Hepatosplenic T cell lymphoma

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Historical Perspective

Classification

Pathophysiology

Causes

Epidemiology and Demographics

Risk Factors

Screening

Differentiating Hepatosplenic T cell lymphoma from other Diseases

Natural History, Complications and Prognosis

Diagnosis

Staging

History and Symptoms

Physical Examination

Laboratory Findings

Biopsy

CT

MRI

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Editor-In-Chief: C. Michael Gibson, M.S., M.D. [2]; Associate Editor(s)-in-Chief: Jogeet Singh Sekhon, M.D. [3]

Synonyms and Keywords: Hepatosplenic γδ T-cell lymphoma, Hepatosplenic gamma delta T-cell lymphoma, HSTCL

Overview

Hepatosplenic T cell lymphoma is a rare type of non Hodgkins lymphoma that occurs in states of immunosupression such as post organ transplant and treatment of inflammatory bowel disease. Hepatosplenic T cell lymphoma was discovered by Farcet et al in 1990. It is also known as "gamma-delta" hepatosplenic T-cell lymphoma. The lymphoma is characterized by malignant T-cell proliferation in the sinusoids of the liver, sinuses and red pulp of the spleen, and sinuses of the bone marrow. The incidence of hepatosplenic T cell lymphoma is 0.3 per 100000 individuals per year. If left untreated, patients can develop liver failure, pancytopenia or spleen rupture. Biopsy of the tumor is the gold standard diagnostic test for diagnosing hepatosplenic T-cell lymphoma. Chemotherapy including CHOP is the mainstay of the treatment along with bone marrow transplant and radiation therapy.

Historical Perspective

Hepatosplenic T cell lymphoma was discovered by Farcet et al in 1990.

Classification

There is no established system for the classification of hepatosplenic T cell lymphoma.

Pathophysiology

  • Hepatosplenic T-cell lymphoma is a peripheral T-cell lymphoma, a type of non Hodgkin's lymphoma.[1]
  • It is also known as "gamma-delta hepatosplenic T-cell lymphoma".[2]
  • It usually occurs in young men with history of immunosuppression including solid organ transplantation.[3]
  • Patients with inflammatory bowel disease receiving immunosuppressants and anti-tumor necrosis factor-α agent are also at risk for developing hepatosplenic T-cell lymphoma.
  • The T-cell receptor consists of either a gamma delta or alpha-beta entity on their cell surface which are a part of the innate immune system.[4][5]
  • Gamma delta T cells represent the first line of defense against bacterial peptides, such as heat-shock proteins.
  • Gamma delta T cells are CD4 and CD8 negative, but CD56 positive which is NK cell marker.
  • Gamma delta cells respond to a stimulus and are responsible for lymphokine production and proliferation.
  • Gamma delta cells are predominantly located in the spleen, liver sinusoids and intestinal epithelium.
  • 75 % of the cases are of gamma delta phenotype and the rest are apha beta phenotype.
  • Chronic antigen stimulation in states of immunosuppression is responsible for the development of the lymphoma.
  • Isochromosome of the long arm of chromosome 7 is a genetic abnormality described in hepatosplenic T cell lymphoma. It could also be in association with trisomy 8 and a loss of a sex chromosome.
  • Mutations in SETD2, INO80, TET3 and STAT5B occur exclusively in hepatosplenic T cell lymphoma as compared to other T and B cell lymphoma types.
  • The lymphoma is characterized by malignant T-cell proliferation in the sinusoids of the liver, sinuses and red pulp of the spleen, and sinuses of the bone marrow.
  • Splenic involvement is characterized by diffuse involvement of the red pulp with small-to-medium-sized atypical lymphocytes.
  • The atypical lymphocytes are present within the cords and sinuses of the red pulp.
  • There occurs a complete loss of the white pulp.
  • The liver also shows sinusoidal infiltration by neoplastic lymphoid cells.
  • The bone marrow is characterized by neoplastic cells in the sinusoids.
  • Bone marrow infiltration results in pancytopenia.
  • The lymphoma cells are typically CD2+, CD3+, CD4−, CD5−, CD7+, CD8− CD42+, CD52+, CD76+, CD82+ with either gamma-delta or alpha-beta T-cell phenotypic receptor expression.
  • It manifests as hepatosplenomegaly without peripheral lymphadenopathy.
  • Pancytopenia and abnormal liver functions are the laboratory findings.
  • Histology and immunohistochemistry of the tumor biopsy shows portal and sinusoidal infiltration by atypical small-to-medium sized lymphocytes with hyperchromatic nuclei and low mitotic activity.

Causes

Common causes of hepatosplenic T cell lymphoma are: [6][7]

Differentiating hepatosplenic T cell lymphoma from Other Diseases

Differential diagnosis for the lymphoma is based on the below table:

Differentiating diagnosis of Lymphoma Symptoms Signs Diagnosis Additional Findings
Fever Rash Diarrhea Abdominal pain Weight loss Painful lymphadenopathy Hepatosplenomegaly Arthritis Lab Findings
Lymphoma + – – + + – + – Increase ESR, increased LDH Night sweats, constant fatigue
Brucellosis + + – + + + + + Relative lymphocytosis Night sweats, often with characteristic smell, likened to wet hay
Typhoid fever + + – + – – + + Decreased hemoglobin Incremental increase in temperature initially and than sustained fever as high as 40°C (104°F)
Malaria + – + + – – + + Microcytosis,

elevated LDH

"Tertian" fever: paroxysms occur every second day
Tuberculosis + + – + + + – + Mild normocytic anemia, hyponatremia, and

hypercalcemia

Night sweats, constant fatigue
Mumps + – – – – + – – Relative lymphocytosis, serum amylaseelevated Parotidswelling/tenderness
Rheumatoid arthritis – + – – – – – + ESR and CRP elevated, positive rheumatoid factor Morning stiffness
SLE – + – + + – – + ESR and CRP elevated, positive ANA Fatigue
HIV – – – + + + – + Leukopenia Constant fatigue

Differentiating different types of T-cell Non-Hodgkin lymphoma. The gold standard for differentiation different types of Non-Hodgkin lymphoma is biopsy.

Disease Etiology Clinical manifestations Paraclinical findings Associated findings
Lab findings
Symptoms Signs Immunochemistry Histopathology
Constitutional symptoms Rash Abdominal

pain

Diarrhea Mass Other
Hodgkin's Lymphoma
[8][9][10][11][12]
  • Activation of (NF-kB)
  • Mutations in JAK-STAT pathway
  • NF-kB leads to activation of many genes like:
- ± -
  • Painless lymphadenopathy with a rubbery consistency.
  • Mostly above the diaphram
Nodular lymphocyte predominant
  • Effacement of the lymph node architecture by Reed-Sternberg cells .
  • Reed-Sternberg cell is a large often bi-nucleated cells with prominent nucleoli and an unusual immuno phenotype.
Non-Hodgkin's Lymphoma (B Cell Lymphoma)
Diffuse large B cell lymphoma
[13][14][15][16][17][18]
  • Mature B-cell Lymphoma
  • 8q24/MYC translocations
  • Hypermutated immunoglobulin genes
  • Mutation of BCL6, MYC, PAX5, PIM1, RhoH /TTFn, TP53 genes
  • Translocations involving c-MYC, BCL6, and IgH gene.
 - + +
  • CD20
  • CD3
  • CD5
  • CD45
  • CD10
  • BCL-2
  • BCl-6
  • MYC
  • IRF-4/ MUM-1
  • Ki-67

Centroblastic

Immunoblastic

  • > 90% immunoblasts
  • Trapezoid shaped large lymphoid cells with significant basophilic cytoplasm

Anaplastic

  • Very large cells with a round, oval, or polygonal shape that may resemble Reed-Sternberg cells
 _
Mantle cell lymphoma
[19][20][21][22][23] 		– + +
  • CD5+
  • B-cell antigen positive
  • Overexpression of Cyclin D1
  • Germinal centers filled by small-to-medium atypical lymphocytes
  • Nodular appearance
 Abdominal distention
B-lymphoblastic leukemia/lymphoma
[24][25][26]
  • Precursor B-cell lymphoma
  • Unknown
  • Inherited mutations of PAX5, ETV6, and TP53
 + – – –
  • CD20+
  • CD10+
  • Consists of small to medium-sized lymphoid cells with blastic nuclear chromatin and a high mitotic rate.
Follicular lymphoma
[27][28][29][30][31]
  • Mature B-cell lymphoma
  • Reciprocal translocation t(14;18)
  • Overexpression of BCL2
 20% of patients present with: + + ±
  • CD21
  • CD23
  • Nodular growth pattern
  • Most common clinically indolent NHL
  • Peripheral nerve compression
Burkitt's lymphoma
[32][33][34][35][36][37][38][39]
  • Mature B-cell lymphoma
  • Translocation of chromosome 8 myc locus such as:
    • t(8;14)
    • t(2;8)
    • t(8;22)
 – + –
  • Round and small nucleoli
  • basophilic cytoplasm
  • "Starry-sky pattern"
B cell chronic lymphocytic leukemia/small lymphocytic lymphoma
[40]
  • Mature B-cell Lymphoma
  • Ch 13 abnormalties

33% of patients present with:

– – –
  • CD5
  • CD38
  • Monoclonal small well differentiated B cells.
  • Significant number of smudge cells or basket cells.
Marginal zone lymphoma Extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue (MALT) type
[41][42][43][44][45][46][47][48][49][50]
  • Mature B-cell lymphoma
  • Recurrent translocation of such as:
    • t(1;14)(p22;q32)
    • t(11;18)(q21;q21)
    • t(14;18)(q32;q21)
    • t(3;14)(p14.1;q32)
  • B symptoms may or may not be present
 ± + + B-cell associated antigens that co-express

Negative for:

  • Presence of dense diffuse lymphoid infiltrate of marginal‐zone cells in lamina propria
  • Prominent lymphoepithelial lesions and consisting of small atypical cells with monocytoid features.
Splenic marginal zone lymphoma
[51][52][53][54][55][56][57]
  • Mature B-cell lymphoma
  • Clonal rearrangements of the immunoglobulin genes (heavy and light chains)
    • Deletion 7q21-32
    • Translocations of the CDK6 gene located on 7q21
 + + –
  • Small lymphocytes
  • Transformed blasts
  • Epithelial histocytes
  • Plasmacytic differentiation of neoplastic cells
Nodal marginal zone B-cell lymphoma
[58][59]
  • Mature B-cell Lymphoma
  • Stimulation of antigen receptor by autoantigen and co-stimulatory molecule CD40
  • Mutations in KMT2D, PTTPRD, NOTCH2, KLF2
 + – –
  • Follicular cells in reactive zone
  • Centrocyte like cells in marginal zone lymphoma
Lymphoplasmacytic lymphoma (Waldenstrom’s macroglobulinemia)
[60][61][62][63][64] 		– – + Express pan B-cell antigens

Variable expression of

Majority express:

  • IgM surface immunoglobulin

Fewer express

  • Russell bodies (intracytoplasmic inclusions) and Dutcher bodies (intranuclear inclusions)
  • Prominent epithelioid histiocytes
Hairy cell leukemia
[65][66][67][68][69]
  • Production of cytokines, such as TNF alpha and IL-2R, provide important stimuli for malignant B cells proliferation in hairy cell leukemia.
    • The p38-MAPK-JNK cascade
    • The MEK-ERK cascade
    • The Phosphatidylinositol 3 kinase (PI3K)-AKT cascade
 – + –
  • N/A
  • Small cells with "fried egg"-like appearance
  • Well-demarcated thread-like cytoplasmic extensions
  • Clear cytoplasm
  • Central round nucleus
  • Peri-nuclear clearing ("water-clear rim" appearance)
Disease Etiology Constitutional symptoms Rash Abdominal pain Diarrhea Mass/Lesion Other Immunochemistry Histopathology Associated findings
Non-Hodgkin's Lymphoma (T Cell Lymphoma)
Precursor T-cell lymphoblastic leukemia/lymphoma
[70][71]
  • Precursor T-cell lymphomas
 + - -
T-cell granular lymphocytic
[72][73][74] 		- - - May be associated with the following conditions:
T-cell prolymphocytic leukemia
[75]
  • Abnormal proliferation of mature T cells (post thymic)
 + - -
  • Lymphocytes with abundant basophilic, nongranular cytoplasm, atypical nucleus
  • Cytoplasmic protrusions (blebs)
Adult T cell leukemia/lymphoma
[76][77][78] 		+ - -
  • Charecterstic leukemia cells with sharp nuclear indentations and a prominent nucleoli
  • "Cloverleaf" or "flower" cells
Anaplastic large cell lymphoma
[79][80][81][82]
  • Mature T-cell lymphoma
 + + -

Painless swelling in :

Strongly immunoreactive for :
  • Nucleoli tend to be more prominent
  • The cytoplasm may be either basophilic or eosinophilic and the cell might have many nuclei with dispersed or clumped chromatin
  • May be caused by textured breast implants
Cutaneous T-cell lymphoma Mycosis fungoides / Sézary syndrome
[83][84][85] 		+ + -
  • Cutaneous manifestations
  • Polymorphous inflammatory infiltrate in the dermis that contains small numbers of frankly atypical lymphoid cells
  • These cells may line up individually along the epidermal basal layer
  • The presence of spongiosis is highly suggestive of mycosis fungoides
Peripheral T-cell lymphoma Subcutaneous panniculitis-like T-cell lymphoma
[86][87][88]
  • Mature T-cell lymphoma
 - - - Painless swellings on:
  • Extremities
  • Trunks
 Positive for:
Hepatosplenic T-cell lymphoma
[89][90][91] 		+ + - Painless swelling in :
  • Intermediate sized tumor cells with clear cytoplasm, oval nuclei, slightly dispersed condensed chromatin, inconspicuous nucleoli
  • Patients with inflammatory bowel diseases taking immunosuppressant and anti-tumor necrosis factor-α agent are also have a higher risk for developing hepatosplenic T-cell lymphoma
Enteropathy-type intestinal T-cell lymphoma
[92][93][94]
  • Mature T-cell lymphoma
 + + + Painless swelling in the :
  • Lymphomatous infiltrate with neoplastic large cells
  • May have pleomorphic, multinucleated cells
  • Adjacent mucosa shows villous atrophy, crypt hyperplasia, increased inflammatory cells
  • Lymphocytosis
  • Mostly diagnosed in the small intestine
Extranodal T-cell lymphoma, nasal type
[95][96][97]
  • Mature T-cell lymphoma
 + - - Painless swelling in :
  • Medium sized tumor cells and polymorphic infiltrate of non-neoplastic inflammatory cells
  • Lymphoma cells may be admixed with a polymorphic infiltrate of non-neoplastic inflammatory cells
Angioimmunoblastic T-cell lymphoma
[98][99][100]
  • Mature T-cell lymphoma
 + + -
Peripheral T-cell lymphoma, unspecified
[101][102]
  • Mature T-cell lymphoma
 - + -
  • Clear cytoplasm, resemble Reed-Sternberg cells, with irregular, pleomorphic, hyperchromatic or nuclei
  • A lot of mitotic figures; very broad cytologic spectrum

Epidemiology and Demographics

  • The incidence of hepatosplenic t cell lymphoma is 0.3 per 100000 individuals per year.
  • It occurs in younger group of patients, most cases falling in 20-40 years of age group.
  • Men are more affected than the females.

Risk Factors

Common risk factors include:

Screening

There is insufficient evidence to recommend routine screening for hepatosplenic T cell lymphoma.

Natural History, Complications, and Prognosis

Natural history

  • Patients have a history of immunosupression such as inflammatory bowel disease under treatment or organ transplant.[103]
  • The mean age group is 35 years and most of the patients are males.
  • Initial symptoms are fever, weight loss, night sweats and then progress to more severe symptoms depending on the organ involvement but there is no lymphadenopathy.
  • Patients also present with symptoms of liver, spleen and bone marrow dysfunction.
  • If left untreated, patients can develop liver failure, pancytopenia, or spleen rupture.

Complications

Prognosis

  • The prognosis is very poor, with patients dying within 2-3 years of diagnosis even after recieving treatment[104].

Diagnosis

Diagnostic Study of Choice

  • Biopsy of the tumor is the gold standard diagnostic test for diagnosing hepatosplenic T cell lymphoma[105].
  • CT scan and PET scan are used to assess the spread of the lymphoma.

Symptoms

The most common symtoms are[106]:

  • Fever
  • Weight loss
  • Night sweats
  • Pain abdomen
  • Jaundice
  • Fatigue
  • Recurrent infections
  • Bleeding

Physical Examination

Temperature

Skin

Thorax

Abdomen

Extremities

Laboratory Findings

  • Biopsy of the tumor:
    • Histology - small-to intermediate sized T lymphocytes infiltrate the sinusoids of the liver and the splenic red pulp.
    • Flow cytometry and immunophenotyping - The lymphoma cells are typically CD2+, CD3+, CD4−, CD5−, CD7+, CD8− CD42+, CD52+, CD76+, CD82+ with either gamma-delta or alpha-beta T-cell phenotypic receptor expression[107].
    • Karyotyping - Isochromosome of the long arm of chromosome 7 is a genetic abnormality described in hepatosplenic t cell lymphoma. It could also be in association with trisomy 8 and a loss of a sex chromosome[108].
  • Bone marrow biopsy; The bone marrow is characterized by neoplastic cells in the sinusoids.
  • Complete blood count; Pancytopenia
  • Liver function tests: Deranged LFT

Electrocardiogram

There are no ECG findings associated with hepatosplenic T cell lymphoma.

X-ray

There are no x-ray findings associated with hepatosplenic T cell lymphoma but pleural effusion might be present.

Echocardiography or Ultrasound

  • There are no echocardiography findings associated with hepatosplenic T cell lymphoma.
  • On ultrasound of abdomen:

CT scan

Tumor mass can be seen in liver or spleen or both.

MRI

Tumor mass can be seen in liver or spleen or both.

Other Imaging Findings

PET scan: On PET scan, tumor mass can be seen in liver or spleen or if it has metastasized to any other organ.

Treatment

Medical Therapy

Surgery

Surgical intervention is not recommended for the management of hepaosplenic T cell lymphoma.

Primary Prevention

There are no established measures for the primary prevention of hepatosplenic T cell lymphoma.

Secondary Prevention

There are no established measures for the secondary prevention of hepatosplenic T cell lymphoma.

References

  1. ↑ Armitage JO (2017). "The aggressive peripheral T-cell lymphomas: 2017". Am J Hematol. 92 (7): 706–715. doi:10.1002/ajh.24791. PMID 28516671.
  2. ↑ Brandt PH, Rahmat LT, Ali SS (2019). "A rare case of hepatosplenic gamma-delta T-cell lymphoma and secondary hemophagocytic lymphohistiocytosis". Clin Case Rep. 7 (1): 164–169. doi:10.1002/ccr3.1924. PMC 6333078. PMID 30656034.
  3. ↑ Choi Y, Jeon SY, Yoo WH (2018). "Hepatosplenic T-Cell Lymphoma Arising in a Patient Treated With Tumor Necrosis Factor-α Inhibitors for Ankylosing Spondylitis". J Clin Rheumatol. doi:10.1097/RHU.0000000000000805. PMID 29933321.
  4. ↑ Gowda L, Foss F (2019). "Hepatosplenic T-Cell Lymphomas". Cancer Treat Res. 176: 185–193. doi:10.1007/978-3-319-99716-2_9. PMID 30596219.
  5. ↑ Gaulard P, Bourquelot P, Kanavaros P, Haioun C, Le Couedic JP, Divine M; et al. (1990). "Expression of the alpha/beta and gamma/delta T-cell receptors in 57 cases of peripheral T-cell lymphomas. Identification of a subset of gamma/delta T-cell lymphomas". Am J Pathol. 137 (3): 617–28. PMC 1877506. PMID 1698028.
  6. ↑ Yabe M, Miranda RN, Medeiros LJ (2018). "Hepatosplenic T-cell Lymphoma: a review of clinicopathologic features, pathogenesis, and prognostic factors". Hum Pathol. 74: 5–16. doi:10.1016/j.humpath.2018.01.005. PMID 29337025.
  7. ↑ Gallamini A, Stelitano C, Calvi R, Bellei M, Mattei D, Vitolo U; et al. (2004). "Peripheral T-cell lymphoma unspecified (PTCL-U): a new prognostic model from a retrospective multicentric clinical study". Blood. 103 (7): 2474–9. doi:10.1182/blood-2003-09-3080. PMID 14645001.
  8. ↑ Mauch PM, Kalish LA, Kadin M, Coleman CN, Osteen R, Hellman S (March 1993). "Patterns of presentation of Hodgkin disease. Implications for etiology and pathogenesis". Cancer. 71 (6): 2062–71. PMID 8443755.
  9. ↑ Gobbi PG, Cavalli C, Gendarini A, Crema A, Ricevuti G, Federico M, Di Prisco U, Ascari E (December 1985). "Reevaluation of prognostic significance of symptoms in Hodgkin's disease". Cancer. 56 (12): 2874–80. PMID 4052959.
  10. ↑ Buri C, Körner M, Schärli P, Cefai D, Uguccioni M, Mueller C, Laissue JA, Mazzucchelli L (March 2001). "CC chemokines and the receptors CCR3 and CCR5 are differentially expressed in the nonneoplastic leukocytic infiltrates of Hodgkin disease". Blood. 97 (6): 1543–8. PMID 11238088.
  11. ↑ Peh SC, Looi LM, Pallesen G (March 1997). "Epstein-Barr virus (EBV) and Hodgkin's disease in a multi-ethnic population in Malaysia". Histopathology. 30 (3): 227–33. PMID 9088951.
  12. ↑ Andriko JA, Aguilera NS, Nandedkar MA, Abbondanzo SL (April 1997). "Childhood Hodgkin's disease in the United States: an analysis of histologic subtypes and association with Epstein-Barr virus". Mod. Pathol. 10 (4): 366–71. PMID 9110300.
  13. ↑ Colomo, L.; López-Guillermo, A; Perales, M; Rives, S; Martínez, A; Bosch, F; Colomer, D; Falini, B; Montserrat, E; Campo, E (2002). "Clinical impact of the differentiation profile assessed by immunophenotyping in patients with diffuse large B-cell lymphoma". Blood. 101 (1): 78–84. doi:10.1182/blood-2002-04-1286. PMID 12393466.
  14. ↑ Hans, C. P.; Weisenburger, D. D.; Greiner, T. C.; Gascoyne, R. D.; Delabie, J; Ott, G; Müller-Hermelink, H. K.; Campo, E; Braziel, R. M.; Jaffe, E. S.; Pan, Z; Farinha, P; Smith, L. M.; Falini, B; Banham, A. H.; Rosenwald, A; Staudt, L. M.; Connors, J. M.; Armitage, J. O.; Chan, W. C. (2004). "Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray". Blood. 103 (1): 275–82. doi:10.1182/blood-2003-05-1545. PMID 14504078.
  15. ↑ Muris, JJF; Meijer, Cjlm; Vos, W; Van Krieken, Jhjm; Jiwa, NM; Ossenkoppele, GJ; Oudejans, JJ (2006). "Immunohistochemical profiling based on Bcl-2, CD10 and MUM1 expression improves risk stratification in patients with primary nodal diffuse large B cell lymphoma". The Journal of Pathology. 208 (5): 714–23. doi:10.1002/path.1924. PMID 16400625.
  16. ↑ Korkolopoulou P, Vassilakopoulos T, Milionis V, Ioannou M (2016). "Recent Advances in Aggressive Large B-cell Lymphomas: A Comprehensive Review". Adv Anat Pathol. 23 (4): 202–43. doi:10.1097/PAP.0000000000000117. PMID 27271843.
  17. ↑ Swerdlow SH, et al (editors). WHO classification of tumours of haematopoietic and lymphoid tissues. 4th edition. 2008. International Agency for Research on Cancer (IARC), Lyon, Franc
  18. ↑ Tilly H, et al. Diffuse large B-cell lymphoma (DLBCL): ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Annals of Oncology. 2015; 26: v116-v125
  19. ↑ Itziar Salaverria, Cristina Royo, Alejandra Carvajal-Cuenca, Guillem Clot, Alba Navarro, Alejandra Valera, Joo Y. Song, Renata Woroniecka, Grzegorz Rymkiewicz, Wolfram Klapper, Elena M. Hartmann, Pierre Sujobert, Iwona Wlodarska, Judith A. Ferry, Philippe Gaulard, German Ott, Andreas Rosenwald, Armando Lopez-Guillermo, Leticia Quintanilla-Martinez, Nancy L. Harris, Elaine S. Jaffe, Reiner Siebert, Elias Campo & Silvia Bea (2013). "CCND2 rearrangements are the most frequent genetic events in cyclin D1(-) mantle cell lymphoma". Blood. 121 (8): 1394–1402. doi:10.1182/blood-2012-08-452284. PMID 23255553. Unknown parameter |month= ignored (help)
  20. ↑ Markus Tiemann, Carsten Schrader, Wolfram Klapper, Martin H. Dreyling, Elias Campo, Andrew Norton, Francoise Berger, Philip Kluin, German Ott, Stephano Pileri, Ennio Pedrinis, Alfred C. Feller, Hartmut Merz, Dirk Janssen, Martin L. Hansmann, Han Krieken, Peter Moller, Harald Stein, Michael Unterhalt, Wolfgang Hiddemann & Reza Parwaresch (2005). "Histopathology, cell proliferation indices and clinical outcome in 304 patients with mantle cell lymphoma (MCL): a clinicopathological study from the European MCL Network". British journal of haematology. 131 (1): 29–38. doi:10.1111/j.1365-2141.2005.05716.x. PMID 16173960. Unknown parameter |month= ignored (help)
  21. ↑ L. H. Argatoff, J. M. Connors, R. J. Klasa, D. E. Horsman & R. D. Gascoyne (1997). "Mantle cell lymphoma: a clinicopathologic study of 80 cases". Blood. 89 (6): 2067–2078. PMID 9058729. Unknown parameter |month= ignored (help)
  22. ↑ Markus Tiemann, Carsten Schrader, Wolfram Klapper, Martin H. Dreyling, Elias Campo, Andrew Norton, Francoise Berger, Philip Kluin, German Ott, Stephano Pileri, Ennio Pedrinis, Alfred C. Feller, Hartmut Merz, Dirk Janssen, Martin L. Hansmann, Han Krieken, Peter Moller, Harald Stein, Michael Unterhalt, Wolfgang Hiddemann & Reza Parwaresch (2005). "Histopathology, cell proliferation indices and clinical outcome in 304 patients with mantle cell lymphoma (MCL): a clinicopathological study from the European MCL Network". British journal of haematology. 131 (1): 29–38. doi:10.1111/j.1365-2141.2005.05716.x. PMID 16173960. Unknown parameter |month= ignored (help)
  23. ↑ Julie M. Vose (2017). "Mantle cell lymphoma: 2017 update on diagnosis, risk-stratification, and clinical management". American journal of hematology. 92 (8): 806–813. doi:10.1002/ajh.24797. PMID 28699667. Unknown parameter |month= ignored (help)
  24. ↑ Lin P, Jones D, Dorfman DM, Medeiros LJ (November 2000). "Precursor B-cell lymphoblastic lymphoma: a predominantly extranodal tumor with low propensity for leukemic involvement". Am. J. Surg. Pathol. 24 (11): 1480–90. PMID 11075849.
  25. ↑ Javed Z, Hanif F (August 2018). "A Rare Presentation of Precursor B-cell Lymphoblastic Lymphoma in a Child". Cureus. 10 (8): e3238. doi:10.7759/cureus.3238. PMC 6209516. PMID 30410844.
  26. ↑ Kim JY, Om SY, Shin SJ, Kim JE, Yoon DH, Suh C (December 2014). "Case series of precursor B-cell lymphoblastic lymphoma". Blood Res. 49 (4): 270–4. doi:10.5045/br.2014.49.4.270. PMC 4278010. PMID 25548762.
  27. ↑ Ganapathi KA, Pittaluga S, Odejide OO, Freedman AS, Jaffe ES (2014). "Early lymphoid lesions: conceptual, diagnostic and clinical challenges". Haematologica. 99 (9): 1421–32. doi:10.3324/haematol.2014.107938. PMC 4562530. PMID 25176983.
  28. ↑ Lorsbach RB, Shay-Seymore D, Moore J, Banks PM, Hasserjian RP, Sandlund JT; et al. (2002). "Clinicopathologic analysis of follicular lymphoma occurring in children". Blood. 99 (6): 1959–64. PMID 11877266.
  29. ↑ Overview at UMDNJ
  30. ↑ Bosga-Bouwer AG, Haralambieva E, Booman M; et al. (November 2005). "BCL6 alternative translocation breakpoint cluster region associated with follicular lymphoma grade 3B". Genes Chromosomes Cancer. 44 (3): 301–4. doi:10.1002/gcc.20246. PMID 16075463.
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  34. ↑ Chuang, Shih-Sung; Ye, Hongtao; Du, Ming-Qing; Lu, Chin-Li; Dogan, Ahmet; Hsieh, Pin-Pen; Huang, Wan-Ting; Jung, Yun-Chih (2007). "Histopathology and Immunohistochemistry in Distinguishing Burkitt Lymphoma From Diffuse Large B-Cell Lymphoma With Very High Proliferation Index and With or Without a Starry-Sky Pattern". American Journal of Clinical Pathology. 128 (4): 558–564. doi:10.1309/EQJR3D3V0CCQGP04. ISSN 0002-9173.
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  38. ↑ Ekemen S, Uzay A, Bassullu N, Dikicioglu-Cetin E, Matsuda K, Ince U; et al. (2018). "Does it take three to tango? An unsuspected multimorbidity of CD8+ T cell lymphoproliferative disorder, malaria, and EBV infection". Malar J. 17 (1): 349. doi:10.1186/s12936-018-2497-9. PMC 6173833. PMID 30290813.
  39. ↑ Kretzmer H, Bernhart SH, Wang W, Haake A, Weniger MA, Bergmann AK; et al. (2015). "DNA methylome analysis in Burkitt and follicular lymphomas identifies differentially methylated regions linked to somatic mutation and transcriptional control". Nat Genet. 47 (11): 1316–1325. doi:10.1038/ng.3413. PMC 5444523. PMID 26437030.
  40. ↑ Klein, Ulf; Tu, Yuhai; Stolovitzky, Gustavo A.; Mattioli, Michela; Cattoretti, Giorgio; Husson, Hervé; Freedman, Arnold; Inghirami, Giorgio; Cro, Lilla; Baldini, Luca; Neri, Antonino; Califano, Andrea; Dalla-Favera, Riccardo (2001). "Gene Expression Profiling of B Cell Chronic Lymphocytic Leukemia Reveals a Homogeneous Phenotype Related to Memory B Cells". The Journal of Experimental Medicine. 194 (11): 1625–1638. doi:10.1084/jem.194.11.1625. ISSN 0022-1007.
  41. ↑ Non-gastric lymphomas – causes, symptoms and treatments. Lymphoma association 2016. https://www.lymphomas.org.uk/sites/default/files/pdfs/Non-Gastric-malt-lymphoma.pdf. Accessed on January 28, 2016
  42. ↑ Risks of Extranodal marginal zone of mucosa-associated lymphoid tissue (MALT lymphoma). Canadian Cancer Society 2016. http://www.cancer.ca/en/cancer-information/cancer-type/non-hodgkin-lymphoma/non-hodgkin-lymphoma/types-of-nhl/malt-lymphoma/?region=on. Accessed on January 25, 2016
  43. ↑ Kinkade, Zoe; Esan, Olukemi A.; Rosado, Flavia G.; Craig, Michael; Vos, Jeffrey A. (2015). "Ileal mucosa-associated lymphoid tissue lymphoma presenting with small bowel obstruction: a case report". Diagnostic Pathology. 10 (1). doi:10.1186/s13000-015-0353-6. ISSN 1746-1596.
  44. ↑ Symptoms of MALT lymphoma. Cancer research UK 2016. http://www.cancerresearchuk.org/about-cancer/type/non-hodgkins-lymphoma/about/types/mucosaassociated-lymphoid-tissue-lymphoma. Accessed on January 28, 2016
  45. ↑ Symptoms of MALT lymphoma. Cancer research UK 2016. http://www.cancerresearchuk.org/about-cancer/type/non-hodgkins-lymphoma/about/types/mucosaassociated-lymphoid-tissue-lymphoma. Accessed on January 28, 2016
  46. ↑ Signs and symptoms of gastric lymphoma. Wikipedia 2016. https://en.wikipedia.org/wiki/Gastric_lymphoma. Accessed on January 28, 2016
  47. ↑ Clinical presentation of orbital lymphoma. Dr Craig Hacking and A.Prof Frank Gaillard et al. Radiopaedia 2016. http://radiopaedia.org/articles/orbital-lymphoma. Accessed on January 28, 2016
  48. ↑ Non-gastric lymphomas – causes, symptoms and treatments. Lymphoma association 2016. https://www.lymphomas.org.uk/sites/default/files/pdfs/Non-Gastric-malt-lymphoma.pdf. Accessed on January 28, 2016
  49. ↑ Taal, B G; Boot, H; van Heerde, P; de Jong, D; Hart, A A; Burgers, J M (1 October 1996). "Primary non-Hodgkin lymphoma of the stomach: endoscopic pattern and prognosis in low versus high grade malignancy in relation to the MALT concept". Gut. 39 (4): 556–561. doi:10.1136/gut.39.4.556.
  50. ↑ Bacon CM, Du MQ, Dogan A (2007). "Mucosa-associated lymphoid tissue (MALT) lymphoma: a practical guide for pathologists". J Clin Pathol. 60 (4): 361–72. doi:10.1136/jcp.2005.031146. PMC 2001121. PMID 16950858.
  51. ↑ Hernández JM, García JL, Gutiérrez NC, Mollejo M, Martínez-Climent JA, Flores T, González MB, Piris MA, San Miguel JF (May 2001). "Novel genomic imbalances in B-cell splenic marginal zone lymphomas revealed by comparative genomic hybridization and cytogenetics". Am. J. Pathol. 158 (5): 1843–50. doi:10.1016/S0002-9440(10)64140-5. PMC 1891967. PMID 11337382.
  52. ↑ Andersen CL, Gruszka-Westwood A, Atkinson S, Matutes E, Catovsky D, Pedersen RK, Pedersen BB, Pulczynski S, Hokland P, Jacobsen E, Koch J (January 2005). "Recurrent genomic imbalances in B-cell splenic marginal-zone lymphoma revealed by comparative genomic hybridization". Cancer Genet. Cytogenet. 156 (2): 122–8. doi:10.1016/j.cancergencyto.2004.04.026. PMID 15642391.
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  59. ↑ Nodal marginal zone lymphoma . Canadian Cancer Society. http://www.cancer.ca/en/cancer-information/cancer-type/non-hodgkin-lymphoma/non-hodgkin-lymphoma/types-of-nhl/nodal-marginal-zone-lymphoma/?region=nb Accessed on March 4, 2016
  60. ↑ Steven P. Treon, Lian Xu, Guang Yang, Yangsheng Zhou, Xia Liu, Yang Cao, Patricia Sheehy, Robert J. Manning, Christopher J. Patterson, Christina Tripsas, Luca Arcaini, Geraldine S. Pinkus, Scott J. Rodig, Aliyah R. Sohani, Nancy Lee Harris, Jason M. Laramie, Donald A. Skifter, Stephen E. Lincoln & Zachary R. Hunter (2012). "MYD88 L265P somatic mutation in Waldenstrom's macroglobulinemia". The New England journal of medicine. 367 (9): 826–833. doi:10.1056/NEJMoa1200710. PMID 22931316. Unknown parameter |month= ignored (help)
  61. ↑ Chi PJ, Pei SN, Huang TL, Huang SC, Ng HY, Lee CT (2014). "Renal MALT lymphoma associated with Waldenström macroglobulinemia". J. Formos. Med. Assoc. 113 (4): 255–7. doi:10.1016/j.jfma.2011.02.007. PMID 24685302.
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  63. ↑ García-Sanz R, Montoto S, Torrequebrada A, de Coca AG, Petit J, Sureda A; et al. (2001). "Waldenström macroglobulinaemia: presenting features and outcome in a series with 217 cases". Br J Haematol. 115 (3): 575–82. PMID 11736938.
  64. ↑ Merlini G, Baldini L, Broglia C, Comelli M, Goldaniga M, Palladini G; et al. (2003). "Prognostic factors in symptomatic Waldenstrom's macroglobulinemia". Semin Oncol. 30 (2): 211–5. doi:10.1053/sonc.2003.50064. PMID 12720138.
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  69. ↑ Forconi F, Raspadori D, Lenoci M, Lauria F (February 2005). "Absence of surface CD27 distinguishes hairy cell leukemia from other leukemic B-cell malignancies". Haematologica. 90 (2): 266–8. PMID 15710587.
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  77. ↑ Matutes E (2007) Adult T-cell leukaemia/lymphoma. J Clin Pathol 60 (12):1373-7. DOI:10.1136/jcp.2007.052456 PMID: 18042693
  78. ↑ Shimoyama M (1991). "Diagnostic criteria and classification of clinical subtypes of adult T-cell leukaemia-lymphoma. A report from the Lymphoma Study Group (1984-87)". Br J Haematol. 79 (3): 428–37. PMID 1751370.
  79. ↑ Al-Ahmad, Selma; Maertens, Vincent; Libeer, Christophe; Schelfhout, Vera; Vanhoenacker, Filip; Boeckx, Nancy; Vandevenne, Marleen (2017). "The masquerading presentation of a systemic anaplastic large cell lymphoma, ALK positive: a case report and review of the literature". Acta Clinica Belgica. 72 (6): 454–460. doi:10.1080/17843286.2017.1312057. ISSN 1784-3286.
  80. ↑ Yu L, Yan LL, Yang SJ (2014). "Sarcomatoid variant of ALK- anaplastic large cell lymphoma involving multiple lymph nodes and both lungs with production of proinflammatory cytokines: report of a case and review of literature". Int J Clin Exp Pathol. 7 (8): 4806–16. PMC 4152041. PMID 25197351.
  81. ↑ de Campos FPF, Zerbini MCN, Felipe-Silva A, Simões AB, Lovisolo SM, da Fonseca LG; et al. (2014). "Unusual clinical presentation of anaplastic large cell lymphoma". Autops Case Rep. 4 (1): 21–27. doi:10.4322/acr.2014.004. PMC 5470561. PMID 28652989.
  82. ↑ Watanabe M, Ogawa Y, Itoh K; et al. (January 2008). "Hypomethylation of CD30 CpG islands with aberrant JunB expression drives CD30 induction in Hodgkin lymphoma and anaplastic large cell lymphoma". Lab. Invest. 88 (1): 48–57. doi:10.1038/labinvest.3700696. PMID 17965727.
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