A Detailed Histologic and Molecular Assessment of the Diffuse Sclerosing Variant of Papillary Thyroid Carcinoma

Diffuse sclerosing variant papillary thyroid carcinoma (DS-PTC) is characterized clinically by a predilection for children and young adults, bulky neck nodes, and pulmonary metastases. Previous studies have suggested infrequent BRAF mutation but common RET gene rearrangements. Using strict criteria,...

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Published in:Modern pathology Vol. 36; no. 12; p. 100329
Main Authors: Chou, Angela, Qiu, Min Ru, Crayton, Henry, Wang, Bin, Ahadi, Mahsa S, Turchini, John, Clarkson, Adele, Sioson, Loretta, Sheen, Amy, Singh, Nisha, Clifton-Bligh, Roderick J, Robinson, Bruce G, Gild, Matti L, Tsang, Venessa, Leong, David, Sidhu, Stanley B, Sywak, Mark, Delbridge, Leigh, Aniss, Ahmad, Wright, Dale, Graf, Nicole, Kumar, Amit, Rathi, Vivek, Benitez-Aguirre, Paul, Glover, Anthony R, Gill, Anthony J
Format: Journal Article
Language:English
Published: United States 01.12.2023
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ISSN:1530-0285, 1530-0285
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Abstract Diffuse sclerosing variant papillary thyroid carcinoma (DS-PTC) is characterized clinically by a predilection for children and young adults, bulky neck nodes, and pulmonary metastases. Previous studies have suggested infrequent BRAF mutation but common RET gene rearrangements. Using strict criteria, we studied 43 DS-PTCs (1.9% of unselected PTCs in our unit). Seventy-nine percent harbored pathogenic gene rearrangements involving RET, NTRK3, NTRK1, ALK, or BRAF; with the remainder driven by BRAF mutations. All 10 pediatric cases were all gene rearranged (P = .02). Compared with BRAF -mutated tumors, gene rearrangement was characterized by psammoma bodies involving the entire lobe (P = .038), follicular predominant or mixed follicular architecture (P = .003), pulmonary metastases (24% vs none, P = .04), and absent classical, so-called "BRAF-like" atypia (P = .014). There was no correlation between the presence of gene rearrangement and recurrence-free survival. Features associated with persistent/recurrent disease included pediatric population (P = .030), gene-rearranged tumors (P = .020), microscopic extrathyroidal extension (P = .009), metastases at presentation (P = .007), and stage II disease (P = .015). We conclude that DS-PTC represents 1.9% of papillary thyroid carcinomas and that actionable gene rearrangements are extremely common in DS-PTC. DS-PTC can be divided into 2 distinct molecular subtypes and all BRAF -negative tumors (1.5% of papillary thyroid carcinomas) are driven by potentially actionable oncogenic fusions.
AbstractList Diffuse sclerosing variant papillary thyroid carcinoma (DS-PTC) is characterized clinically by a predilection for children and young adults, bulky neck nodes, and pulmonary metastases. Previous studies have suggested infrequent BRAFV600E mutation but common RET gene rearrangements. Using strict criteria, we studied 43 DS-PTCs (1.9% of unselected PTCs in our unit). Seventy-nine percent harbored pathogenic gene rearrangements involving RET, NTRK3, NTRK1, ALK, or BRAF; with the remainder driven by BRAFV600E mutations. All 10 pediatric cases were all gene rearranged (P = .02). Compared with BRAFV600E-mutated tumors, gene rearrangement was characterized by psammoma bodies involving the entire lobe (P = .038), follicular predominant or mixed follicular architecture (P = .003), pulmonary metastases (24% vs none, P = .04), and absent classical, so-called "BRAF-like" atypia (P = .014). There was no correlation between the presence of gene rearrangement and recurrence-free survival. Features associated with persistent/recurrent disease included pediatric population (P = .030), gene-rearranged tumors (P = .020), microscopic extrathyroidal extension (P = .009), metastases at presentation (P = .007), and stage II disease (P = .015). We conclude that DS-PTC represents 1.9% of papillary thyroid carcinomas and that actionable gene rearrangements are extremely common in DS-PTC. DS-PTC can be divided into 2 distinct molecular subtypes and all BRAFV600E-negative tumors (1.5% of papillary thyroid carcinomas) are driven by potentially actionable oncogenic fusions.Diffuse sclerosing variant papillary thyroid carcinoma (DS-PTC) is characterized clinically by a predilection for children and young adults, bulky neck nodes, and pulmonary metastases. Previous studies have suggested infrequent BRAFV600E mutation but common RET gene rearrangements. Using strict criteria, we studied 43 DS-PTCs (1.9% of unselected PTCs in our unit). Seventy-nine percent harbored pathogenic gene rearrangements involving RET, NTRK3, NTRK1, ALK, or BRAF; with the remainder driven by BRAFV600E mutations. All 10 pediatric cases were all gene rearranged (P = .02). Compared with BRAFV600E-mutated tumors, gene rearrangement was characterized by psammoma bodies involving the entire lobe (P = .038), follicular predominant or mixed follicular architecture (P = .003), pulmonary metastases (24% vs none, P = .04), and absent classical, so-called "BRAF-like" atypia (P = .014). There was no correlation between the presence of gene rearrangement and recurrence-free survival. Features associated with persistent/recurrent disease included pediatric population (P = .030), gene-rearranged tumors (P = .020), microscopic extrathyroidal extension (P = .009), metastases at presentation (P = .007), and stage II disease (P = .015). We conclude that DS-PTC represents 1.9% of papillary thyroid carcinomas and that actionable gene rearrangements are extremely common in DS-PTC. DS-PTC can be divided into 2 distinct molecular subtypes and all BRAFV600E-negative tumors (1.5% of papillary thyroid carcinomas) are driven by potentially actionable oncogenic fusions.
Diffuse sclerosing variant papillary thyroid carcinoma (DS-PTC) is characterized clinically by a predilection for children and young adults, bulky neck nodes, and pulmonary metastases. Previous studies have suggested infrequent BRAF mutation but common RET gene rearrangements. Using strict criteria, we studied 43 DS-PTCs (1.9% of unselected PTCs in our unit). Seventy-nine percent harbored pathogenic gene rearrangements involving RET, NTRK3, NTRK1, ALK, or BRAF; with the remainder driven by BRAF mutations. All 10 pediatric cases were all gene rearranged (P = .02). Compared with BRAF -mutated tumors, gene rearrangement was characterized by psammoma bodies involving the entire lobe (P = .038), follicular predominant or mixed follicular architecture (P = .003), pulmonary metastases (24% vs none, P = .04), and absent classical, so-called "BRAF-like" atypia (P = .014). There was no correlation between the presence of gene rearrangement and recurrence-free survival. Features associated with persistent/recurrent disease included pediatric population (P = .030), gene-rearranged tumors (P = .020), microscopic extrathyroidal extension (P = .009), metastases at presentation (P = .007), and stage II disease (P = .015). We conclude that DS-PTC represents 1.9% of papillary thyroid carcinomas and that actionable gene rearrangements are extremely common in DS-PTC. DS-PTC can be divided into 2 distinct molecular subtypes and all BRAF -negative tumors (1.5% of papillary thyroid carcinomas) are driven by potentially actionable oncogenic fusions.
Author Sywak, Mark
Wright, Dale
Crayton, Henry
Robinson, Bruce G
Gill, Anthony J
Wang, Bin
Ahadi, Mahsa S
Aniss, Ahmad
Glover, Anthony R
Chou, Angela
Gild, Matti L
Tsang, Venessa
Clarkson, Adele
Sheen, Amy
Sidhu, Stanley B
Qiu, Min Ru
Delbridge, Leigh
Graf, Nicole
Singh, Nisha
Turchini, John
Sioson, Loretta
Rathi, Vivek
Leong, David
Benitez-Aguirre, Paul
Kumar, Amit
Clifton-Bligh, Roderick J
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  givenname: Angela
  surname: Chou
  fullname: Chou, Angela
  email: AngelaShihYuan.Chou@health.nsw.gov.au
  organization: NSW Health Pathology, Department of Anatomical Pathology, Royal North Shore Hospital, St Leonards, New South Wales, Australia; Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Cancer Diagnosis and Pathology Research Group, Kolling Institute of Medical Research, St Leonards, New South Wales, Australia. Electronic address: AngelaShihYuan.Chou@health.nsw.gov.au
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  givenname: Min Ru
  surname: Qiu
  fullname: Qiu, Min Ru
  organization: Department of Anatomical Pathology, SydPATH, St Vincent's Hospital, Darlinghurst, New South Wales, Australia; University of NSW, Randwick, New South Wales, Australia
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  surname: Crayton
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  organization: Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia
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  givenname: Bin
  surname: Wang
  fullname: Wang, Bin
  organization: Department of Anatomical Pathology, SydPATH, St Vincent's Hospital, Darlinghurst, New South Wales, Australia
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  givenname: Mahsa S
  surname: Ahadi
  fullname: Ahadi, Mahsa S
  organization: NSW Health Pathology, Department of Anatomical Pathology, Royal North Shore Hospital, St Leonards, New South Wales, Australia; Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Cancer Diagnosis and Pathology Research Group, Kolling Institute of Medical Research, St Leonards, New South Wales, Australia
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  fullname: Turchini, John
  organization: Department of Anatomical Pathology, Douglass Hanly Moir Pathology (A Sonic Healthcare Practice), Macquarie Park, New South Wales, Australia; Discipline of Pathology, Macquarie Medical School, Macquarie University, New South Wales, Australia
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  organization: NSW Health Pathology, Department of Anatomical Pathology, Royal North Shore Hospital, St Leonards, New South Wales, Australia; Cancer Diagnosis and Pathology Research Group, Kolling Institute of Medical Research, St Leonards, New South Wales, Australia
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  givenname: Loretta
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  organization: Cancer Diagnosis and Pathology Research Group, Kolling Institute of Medical Research, St Leonards, New South Wales, Australia
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  surname: Sheen
  fullname: Sheen, Amy
  organization: Cancer Diagnosis and Pathology Research Group, Kolling Institute of Medical Research, St Leonards, New South Wales, Australia
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  givenname: Nisha
  surname: Singh
  fullname: Singh, Nisha
  organization: NSW Health Pathology, Cytogenetics Department, Royal North Shore Hospital, St Leonards, New South Wales, Australia
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  givenname: Roderick J
  surname: Clifton-Bligh
  fullname: Clifton-Bligh, Roderick J
  organization: Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Department of Endocrinology, Royal North Shore Hospital, St Leonards, New South Wales, Australia
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  givenname: Bruce G
  surname: Robinson
  fullname: Robinson, Bruce G
  organization: Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Department of Endocrinology, Royal North Shore Hospital, St Leonards, New South Wales, Australia
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  givenname: Matti L
  surname: Gild
  fullname: Gild, Matti L
  organization: Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Department of Endocrinology, Royal North Shore Hospital, St Leonards, New South Wales, Australia
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  givenname: Venessa
  surname: Tsang
  fullname: Tsang, Venessa
  organization: Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Department of Endocrinology, Royal North Shore Hospital, St Leonards, New South Wales, Australia
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  givenname: David
  surname: Leong
  fullname: Leong, David
  organization: Endocrine Surgical Unit, Royal North Shore Hospital, St Leonards, University of Sydney, New South Wales, Australia
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  givenname: Stanley B
  surname: Sidhu
  fullname: Sidhu, Stanley B
  organization: Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Endocrine Surgical Unit, Royal North Shore Hospital, St Leonards, University of Sydney, New South Wales, Australia
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  givenname: Mark
  surname: Sywak
  fullname: Sywak, Mark
  organization: Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Endocrine Surgical Unit, Royal North Shore Hospital, St Leonards, University of Sydney, New South Wales, Australia
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  givenname: Leigh
  surname: Delbridge
  fullname: Delbridge, Leigh
  organization: Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Endocrine Surgical Unit, Royal North Shore Hospital, St Leonards, University of Sydney, New South Wales, Australia
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  givenname: Ahmad
  surname: Aniss
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  givenname: Dale
  surname: Wright
  fullname: Wright, Dale
  organization: Cytogenetics Department, Sydney Genome Diagnostics, The Children's Hospital at Westmead, Westmead, New South Wales, Australia; Specialty of Genome Medicine, Faculty of Medicine and Health, University of Sydney, Sydney, New South Wales, Australia
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  givenname: Nicole
  surname: Graf
  fullname: Graf, Nicole
  organization: Histopathology Department, The Children's Hospital at Westmead, Westmead, New South Wales, Australia
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  givenname: Amit
  surname: Kumar
  fullname: Kumar, Amit
  organization: Diagnostic Genomics, Monash Health Pathology, Monash Health, Clayton, Victoria, Australia
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  organization: LifeStrands Genomics, Mount Waverley, Victoria, Australia
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  organization: Institute of Endocrinology and Diabetes, The Children's Hospital at Westmead, Westmead, New South Wales, Australia
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  givenname: Anthony R
  surname: Glover
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  email: Anthony.Glover@sydney.edu.au
  organization: Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Endocrine Surgical Unit, Royal North Shore Hospital, St Leonards, University of Sydney, New South Wales, Australia; The Kinghorn Cancer Centre, Garvan Institute of Medical Research, St. Vincent's Clinical School, Faculty of Medicine, University of New South Wales, Darlinghurst, New South Wales, Australia. Electronic address: Anthony.Glover@sydney.edu.au
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  givenname: Anthony J
  surname: Gill
  fullname: Gill, Anthony J
  email: affgill@med.usyd.edu.au
  organization: NSW Health Pathology, Department of Anatomical Pathology, Royal North Shore Hospital, St Leonards, New South Wales, Australia; Faculty of Medicine and Health Sciences and Northern Clinical School, University of Sydney, Sydney, New South Wales, Australia; Cancer Diagnosis and Pathology Research Group, Kolling Institute of Medical Research, St Leonards, New South Wales, Australia. Electronic address: affgill@med.usyd.edu.au
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Keywords ALK
RET
gene fusions
BRAF
NTRK
papillary thyroid carcinoma
diffuse sclerosing
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Snippet Diffuse sclerosing variant papillary thyroid carcinoma (DS-PTC) is characterized clinically by a predilection for children and young adults, bulky neck nodes,...
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SubjectTerms Carcinoma, Papillary - genetics
Carcinoma, Papillary - pathology
Child
Humans
Lung Neoplasms
Mutation
Proto-Oncogene Proteins B-raf - genetics
Receptor Protein-Tyrosine Kinases - genetics
Thyroid Cancer, Papillary - genetics
Thyroid Neoplasms - genetics
Thyroid Neoplasms - pathology
Young Adult
Title A Detailed Histologic and Molecular Assessment of the Diffuse Sclerosing Variant of Papillary Thyroid Carcinoma
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