Skip to main content
Log in

Multiparametric MRI-based Radiomics approaches on predicting response to neoadjuvant chemoradiotherapy (nCRT) in patients with rectal cancer

  • Hollow Organ GI
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

Purpose

To investigate the value of multiparametric MRI-based radiomics on predicting response to nCRT in patients with rectal cancer.

Methods

This study enrolled 193 patients with pathologically confirmed LARC who received nCRT treatment between Apr. 2014 and Jun. 2018. All patients underwent baseline T1-weighted (T1W), T2-weighted (T2W) and T2-weighted fat-suppression (T2FS) MRI scans before neoadjuvant chemoradiotherapy. Radiomics features were extracted and selected from the MRI data to establish the radiomics signature. Important clinical predictors were identified by Mann–Whitney U test and Chi-square test. The nomogram integrating the radiomics signature and important clinical predictors was constructed using multivariate logistic regression. Prediction capabilities of each model were assessed with receiver operating characteristic (ROC) curve analysis. Performance of the nomogram was evaluated by its calibration and potential clinical usefulness.

Results

For the prediction of good response (GR) and pathologic complete response (pCR), the developed radiomics signature comprising 10 and 7 features, respectively, were significantly associated with the therapeutic response to nCRT. The nomogram incorporating the radiomics signature and important clinical predictors (CEA and CA19-9 for predicting GR; CEA, posttreatment length and posttreatment thickness for predicting pCR) achieved favorable prediction efficacy, with AUCs of 0.918 (95% confidence interval [CI]: 0.867–0.971, Sen = 0.972, Spe = 0.828) and 0.944 (95% CI: 0.891–0.997, Sen = 0.943, Spe = 0.828) in the training and validation cohort for predicting GR, respectively; with AUCs of 0.959 (95% CI: 0.927–0.991, Sen = 1.000, Spe = 0.833) and 0.912 (95% CI: 0.843–0.982, Sen = 1.000, Spe = 0.815) in the training and validation cohort for predicting pCR, respectively. Decision curve analysis confirmed potential clinical usefulness of our nomogram.

Conclusions

This study demonstrated that the MRI-based radiomics nomogram is predictive of response to nCRT and can be considered as a promising tool for facilitating treatment decision-making for patients with LARC.

Graphic abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The data and material that support the findings of this study are available from the corresponding author upon reasonable request.

Code availability

The code that supports the findings of this study is available from the corresponding author upon reasonable request.

References

  1. Ryan JE, Warrier SK, Lynch AC, Ramsay RG, Phillips WA, Heriot AG (2016) Predicting pathological complete response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer: a systematic review. Colorectal Dis 18(3):234-246. https://doi.org/10.1111/codi.13207

    Article  CAS  PubMed  Google Scholar 

  2. Maas M, Nelemans PJ, Valentini V, Das P, Rodel C, Kuo LJ et al (2010) Long-term outcome in patients with a pathological complete response after chemoradiation for rectal cancer: a pooled analysis of individual patient data. Lancet Oncol 11(9):835-844. https://doi.org/10.1016/S1470-2045(10)70172-8

    Article  PubMed  Google Scholar 

  3. Maas M, Beets-Tan RG, Lambregts DM, Lammering G, Nelemans PJ, Engelen SM et al (2011) Wait-and-see policy for clinical complete responders after chemoradiation for rectal cancer. J Clin Oncol 29(35):4633-4640. https://doi.org/10.1200/JCO.2011.37.7176

    Article  PubMed  Google Scholar 

  4. Park IJ, You YN, Agarwal A, Skibber JM, Rodriguez-Bigas MA, Eng C et al (2012) Neoadjuvant treatment response as an early response indicator for patients with rectal cancer. J Clin Oncol 30(15):1770-1776. https://doi.org/10.1200/JCO.2011.39.7901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Lambregts D, Maas M, Boellaard TN, Delli PA, van der Sande ME, Hupkens B et al (2020) Long-term imaging characteristics of clinical complete responders during watch-and-wait for rectal cancer-an evaluation of over 1500 MRIs. Eur Radiol 30(1):272-280. https://doi.org/10.1007/s00330-019-06396-1

    Article  PubMed  Google Scholar 

  6. Fusco R, Petrillo M, Granata V, Filice S, Sansone M, Catalano O et al (2017) Magnetic Resonance Imaging Evaluation in Neoadjuvant Therapy of Locally Advanced Rectal Cancer: A Systematic Review. Radiol Oncol 51(3):252-262. https://doi.org/10.1515/raon-2017-0032

    Article  PubMed  PubMed Central  Google Scholar 

  7. Sclafani F, Brown G, Cunningham D, Wotherspoon A, Mendes L, Balyasnikova S et al (2017) Comparison between MRI and pathology in the assessment of tumour regression grade in rectal cancer. Br J Cancer 117(10):1478-1485. https://doi.org/10.1038/bjc.2017.320

    Article  PubMed  PubMed Central  Google Scholar 

  8. Park H, Kim KA, Jung JH, Rhie J, Choi SY (2020) MRI features and texture analysis for the early prediction of therapeutic response to neoadjuvant chemoradiotherapy and tumor recurrence of locally advanced rectal cancer. Eur Radiol 30(8):4201-4211. https://doi.org/10.1007/s00330-020-06835-4

    Article  PubMed  Google Scholar 

  9. Cui Y, Yang X, Shi Z, Yang Z, Du X, Zhao Z et al (2019) Radiomics analysis of multiparametric MRI for prediction of pathological complete response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Eur Radiol 29(3):1211-1220. https://doi.org/10.1007/s00330-018-5683-9

    Article  PubMed  Google Scholar 

  10. Ludmir EB, Palta M, Willett CG, Czito BG (2017) Total neoadjuvant therapy for rectal cancer: An emerging option. Cancer-Am Cancer Soc 123(9):1497-1506. https://doi.org/10.1002/cncr.30600

    Article  Google Scholar 

  11. Lambin P, Leijenaar R, Deist TM, Peerlings J, de Jong E, van Timmeren J et al (2017) Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol 14(12):749-762. https://doi.org/10.1038/nrclinonc.2017.141

    Article  PubMed  Google Scholar 

  12. Liu Z, Wang S, Dong D, Wei J, Fang C, Zhou X et al (2019) The Applications of Radiomics in Precision Diagnosis and Treatment of Oncology: Opportunities and Challenges. Theranostics 9(5):1303-1322. https://doi.org/10.7150/thno.30309

    Article  PubMed  PubMed Central  Google Scholar 

  13. P. A, A. M, K. NP, A. O, H. B (2019) From Handcrafted to Deep-Learning-Based Cancer Radiomics: Challenges and Opportunities. Ieee Signal Proc Mag 36(4):132-160. https://doi.org/10.1109/MSP.2019.2900993

    Article  Google Scholar 

  14. Huynh E, Hosny A, Guthier C, Bitterman DS, Petit SF, Haas-Kogan DA et al (2020) Artificial intelligence in radiation oncology. Nat Rev Clin Oncol 17(12):771-781. https://doi.org/10.1038/s41571-020-0417-8

    Article  PubMed  Google Scholar 

  15. Wei J, Yang G, Hao X, Gu D, Tan Y, Wang X et al (2019) A multi-sequence and habitat-based MRI radiomics signature for preoperative prediction of MGMT promoter methylation in astrocytomas with prognostic implication. Eur Radiol 29(2):877-888. https://doi.org/10.1007/s00330-018-5575-z

    Article  PubMed  Google Scholar 

  16. Nie K, Shi L, Chen Q, Hu X, Jabbour SK, Yue N et al (2016) Rectal Cancer: Assessment of Neoadjuvant Chemoradiation Outcome based on Radiomics of Multiparametric MRI. Clin Cancer Res 22(21):5256-5264. https://doi.org/10.1158/1078-0432.CCR-15-2997

    Article  PubMed  Google Scholar 

  17. De Cecco CN, Ganeshan B, Ciolina M, Rengo M, Meinel FG, Musio D et al (2015) Texture analysis as imaging biomarker of tumoral response to neoadjuvant chemoradiotherapy in rectal cancer patients studied with 3-T magnetic resonance. Invest Radiol 50(4):239-245. https://doi.org/10.1097/RLI.0000000000000116

    Article  CAS  PubMed  Google Scholar 

  18. Liu Z, Zhang XY, Shi YJ, Wang L, Zhu HT, Tang Z et al (2017) Radiomics Analysis for Evaluation of Pathological Complete Response to Neoadjuvant Chemoradiotherapy in Locally Advanced Rectal Cancer. Clin Cancer Res 23(23):7253-7262. https://doi.org/10.1158/1078-0432.CCR-17-1038

    Article  CAS  PubMed  Google Scholar 

  19. Mandard AM, Dalibard F, Mandard JC, Marnay J, Henry-Amar M, Petiot JF et al (1994) Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma. Clinicopathologic correlations. Cancer-Am Cancer Soc 73(11):2680-2686. https://doi.org/10.1002/1097-0142(19940601)73:11<2680::aid-cncr2820731105>3.0.co;2-c

    Article  CAS  Google Scholar 

  20. van Griethuysen J, Fedorov A, Parmar C, Hosny A, Aucoin N, Narayan V et al (2017) Computational Radiomics System to Decode the Radiographic Phenotype. Cancer Res 77(21):e104-e107. https://doi.org/10.1158/0008-5472.CAN-17-0339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Leijenaar RT, Carvalho S, Velazquez ER, van Elmpt WJ, Parmar C, Hoekstra OS et al (2013) Stability of FDG-PET Radiomics features: an integrated analysis of test-retest and inter-observer variability. Acta Oncol 52(7):1391-1397. https://doi.org/10.3109/0284186X.2013.812798

    Article  CAS  PubMed  Google Scholar 

  22. Sauerbrei W, Royston P, Binder H (2007) Selection of important variables and determination of functional form for continuous predictors in multivariable model building. Stat Med 26(30):5512-5528. https://doi.org/10.1002/sim.3148

    Article  PubMed  Google Scholar 

  23. Tibshirani R (1997) The lasso method for variable selection in the Cox model. Stat Med 16(4):385-395. https://doi.org/10.1002/(sici)1097-0258(19970228)16:4<385::aid-sim380>3.0.co;2-3

    Article  CAS  PubMed  Google Scholar 

  24. Robert T (2011) Regression shrinkage and selection via the lasso: a retrospective. Journal of the Royal Statistical Society. Series B (Statistical Methodology) 73(3):267–288. https://doi.org/10.1111/j.1467-9868.2011.00771.x

  25. Andrew JV (2006) Decision Curve Analysis: A Novel Method for Evaluating Prediction Models. Med Decis Making 26(6):565-74. https://doi.org/10.1177/0272989X06295361

    Article  Google Scholar 

  26. Li Z, Wang X, Li M, Liu X, Ye Z, Song B et al (2020) Multi-modal radiomics model to predict treatment response to neoadjuvant chemotherapy for locally advanced rectal cancer. World J Gastroentero 26(19):2388-402. https://doi.org/10.3748/wjg.v26.i19.2388

    Article  Google Scholar 

  27. Chun Y, Ze-Kun J, Li-Heng L, Meng-Su Z (2020) Pre-treatment ADC image-based random forest classifier for identifying resistant rectal adenocarcinoma to neoadjuvant chemoradiotherapy. Int J Colorectal 35(1):101-7. https://doi.org/10.1007/s00384-019-03455-3

    Article  Google Scholar 

  28. Wang J, Liu X, Hu B, Gao Y, Chen J, Li J (2020) Development and validation of an MRI-based radiomic nomogram to distinguish between good and poor responders in patients with locally advanced rectal cancer undergoing neoadjuvant chemoradiotherapy. Abdom Radiol (NY). https://doi.org/10.1007/s00261-020-02846-3

    Article  Google Scholar 

  29. Giannini V, Mazzetti S, Bertotto I, Chiarenza C, Cauda S, Delmastro E et al (2019) Predicting locally advanced rectal cancer response to neoadjuvant therapy with (18)F-FDG PET and MRI radiomics features. Eur J Nucl Med Mol Imaging 46(4):878-888. https://doi.org/10.1007/s00259-018-4250-6

    Article  CAS  PubMed  Google Scholar 

  30. Delli Pizzi A, Chiarelli AM, Chiacchiaretta P, Croce P, Rosa C et al (2021). MRI-based clinical-radiomics model predicts tumor response before treatment in locally advanced rectal cancer. Sci Rep 11(1): 5379. https://doi.org/10.1038/s41598-021-84816-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Shu Z, Fang S, Ye Q, Mao D, Cao H, Pang P et al (2019) Prediction of efficacy of neoadjuvant chemoradiotherapy for rectal cancer: the value of texture analysis of magnetic resonance images. Abdom Radiol (NY) 44(11):3775-3784. https://doi.org/10.1007/s00261-019-01971-y

    Article  PubMed  Google Scholar 

  32. Horvat N, Veeraraghavan H, Khan M, Blazic I, Zheng J, Capanu M et al (2018). MR Imaging of Rectal Cancer: Radiomics Analysis to Assess Treatment Response after Neoadjuvant Therapy. Radiology 287(3): 833–843. https://doi.org/10.1148/radiol.2018172300

    Article  PubMed  Google Scholar 

  33. Chen H, Shi L, Nguyen K, Monjazeb AM, Matsukuma KE, Loehfelm TW et al (2020). MRI Radiomics for Prediction of Tumor Response and Downstaging in Rectal Cancer Patients after Preoperative Chemoradiation. Adv Radiat Oncol, 5(6):1286–1295. https://doi.org/10.1016/j.adro.2020.04.016

    Article  PubMed  PubMed Central  Google Scholar 

  34. Tixier F, Le Rest CC, Hatt M, Albarghach N, Pradier O, Metges JP et al (2011). Intratumor heterogeneity characterized by textural features on baseline 18F-FDG PET images predicts response to concomitant radiochemotherapy in esophageal cancer. J Nucl Med 52(3):369–378. https://doi.org/10.2967/jnumed.110.082404

    Article  PubMed  Google Scholar 

  35. Li Z, Ma X, Shen F, Lu H, Xia Y, Lu J (2021) Evaluating treatment response to neoadjuvant chemoradiotherapy in rectal cancer using various MRI-based radiomics models. Bmc Med Imaging 21(1):30. https://doi.org/10.1186/s12880-021-00560-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Moureau-Zabotto L, Farnault B, de Chaisemartin C, Esterni B, Lelong B, Viret F et al (2011) Predictive factors of tumor response after neoadjuvant chemoradiation for locally advanced rectal cancer. International journal of radiation oncology, biology, physics 80(2):483-91. https://doi.org/10.1016/j.ijrobp.2010.02.025

    Article  PubMed  Google Scholar 

  37. Song J, Huang X, Chen Z, Chen M, Lin Q, Li A et al (2018) Predictive value of carcinoembryonic antigen and carbohydrate antigen 19-9 related to downstaging to stage 0-I after neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Cancer Manag Res 10:3101-3108. https://doi.org/10.2147/CMAR.S166417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tranchart H, Lefevre JH, Svrcek M, Flejou JF, Tiret E, Parc Y (2013) What is the incidence of metastatic lymph node involvement after significant pathologic response of primary tumor following neoadjuvant treatment for locally advanced rectal cancer? Ann Surg Oncol 20(5):1551-1559. https://doi.org/10.1245/s10434-012-2773-9

    Article  PubMed  Google Scholar 

Download references

Funding

The study was funded by Climbing Fund of National Cancer Center (NCC201806B011), Shenyang Municipal Science and Technology Project (F16-206–9-23), National Natural Science Foundation of China (81872363), Major Technology Plan Project of Shenyang (17–230-9–07), Supporting Fund for Big data in Health Care (HMB201903101), Special foundation for the central government guides the development of local science and technology of Liaoning Province (2018416029), Education Department Foundation of Liaoning (LQNK201744), Key Program of Ministry of Science and Technology of China [2017YFC1309100], China National Natural Science Foundation (31770147) and Medical-Engineering Joint Fund for Cancer Hospital of China Medical University and Dalian University of technology (LD202029).

Author information

Authors and Affiliations

Authors

Contributions

XJ, YL and YC: study design. ZZ and YC: data collection. YC, YH, XW, QY, GL and EC: data analysis and interpretation. XJ and YC: manuscript writing. TY and YL: funding acquisition. All authors contributed to the article and approved the submitted version.

Corresponding author

Correspondence to Xiran Jiang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest. Yuan Cheng, Yahong Luo and Yue Hu have made equal intellectual contributions to the manuscript.

Ethical approval

The studies involving human participants were reviewed and approved by the Cancer Hospital of China Medical University review board approved this retrospective study. Written informed consent for participation was not required for this study in accordance with the national legislation and the institutional requirements.

Consent to participate

The ethics committee of our hospital approved our retrospective study (No.2018010), and waived the requirement of informed consent.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 441 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, Y., Luo, Y., Hu, Y. et al. Multiparametric MRI-based Radiomics approaches on predicting response to neoadjuvant chemoradiotherapy (nCRT) in patients with rectal cancer. Abdom Radiol 46, 5072–5085 (2021). https://doi.org/10.1007/s00261-021-03219-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00261-021-03219-0

Keywords

Navigation