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Geometric characteristics of stromal collagen fibres in breast cancer using differential interference contrast microscopy

Ghannam, Suzan F.; Rutland, Catrin Sian; Allegrucci, Cinzia; Mather, Melissa L.; Alsaleem, Mansour; Bateman-Price, Thomas D.; Patke, Rodhan; Ball, Graham; Mongan, Nigel P.; Rakha, Emad

Geometric characteristics of stromal collagen fibres in breast cancer using differential interference contrast microscopy Thumbnail


Authors

Suzan F. Ghannam

Mansour Alsaleem

Thomas D. Bateman-Price

Rodhan Patke

Graham Ball



Abstract

Breast cancer (BC) is characterised by a high level of heterogeneity, which is influenced by the interaction of neoplastic cells with the tumour microenvironment. The diagnostic and prognostic role of the tumour stroma in BC remains to be defined. Differential interference contrast (DIC) microscopy is a label-free imaging technique well suited to visualise weak optical phase objects such as cells and tissue. This study aims to compare stromal collagen fibre characteristics between in situ and invasive breast tumours using DIC microscopy and investigate the prognostic value of collagen parameters in BC. A tissue microarray was generated from 200 cases, comprising ductal carcinoma in situ (DCIS; n=100) and invasive tumours (n=100) with an extra 50 (25 invasive BC and 25 DCIS) cases for validation was utilised. Two sections per case were used: one stained with haematoxylin and eosin (H&E) stain for histological review and one unstained for examination using DIC microscopy. Collagen fibre parameters including orientation angle, fibre alignment, fibre density, fibre width, fibre length and fibre straightness were measured. Collagen fibre density was higher in the stroma of invasive BC (161.68±11.2fibre/µm2) compared to DCIS (p<0.0001). The collagen fibres were thinner (13.78±1.08µm), straighter (0.96±0.006, on a scale of 0–1), more disorganised (95.07°±11.39°) and less aligned (0.20±0.09, on a 0–1 scale) in the invasive BC compared to DCIS (all p<0.0001). A model considering these features was developed that could distinguish between DCIS and invasive tumours with 94% accuracy. There were strong correlations between fibre characteristics and clinicopathological parameters in both groups. A statistically significant association between fibre characteristics and patients’ outcomes (breast cancer specific survival, and recurrence free survival) was observed in the invasive group but not in DCIS. Although invasive BC and DCIS were both associated with stromal reaction, the structural features of collagen fibres were significantly different in the two disease stages. Analysis of the stroma fibre characteristics in the preoperative core biopsy specimen may help to differentiate pure DCIS from those associated with invasion.

Citation

Ghannam, S. F., Rutland, C. S., Allegrucci, C., Mather, M. L., Alsaleem, M., Bateman-Price, T. D., Patke, R., Ball, G., Mongan, N. P., & Rakha, E. (2024). Geometric characteristics of stromal collagen fibres in breast cancer using differential interference contrast microscopy. Journal of Microscopy, https://doi.org/10.1111/jmi.13361

Journal Article Type Article
Acceptance Date Sep 18, 2024
Online Publication Date Oct 3, 2024
Publication Date Oct 3, 2024
Deposit Date Oct 3, 2024
Publicly Available Date Oct 4, 2024
Journal Journal of Microscopy
Print ISSN 0022-2720
Electronic ISSN 1365-2818
Publisher Wiley
Peer Reviewed Peer Reviewed
DOI https://doi.org/10.1111/jmi.13361
Keywords differential interference contrast microscopy, collagen, invasive tumour, stroma, DCIS, breast cancer
Public URL https://nottingham-repository.worktribe.com/output/40285725
Publisher URL https://onlinelibrary.wiley.com/doi/10.1111/jmi.13361
PMID 39359124

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