Early Detection of Malignant and Premalignant Peripheral Nerve Tumors Using Cell-Free DNA Fragmentomics

Clin Cancer Res. 2024 Oct 1;30(19):4363-4376. doi: 10.1158/1078-0432.CCR-24-0797.

Abstract

Purpose: Early detection of neurofibromatosis type 1 (NF1)-associated peripheral nerve sheath tumors (PNST) informs clinical decision-making, enabling early definitive treatment and potentially averting deadly outcomes. In this study, we describe a cell-free DNA (cfDNA) fragmentomic approach that distinguishes nonmalignant, premalignant, and malignant forms of PNST in the cancer predisposition syndrome, NF1.

Experimental design: cfDNA was isolated from plasma samples of a novel cohort of 101 patients with NF1 and 21 healthy controls and underwent whole-genome sequencing. We investigated diagnosis-specific signatures of copy-number alterations with in silico size selection as well as fragment profiles. Fragmentomics were analyzed using complementary feature types: bin-wise fragment size ratios, end motifs, and fragment non-negative matrix factorization signatures.

Results: The novel cohort of patients with NF1 validated that our previous cfDNA copy-number alteration-based approach identifies malignant PNST (MPNST) but cannot distinguish between benign and premalignant states. Fragmentomic methods were able to differentiate premalignant states including atypical neurofibromas (AN). Fragmentomics also adjudicated AN cases suspicious for MPNST, correctly diagnosing samples noninvasively, which could have informed clinical management.

Conclusions: Novel cfDNA fragmentomic signatures distinguish AN from benign plexiform neurofibromas and MPNST, enabling more precise clinical diagnosis and management. This study pioneers the early detection of malignant and premalignant PNST in NF1 and provides a blueprint for decentralizing noninvasive cancer surveillance in hereditary cancer predisposition syndromes.

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Biomarkers, Tumor* / blood
  • Biomarkers, Tumor* / genetics
  • Cell-Free Nucleic Acids* / blood
  • Cell-Free Nucleic Acids* / genetics
  • Child
  • DNA Copy Number Variations*
  • Early Detection of Cancer* / methods
  • Female
  • Humans
  • Male
  • Middle Aged
  • Nerve Sheath Neoplasms / blood
  • Nerve Sheath Neoplasms / diagnosis
  • Nerve Sheath Neoplasms / genetics
  • Nerve Sheath Neoplasms / pathology
  • Neurofibromatosis 1 / diagnosis
  • Neurofibromatosis 1 / genetics
  • Peripheral Nervous System Neoplasms / diagnosis
  • Peripheral Nervous System Neoplasms / genetics
  • Peripheral Nervous System Neoplasms / pathology
  • Precancerous Conditions / blood
  • Precancerous Conditions / diagnosis
  • Precancerous Conditions / genetics
  • Precancerous Conditions / pathology
  • Whole Genome Sequencing / methods
  • Young Adult

Substances

  • Cell-Free Nucleic Acids
  • Biomarkers, Tumor