Case Report Successful treatment of polymorphic post-transplant lymphoproliferative disorder after allo-hsct with reduction of immunosuppression
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1 Int J Clin Exp Med 2014;7(7): /ISSN: /IJCEM Case Report Successful treatment of polymorphic post-transplant lymphoproliferative disorder after allo-hsct with reduction of immunosuppression Zhenyang Gu, Bo Cai, Lei Yuan, Honghua Li, Wenrong Huang, Yu Jing, Haiyan Zhu, Yu Zhao, Jian Bo, Quanshun Wang, Xiaoping Han, Li Yu, Chunji Gao Department of Hematology, Division of Internal Medicine, Chinese PLA General Hospital, Beijing, China Received February 9, 2014; Accepted April 23, 2014; Epub July 15, 2014; Published July 30, 2014 Abstract: Post-transplant lymphoproliferative disorder (PTLD) is a life-threatening complication for recipients of solid organ transplantation (SOT) and allogeneic hematopoietic stem cell transplantation (allo-hsct). In SOT recipients, who previously have a normal immune system that has been immunosuppressed, reduction of immunosuppression (RI) shows favorable outcome. However, in HSCT recipients, who have been profoundly immunosuppressed and for whom the tempo of immune reconstitution cannot be fast enough to eliminate the lymphoproliferative process, RI is ineffective in most patients. Therefore, cases of tumor regression via RI alone are rare in the setting of HSCT. We present a case of 26-year-old female developing a polymorphic B-cell PTLD 4 months after receiving allo-hsct for T cell lymphoblastic lymphoma. RI alone led to regression of the nasopharyngeal tumor, and no sign or evidence of graft-versus-host disease (GVHD) after RI was observed. The general condition of this patient was quite well just before we submitted our draft. To our knowledge, this is the first case that tumor of PTLD regressed upon RI alone with a favorable prognosis and without any evidence of GVHD and relapse of PTLD after RI therapy in the setting of HSCT, which justify the possible advantage of RI alone for low-risk patients. Keywords: Post-transplant lymphoproliferative disorder, hematopoietic stem cell transplantation, reduction of immunosuppression, T cell lymphoblastic lymphoma Introduction Post-transplant lymphoproliferative disorder (PTLD) is a life-threatening disease which consists of a heterogeneous group of diseases ranging from polyclonal hyperplasia to aggressive lymphoma in recipients of solid organ transplantation (SOT) and hematopoietic stem cell transplantation (HSCT) [1]. According to the WHO classification, PTLD comprises four major categories: early lesions, polymorphic PTLD, monomorphic PTLD, and classical Hodgkin lymphoma. Risk factors for the development of a PTLD after HSCT include the degree of HLAmismatch between donor and recipient, manipulation of the graft to deplete T cells, and the degree and duration of immunosuppression used to prevent and treat graft-versus-host disease (GVHD) [1]. Approximately 1% of patients undergoing allo-hsct could develop PTLD, and the incidence rate can increase to high levels among patients with risk factors [2]. The pathogenesis of PTLD in most patients is thought to be sustained by Epstein-Barr virus (EBV)-driven B-lymphocyte proliferation in the setting of immunosuppression, in which EBV-specific T-cell-mediated immunity is impaired, although EBV-negative cases of PTLD have also been described [1, 3, 4]. Current modalities for treatment of EBV-positive PTLD include reduction of immunosuppression (RI), chemotherapy, anti- CD20 monoclonal antibody (rituximab), antiviral drugs, and infusion of EBV-specific cytotoxic T lymphocytes (CTLs). However, no standard treatment had been established to date. RI is a primary treatment for PTLD in recipients of SOT whose immune system is previously normal [5]. In contrast, for HSCT recipients whose immune system has been previously destroyed by the conditioning regimen, RI therapy fails to bring about favorable results. Cases of tumor
2 Figure 1. A: Nasopharyngeal CT showed the mass on the right side of the nasopharyngeal posterior wall at the time of diagnosis; B: The nasopharyngeal CT performed 55 days later showed a complete disappearance of the tumor mass regression through RI therapy alone are rare in the setting of HSCT. Here we present a case of 26-year-old female who developed a polymorphic PTLD 4 months after receiving allo-hsct for T cell lymphoblastic lymphoma. Upon RI alone, her PTLD lesions regressed and her general condition was well just before we submitted our draft. To our knowledge, this is the first description that PTLD after HSCT regressed with a better prognosis and without any evidence of GVHD and relapse of PTLD following RI therapy. Case report A 26-year-old woman, complaining of cough, chest tightness, and chest pain, was admitted to our hospital on October 23, She also complained of night sweats and weight loss. Her chest X-ray revealed a mediastinal mass and bilateral pleural effusion. CT scan showed a huge mass in the anterior-superior mediastinum, pericardial invasion, and bilateral pleural effusion. CT-guided mediastinal mass biopsy and immunohistochemistry staining revealed homogeneous small tumor cells with Syn negative, CD3 positive, CD20 negative, CD99 positive, Ki-67 positive, TDT positive, CK negative, and PAX-5 negative. A diagnosis of T-lymphoblastic lymphoma at stage IVB (Binet stage) was made. A CHOP regimen of decreased dose was given considering the high risk of tumor lysis syndrome on October 30, Subsequently, Hyper-CAVD, HD-MTX+Ara-C, then a second Hyper CAVD, MTX alone and a third Hyper CAVD chemotherapy were given. Despite no signs of central nervous systematic infiltration, three prophylactic chemotherapies were intrathecally performed during the series of systematic chemotherapy. Complete remission was achieved after the 6th chemotherapy. Then in order to make time for transplantation, maintenance chemotherapy of low dosage was started with methotrexate. Nine months after the initial diagnosis, unrelated donor peripheral blood stem cell transplantation (PBSCT) was performed for this patient. Donor was searched from China Marrow Donor Program. High resolution HLA typing showed B, C, DQB1 matched and A, DRB1 mismatch. The conditioning regimen consisted of 10 Gy total body irritation in 2 fractions with shielding of the lungs (7.5 Gy), cyclophosphamide 60 mg/kg/day for 2 days and Anti-thymocyte globulin 2.5 mg/kg/day for 4 days. GVHD prophylaxis consisted of cyclosporin A, MTX and MMF (mycophenolate mofetil). The dose of infused CD34 positive cells was /kg. Although no severe early complications were noted, the patient experienced sore throat, epigastric pain and intermittent diarrhea. A combination of antibiotics, G-CSF and intermittent platelet and red blood cell transfusions were used during severe neutropenia Int J Clin Exp Med 2014;7(7):
3 Figure 2. Pathological findings. (A) The hematoxylin and eosin (HE)-stained biopsy specimen revealed he lamina propria of nasopharyngeal mucosal tissues was diffusely infiltrated by small, medium, large atypical lymphocytes ( 400); (B and C) Immunohistochemistry for the lymphocyte markers CD3Ab (B, 400) and CD20Ab (C, 400) shows the cell phenotype of the large scattered atypical cells; (D) In situ hybridization for Epstein-Barr virus (EBV)- encoded RNA (EBER) showed many positive cells ( 100). Granulocyte and thrombocyte engraftment were achieved on the 11th and 34th day, respectively. She was noted to have systemic skin rashes on the 27th day post transplantation. Skin biopsy confirmed the diagnosis of acute skin GVHD (grading 3, staging II). Methylprednisolone 80 mg/day was administrated intravenously, and steadily tapered until discontinuation when the signs of acute GVHD disappeared. During the 5th month after HSCT, she gradually felt pharyngeal foreign body sensation and pharyngeal discomfort. 18F-FDG PET/CT performed on December 1, 2009 revealed a metabolically active soft tissue mass on the right side of the nasopharyngeal posterior wall (Figure 1A). She was admitted again to hospital due to suspicion of being involved into PTLD or relapse of lymphoma on December 6, Therefore, we adjusted the dosage of cyclosporine to 50 mg/day. Nasopharyngeal mass biopsy was performed, and histopathology revealed that the lamina propria of nasopharyngeal mucosal tissues was diffusely infiltrated by atypical lymphocytes. Immunohistochemical analysis showed that the vast majority of atypical lymphocytes were positive for CD45RO, CD3, CD20, and EBER (Figure 2). Scattered lymphocytes were positive for CD5, CD38, CD99, CD138, TIA-1, and Ki-67 (focal exceeding 50%). All these cells were negative for CD10, CD1a, TDT, Grazyme B, and CK. Polymorphic PTLD was confirmed. Thus cyclosporine was steadily tapered till stopped. CT scan performed on January 27, 2010 demonstrated the disappearance of the nasopharyngeal mass (Figure 1B). No evidence of GVHD and signs of her lymphoma were detected after RI therapy. And she was still alive just before we submitted our manuscript Int J Clin Exp Med 2014;7(7):
4 Discussion PTLD is a relatively uncommon but life-threatening complication following HSCT. PTLD after HSCT usually appeared as disseminated disease with early and rapid organ dysfunction resulting in a fulminant clinical course with poor outcomes. For this reason, PTLD could be fatal if not treated at an early stage [6]. Nevertheless, several treatments for EBV PTLD have been developed, including RI, chemotherapy, antiviral drugs, anti-cd20 monoclonal antibody (rituximab), donor leukocyte infusion (DLI), and infusion of EBV-specific CTLs. The optimal treatment is controversial since no randomized trial for PTLD has been performed [7, 8]. More than 90 percent of adults are infected with EBV virus, and EBV-specific cytotoxic T-cells control EBV infection with the virus lurking in memory B cells, leading to the lifelong asymptomatic virus persistence throughout life [9]. However, in the setting of immunosuppression in recipients of either SOT or HSCT, the situation could change, resulting in viral reactivation and proliferation of EBV-infected B-lymphocytes and the development of PTLD [10]. Thus we can either target the infected B cells with monoclonal antibodies or chemotherapy, or boost the immune response to EBV by RI, DLI or infusing CTLs. Here we mainly focus on the RI therapy. In PTLD patients of SOT, RI has been proved to be effective, and is currently the fundamental therapy [5]. However, in PTLD patients after HSCT, who has been profoundly immunosuppressed and the tempo of immune reconstitution cannot be fast enough to eliminate the lymphoproliferative process [5, 11], RI therapy alone is therefore ineffective in most patients. Despite the mounting evidence of the efficacy of this approach in treating PTLD, it also carries the risk of inducing or exacerbating graft rejection and GVHD. Thus clinicians should carefully modulate the intensity of immunosuppression and closely monitor the function of allografts [12]. Here in our present case, the nasopharyngeal tumor regressed upon RI therapy alone, and the general condition of this patient is quite well without any evidence of GVHD after RI therapy. Although cases of regression of PTLD upon RI therapy have been described previously [13-16], nearly all the prognosis was poor. To our knowledge, this is the first description that the tumor of PTLD regressed upon RI alone with favorable prognosis and without any evidence of GVHD and relapse of PTLD after RI therapy in the setting of HSCT. With the advent of more effective treatment options, the morbidity and mortality of PTLD in HSCT recipients decreased sharply. Perhaps the most controversial question with PTLD is not only how but also when to treat. For HSCT recipients, four major risk factors have been well defined: (1) T-cell depletion(in vivo or in vitro); (2) unrelated or 2 HLA-antigen mismatched related donor; (3) use of antithymocyte globulin; and (4) the degree and duration of immunosuppression used to prevent and treat graft-versus-host disease [1, 2]. The cumulative incidence rates of PTLD can increase with the number of risk factors [2]. Based on the number of risk factors of PTLD, HSCT recipients can be classified into the low risk group ( 2 factors) and the high risk group ( 3 risk factors). For the high risk patients, we d better reserve preemptive treatments based on the combination of EBV DNA and T cell reconstitution [17], and choose aggressive treatments if these high risk patients were further diagnosed with PTLD. For the low risk group, the incidence rate of PTLD is approximately 1% [2], and there is no need to perform preemptive strategies [17]. The next question is how to treat the PTLD patients out of the low-risk groups. If the general condition of a patient is not life-threatening and the patient has a low risk of developing or exacerbating GVHD, we should first consider RI therapy to restore immune function. If a significant response is not achieved with reduction of immunosuppression or the general condition of the patient continues to deteriorate, we should perform more aggressive treatment options [18]. However, in the early stage after HSCT, the RI therapy alone may not be effective enough to restore the immune system against EBV, as patient s immune system may have not been reconstituted completely [5]. This can be evidenced by the fact that incidence rates for PTLD peak at 2-3 months after allo-hsct, and then decline sharply with increasing time since transplantation [2]. Thus, it is reasonable to monitor immune reconstitution to decide whether to perform further therapy or remain the RI therapy alone. Ideally, we should measure EBV-specific immunity directly. Unfor Int J Clin Exp Med 2014;7(7):
5 tunately, EBV-specific immunity assay is not routinely available commercially. However, we can simply use flow cytometry to evaluate T cell reconstitution, which is illustrated in Austen s study [17]. If T cell immunity has recovered, there is a chance to eradicate PTLD spontaneously simply by reduction of immunosuppression alone. If T cell reconstitution is poor and the disease progresses, additional strategies are needed. As in our patient, considering her relatively mild clinical symptom, we performed RI therapy alone and the patient nasopharyngeal mass regressed. And if we had conducted flow cytometry to evaluate the T cell reconstitution, it can better justify why we didn t perform addition strategies. With this strategy, we could avoid overtreatment and the related risk of complications in low-risk patients [19]. However, this is just a strategy, and further prospective clinical studies are needed to check the real value of this strategy. In conclusion, the strategies of managing PTLD are varied, and we still lack the standard criteria for how to treat PTLD. RI therapy alone shows favorable clinical efficacy in our patient. Monitoring T cell reconstitution of PTLD patients out of low-risk groups could offer us reasonable evidence, which helps us to decide whether to perform further therapy or remain the RI therapy alone. Acknowledgements This work was supported by the fund from NSFC (National Natural Science Foundations of China) (No , and No ). Disclosure of conflict of interest None. Address correspondence to: Dr. Chunji Gao, Department of Hematology, Division of Internal Medicine, Chinese PLA General Hospital, Fuxing Road 28, Haidian District, Beijing, China Tel: (010) ; Fax: (010) ; gaochunji@hotmail.com References [1] Gottschalk S, Rooney CM and Heslop HE. Posttransplant lymphoproliferative disorders. Annu Rev Med 2005; 56: [2] Curtis RE, Travis LB, Rowlings PA, Socie G, Kingma DW, Banks PM, Jaffe ES, Sale GE, Horowitz MM, Witherspoon RP, Shriner DA, Weisdorf DJ, Kolb HJ, Sullivan KM, Sobocinski KA, Gale RP, Hoover RN, Fraumeni JF Jr and Deeg HJ. Risk of lymphoproliferative disorders after bone marrow transplantation: a multi-institutional study. Blood 1999; 94: [3] Cohen JI. Epstein-Barr virus infection. N Engl J Med 2000; 343: [4] Williams H and Crawford DH. Epstein-Barr virus: the impact of scientific advances on clinical practice. Blood 2006; 107: [5] Heslop HE. How I treat EBV lymphoproliferation. Blood 2009; 114: [6] Gross TG, Steinbuch M, DeFor T, Shapiro RS, McGlave P, Ramsay NK, Wagner JE and Filipovich AH. B cell lymphoproliferative disorders following hematopoietic stem cell transplantation: risk factors, treatment and outcome. Bone Marrow Transplant 1999; 23: [7] Loren AW, Porter DL, Stadtmauer EA and Tsai DE. Post-transplant lymphoproliferative disorder: a review. Bone Marrow Transplant 2003; 31: [8] Green M and Webber S. Posttransplantation lymphoproliferative disorders. Pediatr Clin North Am 2003; 50: [9] Thorley-Lawson DA and Gross A. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med 2004; 350: [10] List AF, Greco FA and Vogler LB. Lymphoproliferative diseases in immunocompromised hosts: the role of Epstein-Barr virus. J Clin Oncol 1987; 5: [11] Styczynski J, Reusser P, Einsele H, de la Camara R, Cordonnier C, Ward KN, Ljungman P, Engelhard D; Second European Conference on Infections in Leukemia. Management of HSV, VZV and EBV infections in patients with hematological malignancies and after SCT: guidelines from the Second European Conference on Infections in Leukemia. Bone Marrow Transplant 2009; 43: [12] Cesaro S, Pegoraro A, Tridello G, Calore E, Pillon M, Varotto S, Abate D, Barzon L, Mengoli C, Carli M and Messina C. A prospective study on modulation of immunosuppression for Epstein-Barr virus reactivation in pediatric patients who underwent unrelated hematopoietic stem-cell transplantation. Transplantation 2010; 89: [13] Starzl TE, Nalesnik MA, Porter KA, Ho M, Iwatsuki S, Griffith BP, Rosenthal JT, Hakala TR, Shaw BW Jr, Hardesty RL, et al. Reversibility of lymphomas and lymphoproliferative lesions developing under cyclosporin-steroid therapy. Lancet 1984; 1: [14] Chiu LS, Choi PC, Luk NM, Chang M and Tang WY. Spontaneous regression of primary cuta Int J Clin Exp Med 2014;7(7):
6 neous Epstein-Barr virus-positive, CD30-positive anaplastic large T-cell lymphoma in a heart-transplant recipient. Clin Exp Dermatol 2009; 34: e [15] Krenauer A, Moll A, Ponisch W, Schmitz N, Niedobitek G, Niederwieser D and Aigner T. EBVassociated post-transplantation B-cell lymphoproliferative disorder following allogenic stem cell transplantation for acute lymphoblastic leukaemia: tumor regression after reduction of immunosuppression--a case report. Diagn Pathol 2010; 5: 21. [16] Minauchi K, Koizumi K, Kondo M, Takigami M, Harada H, Fujita H and Mukai M. [Remission induced by dose-reduction of immunosuppressants alone in a patient with post-transplant lymphoproliferative disorder of central nervous system origin]. Rinsho Ketsueki 2011; 52: [17] Worth A, Conyers R, Cohen J, Jagani M, Chiesa R, Rao K, Goulden N, Veys P and Amrolia PJ. Pre-emptive rituximab based on viraemia and T cell reconstitution: a highly effective strategy for the prevention of Epstein-Barr virus-associated lymphoproliferative disease following stem cell transplantation. Br J Haematol 2011; 155: [18] Lieberman F, Yazbeck V, Raptis A, Felgar R and Boyiadzis M. Primary central nervous system post-transplant lymphoproliferative disorders following allogeneic hematopoietic stem cell transplantation. J Neurooncol 2012; 107: [19] Reshef R, Vardhanabhuti S, Luskin MR, Heitjan DF, Hadjiliadis D, Goral S, Krok KL, Goldberg LR, Porter DL, Stadtmauer EA and Tsai DE. Reduction of immunosuppression as initial therapy for posttransplantation lymphoproliferative disorder (bigstar). Am J Transplant 2011; 11: Int J Clin Exp Med 2014;7(7):
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