Clinical, genomic, and metagenomic characterization of oral tongue squamous cell carcinoma in patients who do not smoke

Ryan Li, Daniel L. Faden, Carole Fakhry, Chaz Langelier, Yuchen Jiao, Yuxuan Wang, Matthew D. Wilkerson, Chandra Sekhar Pedamallu, Matthew Old, James Lang, Myriam Loyo, Sun Mi Ahn, Marietta Tan, Zhen Gooi, Jason Chan, Jeremy Richmon, Laura D. Wood, Ralph H. Hruban, Justin Bishop, William H. Westra & 11 others Christine H. Chung, Joseph Califano, Christine G. Gourin, Chetan Bettegowda, Matthew Meyerson, Nickolas Papadopoulos, Kenneth W. Kinzler, Bert Vogelstein, Joseph L. Derisi, Wayne M. Koch, Nishant Agrawal

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

Background Evidence suggests the incidence of oral tongue squamous cell carcinoma is increasing in young patients, many who have no history of tobacco use. Methods We clinically reviewed 89 patients with oral tongue cancer. Exomic sequencing of tumor DNA from 6 nonsmokers was performed and compared to previously sequenced cases. RNA from 20 tumors was evaluated by massively parallel sequencing to search for potentially oncogenic viruses. Results Non-smokers (53 of 89) were younger than smokers (36 of 89; mean, 50.4 vs 61.9 years; p<.001), and seemed more likely to be women (58.5% vs 38.9%; p=.069). Nonsmokers had fewer TP53 mutations (p=.02) than smokers. No tumor-associated viruses were detected. Conclusion The young age of nonsmoking patients with oral tongue cancer and fewer TP53 mutations suggest a viral role in this disease. Our efforts to identify such a virus were unsuccessful. Further studies are warranted to elucidate the drivers of carcinogenesis in these patients.

Original languageEnglish (US)
Pages (from-to)1642-1649
Number of pages8
JournalHead and Neck
Volume37
Issue number11
DOIs
StatePublished - Jan 1 2015

Fingerprint

Metagenomics
Tongue
Smoke
Squamous Cell Carcinoma
Tongue Neoplasms
Oncogenic Viruses
Mouth Neoplasms
Satellite Viruses
High-Throughput Nucleotide Sequencing
Mutation
Tobacco Use
DNA Sequence Analysis
Neoplasms
Carcinogenesis
RNA
Viruses
Incidence

Keywords

  • head and neck cancer
  • next-generation sequencing
  • nonsmokers
  • oral tongue
  • squamous cell carcinoma

ASJC Scopus subject areas

  • Otorhinolaryngology

Cite this

Li, R., Faden, D. L., Fakhry, C., Langelier, C., Jiao, Y., Wang, Y., ... Agrawal, N. (2015). Clinical, genomic, and metagenomic characterization of oral tongue squamous cell carcinoma in patients who do not smoke. Head and Neck, 37(11), 1642-1649. https://doi.org/10.1002/hed.23807

Clinical, genomic, and metagenomic characterization of oral tongue squamous cell carcinoma in patients who do not smoke. / Li, Ryan; Faden, Daniel L.; Fakhry, Carole; Langelier, Chaz; Jiao, Yuchen; Wang, Yuxuan; Wilkerson, Matthew D.; Pedamallu, Chandra Sekhar; Old, Matthew; Lang, James; Loyo, Myriam; Ahn, Sun Mi; Tan, Marietta; Gooi, Zhen; Chan, Jason; Richmon, Jeremy; Wood, Laura D.; Hruban, Ralph H.; Bishop, Justin; Westra, William H.; Chung, Christine H.; Califano, Joseph; Gourin, Christine G.; Bettegowda, Chetan; Meyerson, Matthew; Papadopoulos, Nickolas; Kinzler, Kenneth W.; Vogelstein, Bert; Derisi, Joseph L.; Koch, Wayne M.; Agrawal, Nishant.

In: Head and Neck, Vol. 37, No. 11, 01.01.2015, p. 1642-1649.

Research output: Contribution to journalArticle

Li, R, Faden, DL, Fakhry, C, Langelier, C, Jiao, Y, Wang, Y, Wilkerson, MD, Pedamallu, CS, Old, M, Lang, J, Loyo, M, Ahn, SM, Tan, M, Gooi, Z, Chan, J, Richmon, J, Wood, LD, Hruban, RH, Bishop, J, Westra, WH, Chung, CH, Califano, J, Gourin, CG, Bettegowda, C, Meyerson, M, Papadopoulos, N, Kinzler, KW, Vogelstein, B, Derisi, JL, Koch, WM & Agrawal, N 2015, 'Clinical, genomic, and metagenomic characterization of oral tongue squamous cell carcinoma in patients who do not smoke', Head and Neck, vol. 37, no. 11, pp. 1642-1649. https://doi.org/10.1002/hed.23807
Li, Ryan ; Faden, Daniel L. ; Fakhry, Carole ; Langelier, Chaz ; Jiao, Yuchen ; Wang, Yuxuan ; Wilkerson, Matthew D. ; Pedamallu, Chandra Sekhar ; Old, Matthew ; Lang, James ; Loyo, Myriam ; Ahn, Sun Mi ; Tan, Marietta ; Gooi, Zhen ; Chan, Jason ; Richmon, Jeremy ; Wood, Laura D. ; Hruban, Ralph H. ; Bishop, Justin ; Westra, William H. ; Chung, Christine H. ; Califano, Joseph ; Gourin, Christine G. ; Bettegowda, Chetan ; Meyerson, Matthew ; Papadopoulos, Nickolas ; Kinzler, Kenneth W. ; Vogelstein, Bert ; Derisi, Joseph L. ; Koch, Wayne M. ; Agrawal, Nishant. / Clinical, genomic, and metagenomic characterization of oral tongue squamous cell carcinoma in patients who do not smoke. In: Head and Neck. 2015 ; Vol. 37, No. 11. pp. 1642-1649.
@article{79c6851397e0445694aee0076b813d1a,
title = "Clinical, genomic, and metagenomic characterization of oral tongue squamous cell carcinoma in patients who do not smoke",
abstract = "Background Evidence suggests the incidence of oral tongue squamous cell carcinoma is increasing in young patients, many who have no history of tobacco use. Methods We clinically reviewed 89 patients with oral tongue cancer. Exomic sequencing of tumor DNA from 6 nonsmokers was performed and compared to previously sequenced cases. RNA from 20 tumors was evaluated by massively parallel sequencing to search for potentially oncogenic viruses. Results Non-smokers (53 of 89) were younger than smokers (36 of 89; mean, 50.4 vs 61.9 years; p<.001), and seemed more likely to be women (58.5{\%} vs 38.9{\%}; p=.069). Nonsmokers had fewer TP53 mutations (p=.02) than smokers. No tumor-associated viruses were detected. Conclusion The young age of nonsmoking patients with oral tongue cancer and fewer TP53 mutations suggest a viral role in this disease. Our efforts to identify such a virus were unsuccessful. Further studies are warranted to elucidate the drivers of carcinogenesis in these patients.",
keywords = "head and neck cancer, next-generation sequencing, nonsmokers, oral tongue, squamous cell carcinoma",
author = "Ryan Li and Faden, {Daniel L.} and Carole Fakhry and Chaz Langelier and Yuchen Jiao and Yuxuan Wang and Wilkerson, {Matthew D.} and Pedamallu, {Chandra Sekhar} and Matthew Old and James Lang and Myriam Loyo and Ahn, {Sun Mi} and Marietta Tan and Zhen Gooi and Jason Chan and Jeremy Richmon and Wood, {Laura D.} and Hruban, {Ralph H.} and Justin Bishop and Westra, {William H.} and Chung, {Christine H.} and Joseph Califano and Gourin, {Christine G.} and Chetan Bettegowda and Matthew Meyerson and Nickolas Papadopoulos and Kinzler, {Kenneth W.} and Bert Vogelstein and Derisi, {Joseph L.} and Koch, {Wayne M.} and Nishant Agrawal",
year = "2015",
month = "1",
day = "1",
doi = "10.1002/hed.23807",
language = "English (US)",
volume = "37",
pages = "1642--1649",
journal = "Head and Neck",
issn = "1043-3074",
publisher = "Wiley-Liss Inc.",
number = "11",

}

TY - JOUR

T1 - Clinical, genomic, and metagenomic characterization of oral tongue squamous cell carcinoma in patients who do not smoke

AU - Li, Ryan

AU - Faden, Daniel L.

AU - Fakhry, Carole

AU - Langelier, Chaz

AU - Jiao, Yuchen

AU - Wang, Yuxuan

AU - Wilkerson, Matthew D.

AU - Pedamallu, Chandra Sekhar

AU - Old, Matthew

AU - Lang, James

AU - Loyo, Myriam

AU - Ahn, Sun Mi

AU - Tan, Marietta

AU - Gooi, Zhen

AU - Chan, Jason

AU - Richmon, Jeremy

AU - Wood, Laura D.

AU - Hruban, Ralph H.

AU - Bishop, Justin

AU - Westra, William H.

AU - Chung, Christine H.

AU - Califano, Joseph

AU - Gourin, Christine G.

AU - Bettegowda, Chetan

AU - Meyerson, Matthew

AU - Papadopoulos, Nickolas

AU - Kinzler, Kenneth W.

AU - Vogelstein, Bert

AU - Derisi, Joseph L.

AU - Koch, Wayne M.

AU - Agrawal, Nishant

PY - 2015/1/1

Y1 - 2015/1/1

N2 - Background Evidence suggests the incidence of oral tongue squamous cell carcinoma is increasing in young patients, many who have no history of tobacco use. Methods We clinically reviewed 89 patients with oral tongue cancer. Exomic sequencing of tumor DNA from 6 nonsmokers was performed and compared to previously sequenced cases. RNA from 20 tumors was evaluated by massively parallel sequencing to search for potentially oncogenic viruses. Results Non-smokers (53 of 89) were younger than smokers (36 of 89; mean, 50.4 vs 61.9 years; p<.001), and seemed more likely to be women (58.5% vs 38.9%; p=.069). Nonsmokers had fewer TP53 mutations (p=.02) than smokers. No tumor-associated viruses were detected. Conclusion The young age of nonsmoking patients with oral tongue cancer and fewer TP53 mutations suggest a viral role in this disease. Our efforts to identify such a virus were unsuccessful. Further studies are warranted to elucidate the drivers of carcinogenesis in these patients.

AB - Background Evidence suggests the incidence of oral tongue squamous cell carcinoma is increasing in young patients, many who have no history of tobacco use. Methods We clinically reviewed 89 patients with oral tongue cancer. Exomic sequencing of tumor DNA from 6 nonsmokers was performed and compared to previously sequenced cases. RNA from 20 tumors was evaluated by massively parallel sequencing to search for potentially oncogenic viruses. Results Non-smokers (53 of 89) were younger than smokers (36 of 89; mean, 50.4 vs 61.9 years; p<.001), and seemed more likely to be women (58.5% vs 38.9%; p=.069). Nonsmokers had fewer TP53 mutations (p=.02) than smokers. No tumor-associated viruses were detected. Conclusion The young age of nonsmoking patients with oral tongue cancer and fewer TP53 mutations suggest a viral role in this disease. Our efforts to identify such a virus were unsuccessful. Further studies are warranted to elucidate the drivers of carcinogenesis in these patients.

KW - head and neck cancer

KW - next-generation sequencing

KW - nonsmokers

KW - oral tongue

KW - squamous cell carcinoma

UR - http://www.scopus.com/inward/record.url?scp=84944031585&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84944031585&partnerID=8YFLogxK

U2 - 10.1002/hed.23807

DO - 10.1002/hed.23807

M3 - Article

VL - 37

SP - 1642

EP - 1649

JO - Head and Neck

JF - Head and Neck

SN - 1043-3074

IS - 11

ER -