Skip to main content
Top
Published in: BMC Medical Imaging 1/2022

Open Access 01-12-2022 | Ultrasound | Research

An endorectal ultrasound-based radiomics signature for preoperative prediction of lymphovascular invasion of rectal cancer

Authors: Yu-quan Wu, Rui-zhi Gao, Peng Lin, Rong Wen, Hai-yuan Li, Mei-yan Mou, Feng-huan Chen, Fen Huang, Wei-jie Zhou, Hong Yang, Yun He, Ji Wu

Published in: BMC Medical Imaging | Issue 1/2022

Login to get access

Abstract

Objective

To investigate whether radiomics based on ultrasound images can predict lymphovascular invasion (LVI) of rectal cancer (RC) before surgery.

Methods

A total of 203 patients with RC were enrolled retrospectively, and they were divided into a training set (143 patients) and a validation set (60 patients). We extracted the radiomic features from the largest gray ultrasound image of the RC lesion. The intraclass correlation coefficient (ICC) was applied to test the repeatability of the radiomic features. The least absolute shrinkage and selection operator (LASSO) was used to reduce the data dimension and select significant features. Logistic regression (LR) analysis was applied to establish the radiomics model. The receiver operating characteristic (ROC) curve, calibration curve, and decision curve analysis (DCA) were used to evaluate the comprehensive performance of the model.

Results

Among the 203 patients, 33 (16.7%) were LVI positive and 170 (83.7%) were LVI negative. A total of 5350 (90.1%) radiomic features with ICC values of ≥ 0.75 were reported, which were subsequently subjected to hypothesis testing and LASSO regression dimension reduction analysis. Finally, 15 selected features were used to construct the radiomics model. The area under the curve (AUC) of the training set was 0.849, and the AUC of the validation set was 0.781. The calibration curve indicated that the radiomics model had good calibration, and DCA demonstrated that the model had clinical benefits.

Conclusion

The proposed endorectal ultrasound-based radiomics model has the potential to predict LVI preoperatively in RC.
Appendix
Available only for authorised users
Literature
1.
go back to reference Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49.CrossRef Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49.CrossRef
2.
go back to reference Asoglu O, Tokmak H, Bakir B, Demir G, Ozyar E, Atalar B, Goksel S, Koza B, Guven Mert A, Demir A, et al. The impact of total neo-adjuvant treatment on nonoperative management in patients with locally advanced rectal cancer: The evaluation of 66 cases. Eur J Surg Oncol. 2020;46(3):402–9.CrossRef Asoglu O, Tokmak H, Bakir B, Demir G, Ozyar E, Atalar B, Goksel S, Koza B, Guven Mert A, Demir A, et al. The impact of total neo-adjuvant treatment on nonoperative management in patients with locally advanced rectal cancer: The evaluation of 66 cases. Eur J Surg Oncol. 2020;46(3):402–9.CrossRef
3.
go back to reference van Groningen JT, van Hagen P, Tollenaar R, Tuynman JB, de Mheen PJM, Doornebosch PG, Tanis PJ, de Graaf EJR, Dutch Colorectal A. Evaluation of a completion total mesorectal excision in patients after local excision of rectal cancer: a word of caution. J Natl Compr Canc Netw. 2018;16(7):822–8.CrossRef van Groningen JT, van Hagen P, Tollenaar R, Tuynman JB, de Mheen PJM, Doornebosch PG, Tanis PJ, de Graaf EJR, Dutch Colorectal A. Evaluation of a completion total mesorectal excision in patients after local excision of rectal cancer: a word of caution. J Natl Compr Canc Netw. 2018;16(7):822–8.CrossRef
4.
go back to reference Lee L, de Lacy B, Gomez Ruiz M, Liberman AS, Albert MR, Monson JRT, Lacy A, Kim SH, Atallah SB. A multicenter matched comparison of transanal and robotic total mesorectal excision for mid and low-rectal adenocarcinoma. Ann Surg. 2019;270(6):1110–6.CrossRef Lee L, de Lacy B, Gomez Ruiz M, Liberman AS, Albert MR, Monson JRT, Lacy A, Kim SH, Atallah SB. A multicenter matched comparison of transanal and robotic total mesorectal excision for mid and low-rectal adenocarcinoma. Ann Surg. 2019;270(6):1110–6.CrossRef
5.
go back to reference Bonnetain F, Bosset JF, Gerard JP, Calais G, Conroy T, Mineur L, Bouche O, Maingon P, Chapet O, Radosevic-Jelic L, et al. What is the clinical benefit of preoperative chemoradiotherapy with 5FU/leucovorin for T3–4 rectal cancer in a pooled analysis of EORTC 22921 and FFCD 9203 trials: surrogacy in question? Eur J Cancer. 2012;48(12):1781–90.CrossRef Bonnetain F, Bosset JF, Gerard JP, Calais G, Conroy T, Mineur L, Bouche O, Maingon P, Chapet O, Radosevic-Jelic L, et al. What is the clinical benefit of preoperative chemoradiotherapy with 5FU/leucovorin for T3–4 rectal cancer in a pooled analysis of EORTC 22921 and FFCD 9203 trials: surrogacy in question? Eur J Cancer. 2012;48(12):1781–90.CrossRef
6.
go back to reference Kim YC, Kim JK, Kim MJ, Lee JH, Kim YB, Shin SJ. Feasibility of mesorectal vascular invasion in predicting early distant metastasis in patients with stage T3 rectal cancer based on rectal MRI. Eur Radiol. 2016;26(2):297–305.CrossRef Kim YC, Kim JK, Kim MJ, Lee JH, Kim YB, Shin SJ. Feasibility of mesorectal vascular invasion in predicting early distant metastasis in patients with stage T3 rectal cancer based on rectal MRI. Eur Radiol. 2016;26(2):297–305.CrossRef
7.
go back to reference Smith NJ, Barbachano Y, Norman AR, Swift RI, Abulafi AM, Brown G. Prognostic significance of magnetic resonance imaging-detected extramural vascular invasion in rectal cancer. Br J Surg. 2008;95(2):229–36.CrossRef Smith NJ, Barbachano Y, Norman AR, Swift RI, Abulafi AM, Brown G. Prognostic significance of magnetic resonance imaging-detected extramural vascular invasion in rectal cancer. Br J Surg. 2008;95(2):229–36.CrossRef
8.
go back to reference Schaap DP, Ogura A, Nederend J, Maas M, Cnossen JS, Creemers GJ, van Lijnschoten I, Nieuwenhuijzen GAP, Rutten HJT, Kusters M. Prognostic implications of MRI-detected lateral nodal disease and extramural vascular invasion in rectal cancer. Br J Surg. 2018;105(13):1844–52.CrossRef Schaap DP, Ogura A, Nederend J, Maas M, Cnossen JS, Creemers GJ, van Lijnschoten I, Nieuwenhuijzen GAP, Rutten HJT, Kusters M. Prognostic implications of MRI-detected lateral nodal disease and extramural vascular invasion in rectal cancer. Br J Surg. 2018;105(13):1844–52.CrossRef
9.
go back to reference Ogura A, Konishi T, Cunningham C, Garcia-Aguilar J, Iversen H, Toda S, Lee IK, Lee HX, Uehara K, Lee P, et al. Neoadjuvant (chemo)radiotherapy with total mesorectal excision only is not sufficient to prevent lateral local recurrence in enlarged nodes: results of the multicenter lateral node study of patients with low cT3/4 rectal cancer. J Clin Oncol. 2019;37(1):33–43.CrossRef Ogura A, Konishi T, Cunningham C, Garcia-Aguilar J, Iversen H, Toda S, Lee IK, Lee HX, Uehara K, Lee P, et al. Neoadjuvant (chemo)radiotherapy with total mesorectal excision only is not sufficient to prevent lateral local recurrence in enlarged nodes: results of the multicenter lateral node study of patients with low cT3/4 rectal cancer. J Clin Oncol. 2019;37(1):33–43.CrossRef
10.
go back to reference Horvat N. Carlos Tavares Rocha C, Clemente Oliveira B, Petkovska I, Gollub MJ: MRI of rectal cancer: tumor staging, imaging techniques, and management. Radiographics. 2019;39(2):367–87.CrossRef Horvat N. Carlos Tavares Rocha C, Clemente Oliveira B, Petkovska I, Gollub MJ: MRI of rectal cancer: tumor staging, imaging techniques, and management. Radiographics. 2019;39(2):367–87.CrossRef
11.
go back to reference Van Calster B, Wynants L, Verbeek JFM, Verbakel JY, Christodoulou E, Vickers AJ, Roobol MJ, Steyerberg EW. Reporting and interpreting decision curve analysis: a guide for investigators. Eur Urol. 2018;74(6):796–804.CrossRef Van Calster B, Wynants L, Verbeek JFM, Verbakel JY, Christodoulou E, Vickers AJ, Roobol MJ, Steyerberg EW. Reporting and interpreting decision curve analysis: a guide for investigators. Eur Urol. 2018;74(6):796–804.CrossRef
12.
go back to reference Chan BPH, Patel R, Mbuagbaw L, Thabane L, Yaghoobi M. EUS versus magnetic resonance imaging in staging rectal adenocarcinoma: a diagnostic test accuracy meta-analysis. Gastrointest Endosc. 2019;90(2):196–203.CrossRef Chan BPH, Patel R, Mbuagbaw L, Thabane L, Yaghoobi M. EUS versus magnetic resonance imaging in staging rectal adenocarcinoma: a diagnostic test accuracy meta-analysis. Gastrointest Endosc. 2019;90(2):196–203.CrossRef
13.
go back to reference Xu Q, Xu Y, Sun H, Jiang T, Xie S, Ooi BY, Ding Y. MRI evaluation of complete response of locally advanced rectal cancer after neoadjuvant therapy: current status and future trends. Cancer Manag Res. 2021;13:4317–28.CrossRef Xu Q, Xu Y, Sun H, Jiang T, Xie S, Ooi BY, Ding Y. MRI evaluation of complete response of locally advanced rectal cancer after neoadjuvant therapy: current status and future trends. Cancer Manag Res. 2021;13:4317–28.CrossRef
14.
go back to reference Davey MS, Davey MG, Ryan EJ, Hogan AM, Kerin MJ, Joyce M. The use of radiomic analysis of magnetic resonance imaging in predicting distant metastases of rectal carcinoma following surgical resection: a systematic review and meta-analysis. Colorectal Dis. 2021;23(12):3065–72.CrossRef Davey MS, Davey MG, Ryan EJ, Hogan AM, Kerin MJ, Joyce M. The use of radiomic analysis of magnetic resonance imaging in predicting distant metastases of rectal carcinoma following surgical resection: a systematic review and meta-analysis. Colorectal Dis. 2021;23(12):3065–72.CrossRef
15.
go back to reference Hou M, Sun JH. Emerging applications of radiomics in rectal cancer: state of the art and future perspectives. World J Gastroenterol. 2021;27(25):3802–14.CrossRef Hou M, Sun JH. Emerging applications of radiomics in rectal cancer: state of the art and future perspectives. World J Gastroenterol. 2021;27(25):3802–14.CrossRef
16.
go back to reference Stanzione A, Verde F, Romeo V, Boccadifuoco F, Mainenti PP, Maurea S. Radiomics and machine learning applications in rectal cancer: current update and future perspectives. World J Gastroenterol. 2021;27(32):5306–21.CrossRef Stanzione A, Verde F, Romeo V, Boccadifuoco F, Mainenti PP, Maurea S. Radiomics and machine learning applications in rectal cancer: current update and future perspectives. World J Gastroenterol. 2021;27(32):5306–21.CrossRef
17.
go back to reference Huang YQ, Liang CH, He L, Tian J, Liang CS, Chen X, Ma ZL, Liu ZY. Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol. 2016;34(18):2157–64.CrossRef Huang YQ, Liang CH, He L, Tian J, Liang CS, Chen X, Ma ZL, Liu ZY. Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol. 2016;34(18):2157–64.CrossRef
18.
go back to reference Ge YX, Xu WB, Wang Z, Zhang JQ, Zhou XY, Duan SF, Hu SD, Fei BJ. Prognostic value of CT radiomics in evaluating lymphovascular invasion in rectal cancer: diagnostic performance based on different volumes of interest. J Xray Sci Technol. 2021;29(4):663–74.PubMed Ge YX, Xu WB, Wang Z, Zhang JQ, Zhou XY, Duan SF, Hu SD, Fei BJ. Prognostic value of CT radiomics in evaluating lymphovascular invasion in rectal cancer: diagnostic performance based on different volumes of interest. J Xray Sci Technol. 2021;29(4):663–74.PubMed
19.
go back to reference Zhang Y, He K, Guo Y, Liu X, Yang Q, Zhang C, Xie Y, Mu S, Guo Y, Fu Y, et al. A novel multimodal radiomics model for preoperative prediction of lymphovascular invasion in rectal cancer. Front Oncol. 2020;10:457.CrossRef Zhang Y, He K, Guo Y, Liu X, Yang Q, Zhang C, Xie Y, Mu S, Guo Y, Fu Y, et al. A novel multimodal radiomics model for preoperative prediction of lymphovascular invasion in rectal cancer. Front Oncol. 2020;10:457.CrossRef
20.
go back to reference Yang YS, Qiu YJ, Zheng GH, Gong HP, Ge YQ, Zhang YF, Feng F, Wang YT. High resolution MRI-based radiomic nomogram in predicting perineural invasion in rectal cancer. Cancer Imaging. 2021;21(1):40.CrossRef Yang YS, Qiu YJ, Zheng GH, Gong HP, Ge YQ, Zhang YF, Feng F, Wang YT. High resolution MRI-based radiomic nomogram in predicting perineural invasion in rectal cancer. Cancer Imaging. 2021;21(1):40.CrossRef
21.
go back to reference Tibermacine H, Rouanet P, Sbarra M, Forghani R, Reinhold C, Nougaret S, Group GS. Radiomics modelling in rectal cancer to predict disease-free survival: evaluation of different approaches. Br J Surg. 2021;108(10):1243–50.CrossRef Tibermacine H, Rouanet P, Sbarra M, Forghani R, Reinhold C, Nougaret S, Group GS. Radiomics modelling in rectal cancer to predict disease-free survival: evaluation of different approaches. Br J Surg. 2021;108(10):1243–50.CrossRef
22.
go back to reference Delli Pizzi A, Chiarelli AM, Chiacchiaretta P, d’Annibale M, Croce P, Rosa C, Mastrodicasa D, Trebeschi S, Lambregts DMJ, Caposiena D, et al. MRI-based clinical-radiomics model predicts tumor response before treatment in locally advanced rectal cancer. Sci Rep. 2021;11(1):5379.CrossRef Delli Pizzi A, Chiarelli AM, Chiacchiaretta P, d’Annibale M, Croce P, Rosa C, Mastrodicasa D, Trebeschi S, Lambregts DMJ, Caposiena D, et al. MRI-based clinical-radiomics model predicts tumor response before treatment in locally advanced rectal cancer. Sci Rep. 2021;11(1):5379.CrossRef
23.
go back to reference Horvat N, Veeraraghavan H, Khan M, Blazic I, Zheng J, Capanu M, Sala E, Garcia-Aguilar J, Gollub MJ, Petkovska I. MR imaging of rectal cancer: radiomics analysis to assess treatment response after neoadjuvant therapy. Radiology. 2018;287(3):833–43.CrossRef Horvat N, Veeraraghavan H, Khan M, Blazic I, Zheng J, Capanu M, Sala E, Garcia-Aguilar J, Gollub MJ, Petkovska I. MR imaging of rectal cancer: radiomics analysis to assess treatment response after neoadjuvant therapy. Radiology. 2018;287(3):833–43.CrossRef
24.
go back to reference Peng Y, Lin P, Wu L, Wan D, Zhao Y, Liang L, Ma X, Qin H, Liu Y, Li X, et al. Ultrasound-based radiomics analysis for preoperatively predicting different histopathological subtypes of primary liver cancer. Front Oncol. 2020;10:1646.CrossRef Peng Y, Lin P, Wu L, Wan D, Zhao Y, Liang L, Ma X, Qin H, Liu Y, Li X, et al. Ultrasound-based radiomics analysis for preoperatively predicting different histopathological subtypes of primary liver cancer. Front Oncol. 2020;10:1646.CrossRef
25.
go back to reference Li F, Pan D, He Y, Wu Y, Peng J, Li J, Wang Y, Yang H, Chen J. Using ultrasound features and radiomics analysis to predict lymph node metastasis in patients with thyroid cancer. BMC Surg. 2020;20(1):315.CrossRef Li F, Pan D, He Y, Wu Y, Peng J, Li J, Wang Y, Yang H, Chen J. Using ultrasound features and radiomics analysis to predict lymph node metastasis in patients with thyroid cancer. BMC Surg. 2020;20(1):315.CrossRef
26.
go back to reference Keller DS, Berho M, Perez RO, Wexner SD, Chand M. The multidisciplinary management of rectal cancer. Nat Rev Gastroenterol Hepatol. 2020;17(7):414–29.CrossRef Keller DS, Berho M, Perez RO, Wexner SD, Chand M. The multidisciplinary management of rectal cancer. Nat Rev Gastroenterol Hepatol. 2020;17(7):414–29.CrossRef
27.
go back to reference Crivelli P, Ledda RE, Parascandolo N, Fara A, Soro D, Conti M. A new challenge for radiologists: radiomics in breast cancer. Biomed Res Int. 2018;2018:6120703.CrossRef Crivelli P, Ledda RE, Parascandolo N, Fara A, Soro D, Conti M. A new challenge for radiologists: radiomics in breast cancer. Biomed Res Int. 2018;2018:6120703.CrossRef
28.
go back to reference Lee M, Wei S, Anaokar J, Uzzo R, Kutikov A. Kidney cancer management 3.0: can artificial intelligence make us better? Curr Opin Urol. 2021;31(4):409–15.CrossRef Lee M, Wei S, Anaokar J, Uzzo R, Kutikov A. Kidney cancer management 3.0: can artificial intelligence make us better? Curr Opin Urol. 2021;31(4):409–15.CrossRef
29.
go back to reference Alvarez-Jimenez C, Antunes JT, Talasila N, Bera K, Brady JT, Gollamudi J, Marderstein E, Kalady MF, Purysko A, Willis JE, et al. Radiomic texture and shape descriptors of the rectal environment on post-chemoradiation T2-weighted MRI are associated with pathologic tumor stage regression in rectal cancers: a retrospective, multi-institution study. Cancers (Basel). 2020;12(8):2027.CrossRef Alvarez-Jimenez C, Antunes JT, Talasila N, Bera K, Brady JT, Gollamudi J, Marderstein E, Kalady MF, Purysko A, Willis JE, et al. Radiomic texture and shape descriptors of the rectal environment on post-chemoradiation T2-weighted MRI are associated with pathologic tumor stage regression in rectal cancers: a retrospective, multi-institution study. Cancers (Basel). 2020;12(8):2027.CrossRef
30.
go back to reference Liu Z, Zhang XY, Shi YJ, Wang L, Zhu HT, Tang Z, Wang S, Li XT, Tian J, Sun YS. Radiomics analysis for evaluation of pathological complete response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Clin Cancer Res. 2017;23(23):7253–62.CrossRef Liu Z, Zhang XY, Shi YJ, Wang L, Zhu HT, Tang Z, Wang S, Li XT, Tian J, Sun YS. Radiomics analysis for evaluation of pathological complete response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Clin Cancer Res. 2017;23(23):7253–62.CrossRef
31.
go back to reference van Timmeren JE, Cester D, Tanadini-Lang S, Alkadhi H, Baessler B. Radiomics in medical imaging-"how-to" guide and critical reflection. Insights Imaging. 2020;11(1):91.CrossRef van Timmeren JE, Cester D, Tanadini-Lang S, Alkadhi H, Baessler B. Radiomics in medical imaging-"how-to" guide and critical reflection. Insights Imaging. 2020;11(1):91.CrossRef
32.
go back to reference Yao Z, Dong Y, Wu G, Zhang Q, Yang D, Yu JH, Wang WP. Preoperative diagnosis and prediction of hepatocellular carcinoma: radiomics analysis based on multi-modal ultrasound images. BMC Cancer. 2018;18(1):1089.CrossRef Yao Z, Dong Y, Wu G, Zhang Q, Yang D, Yu JH, Wang WP. Preoperative diagnosis and prediction of hepatocellular carcinoma: radiomics analysis based on multi-modal ultrasound images. BMC Cancer. 2018;18(1):1089.CrossRef
33.
go back to reference Li M, Zhu YZ, Zhang YC, Yue YF, Yu HP, Song B. Radiomics of rectal cancer for predicting distant metastasis and overall survival. World J Gastroenterol. 2020;26(33):5008–21.CrossRef Li M, Zhu YZ, Zhang YC, Yue YF, Yu HP, Song B. Radiomics of rectal cancer for predicting distant metastasis and overall survival. World J Gastroenterol. 2020;26(33):5008–21.CrossRef
34.
go back to reference Mongan J, Moy L, Kahn CE Jr. Checklist for Artificial Intelligence in Medical Imaging (CLAIM): a guide for authors and reviewers. Radiol Artif Intell. 2020;2(2):CrossRef Mongan J, Moy L, Kahn CE Jr. Checklist for Artificial Intelligence in Medical Imaging (CLAIM): a guide for authors and reviewers. Radiol Artif Intell. 2020;2(2):CrossRef
Metadata
Title
An endorectal ultrasound-based radiomics signature for preoperative prediction of lymphovascular invasion of rectal cancer
Authors
Yu-quan Wu
Rui-zhi Gao
Peng Lin
Rong Wen
Hai-yuan Li
Mei-yan Mou
Feng-huan Chen
Fen Huang
Wei-jie Zhou
Hong Yang
Yun He
Ji Wu
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Medical Imaging / Issue 1/2022
Electronic ISSN: 1471-2342
DOI
https://doi.org/10.1186/s12880-022-00813-6

Other articles of this Issue 1/2022

BMC Medical Imaging 1/2022 Go to the issue