq. Neuropsiquiatr. 70, 28–33 (2012).
Lau, N. M. et al. Markers of celiac disease and gluten sensitivity in children with autism. PLoS ONE 8, e66155 (2013).
Ludvigsson, J. F., Reichenberg, A., Hultman, C. M. & Murray, J. A. A nationwide study of the association between celiac disease and the risk of autistic spectrum disorders. JAMA Psychiatry 70, 1224–1230 (2013).
Dohan, F. C. Is celiac disease a clue to the pathogenesis of schizophrenia? Ment. Hyg. 53, 525–529 (1969).
Vlissides, D. N., Venulet, A. & Jenner, F. A. A double-blind gluten-free/gluten-load controlled trial in a secure ward population. Br. J. Psychiatry 148, 447–452 (1986).
Potkin, S. G. et al. Wheat gluten challenge in schizophrenic patients. Am. J. Psychiatry 138, 1208–1211 (1981).
Storms, L. H., Clopton, J. M. & Wright, C. Effects of gluten on schizophrenics. Arch. Gen. Psychiatry 39, 323–327 (1982).
Cascella, N. G. et al. Prevalence of celiac disease and gluten sensitivity in the United States clinical antipsychotic trials of intervention effectiveness study population. Schizophr. Bull. 37, 94–100 (2011).
Samaroo, D. et al. Novel immune response to gluten in individuals with schizophrenia. Schizophr. Res. 118, 248–255 (2010).
Cascella, N. G. et al. Increased prevalence of transglutaminase 6 antibodies in sera from schizophrenia patients. Schizophr. Bull. 39, 867–871 (2013).
Dickerson, F. et al. Markers of gluten sensitivity and celiac disease in recent-onset psychosis and multi-episode schizophrenia. Biol. Psychiatry 68, 100–104 (2010).
Jackson, J. R., Eaton, W. W., Cascella, N. G., Fasano, A. & Kelly, D. L. Neurologic and psychiatric manifestations of celiac disease and gluten sensitivity. Psychiatr. Q. 83, 91–102 (2012).
Garud, S. et al. Interaction between psychiatric and autoimmune disorders in coeliac disease patients in the Northeastern United States. Aliment. Pharmacol. Ther. 29, 898–905 (2009).
Shen, T. C. et al. Peripheral neuropathic symptoms in celiac disease and inflammatory bowel disease. J. Clin. Neuromuscul. Dis. 13, 137–145 (2012).
Iughetti, L. et al. Endocrine aspects of coeliac disease. J. Pediatr. Endocrinol. Metab. 16, 805–818 (2003).
Queiroz, M. S., Nery, M., Cancado, E. L., Gianella-Neto, D. & Liberman, B. Prevalence of celiac disease in Brazilian children of short stature. Braz. J. Med. Biol. Res. 37, 55–60 (2004).
Hyer, W., Cotterill, A. M. & Savage, M. O. Common causes of short stature detectable by a height surveillance programme. J. Med. Screen. 2, 150–153 (1995).
Locuratolo, N. et al. The circulating insulin-like growth factor system in children with coeliac disease: an additional marker for disease activity. Diabetes Metab. Res. Rev. 15, 254–260 (1999).
Peracchi, M. et al. Abnormal growth hormone responsiveness to stimuli in women with active celiac sprue. Am. J. Gastroenterol. 87, 580–583 (1992).
Meazza, C. et al. Short stature in children with coeliac disease. Pediatr. Endocrinol. Rev. 6, 457–463 (2009).
Bona, G., Marinello, D. & Oderda, G. Mechanisms of abnormal puberty in coeliac disease. Horm. Res. 57, 63–65 (2002).
Volta, U. et al. Coeliac disease hidden by cryptogenic hypertransaminasaemia. Lancet 352, 26–29 (1998).
Bardella, M. T. et al. Chronic unexplained hypertransaminasemia may be caused by occult celiac disease. Hepatology 29, 654–657 (1999).
Bardella, M. T. et al. Prevalence of hypertransaminasemia in adult celiac patients and effect of gluten-free diet. Hepatology 22, 833–836 (1995).
Bonamico, M. et al. [Hepatic damage in celiac disease in children]. Minerva Pediatr. 38, 959–962 (1986).
Vajro, P., Paolella, G., Pisano, P. & Maggiore, G. Hypertransaminasemia and coeliac disease. Aliment. Pharmacol. Ther. 35, 202–203; author reply 203–204 (2012).
Sainsbury, A., Sanders, D. S. & Ford, A. C. Meta-analysis: coeliac disease and hypertransaminasaemia. Aliment. Pharmacol. Ther. 34, 33–40 (2011).
Ludvigsson, J. F., Elfstrom, P., Broome, U., Ekbom, A. & Montgomery, S. M. Celiac disease and risk of liver disease: a general population-based study. Clin. Gastroenterol. Hepatol. 5, 63–69 (2007).
Castillo, N. et al. Prevalence of abnormal liver function tests in celiac disease and the effect of the gluten free diet in the US population. Am. J. Gastroenterol. http://dx.doi.org/10.1038/ajg.2015.192.
Kaukinen, K. et al. Celiac disease in patients with severe liver disease: gluten-free diet may reverse hepatic failure. Gastroenterology 122, 881–888 (2002).
Peters, U., Askling, J., Gridley, G., Ekbom, A. & Linet, M. Causes of death in patients with celiac disease in a population-based Swedish cohort. Arch. Intern. Med. 163, 1566–1572 (2003).
Silvester, J. A. & Rashid, M. Long-term follow-up of individuals with celiac disease: an evaluation of current practice guidelines. Can. J. Gastroenterol. 21, 557–564 (2007).
Pietzak, M. M. Follow-up of patients with celiac disease: achieving compliance with treatment. Gastroenterology 128, S135–S141 (2005).
Rubio-Tapia, A. & Murray, J. A. The liver in celiac disease. Hepatology 46, 1650–1658 (2007).
Ferguson, A., Hutton, M. M., Maxwell, J. D. & Murray, D. Adult coeliac disease in hyposplenic patients. Lancet 1, 163–164 (1970).
Di Sabatino, A., Brunetti, L., Carnevale Maffe, G., Giuffrida, P. & Corazza, G. R. Is it worth investigating splenic function in patients with celiac disease? World J. Gastroenterol. 19, 2313–2318 (2013).
Magalotti, D. et al. Splanchnic haemodynamics in patients with coeliac disease: effects of a gluten-free diet. Dig. Liver Dis. 35, 262–268 (2003).
Ludvigsson, J. F., Olen, O., Bell, M., Ekbom, A. & Montgomery, S. M. Coeliac disease and risk of sepsis. Gut 57, 1074–1080 (2008).
Husby, S. et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition guidelines for the diagnosis of coeliac disease. J. Pediatr. Gastroenterol. Nutr. 54, 136–160 (2012).
Hendrickx, G. F., Somers, K. & Vandenplas, Y. Lane-Hamilton syndrome: case report and review of the literature. Eur. J. Pediatr. 170, 1597–1602 (2011).
Welander, A., Prutz, K. G., Fored, M. & Ludvigsson, J. F. Increased risk of end-stage renal disease in individuals with coeliac disease. Gut 61, 64–68 (2012).
Ludvigsson, J. F. et al. Coeliac disease and risk of renal disease—a general population cohort study. Nephrol. Dial. Transplant. 21, 1809–1815 (2006).
Ismail-Beigi, F. et al. Effect of intensive treatment of hyperglycaemia on microvascular outcomes in type 2 diabetes: an analysis of the ACCORD randomised trial. Lancet 376, 419–430 (2010).
Whorwell, P. J., Alderson, M. R., Foster, K. J. & Wright, R. Death from ischaemic heart-disease and malignancy in adult patients with coeliac disease. Lancet 2, 113–114 (1976).
West, J., Logan, R. F., Card, T. R., Smith, C. & Hubbard, R. Risk of vascular disease in adults with diagnosed coeliac disease: a population-based study. Aliment. Pharmacol. Ther. 20, 73–79 (2004).
Wolf-Maier, K. et al. Hypertension prevalence and blood pressure levels in 6 European countries, Canada, and the United States. JAMA 289, 2363–2369 (2003).
Kabbani, T. A. et al. Body mass index and the risk of obesity in coeliac disease treated with the gluten-free diet. Aliment. Pharmacol. Ther. 35, 723–729 (2012).
Frustaci, A. et al. Celiac disease associated with autoimmune myocarditis. Circulation 105, 2611–2618 (2002).
Addolorato, G. et al. Regional cerebral hypoperfusion in patients with celiac disease. Am. J. Med. 116, 312–317 (2004).
Emilsson, L., Smith, J. G., West, J., Melander, O. & Ludvigsson, J. F. Increased risk of atrial fibrillation in patients with coeliac disease: a nationwide cohort study. Eur. Heart J. 32, 2430–2437 (2011).
Patel, R. S., Johlin, F. C., Jr & Murray, J. A. Celiac disease and recurrent pancreatitis. Gastrointest. Endosc. 50, 823–827 (1999).
Sadr-Azodi, O., Sanders, D. S., Murray, J. A. & Ludvigsson, J. F. Patients with celiac disease have an increased risk for pancreatitis. Clin. Gastroenterol. Hepatol. 10, 1136–1142 (2012).
Rodrigo, L. et al. [Relapsing acute pancreatitis associated with gluten enteropathy. Clinical, laboratory, and evolutive characteristics in thirty-four patients]. Rev. Esp. Enferm. Dig. 100, 746–751 (2008).
Abdulkarim, A. S., Burgart, L. J., See, J. & Murray, J. A. Etiology of nonresponsive celiac disease: results of a systematic approach. Am. J. Gastroenterol. 97, 2016–2021 (2002).
Walkowiak, J. & Herzig, K. H. Fecal elastase-1 is decreased in villous atrophy regardless of the underlying disease. Eur. J. Clin. Invest. 31, 425–430 (2001).
Shah, S. & Leffler, D. Celiac disease: an underappreciated issue in women's health. Womens Health (Lond. Engl.) 6, 753–766 (2010).
De Felice, K. M. & Kane, S. V. Inflammatory bowel disease in women of reproductive age. Expert Rev. Gastroenterol. Hepatol. 8, 417–425 (2014).
Rashid, M., Zarkadas, M., Anca, A. & Limeback, H. Oral manifestations of celiac disease: a clinical guide for dentists. J. Mich. Dent. Assoc. 93, 42–46 (2011).
Cheng, J., Malahias, T., Brar, P., Minaya, M. T. & Green, P. H. The association between celiac disease, dental enamel defects, and aphthous ulcers in a United States cohort. J. Clin. Gastroenterol. 44, 191–194 (2009).
Pastore, L. et al. Oral manifestations of celiac disease. J. Clin. Gastroenterol. 42, 224–232 (2008).
Losowsky, M. S. A history of coeliac disease. Dig. Dis. 26, 112–120 (2008).
D.A.L. has received funding from Alba Therapeutics, Alvine Pharmaceuticals, Coronado Bioscience, Inova diagnostics, Ironwood Pharmaceuticals, Sidney Frank Foundation and Shire Pharmaceuticals. P.H.R.G. has received funding from Alba Therapeutics, Alvine Pharmaceuticals and Immusan. A.F. has received funding from Alba Therapeutics, Inova diagnostics, Mead Johnson Nutrition and Pfizer Pharmaceutical.
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Leffler, D., Green, P. & Fasano, A. Extraintestinal manifestations of coeliac disease. Nat Rev Gastroenterol Hepatol 12, 561–571 (2015). https://doi.org/10.1038/nrgastro.2015.131
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