Liquid BIOpsy for MiNimal RESidual DiSease Detection in Head and Neck Squamous Cell Carcinoma (LIONESS)-a personalised circulating tumour DNA analysis in head and neck squamous cell carcinoma.


Journal

British journal of cancer
ISSN: 1532-1827
Titre abrégé: Br J Cancer
Pays: England
ID NLM: 0370635

Informations de publication

Date de publication:
05 2022
Historique:
received: 09 05 2021
accepted: 21 01 2022
revised: 11 12 2021
pubmed: 9 2 2022
medline: 26 4 2022
entrez: 8 2 2022
Statut: ppublish

Résumé

Head and neck squamous cell carcinoma (HNSCC) remain a substantial burden to global health. Cell-free circulating tumour DNA (ctDNA) is an emerging biomarker but has not been studied sufficiently in HNSCC. We conducted a single-centre prospective cohort study to investigate ctDNA in patients with p16-negative HNSCC who received curative-intent primary surgical treatment. Whole-exome sequencing was performed on formalin-fixed paraffin-embedded (FFPE) tumour tissue. We utilised RaDaR In 17 patients analysed, personalised panels were designed to detect 34 to 52 somatic variants. Data show ctDNA detection in baseline samples taken prior to surgery in 17 of 17 patients. In post-surgery samples, ctDNA could be detected at levels as low as 0.0006% variant allele frequency. In all cases with clinical recurrence to date, ctDNA was detected prior to progression, with lead times ranging from 108 to 253 days. This study illustrates the potential of ctDNA as a biomarker for detecting minimal residual disease and recurrence in HNSCC and demonstrates the feasibility of personalised ctDNA assays for the detection of disease prior to clinical recurrence.

Sections du résumé

BACKGROUND
Head and neck squamous cell carcinoma (HNSCC) remain a substantial burden to global health. Cell-free circulating tumour DNA (ctDNA) is an emerging biomarker but has not been studied sufficiently in HNSCC.
METHODS
We conducted a single-centre prospective cohort study to investigate ctDNA in patients with p16-negative HNSCC who received curative-intent primary surgical treatment. Whole-exome sequencing was performed on formalin-fixed paraffin-embedded (FFPE) tumour tissue. We utilised RaDaR
RESULTS
In 17 patients analysed, personalised panels were designed to detect 34 to 52 somatic variants. Data show ctDNA detection in baseline samples taken prior to surgery in 17 of 17 patients. In post-surgery samples, ctDNA could be detected at levels as low as 0.0006% variant allele frequency. In all cases with clinical recurrence to date, ctDNA was detected prior to progression, with lead times ranging from 108 to 253 days.
CONCLUSIONS
This study illustrates the potential of ctDNA as a biomarker for detecting minimal residual disease and recurrence in HNSCC and demonstrates the feasibility of personalised ctDNA assays for the detection of disease prior to clinical recurrence.

Identifiants

pubmed: 35132238
doi: 10.1038/s41416-022-01716-7
pii: 10.1038/s41416-022-01716-7
pmc: PMC9023460
doi:

Substances chimiques

Biomarkers, Tumor 0
Circulating Tumor DNA 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1186-1195

Informations de copyright

© 2022. The Author(s).

Références

Cohen N, Fedewa S, Chen AY. Epidemiology and demographics of the head and neck cancer population. Oral Maxillofacial Surg Clin North Am. 2018;30:381–95.
Huang SH, O’Sullivan B. Overview of the 8th edition TNM classification for head and neck cancer. Curr Treat Option. 2017;18:40.
doi: 10.1007/s11864-017-0484-y
Hsieh JC, Wang H, Wu M, Chang K, Chang P, Liao C, et al. Review of emerging biomarkers in head and neck squamous cell carcinoma in the era of immunotherapy and targeted therapy. Head Neck. 2019;41:19–45.
doi: 10.1002/hed.25932 pubmed: 31573749
Machiels J-P, Leemans CR, Golusinski W, Grau C, Licitra L, Gregoire V, et al. Squamous cell carcinoma of the oral cavity, larynx, oropharynx and hypopharynx: EHNS–ESMO–ESTRO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2020;31:1462–75.
doi: 10.1016/j.annonc.2020.07.011 pubmed: 33239190
Gatta G, Botta L, Sánchez MJ, Anderson LA, Pierannunzio D, Licitra L, et al. Prognoses and improvement for head and neck cancers diagnosed in Europe in early 2000s: The EUROCARE-5 population-based study. Eur J Cancer. 2015;51(Oct):2130–43.
doi: 10.1016/j.ejca.2015.07.043 pubmed: 26421817
McDonald B, Contente-Cuomo T, Sammut S-J, Odenheimer-Bergman A, Ernst B, Perdigones N, et al. Personalized circulating tumor DNA analysis to detect residual disease after neoadjuvant therapy in breast cancer. Sci Transl Med. 2019;11:1–14.
Cohen JD, Li L, Wang Y, Thoburn C, Afsari B, Danilova L, et al. Detection and localization of surgically resectable cancers with a multi-analyte blood test. Science. 2018;359:eaar3247.
doi: 10.1126/science.aar3247
Wan JCM, Massie C, Garcia-Corbacho J, Mouliere F, Brenton JD, Caldas C, et al. Liquid biopsies come of age: towards implementation of circulating tumour DNA. Nat Rev Cancer. 2017;17:223–38.
doi: 10.1038/nrc.2017.7 pubmed: 28233803
Chabon JJ, Simmons AD, Lovejoy AF, Esfahani MS, Newman AM, Haringsma HJ, et al. Circulating tumour DNA profiling reveals heterogeneity of EGFR inhibitor resistance mechanisms in lung cancer patients. Nat Commun. 2016;7:11815.
doi: 10.1038/ncomms11815 pubmed: 27283993 pmcid: 4906406
Chabon JJ, Hamilton EG, Kurtz DM, Esfahani MS, Moding EJ, Stehr H, et al. Integrating genomic features for non-invasive early lung cancer detection. Nature. 2020;580:245–51.
doi: 10.1038/s41586-020-2140-0 pubmed: 32269342 pmcid: 8230734
Tie J, Wang Y, Tomasetti C, Li L, Springer S, Kinde I, et al. Circulating tumor DNA analysis detects minimal residual disease and predicts recurrence in patients with stage II colon cancer. Sci Transl Med. 2016;8:346ra92.
doi: 10.1126/scitranslmed.aaf6219 pubmed: 27384348 pmcid: 5346159
Tie J, Cohen JD, Wang Y, Christie M, Simons K, Lee M, et al. Circulating tumor DNA analyses as markers of recurrence risk and benefit of adjuvant therapy for stage III colon cancer. Jama Oncol. 2019;5:1710–7.
doi: 10.1001/jamaoncol.2019.3616 pubmed: 31621801 pmcid: 6802034
Radovich M, Jiang G, Hancock BA, Chitambar C, Nanda R, Falkson C, et al. Association of circulating tumor DNA and circulating tumor cells after neoadjuvant chemotherapy with disease recurrence in patients with triple-negative breast cancer. Jama Oncol. 2020;6:1410–5.
doi: 10.1001/jamaoncol.2020.2295 pubmed: 32644110
Shaw JA, Guttery DS, Hills A, Fernandez-Garcia D, Page K, Rosales BM, et al. Mutation analysis of cell-free DNA and single circulating tumor cells in metastatic breast cancer patients with high circulating tumor cell counts. Clin Cancer Res. 2017;23:88–96.
doi: 10.1158/1078-0432.CCR-16-0825 pubmed: 27334837
Dawson S-J, Tsui DWY, Murtaza M, Biggs H, Rueda OM, Chin S-F, et al. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N. Engl J Med. 2013;368(Mar):1199–209.
doi: 10.1056/NEJMoa1213261 pubmed: 23484797
Ococks E, Frankell AM, Soler NM, Grehan N, Northrop A, Coles H, et al. Longitudinal tracking of 97 esophageal adenocarcinomas using liquid biopsy sampling. Ann Oncol. 2021;32:522–32.
doi: 10.1016/j.annonc.2020.12.010 pubmed: 33359547
Openshaw MR, Mohamed AA, Ottolini B, Fernandez-Garcia D, Richards CJ, Page K, et al. Longitudinal monitoring of circulating tumour DNA improves prognostication and relapse detection in gastroesophageal adenocarcinoma. Brit J Cancer. 2020;123:1271–9.
doi: 10.1038/s41416-020-1002-8 pubmed: 32719550 pmcid: 7555811
Lee JH, Saw RP, Thompson JF, Lo S, Spillane AJ, Shannon KF, et al. Pre-operative ctDNA predicts survival in high-risk stage III cutaneous melanoma patients. Ann Oncol. 2019;30:mdz075.
Capone RB, Pai SI, Koch WM, Gillison ML, Danish HN, Westra WH, et al. Detection and quantitation of human papillomavirus (HPV) DNA in the sera of patients with HPV-associated head and neck squamous cell carcinoma. Clin Cancer Res. 2000;6:4171–5.
pubmed: 11106228
Ahn SM, Chan JYK, Zhang Z, Wang H, Khan Z, Bishop JA, et al. Saliva and plasma quantitative polymerase chain reaction–based detection and surveillance of human papillomavirus–related head and neck cancer. Jama Otolaryngol Head Neck Surg. 2014;140:846–54.
doi: 10.1001/jamaoto.2014.1338 pubmed: 25078109 pmcid: 4313904
Borsetto D, Cheng J, Payne K, Nankivell P, Batis N, Rao K, et al. Surveillance of HPV-positive head and neck squamous cell carcinoma with circulating and salivary DNA biomarkers. Crit Rev Oncogenesis. 2018;23:235–45.
doi: 10.1615/CritRevOncog.2018027689 pubmed: 30311577
Damerla RR, Lee NY, You D, Soni R, Shah R, Reyngold M, et al. Detection of early human papillomavirus–associated cancers by liquid biopsy. Jco Precis Oncol 2019;3:1–17.
Fakhry C, Blackford AL, Neuner G, Xiao W, Jiang B, Agrawal A, et al. Association of oral human papillomavirus DNA persistence with cancer progression after primary treatment for oral cavity and oropharyngeal squamous cell carcinoma. Jama Oncol. 2019;5:985–92.
doi: 10.1001/jamaoncol.2019.0439 pubmed: 31046104 pmcid: 6499134
Hanna GJ, Lau CJ, Mahmood U, Supplee JG, Mogili AR, Haddad RI, et al. Salivary HPV DNA informs locoregional disease status in advanced HPV-associated oropharyngeal cancer. Oral Oncol. 2019;95:120–6.
doi: 10.1016/j.oraloncology.2019.06.019 pubmed: 31345379
Chera BS, Kumar S, Beaty BT, Marron D, Jefferys S, Green R, et al. Rapid clearance profile of plasma circulating tumor HPV type 16 DNA during chemoradiotherapy correlates with disease control in HPV-associated oropharyngeal cancer. Clin Cancer Res. 2019;25:4682–90.
doi: 10.1158/1078-0432.CCR-19-0211 pubmed: 31088830 pmcid: 6679766
Chera BS, Kumar S, Shen C, Amdur R, Dagan R, Green R, et al. Plasma circulating tumor HPV DNA for the surveillance of cancer recurrence in HPV-associated oropharyngeal cancer. J Clin Oncol. 2020;38:1050–8.
doi: 10.1200/JCO.19.02444 pubmed: 32017652 pmcid: 7106982
Wang Y, Springer S, Mulvey CL, Silliman N, Schaefer J, Sausen M, et al. Detection of somatic mutations and HPV in the saliva and plasma of patients with head and neck squamous cell carcinomas. Sci Transl Med. 2015;7:293ra104.
pubmed: 26109104 pmcid: 4587492 doi: 10.1126/scitranslmed.aaa8507
Bettegowda C, Sausen M, Leary RJ, Kinde I, Wang Y, Agrawal N, et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med. 2014;6:224ra24.
doi: 10.1126/scitranslmed.3007094 pubmed: 24553385 pmcid: 4017867
Bratman SV, Yang SYC, Iafolla MAJ, Liu Z, Hansen AR, Bedard PL, et al. Personalized circulating tumor DNA analysis as a predictive biomarker in solid tumor patients treated with pembrolizumab. Nat Cancer. 2020;1:873–81.
doi: 10.1038/s43018-020-0096-5 pubmed: 35121950
Schirmer MA, Beck J, Leu M, Oellerich M, Rave-Fränk M, Walson PD, et al. Cell-free plasma DNA for disease stratification and prognosis in head and neck cancer. Clin Chem. 2018;64:959–70.
doi: 10.1373/clinchem.2017.285668 pubmed: 29661793
Perdomo S, Avogbe PH, Foll M, Abedi-Ardekani B, Facciolla VL, Anantharaman D, et al. Circulating tumor DNA detection in head and neck cancer: evaluation of two different detection approaches. Oncotarget. 2014;5:72621–32.
Onidani K, Shoji H, Kakizaki T, Yoshimoto S, Okaya S, Miura N, et al. Monitoring of cancer patients via next‐generation sequencing of patient‐derived circulating tumor cells and tumor DNA. Cancer Sci. 2019;110:2590–9.
doi: 10.1111/cas.14092 pubmed: 31169336 pmcid: 6676129
Braig F, Voigtlaender M, Schieferdecker A, Busch C-J, Laban S, Grob T, et al. Liquid biopsy monitoring uncovers acquired RAS-mediated resistance to cetuximab in a substantial proportion of patients with head and neck squamous cell carcinoma. Oncotarget. 2016;7:42988–95.
doi: 10.18632/oncotarget.8943 pubmed: 27119512 pmcid: 5190002
Egyud M, Sridhar P, Devaiah A, Yamada E, Saunders S, Ståhlberg A, et al. Plasma circulating tumor DNA as a potential tool for disease monitoring in head and neck cancer. Head Neck. 2018;68:7–8.
TCGA. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature 2015;517:576–82.
doi: 10.1038/nature14129
Agrawal N, Frederick MJ, Pickering CR, Bettegowda C, Chang K, Li RJ, et al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science. 2011;333:1154–7.
doi: 10.1126/science.1206923 pubmed: 21798897 pmcid: 3162986
Gaykalova DA, Mambo E, Choudhary A, Houghton J, Buddavarapu K, Sanford T, et al. Novel insight into mutational landscape of head and neck squamous cell carcinoma. Amin ARMR. PLoS ONE. 2014;9:e93102-9.
Leemans CR, Snijders PJF, Brakenhoff RH. The molecular landscape of head and neck cancer. Nat Rev Cancer. 2018;18:269–82.
doi: 10.1038/nrc.2018.11 pubmed: 29497144
Lechner M, Frampton GM, Fenton T, Feber A, Palmer G, Jay A, et al. Targeted next-generation sequencing of head and neck squamous cell carcinoma identifies novel genetic alterations in HPV+ and HPV- tumors. Genome Med. 2013;5:1–12.
doi: 10.1186/gm453
Stransky N, Egloff AM, Tward AD, Kostic AD, Cibulskis K, Sivachenko A, et al. The Mutational landscape of head and neck squamous cell carcinoma. Science. 2011;333:1157–60.
doi: 10.1126/science.1208130 pubmed: 21798893 pmcid: 3415217
National Comprehensive Cancer Network guidelines [Internet]. n.d. [cited 2021 May 6]. Available from: https://www.nccn.org/about/default.aspx.
Gale D, Lawson ARJ, Howarth K, Madi M, Durham B, Smalley S, et al. Development of a highly sensitive liquid biopsy platform to detect clinically-relevant cancer mutations at low allele fractions in cell-free DNA. PLoS ONE. 2018;13:e0194630.
doi: 10.1371/journal.pone.0194630 pubmed: 29547634 pmcid: 5856404
Plagnol V, Woodhouse S, Howarth K, Lensing S, Smith M, Epstein M, et al. Analytical validation of a next generation sequencing liquid biopsy assay for high sensitivity broad molecular profiling. PLoS ONE. 2018;13:e0193802.
doi: 10.1371/journal.pone.0193802 pubmed: 29543828 pmcid: 5854321
Cutts RJ, Coakley M, Garcia-Murillas I, Ulrich L, Howarth K, Emmett W, et al. Abstract 536: Molecular residual disease detection in early stage breast cancer with a personalized sequencing approach. Presented at: AACR Annual Meeting; April 10-15, 2021; virtual.
Heider K, Gale DG, Marsico G, Ruiz-Valdepeñas A, Sharma G, Perry M, et al. Detection of residual disease and recurrence in early-stage non-small cell lung cancer (NSCLC) patients using sensitive personalized ctDNA sequencing assays. J Clin Oncol. 2020;38:e15560.
doi: 10.1200/JCO.2020.38.15_suppl.e15560
Gillison ML, D’Souza G, Westra W, Sugar E, Xiao W, Begum S, et al. Distinct risk factor profiles for human papillomavirus type 16–positive and human papillomavirus type 16–negative head and neck cancers. J Natl Cancer Inst. 2008;100:407–20.
doi: 10.1093/jnci/djn025 pubmed: 18334711
Begum S, Westra WH. Basaloid squamous cell carcinoma of the head and neck is a mixed variant that can be further resolved by HPV status. Am J Surg Pathol. 2008;32:1044–50.
doi: 10.1097/PAS.0b013e31816380ec pubmed: 18496144
Seiwert TY, Zuo Z, Keck MK, Khattri A, Pedamallu CS, Stricker T, et al. Integrative and comparative genomic analysis of HPV-positive and HPV-negative head and neck squamous cell carcinomas. Clin Cancer Res. 2015;21:632–41.
doi: 10.1158/1078-0432.CCR-13-3310 pubmed: 25056374
Mazurek AM, Rutkowski T, Fiszer-Kierzkowska A, Małusecka E, Składowski K. Assessment of the total cfDNA and HPV16/18 detection in plasma samples of head and neck squamous cell carcinoma patients. Oral Oncol. 2016;54:36–41.
doi: 10.1016/j.oraloncology.2015.12.002 pubmed: 26786940
Zwirner K, Hilke FJ, Demidov G, Ossowski S, Gani C, Rieß O, et al. Circulating cell-free DNA: a potential biomarker to differentiate inflammation and infection during radiochemotherapy. Radiother Oncol. 2018;129:575–81.
doi: 10.1016/j.radonc.2018.07.016 pubmed: 30097252
Lee JH, Ba D, Liu G, Leslie D, Zacharia BE, Goyal N. Association of head and neck cancer with mental health disorders in a large insurance claims database. Jama Otolaryngol Head Neck Surg. 2019;145:339–44.
doi: 10.1001/jamaoto.2018.4512 pubmed: 30816930 pmcid: 6481424
Lazure KE, Lydiatt WM, Denman D, Burke WJ. Association between depression and survival or disease recurrence in patients with head and neck cancer enrolled in a depression prevention trial. Head Neck. 2009;31:888–92.
doi: 10.1002/hed.21046 pubmed: 19309726
Leeuw IMV, Jansen F, Brakenhoff RH, Langendijk JA, Takes R, Terhaard CHJ, et al. Advancing interdisciplinary research in head and neck cancer through a multicenter longitudinal prospective cohort study: the NETherlands QUality of life and BIomedical Cohort (NET-QUBIC) data warehouse and biobank. Bmc Cancer. 2019;19:765.
doi: 10.1186/s12885-019-5866-z
Jurmeister P, Bockmayr M, Seegerer P, Bockmayr T, Treue D, Montavon G, et al. Machine learning analysis of DNA methylation profiles distinguishes primary lung squamous cell carcinomas from head and neck metastases. Sci Transl Med. 2019;11:eaaw8513.
doi: 10.1126/scitranslmed.aaw8513 pubmed: 31511427
Brands MT, Brennan PA, Verbeek ALM, Merkx MAW, Geurts SME. Follow-up after curative treatment for oral squamous cell carcinoma. A critical appraisal of the guidelines and a review of the literature. Eur J Surg Oncol. 2018;44:559–65.
doi: 10.1016/j.ejso.2018.01.004 pubmed: 29433990
Manikantan K, Khode S, Dwivedi RC, Palav R, Nutting CM, Rhys-Evans P, et al. Making sense of post-treatment surveillance in head and neck cancer: when and what of follow-up. Cancer Treat Rev. 2009;35:744–53.
doi: 10.1016/j.ctrv.2009.08.007 pubmed: 19744793
Bailey MH, Tokheim C, Porta-Pardo E, Sengupta S, Bertrand D, Weerasinghe A, et al. Comprehensive characterization of cancer driver genes and mutations. Cell. 2018;173:371–85.
doi: 10.1016/j.cell.2018.02.060 pubmed: 29625053 pmcid: 6029450

Auteurs

Susanne Flach (S)

Department of Otorhinolaryngology, Head and Neck Surgery, Hospital of the Ludwig-Maximilians-University (LMU) of Munich, Marchioninistrasse 15, 81377, Munich, Germany. susanne.flach@med.uni-muenchen.de.

Karen Howarth (K)

Inivata Ltd, Babraham Research Park, Cambridge, UK.

Sophie Hackinger (S)

Inivata Ltd, Babraham Research Park, Cambridge, UK.

Christodoulos Pipinikas (C)

Inivata Ltd, Babraham Research Park, Cambridge, UK.

Pete Ellis (P)

Inivata Ltd, Babraham Research Park, Cambridge, UK.

Kirsten McLay (K)

Inivata Ltd, Babraham Research Park, Cambridge, UK.

Giovanni Marsico (G)

Inivata Ltd, Babraham Research Park, Cambridge, UK.

Tim Forshew (T)

Inivata Ltd, Babraham Research Park, Cambridge, UK.

Christoph Walz (C)

Institute of Pathology, Faculty of Medicine, LMU Munich, Munich, Germany.

Christoph A Reichel (CA)

Department of Otorhinolaryngology, Head and Neck Surgery, Hospital of the Ludwig-Maximilians-University (LMU) of Munich, Marchioninistrasse 15, 81377, Munich, Germany.

Olivier Gires (O)

Department of Otorhinolaryngology, Head and Neck Surgery, Hospital of the Ludwig-Maximilians-University (LMU) of Munich, Marchioninistrasse 15, 81377, Munich, Germany.
Clinical Cooperation Group "Personalised Radiotherapy in Head and Neck Cancer", German Research Centre for Environmental Health GmbH, Neuherberg, Munich, Germany.

Martin Canis (M)

Department of Otorhinolaryngology, Head and Neck Surgery, Hospital of the Ludwig-Maximilians-University (LMU) of Munich, Marchioninistrasse 15, 81377, Munich, Germany.
Clinical Cooperation Group "Personalised Radiotherapy in Head and Neck Cancer", German Research Centre for Environmental Health GmbH, Neuherberg, Munich, Germany.

Philipp Baumeister (P)

Department of Otorhinolaryngology, Head and Neck Surgery, Hospital of the Ludwig-Maximilians-University (LMU) of Munich, Marchioninistrasse 15, 81377, Munich, Germany.
Clinical Cooperation Group "Personalised Radiotherapy in Head and Neck Cancer", German Research Centre for Environmental Health GmbH, Neuherberg, Munich, Germany.

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