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post - transplant lymphoproliferative disorder ( ptld ) is a well - recognized and potentially life - threatening morbidity that can occur following transplantation of allogeneic hematopoietic stem cells and solid organs , including the heart ( 13 ) .
it is estimated to occur in 16.3% cardiac recipients , and manifests as a spectrum of lymphoproliferative disorders , from benign lymphoid hyperplasia to invasive lymphoma ( 13 ) .
an epstein - barr virus ( ebv ) infection resulting from post - transplantation use of immunosuppressive agents is understood to drive the neoplastic pathogenesis of b cells in ptld ( 2 ) .
treatment for ptld primarily includes the reduction or cessation of immunosuppressive therapy , anti - ebv therapy , anti - neoplastic therapy , such as chemoradiation therapy and surgery , and immunotherapy ( 4 ) .
two subtypes of ptld , early- and late - onset ptld , occur within the first year post - transplantation and afterwards , respectively , and exhibit distinct pathological profiles and prognoses ( 5,6 ) .
it has been reported that ebv - positive patients are more frequently afflicted with early - onset ptld than their ebv - negative counterparts ( 5,6 ) .
conversely , late - onset ptld occurs more frequently in older patients who are typically ebv - negative , following a longer latency period ; these patients generally have a poor treatment response and unfavorable prognosis , as late - onset ptld frequently acts like aggressive lymphoma ( 7 ) .
the present study reports a case of an ebv - negative , middle - aged han chinese man who developed late - onset ptld 12 years after heart transplantation .
rituximab ( a monoclonal cd20 antibody ) and a modified mini - chop ( r - mini - chop ) chemotherapy regimen was well tolerated and resulted in a 5-year clinical remission , free of allograft rejection .
a 54-year - old han chinese patient received orthotopic heart transplantation due to a diagnosis of end - stage dilated cardiomyopathy at the zhejiang provincial people 's hospital ( hangzhou , china ) in june 1997 .
the patient underwent an uneventful perioperative course and remained on immunosuppressive therapy with cyclosporine and prednisone .
the patient exhibited a good general condition free of allograft rejection , infection , or other clinically significant transplant - associated complications .
however , at a follow - up visit in april 2009 , the patient complained of multiple , bilateral , painless , cervical masses , in the absence of other discomforts such as fever , toothache , cough or dyspnea .
these masses were 13 cm in size and less mobile on palpation , and the local skin showed no redness or rash .
histologic examination with hematoxylin ( regal biotechnology co. , ltd . , bengbu , china ) and eosin ( shanghai xinsheng chemical technology co. , ltd . ,
shanghai , china ) was performed on a paraffin - embedded lymph node biopsy specimen ( 4 m ; leica rm2135 microtome ; leica microsystems gmbh , wetzlar , germany ) , and showed non - hodgkin lymphoma - diffuse large b - cell lymphoma ( dlbcl ; fig .
1a ) under the microscope ( bx5 ; olympus corporation , tokyo , japan ) .
immunohistochemistry was performed on lymph node paraffin - embedded tissue ( 4 m ) by blocking with hydrogen peroxide , followed by incubation with primary antibodies against cd20 ( 1:150 ; rabbit monoclonal / polyclonal ; cat .
gp1.4 ) for 15 h at 4c ( all purchased from origene technologies , inc .
the results identified strong immuno - positivity for cd20 and cd79a ( table i ) using abc series ( avidin - biotin complex ; vector laboratories , ltd .
1b ) , and chest / abdominal computed tomography ( ge hispeec tc / i ; the general electric company , coventry , uk ) detected no distant metastasis .
thus , a diagnosis of monomorphic ptld - dlbcl was established based on the previous history of heart transplantation and medication with immunosuppressive agents , in accordance with the world health organization classification of ptld ( 8) .
the present study was approved by the ethics committee of zhejiang provincial people 's hospital routine hematologic ( sysmex 2100 ; sysmex corporation co. , ltd . , kobe , japan ) , clinical biochemistry ( au5800 ; beckman coulter , brea , ca , usa ) , serologic ( abbott i2000 ; beckman coulter ) , and virologic ( ebv and cytomegalovirus ) tests ( euroimmun uk , ltd . , london , uk ) showed no clinically significant abnormality .
the immunosuppressive regimen of the patient was changed to dose - reduced tacrolimus ( 2 mg daily ) and mycophenolate mofetil ( 1.5 g daily ) prior to the initiation of chemotherapy .
a rituximab ( roche diagnostics , basel , switzerland ) and r - mini - chop chemotherapy regimen for non - hodgkin lymphoma was administered as follows : 375 mg / m rituximab , 400 mg / m cyclophosphamide ( jiangsu hengrui medicine co. , ltd . , shanghai , china ) , 30 mg / m pirarubicin ( shenzhen wanle pharmaceutical co. , ltd . , shenzen , china ) , and 1 mg vincristine ( hangzhou minsheng pharmaceutical group co. , ltd . ,
hangzhou , china ) on day 1 and 40 mg / m prednisone ( shanghai xinyi pharmaceutical co. , ltd . ,
the r - mini - chop therapy was well tolerated , and myocardial biopsy confirmed a grade 01 allograft rejection at 2.5 years after the previous rituximab maintenance therapy ( fig .
2 ) . the patient remained in clinical remission , as shown by follow - up positron emission tomography ( biograoh mct ; siemens ag , munich , germany ) and computed tomography 1 and 5 years after r - mini - chop therapy ( fig .
the first heart transplantation was performed in 1967 ( 9 ) , and ptld was first reported in a kidney recipient in 1979 ( 10 ) .
ptld is the most common malignancy second to skin / lip cancer in patients who have undergone solid organ transplantation , with an estimated incidence rate of 159/100,000 persons per year ( 11 ) .
skin and splenic lymph nodes ( 56% ) are most frequently involved in ptld at the time of presentation ( 8) . in addition , non - renal transplant recipients , in particular heart and lung recipients , have a higher risk of developing ptld than renal transplant recipients ( 12 ) . to the best of our knowledge ,
the present study reports the first case of late - onset ptld following heart transplantation in a chinese patient , although ~200 cases of ptld have been reported among heart recipients in the english literature .
ptld is the overproliferation of lymphoid cells , with disease severity ranging from benign polyclonal histology to malignant lymphoma ( 13 ) .
the most common pathologies of ptld include dlbcl and immunoblastic lymphoma ( 14 ) , whereas t - cell lymphomas , hodgkin disease and plasma cell neoplasms are less frequently encountered ( 15 ) .
post - transplantation , patients are at the highest risk of developing early - onset ptld , which occurs within the first postoperative year ( 3,16,17 ) .
the early - onset subtype more frequently affects pediatric and younger adult patients as polymorphic lymphoid proliferation with a possible causative association with ebv infection ( 3 ) , whereas the late - onset subtype , which manifests as monomorphic lymphomas of b - cells , or less often , t - cells , primarily occurs in older patients without a definitive association with ebv infection ( 18,19 ) .
late - onset ptld patients ( 21% ) are more likely to be negative on the epstein - barr encoding region ( eber ) in situ hybridization , compared with early - onset patients ( 10% ) ( 12 ) .
as the ebv - associated b - cell tumor is understood to result from impaired immunity following immunosuppressive therapy , the reduction or cessation of immunosuppressive therapy is essential for the treatment of ptld and may lead to spontaneous remission in early cases ; however , reduced immunosuppression may elicit allograft rejection ( 4 ) .
au et al ( 20 ) reported a case of brain ptld ( eber+ , cd20 + , dlbcl ) in a chinese patient following heart transplantation , and the patient achieved complete remission following a reduction of immunosuppression .
intensive chemotherapy is typically required if reduced immunosuppression fails to control early - onset disease , and is the initial therapy for the majority of cases of late - onset ptld ( 2 ) .
an antracyclin - based multi - drug regimen , such as the chop regimen with granulocyte - colony stimulating factor ( 21 ) , is used in the majority of transplantation centers .
an underlying adverse effect of cytotoxic chemotherapy is enhanced hematotoxicity in patients with ptld , as previous long - term immunosuppression may result in kidney and marrow toxicities ( 22 )
. these patients also have a higher susceptibility to infectious complications and sepsis , due to the underlying impairment of immunity ( 22 ) . a low - dose chop , namely the mini - chop regimen ,
was developed by windebank et al ( 23 ) and gross et al ( 24 ) and is associated with reduced drug toxicity and better tolerability .
ptld following solid organ transplantation is understood to be immunoreactive to cd20 in > 90% of cases , and dlbcl affects 75% of adult ptld cases with monomorphic histology ( 25 ) .
the chimeric antibody rituximab , which specifically targets the cd20 antigen , has been incorporated in the treatment of ptld in a number of case reports and retrospective studies ( 2628 ) .
the use of rituximab may allow a reduction in chemotherapy dose and result in reduced cytoxicity , particularly in pediatric patients .
in 5 out of 6 pediatric ptld patients , rituximab combined with dose - reduced chemotherapy resulted in a complete response within an 8- to 29-month follow - up period , with limited toxicity ( 29 ) .
gupta et al ( 13 ) reported that direct rituximab and reduced dose chemotherapy following the failure of reduced immunosuppression appeared to be effective as an alternative treatment of option for b - cell ptld .
kusuki et al ( 30 ) reported that the rituximab and combination chemotherapy regimen was effective in inducing and maintaining remission of ptld .
the present study is the first case report to evaluate the efficacy and safety of the r - mini - chop regimen in an adult ptld patient following solid organ transplantation .
ptld patients , in particular those suffering from the late - onset subtype , typically have an unfavorable prognosis , and approximately one - third of post - heart transplantation patients succumb to ptld ( 31,32 ) .
the survival probability of pediatric early - onset ptld heart recipients varies among previous reports ( 31,32 ) , although remains low in adult late - onset patients . in a case study of 56 pediatric heart recipients with ptld ,
the patient in the current study exhibited clinical remission free of cytoxicity and allograft rejection at 5 years following r - mini - chop therapy for ptld . in conclusion , the patient in the present study presented ebv - negative , late - onset ptld following heart transplantation .
reduced immunosuppression and the r - mini - chop regimen resulted in long - term clinical remission in the patient .
this treatment regimen exhibited good tolerability and a good safety profile with respect to cytoxicity and allograft rejection .
these results support the clinical practice of the management of b - cell ptld in adult late - onset patients .
post - transplant lymphoproliferative disorder ( ptld ) is one of the most frequent secondary malignancies that can follow immunosuppressive therapy for solid organ transplantation , and may result in severe morbidities and even mortality . a middle - aged han chinese patient , prescribed with immunosuppressive cyclosporine and prednisone , developed ptld that manifested as a painless cervical lymph node enlargement , 12 years following heart transplantation . 
 histology revealed monomorphic b - cell ptld ( diffuse large - cell lymphoma ) ; as a result the immunosuppressive regimen of the patient was changed to tacrolimus and mycophenolate mofetil . in addition , the patient was changed to 6-cycle rituximab with a modified mini - chop ( r - mini - chop ) regimen for induction , and 8-cycle quarterly rituximab treatment and maintenance therapy . 
 r - mini - chop therapy was well tolerated , and no allograft rejection occurred . 
 the patient exhibited clinical remission as demonstrated by the results of the positron emission tomography - computed tomography at the 5-year follow - up visit following r - mini - chop therapy . in conclusion , 
 r - mini - chop therapy following reduced immunosuppression is effective and safe for the treatment of late - onset ptld following heart transplantation .