Тuberculous enterocolitis as a reflection of immunosuppressive conditions

The aim: to determine the main risk factors and their impact on the development of tuberculous enterocolitis (TEC) in Moscow. Materials and methods. Risk factors for the development of intestinal tuberculosis were studied in 217 adult patients with a combination of respiratory tuberculosis and intestinal tuberculosis compared with 22 663 adult patients with respiratory tuberculosis without tuberculosis intestines registered in 2016–2023.

Results and discussion. As a result of the calculations, the main risk factors for the development of tuberculous enterocolitis were immunosuppressive therapy (aOR 12.05; 95% CI 6.71–20.69), diabetes mellitus (aOR 9.06; 95% CI 4.45–16.81) and HIV infection (aOR 7.55; 95% CI 5,40–10,67). In our study, we were able to identify the main risk factors affecting the development of tuberculous enterocolitis and adapt the results obtained to the diagnostic search scheme in patients with generalized tuberculosis: the examination algorithm for such patients must necessarily include performing an abdominal CT scan with double contrast enhancement and colonoscopy with biopsy.

Conclusion. Taking into account predictors of tuberculous enterocolitis and including them in clinical diagnostic algorithms can help in early diagnosis of the disease and avoid the appearance of its complicated forms.

1. Jha D.K., Pathiyil M.M., Sharma V. Evidence-based approach to diagnosis and management of abdominal tuberculosis // Indian J. Gastroenterol. 2023. Vol. 42, No. 1. Р. 17–31. doi: https://doi.org/10.1007/s12664-023-01343-x.

2. Reshetnikov M.N., Plotkin D.V., Sinitsyn M.V., Gafarov U.O., Belentseva O.V. Surgical complications of abdominal tuberculosis in patients with different immune status. Experimental and Clinical Gastroenterology, 2019, No. 4, рр. 46–53 (In Russ.)]. doi: https://doi.org/10.31146/16828658-ecg-164-4-46–53.

3. Hayward S.E., Rustage K., Nellums L.B. et al. Extrapulmonary tuberculosis among migrants in Europe, 1995 to 2017 // Clin. Microbiol. Infect. 2021. Vol. 27, No. 9. Р. 1347.e1–1347.e7. doi: https://doi.org/10.1016/j.cmi.2020.12.006.

4. Fang Y., Zhou Q., Li L., Zhou Y., Sha W. Epidemiological characteristics of extrapulmonary tuberculosis patients with or without pulmonary tuberculosis // Epidemiol Infect. 2022. Vol. 150. Р. e158. doi: https://doi.org/10.1017/S0950268822001236.

5. Nath. P. Epidemiology of Gastrointestinal Tuberculosis // Sharma V. (eds.) Tuberculosis of the Gastrointestinal system. Singapore: Springer, 2022. https://doi.org/10.1007/978-981-16-9053-2_2.

6. Rolo M., González-Blanco B., Reyes C.A., Rosillo N., López-Roa P. Epidemiology and factors associated with Extra-pulmonary tuberculosis in a Low-prevalence area // J. Clin. Tuberc. Other Mycobact. Dis. 2023. Vol. 32. Р. 100377. doi: https://doi.org/10.1016/j.jctube.2023.100377.

7. Niu T., He F., Yang J., Ma C. et al. The epidemiological characteristics and infection risk factors for extrapulmonary tuberculosis in patients hospi-talized with pulmonary tuberculosis infection in China from 2017 to 2021 // BMC Infect Dis. 2023. Vol. 23, No. 1. Р. 488. Published 2023 Sep 1. doi: https://doi.org/10.1186/s12879-023-08410-w.

8. Belilovsky E. M., Borisov S.E. Organization of epidemiological monitoring of tuberculosis in the city of Moscow. Problems of social hygiene, health care and history of medicine, 2021, Vol. 29, No. S2, pp. 1275–1280 (In Russ.)]. doi: https://doi.org/10.32687/0869-866X-2021-29-s2-1275-1280.

9. Silva D.R., Muñoz-Torrico M., Duarte R. et al. Risk factors for tuberculosis: diabetes, smoking, alcohol use, and the use of other drugs // J. Bras. Pneumol. 2018. Vol. 44, No. 2. Р. 145–152. doi: https://doi.org/10.1590/s1806-37562017000000443.

10. Al-Zanbagi A.B., Shariff M.K. Gastrointestinal tuberculosis: A systematic review of epidemiology, presentation, diagnosis and treatment // Saudi J. Gastroenterol. 2021. Vol. 27, No. 5. Р. 261–274. doi: https://doi.org/10.4103/sjg.sjg_148_21.

11. Reichardt H.M., Tuckermann J.P., Göttlicher M. et al. Repression of inflammatory responses in the absence of DNA binding by the glucocorticoid receptor // EMBO J. 2001. Vol. 20, No. 24. Р. 7168–7173. doi: https://doi.org/10.1093/emboj/20.24.7168.

12. Schutz C., Davis A.G., Sossen B. et al. Corticosteroids as an adjunct to tuberculosis therapy // Expert. Rev. Respir. Med. 2018. Vol. 12, No. 10. Р. 881–891. doi: https://doi.org/10.1080/17476348.2018.1515628.

13. Jick S.S., Lieberman E.S., Rahman M.U., Choi H.K. Glucocorticoid use, other associated factors, and the risk of tuberculosis // Arthritis Rheum. 2006. Vol. 55, No. 1. Р. 19–26. doi: https://doi.org/10.1002/art.21705.

14. Machuca I., Vidal E., de la Torre-Cisneros J., Rivero-Román A. Tuberculosis in immunosuppressed patients. Tuberculosisen pacientes inmun-odeprimidos // Enferm. Infec. Microbiol Clin (Engl Ed). 2018. Vol. 36, No. 6, pp. 366–374. doi: https://doi.org/10.1016/j.eimc.2017.10.009.

15. Razafindrazoto C.I., Randriamifidy N.H., Rakotomalala J.A. et al. Inappropriate prescription of corticosteroid therapy during inflammatory ileo-colitis revealing disseminated tuberculosis with digestive involvement: Two case reports // Clin. Case Rep. 2021. Vol. 9, No. 6. Р. e04215. doi: https://doi.org/10.1002/ccr3.4215.

16. Mezouar S., Diarra I., Roudier J., Desnues B., Mege J.L. Tumor Necrosis Factor-Alpha Antagonist Interferes With the Formation of Granulomatous Multinucleated Giant Cells: New Insights Into Mycobacterium tuberculosis Infection // Front Immunol. 2019. Vol. 10. Р. 1947. doi: https://doi.org/10.3389/fimmu.2019.01947.

17. Harris J., Keane J. How tumour necrosis factor blockers interfere with tuberculosis immunity // Clin. Exp. Immunol. 2010. Vol. 161, No. 1. Р. 1–9. doi: https://doi.org/10.1111/j.1365-2249.2010.04146.x.

18. Wallis R.S. Mathematical modeling of the cause of tuberculosis during tumor necrosis factor blockade // Arthritis Rheum. 2008. Vol. 58, No. 4. Р. 947–952. doi: https://doi.org/doi:10.1002/art.23285.

19. Katrak S.S., Li R., Reynolds S. et al. Association of Tumor Necrosis Factor Inhibitor Use with Diagnostic Features and Mortality of Tuberculosis in the United States, 2010–2017 // Open Forum Infect Dis. 2021. Vol. 9, No. 2. Р. ofab641. doi: https://doi.org/10.1093/ofid/ofab641.

20. Riestra S., de Francisco R., Arias-Guillén M. et al. Risk factors for tuberculosis in inflammatory bowel disease: anti-tumor necrosis factor and hos-pitalization // Rev. Esp. Enferm. Dig. 2016. Vol. 108, No. 9. Р. 541–549. doi: https://doi.org/10.17235/reed.2016.4440/2016.

21. Torres T., Chiricozzi A., Puig L., Lé A.M. et al. Treatment of Psoriasis Patients with Latent Tuberculosis Using IL-17 and IL-23 Inhibitors: A Retrospective, Multinational, Multicentre Study // Am. J. Clin. Dermatol. 2024. Vol. 25, No. 2. Р. 333–342. doi: https://doi.org/10.1007/s40257024-00845-4.

22. Ronacher K., Joosten S.A., van Crevel R. et al. Acquired immunodeficiencies and tuberculosis: focus on HIV/AIDS and diabetes mellitus // Immunol. Rev. 2015. Vol. 264, No. 1. Р. 121–137. doi: https://doi.org/10.1111/imr.12257.

23. Yanqiu X., Yang Y., Xiaoqing W., Zhixuan L., Kuan Z., Xin G., Bo Z., Jinyu W., Jing C., Yan M., Aiguo M. Impact of hyperglycemia on tubercu-losis treatment outcomes: a cohort study // Sci Rep. 2024. Vol. 14, No. 1. Р. 13586. doi: https://doi.org/10.1038/s41598-024-64525-3.

24. Repine J.E., Clawson C.C., Goetz F.C. Bactericidal function of neutrophils from patients with acute bacterial infections and from diabetics // J. Infect Dis. 1980. Vol. 142, No. 6. Р. 869–875. doi: https://doi.org/10.1093/infdis/142.6.869.

25. Foe-Essomba J.R., Kenmoe S., Tchatchouang S. et al. Diabetes mellitus and tuberculosis, a systematic review and meta-analysis with sensitivity analy-sis for studies comparable for confounders // PLoS One. 2021. Vol. 16, No. 12. Р. e0261246. doi: https://doi.org/10.1371/journal.pone.0261246.

26. Restrepo B.I. Diabetes and Tuberculosis // Microbiol Spectr. 2016. Vol. 4. Р. 6.10.1128/microbiolspec.TNMI7-0023-2016. doi: https://doi.org/10.1128/microbiolspec.tnmi7-0023-2016.

27. Bell L.C.K., Noursadeghi M. Pathogenesis of HIV-1 and Mycobacterium tuberculosis co-infection // Nat. Rev. Microbiol. 2018. Vol. 16, No. 2. Р. 80–90. doi: https://doi.org/10.1038/nrmicro.2017.128.

28. Wong K., Nguyen J., Blair L. et al. Pathogenesis of Human Immunodeficiency Virus-Mycobacterium tuberculosis Co-Infection // J. Clin. Med. 2020. Vol. 9, No. 11. Р. 3575. doi: https://doi.org/10.3390/jcm9113575.

29. Gao J., Zheng P., Fu H. Prevalence of TB/HIV co-infection in countries except China: a systematic review and meta-analysis // PLoS One. 2013. Vol. 8, No. 5. Р. e64915. doi: https://doi.org/10.1371/journal.pone.0064915.

30. Monreal-Robles R., González-González J.A., Sordia-Ramírez J. et al. High mortality due to gastrointestinal TB in HIV and non-HIV patients // Int. J. Tuberc. Lung Dis. 2022. Vol. 26, No. 4. Р. 348–355. doi: https://doi.org/10.5588/ijtld.21.0446.