Deciphering molecular relapse and intra-tumor heterogeneity in non-metastatic resectable head and neck squamous cell carcinoma using circulating tumor DNA

Oral Oncol. 2025 Jan:160:107111. doi: 10.1016/j.oraloncology.2024.107111. Epub 2024 Nov 29.

Abstract

Objectives: Head and neck squamous cell carcinoma (HNSCC) is characterized by significant genetic intra-tumor heterogeneity (ITH), which may hinder precision medicine strategies that depend on results from single tumor-biopsy specimens. Treatment response assessment relies on radiologic imaging, which cannot detect minimal residual disease (MRD). We assessed the relevance of circulating tumor DNA (ctDNA) as a biomarker for ITH and MRD in HNSCC.

Materials and methods: We recruited 41 non-metastatic resectable HNSCC patients treated with upfront curative-intent surgery in the prospective biobanking SCANDARE study (NCT03017573). Thirty-one patients (76 %) showed recurrent disease at a median follow-up of 41 months. Targeted next-generation sequencing was performed on resected tumor tissues, as well as on serial blood samples obtained at surgery, within 14 weeks after surgery, at six months and at recurrence.

Results: ctDNA was detected in 21/41 patients at surgery (sensitivity: 51 %; 95 % CI, 35-67 %) and 15/22 patients at recurrence (sensitivity: 68 %; 95 % confidence interval [CI], 45-86 %). Among patients with mutations identified in longitudinal plasma samples, additional mutations missed in tumor tissues were reported in 3/21 patients (14 %), while emerging mutations were reported in 9/21 patients (43 %). In the postoperative surveillance setting, ctDNA-based MRD detection anticipated clinical recurrence with a median lead-time of 9.9 months (interquartile range, 8.0-14.5 months) in 17/27 patients (63 %). When detected within 14 weeks after surgery, MRD correlated with disease recurrence after adjusting for classical prognostic variables (HR = 3.0; 95 % CI, 1.1-7.9; p = 0.03).

Conclusions: ctDNA detection is a useful biomarker for ITH and MRD in resectable HNSCC patients.

Keywords: Biomarkers; Head and neck squamous cell carcinoma; Liquid biopsy; Next-generation sequencing; Tumor heterogeneity; circulating tumor DNA.

Publication types

  • Clinical Study

MeSH terms

  • Adult
  • Aged
  • Biomarkers, Tumor / blood
  • Biomarkers, Tumor / genetics
  • Circulating Tumor DNA* / blood
  • Circulating Tumor DNA* / genetics
  • Female
  • Genetic Heterogeneity
  • Head and Neck Neoplasms* / blood
  • Head and Neck Neoplasms* / genetics
  • Head and Neck Neoplasms* / pathology
  • Head and Neck Neoplasms* / surgery
  • High-Throughput Nucleotide Sequencing / methods
  • Humans
  • Male
  • Middle Aged
  • Mutation
  • Neoplasm Recurrence, Local* / blood
  • Neoplasm Recurrence, Local* / genetics
  • Neoplasm, Residual
  • Prospective Studies
  • Squamous Cell Carcinoma of Head and Neck* / blood
  • Squamous Cell Carcinoma of Head and Neck* / genetics
  • Squamous Cell Carcinoma of Head and Neck* / pathology
  • Squamous Cell Carcinoma of Head and Neck* / surgery

Substances

  • Biomarkers, Tumor
  • Circulating Tumor DNA