Almanac of Clinical MedicineAlmanac of Clinical MedicineАльманах клинической медицины2072-05052587-9294Moscow Regional Research and Clinical Institute (MONIKI)116310.18786/2072-0505-2019-47-062REVIEW ARTICLEОБЗОРPsoriasis and inflammatory bowel diseases: pathogenetic pathways and the choice of biologic therapy (a literature review)Псориаз и воспалительные заболевания кишечника: пути патогенеза и вопросы выбора генно-инженерных препаратов (обзор литературы)https://orcid.org/0000-0002-5044-5265KruglovaL. S.КругловаЛ. С.
Russian Federation

Larisa S. Kruglova – MD, PhD, Professor, Head of the Chair of Dermatovenereology and Cosmetology

19/1A Marshala Timoshenko ul., Moscow, 121359

Круглова Лариса Сергеевна – доктор медицинских наук, профессор, заведующая кафедрой дерматовенерологии и косметологии

121359, г. Москва, ул. Маршала Тимошенко, 19/1А

kruglovals@mail.ruhttps://orcid.org/0000-0002-3875-4030LvovA. N.ЛьвовА. Н.
Russian Federation

Andrey N. Lvov – MD, PhD, Professor, Head of the Department of Clinical Dermatovenereology and Cosmetology

17 Leninskiy prospekt, Moscow, 119071

Львов Андрей Николаевич – доктор медицинских наук, профессор, руководитель отдела клинической дерматовенерологии и косметологии

119071, г. Москва, Ленинский проспект, 17

alvov@mail.ruKagramanovaA. V.КаграмановаА. В.
Russian Federation

Anna V. Kagramanova – MD, PhD, Senior Research Fellow, Department of Inflammatory Bowel Diseases

86 Shosse Entuziastov, Moscow, 111123

Каграманова Анна Валерьевна – кандидат медицинских наук, старший научный сотрудник отделения лечения воспалительных заболеваний кишечника

111123, г. Москва, шоссе Энтузиастов, 86

a.kagramanova@mknc.ruKnyazevO. V.КнязевО. В.
Russian Federation

Oleg V. Knyazev – MD, PhD, Head of the Department of Inflammatory Bowel Diseases

86 Shosse Entuziastov, Moscow, 111123

Князев Олег Владимирович – доктор медицинских наук, заведующий отделением лечения воспалительных заболеваний кишечника

111123, г. Москва, шоссе Энтузиастов, 86

o.knyazev@mknc.ruCentral State Medical Academy of the Presidential Administration of the Russian FederationФГБУ ДПО «Центральная государственная медицинская академия» УД Президента РФMoscow Scientific and Practical Center of Dermatovenereology and CosmetologyГБУЗ г. Москвы «Московский научно-практический центр дерматовенерологии и косметологии Департамента здравоохранения г. Москвы»Loginov Moscow Clinical Scientific Center, Moscow Healthcare DepartmentГБУЗ г. Москвы «Московский клинический научно-практический центр имени А.С. Логинова Департамента здравоохранения г. Москвы»221220194765685781311201913112019Copyright ©; 2019, Kruglova L.S., Lvov A.N., Kagramanova A.V., Knyazev O.V.Copyright ©; 2019, Круглова Л.С., Львов А.Н., Каграманова А.В., Князев О.В.2019Kruglova L.S., Lvov A.N., Kagramanova A.V., Knyazev O.V.Круглова Л.С., Львов А.Н., Каграманова А.В., Князев О.В.https://creativecommons.org/licenses/by/4.0https://almclinmed.ru/jour/article/view/1163

Psoriasis and inflammatory bowel disease (IBD) are multifactorial chronic immuno-inflammatory potentially disabling disorders with similar genetic factors and immunological pathways, in particular, genetic polymorphisms of IL-23R, which determines the signal IL-12/23-mediated pathway of immunopathogenesis. The emergence of genetically engineered biological agents has changed the prognosis for both psoriasis and IBD. The intersection of the therapeutic spectrum in psoriasis and IBD is a very important point when choosing the management strategy for these patients. Infliximab and adalimumab are effective in the treatment of psoriasis, psoriatic arthritis, Crohn's disease, ulcerative colitis (evidence level 1A). Ustekinumab demonstrates effectiveness in the treatment of psoriasis, psoriatic arthritis (evidence level 1A) and Crohn's disease (evidence level 1B). Etanercept and secukinumab have been shown to be effective against psoriasis, psoriatic arthritis (evidence level 1A) and ineffective and even associated with exacerbation risk in Crohn's disease and ulcerative colitis. Inhibition of regulatory cytokines IL-12/23 also has a number of advantages compared to the blockade of effector cytokines (TNF-α, IL-17) due to potentially long-term and stable treatment results and less frequent administration.

Псориаз и воспалительные заболевания кишечника (ВЗК) относятся к многофакторным хроническим иммуновоспалительным потенциально инвалидизирующим заболеваниям, при которых выявляют сходные генетические факторы и иммунологические пути развития, в частности генетический полиморфизм ИЛ-23R (IL-23R), определяющий сигнальный ИЛ-12/23 путь иммунопатогенеза. Появление генно-инженерных биологических препаратов изменило прогноз как при псориазе, так и при ВЗК. Пересечение терапевтического спектра при псориазе и ВЗК – важный аспект, который необходимо учитывать, выбирая тактику ведения пациентов с данными заболеваниями. Инфликсимаб и адалимумаб демонстрируют эффективность в лечении псориаза, псориатического артрита, болезни Крона, язвенного колита (уровень доказательности 1А). Устекинумаб эффективен в терапии псориаза, псориатического артрита (уровень доказательности 1А) и болезни Крона (уровень доказательности 1В). Для этанерцепта и секукинумаба показана эффективность в отношении псориаза, псориатического артрита (уровень доказательности 1А) и отсутствие эффективности и потенциальный риск обострения при болезни Крона и язвенном колите. Ингибирование регуляторных цитокинов ИЛ-12/23 также имеет ряд преимуществ в сравнении с блокированием эффекторных цитокинов (фактор некроза опухоли-α, ИЛ-17) за счет потенциально долгосрочного устойчивого результата терапии и более редкого режима введения препарата.

biologic therapyIL-12IL-23immunotherapyinflammatory bowel diseasesCrohn's diseasepsoriasispsoriatic arthritismonoclonal antibodyustekinumabбиологическая терапияИЛ-12ИЛ-23иммунотерапиявоспалительные заболевания кишечникаболезнь Кронапсориазпсориатический артритмоноклональные антителаустекинумаб1.Потекаев НН, Круглова ЛС. Псориатическая болезнь. М.: МДВ; 2014. 264 с.2. Lowes MA, Bowcock AM, Krueger JG. Pathogenesis and therapy of psoriasis. Nature. 2007;445(7130):866–73. doi: 10.1038/nature05663.3. Pappu R, Ramirez-Carrozzi V, Ota N, Ouyang W, Hu Y. The IL-17 family cytokines in immunity and disease. J Clin Immunol. 2010;30(2):185–95. doi: 10.1007/s10875-010-9369-6.4. Loftus EV, Augustin M, Bissonnette R, Krueger G, Calabro S, Langholff W, Popp J, Goyal K, Sloan S. Mo1884 Prevalence of Inflammatory Bowel Disease Among Patients With Psoriasis and Incidence of Serious Infections in This Subset: Results From the PSOLAR Registry. Gastroenterology. 2016;150(4 Suppl 1):S805. doi: 10.1016/S0016-5085(16)32726-3.5. Feagan BG, Sandborn WJ, Gasink C, Jacobstein D, Lang Y, Friedman JR, Blank MA, Johanns J, Gao LL, Miao Y, Adedokun OJ, Sands BE, Hanauer SB, Vermeire S, Targan S, Ghosh S, de Villiers WJ, Colombel JF, Tulassay Z, Seidler U, Salzberg BA, Desreumaux P, Lee SD, Loftus EV Jr, Dieleman LA, Katz S, Rutgeerts P; UNITI–IM-UNITI Study Group. Ustekinumab as Induction and Maintenance Therapy for Crohn's Disease. N Engl J Med. 2016;375(20):1946–60. doi: 10.1056/NEJMoa1602773.6. Cohen R, Robinson D Jr, Paramore C, Fraeman K, Renahan K, Bala M. Autoimmune disease concomitance among inflammatory bowel disease patients in the United States, 2001–2002. Inflamm Bowel Dis. 2008;14(6): 738–43. doi: 10.1002/ibd.20406.7. Gottlieb AB, Chao C, Dann F. Psoriasis comorbidities. J Dermatolog Treat. 2008;19(1):5–21. doi: 10.1080/09546630701364768.8. Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA, Sedgwick JD, Cua DJ. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med. 2003;198(12):1951–7. doi: 10.1084/jem.20030896.9. Lo CH, Lee SC, Wu PY, Pan WY, Su J, Cheng CW, Roffler SR, Chiang BL, Lee CN, Wu CW, Tao MH. Antitumor and antimetastatic activity of IL-23. J Immunol. 2003;171(2):600–7. doi: 10.4049/jimmunol.171.2.600.10. Onishi RM, Gaffen SL. Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease. Immunology. 2010;129(3):311–21. doi: 10.1111/j.1365-2567.2009.03240.x.11. Ebert LM, Meuter S, Moser B. Homing and function of human skin gammadelta T cells and NK cells: relevance for tumor surveillance. J Immunol. 2006;176(7):4331–6. doi: 10.4049/jimmunol.176.7.4331.12. Cai Y, Shen X, Ding C, Qi C, Li K, Li X, Jala VR, Zhang HG, Wang T, Zheng J, Yan J. Pivotal role of dermal IL-17-producing γδ T cells in skin inflammation. Immunity. 2011;35(4):596–610. doi: 10.1016/j.immuni.2011.08.001.13. Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M, Onoue M, Yagita H, Ishii N, Evans R, Honda K, Takeda K. ATP drives lamina propria T(H)17 cell differentiation. Nature. 2008;455(7214):808–12. doi: 10.1038/nature07240.14. Kamada N, Seo SU, Chen GY, Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13(5): 321–35. doi: 10.1038/nri3430.15. Ogawa A, Andoh A, Araki Y, Bamba T, Fujiyama Y. Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice. Clin Immunol. 2004;110(1):55–62. doi: 10.1016/j.clim.2003.09.013.16. Esplugues E, Huber S, Gagliani N, Hauser AE, Town T, Wan YY, O'Connor W Jr, Rongvaux A, Van Rooijen N, Haberman AM, Iwakura Y, Kuchroo VK, Kolls JK, Bluestone JA, Herold KC, Flavell RA. Control of TH17 cells occurs in the small intestine. Nature. 2011;475(7357):514–8. doi: 10.1038/nature10228.17. O'Connor W Jr, Kamanaka M, Booth CJ, Town T, Nakae S, Iwakura Y, Kolls JK, Flavell RA. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol. 2009;10(6):603–9. doi: 10.1038/ni.1736.18. Vind I, Riis L, Jess T, Knudsen E, Pedersen N, Elkjaer M, Bak Andersen I, Wewer V, Nørregaard P, Moesgaard F, Bendtsen F, Munkholm P; DCCD study group. Increasing incidences of inflammatory bowel disease and decreasing surgery rates in Copenhagen City and County, 2003–2005: a population-based study from the Danish Crohn colitis database. Am J Gastroenterol. 2006;101(6):1274–82. doi: 10.1111/j.1572-0241.2006.00552.x.19. Qiu Y, Chen BL, Mao R, Zhang SH, He Y, Zeng ZR, Ben-Horin S, Chen MH. Systematic review with meta-analysis: loss of response and requirement of anti-TNFα dose intensification in Crohn's disease. J Gastroenterol. 2017;52(5): 535–54. doi: 10.1007/s00535-017-1324-3.20. Vavricka SR, Brun L, Ballabeni P, Pittet V, Prinz Vavricka BM, Zeitz J, Rogler G, Schoepfer AM. Frequency and risk factors for extraintestinal manifestations in the Swiss inflammatory bowel disease cohort. Am J Gastroenterol. 2011;106(1):110–9. doi: 10.1038/ajg.2010.343.21. Conrad C, Gilliet M. Psoriasis: from Pathogenesis to Targeted Therapies. Clin Rev Allergy Immunol. 2018;54(1):102–13. doi: 10.1007/s12016-018-8668-1.22. Carretero G, Ferrandiz C, Dauden E, Vanaclocha Sebastián F, Gómez-García FJ, Herrera-Ceballos E, De la Cueva-Dobao P, Belinchón I, Sánchez-Carazo JL, Alsina-Gibert M, López-Estebaranz JL, Ferrán M, Torrado R, Carrascosa JM, Carazo C, Rivera R, Jiménez-Puya R, GarcíaDoval I; BIOBADADERM Study Group. Risk of adverse events in psoriasis patients receiving classic systemic drugs and biologics in a 5-year observational study of clinical practice: 2008–2013 results of the Biobadaderm registry. J Eur Acad Dermatol Venereol. 2015;29(1):156–63. doi: 10.1111/jdv.12492.23. Frieder J, Kivelevitch D, Menter A. Secukinumab: a review of the anti-IL-17A biologic for the treatment of psoriasis. Ther Adv Chronic Dis. 2018;9(1):5–21. doi: 10.1177/2040622317738910.24. Whitlock SM, Enos CW, Armstrong AW, Gottlieb A, Langley RG, Lebwohl M, Merola JF, Ryan C, Siegel MP, Weinberg JM, Wu JJ, Van Voorhees AS. Management of psoriasis in patients with inflammatory bowel disease: From the Medical Board of the National Psoriasis Foundation. J Am Acad Dermatol. 2018;78(2): 383–94. doi: 10.1016/j.jaad.2017.06.043.25. Varu A, Wilson FR, Dyrda P, Hazel M, Hutton B, Cameron C. Treatment sequence network meta-analysis in Crohn's disease: a methodological case study. Curr Med Res Opin. 2019;35(5): 733–56. doi: 10.1080/03007995.2019.1580094.26. Nast A, Boehncke WH, Mrowietz U, Ockenfels HM, Philipp S, Reich K, Rosenbach T, Sammain A, Schlaeger M, Sebastian M, Sterry W, Streit V, Augustin M, Erdmann R, Klaus J, Koza J, Muller S, Orzechowski HD, Rosumeck S, Schmid-Ott G, Weberschock T, Rzany B; Deutsche Dermatologische Gesellschaft (DDG); Berufsverband Deutscher Dermatologen (BVDD). S3 – Guidelines on the treatment of psoriasis vulgaris (English version). Update. J Dtsch Dermatol Ges. 2012;10 Suppl 2:S1–95. doi: 10.1111/j.1610-0387.2012.07919.x.27. American Academy of Dermatology Work Group, Menter A, Korman NJ, Elmets CA, Feldman SR, Gelfand JM, Gordon KB, Gottlieb A, Koo JY, Lebwohl M, Leonardi CL, Lim HW, Van Voorhees AS, Beutner KR, Ryan C, Bhushan R. Guidelines of care for the management of psoriasis and psoriatic arthritis: section 6. Guidelines of care for the treatment of psoriasis and psoriatic arthritis: case-based presentations and evidence-based conclusions. J Am Acad Dermatol. 2011;65(1):137–74. doi: 10.1016/j.jaad.2010.11.055.28. Coates LC, Moverley AR, McParland L, Brown S, Navarro-Coy N, O'Dwyer JL, Meads DM, Emery P, Conaghan PG, Helliwell PS. Effect of tight control of inflammation in early psoriatic arthritis (TICOPA): a UK multicentre, open-label, randomised controlled trial. Lancet. 2015;386(10012):2489–98. doi: 10.1016/S0140-6736(15)00347-5.29. Coates LC, Helliwell PS. Treating to target in psoriatic arthritis: how to implement in clinical practice. Ann Rheum Dis. 2016;75(4):640–3. doi: 10.1136/annrheumdis-2015-208617.30. Macaluso F, Guggino G, Mauro D, Rizzo C, Bignone R, Ciccia F. Safety and efficacy of secukinumab treatment in a patient with ankylosing spondylitis and concomitant multiple sclerosis. Clin Exp Rheumatol. Forthcoming 2019.31. Smith CH, Jabbar-Lopez ZK, Yiu ZZ, Bale T, Burden AD, Coates LC, Cruickshank M, Hadoke T, MacMahon E, Murphy R, Nelson-Piercy C, Owen CM, Parslew R, Peleva E, Pottinger E, Samarasekera EJ, Stoddart J, Strudwicke C, Venning VA, Warren RB, Exton LS, Mohd Mustapa MF. British Association of Dermatologists guidelines for biologic therapy for psoriasis 2017. Br J Dermatol. 2017;177(3):628–36. doi: 10.1111/bjd.15665.32. Mylle S, Grine L, Speeckaert R, Lambert JLW, van Geel N. Targeting the IL-23/IL-17 Pathway in Psoriasis: the Search for the Good, the Bad and the Ugly. Am J Clin Dermatol. 2018;19(5): 625–37. doi: 10.1007/s40257-018-0366-5.33. Gooderham MJ, Papp KA, Lynde CW. Shifting the focus – the primary role of IL-23 in psoriasis and other inflammatory disorders. J Eur Acad Dermatol Venereol. 2018;32(7):1111–9. doi: 10.1111/jdv.14868.34. Chan TC, Hawkes JE, Krueger JG. Interleukin 23 in the skin: role in psoriasis pathogenesis and selective interleukin 23 blockade as treatment. Ther Adv Chronic Dis. 2018;9(5):111–9. doi: 10.1177/2040622318759282.35. Siegel SAR, Winthrop KL. In the Real World: Infections Associated with Biologic and Small Molecule Therapies in Psoriatic Arthritis and Psoriasis. Curr Rheumatol Rep. 2019;21(7):36. doi: 10.1007/s11926-019-0832-y.36. Egeberg A, Ottosen MB, Gniadecki R, Broesby-Olsen S, Dam TN, Bryld LE, Rasmussen MK, Skov L. Safety, efficacy and drug survival of biologics and biosimilars for moderate-to-severe plaque psoriasis. Br J Dermatol. 2018;178(2): 509–19. doi: 10.1111/bjd.16102.37. Lunder T, Zorko MS, Kolar NK, Suhodolcan AB, Marovt M, Leskovec NK, Marko PB. Drug survival of biological therapy is showing class effect: updated results from Slovenian National Registry of psoriasis. Int J Dermatol. 2019;58(6): 631–41. doi: 10.1111/ijd.14429.38. Абдулганиева ДИ, Бакулев АЛ, Белоусова ЕА, Знаменская ЛФ, Коротаева ТВ, Круглова ЛС, Кохан ММ, Лила АМ, Хайрутдинов ВР, Халиф ИЛ, Хобейш ММ. Проект междисциплинарных рекомендаций по диагностике, методам оценки степени активности, терапевтической эффективности и применению генно-инженерных биологических препаратов у пациентов с сочетанными иммуновоспалительными заболеваниями (псориаз, псориатический артрит, болезнь Крона). Современная ревматология. 2018;12(3):4–18. doi: 10.14412/1996-7012-2018-3-4-18.39. Amin M, No DJ, Egeberg A, Wu JJ. Choosing First-Line Biologic Treatment for Moderate-to-Severe Psoriasis: What Does the Evidence Say? Am J Clin Dermatol. 2018;19(1): 1–13. doi: 10.1007/s40257-017-0328-3.40. Allen PB, Olivera P, Emery P, Moulin D, Jouzeau JY, Netter P, Danese S, Feagan B, Sandborn WJ, Peyrin-Biroulet L. Review article: moving towards common therapeutic goals in Crohn's disease and rheumatoid arthritis. Aliment Pharmacol Ther. 2017;45(8):1058–72. doi: 10.1111/apt.13995.41. Kim BS, Lee WK, Pak K, Han J, Kim GW, Kim HS, Ko HC, Kim MB, Kim SJ. Ustekinumab treatment is associated with decreased systemic and vascular inflammation in patients with moderate-to-severe psoriasis: Feasibility study using 18F-fluorodeoxyglucose PET/CT. J Am Acad Dermatol. 2019;80(5):1322–31. doi: 10.1016/j.jaad.2018.03.011.42. Hindryckx P, Novak G, Bonovas S, Peyrin-Biroulet L, Danese S. Infection Risk With Biologic Therapy in Patients With Inflammatory Bowel Disease. Clin Pharmacol Ther. 2017;102(4): 633–41. doi: 10.1002/cpt.791.43. Weizman AV, Nguyen GC, Seow CH, Targownik L, Murthy SK, Boland K, Afzal NM, Khanna R, Jones J, Afif W, Halder S, Reinglas J, Fowler S, Huang V, Kaplan GG, Melmed GY. Appropriateness of Biologics in the Management of Crohn's Disease Using RAND/UCLA Appropriateness Methodology. Inflamm Bowel Dis. 2019;25(2):328–35. doi: 10.1093/ibd/izy333.