HIV-infection and rheumatic diseases: the current state of the problem
https://doi.org/10.22328/2077-9828-2025-17-1-7-18
Abstract
The problem of autoimmune diseases in HIV-infected patients is interdisciplinary, and differential diagnosis issues often come to the fore. The interaction between HIV and the human immune system is characterized by an imbalance in lymphocyte populations with selective depletion of certain subtypes of CD4 lymphocytes and preservation of immune activation. This imbalance, which persists for a long time, provokes the early appearance of the immune aging phenotype, which is associated with an increase in the frequency of autoimmune reactions. The incidence of rheumatic diseases in people living with HIV (PLHIV) is increasing, while timely diagnosis, justification, selection and early initiation of complex therapy for comorbid pathology are extremely urgent tasks. The incidence of autoimmune diseases in PLHIV varies: systemic lupus erythematosus — 6.25%, reactive arthritis (often HLA-B27-associated) — 2.67%, psoriatic arthritis — 1–3%, rheumatoid arthritis — 0.29%, Sjogren’s syndrome — 0.03%, systemic vasculitis — 1%, also several pathological processes can develop simultaneously. It is not uncommon to detect a number of autoantibodies without developing an autoimmune disease symptoms. It is necessary to take into account the features of prescribing antirheumatic therapy in the context of mandatory and continuous antiretroviral therapy (ART), constant monitoring of the number of CD4 lymphocytes and HIV RNA in the blood, the risk of developing immune reconstitution inflammatory syndrome and reactivation of opportunistic infections with severe immunosuppression. Management of patients with complex comorbidity, such as HIV infection and rheumatic diseases, should be carried out as part of an interdisciplinary team with the mandatory participation of an infectious disease specialist, constant monitoring of the number of CD4 lymphocytes and the level of HIV viral load in the blood.
About the Authors
G. I. GridnevaRussian Federation
B. S. Belov
Russian Federation
E. S. Aronova
Russian Federation
References
1. HIV infection in adults. Clinical guidelines. 2024 (In Russ.). https://cr.minzdrav.gov.ru/schema/79_2.
2. HIV infection in the Russian Federation as of June 30, 2023. Specialized research department for the prevention and control of AIDS of the Central Research Institute of Epidemiology of Rospotrebnadzor (In Russ.). https://files.antispidnn.ru/uploads/docs/spec/vich2023.pdf.
3. Steve R.J., Alex D., Yesudhason B.L. et al. Autoantibodies Among HIV-1 Infected Individuals and the Effect of Anti-Retroviral Therapy (ART) on It // Current HIV research. 2021. Vol. 19, No. 3. R. 277-285. https://doi.org/10.2174/1570162X19666210217120337.
4. Zandman-Goddard G., Shoenfeld Y. HIV and autoimmunity // Autoimmunity reviews. 2002. Vol. 1, No. 6. P. 329-337. https://doi.org/10.1016/s1568-9972(02)00086-1.
5. Fox C., Walker-Bone K. Evolving spectrum of HIV-associated rheumatic syndromes. Best practice research // Clinical rheumatology. 2015. Vol. 29, No. 2. P. 244-258. https://doi.org/10.1016/j.berh.2015.04.019.
6. Ramos-Ruperto L., Busca C., Díez-Vidal A. et al. Prevalence and Temporal Trends of Autoimmune Diseases in People Living with HIV // AIDS Res. Hum. Retroviruses. 2023 Mar; Vol. 39, No. 3. R. 130-135. https://doi.org/10.1089/AID.2022.0090.
7. Ramos-Ruperto L. et al. Autoimmunity and HIV infection. Chapter 7 // Translational Autoimmunity. Vol. 3. R. 141. https://doi.org/10.1016/B978-0-323-85415-3.00015-5.
8. Evans R., Gueret-Wardle A., Edwards S., Salama A. ANCA-associated vasculitis and pauci-immune glomerulonephritis in HIV disease // BMJ case reports 2014. P. 1-3. Published online 1 April 2014. https://doi.org/10.1136/bcr-2013-202423.
9. Mirsaeidi M., Syed F., Jaffe E.S. Antineutrophil Cytoplasmic Autoantibody Associated Systemic Vasculitis Is Associated with Epstein-Barr virus in the Setting of HIV Infection // Infectious diseases in clinical practice (Baltimore, Md.). 2013. Vol. 21, No. 1. P. 50-53. https://doi.org/10.1097/IPC.0b013e3182601ea1.
10. Savige J.A., Chang L., Horn S., Crowe S.M. Anti-nuclear, anti-neutrophil cytoplasmic and anti-glomerular basement membrane antibodies in HIV-infected individuals // Autoimmunity. 1994. Vol. 18, No. 3. P. 205-211. https://doi.org/10.3109/08916939409007997
11. Mohapatra P. R., Khanduri S., Dutt N., Sharma P., Janmeja A. K. Diagnostic dilemma of antineutrophil cytoplasmic antibody seropositivity in human immunodeficiency virus infection // The Indian journal of chest diseases allied sciences. 2011. Vol. 53, No. 1. P. 55-57.
12. Gherardi R., Belec L., Mhiri C. et al. The spectrum of vasculitis in human immunodeficiency virus-infected patients. A clinicopathologic evaluation // Arthritis and rheumatism. 1993. Vol. 36, No. 8. P. 1164-1174. https://doi.org/10.1002/art.1780360818.
13. Bottlaender L., Sève P., Cotte L., Gerfaud-Valentin M., Jamilloux Y. Successful treatment with anakinra of an HIV-associated immune reconstitution inflammatory syndrome mimicking adult-onset Still’s disease // Rheumatology (Oxford, England). 2019. Vol. 58, No. 2. P. 363-365. https://doi.org/10.1093/rheumatology/key291.
14. Russian clinical recommendations. Rheumatology / ed. E. L. Nasonova. Moscow: GEOTAR-Media, 2017, r. 113 (In Russ).
15. Akram B., Khan M., Humphrey M.B. HIV-Associated Rheumatic Diseases: A Narrative Review // Journal of clinical rheumatology: practical reports on rheumatic musculoskeletal diseases. 2024. Vol. 30, No. 2. P. e42-e45. https://doi.org/10.1097/RHU.0000000000002028.
16. Lebrun D., Hentzien M., Cuzin L. et al.; the Dat’AIDS study group. Epidemiology of autoimmune and inflammatory diseases in a French nationwide HIV cohort // AIDS. 2017. Sep 24; Vol. 31, No. 15. R. 2159-2166. https://doi.org/10.1097/QAD.0000000000001603.
17. Kawakita C., Kinomura M., Otaka N. et al. HIV-associated Immune Complex Kidney Disease with C3-dominant Deposition Induced by HIV Infection after Treatment of IgA Nephropathy // Internal medicine (Tokyo, Japan). 2019. Vol. 58, No. 20. P. 3001-3007. https://doi.org/10.2169/internalmedicine.2439-18.
18. Naovarat B.S., Reveille J.D., Salazar G.A., William F.M., Nguyen B.Y. Systemic lupus erythematosus in the setting of HIV-1 infection: a longitudinal analysis // Clinical rheumatology. 2020. Vol. 39, No. 2. P. 413-418. https://doi.org/10.1007/s10067-019-04867-w.
19. Torgashina A.V., Solovyev S.K. Specific features of regulatory T cells in patients with systemic lupus erythematosus // Modern Rheumatology Journal. 2018. Vol. 12, No. 4. P. 9-15. https://doi.org/10.14412/1996-7012-2018-4-9-15.
20. Liao H.Y., Tao C.M., Su J. Concomitant systemic lupus erythematosus and HIV infection: A rare case report and literature review // Medicine. 2017. Vol. 96, No. 51. P. e9337. https://doi.org/10.1097/MD.0000000000009337.
21. O’Kelly B., McNally C., McConkey S., Durcan L. HIV and systemic lupus erythematosus: where immunodeficiency meets autoimmunity // Lupus. 2020. Vol. 29, No. 9. P. 1130-1132. https://doi.org/10.1177/0961203320934851.
22. Russian clinical recommendations. Rheumatology / pod red. E. L. Nasonova. Moscow: GJeOTAR-Media, 2020, r. 17 (In Russ.).
23. Smolen J.S., Aletaha D., McInnes I.B. Rheumatoid arthritis // Lancet (London, England). 2016. Vol. 388, No. 10055. P. 2023-2038. https://doi.org/10.1016/S0140-6736(16)30173-8.
24. Reveille J.D., Williams F.M. Infection and musculoskeletal conditions: Rheumatologic complications of HIV infection. Best practice and research // Clinical rheumatology. 2006. Vol. 20, No. 6. P. 1159-1179. https://doi.org/10.1016/j.berh.2006.08.015.
25. Bukhanova D.V., Belov B.S. Joint damage in HIV positive patients. Medical advice, 2018, No. 9, rr. 82-87 (In Russ.).
26. Hanberg J.S., Hsieh E., Akgün K.M., Weinstein E., Fraenkel L., Justice A.C., VACS Project Team. Incident Rheumatoid Arthritis in HIV Infection: Epidemiology and Treatment // Arthritis rheumatology (Hoboken N.J.). 2021. Vol. 73, No. 12. P. 2189-2199. https://doi.org/10.1002/art.41802.
27. Cunha B.M., Mota L.M., Pileggi G.S., Safe I.P., Lacerda M.V. HIV/AIDS and rheumatoid arthritis // Autoimmunity reviews. 2015. Vol. 14, No. 5. P. 396-400. https://doi.org/10.1016/j.autrev.2015.01.001.
28. Azeroual A., Harmouche H., Benjilali L. et al. Rheumatoid arthritis associated to HIV infection // European journal of internal medicine. 2008. Vol. 19, No. 6. P. e34-e35. https://doi.org/10.1016/j.ejim.2007.09.020.
29. Mariette X., Criswell L.A. Primary Sjögren’s Syndrome // The New England journal of medicine. 2018. Vol. 378, No. 10. P. 931-939. https://doi.org/10.1056/NEJMcp1702514.
30. Ghrenassia E., Martis N., Boyer J. et al. The diffuse infiltrative lymphocytosis syndrome (DILS). A comprehensive review // Journal of autoimmunity. 2015. No. 59, P. 19-25. https://doi.org/10.1016/j.jaut.2015.01.010.
31. Yang J.J., Tsai M.S., Sun H.Y. et al. Autoimmune diseases-related arthritis in HIV-infected patients in the era of highly active antiretroviral therapy // Journal of microbiology, immunology, and infection=Wei mian yu gan ran za zhi. 2015. Vol. 48, No. 2. P. 130-136. https://doi.org/10.1016/j.jmii.2013.08.002.
32. Kanevskaya M.Z. Rheumatological syndromes in HIV infection. Clinical Medicine, 2014, Vol. 92, No. 12, pp. 12-19 (In Russ.).
33. McArthur C.P., Africa C.W., Castellani W.J. et al. Salivary gland disease in HIV/AIDS and primary Sjögren’s syndrome: analysis of collagen I distribution and histopathology in American and African patients // Journal of oral pathology medicine: official publication of the International Association of Oral Pathologists and the American Academy of Oral Pathology. 2003. Vol. 32, No. 9. P. 544-551. https://doi.org/10.1034/j.1600-0714.2003.00159.x.
34. Saigal R., Chakraborty A., Yadav R.N., Goyal L.K. Rheumatological Manifestations in HIV-Positive Patients: A Single-Center Study // Advances in therapy. 2020. Vol. 37, No. 10. P. 4336-4345. https://doi.org/10.1007/s12325-020-01470-3.
35. Kordossis T., Paikos S., Aroni K. et al. Prevalence of Sjögren’s-like syndrome in a cohort of HIV-1-positive patients: descriptive pathology and immunopathology // British journal of rheumatology. 1998. Vol. 37, No. 6. P. 691-695. https://doi.org/10.1093/rheumatology/37.6.691
36. Kuvardin E.S., Grigor’yeva I.N., Bekhtereva I.A., Maslyansky A.L., Krivolapov Yu.A., Belyakova E.A. Cellular composition of the minor salivary gland inflammatory infiltrates as an additional diagnostic criterion for primary Sjogren’s syndrome // Rheumatology Science and Practice. 2021. Vol. 59, No. 4. P. 434-441 (In Russ.). https://doi.org/10.47360/1995-4484-2021-434-441.
37. Russian clinical recommendations. Rheumatology / ed. E. L. Nasonova. Moscow: GEOTAR-Media, 2020. 182 p. (In Russ.).
38. Vega L.E., Espinoza L.R. Vasculitides in HIV Infection // Current rheumatology reports. 2020. Vol. 22, No. 10. P. 60. https://doi.org/10.1007/s11926-020-00945-0.
39. Zhang X., Li H., Li T., Zhang F., Han Y. Distinctive rheumatic manifestations in 98 patients with human immunodeficiency virus infection in China // The Journal of rheumatology. 2007. Vol. 34, No. 8. P. 1760-1764.
40. Vornicu A., Obrișcă B., Sorohan B., Berechet A., Ismail G. ANCA-associated vasculitis in a HIV-infected patient:a case-based review // BMC nephrology. 2023. Vol. 24, No. 1. P. 210. https://doi.org/10.1186/s12882-023-03244-9.
41. De Paoli M.C., Moretti D., Scolari Pasinato C.M., Buncuga M.G. Púrpura de Schönlein-Henoch en adulto HIV positivo adicto a cocaína y ANCAp positivo Henoch-Schönlein purpura in a cocaine consumer man with HIV infection and ANCA-p positivity. Spanish Medicina. 2016. Vol. 76, No. 4. P. 245-248.
42. Monteiro E.J., Caron D., Balda C.A. et al. Anti-glomerular basement membrane glomerulonephritis in an HIV positive patient: case report // The Brazilian journal of infectious diseases: an official publication of the Brazilian Society of Infectious Diseases. 2006. Vol. 10, No. 1. P. 55-58. https://doi.org/10.1590/s1413-86702006000100011.
43. Maharaj A.B. Rheumatoid arthritis and HIV-associated arthritis: Two sides of the same coin or different coins. Best practice research // Clinical rheumatology. 2022. Vol. 36, No. 1. P. 101739. https://doi.org/10.1016/j.berh.2021.101739.
44. Mody G.M., Parke F.A., Reveille, J.D. Articular manifestations of human immunodeficiency virus infection // Best practice and research // Clinical rheumatology. 2003. Vol. 17, No. 2. P. 265-287. https://doi.org/10.1016/s1521-6942(03)00003-2.
45. Lawson E., Walker-Bone K. The changing spectrum of rheumatic disease in HIV infection // British medical bulletin. 2012. Vol. 103, No. 1. P. 203-221. https://doi.org/10.1093/bmb/lds022.
46. Kruglova L.S., Pereverzina N.O. Risks of infectious diseases in patients with skin psoriasis taking genetically engineered drugs: data from our own study. Effective pharmacotherapy, 2024, Vol. 20, No. 1, pp. 6-16 (In Russ.) https://doi.org/10.33978/2307-3586-2024-20-1-6-16.
47. Ceccarelli M., Venanzi Rullo E., Vaccaro M. et al. HIV-associated psoriasis: Epidemiology, pathogenesis, and management // Dermatologic therapy. 2019. Vol. 32, No. 2. P. e12806. https://doi.org/10.1111/dth.12806.
48. Fink D.L., Hedley L., Miller R.F. Systematic review of the efficacy and safety of biological therapy for inflammatory conditions in HIV-infected individuals // International journal of STD AIDS. 2017. Vol. 28, No. 2. P. 110-119. https://doi.org/10.1177/0956462416675109.
49. Nakamura M., Abrouk M., Farahnik B., Zhu T. H., Bhutani T. Psoriasis treatment in HIV-positive patients: a systematic review of systemic immunosuppressive therapies // Cutis. 2018. Vol. 101, No. 1. P. 38-56.
50. Alpalhão M., Borges-Costa J., Filipe P. Psoriasis in HIV infection: an update // International journal of STD AIDS. 2019. Vol. 30, No. 6. P. 596- 604. https://doi.org/10.1177/0956462419827673.
51. Gridneva G.I., Belov B.S. Current issues in the management of patients with HIV infection and rheumatic diseases. Modern Rheumatology Journal, 2021, Vol. 15, No. 6, rr. 7-12 (In Russ.). https://doi.org/10.14412/1996-7012-2021-6-7-12.
52. Eliseeva M.E., Eliseev M.S. The significance of hyperuricemia in the development of human diseases and methods of its correction. Doctor. Ru. 2019, Vol. 2, No. 157, pp. 47-54 (In Russ.). https://doi.org/10.31550/1727-2378-2019-157-2-47-54.
53. Creighton S., Miller R., Edwards S., Copas A., French P. Is ritonavir boosting associated with gout? // International journal of STD AIDS. 2005. Vol. 16, No. 5. P. 362-364. https://doi.org/10.1258/0956462053888907.
54. Nicholson P., Saunsbury E., D’Angelo S., Churchill D., Walker-Bone K. Prevalence of and risk factors for gout in HIV-positive adults: A casecontrol study // International journal of STD AIDS. 2019. Vol. 30, No. 3. P. 249-255. https://doi.org/10.1177/0956462418799803.
55. Afzal W., Wali O.M., Cervellione K.L., Singh B.B., Bagheri F. Coexistent Pseudogout and Mycobacterium avium-intracellulare Septic Arthritis in a Patient with HIV and ESRD // Case reports in rheumatology. 2016. 5495928. https://doi.org/10.1155/2016/5495928.
56. Hanberg J.S., Akgün K.M., Hsieh E., Fraenkel L., Justice A.C. Incidence and Presentation of Sarcoidosis With and Without HIV Infection // Open forum infectious diseases. 2020. Vol. 7, No. 10. ofaa441. https://doi.org/10.1093/ofid/ofaa441.
57. Foulon G., Wislez M., Naccache J. M. et al. Sarcoidosis in HIV-infected patients in the era of highly active antiretroviral therapy // Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. 2004. Vol. 38, No. 3. P. 418-425. https://doi.org/10.1086/381094.
58. Trevenzoli M., Cattelan A.M., Marino F., Marchioro U., Cadrobbi P. Sarcoidosis and HIV infection: a case report and a review of the literature // Postgraduate medical journal. 2003. Vol. 79, No. 935. P. 535-538. https://doi.org/10.1136/pmj.79.935.535.
59. Ibrahim I.A., Estaitieh O.M., Alrabee H.A., Alzahrani M. Sarcoidosis and HIV infection in a native Saudi man // BMJ case reports. 2018. bcr2018224386. https://doi.org/10.1136/bcr-2018-224386.
60. Adizie T., Moots R.J., Hodkinson B., French N., Adebajo A.O. Inflammatory arthritis in HIV positive patients: A practical guide // BMC infectious diseases. 2016. No. 16. R. 100. https://doi.org/10.1186/s12879-016-1389-2.
61. Packham J., Arkell P., Sheeran T., Brownfield A., Cadwgan A., Ryan, S. Patient experiences, attitudes and expectations towards receiving information about anti-TNF medication: a quantitative study // Clinical rheumatology. 2017. Vol. 36, No. 11. P. 2595-2600. https://doi.org/10.1007/s10067-017-3642-5.
62. Fink D.L., Hedley L., Miller R.F. Systematic review of the efficacy and safety of biological therapy for inflammatory conditions in HIV-infected individuals // International journal of STD AIDS. 2017. Vol. 28, No. 2. P. 110-119. https://doi.org/10.1177/0956462416675109.
63. Pangilinan M. C. G., Sermswan P., Asawanonda P. Use of Anti-IL-17 Monoclonal Antibodies in HIV Patients with Erythrodermic Psoriasis // Case reports in dermatology. 2020. Vol. 12, No. 2. P. 132-137. https://doi.org/10.1159/000508781.
64. Di Lernia V., Casanova D. M., Garlassi E. Secukinumab in an HIV-positive patient with psoriasis // Journal der Deutschen Dermatologischen Gesellschaft=Journal of the German Society of Dermatology: JDDG. 2019. Vol. 17, No. 6. P. 646-648. https://doi.org/10.1111/ddg.13851.
65. Bartos G., Cline A., Beroukhim K., Burrall B. A., Feldman S. R. Current biological therapies for use in HIV-positive patients with psoriasis: case report of gesulkumab used and review // Dermatology online journal. 2018. Vol. 24, No. 11. 13030/qt3db748cg.
66. Paparizos V., Rallis E., Kirsten L., Kyriakis K. Ustekinumab for the treatment of HIV psoriasis // The Journal of dermatological treatment. 2012. Vol. 23, No. 6. P. 398-399. https://doi.org/10.3109/09546634.2011.579085.
67. Saeki H., Ito T., Hayashi M. et al. Successful treatment of ustekinumab in a severe psoriasis patient with human immunodeficiency virus infection // Journal of the European Academy of Dermatology and Venereology: JEADV. 2015. Vol. 29, No. 8. P. 1653-1655. https://doi.org/10.1111/jdv.12531.
68. Bardazzi F., Magnano M., Campanati A. et al. Biologic Therapies in HIV-infected Patients with Psoriasis: An Italian Experience // Acta dermato- venereologica. 2017. Vol. 97, No. 8. P. 989-990. https://doi.org/10.2340/00015555-2698.
69. Wang D.M., Fernandez A.P., Calabrese C.M., Calabrese L.H. Treatment of psoriasis with ustekinumab in a patient with HIV-related Kaposi sarcoma // Clinical and experimental dermatology. 2019. Vol. 44, No. 1. P. 113-115. https://doi.org/10.1111/ced.13630.
70. Cepeda E.J., Williams F.M., Ishimori M.L. et al. The use of anti-tumour necrosis factor therapy in HIV-positive individuals with rheumatic disease // Annals of the rheumatic diseases. 2008. Vol. 67, No. 5. P. 710-712. https://doi.org/10.1136/ard.2007.081513.
71. Wangsiricharoen S., Ligon C., Gedmintas L. et al. Rates of Serious Infections in HIV-Infected Patients Receiving Tumor Necrosis Factor Inhibitor Therapy for Concomitant Autoimmune Diseases // Arthritis care research. 2017. Vol. 69, No. 3. P. 449-452. https://doi.org/10.1002/acr.22955.
72. Narcisi A., Bernardini N., Orsini D. et al. Long-term safety and efficacy of adalimumab in psoriasis: a multicentric study focused on infections (connecting study) // Postepy dermatologii i alergologii. 2020. Vol. 37, No. 3. P. 428-434. https://doi.org/10.5114/ada.2020.96910.
73. Liang S.J., Zheng Q.Y., Yang Y. L. et al. Use of etanercept to treat rheumatoid arthritis in an HIV-positive patient: a case-based review // Rheumatology international. 2017. Vol. 37, No. 7. P. 1207-1212. https://doi.org/10.1007/s00296-017-3690-9.
74. Marcelin A.G., Aaron L., Mateus C. et al. Rituximab therapy for HIV-associated Castleman disease // Blood. 2003. Vol. 102, No. 8. P. 2786- 2788. https://doi.org/10.1182/blood-2003-03-0951.
75. Zalmanovich A., Ben-Ami R., Rahav G. et al. Rituximab identified as an independent risk factor for severe PJP: A case-control study // PloS One. 2020. Vol. 15, No. 9. P. e0239042. https://doi.org/10.1371/journal.pone.0239042.
76. Habbous S., Guo H., Beca J. et al. The effectiveness of rituximab and HIV on the survival of Ontario patients with diffuse large B-cell lymphoma // Cancer medicine. 2020. Vol. 9, No. 19. P. 7072-7082. https://doi.org/10.1002/cam4.3362.
77. Hoff P., Walther M., Wesselmann H. et al. Erfolgreiche Behandlung eines adulten Morbus Still mit Tofacitinib bei einer HIV-2-positiven Patientin Successful treatment of adult Still’s disease with tofacitinib in a HIV-2 positive female patient // Zeitschrift fur Rheumatologie. 2020. Vol. 79, No. 10. P. 1046-1049. https://doi.org/10.1007/s00393-020-00853-9.
Review
For citations:
Gridneva G.I., Belov B.S., Aronova E.S. HIV-infection and rheumatic diseases: the current state of the problem. HIV Infection and Immunosuppressive Disorders. 2025;17(1):7-18. (In Russ.) https://doi.org/10.22328/2077-9828-2025-17-1-7-18