|Year : 2012 | Volume
| Issue : 1 | Page : 62-67
Bone marrow involvement by lymphoproliferative disorders after renal transplantation: PTLD. Int. Survey
Morteza Izadi1, Mozhgan Fazel2, Seyed Hasan Saadat1, Saeed Taheri3
1 Department of Medicine, Health Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran
2 Department of Medicine, International Travel Medicine Center of Iran, Tehran, Iran
3 Department of Medicine, Dr. Taheri Medical Research Group, Tehran, Iran
|Date of Web Publication||19-Apr-2012|
Seyed Hasan Saadat
The Health Research Center; Deputy of Research, Headquarters' building, Baqiyatallah University of Medical Sciences, Mollasadrast, Vanaksq, Tehran
Source of Support: Baqiyatallah University of Medical Sciences, Conflict of Interest: None
Context: Renal graft recipients who develop post-transplant lymphoproliferative disorders (PTLD) that complicate bone marrow (BM).
Aims: To investigate features, predictors and prognosis of BM involvement by PTLD in renal transplant patients.
Settings and Design: A comprehensive search for the available data though PubMed and Google Scholar for reports of PTLD localization in BM in renal allograft recipients.
Materials and Methods: Data of 168 PTLD cases in renal transplant context who have developed bone marrow PTLD gathered from 18 studies and were pooled and analyzed.
Statistical Analysis Used: Chi-square test, Student's t test and fissure's exact test were employed.
Results: Chi-square test showed that renal recipients with BM PTLD were significantly more likely to represent multi-organ disease (P<0.001), and disseminated PTLD (P<0.001). BM PTLD was also more frequently seen among pediatric renal recipients who had developed PTLD (P=0.016). PTLD, in BM PTLD renal recipients more significantly complicated liver (P=0.008), but less commonly affected skin (P=0.045). BM PTLD lesions were relatively more likely to be of monomorph phenomenon (P=0.06).
Conclusions: Renal recipients with BM PTLD represent worse outcome and more unfavorable histopathological phenomenon than in other organ involvements. Moreover, a concomitant PTLD involvement site in liver was found which necessitates full hepatic evaluation for a potential complication by the disease in renal recipients whose BM is involved.
Keywords: Bone marrow disease, post-transplant lymphoproliferative disorder, renal transplantation
|How to cite this article:|
Izadi M, Fazel M, Saadat SH, Taheri S. Bone marrow involvement by lymphoproliferative disorders after renal transplantation: PTLD. Int. Survey. J Can Res Ther 2012;8:62-7
|How to cite this URL:|
Izadi M, Fazel M, Saadat SH, Taheri S. Bone marrow involvement by lymphoproliferative disorders after renal transplantation: PTLD. Int. Survey. J Can Res Ther [serial online] 2012 [cited 2019 Nov 14];8:62-7. Available from: http://www.cancerjournal.net/text.asp?2012/8/1/62/95176
| > Introduction|| |
The development of post transplant lymphoproliferative disorder (PTLD) remains a challenging diagnostic and therapeutic problem characterized by neoplastic lymphoid proliferation of B- or T-cell origins. The first evidence on this entity was provided in 1969 by Penn et al.  in a patient who had undergone living related kidney transplantation. Since then, several reports from different centers throughout the world showed a high incidence of PTLD among recipients of all types of organs including the kidney. A wide range of 1-20% incidence of PTLD after organ transplantation has been reported, ,,, representing a 10 to over 100 fold higher risk compared to that in the general population; , with renal transplant patients representing one of the lowest rates.
PTLD emerges in a wide spectrum from a limited disease to quite a disseminated neoplasm. Bone marrow (BM) examination is an integral part of non-Hodgkin lymphomas evaluations, since its involvement indicates stage IV disease, which is an adverse prognostic factor independently associated with a worse outcome.  The frequency of BM involvement by the lymphoma varies according to the disease subtype with higher frequency in patients with low grade non-hodgkin's lymphoma, ranging from 30% for marginal zone lymphomas to almost 100% for chronic lymphocytic leukemias , than in diffuse large B cell lymphomas (8-35%). ,,,,
Differences in the incidence of BM complication by PTLD with regard to their histopathological phenotype or association with Epstein-Barr virus (EBV) infection are currently not known. Although general belief is that BM involvement by monomorphic PTLD is uncommon, gradually emerging evidence indicates several individual reports on the occurrence of BM infiltrations in the PTLD population of this phenotype. On the other hand, no study with substantial number of patients has been conducted to investigate different characters, predictors and prognosis including changeable prognostic factor in renal transplant recipients. Knowing these factors, we can design preventive and screening methods that potentially decrease the incidence of the disease or promote its diagnosis in earlier stages which can result in survival advantages both for the graft and the patients.
Considering the above mentioned factors, in the current study we aimed to search the existing literature to find reported cases of renal recipients developing PTLD within their BM, and to compare their demographic data, histological phenomena and survival with renal recipients who represented PTLD in other organs to find potential predictive and prognostic factors which play major roles in this patient population.
| > Materials and Methods|| |
Approach to the study
We conducted a comprehensive search for the available data though PubMed and Google Scholar for reports of PTLD localization in BM in renal allograft recipients. Search terms used were "lymphoproliferative disorders + renal transplantation + BM," "lymphoproliferative disorders + kidney transplantation + BM localization," "lymphoproliferative disorder + renal transplantation + marrow infiltration". In cases where we were not able to obtain the full text of the article, emails were sent to the correspondent authors requesting the article. Of the full texts obtained, we enrolled subjects from studies in which data of each patient was presented separately. To minimize selection bias, we only included studies reporting their series of patients from single- or multi-center populations, and studies with any specific selection criterion were excluded from the analysis. Control patients were renal recipients whose PTLD localization organ was not BM. For minimizing interfering factors including center-selection bias, control patients were also enrolled from the same studies reporting BM PTLD renal recipients. A standard questionnaire was developed to collect data from different published studies. The time between transplantation and PTLD onset was defined as the period between the graft and the first signs of PTLD or diagnosis, depending on the study's approach.
Eighteen international published studies ,,,,,,,,,,,,,,,, were found that met our criteria. A total of 168 renal recipients with a documented PTLD site were included in the analysis; of whom 31 (18.5%) had BM PTLD and the remaining 137 (81.5%) patients had developed non-BM PTLD. EBV status was documented in 108 (64.3%) patients, of whom 75 (69.4%) were reportedly positive.
Because of different methodologies employed in the published studies enrolled into the current survey, some of our measures were not available for all the patients. So we tried to standardize the data. We recorded disseminated PTLD when it was reported by the study authors or if at least three different organs were involved by the PTLD (different lymph node areas were excluded from analysis due to lack of knowledge on how to categorize; unless they were concomitant with other organs involvements; or other authors specifically presented them as having disseminated disease). According to the above mentioned, data on disseminated PTLD was available for 90 patients (53.6%; 78 unreported data) of which 29 (32.2%) were disseminated PTLD. Multi-organ involvement, defined as involvement of more than one organ (the second organ could be a lymphatic region), was available in 117 patients (69.6%%; 51 unavailable data) of which 64 (54.7%) were multi-organ PTLD.
At PTLD onset, all patients were under immunosuppressive regimens consisting of varying combinations of azathioprine, prednisone, cyclosporine, mycophenolatemofetil, ATG/ALG and OKT3. A rather uniform approach was used to manage most of the included PTLD renal recipients. On diagnosis of PTLD, the first step in almost all reports was to decrease or discontinue immunosuppressive therapy; various regimens of chemotherapy with or without surgical interventions were also used for some patients.
Response to treatment
We defined response to treatment as any favorable change both in PTLD measures and the patient's clinical condition. Data on response to treatment was reported for 96 patients (57.1%), of whom 69 (71.9%) responded to treatment and had a remission episode. To create a common standard across the studies, we defined a remission episode as when a patient was alive 24 months after PTLD onset (because all reported cases meeting this criterion had at least one confirmed remission episode) and no remission as when a patient died within the first month after PTLD onset (because there were no patients dying at the first post-transplant month that was reported to have any remission episodes). According to these criteria, data on remission was available for 123 patients (73.2%), of whom 76 (61.8%) had at least one response to treatment, irrespective of their future disease course. Data on mortality was available for 154 patients (91.7%), of whom 85 (55.2%) died. We defined death due to PTLD when the authors stated it, death was within six months after onset, or death was reported to be due to PTLD treatment complications. Based on these criteria, 50 patients (58.8% of reported deaths) died due to PTLD.
SPSS v.13.0 software was used for data analyses. Statistical comparisons between patient subgroups were performed using Chi-square and Fisher's exact tests for proportions, and the Student's t-test for continuous data. Survival analysis was done with life tables, Kaplan-Meier method and log-rank test. A P-value of 0.05 was taken as the threshold for significance and of 0.1 was defined as relevance level.
| > Results|| |
Overall 168 patients with lymphoproliferative disorders after renal transplantation were entered into analysis. There were 95 (62.5%) males and 57 (37.5%) female patients (16 unreported). Mean age at diagnosis of PTLD was 42.6±16 years. The mean interval between transplantation and the diagnosis of PTLD was 57.1±52.6 months whereas follow up time after diagnosis of PTLD was 22.9±32.3 months.
Characteristics of the patients regarding their malignancy site are summarized in [Table 1]. Chi-square test showed that renal recipients with BM PTLD were significantly more likely to represent multi-organ disease (P<0.001), and disseminated PTLD (P<0.001). BM PTLD was also more frequently seen among pediatric renal recipients who had developed PTLD (P=0.016). Renal transplant recipients with BM PTLD localization were comparable to their counterparts with other PTLD localization in their gender, lymphoma cell types, immunosuppression type, presentation time, and EBV positive rate. Overall mortality rate was relevantly more frequent in the BM PTLD group than in controls (P=0.06); however, death due to the PTLD was not statistically different between the two groups.
|Table 1: Characteristics of renal transplant recipients with or without bone marrow involvement by post-transplant lymphoproliferative disorder|
Click here to view
[Table 2] summarizes different organ involvements by PTLD when they concomitantly do or do not complicate the BM. PTLD, in BM PTLD renal recipients more significantly complicated liver (P=0.008), but less commonly affected skin (P=0.045), simultaneous to the BM. Other organs were equally involved by the neoplasm between the two groups.
|Table 2: Frequency of involved organs in 120 kidney transplant recipients with or without bone marrow|
complication by post-transplant lymphoproliferative disorder
Click here to view
Patients with BM PTLD were significantly younger at the time of transplantation (P=0.04); but had comparable time from transplantation to PTLD development (P=0.728). Histopathological evaluations were also comparable for PTLD occurring within BM PTLD patients versus other renal recipients developing PTLD [Table 1]. However, BM PTLD lesions were relevantly more likely to be of monomorph phenomenon (P=0.06).
When death irrespective of the reason was used as the outcome, log-rank test showed a significant inferior outcome for BM PTLD renal recipients (P=0.001; [Figure 1]); as well, when death only due to PTLD was used as the outcome (based on the defined criteria in the methods section), the BM PTLD group again represented lower survival than patients with other localizations (P=0.02; [Figure 2]). One and two years survival rates for BM PTLD patients were 46 and 17%, respectively, compared to 63 and 50%, respectively, for the control group.
|Figure 1: Survival curves of renal transplant recipients regarding bone marrow involvement by the PTLD (outcome: death irrespective of reason)|
Click here to view
|Figure 2: Survival curves of renal transplant recipients regarding bone marrow involvement by the PTLD (outcome: death due to PTLD)|
Click here to view
| > Discussion|| |
PTLD are one of the most prevalent malignancies complicating recipients of various organs reducing graft and patient survival and inducing a high financial and medical burden to patients and the society. PTLD. Int. survey is an attempt at reviewing and gathering international data from PTLD patients to conduct analyses on the largest possible patient population to discover new perspectives on the disease. In this study, we analyzed one of the ever largest series of PTLD patients to discover various characteristics of PTLD presenting within BM in renal transplant recipients, and their histopathological features, disease behavior and prognostic factors.
In general practice, BM biopsy is recommended routinely for the staging of patients developing PTLD in their disease course.  According to the Ann Arbor staging system for non-Hodgkin's lymphoma, BM involvement at diagnosis defines stage IV disease,  and is associated with a more ominous clinical course. , Our data shows that BM involvement by neoplastic lymphomatoid cells in PTLD, as mentioned for that in non-transplant era, is associated with an inferior outcome. Moreover, we found that BM PTLD lesions were more likely to be monomorphic than benign features with no case in the early lesion category, although the difference did not reach significance level. These findings are consistent with our previous knowledge in transplant ear, where PTLD involving BM was a predictor for a worse outcome.  These findings confirm our previous assumptions on considering BM complication as a high-grade disease for lymphoma.
There is a high inconsistency in the current literature respecting the incidence of BM involvement in different patient groups and in various PTLD subtypes. The incidence of BM PTLD in different series have been reported from 15%  to 40%  in different series. Methodology employed in the current study does not empower us to present a precise frequency of BM involvement by the PTLD in renal transplant population; however, nothing wrong exists if we want to compare these frequencies among different subpopulations of our study data. Our study showed that BM PTLD is significantly more likely to occur in pediatric renal recipients. There is a shortage of data on this in the literature, but comparing different studies, our finding is novel. While Maeckeret al.,  have reported a 15% incidence rate for BM involvement in children developing PTLD, Knight et al.  have reported 19.6% BM PTLD in their series of adult patients and Houriganet al.,  also reported a 40% incidence of BM PTLD in renal transplant context. Putting together, one may assume that BM PTLD incidence in pediatric setting is comparable to that in adults. Nevertheless, this conclusion is not in concordance with what we may expect from outcome analysis. Overwhelming data has confirmed that PTLD has a substantially higher mortality among children than in adults. So, we should expect that children also represent more aggressive types of the disease like that in BM PTLD. Our study finding is consistent with this assumption, but we should take attention that this finding is in renal recipients developing PTLD and may not be globalized to other solid organ recipients, as the study populations of Knight et al.  and Hougarianet al.  enrolled other types of organ recipients.
PTLDs are believed to have a tendency for extranodal organ involvements. ,,,,,, However, factors playing major roles in spread of the disease are not well defined. The current study showed that almost 90% of renal recipients who have developed within their BM have had a multi-organ involvement whose proportion is almost twice as the controls. Moreover, we found some predilection to some specific organs involvement for patients with BM PTLD. As summarized in [Table 2], over 44% of BM PTLD renal recipients had a concomitant liver involvement which was significantly higher than controls while skin complication was significantly lower in the case group. In a previous study on hepatic graft involvement by the PTLD in liver recipients, we found a similar finding indicating a higher prevalence of BM involvement by the PTLD in patients whose hepatic graft was complicated by the disease.  These findings are of outmost relevance, because discovering concomitant involvement organs by the disease will alert us to more directly search for the PTLD sites in different patient populations which results in an earlier diagnosis and survival advantages.
In summary, our study population of renal recipients with BM PTLD can be considered as a good representative for the mentioned patient population, because it was gathered from different series with no special selection bias. Through this study, we found that renal recipients with BM PTLD represent worse outcome and more unfavorable histopathological phenomenon than in other organ involvements. Moreover, a concomitant PTLD involvement site in liver was found which necessitates full hepatic evaluation for a potential complication by the disease in renal recipients whose BM is involved.
| > References|| |
|1.||Penn I, Hammond W, Brettschneider L, Starzl TE. Malignant lymphomas in transplantation patients. Transplant Proc 1969;1:106-12. |
|2.||Levy M, Backman L, Husberg B, Goldstein R, McMillan R, Gibbs J, et al. De novo malignancy following liver transplantation: A single-center study. Transplant Proc 1993;25:1397-9. |
|3.||Malatack JF, Gartner JC Jr, Urbach AH, Zitelli BJ. Orthotopic liver transplantation, Epstein-Barr virus, cyclosporine, and lymphoproliferative disease: A growing concern. J Pediatr 1991;118:667-75. |
|4.||Cox KL, Lawrence-Miyasaki LS, Garcia-Kennedy R, Lennette ET, Martinez OM, Krams SM, et al. An increased incidence of Epstein-Barr virus infection and lymphoproliferative disorder in young children on FK506 after liver transplantation. Transplantation 1995;59:524-9. |
|5.||Stieber AO, Boillot O, Scotti-Foglieni C, Nalesnik MA, Gordon RD, Marino I, et al. The surgical implications of the posttransplantlymphoproliferative disorders. Transplant Proc 1991;23:1477-9. |
|6.||Nalesnik MA, Jaffe R, Starzl TE, Demetris AJ, Porter K, Burnham JA, et al. The pathology of posttransplantlymphoproliferative disorders occurring in the setting of cyclosporine A-prednisone immunosuppression. Am J Pathol 1988;133:173-92. |
|7.||Opelz G, Henderson R. Incidence of non-Hodgkins lymphomas in kidney and heart transplant recipients. Lancet 1993;342:1514-6. |
|8.||Wilder RB, Rodriguez MA, Medeiros LJ, Tucker SL, Ha CS, Romaguera JE, et al. International prognostic index-based outcomes for diffuse large B-cell lymphomas. Cancer 2002;94:3083-8. |
|9.||Arber DA, George TI. Bone marrow biopsy involvement by non-Hodgkin's lymphoma: Frequency of lymphoma types, patterns, blood involvement, and discordance with other sites in 450 specimens. Am J Surg Pathol 2005;29:1549-57. |
|10.||Conlan MG, Bast M, Armitage JO, Weisenburger DD. Bone marrow involvement by non-Hodgkin's lymphoma: The clinical significance of morphologic discordance between the lymph node and bone marrow. Nebraska Lymphoma Study Group. J Clin Oncol 1990;8:1163-72. |
|11.||Campbell J, Seymour JF, Matthews J, Wolf M, Stone J, Juneja S. The prognostic impact of bonemarrow involvement in patientswith diffuse large cell lymphoma varies according to the degree of infiltration and presence of discordant marrow involvement. Eur J Haematol 2006;76:473-80. |
|12.||Park S, Lee J, Ko YH, Han A, Jun HJ, Lee SC, et al. The impact of Epstein-Barr virus status on clinical outcome in diffuse large B-cell lymphoma. Blood 2007;110:972-8. |
|13.||Ohshima K, Suzumiya J, Tasiro K, Mukai Y, Tanaka T, Kato A, et al. Epstein-Barr virus infection and associated products (LMP, EBNA2, vIL-10) in nodal non-Hodgkin's lymphoma of human immunodeficiency virusnegative Japanese. Am J Hematol 1996;52:21-8. |
|14.||Benkerrou M, Durandy A, Fischer A. Therapy for transplant-related lymphoproliferative disease. Hematol Oncol Clin North Am 1993;7:467-75. |
|15.||Chen W, Huang Q, Zuppan CW, Rowsell EH, Cao JD, Weiss LM, et al. Complete absence of KSHV/HHV-8 in posttransplantlymphoproliferative disorders: An immunohistochemical and molecular study of 52 cases. Am J Clin Pathol 2009;131:632-9. |
|16.||O'Conner AR, Franc BL. FDG PET imaging in the evaluation of posttransplantlymphoproliferative disorder following renal transplantation. Nucl Med Commun 2005;12:1107-11. |
|17.||Sun X, Peterson LC, Gong Y, Traynor AE, Nelson BP. Post-transplant plasma cell myeloma and polymorphic lymphoproliferative disorder with monoclonal serum protein occurring in solid organ transplant recipients. Mod Pathol 2004;17:389-94. |
|18.||Kim HK, Jin SY, Lee NS, Won JH, Park HS, Yang WI. Posttransplant primary cutaneous Ki-1 (CD30)+/CD56+ anaplastic large cell lymphoma. Arch Pathol Lab Med 2004;128:e96-9. |
|19.||Morrison VA, Dunn DL, Manivel JC, GajlPeczalska KJ, Peterson BA. Clinical characteristics of post-transplant lymphoproliferative disorders. Am J Med 1994;97:14-24. |
|20.||Abe T, Ichimaru N, Kokado Y, Maeda T, Kakuta Y, Okumi M, et al. Post-transplant lymphoproliferative disorder following renal transplantation: Asingle-center experience over 40 years. Int J Urol 2010;17:48-54. |
|21.||Ziarkiewicz-Wróblewska B, Górnicka B, Gierej B, Suleiman W, Nowacka-Cieciura E, Durlik M, et al. Posttransplantlymphoproliferative disorder: Morphological picture and diagnostic difficulties. Transplant Proc 2006;38:168-72. |
|22.||Soler MJ, Puig JM, Mir M, Parrilla J, Pedro C, Salar A,et al. Posttransplantlymphoproliferative disease: Treatment and outcome in renal transplant recipients. Transplant Proc 2003;35:1709-13. |
|23.||Morovic A, Jaffe ES, Raffeld M, Schrager JA. Metachronous EBV-associated B-cell and T-cell posttransplantlymphoproliferative disorders in a heart transplant recipient. Am J Surg Pathol 2009;33:149-54. |
|24.||Djokic M, Le Beau MM, Swinnen LJ, Smith SM, Rubin CM, Anastasi J, et al. Post-transplant lymphoproliferative disorder subtypes correlate with different recurring chromosomal abnormalities. Genes Chromosomes Cancer 2006;45:313-8. |
|25.||Ravat FE, Spittle MF, Russell-Jones R. Primary cutaneous T-cell lymphoma occurring after organ transplantation. J Am Acad Dermatol 2006;54:668-75. |
|26.||Bakker NA, van Imhoff GW, Verschuuren EA, van Son WJ, Homan van der Heide JJ, Veeger NJ,et al. Early onset post-transplant lymphoproliferative disease is associated with allograft localization. Clin Transplant 2005;19:327-34. |
|27.||Muti G, Cantoni S, Oreste P, Klersy C, Gini G, Rossi V, et al. Post-transplant lympoproliferative disorders: Improved outcome after clinico-pathologically tailored treatment. Haematologica 2002;87:67-77. |
|28.||Paraskevas S, Coad JE, Gruessner A, Kandaswamy R, Humar A, Sutherland DE, et al. PosttransplantLymphoproliferative Disorder in Pancreas Transplantation: A Single-Center Experience.Transplantation 2005;80:613-22. |
|29.||Hanto DW, Frizzera G, Purtilo DT, Sakamoto K, Sullivan JL, Saemundsen AK, et al. Clinical spectrum of lymphoproliferative disorders in renal transplant recipients and evidence for the role of Epstein-Barr virus. Cancer Res 1981;41:4253-61. |
|30.||Abramson JS, Kotton CN, Elias N, Sahani DV, Hasserjian RP. Case records of the Massachusetts General Hospital. Case 8-2008. A 33-year-old man with fever, abdominal pain, and pancytopenia after renal transplantation. N Engl J Med 2008;358:1176-87. |
|31.||Nalesnik MA. Clinicopathologic characteristics of post-transplant lymphoproliferative disorders. Recent Results Cancer Res 2002;159:9-18. |
|32.||Rosenberg SA. Validity of the Ann Arbor staging classification for the non-Hodgkin's lymphomas. Cancer Treat Rep 1977;61:1023-7. |
|33.||Maecker B, Jack T, Zimmermann M, Abdul-Khaliq H, Burdelski M, Fuchs A, et al. CNS or bone marrow involvement as risk factors for poor survival in post-transplantation lymphoproliferative disorders in children after solid organ transplantation. J Clin Oncol 2007;25:4902-8. |
|34.||Montanari F, O'Connor OA, Savage DG, Zain JM, Venkatraman S, McCormick EK, et al. Bone marrow involvement in patients with posttransplantlymphoproliferative disorders: Incidence and prognostic factors. Hum Pathol 2010;41:1150-8. |
|35.||Hourigan MJ, Doecke J, Mollee PN, Gill DS, Norris D, Johnson DW, et al. A new prognosticator for post-transplant lymphoproliferative disorders after renal transplantation. Br J Haematol 2008;141:904-7. |
|36.||Knight JS, Tsodikov A, Cibrik DM, Ross CW, Kaminski MS, Blayney DW. Lymphoma after solid organ transplantation: Risk, response to therapy, and survival at a transplantation center. J Clin Oncol 2009;10;27:3354-62. |
|37.||Ghobrial IM, Habermann TM, Maurer MJ, Geyer SM, Ristow KM, Larson TS, et al. Prognostic analysis for survival in adult solid organ transplant recipients with posttransplantationlymphoproliferative disorders. J Clin Oncol 2005;23:7574-82. |
|38.||Khedmat H, Taheri S. Characteristics and prognosis of post-transplant lymphoproliferative disorders within renal allograft: Report from the PTLD.Int. Survey. Ann Transplant 2010;15:80-6. |
|39.||Izadi M, Taheri S. Significance of in situ hybridization results for EBV-encoded RNA in post-transplantation lymphoproliferative disorder setting: Report from the PTLD.Int Survey. Ann Transplant 2010;15:102-9. |
|40.||Izadi M, Taheri S. Features, predictors and prognosis of lymphoproliferative disorders post-liver transplantation regarding disease presentation time: Report from the PTLD.Int. survey. Ann Transplant 2011;16:39-47. |
|41.||Khedmat H, Taheri S. Post-Transplantation Lymphoproliferative disorders localizing in the adenotonsillar region: Report from the PTLD.Int survey. Ann Transplant 2011;16:109-16. |
|42.||Khedmat H, Taheri S. Early versus late outset of lymphoproliferative disorders post-heart and lung transplantation: The PTLD. Int Survey. Hematol Oncol Stem Cell Ther 2011;4:10-6. |
|43.||Izadi M, Fazel M, Saadat SH, Taheri S. Hepatic involvement by lymphoproliferative disorders post liver transplantation: PTLD. Int. Survey. Hepatol Int 2011;5:759-66. |
[Figure 1], [Figure 2]
[Table 1], [Table 2]