Characterization and treatment of chronic active Epstein-Barr virus disease: a 28-year experience in the United States.

Chronic active EBV disease (CAEBV) is a lymphoproliferative disorder characterized by markedly elevated levels of antibody to EBV or EBV DNA in the blood and EBV RNA or protein in lymphocytes in tissues. We present our experience with CAEBV during the last 28 years, including the first 8 cases treated with hematopoietic stem cell transplantation in the United States. Most cases of CAEBV have been reported from Japan. Unlike CAEBV in Japan, where EBV is nearly always found in T or natural killer (NK) cells in tissues, EBV was usually detected in B cells in tissues from our patients. Most patients presented with lymphadenopathy and splenomegaly; fever, hepatitis, and pancytopenia were common. Most patients died of infection or progressive lymphoproliferation. Unlike cases reported from Japan, our patients often showed a progressive loss of B cells and hypogammaglobulinemia. Although patients with CAEBV from Japan have normal or increased numbers of NK cells, many of our patients had reduced NK-cell numbers. Although immunosuppressive agents, rituximab, autologous cytotoxic T cells, or cytotoxic chemotherapy often resulted in short-term remissions, they were not curative. Hematopoietic stem cell transplantation was often curative for CAEBV, even in patients with active lymphoproliferative disease that was unresponsive to chemotherapy. These studies are registered at http://www.clinicaltrials.gov as NCT00032513 for CAEBV, NCT00062868 and NCT00058812 for EBV-specific T-cell studies, and NCT00578539 for the hematopoietic stem cell transplantation protocol.

[1]  C. Bollard,et al.  Long-term remission in a child with refractory EBV+ hydroa vacciniforme-like T-cell lymphoma through sequential matched EBV+-related allogeneic hematopoietic SCT followed by donor-derived EBV-specific cytotoxic T-lymphocyte immunotherapy , 2011, Bone Marrow Transplantation.

[2]  W. Wilson,et al.  disease: a 28-year experience in the United States Characterization and treatment of chronic active Epstein-Barr virus , 2011 .

[3]  T. Okamura,et al.  Excellent outcome of allogeneic hematopoietic SCT with reduced-intensity conditioning for the treatment of chronic active EBV infection , 2011, Bone Marrow Transplantation.

[4]  S. Calattini,et al.  Detection of EBV genomes in plasmablasts/plasma cells and non-B cells in the blood of most patients with EBV lymphoproliferative disorders by using Immuno-FISH. , 2010, Blood.

[5]  Hao Liu,et al.  Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. , 2010, Blood.

[6]  Y. Nishiyama,et al.  Quantitative analysis of Epstein-Barr virus (EBV)-related gene expression in patients with chronic active EBV infection. , 2010, The Journal of general virology.

[7]  E. Jaffe,et al.  Epstein-Barr virus-associated lymphoproliferative disease in non-immunocompromised hosts: a status report and summary of an international meeting, 8-9 September 2008. , 2009, Annals of oncology : official journal of the European Society for Medical Oncology.

[8]  T. Pierson,et al.  Human antibody titers to Epstein-Barr Virus (EBV) gp350 correlate with neutralization of infectivity better than antibody titers to EBV gp42 using a rapid flow cytometry-based EBV neutralization assay. , 2009, Virology.

[9]  O. Arisaka,et al.  Chronic active Epstein–Barr virus infection with mosquito allergy successfully treated with reduced‐intensity unrelated allogeneic bone marrow transplantation in a boy , 2009, Pediatric transplantation.

[10]  K. Kawa,et al.  Allogeneic hematopoietic stem cell transplantation for Epstein–Barr virus‐associated T/natural killer‐cell lymphoproliferative disease in Japan , 2008, American journal of hematology.

[11]  K. Yamaguchi,et al.  Two cases of chronic active Epstein–Barr virus infection in which EBV‐specific cytotoxic T lymphocyte was induced after allogeneic bone marrow transplantation , 2008, Pediatric transplantation.

[12]  D. de Jong,et al.  Poor outcomes of chronic active Epstein-Barr virus infection and hemophagocytic lymphohistiocytosis in non-Japanese adult patients. , 2008, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[13]  S. Kojima,et al.  Clinical and virological characteristics of 15 patients with chronic active Epstein-Barr virus infection treated with hematopoietic stem cell transplantation. , 2008, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[14]  Chung-Che Chang,et al.  Complete responses of relapsed lymphoma following genetic modification of tumor-antigen presenting cells and T-lymphocyte transfer. , 2007, Blood.

[15]  M. Asaka,et al.  Successful Reduced-Intensity Stem Cell Transplantation With Cord Blood for a Poor-Prognosis Adult with Refractory Chronic Active Epstein-Barr Virus Infection , 2007, International journal of hematology.

[16]  T. Ariga,et al.  Successful report of reduced-intensity stem cell transplantation from unrelated umbilical cord blood in a girl with chronic active Epstein-Barr virus infection. , 2006, Journal of pediatric hematology/oncology.

[17]  H. Kimura [Chronic active EBV infection]. , 2006, Nihon rinsho. Japanese journal of clinical medicine.

[18]  H. Takada,et al.  Successful umbilical cord blood transplantation for severe chronic active Epstein‐Barr virus infection after the double failure of hematopoietic stem cell transplantation , 2005, American journal of hematology.

[19]  H. Kanegane,et al.  Proposed guidelines for diagnosing chronic active Epstein‐Barr virus infection , 2005, American journal of hematology.

[20]  S. Kojima,et al.  Differences between T cell-type and natural killer cell-type chronic active Epstein-Barr virus infection. , 2005, The Journal of infectious diseases.

[21]  T. Tsurumi,et al.  Quantitative analysis of Epstein-Barr virus (EBV)-specific CD8+ T cells in patients with chronic active EBV infection. , 2004, The Journal of infectious diseases.

[22]  C. Nakaseko,et al.  Successful control of Epstein–Barr virus (EBV)‐infected cells by allogeneic nonmyeloablative stem cell transplantation in a patient with the lethal form of chronic active EBV infection , 2004, American journal of hematology.

[23]  敬世 河,et al.  Reduced intensity stem cell transplantationを施行した慢性活動性EBウイルス感染症 , 2004 .

[24]  E. Jaffe,et al.  Chronic active Epstein-Barr virus infection associated with mutations in perforin that impair its maturation. , 2004, Blood.

[25]  K. Ohta,et al.  A case of a long‐time survivor with chronic active Epstein–Barr virus infection , 2004, European journal of haematology.

[26]  K. Kawa,et al.  [Chronic active Epstein-Barr virus infection treated with reduced intensity stem cell transplantation]. , 2004, [Rinsho ketsueki] The Japanese journal of clinical hematology.

[27]  S. Kato,et al.  Complete resolution of severe chronic active Epstein–Barr virus infection by cultured, activated donor T lymphocyte infusion after nonmyeloablative stem cells allografting , 2003, Bone Marrow Transplantation.

[28]  S. Asano,et al.  Successful treatment of natural killer (NK) cell leukemia following a long-standing chronic active Epstein–Barr virus (CAEBV) infection with allogeneic bone marrow transplantation , 2003, Bone Marrow Transplantation.

[29]  H. Kanegane,et al.  Prognostic factors for chronic active Epstein-Barr virus infection. , 2003, The Journal of infectious diseases.

[30]  T. Okamura,et al.  Unrelated bone marrow transplantation for Epstein–Barr virus-associated T/NK-cell lymphoproliferative disease , 2003, Bone Marrow Transplantation.

[31]  James F. Jones,et al.  Autologous Epstein-Barr virus (EBV)-specific cytotoxic T cells for the treatment of persistent active EBV infection. , 2002, Blood.

[32]  R. Hanada,et al.  Chronic active Epstein–Barr virus infection (CAEBV) successfully treated with allogeneic peripheral blood stem cell transplantation , 2002, Bone Marrow Transplantation.

[33]  T. Okamura,et al.  [CD34+ progenitor cell transplantation from HLA-mismatched donors to two patients with chronic active Epstein-Barr virus infection]. , 2001, [Rinsho ketsueki] The Japanese journal of clinical hematology.

[34]  Zhensheng Liu,et al.  Generation of autologous Epstein-Barr virus-specific cytotoxic T cells for adoptive immunotherapy in solid organ transplant recipients. , 2001, Transplantation.

[35]  H. Kanegane,et al.  Clinical and virologic characteristics of chronic active Epstein-Barr virus infection. , 2001, Blood.

[36]  H. Takada,et al.  Epstein-Barr virus (EBV) load and cytokine gene expression in activated T cells of chronic active EBV infection. , 2000, The Journal of infectious diseases.

[37]  K. Takenaka,et al.  Allogeneic peripheral blood stem cell transplantation for the treatment of chronic active Epstein–Barr virus infection , 2000, Bone Marrow Transplantation.

[38]  E. Jaffe,et al.  Fulminant EBV+ T-cell lymphoproliferative disorder following acute/chronic EBV infection: a distinct clinicopathologic syndrome , 2000 .

[39]  T. Okamura,et al.  Blood stem-cell transplantation for chronic active Epstein-Barr virus with lymphoproliferation. , 2000, The Lancet.

[40]  E. Jaffe,et al.  Fulminant EBV(+) T-cell lymphoproliferative disorder following acute/chronic EBV infection: a distinct clinicopathologic syndrome. , 2000, Blood.

[41]  J. Henter,et al.  Effective control of Epstein-Barr virus-related hemophagocytic lymphohistiocytosis with immunochemotherapy. Histiocyte Society. , 1999, Blood.

[42]  H. Takada,et al.  Interferon-α Therapy for Chronic Active Epstein‐Barr Virus Infection: Potential Effect on the Development of T‐Lymphoproliferative Disease , 1998, Journal of pediatric hematology/oncology.

[43]  J. Bell,et al.  Large clonal expansions of CD8+ T cells in acute infectious mononucleosis , 1996, Nature Medicine.

[44]  T. Morishima,et al.  Establishment of anti‐Epstein–Barr virus (EBV) cellular immunity by adoptive transfer of virus‐specific cytotoxic T lymphocytes from an HLA‐matched sibling to a patient with severe chronic active EBV infection , 1996, Clinical and experimental immunology.

[45]  G. Storch,et al.  EPSTEIN‐BARR VIRUS DNA IN PERIPHERAL BLOOD LEUKOCYTES OF PATIENTS WITH POSTTRANSPLANT LYMPHOPROLIFERATIVE DISEASE , 1995, Transplantation.

[46]  M. Fujieda,et al.  Defective activity of Epstein‐Barr virus (EBV) specific cytotoxic T lymphocytes in children with chronic active EBV infection and in their parents , 1993, Acta paediatrica Japonica : Overseas edition.

[47]  S. Straus Acute progressive Epstein-Barr virus infections. , 1992, Annual review of medicine.

[48]  Y. Sakiyama,et al.  Severe chronic active Epstein-Barr virus infection syndrome , 1991, Clinical Microbiology Reviews.

[49]  Y. Monczak,et al.  Brief report: Killer cell defect and persistent immunological abnormalities in two patients with chronic active epstein‐barr virus infection , 1989, Journal of medical virology.

[50]  M. Fujieda,et al.  Defective killer cell activity in patients with chronic active Epstein-Barr virus infection. , 1988, Acta medica Okayama.

[51]  A. Tawa,et al.  SUCCESSFUL TREATMENT OF CHRONIC ACTIVE EPSTEIN-BARR VIRUS INFECTION WITH RECOMBINANT INTERLEUKIN-2 , 1987, The Lancet.

[52]  R. Schooley,et al.  Chronic Epstein-Barr virus infection associated with fever and interstitial pneumonitis. Clinical and serologic features and response to antiviral chemotherapy. , 1986, Annals of internal medicine.

[53]  D. Zych,et al.  The Kviem controversy. , 1972, Lancet.