Tissue flow cytometry immunophenotyping in the diagnosis and classification of non-Hodgkin's lymphomas: A retrospective evaluation of 1,792 cases

Cytometry Part B - Clinical Cytometry

Volumn 84 B, Issue 2, 2013, Pages 82-95

  Demurtas, Anna ^a   Stacchini, Alessandra ^a   Aliberti, Sabrina ^a   Chiusa, Luigi ^a   Chiarle, Roberto ^a   Novero, Domenico ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

flow cytometry; non Hodgkin's lymphomas; tissue biopsy

Indexed keywords

ACUTE LEUKEMIA; ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; BENIGN TUMOR; CANCER CLASSIFICATION; CANCER DIAGNOSIS; CANCER MORPHOLOGY; CANCER TISSUE; CARCINOMA; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CHILD; COMPOSITE LYMPHOMA; DIFFERENTIAL DIAGNOSIS; ENZYME CHEMISTRY; FEMALE; FLOW CYTOMETRY; FOLLICULAR LYMPHOMA; HEMATOLOGIC MALIGNANCY; HISTOPATHOLOGY; HODGKIN DISEASE; HUMAN; HUMAN TISSUE; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; INFANT; LYMPHATIC LEUKEMIA; LYMPHOPROLIFERATIVE DISEASE; MAJOR CLINICAL STUDY; MALE; NATURAL KILLER CELL; NONHODGKIN LYMPHOMA; PHENOTYPE; PRE T LYMPHOCYTE; PRESCHOOL CHILD; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SCHOOL CHILD; TUMOR CELL;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CHILD; CHILD, PRESCHOOL; FEMALE; FLOW CYTOMETRY; HODGKIN DISEASE; HUMANS; HYPERPLASIA; IMMUNOPHENOTYPING; INFANT; KILLER CELLS, NATURAL; LEUKEMIA; LYMPHOMA, NON-HODGKIN; MALE; MIDDLE AGED; RETROSPECTIVE STUDIES; T-LYMPHOCYTES; YOUNG ADULT;

EID: 84874231420     PISSN: 15524949     EISSN: 15524957     Source Type: Journal    
DOI: 10.1002/cyto.b.21065     Document Type: Article

References (67)

1. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J,Vardiman, JW,. WHO Classification of Tumors of Hematopoietic and Lymphoid Tissues, 4th ed. Lyon: IARC Press; 2008.
2. Tan LH,. A practical approach to the understanding and diagnosis of lymphoma: An assessment of the WHO classification based on immunoarchitecture and immuno-ontogenic principles. Pathology 2009; 41: 305-326.
3. Dunphy CH,. Applications of flow cytometry and immunohistochemistry to diagnostic hematopathology. Arch Pathol Lab Med 2004; 128: 1004-1022.
4. Kaleem Z,. Flow cytometric analysis of lymphomas: current status and usefulness. Arch Pathol Lab Med 2006; 130: 1850-1858.
5. Craig FE, Foon KA,. Flow cytometric immunophenotyping for hematologic neoplasms. Blood 2008; 111: 3941-3967.
6. Demurtas A, Aliberti S, Bonello L, Francia Di Celle P, Cavaliere C, Barreca A, Novero D, Stacchini A,. Usefulness of multiparametric flow cytometry in detecting composite lymphoma: Study of 17 cases in a 12-year period. Am J Clin Pathol 2011; 135: 541-555.
7. Novelli M, Savoia P, Cambieri I, Ponti R, Comessatti A, Lisa F, Bernengo MG,. Collagenase digestion and mechanical disaggregation as a method to extract and immunophenotype tumor lymphocytes in cutaneous T-cell lymphomas. Clin Exp Dermatol 2000; 25: 423-431.
8. Calvo KR, McCoy CS, Stetler-Stevenson M,. Flow cytometry immunophenotyping of hematolymphoid neoplasia. Methods Mol Biol 2011; 699: 295-316.
9. Maiese RL, Segal GH, Iturraspe JA, Braylan RC,. The cell surface antigen and DNA content distribution of lymph nodes with reactive hyperplasia. Mod Pathol 1995; 8: 536-543.
10. Li S, Eshleman JR, Borowitz MJ,. Lack of surface immunoglobulin light chain expression by flow cytometric immunophenotyping can help diagnose peripheral B-cell lymphoma. Am J Clin Pathol 2002; 118: 229-234.
11. Karube K, Aoki R, Nomura Y, Yamamoto K, Shimizu K, Yoshida S, Komatani H, Sugita Y, Ohshima K,. Usefulness of flow cytometry for differential diagnosis of precursor and peripheral T-cell and NK-cell lymphomas: analysis of 490 cases. Pathol Int 2008; 58: 89-97.
12. Stacchini A, Demurtas A, Aliberti S, Francia di Celle P, Godio L, Novero D,. The usefulness of flow cytometric CD10 detection in the differential diagnosis of peripheral T-cell lymphomas. Am J Clin Pathol 2007; 128: 854-864.
13. Wood BL, Arroz M, Barnett D, DiGiuseppe J, Greig B, Kussick SJ, Oldaker T, Shenkin M, Stone E, Wallace P,. 2006 Bethesda International Consensus recommendations on the immunophenotypic analysis of hematolymphoid neoplasia by flow cytometry: optimal reagents and reporting for the flow cytometric diagnosis of hematopoietic neoplasia. Cytometry B Clin Cytom 2007; 72B (Suppl 1): S14-22.
14. Cunningham RE,. Tissue disaggregation. Methods Mol Biol. 2010; 588: 327-330.
15. Vos JA, Simurdak JH, Davis BJ, Myers JB, Brissette MD,. Vortex disaggregation for flow cytometry allows direct histologic correlation: A novel approach for small biopsies and inaspirable bone marrows. Cytometry B Clin Cytom 2003; 52B: 20-31.
16. Bernengo MG, Novelli M, Quaglino P, Lisa F, De Matteis A, Savoia P, Cappello N, Fierro MT,. The relevance of the CD4+ CD26- subset in the identification of circulating Sézary cells. Br J Dermatol 2001; 144: 125-135.
17. Chang A, Benda PM, Wood BL, Kussick SJ,. Lineage-specific identification of nonhematopoietic neoplasms by flow cytometry. Am J Clin Pathol 2003; 119: 643-55.
18. Meda BA, Buss DH, Woodruff RD, Cappellari JO, Rainer RO, Powell BL, Geisinger KR,. Diagnosis and subclassification of primary and recurrent lymphoma. The usefulness and limitations of combined fine-needle aspiration cytomorphology and flow cytometry. Am J Clin Pathol 2000; 113: 688-699.
19. Mourad WA, Tulbah A, Shoukri M, Al Dayel F, Akhtar M, Ali MA, Hainau B, Martin J,. Primary diagnosis and REAL/WHO classification of non-Hodgkin's lymphoma by fine-needle aspiration: Cytomorphologic and immunophenotypic approach. Diagn Cytopathol 2003; 28: 191-195.
20. Zeppa P, Vigliar E, Cozzolino I, Troncone G, Picardi M, De Renzo A, Grimaldi F, Pane F, Vetrani A, Palombini L,. Fine needle aspiration cytology and flow cytometry immunophenotyping of non-Hodgkin lymphoma: Can we do better? Cytopathology 2010; 21: 300-310.
21. Demurtas A, Accinelli G, Pacchioni D, Godio L, MD, Novero D, MD, Bussolati G, Palestro G, Papotti M, Stacchini A,. Utility of flow cytometry immunophenotyping in fine-needle aspirate cytologic diagnosis of non-Hodgkin lymphoma: A series of 252 cases and review of the literature. Appl Immunohistochem Mol Morphol 2010; 18: 311-322.
22. Stacchini A, Carucci P, Pacchioni D, Accinelli G, Demurtas A, Aliberti S, Bosco M, Bruno M, Balbo Mussetto A, Rizzetto M, et al. Diagnosis of deep-seated lymphomas by endoscopic ultrasound-guided fine needle aspiration combined with flow cytometry. Cytopathology 2012; 23: 50-56.
23. Barrena S, Almeida J, Del Carmen García-Macias M, López A, Rasillo A, Sayagués JM, Rivas RA, Gutiérrez ML, Ciudad J, Flores T, et al. Flow cytometry immunophenotyping of fine-needle aspiration specimens: utility in the diagnosis and classification of non-Hodgkin lymphomas. Histopathology 2011; 58: 906-918.
24. Savage EC, Vanderheyden AD, Bell AM, Syrbu SI, Jensen CS,. Independent diagnostic accuracy of flow cytometry obtained from fine-needle aspirates: A 10-year experience with 451 cases. Am J Clin Pathol 2011; 135: 304-309.
25. Witzig TE, Banks PM, Stenson MJ, Griepp PR, Katzmann JA, Habermann TM, Colgan JP, Gonchoroff NJ,. Rapid immunotyping of B-cell non-Hodgkin's lymphomas by flow cytometry. A comparison with the standard frozen-section method. Am J Clin Pathol 1990; 94: 280-286.
26. Morse EE, Yamase HT, Greenberg BR, Sporn J, Harshaw SA, Kiraly TR, Ziemba RA, Fallon MA,. The role of flow cytometry in the diagnosis of lymphoma: A critical analysis. Ann Clin Lab Sci 1994; 24: 6-11.
27. Ichinohasama R, DeCoteau JF, Myers J, Kadin ME, Sawai T, Ooya K,. Three-color flow cytometry in the diagnosis of malignant based on the comparative cell morphology of lymphoma cells and reactive lymphocytes. Leukemia 1997; 11: 1891-1903.
28. Dunphy CH,. Contribution of flow cytometric immunophenotyping to the evaluation of tissues with suspected lymphoma? Cytometry 2000; 42: 296-306.
29. Martínez A, Aymerich M, Castillo M, Colomer D, Bellosillo B, Campo E, Villamor N,. Routine use of immunophenotype by flow cytometry in tissues with suspected hematological malignancies. Cytometry B Clin Cytom 2003; 56: 8-15.
30. Ravoet C, Demartin S, Gerard R, Dehon M, Peny MO, Petit B, Delannoy A, Husson B,. Contribution of flow cytometry to the diagnosis of malignant and non malignant conditions in lymph node biopsies. Leuk Lymphoma 2004; 45: 1587-1593.
31. Colorado M, Cuadrado MA, Insunza A, Mazorra F, Acinas O, Iriondo A,. Simultaneous cytomorphologic and multiparametric flow cytometric analysis on lymph node samples is faster than and as valid as histopathologic study to diagnose most non-Hodgkin lymphomas. Am J Clin Pathol 2010; 133: 83-91.
32. Tiesinga JJ, Wu CD, Inghirami G,. CD5+ follicle center lymphoma. Immunophenotyping detects a unique subset of "floral" follicular lymphoma. Am J Clin Pathol 2000; 114: 912-921.
33. Bertram HC, Check IJ, Milano MA,. Immunophenotyping large B-cell lymphomas. Flow cytometric pitfalls and pathologic correlation. Am J Clin Pathol 2001; 116: 191-203.
34. Kaleem Z, White G, Zutter MM,. Aberrant expression of T-cell-associated antigens on B-cell non-Hodgkin lymphomas. Am J Clin Pathol 2001; 115: 396-403.
35. Xu Y, McKenna RW, Molberg KH, Kroft SH,. Clinicopathologic analysis of CD10+ and CD10- diffuse large B-cell lymphoma. Identification of a high-risk subset with coexpression of CD10 and bcl-2. Am J Clin Pathol 2001; 116: 183-190.
36. Barry TS, Jaffe ES, Kingma DW, Martin AW, Sorbara L, Raffeld M, Pittaluga S,. CD5+ follicular lymphoma: A clinicopathologic study of three cases. Am J Clin Pathol 2002; 118: 589-598.
37. Xu Y, McKenna RW, Kroft SH,. Assessment of CD10 in the diagnosis of small B-cell lymphomas: A multiparameter flow cytometric study. Am J Clin Pathol 2002; 117: 291-300.
38. Kaleem Z, Hassan A, Pathan MH, White G,. Flow cytometric evaluation of posttransplant B-cell lymphoproliferative disorders. Arch Pathol Lab Med 2004; 128: 181-186.
39. Manazza AD, Bonello L, Pagano M, Chiusa L, Novero D, Stacchini A, Martini G, Vitolo U, Tarella C, Inghirami G, et al. Follicular origin of a subset of CD5+ diffuse large B-cell lymphomas. Am J Clin Pathol 2005; 124: 182-190.
40. Kelemen K, Peterson LC, Helenowski I, Goolsby CL, Jovanovic B, Miyata S, Aranha O, Rosen ST, Winter JN, Nelson BP, et al. CD23+ mantle cell lymphoma: A clinical pathologic entity associated with superior outcome compared with CD23- disease. Am J Clin Pathol 2008; 130: 166-177.
41. Kost CB, Holden JT, Mann KP,. Marginal zone B-cell lymphoma: A retrospective immunophenotypic analysis. Cytometry B Clin Cytom 2008; 74B: 282-286.
42. Fromm JR, Thomas A, Wood BL,. Flow cytometry can diagnose classical Hodgkin lymphoma in lymph nodes with high sensitivity and specificity. Am J Clin Pathol 2009; 131: 322-332.
43. Wang E, West D, Kulbacki E,. An unusual nodal marginal zone lymphoma with bright CD10 expression: A potential diagnostic pitfall. Am J Hematol 2010; 85: 546-548.
44. Arrondini M, Barreca A, Aliberti, Demurtas A, Tondat F, Novero D, Stacchini A,. CD4-positive diffuse large B cell lymphoma identified by flow cytometry: Two case reports. Int J Hematol 2010; 92: 198-203.
45. Stacchini A, Barreca A, Demurtas A, Aliberti S, Francia Di Celle P, Novero D,. Flow cytometric detection and quantification of CD56 (neural cell adhesion molecule, NCAM) expression in diffuse large B-cell lymphomas and review of the literature. Histopathology 2012; 60: 452-459.
46. Cornfield DB, Mitchell DM, Almasri NM, Anderson JB, Ahrens KP, Dooley EO, Braylan RC,. Follicular lymphoma can be distinguished from benign follicular hyperplasia by flow cytometry using simultaneous staining of cytoplasmic bcl-2 and cell surface CD20. Am J Clin Pathol 2000; 114: 258-263.
47. Cook JR, Craig FE, Swerdlow SH,. bcl-2 expression by multicolor flow cytometric analysis assists in the diagnosis of follicular lymphoma in lymph node and bone marrow. Am J Clin Pathol 2003; 119: 145-151.
48. Salameire D, Le Bris Y, Fabre B, Fauconnier J, Solly F, Pernollet M, Bonnefoix T, Leroux D, Plumas J, Jacob MC,. Efficient characterization of the TCR repertoire in lymph nodes by flow cytometry. Cytometry A 2009; 75A: 743-751.
49. Kojima M, Sato E, Oshimi K, Murase T, Koike T, Tsunoda S, Matsumoto T, Marutsuka K, Ogiya D, Moriuchi M, et al. Characteristics of CD5-positive splenic marginal zone lymphoma with leukemic manifestation: Clinical, flow cytometry, and histopathological findings of 11 cases. J Clin Exp Hematop 2010; 50: 107-112.
50. Dong HY, Gorczyca W, Liu Z, Tsang P, Wu CD, Cohen P, Weisberger J,. B-cell lymphomas with coexpression of CD5 and CD10. Am J Clin Pathol 2003; 119: 218-230.
51. Barekman CL, Aguilera NS, Abbondanzo SL,. Low-grade B-cell lymphoma with coexpression of both CD5 and CD10. A report of 3 cases. Arch Pathol Lab Med 2001; 125: 951-953.
52. Chen YH, Tallman MS, Goolsby C, Peterson L,. Immunophenotypic variations in hairy cell leukemia. Am J Clin Pathol 2006; 125: 251-259.
53. Miyazaki K, Yamaguchi M, Suzuki R, Kobayashi Y, Maeshima AM, Niitsu N, Ennishi D, Tamaru JI, Ishizawa K, Kashimura M, et al. CD5-positive diffuse large B-cell lymphoma: A retrospective study in 337 patients treated by chemotherapy with or without rituximab. Ann Oncol 2011; 22: 1601-1607.
54. The non Hodgkin's Lymphoma Classification Project. A clinical evaluation of the International Lymphoma Study Group Classification of non Hodgkin's Lymphoma. Blood 1997; 89: 3909-3918.
55. Laane E, Tani E, Björklund E, Elmberger G, Everaus H, Skoog L, Porwit-MacDonald A,. Flow cytometric immunophenotyping including Bcl-2 detection on fine needle aspirates in the diagnosis of reactive lymphadenopathy and non-Hodgkin's lymphoma. Cytometry B Clin Cytom 2005; 64B: 34-42.
56. Carulli G, Stacchini A, Marini A, Ciriello MM, Zucca A, Cannizzo E, Aliberti S, Demurtas A, Novero D, Calcagno L, et al. Aberrant expression of CD8 in B-cell non-Hodgkin lymphoma: A multicenter study of 951 bone marrow samples with lymphomatous infiltration. Am J Clin Pathol 2009; 132: 186-190.
57. Mourad WA, Rawas F, Shoukri M, Tbakhi A, Al Omari M, Tulbah A, Al Dayel F,. Grading of follicular lymphoma using flow cytometry. Ann Saudi Med 2006; 26: 205-210.
58. Young NA,. Grading Follicular lymphoma on Fine-needle aspiration specimens. A practical approach. Cancer 2006; 108: 1-9.
59. de Tute RM,. Flow cytometry and its use in the diagnosis and management of mature lymphoid malignancies. Histopathology 2011; 58: 90-105.
60. Muzzafar T, Wei EX, Lin P, Medeiros LJ, Jorgensen JL,. Flow cytometric immunophenotyping of anaplastic large cell lymphoma. Arch Pathol Lab Med 2009; 133: 49-56.
61. Zeng G, Ewton A, Zu Y, An C, Nishino H, Ponce de Lion A, Chang C,. Quantitative analysis of CD4/CD8 ratios by flow cytometry as an adjunct in diagnosis of Hodgkin's lymphomas [abstract]. Mod Pathol 2005; 18 (suppl 1): 259A-260A.
62. Hudnall SD, Betancour E, Bernhart E, Patel J,. Comparative flow immunophenotypic features of the inflammatory infiltrates of Hodgkin lymphoma and lymphoid hyperplasia. Cytometry B Clin Cytom 2008; 74B: 1-8.
63. Rahemullah A, Reichard KK, Preffer FI, Harris NL, Hasserijan RP,. A double-positive CD4+CD8+ T-cell population is commonly found in nodular lymphocyte predominant Hodgkin lymphoma. Am J Clin Pathol 2006; 126: 805-814.
64. Rahemullah A, Harris NL, Dorn ME, Preffer FI, Hasserijan RP,. Beyond the lymphocyte predominant cell: CD4+CD8+ T-cell in nodular lymphocyte predominant Hodgkin lymphoma. Leuk Lymph 2008; 49: 1870-1878.
65. Attygalle A, Al-Jehani R, Diss TC, Munson P, Liu H, Du MQ, Isaacson PG, Dogan A,. Neoplastic T cells in angioimmunoblastic T-cell lymphoma express CD10. Blood 2002; 99: 627-633.
66. Greig B, Oldaker T, Warzynski M, Wood B,. 2006 Bethesda International Consensus recommendations on the immunophenotypic analysis of hematolymphoid neoplasia by flow cytometry: Recommendations for training and education to perform clinical flow cytometry. Cytometry B Clin Cytom 2007; 72B (Suppl 1): S23-S33.
67. Costa ES, Pedreira CE, Barrena S, Lecrevisse Q, Flores J, Quijano S, Almeida J, del Carmen García-Macias M, Bottcher S, Van Dongen JJ, et al. Automated pattern-guided principal component analysis vs expert-based immunophenotypic classification of B-cell chronic lymphoproliferative disorders: A step forward in the standardization of clinical immunophenotyping. Leukemia 2010; 24: 1927-1933.