Transfusion of ABO major incompatible red
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1 ORIGINAL ARTICLE Successful use of eculizumab for treatment of an acute hemolytic reaction after ABO-incompatible red blood cell transfusion Christof Weinstock, 1 Robert Möhle, 2 Christiane Dorn, 2 Katja Weisel, 2 Britta Höchsmann, 1 Hubert Schrezenmeier, 1 * and Lothar Kanz 2 * BACKGROUND: Transfusion of ABO major incompatible red blood cells (RBCs) can activate the complement system and can cause severe and even lethal acute hemolytic reactions. The activation of the complement system with formation of C3a and C5a (anaphylatoxins) and the release of hemoglobin from the lysed RBCs are thought to mediate clinical signs like fever, hypotension, pain, and acute renal failure. Therapeutic inhibition of the complement cascade in case of ABO-incompatible RBC transfusion would be desirable to ameliorate the signs and symptoms and to improve the outcome of the reaction. STUDY DESIGN AND METHODS: A patient with blood group B was erroneously transfused with a unit of group A 2 RBCs. Within 1 hour after transfusion she received eculizumab, a monoclonal antibody that binds to the complement component C5 and blocks its cleavage. Clinical and immunohematologic observations are reported here. RESULTS: Hemoglobinemia and hemoglobinuria were present for several hours after transfusion, but she developed no hypotension, no renal failure, and no disseminated intravascular coagulation. As shown by flow cytometry, group A cells survived in the peripheral blood for more than 75 days. No immunoglobulin G was detectable by column agglutination technique on these cells. CONCLUSION: A low isoagglutinin titer and blood group A 2 of the erroneously transfused cells most likely were the reason for the absence of clinical signs during and immediately after the ABO-incompatible transfusion. In the further course, eculizumab successfully protected the incompatible RBCs from hemolysis for several weeks. Transfusion of ABO major incompatible red blood cells (RBCs) may result in severe hemolysis leading to major morbidity or death. 1 The hemolysis is caused by the isoagglutinins (anti-a, anti-b), antibodies directed against the ABO antigens that are not expressed on the cells of the transfused individual. Because most of the isoagglutinins are of the immunoglobulin (Ig)M type, and because ABO antigens are present in high density on the surface of RBCs, activation of complement with immediate, intravascular hemolysis often occurs in ABO-incompatible transfusion. The cleavage of the complement components releases the fragments C3a and C5a, which are chemoattractants and ABBREVIATIONS: ahus = atypical hemolytic uremic syndrome; AP(s) = anchored protein(s); GPI = glycosylphosphatidylinositol; MAC = membrane attack complex; PNH = paroxysmal nocturnal hemoglobinuria. From the 1 Institute of Clinical Transfusion Medicine and Immunogenetics Ulm, German Red Cross Blood Service Baden-Württemberg Hessen, and the Institute of Transfusion Medicine, University of Ulm, Ulm, Germany; and the 2 Department of Medicine, University Hospital of Tuebingen, Tuebingen, Germany. Address reprint requests to: Christof Weinstock, Institute of Clinical Transfusion Medicine and Immunogenetics Ulm, Helmholtzstrasse 10, Ulm, Germany; c.weinstock@blutspende.de. *HS and LK contributed equally to this work and share the last authorship. Part of these data has been published in abstract form at the annual meeting of the German Society of Transfusion Medicine and Immunohematology (DGTI) in Münster, September 2013, and at the 33rd International Congress of the International Society for Blood Transfusion (ISBT), in Seoul, May/June Received for publication March 17, 2014; revision received July 24, 2014, and accepted August 5, doi: /trf AABB TRANSFUSION **;**:**-**. Volume **, ** ** TRANSFUSION 1
2 WEINSTOCK ET AL. which may induce cytokine production in monocytes. 2 In addition, C3a and C5a can trigger the oxidative burst in macrophages and neutrophils, and they can release histamine from mast cells. Histamine causes contraction of smooth muscle cells and increases the permeability of blood vessels. 3 A substantial part of the clinical signs and symptoms of an acute hemolytic transfusion reaction is thought to be mediated by C3a and C5a. 4 Activation of the terminal complement cascade leads to the formation of the membrane attack complex (MAC), which can cause severe intravascular hemolysis. Intravascular hemolysis may result in renal failure and disseminated intravascular coagulation. 5 Eculizumab is a monoclonal antibody that blocks the cleavage of C5 and therefore inhibits formation of the MAC. Eculizumab has been used successfully in the treatment of patients with paroxysmal nocturnal hemoglobinuria (PNH) 6 and atypical hemolytic uremic syndrome (ahus). 7 Since blocking of C5 prevents both formation of the anaphylatoxin C5a and the lysis of the RBC, the use of eculizumab in case of ABO-incompatible transfusion might be beneficial. We report on a case of an erroneous ABO-incompatible transfusion, who received eculizumab early in the course of the hemolytic reaction. PATIENT A patient with anemia due to PNH required transfusion of RBCs (Day 0). The patient harbored a large population of cells deficient of glycosylphosphatidylinositol (GPI)- anchored proteins (GPI-APs). At time of transfusion, the proportion of granulocytes deficient of the GPI-AP CD24 and CD66b was 91%. The GPI-AP CD58 and CD59 were absent on 18.0 and 33.5% of RBCs and on 68.8 and 87.7% of reticulocytes, respectively. The patient had blood group B, but for inventory reasons the blood bank matched 2 units with blood group O. In the outpatient clinic the bedside test was done, compatibility of the group O units was ascertained, and the first of the 2 units was transfused. After this transfusion was completed, accidentally a unit with blood group A 2, which was prepared nearby for another patient, was taken. Immediately after transfusion of the complete unit, the error was noted and the patient was transferred to the intensive care unit. A quantity of 250 mg of prednisolone and 900 mg of eculizumab were administered intravenously within 1 hour after the end of the incompatible transfusion. The dose of 900 mg was selected since we aimed an immediate complete blockade of C5 and this dose is in the established dose range in the registered indications PNH and ahus according to the prescribing information. 6-8 Until this off-label use of eculizumab the patient had declined treatment with eculizumab. Between 18 and 4% group A cells were present in the patient s blood for about 4 weeks. To prevent delayed hemolysis, doses of 600 mg were repeated on Days 8, 15, and 22, doses of 900 mg were given on Days 29, 32, and 47. After Day 47, 900 mg eculizumab was given fortnightly. Thrombosis is the most frequent and feared complication of PNH. Both activation of the complement system and intravascular hemolysis are thought to be major contributors to thromboembolism in PNH. 9 Thus, heparin infusion was started with 24,000 IU/24 hours. In the course of therapy, the dose was adjusted to achieve an activated partial thromboplastin time of 50 to 70 seconds. Heparin was continued until discharge. Saline 0.9% (200 ml/hr) was infused for 20 hours to force diuresis. On Day 3 the patient was transferred to a general ward, and on Day 12 she was discharged without sequelae. MATERIALS AND METHODS Blood counts and clinical chemistry tests were performed in the central laboratory of the University Hospital of Tuebingen. Serologic testing by routine blood bank methods and by flow cytometry was performed in the IKT Ulm/Institute of Transfusion Medicine of the University of Ulm: ABO grouping of RBCs was done with the column agglutination method (Grifols, Langen, Germany). Reverse grouping (Immucor, Rödermark, Germany) and titration of the patient s anti-a (using A 1 cells) was done in the tube method. The direct antiglobulin test (DAT) was performed in the column agglutination method (Grifols). Surviving RBCs with blood group A were determined by flow cytometry as described recently. 10 In brief, RBCs were incubated overnight with 5% formaldehyde. The cells were washed with phosphate-buffered saline and 100 μl of fluorescein isothiocyanate labeled monoclonal anti-a (Clone NaM87-1F6; Becton-Dickinson, Heidelberg, Germany) diluted 1:100 in 1% bovine serum albumin was added to 10 μl of a 10% RBC suspension and incubated for 30 minutes. The cells were then washed and measured in a flow cytometer (FC500, Beckman-Coulter, Krefeld, Germany). In addition, double staining with anti-a and CD59 (Clone p282h19; Becton Dickinson, Heidelberg, Germany) was performed as previously described. 11 RESULTS Clinical chemistry Intravascular hemolysis was demonstrable by free hemoglobin (Hb) in plasma (Fig. 1) and in urine (visible hemoglobinuria and 3+ reacting urinalysis reagent strips). The free Hb and the elevated bilirubin concentration returned to normal within 1 day (Fig. 1). Due to the patient s PNH the plasma concentration of lactate dehydrogenase (LDH) was elevated before the transfusion, but did not further increase despite the incompatible transfusion. During eculizumab therapy LDH declined to normal values within 3 weeks. Fibrinogen and antithrombin were monitored and their concentrations in plasma stayed in the 2 TRANSFUSION Volume **, ** **
3 ECULIZUMAB TREATMENT OF ACUTE HEMOLYSIS Hb Bilirubin (g/dl) (mg/dl) days after ABO-incompatible transfusion Free Hb (mg/dl) normal range during the whole hospital stay. In addition, no D-dimers were measurable, indicating that no disseminated intravascular coagulation ensued. Creatinine was always below 0.6 mg/dl. The transfusion of the 2 units transiently increased the patient s Hb from 7.8 to 9.5 g/dl. Because of the hemolysis the Hb declined again, reaching the nadir at 7.6 g/dl on Day 2. During eculizumab therapy the Hb increased within 14 days to a constant level of approximately 10.0 g/dl. Blood group serology Only part of the group A RBCs was hemolyzed immediately during and after transfusion. For more than 2 weeks 10% to 20% of the circulating RBCs were found to be of blood group A (Table 1). To reassess these numbers we estimated the patient s blood volume and the volumes of the RBC units: The patient had a total blood volume of approximately 4124 ml (2.44 L/m 2 body surface area; 12 patient s surface area, 1.69 m 2 ). The volume of her RBCs before transfusion was approximately 949 ml (4124 ml hematocrit [Hct] 0.23). An average RBC unit (297 ml, Hct 0.6) was assumed to contain 178 ml of RBCs. Immediately after the transfusion of the 2 RBC units, the patient s volume of RBCs was increased to 1305 ml; 178 ml (13.6%) of them were of blood group A. On Day 2 the Hb was lower than before transfusion, indicating the lysis of patient RBCs. Thus, the proportion of the surviving group A cells was relatively increased, explaining the high percentage of 10% to 20% found by flow cytometry. Whereas the patient s autologous RBCs showed the typical mosaic of a cell population with normal expression of GPI-AP and a population with deficient GPI-AP expression, the transfused group A cells all showed normal LDH (U/L) Fig. 1. One unit of group O and erroneously one unit of group A were transfused on Day 0. Eculizumab was administered within 1 hour after the incompatible transfusion. Values for Hb (g/dl; ), bilirubin (mg/dl; ), free Hb in plasma (mg/dl; ), and LDH (U/L; ) are shown for 42 days TABLE 1. Serologic findings after an erroneous transfusion of ABO-incompatible RBCs Day after transfusion of ABO-incompatible RBCs Serologic test Patient RBCs ABO grouping Anti-A 0* MA MA MA MA MA MA MA MA Anti-B 3+ MA MA MA MA MA MA MA MA Residual A cells (%) DAT Polyspecific Negative Negative (+) (+) (+) + (+) Anti-IgG Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Anti-C3 Negative Negative (+) (+) (+) + (+) Patient serum Reverse grouping A1 cells A2 cells B cells Titer of anti-a * Reaction strength: + (reactive) to 4+ (very strong reactive); 0 = nonreactive; (+) = weakly reactive. MA = mixed-field agglutination. MFA describes the simultaneous presence of agglutinated (antigen-positive) and nonagglutinated (antigen-negative) RBCs in a hemagglutination test. Volume **, ** ** TRANSFUSION 3
4 WEINSTOCK ET AL. expression of GPI-AP. The incompatible group A cells survived surprisingly long. On Day 75 still group A cells were present in flow cytometry, whereas on Day 91 group A cells were no longer detectable (Table 1). The survival of group A cells was demonstrable not only by flow cytometry but also by column agglutination technique. Mixed-field agglutination with anti-a was observed until Day 22. When the group A cells were below 4% (as measured by flow cytometry), mixed-field agglutination in column agglutination technique was no longer detectable. Before transfusion the titer of the isoagglutinin anti-a was 2, immediately after transfusion of the group A unit the titer was 1. The anti-a was not boostered by the transfused group A cells but had a titer between 2 and 8 during the whole observation period. The DAT of the patient s cells was negative before and immediately after transfusion. With the start of eculizumab, a weak deposit of Complement Component 3 was detectable on the RBCs, which continuously increased. DISCUSSION Acute intravascular hemolysis is a severe complication of transfusion therapy, which may result in major morbidity or death. 1,4 Both the release of anaphylatoxins during the activation of the complement cascade and the release of intracellular components and cell fragments are thought to cause the major part of the clinical signs and symptoms. 2 Eculizumab inhibits the cleavage of C5, 13 thereby preventing the release of the anaphylatoxin C5a and the formation of the MAC, which finally lyses the attacked cell. So far, eculizumab is only licensed for the treatment of PNH and ahus. We report here on a case of an unintended transfusion of ABO-incompatible RBCs followed by the off-label use of eculizumab, which was administered within 1 hour after transfusion. A PNH patient (blood group B), who had not been treated with eculizumab to this date, was transfused with 1 unit of group O RBCs and, erroneously, with a unit of group A cells. An acute intravascular hemolysis followed, to which at least three mechanisms may have contributed: 1) The patient s anti-a isoagglutinins lysed incompatible group A cells. 2) The transfused group O unit and the group A unit both carried anti-b isoagglutinins in the residual plasma. Passively administered anti-b bound to patient cells might have activated the complement system causing intravascular hemolysis. 3) Lysis of innocent bystander PNH RBCs. The activation of the complement system by isoagglutinins is not limited to the cells, to which the isoagglutinins have bound. Activated complement components are carried away with the blood stream and are deposited on the surface of other RBCs. Normal RBCs carrying complement-inhibiting proteins on their surface can often inactivate the deposited complement. PNH cells lack GPI-APs like the complement regulating proteins CD55 or CD59. Deposition of activated complement components on PNH cells, therefore, may lead to the formation of the MAC and to the lysis of PNH RBCs as innocent bystanders. Hemolysis after the transfusion of group O blood units to PNH patients with group A or AB, respectively, has been reported. 14,15 However, three of six patients did not show signs of hemolysis, one of them being a patient with group AB receiving 2 units of group B apheresis platelets. 15 The patient presented here received leukoreduced RBC suspensions in additive solution (SAG-M). The exact residual donor plasma volume and the titers of the anti-b present in the transfused units are not known, but according to the continuous quality control these units contain a mean residual plasma volume of only 13 ml. In the past this patient already had received at least six group O units without notice of hemolysis. Thus, the hemolysis likely started with the destruction of a part of the incompatible group A cells. The marked decrease of the Hb value after transfusion indicated that in addition to group A cells a considerable number of patient PNH cells were lysed. Most likely these cells were destroyed as innocent bystanders. In addition to eculizumab administered early after transfusion, other circumstances probably contributed to the advantageous outcome: First, the transfused RBCs had blood group A 2. Cells with blood group A 2 carry far less A antigens (approx. 200,000) than RBCs with blood group A 1 (approx. 1 million antigens) 16 and may, therefore, be at lesser risk of complement-mediated hemolysis. Second, the patient had an anti-a titer of only 2, which is rather low when compared to literature. 16 Third, seemingly no IgGmediated extravascular hemolysis took place. In most individuals with blood group A or B the majority of the isoagglutinins are IgM, and few are IgG. 16 Sera containing larger amounts of IgG isoagglutinins are mostly from individuals with blood group O. Because this patient had blood group B, we speculate that only few isoagglutinins were IgG. This speculation was encouraged by the results of the DAT which, showed only C3d but no IgG on the RBCs of the patient. Deposition of C3 fragments on RBCs is a known phenomenon that develops in the majority of PNH patients treated with eculizumab. 17,18 ABO-incompatible hemolysis is a rare event and so far no experience exists on the use of eculizumab in this situation. We, therefore, cannot exactly define to what extent the advantageous course of the hemolysis in the patient presented is attributable to the effect of eculizumab or to the low isoagglutinin titer. In our opinion eculizumab given early after the ABO-incompatible transfusion, substantially contributed to the survival of a surprising large portion of incompatible group A cells for several weeks. Some of the cells survived for at least 75 days, which get close to the physiologic survival of ABO- 4 TRANSFUSION Volume **, ** **
5 ECULIZUMAB TREATMENT OF ACUTE HEMOLYSIS identical RBCs. Further cases need to be studied to clarify the value of eculizumab in acute hemolytic reactions. Intravascular hemolysis proceeds rather fast. Therefore, eculizumab must be given as soon as possible after an incompatible transfusion. We recommend drawing blood samples just before administration of eculizumab to determine the amount of ongoing hemolysis and the percentage of circulating incompatible cells at time of treatment. A dose of 900 mg is in the established dose range for the registered indications PNH (600 mg weekly in the induction period and 900 mg every 14 ± 2 days in the maintenance period). 6,7 It completely blocks terminal complement for at least 1 week. 6-8,13 Like in the induction period of PNH and ahus treatment we recommend to repeat eculizumab weekly as long as a substantial proportion of incompatible RBCs is still present and there is evidence of ongoing hemolysis. This time period may be highly variable. Therefore, regular assessment of remaining incompatible cells and hemolysis should be performed to facilitate decision making on further eculizumab doses. Adverse effects of eculizumab may be headache, dizziness, nausea, vomiting, joint aches, and upper respiratory tract infections. In addition, treatment with eculizumab is associated with an increased risk for meningococcal infections. 19 The product labeling contains a boxed warning recommending immunization with a polyvalent meningococcal vaccine at least 2 weeks before start of treatment. If eculizumab is given as an emergency treatment as in the case reported here, physicians must be aware of that risk for infection by Neisseria meningitidis. Antibiotic prophylaxis (penicillin G or ciprofloxacin) should be considered and delayed vaccination against meningococci should be administered in particular if additional eculizumab doses will be given. Transfusion of incorrect blood components is still a major cause of transfusion-related mortality and morbidity. 1 Our efforts in the first place must focus on avoiding such events. If it happens, optimal treatment must be given. Based on pathophysiology of acute hemolytic transfusion reaction and its mechanism of action, eculizumab might be a suitable intervention to limit sequelae of ABO-incompatible RBC transfusion. Rescue of antibody-mediated rejection after ABO-incompatible kidney transplant has been reported. 20,21 To our knowledge, this is the first report on successful use of eculizumab in acute hemolytic transfusion reaction. Further data should be collected to assess the role of eculizumab in management of acute transfusion reactions. ACKNOWLEDGMENTS The authors acknowledge the technical assistance of Sabrina Finn and Gabriele Braun. CONFLICT OF INTEREST HS served on an advisory committee for and received honoraria and research funding from Alexion Pharmaceuticals. The other authors have disclosed no conflicts of interest. REFERENCES 1. Serious Hazards of Transfusion Steering Committee. Serious hazards of transfusion: annual report Manchester (UK): SHOT Office; Available from: -Annual-Report-2012.pdf 2. Kohl J. Anaphylatoxins and infectious and non-infectious inflammatory diseases. Mol Immunol 2001;38: Egawa G, Nakamizo S, Natsuaki Y, et al. Intravital analysis of vascular permeability in mice using two-photon microscopy. Sci Rep 2013;3: Webster BH. Clinical presentation of haemolytic transfusion reactions. Anaesth Intensive Care 1980;8: Goldfinger D. Acute hemolytic transfusion reactions a fresh look at pathogenesis and considerations regarding therapy. Transfusion 1977;17: Hillmen P, Young NS, Schubert J, et al. The complement inhibitor eculizumab in paroxysmal nocturnal hemoglobinuria. N Engl J Med 2006;355: Legendre CM, Licht C, Muus P, et al. Terminal complement inhibitor eculizumab in atypical hemolytic-uremic syndrome. N Engl J Med 2013;368: Soliris.net. U.S. prescribing information. April 2014 [cited 2014 Sep 12]. Available from: default/files/assets/soliris_pi.pdf 9. Hill A, Kelly RJ, Hillmen P. Thrombosis in paroxysmal nocturnal hemoglobinuria. Blood 2013;121: Wagner FF, Flegel WA. Analysis by flow cytometry of chimerism after bone marrow transplantation and of erythrocyte antigen density. In: Gutensohn K, Sonneborn HH, Kühnl P, editors. Aspects of the flow-cytometric analysis of red blood cells. 1st ed. Heidelberg: Clin Lab Publications; p Höchsmann B, Rojewski M, Schrezenmeier H. Paroxysmal nocturnal hemoglobinuria (PNH): higher sensitivity and validity in diagnosis and serial monitoring by flow cytometric analysis of reticulocytes. Ann Hematol 2011;90: Feldschuh J, Enson Y. Prediction of the normal blood volume. Relation of blood volume to body habitus. Circulation 1977;56: Rother RP, Rollins SA, Mojcik CF, et al. Discovery and development of the complement inhibitor eculizumab for the treatment of paroxysmal nocturnal hemoglobinuria. Nat Biotechnol 2007;25: Dacie JV, Firth D. Blood transfusion in nocturnal haemoglobinuria. Br Med J 1943;1: Volume **, ** ** TRANSFUSION 5
6 WEINSTOCK ET AL. 15. Brecher ME, Taswell HF. Paroxysmal nocturnal hemoglobinuria and the transfusion of washed red cells. A myth revisited. Transfusion 1989;29: Klein HG, Anstee DJ. ABO, Lewis and P groups and Ii antigens. In: Klein HG, Anstee DJ, editors. Mollison s blood transfusion in clinical medicine. 11th ed. London: Blackwell Publishing Ltd.; p Risitano AM, Notaro R, Pascariello C, et al. The complement receptor 2/factor H fusion protein TT30 protects paroxysmal nocturnal hemoglobinuria erythrocytes from complement-mediated hemolysis and C3 fragment. Blood 2012;119: Hochsmann B, Leichtle R, von Zabern I, et al. Paroxysmal nocturnal haemoglobinuria treatment with eculizumab is associated with a positive direct antiglobulin test. Vox Sang 2012;102: Hillmen P, Muus P, Roth A, et al. Long-term safety and efficacy of sustained eculizumab treatment in patients with paroxysmal nocturnal haemoglobinuria. Br J Haematol 2013;162: Stewart ZA, Collins TE, Schlueter AJ, et al. Case report: eculizumab rescue of severe accelerated antibodymediated rejection after ABO-incompatible kidney transplant. Transplant Proc 2012;44: Biglarnia AR, Nilsson B, Nilsson T, et al. Prompt reversal of a severe complement activation by eculizumab in a patient undergoing intentional ABO-incompatible pancreas and kidney transplantation. Transpl Int 2011;24:e TRANSFUSION Volume **, ** **
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