T-Cell Large Granular Lymphocyte Leukemia of Donor Origin After Allogeneic Bone Marrow Transplantation
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1 Hematopathology / T-CELL LARGE GRANULAR LYMPHOCYTE LEUKEMIA AFTER ALLOGENEIC BMT T-Cell Large Granular Lymphocyte Leukemia of Donor Origin After Allogeneic Bone Marrow Transplantation Wing Y. Au, MRCP, 1 Clarence C.K. Lam, MRCPath, 2 Albert K.W. Lie, FRCPA, 1 Annie Pang, 1 and Yok L. Kwong, FRCPath 1 Key Words: T-cell large granular lymphocyte leukemia; Allogeneic BMT; Bone marrow transplantation Abstract A 39-year-old man with chronic myeloid leukemia in accelerated phase underwent allogeneic bone marrow transplantation (BMT). At 6 months after BMT, lymphocytosis (WBC count, 23,1/µL [ /L]; 8% (.8) large granular lymphocytes [LGLs]) occurred. The LGLs were CD3+CD4 CD8+, with clonally rearranged T-cell receptor γ gene, and of donor origin, as shown by analysis of polymorphic microsatellite markers. Epstein-Barr virus was not present. The diagnosis, therefore, was consistent with T-cell large granular lymphocytic (T-LGL) leukemia. Corticosteroids controlled the LGL count, but progressive pancytopenia led to death 4 months later. Retrospective analysis showed that the T-LGL leukemia apparently had arisen as early as 3 months after BMT. The distinguishing features of this case included donor origin, neoplastic nature, and the aggressive fatal outcome. Large granular lymphocytes (LGLs) are medium to large lymphocytes with azurophilic granules in the cytoplasm. The majority are T cells that characteristically express CD3 and CD8 and probably represent cytotoxic T-cell populations. CD3+CD8+ T-cell LGLs normally account for less than 5% of peripheral blood lymphocytes. An increase in the LGL count may occur as a result of viral infections, autoimmune disorders, and, occasionally, underlying malignant neoplasms and lymphoproliferative disorders. 1 As the increase in the LGL count is reactive, it usually is asymptomatic, transient, and, more important, polyclonal. However, neoplastic proliferation of T-cell LGL also is a well-defined chronic T-cell lymphoproliferative disorder and is classified as T-cell large granular lymphocytic (T-LGL) leukemia in the World Health Organization classification of lymphoid malignant neoplasms. 2 T-LGL leukemia is a rare disease 1,2 characterized by persistently increased circulating T- cell LGLs with a typical immunophenotype (CD3+CD4 CD8+) and cytogenetic or molecular evidence of clonal T-cell lymphoproliferation. 1-3 Rare cases may show low LGL counts. 2 The disease usually is indolent and marked by neutropenia with recurrent infections, 3 although rare cases may be aggressive. 4 Pure red cell aplasia is the most common complication in Asian patients 5 and is recognized increasingly in western patients. 6 Expansion of T-cell LGLs after allogeneic bone marrow transplantation (BMT) has been described. 7,8 Notably, these T- cell LGL expansions were polyclonal or oligoclonal. A relationship with viral infections has been postulated. 7 Although T- cell LGL expansion after BMT might be asymptomatic, autoimmune manifestations and mild to severe suppression of hematopoiesis were encountered in other cases. 8 Owing to their nonclonal nature, these T-cell LGL expansions were 626 Am J Clin Pathol 23;12: Downloaded 626 from
2 Hematopathology / CASE REPORT nonprogressive and self-limiting. Furthermore, it has been reported that nonclonal T-cell LGL expansions might be associated with a lower rate of disease relapse after BMT. 7,8 We report a case of early onset T-cell LGL expansion of donor origin. The subsequent finding of clonal rearrangement of the T-cell receptor (TCR) γ gene and the aggressive and fatal clinical course showed that it was, in fact, a T-LGL leukemia of donor origin after allogeneic BMT. Materials and Methods Case History A 39-year-old man with chronic myeloid leukemia in accelerated phase received a myeloablative allogeneic BMT from a fully HLA-matched unrelated donor. Acute skin graft-vs-host disease (GVHD) developed after engraftment, which was treated with cyclosporine and mycophenolate mofetil. Three months after BMT, progressive shortness of breath developed due to bronchiolitis obliterans, which prevented tapering of the immunosuppressive therapy. Owing to the high doses of immunosuppressive agents (cyclosporine, 25 mg daily; mycophenolate mofetil, 1,5 mg daily), the results of polymerase chain reaction (PCR) for cytomegalovirus (CMV) and serum pp65 antigen also became positive, and treatment with ganciclovir became necessary. Subsequently, there were intermittent episodes of CMV reactivation, which were treated with ganciclovir, foscarnet, or both. At 6 months, there was a sudden resurgence of skin GVHD. A concomitant lymphocytosis developed, and laboratory results were as follows: hemoglobin concentration, 9.9 g/dl (99 g/l); WBC count, 23,1/µL ( /L; 8% [.8] lymphocytes); and platelet count, /µl ( /L). Subsequent examination of peripheral blood and bone marrow samples confirmed the diagnosis of T-LGL leukemia. Screening for autoimmune markers was negative. Oral corticosteroid therapy (prednisolone, 5 mg daily) was started for the skin GVHD. This led to a gradual subsidence of the skin rashes. At the same time, the lymphocytosis also responded, with a decrease of the WBC count to normal within 6 weeks of corticosteroid treatment. However, the blood cell count continued to deteriorate, and pancytopenia gradually developed. The cyclosporine and mycophenolate mofetil dosages were tapered, but the drugs could not be stopped owing to the ongoing bronchiolitis obliterans. Ten months after BMT, the patient was admitted because of severe shortness of breath; laboratory results were as follows: hemoglobin concentration, 9.1 g/dl (91 g/l); WBC count, 2,2/µL ( /L; 4% [.4] LGL); and platelet count, /µl (2 1 9 /L). Acute respiratory failure soon developed, requiring mechanical ventilation. The patient died of uncontrolled sepsis 2 weeks later. A postmortem lung biopsy showed extensive intraalveolar hemorrhage. Molecular Studies Donor-recipient DNA chimerism was studied by using semiquantitative PCR with fluorochrome-labeled primers for polymorphic microsatellite markers as described. 9 PCR for the TCR-γ gene and DNA sequencing was performed as reported. 1 The PCR has a sensitivity of 1 3. Reverse transcription PCR for bcr/abl was performed as described. 11 Results Histopathologic Features At 6 months, the peripheral blood showed 8% (.8) lymphocytes. Most of these were LGLs Image 1. Immunophenotyping by flow cytometry showed that 55% of the lymphocytes were CD3+CD8+CD56 Image 2. Examination of the bone marrow showed trilineage hematopoietic suppression. About 5% of the marrow nucleated cells were LGLs, which immunophenotyping revealed as CD3+CD8+. In situ hybridization for Epstein- Barr virus (EBV)-encoded RNA did not show positive cells (data not shown). Molecular Findings Analysis of donor-recipient DNA chimerism showed that the marrow (containing 5% LGLs) and peripheral blood (containing 8% [.8] LGLs) were exclusively of donor origin Image 3. The results, therefore, confirmed the donor origin of the T-cell LGLs. PCR for the TCR-γ gene showed a single rearrangement band at the time of T-cell LGL lymphocytosis (peripheral blood sample 6 months after BMT) Image 4. The rearrangement band became stronger around the time of death (in a bone marrow sample at 1 months), implying an increase in the size of the neoplastic clone. Sequencing of this band showed a clonal rearrangement of the TCR-γ gene Image 5. A retrospective analysis of all available samples from the patient before and after BMT showed that the neoplastic clone was first detectable in the peripheral blood 3 months after BMT, with progressive clonal expansion until death. Results for bcr/abl, however, remained negative in all samples (data not shown). Last, as this was an HLA-matched unrelated donor BMT, donor anonymity was observed. Therefore, it was not possible to determine whether the same T-cell clone might subsequently have developed in the donor as well. Downloaded from Am J Clin Pathol 23;12:
3 Au et al / T-CELL LARGE GRANULAR LYMPHOCYTE LEUKEMIA AFTER ALLOGENEIC BMT 1, 1 2 CD4 D , CD8 Image 1 T-cell large granular lymphocytic leukemia of donor origin after allogeneic bone marrow transplantation. A blood smear showed typical large granular lymphocytes (LGLs), with abundant pale cytoplasm possessing coarse granules. Note that the RBC next to the LGL showed a Howell-Jolly body, as the patient had a splenectomy for persistent symptomatic splenomegaly before the bone marrow transplantation (Wright stain, 1,). Discussion To our knowledge, this is the first documented case of donor-derived T-LGL leukemia after allogeneic BMT. Oligoclonal or polyclonal T-cell LGL expansion after BMT has been described, usually in response to CMV infection. 7,8 Interestingly, although the T-cell LGL expansion was nonclonal, a syndrome similar to de novo clonal T-LGL leukemia also might develop in some cases, 8 with clinical manifestations including hematopoietic suppression and autoimmune phenomena, such as polyarthritis, polyclonal hypergammaglobulinemia, and a positive antiglobulin test result. It is important to note, however, that these cases contained LGL expansions that were polyclonal and, therefore, did not represent T-LGL leukemia. However, the features that distinguished our case from T-cell LGL expansion after BMT were the clonal nature of the T-cell LGLs and the leukemic progression manifesting as worsening pancytopenia during the clinical course. The features thus were typical of de novo T-LGL leukemia in Asian patients, 5,12 in whom hematopoietic suppression is prominent, but autoimmune phenomena were absent. How the T-LGL leukemia was related to the BMT remains undefined. The pathogenetic mechanisms might be similar to nonclonal T-cell LGL expansion after BMT, which Image 2 Dual-color flow cytometric analysis showing a predominant population of CD4 CD8+ neoplastic cells in a case of T-cell large granular lymphocytic leukemia of donor origin after allogeneic bone marrow transplantation. Relative Fluorescence Units 3, 1,5 3, 1,5 4,2 2,1 4,2 2,1 Size of Alleles (base pairs) Donor Recipient Marrow (5% LGL) Peripheral blood (8% LGL) Image 3 Semiquantitative analysis of bone marrow and peripheral blood smear in a case of T-cell large granular lymphocytic (T-LGL) leukemia of donor origin after allogeneic bone marrow transplantation. The donor-specific allele is indicated by closed arrows and recipient-specific alleles by open arrows. With the development of T-LGL leukemia, the bone marrow and peripheral blood remained exclusively donor-derived. LGL, large granular lymphocyte. might be related to chronic antigenic stimulation due to GVHD or viral infection. In our case, additional genetic mutation(s) in these expanded T-cell LGLs might then lead to the formation of LGL leukemia. Indeed, this patient had active GVHD and repeated episodes of CMV infection. 628 Am J Clin Pathol 23;12: Downloaded 628 from
4 Hematopathology / CASE REPORT 118 bp 89 bp 72 bp M P N Image 4 Polymerase chain reaction for the T-cell receptor γ gene in a case of T-cell large granular lymphocytic leukemia of donor origin after allogeneic bone marrow transplantation (BMT). Lane M, molecular weight marker; lanes 16 to 1, time (mo) before and after allogeneic BMT; P, positive control sample from a case of T-cell acute lymphoblastic leukemia; N, normal DNA. A weak clonal band was visible at 3 months (peripheral blood) after BMT. The band became progressively stronger at 6 months (peripheral blood) and was obvious at 1 months (bone marrow) shortly before death. bp, base pairs. Furthermore, the first appearance of the neoplastic T-cell clone coincided with the occurrence of bronchiolitis obliterans and CMV infection. In this respect, it is intriguing to note that 3 cases of T-LGL leukemia have been reported after renal allografting, 13 in which the pathogenetic milieu might be similar. However, it must be noted that in such cases, the leukemia would be of recipient origin. Alternatively, this might represent a case of EBV-negative posttransplantation lymphoproliferative disease. 14 These disorders arise at a median of more than 2 years after organ allografting and mostly are diffuse large B-cell lymphomas. 14 As EBV is not found, it is unknown whether these lymphomas are mere chance associations, secondary to the effects of previous mutagenic drugs, or truly related to immunosuppression. Interestingly, in our case, the apparent onset of the neoplastic T-cell clone was at 3 months after allografting, which would, in fact, be typical of immunosuppression-related, EBV-positive posttransplantation lymphoproliferative disease. 14 So, it is likely that a combination of chronic antigenic stimulation related to GVHD or viral infection and immunosuppression with decreased immunosurveillance led to neoplastic transformation of a donor-derived T- cell population. Another possibility, although remote, is the transfer of a neoplastic T-cell clone from the donor to the recipient. The rare occurrence of inadvertent transfer of neoplastic cells from donors to recipients has been described after solid organ allografting. 15,16 In our case, this was unlikely because the donor was healthy and had normal blood cell counts, and the neoplastic T-cell clone was not detectable at engraftment of donor hematopoiesis 1 month after BMT. However, it would be useful if the donor also could be examined, particularly with PCR, to exclude the occult presence of a clonal LGL proliferation. Unfortunately, our institutional guidelines for HLA-matched unrelated donor BMT stipulate that donor anonymity must be maintained. Disclosure of identity is possible only when informed consent is obtained from the donor and the recipient, and disclosure should take place at least 1 year after transplantation. Both criteria were not met in our case. It is important, however, to note that different institutions may have different guidelines. Therefore, in similar situations in which the possibility exists that an occult disease might be present in an anonymous organ donor, the ethical issues of identity disclosure should be discussed thoroughly, in line with the institutional policies. Finally, this case has important clinical implications, notwithstanding the still unclear pathogenetic mechanism. The morphologic features of T-LGL leukemia are subtle. Furthermore, the pancytopenia accompanying T-LGL Image 5 DNA sequencing of the clonal band on polymerase chain reaction (PCR) for the T-cell receptor γ gene in a case of T-cell large granular lymphocytic leukemia of donor origin after allogeneic bone marrow transplantation. Vγ11 (purple) and Jγp (brown) were the forward and reverse primers for the PCR. For the 89-base-pair PCR product, the Vγ and Jγp sequences are shown in purple and brown respectively, while the N region is shown in black and boxed. The actual DNA sequencing result is shown above the VNJ junction. Downloaded from Am J Clin Pathol 23;12:
5 Au et al / T-CELL LARGE GRANULAR LYMPHOCYTE LEUKEMIA AFTER ALLOGENEIC BMT leukemia also can be found in other complications after BMT. Therefore, this disease might be missed very easily in the post-bmt setting. Physicians and hematopathologists, therefore, should be aware of this complication. Albeit rare, T-LGL leukemia might have to be considered when unexplained lymphocytosis or pancytopenia develops after BMT. This case also illustrates the rare occurrence of donorderived leukemia after allogeneic-bmt, 17 further underlining the importance of defining the donor or recipient origin of the neoplastic cells in malignant neoplasms that arise after allogeneic BMT. From the University Departments of 1 Medicine and 2 Pathology, Queen Mary Hospital, Hong Kong, People s Republic of China. Supported by the Kadoorie Charitable Foundation, Hong Kong. Address reprint requests to Dr Kwong: Dept of Medicine, University of Hong Kong, Professorial Block, Queen Mary Hospital, Pokfulam Rd, Hong Kong, People s Republic of China. References 1. Loughran TP Jr. Clonal diseases of large granular lymphocytes. Blood. 1993;82: Chan WC, Catovsky D, Focuar K, et al. T-cell large granular lymphocytic leukaemia. In: Jaffe ES, Harris NL, Stein H, et al, eds. Tumours of Haematopoietic and Lymphoid Tissues. Lyon, France: IARC Press; 21: World Health Organization Classification of Tumours. 3. Semenzato G, Zambello R, Starkebaum G, et al. The lymphoproliferative disease of granular lymphocytes: updated criteria for diagnosis. Blood. 1997;89: Lamy T, Bauer FA, Liu JH, et al. Clinicopathological features of aggressive large granular lymphocyte leukaemia resemble Fas ligand transgenic mice. Br J Haematol. 2;18: Kwong YL, Wong KF, Chan LC, et al. Large granular lymphocyte leukemia: a study of nine cases in a Chinese population. Am J Clin Pathol. 1995;13: Go RS, Li CY, Tefferi A, et al. Acquired pure red cell aplasia associated with lymphoproliferative disease of granular T lymphocytes. Blood. 21;98: Dolstra H, Preijers F, Van de Wiel-van Kemenade E, et al. Expansion of CD8+CD57+ T cells after allogeneic BMT is related with a low incidence of relapse and with cytomegalovirus infection. Br J Haematol. 1995;9: Mohty M, Faucher C, Vey N, et al. Features of large granular lymphocytes (LGL) expansion following allogeneic stem cell transplantation: a long-term analysis. Leukemia. 22;16: Au WY, Lie AK, Siu LL, et al. Therapy related myelodysplastic syndrome of recipient origin after allogeneic bone marrow transplantation for acute lymphoblastic leukemia. Br J Haematol. 21;112: Chim CS, Fung A, Shek TW, et al. Analysis of clonality in Kimura s disease. Am J Surg Pathol. 22;26: Au WY, Lie AK, Ma SK, et al. Tyrosine kinase inhibitor STI571 in the treatment of Philadelphia chromosome positive leukaemia failing myeloablative stem cell transplantation. Bone Marrow Transplant. 22;3: Kwong YL, Wong KF. Association of pure red cell aplasia with T large granular lymphocyte leukaemia. J Clin Pathol. 1998;51: Gentile TC, Hadlock KG, Uner AH, et al. Large granular lymphocyte leukaemia occurring after renal transplantation. Br J Haematol. 1998;11: Leblond V, Davi F, Charlotte F, et al. Posttransplant lymphoproliferative disorders not associated with Epstein-Barr virus: a distinct entity? J Clin Oncol. 1998;16: Loh E, Couch FJ, Hendricksen C, et al. Development of donor-derived prostate cancer in a recipient following orthotopic heart transplantation. JAMA. 1997;277: Stephens JK, Everson GT, Elliott CL, et al. Fatal transfer of malignant melanoma from multiorgan donor to four allograft recipients. Transplantation. 2;7: Au WY, Chan EC, Siu LL, et al. Leukaemic relapse of donor origin after allogeneic bone marrow transplantation from a donor who later developed bronchogenic carcinoma. Br J Haematol. 22;119: Am J Clin Pathol 23;12: Downloaded 63 from
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