Post-Babesiosis Warm Autoimmune Hemolytic Anemia
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1 The new england journal of medicine Original Article Post-Babesiosis Warm Autoimmune Hemolytic Anemia Ann E. Woolley, M.D., Mary W. Montgomery, M.D., William J. Savage, M.D., Ph.D., Maureen O. Achebe, M.D., Kathleen Dunford, B.S., Sarah Villeda, B.S., James H. Maguire, M.D., and Francisco M. Marty, M.D. ABSTRACT BACKGROUND Babesiosis, a tickborne zoonotic disease caused by intraerythrocytic protozoa of the genus babesia, is characterized by nonimmune hemolytic anemia that resolves with antimicrobial treatment and clearance of parasitemia. The development of warm-antibody autoimmune hemolytic anemia (also known as warm autoimmune hemolytic anemia [WAHA]) in patients with babesiosis has not previously been well described. METHODS After the observation of sporadic cases of WAHA that occurred after treatment of patients for babesiosis, we conducted a retrospective cohort study of all the patients with babesiosis who were cared for at our center from January 2009 through June Data on covariates of interest were extracted from the medical records, including any hematologic complications that occurred within 3 months after the diagnosis and treatment of babesiosis. From the Divisions of Infectious Diseases (A.E.W., M.W.M., K.D., S.V., J.H.M., F.M.M.), Transfusion Medicine (W.J.S.), and Hematology (M.O.A.), Brigham and Women s Hospital, Harvard Medical School (A.E.W., M.W.M., W.J.S., M.O.A., J.H.M., F.M.M.), and Dana Farber Cancer Institute (A.E.W., M.O.A., F.M.M.) all in Boston. Address reprint requests to Dr. Woolley at the Division of Infectious Diseases, Brigham and Women s Hospital, 75 Francis St., Boston, MA 02115, or at awoolley@ bwh. harvard. edu. N Engl J Med 2017;376: DOI: /NEJMoa Copyright 2017 Massachusetts Medical Society. RESULTS A total of 86 patients received a diagnosis of babesiosis during the 7.5-year study period; 18 of these patients were asplenic. WAHA developed in 6 patients 2 to 4 weeks after the diagnosis of babesiosis, by which time all the patients had had clinical and laboratory responses to antimicrobial treatment of babesiosis, including clearance of Babesia microti parasitemia. All 6 patients were asplenic (P<0.001) and had positive direct antiglobulin tests for IgG and complement component 3; warm autoantibodies were identified in all these patients. No alternative explanation for clinical hemolysis was found. WAHA required immunosuppressive treatment in 4 of the 6 patients. CONCLUSIONS We documented post-babesiosis WAHA in patients who did not have a history of autoimmunity; asplenic patients appeared to be particularly at risk. n engl j med 376;10 nejm.org March 9,
2 The new england journal of medicine A B Babesiosis is a tickborne zoonotic disease that is caused by intraerythrocytic protozoa of the genus babesia. In the northeastern and upper midwestern regions of the United States, where Babesia microti is endemic, the incidence of babesiosis has increased dramatically in the past 10 years, particularly in New England. 1,2 The severity of babesiosis varies from asymptomatic infection to life-threatening disease. The most common clinical presentation is a viral-like illness with fever and laboratory abnormalities including anemia. 3 Risk factors for the development of severe babesiosis include older age, asplenia, immunodeficiency due to malignant or nonmalignant disease, human immunodeficiency virus (HIV) infection, and immunosuppressive therapy, such as B-cell depletion caused by rituximab. 4-8 Patients with babesiosis frequently have clinical hemolysis. Intraerythrocytic protozoa replicate asexually and leave red cells to invade other erythrocytes by disrupting the cell membrane and lysing the cell. 1 Non immune-mediated hemolysis associated with babesiosis resolves with appropriate antimicrobial treatment and clearing of the parasitemia. Autoimmune hemolytic anemia, on the other hand, is caused by autoantibodies produced against the patient s own erythrocytes, which leads to premature elimination of these cells from the circulation. Warm-antibody autoimmune hemolytic anemia (also known as warm autoimmune hemolytic anemia [WAHA]) is a type of anemia that is frequently seen in patients who have lymphoproliferative disorders or autoimmune conditions or who use certain medications. 9 Autoimmune hemolytic anemia is associated with certain infections, including HIV 8 and malaria. 10 There have been sporadic cases reported of immune hemolysis complicating babesiosis in patients with ongoing parasitemia or a history of autoimmune hemolysis We present six cases of asplenic patients without previous autoimmune hemolytic anemia in whom WAHA developed 2 to 4 weeks after diagnosis of babesiosis despite antimicrobial treatment and resolution of B. microti parasitemia. Methods Figure 1. Peripheral-Blood Smear from Patient 6 with Post-Babesiosis Warm-Antibody Autoimmune Hemolytic Anemia. Panel A (Wright Giemsa stain) shows Babesia microti ring forms (arrowheads) from the day of diagnosis of babesiosis. Panel B (Wright Giemsa stain) shows evidence of warm-antibody autoimmune hemolytic anemia including polychromasia, nucleated red cells (arrow), and erythrophagocytosis (inset). In both panels, Howell Jolly bodies (asterisks) are indicative of asplenia. Study Cohort All the patients with a diagnosis of babesiosis who received care at Brigham and Women s Hospital between January 1, 2009, and June 30, 2016, were identified through the hospital Research Patient Data Registry and a review of parasitology laboratory records. The Partners HealthCare Human Research Committee approved this study and waived the requirement for written informed consent. 940 n engl j med 376;10 nejm.org March 9, 2017
3 Post-Babesiosis Warm Autoimmune Hemolytic Anemia Data on covariates of interest were extracted from the medical records, including patient demographic characteristics, underlying disease and coexisting conditions, level of B. microti parasitemia, antimicrobial treatment, transfusions of blood products, blood counts, and the results of blood-bank testing, including antibody screening, Coombs test (direct antiglobulin test), and antibody identification. We collected data on all hematologic complications and treatments that occurred in the ensuing 3 months after the diagnosis of babesiosis. Laboratory Assessments A warm was identified if the following standard criteria were met: antibody screening was positive; all cells on the red-cell panel were reactive with patient plasma, including autologous red cells; the direct antiglobulin test was positive; and eluate from patient red cells reacted with all cells tested. Clinical and Laboratory Standards Institute recommendations were followed for assessment of parasitemia: thick and thin blood smears were evaluated by examination of a minimum of 300 oil-immersion fields per blood film to determine the presence of babesia parasites. Results Babesiosis Cohort A total of 86 patients had a diagnosis of babesiosis during the 7.5-year period, with confirmation by blood smear (Fig. 1A) or polymerase-chainreaction (PCR) assay (Table 1). Of the 86 patients, 18 were asplenic. Blood-bank testing was performed in 20 patients (23%) after the diagnosis of babesiosis, and 12 (14%) had direct antiglobulin Table 1. Characteristics of Patients with Babesiosis Treated at Brigham and Women s Hospital from January 1, 2009, through June 30, Characteristic Total (N = 86) Post-Babesiosis WAHA (N = 6) No WAHA (N = 80) number (percent) Male sex 57 (66) 4 (67) 53 (66) Inpatient admission for babesiosis 68 (79) 6 (100) 62 (78) Asplenia 18 (21) 6 (100) 12 (15) Blood-product transfusion Within 90 days before diagnosis of babesiosis 8 (9) 1 (17) 7 (9) Within 2 wk after diagnosis of babesiosis 32 (37) 1 (17) 31 (39) Exchange transfusion for babesiosis 6 (7) 0 6 (8) Clinical follow-up after diagnosis of babesiosis 75 (87) 6 (100) 69 (86) Laboratory assessments 73 (85) 6 (100) 67 (84) Evidence of hemolysis 10 (12) 6 (100) 4 (5) Blood-bank testing Antibody screening performed 20 (23) 6 (100) 14 (18) Positive antibody screening 8 (9) 6 (100) 2 (2) DAT performed 12 (14) 6 (100) 6 (8) Positive DAT 9 (10) 6 (100) 3 (4) Warm 7 (8) 6 (100) 1 (1) WAHA denotes warm autoimmune hemolytic anemia. A total of 17 of the 18 splenectomized patients were hospitalized during the initial diagnosis of babesiosis. Direct antiglobulin testing (DAT) was performed at the discretion of the treating physician. n engl j med 376;10 nejm.org March 9,
4 The new england journal of medicine tests performed. Nine of 12 direct antiglobulin tests were positive. Seven asplenic patients had warm autoantibodies identified, 6 of whom had clinical post-babesiosis WAHA and no alternative or additional explanations for clinical hemolysis. Sentinel Case The sentinel case involved a 43-year-old woman who had undergone splenectomy for Hodgkin s lymphoma 15 years before the onset of babesiosis. She was hospitalized in 2009 with low-grade fevers and fatigue 2 weeks after receiving a tick bite. The level of B. microti parasitemia was 11%, and the hematocrit was 33%. Serologic tests for anaplasmosis, ehrlichiosis, and Lyme borreliosis were negative at that time. She was treated with azithromycin, atovaquone, and clindamycin. At discharge, the parasitemia level was 0.2% and the hematocrit was 34%. Four weeks after the diagnosis of babesiosis, the hematocrit declined to 25%, although no parasites were detected on smears. She had evidence of hemolysis with a lactate dehydrogenase (LDH) level of 773 U per liter, a reticulocyte count of 11%, and undetectable haptoglobin. Blood-bank testing was notable for a positive direct antiglobulin test for both IgG and complement component 3 (C3). A warm autoimmune antibody was identified. She received 4 weeks of prednisone treatment for WAHA, and antiparasitic treatment was continued for a total of 12 weeks because of uncertainty about the cause of her recrudescent hemolysis. The hemolysis resolved within 2 weeks after the initiation of prednisone. Cases of Post-Babesiosis WAHA Characteristics of the six cases of post-babesiosis WAHA are summarized in Table 2. Patients had various underlying medical conditions but no history of autoimmunity. All had undergone splenectomy, five at least 1 year before presentation. B. microti was confirmed by PCR assay, and the parasitemia level ranged from 2.5% to 11.8%. All the patients had clinical and laboratory responses to antimicrobial treatment. All six patients were hospitalized for the initial management of babesiosis, and one required intensive care for the acute respiratory distress syndrome and intracranial hemorrhage. None of the six patients had evidence of coinfection with anaplasmosis, ehrlichiosis, or Lyme borreliosis. At 2 to 4 weeks after diagnosis, acute anemia, characterized by an elevated mean corpuscular volume (MCV), reticulocytosis, an undetectable haptoglobin level, and an increased LDH level, developed in all six patients (Fig. 1B). Although B. microti PCR tests remained positive in five of the six cases, parasitemia was undetectable on smears in all the cases. Direct antiglobulin tests for IgG and C3 were positive, eluates were panreactive (panagglutinins) without any antigen specificity, and a warm was present. Only one patient had received a blood transfusion within 2 months before the development of WAHA. In one patient, idiopathic thrombocytopenic purpura developed in addition to WAHA (the Evans syndrome). The other five patients did not have additional autoimmune phenomena other than WAHA. The severity of WAHA varied, as did the medical management of the condition. Four of the six patients required immunosuppressive treatment. Three patients received glucocorticoids alone for 3 to 6 weeks, and one patient received prednisone for 5 months and cyclophosphamide for 8 months. WAHA resolved within a few weeks without intervention in two patients. In the three cases in which blood-bank testing was repeated, the time to a negative direct antiglobulin test ranged from 10 days to 5.5 months. An additional patient with a history of thalassemia major, previous splenectomy, and erythrocyte transfusions every 2 weeks had a weakly positive direct antiglobulin test result starting 4 weeks after the diagnosis of babesiosis, after the resolution of parasitemia on blood smear. A warm was not identified until 11 weeks after babesiosis was diagnosed. Given the confounding factors of chronic hemolytic anemia and frequent transfusion requirements, the contribution of the warm to her underlying clinical hemolysis could not be assessed; therefore, her case was not included among the cases of post-babesiosis WAHA. Risk Factors for Post-Babesiosis WAHA All the case patients had undergone splenectomy, as compared with 12 of the 80 patients in whom the syndrome did not develop (P<0.001 by Fisher s exact test). No patient with post-babesiosis WAHA underwent exchange transfusion for the treatment of babesiosis, whereas 6 of the 942 n engl j med 376;10 nejm.org March 9, 2017
5 Post-Babesiosis Warm Autoimmune Hemolytic Anemia Table 2. Clinical Characteristics of Patients with Babesiosis in Whom WAHA Developed. Characteristic Patient 1 Patient 2 Patient 3 Patient 4 Patient 5 Patient 6 Year of diagnosis Age (yr) Sex Female Male Female Male Male Male Underlying conditions Hodgkin s disease, 15 yr earlier; breast cancer, 1 yr earlier Time from splenectomy to diagnosis of babesiosis AML, allogeneic HSCT Gastric cancer Hereditary spherocytosis Previous trauma Metastatic pancreatic neuroendocrine tumor 15 yr 1 yr 1 mo 29 yr 36 yr 4 yr Peak Babesia microti parasitemia (%) Babesiosis treatment Agents Azithromycin, atovaquone, clindamycin Azithromycin, atovaquone Azithromycin, atovaquone Azithromycin, atovaquone Clindamycin and quinine, then atovaquone and azithromycin Azithromycin, atovaquone Duration (wk) Time from diagnosis of babesiosis to diagnosis of WAHA (wk) Hematocrit at diagnosis of babesiosis (%) Laboratory values at diagnosis of WAHA Hematocrit (%) MCV (fl) Reticulocyte count (%) Not assessed 37 Platelet count (per mm 3 ) 448, , , , ,000 48,000 Blood type A+ B+ O+ B+ O+ O Blood-bank testing confirming diagnosis of WAHA Treatment for WAHA Prednisone, 4 wk None Prednisone, 20 wk; cyclophosphamide, 32 wk Prednisone, 6 wk None Dexamethasone, 1 wk; prednisone, 3 wk Transfusion during WAHA No Yes No No No Yes Time to negative DAT Not assessed Not assessed 5.5 mo 2 wk Not assessed 10 days Relapse of babesiosis or WAHA No No No No No No Months of follow-up Ab denotes antibody, AHG antihuman globulin, AML acute myeloid leukemia, C3 complement component 3, HSCT hematopoietic stem-cell transplantation, and MCV mean corpuscular volume. Gastric cancer was fully resected at the time of the splenectomy without further evidence of metastatic disease. n engl j med 376;10 nejm.org March 9,
6 The new england journal of medicine other 80 patients in the cohort did undergo transfusion (P = 1.0); only 2 of the 18 splenectomized patients underwent exchange transfusion (P = 0.74). Discussion Persons who have undergone splenectomy are at higher risk for severe and relapsing babesiosis and, like other immunocompromised persons, typically receive longer courses of antiparasitic medications than otherwise healthy persons. 7 Although prolonged antimicrobial treatment may prevent relapsing babesiosis, the cases presented here show a unique syndrome of recrudescent clinical hemolysis 2 to 4 weeks after the initiation of antiparasitic treatment, in the absence of parasitemia on peripheral-blood smear. The post-babesiosis WAHA syndrome occurred in 7% of all the patients with babesiosis during the study period and in one third of asplenic patients. Although four patients required immunosuppressive treatment owing to the severity of their clinical hemolysis, there were no deaths as may occur in severe cases of autoimmune hemolytic anemia, especially when there are delays in the administration of immunosuppressive treatment or the transfusion of blood products. 15 We have described here a clinical syndrome of post-babesiosis WAHA in patients without a history of immune-mediated hemolysis. Although the development of autoimmunity to red cells in asplenic patients with babesiosis has been noted previously in seven cases, there was ongoing parasitemia in five of these cases at the time of positivity on direct antiglobulin tests In one of these cases, immune hemolysis developed in the context of transfusion-related alloantibodies. 11 Two of the seven patients had a history of autoimmune hemolytic anemia before acquiring babesiosis and subsequently had the Evans syndrome. 14 The cases in the current report are distinct in that WAHA developed despite the clearance of B. microti parasitemia, and none of the patients had a history of autoimmune hemolytic anemia. An asplenic patient recently received a diagnosis of post-babesiosis WAHA at Nantucket Cottage Hospital, Massachusetts, and has required immunosuppression with glucocorticoids and rituximab (Pearl D: personal communication). The infrequency of asplenia in the general population may explain why post-babesiosis WAHA had not been recognized previously in endemic areas. We considered alternative explanations for WAHA in our patients, but none seemed plausible. Although Hodgkin s lymphoma and acute myeloid leukemia are rarely associated with autoimmune hemolytic anemia, our two patients with these cancers were in remission at the time of presentation. The one patient in whom the syndrome developed 3 years after allogeneic stemcell transplantation had a self-limited course without the need for immunosuppression, making a graft-versus-host disease like phenomenon unlikely. Only one patient with the syndrome had received a transfusion in the 3 months before presentation, and no alloantibodies were detected. Drug-induced autoimmune hemolytic anemia is unlikely, because only one patient received quinine, 16 and autoimmune hemolytic anemia has not been associated with atovaquone, azithromycin, or clindamycin. 17 Although PCR testing for B. microti remained positive in five of the six cases at the time of the diagnosis of WAHA, there was no evidence of parasitemia on peripheral-blood smears. Microscopic examination of Giemsa-stained thick and thin blood smears has a detection limit of 10 to 100 parasites per microliter ( to 0.002% parasitemia), whereas PCR testing for B. microti lowers the limit of detection to 5 parasites per microliter (approximately % parasitemia). 18 Such a low parasite burden cannot clinically explain the degree of hemolytic anemia that developed in these patients at the time of the diagnosis of WAHA. A plausible mechanism for post-babesiosis WAHA in asplenic patients is immune-complex mediated, or type III, hypersensitivity. In type III hypersensitivity, the antibody response to foreign antigens leads to the overproduction of immunoglobulins and increased amounts of insoluble immune complexes. These immune complexes are removed inefficiently by phagocytosis, particularly in asplenic patients, and can trigger the classical complement cascade and intense release of inflammatory mediators and subsequent lysis of red cells. 19 In the absence of a spleen to maintain red-cell surfaces free of immune com- 944 n engl j med 376;10 nejm.org March 9, 2017
7 Post-Babesiosis Warm Autoimmune Hemolytic Anemia plexes, accumulation of these complexes may occur to a critical threshold, leading to clinically significant red-cell phagocytic clearance and complement-mediated destruction. 19 An alternative explanation for the development of post-babesiosis WAHA is antibody-mediated, or type II, hypersensitivity, in which cross-reacting antibodies initially elicited against B. microti antigens that have been adsorbed onto red cells are subsequently elicited against similar human antigens. Splenectomy would facilitate the persistence of these erythrocytic surface antigens, which otherwise would be removed rapidly by the spleen, and the subsequent development of autoreactive antibodies. The time needed to stimulate and accumulate autoreactive antibodies may account for the delay of a few weeks that we observed for the development of WAHA after the initial diagnosis of babesiosis. A postinfectious delayed autoimmune hemolytic anemia has also been described with malaria, 20 including in a few cases that occurred 1 to 4 weeks after the treatment of severe malaria with parenteral artesunate, by which time the patients had clinical improvement and resolution of parasitemia. 21,22 The pathogenesis of post-babesiosis WAHA seems distinct from that of autoimmune hemolytic anemia in general. Splenectomy is a treatment for autoimmune hemolytic anemia, whereas in this syndrome, asplenia is a risk factor. In addition, in typical autoimmune hemolytic anemia, direct binding of antibody or complement to red-cell membranes leads to clearance by reticuloendothelial system cells rather than immune-complex deposition on the surface of red cells. 23 In summary, the post-babesiosis WAHA syndrome can be a hematologic complication of babesiosis, and asplenic patients appear to be particularly at risk. Immune-mediated hemolysis and screening for WAHA should be considered in patients with worsening or recrudescent hemolytic anemia after treatment of babesiosis, especially in asplenic patients. Post-babesiosis WAHA responds to immunosuppressive treatment rather than antiparasitic treatment. Understanding the activation of the immune response to babesiosis may elucidate the mechanisms of other causes of autoimmune hemolytic anemias. Disclosure forms provided by the authors are available with the full text of this article at NEJM.org. We thank Tania Torres for her assistance in the blood-bank review of the cases presented and Sam Telford III, for his critical input and review of an earlier version of the manuscript. References 1. Vannier E, Krause PJ. Human babesiosis. N Engl J Med 2012; 366: Krause PJ, McKay K, Gadbaw J, et al. Increasing health burden of human babesiosis in endemic sites. Am J Trop Med Hyg 2003; 68: Vannier E, Gewurz BE, Krause PJ. Human babesiosis. Infect Dis Clin North Am 2008; 22: Rosner F, Zarrabi MH, Benach JL, Habicht GS. Babesiosis in splenectomized adults: review of 22 reported cases. Am J Med 1984; 76: White DJ, Talarico J, Chang HG, Birkhead GS, Heimberger T, Morse DL. Human babesiosis in New York State: review of 139 hospitalized cases and analysis of prognostic factors. Arch Intern Med 1998; 158: Hatcher JC, Greenberg PD, Antique J, Jimenez-Lucho VE. Severe babesiosis in Long Island: review of 34 cases and their complications. Clin Infect Dis 2001; 32: Krause PJ, Gewurz BE, Hill D, et al. Persistent and relapsing babesiosis in immunocompromised patients. Clin Infect Dis 2008; 46: Telen MJ, Roberts KB, Bartlett JA. HIV-associated autoimmune hemolytic anemia: report of a case and review of the literature. J Acquir Immune Defic Syndr 1990; 3: Gehrs BC, Friedberg RC. Autoimmune hemolytic anemia. Am J Hematol 2002; 69: Sonani R, Bhatnagar N, Maitrey G. Autoimmune hemolytic anemia in a patient with malaria. Asian J Transfus Sci 2013; 7: Wolf CF, Resnick G, Marsh WL, Benach J, Habicht G. Autoimmunity to red blood cells in babesiosis. Transfusion 1982; 22: Evenson DA, Perry E, Kloster B, Hurley R, Stroncek DF. Therapeutic apheresis for babesiosis. J Clin Apher 1998; 13: Herman JH, Ayache S, Olkowska D. Autoimmunity in transfusion babesiosis: a spectrum of clinical presentations. J Clin Apher 2010; 25: Shatzel JJ, Donohoe K, Chu NQ, et al. Profound autoimmune hemolysis and Evans syndrome in two asplenic patients with babesiosis. Transfusion 2015; 55: King KE, Ness PM. Treatment of autoimmune hemolytic anemia. Semin Hematol 2005; 42: Johnson ST, Fueger JT, Gottschall JL. One center s experience: the serology and drugs associated with drug-induced immune hemolytic anemia a new paradigm. Transfusion 2007; 47: Petz LD, Garratty G. Immune hemolytic anemias. 2nd ed. Philadelphia: Churchill Livingstone, Teal AE, Habura A, Ennis J, Keithly JS, Madison-Antenucci S. A new real-time PCR assay for improved detection of the parasite Babesia microti. J Clin Microbiol 2012; 50: Janeway CA, Travers P, Walport M, Shlomchik M. Immunobiology: the immune system in health and disease. 5th ed. New York: Garland, Abdalla S, Weatherall DJ. The direct n engl j med 376;10 nejm.org March 9,
8 Post-Babesiosis Warm Autoimmune Hemolytic Anemia antiglobulin test in P. falciparum malaria. Br J Haematol 1982; 51: Sharma V, Samant R, Hegde A, Bhaja K. Autoimmune hemolysis in malaria: a report of three cases. J Assoc Physicians India 2012; 60: Raffray L, Receveur MC, Beguet M, Lauroua P, Pistone T, Malvy D. Severe delayed autoimmune haemolytic anaemia following artesunate administration in severe malaria: a case report. Malar J 2014; 13: Berentsen S, Sundic T. Red blood cell destruction in autoimmune hemolytic anemia: role of complement and potential new targets for therapy. Biomed Res Int 2015; 2015: Copyright 2017 Massachusetts Medical Society. 946 n engl j med 376;10 nejm.org March 9, 2017
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