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Published in: Annals of Surgical Oncology 11/2020

01-10-2020 | Computed Tomography | Colorectal Cancer

Radiomics Approach Outperforms Diameter Criteria for Predicting Pathological Lateral Lymph Node Metastasis After Neoadjuvant (Chemo)Radiotherapy in Advanced Low Rectal Cancer

Authors: Ryota Nakanishi, MD, PhD, Takashi Akiyoshi, MD, PhD, Shigeo Toda, MD, Yu Murakami, MSc, Senzo Taguchi, MD, PhD, Koji Oba, PhD, Yutaka Hanaoka, MD, Toshiya Nagasaki, MD, PhD, Tomohiro Yamaguchi, MD, PhD, Tsuyoshi Konishi, MD, PhD, Shuichiro Matoba, MD, PhD, Masashi Ueno, MD, PhD, Yosuke Fukunaga, MD, PhD, Hiroya Kuroyanagi, MD, PhD

Published in: Annals of Surgical Oncology | Issue 11/2020

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Abstract

Background

Advanced low rectal cancer has a non-negligible risk of lateral pelvic lymph node (LPLN) metastasis (LPLNM) and lateral local recurrence (LR) after neoadjuvant (chemo)radiotherapy and total mesorectal excision. LPLN dissection (LPLND) reduces LR but increases postoperative complications and sexual/urinary dysfunction.

Objective

The aim of this study was to develop a new radiomics-based prediction model for LPLNM in patients with rectal cancer.

Methods

A total of 247 patients with rectal cancer and enlarged LPLNs treated by (chemo)radiotherapy and LPLND were enrolled in this retrospective, multicenter study. LPLN radiomic features were extracted from pretreatment portal venous-phase computed tomography images. A radiomics score of LPLN was constructed based on the least absolute shrinkage and selection operator regression in a primary cohort of 175 patients. Model performance was assessed in terms of discrimination, calibration, and decision curve analysis, and was externally validated in 72 patients.

Results

The radiomics score showed significantly better discrimination compared with pretreatment short-axis diameter measurements in both the primary (area under the curve [AUC] 0.91 vs. 0.83, p = 0.0015) and validation (AUC 0.90 vs. 0.80, p = 0.0298) cohorts. Decision curve analysis also indicated the superiority of the radiomics score. In a subanalysis of patients with a short-axis diameter ≥ 7 mm, the radiomics nomogram, incorporating the radiomics score and LPLN shrinkage to ≤ 4 mm, had better discrimination compared with a model incorporating only LPLN shrinkage in both cohorts.

Conclusions

Radiomics-based prediction modeling provides individualized risk estimation of LPLNM in rectal cancer patients treated with (chemo)radiotherapy, and outperforms measurements of pretreatment LPLN diameter.
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Literature
1.
go back to reference Kapiteijn E, Marijnen CA, Nagtegaal ID, et al. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001;345:638–46.PubMed Kapiteijn E, Marijnen CA, Nagtegaal ID, et al. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001;345:638–46.PubMed
2.
go back to reference Sauer R, Becker H, Hohenberger W, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med. 2004;351:1731–40.PubMed Sauer R, Becker H, Hohenberger W, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med. 2004;351:1731–40.PubMed
3.
go back to reference Bosset JF, Collette L, Calais G, et al. Chemotherapy with preoperative radiotherapy in rectal cancer. N Engl J Med. 2006;355:1114–23.PubMed Bosset JF, Collette L, Calais G, et al. Chemotherapy with preoperative radiotherapy in rectal cancer. N Engl J Med. 2006;355:1114–23.PubMed
4.
go back to reference Akiyoshi T, Watanabe T, Miyata S, Kotake K, Muto T, Sugihara K. Results of a Japanese nationwide multi-institutional study on lateral pelvic lymph node metastasis in low rectal cancer: is it regional or distant disease? Ann Surg. 2012;255:1129–34.PubMed Akiyoshi T, Watanabe T, Miyata S, Kotake K, Muto T, Sugihara K. Results of a Japanese nationwide multi-institutional study on lateral pelvic lymph node metastasis in low rectal cancer: is it regional or distant disease? Ann Surg. 2012;255:1129–34.PubMed
5.
go back to reference Hashiguchi Y, Muro K, Saito Y, et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol. 2020;25:1–42.PubMed Hashiguchi Y, Muro K, Saito Y, et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol. 2020;25:1–42.PubMed
6.
go back to reference Georgiou P, Tan E, Gouvas N, et al. Extended lymphadenectomy versus conventional surgery for rectal cancer: a meta-analysis. Lancet Oncol. 2009;10:1053–62.PubMed Georgiou P, Tan E, Gouvas N, et al. Extended lymphadenectomy versus conventional surgery for rectal cancer: a meta-analysis. Lancet Oncol. 2009;10:1053–62.PubMed
7.
go back to reference Benson AB, Venook AP, Al-Hawary MM, et al. Rectal cancer, version 2.2018, NCCN clinical practice guidelines in oncology. J Natl Compr Cancer Netw. 2018;16:874–901. Benson AB, Venook AP, Al-Hawary MM, et al. Rectal cancer, version 2.2018, NCCN clinical practice guidelines in oncology. J Natl Compr Cancer Netw. 2018;16:874–901.
8.
go back to reference Ogura A, Konishi T, Cunningham C, 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;37:33–43.PubMed Ogura A, Konishi T, Cunningham C, 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;37:33–43.PubMed
9.
go back to reference Akiyoshi T, Ueno M, Matsueda K, et al. Selective lateral pelvic lymph node dissection in patients with advanced low rectal cancer treated with preoperative chemoradiotherapy based on pretreatment imaging. Ann Surg Oncol. 2014;21:189–96.PubMed Akiyoshi T, Ueno M, Matsueda K, et al. Selective lateral pelvic lymph node dissection in patients with advanced low rectal cancer treated with preoperative chemoradiotherapy based on pretreatment imaging. Ann Surg Oncol. 2014;21:189–96.PubMed
10.
go back to reference Akiyoshi T, Toda S, Tominaga T, et al. Prognostic impact of residual lateral lymph node metastasis after neoadjuvant (chemo)radiotherapy in patients with advanced low rectal cancer. BJS Open. 2019;3:822–9.PubMedPubMedCentral Akiyoshi T, Toda S, Tominaga T, et al. Prognostic impact of residual lateral lymph node metastasis after neoadjuvant (chemo)radiotherapy in patients with advanced low rectal cancer. BJS Open. 2019;3:822–9.PubMedPubMedCentral
11.
go back to reference Kim HJ, Choi GS, Park JS, et al. Optimal treatment strategies for clinically suspicious lateral pelvic lymph node metastasis in rectal cancer. Oncotarget. 2017;8:100724–33.PubMedPubMedCentral Kim HJ, Choi GS, Park JS, et al. Optimal treatment strategies for clinically suspicious lateral pelvic lymph node metastasis in rectal cancer. Oncotarget. 2017;8:100724–33.PubMedPubMedCentral
12.
go back to reference Ishihara S, Kawai K, Tanaka T, et al. Oncological outcomes of lateral pelvic lymph node metastasis in rectal cancer treated with preoperative chemoradiotherapy. Dis Colon Rectum. 2017;60:469–76.PubMed Ishihara S, Kawai K, Tanaka T, et al. Oncological outcomes of lateral pelvic lymph node metastasis in rectal cancer treated with preoperative chemoradiotherapy. Dis Colon Rectum. 2017;60:469–76.PubMed
13.
go back to reference Malakorn S, Yang Y, Bednarski BK, et al. Who should get lateral pelvic lymph node dissection after neoadjuvant chemoradiation? Dis Colon Rectum. 2019;62:1158–66.PubMed Malakorn S, Yang Y, Bednarski BK, et al. Who should get lateral pelvic lymph node dissection after neoadjuvant chemoradiation? Dis Colon Rectum. 2019;62:1158–66.PubMed
14.
go back to reference Aerts HJ, Velazquez ER, Leijenaar RT, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun. 2014;5:4006.PubMed Aerts HJ, Velazquez ER, Leijenaar RT, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun. 2014;5:4006.PubMed
15.
go back to reference Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures, they are data. Radiology. 2016;278:563–77.PubMed Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures, they are data. Radiology. 2016;278:563–77.PubMed
16.
go back to reference Huang YQ, Liang CH, He L, et al. Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol. 2016;34:2157–64.PubMed Huang YQ, Liang CH, He L, et al. Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol. 2016;34:2157–64.PubMed
17.
go back to reference Liu Z, Zhang XY, Shi YJ, et al. Radiomics analysis for evaluation of pathological complete response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Clin Cancer Res. 2017;23:7253–62.PubMed Liu Z, Zhang XY, Shi YJ, et al. Radiomics analysis for evaluation of pathological complete response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Clin Cancer Res. 2017;23:7253–62.PubMed
18.
go back to reference Horvat N, Veeraraghavan H, Khan M, et al. MR imaging of rectal cancer: radiomics analysis to assess treatment response after neoadjuvant therapy. Radiology. 2018;287:833–43.PubMed Horvat N, Veeraraghavan H, Khan M, et al. MR imaging of rectal cancer: radiomics analysis to assess treatment response after neoadjuvant therapy. Radiology. 2018;287:833–43.PubMed
19.
go back to reference Akiyoshi T, Matsueda K, Hiratsuka M, et al. Indications for lateral pelvic lymph node dissection based on magnetic resonance imaging before and after preoperative chemoradiotherapy in patients with advanced low-rectal cancer. Ann Surg Oncol. 2015;22 Suppl 3:S614–20.PubMed Akiyoshi T, Matsueda K, Hiratsuka M, et al. Indications for lateral pelvic lymph node dissection based on magnetic resonance imaging before and after preoperative chemoradiotherapy in patients with advanced low-rectal cancer. Ann Surg Oncol. 2015;22 Suppl 3:S614–20.PubMed
20.
go back to reference Fedorov A, Beichel R, Kalpathy-Cramer J, et al. 3D Slicer as an image computing platform for the quantitative imaging network. Magn Reson Imaging. 2012;30:1323–41.PubMedPubMedCentral Fedorov A, Beichel R, Kalpathy-Cramer J, et al. 3D Slicer as an image computing platform for the quantitative imaging network. Magn Reson Imaging. 2012;30:1323–41.PubMedPubMedCentral
21.
go back to reference Griethuysen JJM, Fedorov A, Parmar C, et al. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77:e104–7.PubMedPubMedCentral Griethuysen JJM, Fedorov A, Parmar C, et al. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77:e104–7.PubMedPubMedCentral
22.
go back to reference Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15:155–63.PubMedPubMedCentral Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15:155–63.PubMedPubMedCentral
23.
go back to reference Tibshirani R. The lasso method for variable selection in the Cox model. Stat Med. 1997;16:385–95.PubMed Tibshirani R. The lasso method for variable selection in the Cox model. Stat Med. 1997;16:385–95.PubMed
24.
go back to reference Vickers AJ, Elkin EB. Decision curve analysis: a novel method for evaluating prediction models. Med Decis Mak. 2006;26:565–74. Vickers AJ, Elkin EB. Decision curve analysis: a novel method for evaluating prediction models. Med Decis Mak. 2006;26:565–74.
25.
go back to reference Ogura A, Konishi T, Beets GL, et al. Lateral nodal features on restaging magnetic resonance imaging associated with lateral local recurrence in low rectal cancer after neoadjuvant chemoradiotherapy or radiotherapy. JAMA Surg. 2019;154(9):e192172.PubMedPubMedCentral Ogura A, Konishi T, Beets GL, et al. Lateral nodal features on restaging magnetic resonance imaging associated with lateral local recurrence in low rectal cancer after neoadjuvant chemoradiotherapy or radiotherapy. JAMA Surg. 2019;154(9):e192172.PubMedPubMedCentral
26.
go back to reference Kim TG, Park W, Choi DH, et al. Factors associated with lateral pelvic recurrence after curative resection following neoadjuvant chemoradiotherapy in rectal cancer patients. Int J Colorectal Dis. 2014;29:193–200.PubMed Kim TG, Park W, Choi DH, et al. Factors associated with lateral pelvic recurrence after curative resection following neoadjuvant chemoradiotherapy in rectal cancer patients. Int J Colorectal Dis. 2014;29:193–200.PubMed
27.
go back to reference Brown G, Richards CJ, Bourne MW, et al. Morphologic predictors of lymph node status in rectal cancer with use of high-spatial-resolution MR imaging with histopathologic comparison. Radiology. 2003;227:371–7.PubMed Brown G, Richards CJ, Bourne MW, et al. Morphologic predictors of lymph node status in rectal cancer with use of high-spatial-resolution MR imaging with histopathologic comparison. Radiology. 2003;227:371–7.PubMed
28.
go back to reference Cong M, Feng H, Ren JL, et al. Development of a predictive radiomics model for lymph node metastases in pre-surgical CT-based stage IA non-small cell lung cancer. Lung Cancer. 2020;139:73–9.PubMed Cong M, Feng H, Ren JL, et al. Development of a predictive radiomics model for lymph node metastases in pre-surgical CT-based stage IA non-small cell lung cancer. Lung Cancer. 2020;139:73–9.PubMed
29.
go back to reference Ji GW, Zhang YD, Zhang H, et al. Biliary tract cancer at CT: a radiomics-based model to predict lymph node metastasis and survival outcomes. Radiology. 2019;290:90–8.PubMed Ji GW, Zhang YD, Zhang H, et al. Biliary tract cancer at CT: a radiomics-based model to predict lymph node metastasis and survival outcomes. Radiology. 2019;290:90–8.PubMed
30.
go back to reference Tan X, Ma Z, Yan L, Ye W, Liu Z, Liang C. Radiomics nomogram outperforms size criteria in discriminating lymph node metastasis in resectable esophageal squamous cell carcinoma. Eur Radiol. 2019;29:392–400.PubMed Tan X, Ma Z, Yan L, Ye W, Liu Z, Liang C. Radiomics nomogram outperforms size criteria in discriminating lymph node metastasis in resectable esophageal squamous cell carcinoma. Eur Radiol. 2019;29:392–400.PubMed
31.
go back to reference Zhu H, Zhang X, Li X, Shi Y, Zhu H, Sun Y. Prediction of pathological nodal stage of locally advanced rectal cancer by collective features of multiple lymph nodes in magnetic resonance images before and after neoadjuvant chemoradiotherapy. Chin J Cancer Res. 2019;31:984–92.PubMedPubMedCentral Zhu H, Zhang X, Li X, Shi Y, Zhu H, Sun Y. Prediction of pathological nodal stage of locally advanced rectal cancer by collective features of multiple lymph nodes in magnetic resonance images before and after neoadjuvant chemoradiotherapy. Chin J Cancer Res. 2019;31:984–92.PubMedPubMedCentral
32.
go back to reference Cercek A, Roxburgh CSD, Strombom P, et al. Adoption of total neoadjuvant therapy for locally advanced rectal cancer. JAMA Oncol. 2018;4:e180071.PubMedPubMedCentral Cercek A, Roxburgh CSD, Strombom P, et al. Adoption of total neoadjuvant therapy for locally advanced rectal cancer. JAMA Oncol. 2018;4:e180071.PubMedPubMedCentral
33.
go back to reference Konishi T, Shinozaki E, Murofushi K, et al. Phase II trial of neoadjuvant chemotherapy, chemoradiotherapy, and laparoscopic surgery with selective lateral node dissection for poor-risk low rectal cancer. Ann Surg Oncol. 2019;26:2507–13.PubMed Konishi T, Shinozaki E, Murofushi K, et al. Phase II trial of neoadjuvant chemotherapy, chemoradiotherapy, and laparoscopic surgery with selective lateral node dissection for poor-risk low rectal cancer. Ann Surg Oncol. 2019;26:2507–13.PubMed
34.
go back to reference Maas M, Nelemans PJ, Valentini V, et al. Long-term outcome in patients with a pathological complete response after chemoradiation for rectal cancer: a pooled analysis of individual patient data. Lancet Oncol. 2010;11:835–44.PubMed Maas M, Nelemans PJ, Valentini V, et al. Long-term outcome in patients with a pathological complete response after chemoradiation for rectal cancer: a pooled analysis of individual patient data. Lancet Oncol. 2010;11:835–44.PubMed
35.
go back to reference van Timmeren JE, Leijenaar RTH, van Elmpt W, et al. Test-retest data for radiomics feature stability analysis: generalizable or study-specific? Tomography. 2016;2:361–5.PubMedPubMedCentral van Timmeren JE, Leijenaar RTH, van Elmpt W, et al. Test-retest data for radiomics feature stability analysis: generalizable or study-specific? Tomography. 2016;2:361–5.PubMedPubMedCentral
36.
go back to reference Varghese BA, Hwang D, Cen SY, et al. Reliability of CT-based texture features: phantom study. J Appl Clin Med Phys. 2019;20:155–63.PubMedPubMedCentral Varghese BA, Hwang D, Cen SY, et al. Reliability of CT-based texture features: phantom study. J Appl Clin Med Phys. 2019;20:155–63.PubMedPubMedCentral
37.
go back to reference Bagher-Ebadian H, Siddiqui F, Liu C, Movsas B, Chetty IJ. On the impact of smoothing and noise on robustness of CT and CBCT radiomics features for patients with head and neck cancers. Med Phys. 2017;44:1755–70.PubMed Bagher-Ebadian H, Siddiqui F, Liu C, Movsas B, Chetty IJ. On the impact of smoothing and noise on robustness of CT and CBCT radiomics features for patients with head and neck cancers. Med Phys. 2017;44:1755–70.PubMed
38.
go back to reference Yang F, Dogan N, Stoyanova R, Ford JC. Evaluation of radiomic texture feature error due to MRI acquisition and reconstruction: a simulation study utilizing ground truth. Phys Med. 2018;50:26–36.PubMed Yang F, Dogan N, Stoyanova R, Ford JC. Evaluation of radiomic texture feature error due to MRI acquisition and reconstruction: a simulation study utilizing ground truth. Phys Med. 2018;50:26–36.PubMed
39.
go back to reference Fiset S, Welch ML, Weiss J, et al. Repeatability and reproducibility of MRI-based radiomic features in cervical cancer. Radiother Oncol. 2019;135:107–14.PubMed Fiset S, Welch ML, Weiss J, et al. Repeatability and reproducibility of MRI-based radiomic features in cervical cancer. Radiother Oncol. 2019;135:107–14.PubMed
Metadata
Title
Radiomics Approach Outperforms Diameter Criteria for Predicting Pathological Lateral Lymph Node Metastasis After Neoadjuvant (Chemo)Radiotherapy in Advanced Low Rectal Cancer
Authors
Ryota Nakanishi, MD, PhD
Takashi Akiyoshi, MD, PhD
Shigeo Toda, MD
Yu Murakami, MSc
Senzo Taguchi, MD, PhD
Koji Oba, PhD
Yutaka Hanaoka, MD
Toshiya Nagasaki, MD, PhD
Tomohiro Yamaguchi, MD, PhD
Tsuyoshi Konishi, MD, PhD
Shuichiro Matoba, MD, PhD
Masashi Ueno, MD, PhD
Yosuke Fukunaga, MD, PhD
Hiroya Kuroyanagi, MD, PhD
Publication date
01-10-2020
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 11/2020
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-020-08974-w

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