Ionizing radiation improves skin bacterial dysbiosis in cutaneous T-cell lymphoma

Front Immunol. 2024 Dec 24:15:1520214. doi: 10.3389/fimmu.2024.1520214. eCollection 2024.

Abstract

Introduction: Cutaneous T-cell lymphoma (CTCL) is closely associated with the host microbiome. While recent evidence suggests that shifts in specific bacterial taxa are associated with response to UV-B, a form of non-ionizing radiation, the impact of ionizing radiation (IR) has not been investigated.

Methods: 16S rRNA and tuf gene amplicon sequencing were performed on DNA extracted from swabs of lesional/non-lesional skin of 12 CTCL patients before/after TSEBT or local IR and from 25 matched healthy controls (HC). Microbial diversity and taxonomic profiles were analyzed.

Results: Radiation exposure increased CTCL skin α-diversity to levels approximating HC. TSEBT appeared to carry the greatest effect compared to local IR. Both α and β-diversity differed significantly post versus pre-IR for TSEBT, but not for local IR. IR was associated with decreases in known pathogenic bacteria such as Streptococcus and S. aureus and increases in healthy commensal bacteria such as Anaerococcus, Bifidobacterium and commensal staphylococci including S. pettenkoferi. Substantially more taxa shifts were seen with TSEBT versus local IR.

Discussion: IR not only eliminates CTCL lesions via induction of apoptosis, but also facilitates skin barrier restoration and recolonization of bacterial taxa associated with a healthy skin microbiome. Local IR does not have as strong an effect on the skin microbiome as TSEBT. As skin microbiota act as immunomodulators with local and potentially systemic influence, TSEBT may also improve CTCL lesions via global effects on the skin microbiome. Future larger-scale studies are required to fully elucidate the relationship between cutaneous microbes and IR treatment in CTCL.

Keywords: cutaneous T-cell lymphoma; lymphoma; microbiome; radiation; radiotherapy; skin cancer; total skin electron beam therapy.

MeSH terms

  • Adult
  • Aged
  • Bacteria / classification
  • Bacteria / isolation & purification
  • Bacteria / radiation effects
  • Dysbiosis* / microbiology
  • Female
  • Humans
  • Lymphoma, T-Cell, Cutaneous* / microbiology
  • Lymphoma, T-Cell, Cutaneous* / radiotherapy
  • Male
  • Microbiota* / radiation effects
  • Middle Aged
  • RNA, Ribosomal, 16S / genetics
  • Radiation, Ionizing*
  • Skin Neoplasms / etiology
  • Skin Neoplasms / microbiology
  • Skin Neoplasms / radiotherapy
  • Skin* / microbiology
  • Skin* / radiation effects

Substances

  • RNA, Ribosomal, 16S

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. Supported by a Cutaneous Lymphoma Foundation Catalyst Research Grant, American Cancer Society Institutional Research Grant, Lymphoma Research Foundation Clinical Career Development Award, Gilead Research Scholars Program Award in Hematologic Malignancies, and an institutional grant from the Northwestern University Clinical and Translational Sciences Institute (NUCATS) and the National Institutes of Health (NIH) (GRANT KL2TR001424).