The Long-Term Safety and Quality of Life Effects of Oats in Dermatitis Herpetiformis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Patients and Study Design
2.2. Clinical and Dietary Information
2.3. Questionnaires
Validated Questionnaires
2.4. Statistics
3. Results
3.1. Baseline data of DH Patients on a Gluten-Free Diet with and without Oats
3.2. Follow-Up Data of DH Patients on a Gluten-Free Diet with or without Oats
4. Discussion
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Kárpáti, S. Dermatitis Herpetiformis. Clin. Dermatol. 2012, 30, 56–59. [Google Scholar] [CrossRef] [PubMed]
- Mansikka, E.; Hervonen, K.; Salmi, T.T.; Kautiainen, H.; Kaukinen, K.; Collin, P.; Reunala, T. The Decreasing Prevalence of Severe Villous Atrophy in Dermatitis Herpetiformis: A 45-Year Experience in 393 Patients. J. Clin. Gastroenterol. 2017, 51, 235–239. [Google Scholar] [CrossRef] [PubMed]
- Alakoski, A.; Salmi, T.T.; Hervonen, K.; Kautiainen, H. Chronic Gastritis in Dermatitis Herpetiformis: A Controlled Study. Clin. Dev. Immunol. 2012, 2012. [Google Scholar] [CrossRef] [PubMed]
- Dieterich, W.; Laag, E.; Schöpper, H.; Volta, U. Autoantibodies to Tissue Transglutaminase as Predictors of Celiac Disease. Gastroenterology 1998, 115, 1317–1321. [Google Scholar] [CrossRef]
- Dieterich, W.; Schuppan, D.; Laag, E.; Bruckner-Tuderman, L. Antibodies to Tissue Transglutaminase as Serologic Markers in Patients with Dermatitis Herpetiformis. J. Investig. Dermatol. 1999, 113, 133–136. [Google Scholar] [CrossRef] [Green Version]
- Sárdy, M.; Kárpáti, S.; Merkl, B.; Paulsson, M. Epidermal Transglutaminase (TGase 3) Is the Autoantigen of Dermatitis Herpetiformis. J. Exp. Med. 2002, 195, 747–757. [Google Scholar] [CrossRef] [Green Version]
- Fry, L.; Seah, P.P.; Riches, D.J.; Hoffbrand, A.V. Clearance of Skin Lesions in Dermatitis Herpetiformis after Gluten Withdrawal. Lancet Lond. Engl. 1973, 1, 288. [Google Scholar] [CrossRef]
- Reunala, T.; Blomqvist, K.; Tarpila, S.; Halme, H.; Kangas, K. Gluten-Free Diet in Dermatitis Herpetiformis. I. Clinical Response of Skin Lesions in 81 Patients. Br. J. Dermatol. 1977, 97, 473. [Google Scholar] [CrossRef]
- Galli, G.; Esposito, G.; Lahner, E.; Pilozzi, E.; Corleto, V.D.; Di Giulio, E.; Aloe Spiriti, M.A.; Annibale, B. Histological Recovery and Gluten-free Diet Adherence: A Prospective 1-year Follow-up Study of Adult Patients with Coeliac Disease. Aliment. Pharmacol. Ther. 2014, 40, 639–647. [Google Scholar] [CrossRef] [Green Version]
- Ciacci, C.; Cirillo, M.; Cavallaro, R.; Mazzacca, G. Long-Term Follow-up of Celiac Adults on Gluten-Free Diet: Prevalence and Correlates of Intestinal Damage. Digestion 2002, 66, 178. [Google Scholar] [CrossRef]
- Reunala, T.; Salmi, T.T.; Hervonen, K.; Laurila, K.; Kautiainen, H.; Collin, P.; Kaukinen, K. IgA Antiepidermal Transglutaminase Antibodies in Dermatitis Herpetiformis: A Significant but Not Complete Response to a Gluten-free Diet Treatment. Br. J. Dermatol. 2015, 172, 1139–1141. [Google Scholar] [CrossRef] [PubMed]
- Dipper, C.R.; Maitra, S.; Thomas, R.; Lamb, C.A. Anti-Tissue Transglutaminase Antibodies in the Follow-up of Adult Coeliac Disease. Aliment. Pharmacol. Ther. 2009, 30, 236. [Google Scholar] [CrossRef] [PubMed]
- Lewis, H.M.; Renaula, T.L.; Garioch, J.J.; Leonard, J.N. Protective Effect of Gluten-Free Diet against Development of Lymphoma in Dermatitis Herpetiformis. Br. J. Dermatol. 1996, 135, 363. [Google Scholar] [CrossRef] [PubMed]
- Grainge, M.J.; West, J.; Solaymani-Dodaran, M.; Card, T.R. The Long-Term Risk of Malignancy Following a Diagnosis of Coeliac Disease or Dermatitis Herpetiformis: A Cohort Study. Aliment. Pharmacol. Ther. 2012, 35, 730. [Google Scholar] [CrossRef]
- Pinto-Sánchez, M.; Mohaidle, A.; Baistrocchi, A.; Matoso, D.; Vázquez, H.; González, A.; Mazure, R.; Maffei, E.; Ferrari, G.; Smecuol, E.; et al. Risk of Fracture in Celiac Disease: Gender, Dietary Compliance, or Both. World J. Gastroenterol. 2011, 17, 3035–3042. [Google Scholar] [CrossRef]
- Pasternack, C.; Kaukinen, K.; Kurppa, K.; Mäki, M.; Collin, P.; Reunala, T.; Huhtala, H.; Salmi, T. Quality of Life and Gastrointestinal Symptoms in Long-Term Treated Dermatitis Herpetiformis Patients: A Cross-Sectional Study in Finland. Am. J. Clin. Dermatol. 2015, 16, 545–552. [Google Scholar] [CrossRef]
- Wagner, G.; Berger, G.; Sinnreich, U.; Grylli, V. Quality of Life in Adolescents with Treated Coeliac Disease: Influence of Compliance and Age at Diagnosis. J. Pediatr. Gastroenterol. Nutr. 2008, 47, 555. [Google Scholar] [CrossRef]
- Lee, A.R.; Wolf, R.L.; Lebwohl, B.; Ciaccio, E.J. Persistent Economic Burden of the Gluten Free Diet. Nutrients 2019, 11, 399. [Google Scholar] [CrossRef] [Green Version]
- Wild, D.; Robins, G.G.; Burley, V.J.; Howdle, P.D. Evidence of High Sugar Intake, and Low Fibre and Mineral Intake, in the Gluten-free Diet. Aliment. Pharmacol. Ther. 2010, 32, 573–581. [Google Scholar] [CrossRef]
- Ciacci, C.; Ciclitira, P.; Hadjivassiliou, M.; Kaukinen, K.; Ludvigsson, J.; McGough, N.; Sanders, D.; Woodward, J.; Leonard, J.; Swift, G. The Gluten-Free Diet and Its Current Application in Coeliac Disease and Dermatitis Herpetiformis. United Eur. Gastroenterol. J. 2015, 3, 121. [Google Scholar] [CrossRef]
- Aaltonen, K.; Laurikka, P.; Huhtala, H.; Mäki, M.; Kaukinen, K.; Kurppa, K. The Long-Term Consumption of Oats in Celiac Disease Patients Is Safe: A Large Cross-Sectional Study. Nutrients 2017, 9, 611. [Google Scholar] [CrossRef] [PubMed]
- Kaukinen, K.; Collin, P.; Huhtala, H.; Mäki, M. Long-Term Consumption of Oats in Adult Celiac Disease Patients. Nutrients 2013, 5, 4380. [Google Scholar] [CrossRef] [PubMed]
- Janatuinen, E.K.; Pikkarainen, P.H.; Kemppainen, T.A.; Kosma, V.-M. A Comparison of Diets with and without Oats in Adults with Celiac Disease. N. Engl. J. Med. 1995, 333, 1033. [Google Scholar] [CrossRef] [PubMed]
- Janatuinen, E.K.; Kemppainen, T.A.; Julkunen, R.J.K.; Kosma, V.-M. No Harm from Five Year Ingestion of Oats in Coeliac Disease. Gut 2002, 50, 332. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peräaho, M.; Kaukinen, K.; Mustalahti, K.; Vuolteenaho, N.; Mäki, M.; Laippala, P.; Collin, P. Effect of an Oats-Containing Gluten-Free Diet on Symptoms and Quality of Life in Coeliac Disease. A Randomized Study. Scand. J. Gastroenterol. 2004, 39, 27–31. [Google Scholar] [CrossRef]
- Lundin, K.E.A.; Nilsen, E.M.; Scott, H.G.; Løberg, E.M.; Gjøen, A.; Bratlie, J.; Skar, V.; Mendez, E.; Løvik, A.; Kett, K. Oats Induced Villous Atrophy in Coeliac Disease. Gut 2003, 52, 1649–1652. [Google Scholar] [CrossRef] [Green Version]
- Sjöberg, V.; Hollén, E.; Pietz, G.; Magnusson, K.-E.; Fälth-Magnusson, K.; Sundström, M.; Holmgren Peterson, K.; Sandström, O.; Hernell, O.; Hammarström, S.; et al. Noncontaminated Dietary Oats May Hamper Normalization of the Intestinal Immune Status in Childhood Celiac Disease. Clin. Transl. Gastroenterol. 2014, 5, e58. [Google Scholar] [CrossRef]
- Reunala, T.; Collin, P.; Holm, K.; Pikkarainen, P.; Miettinen, A.; Vuolteenaho, N.; Mäki, M. Tolerance to Oats in Dermatitis Herpetiformis. Gut 1998, 43, 490–493. [Google Scholar] [CrossRef] [Green Version]
- Hardman, C.M.; Garioch, J.J.; Leonard, J.N.; Thomas, H.J. Absence of Toxicity of Oats in Patients with Dermatitis Herpetiformis. N. Engl. J. Med. 1997, 337, 1884. [Google Scholar] [CrossRef]
- Smulders, M.J.M.; van de Wiel, C.C.M.; van den Broeck, H.C.; van der Meer, I.M.; Israel-Hoevelaken, T.P.M.; Timmer, R.D.; van Dinter, B.-J.; Braun, S.; Gilissen, L.J.W.J. Oats in Healthy Gluten-Free and Regular Diets: A Perspective. Food Res. Int. 2018, 110, 3–10. [Google Scholar] [CrossRef] [Green Version]
- Comino, I.; de Lourdes, M.M.; Sousa, C. Role of Oats in Celiac Disease. World J. Gastroenterol. 2015, 21, 11825–11831. [Google Scholar] [CrossRef] [PubMed]
- Peräaho, M.; Collin, P.; Kaukinen, K.; Kekkonen, L. Oats Can Diversify a Gluten-Free Diet in Celiac Disease and Dermatitis Herpetiformis. J. Am. Diet. Assoc. 2004, 104, 1148–1150. [Google Scholar] [CrossRef] [PubMed]
- Salmi, T.T.; Hervonen, K.; Kautiainen, H.; Collin, P. Prevalence and Incidence of Dermatitis Herpetiformis: A 40-year Prospective Study from Finland. Br. J. Dermatol. 2011, 165, 354–359. [Google Scholar] [CrossRef] [PubMed]
- Hervonen, K.; Alakoski, A.; Salmi, T.T.; Helakorpi, S.; Kautiainen, H.; Kaukinen, K.; Pukkala, E.; Collin, P.; Reunala, T. Reduced Mortality in Dermatitis Herpetiformis: A Population-based Study of 476 Patients. Br. J. Dermatol. 2012, 167, 1331–1337. [Google Scholar] [CrossRef]
- Mansikka, E.; Salmi, T.; Kaukinen, K.; Collin, P.; Huhtala, H.; Reunala, T.; Hervonen, K. Diagnostic Delay in Dermatitis Herpetiformis in a High-Prevalence Area. Acta Derm. Venereol. 2018, 98, 195–199. [Google Scholar] [CrossRef] [Green Version]
- Korponay-Szabó, I.R.; Halttunen, T.; Szalai, Z.; Laurila, K. In Vivo Targeting of Intestinal and Extraintestinal Transglutaminase 2 by Coeliac Autoantibodies. Gut 2004, 53, 641. [Google Scholar] [CrossRef] [Green Version]
- Svedlund, J.; Sjödin, I.; Dotevall, G. GSRS—A Clinical Rating Scale for Gastrointestinal Symptoms in Patients with Irritable Bowel Syndrome and Peptic Ulcer Disease. Dig. Dis. Sci. 1988, 33, 129. [Google Scholar] [CrossRef]
- Dimenäs, E.; Carlsson, G.; Glise, H.; Israelsson, B.; Wiklund, I. Relevance of Norm Values as Part of the Documentation of Quality of Life Instruments for Use in Upper Gastrointestinal Disease. Scand. J. Gastroenterol. Suppl. 1996, 221, 8. [Google Scholar] [CrossRef]
- Finlay, A.Y.; Khan, G.K. Dermatology Life Quality Index (DLQI)—A Simple Practical Measure for Routine Clinical Use. Clin. Exp. Dermatol. 1994, 19, 210. [Google Scholar] [CrossRef]
- Hallert, C.; Svensson, M.; Tholstrup, J.; Hultberg, B. Clinical Trial: B Vitamins Improve Health in Patients with Coeliac Disease Living on a Gluten-Free Diet. Aliment. Pharmacol. Ther. 2009, 29, 811. [Google Scholar] [CrossRef]
- Lewis, V.; Finlay, A.Y. 10 Years Experience of the Dermatology Life Quality Index (DLQI). J. Investig. Dermatol. Symp. Proc. 2004, 9, 169–180. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pinto-Sánchez, M.; Causada-Calo, N.; Bercik, P.; Ford, A.C.; Murray, J.A.; Armstrong, D.; Semrad, C. Safety of Adding Oats to a Gluten-Free Diet for Patients with Celiac Disease: Systematic Review and Meta-Analysis of Clinical and Observational Studies. Gastroenterology 2017, 153, 395–409. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reunala, T. Gluten-free diet in dermatitis herpetiformis. II. Morphological and immunological findings in the skin and small intestine of 12 patients and matched controls. Br. J. Dermatol. 1978, 98, 69–78. [Google Scholar] [CrossRef] [PubMed]
Oats, n = 256 (82%) | No Oats, n = 56 (18%) | p-Value | ||
---|---|---|---|---|
Females, n (%) | 125 (49) | 26 (46) | 0.745 | |
Age at diagnosis, median (Q1–Q3), years | 37 (27–50) | 39 (24–48) | 0.481 | |
Year of diagnosis (dg), median (Q1–Q3) | 1993 (1982–2002) | 1988 (1982–2000) | 0.184 | |
Dg < 1985, n (%) | 74 (29) | 18 (32) | ||
Dg 1985–1999, n (%) | 96 (38) | 24 (43) | ||
Dg 2000–2014, n (%) | 86 (34) | 14 (25) | ||
Duration of skin symptoms before diagnosis, median (Q1–Q3), months 1 | 11 (6–36) | 10 (5–60) | 0.671 | |
Severity of skin symptoms 2 at diagnosis, n (%)3 | 0.076 | |||
Mild | 26/167 (16) | 6/31 (19) | ||
Moderate | 90/167 (54) | 10/31 (32) | ||
Severe | 51/167 (31) | 15/31 (48) | ||
Gastrointestinal symptoms at diagnosis, n (%) | 108/227 (48) | 25/50 (50) | 0.756 | |
Small bowel histology at diagnosis, n (%) | 0.530 | |||
Normal | 43/207 (21) | 5/36 (14) | ||
Partial villous atrophy | 78/207 (37) | 13/36 (36) | ||
Subtotal/total villous atrophy | 86/207 (42) | 18/36 (50) | ||
Positive coeliac serology 3 at diagnosis, n (%) | 121/164 (74) | 19/31 (61) | 0.156 |
Oats, n = 256 (82%) | No Oats, n = 56 (18%) | p-Value | |
---|---|---|---|
Age, median (range), years | 62 (18–96) | 62 (32–85) | 0.963 |
Duration of GFD, median (range), years | 21 (1–47) | 24 (2–41) | 0.161 |
GFD adherence | 0.229 | ||
Strict, no dietary lapses, n (%) | 200/254 (79) | 49/56 (88) | |
Dietary lapses less than once a month, n (%) | 36/254 (14) | 6/56 (11) | |
Dietary lapses once a month or more often, n (%) | 18/254 (7) | 1/56 (2) | |
Skin symptoms, n (%)1 | 30/188 (16) | 10/36 (28) | 0.090 |
Dapsone treatment, n (%)1 | 8/188 (4) | 5/36 (14) | 0.040 |
Gastrointestinal symptoms, n (%)1 | 8/188 (4) | 7/36 (19) | 0.004 |
The total number of long-term illnesses, median (range)1 | 1 (0–12) | 1 (0–9) | 0.850 |
Coronary heart disease, n (%) | 20 (8) | 2 (4) | 0.261 |
Cerebrovascular disease, n (%) | 7 (3) | 1 (2) | 1.000 |
Osteoporosis or osteopenia, n (%) | 15 (6) | 3 (6) | 1.000 |
Bone fractures, n (%) | 49 (19) | 12 (21) | 0.696 |
Malignancy, n (%) | 22 (9) | 2 (4) | 0.273 |
Number of prescription medications used, median (range) 1 | 2 (0–4) | 2 (0–9) | 0.510 |
Number of over-the-counter medications used, median (range) 1 | 1 (0–5) | 1 (0–5) | 0.769 |
Current smoking, n (%)1 | 18 (7) | 9 (16) | 0.032 |
Body mass index, kg/m2, median (range)1 | 25 (17–40) | 26 (20–33) | 0.242 |
Oats, n = 256 (82%) | No Oats, n = 56 (18%) | p-Value | ||
---|---|---|---|---|
median (Q1–Q3) | median (Q1–Q3) | |||
GSRS scores 1 | ||||
Total score | 1.7 (1.3–2.2) | 1.7 (1.4–2.2) | 0.322 | |
Abdominal pain | 1.7 (1.0–2.0) | 1.7 (1.0–2.0) | 0.722 | |
Reflux | 1.0 (1.0–2.0) | 1.0 (1.0–2.0) | 0.483 | |
Diarrhoea | 1.3 (1.0–2.0) | 1.3 (1.0–2.7) | 0.045 | |
Indigestion | 2.0 (1.5–2.8) | 2.0 (1.5–2.5) | 0.931 | |
Constipation | 1.3 (1.0–2.3) | 1.7 (1.0–2.3) | 0.570 | |
PGWB scores 2 | ||||
Total score | 110 (99–117) | 103 (94–118) | 0.083 | |
Anxiety | 26 (23–27) | 25 (22–27) | 0.364 | |
Depressed mood | 17 (16–18) | 17 (15–18) | 0.181 | |
Positive well-being | 18 (16–20) | 17 (15–20) | 0.266 | |
Self-control | 16 (15–17) | 15 (14–17) | 0.145 | |
General health | 14 (12–16) | 13 (11–15) | 0.020 | |
Vitality | 19 (17–21) | 18 (15–20) | 0.025 | |
DLQI score 3, 4 | 0 (0–0) | 0 (0–1) | 0.028 |
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Alakoski, A.; Hervonen, K.; Mansikka, E.; Reunala, T.; Kaukinen, K.; Kivelä, L.; Laurikka, P.; Huhtala, H.; Kurppa, K.; Salmi, T. The Long-Term Safety and Quality of Life Effects of Oats in Dermatitis Herpetiformis. Nutrients 2020, 12, 1060. https://doi.org/10.3390/nu12041060
Alakoski A, Hervonen K, Mansikka E, Reunala T, Kaukinen K, Kivelä L, Laurikka P, Huhtala H, Kurppa K, Salmi T. The Long-Term Safety and Quality of Life Effects of Oats in Dermatitis Herpetiformis. Nutrients. 2020; 12(4):1060. https://doi.org/10.3390/nu12041060
Chicago/Turabian StyleAlakoski, Anna, Kaisa Hervonen, Eriika Mansikka, Timo Reunala, Katri Kaukinen, Laura Kivelä, Pilvi Laurikka, Heini Huhtala, Kalle Kurppa, and Teea Salmi. 2020. "The Long-Term Safety and Quality of Life Effects of Oats in Dermatitis Herpetiformis" Nutrients 12, no. 4: 1060. https://doi.org/10.3390/nu12041060
APA StyleAlakoski, A., Hervonen, K., Mansikka, E., Reunala, T., Kaukinen, K., Kivelä, L., Laurikka, P., Huhtala, H., Kurppa, K., & Salmi, T. (2020). The Long-Term Safety and Quality of Life Effects of Oats in Dermatitis Herpetiformis. Nutrients, 12(4), 1060. https://doi.org/10.3390/nu12041060