Complement-directed therapy for cold agglutinin disease: sutimlimab

References

• Alaggio R, Amador C, Anagnostopoulos I, et al. The 5th edition of the World Health Organization classification of haematolymphoid tumours: lymphoid neoplasms. Leukemia. 2022;36(7):1720–1748. DOI:10.1038/s41375-022-01620-2
   PubMed Web of Science ®Google Scholar
• Campo E, Jaffe ES, Cook JR, et al. The international consensus classification of mature lymphoid neoplasms: a report from the clinical advisory committee. Blood. 2022;140(11):1229–1253. DOI:10.1182/blood.2022015851
   PubMed Web of Science ®Google Scholar
• Climent F, Cid J, Sureda A. Cold agglutinin disease: a distinct clonal B-cell lymphoproliferative disorder of the bone marrow. Hemato. 2022;3(1):163–173.
   Google Scholar
• Berentsen S. Cold agglutinin disease. Hematology Am Soc Hematol Educ Program. 2016;2016(1):226–231.
   PubMed Web of Science ®Google Scholar
• Justiz Vaillant AA, Stang CM. Lymphoproliferative disorders. [Updated 2022 Aug 22]. In StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2023:1–8.
   Google Scholar
• Quintanilla-Martinez L. The 2016 updated WHO classification of lymphoid neoplasias. Hematol Oncol. 2017;35(S1):37–45.
   PubMedGoogle Scholar
• Randen U, Trøen G, Tierens A, et al. Primary cold agglutinin-associated lymphoproliferative disease: a B-cell lymphoma of the bone marrow distinct from lymphoplasmacytic lymphoma. Haematologica. 2014;99(3):497–504. DOI:10.3324/haematol.2013.091702
   PubMed Web of Science ®Google Scholar
• Broome CM, Hooda N, Su J, et al. Medically-attended anxiety and depression is increased among newly diagnosed patients with cold agglutinin disease: analysis of an integrated claim-clinical cohort in the United States. PLoS One. 2022;17(12):e0276617.
   PubMed Web of Science ®Google Scholar
• Jäger U, Barcellini W, Broome CM, et al. Diagnosis and treatment of autoimmune hemolytic anemia in adults: recommendations from the first international consensus meting. Blood Rev. 2020;41:100648.
   PubMed Web of Science ®Google Scholar
• Berentsen S. Complement activation and inhibition in autoimmune hemolytic anemia: focus on cold agglutinin disease. Semin Hematol. 2018;55(3):141–149.
   PubMed Web of Science ®Google Scholar
• Berentsen S. How I manage patients with cold agglutinin disease. Br J Haematol. 2018;181(3):320–330.
   PubMed Web of Science ®Google Scholar
• Berentsen S, Malecka A, Randen U, et al. Cold agglutinin disease: where do we stand, and where are we going? Clin Adv Hematol Oncol. 2020;18(1):35–44.
   PubMed Web of Science ®Google Scholar
• Berentsen S, Barcellini W, D’Sa S, et al. Cold agglutinin disease revisited: a multinational, observational study of 232 patients. Blood. 2020;136(4):480–488. DOI:10.1182/blood.2020005674
   PubMed Web of Science ®Google Scholar
• Berentsen S. New insights in the pathogenesis and therapy of cold agglutinin-mediated autoimmune hemolytic anemia. Front Immunol. 2020;11:590.
   PubMed Web of Science ®Google Scholar
• Gabbard AP, Booth GS. Cold agglutinin disease. Clin Hematol Int. 2020;2(3):95–100.
   PubMedGoogle Scholar
• Kumar V, Abbas AK, Aster JC. Red blood cell and bleeding disorders. Robbins & Cotran Pathological Basis of Disease. 10th Edition; 2020. p. 635–672.
   Google Scholar
• Röth A, Fryzek J, Jiang X, et al. Complement-mediated hemolysis persists year round in patients with cold agglutinin disease. Transfusion. 2022;62(1):51–59. DOI:10.1111/trf.16745
   PubMed Web of Science ®Google Scholar
• Murphy K. Janeway’s Immunobiology. 9th ed. New York, NY: Garland Science, Taylor & Francis Group, LLC; 2016.
   Google Scholar
• Jäger U, D’Sa S, Schörgenhofer C, et al. Inhibition of complement C1s improves severe hemolytic anemia in cold agglutinin disease: a first-in-human trial. Blood. 2019;133(9):893–901. DOI:10.1182/blood-2018-06-856930
   PubMed Web of Science ®Google Scholar
• Bartko J, Schoergenhofer C, Schwameis M, et al. A randomized, first-in-human, healthy volunteer trial of sutimlimab, a humanized antibody for the specific inhibition of the classical complement pathway. Clin Pharmacol Ther. 2018;104(4):655–663. DOI:10.1002/cpt.1111
   PubMed Web of Science ®Google Scholar
• Berentsen S, Röth A, Randen U, et al. Cold agglutinin disease: current challenges and future prospects. J Blood Med. 2019;10:93–103.
   PubMed Web of Science ®Google Scholar
• Berentsen S, Randen U, Tjønnfjord GE. Cold agglutinin-mediated autoimmune hemolytic anemia. Hematol Oncol Clin North Am. 2015;29(3):455–471.
   PubMed Web of Science ®Google Scholar
• Mullins M, Jiang X, Bylsma LC, et al. Cold agglutinin disease burden: a longitudinal analysis of anemia, medications, transfusions, and health care utilization. Blood Adv. 2017;1(13):839–848. DOI:10.1182/bloodadvances.2017004390
   PubMed Web of Science ®Google Scholar
• Berentsen S, Beiske K, Tjønnfjord GE. Primary chronic cold agglutinin disease: an update on pathogenesis, clinical features and therapy. Hematology. 2007;12(5):361–370.
   PubMed Web of Science ®Google Scholar
• Barcellini W, Fattizzo B, Zaninoni A, et al. Clinical heterogeneity and predictors of outcome in primary autoimmune hemolytic anemia: a GIMEMA study of 308 patients. Blood. 2014;124(19):2930–2936. DOI:10.1182/blood-2014-06-583021
   PubMed Web of Science ®Google Scholar
• Patriquin CJ, Pavenski K. O, wind, if winter comes … will symptoms be far behind?: exploring the seasonality (or lack thereof) and management of cold agglutinin disease. Transfusion. 2022;62(1):2–10.
   PubMed Web of Science ®Google Scholar
• Joly F, Dasmahapatra P, Su J, et al. Development of a cold agglutinin disease-specific patient-reported outcome symptom measure. Blood. 2021;138(Supplement 1):4057. DOI:10.1182/blood-2021-147199
   Google Scholar
• Joly F, Schmitt LA, McGee Watson PA, et al. Impact of cold agglutinin disease and its related fatigue on patients’ daily life: an online survey among 50 US patients. The Professional Society for Health Economics and Outcomes Research (ISPOR); 2021.
   Google Scholar
• Hansen DL, Möller S, Frederiksen H. Survival in autoimmune hemolytic anemia remains poor, results from a nationwide cohort with 37 years of follow-up. Eur J Haematol. 2022;109(1):10–20.
   PubMed Web of Science ®Google Scholar
• Broome CM, Cunningham JM, Mullins M, et al. Increased risk of thrombotic events in cold agglutinin disease: a 10-year retrospective analysis. Res Pract Thromb Haemost. 2020;4(4):628–635. DOI:10.1002/rth2.12333
   PubMed Web of Science ®Google Scholar
• Kamesaki T, Nishimura JI, Wada H, et al. Demographic characteristics, thromboembolism risk, and treatment patterns for patients with cold agglutinin disease in Japan. Int J Hematol. 2020;112(3):307–315. DOI:10.1007/s12185-020-02899-6
   PubMed Web of Science ®Google Scholar
• Broome CM, Barcellini W, Röth A, et al. Hemolytic markers, mortality, and thromboembolic events in cold agglutinin disease (CAD): a retrospective analysis of the optum electronic health record database in the United States. Blood. 2022;140(Supplement 1):5306–5308. DOI:10.1182/blood-2022-163232
   Google Scholar
• Bylsma LC, Gulbech Ording A, Rosenthal A, et al. Occurrence, thromboembolic risk, and mortality in Danish patients with cold agglutinin disease. Blood Adv. 2019;3(20):2980–2985. DOI:10.1182/bloodadvances.2019000476
   PubMed Web of Science ®Google Scholar
• Su J, Kosa K, DiBenedetti D. Patient-reported disease burden: in-depth interviews of patients with CAD. Blood. 2020;136(Supplement 1):29–30.
   Google Scholar
• Su J, Bylsma LC, Jiang X, et al. Healthcare resource utilization among commercially insured patients with cold agglutinin disease in the United States. J Med Econ. 2020;23(8):902–907. DOI:10.1080/13696998.2020.1764006
   PubMed Web of Science ®Google Scholar
• Mazonson P, Efrusy M, Santas C, et al. The HI-STAR study: resource utilization and costs associated with serologic testing for antibody-positive patients at four United States medical centers. Transfusion. 2014;54(2):271–277. DOI:10.1111/trf.12176
   PubMed Web of Science ®Google Scholar
• Fryzek JP, Hooda N, Öztürk Esen B, et al. P1539: seasonality of healthcare resource utilization among cold agglutinin disease among patients in Denmark: a retrospective analysis. Hemasphere. 2022;6:1420–1421.
   Google Scholar
• Wilson A, Joly F, Miles G, et al. Longitudinal analysis of anemia severity, treatment and healthcare resource utilization among patients with primary cold agglutinin disease in a large US database. Blood. 2020;136(Supplement 1):48–49. DOI:10.1182/blood-2020-139637
   Google Scholar
• Schietzel S, Anderegg M, Limacher A, et al. Humoral and cellular immune responses on SARS-CoV-2 vaccines in patients with anti-CD20 therapies: a systematic review and meta-analysis of 1342 patients. RMD Open. 2022;8(1):e002036. DOI:10.1136/rmdopen-2021-002036
   PubMed Web of Science ®Google Scholar
• Berentsen S. How I treat cold agglutinin disease. Blood. 2021;137(10):1295–1303.
   PubMed Web of Science ®Google Scholar
• Röth A, Bommer M, Hüttmann A, et al. Eculizumab in cold agglutinin disease (DECADE): an open-label, prospective, bicentric, nonrandomized phase 2 trial. Blood Adv. 2018;2(19):2543–2549. DOI:10.1182/bloodadvances.2018024190
   PubMed Web of Science ®Google Scholar
• Johnson ST, Puca KE. Evaluating patients with autoimmune hemolytic anemia in the transfusion service and immunohematology reference laboratory: pretransfusion testing challenges and best transfusion-management strategies. Hematology. 2022;2022(1):96–104.
   PubMedGoogle Scholar
• Rossi G, Gramegna D, Paoloni F, et al. Short course of bortezomib in anemic patients with relapsed cold agglutinin disease: a phase 2 prospective GIMEMA study. Blood. 2018;132(5):547–550. DOI:10.1182/blood-2018-03-835413
   PubMed Web of Science ®Google Scholar
• Berentsen S, Hill A, Hill QA, et al. Novel insights into the treatment of complement-mediated hemolytic anemias. Ther Adv Hematol. 2019;10:2040620719873321.
   Web of Science ®Google Scholar
• Jalink M, Berentsen S, Castillo JJ, et al. Effect of ibrutinib treatment on hemolytic anemia and acrocyanosis in cold agglutinin disease/cold agglutinin syndrome. Blood. 2021;138(20):2002–2005. DOI:10.1182/blood.2021012039
   PubMed Web of Science ®Google Scholar
• Röth A, Barcellini W, D’Sa S, et al. Sutimlimab in cold agglutinin disease. N Engl J Med. 2021;384(14):1323–1334. DOI:10.1056/NEJMoa2027760
   PubMed Web of Science ®Google Scholar
• Gelbenegger G, Jaeger U, Fillitz M, et al. Sustained sutimlimab response for 3 years in patients with cold agglutinin disease: a phase I, open-label, extension trial. Br J Haematol. 2022;198(4):e59–e62. DOI:10.1111/bjh.18289
   PubMed Web of Science ®Google Scholar
• Gelbenegger G, Schoergenhofer C, Derhaschnig U, et al. Inhibition of complement C1s in patients with cold agglutinin disease: lessons learned from a named patient program. Blood Adv. 2020;4(6):997–1005. DOI:10.1182/bloodadvances.2019001321
   PubMed Web of Science ®Google Scholar
• Clinicaltrials.gov. A study to assess the efficacy and safety of BIVV009 (sutimlimab) in participants with primary cold agglutinin disease who have a recent history of blood transfusion (CARDINAL Study). ClinicalTrials.Gov Identifier: NCT03347396. https://www.clinicaltrials.gov/ct2/show/NCT03347396 Last accessed 30 May 2023.
   Google Scholar
• Clinicaltrials.gov. A study to assess the efficacy and safety of BIVV009 (sutimlimab) in participants with primary cold agglutinin disease without a recent history of blood transfusion (CADENZA). ClinicalTrials.Gov Identifier: NCT03347422. https://clinicaltrials.gov/ct2/show/NCT03347422 Last accessed 30 May 2023.
   Google Scholar
• Röth A, Berentsen S, Barcellini W, et al. Sutimlimab in patients with cold agglutinin disease: results of the randomized placebo-controlled phase 3 CADENZA trial. Blood. 2022;140(9):980–991. DOI:10.1182/blood.2021014955
   PubMed Web of Science ®Google Scholar
• Röth A, Barcellini W, Tvedt THA, et al. Sutimlimab improves quality of life in patients with cold agglutinin disease: results of patient-reported outcomes from the CARDINAL study. Ann Hematol. 2022;101(10):2169–2177. DOI:10.1007/s00277-022-04948-y
   PubMed Web of Science ®Google Scholar
• Röth A, Broome CM, Barcellini W, et al. Sutimlimab provides clinically meaningful improvements in patient-reported outcomes in patients with cold agglutinin disease: results from the randomised, placebo-controlled, Phase 3 CADENZA study. Eur J Haematol. 2023;110(3):280–288. DOI:10.1111/ejh.13903
   PubMedGoogle Scholar
• ENJAYMO (sutimlimab-jome). Summary of Product Characteristics (First published: 17/11/2022) GEB. https://www.ema.europa.eu/en/documents/product-information/enjaymo-epar-product-information_en.pdf Lastaccessed 30 May 2023.
   Google Scholar
• Röth A, Barcellini W, D’Sa S, et al. Complement C1s inhibition with sutimlimab results in durable response in cold agglutinin disease: CARDINAL study 1-year interim follow-up results. Haematologica. 2022;107(7):1698–1702. DOI:10.3324/haematol.2021.279812
   PubMed Web of Science ®Google Scholar
• Röth A, Barcellini W, D’Sa S, et al. Inhibition of complement C1s with sutimlimab in patients with cold agglutinin disease (CAD): 2-Year Follow-up from the CARDINAL Study. European Hematology Association (EHA). Presentation S285. 2022.
   Google Scholar
• Röth A, Broome CM, Barcellini W, et al. Sutimlimab, a targeted complement c1s inhibitor, improves quality of life (QOL) in patients with cold agglutinin disease (CAD): results from the randomized, placebo-controlled phase 3 CADENZA study. Oral Presentation At EHA. 2021;138(Supplement 1):S349–349. DOI:10.1182/blood-2021-148066
   Google Scholar
• Weitz IC, Ueda Y, Shafer FE, et al. Inflammation and fatigue in patients with cold agglutinin disease (CAD): analysis from the phase 3 Cardinal study. Blood. 2020;136(Supplement 1):7–8. doi:10.1182/blood-2020-140335.
   Google Scholar
• Röth A, Berentsen S, Barcellini W, et al. Sustained complement C1s inhibition with sutimlimab in patients with cold agglutinin disease results in continued efficacy during Part B of the randomized placebo-controlled Phase 3 CADENZA study (NCT03347422). American Society of Hematology (ASH). 2022.
   Google Scholar
• Röth A, Broome CM, Barcellini W, et al. Sutimlimab provides sustained improvements in patient-reported outcomes and quality of life in patients with cold agglutinin disease: open-label extension of the randomized, phase 3 CADENZA study. Blood. 2022;140(Supplement 1):70–72. DOI:10.1182/blood-2022-159966
   Google Scholar
• Röth, A. Cold Agglutinin Disease Real World Evidence Registry. CADENCE. EU PAS Register Number: EUPAS47940 [Cited 2023 May 30]. Available from: https://www.encepp.eu/encepp/viewResource.htm?id=47941
   Google Scholar
• ENJAYMO (sutimlimab-jome). U.S Food and Drug Administration. Prescribing Information (Revised: 1/2023) BUIASC. Bioverativ USA Inc a SANOFI COMPANY. 2022 [Cited 2023 May 30]. Available from:https://www.accessdata.fda.gov/drugsatfda_docs/label/2022/761164s000lbl.pdf
   Google Scholar
• Sanofi. ”European Commission approves Enjaymo® (sutimlimab) for treatment of hemolytic anemia in adult patients with cold agglutinin disease.” Press release, 17 Nov 2022. [Cited 2023 May 30]. Available from:https://www.sanofi.com/en/media-room/press-releases/2022/2022-11-17-17-50-00-2558583
   Google Scholar
• Sanofi. ”FDA approves Enjaymo™ (sutimlimab-jome), first treatment for use in patients with cold agglutinin disease.” Press release, 4 Feb 2022. https://www.sanofi.com/en/media-room/press-releases/2022/2022-02-04-22-00-00-2379517. Last accessed 30 May 2023.
   Google Scholar
• Berentsen S, Ulvestad E, Gjertsen BT, et al. Rituximab for primary chronic cold agglutinin disease: a prospective study of 37 courses of therapy in 27 patients. Blood. 2004;103(8):2925–2928. DOI:10.1182/blood-2003-10-3597
   PubMed Web of Science ®Google Scholar
• Schöllkopf C, Kjeldsen L, Bjerrum OW, et al. Rituximab in chronic cold agglutinin disease: a prospective study of 20 patients. Leuk Lymphoma. 2006;47(2):253–260. DOI:10.1080/10428190500286481
   PubMed Web of Science ®Google Scholar
• Berentsen S, Randen U, Oksman M, et al. Bendamustine plus rituximab for chronic cold agglutinin disease: results of a Nordic prospective multicenter trial. Blood. 2017;130(4):537–541. DOI:10.1182/blood-2017-04-778175
   PubMed Web of Science ®Google Scholar
• Berentsen S, Randen U, Vågan AM, et al. High response rate and durable remissions following fludarabine and rituximab combination therapy for chronic cold agglutinin disease. Blood. 2010;116(17):3180–3184. DOI:10.1182/blood-2010-06-288647
   PubMed Web of Science ®Google Scholar
• Berentsen S, Tjønnfjord GE. Current treatment options in cold agglutinin disease: B-cell directed or complement directed therapy? Transfus Med Rev. 2022;36(4):181–187.
   PubMed Web of Science ®Google Scholar
• Schrezenmeier H, Muus P, Socié G, et al. Baseline characteristics and disease burden in patients in the International Paroxysmal Nocturnal Hemoglobinuria Registry. Haematologica. 2014;99(5):922–929. DOI:10.3324/haematol.2013.093161
   PubMed Web of Science ®Google Scholar
• Lee JW, Jang JH, Kim JS, et al. Clinical signs and symptoms in non-transfused patients with paroxysmal nocturnal hemoglobinuria from a Korean prospective PNH registry. Blood. 2013;122(21):3720. DOI:10.1182/blood.V122.21.3720.3720
   Web of Science ®Google Scholar
• Berentsen S, Barcellini W, D’Sa S, et al. Sutimlimab for treatment of cold agglutinin disease: why, how and for whom? Immunotherapy. 2022;14(15):1191–1204. DOI:10.2217/imt-2022-0085
   PubMed Web of Science ®Google Scholar
• Reynaud Q, Durieu I, Dutertre M, et al. Efficacy and safety of rituximab in auto-immune hemolytic anemia: a meta-analysis of 21 studies. Autoimmun Rev. 2015;14(4):304–313. DOI:10.1016/j.autrev.2014.11.014
   PubMed Web of Science ®Google Scholar
• M-N J, Qiu Y, Y-Y W, et al. Rituximab-containing therapy for cold agglutinin disease: a retrospective study of 16 patients. Sci Rep. 2020;10(1):12694. DOI:10.1038/s41598-020-69465-2
   PubMed Web of Science ®Google Scholar
• Fattizzo B, Bortolotti M, Rampi N, et al. Seroconversion to mRNA SARS-CoV-2 vaccines in hematologic patients. Front Immunol. 2022;13:852158.
   PubMed Web of Science ®Google Scholar
• Fattizzo B, Röth A, Broome CM, et al. Concomitant use of sutimlimab and COVID-19 vaccines in patients with cold agglutinin disease from the phase 3 CARDINAL and CADENZA studies. American Society of Hematology (ASH). 2022. Poster 1208.
   Google Scholar
• Röth A, Karaouni A, Msihid J, et al. Sutimlimab after prior rituximab use in patients with cold agglutinin disease (CAD): pooled post-hoc analyses from the CARDINAL and CADENZA trials. European Hematology Association (EHA). 2022. Poster P1532.
   Google Scholar
• Despotovic JM, Kim TO. Cold AIHA and the best treatment strategies. Hematology. 2022;2022(1):90–95.
   PubMedGoogle Scholar