308
Views
29
CrossRef citations to date
0
Altmetric
Review

Cold agglutinin disease: current challenges and future prospects

, , , &
Pages 93-103 | Published online: 09 Apr 2019

References

  • Michel M. Classification and therapeutic approaches in autoimmune hemolytic anemia: an update. Expert Rev Hematol. 2011;4(6):607–618. doi:10.1586/ehm.11.6022077525
  • Sokol RJ, Hewitt S, Stamps BK. Autoimmune haemolysis: an 18-year study of 865 cases referred to a regional transfusion centre. Br Med J (Clin Res Ed). 1981;282(6281):2023–2027.
  • Berentsen S, Ulvestad E, Langholm R, et al. Primary chronic cold agglutinin disease: a population based clinical study of 86 patients. Haematologica. 2006;91(4):460–466.16585012
  • Swiecicki PL, Hegerova LT, Gertz MA. Cold agglutinin disease. Blood. 2013;122(7):1114–1121. doi:10.1182/blood-2013-02-47443723757733
  • 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.2013.09170224143001
  • de Tute R, Rawstron A, Evans P, Owen R. Cold agglutinin disease is a phenotypically distinct clonal B-cell disorder. 15 International Myeloma Workshop, Rome, Italy: sept 23–26, 2015. Clin Lymphoma Myeloma Leuk. 2015;15:e184.
  • Malecka A, Trøen G, Tierens A, et al. Frequent somatic mutations of KMT2D (MLL2) and CARD11 genes in primary cold agglutinin disease. Br J Haematol. 2018;183(5):838–842. doi:10.1111/bjh.1506329265349
  • Arthold C, Skrabs C, Mitterbauer-Hohendanner G, et al. Cold antibody autoimmune hemolytic anemia and lymphoproliferative disorders: a retrospective study of 20 patients including clinical, hematological, and molecular findings. Wien Klin Wochenschr. 2014;126(11–12):376–382. doi:10.1007/s00508-014-0547-z24842748
  • Berentsen S, Randen U, Tjønnfjord GE. Cold agglutinin-mediated autoimmune hemolytic anemia. Hematol Oncol Clin North Am. 2015;29(3):455–471. doi:10.1016/j.hoc.2015.01.00226043385
  • Schubothe H. The cold hemagglutinin disease. Semin Hematol. 1966;3(1):27–47.5323366
  • Rosse WF, Adams JP. The variability of hemolysis in the cold agglutinin syndrome. Blood. 1980;56(3):409–416.7407408
  • Ulvestad E, Berentsen S, Bo K, Shammas FV. Clinical immunology of chronic cold agglutinin disease. Eur J Haematol. 1999;63(4):259–266.10530415
  • Harboe M, van Furth R, Schubothe H, Lind K, Evans RS. Exclusive occurrence of K chains in isolated cold haemagglutinins. Scand J Haematol. 1965;2(3):259–266.4158055
  • Stone MJ, McElroy YG, Pestronk A, Reynolds JL, Newman JT, Tong AW. Human monoclonal macroglobulins with antibody activity. Semin Oncol. 2003;30(2):318–324. doi:10.1053/sonc.2003.5007712720161
  • Issitt PD. I blood group system and its relationship to disease. J Med Lab Technol. 1968;25(1):1–6.5638906
  • Berentsen S. Complement activation and inhibition in autoimmune hemolytic anemia: focus on cold agglutinin disease. Semin Hematol. 2018;55(3):141–149. doi:10.1053/j.seminhematol.2018.04.00230032751
  • Jonsen J, Kåss E, Harboe M. Complement and complement components in acquired hemolytic anemia with high titer cold antibodies. Acta Med Scand. 1961;170:725–729.14452388
  • Jaffe CJ, Atkinson JP, Frank MM. The role of complement in the clearance of cold agglutinin-sensitized erythrocytes in man. J Clin Invest. 1976;58(4):942–949. doi:10.1172/JCI108547965497
  • Shi J, Rose EL, Singh A, et al. TNT003, an inhibitor of the serine protease C1s, prevents complement activation induced by cold agglutinins. Blood. 2014;123(26):4015–4022. doi:10.1182/blood-2014-02-55602724695853
  • 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.201802419030291112
  • Tesfaye A, Broome C. A novel approach for treatment of cold agglutinin syndrome-related severe hemolysis. J Hematol. 2016;5(1):30–33. doi:10.14740/jh242w
  • 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-2017-04-77817528533306
  • Lyckholm LJ, Edmond MB. Images in clinical medicine. Seasonal hemolysis due to cold-agglutinin syndrome. N Engl J Med. 1996;334(7):437. doi:10.1056/NEJM1996061333424048552146
  • Ulvestad E. Paradoxical haemolysis in a patient with cold agglutinin disease. Eur J Haematol. 1998;60(2):93–100.9508349
  • Ulvestad E, Berentsen S, Mollnes TE. Acute phase haemolysis in chronic cold agglutinin disease. Scand J Immunol. 2001;54(1–2):239–242.11439172
  • Tjønnfjord E, Vengen OA, Berentsen S, Tjønnfjord GE. Prophylactic use of eculizumab during surgery in chronic cold agglutinin disease. BMJ Case Rep. 2017. doi:10.1136/bcr-2016-219066
  • Rørvik K. The syndrome of high-titre cold haemagglutination; a survey and a case report. Acta Med Scand. 1954;148(4):299–308.13157944
  • Shiiya C, Ota M. Cold agglutinin disease presenting as livedo racemosa. Cmaj. 2017;189(22):E781. doi:10.1503/cmaj.17138928584043
  • Stone MJ, Berentsen S. Hyperviscosity syndrome, cold agglutinin hemolytic anemia, and cryoglobulinemia In: Leblond V, Treon SP, Dimopoulos M, editors. Waldenström’s Macroglobulinemia. Switzerland: Springer International Publishing; 2017:171–183.
  • Hill QA, Stamps R, Massey E, et al. The diagnosis and management of primary autoimmune haemolytic anaemia. Br J Haematol. 2017;176(3):395–411. doi:10.1111/bjh.1447828005293
  • Bendix BJ, Tauscher CD, Bryant SC, Stubbs JR, Jacob EK. Defining a reference range for cold agglutinin titers. Transfusion. 2014;54(5):1294–1297. doi:10.1111/trf.1245324898454
  • Berentsen S. How I manage patients with cold agglutinin disease. Br J Haematol. 2018;181(3):320–330. doi:10.1111/bjh.1510929363757
  • Bessman JD, Banks D. Spurious macrocytosis, a common clue to erythrocyte cold agglutinins. Am J Clin Pathol. 1980;74(6):797–800.7446489
  • Dacie J. Auto-immune haemolytic anaemia (AIHA): cold-antibody syndromes I: idiopathic types: clinical presentation and haematological and serological findings In: Dacie J, editor. The Haemolytic Anaemias. Vol. 3 London: Churchill Livingstone; 1992:210–239.
  • Litman GW. Sharks and the origins of vertebrate immunity. Sci Am. 1996;275(5):67–71.8875809
  • Jain MD, Cabrerizo-Sanchez R, Karkouti K, Yau T, Pendergrast JM, Cserti-Gazdewich CM. Seek and you shall find–but then what do you do? Cold agglutinins in cardiopulmonary bypass and a single-center experience with cold agglutinin screening before cardiac surgery. Transfus Med Rev. 2013;27(2):65–73. doi:10.1016/j.tmrv.2012.12.00123375735
  • La Gioia A, Fumi M, Fiorini F, et al. Short preheating at 41 degrees C leads to a red blood cells count comparable to that in RET channel of Sysmex analysers in samples showing cold agglutination. J Clin Pathol. 2018;71(8):729–734. doi:10.1136/jclinpath-2017-20495429535214
  • Christenson WN, Dacie JV, Croucher BE, Charlwood PA. Electrophoretic studies on sera containing high-titre cold haemagglutinins: identification of the antibody as the cause of an abnormal gamma 1 peak. Br J Haematol. 1957;3(3):262–275.13460195
  • Pascual V, Victor K, Spellerberg M, Hamblin TJ, Stevenson FK, Capra JD. VH restriction among human cold agglutinins. The VH4-21 gene segment is required to encode anti-I and anti-i specificities. J Immunol. 1992;149(7):2337–2344.1382098
  • Berentsen S, Bø K, Shammas FV, Myking AO, Ulvestad E. Chronic cold agglutinin disease of the “idiopathic” type is a premalignant or low-grade malignant lymphoproliferative disease. APMIS. 1997;105(5):354–362.9201236
  • Treon SP, Xu L, Yang G, et al. MYD88 L265P somatic mutation in Waldenstrom’s macroglobulinemia. N Engl J Med. 2012;367(9):826–833. doi:10.1056/NEJMoa120071022931316
  • Malecka A, Trøen G, Tierens A, et al. Immunoglobulin heavy and light chain gene features are correlated with primary cold agglutinin disease onset and activity. Haematologica. 2016;101(9):e361–364. doi:10.3324/haematol.2016.14612627198717
  • Cao XX, Meng Q, Cai H, et al. Detection of MYD88 L265P and WHIM-like CXCR4 mutation in patients with IgM monoclonal gammopathy related disease. Ann Hematol. 2017. doi:10.1007/s00277-017-2968-z
  • Varettoni M, Zibellini S, Defrancesco I, et al. Pattern of somatic mutations in patients with Waldenstrom macroglobulinemia or IgM monoclonal gammopathy of undetermined significance. Haematologica. 2017;102(12):2077–2085. doi:10.3324/haematol.2017.17271828983055
  • Schreiber AD, Frank MM. Role of antibody and complement in the immune clearance and destruction of erythrocytes. I. In vivo effects of IgG and IgM complement-fixing sites. J Clin Invest. 1972;51(3):575–582. doi:10.1172/JCI1068464536807
  • Schreiber AD, Frank MM. Role of antibody and complement in the immune clearance and destruction of erythrocytes. II. Molecular nature of IgG and IgM complement-fixing sites and effects of their interaction with serum. J Clin Invest. 1972;51(3):583–589. doi:10.1172/JCI1068474622104
  • Jäger U, Gilbert JC, Panicker S, et al. The anti C1s complement antibody TNT009 induces rapid complete remissions of anaemia in patients with primary cold agglutinin disease. 21st Congress of the European Hematology Association; 6 9–12; 2016; Copenhagen.
  • Baines AC, Brodsky RA. Complementopathies. Blood Rev. 2017;31(4):213–223. doi:10.1016/j.blre.2017.02.00328215731
  • Röth A, Hüttmann A, Rother RP, Dührsen U, Philipp T. Long-term efficacy of the complement inhibitor eculizumab in cold agglutinin disease. Blood. 2009;113(16):3885–3886. doi:10.1182/blood-2009-01-19632919372265
  • Gupta N, Wang ES. Long-term response of refractory primary cold agglutinin disease to eculizumab therapy. Ann Hematol. 2014;93(2):343–344. doi:10.1007/s00277-013-1800-723722501
  • 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-2014-06-58302125232059
  • Yusuf HR, Hooper WC, Grosse SD, Parker CS, Boulet SL, Ortel TL. Risk of venous thromboembolism occurrence among adults with selected autoimmune diseases: a study among a U.S. cohort of commercial insurance enrollees. Thromb Res. 2015;135(1):50–57. doi:10.1016/j.thromres.2014.10.01225456001
  • Broome C, Cunningham JM, Mullins M, et al. Incidence of thromboembolic events is increased in a retrospective analysis of a large cold agglutinin disease (CAD) Cohort. 59th annual meeting of the American Society of Hematology, Atlanta, GA. Blood. 2017;130:928.
  • Bylsma L, Ording AG, Frøslev T, et al. The occurrence and survival of cold agglutinin disease in Denmark. 23rd congress of the Eurpopean Hematology Association, Stockholm, June 2018. HemaSphere. 2018;2(S1):513.
  • Dacie J. Treatment and prognosis of cold-antibody AIHA In: Dacie J, editor. The Haemolytic Anaemias. Vol. 3 London: Churchill Livingstone; 1992:502–520.
  • Michel M, Jäger U. Autoimmune hemolytic anemia In: Hoffman R, Benz EJ, Silberstein LE, Heslop H, Weitz J, Anastasi J, editors. Hematology: Basic Principles and Practice. 7 ed. Philadelphia, PA: Elsevier; 2017:648–662.
  • 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.201700439029296728
  • Gertz MA. Management of cold haemolytic syndrome. Br J Haematol. 2007;138(4):422–429. doi:10.1111/j.1365-2141.2007.06664.x17561970
  • Barcellini W, Fattizzo B, Zaninoni A. Current and emerging treatment options for autoimmune hemolytic anemia. Expert Rev Clin Immunol. 2018;14(10):857–872. doi:10.1080/1744666X.2018.152172230204521
  • Worlledge SM, Brain MC, Cooper AC, Hobbs JR, Dacie JV. Immmunosuppressive drugs in the treatment of autoimmune haemolytic anaemia. Proc R Soc Med. 1968;61(12):1312–1315.4177973
  • Hillen HF, Bakker SJ. Failure of interferon-alpha-2b therapy in chronic cold agglutinin disease. Eur J Haematol. 1994;53(4):242–243.7957810
  • O’Connor BM, Clifford JS, Lawrence WD, Logue GL. Alpha-interferon for severe cold agglutinin disease. Ann Intern Med. 1989;111(3):255–256.2502059
  • Rordorf R, Barth A, Nydegger U, Tobler A. Treatment of severe idiopathic cold-agglutinin diseases using interferon-alpha 2b. Schweiz Med Wochenschr. 1994;124(1–2):56–61.8296193
  • Salama A, Hartnack D, Lindemann HW, Lange HJ, Rummel M, Loew A. The effect of erythropoiesis-stimulating agents in patients with therapy-refractory autoimmune hemolytic anemia. Transfus Med Hemother. 2014;41(6):462–468. doi:10.1159/00036624425670934
  • Lee EJ, Kueck B. Rituxan in the treatment of cold agglutinin disease. Blood. 1998;92(9):3490–3491.9787200
  • 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-2003-10-359715070665
  • 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:10.1080/1042819050028648116321854
  • 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-2010-06-28864720634373
  • 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-2018-03-83541329898955
  • Hippe E, Jensen KB, Olesen H, Lind K, Thomsen PE. Chlorambucil treatment of patients with cold agglutinin syndrome. Blood. 1970;35(1):68–72.4189663
  • Berentsen S, Tjønnfjord GE, Shammas FV, et al. No response to cladribine in five patients with chronic cold agglutinin disease. Eur J Haematol. 2000;65(1):88–90.10914950
  • Treon SP, Tripsas CK, Meid K, et al. Ibrutinib in previously treated Waldenstrom’s macroglobulinemia. N Engl J Med. 2015;372(15):1430–1440. doi:10.1056/NEJMoa150154825853747
  • Abeykoon JP, Paludo J, King RL, et al. MYD88 mutation status does not impact overall survival in Waldenstrom macroglobulinemia. Am J Hematol. 2018;93(2):187–194. doi:10.1002/ajh.2495529080258
  • Risitano AM. Current and future pharmacologic complement inhibitors. Hematol Oncol Clin North Am. 2015;29(3):561–582. doi:10.1016/j.hoc.2015.01.00926043392
  • Shapiro R, Chin-Yee I, Lam S. Eculizumab as a bridge to immunosuppressive therapy in severe cold agglutinin disease of anti-Pr specificity. Clin Case Rep. 2015;3(11):942–944. doi:10.1002/ccr3.39926576277
  • Makishima K, Obara N, Ishitsuka K, et al. High efficacy of eculizumab treatment for fulminant hemolytic anemia in primary cold agglutinin disease. Ann Hematol. 2018 Oct 15. doi: 10.1007/s00277-018-3521-4. [Epub ahead of print]
  • Wouters D, Stephan F, Strengers P, et al. C1-esterase inhibitor concentrate rescues erythrocytes from complement-mediated destruction in autoimmune hemolytic anemia. Blood. 2013;121(7):1242–1244. doi:10.1182/blood-2012-11-46720923411737
  • Wouters D, Zeerleder S. Complement inhibitors to treat IgM-mediated autoimmune hemolysis. Haematologica. 2015;100(11):1388–1395. doi:10.3324/haematol.2015.12853826521297
  • 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.111129737533
  • 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-2018-06-85693030559259
  • Gertz MA, Qiu H, Kendall L, Saltarelli M, Yednock T, Sankaranarayanan S. ANX005, an inhibitory antibody against C1q, blocks complement activation triggered by cold agglutinins in human disease. 58th meeting of the American Society of Hematology, San Diego, CA. Blood. 2016;128:1265. doi:10.1182/blood-2016-06-724161
  • Lansita JA, Mease KM, Qiu H, Yednock T, Sankaranarayanan S, Kramer S. Nonclinical development of ANX005: a humanized anti-C1q antibody for treatment of autoimmune and neurodegenerative diseases. Int J Toxicol. 2017;36(6):449–462. doi:10.1177/109158181774087329202623
  • Grossi FV, Bedwell P, Deschatelets P, et al. APL-2, a complement C3 inhibitor for the potential treatment of paroxysmal nocturnal hemoglobinuria (PNH): phase I data from two completed studies in healthy volunteers. 58th annual meeting of the American Society of Hematology, San Diego, CA. Blood. 2016;128:1251. doi:10.1182/blood-2016-06-724161
  • Risitano AM, Ricklin D, Huang Y, et al. Peptide inhibitors of C3 activation as a novel strategy of complement inhibition for the treatment of paroxysmal nocturnal hemoglobinuria. Blood. 2014;123(13):2094–2101. doi:10.1182/blood-2013-11-53657324497537
  • Wong RSM, Pullon RWH, Deschatelets P, et al. Inhibition of C3 with APL-2 results in normalisation of markers of intravascular and extravascular hemolysis in patients with paroxysmal nocturnal hemoglobinuria (PNH). 60th annual meeting of the American Society of Hematology, San Diego, CA. Blood. 2018;132:2314.30467190
  • Hadnagy C. Agewise distribution of idiopathic cold agglutinin disease. Z Gerontol. 1993;26(3):199–201.8337916
  • Sparling TG, Andricevic M, Wass H. Remission of cold hemagglutinin disease induced by rituximab therapy. Cmaj. 2001;164(10):1405.
  • Engelhardt M, Jakob A, Ruter B, Trepel M, Hirsch F, Lubbert M. Severe cold hemagglutinin disease (CHD) successfully treated with rituximab. Blood. 2002;100(5):1922–1923.12211193
  • Gharib M, Poynton C. Complete, long-term remission of refractory idiopathic cold haemagglutinin disease after Mabthera. Br J Haematol. 2002;117(1):248–249.11918564
  • Berentsen S, Tjønnfjord GE, Brudevold R, et al. Favourable response to therapy with the anti-CD20 monoclonal antibody rituximab in primary chronic cold agglutinin disease. Br J Haematol. 2001;115(1):79–83.11722415
  • Finazzi G. Rituximab in autoimmune cytopenias: for which patients? Haematologica. 2002;87(2):113–114.11836158
  • Camou F, Viallard JF, Pellegrin JL. Rituximab in cold agglutinin disease. Rev Med Interne. 2003;24(8):501–504.12888170
  • Aggarwal R, Sestak AL, D’Souza A, Dillon SP, Namjou B, Scofield RH. Complete complement deficiency in a large cohort of familial systemic lupus erythematosus. Lupus. 2010;19(1):52–57. doi:10.1177/096120330934650819910391
  • Berentsen S. Cold agglutinins: fending off the attack. Blood. 2019;133(9):885–886. doi:10.1182/blood-2019-01-89430330819775