Clinical and sonographic characteristics of enthesis lesions in inflammatory bowel disease
DOI: 10.32364/2587-6821-2021-5-6-385-390
G.R. Gainullina1, E.R. Kirillova1,2, A.Kh. Odintsova2, D.I. Abdulganieva1,2
1Kazan State Medical University, Kazan, Russian Federation
2Republican Clinical Hospital of the Ministry of Health of the Republic of Tatarstan, Kazan,
Russian Federation
Aim: to assess enthesis lesions in patients with inflammatory bowel disease/IBD (ulcerative colitis/UC and Crohn’s disease/CD) and associations between the clinical pattern of the underlying disease and enthesopathy verified by ultrasound.
Patients and Methods: this study included 95 patients with IBD aged 26–37 (the mean age was 37 years). Each patient underwent clinical examination and ultrasound of the entheses of the upper and lower extremities with calculating enthesial indices. The pattern of enthesopathy in patients with UC and CD was compared. Correlations between clinical characteristics of IBD and enthesopathy were evaluated. The analysis of individual anatomical sites of tendon and ligament insertions in patients with IBD was performed for the first time.
Results: pain elicited on local pressure of entheseal points was seen in 52%. Enthesitis was diagnosed through ultrasound in 76% of patients (enthesitis with vascularization in 76%, erosions at insertions in 80%, and enthesophytes in 39%). When assessing anatomical sites, the most common impairment was a medial collateral ligament lesion, while the most common localization of enthesophytes was the insertion point of the quadriceps femoris muscle. Disease duration directly correlated to the number of painful entheses on palpation (SR=0.24, р=0.017) and the number of enthesophytes (SR=0.20, р=0.044). We failed to identify any significant associations between the severity of the attack and enthesis lesions in UC and CD. Direct correlations between the number of extraintestinal manifestations and the number of painful entheses on palpation (SR=0.35, р=0.0004) and LEI (SR=0.2, р=0.04) and GUESS scores (SR=0.28, р=0.004); the number of erosions with vascularization and ESR (SR=0.26, р=0.01) and CRP (SR=0.25, р=0.01); the number of painful entheses on palpation and the number of enthesitis (SR=0.71, р=0.00) including those with vascularization (SR=0.27, р=0.00) were revealed.
Conclusion: enthesopathy is a common extraintestinal manifestation of IBD independent of a nosology of the severity of the attack of the underlying disease. Greater disease duration, pain at entheses on palpation, and increased inflammatory markers (ESR, CRP) are associated with enthesis lesions. Therefore, current enthesopathy indices can be applied to assess and monitor entheses.
Keywords: inflammatory bowel disease, ultrasound, enthesitis, vascularization, Power Doppler imaging, enthesopathy scores.
For citation: Gainullina G.R., Kirillova E.R., Odintsova A.Kh., Abdulganieva D.I. Clinical and sonographic characteristics of enthesis lesions in inflammatory bowel disease. Russian Medical Inquiry. 2021;5(6):385–390 (in Russ.). DOI: 10.32364/2587-6821-2021-5-6-385-390.
About the authors:
Guliya R. Gainullina — postgraduate student of the Department of Hospital Therapy, Kazan State Medical University; 49, Butlerov str., Kazan, 420012, Russian Federation; ORCID iD 0000-0002-3929-9973.
Elina R. Kirillova — C. Sc. (Med.), associate professor of the Department of Hospital Therapy, Kazan State Medical University, 49, Butlerov str., Kazan, 420012, Russian Federation; sonographer, Republican Clinical Hospital of the Ministry of Health of the Republic of Tatarstan, 138, Orenburgskiy tract, Kazan, 420064, Russian Federation; ORCID iD 0000-0002-2152-7472.
Alfiya Kh. Odintsova — C. Sc. (Med.), head of the Department of Gastroenterology, Republican Clinical Hospital of the Ministry of Health of the Republic of Tatarstan; 138, Orenburgskiy tract, Kazan, 420064, Russian Federation.
Diana I. Abdulganieva — Dr. Sc. (Med.), Professor, Head of the Department of Hospital Therapy, Kazan State Medical University; 49, Butlerov str., Kazan, 420012, Russian Federation; Chief Specialist in Therapy, Republican Clinical Hospital of the Ministry of Health of the Republic of Tatarstan, 138, Orenburgskiy tract, Kazan, 420064, Russian Federation; ORCID iD 0000-0001-7069-2725.
Contact information: Guliya R. Gainullina, e-mail: nice.gaynullina@bk.ru.
Financial Disclosure: no authors have a financial or property interest in any material or method mentioned.
There is no conflict of interests.
Received 09.07.2021.
Revised 30.07.2021.
Accepted 24.08.2021.
2. Ивашкин В.Т., Шелыгин Ю.А., Абдулганиева Д.И. и др. Рекомендации Российской гастроэнтерологической ассоциации и Ассоциации колопроктологов России по диагностике и лечению взрослых больных язвенным колитом. Российский журнал гастроэнтерологии, гепатологии, колопроктологии. 2015;1:48–65. [Ivashkin V.T., Shelygin Y.A., Abdulganieva D.I. et al. Recommendations of the Russian Gastroenterological Association and the Association of Coloproctologists of Russia for the diagnosis and treatment of adult patients with ulcerative colitis. Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2015;1:48–65 (in Russ.)].
3. Ивашкин В.Т., Шелыгин Ю.А., Абдулганиева Д.И. и др. Клинические рекомендации по диагностике и лечению взрослых пациентов с болезнью Крона. 2013. [Ivashkin V.T., Shelygin Y.A., Abdulganieva D.I. et al. Clinical guidelines for the diagnosis and treatment of adult patients with Crohn’s disease. 2013 (in Russ.)].
4. Абдулганиева Д.И., Кириллова Э.Р., Файрушина И.Ф. и др. Энтезопатии при спондилоартритах: обзор литературы. Научно-практическая ревматология. 2021;59(3):316–325. DOI: 10.47360/1995-4484-2021-316-325. [Abdulganieva D.I., Kirillova E.R., Fairushina I.F. et al. Enthesopathy in spondyloarthritis: a literature review. Rheumatology Science and Practice. 2021;59(3):316–325 (in Russ.)]. DOI: 10.47360/1995-4484-2021-316-325.
5. McGonagle D., Khan M.A., Marzo-Ortega H. et al. Enthesitis in spondyloarthropathy. Curr Opin Rheumatol. 1999;11:244–250. DOI: 10.1097/00002281-199907000-00004.
6. Khan M.A. Enthesitis: a broader definition. Ann Rheum Dis. 2000;59:998. DOI: 10.1136/ard.59.12.985.
7. Cantini F., Niccoli L., Nannini C. 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;44:1341–1346. DOI: 10.3899/jrheum.161518.
8. Ureyen B.S., Karacaer C., Toka B. et al. Similar subclinical enthesitis in celiac and inflammatory bowel diseases by ultrasound suggests a gut enthesis axis independent of spondyloarthropathy spectrum. Rheumatology (Oxford). 2018;57(8):1417–1422. DOI: 10.1093/rheumatology/key102.
9. Arvikar S.L., Fisher M.C. Inflammatory bowel disease associated arthropathy. Curr Rev Musculoskelet Med. 2011;4:123–131. DOI: 10.1007/s12178-011-9085-8.
10. Bandinelli F., Milla M., Genise S. et al. Ultrasound discloses entheseal involvement in inactive and low active inflammatory bowel disease without clinical signs and symptoms of spondyloarthropathy. Rheumatology (Oxford). 2011;50(7):1275–1279. DOI: 10.1093/rheumatology/keq447.
11. Rovisco J., Duarte C., Batticcioto A. et al. Hidden musculoskeletal involvement in inflammatory bowel disease: a multicenter ultrasound study. BMC Musculoskelet Disord. 2016;17:84. DOI: 10.1186/s12891-016-0932-z.
12. Кузьмин Д.Б., Кокорин В.В., Епифанов С.А., Крайнюков П.Е. Роль инфекции в этиопатогенезе энтезопатий. Вестник Национального медико-хирургического Центра им. Н.И. Пирогова. 2020;15(3):143–151. DOI: 10.25881/БРММ8С.2020.61.59.026. [Kuzmin D.B., Kokorin V.V., Epifanov S.A., Krainyukov P.E. Role of infection in the etiopathogenesis of enthesopathies. Bulletin of Pirogov National Medical and Surgical Center. 2020;15(3):143–151 (in Russ.)]. DOI: 10.25881/БРММ8С.2020.61.59.026.
13. Hsiao Y., Wei Sh., Lu Ch. et al. Patients with inflammatory bowel disease have higher sonographic enthesitis scores than normal individuals: pilot study in Taiwan. J Med Ultrasound. 2014;22(4):194–199. DOI: 10.1016/j.jmu.2014.03.004.
14. Balint P.V., Kane D., Wilson H. et al. Ultrasonography of entheseal insertions in the lower limb in spondyloarthropathy. Ann Rheum Dis. 2002;61(10):905–910. DOI: 10.1136/ard.61.10.905.
15. Schett G., Lories R., D’Agostino M. et al. Enthesitis: from pathophysiology to treatment. Nat Rev Rheumatol. 2017;13:731–741. DOI: 10.1038/nrrheum.2017.188.
16. Ruyssen-Witrand A., Jamard B., Cantagrel A. et al. Relationships between ultrasound enthesitis, disease activity and axial radiographic structural changes in patients with early spondyloarthritis: data from DESIR cohort. RMD Open. 2017;3(2):e000482. DOI: 10.1136/rmdopen-2017-000482.
17. Mease P.J. Measures of psoriatic arthritis: Tender and Swollen Joint Assessment, Psoriasis Area and Severity Index (PASI), Nail Psoriasis Severity Index (NAPSI), Modified Nail Psoriasis Severity Index (mNAPSI), Mander/Newcastle Enthesitis Index (MEI), Leeds Enthesitis Index (LEI), Spondyloarthritis Research Consortium of Canada (SPARCC), Maastricht Ankylosing Spondylitis Enthesis Score (MASES), Leeds Dactylitis Index (LDI), Patient Global for Psoriatic Arthritis, Dermatology Life Quality Index (DLQI), Psoriatic Arthritis Quality of Life (PsAQOL), Functional Assessment of Chronic Illness Therapy-Fatigue (FACIT-F), Psoriatic Arthritis Response Criteria (PsARC), Psoriatic Arthritis Joint Activity Index (PsAJAI), Disease Activity in Psoriatic Arthritis (DAPSA), and Composite Psoriatic Disease Activity Index (CPDAI). Arthritis Care Res. (Hoboken). 2011;63(Suppl 11):S64–S85. DOI: 10.1002/acr.20577.
18. Heuft-Dorenbosch L., Spoorenberg A., van Tubergen A. et al. Assessment of enthesitis in ankylosing spondylitis. Ann Rheum Dis. 2003;62:127–132. DOI: 10.1136/ard.62.2.127.
19. Mease P.J., Bosch F., Sieper J. et al. Performance of 3 enthesitis indices in patients with peripheral spondyloarthritis during treatment with adalimumab. J Rheumatol. 2017;44(5):599–608. DOI: 10.3899/jrheum.160387.
20. Balint P.V., Terslev L., Aegerter P. et al. Reliability of a consensus-based ultrasound definition and scoring for enthesitis in spondyloarthritis and psoriatic arthritis: an OMERACT US initiative. Ann Rheum Dis. 2018;77(12):1730–1735. DOI: 10.1136/ annrheumdis-2018-213609.
21. Ozsoy-Unubol T., Yagci I. Is ultrasonographic enthesitis evaluation helpful for diagnosis of non-radiographic axial spondyloarthritis? Rheumatol Int. 2018;38(11):2053–2061. DOI: 10.1007/s00296-018-4164-4.
22. Eder L., Jayakar J., Thavaneswaran A. et al. Is the MAdrid Sonographic Enthesitis Index useful for differentiating psoriatic arthritis from psoriasis alone and healthy controls? J Rheumatol. 2014;41(3):466–472. DOI: 10.3899/jrheum.130949.
23. Milutinovic S., Radunovic G., Veljkovic K. et al. Construct validity and sensitivity to change of Belgrade Ultrasound Enthesitis Score in patients with spondyloarthritis: a pilot study. Rheumatol Int. 2018;38(3):383–391. DOI: 10.1007/s00296-017-3898-8.
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