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T-cell lymphoma with a granulomatous lesion of the lungs after autologous hematopoietic stem cell transplantation for Epstein–Barr virus-positive diffuse large B-cell lymphoma: a unique rare case of metachronous B-cell and T-cell lymphoma
Diagnostic Pathology volume 15, Article number: 125 (2020)
Epstein–Barr virus (EBV) is associated with the pathogenesis of a variety of malignancies, most notably lymphomas. Especially in the background of immunodeficiency, such as primary immunodeficiency disorder (PID) and post-transplant lymphoproliferative disorder (PTLD), the role of EBV might be crucial. PIDs are rare heterogeneous diseases affecting the development and/or the function of the innate and adaptive immune system. Malignancy is the second-highest cause of death after infection, and lymphoma accounts for about half of malignancies. The most frequently reported lymphoma type is diffuse large B-cell lymphoma (DLBCL) and the incidence of T-cell lymphoma is rare. PTLDs are also rare serious lymphoid and/or plasmacytic proliferative disorders that occur after undergoing solid organ or hematopoietic stem cell transplantation (HSCT). In the context of HSCT, most reported PTLDs have occurred in patients who received allogenic HSCT, but only a few cases have been reported in autologous HSCT (AutoHSCT) recipients.
A 53-year-old female patient initially presented with enlargement of the left cervical lymph nodes and was diagnosed with EBV-positive DLBCL. She was treated with R-CHOP, R-ACES, and AutoHSCT and went into remission. Four years later, computed tomography results revealed multiple lung nodules and abnormal infiltration, and sustained and progressing hypogammaglobulinemia was observed. The pathological specimen of video-assisted thoracoscopic surgical lung biopsy demonstrated extensive invasion of lymphocytes with notable granuloma findings. Flow cytometric immunophenotyping analysis showed that lymphocytes were positive for CD3 and CD5; especially, CD3 was expressed in the cytoplasm. Southern blot analysis revealed rearrangements of the T-cell receptor Cβ1 gene. She was diagnosed with peripheral T-cell lymphoma, not otherwise specified, accompanied by notable granulomatous lesions.
Here, as a unique case of metachronous B-cell and T-cell lymphoma, we report a rare case of T-cell lymphoma that mainly affected the lungs with the presentation of notable granulomatous findings following AutoHSCT for EBV-positive DLBCL at the age of 53 years. These lung lesions of granulomatous T-cell lymphoma could be related to the underlying primary immunodeficiency background associated with sustained hypogammaglobulinemia.
Epstein–Barr virus (EBV) is associated with the pathogenesis of a variety of malignancies, most notably lymphomas. Especially in the background of immunodeficiency, such as primary immunodeficiency disorder (PID) and post-transplant lymphoproliferative disorder (PTLD), the role of EBV might be crucial . PIDs are heterogeneous diseases affecting the development and/or the function of various components of the innate and adaptive immune system . The prevalence of PIDs is approximately 41–51:100,000. Malignancy is the second-highest cause of death after infection, and lymphoma accounts for approximately half of malignancies in both children and adults [3, 4]. The risk of lymphoma increases up to 10 times in PID patients, and EBV is associated with 30–60% of lymphoma cases in PIDs [4, 5]. In PIDs, the most frequently reported lymphoma types are diffuse large B-cell lymphoma (DLBCL; 33.5%) and Burkitt’s lymphoma (7.1%), but the incidence of T-cell lymphoma is rare [1, 6, 7].
PTLDs are also rare serious lymphoid and/or plasmacytic proliferative disorders that occur after solid organ or hematopoietic stem cell transplantation (HSCT) . The incidence of PTLDs is 30–50 times higher than that in the general population and ranges from 2 to 10%, whereas the incidence of PTLDs after HSCT is less than 1% [9, 10]. Most PTLDs are of B-cell origin and are related to EBV infection. T-cell PTLDs, in contrast, constitute fewer than 15% of PTLDs in Western countries . In the context of HSCT, most reported PTLDs have occurred in patients who received allogenic HSCT (AlloHSCT). However, only 25 published cases of PTLD following autologous HSCT (AutoHSCT) have been reported as case reports, with six cases having a T-cell origin reported (Table 1) [12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32]. Here, as a unique case of metachronous B-cell and T-cell lymphoma, we report a rare case of T-cell lymphoma that mainly affected the lungs with notable granulomatous findings following AutoHSCT with sustained hypogammaglobulinemia against EBV-positive DLBCL at the age of 53 years.
First lymphoid neoplasm
A 53-year-old woman initially presented with enlargement of the left cervical lymph nodes (LNs) in 2013. Cervical node biopsy revealed the diffuse infiltration of atypical medium to large lymphocytes (Fig. 1a, b). Laboratory studies showed low IgG and IgA levels (445 and 83 mg/dL, respectively) with normal IgM levels. Immunohistochemistry analysis showed that lymphocytes were positive for CD20 (Fig. 1c) and negative for CD3 and CD10 (data not shown). Furthermore, in situ hybridization (ISH) revealed that lymphocytes were positive for EBV-encoded small RNA (EBER) (Fig. 1d). She was diagnosed with EBV-positive DLBCL. She received six cycles of R-CHOP (rituximab, cyclophosphamide, doxorubicin, vincristine, and prednisone) chemotherapy in 2013 and was treated with three cycles of R-ACES (rituximab, high-dose Ara C, carboplatin, etoposide, and steroids) chemotherapy followed by AutoHSCT in 2014. She then achieved complete remission.
Second lymphoid neoplasm
She was temporarily affected by pneumonia in 2017 and paranasal sinusitis in 2018. Subsequently, she presented with wheezing, and chest X-ray and computed tomography revealed multiple lung nodules and consolidations (Fig. 2a-c) in 2018. Positron emission tomography showed the abnormal accumulation of 18F-fluorodeoxyglucose (FDG) in bilateral lungs (Fig. 2d). In addition, the abnormal uptake of FDG was observed in the supraclavicular, mediastinal, hilar, paraaortic, and mesenteric LNs (Fig. 2d).
Laboratory tests showed the gradual progression of hypogammaglobulinemia with low IgG, IgA, and IgM levels (367, 25, and 33 mg/dL, respectively). Polymerase chain reaction was conducted on the whole-blood EBV DNA, and the DNA levels were found to have increased up to 1.0 × 103 copies/mL from 2.0 × 102 copies/mL. Video-assisted thoracoscopic surgery (VATS) was performed for a biopsy of the left upper lobe of the lung. Macroscopic examination of the lung revealed multiple nodules, whereas the microscopic examination demonstrated diffuse infiltration of lymphocytes with multiple granulomas (Fig. 3a-c). The lymphocytes were mainly small to medium-sized and contained slight nuclear irregularities (Fig. 3d). Immunohistochemical staining revealed that lymphocytes were positive for CD3 and focally positive for CD20 (Fig. 3e, f). The lymphocytes had destructively infiltrated the alveolar epithelium based on immunostaining for AE1/AE3 (Fig. 3g). The lymphocytes were positive for CD4 (Fig. 3j) and focally positive for CD8, TIA1, and granzyme B (data not shown). The lymphocytes were negative for BCL-6, CD10 (Fig. 3k, l), CD30, CD56, and ALK (data not shown). In the granulomas, epithelioid cells were positive for CD68 (Fig. 3h). ISH results revealed that some lymphocytes were positive for EBER (Fig. 3i). Grocott staining, Wade-Fite staining, and Giemsa staining were negative. The blood test and lung pathological findings did not show any evidence of infection or other granulomatous lesions such as granulomatous angiitis and sarcoidosis.
Flow cytometric immunophenotyping analysis of the specimen revealed that the proportion of surface CD3 was 29.9% and that of cytoplasmic CD3 was 74.4% (Fig. 4a, b). The proportions of CD2+, CD4+, CD5+, CD7+, and CD8+ cells were 92.5, 73.6, 84.7, 71.0, and 16.0%, respectively. In contrast, the proportions of cells positive for CD10, CD19, CD20, CD25, surface Ig, and TdT were all < 10% (data not shown). Southern blot analysis of the specimen indicated rearrangements of the T-cell receptor Cβ1 gene, and rearrangements of the immunoglobulin heavy chain gene were not found (Fig. 4c, d). She was subsequently diagnosed with peripheral T-cell lymphoma, not otherwise specified (PTCL-NOS), accompanied by notable granulomatous lesions.
The patient was treated with prednisolone and received AlloHSCT, which was followed by tacrolimus and methotrexate. However, she did not achieve neutrophil engraftment and developed pneumonia. Finally, she died of septic shock on day 20 post-AlloHSCT approximately 8 months after the diagnosis of T-cell lymphoma.
We describe a case of T-cell lymphoma after chemotherapy and AutoHSCT for EBV-positive DLBCL as a unique rare case of metachronous B-cell and T-cell lymphoma. Our patient was diagnosed with EBV-positive DLBCL of the cervical LNs at the age of 53 years, and multiple lung lesions of PTCL-NOS associated notable granulomas were observed 4 years after complete remission following chemotherapy and AutoHSCT for DLBCL with sustained hypogammaglobulinemia.
EBV is etiologically linked to a remarkably wide range of lymphoproliferative lesions, including malignant lymphomas, as EBV-associated lymphoproliferative disorders (LPDs) . It was recently reported that EBV-associated LPDs could be categorized into two groups, including disorders in which the host is usually immunocompetent and the role of EBV might be secondary or essential in only a subset of patients such as DLBCL, and disorders that arise in patients with immunodeficiency in which the role of EBV might be crucial, such as LPD associated with PID or PTLD, etc. There is a strong association between the pattern of EBV latency and the immune status of the host, suggesting that the underlying immune condition and the microenvironment are essential for the pathogenesis and manifestations of lymphomas associated with EBV .
Our patient developed EBV-positive DLBCL at the age of 53 years. EBV-positive DLBCL usually develops in individuals aged > 50 years, with a peak in the eighth decade , thus the onset age of DLBCL of our case seemed relatively young. Our patient also showed sustained and progressive hypogammaglobulinemia with recurrent respiratory infections after R-CHOP for DLBCL. Because hypogammaglobulinemia has been recognized before AutoHSCT for DLBCL treatment, this condition could not be related to transplantation. Thus, the age of onset for EBV-positive DLBCL, hypogammaglobulinemia, and respiratory infections, which comprised the background of our case, led us to consider the possibility of underlying primary immunodeficiency, such as PID including common variable immunodeficiency (CVID).
Monogenic and other genetic defects of the immune system are categorized as PIDs, which affect various components of the immune system with susceptibility to infections but also to malignancies, including lymphoma [2, 6, 35, 36]. Recent investigations reported that the risk of lymphoma is increased tenfold in PID patients and that EBV is associated with 30–60% of lymphoma cases in PIDs [4, 5]. CVID is one of the most prevalent types of PIDs, occurring in approximately 1:50,000–1:25,000 individuals, and is typically characterized by significantly decreased serum levels of IgG with low IgA and/or IgM and recurrent bacterial infections [37,38,39]. CVID is most often diagnosed in individuals between the ages of 20 and 40 years, however, can occur at any age [37, 39].
In our case, there was indeed an EBV-positive DLBCL first occurring at the age of 53 years, with both IgG and IgA hypogammaglobulinemia at the initial diagnosis of DLBCL, as well as marked hypogammaglobulinemia that persisted and progressed for at least 4 years after DLBCL treatment until the onset of T-cell lymphoma with prominent granulomatous lesions. Therefore, a potential immune deficiency, such as CVID, cannot be ruled out in our case as one of the causes of this unique duplex T-cell after B-cell lymphoma.
In our case, metachronous tumor of T-cell lymphoma occurred and mainly affected the lungs 4 years after AutoHSCT for EBV-positive DLBCL, and thus, our case could be regarded as T-cell PTLD. PTLDs are lymphoid and/or plasmacytic proliferation disorders, including lymphoma, which develop as a consequence of immunosuppression after transplantation [8, 40]. In the context of HSCT, most cases of PTLD are reported in patients who received AlloHSCT and the incidence of PTLDs after AlloHSCT is less than 1% [9, 10]. Moreover, to the best of our knowledge, only 25 published cases of PTLD following AutoHSCT have been reported as case reports, with six cases of T-cell origin after AutoHSCT [12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32]. Thus our case could be regarded as a very rare case of T-cell PTLD after AutoHSCT. We reviewed the clinicopathological data of seven previously reported cases of T-cell PTLD after AutoHSCT including this case and found that five of seven (71.4%) cases were EBV infection-positive and two of seven (28.6%) cases had macrophage proliferative lesions (Table 1). Therefore, although EBV-positive findings in our case were considered relatively low, the possibility that EBV infection has some influence on the development of T-cell lymphoma in our case cannot be completely ruled out, in addition to the possibility that background immunodeficiency might have been involved. However, the most recent WHO classification of lymphoid neoplasms favors these rarely reported lesions of PTLD after AutoHSCT as being more likely iatrogenic and related to the therapy than related to the transplant itself . Thus, we can use the term “PTLD-like lesion” for the T-cell lymphoma lesion in our case, if we use the term “PTLD”.
In our case, the VATS specimen showed notable lymphocyte infiltration and multiple granulomas. No clinicopathological cause of the granuloma was found such as tuberculosis, fungal infection, sarcoidosis, or granulomatous angiitis. As a differential diagnosis, the granulomatous findings can be cited as being related to Lennert’s lymphoma (LeL), a rare variant of PTCL-NOS, characterized by prominent small clusters of epithelioid histiocytes [41, 42]. However, LeL was reported to comprise only 0.71% of PTCLs and relatively rarely invades the extranodal foci; therefore, this pulmonary lesion is not considered a typical LeL-related finding [43, 44]. In contrast, considering hypogammaglobulinemia in our patient, these granulomatous findings could also be interpreted as histological changes associated with the underlying immunodeficiency of this case, as mentioned previously, in addition to a PTCL-NOS lesion. This is because recent studies reported that 1–4% of PID patients have granulomas and the most common types of granulomas are sino-pulmonary (50%), hematologic-lymphoid (33%), and skin (16%); further, 42% are considered to have prominent granulomas .
In conclusion, we report a rare case of T-cell lymphoma mainly affecting the lungs with notable granulomatous findings that developed post-AutoHSCT for EBV-positive DLBCL as a unique case of metachronous B-cell and T-cell lymphoma. These lung lesions of granulomatous T-cell lymphoma could be related to an underlying primary immunodeficiency background associated with sustained hypogammaglobulinemia.
Availability of data and materials
The data and materials are available upon request from the corresponding author.
Primary immunodeficiency disorder
Common variable immunodeficiency
Diffuse large B-cell lymphoma
EBV-encoded small RNA
Hematopoietic stem cell transplantation
peripheral T-cell lymphoma, not otherwise specified
Post-transplant lymphoproliferative disorder
Video-assisted thoracoscopic surgery
Marques-Piubelli ML, Salas YI, Pachas C, Becker-Hecker R, Vega F, Miranda RN. Epstein-Barr virus-associated B-cell lymphoproliferative disorders and lymphomas: a review. Pathology. 2020;52:40–52.
Picard C, Bobby Gaspar H, Al-Herz W, Bousfiha A, Casanova JL, Chatila T, et al. International Union of Immunological Societies: 2017 primary immunodeficiency diseases committee report on inborn errors of immunity. J Clin Immunol. 2018;38:96–128.
Kobrynski L, Powell RW, Bowen S. Prevalence and morbidity of primary immunodeficiency diseases, United States 2001-2007. J Clin Immunol. 2014;34:954–61.
Shapiro RS. Malignancies in the setting of primary immunodeficiency: implications for hematologists/oncologists. Am J Hematol. 2011;86:48–55.
Mayor PC, Eng KH, Singel KL, Abrams SI, Odunsi K, Moysich KB, et al. Cancer in primary immunodeficiency diseases: Cancer incidence in the United States immune deficiency network registry. J Allergy Clin Immunol. 2018;141:1028–35.
Riaz IB, Faridi W, Patnaik MM, Abraham RS. A systematic review on predisposition to lymphoid (B and T cell) neoplasias in patients with primary immunodeficiencies and immune dysregulatory disorders (inborn errors of immunity). Front Immunol. 2019;10:777.
Hermaszewski RA, Webster AD. Primary hypogammaglobulinaemia: a survey of clinical manifestations and complications. Q J Med. 1993;86:31–42.
Swerdlow SH, Webber SA, Chadburn A, Ferry JA. Post-transplant lymphoproliferative disorders. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Jürgen T, editors. WHO classification of tumors of haematopoietic and lymphoid tissues. Lyon: International Agency for Research on Cancer (IARC); 2017. p. 453–62.
Cockfield SM. Identifying the patient at risk for post-transplant lymphoproliferative disorder. Transpl Infect Dis. 2001;3:70–8.
Herreman A, Dierickx D, Morscio J, Camps J, Bittoun E, Verhoef G, et al. Clinicopathological characteristics of posttransplant lymphoproliferative disorders of T-cell origin: single-center series of nine cases and meta-analysis of 147 reported cases. Leuk Lymphoma. 2013;54:2190–9.
Swerdlow SH. T-cell and NK-cell posttransplantation lymphoproliferative disorders. Am J Clin Pathol. 2007;127:887–95.
Yufu Y, Kimura M, Kawano R, Noguchi Y, Takatsuki H, Uike N, et al. Epstein-Barr virus-associated T cell lymphoproliferative disorder following autologous blood stem cell transplantation for relapsed Hodgkin's disease. Bone Marrow Transplant. 2000;26:1339–41.
Narumi H, Kojima K, Matsuo Y, Shikata H, Sekiya K, Niiya T, et al. T-cell large granular lymphocytic leukemia occurring after autologous peripheral blood stem cell transplantation. Bone Marrow Transplant. 2004;33:99–101.
Miyazaki K, Masuya M, Yamaguchi M, Isaka S, Nakase K, Kobayashi T, et al. Angioimmunoblastic T-cell lymphoma occurring four months after autologous peripheral blood stem cell transplantation with high-dose chemotherapy for follicular lymphoma. Rinsho Ketsueki. 2005;46:1065–70.
Awaya N, Adachi A, Mori T, Kamata H, Nakahara J, Yokoyama K, et al. Fulminant Epstein-Barr virus (EBV)-associated T-cell lymphoproliferative disorder with hemophagocytosis following autologous peripheral blood stem cell transplantation for relapsed angioimmunoblastic T-cell lymphoma. Leuk Res. 2006;30:1059–62.
Nava VE, Cohen P, Bishop M, Fowler D, Jaffe ES, Ozdemirli M. Enteropathy-type T-cell lymphoma after intestinal diffuse large B-cell lymphoma. Am J Surg Pathol. 2007;31:476–80.
Ishikawa T, Shimizu H, Takei T, Koya H, Iriuchishima H, Hosiho T, et al. Monomorphic post-transplant T-lymphoproliferative disorder after autologous stem cell transplantation for multiple myeloma. Rinsho Ketsueki. 2016;57:36–40.
Sumitani R, Sekimoto E, Shibata H, Mori K, Shigekiyo T, Yano M, et al. A case of diffuse large B-cell lymphoma presented Epstein-Barr Virus associated T-cell and B-cell lymphoproliferative disorders followed by autologous peripheral blood stem cell transplantation. Nihon Naika Gakkai Zasshi. 2016;105:1275–81.
Peniket AJ, Perry AR, Williams CD, MacMillan A, Watts MJ, Isaacson PG, et al. A case of EBV-associated lymphoproliferative disease following high-dose therapy and CD34-purified autologous peripheral blood progenitor cell transplantation. Bone Marrow Transplant. 1998;22:307–9.
Fassas A, Jagannath S, Desikan KR, Shah HR, Shaver R, Waldron J, et al. Lymphomatoid granulomatosis following autologous stem cell transplantation. Bone Marrow Transplant. 1999;23:79–81.
Jenkins D, DiFrancesco L, Chaudhry A, Morris D, Glück S, Jones A, et al. Successful treatment of post-transplant lymphoproliferative disorder in autologous blood stem cell transplant recipients. Bone Marrow Transplant. 2002;30:321–6.
Takahashi S, Watanabe D, Miura K, Ozawa H, Tamada Y, Hara K, et al. Epstein-Barr virus-associated post-transplant lymphoproliferative disorder presenting with skin involvement after CD34-selected autologous peripheral blood stem cell transplantation. Eur J Dermatol. 2007;17:242–4.
Zambelli A, Lilleri D, Baldanti F, Scelsi M, Villani L, Da Prada GA. Hodgkin's disease as unusual presentation of post-transplant lymphoproliferative disorder after autologous hematopoietic cell transplantation for malignant glioma. BMC Cancer. 2005;5:109.
Izumiya S, Ishida M, Hodohara K, Yoshida T, Okabe H. Epstein-Barr virus-associated lymphoproliferative disorder developed following autologous peripheral blood stem cell transplantation for relapsing Hodgkin's lymphoma. Oncol Lett. 2012;3:1203–6.
Oon ML, Soon G, Poon LM, Wang S. Development of monomorphic B-cell plasmacytoma post-transplant lymphoproliferative disorder in a patient with previous autologous stem cell transplant. Pathology. 2019;51:644–6.
Viola GM, Zu Y, Baker KR, Aslam S. Epstein-Barr virus-related lymphoproliferative disorder induced by equine anti-thymocyte globulin therapy. Med Oncol. 2011;28:1604–8.
Matsuo T, Tanaka T, Fujii N. Orbital MALT lymphoma after autologous stem cell transplantation for follicular lymphoma as relapse of diffuse large B-cell lymphoma. J Clin Exp Hematop. 2017;56:170–5.
Hauke RJ, Greiner TC, Smir BN, Vose JM, Tarantolo SR, Bashir RM, et al. Epstein-Barr virus-associated lymphoproliferative disorder after autologous bone marrow transplantation: report of two cases. Bone Marrow Transplant. 1998;21:1271–4.
Young L, Alfieri C, Hennessy K, Evans H, O'Hara C, Anderson KC, et al. Expression of Epstein-Barr virus transformation-associated genes in tissues of patients with EBV lymphoproliferative disease. N Engl J Med. 1989;321:1080–5.
Chao NJ, Berry GJ, Advani R, Horning SJ, Weiss LM, Blume KG. Epstein-Barr virus-associated lymphoproliferative disorder following autologous bone marrow transplantation for non-Hodgkin's lymphoma. Transplantation. 1993;55:1425–8.
Shepherd JD, Gascoyne RD, Barnett MJ, Coghlan JD, Phillips GL. Polyclonal Epstein-Barr virus-associated lymphoproliferative disorder following autografting for chronic myeloid leukemia. Bone Marrow Transplant. 1995;15:639–41.
Briz M, Forés R, Regidor C, Busto MJ, Ramon y Cajal S, Cabrera R, et al. Epstein-Barr virus associated B-cell lymphoma after autologous bone marrow transplantation for T-cell acute lymphoblastic leukaemia. Br J Haematol. 1997;98:485–7.
Shannon-Lowe C, Rickinson AB, Bell AI. Epstein-Barr virus-associated lymphomas. Philos Trans R Soc Lond Ser B Biol Sci. 2017;372:20160271.
Nakamura S, Jaffe ES, Swerdlow SH. EBV-positive diffuse large B-cell lymphoma, not otherwise specified (NOS). In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Jürgen T, editors. WHO classification of tumors of haematopoietic and lymphoid tissues: International Agency for Research on Cancer (IARC); 2017. p. 304–6.
Herber M, Mertz P, Dieudonné Y, Guffroy B, Jung S, Gies V, et al. Primary immunodeficiencies and lymphoma: a systematic review of literature. Leuk Lymphoma. 2020;61:274–84.
Mortaz E, Tabarsi P, Mansouri D, Khosravi A, Garssen J, Velayati A, et al. Cancers related to immunodeficiencies: update and perspectives. Front Immunol. 2016;7:365.
Bonilla FA, Barlan I, Chapel H, Costa-Carvalho BT, Cunningham-Rundles C, de la Morena MT, et al. International consensus document (ICON): common variable immunodeficiency disorders. J Allergy Clin Immunol Pract. 2016;4:38–59.
Yong PF, Thaventhiran JE, Grimbacher B. "A rose is a rose is a rose," but CVID is not CVID common variable immune deficiency (CVID), what do we know in 2011? Adv Immunol. 2011;111:47–107.
Gupta S, Pattanaik D, Krishnaswamy G. Common variable immune deficiency and associated complications. Chest. 2019;156:579–93.
Dierickx D, Tousseyn T, Sagaert X, Fieuws S, Wlodarska I, Morscio J, et al. Single-center analysis of biopsy-confirmed posttransplant lymphoproliferative disorder: incidence, clinicopathological characteristics and prognostic factors. Leuk Lymphoma. 2013;54:2433–40.
Choi S, Go JH. Follicular T-cell lymphoma with concomitant Lennert lymphoma. J Pathol Transl Med. 2018;52:425–7.
Pileri SA, Weisenburger DD, Sng I, Nakamura S, Müller-Hermelink HK, Chan WC, Jaffe ES. Peripheral T-cell lymphoma, NOS. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Jürgen T, eds. WHO classification of tumors of haematopoietic and lymphoid tissues: International Agency for Research on Cancer (IARC), 2017. p. 403–407.
Kurita D, Miyoshi H, Yoshida N, Sasaki Y, Kato S, Niino D, et al. A clinicopathologic study of Lennert lymphoma and possible prognostic factors: the importance of follicular helper T-cell markers and the association with angioimmunoblastic T-cell lymphoma. Am J Surg Pathol. 2016;40:1249–60.
Parimal S, Pai R, Manipadam MT, Nair S. Lennert's lymphoma: clinicopathological profile of five cases. Indian J Pathol Microbiol. 2013;56:248–51.
Leung J, Sullivan KE, Perelygina L, Icenogle JP, Fuleihan RL, Lanzieri TM. Prevalence of granulomas in patients with primary immunodeficiency disorders, United States: Data from National Health Care Claims and the US Immunodeficiency Network registry. J Clin Immunol. 2018;38:717–26.
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Kajimoto, Y., Terasaki, Y., Terasaki, M. et al. T-cell lymphoma with a granulomatous lesion of the lungs after autologous hematopoietic stem cell transplantation for Epstein–Barr virus-positive diffuse large B-cell lymphoma: a unique rare case of metachronous B-cell and T-cell lymphoma. Diagn Pathol 15, 125 (2020). https://doi.org/10.1186/s13000-020-01038-3
- Epstein–Barr virus
- Primary immunodeficiency disorder
- Common variable immunodeficiency
- Peripheral T-cell lymphoma
- Diffuse large B-cell lymphoma
- Post-transplant lymphoproliferative disorder
- Autologous hematopoietic stem cell transplantation