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Enteropathy in Psoriasis: A Systematic Review of Gastrointestinal Disease Epidemiology and Subclinical Inflammatory and Functional Gut Alterations

  • Psoriasis (J Wu, Section Editor)
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Abstract

Purpose of Review

Psoriasis in an inflammatory skin disorder associated with systemic inflammation. This systematic review summarizes the epidemiology, histology, and function of the gastrointestinal (GI) system in patients with psoriasis.

Recent Findings

Although psoriasis patients are at higher risk for developing inflammatory bowel disease and celiac disease, estimates of their prevalence have varied and it is unclear whether psoriasis patients without GI symptoms may harbor subclinical inflammation.

Summary

In a meta-analysis, the pooled prevalence of Crohn disease, ulcerative colitis (UC), and celiac disease among patients with psoriasis was 0.4, 0.5, and 2%, respectively. The pooled prevalence of psoriasis among patients with Crohn disease was 9.5% and among patients with UC was 6.6%. A significant proportion of psoriasis patients harbor lymphocytic infiltrates in the small and large intestine; 40–50% of the psoriasis patients demonstrate abnormal intestinal absorption based on fecal fat, D-xylose, and lactose tolerance tests. These results suggest that the inflammatory state of psoriasis may in some patients extend to the GI tract.

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References

Recently published papers of particular interest have been highlighted as: • Of importance •• Of major importance

  1. •• Rachakonda TD, Schupp CW, Armstrong AW. Psoriasis prevalence among adults in the United States. J Am Acad Dermatol. 2014;70(3):512–6. https://doi.org/10.1016/j.jaad.2013.11.013. Provides the most recently updated prevalence of physician-diagnosed psoriasis in the United States, from a multi-site national population.

    Article  PubMed  Google Scholar 

  2. Najarian DJ, Gottlieb AB. Connections between psoriasis and Crohn’s disease. J Am Acad Dermatol. 2003;48(6):805–21; quiz 22-4. https://doi.org/10.1067/mjd.2003.540.

    Article  PubMed  Google Scholar 

  3. Chodorowska G, Wojnowska D, Juszkiewicz-Borowiec M. C-reactive protein and α2-macroglobulin plasma activity in medium-severe and severe psoriasis. J Eur Acad Dermatol Venereol. 2004;18(2):180–3. https://doi.org/10.1111/j.1468-3083.2004.00863.x.

    Article  CAS  PubMed  Google Scholar 

  4. Nielsen HJ, Christensen IJ, Svendsen MN, Hansen U, Werther K, Brunner N, et al. Elevated plasma levels of vascular endothelial growth factor and plasminogen activator inhibitor-1 decrease during improvement of psoriasis. Inflamm Res. 2002;51(11):563–7. https://doi.org/10.1007/PL00012428.

    Article  CAS  PubMed  Google Scholar 

  5. Vanizor Kural B, Orem A, Cimsit G, Uydu HA, Yandi YE, Alver A. Plasma homocysteine and its relationships with atherothrombotic markers in psoriatic patients. Clin Chim Acta. 2003;332(1–2):23–30. https://doi.org/10.1016/S0009-8981(03)00082-2.

    Article  CAS  PubMed  Google Scholar 

  6. Vanizor Kural B, Orem A, Cimsit G, Yandi YE, Calapoglu M. Evaluation of the atherogenic tendency of lipids and lipoprotein content and their relationships with oxidant-antioxidant system in patients with psoriasis. Clin Chim Acta. 2003;328(1–2):71–82. https://doi.org/10.1016/S0009-8981(02)00373-X.

    Article  CAS  PubMed  Google Scholar 

  7. Mehta NN, Torigian DA, Gelfand JM, Saboury B, Alavi A. Quantification of atherosclerotic plaque activity and vascular inflammation using [18-F] fluorodeoxyglucose positron emission tomography/computed tomography (FDG-PET/CT). J Visual Exp. 2012;63(63):e3777. https://doi.org/10.3791/3777.

    Google Scholar 

  8. Mehta NN, Yu Y, Saboury B, Foroughi N, Krishnamoorthy P, Raper A, et al. Systemic and vascular inflammation in patients with moderate to severe psoriasis as measured by [18F]-fluorodeoxyglucose positron emission tomography-computed tomography (FDG-PET/CT): a pilot study. Arch Dermatol. 2011;147(9):1031–9. https://doi.org/10.1001/archdermatol.2011.119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Rose S, Sheth NH, Baker JF, Ogdie A, Raper A, Saboury B, et al. A comparison of vascular inflammation in psoriasis, rheumatoid arthritis, and healthy subjects by FDG-PET/CT: a pilot study. Am J Cardiovasc Dis. 2013;3(4):273–8.

    PubMed  PubMed Central  Google Scholar 

  10. Yu Y, Sheth N, Krishnamoorthy P, Saboury B, Raper A, Baer A, et al. Aortic vascular inflammation in psoriasis is associated with HDL particle size and concentration: a pilot study. Am J Cardiovasc Dis. 2012;2(4):285–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Gottlieb AB, Dann F. Comorbidities in patients with psoriasis. Am J Med. 2009;122(12):1150.e1–9. https://doi.org/10.1016/j.amjmed.2009.06.021.

    Article  Google Scholar 

  12. Ford AC, Moayyedi P, Hanauer SB. Ulcerative colitis. BMJ (Clin Res Ed). 2013;346:f432. https://doi.org/10.1136/bmj.f432.

    Google Scholar 

  13. Lichtenstein GR, Hanauer SB, Sandborn WJ. Management of Crohn’s disease in adults. Am J Gastroenterol. 2009;104(2):465–83; quiz 4, 84. https://doi.org/10.1038/ajg.2008.168.

    Article  PubMed  Google Scholar 

  14. Menter A, Gottlieb A, Feldman SR, Van Voorhees AS, Leonardi CL, Gordon KB, et al. Guidelines of care for the management of psoriasis and psoriatic arthritis: section 1. Overview of psoriasis and guidelines of care for the treatment of psoriasis with biologics. J Am Acad Dermatol. 2008;58(5):826–50. https://doi.org/10.1016/j.jaad.2008.02.039.

    Article  PubMed  Google Scholar 

  15. Dideberg V, Kristjansdottir G, Milani L, Libioulle C, Sigurdsson S, Louis E, et al. An insertion-deletion polymorphism in the interferon regulatory factor 5 (IRF5) gene confers risk of inflammatory bowel diseases. Hum Mol Genet. 2007;16(24):3008–16. https://doi.org/10.1093/hmg/ddm259.

    Article  CAS  PubMed  Google Scholar 

  16. Sanchez FO, Linga Reddy MV, Mallbris L, Sakuraba K, Stahle M, Alarcon-Riquelme ME. IFN-regulatory factor 5 gene variants interact with the class I MHC locus in the Swedish psoriasis population. J Invest Dermatol. 2008;128(7):1704–9. https://doi.org/10.1038/sj.jid.5701254.

    Article  CAS  PubMed  Google Scholar 

  17. Ellinghaus D, Ellinghaus E, Nair RP, Stuart PE, Esko T, Metspalu A, et al. Combined analysis of genome-wide association studies for Crohn disease and psoriasis identifies seven shared susceptibility loci. Am J Hum Genet. 2012;90(4):636–47. https://doi.org/10.1016/j.ajhg.2012.02.020.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cargill M, Schrodi SJ, Chang M, Garcia VE, Brandon R, Callis KP, et al. A large-scale genetic association study confirms IL12B and leads to the identification of IL23R as psoriasis-risk genes. Am J Hum Genet. 2007;80(2):273–90. https://doi.org/10.1086/511051.

    Article  CAS  PubMed  Google Scholar 

  19. Duerr RH, Taylor KD, Brant SR, Rioux JD, Silverberg MS, Daly MJ, et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science (New York, NY). 2006;314(5804):1461–3. https://doi.org/10.1126/science.1135245.

    Article  CAS  Google Scholar 

  20. Nunez C, Dema B, Cenit MC, Polanco I, Maluenda C, Arroyo R, et al. IL23R: a susceptibility locus for celiac disease and multiple sclerosis? Genes Immun. 2008;9(4):289–93. https://doi.org/10.1038/gene.2008.16.

    Article  CAS  PubMed  Google Scholar 

  21. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ (Clin Res Ed). 2003;327(7414):557–60. https://doi.org/10.1136/bmj.327.7414.557.

    Article  Google Scholar 

  22. Makredes M, Robinson D Jr, Bala M, Kimball AB. The burden of autoimmune disease: a comparison of prevalence ratios in patients with psoriatic arthritis and psoriasis. J Am Acad Dermatol. 2009;61(3):405–10. https://doi.org/10.1016/j.jaad.2009.02.015.

    Article  PubMed  Google Scholar 

  23. •• Vanaclocha F, Crespo-Erchiga V, Jiménez-Puya R, Puig L, Sánchez-Carazo JL, Ferrán M, et al. Immune-mediated inflammatory diseases and other comorbidities in patients with psoriasis: baseline characteristics of patients in the AQUILES study. Actas Dermo-Sifiliograficas. 2015;106(1):35–43. https://doi.org/10.1016/j.ad.2014.06.003. Indicates the prevalence of comorbidities with psoriasis in Spain. This study was from a multicenter population, and psoriasis data used in this study was diagnosed by physicians.

    Article  CAS  PubMed  Google Scholar 

  24. Augustin M, Glaeske G, Radtke MA, Christophers E, Reich K, Schäfer I. Epidemiology and comorbidity of psoriasis in children. Br J Dermatol. 2010;162(3):633–6. https://doi.org/10.1111/j.1365-2133.2009.09593.x.

    Article  CAS  PubMed  Google Scholar 

  25. •• Kelati A, Baybay H, Najdi A, Zinoune S, Mernissi FZ. Pediatric psoriasis: should we be concerned with comorbidity? Cross-sectional study. Pediatr Int. 2017;59(8):923–8. https://doi.org/10.1111/ped.13309. Describes the prevalence of GI disease and other comorbidities among pediatric psoriasis patients in Morocco, a unique study population.

    Article  PubMed  Google Scholar 

  26. •• Zisman D, Gladman DD, Stoll ML, Strand V, Lavi I, Hsu JJ, et al. The juvenile psoriatic arthritis cohort in the CARRA registry: clinical characteristics, classification, and outcomes. J Rheumatol. 2017;44(3):342–51. https://doi.org/10.3899/jrheum.160717. This article provides the prevalence of GI disease among pediatric psoriasis patients in the United States and Canada. This study was from a multisite, international population and psoriasis data used in this study was diagnosed by physicians.

    Article  PubMed  Google Scholar 

  27. Cohen AD, Dreiher J, Birkenfeld S. Psoriasis associated with ulcerative colitis and Crohn’s disease. J Eur Acad Dermatol Venereol. 2009;23(5):561–5. https://doi.org/10.1111/j.1468-3083.2008.03031.x.

    Article  CAS  PubMed  Google Scholar 

  28. •• Egeberg A, Mallbris L, Warren RB, Bachelez H, Gislason GH, Hansen PR, et al. Association between psoriasis and inflammatory bowel disease: a Danish nationwide cohort study. Br J Dermatol. 2016;175(3):487–92. https://doi.org/10.1111/bjd.14528. This article provides the prevalence of GI disease in psoriasis patients in Denmark. This study was from a multisite, national population, and psoriasis data used in this study was assessed according to hospital visits and medication.

    Article  CAS  PubMed  Google Scholar 

  29. Li WQ, Han JL, Chan AT, Qureshi AA. Psoriasis, psoriaticarthritis and increased risk of incident Crohn’s disease in US women. Ann Rheum Dis. 2013;72(7):1200–5. https://doi.org/10.1136/annrheumdis-2012-202143.

    Article  PubMed  Google Scholar 

  30. •• Lolli E, Saraceno R, Calabrese E, Ascolani M, Scarozza P, Chiricozzi A, et al. Psoriasis phenotype in inflammatory bowel disease: a case-control prospective study. J Crohn's Colitis. 2015;9(9):699–707. https://doi.org/10.1093/ecco-jcc/jjv068. This article provides the prevalence of psoriasis in patients with GI disease in Italy. This study was from a multisite, national population. Both GI and psoriasis data used in this study were as diagnosed by physicians.

    Article  Google Scholar 

  31. •• Park HS, Koh SJ, Park GY, Lee DH, Yoon HS, Youn JI, et al. Psoriasis concurrent with inflammatory bowel disease. J Eur Acad Dermatol Venereol. 2014;28(11):1436–41. https://doi.org/10.1111/jdv.12305. This article provides the prevalence of psoriasis in patients with GI disease in Italy. This study was from a multisite, national population. Both GI and psoriasis data used in this study were diagnosed by physicians.

    Article  CAS  PubMed  Google Scholar 

  32. •• Zohar A, Cohen AD, Bitterman H, Feldhamer I, Greenberg-Dotan S, Lavi I, et al. Gastrointestinal comorbidities in patients with psoriatic arthritis. Clin Rheumatol. 2016;35(11):2679–84. https://doi.org/10.1007/s10067-016-3374-y. This article provides the prevalence of GI disease in Jewish and Arabic psoriasis patients in Israel, which is one of the few publications that specifies ethnicity. This study was from a multisite, national population. Psoriasis and GI data used in this study were diagnosed by physicians.

    Article  PubMed  Google Scholar 

  33. Augustin M, Reich K, Glaeske G, Schaefer I, Radtke M. Co-morbidity and age-related prevalence of psoriasis: analysis of health insurance data in Germany. Acta Derm Venereol. 2010;90(2):147–51. https://doi.org/10.2340/00015555-0770.

    Article  PubMed  Google Scholar 

  34. Cantini F, Niccoli L, Nannini C, Cassarà E, Kaloudi O, Rizzello F, et al. Case-control study on dactylitis, enthesitis, and anterior uveitis in spondyloarthritis associated with inflammatory bowel diseases: role of coexistent psoriasis. J Rheumatol. 2017;44(9):1341–6. https://doi.org/10.3899/jrheum.161518.

    Article  PubMed  Google Scholar 

  35. •• De Bastiani R, Gabrielli M, Lora L, Napoli L, Tosetti C, Pirrotta E, et al. Association between coeliac disease and psoriasis: Italian primary care multicentre study. Dermatol (Basel, Switzerland). 2015;230(2):156–60. https://doi.org/10.1159/000369615. Indicates the prevalence of celiac disease in psoriasis patients in Italy. This study was from a multisite, national population. Both celiac disease and psoriasis data used in this study were as diagnosed by physicians.

    Article  Google Scholar 

  36. Ojetti V, De Simone C, Sanchez JA, Capizzi R, Migneco A, Guerriero C, et al. Malabsorption in psoriatic patients: cause or consequence? Scand J Gastroenterol. 2006;41(11):1267–71. https://doi.org/10.1080/00365520600633529.

    Article  PubMed  Google Scholar 

  37. Birkenfeld S, Dreiher J, Weitzman D, Cohen AD. Coeliac disease associated with psoriasis. Br J Dermatol. 2009;161(6):1331–4. https://doi.org/10.1111/j.1365-2133.2009.09398.x.

    Article  CAS  PubMed  Google Scholar 

  38. Khraishi M, MacDonald D, Rampakakis E, Vaillancourt J, Sampalis JS. Prevalence of patient-reported comorbidities in early and established psoriatic arthritis cohorts. Clin Rheumatol. 2011;30(7):877–85. https://doi.org/10.1007/s10067-011-1692-7.

    Article  PubMed  Google Scholar 

  39. Lindqvist U, Rudsander Å, Boström Å, Nilsson B, Michaëlsson G. IgA antibodies to gliadin and coeliac disease in psoriatic arthritis. Rheumatology. 2002;41(1):31–7. https://doi.org/10.1093/rheumatology/41.1.31.

    Article  CAS  PubMed  Google Scholar 

  40. Ludvigsson JF, Lindelöf B, Zingone F, Ciacci C. Psoriasis in a nationwide cohort study of patients with celiac disease. J Investig Dermatol. 2011;131(10):2010–6. https://doi.org/10.1038/jid.2011.162.

    Article  CAS  PubMed  Google Scholar 

  41. •• Eppinga H, Poortinga S, Thio HB, Nijsten TEC, Nuij VJAA, Van Der Woude CJ, et al. Prevalence and phenotype of concurrent psoriasis and inflammatory bowel disease. Inflamm Bowel Dis. 2017;23(10):1783–9. https://doi.org/10.1097/MIB.0000000000001169. Describes the prevalence of GI disease in psoriasis patients in the Netherlands. This study was from a multisite, national population. GI and psoriasis data used in this study were diagnosed by physicians.

    Article  PubMed  Google Scholar 

  42. Tsai TF, Wang TS, Hung ST, Tsai PIC, Schenkel B, Zhang M, et al. Epidemiology and comorbidities of psoriasis patients in a national database in Taiwan. J Dermatol Sci. 2011;63(1):40–6. https://doi.org/10.1016/j.jdermsci.2011.03.002.

    Article  PubMed  Google Scholar 

  43. Woo WK, McMillan SA, Watson RGP, McCluggage WG, Sloan JM, McMillan JC. Coeliac disease-associated antibodies correlate with psoriasis activity. Br J Dermatol. 2004;151(4):891–4. https://doi.org/10.1111/j.1365-2133.2004.06137.x.

    Article  CAS  PubMed  Google Scholar 

  44. Yates VM, Watkinson G, Kelman A. Further evidence for an association between psoriasis, Crohn’s disease and ulcerative colitis. Br J Dermatol. 1982;106(3):323–30.

    Article  CAS  PubMed  Google Scholar 

  45. World Health Organization Regions. 2017. http://www.who.int/about/regions/en/. Accessed December 8, 2017.

  46. Kia KF, Nair RP, Ike RW, Hiremagalore R, Elder JT, Ellis CN. Prevalence of antigliadin antibodies in patients with psoriasis is not elevated compared with controls. Am J Clin Dermatol. 2007;8(5):301–5. https://doi.org/10.2165/00128071-200708050-00005.

    Article  PubMed  Google Scholar 

  47. Lindqvist U, Kristjansson G, Pihl-Lundin I, Hagforsen E, Michaelsson G. Patients with psoriatic arthritis have an increased number of lymphocytes in the duodenal mucosa in comparison with patients with psoriasis vulgaris. J Rheumatol. 2006;33(5):924–7.

    PubMed  Google Scholar 

  48. Ojetti V, Aguilar Sanchez J, Guerriero C, Fossati B, Capizzi R, De Simone C, et al. High prevalence of celiac disease in psoriasis. Am J Gastroenterol. 2003;98(11):2574–5. https://doi.org/10.1111/j.1572-0241.2003.08684.x.

    Article  CAS  PubMed  Google Scholar 

  49. Khardikova SA, Nepomnyashchikh GI, Aidagulova SV, Lapii GA. Ultrastructural characteristics of cell populations in the gastric and duodenal mucosa during psoriasis. Bull Exp Biol Med. 2002;134(5):489–93. https://doi.org/10.1023/A:1022658818267.

    Article  CAS  PubMed  Google Scholar 

  50. Michaelsson G, Gerden B, Hagforsen E, Nilsson B, Pihl-Lundin I, Kraaz W, et al. Psoriasis patients with antibodies to gliadin can be improved by a gluten-free diet. Br J Dermatol. 2000;142(1):44–51. https://doi.org/10.1046/j.1365-2133.2000.03240.x.

    Article  CAS  PubMed  Google Scholar 

  51. Michaelsson G, Kraaz W, Hagforsen E, Pihl-Lundin I, Loof L, Scheynius A. The skin and the gut in psoriasis: the number of mast cells and CD3+ lymphocytes is increased in non-involved skin and correlated to the number of intraepithelial lymphocytes and mast cells in the duodenum. Acta Derm Venereol. 1997;77(5):343–6.

    CAS  PubMed  Google Scholar 

  52. Michaelsson G, Kraaz W, Hagforsen E, Pihl-Lundin I, Loof L. Psoriasis patients have highly increased numbers of tryptase-positive mast cells in the duodenal stroma. Br J Dermatol. 1997;136(6):866–70.

    Article  CAS  PubMed  Google Scholar 

  53. Michaelsson G, Kraaz W, Gerden B, Hagforsen E, Lundin IP, Loof L, et al. Patients with psoriasis have elevated levels of serum eosinophil cationic protein and increased numbers of EG2 positive eosinophils in the duodenal stroma. Br J Dermatol. 1996;135(3):371–8. https://doi.org/10.1111/j.1365-2133.1996.tb01498.x.

    Article  CAS  PubMed  Google Scholar 

  54. Michaelsson G, Kraaz W, Gerden B, Hagforsen E, Hjelmqvist G, Loof L, et al. Increased lymphocyte infiltration in duodenal mucosa from patients with psoriasis and serum IgA antibodies to gliadin. Br J Dermatol. 1995;133(6):896–904. https://doi.org/10.1111/j.1365-2133.1995.tb06922.x.

    Article  CAS  PubMed  Google Scholar 

  55. Hendel L, Larsen JK, Ammitzboll T, Asboe-Hansen G. A study of cell proliferation kinetics in the small intestinal epithelium of psoriasis patients. Clin Exp Dermatol. 1984;9(4):329–35. https://doi.org/10.1111/j.1365-2230.1984.tb00812.x.

    Article  CAS  PubMed  Google Scholar 

  56. Hendel L, Hendel J, Johnsen A, Gudmand-Hoyer E. Intestinal function and methotrexate absorption in psoriatic patients. Clin Exp Dermatol. 1982;7(5):491–7. https://doi.org/10.1111/j.1365-2230.1982.tb02465.x.

    Article  CAS  PubMed  Google Scholar 

  57. Bansal NK, Mathur KN, Sharma RP. Histopathological studies of intestinal (jejunal) mucosa in psoriasis and exfoliative dermatitis. Ind J Dermatol Venereol Leprol. 1980;46(5):274–81.

    Google Scholar 

  58. Bedi TR, Bhutani LK, Kandhari KC, Tandon BN. Small bowel in skin diseases. Indian J Med Res. 1974;62(1):142–9.

    CAS  PubMed  Google Scholar 

  59. Madanagopalan N, Shantha M, Rao UP, Thambiah AS. Peroral jejunal mucosal biopsy in dermatological and some non-diarrhoeal diseases. Aust J Dermatol. 1973;14(1):47–52.

    Article  CAS  Google Scholar 

  60. Barry RE, Salmon PR, Read AE, Warin RP. Mucosal architecture of the small bowel in cases of psoriasis. Gut. 1971;12(11):873–7. https://doi.org/10.1136/gut.12.11.873.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Roberts DM, Preston FE. Intestinal disaccharidase activity in psoriatic enteropathy. Scand J Gastroenterol. 1971;6(1):93–6. https://doi.org/10.3109/00365527109180676.

    Article  CAS  PubMed  Google Scholar 

  62. Themann H, Preston FE, Roberts DM, Knust FJ. Electron microscope findings in the jejunal mucosa of patients with psoriasis. Arch Klin Exp Dermatol. 1970;238(4):323–32. https://doi.org/10.1007/BF00525726.

    Article  CAS  PubMed  Google Scholar 

  63. Shuster S, Watson AJ, Marks J. Small intestine in psoriasis. Br Med J. 1967;3(5563):458–60. https://doi.org/10.1136/bmj.3.5563.458.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Scarpa R, Manguso F, D’Arienzo A, D’Armiento FP, Astarita C, Mazzacca G, et al. Microscopic inflammatory changes in colon of patients with both active psoriasis and psoriatic arthritis without bowel symptoms. J Rheumatol. 2000;27(5):1241–6.

    CAS  PubMed  Google Scholar 

  65. Schatteman L, Mielants H, Veys EM, Cuvelier C, De Vos M, Gyselbrecht L, et al. Gut inflammation in psoriatic arthritis: a prospective ileocolonoscopic study. J Rheumatol. 1995;22(4):680–3.

    CAS  PubMed  Google Scholar 

  66. Preger L, Maibach HI, Osborne RB, Shapiro HA, Lee JC. On the question of psoriatic enteropathy. Arch Dermatol. 1970;102(2):151–3. https://doi.org/10.1001/archderm.1970.04000080023004.

    Article  CAS  PubMed  Google Scholar 

  67. Marks J, Shuster S. Small-intestinal mucosal abnormalities in various skin diseases—fact or fancy? Gut. 1970;11(4):281–91. https://doi.org/10.1136/gut.11.4.281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Humbert P, Bidet A, Treffel P, Drobacheff C, Agache P. Intestinal permeability in patients with psoriasis. J Dermatol Sci. 1991;2(4):324–6. https://doi.org/10.1016/0923-1811(91)90057-5.

    Article  CAS  PubMed  Google Scholar 

  69. Hamilton I, Fairris GM, Rothwell J, Cunliffe WJ, Dixon MF, Axon AT. Small intestinal permeability in dermatological disease. Q J Med. 1985;56(221):559–67.

    CAS  PubMed  Google Scholar 

  70. Chapman PH, Kersey PJ, Keys B, Shuster S, Rawlins MD. Generalised tissue abnormality of aryl hydrocarbon hydroxylase in psoriasis. Br Med J. 1980;281(6251):1315–6. https://doi.org/10.1136/bmj.281.6251.1315.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Summerly R, Giles C. Question of psoriatic enteropathy. Arch Dermatol. 1971;103(6):678–9. https://doi.org/10.1001/archderm.1971.04000180104016.

    Article  CAS  PubMed  Google Scholar 

  72. Knowles JP, Shuster S, Wells GC. Folic-acid deficiency in patients with skin disease. Lancet (London, England). 1963;1(7291):1138–9.

    Article  CAS  Google Scholar 

  73. Naldi L, Mercuri SR. Epidemiology of comorbidities in psoriasis. Dermatol Ther. 2010;23(2):114–8. https://doi.org/10.1111/j.1529-8019.2010.01304.x.

    Article  PubMed  Google Scholar 

  74. • Takeshita J, Grewal S, Langan SM, Mehta NN, Ogdie A, Van Voorhees AS, et al. Psoriasis and comorbid diseases: implications for management. J Am Acad Dermatol. 2017;76(3):393–403. https://doi.org/10.1016/j.jaad.2016.07.065. Provides a brief summary and discussion of IBD in psoriasis, highlighting some high-quality important studies that our review has also covered. However, there are many publications that were not included in this discussion. The main focus of this article was on cardiometabolic comorbidities and risk factors associated with psoriasis.

    Article  PubMed  Google Scholar 

  75. Scher JU, Ubeda C, Artacho A, Attur M, Isaac S, Reddy SM, et al. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol (Hoboken, NJ). 2015;67(1):128–39. https://doi.org/10.1002/art.38892.

    Article  CAS  Google Scholar 

  76. Ahadi Z, Shafiee G, Razmandeh R, Keshtkar AA, Najafi Sani M, Azemati B, et al. Prevalence of celiac disease among the Iranian population: a systematic review and meta-analysis of observational studies. Turk J Gastroenterol. 2016;27(2):122–8. https://doi.org/10.5152/tjg.2015.150191.

    Article  PubMed  Google Scholar 

  77. Altobelli E, Paduano R, Petrocelli R, Di Orio F. Burden of celiac disease in Europe: a review of its childhood and adulthood prevalence and incidence as of September 2014. Ann Ig. 2014;26(6):485–98. https://doi.org/10.7416/ai.2014.2007.

    CAS  PubMed  Google Scholar 

  78. Dehghani SM, Haghighat M, Mobayen A, Rezaianzadeh A, Geramizadeh B. Prevalence of celiac disease in healthy Iranian school children. Ann Saudi Med. 2013;33(2):159–61. https://doi.org/10.5144/0256-4947.2013.159.

    Article  PubMed  Google Scholar 

  79. Garnier-Lengline H, Cerf-Bensussan N, Ruemmele FM. Celiac disease in children. Clin Res Hepatol Gastroenterol. 2015;39(5):544–51. https://doi.org/10.1016/j.clinre.2015.05.024.

    Article  CAS  PubMed  Google Scholar 

  80. Kratzer W, Kibele M, Akinli A, Porzner M, Boehm BO, Koenig W, et al. Prevalence of celiac disease in Germany: a prospective follow-up study. World J Gastroenterol. 2013;19(17):2612–20. https://doi.org/10.3748/wjg.v19.i17.2612.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Laass MW, Schmitz R, Uhlig HH, Zimmer KP, Thamm M, Koletzko S. The prevalence of celiac disease in children and adolescents in Germany. Dtsch Arztebl Int. 2015;112(33–34):553–60. https://doi.org/10.3238/arztebl.2015.0553.

    PubMed  PubMed Central  Google Scholar 

  82. Mardini HE, Westgate P, Grigorian AY. Racial differences in the prevalence of celiac disease in the US population: National Health and Nutrition Examination Survey (NHANES) 2009–2012. Dig Dis Sci. 2015;60(6):1738–42. https://doi.org/10.1007/s10620-014-3514-7.

    Article  PubMed  Google Scholar 

  83. Parra-Medina R, Molano-Gonzalez N, Rojas-Villarraga A, Agmon-Levin N, Arango MT, Shoenfeld Y, et al. Prevalence of celiac disease in Latin America: a systematic review and meta-regression. PLoS One. 2015;10(5):e0124040. https://doi.org/10.1371/journal.pone.0124040.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Rubio-Tapia A, Ludvigsson JF, Brantner TL, Murray JA, Everhart JE. The prevalence of celiac disease in the United States. Am J Gastroenterol. 2012;107(10):1538–44; quiz 7, 45. https://doi.org/10.1038/ajg.2012.219.

    Article  PubMed  Google Scholar 

  85. Savvateeva LV, Erdes SI, Antishin AS, Zamyatnin AA Jr. Overview of celiac disease in Russia: regional data and estimated prevalence. J Immunol Res. 2017;2017:2314813. https://doi.org/10.1155/2017/2314813.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Singh P, Arora S, Singh A, Strand TA, Makharia GK. Prevalence of celiac disease in Asia: a systematic review and meta-analysis. J Gastroenterol Hepatol. 2016;31(6):1095–101. https://doi.org/10.1111/jgh.13270.

    Article  PubMed  Google Scholar 

  87. Unalp-Arida A, Ruhl CE, Choung RS, Brantner TL, Murray JA. Lower prevalence of celiac disease and gluten-related disorders in persons living in southern vs northern latitudes of the United States. Gastroenterology. 2017;152(8):1922–32.e2. https://doi.org/10.1053/j.gastro.2017.02.012.

    Article  PubMed  Google Scholar 

  88. Kappelman MD, Rifas-Shiman SL, Kleinman K, Ollendorf D, Bousvaros A, Grand RJ, et al. The prevalence and geographic distribution of Crohn’s disease and ulcerative colitis in the United States. Clin Gastroenterol Hepatol. 2007;5(12):1424–9. https://doi.org/10.1016/j.cgh.2007.07.012.

    Article  PubMed  Google Scholar 

  89. Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 2012;142(1):46–54.e42; quiz e30. https://doi.org/10.1053/j.gastro.2011.10.001.

    Article  PubMed  Google Scholar 

  90. • Ungprasert P, Wijarnpreecha K, Kittanamongkolchai W. Psoriasis and risk of celiac disease: a systematic review and meta-analysis. Ind J Dermatol. 2017;62(1):41–6. https://doi.org/10.4103/0019-5154.198031. This meta-analysis examines celiac disease risk among psoriasis patients, but may be limited by the questionable quality and small number of participants.

    Article  Google Scholar 

  91. Ye L, Cao Q, Cheng J. Review of inflammatory bowel disease in China. TheScientificWorldJOURNAL. 2013;2013:296470. https://doi.org/10.1155/2013/296470.

    Article  PubMed  PubMed Central  Google Scholar 

  92. Weng SW, Chen BC, Wang YC, Liu CK, Sun MF, Chang CM, et al. Traditional Chinese medicine use among patients with psoriasis in Taiwan: a nationwide population-based study. Evid Based Complement Alternat Med. 2016;2016:3164105. https://doi.org/10.1155/2016/3164105.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Marks J, Shuster S. Psoriatic enteropathy. Arch Dermatol. 1971;103(6):676–8. https://doi.org/10.1001/archderm.1971.04000180102014.

    Article  CAS  PubMed  Google Scholar 

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Author notes

  1. Isabelle M. Sanchez and Wei Jiang contributed equally to this work.

Authors and Affiliations

  1. Department of Dermatology, University of California, San Francisco, San Francisco, CA, USA

    Isabelle M. Sanchez, Wei Jiang, Eric J. Yang, Rasnik K. Singh, Kristen Beck, Ladan Afifi & Wilson Liao

  2. University of Illinois at Chicago College of Medicine, Chicago, IL, USA

    Isabelle M. Sanchez

  3. Department of Dermatology, Peking University Third Hospital, Beijing, China

    Wei Jiang

  4. Chicago Medical School, Rosalind Franklin University of Medicine and Science, North Chicago, IL, USA

    Eric J. Yang

  5. Department of Internal Medicine, Yale School of Medicine, New Haven, CT, USA

    Rasnik K. Singh

  6. Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA

    Claire Liu

  7. University of Miami Miller School of Medicine, Miami, FL, USA

    Ladan Afifi

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  1. Isabelle M. Sanchez
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Correspondence to Wilson Liao.

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IS, WJ, EY, RS, KB, CL, LA declare that they have no conflict of interest.

Wilson Liao has received research funding from AbbVie, Janssen, Novartis, and Pfizer.

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Sanchez, I.M., Jiang, W., Yang, E.J. et al. Enteropathy in Psoriasis: A Systematic Review of Gastrointestinal Disease Epidemiology and Subclinical Inflammatory and Functional Gut Alterations. Curr Derm Rep 7, 59–74 (2018). https://doi.org/10.1007/s13671-018-0213-1

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