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Diffuse Large B-Cell Lymphoma

DLBCL

Diffuse large B-cell lymphoma is the most common type of non-Hodgkin lymphoma and is potentially curable. It may originate from distinct subpopulations of B lymphocytes and manifest in the form of constitutiional symptoms, lymphadenopathy and organ failure.

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Presentation

While the majority of DLBCL arises de novo, it may also result from the transformation of an indolent lymphoma. Thus, patients previously diagnosed with lymphoproliferative diseases like follicular lymphoma may be suspected to have DLBCL if presenting with symptoms consistent with this aggressive malignancy.

Patients suffering from DLBCL usually present with non-specific constitutive symptoms like fever, night sweats, and weight loss. Local invasiveness and rapid growth characterize solid tumors that most frequently develop in lymph nodes. Nevertheless, extranodal involvement is observed in about a third of DLBCL patients, particularly upon recurrence. Accordingly, lymphadenopathy is common, and patients may claim symptoms due to local mass effects mediated by enlarged lymph nodes. For instance, mediastinal lymphadenopathy may be associated with dyspnea, chest pain, and superior vena cava syndrome. Edema may form in poorly drained regions. Distant metastases may affect virtually any organ and may cause a wide variety of symptoms triggered by functional impairment,local mass effects and consequently pain. Patients should be subjected to a thorough physical examination in order to detect primary tumors as well as metastases and to guide the subsequent workup by means of diagnostic imaging.

With regards to DLBCL-induced paraneoplastic syndrome, cutaneous lesions and neurological deficits like erythroderma and cerebellar degeneration have been described.

Mediastinal Lymphadenopathy
  • For instance, mediastinal lymphadenopathy may be associated with dyspnea, chest pain, and superior vena cava syndrome. Edema may form in poorly drained regions.[symptoma.com]
  • lymphadenopathy and displaying some molecular genetic similarities to Hodgkin lymphoma. 3 – 6 A small number of cases do not fit into any of these categories and have been designated as “unclassifiable.” 7 The CHOP (cyclophosphamide, doxorubicin, vincristine[bloodjournal.org]
Splenomegaly
  • One month later, he presented with progressive leukocytosis (mostly neutrophilia) and splenomegaly.[ncbi.nlm.nih.gov]
Cervical Lymphadenopathy
  • PET (positron emission tomography)/CT (computed tomography) was performed and revealed inguinal, pelvic, retroperitoneal, axillary, and cervical lymphadenopathy.[ncbi.nlm.nih.gov]
Axillary Lymphadenopathy
  • We herein report a 56 years old male patient diagnosed with diffuse large B cell lymphoma, after clinically presenting with a visible tumor in the left breast and showing no axillary lymphadenopathy.[ncbi.nlm.nih.gov]
Lymphadenopathy
  • Her lymphadenopathy regressed without treatment. In 2014, the patient presented with nasal obstruction because of a left nasal mass.[ncbi.nlm.nih.gov]
  • One month later, lymphadenopathy was palpated in the neck, the lower left region of the umbilicus, and the left calf. Then he received chemotherapy with rituximab and lenalidomide.[ncbi.nlm.nih.gov]
  • We are reporting a 9-year-old female child presented with diffuse lymphadenopathy postheart transplantation.[ncbi.nlm.nih.gov]
  • Computed tomography showed multiple nodules in the lungs and liver, associated with mediastinal and para-aortic lymphadenopathy. Bone marrow aspiration revealed diffuse large B-cell lymphoma (DLBCL).[ncbi.nlm.nih.gov]
  • We herein report a 56 years old male patient diagnosed with diffuse large B cell lymphoma, after clinically presenting with a visible tumor in the left breast and showing no axillary lymphadenopathy.[ncbi.nlm.nih.gov]
Fever
  • Abstract A 67-year-old man presented with a fever and general malaise. Computed tomography showed multiple nodules in the lungs and liver, associated with mediastinal and para-aortic lymphadenopathy.[ncbi.nlm.nih.gov]
  • In this paper, we discuss a case of a 58-year-old man who presented with fever and fatigue, and was diagnosed with PBM DLBCL.[ncbi.nlm.nih.gov]
  • We report a case of a primary CD20-negative DLBCL in an HIV-infected female patient with an Epstein Barr virus (EBV) coinfection, who presented with generalized lymphadenopathy and fever.[ncbi.nlm.nih.gov]
  • […] initial presentation being single or multiple rapidly growing masses (that may or may not be painful) in nodal or extranodal sites (such as thyroid, skin, breast, gastrointestinal tract, testes, bone, or brain) and that can be accompanied by symptoms of fever[orpha.net]
  • Some people may also develop patches of inflamed skin across their body or experience fevers, night sweats and unexplained weight loss.[leukaemia.org.au]
Falling
  • DLBCL not otherwise specified (NOS): When DLBCL doesn’t fall into one of the subtypes listed above, it is classified as DLBCL not otherwise specified (NOS). A large number of diagnoses fall into this category.[lymphoma.org]
  • DLBCL would fall in the large lymphocyte region as shown below. The CD45 vs FS gating plot reveals both a small(red) and large (green) population of lymphocytes.[wiki.clinicalflow.com]
  • In line with published estimates, first-line clinical trial entry varied widely by disease subtype and age, falling from 59.5% in those aged 15 years to 1.9% in those aged over 75 years - underscoring the need for contextual population-based treatment[ncbi.nlm.nih.gov]
  • Finally, patients with 3, 4, or 5 risk factors fall into a “poor” risk group with a long-term chance of cure in the range of 50%.[bloodjournal.org]
Weight Loss
  • Some people may also develop patches of inflamed skin across their body or experience fevers, night sweats and unexplained weight loss.[leukaemia.org.au]
  • Nevertheless, patients suffering from DLBCL may notice non-specific symptoms like fever, night sweats, and weight loss long before tumors become palpable.[symptoma.com]
  • Some common symptoms patients develop that lead to a specialist include: fevers sweats weight loss Your first tests for diagnosis Your specialist will need to perform a biopsy to confirm if you have Diffuse large B-cell lymphoma.[petermac.org]
  • Some people may also develop reddened patches or lumps in their skin or experience B symptoms (fevers, night sweats and unexplained weight loss). ILCL is often treated with R-CHOP and/or more aggressive therapies.[lymphoma.ca]
Fatigue
  • In this paper, we discuss a case of a 58-year-old man who presented with fever and fatigue, and was diagnosed with PBM DLBCL.[ncbi.nlm.nih.gov]
  • Rarely ( CASE PRESENTATION: A 53-year old man presented to our Dermatology Clinic due to a 1-year history of generalized itching, fatigue of 2-3 month's duration, nausea and mid back rash that was biopsied.[ncbi.nlm.nih.gov]
  • The most common side effects of vistusertib so far include Loss of appetite Tiredness ( fatigue ) Feeling or being sick Diarrhoea Sore mouth or mouth ulcers Tummy pain Skin rash Low level of potassium or phosphate in your blood Confusion High blood pressure[cancerresearchuk.org]
  • Do exercise, like walking, to help you fight fatigue. Check with your doctor first. Have a light meal before chemotherapy sessions to prevent nausea. What to Expect Many people with DLBCL feel OK during treatment and recover within a few months.[webmd.com]
  • Patients may also experience fatigue, loss of appetite, or itchy skin. Diagnosis DLBCL is commonly diagnosed with a biopsy. A biopsy involves removing a sample of tissue (cells), usually performed by a surgeon.[lymphoma.ca]
Cough
  • The lymphoma may press on the trachea and cause trouble breathing or coughing and it can also block the large vein that returns blood to the heart from the arms and head (the superior vena cava), which can make the arms, neck and face swell.[lymphoma.ca]
  • […] and can cause problems due to the pressure of the mass on the lungs or gut, or on the superior vena cava (the second largest vein in the body which returns blood from the upper half of the body to the heart).Symptoms include breathlessness, persistent cough[leukaemia.org.au]
  • You may also have: Fever Drenching night sweats Weight loss Belly or chest pain or pressure Shortness of breath or cough Itching Getting a Diagnosis Your doctor may ask you: Do you have swelling in your groin, armpits, neck, or another part of your body[webmd.com]
  • Possible early symptoms are: breathlessness cough difficulty swallowing swelling of the neck and face headaches dizziness.[lymphomas.org.uk]
Dyspnea
  • For instance, mediastinal lymphadenopathy may be associated with dyspnea, chest pain, and superior vena cava syndrome. Edema may form in poorly drained regions.[symptoma.com]
Nausea
  • Rarely ( CASE PRESENTATION: A 53-year old man presented to our Dermatology Clinic due to a 1-year history of generalized itching, fatigue of 2-3 month's duration, nausea and mid back rash that was biopsied.[ncbi.nlm.nih.gov]
  • Common grade 3-4 adverse events were haematological toxicities (thrombocytopenia in five [8%] patients, anaemia in four [7%], and neutropenia in nine [15%]) and gastrointestinal complications (nausea in five [8%] patients, vomiting in three [5%], and[ncbi.nlm.nih.gov]
  • This can be a tough process because you may get side effects such as mouth and throat sores or nausea and vomiting. You can take medication that eases some of these side effects.[webmd.com]
  • Major toxicities associated with these conditioning regimens included nausea (69%), anorexia (66%), febrile neutropenia (62%), diarrhea (59%), and mucositis (34%).[ncbi.nlm.nih.gov]
Night Sweats
  • sweats and weight loss.[orpha.net]
  • Some people may also develop patches of inflamed skin across their body or experience fevers, night sweats and unexplained weight loss.[leukaemia.org.au]
  • Nevertheless, patients suffering from DLBCL may notice non-specific symptoms like fever, night sweats, and weight loss long before tumors become palpable.[symptoma.com]
  • Some people may also develop reddened patches or lumps in their skin or experience B symptoms (fevers, night sweats and unexplained weight loss). ILCL is often treated with R-CHOP and/or more aggressive therapies.[lymphoma.ca]
  • Patients may also experience fever, weight loss, or drenching night sweats (“B-symptoms”). In approximately 40% of cases, the cancer begins outside of the lymph nodes.[tuftsmedicalcenter.org]
Pruritus
  • PATIENT CONCERNS AND DIAGNOSIS: A 52-year-old man complained of worsening appetite, abdominal distension, and pruritus.[ncbi.nlm.nih.gov]
Headache
  • Most patients relapse in intracranial sites and PATIENT CONCERNS: A 72-year-old woman, first presented 7 years ago with complaints of headache and dizziness.[ncbi.nlm.nih.gov]
  • […] superior vena cava (the second largest vein in the body which returns blood from the upper half of the body to the heart).Symptoms include breathlessness, persistent cough, difficulty swallowing (dysphagia), swelling of the neck and face, dizziness and headaches[leukaemia.org.au]
  • […] the 2017 criteria Diagnosis of Multiple System Atrophy (MSA) Diagnose Multiple Systems Atrophy based on the 2008 criteria Arteriovenous Malformation Coma/Level of Consciousness Demyelinating Disease Dermatome Map Functional Outcome Head & Neck Trauma Headache[qxmd.com]
  • Other symptoms include difficulty swallowing (dysphagia), dizziness and headaches. Treatment usually involves the use of R-CHOP followed by radiotherapy and PMBL usually responds well to treatment.[lymphoma.ca]
  • Possible early symptoms are: breathlessness cough difficulty swallowing swelling of the neck and face headaches dizziness.[lymphomas.org.uk]
Ataxia
  • PMID 9824206 Acquired chromosome 11q deletion involving the ataxia teleangiectasia locus in B-cell non-Hodgkin's lymphoma: correlation with clinicobiologic features.[atlasgeneticsoncology.org]

Workup

The diagnosis of DLBCL is based on histopathological, immunohistochemical and molecular features of tumors and tumor cells. In order to carry out the respective analyses, an excisional biopsy of an enlarged lymph node should be performed. Tissue samples obtained by means of core biopsy may also be examined, particularly if an excisional biopsy is not feasible. Fine-needle aspiration analyses is not advisable for lymphoma diagnosis [11]. In the case of extranodal tumor growth, tissue samples can be obtained from the respective sites.

Computed tomography scans, as well as positron emission tomography/computed tomography (PET/CT) are of great value to visualize tumors in the thoracic or abdominal cavity, while cardiac involvement is generally assessed by means of echocardiography. This information is essential for tumor staging, for estimating the patient's prognosis and choosing an appropriate therapy. It is to be noted that extranodal tumors most commonly develop in the liver,spleen, bone marrow, gastrointestinal tract, lungs, serous membranes, kidneys and adrenal glands, breasts, testicles, skin and the central nervous system. Although bone marrow biopsies have been routinely performed to detect bone marrow involvement in DLBCL patients, they do not seem to add diagnostic or prognostic value after the performance of PET/CT [13].

Furthermore, laboratory analyses of blood samples should be carried out to assess the patient's general condition and organ function as well as lactate dehydrogenase levels. Due to a high incidence rate of DLBCL in people infected with human immunodeficiency virus and hepatitis C virus, patients should be tested in this regards. The distinction between Epstein-Barr virus positive and negative patients is of prognostic relevance [14].

Right Pleural Effusion
  • A CT of an abdomen and pelvis with contrast was performed and revealed bilateral large heterogeneous pelvic adnexal masses with large ascites and right pleural effusion. Tumour markers CA 125 was 766 U/mL and lactate dehydrogenase was 654 U/L.[ncbi.nlm.nih.gov]
Polyps
  • KEYWORDS: Diffuse large B-cell lymphoma; Intrauterine device; Uterine polyp[ncbi.nlm.nih.gov]

Treatment

Combination of anti-CD20 monoclonal antibody rituximab with classical chemotherapeutic regimens (namely CHOP: cyclophosphamide, hydroxy daunomycin, vincristine, and prednisone) is the mainstay of DLBCL treatment. Etoposide may be added if so indicated by the results of molecular analyses [11]. Moreover, the combined application of etoposide or methotrexate with doxorubicin, cyclophosphamide, vincristine, prednisolone and bleomycin (VACOP-B or MACOP-B, respectively) has proven effective in DLBCL patients. For patients with bone marrow, testicular or epidural involvement, prophylactic systemic or intrathecal application of methotrexate has been recommended to prevent central nervous system compromise [15]. Evidence proving the efficacy of this procedure is scarce, though. Additionally, patients may be considered for consolidative radiotherapy, especially if low-dose or abbreviated chemotherapy has been employed.

Due to the systemic character of the disease, resection of tumors is rarely curative. However, surgical interventions may relieve symptoms and are an essential part of therapy in certain subtypes of DLBCL, e.g., in primary testicular DLBCL. Patients who don't response favorably to the aforementioned therapies can be recommended for hematopoietic stem cell transplantation (HSCT). Owing to the inherent risks of this procedure and encouraging success rates of chemo-immunotherapy, HSCT is not a first-line treatment even in high-risk patients [15].

It is to be expected that future therapeutic regimens will take greater account of the histological and molecular features of tumor cells encountered in an individual patient. Personalized therapy may target B cell receptor or NF-κB signaling pathways, constitutively active enzymes and cytokine-mediated effects, among others [4].

Prognosis

The prognosis for patients diagnosed with DLBCL depends on a variety of factors:

  • Overall survival rates of patients suffering from germinal center DLBCL or primary mediastinal B cell lymphoma are higher than those observed in individuals affected by activated B cell-like DLBCL. For germinal center DLBCL, five-year-survival rates of more than 80% have been reported, while only half of those people diagnosed with activated B cell-like DLBCL remain alive after this time [11].
  • Use of the monoclonal antibody rituximab for DLBCL treatment has considerably improved the prognosis of patients with DLBCL.
  • Advanced age, enhanced serum concentrations of lactate dehydrogenase, worse Eastern Cooperative Oncology Group performance status, Ann Arbor stage III to IV, and extranodal involvement are unfavorable prognostic factors. Each patient may be assigned an individual risk according to the enhanced International Prognostic Index developed by the National Comprehensive Cancer Network of the United States (NCCN-IPI) [12]. In this context, five-year-survival rates of 90 and 54% have been observed in low- and high-risk patient groups, respectively.

Etiology

DLBCL is the result of malignant transformation and uncontrolled proliferation of B lymphocytes, but the causes of this degeneration remain unknown. A variety of conditions have been associated with the development of this lymphoproliferative disorder, namely B cell-activating autoimmune disease, acquired immunodeficiency, infection with hepatitis C virus, as well as a family history of non-Hodgkin or Hodgkin lymphoma [2] [3]. These observations imply DLBCL to be a multifactorial disease. Presumably, exposure of a genetically predisposed individual to certain environmental factors provokes the onset of this neoplasm.

With regards to the gene defects underlying malignant transformation, considerable differences exist among DLBCL subtypes [1] [4] [5]:

  • In germinal center DLBCL, translocation t(14;18) results in a dysregulation of the anti-apoptotic protein encoded by protooncogene BCL2 (B cell lymphoma 2). Furthermore, mutation of BCL6 (B cell lymphoma 6: encodes for a transcription factor involved in cell cycle regulation), deletion of PTEN (phosphatase and tensin homolog: encodes for an enzyme involved in the regulation of cell division and growth), deletion of ING1 and mutation of TP53 (both encoding for tumor suppressors), as well as gain-of-function mutations of oncogene MDM2 (encodes for E3 ubiquitin-protein ligase) and a variety of other gene defects have been reported.
  • Dysregulation of BCL2 and BCL6 also contribute to activated B cell-like DLBCL pathogenesis. Mutation or deletion of signaling molecules CD79A and CD79B result in constitutive activation of B cell receptor signaling, while loss of function of proteins encoded by CARD11 (caspase-associated recruitment domain 11) and MYD88 (myeloid differentiation primary response 88) favors an abnormal activation of NF-κB signaling pathways. These and other gene defects provoke genomic instability and a maturation arrest.
  • Amplification of chromosomal bands of the short arms of chromosomes 2 and 9 is most characteristic of primary mediastinal B cell lymphoma. Genes located here encode for the anti-apoptotic transcription factor c-Rel, for Janus kinase 2, a non-receptor tyrosine kinase affecting the responsiveness to growth factors, and several other proteins. BCL2 and BCL6 are usually unaltered in this type of DLBCL.

On an average, B cell clones found in DLBCL samples per case present more than 30 gene alterations [6].

Epidemiology

DLBCL account for up to 40% of non-Hodgkin lymphoma and their annual incidence has been estimated to 3.8 per 100,000 inhabitants in Europe [7]. During the last decades, incidence rates have been rising [8]. Most patients diagnosed with DLBCL suffer from germinal center DLBCL. Primary mediastinal B cell lymphoma is the least frequent entity and affects less than 10% of this patient group [9].

A slight predilection for males has been observed with the incidence rates increasing with age [7]. However, corresponding epidemiological data vary considerably depending on the subtype of DLBCL. The respective differences are best illustrated by the fact that primary mediastinal B cell lymphoma preferentially affects women in the 30 -35 age group [1].

Sex distribution
Age distribution

Pathophysiology

This malignancy is characterized by an uncontrolled proliferation of B lymphocytes. In general, B cells develop from hematopoietic stem cells and progress through different developmental stages until they arrive in the secondary follicles of lymph nodes and spleen. Secondary follicles comprise a germinal center and are rich in B lymphocytes that proliferate, differentiate and undergo somatic hypermutation before being selected by T helper cells located in the periphery. Additionally, a small proportion of the B cell population may be encountered in the thymus. Their function remains largely unclear, but they have been suggested to be involved in T cell selection [10]. Malignant transformation of B cells during any of the aforementioned developmental stages may give rise to germinal center DLBCL, activated B cell-like DLBCL (also referred to as post-germinal center DLBCL), and primary mediastinal B cell lymphoma.

Prevention

No specific measures can be recommended to prevent DLBCL.However, it is recommended that necessary steps should be taken to reduce the individual risk of contracting human immunodeficiency virus and hepatitis C virus.

Summary

Diffuse large B-cell lymphoma (DLBCL) is the most common type of non-Hodgkin lymphoma and refers to a heterogeneous group of malignancies originating from distinct subpopulations of B lymphocytes. Nevertheless, all forms of DLBCL are characterized by diffuse growth patterns and the presence of large, degenerated lymphocytes as observable during histopathological analyses of tissue specimens.

The following subtypes of DLBCL have been identified by means of gene expression profiling [1]:

  • Germinal center DLBCL
  • Activated B cell-like DLBCL
  • Primary mediastinal B cell lymphoma

Further classification of DLBCL may be based on morphological features of tumor cells and immune cells encountered in biopsy samples, site of primary tumor growth, the patient's seropositivity or negativity for Epstein-Barr virus as well as the presence of chronic inflammation.

Patient Information

Diffuse large B-cell lymphoma (DLBCL) is a very common subtype of non-Hodgkin lymphoma. It is characterized by an uncontrolled proliferation of B lymphocytes that may form solid tumors in lymph nodes, liver and spleen and other organs. These tumors typically grow rapidly and may cause pain or functional impairment of affected organs or tissues located in close proximity. Nevertheless, patients suffering from DLBCL may notice non-specific symptoms like fever, night sweats, and weight loss long before tumors become palpable.

Imaging techniques like computed tomography scans and positron emission tomography are employed to detect tumors in the patient's body,and to assess the extension of the disease. Still, histopathological analyses of biopsy specimens are required to confirm a tentative diagnosis of DLBCL. Other types of lymphoma may trigger similar symptoms, but differ with regards to the patient's prognosis and treatment regimens. Additional measures may be taken to rule out the involvement of vital organs such as the bone marrow and the central nervous system.

Patients diagnosed with DLBCL are usually treated with chemotherapeutics. Rituximab, an antibody directed against a specific molecule expressed by B lymphocytes, has been used for a few years in addition to standard chemotherapeutic regimens and survival rates have since increased considerably. Radiotherapy may be indicated in some cases. The usefulness of surgical tumor resection is very limited. A small group of patients may be considered for hematopoietic stem cell transplantation. In sum, five-year-survival rates range between 50 and 90%, depending on the patient's condition at the time of diagnosis and the precise subtype of DLBCL.

References

Article

  1. Frick M, Dorken B, Lenz G. The molecular biology of diffuse large B-cell lymphoma. Ther Adv Hematol. 2011; 2(6):369-379.
  2. Engels EA, Biggar RJ, Hall HI, et al. Cancer risk in people infected with human immunodeficiency virus in the United States. Int J Cancer. 2008; 123(1):187-194.
  3. Morton LM, Slager SL, Cerhan JR, et al. Etiologic heterogeneity among non-Hodgkin lymphoma subtypes: the InterLymph Non-Hodgkin Lymphoma Subtypes Project. J Natl Cancer Inst Monogr. 2014; 2014(48):130-144.
  4. Dunleavy K, Wilson WH. Primary mediastinal B-cell lymphoma and mediastinal gray zone lymphoma: do they require a unique therapeutic approach? Blood. 2015; 125(1):33-39.
  5. Schneider C, Pasqualucci L, Dalla-Favera R. Molecular pathogenesis of diffuse large B-cell lymphoma. Semin Diagn Pathol. 2011; 28(2):167-177.
  6. Pasqualucci L, Trifonov V, Fabbri G, et al. Analysis of the coding genome of diffuse large B-cell lymphoma. Nat Genet. 2011; 43(9):830-837.
  7. Sant M, Allemani C, Tereanu C, et al. Incidence of hematologic malignancies in Europe by morphologic subtype: results of the HAEMACARE project. Blood. 2010; 116(19):3724-3734.
  8. Friedberg JW, Fisher RI. Diffuse large B-cell lymphoma. Hematol Oncol Clin North Am. 2008; 22(5):941-952, ix.
  9. Savage KJ. Primary mediastinal large B-cell lymphoma. Oncologist. 2006; 11(5):488-495.
  10. Perera J, Huang H. The development and function of thymic B cells. Cell Mol Life Sci. 2015; 72(14):2657-2663.
  11. Caimi PF, Hill BT, Hsi ED, Smith MR. Clinical approach to diffuse large B cell lymphoma. Blood Rev. 2016.
  12. Zhou Z, Sehn LH, Rademaker AW, et al. An enhanced International Prognostic Index (NCCN-IPI) for patients with diffuse large B-cell lymphoma treated in the rituximab era. Blood. 2014; 123(6):837-842.
  13. Alzahrani M, El-Galaly TC, Hutchings M, et al. The value of routine bone marrow biopsy in patients with diffuse large B-cell lymphoma staged with PET/CT: a Danish-Canadian study. Ann Oncol. 2016; 27(6):1095-1099.
  14. Grywalska E, Rolinski J. Epstein-Barr virus-associated lymphomas. Semin Oncol. 2015; 42(2):291-303.
  15. Vitolo U, Seymour JF, Martelli M, et al. Extranodal diffuse large B-cell lymphoma (DLBCL) and primary mediastinal B-cell lymphoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016; 27(suppl 5):v91-v102.

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Last updated: 2018-06-21 19:25