B-Cell Targeted Therapies in Pediatric Rheumatology
Gülşah KAVRUL KAYAALPa , Nuray AKTAY AYAZa
aİstanbul University İstanbul Faculty of Medicine, Department of Pediatric Rheumatology, İstanbul, Türkiye
ABSTRACT
B cells play a pivotal role in autoimmune rheumatic diseases by virtue of their contributions to antibody production, antigen presentation, and cytokine release. Consequently, therapeutic approaches targeting B cells have emerged as a promising strategy for managing autoimmune rheumatic diseases. In this article, we discuss the significance of B cells in pediatric rheumatic diseases and explore the B cell-targeted treatments employed in these conditions.
Keywords: Pediatric rheumatology; B-cell; belimumab; rituximab
Referanslar
- Rubin SJS, Bloom MS, Robinson WH. B cell checkpoints in autoimmune rheumatic diseases. Nat Rev Rheumatol. 2019;15(5):303-15. [Crossref] [PubMed]
- Townsend MJ, Monroe JG, Chan AC. B-cell targeted therapies in human autoimmune diseases: an updated perspective. Immunol Rev. 2010;237(1):264-83. [Crossref] [PubMed]
- Yuseff MI, Pierobon P, Reversat A, Lennon-Dumenil AM. How B cells capture, process and present antigens: a crucial role for cell polarity. Nat Rev Immunol. 2013;13(7):475-86. [Crossref] [PubMed]
- Cyster JG, Allen CDC. B Cell Responses: Cell Interaction Dynamics and Decisions. Cell. 2019;177(3):524-40. [Crossref] [PubMed] [PMC]
- Gaffney PM, Ortmann WA, Selby SA, Shark KB, Ockenden TC, Rohlf KE, et al. Genome screening in human systemic lupus erythematosus: results from a second Minnesota cohort and combined analyses of 187 sib-pair families. Am J Hum Genet. 2000;66(2):547-56. [Crossref] [PubMed] [PMC]
- Lee DSW, Rojas OL, Gommerman JL. B cell depletion therapies in autoimmune disease: advances and mechanistic insights. Nat Rev Drug Discov. 2021;20(3):179-99. [Crossref] [PubMed] [PMC]
- Lu DR, McDavid AN, Kongpachith S, Lingampalli N, Glanville J, Ju CH, et al. T Cell-Dependent Affinity Maturation and Innate Immune Pathways Differentially Drive Autoreactive B Cell Responses in Rheumatoid Arthritis. Arthritis Rheumatol. 2018;70(11):1732-44. [Crossref] [PubMed] [PMC]
- Harris DP, Haynes L, Sayles PC, Duso DK, Eaton SM, Lepak NM, et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat Immunol. 2000;1(6):475-82. [Crossref] [PubMed]
- Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, Tedder TF. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity. 2008;28(5):639-50. [Crossref] [PubMed] [PMC]
- Yap DYH, Chan TM. B Cell Abnormalities in Systemic Lupus Erythematosus and Lupus Nephritis-Role in Pathogenesis and Effect of Immunosuppressive Treatments. Int J Mol Sci. 2019;20(24). [Crossref] [PubMed] [PMC]
- Meffre E, O'Connor KC. Impaired B-cell tolerance checkpoints promote the development of autoimmune diseases and pathogenic autoantibodies. Immunol Rev. 2019;292(1):90-101. [Crossref] [PubMed] [PMC]
- Moura RA, Fonseca JE. B Cells on the Stage of Inflammation in Juvenile Idiopathic Arthritis: Leading or Supporting Actors in Disease Pathogenesis? Front Med (Lausanne). 2022;9:851532. [Crossref] [PubMed] [PMC]
- Storwick JA, Brett AC, Buhler K, Chin A, Schmeling H, Johnson NA, et al. Prevalence and titres of antinuclear antibodies in juvenile idiopathic arthritis: A systematic review and meta-analysis. Autoimmun Rev. 2022;21(6):103086. [Crossref] [PubMed]
- Guillaume S, Prieur AM, Coste J, Job-Deslandre C. Long-term outcome and prognosis in oligoarticular-onset juvenile idiopathic arthritis. Arthritis Rheum. 2000;43(8):1858-65. [Crossref] [PubMed]
- Gregorio A, Gambini C, Gerloni V, Parafioriti A, Sormani MP, Gregorio S, et al. Lymphoid neogenesis in juvenile idiopathic arthritis correlates with ANA positivity and plasma cells infiltration. Rheumatology (Oxford). 2007;46(2):308-13. [Crossref] [PubMed]
- Tappeiner C, Klotsche J, Sengler C, Niewerth M, Liedmann I, Walscheid K, et al. Risk Factors and Biomarkers for the Occurrence of Uveitis in Juvenile Idiopathic Arthritis: Data From the Inception Cohort of Newly Diagnosed Patients With Juvenile Idiopathic Arthritis Study. Arthritis Rheumatol. 2018;70(10):1685-94. [Crossref] [PubMed] [PMC]
- Angeles-Han ST, McCracken C, Yeh S, Jenkins K, Stryker D, Rouster-Stevens K, et al. Characteristics of a cohort of children with Juvenile Idiopathic Arthritis and JIA-associated Uveitis. Pediatr Rheumatol Online J. 2015;13:19. [Crossref] [PubMed] [PMC]
- Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature. 2002;416(6881):603-7. [Crossref] [PubMed]
- van Delft MAM, Huizinga TWJ. An overview of autoantibodies in rheumatoid arthritis. J Autoimmun. 2020;110:102392. [Crossref] [PubMed]
- Moore TL. Immune Complexes in Juvenile Idiopathic Arthritis. Front Immunol. 2016;7:177. [Crossref] [PubMed] [PMC]
- Mahmud SA, Binstadt BA. Autoantibodies in the Pathogenesis, Diagnosis, and Prognosis of Juvenile Idiopathic Arthritis. Front Immunol. 2018;9:3168. [Crossref] [PubMed] [PMC]
- Kruithof E, Van den Bossche V, De Rycke L, Vandooren B, Joos R, Canete JD, et al. Distinct synovial immunopathologic characteristics of juvenile-onset spondylarthritis and other forms of juvenile idiopathic arthritis. Arthritis Rheum. 2006;54(8):2594-604. [Crossref] [PubMed]
- Fischer J, Dirks J, Haase G, Holl-Wieden A, Hofmann C, Girschick H, et al. IL-21(+) CD4(+) T helper cells co-expressing IFN-gamma and TNF-alpha accumulate in the joints of antinuclear antibody positive patients with juvenile idiopathic arthritis. Clin Immunol. 2020;217:108484. [Crossref] [PubMed]
- Dirks J, Fischer J, Haase G, Holl-Wieden A, Hofmann C, Girschick H, et al. CD21(lo/-)CD27(-)IgM(-) Double-Negative B Cells Accumulate in the Joints of Patients With Antinuclear Antibody-Positive Juvenile Idiopathic Arthritis. Front Pediatr. 2021;9:635815. [Crossref] [PubMed] [PMC]
- Fischer J, Dirks J, Klaussner J, Haase G, Holl-Wieden A, Hofmann C, et al. Effect of Clonally Expanded PD-1(high) CXCR5-CD4+ Peripheral T Helper Cells on B Cell Differentiation in the Joints of Patients With Antinuclear Antibody-Positive Juvenile Idiopathic Arthritis. Arthritis Rheumatol. 2022;74(1):150-62. [Crossref] [PubMed]
- Corcione A, Ferlito F, Gattorno M, Gregorio A, Pistorio A, Gastaldi R, et al. Phenotypic and functional characterization of switch memory B cells from patients with oligoarticular juvenile idiopathic arthritis. Arthritis Res Ther. 2009;11(5):R150. [Crossref] [PubMed] [PMC]
- Morbach H, Wiegering V, Richl P, Schwarz T, Suffa N, Eichhorn EM, et al. Activated memory B cells may function as antigen-presenting cells in the joints of children with juvenile idiopathic arthritis. Arthritis Rheum. 2011;63(11):3458-66. [Crossref] [PubMed]
- Kalampokis I, Venturi GM, Poe JC, Dvergsten JA, Sleasman JW, Tedder TF. The Regulatory B Cell Compartment Expands Transiently During Childhood and Is Contracted in Children With Autoimmunity. Arthritis Rheumatol. 2017;69(1):225-38. [Crossref] [PubMed] [PMC]
- Zhao Q, Jung LK. Frequency of CD19(+)CD24(hi)CD38(hi) regulatory B cells is decreased in peripheral blood and synovial fluid of patients with juvenile idiopathic arthritis: a preliminary study. Pediatr Rheumatol Online J. 2018;16(1):44. [Crossref] [PubMed] [PMC]
- Flores-Borja F, Bosma A, Ng D, Reddy V, Ehrenstein MR, Isenberg DA, et al. CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci Transl Med. 2013;5(173):173ra23. [Crossref] [PubMed]
- Yeo L, Toellner KM, Salmon M, Filer A, Buckley CD, Raza K, et al. Cytokine mRNA profiling identifies B cells as a major source of RANKL in rheumatoid arthritis. Ann Rheum Dis. 2011;70(11):2022-8. [Crossref] [PubMed] [PMC]
- Ota Y, Niiro H, Ota S, Ueki N, Tsuzuki H, Nakayama T, et al. Generation mechanism of RANKL(+) effector memory B cells: relevance to the pathogenesis of rheumatoid arthritis. Arthritis Res Ther. 2016;18:67. [Crossref] [PubMed] [PMC]
- Feng Y, Yang M, Wu H, Lu Q. The pathological role of B cells in systemic lupus erythematosus: From basic research to clinical. Autoimmunity. 2020;53(2):56-64. [Crossref] [PubMed]
- Jacobi AM, Reiter K, Mackay M, Aranow C, Hiepe F, Radbruch A, et al. Activated memory B cell subsets correlate with disease activity in systemic lupus erythematosus: delineation by expression of CD27, IgD, and CD95. Arthritis Rheum. 2008;58(6):1762-73. [Crossref] [PubMed]
- Menon M, Blair PA, Isenberg DA, Mauri C. A Regulatory Feedback between Plasmacytoid Dendritic Cells and Regulatory B Cells Is Aberrant in Systemic Lupus Erythematosus. Immunity. 2016;44(3):683-97. [Crossref] [PubMed] [PMC]
- Barnas JL, Looney RJ, Anolik JH. B cell targeted therapies in autoimmune disease. Curr Opin Immunol. 2019;61:92-9. [Crossref] [PubMed] [PMC]
- Hui-Yuen JS, Nguyen SC, Askanase AD. Targeted B cell therapies in the treatment of adult and pediatric systemic lupus erythematosus. Lupus. 2016;25(10):1086-96. [Crossref] [PubMed]
- Looney RJ, Srinivasan R, Calabrese LH. The effects of rituximab on immunocompetency in patients with autoimmune disease. Arthritis Rheum. 2008;58(1):5-14. [Crossref] [PubMed]
- Rovin BH, Furie R, Latinis K, Looney RJ, Fervenza FC, Sanchez-Guerrero J, et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum. 2012;64(4):1215-26. [Crossref] [PubMed]
- Merrill JT, Neuwelt CM, Wallace DJ, Shanahan JC, Latinis KM, Oates JC, et al. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum. 2010;62(1):222-33. [Crossref] [PubMed] [PMC]
- Tokunaga M, Saito K, Kawabata D, Imura Y, Fujii T, Nakayamada S, et al. Efficacy of rituximab (anti-CD20) for refractory systemic lupus erythematosus involving the central nervous system. Ann Rheum Dis. 2007;66(4):470-5. [Crossref] [PubMed] [PMC]
- Cobo-Ibanez T, Loza-Santamaria E, Pego-Reigosa JM, Marques AO, Rua-Figueroa I, Fernandez-Nebro A, et al. Efficacy and safety of rituximab in the treatment of non-renal systemic lupus erythematosus: a systematic review. Semin Arthritis Rheum. 2014;44(2):175-85. [Crossref] [PubMed]
- Terrier B, Amoura Z, Ravaud P, Hachulla E, Jouenne R, Combe B, et al. Safety and efficacy of rituximab in systemic lupus erythematosus: results from 136 patients from the French AutoImmunity and Rituximab registry. Arthritis Rheum. 2010;62(8):2458-66. [Crossref] [PubMed]
- Ramos-Casals M, Garcia-Hernandez FJ, de Ramon E, Callejas JL, Martinez-Berriotxoa A, Pallares L, et al. Off-label use of rituximab in 196 patients with severe, refractory systemic autoimmune diseases. Clin Exp Rheumatol. 2010;28(4):468-76.
- Fanouriakis A, Kostopoulou M, Alunno A, Aringer M, Bajema I, Boletis JN, et al. 2019 update of the EULAR recommendations for the management of systemic lupus erythematosus. Ann Rheum Dis. 2019;78(6):736-45. [Crossref] [PubMed]
- Willems M, Haddad E, Niaudet P, Kone-Paut I, Bensman A, Cochat P, et al. Rituximab therapy for childhood-onset systemic lupus erythematosus. J Pediatr. 2006;148(5):623-7. [Crossref] [PubMed]
- Marks SD, Patey S, Brogan PA, Hasson N, Pilkington C, Woo P, et al. B lymphocyte depletion therapy in children with refractory systemic lupus erythematosus. Arthritis Rheum. 2005;52(10):3168-74. [Crossref] [PubMed]
- Podolskaya A, Stadermann M, Pilkington C, Marks SD, Tullus K. B cell depletion therapy for 19 patients with refractory systemic lupus erythematosus. Arch Dis Child. 2008;93(5):401-6. [Crossref] [PubMed]
- Polido-Pereira J, Ferreira D, Rodrigues AM, Nascimento C, Costa P, Almeida M, et al. Rituximab use in pediatric autoimmune diseases: four case reports. Ann N Y Acad Sci. 2009;1173:712-20. [Crossref] [PubMed]
- Nwobi O, Abitbol CL, Chandar J, Seeherunvong W, Zilleruelo G. Rituximab therapy for juvenile-onset systemic lupus erythematosus. Pediatr Nephrol. 2008;23(3):413-9. [Crossref] [PubMed] [PMC]
- Watson L, Beresford MW, Maynes C, Pilkington C, Marks SD, Glackin Y, et al. The indications, efficacy and adverse events of rituximab in a large cohort of patients with juvenile-onset SLE. Lupus. 2015;24(1):10-7. [Crossref] [PubMed]
- Groot N, de Graeff N, Marks SD, Brogan P, Avcin T, Bader-Meunier B, et al. European evidence-based recommendations for the diagnosis and treatment of childhood-onset lupus nephritis: the SHARE initiative. Ann Rheum Dis. 2017;76(12):1965-73. [Crossref] [PubMed]
- Neely J, von Scheven E. Autoimmune haemolytic anaemia and autoimmune thrombocytopenia in childhood-onset systemic lupus erythematosus: updates on pathogenesis and treatment. Curr Opin Rheumatol. 2018;30(5):498-505. [Crossref] [PubMed]
- Correll CK, Miller DD, Maguiness SM. Treatment of Childhood-Onset Lupus Erythematosus Panniculitis With Rituximab. JAMA Dermatol. 2020;156(5):566-9. [Crossref] [PubMed] [PMC]
- Groot N, de Graeff N, Avcin T, Bader-Meunier B, Brogan P, Dolezalova P, et al. European evidence-based recommendations for diagnosis and treatment of childhood-onset systemic lupus erythematosus: the SHARE initiative. Ann Rheum Dis. 2017;76(11):1788-96. [Crossref] [PubMed]
- Kearsley-Fleet L, Sampath S, McCann LJ, Baildam E, Beresford MW, Davies R, et al. Use and effectiveness of rituximab in children and young people with juvenile idiopathic arthritis in a cohort study in the United Kingdom. Rheumatology (Oxford). 2019;58(2):331-5. [Crossref] [PubMed] [PMC]
- Emery P, Fleischmann R, Filipowicz-Sosnowska A, Schechtman J, Szczepanski L, Kavanaugh A, et al. The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, dose-ranging trial. Arthritis Rheum. 2006;54(5):1390-400. [Crossref] [PubMed]
- Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med. 2004;350(25):2572-81. [Crossref] [PubMed]
- Kuek A, Hazleman BL, Gaston JH, Ostor AJ. Successful treatment of refractory polyarticular juvenile idiopathic arthritis with rituximab. Rheumatology (Oxford). 2006;45(11):1448-9. [Crossref] [PubMed]
- Narvaez J, Diaz-Torne C, Juanola X, Geli C, Llobet JM, Nolla JM, et al. Rituximab therapy for refractory systemic-onset juvenile idiopathic arthritis. Ann Rheum Dis. 2009;68(4):607-8. [Crossref] [PubMed]
- Alexeeva EI, Valieva SI, Bzarova TM, Semikina EL, Isaeva KB, Lisitsyn AO, et al. Efficacy and safety of repeat courses of rituximab treatment in patients with severe refractory juvenile idiopathic arthritis. Clin Rheumatol. 2011;30(9):1163-72. [Crossref] [PubMed]
- Zaripova LN, Midgley A, Christmas SE, Beresford MW, Baildam EM, Oldershaw RA. Juvenile idiopathic arthritis: from aetiopathogenesis to therapeutic approaches. Pediatr Rheumatol Online J. 2021;19(1):135. [Crossref] [PubMed] [PMC]
- Oddis CV, Reed AM, Aggarwal R, Rider LG, Ascherman DP, Levesque MC, et al. Rituximab in the treatment of refractory adult and juvenile dermatomyositis and adult polymyositis: a randomized, placebo-phase trial. Arthritis Rheum. 2013;65(2):314-24. [Crossref] [PubMed] [PMC]
- Aggarwal R, Loganathan P, Koontz D, Qi Z, Reed AM, Oddis CV. Cutaneous improvement in refractory adult and juvenile dermatomyositis after treatment with rituximab. Rheumatology (Oxford). 2017;56(2):247-54. [Crossref] [PubMed] [PMC]
- Bellutti Enders F, Bader-Meunier B, Baildam E, Constantin T, Dolezalova P, Feldman BM, et al. Consensus-based recommendations for the management of juvenile dermatomyositis. Ann Rheum Dis. 2017;76(2):329-40. [Crossref] [PubMed] [PMC]
- Stone JH, Merkel PA, Spiera R, Seo P, Langford CA, Hoffman GS, et al. Rituximab versus cyclophosphamide for ANCA-associated vasculitis. N Engl J Med. 2010;363(3):221-32. [Crossref] [PubMed] [PMC]
- Hellmich B, Sanchez-Alamo B, Schirmer JH, Berti A, Blockmans D, Cid MC, et al. EULAR recommendations for the management of ANCA-associated vasculitis: 2022 update. Ann Rheum Dis. 2023. [Crossref] [PubMed]
- Brogan P, Yeung RSM, Cleary G, Rangaraj S, Kasapcopur O, Hersh AO, et al. Phase IIa Global Study Evaluating Rituximab for the Treatment of Pediatric Patients With Granulomatosis With Polyangiitis or Microscopic Polyangiitis. Arthritis Rheumatol. 2022;74(1):124-33. [Crossref] [PubMed] [PMC]
- de Graeff N, Groot N, Brogan P, Ozen S, Avcin T, Bader-Meunier B, et al. European consensus-based recommendations for the diagnosis and treatment of rare paediatric vasculitides - the SHARE initiative. Rheumatology (Oxford). 2019;58(4):656-71. [Crossref]
- Carruthers MN, Topazian MD, Khosroshahi A, Witzig TE, Wallace ZS, Hart PA, et al. Rituximab for IgG4-related disease: a prospective, open-label trial. Ann Rheum Dis. 2015;74(6):1171-7. [Crossref] [PubMed]
- Goswami RP, Ray A, Chatterjee M, Mukherjee A, Sircar G, Ghosh P. Rituximab in the treatment of systemic sclerosis-related interstitial lung disease: a systematic review and meta-analysis. Rheumatology (Oxford). 2021;60(2):557-67. [Crossref] [PubMed]
- Donnithorne KJ, Atkinson TP, Hinze CH, Nogueira JB, Saeed SA, Askenazi DJ, et al. Rituximab therapy for severe refractory chronic Henoch-Schonlein purpura. J Pediatr. 2009;155(1):136-9. [Crossref] [PubMed]
- Baker KP, Edwards BM, Main SH, Choi GH, Wager RE, Halpern WG, et al. Generation and characterization of LymphoStat-B, a human monoclonal antibody that antagonizes the bioactivities of B lymphocyte stimulator. Arthritis Rheum. 2003;48(11):3253-65. [Crossref] [PubMed]
- Furie R, Stohl W, Ginzler EM, Becker M, Mishra N, Chatham W, et al. Biologic activity and safety of belimumab, a neutralizing anti-B-lymphocyte stimulator (BLyS) monoclonal antibody: a phase I trial in patients with systemic lupus erythematosus. Arthritis Res Ther. 2008;10(5):R109. [Crossref] [PubMed] [PMC]
- Blair HA, Duggan ST. Belimumab: A Review in Systemic Lupus Erythematosus. Drugs. 2018;78(3):355-66. [Crossref] [PubMed]
- Furie R, Petri M, Zamani O, Cervera R, Wallace DJ, Tegzova D, et al. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum. 2011;63(12):3918-30. [Crossref] [PubMed] [PMC]
- Navarra SV, Guzman RM, Gallacher AE, Hall S, Levy RA, Jimenez RE, et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet. 2011;377(9767):721-31. [Crossref] [PubMed]
- Iaccarino L, Andreoli L, Bocci EB, Bortoluzzi A, Ceccarelli F, Conti F, et al. Clinical predictors of response and discontinuation of belimumab in patients with systemic lupus erythematosus in real life setting. Results of a large, multicentric, nationwide study. J Autoimmun. 2018;86:1-8. [Crossref] [PubMed]
- Manzi S, Sanchez-Guerrero J, Merrill JT, Furie R, Gladman D, Navarra SV, et al. Effects of belimumab, a B lymphocyte stimulator-specific inhibitor, on disease activity across multiple organ domains in patients with systemic lupus erythematosus: combined results from two phase III trials. Ann Rheum Dis. 2012;71(11):1833-8. [Crossref] [PubMed] [PMC]
- van Vollenhoven RF, Petri MA, Cervera R, Roth DA, Ji BN, Kleoudis CS, et al. Belimumab in the treatment of systemic lupus erythematosus: high disease activity predictors of response. Ann Rheum Dis. 2012;71(8):1343-9. [Crossref] [PubMed] [PMC]
- Wise LM, Stohl W. Belimumab and Rituximab in Systemic Lupus Erythematosus: A Tale of Two B Cell-Targeting Agents. Front Med (Lausanne). 2020;7:303. [Crossref] [PubMed] [PMC]
- Chen F, Zheng Y, Chen X, Wen Z, Xu Y, Yang J, et al. Belimumab in childhood systemic lupus erythematosus: A review of available data. Front Immunol. 2022;13:940416. [Crossref] [PubMed] [PMC]
- Brunner HI, Abud-Mendoza C, Viola DO, Calvo Penades I, Levy D, Anton J, et al. Safety and efficacy of intravenous belimumab in children with systemic lupus erythematosus: results from a randomised, placebo-controlled trial. Ann Rheum Dis. 2020;79(10):1340-8. [Crossref] [PubMed] [PMC]
- Brunner HI, Ruperto N. Therapeutics: Biologics and small molecules. In: Petty RE, Laxer ML, Lindsley CB, Wedderburn LR, Mellins ED, Fuhlbrigge RC (eds). Textbook of Pediatric Rheumatology (8th ed). Philadelphia: Elsevier, 2021:175-194.
- Jansen MH, Rondaan C, Legger G, Minden K, Uziel Y, Toplak N, et al. Efficacy, Immunogenicity and Safety of Vaccination in Pediatric Patients With Autoimmune Inflammatory Rheumatic Diseases (pedAIIRD): A Systematic Literature Review for the 2021 Update of the EULAR/PRES Recommendations. Front Pediatr. 2022;10:910026. [Crossref] [PubMed] [PMC]
- Jansen MHA, Rondaan C, Legger GE, Minden K, Uziel Y, Toplak N, et al. EULAR/PRES recommendations for vaccination of paediatric patients with autoimmune inflammatory rheumatic diseases: update 2021. Ann Rheum Dis. 2022. [Crossref] [PubMed]