{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,28]],"date-time":"2026-10-28T02:58:07Z","timestamp":1793156287173,"version":"4.5.0"},"reference-count":47,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2024,12,2]],"date-time":"2024-12-02T00:00:00Z","timestamp":1733097600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Science Center in Poland","award":["2017\/25\/N\/NZ5\/02595"],"award-info":[{"award-number":["2017\/25\/N\/NZ5\/02595"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Medicina"],"abstract":"<jats:p>Background\/Objectives: Systemic lupus erythematosus (SLE) is an autoimmune disease characterized by the abnormal activation of autoreactive T and B cells, autoantibody production, complement activation, and immune-complex deposition, resulting in tissue damage. However, data on immunologic disturbances in SLE, particularly regarding flares, are scarce. Methods: We investigated 35 patients with SLE: 12 (34.3%) with disease exacerbation (SLE disease activity index [SLEDAI] \u2265 5 points) and 23 (65.7%) in remission (SLEDAI &lt; 5 points). All patients met the 2019 EULAR\/ACR SLE criteria. Flow cytometry was used to identify B cell subsets, including memory B cells. Results: In the whole patient group, SLEDAI was positively related to the percentage of transitional\/regulatory B cells (r = 0.38, p = 0.034). Some lymphocyte subsets correlated with complement levels, e.g., the percentage of na\u00efve and memory B cells showed associations with C3c complement (r = 0.43, p = 0.018 and r = \u22120.45, p = 0.016, respectively). Furthermore, regarding inflammatory markers, we found associations between C-reactive protein and the percentage of plasmablasts (r = 0.40, p = 0.026) and plasmocytes (r = 0.44, p = 0.017). Finally, the percentage of plasmablasts correlated with SLE duration (r = 0.42, p = 0.016). In the follow-up analysis, during a median observation of 5 years, 5 out of the initially 23 inactive SLE patients developed a disease flare. They were characterized by longer disease duration stated in the beginning compared to patients who remained in remission (p = 0.019). Conclusions: Our study highlights significant associations between various B cell subsets and SLE disease activity. A more personalized approach to indicate patients with SLE at a higher risk of lupus flares is crucial for better management.<\/jats:p>","DOI":"10.3390\/medicina60121994","type":"journal-article","created":{"date-parts":[[2024,12,2]],"date-time":"2024-12-02T13:34:04Z","timestamp":1733146444000},"page":"1994","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Circulating B Lymphocyte Subsets in Patients with Systemic Lupus Erythematosus"],"prefix":"10.3390","volume":"60","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1013-2253","authenticated-orcid":false,"given":"Joanna","family":"Kosa\u0142ka-W\u0119giel","sequence":"first","affiliation":[{"name":"Jagiellonian University Medical College, Department of Rheumatology and Immunology, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"},{"name":"University Hospital, Department of Rheumatology, Immunology and Internal Medicine, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0444-981X","authenticated-orcid":false,"given":"Bogdan","family":"Jakie\u0142a","sequence":"additional","affiliation":[{"name":"Jagiellonian University Medical College, Department of Internal Medicine, Faculty of Medicine, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0321-3557","authenticated-orcid":false,"given":"Rados\u0142aw","family":"Dziedzic","sequence":"additional","affiliation":[{"name":"Jagiellonian University Medical College, Doctoral School of Medical and Health Sciences, \u015aw. \u0141azarza 16, 31-530 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mamert","family":"Milewski","sequence":"additional","affiliation":[{"name":"University Hospital, Department of Rheumatology, Immunology and Internal Medicine, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2258-0248","authenticated-orcid":false,"given":"And\u017celika","family":"Siwiec-Ko\u017alik","sequence":"additional","affiliation":[{"name":"University Hospital, Department of Rheumatology, Immunology and Internal Medicine, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2221-614X","authenticated-orcid":false,"given":"Lech","family":"Zar\u0119ba","sequence":"additional","affiliation":[{"name":"University of Rzesz\u00f3w, College of Natural Sciences, Institute of Computer Science, Pigonia 1, 35-310 Rzesz\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9634-0963","authenticated-orcid":false,"given":"Stanis\u0142awa","family":"Bazan-Socha","sequence":"additional","affiliation":[{"name":"University Hospital, Department of Rheumatology, Immunology and Internal Medicine, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"},{"name":"Jagiellonian University Medical College, Department of Internal Medicine, Faculty of Medicine, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7635-8103","authenticated-orcid":false,"given":"Marek","family":"Sanak","sequence":"additional","affiliation":[{"name":"Jagiellonian University Medical College, Department of Internal Medicine, Faculty of Medicine, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacek","family":"Musia\u0142","sequence":"additional","affiliation":[{"name":"Jagiellonian University Medical College, Department of Internal Medicine, Faculty of Medicine, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariusz","family":"Korkosz","sequence":"additional","affiliation":[{"name":"Jagiellonian University Medical College, Department of Rheumatology and Immunology, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"},{"name":"University Hospital, Department of Rheumatology, Immunology and Internal Medicine, Jakubowskiego 2, 30-688 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,12,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2326","DOI":"10.1016\/S0140-6736(24)00398-2","article-title":"Systemic Lupus Erythematosus","volume":"403","author":"Hoi","year":"2024","journal-title":"Lancet"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1878","DOI":"10.1016\/S0140-6736(14)60128-8","article-title":"Systemic Lupus Erythematosus","volume":"384","author":"Lisnevskaia","year":"2014","journal-title":"Lancet"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"101938","DOI":"10.1016\/j.berh.2024.101938","article-title":"Clinical Patterns of Disease: From Early Systemic Lupus Erythematosus to Late-Onset Disease","volume":"37","author":"Piga","year":"2024","journal-title":"Best Pract. Res. Clin. Rheumatol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"110224","DOI":"10.1016\/j.clim.2024.110224","article-title":"Potential Therapies Targeting Metabolic Pathways in Systemic Lupus Erythematosus","volume":"263","author":"Hisada","year":"2024","journal-title":"Clin. Immunol."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Dema, B., and Charles, N. (2016). Autoantibodies in SLE: Specificities, Isotypes and Receptors. Antibodies, 5.","DOI":"10.3390\/antib5010002"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Accapezzato, D., Caccavale, R., Paroli, M.P., Gioia, C., Nguyen, B.L., Spadea, L., and Paroli, M. (2023). Advances in the Pathogenesis and Treatment of Systemic Lupus Erythematosus. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24076578"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1016\/S0140-6736(07)60279-7","article-title":"Systemic Lupus Erythematosus","volume":"369","author":"Khamashta","year":"2007","journal-title":"Lancet"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Yu, H., Nagafuchi, Y., and Fujio, K. (2021). Clinical and Immunological Biomarkers for Systemic Lupus Erythematosus. Biomolecules, 11.","DOI":"10.3390\/biom11070928"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"101895","DOI":"10.1016\/j.berh.2023.101895","article-title":"Management of Systemic Lupus Erythematosus: A New Scenario","volume":"37","author":"Moysidou","year":"2023","journal-title":"Best Pract. Res. Clin. Rheumatol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e073980","DOI":"10.1136\/bmj-2022-073980","article-title":"Advances in the Management of Systemic Lupus Erythematosus","volume":"383","author":"Morand","year":"2023","journal-title":"BMJ"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"ii85","DOI":"10.1136\/annrheumdis-2012-202341","article-title":"Regulatory Cell Subsets in the Control of Autoantibody Production Related to Systemic Autoimmunity","volume":"72","author":"Fujio","year":"2013","journal-title":"Ann. Rheum. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1038\/nri3795","article-title":"The Generation of Antibody-Secreting Plasma Cells","volume":"15","author":"Nutt","year":"2015","journal-title":"Nat. Rev. Immunol."},{"key":"ref_13","first-page":"32","article-title":"Changes of Memory B- and T-Cell Subsets in Lupus Nephritis Patients","volume":"54","author":"Kosalka","year":"2016","journal-title":"Folia Histochem. Cytobiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1146\/annurev-immunol-020711-075043","article-title":"Induced CD4+Foxp3+ Regulatory T Cells in Immune Tolerance","volume":"30","author":"Bilate","year":"2012","journal-title":"Annu. Rev. Immunol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1093\/intimm\/dxv033","article-title":"IL-10-Independent Regulatory B-Cell Subsets and Mechanisms of Action","volume":"27","author":"Ray","year":"2015","journal-title":"Int. Immunol."},{"key":"ref_16","first-page":"383","article-title":"Systemic Lupus Erythematosus: Diagnosis and Treatment","volume":"107","author":"Lam","year":"2023","journal-title":"Am. Fam. Physician"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"S14","DOI":"10.1016\/j.semarthrit.2019.09.009","article-title":"EULAR\/ACR Classification Criteria for SLE","volume":"49","author":"Aringer","year":"2019","journal-title":"Semin. Arthritis Rheum."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"218","DOI":"10.5603\/FHC.2014.0025","article-title":"Renal Interstitial Mast Cell Counts Differ across Classes of Proliferative Lupus Nephritis","volume":"52","author":"Kaczmarczyk","year":"2014","journal-title":"Folia Histochem. Cytobiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.advms.2021.01.004","article-title":"Retrospective Analysis of Clinical and Pathomorphological Features of Lupus Nephritis in Children","volume":"66","author":"Barabasz","year":"2021","journal-title":"Adv. Med. Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1259","DOI":"10.1177\/0961203318770006","article-title":"Urinary Cytokines and mRNA Expression as Biomarkers of Disease Activity in Lupus Nephritis","volume":"27","author":"Jakiela","year":"2018","journal-title":"Lupus"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e000631","DOI":"10.1136\/lupus-2021-000631","article-title":"Clinical Measurement of Lupus Nephritis Activity Is Inferior to Biomarker-Based Activity Assessment Using the Renal Activity Index for Lupus Nephritis in Childhood-Onset Systemic Lupus Erythematosus","volume":"9","author":"Aljaberi","year":"2022","journal-title":"Lupus Sci. Med."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.2215\/CJN.12791019","article-title":"Kidney Disease, Race, and GFR Estimation","volume":"15","author":"Levey","year":"2020","journal-title":"CJASN"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"\u017babi\u0144ska, M., Ko\u015bcielska-Kasprzak, K., Krajewska, J., Bartoszek, D., Augustyniak-Bartosik, H., and Krajewska, M. (2021). Immune Cells Profiling in ANCA-Associated Vasculitis Patients\u2014Relation to Disease Activity. Cells, 10.","DOI":"10.3390\/cells10071773"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e17341","DOI":"10.15252\/emmm.202217341","article-title":"Functions of Double-negative B Cells in Autoimmune Diseases, Infections, and Cancers","volume":"15","author":"Chung","year":"2023","journal-title":"EMBO Mol. Med."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Lebel, E., Nachmias, B., Pick, M., Gross Even-Zohar, N., and Gatt, M.E. (2022). Understanding the Bioactivity and Prognostic Implication of Commonly Used Surface Antigens in Multiple Myeloma. J. Clin. Med., 11.","DOI":"10.3390\/jcm11071809"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Agarbati, S., Benfaremo, D., Viola, N., Paolini, C., Svegliati Baroni, S., Funaro, A., Moroncini, G., Malavasi, F., and Gabrielli, A. (2022). Increased Expression of the Ectoenzyme CD38 in Peripheral Blood Plasmablasts and Plasma Cells of Patients with Systemic Sclerosis. Front. Immunol., 13.","DOI":"10.3389\/fimmu.2022.1072462"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1480","DOI":"10.1001\/jama.2024.2315","article-title":"Systemic Lupus Erythematosus: A Review","volume":"331","author":"Siegel","year":"2024","journal-title":"JAMA"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4","DOI":"10.31138\/mjr.28.1.4","article-title":"Flares in Systemic Lupus Erythematosus: Diagnosis, Risk Factors and Preventive Strategies","volume":"28","author":"Adamichou","year":"2017","journal-title":"Mediterr. J. Rheumatol."},{"key":"ref_29","first-page":"i3","article-title":"Systemic Lupus Erythematosus Diagnosis and Management","volume":"56","author":"Thong","year":"2016","journal-title":"Rheumatology"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"R108","DOI":"10.1186\/ar3042","article-title":"Decreased Frequency and Activated Phenotype of Blood CD27 IgD IgM B Lymphocytes Is a Permanent Abnormality in Systemic Lupus Erythematosus Patients","volume":"12","author":"Brieva","year":"2010","journal-title":"Arthritis Res. Ther."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"101896","DOI":"10.1016\/j.berh.2023.101896","article-title":"Assessment of Disease Activity and Damage in SLE: Are We There Yet?","volume":"37","author":"Cruciani","year":"2023","journal-title":"Best Pract. Res. Clin. Rheumatol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1601","DOI":"10.1136\/annrheumdis-2014-205287","article-title":"The Complement System in Systemic Lupus Erythematosus: An Update","volume":"73","author":"Leffler","year":"2014","journal-title":"Ann. Rheum. Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1007\/s11926-021-00984-1","article-title":"A Review of Complement Activation in SLE","volume":"23","author":"Weinstein","year":"2021","journal-title":"Curr. Rheumatol. Rep."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.imlet.2021.06.006","article-title":"New Aspects in the Regulation of Human B Cell Functions by Complement Receptors CR1, CR2, CR3 and CR4","volume":"237","author":"Erdei","year":"2021","journal-title":"Immunol. Lett."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Parodis, I., Gatto, M., and Sj\u00f6wall, C. (2022). B Cells in Systemic Lupus Erythematosus: Targets of New Therapies and Surveillance Tools. Front. Med., 9.","DOI":"10.3389\/fmed.2022.952304"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2029","DOI":"10.1177\/09612033211051637","article-title":"Erosive Arthritis in Systemic Lupus Erythematosus: Not Only Rhupus","volume":"30","author":"Ceccarelli","year":"2021","journal-title":"Lupus"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Enocsson, H., Karlsson, J., Li, H.-Y., Wu, Y., Kushner, I., Wetter\u00f6, J., and Sj\u00f6wall, C. (2021). The Complex Role of C-Reactive Protein in Systemic Lupus Erythematosus. J. Clin. Med., 10.","DOI":"10.3390\/jcm10245837"},{"key":"ref_38","first-page":"1489","article-title":"Management of Systemic Lupus Erythematosus: A Systematic Literature Review Informing the 2023 Update of the EULAR Recommendations","volume":"83","author":"Kostopoulou","year":"2024","journal-title":"Ann. Rheum. Dis."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Alduraibi, F.K., and Tsokos, G.C. (2024). Lupus Nephritis Biomarkers: A Critical Review. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25020805"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Kitagori, K., Yoshifuji, H., Oku, T., Sasaki, C., Miyata, H., Mori, K.P., Nakajima, T., Ohmura, K., Kawabata, D., and Yukawa, N. (2016). Cleaved Form of Osteopontin in Urine as a Clinical Marker of Lupus Nephritis. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0167141"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Omer, M.H., Shafqat, A., Ahmad, O., Nadri, J., AlKattan, K., and Yaqinuddin, A. (2024). Urinary Biomarkers for Lupus Nephritis: A Systems Biology Approach. J. Clin. Med., 13.","DOI":"10.3390\/jcm13082339"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Alenzi, F., Ateka-Barrutia, O., Ken Cheah, C., Khamashta, M., Sangle, S.R., and D\u2019Cruz, D.P. (2024). Lupus Nephritis Outcomes after Stopping Immunosuppression. J. Clin. Med., 13.","DOI":"10.3390\/jcm13082211"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s10157-015-1179-y","article-title":"Lupus Nephritis: An Update","volume":"20","author":"Imran","year":"2016","journal-title":"Clin. Exp. Nephrol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Szab\u00f3, E., Farag\u00f3, A., Bodor, G., G\u00e9mes, N., Pusk\u00e1s, L.G., Kov\u00e1cs, L., and Szebeni, G.J. (2024). Identification of Immune Subsets with Distinct Lectin Binding Signatures Using Multi-Parameter Flow Cytometry: Correlations with Disease Activity in Systemic Lupus Erythematosus. Front. Immunol., 15.","DOI":"10.3389\/fimmu.2024.1380481"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1186\/s42358-022-00279-8","article-title":"CD19+CD24highCD27+ B Cell and Interleukin 35 as Potential Biomarkers of Disease Activity in Systemic Lupus Erythematosus Patients","volume":"62","author":"Xiong","year":"2022","journal-title":"Adv. Rheumatol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"8450947","DOI":"10.1155\/2019\/8450947","article-title":"Dysregulated T Cell Activation and Aberrant Cytokine Expression Profile in Systemic Lupus Erythematosus","volume":"2019","author":"Zhou","year":"2019","journal-title":"Mediat. Inflamm."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1002\/art.41955","article-title":"Association of Increased Serum Lipopolysaccharide, But Not Microbial Dysbiosis, With Obesity-Related Osteoarthritis","volume":"74","author":"Loeser","year":"2022","journal-title":"Arthritis Rheumatol."}],"container-title":["Medicina"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1648-9144\/60\/12\/1994\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:45:14Z","timestamp":1760114714000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1648-9144\/60\/12\/1994"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,2]]},"references-count":47,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["medicina60121994"],"URL":"https:\/\/doi.org\/10.3390\/medicina60121994","relation":{},"ISSN":["1648-9144"],"issn-type":[{"value":"1648-9144","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,2]]}}}