Comorbid Infections in Spondyloarthritis: the Current State of the Problem
https://doi.org/10.37489/0235-2990-2024-69-11-12-127-135
EDN: NGHLKV
Abstract
Comorbid infections (CI) in immuno-inflammatory rheumatic diseases (IIRDs) are associated with significant morbidity and mortality and, in addition, involve significant costs in the health care system due to the need for additional treatment and hospitalization. The development of CI requires the temporary cancellation of ongoing immunosuppressive therapy, which can lead to an exacerbation of IIRD. High activity of rheumatic disease and treatment with immunosuppressive drugs may increase the risk of CI. Of particular interest is the study of the frequency, structure and risk factors in patients with spondyloarthritis (SpA) — ankylosing spondylitis (AS) and psoriatic arthritis (PsA), especially in the aspect of the increasing use of biologics or targeted (b/tsDMARD) modifying disease agents and contradictory literature data.
About the Authors
M. M. Baranova
V.A. Nasonova Research Institute of Rheumatology
Russian Federation
Competing Interests:
Russian Federation
Marina M. Baranova — Junior Researcher at the Laboratory of Comorbid Infections and Vaccine Prevention, ResearcherID: JDD-0658-2023, Scopus Author ID: 57222430929.
Moscow
Competing Interests:
none
N. V. Muravyeva
V.A. Nasonova Research Institute of Rheumatology
Russian Federation
Competing Interests:
Russian Federation
Natalia V. Muravyeva — Ph. D. in Medicine, Senior Researcher at the Laboratory of Comorbid Infections and Vaccine Prevention, ResearcherID: AAF-4853-2021. eLIBRARY SPIN-code: 8418-4469. Scopus Author ID: 57210263706.
Moscow
Competing Interests:
none
B. S. Belov
V.A. Nasonova Research Institute of Rheumatology
Russian Federation
Competing Interests:
Russian Federation
Boris S. Belov — D. Sc. in MEdicine Head of the Laboratory of Comorbid Infections and Vaccine Prevention, ResearcherID: ABD-2219-2020. eLIBRARY SPIN-code: 3298-4315. Scopus Author ID: 7004592537.
Moscow
Competing Interests:
none
References
1. Erdes Sh. F., Rebrov A. P., Dubinina T. V., et al. Spondyloarthritis: modern terminology and definitions. Therapeutic Archive. 2019; 91 (5): 84–88.] doi: https://doi.org/10.26442/00403660.2019.05.000208. (in Russian)
2. Haroon N., Inman R. D., Learch T. J. et al. The impact of tumor necrosis factor alpha inhibi-tors on radiographic progression in ankylosing spondylitis. Arthritis Rheum. 2013, 65: 2645–2654. doi: 10.1002/art.38070.
3. Barkham N., Keen H. I., Coates L. C. et al. Clinical and imaging efficacy of inflixi-mab in HLA-B27-positive patients with magnetic resonance imaging-determined early sacroiliitis. Arthritis Rheum. 2009, 60: 946–954. doi: 10.1002/art.24408.
4. Baillet A., Gossec L., Carmona L. et al. Points to consider for reporting, screening for and preventing selected comorbidities in chronic inflammatory rheumatic diseases in daily practice: a EULAR initiative. Ann Rheum Dis. 2016; 75 (6): 965–973. doi: 10.1136/annrheumdis-2016-209233.
5. Belov B. S., Tarasova G. M., Bukhanova D. V. Comorbid infections in rheumatic diseases. Antibiot Khimioter = Antibiotics and Chemotherapy. 2019; 64 (1–2): 50–57. doi: https://doi.org/10.24411/0235W2990W2019W10009. (in Russian)
6. Lapshina S. A., Dubinina T. V., Badokin V. V. et al. Tumor necrosis factor-α inhibitors in the treatment of axial spondy-loarthritis, including ankylosing spondylitis. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2016; 54 (Suppl. 1): 75–79.] doi: https://doi.org/10.14412/19954484-2016-1S-75-79.
7. Aureal M., Seauve M., Laplane S. et al. Incidence of infections in patients with psoriatic arthritis and axial spondyloarthritis treated with biological or targeted disease-modifying agents: a systematic review and metaanalysis of randomised controlled trials, open-label studies and obser- vational studies. RMD Open. 2023; 9: e003064. doi: 10.1136/rmdopen2023-003064.
8. Atzeni F., Sarzi-Puttini P., Sebastiani M. et al. Rate of serious infections in spondyloarthropathy patients treated with anti-tumour necrosis factor drugs: a survey from the Italian registry GISEA. Clin Exp Rheumatol. 2019; 37 (4): 649–655.
9. Burmester G. R., Gordon K. B., Rosenbaum J. T. et al. Long-term safety of adalimumab in 29,967 adult patients from global clinical trials across multiple indications: an updated analysis. Adv Ther. 2020; 37 (1): 364–380. doi: 10.1007/s12325-019-01145-8.
10. Aureal M., Seauve M., Laplane S. et al. Incidence of infections in patients with psoriatic arthritis and axial spondyloarthritis treated with biological or targeted disease-modifying agents: a systematic review and metaanalysis of randomised controlled trials, open-label studies and observational studies. RMD Open. 2023; 9 (3): e003064. doi: 10.1136/rmdopen2023-003064.
11. Deodhar A., Mease P. J., McInnes I. B. et al. Long-term safety of secukinumab in patients with moderate-to-severe plaque psoriasis, psoriatic arthritis, and ankylosing spondylitis: integrated pooled clinical trial and postmarketing surveillance data. Arthritis Res Ther. 2019; 21 (1): 111. doi: 10.1186/s13075-019-1882-2.
12. Combe B., Rahman P., Kameda H. et al. Safety results of ixekizumab with 1822.2 patient-years of exposure: an integrated analysis of 3 clinical trials in adult patients with psoriatic arthritis. Ar-thritis Res Ther. 2020; 22 (1): 14. doi: 10.1186/s13075-020-2099-0.
13. Ghosh S., Gensler L. S., Yang Z. et al. Ustekinumab safety in psoriasis, psoriatic arthritis, and crohn's disease: an integrated analysis of phase II/III clinical development programs. Drug Saf. 2019; 42 (6): 751–768. doi: 10.1007/s40264-019-00797-3.
14. Ritchlin C. T., Stahle M., Poulin Y., Bagel J., Chakravarty S. D., Kafka S., Srivastava B., Langholff W., Gottlieb A. B. Serious infections in patients with self-reported psoriatic arthritis from the Psoriasis Longitudinal Assessment and Registry (PSOLAR) treated with biologics. BMC Rheumatol. 2019; 3: 52. doi: 10.1186/s41927-019-0094-3.
15. Li X., Andersen K. M., Chang H. Y., Curtis J. R., Alexander G. C. Comparative risk of serious infections among real-world users of biologics for psoriasis or psoriatic arthritis. Ann Rheum Dis. 2020; 79 (2): 285–291. doi: 10.1136/annrheumdis-2019-216102.
16. Quartuccio L., Zabotti A., Del Zotto S. et al. Risk of serious infection among patients receiving biologics for chronic inflammatory diseases: Usefulness of administrative data. J Adv Res. 2018; 15: 87–93. doi: 10.1016/j.jare.2018.09.003.
17. Baranova M. M., Muravyeva N. V., Belov B. S., Korotaeva T. V., Glukhova S. I. Comorbid infections in patients with spondyloarthritis: frequency, structure and risk factors. Sovremennaya Revmatologiya = Modern Rheumatology Journal. 2023; 17 (4): 64= 70. doi: https://doi.org/10.14412/1996-7012-2023-4-64-70. (in Russian)
18. Lee S. K., Kim S. Y., Kim E. Y. et al. Mycobacterial infections in patients treated with tumor necrosis factor antagonists in South Korea. Lung. 2013; 191 (5): 565–71. doi: 10.1007/s00408-013-9481-5.
19. Murdaca G., Negrini S., Pellecchio M. et al. Update upon the infection risk in patients receiving TNF alpha inhibitors. Expert Opin Drug Saf. 2019; 18 (3): 219–229. doi: 10.1080/14740338.2019.1577817.
20. Aydin V., Akici A., Isli F. et al. Relative risk of tuberculosis in pa-tients with rheumatic diseases managed with anti-tumour necrosis factoralpha therapy: A nationwide cohort study. J Clin Pharm Ther. 2019; 44 (4): 553–560. doi: 10.1111/jcpt.12814.
21. Lin T. C., Yoshida K., Tedeschi S. K. et al. Risk of hepatitis b virus reactivation in patients with inflammatory arthritis receiving diseasemodifying antirheumatic drugs: a systematic review and meta-analysis. Arthritis Care Res (Hoboken). 2018; 70 (5): 724–731. doi: 10.1002/acr.23346.
22. Blumen Wroński J., Fiedor P. The safety profile of tumor necrosis factor inhibitors in ankylosing spondylitis: are TNF inhibitors safer than we thought? J Clin Pharmacol. 2019; 59 (4): 445–462. doi: 10.1002/jcph.1348.
23. Fragoulis G. E., Dey M., Zhao S. et al. Systematic literature review informing the 2022 EULAR recommendations for screening and prophylaxis of chronic and opportunistic infections in adults with autoimmune inflammatory rheumatic diseases. RMD Open. 2022; 8 (2): e002726. doi: 10.1136/rmdopen-2022-002726.
24. Hagberg K. W., Persson R., Vasilakis-Scaramozza C. et al. Herpes Zoster, Hepatitis C, and tuberculosis risk with apremilast compared to biologics, DMARDs and corticosteroids to treat psoriasis and psoriatic arthritis. Clin Epidemiol. 2020; 12: 153–161. doi: 10.2147/CLEP.S239511.
25. Deodhar A., van der Heijde D., Gensler L. S. et al. COAST-X Study Group. Ixekizumab for patients with non-radiographic axial spondyloarthritis (COAST-X): a randomised, placebo-controlled trial. Lancet. 2020; 395 (10217): 53–64. doi: 10.1016/S0140-6736(19)32971-X.
26. Wang P., Zhang S., Hu B. et al. Efficacy and safety of interleukin-17A inhibitors in patients with ankylosing spondylitis: a systematic review and meta-analysis of randomized controlled trials. Clin Rheumatol. 2021; 40 (8): 3053–3065. doi: 10.1007/s10067-020-05545-y.
27. Yin Y., Wang M., Liu M. et al. Efficacy and safety of IL-17 inhibitors for the treatment of ankylosing spondylitis: a systematic re-view and metaanalysis. Arthritis Res Ther. 2020; 22 (1): 111. doi: 10.1186/s13075-02002208-w.
28. Korotaeva T. V., Mazurov V. I., Lila A. M. et al. Efficacy and safety of ne-takimab in patients with psoriatic arthritis: results of the phase III PATERA clinical study. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice 2020; 58 (5): 480–488. doi: https://doi.org/10.47360/1995-4484-2020-480-488. (in Russian)
29. Korotaeva T. V., Mazurov V. I., Lila A. M., et al. Netakimab for the treatment of psoriatic arthritis: 3-year results of the phase III BCD-085-8/PATERA study. Sovremennaya Revmatologiya = Modern Rheumatology Journal. 2024; 18 (4): 33–42.]. doi: https://doi.org/10.14412/1996-7012-2024-4-33-42. (in Russian)
30. McInnes I.B., Mease P. J., Kirkham B. et al. FUTURE 2 Study Group. Secukinumab, a human anti-interleukin-17A monoclonal antibody, in patients with psoriatic arthritis (FUTURE 2): a randomised, double-blind, placebocontrolled, phase 3 trial. Lancet. 2015; 386 (9999): 1137–46. doi: 10.1016/S0140-6736(15)61134-5.
31. Saunte D. M., Mrowietz U., Puig L., Zachariae C. Candida infections in patients with psoriasis and psoriatic arthritis treated with interleukin17 inhibitors and their practical management. Br J Dermatol. 2017; 177 (1) : 47–62. doi: 10.1111/bjd.15015.
32. Winthrop K. L., Mariette X., Silva J. T. et al. ESCMID Study Group for Infections in Compromised Hosts (ESGICH) Consensus Document on the safety of targeted and biological therapies: an infectious diseases perspective (Soluble immune effector molecules [II]: agents targeting interleukins, immunoglobulins and complement factors). Clin Microbiol Infect. 2018; 24 Suppl 2: S21–S40. doi: 10.1016/j.cmi.2018.02.002.
33. McKeage K. Ustekinumab: a review of its use in psoriatic arthritis. Drugs. 2014; 74 (9): 1029–39. doi: 10.1007/s40265-014-0242-4.
34. Mease P. J., Rahman P., Gottlieb A. B. et al. DISCOVER-2 Study Group. Guselkumab in biologic-naive patients with active psoriatic arthritis (DISCOVER2): a double-blind, randomised, placebo-controlled phase 3 trial. Lancet. 2020; 395 (10230): 1126–1136. doi: 10.1016/S0140-6736(20)30263-4.
35. McInnes I.B., Rahman P., Gottlieb A. B. et al. Efficacy and safety of Guselkumab, a monoclonal antibody specific to the p19 Subunit of Interleukin-23, through two years: results from a phase iii, randomized, double-blind, placebo-controlled study conducted in biologic-naive patients with active psoriatic arthritis. Arthritis Rheumatol. 2022; 74 (3): 475–485. doi: 10.1002/art.42010.
36. Lukina G. V., Borisov S. E. Screening and monitoring of tuberculosis infection in patients with rheumatic diseases receiving genetically engineered biological drugs. In: Nasonov E. L. (ed.). Rossiiskie Klinicheskie Rekomendatsii. Revmatologiya. Russian Clinical Guidelines. Rheumatology]. Moscow: GEOTAR-Media; 2017; 394–410]. (in Russian)
37. Nasonov E. L., Korotaeva T. V. Janus kinase inhibitors in immunoinflammatory diseases: 10 years of clinical practice in rheumatology. Rheumatology Science and Practice. 2022; 60 (2): 131–148. doi: https://doi.org/10.47360/1995-4484-2022-131-148. (in Russian)
38. Keeling S., Maksymowych W. P. JAK inhibitors, psoriatic arthritis, and axial spondyloarthritis: a critical review of clinical trials. Expert Rev Clin Immunol. 2021; 17 (7): 701–715. doi: 10.1080/1744666X.2021.1925541.
39. Mease P., Coates L. C., Helliwell P. S. et al. Efficacy and safety of filgotinib, a selective Janus kinase 1 inhibitor, in patients with active psoriatic arthritis (EQUATOR): results from a randomised, placebo-controlled, phase 2 trial. Lancet. 2018 Dec 1; 392 (10162): 2367–2377. doi: 10.1016/S0140-6736(18)32483-8. Epub 2018 Oct 22. PMID: 30360969.
40. Almanzar G., Kienle F., Schmalzing M. et al. Tofacitinib modulates the VZV-specific CD4+ T cell immune response in vitro in lymphocytes of patients with rheumatoid arthritis. Rheumatology (Oxford). 2019; 58 (11): 2051–2060. doi: 10.1093/rheumatology/kez175.
41. Atzeni F., Talotta R., Nucera V. et al. Adverse events, clinical considerations and management recommendations in rheumatoid arthritis patients treated with JAK inhibitors. Expert Rev Clin Immunol. 2018; 14 (11): 945–956. doi: 10.1080/1744666X.2018.1504678.
42. Burmester G. R., Curtis J. R., Yun H. et al. An integrated analysis of the safety of Tofacitinib in psoriatic arthritis across phase III and long-term extension studies with comparison to real-world observational data. Drug Saf. 2020; 43 (4): 379–392. doi: 10.1007/s40264-020-00904-9.
43. Burmester G. R., Winthrop K., Blanco R. et al. Safety profile of Upadacitinib up to 3 years in psoriatic arthritis: an integrated analysis of two pivotal phase 3 trials. Rheumatol Ther. 2022; 9 (2): 521–539. doi: 10.1007/s40744021-00410-z.
44. Baumrin E., Van Voorhees A., Garg A. et al. A systematic review of herpes zoster incidence and consensus recommendations on vaccination in adult patients on systemic therapy for psoriasis or psoriatic arthritis: From the Medical Board of the National Psoriasis Foundation. J Am Acad Dermatol. 2019; 81 (1): 102–110. doi: 10.1016/j.jaad.2019.03.017.
45. Haber S. L., Hamilton S., Bank M. et al. Apremilast: a novel drug for treatment of psoriasis and psoriatic arthritis. Ann Pharmacother. 2016; 50 (4): 282–90. doi: 10.1177/1060028015627467.
46. Nash P., Ohson K., Walsh J. et al. Early and sustained efficacy with apremilast monotherapy in biological-naïve patients with psoriatic arthritis: a phase IIIB, randomised controlled trial (ACTIVE). Ann Rheum Dis. 2018; 77 (5): 690–698. doi: 10.1136/annrheumdis-2017-211568.
47. Wells A. F., Edwards C. J., Kivitz A. J. et al. Apremilast monotherapy in DMARD-naive psoriatic arthritis patients: results of the randomized, placebo-controlled PALACE 4 trial. Rheumatology (Oxford). 2018; 57 (7): 1253–1263. doi: 10.1093/rheumatology/key032.
48. Keating G. M. Apremilast: a review in psoriasis and psoriatic arthritis. Drugs. 2017; 77 (4): 459–472. doi: 10.1007/s40265-017-0709-1.
49. Hagberg K. W., Persson R., Vasilakis-Scaramozza C. et al. Herpes Zoster, Hepatitis C, and tuberculosis risk with apremilast compared to biologics, DMARDs and corticosteroids to treat psoriasis and psoriatic arthritis. Clin Epidemiol. 2020; 12: 153–161. doi: 10.2147/CLEP.S239511.
50. Germano V., Cattaruzza M. S., Osborn J. et al. Infection risk in rheumatoid arthritis and spondyloarthropathy patients under treatment with DMARDs, corticosteroids and TNF-α antagonists. J Transl Med. 2014; 12: 77. doi: 10.1186/1479-5876-12-77.
51. Fouque-Aubert A., Jette-Paulin L., Combescure C. et al. Serious infections in patients with ankylosing spondylitis with and without TNF blockers: a systematic review and meta-analysis of randomised placebo-controlled trials. Ann Rheum Dis. 2010; 69 (10): 1756–61. doi: 10.1136/ard.2008.098822.
52. Wang S., He Q., Shuai Z. Risk of serious infections in biological treatment of patients with ankylosing spondylitis and non-radiographic axial spondyloarthritis: a meta-analysis. Clin Rheumatol. 2018; 37 (2): 439–450. doi: 10.1007/s10067-017-3966-1.
53. Xu Z., Xu P., Fan W. et al. Risk of infection in patients with spondyloarthritis and ankylosing spondylitis receiving antitumor necrosis factor therapy: A meta-analysis of randomized controlled trials. Exp Ther Med. 2017; 14 (4): 3491–3500. doi: 10.3892/etm.2017.5003.
54. Moura C. S., Rahme E., Maksymowych W. P. et al. Use of disease-modifying anti-rheumatic or anti-tumour necrosis factor drugs and risk of hospitalized infection in ankylosing spondylitis. Scand J Rheumatol. 2019; 48 (2) : 121–127. doi: 10.1080/03009742.2018.1470253.
55. Wallis D., Thavaneswaran A., Haroon N. et al. Tumour necrosis factor in-hibitor therapy and infection risk in axial spondyloarthritis: results from a longitudinal observational cohort. Rheumatology (Oxford). 2015; 54 (1): 152–6. doi: 10.1093/rheumatology/keu255.
56. Lim D. H., Kim Y. J., Kim S. O. et al. The risk of herpes zoster in patients with ankylosing spondylitis: Analysis of the Korean National Health Insurance Service — Sample cohort database. Mod Rheumatol. 2018; 28 (1): 168–173. doi: 10.1080/14397595.2017.1325034.
57. Takeshita J., Grewal S., Langan S. M. et al. Psoriasis and comorbid diseases: Implications for management. J Am Acad Dermatol. 2017; 76 (3) : 393–403. doi: 10.1016/j.jaad.2016.07.065.
58. Britanova O. V., Lupyr K. R., Staroverov D. B. et al. Targeted depletion of TRBV9+ T cells as immunotherapy in a patient with ankylosing spondylitis. Nat Med. 2023; 29 (11): 2731–2736. doi: 10.1038/s41591-023-02613-z.
59. Nasonov E. L., Mazurov V. I., Lila A. M. et al. Effectiveness and safety of BCD180, anti-TRBV9+ T-lymphocytes monoclonal antibody in patients with active radiographic axial spondyloarthritis: 36-week results of double-blind randomized placebo-controlled phase II clinical study ELEFTA. Rheumatology Science and Practice. 2024; 62 (1): 65–80. doi: https://doi.org/10.47360/1995-4484-2024-65-80. (in Russian)
60. WHO Coronavirus (COVID-19) Dashboard/https://www.who.int/emergencies/diseases/novel-coronavirus-2019.
61. Belov B. S., Karateev A. E. COVID-19: the new challenge for rheumatologists. Sovremennaya Revmatologiya = Modern Rheumatology Journal. 2020; 14 (2): 110–116.]. doi: https://doi.org/10.14412/1996-7012-2020-2-110-116. (in Russian)
62. Gianfrancesco M., Hyrich K. L., Al-Adely S. et al. COVID-19 Global Rheumatology Alliance. Characteristics associated with hospitalisation for COVID-19 in people with rheumatic disease: data from the COVID-19 Global Rheumatology Alliance physician-reported registry. Ann Rheum Dis. 2020; 79 (7): 859–866. doi: 10.1136/annrheumdis-2020-217871.
63. Raiker R., Pakhchanian H., Kavadichanda C. et al. Axial spondyloarthritis may protect against poor outcomes in COVID-19: propensity score matched analysis of 9766 patients from a nationwide multi-centric research network. Clin Rheumatol. 2022; 41 (3): 721–730. doi: 10.1007/s10067-021-05979-y.
64. Kulikov A. N., Muravyeva N. V., Belov B. S. Risk factors for severe COVID-19 in patients with rheumatic diseases. Nauchno-Prakticheskaya Revmatologia = Rheumatology Science and Practice. 2024; 62 (1): 24–31. doi: https://doi.org/10.47360/1995-4484-2024-24-31. (in Russian)]
65. Furer V., Rondaan C., Heijstek M. W. et al. 2019 update of EULAR recommendations for vaccination in adult patients with autoimmune inflammatory rheumatic diseases. Ann Rheum Dis. 2020; 79 (1): 39–52. doi: 10.1136/annrheumdis-2019-215882.
66. Bass A. R., Chakravarty E., Akl E. A. et al. 2022 American College of Rheumatology Guideline for Vaccinations in patients with rheumatic and musculoskeletal diseases. Arthritis Care Res (Hoboken). 2023; 75 (3): 449–464. doi: 10.1002/acr.25045.
67. Baranova M. M., Muravyeva N. V., Belov B. S., Diatroptov M. E. Immunogenicity, efficacy and safety of the three-valent in-activated influenza split vaccine in patients with ankylosing spondylitis and psoriatic arthritis. Nauchno-Prakticheskaya Revmatologia = Rheumatology Science and Practice. 2024; 62 (3): 293–299. doi: https://doi.org/10.47360/1995-4484-2024-293-299. (in Russian)
68. Baranova M. M., Muravyeva N. V., Belov B. S., Verizhnikova Zh.G. Experience with 23valent pneumococcal polysaccharide vaccine in patients with ankylosing spondylitis and pso-riatic arthritis. Medical alphabet. 2023; (31): 15–20. doi: https://doi.org/10.33667/2078-5631-2023-31-15-20. (in Russian)
Review
For citations:
Baranova M.M., Muravyeva N.V., Belov B.S. Comorbid Infections in Spondyloarthritis: the Current State of the Problem. Antibiot Khimioter = Antibiotics and Chemotherapy. 2024;69(11-12):127-135. (In Russ.) https://doi.org/10.37489/0235-2990-2024-69-11-12-127-135. EDN: NGHLKV
Views:
477
Email this article 