Abstract
Background
Structural abnormality is a well-recognized feature of malignancy. On the other hand, diffusion-weighted MRI (DWI) has been reported as a tool that can reflect tumor biology.
Aims
The purpose of this study is to apply histogram analysis to DWI to quantify structural abnormality of colorectal cancer, and evaluate its biomarker value.
Methods
This is a retrospective study of 80 (46 men and 34 women; median age: 68.0 years) colorectal cancer patients who underwent DWI followed by curative surgery at the Chiba University Hospital between 2009 and 2011. Median follow-up time was 62.2 months. Histogram parameters including signal intensity of kurtosis and skewness of the tumor were measured on DWI at b = 1000, and mean apparent diffusion coefficient value (ADC) of the tumor was also measured on ADC map generated by DWIs at b = 0 and 1000. Associations of tumor parameters (kurtosis, skewness, and ADC) with pathological features were analyzed, and these parameters were also compared with overall survival (OS) and relapse-free survival (RFS) using Cox regression and Kaplan–Meier analysis.
Results
ADC of the tumor did not have significant associations with any pathological factors, but kurtosis and skewness of signal intensity in the tumor was significantly different between tumors with distant metastases and those without (4.23 ± 1.31 vs. 3.24 ± 1.32, p = 0.04; 1.09 ± 0.39 vs. 0.57 ± 0.58, p = 0.03). Kurtosis of the tumor was significantly correlated with OS and RFS (p = 0.04, p = 0.03, respectively), and skewness was significantly correlated with OS (p = 0.03) in Cox regression analysis. Higher kurtosis or higher skewness of the tumor was associated with worse OS in Kaplan–Meier analysis (p = 0.01, p = 0.009, log-rank). In subset analysis, there were 50 patients (32 men and 18 women) of lymph node-negative colorectal cancers (≤ stage II); skewness of signal intensity in the tumor was associated with OS using univariate Cox regression analysis (p = 0.04).
Conclusions
Histogram analysis of DWI can be a prognostic biomarker for colorectal cancer.
Similar content being viewed by others
Abbreviations
- CRC:
-
Colorectal cancer
- MRI:
-
Magnetic resonance imaging
- DWI:
-
Diffusion-weighted MR image
- ADC:
-
Apparent diffusion coefficient
- OS:
-
Overall survival
- RFS:
-
Relapse-free survival
References
Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–E386.
Tomlinson JS, Jarnagin WR, DeMatteo RP, et al. Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol. 2007;25:4575–4580.
Durrett R, Foo J, Leder K, Mayberry J, Michor F. Intratumor heterogeneity in evolutionary models of tumor progression. Genetics. 2011;188:461–477.
Miles KA, Ganeshan B, Hayball MP. CT texture analysis using the filtration-histogram method: what do the measurements mean? Cancer Imaging. 2013;13:400–406.
Yip C, Landau D, Kozarski R, et al. Primary esophageal cancer: heterogeneity as potential prognostic biomarker in patients treated with definitive chemotherapy and radiation therapy. Radiology. 2014;270:141–148.
Goh V, Ganeshan B, Nathan P, Juttla JK, Vinayan A, Miles KA. Assessment of response to tyrosine kinase inhibitors in metastatic renal cell cancer: CT texture as a predictive biomarker. Radiology. 2011;261:165–171.
Zhang H, Graham CM, Elci O, et al. Locally advanced squamous cell carcinoma of the head and neck: CT texture and histogram analysis allow independent prediction of overall survival in patients treated with induction chemotherapy. Radiology. 2013;269:801–809.
Hayano K, Tian F, Kambadakone AR, et al. Texture analysis of non-contrast-enhanced computed tomography for assessing angiogenesis and survival of soft tissue sarcoma. J Comput Assist Tomogr. 2015;39:607–612.
Cho SH, Kim GC, Jang YJ, et al. Locally advanced rectal cancer: post-chemoradiotherapy ADC histogram analysis for predicting a complete response. Acta Radiol. 2015;56:1042–1050.
Choi MH, Oh SN, Rha SE, et al. J Magn Reson Imaging. 2016;44:212–220.
Schob S, Meyer HJ, Dieckow J, et al. Histogram analysis of diffusion weighted imaging at 3T is useful for prediction of lymphatic metastatic spread, proliferative activity, and cellularity in thyroid cancer. Int J Mol Sci. 2017;18:821.
Xu XQ, Hu H, Su GY, et al. Utility of histogram analysis of ADC maps for differentiating orbital tumors. Diagn Interv Radiol. 2016;22:161–167.
Padhani AR, Liu G, Koh DM, et al. Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia. 2009;11:102–125.
Hayano K, Miura F, Wada K, et al. Diffusion-weighted MR imaging of pancreatic cancer and inflammation: prognostic significance of pancreatic inflammation in pancreatic cancer patients. Pancreatology. 2016;16:121–126.
Aoyagi T, Shuto K, Okazumi S, Hayano K, et al. Apparent diffusion coefficient correlation with oesophageal tumour stroma and angiogenesis. Eur Radiol. 2012;22:1172–1177.
Hayano K, Lee SH, Yoshida H, Zhu AX, Sahani DV. Fractal analysis of CT perfusion images for evaluation of antiangiogenic treatment and survival in hepatocellular carcinoma. Acad Radiol. 2014;21:654–660.
Razek AA. Diffusion-weighted magnetic resonance imaging of head and neck. J Comput Assist Tomogr. 2010;34:808–815.
Abdel Razek AAK. Routine and advanced diffusion imaging modules of the salivary glands. Neuroimaging Clin N Am. 2018;28:245–254.
Razek A, Nada N, Ghaniem M, Elkhamary S. Assessment of soft tissue tumours of the extremities with diffusion echoplanar MR imaging. Radiol Med. 2012;117:96–101.
Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6:392–401.
Hansen TF, Kjær-Frifeldt S, Lindebjerg J, et al. Tumor-stroma ratio predicts recurrence in patients with colon cancer treated with neoadjuvant chemotherapy. Acta Oncol. 2018;57:528–533.
King AD, Chow KK, Yu KH, et al. Head and neck squamous cell carcinoma: diagnostic performance of diffusion-weighted MR imaging for the prediction of treatment response. Radiology. 2013;266:531–538.
Acknowledgments
This study was partly supported by the Cancer Research Funds for Patients and Family.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There are no financial or other relations that could lead to a conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Takahashi, Y., Hayano, K., Ohira, G. et al. Histogram Analysis of Diffusion-Weighted MR Imaging as a Biomarker to Predict Survival of Surgically Treated Colorectal Cancer Patients. Dig Dis Sci 66, 1227–1232 (2021). https://doi.org/10.1007/s10620-020-06318-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10620-020-06318-y