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1
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Bold J. Gluten and its main food sources and other components of grains that may impact on health. GLUTEN-RELATED DISORDERS 2022:33-48. [DOI: 10.1016/b978-0-12-821846-4.00007-3] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/04/2025]
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Quddusi FI, Youssef MJ, Davis DMR. Dermatologic Manifestations of Systemic Diseases in Childhood. Pediatr Rev 2021; 42:655-671. [PMID: 34850179 DOI: 10.1542/pir.2020-000679] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/24/2022]
Affiliation(s)
| | - Molly J Youssef
- Department of Pediatric and Adolescent Medicine.,Department of Dermatology, Mayo Clinic, Rochester, MN
| | - Dawn Marie R Davis
- Department of Pediatric and Adolescent Medicine.,Department of Dermatology, Mayo Clinic, Rochester, MN
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3
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Lavery HA. Fad Diets Past and Present - Including Taurine for Psoriasis, Diet Therapy for Atopic Dermatitis and the Role of Elimination Diets. Clin Dermatol 2021; 40:193-197. [PMID: 34808245 DOI: 10.1016/j.clindermatol.2021.11.003] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/17/2022]
Abstract
The impact of diets and foods on cutaneous afflictions has never been a moot point. The number of enquiries from patients and the wider public about how certain foods have impacted upon, or indeed, caused their skin eruption is increasing. While this inquisition is at the forefront of people's and physicians mind in today's modern practice, this has long been a discussion in the scientific world. Metchnikoff alluded to this at the turn of the 20th century. How foods and certain dietary programs impact on diseases has been postulated, although there is still more to learn, despite the patient's advocacy for a particular dietary regime. The study of the role of the microbiome is increasing. Gut dysbiosis, along with the interaction of the gastrointestinal tract, skin, and brain - gut-skin-brain axis is discussed . The role and impact of neuroendocrine transmitters and the skin are explored.
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Görög A, Antiga E, Caproni M, Cianchini G, De D, Dmochowski M, Dolinsek J, Drenovska K, Feliciani C, Hervonen K, Lakos Jukic I, Kinyó Á, Koltai T, Korponay-Szabó I, Marzano AV, Patsatsi A, Rose C, Salmi T, Schmidt E, Setterfield J, Shahid M, Sitaru C, Uzun S, Valitutti F, Vassileva S, Yayli S, Sárdy M. S2k guidelines (consensus statement) for diagnosis and therapy of dermatitis herpetiformis initiated by the European Academy of Dermatology and Venereology (EADV). J Eur Acad Dermatol Venereol 2021; 35:1251-1277. [PMID: 34004067 DOI: 10.1111/jdv.17183] [Citation(s) in RCA: 30] [Impact Index Per Article: 7.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/26/2020] [Accepted: 01/14/2021] [Indexed: 12/15/2022]
Abstract
INTRODUCTION Dermatitis herpetiformis (DH) is a chronic, pruritic, gluten-induced skin disorder characterized by subepidermal granular IgA deposition and a variable degree of enteropathy identical to that seen in coeliac disease. So far, there has been no European consensus about the management of DH. METHODS The guidelines were created by small subgroups of a guideline committee consisting of 26 specialists from various medical fields and one patients' representative. The members of the committee then discussed the guidelines and voted for the final version at two consensus meetings. The guidelines were developed under the support of the European Academy of Dermatology and Venereology (EADV) and in collaboration with the European Dermatology Forum (EDF). RESULTS The guidelines summarize evidence-based and expert-based recommendations (S2 level) for the management of DH (see Appendix). CONCLUSION These guidelines will improve the quality of management of DH and support dermatologists in their diagnostic and therapeutic decisions.
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Affiliation(s)
- A Görög
- Department of Dermatology, Venereology and Dermatooncology, Semmelweis University, Budapest, Hungary
| | - E Antiga
- Section of Dermatology, Department of Health Sciences, University of Florence, Florence, Italy
| | - M Caproni
- Rare Diseases Unit, Section of Dermatology, Department of Health Sciences, USL Toscana Centro, European Reference Network-Skin Member, University of Florence, Florence, Italy
| | - G Cianchini
- Department of Dermatology, Cristo Re Hospital, Rome, Italy
| | - D De
- Department of Dermatology, Postgraduate Institute of Medical Education Research, Chandigarh, India
| | - M Dmochowski
- Autoimmune Blistering Dermatoses Section, Department of Dermatology, Poznan University of Medical Sciences, Poznań, Poland
| | - J Dolinsek
- Gastroenterology Unit, Department of Pediatrics, University Medical Center Maribor, Maribor, Slovenia.,Medical Faculty, University of Maribor, Maribor, Slovenia
| | - K Drenovska
- Department of Dermatology and Venereology, Medical University, Sofia, Bulgaria
| | - C Feliciani
- Dermatology Unit Azienda Ospedaliero - Universitaria, Università di Parma, Parma, Italy
| | - K Hervonen
- Coeliac Disease Research Center, Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland.,Department of Dermatology, Tampere University Hospital, Tampere, Finland
| | - I Lakos Jukic
- Department of Dermatology and Venereology, University Hospital Center Zagreb, School of Medicine University of Zagreb, Zagreb, Croatia
| | - Á Kinyó
- Department of Dermatology, Venereology and Oncodermatology, University of Pécs Medical School, Pécs, Hungary
| | - T Koltai
- Association of European Coeliac Societies, Brussels, Belgium.,Hungarian Coeliac Society, Budapest, Hungary
| | - I Korponay-Szabó
- Coeliac Disease Centre, Heim Pál National Paediatric Institute, Budapest, Hungary.,Faculty of Medicine, Institute of Paediatrics, University of Debrecen, Debrecen, Hungary
| | - A V Marzano
- Dermatology Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy.,Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy
| | - A Patsatsi
- Autoimmune Bullous Diseases Unit, 2nd Dermatology Department, Aristotle University School of Medicine, Thessaloniki, Greece
| | - C Rose
- Dermatopathology Laboratory, Lübeck, Germany.,German Coeliac Disease Society e. V., Stuttgart, Germany
| | - T Salmi
- Coeliac Disease Research Center, Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland.,Department of Dermatology, Tampere University Hospital, Tampere, Finland
| | - E Schmidt
- Department of Dermatology, University of Lübeck, Lübeck, Germany.,Lübeck Institute of Experimental Dermatology (LIED), University of Lübeck, Lübeck, Germany
| | - J Setterfield
- St John's Institute of Dermatology, Guy's and St Thomas' NHS Foundation Trust, London, UK.,Centre for Host Microbiome Interactions, Faculty of Dentistry Oral & Craniofacial Sciences, King's College London, London, UK
| | - M Shahid
- Department of Dermatology and Venereology, Medical University, Sofia, Bulgaria
| | - C Sitaru
- Department of Dermatology, Faculty of Medicine, Medical Center - University of Freiburg, Freiburg, Germany.,BIOSS Centre for Biological Signalling, University of Freiburg, Freiburg, Germany
| | - S Uzun
- Department of Dermatology, Akdeniz University Faculty of Medicine, Antalya, Turkey
| | - F Valitutti
- Pediatric Unit, AOU San Giovanni di Dio e Ruggi d'Aragona, Salerno, Italy
| | - S Vassileva
- Department of Dermatology and Venereology, Medical University, Sofia, Bulgaria
| | - S Yayli
- Department of Dermatology, Karadeniz Technical University Faculty of Medicine, Trabzon, Turkey
| | - M Sárdy
- Department of Dermatology, Venereology and Dermatooncology, Semmelweis University, Budapest, Hungary.,Department of Dermatology and Allergy, University Hospital of LMU, Munich, Germany
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Abstract
Dermatitis herpetiformis (DH), presenting with an intense itch and blistering symmetrical rash, typically on the elbows, knees, and buttocks, is a cutaneous manifestation of celiac disease. Though overt gastrointestinal symptoms are rare, three-fourths of patients with DH have villous atrophy in the small bowel, and the rest have celiac-type inflammatory changes. DH affects mostly adults and slightly more males than females. The mean age at onset is about 50 years. DH diagnosis is confirmed by showing granular immunoglobulin A deposits in the papillary dermis. The DH autoantigen, transglutaminase 3, is deposited at the same site in tightly bound immune complexes. At present, the DH-to-celiac disease prevalence is 1:8. The incidence of DH is decreasing, whereas that of celiac disease is increasing, probably because of improved diagnostics. In DH, the treatment of choice for all patients is a gluten-free diet (GFD) in which uncontaminated oats are allowed. At onset, most patients need additional dapsone to rapidly control the rash and itching. Dapsone can be stopped after a mean of 2 years, and a strict lifelong GFD alone is required. Dietary adherence offers an excellent long-term prognosis for patients with DH, with a normal quality of life and all-cause mortality.
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Affiliation(s)
- Timo Reunala
- Celiac Disease Research Center, Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland.
| | - Kaisa Hervonen
- Celiac Disease Research Center, Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland
- Department of Dermatology, Tampere University Hospital, Tampere, Finland
| | - Teea Salmi
- Celiac Disease Research Center, Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland
- Department of Dermatology, Tampere University Hospital, Tampere, Finland
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6
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Kemppainen E, Salmi T, Lindfors K. Missing Insight Into T and B Cell Responses in Dermatitis Herpetiformis. Front Immunol 2021; 12:657280. [PMID: 33854513 PMCID: PMC8039136 DOI: 10.3389/fimmu.2021.657280] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/22/2021] [Accepted: 03/12/2021] [Indexed: 12/18/2022] Open
Abstract
Dermatitis herpetiformis is a cutaneous form of celiac disease manifesting as an itching rash typically on the elbows, knees and buttocks. It is driven by the ingestion of gluten-containing cereals and characterized by granular deposits of immunoglobulin A in the papillary dermis. These antibodies target transglutaminase (TG) 3 and in the majority of patients they are also found in circulation. The circulating antibodies disappear and skin symptoms resolve as a result of gluten-free diet but the cutaneous anti-TG3 IgA deposits may persist for several years. In dermatitis herpetiformis, plasma cells secreting antibodies against TG3 are located in the intestinal mucosa similarly to those producing TG2 antibodies characteristic for celiac disease. In fact, both TG2- and TG3-specific plasma cells and gluten responsive T cells are found in dermatitis herpetiformis patients but the interplay between these cell populations is unknown. The small bowel mucosal damage in celiac disease is believed to be mediated by co-operation of cytotoxic intraepithelial T cells and the inflammatory milieu contributed by gluten-reactive CD4+ T cells, whereas the skin lesions in dermatitis herpetiformis appear to be devoid of gluten reactive T cells. Thus, how celiac disease-type intestinal T and B cell responses develop into an autoimmune condition affecting the skin is still incompletely understood. Finally, the skin and small bowel lesions may reappear upon reintroduction of gluten in patients treated with gluten-free diet but virtually nothing is known about the long-lived B cell and memory T cell populations activating in response to dietary gluten in dermatitis herpetiformis.
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Affiliation(s)
- Esko Kemppainen
- Celiac Disease Research Center, Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland
| | - Teea Salmi
- Celiac Disease Research Center, Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland.,Department of Dermatology, Tampere University Hospital, Tampere, Finland
| | - Katri Lindfors
- Celiac Disease Research Center, Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland
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Khan S, Patel S, M S, Hamid P. Another Chicken and Egg Story: Systematic Review on Lichen Planus as a Precursor for Celiac Disease in Adult Population. Cureus 2020; 12:e9526. [PMID: 32775115 PMCID: PMC7402537 DOI: 10.7759/cureus.9526] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/30/2020] [Accepted: 08/02/2020] [Indexed: 11/05/2022] Open
Abstract
Celiac disease is receiving much attention due to the gluten-free diet trend. Many health-conscious individuals practice a gluten-free diet, even if they do not have celiac disease. As it is an autoimmune disorder, it is associated with many other autoimmune diseases. We were interested in one skin condition, another autoimmune disorder lichen planus as a correlative factor for celiac disease. The following systematic review may give some clues. We searched online resources including PubMed, PubMed Central, Cochrane library, and Google scholar for systematic reviews, traditional reviews, randomized controlled trials, and meta-analysis on celiac disease and lichen planus. We included human studies published in peer-reviewed journals in the English language. After reviewing 2389 initial results of our search, we excluded 1250 duplicates, 1108 abstracts, 42 irrelevant articles. We assessed the remaining 26 articles for their quality using various quality assessment tools. After the quality assessment, we included nine final articles in our systematic review. Out of these nine studies, there were four systematic reviews, one traditional review, two case reports, and two observational studies. Only two articles had exclusively studied the specific association between celiac and lichen planus. The remaining studies included data that gave an overall association between other skin manifestations of celiac disease. From our study, we could not establish the relationship between celiac disease and lichen planus. We need more case-control studies and clinical trials with a larger population to get conclusive data. From current data, we can conclude that both immunological processes correlate but there is no causation. There is also a need for clinical trials to explore the exacerbation of lichen planus due to celiac disease.
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Affiliation(s)
- Sahar Khan
- Internal Medicine, California Institute of Behavioral Neurosciences & Psychology, Fairfield, USA
| | - Shweta Patel
- Psychiatry, California Institute of Behavioral Neurosciences & Psychology, Fairfield, USA
| | - Saipavankumar M
- Pediatrics, California Institute of Behavioral Neurosciences & Psychology, Fairfield, USA
| | - Pousettef Hamid
- Neurology, California Institute of Behavioral Neurosciences & Psychology, Fairfield, USA
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Abstract
Celiac disease (CD) is an immune-mediated enteropathy triggered by dietary ingestion of gluten in genetically susceptible patients. CD is often diagnosed by a "case-finding" approach of symptomatic patients. In recent times, the diagnostic paradigm has shifted to investigate patients who may be asymptomatic, but are at high risk of developing CD due to shared genetic susceptibilities. These high-risk groups include first-degree relatives of CD patients and patients with Type 1 diabetes mellitus, autoimmune thyroid disease, Down's syndrome, and Turner syndrome. Moreover, CD is often diagnosed as the cause of iron deficiency anemia or unexplained chronic diarrhea. Although screening for CD with serological tests is not recommended for the general population, it should be considered in these special populations. In this review, we explore screening for CD among high-risk groups in light of recent research and development in the CD arena.
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Affiliation(s)
- Dennis Kumral
- Department of Medicine, Division of Gastroenterology and Hepatology, University of Virginia, 1215 Lee Street, PO Box 800708, Charlottesville, VA, 22908, USA.
| | - Sana Syed
- Department of Pediatrics, Division of Gastroenterology, Hepatology and Nutrition, School of Medicine, University of Virginia, MR-4 Bldg, 409 Lane Rd., Charlottesville, VA, 22908, USA
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9
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Costin A, António AM, Furtado C, Bártolo E. Dermatitis herpetiformis in an adolescent patient. An Bras Dermatol 2019; 94:495-496. [PMID: 31644636 PMCID: PMC7007020 DOI: 10.1590/abd1806-4841.20198227] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/25/2017] [Accepted: 08/09/2018] [Indexed: 11/22/2022] Open
Affiliation(s)
- Adelina Costin
- Dermatology and Venereology Service, Hospital Garcia de Orta, Almada, Portugal
| | - Ana Marta António
- Dermatology and Venereology Service, Hospital Garcia de Orta, Almada, Portugal
| | - Constança Furtado
- Dermatology and Venereology Service, Hospital Garcia de Orta, Almada, Portugal
| | - Elvira Bártolo
- Dermatology and Venereology Service, Hospital Garcia de Orta, Almada, Portugal
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10
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Antiga E, Maglie R, Quintarelli L, Verdelli A, Bonciani D, Bonciolini V, Caproni M. Dermatitis Herpetiformis: Novel Perspectives. Front Immunol 2019; 10:1290. [PMID: 31244841 PMCID: PMC6579917 DOI: 10.3389/fimmu.2019.01290] [Citation(s) in RCA: 47] [Impact Index Per Article: 7.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/01/2019] [Accepted: 05/21/2019] [Indexed: 02/06/2023] Open
Abstract
Dermatitis herpetiformis (DH) is an inflammatory disease of the skin, considered the specific cutaneous manifestation of celiac disease (CD). Both DH and CD occur in gluten-sensitive individuals, share the same Human Leukocyte Antigen (HLA) haplotypes (DQ2 and DQ8), and improve following the administration of a gluten-free diet. Moreover, almost all DH patients show typical CD alterations at the small bowel biopsy, ranging from villous atrophy to augmented presence of intraepithelial lymphocytes, as well as the generation of circulating autoantibodies against tissue transglutaminase (tTG). Clinically, DH presents with polymorphic lesions, including papules, vesicles, and small blisters, symmetrically distributed in typical anatomical sites including the extensor aspects of the limbs, the elbows, the sacral regions, and the buttocks. Intense pruritus is almost the rule. However, many atypical presentations of DH have also been reported. Moreover, recent evidence suggested that DH is changing. Firstly, some studies reported a reduced incidence of DH, probably due to early recognition of CD, so that there is not enough time for DH to develop. Moreover, data from Japanese literature highlighted the absence of intestinal involvement as well as of the typical serological markers of CD (i.e., anti-tTG antibodies) in Japanese patients with DH. Similar cases may also occur in Caucasian patients, complicating DH diagnosis. The latter relies on the combination of clinical, histopathologic, and immunopathologic findings. Detecting granular IgA deposits at the dermal-epidermal junction by direct immunofluorescence (DIF) from perilesional skin represents the most specific diagnostic tool. Further, assessing serum titers of autoantibodies against epidermal transglutaminase (eTG), the supposed autoantigen of DH, may also serve as a clue for the diagnosis. However, a study from our group has recently demonstrated that granular IgA deposits may also occur in celiac patients with non-DH inflammatory skin diseases, raising questions about the effective role of eTG IgA autoantibodies in DH and suggesting the need of revising diagnostic criteria, conceivably emphasizing clinical aspects of the disease along with DIF. DH usually responds to the gluten-free diet. Topical clobetasol ointment or dapsone may be also applied to favor rapid disease control. Our review will focus on novel pathogenic insights, controversies, and management aspects of DH.
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Affiliation(s)
- Emiliano Antiga
- Section of Dermatology, Department of Health Sciences, University of Florence, Florence, Italy
| | - Roberto Maglie
- Section of Dermatology, Department of Health Sciences, University of Florence, Florence, Italy
| | - Lavinia Quintarelli
- Section of Dermatology, Department of Health Sciences, University of Florence, Florence, Italy
| | - Alice Verdelli
- Section of Dermatology, Department of Health Sciences, University of Florence, Florence, Italy
| | - Diletta Bonciani
- Section of Dermatology, Department of Health Sciences, University of Florence, Florence, Italy
| | - Veronica Bonciolini
- Section of Dermatology, Department of Health Sciences, University of Florence, Florence, Italy
| | - Marzia Caproni
- Section of Dermatology, Department of Health Sciences, University of Florence, Florence, Italy
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11
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Bullous Diseases of the Skin and Mucous Membranes. Clin Immunol 2019. [DOI: 10.1016/b978-0-7020-6896-6.00063-6] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/17/2022]
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12
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Shuster S. The dead hand of research committees. BMJ 2018; 363:k4415. [PMID: 30361240 DOI: 10.1136/bmj.k4415] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/03/2022]
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Prognosis of Dermatitis Herpetiformis Patients with and without Villous Atrophy at Diagnosis. Nutrients 2018; 10:nu10050641. [PMID: 29783727 PMCID: PMC5986520 DOI: 10.3390/nu10050641] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/18/2018] [Revised: 05/11/2018] [Accepted: 05/15/2018] [Indexed: 12/14/2022] Open
Abstract
Dermatitis herpetiformis (DH) is a cutaneous manifestation of coeliac disease. At diagnosis, the majority of patients have villous atrophy in the small bowel mucosa. The objective of this study was to investigate whether the presence or absence of villous atrophy at diagnosis affects the long-term prognosis of DH. Data were gathered from the patient records of 352 DH and 248 coeliac disease patients, and follow-up data via questionnaires from 181 DH and 128 coeliac disease patients on a gluten-free diet (GFD). Of the DH patients, 72% had villous atrophy when DH was diagnosed, and these patients were significantly younger at diagnosis compared to those with normal small bowel mucosa (37 vs. 54 years, p < 0.001). Clinical recovery on a GFD did not differ significantly between the DH groups, nor did current adherence to a GFD, the presence of long-term illnesses, coeliac disease-related complications or gastrointestinal symptoms, or quality of life. By contrast, the coeliac disease controls had more often osteopenia/osteoporosis, thyroid diseases, malignancies and current gastrointestinal symptoms compared to the DH patients. In conclusion, villous atrophy at the time of DH diagnosis does not have an impact on the clinical recovery or long-term general health of DH patients.
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Dermatitis Herpetiformis: A Common Extraintestinal Manifestation of Coeliac Disease. Nutrients 2018; 10:nu10050602. [PMID: 29757210 PMCID: PMC5986482 DOI: 10.3390/nu10050602] [Citation(s) in RCA: 59] [Impact Index Per Article: 8.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/13/2018] [Revised: 05/04/2018] [Accepted: 05/09/2018] [Indexed: 12/20/2022] Open
Abstract
Dermatitis herpetiformis (DH) is a common extraintestinal manifestation of coeliac disease presenting with itchy papules and vesicles on the elbows, knees, and buttocks. Overt gastrointestinal symptoms are rare. Diagnosis of DH is easily confirmed by immunofluorescence biopsy showing pathognomonic granular immunoglobulin A (IgA) deposits in the papillary dermis. A valid hypothesis for the immunopathogenesis of DH is that it starts from latent or manifest coeliac disease in the gut and evolves into an immune complex deposition of high avidity IgA epidermal transglutaminase (TG3) antibodies, together with the TG3 enzyme, in the papillary dermis. The mean age at DH diagnosis has increased significantly in recent decades and presently is 40⁻50 years. The DH to coeliac disease prevalence ratio is 1:8 in Finland and the United Kingdom (U.K.). The annual DH incidence rate, currently 2.7 per 100,000 in Finland and 0.8 per 100,000 in the U.K., is decreasing, whereas the reverse is true for coeliac disease. The long-term prognosis of DH patients on a gluten-free diet is excellent, with the mortality rate being even lower than for the general population.
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15
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Lowrie M, Garden OA, Hadjivassiliou M, Sanders DS, Powell R, Garosi L. Characterization of Paroxysmal Gluten-Sensitive Dyskinesia in Border Terriers Using Serological Markers. J Vet Intern Med 2018; 32:775-781. [PMID: 29424456 PMCID: PMC5866963 DOI: 10.1111/jvim.15038] [Citation(s) in RCA: 28] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/05/2017] [Revised: 11/10/2017] [Accepted: 12/14/2017] [Indexed: 11/27/2022] Open
Abstract
BACKGROUND Paroxysmal gluten-sensitive dyskinesia (PGSD) in border terriers (BTs) results from an immunologic response directed against transglutaminase (TG)2 and gliadin. Recent evidence suggests that PGSD is only one aspect of a range of possible manifestations of gluten sensitivity in the breed. HYPOTHESIS/OBJECTIVES Gluten sensitivity in BTs is a heterogeneous disease process with a diverse clinical spectrum; to characterize the phenotype of PGSD using TG2 and gliadin autoantibodies as diagnostic markers. ANIMALS One hundred twenty-eight client-owned BTs with various disorders. METHODS Prospective study. BTs with paroxysmal episodes and a normal interictal examination were phenotyped using footage of a representative episode and assigned to 3 groups: idiopathic epilepsy (IE), paroxysmal dyskinesia (PD), or other. Owners of each dog completed a questionnaire to obtain information regarding clinical signs. Healthy BTs formed a control group. Serum antibodies against TG2 and AGA were measured in all dogs. RESULTS One hundred twenty-eight BTs were enrolled; 45 with PD, 28 with IE, 35 with other conditions, and 20 controls. Three overlapping phenotypes were identified; PD, signs suggestive of gastrointestinal disease, and dermatopathy. AGA-IgG concentrations were increased in PD, compared with IE (P = 0.012), controls (P < 0.0001) and other (P = 0.018) conditions. Anti-canine TG2-IgA concentrations were increased in PD, compared with IE (P < 0.0001), controls (P < 0.0001) and other (P = 0.012) conditions. Serological markers are highly specific for PGSD but lack sensitivity. CONCLUSIONS PGSD appears part of a syndrome of gluten intolerance consisting of episodes of transient dyskinesia, signs suggestive of gastrointestinal disease, and dermatological hypersensitivity.
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Affiliation(s)
- M Lowrie
- Dovecote Veterinary Hospital, Derby DE74 2LJ, England
| | - O A Garden
- Department of Clinical Sciences and Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA
| | - M Hadjivassiliou
- Department of Neurology, Royal Hallamshire Hospital, Sheffield S10 2JF, England
| | - D S Sanders
- Department of Gastroenterology, Royal Hallamshire Hospital, Sheffield S10 2JF, England
| | - R Powell
- Powell Torrance Diagnostic Services, Unit 2a Manor Farm Business Park, Higham Gobion, Hitchin, SG5 3HR, England
| | - L Garosi
- Davies Veterinary Specialists, Manor Farm Business Park, Higham Gobion, Hitchin, SG5 3HR, England
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16
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The Decreasing Prevalence of Severe Villous Atrophy in Dermatitis Herpetiformis: A 45-Year Experience in 393 Patients. J Clin Gastroenterol 2017; 51:235-239. [PMID: 27136959 DOI: 10.1097/mcg.0000000000000533] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/15/2022]
Abstract
GOALS We analyzed from our prospectively collected series of patients with dermatitis herpetiformis (DH) whether small-bowel histologic findings are changing and how serum tissue transglutaminase (TG2) IgA antibodies correlate to mucosal damage. BACKGROUND DH is an extraintestinal manifestation of celiac disease presenting with itchy blistering rash and pathognomonic IgA deposits in the skin. Prominent gastrointestinal symptoms are rare, and small-bowel findings range from severe villous atrophy (SVA) and partial villous atrophy (PVA) to normal mucosa with inflammatory changes. METHODS The cohort included 393 patients (214 male and 179 female) with DH having small-bowel biopsies performed at Tampere University Hospital since 1970. The small-bowel findings were calculated in the three 15-year periods, and in the last period they were correlated with serum IgA class TG2 antibody levels measured by enzyme-linked immunosorbent assay. RESULTS The prevalence of SVA decreased significantly (P=0.032), from 42% in the first study period to 29% in the last study period. A concomitant increase was seen in PVA, from 33% to 41%, and normal villous architecture, from 25% to 30%. The patients with SVA (P<0.001) and PVA (P=0.046) had significantly higher TG2 antibody levels than those with normal villous architecture. CONCLUSIONS This long-term study in patients with DH disclosed a significant decrease in the occurrence of SVA. Serum IgA TG2 antibody levels correlated to damage in the small bowel. The trend toward milder small-bowel histology in DH suggests that a similar pattern could occur in the pool of undiagnosed celiac disease from which DH develops.
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Collin P, Salmi TT, Hervonen K, Kaukinen K, Reunala T. Dermatitis herpetiformis: a cutaneous manifestation of coeliac disease. Ann Med 2017; 49:23-31. [PMID: 27499257 DOI: 10.1080/07853890.2016.1222450] [Citation(s) in RCA: 61] [Impact Index Per Article: 7.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/07/2023] Open
Abstract
Dermatitis herpetiformis (DH) is an itchy blistering skin disease with predilection sites on elbows, knees, and buttocks. Diagnosis is confirmed by showing granular immunoglobulin A deposits in perilesional skin. DH is one manifestation of coeliac disease; the skin symptoms heal with gluten free diet (GFD) and relapse on gluten challenge. Of the first-degree relatives, 5% may be affected by either condition. Tissue transglutaminase (TG2) is the autoantigen in coeliac disease and epidermal transglutaminase (TG3) in DH. Both diseases conditions exhibit TG2-specific autoantibodies in serum and small bowel mucosa; patients with DH have IgA-TG3 in the skin. There are some divergencies between these two phenotypes. One-fourth of DH patients do not have small bowel mucosal villous atrophy, but virtually all have coeliac-type inflammatory changes. The skin symptoms respond slowly to GFD. The incidence of coeliac disease is increasing, whereas the opposite is true for DH. A female predominance is evident in coeliac disease, while DH may be more common in males. Coeliac disease carries the risk of small intestinal T-cell lymphoma; in DH B-cell lymphomas at any site may prevail. Adult coeliac disease carries a slightly increased elevated mortality risk, whereas in DH, the relative mortality rate is significantly decreased. Key messages Dermatitis herpetiformis is a cutaneous manifestation of coeliac disease; both conditions are genetically determined and gluten-dependent. Gastrointestinal symptoms and the degree of villous atrophy are less obvious in dermatitis herpetiformis than in coeliac disease. Both show tissue transglutaminase (TG2) specific autoantibodies in serum and small bowel mucosa. In addition, TG3-targeted IgA antibodies are found in the skin of DH patients Both conditions carry an increased elevated risk of lymphoma, in coeliac disease small intestinal T-cell lymphoma, in dermatitis herpetiformis mainly B-cell lymphoma at various sites. Coeliac disease is currently eight times more common that DH; the incidence of DH is decreasing in contrast to that of coeliac disease, where it is increasing.
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Affiliation(s)
- Pekka Collin
- a Department of Gastroenterology and Alimentary Tract Surgery , Tampere University Hospital , Tampere , Finland
| | - Teea T Salmi
- b Department of Dermatology , Tampere University Hospital , Tampere , Finland.,c School of Medicine , University of Tampere , Tampere , Finland
| | - Kaisa Hervonen
- b Department of Dermatology , Tampere University Hospital , Tampere , Finland.,c School of Medicine , University of Tampere , Tampere , Finland
| | - Katri Kaukinen
- c School of Medicine , University of Tampere , Tampere , Finland.,d Department of Internal Medicine , Tampere University Hospital , Tampere , Finland
| | - Timo Reunala
- b Department of Dermatology , Tampere University Hospital , Tampere , Finland.,c School of Medicine , University of Tampere , Tampere , Finland
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Stimpson PJ, Marks DJ. Leading articles in medical journals in 1966. Br J Hosp Med (Lond) 2016; 77:575-577. [PMID: 27723411 DOI: 10.12968/hmed.2016.77.10.575] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/11/2022]
Abstract
The British Journal of Hospital Medicine is 50 years old. This article takes a look back at articles published during the year of its inception from the British Medical Journal, the Lancet and the Journal of the American Medical Association.
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Affiliation(s)
| | - Daniel Jb Marks
- ST7 in Clinical Pharmacology and Acute Medicine, University College London, London
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Garcia-Doval I, Ingram JR, Naldi L, Anstey A. Case reports in dermatology: loved by clinicians, loathed by editors, and occasionally important. Br J Dermatol 2016; 175:449-51. [PMID: 27632956 DOI: 10.1111/bjd.14869] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/27/2023]
Affiliation(s)
- I Garcia-Doval
- Complexo Hospitalario Universitario de Vigo, Vigo. Meixoeiro s.n. 36200, Vigo, Spain. .,Research Unit, Fundación Piel Sana AEDV, Madrid, Spain.
| | - J R Ingram
- Department of Dermatology & Wound Healing, Division of Infection and Immunity, Cardiff University, University Hospital of Wales, 3rd Floor Glamorgan House, Heath Park, Cardiff, CF14 4XN, U.K
| | - L Naldi
- Centro Studi GISED, Via Garibaldi 13/15, Azienda Ospedaliera papa Giovanni XXIII, 24100, Bergamo, Italy
| | - A Anstey
- Betsi Cadwaladr University Health Board, Ysbyty Gwynedd, Penrhosgarnedd, Bangor, Gwynedd, LL57 2PY, U.K
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Mocan O, Dumitraşcu DL. The broad spectrum of celiac disease and gluten sensitive enteropathy. ACTA ACUST UNITED AC 2016; 89:335-42. [PMID: 27547052 PMCID: PMC4990427 DOI: 10.15386/cjmed-698] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/25/2016] [Accepted: 06/29/2016] [Indexed: 12/27/2022]
Abstract
The celiac disease is an immune chronic condition with genetic transmission, caused by the intolerance to gluten. Gluten is a protein from cereals containing the following soluble proteins: gliadine, which is the most toxic, and the prolamins. The average prevalence is about 1% in USA and Europe, but high in Africa: 5.6% in West Sahara. In the pathogenesis several factors are involved: gluten as external trigger, genetic predisposition (HLA, MYO9B), viral infections, abnormal immune reaction to gluten. Severity is correlated with the number of intraepithelial lymphocytes, cryptic hyperplasia and villous atrophy, as well as with the length of intestinal involvement. The severity is assessed according to the Marsh–Oberhuber staging. Diagnostic criteria are: positive serological tests, intestinal biopsy, the reversal after gluten free diet (GFD). Beside refractory forms, new conditions have been described, like the non celiac gluten intolerance. In a time when more and more people adhere to GFD for nonscientific reasons, practitioners should be updated with the progress in celiac disease knowledge.
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Affiliation(s)
- Oana Mocan
- Biochemistry Department, Iuliu Hatieganu University of Medicine and Pharmacy, Polaris Medical Rehabilitation Hospital, Suceagu, Cluj County, Romania
| | - Dan L Dumitraşcu
- 2nd Department of Internal Medicine, Iuliu Hatieganu University of Medicine and Pharmacy, Cluj-Napoca, Romania
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Mitoma H, Adhikari K, Aeschlimann D, Chattopadhyay P, Hadjivassiliou M, Hampe CS, Honnorat J, Joubert B, Kakei S, Lee J, Manto M, Matsunaga A, Mizusawa H, Nanri K, Shanmugarajah P, Yoneda M, Yuki N. Consensus Paper: Neuroimmune Mechanisms of Cerebellar Ataxias. CEREBELLUM (LONDON, ENGLAND) 2016; 15:213-32. [PMID: 25823827 PMCID: PMC4591117 DOI: 10.1007/s12311-015-0664-x] [Citation(s) in RCA: 114] [Impact Index Per Article: 12.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Indexed: 02/06/2023]
Abstract
In the last few years, a lot of publications suggested that disabling cerebellar ataxias may develop through immune-mediated mechanisms. In this consensus paper, we discuss the clinical features of the main described immune-mediated cerebellar ataxias and address their presumed pathogenesis. Immune-mediated cerebellar ataxias include cerebellar ataxia associated with anti-GAD antibodies, the cerebellar type of Hashimoto's encephalopathy, primary autoimmune cerebellar ataxia, gluten ataxia, Miller Fisher syndrome, ataxia associated with systemic lupus erythematosus, and paraneoplastic cerebellar degeneration. Humoral mechanisms, cell-mediated immunity, inflammation, and vascular injuries contribute to the cerebellar deficits in immune-mediated cerebellar ataxias.
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Affiliation(s)
- Hiroshi Mitoma
- Department of Medical Education, Tokyo Medical University, Tokyo, Japan.
| | - Keya Adhikari
- Department of Haematology, Nil Ratan Sircar Medical College, 138 A J C Bose Road, Kolkata, 700014, West Bengal, India
| | - Daniel Aeschlimann
- Matrix Biology &Tissue Repair Research Unit, School of Dentistry, College of Biomedical and Life Sciences, Cardiff University, Cardiff, Wales, UK
| | - Partha Chattopadhyay
- Department of General Medicine, College of Medicine & Sagore Dutta Hospital, 578 B T Road, Kamarhati-Kolkata, 700056, West Bengal, India
| | | | - Christiane S Hampe
- School of Medicine, University of Washington, 850 Republication, Seattle, WA, 98109, USA
| | - Jérôme Honnorat
- University Lyon 1, University Lyon, Rue Guillaume Paradin, 69372, Lyon Cedex 08, France
- INSERM, UMR-S1028, CNRS, UMR-5292, Neuro-Oncology and Neuro-Inflammation Team, 7, Lyon Neuroscience Research Center, Rue Guillaume Paradin, 69372, Lyon Cedex 08, France
- National Reference Centre for Paraneoplastic Neurological Diseases, Hospices Civils de Lyon, Hôpital Neurologique, 69677, Bron, France
- Hospices Civils de Lyon, Neuro-oncology, Hôpital Neurologique, 69677, Bron, France
| | - Bastien Joubert
- University Lyon 1, University Lyon, Rue Guillaume Paradin, 69372, Lyon Cedex 08, France
- INSERM, UMR-S1028, CNRS, UMR-5292, Neuro-Oncology and Neuro-Inflammation Team, 7, Lyon Neuroscience Research Center, Rue Guillaume Paradin, 69372, Lyon Cedex 08, France
| | - Shinji Kakei
- Tokyo Metropolitan Institute of Medical Science, Tokyo, Japan
| | - Jongho Lee
- Tokyo Metropolitan Institute of Medical Science, Tokyo, Japan
| | - Mario Manto
- Unité d'Etude du Mouvement, FNRS, Neurologie ULB-Erasme, 808 Route de Lennik, 1070, Brussels, Belgium
| | - Akiko Matsunaga
- Department of Neurology, University of Fukui Hospital, Fukui, Japan
| | | | - Kazunori Nanri
- Department of Neurology, Tokyo Medical University Hachioji Medical Center, Tokyo, Japan
| | - Priya Shanmugarajah
- Academic Department of Neurosciences, Royal Hallamshire Hospital, Sheffield, UK
| | - Makoto Yoneda
- Faculty of Nursing and Social Welfare Sciences, Fukui Prefectural University, Fukui, Japan
| | - Nobuhiro Yuki
- Departments of Medicine and Physiology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore
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Hadjivassiliou M, Sanders DS, Aeschlimann D. The Neuroimmunology of Gluten Intolerance. NEURO-IMMUNO-GASTROENTEROLOGY 2016:263-285. [DOI: 10.1007/978-3-319-28609-9_15] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/03/2025]
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Bresler SC, Granter SR. Utility of direct immunofluorescence testing for IgA in patients with high and low clinical suspicion for dermatitis herpetiformis. Am J Clin Pathol 2015; 144:880-4. [PMID: 26572994 DOI: 10.1309/ajcpxivsr6ozk1hu] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/22/2022] Open
Abstract
OBJECTIVES The purpose of this study was to examine the utility of direct immunofluorescence (DIF) testing for the characteristic immunoglobulin A deposits of dermatitis herpetiformis (DH) in patients stratified into high and low clinical suspicion subgroups. METHODS We retrospectively analyzed the results of H&E and DIF testing in 77 cases of suspected DH and separated them into high and low clinical suspicion subgroups based on clinical impression at the time of biopsy. RESULTS The overall sensitivity and specificity of routine (H&E) histologic evaluation were 0.75 and 0.951, respectively. Although there were 13 cases of DH (of 36 total cases) in the high clinical suspicion subgroup, there were only three (of 41 total cases) in the low clinical suspicion subgroup. In the high clinical suspicion subgroup, the positive predictive value (PPV) was 0.9, and the negative predictive value (NPV) was 0.846. Alternatively, the PPV was 0.6 and the NPV was 1.0 for the low clinical suspicion subgroup. Histologic false negatives did occur, but all were in patients within the high clinical suspicion subgroup. CONCLUSIONS It is anticipated that the NPV and PPV will vary due to differing clinical practice characteristics; however, in patients with a low clinical suspicion for DH, these data argue that it may be reasonable to first perform a biopsy for routine histologic evaluation before requesting DIF analysis.
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Lowrie M, Garden OA, Hadjivassiliou M, Harvey RJ, Sanders DS, Powell R, Garosi L. The Clinical and Serological Effect of a Gluten-Free Diet in Border Terriers with Epileptoid Cramping Syndrome. J Vet Intern Med 2015; 29:1564-8. [PMID: 26500168 PMCID: PMC4895653 DOI: 10.1111/jvim.13643] [Citation(s) in RCA: 39] [Impact Index Per Article: 3.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/09/2015] [Revised: 08/28/2015] [Accepted: 09/15/2015] [Indexed: 11/27/2022] Open
Abstract
Background Canine epileptoid cramping syndrome (CECS) is a paroxysmal movement disorder of Border Terriers (BTs). These dogs might respond to a gluten‐free diet. Objectives The objective of this study was to examine the clinical and serological effect of a gluten‐free diet in BTs with CECS. Animals Six client‐owned BTs with clinically confirmed CECS. Methods Dogs were prospectively recruited that had at least a 6‐month history of CECS based on the observed phenomenology (using video) and had exhibited at least 2 separate episodes on different days. Dogs were tested for anti‐transglutaminase 2 (TG2 IgA) and anti‐gliadin (AGA IgG) antibodies in the serum at presentation, and 3, 6, and 9 months after the introduction of a gluten‐free diet. Duodenal biopsies were performed in 1 dog. Results Serum TG2 IgA titers were increased in 6/6 BTs (P = .006) and AGA IgG titers were increased in 5/6 BTs at presentation compared to those of controls (P = .018). After 9 months, there was clinical and serological improvement in all BTs with CECS strictly adhering to a gluten‐free diet (5/5). One dog had persistently increased antibody titers. This dog scavenged horse manure. On the strict introduction of a gluten‐free diet this dog also had an improved clinical and serological response. The diet‐associated improvement was reversible in 2 dogs on completion of the study, both of which suffered a relapse of CECS on the re‐introduction of gluten. Conclusions Canine epileptoid cramping syndrome in BTs is a gluten‐sensitive movement disorder triggered and perpetuated by gluten and thus responsive to a gluten‐free diet.
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Affiliation(s)
- M Lowrie
- Davies Veterinary Specialists, Hitchin, UK
| | - O A Garden
- Department of Clinical Sciences and Services, Royal Veterinary College, Hatfield, Hertfordshire, UK
| | - M Hadjivassiliou
- Department of Neurology, Royal Hallamshire Hospital, Sheffield, UK
| | - R J Harvey
- Department of Pharmacology, UCL School of Pharmacy, London, UK
| | - D S Sanders
- Department of Gastroenterology, Royal Hallamshire Hospital, Sheffield, UK
| | - R Powell
- Powell Torrance Diagnostic Services, Higham Gobion, UK
| | - L Garosi
- Davies Veterinary Specialists, Hitchin, UK
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Abstract
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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Affiliation(s)
- Daniel A Leffler
- The Celiac Centre at Beth Israel Deaconess Medical Centre, 330 Brookline Avenue, Boston, MA 02215, USA
| | - Peter H R Green
- Celiac Disease Centre at Columbia University, 180 Fort Washington Avenue, HP 934, New York, NY 10032, USA
| | - Alessio Fasano
- Centre for Celiac Research, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02114, USA
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Abstract
The term gluten-related disorders (GRD) refers to a spectrum of diverse clinical manifestations triggered by the ingestion of gluten in genetically susceptible individuals. They include both intestinal and extraintestinal manifestations. Gluten ataxia (GA) is one of the commonest neurological manifestations of GRD. It was originally defined as otherwise idiopathic sporadic ataxia in the presence of circulating antigliadin antibodies of IgA and/or IgG type. Newer more specific serological markers have been identified but are not as yet readily available. GA has a prevalence of 15% amongst all ataxias and 40% of all idiopathic sporadic ataxias. It usually presents with gait and lower limb ataxia. It is of insidious onset with a mean age at onset of 53 years. Up to 40% of patients have evidence of enteropathy on duodenal biopsy. Gastrointestinal symptoms are seldom prominent and are not a reliable indicator for the presence of enteropathy. Furthermore, the presence of enteropathy does not influence the response to a gluten-free diet. Most patients will stabilise or improve with strict adherence to gluten-free diet depending on the duration of the ataxia prior to the treatment. Up to 60% of patients with GA have evidence of cerebellar atrophy on MR imaging, but all patients have spectroscopic abnormalities primarily affecting the vermis. Recent evidence suggests that patients with newly diagnosed coeliac disease presenting to the gastroenterologists have abnormal MR spectroscopy at presentation associated with clinical evidence of subtle cerebellar dysfunction. The advantage of early diagnosis and treatment (mean age 42 years in patients presenting with gastrointestinal symptoms vs. 53 years in patients presenting with ataxia) may protect the first group from the development and/or progression of neurological dysfunction.
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Srinivas M, Basumani P, Podmore G, Shrimpton A, Bardhan KD. Utility of testing patients, on presentation, for serologic features of celiac disease. Clin Gastroenterol Hepatol 2014; 12:946-52. [PMID: 24262940 DOI: 10.1016/j.cgh.2013.10.037] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/31/2013] [Revised: 10/11/2013] [Accepted: 10/30/2013] [Indexed: 02/07/2023]
Abstract
BACKGROUND & AIMS Celiac disease shares features of other disorders. It can be diagnosed conclusively only based on duodenal histology analysis, which is not practical for screening purposes. Serologic analysis might be used to identify candidates for biopsy analysis. We aimed to develop a simple diagnostic approach that all clinicians could follow to increase the percentage of patients accurately diagnosed with celiac disease at initial presentation. METHODS We performed a retrospective analysis of data from 752 patients (88 with celiac disease, none were IgA deficient) who attended a UK district general hospital from January 2007 through December 2008 and underwent biopsy analysis and serologic tests to measure endomyseal antibodies and IgA antibodies against tissue transglutaminase (tTG). Patients avoiding gluten in their diet were excluded. Patients were assigned to 1 of 4 groups: high-risk (based on presence of anemia, chronic diarrhea, unintentional weight loss, or dermatitis herpetiformis), low-risk (based on such factors as dyspepsia, abnormal liver function, ataxia, or chronic cough), nutrient deficiency (based on levels of iron, vitamins B12 and D, or folate), or screening (because they had type 1 diabetes or a family history of celiac disease). Patients with celiac disease were identified using the modified Marsh criteria (grades 1-3) for interpreting duodenal histology. We compared clinical category, serology profiles, and biopsy results between patients with and without celiac disease. RESULTS Celiac disease was diagnosed in 64 of 565 patients in the high-risk group (11%), 14 of 156 patients in the low-risk group (9%; P = .47 compared with high-risk group), 7 of 28 patients in the nutrient-deficiency group, and 3 of 3 patients in the screening group. Among 71 patients who tested positive for both antibodies (tTG and endomyseal antibodies), the positive predictive value for celiac disease was 97%; a negative test result for tTG had a negative predictive value of 98%. Among 708 patients with normal-looking biopsy samples, only 62 had celiac disease (9%). Among 44 patients with abnormal biopsy samples, 26 had celiac disease (59%). CONCLUSIONS Based on a retrospective analysis, patients with and without celiac disease cannot be distinguished based on clinical features. Patients who present with symptoms of celiac disease should be tested for tTG, to identify candidates for duodenal biopsy analysis.
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Affiliation(s)
- Melpakkam Srinivas
- Department of Gastroenterology, The Rotherham NHS Foundation Trust, Rotherham, South Yorkshire, United Kingdom
| | - Pandurangan Basumani
- Department of Gastroenterology, The Rotherham NHS Foundation Trust, Rotherham, South Yorkshire, United Kingdom
| | - Geoff Podmore
- Department of Immunology, The Rotherham NHS Foundation Trust, Rotherham, South Yorkshire, United Kingdom
| | - Anna Shrimpton
- Department of Immunology, The Rotherham NHS Foundation Trust, Rotherham, South Yorkshire, United Kingdom
| | - Karna Dev Bardhan
- Department of Gastroenterology, The Rotherham NHS Foundation Trust, Rotherham, South Yorkshire, United Kingdom.
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Kotze LMDS. Dermatitis herpetiformis, the celiac disease of the skin! ARQUIVOS DE GASTROENTEROLOGIA 2014; 50:231-5. [PMID: 24322197 DOI: 10.1590/s0004-28032013000200041] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Received: 05/24/2013] [Accepted: 07/12/2013] [Indexed: 12/14/2022]
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Hadjivassiliou M, Duker AP, Sanders DS. Gluten-related neurologic dysfunction. HANDBOOK OF CLINICAL NEUROLOGY 2014; 120:607-19. [PMID: 24365341 DOI: 10.1016/b978-0-7020-4087-0.00041-3] [Citation(s) in RCA: 31] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/14/2022]
Abstract
The term gluten-related disorders (GRD) encompasses a spectrum of systemic autoimmune diseases with diverse manifestations. GRD are characterized by abnormal immunological responsiveness to ingested gluten in genetically susceptible individuals. Celiac disease (CD) or gluten-sensitive enteropathy is only one of a number of GRD. Extraintestinal manifestations include dermatitis herpetiformis (DH) and neurologic dysfunction. Furthermore it is only recently that the concept of extraintestinal manifestations without enteropathy has become accepted. In this chapter we review the spectrum of neurologic manifestations in GRD, discuss recent advances in their diagnosis, and look at their possible pathophysiologic mechanisms.
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Affiliation(s)
| | - Andrew P Duker
- Department of Gastroenterology, Royal Hallamshire Hospital, Sheffield, UK
| | - David S Sanders
- Department of Neurology, University of Cincinnati, Cincinnati, OH, USA
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Celiac disease and autoimmune-associated conditions. BIOMED RESEARCH INTERNATIONAL 2013; 2013:127589. [PMID: 23984314 PMCID: PMC3741914 DOI: 10.1155/2013/127589] [Citation(s) in RCA: 112] [Impact Index Per Article: 9.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 05/10/2013] [Accepted: 06/20/2013] [Indexed: 02/06/2023]
Abstract
Celiac disease (CD) is frequently accompanied by a variety of extradigestive manifestations, thus making it a systemic disease rather than a disease limited to the gastrointestinal tract. This is primarily explained by the fact that CD belongs to the group of autoimmune diseases. The only one with a known etiology is related to a permanent intolerance to gluten. Remarkable breakthroughs have been achieved in the last decades, due to a greater interest in the diagnosis of atypical and asymptomatic patients, which are more frequent in adults. The known presence of several associated diseases provides guidance in the search of oligosymptomatic cases as well as studies performed in relatives of patients with CD. The causes for the onset and manifestation of associated diseases are diverse; some share a similar genetic base, like type 1 diabetes mellitus (T1D); others share pathogenic mechanisms, and yet, others are of unknown nature. General practitioners and other specialists must remember that CD may debut with extraintestinal manifestations, and associated illnesses may appear both at the time of diagnosis and throughout the evolution of the disease. The implementation of a gluten-free diet (GFD) improves the overall clinical course and influences the evolution of the associated diseases. In some cases, such as iron deficiency anemia, the GFD contributes to its disappearance. In other disorders, like T1D, this allows a better control of the disease. In several other complications and/or associated diseases, an adequate adherence to a GFD may slow down their evolution, especially if implemented during an early stage.
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Abstract
BACKGROUND Autoantibodies targeted against a variety of self-antigens are detected in autoimmune diseases and cancer. Emerging evidence has suggested the involvement of environmental factors such as infections and xenobiotics, and some dietary proteins and their antibodies in the pathogenesis of many autoimmune diseases. These antibodies appear in the blood years before presentation of symptoms in various disorders. Therefore, these antibodies may be used as biomarkers for early detection of various diseases. OBJECTIVE To provide an overview of antibody arrays that are measured against different human tissue antigens, crossreactive epitopes of infectious agents, dietary proteins, and haptenic chemicals in autoimmune diseases and cancer. METHOD Microarray analysis of antigen-antibody reaction. CONCLUSION The application of these antibody arrays to human autoimmune disease is expanding and is allowing for the identification of patterns or antibody signatures, thus establishing the premises for increased sensitivity and specificity of prediction, as well as positive predictive values. The presence of these antibodies would not necessarily mean that a patient would definitely become sick but may give a percentage of risk for different conditions that may develop over future months or years. Using this high-throughput microarray method, it is possible to screen rapidly for dozens of autoantibodies at low cost. This is an important factor in the implementation of autoantibody testing as a routine part of medical examinations.
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Affiliation(s)
- Aristo Vojdani
- Immunosciences Lab., Inc., 8693 Wilshire Blvd, Ste. 200, Beverly Hills, CA 90211, USA +1 310 657 1077 ; +1 310 657 1053 ;
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Edhegard KD, Hall RP. Bullous diseases of the skin and mucous membranes. Clin Immunol 2013. [DOI: 10.1016/b978-0-7234-3691-1.00076-3] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/23/2022]
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Tsuruta D, Dainichi T, Hamada T, Ishii N, Hashimoto T. Molecular diagnosis of autoimmune blistering diseases. Methods Mol Biol 2013; 961:17-32. [PMID: 23325635 DOI: 10.1007/978-1-62703-227-8_2] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 06/01/2023]
Abstract
Autoimmune bullous diseases are the best-characterized autoimmune skin diseases. Molecular diagnosis of these diseases has become possible due to the identification of their target autoantigens over the past three decades. In this review, we summarize methodology for categorizing autoimmune bullous diseases by means of combinations of direct and indirect immunofluorescence techniques using normal human skin sections, rat bladder sections and COS7 cells transfected with desmocollins 1-3 encoded vectors, enzyme-linked immunosorbent assays and immunoblotting with normal human epidermal extracts, dermal extracts, purified proteins from cell cultures and recombinant proteins.
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Affiliation(s)
- Daisuke Tsuruta
- Department of Dermatology, School of Medicine, and Institute of Cutaneous Cell Biology, Kurume University, Kurume, Fukuoka, Japan
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The bowel and migraine: update on celiac disease and irritable bowel syndrome. Curr Pain Headache Rep 2012; 16:278-86. [PMID: 22447132 DOI: 10.1007/s11916-012-0258-y] [Citation(s) in RCA: 37] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/25/2022]
Abstract
This article explores possible relationships between migraine, irritable bowel syndrome (IBS), celiac disease (CD), and gluten sensitivity. These seemingly distinct medical entities curiously share many common epidemiological, psychosocial, and pathophysiological similarities. Considerable evidence is emerging to support a concept that experiencing significant threatening adverse events creates a state of hypervigilance in the nervous system, which associates with exaggerated response to future threats and episodic attacks of migraine and IBS. While this sensitizing response is generally considered to reside in the central nervous system, it may be possible that the initiation resides in the enteric nervous system as well. What appears to link migraine, IBS, and CD is a disease model of a genetically sensitive nervous system transformed into one that is hypervigilant, and that over time can often develop disabling and pervasive disease.
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Newly described clinical and immunopathological feature of dermatitis herpetiformis. Clin Dev Immunol 2012; 2012:967974. [PMID: 22701503 PMCID: PMC3371679 DOI: 10.1155/2012/967974] [Citation(s) in RCA: 22] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/13/2012] [Accepted: 04/13/2012] [Indexed: 12/19/2022]
Abstract
Dermatitis herpetiformis (DH) is an inflammatory cutaneous disease with typical histopathological and immunopathological findings clinically characterized by intensely pruritic polymorphic lesions with a chronic-relapsing course. In addition to classic clinical manifestations of DH, atypical variants are more and more frequently reported and histological and immunological are added to them, whereas the impact on quality of life of patients with DH is increasingly important to a certain diagnosis. The aim of this paper is to describe all the possible clinical, histological, and immunological variants of DH in order to facilitate the diagnosis of a rare disease and, therefore, little known.
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Cardones ARG, Hall RP. Pathophysiology of Dermatitis Herpetiformis: A Model for Cutaneous Manifestations of Gastrointestinal Inflammation. Immunol Allergy Clin North Am 2012; 32:263-74, vi. [DOI: 10.1016/j.iac.2012.04.006] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
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Chronic gastritis in dermatitis herpetiformis: a controlled study. Clin Dev Immunol 2012; 2012:640630. [PMID: 22611420 PMCID: PMC3351085 DOI: 10.1155/2012/640630] [Citation(s) in RCA: 10] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/09/2012] [Accepted: 02/27/2012] [Indexed: 12/13/2022]
Abstract
Background and Objective. Previous small studies suggest that chronic atrophic gastritis is common in dermatitis herpetiformis (DH). We here examined the frequency and topography of chronic gastritis in 93 untreated DH subjects and in 186 controls with dyspepsia. Methods. Specimens were drawn from the gastric corpus and antrum and examined for atrophy, intestinal metaplasia, and Helicobacter pylori. Duodenal biopsies were taken. Results. Atrophic corpus gastritis was more frequent in DH than in controls (16.0% and 2.7%, resp., P < 0.001); atrophy in the antrum was rare in both groups (3.2% and 1.1%, P = 0.34). Intestinal metaplasia was present in 13 (14.0%) DH and 12 (6.5%) control patients (P = 0.038) and H. pylori in 17 (18.3%) and 17 (9.3%) (P = 0.028), respectively. Small-bowel villous atrophy was seen in 76% of the DH patients, equally in patients with and without chronic gastritis. One DH patient with atrophic gastritis developed gastric cancer. Conclusion. In DH, chronic atrophic gastritis was common in the corpus, but not in the antrum. H. pylori will partly explain this, but corpus atrophy is suggestive of an autoimmune etiology. Atrophic gastritis may increase the risk of gastric cancer. We advocate performing upper endoscopy with sufficient histologic samples in DH.
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Heinlin J, Knoppke B, Kohl E, Landthaler M, Karrer S. Dermatitis herpetiformis presenting as digital petechiae. Pediatr Dermatol 2012; 29:209-12. [PMID: 21848992 DOI: 10.1111/j.1525-1470.2011.01401.x] [Citation(s) in RCA: 17] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
Abstract
We present a 15-year-old female patient with a 6-month history of recurrent painful petechiae on the fingers and feet. Trauma or pressure were denied, but she reported recurrent tonsillitis and urinary tract infections and a single event of bilateral scotoma. Extensive investigations (e.g., echocardiography) for a suspected diagnosis of septic emboli were unremarkable. Routine histopathology, direct and indirect immunofluorescence, and esophagogastroduodenoscopy led to the diagnosis of dermatitis herpetiformis. The therapeutic strategy comprised gluten-free diet and dapsone to alleviate the symptoms. Dermatitis herpetiformis should be included in the differential diagnosis of palmar or plantar petechiae, especially when occurring in children or young adults.
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Affiliation(s)
- Julia Heinlin
- Department of Dermatology, University Hospital Regensburg, Regensburg, Germany
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Abstract
The cerebellum, and in particular the Purkinje cells within it, appear to be a frequent immunological target in the context of some systemic diseases. This is perhaps more often the case with the cerebellum by comparison to other structures within the central nervous system. This observation may relate to the fact that the cerebellum is one of the largest, oldest, and most structurally conserved structures in the vertebrate nervous system and/or that Purkinje cells possess good and multiple antigenic targets. Immune-mediated ataxias include paraneoplastic cerebellar degeneration and post-infective cerebellitis, but these will be discussed elsewhere. This chapter covers in detail the epidemiology, clinical characteristics, pathophysiology, and treatment of some other examples of immune-mediated ataxias, including gluten ataxia and ataxia associated with anti-GAD antibodies. There is particular emphasis on gluten ataxia as this is one of the commonest immune-mediated cerebellar ataxias and one of the few ataxias that are potentially treatable. The chapter also introduces the concept of primary autoimmune cerebellar ataxia as a form of organ-specific autoimmune disease for the first time. The pathophysiology leading to cerebellar damage, loss of Purkinje cells, and the development of ataxia remains speculative, but existing clues are discussed in detail.
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A Retrospective Study of Clinical, Histological, and Immunological Characteristics in Patients With Dermatitis Herpetiformis. The Experience of Hospital Clinic de Barcelona, Spain between 1995 and 2010 and a Review of the Literature. ACTAS DERMO-SIFILIOGRAFICAS 2011. [DOI: 10.1016/j.adengl.2011.11.001] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/17/2022] Open
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Estudio retrospectivo de las características clínicas, histológicas e inmunológicas de los pacientes con dermatitis herpetiforme. Experiencia del Hospital Clínic de Barcelona entre los años 1995 y 2010 y revisión de la literatura. ACTAS DERMO-SIFILIOGRAFICAS 2011; 102:699-705. [DOI: 10.1016/j.ad.2010.11.007] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/13/2010] [Revised: 11/17/2010] [Accepted: 11/18/2010] [Indexed: 11/17/2022] Open
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Cardones ARG, Hall RP. Pathophysiology of dermatitis herpetiformis: a model for cutaneous manifestations of gastrointestinal inflammation. Dermatol Clin 2011; 29:469-77, x. [PMID: 21605814 DOI: 10.1016/j.det.2011.03.005] [Citation(s) in RCA: 12] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/13/2023]
Abstract
Dermatitis herpetiformis (DH) is an autoimmune blistering skin disease in which antigen presentation in the gastrointestinal mucosa results in cutaneous IgA deposition and distinct, neutrophil-driven cutaneous lesions. Our findings suggest that the qualitatively different immune response to gluten in the intestinal mucosa of patients with DH results in minimal clinical symptoms, allowing the continued ingestion of gluten and the eventual development of DH. Our model may provide a new way to understand the pathogenesis of other skin diseases associated with gastrointestinal inflammation such as pyoderma gangrenosum or erythema nodosum, or explain association of seronegative inflammatory arthritis with inflammatory bowel disease.
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Abstract
The major treatment strategies for DH are gluten restriction or medical treatment with sulfones. Control of the cutaneous manifestations, but not the gastrointestinal changes, is rapid with dapsone. In addition to control of the cutaneous signs and symptoms of DH, dietary gluten restriction also induces improvement of gastrointestinal morphology and is possibly protective against the development of lymphoma.
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Salmi T, Hervonen K, Kautiainen H, Collin P, Reunala T. Prevalence and incidence of dermatitis herpetiformis: a 40-year prospective study from Finland. Br J Dermatol 2011; 165:354-9. [DOI: 10.1111/j.1365-2133.2011.10385.x] [Citation(s) in RCA: 94] [Impact Index Per Article: 6.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/06/2023]
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[Dermatitis herpetiformis: a review]. Ann Dermatol Venereol 2011; 138:221-7. [PMID: 21397152 DOI: 10.1016/j.annder.2011.01.005] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/08/2010] [Accepted: 01/06/2011] [Indexed: 01/08/2023]
Abstract
BACKGROUND Dermatitis herpetiformis (DH) is a rare auto-immune bullous disease characterized by its almost constant association to gluten sensitivity. OBJECTIVE Review of literature about epidemiology, physiopathology, clinical data and treatment of DH. METHODS Research on Medline and Embase database without any time limit until April 2010. Because of the lack of randomized therapeutic trials in DH, retrospective series and case reports have been analyzed. RESULTS DH is related to auto-antibodies against epidermal transglutaminase, which belongs to the same family as tissue transglutaminase, the auto-antigen of celiac disease. Physiopathology is complex, occurring in HLA DQ2 or DQ8 predisposed patients, and implies gluten, immunological reaction in the intestinal wall then in the skin. DH and celiac disease may be encountered in the same family. DH is characterized by a very pruritic microvesicular eruption typically located on elbows, knees and buttocks. Digestive manifestations of celiac disease occur in 15% of cases. Direct immunofluorescence is necessary to confirm the diagnosis, showing granular IgA±C3 deposits in the papillary dermis. Circulating IgA and IgG antiendomysium and antitransglutaminase antibodies are detected in almost all patients at the acute phase and follow the clinical course of the disease. Gastro-intestinal endoscopy with multiple duodenal biopsies shows partial or complete villous atrophy in two thirds of cases, intraepithelial lymphocyte infiltrate in the other cases. Other auto-immune diseases may be associated in 10-20% of cases. The main long-term risk is the occurrence of T or B nodal or intestinal tract lymphoma in 2% of cases (relative risk close to 6 in several studies, but not admitted by all authors), especially if adherence to gluten-free diet is not strict. Treatment is based on dapsone, which is quickly efficient on cutaneous manifestations, but not on the digestive involvement and on strict and definitive gluten-free diet, which cures villous atrophy and reduces the risk of lymphoma. CONCLUSION DH is associated to a gluten enteropathy and its physiopathology is better known. Even if the risk of secondary lymphoma seems little, most of the authors recommend a definitive gluten-free diet.
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Asano Y, Makino T, Ishida W, Furuichi M, Shimizu T. Detection of antibodies to epidermal transglutaminase but not tissue transglutaminase in Japanese patients with dermatitis herpetiformis. Br J Dermatol 2011; 164:883-4. [PMID: 21114479 DOI: 10.1111/j.1365-2133.2010.10153.x] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
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Herrero-González J. Guía clínica de diagnóstico y tratamiento de la dermatitis herpetiforme. ACTAS DERMO-SIFILIOGRAFICAS 2010. [DOI: 10.1016/j.ad.2010.06.018] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/11/2023] Open
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Abstract
Intestinal biopsies constitute an ever-increasing portion of the pathologist's workload, accounting for nearly two-thirds of specimens accessioned yearly by the pathology department at The Children's Hospital of Philadelphia. The widespread use of endoscopy and gastrointestinal biopsies in current clinical practice presents the pathologist with a diversity of intestinal mucosal appearances corresponding to disease states of variable clinical severity, requiring close collaboration between clinician and pathologist for optimal interpretation. Many of the entities resulting in severe diarrhea of infancy have been recognized only in the last several decades, and although rare, the study of these disorders, especially when combined with the powerful methods of present-day genetics and molecular biology, has afforded important insights into enterocyte development and function, and intestinal immunity and tolerance. Other conditions once considered infrequent, such as celiac disease, have now been recognized to be much more common and can present with a wide range of pathologic features.
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Affiliation(s)
- Pierre Russo
- Department of Pathology and Laboratory Medicine, The University of Pennsylvania School of Medicine, Philadelphia, PA, USA.
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