Peripheral T-cell lymphomas of follicular helper T-cell type frequently display an aberrant CD3-/dimCD4+ population by flow cytometry: an important clue to the diagnosis of a Hodgkin lymphoma mimic

Mir Alikhan, Joo Y. Song, Aliyah R. Sohani, Julien Moroch, Anne Plonquet, Amy S Duffield, Michael J Borowitz, Liuyan Jiang, Carlos Bueso-Ramos, Kedar Inamdar, Madhu P. Menon, Sandeep Gurbuxani, Ernest Chan, Sonali M. Smith, Alina Nicolae, Elaine S. Jaffe, Philippe Gaulard, Girish Venkataraman

Research output: Contribution to journalArticle

Abstract

Nodal follicular helper T-cell-derived lymphoproliferations (specifically the less common peripheral T-cell lymphomas of follicular type) exhibit a spectrum of histologic features that may mimic reactive hyperplasia or Hodgkin lymphoma. Even though angioimmunoblastic T-cell lymphoma and peripheral T-cell lymphoma of follicular type share a common biologic origin from follicular helper T-cells and their morphology has been well characterized, flow cytometry of peripheral T-cell lymphomas of follicular type has not been widely discussed as a tool for identifying this reactive hyperplasia/Hodgkin lymphoma mimic. We identified 10 peripheral T-cell lymphomas of follicular type with available flow cytometry data from five different institutions, including two cases with peripheral blood evaluation. For comparison, we examined flow cytometry data for 8 classical Hodgkin lymphomas (including 1 lymphocyte-rich classical Hodgkin lymphoma), 15 nodular lymphocyte predominant Hodgkin lymphomas, 15 angioimmunoblastic T-cell lymphomas, and 26 reactive nodes. Lymph node histology and flow cytometry data were reviewed, specifically for the presence of a CD3-/dimCD4+ aberrant T-cell population (described in angioimmunoblastic T-cell lymphomas), besides other T-cell aberrancies. Nine of 10 (90%) peripheral T-cell lymphomas of follicular type showed a CD3-/dimCD4+ T-cell population constituting 29.3% (range 7.9–62%) of all lymphocytes. Five of 10 (50%) had nodular lymphocyte predominant Hodgkin lymphoma or lymphocyte-rich classical Hodgkin lymphoma-like morphology with scattered Hodgkin-like cells that expressed CD20, CD30, CD15, and MUM1. Three cases had a nodular growth pattern and three others exhibited a perifollicular growth pattern without Hodgkin-like cells. Epstein–Barr virus was positive in 1 of 10 cases (10%). PCR analysis showed clonal T-cell receptor gamma gene rearrangement in all 10 peripheral T-cell lymphomas of follicular type. By flow cytometry, 11 of 15 (73.3%) angioimmunoblastic T-cell lymphomas showed the CD3-/dimCD4+ population (mean: 19.5%, range: 3–71.8%). Using a threshold of 3% for CD3-/dimCD4+ T cells, all 15 nodular lymphocyte predominant Hodgkin lymphoma controls and 8 classical Hodgkin lymphomas were negative (Mann–Whitney P=0.01, F-PTCL vs Hodgkin lymphomas), as were 25 of 26 reactive lymph nodes. The high frequency of CD3-/dimCD4+ aberrant T cells is similar in angioimmunoblastic T-cell lymphomas and peripheral T-cell lymphomas of follicular type, and is a useful feature in distinguishing peripheral T-cell lymphomas of follicular type from morphologic mimics such as reactive hyperplasia or Hodgkin lymphoma.Modern Pathology advance online publication, 17 June 2016; doi:10.1038/modpathol.2016.113.

Original languageEnglish (US)
JournalModern Pathology
DOIs
StateAccepted/In press - Jun 17 2016

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Peripheral T-Cell Lymphoma
Helper-Inducer T-Lymphocytes
Hodgkin Disease
Flow Cytometry
Population
T-Cell Lymphoma
T-Lymphocytes
Hyperplasia
Lymph Nodes
T-Cell Receptor gamma Genes
Gene Rearrangement
Growth

ASJC Scopus subject areas

  • Pathology and Forensic Medicine

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Peripheral T-cell lymphomas of follicular helper T-cell type frequently display an aberrant CD3-/dimCD4+ population by flow cytometry : an important clue to the diagnosis of a Hodgkin lymphoma mimic. / Alikhan, Mir; Song, Joo Y.; Sohani, Aliyah R.; Moroch, Julien; Plonquet, Anne; Duffield, Amy S; Borowitz, Michael J; Jiang, Liuyan; Bueso-Ramos, Carlos; Inamdar, Kedar; Menon, Madhu P.; Gurbuxani, Sandeep; Chan, Ernest; Smith, Sonali M.; Nicolae, Alina; Jaffe, Elaine S.; Gaulard, Philippe; Venkataraman, Girish.

In: Modern Pathology, 17.06.2016.

Research output: Contribution to journalArticle

Alikhan, M, Song, JY, Sohani, AR, Moroch, J, Plonquet, A, Duffield, AS, Borowitz, MJ, Jiang, L, Bueso-Ramos, C, Inamdar, K, Menon, MP, Gurbuxani, S, Chan, E, Smith, SM, Nicolae, A, Jaffe, ES, Gaulard, P & Venkataraman, G 2016, 'Peripheral T-cell lymphomas of follicular helper T-cell type frequently display an aberrant CD3-/dimCD4+ population by flow cytometry: an important clue to the diagnosis of a Hodgkin lymphoma mimic', Modern Pathology. https://doi.org/10.1038/modpathol.2016.113
Alikhan, Mir ; Song, Joo Y. ; Sohani, Aliyah R. ; Moroch, Julien ; Plonquet, Anne ; Duffield, Amy S ; Borowitz, Michael J ; Jiang, Liuyan ; Bueso-Ramos, Carlos ; Inamdar, Kedar ; Menon, Madhu P. ; Gurbuxani, Sandeep ; Chan, Ernest ; Smith, Sonali M. ; Nicolae, Alina ; Jaffe, Elaine S. ; Gaulard, Philippe ; Venkataraman, Girish. / Peripheral T-cell lymphomas of follicular helper T-cell type frequently display an aberrant CD3-/dimCD4+ population by flow cytometry : an important clue to the diagnosis of a Hodgkin lymphoma mimic. In: Modern Pathology. 2016.
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abstract = "Nodal follicular helper T-cell-derived lymphoproliferations (specifically the less common peripheral T-cell lymphomas of follicular type) exhibit a spectrum of histologic features that may mimic reactive hyperplasia or Hodgkin lymphoma. Even though angioimmunoblastic T-cell lymphoma and peripheral T-cell lymphoma of follicular type share a common biologic origin from follicular helper T-cells and their morphology has been well characterized, flow cytometry of peripheral T-cell lymphomas of follicular type has not been widely discussed as a tool for identifying this reactive hyperplasia/Hodgkin lymphoma mimic. We identified 10 peripheral T-cell lymphomas of follicular type with available flow cytometry data from five different institutions, including two cases with peripheral blood evaluation. For comparison, we examined flow cytometry data for 8 classical Hodgkin lymphomas (including 1 lymphocyte-rich classical Hodgkin lymphoma), 15 nodular lymphocyte predominant Hodgkin lymphomas, 15 angioimmunoblastic T-cell lymphomas, and 26 reactive nodes. Lymph node histology and flow cytometry data were reviewed, specifically for the presence of a CD3-/dimCD4+ aberrant T-cell population (described in angioimmunoblastic T-cell lymphomas), besides other T-cell aberrancies. Nine of 10 (90{\%}) peripheral T-cell lymphomas of follicular type showed a CD3-/dimCD4+ T-cell population constituting 29.3{\%} (range 7.9–62{\%}) of all lymphocytes. Five of 10 (50{\%}) had nodular lymphocyte predominant Hodgkin lymphoma or lymphocyte-rich classical Hodgkin lymphoma-like morphology with scattered Hodgkin-like cells that expressed CD20, CD30, CD15, and MUM1. Three cases had a nodular growth pattern and three others exhibited a perifollicular growth pattern without Hodgkin-like cells. Epstein–Barr virus was positive in 1 of 10 cases (10{\%}). PCR analysis showed clonal T-cell receptor gamma gene rearrangement in all 10 peripheral T-cell lymphomas of follicular type. By flow cytometry, 11 of 15 (73.3{\%}) angioimmunoblastic T-cell lymphomas showed the CD3-/dimCD4+ population (mean: 19.5{\%}, range: 3–71.8{\%}). Using a threshold of 3{\%} for CD3-/dimCD4+ T cells, all 15 nodular lymphocyte predominant Hodgkin lymphoma controls and 8 classical Hodgkin lymphomas were negative (Mann–Whitney P=0.01, F-PTCL vs Hodgkin lymphomas), as were 25 of 26 reactive lymph nodes. The high frequency of CD3-/dimCD4+ aberrant T cells is similar in angioimmunoblastic T-cell lymphomas and peripheral T-cell lymphomas of follicular type, and is a useful feature in distinguishing peripheral T-cell lymphomas of follicular type from morphologic mimics such as reactive hyperplasia or Hodgkin lymphoma.Modern Pathology advance online publication, 17 June 2016; doi:10.1038/modpathol.2016.113.",
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T2 - an important clue to the diagnosis of a Hodgkin lymphoma mimic

AU - Alikhan, Mir

AU - Song, Joo Y.

AU - Sohani, Aliyah R.

AU - Moroch, Julien

AU - Plonquet, Anne

AU - Duffield, Amy S

AU - Borowitz, Michael J

AU - Jiang, Liuyan

AU - Bueso-Ramos, Carlos

AU - Inamdar, Kedar

AU - Menon, Madhu P.

AU - Gurbuxani, Sandeep

AU - Chan, Ernest

AU - Smith, Sonali M.

AU - Nicolae, Alina

AU - Jaffe, Elaine S.

AU - Gaulard, Philippe

AU - Venkataraman, Girish

PY - 2016/6/17

Y1 - 2016/6/17

N2 - Nodal follicular helper T-cell-derived lymphoproliferations (specifically the less common peripheral T-cell lymphomas of follicular type) exhibit a spectrum of histologic features that may mimic reactive hyperplasia or Hodgkin lymphoma. Even though angioimmunoblastic T-cell lymphoma and peripheral T-cell lymphoma of follicular type share a common biologic origin from follicular helper T-cells and their morphology has been well characterized, flow cytometry of peripheral T-cell lymphomas of follicular type has not been widely discussed as a tool for identifying this reactive hyperplasia/Hodgkin lymphoma mimic. We identified 10 peripheral T-cell lymphomas of follicular type with available flow cytometry data from five different institutions, including two cases with peripheral blood evaluation. For comparison, we examined flow cytometry data for 8 classical Hodgkin lymphomas (including 1 lymphocyte-rich classical Hodgkin lymphoma), 15 nodular lymphocyte predominant Hodgkin lymphomas, 15 angioimmunoblastic T-cell lymphomas, and 26 reactive nodes. Lymph node histology and flow cytometry data were reviewed, specifically for the presence of a CD3-/dimCD4+ aberrant T-cell population (described in angioimmunoblastic T-cell lymphomas), besides other T-cell aberrancies. Nine of 10 (90%) peripheral T-cell lymphomas of follicular type showed a CD3-/dimCD4+ T-cell population constituting 29.3% (range 7.9–62%) of all lymphocytes. Five of 10 (50%) had nodular lymphocyte predominant Hodgkin lymphoma or lymphocyte-rich classical Hodgkin lymphoma-like morphology with scattered Hodgkin-like cells that expressed CD20, CD30, CD15, and MUM1. Three cases had a nodular growth pattern and three others exhibited a perifollicular growth pattern without Hodgkin-like cells. Epstein–Barr virus was positive in 1 of 10 cases (10%). PCR analysis showed clonal T-cell receptor gamma gene rearrangement in all 10 peripheral T-cell lymphomas of follicular type. By flow cytometry, 11 of 15 (73.3%) angioimmunoblastic T-cell lymphomas showed the CD3-/dimCD4+ population (mean: 19.5%, range: 3–71.8%). Using a threshold of 3% for CD3-/dimCD4+ T cells, all 15 nodular lymphocyte predominant Hodgkin lymphoma controls and 8 classical Hodgkin lymphomas were negative (Mann–Whitney P=0.01, F-PTCL vs Hodgkin lymphomas), as were 25 of 26 reactive lymph nodes. The high frequency of CD3-/dimCD4+ aberrant T cells is similar in angioimmunoblastic T-cell lymphomas and peripheral T-cell lymphomas of follicular type, and is a useful feature in distinguishing peripheral T-cell lymphomas of follicular type from morphologic mimics such as reactive hyperplasia or Hodgkin lymphoma.Modern Pathology advance online publication, 17 June 2016; doi:10.1038/modpathol.2016.113.

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