Русский
Impact of hyperuricemia at the clinical course of systemic lupus erythematosus and comorbid conditions in young and middle-aged female patients
DOI: https://dx.doi.org/10.18565/therapy.2025.1.37-46
Musiychuk M.M., Gaydukova I.Z., Mazurov V.I., Inamova O.V., Aliev D.B., Lapin S.V.
1) V.A. Nasonova Clinical Rheumatology Hospital No. 25, Saint Petersburg; 2) I.I. Mechnikov North-West State Medical University of the Ministry of Healthcare of Russia, Saint Petersburg; 3) Academician I.P. Pavlov First Saint Petersburg State Medical University of the Ministry of Healthcare of Russia
The aim: to estimate the peculiarities of the clinical course and treatment of SLE, as well as the incidence and characteristics of comorbid conditions in female patients with HU.
Material and methods. The data of 187 SLE female patients aged 18–60 years, observed in V.A. Nasonova Clinical Rheumatology Hospital No. 25 were studied. Clinical and laboratory manifestations and treatment of SLE, as well as the structure of comorbid conditions with an increase of serum uric acid (UA) > 360 μmol/l (n = 104) and with UA ≤ 360 μmol/l (n = 83) were compared.
Results. In case of SLE and HU combination (huSLE), a longer duration of the disease and a higher body mass index (BMI) were observed than in case of SLE with normouricemia (nuSLE). In addition, in the first case, skin lesions (33.33 and 27.16%, respectively, p = 0.035), serositis (22.12 and 8.3%, p = 0.005), and after 45 years, lupus nephritis (28.92 and 8.43%, p = 0.03) were more often detected. With comparable activity and frequency of achieving remission, basic drugs were used more often in huSLE than in nuSLE, and the risk of steroid resistance was higher. In patients with huSLE, comparatively to nuSLE, arterial hypertension (AH) (50 and 25.3%, p = 0.0006), chronic kidney disease (CKD) (5.95 and 17.31%, p = 0.008), autoimmune thyroiditis (17.31 and 4.82, p = 0.0097) were more often observed, also there was a higher risk of cardiovascular events (5.3 and 2.8% according to the QRISK3 scale, p = 0.0004) and the Charlson comorbidity index (2.18 ± 1.34 and 1.84 ± 1.07, p = 0.032). Also, in case of huSLE, acute cerebrovascular accidents (ACVA) developed significantly more often than with nuSLE.
Conclusion. Comparatively to patients without HU, 18–60 years old females with SLE and HU had a longer disease duration, higher BMI, higher incidence of arterial hypertension, ACVA, stage 2–3 CKD, autoimmune thyroiditis, lupus nephritis, lower levels of complement fractions C3 and C4, higher erythrocyte sedimentation rate, as well as a higher risk of steroid resistance, cardiovascular events, and the total risk of comorbidity according to the Charlson index. Achieving remission or low SLE activity in case of HU required more frequent use of disease-modifying drugs than in case of normouricemia.
Literature
1. Мазуров В.И., Сайганов С.А., Башкинов Р.А. с соавт. Влияние уратснижающей терапии на течение хронической болезни почек у пациентов с остеоартритом и бессимптомной гиперурикемией. Терапия. 2023; 9(7): 56–71. (Mazurov V.I., Sayganov S.A., Bashkinov R.A. et al. Effect of urate-lowering therapy on the progression of chronic kidney disease in patients with osteoarthritis and asymptomatic hyperuricemia. Terapiya = Therapy. 2023; 9(7): 56–71 (In Russ.)). https://dx.doi.org/10.18565/therapy.2023.7.56-71. EDN: RDYJFA. 2. Цинзерлинг А.Ю., Мазуров В.И., Гайдукова И.З. с соавт. Бессимптомная гиперурикемия и рентгенологическое прогрессирование ревматоидного артрита. РМЖ. Медицинское обозрение. 2022; 6(8): 470–479. (Tsinserling A.Yu., Mazurov V.I., Gaydukova I.Z. et al. Asymptomatic hyperuricemia and radiographic progression of rheumatoid arthritis. Russkiy meditsisnkiy zhurnal. Meditsinskoye obozreniye = Russian Medical Journal. Medical Review. 2022; 6(8): 470–479 (In Russ.)). https://doi.org/10.32364/2587-6821-2022-6-8-470-479. EDN: UNBZWA. 3. Драпкина О.М., Мазуров В.И., Мартынов А.И. с соавт. «В фокусе гиперурикемия». Резолюция совета экспертов. Кардиоваскулярная терапия и профилактика. 2023; 22(4): 77–84. (Drapkina O.M., Mazurov V.I., Martynov A.I. et al. “Focus on hyperuricemia”. The resolution of the expert council. Kardiovaskulyarnaya terapiya i profilaktika = Cardiovascular Therapy and Prevention. 2023; 22(4): 77–84 (In Russ.)). https://doi.org/10.15829/1728-8800-2023-3564. EDN: KRCKAU. 4. Драпкина О.М., Мазуров В.И., Мартынов А.И. с соавт. Консенсус для врачей по ведению пациентов с бессимптомной гиперурикемией в общетерапевтической практике. Кардиоваскулярная терапия и профилактика. 2024; 23(1): 89–104. (Drapkina O.M., Mazurov V.I., Martynov A.I. et al. Consensus statement on the management of patients with asymptomatic hyperuricemia in general medical practice. Kardiovaskulyarnaya terapiya i profilaktika = Cardiovascular Therapy and Prevention. 2024; 23(1): 89–104 (In Russ.)). https://doi.org/10.15829/1728-8800-2024-3737. EDN: WXKMIG. 5. Cai M., Liu W., Wu Y. et al. The serum uric acid is longitudinally related to patients global assessment of disease activity in male patients with axial spondyloarthritis. BMC Musculoskelet Disord. 2022; 23(1): 717. https://doi.org/10.1186/s12891-022-05657-3. PMID: 35897055. PMCID: PMC9327298. 6. Widawski L., Fabacher T., Spielmann L. et al. Psoriatic arthritis with hyperuricemia: More peripheral, destructive, and challenging to treat. Clin Rheumatol. 2022; 41(5): 1421–29. https://doi.org/10.1007/s10067-022-06061-x. PMID: 35059880. PMCID: PMC9056476. 7. Мазуров В.И., Драпкина О.М., Мартынов А.И. с соавт. Метаанализ наблюдательных когортных исследований о взаимосвязях бессимптомной гиперурикемии с хронической болезнью почек. Терапия. 2023; 9(10): 21–39. (Mazurov V.I., Drapkina O.M., Martynov A.I. et al. Meta-analysis of observational cohort studies on the relationships between asymptomatic hyperuricemia and chronic kidney disease. Terapiya = Therapy. 2023; 9(10): 21–39 (In Russ.)). https://doi.org/10.18565/therapy.2023.10.21-39. EDN: MWVPUQ. 8. Шальнова С.А., Деев А.Д., Артамонова Г.В. с соавт. Гиперурикемия и ее корреляты в российской популяции (результаты эпидемиологического исследования ЭССЕ-РФ). Рациональная фармакотерапия в кардиологии. 2014; 10(2): 153–159. (Shalnova S.A., Deev A.D., Artamonova G.V. et al. Hyperuricemia and its correlates in the Russian population (results of ESSE- RF epidemiological study). Ratsional’naya farmakoterapiya v kardiologii = Rational Pharmacotherapy in Cardiology. 2014; 10(2): 153–159 (In Russ.)). https://doi.org/10.20996/1819- 6446-2014-10-2-153-159. EDN: SCOUHN. 9. Reategui-Sokolova C., Ugarte-Gil M.F., Gamboa-Cárdenas R.V. et al. Serum uric acid levels contribute to new renal damage in systemic lupus erythematosus patients. Clin Rheumatol. 2017; 36(4): 845–52. https://doi.org/10.1007/s10067-017-3538-4. PMID: 28101832. 10. Han Y., Lu X., Xiao S. et al. Association between serum uric acid level and systemic lupus erythematosus kidney outcome: An observational study in Southern Chinese population and a meta-analysis. Lupus. 2023; 32(1): 83–93. https://doi.org/10.1177/09612033221140267. PMID: 36396610. 11. Bertoli A.M., Vilá L.M., Apte M. et al.; LUMINA Study Group. Systemic lupus erythematosus in a multiethnic US cohort LUMINA LI: Anaemia as a predictor of disease activity and damage accrual. Rheumatology (Oxford). 2007; 46(9): 1471–76. https://doi.org/10.1093/rheumatology/kem153. PMID: 17650522. 12. Aghdashi M., Behnemoon M., Mahmoodi Rad J., Rabiepour M. Evaluation of serum uric acid level in systemic lupus erythematosus patients with normal and high pulmonary arterial hypertension. Biomedicine (Taipei). 2018; 8(3): 16. https://doi.org/10.1051/bmdcn/2018080316. PMID: 30141403. PMCID: PMC6108231. 13. Duarte-Garcia A., Hocaoglu M., Valenzuela-Almada M. et al. Rising incidence and prevalence of systemic lupus erythematosus: A population-based study over four decades. Ann Rheum Dis. 2022; 81(9): 1260–66. https://doi.org/10.1136/annrheumdis-2022-222276. PMID: 35577385. PMCID: PMC10481386. 14. Lerkvaleekul B., Chobchai P., Rattanasiri S., Vilaiyuk S. Evaluating performance of the 2019 EULAR/ACR, 2012 SLICC, and 1997 ACR criteria for classifying adult-onset and childhood-onset systemic lupus erythematosus: A systematic review and meta-analysis. Front Med (Lausanne). 2022; 9: 1093213. https://doi.org/10.3389/fmed.2022.1093213. PMID: 36619627. PMCID: PMC9813386. 15. Sanchez A.R.P., van Vollenhoven R.F., Morand E.F. et al. Targeting DORIS remission and LLDAS in SLE: A review. Rheumatol Ther. 2023; 10(6): 1459–77. https://doi.org/10.1007/s40744-023-00601-w. PMID: 37798595. PMCID: PMC10654283. 16. Алиев Д.Б., Гайдукова Е.К., Гайдукова И.З., Мазуров В.И., Инамова О.В., Маслянский А.Л., Костик М.М., Чудинов А.Л., Мусийчук М.М. Оценка риска развития стероидорезистентности у пациентов с системной красной волчанкой. Свидетельство о регистрации программы для ЭВМ RU 2024662581, 29.05.2024. Заявка от 23.05.2024. (Aliev D.B., Gaydukova E.K., Gaydukova I.Z., Mazurov V.I., Inamova O.V., Maslyansky A.L., Kostik M.M., Chudinov A.L., Musiychuk M.M. Risk assessment of steroid resistance in patients with systemic lupus erythematosus. Certificate of registration of the computer program RU 2024662581, 05/29/2024. Application dated 05/23/2024 (In Russ.)). 17. Ruiz-Irastorza G., Danza A., Khamashta M. Glucocorticoid use and abuse in SLE. Rheumatology (Oxford). 2012; 51(7): 1145–53. https://doi.org/10.1093/rheumatology/ker410. PMID: 22271756. 18. Deyo R.A., Cherkin D.C., Ciol M.A. Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol. 1992; 45(6): 613–19. https://doi.org/10.1016/0895-4356(92)90133-8. PMID: 1607900. 19. Hippisley-Cox J., Coupland C., Brindle P. Development and validation of QRISK3 risk prediction algorithms to estimate future risk of cardiovascular disease: Prospective cohort study. BMJ. 2017: 357: j2099. https://doi.org/10.1136/bmj.j2099. PMID: 28536104. PMCID: PMC5441081. 20. Song Y., Tang L., Han J. et al. Uric acid provides protective role in red blood cells by antioxidant defense: A hypothetical analysis. Oxid Med Cell Longev. 2019; 2019: 3435174. https://doi.org/10.1155/2019/3435174. PMID: 31049132. PMCID: PMC6458867. 21. Li L., Yang C., Zhao Y. et al. Is hyperuricemia an independent risk factor for new-onset chronic kidney disease? A systematic review and meta-analysis based on observational cohort studies. BMC Nephrol. 2014; 15: 122. https://doi.org/10.1186/1471-2369-15-122. PMID: 25064611. PMCID: PMC4132278. 22. Akasaka H., Yoshida H., Takizawa H. et al.; BOREAS-CKD1 Investigators. The impact of elevation of serum uric acid level on the natural history of glomerular filtration rate (GFR) and its sex difference. Nephrol Dial Transplant. 2014; 29(10): 1932–39. https://doi.org/10.1093/ndt/gfu197. PMID: 24891435. 23. Park D.-J., Choi S.-E., Xu H. et al. Uric acid as a risk factor for progression to chronic kidney disease in patients with lupus nephritis: Results from the KORNET registry. Clin Exp Rheumatol. 2021; 39(5): 947–54. https://doi.org/10.55563/clinexprheumatol/k4rdi7. PMID: 33124574. 24. Sharma G., Dubey A., Nolkha N., Singh J.A. Hyperuricemia, urate-lowering therapy, and kidney outcomes: A systematic review and meta-analysis. Ther Adv Musculoskelet Dis. 2021; 13: 1759720X211016661. https://doi.org/10.1177/1759720X211016661. PMID: 34104231. PMCID: PMC8161880. 25. Pisano A., Cernaro V., Gembillo G. et al. Xanthine oxidase inhibitors for improving renal function in chronic kidney disease patients: An updated systematic review and meta-analysis. Int J Mol Sci. 2017; 18(11): 2283. https://doi.org/10.3390/ijms18112283. PMID: 29088122. PMCID: PMC5713253. 26. Yang Z., Liang Y., Li C. et al. Associations of serum urea, creatinine and uric acid with clinical and laboratory features in patients with systemic lupus erythematosus. Rheumatol Int. 2012; 32(9): 2715–23. https://doi.org/10.1007/s00296-011-1987-7. PMID: 21800118. 27. Nie P., Hu L., Li B. et al. Relationship between hyperuricemia and serositis in patients with lupus nephritis. Int Urol Nephrol. 2022; 54(2): 357–64. https://doi.org/10.1007/s11255-021-02873-z. PMID: 33970417. 28. Krzemien P., Kasperczyk S., Banach M. et al. Serum antinuclear autoantibodies are associated with measures of oxidative stress and lifestyle factors: Analysis of LIPIDOGRAM2015 and LIPIDOGEN2015 studies. Arch Med Sci. 2021; 19(5): 1214–27. https://doi.org/10.5114/aoms/139313. PMID: 37732061. PMCID: PMC10507751. 29. Baier E., Kluge I.A., Hakroush S. et al. Serum uric acid associates with systemic complement C3 activation in severe ANCA-associated renal vasculitides. Int J Mol Sci. 2024; 25(2): 713. https://doi.org/10.3390/ijms25020713. PMID: 38255787. PMCID: PMC10815696. 30. Шальнова С.А., Имаева А.Э., Куценко В.А. с соавт. Гиперурикемия и артериальная гипертония у лиц трудоспособного возраста: результаты популяционного исследования. Кардиоваскулярная терапия и профилактика. 2023; 22(S9): 93–102. (Shalnova S.A., Imaeva A.E., Kutsenko V.A. et al. Hyperuricemia and hypertension in working-age people: Results of a population study. Kardiovaskulyarnaya terapiya i profilaktika = Cardiovascular Therapy and Prevention. 2023; 22(S9): 93–102 (In Russ.)). https://doi.org/10.15829/1728-8800-2023-3783. EDN: TAHKSZ. 31. Schoenfeld S.R., Kasturi S., Costenbader K.H. The epidemiology of atherosclerotic cardiovascular disease among patients with SLE: A systematic review. Semin Arthritis Rheum. 2013; 43(1): 77–95. https://doi.org/10.1016/j.semarthrit.2012.12.002. PMID: 23422269. 32. Xu J., Wang B., Li Q. et al. Risk of thyroid disorders in patients with gout and hyperuricemia. Horm Metab Res. 2019; 51(8): 522–30. https://doi.org/10.1055/a-0923-9184. PMID: 31408898. 33. Bos M.J., Koudstaal P.J., Hofman A. et al. Uric acid is a risk factor for myocardial infarction and stroke: The Rotterdam study. Stroke. 2006; 37(6): 1503–7. https://doi.org/10.1161/01.STR.0000221716.55088.d4. PMID: 16675740. 34. Sheikh M., Movassaghi S., Khaledi M., Moghaddassi M. Hyperuricemia in systemic lupus erythematosus: Is it associated with the neuropsychiatric manifestations of the disease? Rev Bras Reumatol Engl Ed. 2016; 56(6): 471–77. https://doi.org/10.1016/j.rbre.2015.07.011. PMID: 27914592.
About the Autors
Maria M. Musiychuk, MD, rheumatologist at V.A. Nasonova Clinical Rheumatology Hospital No. 25. Address: 190068, Saint Petersburg, 30 Bol`shaya Pod`yacheskaya St.
ORCID: https://orcid.org/0009-0001-7694-4740. Scopus Author ID: 59392803600. eLibrary SPIN: 8773-2851
Inna Z. Gaydukova, MD, Dr. Sci. (Medicine), deputy director of the Research Institute of Rheumatology, professor of the Department of therapy, rheumatology, examination of temporary disability and quality of medical care with a course in hematology and transfusiology named after E.E. Eichwald of I.I. Mechnikov North-West State Medical University of the Ministry of Healthcare of Russia, rheumatologist at V.A. Nasonova Clinical Rheumatology Hospital No. 25. Address: 191015, Saint Petersburg, 41 Kirochnaya St.
E-mail: ubp1976@list.ru
ORCID: https://orcid.org/0000-0003-3500-7256. Scopus Author ID: 55237525900. eLibrary SPIN: 3083-7996
Vadim I. Mazurov, MD, Dr. Sci. (Medicine), professor, academician of RAS, vice president of RSMSIM, principal scientific advisor and director of the Research Institute of Rheumatology, head of the Department of therapy, rheumatology, examination of temporary disability and quality of medical care with a course in hematology and transfusiology named after E.E. Eichwald of I.I. Mechnikov North-West State Medical University of the Ministry of Healthcare of Russia, head of Autoimmune center of V.A. Nasonova Clinical Rheumatology Hospital No. 25, chief freelance specialist – rheumatologist of the Healthcare Committee of the Government of Saint Petersburg, Honored Worker of Science of the Russian Federation. Address: 191015, Saint Petersburg, 41 Kirochnaya St.
E-mail: maz.nwgmu@yandex.ru
ORCID: https://orcid.org/0000-0002-0797-2051. Scopus Author ID: 16936315400. eLibrary SPIN: 6823-5482
Oksana V. Inamova, MD, PhD (Medicine), deputy director of the Research Institute of Rheumatology, assistant at the Department of therapy, rheumatology, examination of temporary disability and quality of medical care with a course in hematology and transfusiology named after E.E. Eichwald of I.I. Mechnikov North-West State Medical University of the Ministry of Healthcare of Russia, chief physician of V.A. Nasonova Clinical Rheumatology Hospital No. 25. Address: 191015, Saint Petersburg, 41 Kirochnaya St.
E-mail: ovig74@mail.ru
ORCID: https://orcid.org/0000-0001-9126-3639. eLibrary SPIN: 8841-5496
Damir B. Aliev, MD, rheumatologist at V.A. Nasonova Clinical Rheumatology Hospital No. 25. Address: 190068, Saint Petersburg, 30 Bol`shaya Pod`yacheskaya St.
ORCID: https://orcid.org/0000-0001-8367-4622. Scopus Author ID: 57873750600. eLibrary SPIN: 6068-4966
Sergey V. Lapin, MD, PhD (Medicine), head of the Department for diagnostics of autoimmune diseases of Scientific and Methodological Center for Molecular Medicine, Academician I.P. Pavlov First Saint Petersburg State Medical University of the Ministry of Healthcare of Russia. Address: 197022, St. Petersburg, 6-8/ of.28 L. Tolstogo St.
ORCID: https://orcid.org/0000-0002-4998-3699. Scopus Author ID: 7006205727. eLibrary SPIN: 9852-7501
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