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. 2021 Nov 5;13(21):5553.
doi: 10.3390/cancers13215553.

Characterisation of Collagen Re-Modelling in Localised Prostate Cancer Using Second-Generation Harmonic Imaging and Transrectal Ultrasound Shear Wave Elastography

Wael Ageeli  1   2 , Xinyu Zhang  3 , Chidozie N Ogbonnaya  1 , Yuting Ling  4 , Jennifer Wilson  5 , Chunhui Li  6 , Ghulam Nabi  1
Affiliations

Characterisation of Collagen Re-Modelling in Localised Prostate Cancer Using Second-Generation Harmonic Imaging and Transrectal Ultrasound Shear Wave Elastography

Wael Ageeli et al. Cancers (Basel). .

Abstract

Prostate cancer has a poor prognosis and high mortality rate due to metastases. Extracellular matrix (ECM) re-modelling and stroma composition have been linked to cancer progression, including key components of cell migration, tumour metastasis, and tissue modulus. Moreover, collagens are one of the most significant components of the extracellular matrix and have been ascribed to many aspects of neoplastic transformation. This study characterises collagen re-modelling around localised prostate cancer using the second harmonic generation of collagen (SHG), genotyping and ultrasound shear wave elastography (USWE) measured modulus in men with clinically localised prostate cancer. Tempo-sequence assay for gene expression of COL1A1 and COL3A1 was used to confirm the expression of collagen. Second-harmonic generation imaging and genotyping of ECM around prostate cancer showed changes in content, orientation, and type of collagen according to Gleason grades (cancer aggressivity), and this correlated with the tissue modulus measured by USWE in kilopascals. Furthermore, there were clear differences between collagen orientation and type around normal and cancer tissues.

Keywords: collagen; elastography; prostate; second-generation harmonics; shear wave; ultrasound.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Bar chart of the Gleason score and USWE modulus in 30 patients with prostate cancer (the bar is the mean modulus in each Gleason score category with standard deviation sitting on the top of the bar), (rs = 0.67, p < 0.001, n = 30).
Figure 2
Figure 2
Comparison between normal prostate tissue and cancer prostate tissue. SHG images of collagen alignment in (a) normal prostate tissue and (b) cancer prostate tissue. Histopathology images of (c) normal prostate glands and (d) fused prostate glands occupied by cancer cells. The scale bar is 100 μm. The microscope magnification is 200×.
Figure 3
Figure 3
Prostate cancer sections with different Gleason scores. (A1–A5) SHG images, and (B1–B5) H&E images. In specimens with prostate cancer GS 3 + 3 (1), the SHG signals in prostate cancer were surrounding the glands with more closed margins; however, these became fainter and partially lost in GS 3 + 4 (2) and 4 + 3 (3). As the cancer is more aggressive GS (3 + 5 (4) and 4 + 5 (5)), the cancer cells fill the gland, and some spread to the stroma. In GS 4 + 5, the glands are fused, and there are only sheets of cancer cells left with no glandular shape. The scale bar is 300 μm, and the microscope magnification is 100×.
Figure 4
Figure 4
Violin Plot showing data distribution between cancer fibre orientation and Gleason score groups (grey rectangular sport in each violin is the mean of each group).
Figure 5
Figure 5
Scatter plot of the USWE modulus and SHG collagen orientation in 30 patients with prostate cancer (r = 0.74, p < 0.001, n = 30).
Figure 6
Figure 6
Residual plot between residuals and cancer orientation.
Figure 7
Figure 7
Bar chart of Gleason score and cancer collagen orientation in 30 patients with prostate cancer (the bar is the mean A:I ratio in each Gleason score category with standard deviation sitting on the top of the bar), rs = 0.93, p < 0.001, n = 30.
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