Complete Response Evaluation of Locally Advanced Rectal Cancer to Neoadjuvant Chemoradiotherapy Using Textural Features Obtained from T2 Weighted Imaging and ADC Maps

Article ID: e030322201646 Pages: 9

  • * (Excluding Mailing and Handling)

Abstract

Background: The prediction of pathological responses for locally advanced rectal cancer using magnetic resonance imaging (MRI) after neoadjuvant chemoradiotherapy (CRT) is a challenging task for radiologists, as residual tumor cells can be mistaken for fibrosis. Texture analysis of MR images has been proposed to understand the underlying pathology.

Objective: This study aimed to assess the responses of lesions to CRT in patients with locally advanced rectal cancer using the first-order textural features of MRI T2-weighted imaging (T2-WI) and apparent diffusion coefficient (ADC) maps.

Methods: Forty-four patients with locally advanced rectal cancer (median age: 57 years) who underwent MRI before and after CRT were enrolled in this retrospective study. The first-order textural parameters of tumors on T2-WI and ADC maps were extracted. The textural features of lesions in pathologic complete responders were compared to partial responders using Student’s t- or Mann–Whitney U tests. A comparison of textural features before and after CRT for each group was performed using the Wilcoxon rank sum test. Receiver operating characteristic curves were calculated to detect the diagnostic performance of the ADC.

Results: Of the 44 patients evaluated, 22 (50%) were placed in a partial response group and 50% were placed in a complete response group. The ADC changes of the complete responders were statistically more significant than those of the partial responders (P = 0.002). Pathologic total response was predicted with an ADC cut-off of 1310 x 10-6 mm2/s, with a sensitivity of 72%, a specificity of 77%, and an accuracy of 78.1% after neoadjuvant CRT. The skewness of the T2-WI before and after neoadjuvant CRT showed a significant difference in the complete response group compared to the partial response group (P = 0.001 for complete responders vs. P = 0.482 for partial responders). Also, relative T2-WI signal intensity in the complete response group was statistically lower than that of the partial response group after neoadjuvant CRT (P = 0.006).

Conclusion: As a result of the conversion of tumor cells to fibrosis, the skewness of the T2-WI before and after neoadjuvant CRT was statistically different in the complete response group compared to the partial response group, and the complete response group showed statistically lower relative T2-WI signal intensity than the partial response group after neoadjuvant CRT. Additionally, the ADC cut-off value of 1310 × 10-6 mm2/s could be used as a marker for a complete response along with absolute ADC value changes within this dataset.

Keywords: Rectum MRI, computer aided-detection, tissue characterization, textural features, locally advanced rectal cancer, apparent diffusion coefficient (ADC).

[1]
Ferlay J, Colombet M, Soerjomataram I, et al. Cancer statistics for the year 2020: An overview. Int J Cancer 2021; 149(4): 778-89.
[http://dx.doi.org/10.1002/ijc.33588] [PMID: 33818764]
[2]
Viale PH. The American cancer society’s facts & figures: 2020 Edition. J Adv Pract Oncol 2020; 11(2): 135-6.
[PMID: 33532112]
[3]
Nagtegaal I, Gaspar C, Marijnen C, Van De Velde C, Fodde R, Van Krieken H. Morphological changes in tumour type after radiotherapy are accompanied by changes in gene expression profile but not in clinical behaviour. J Pathol 2004; 204(2): 183-92.
[http://dx.doi.org/10.1002/path.1621] [PMID: 15378567]
[4]
Sauer R, Becker H, Hohenberger W, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med 2004; 351(17): 1731-40.
[http://dx.doi.org/10.1056/NEJMoa040694] [PMID: 15496622]
[5]
Glimelius B, Tiret E, Cervantes A, Arnold D, Group EGW. Rectal cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2013; 24(Suppl. 6): vi81-8.
[http://dx.doi.org/10.1093/annonc/mdt240] [PMID: 24078665]
[6]
Habr-Gama A, Perez RO, Nadalin W, et al. Operative versus nonoperative treatment for stage 0 distal rectal cancer following chemoradiation therapy: Long-term results. Ann Surg 2004; 240(4): 711-7.
[http://dx.doi.org/10.1097/01.sla.0000141194.27992.32] [PMID: 15383798]
[7]
Habr-Gama A, Perez RO. Non-operative management of rectal cancer after neoadjuvant chemoradiation. Br J Surg 2009; 96(2): 125-7.
[http://dx.doi.org/10.1002/bjs.6470] [PMID: 19160360]
[8]
Maas M, Beets-Tan RG, Lambregts DM, et al. Wait-and-see policy for clinical complete responders after chemoradiation for rectal cancer. J Clin Oncol 2011; 29(35): 4633-40.
[http://dx.doi.org/10.1200/JCO.2011.37.7176] [PMID: 22067400]
[9]
Påhlman L, Bohe M, Cedermark B, et al. The Swedish rectal cancer registry. Br J Surg 2007; 94(10): 1285-92.
[http://dx.doi.org/10.1002/bjs.5679] [PMID: 17661309]
[10]
Monguzzi L, Ippolito D, Bernasconi DP, Trattenero C, Galimberti S, Sironi S. Locally advanced rectal cancer: Value of ADC mapping in prediction of tumor response to radiochemotherapy. Eur J Radiol 2013; 82(2): 234-40.
[http://dx.doi.org/10.1016/j.ejrad.2012.09.027] [PMID: 23122748]
[11]
Battersby NJ, Balyasnikova S, Brown G. Guiding post-treatment decisions in rectal cancer: mrTRG is a practical place to start. Oncology (Williston Park) 2014; 28(8): 677-80.
[PMID: 25140621]
[12]
O’Neill BD, Brown G, Heald RJ, Cunningham D, Tait DM. Non-operative treatment after neoadjuvant chemoradiotherapy for rectal cancer. Lancet Oncol 2007; 8(7): 625-33.
[http://dx.doi.org/10.1016/S1470-2045(07)70202-4] [PMID: 17613424]
[13]
Hartley A, Ho KF, McConkey C, Geh JI. Pathological complete response following pre-operative chemoradiotherapy in rectal cancer: Anal-ysis of phase II/III trials. Br J Radiol 2005; 78(934): 934-8.
[http://dx.doi.org/10.1259/bjr/86650067] [PMID: 16177017]
[14]
Maas M, Lambregts DM, Nelemans PJ, et al. Assessment of clinical complete response after chemoradiation for rectal cancer with digital rectal examination, endoscopy, and MRI: Selection for organ-saving treatment. Ann Surg Oncol 2015; 22(12): 3873-80.
[http://dx.doi.org/10.1245/s10434-015-4687-9] [PMID: 26198074]
[15]
Nougaret S, Reinhold C, Mikhael HW, Rouanet P, Bibeau F, Brown G. The use of MR imaging in treatment planning for patients with rectal carcinoma: Have you checked the “DISTANCE”? Radiology 2013; 268(2): 330-44.
[http://dx.doi.org/10.1148/radiol.13121361] [PMID: 23882096]
[16]
Curvo-Semedo L, Lambregts DM, Maas M, et al. Rectal cancer: assessment of complete response to preoperative combined radiation thera-py with chemotherapy-conventional MR volumetry versus diffusion-weighted MR imaging. Radiology 2011; 260(3): 734-43.
[http://dx.doi.org/10.1148/radiol.11102467] [PMID: 21673229]
[17]
Kim SH, Lee JM, Hong SH, et al. Locally advanced rectal cancer: added value of diffusion-weighted MR imaging in the evaluation of tumor response to neoadjuvant chemo- and radiation therapy. Radiology 2009; 253(1): 116-25.
[http://dx.doi.org/10.1148/radiol.2532090027] [PMID: 19789256]
[18]
Ha HI, Kim AY, Yu CS, Park SH, Ha HK. Locally advanced rectal cancer: Diffusion-weighted MR tumour volumetry and the apparent dif-fusion coefficient for evaluating complete remission after preoperative chemoradiation therapy. Eur Radiol 2013; 23(12): 3345-53.
[http://dx.doi.org/10.1007/s00330-013-2936-5] [PMID: 23812242]
[19]
Lambregts DM, Rao SX, Sassen S, et al. MRI and diffusion-weighted MRI volumetry for identification of complete tumor responders after preoperative chemoradiotherapy in patients with rectal cancer: A bi-institutional validation study. Ann Surg 2015; 262(6): 1034-9.
[http://dx.doi.org/10.1097/SLA.0000000000000909] [PMID: 25211270]
[20]
Dworak O, Keilholz L, Hoffmann A. Pathological features of rectal cancer after preoperative radiochemotherapy. Int J Colorectal Dis 1997; 12(1): 19-23.
[http://dx.doi.org/10.1007/s003840050072] [PMID: 9112145]
[21]
Siddiqui MR, Bhoday J, Battersby NJ, et al. Defining response to radiotherapy in rectal cancer using magnetic resonance imaging and histo-pathological scales. World J Gastroenterol 2016; 22(37): 8414-34.
[http://dx.doi.org/10.3748/wjg.v22.i37.8414] [PMID: 27729748]
[22]
Trakarnsanga A, Gönen M, Shia J, et al. Comparison of tumor regression grade systems for locally advanced rectal cancer after multimodal-ity treatment. J Natl Cancer Inst 2014; 106(10): dju248.
[http://dx.doi.org/10.1093/jnci/dju248] [PMID: 25249540]
[23]
Patel UB, Brown G, Rutten H, et al. Comparison of magnetic resonance imaging and histopathological response to chemoradiotherapy in locally advanced rectal cancer. Ann Surg Oncol 2012; 19(9): 2842-52.
[http://dx.doi.org/10.1245/s10434-012-2309-3] [PMID: 22526897]
[24]
Siddiqui MR, Gormly KL, Bhoday J, et al. Interobserver agreement of radiologists assessing the response of rectal cancers to preoperative chemoradiation using the MRI tumour regression grading (mrTRG). Clin Radiol 2016; 71(9): 854-62.
[http://dx.doi.org/10.1016/j.crad.2016.05.005] [PMID: 27381221]
[25]
Kim YH, Kim DY, Kim TH, et al. Usefulness of magnetic resonance volumetric evaluation in predicting response to preoperative concur-rent chemoradiotherapy in patients with resectable rectal cancer. Int J Radiat Oncol Biol Phys 2005; 62(3): 761-8.
[http://dx.doi.org/10.1016/j.ijrobp.2004.11.005] [PMID: 15936557]
[26]
De Cecco CN, Ganeshan B, Ciolina M, et al. Texture analysis as imaging biomarker of tumoral response to neoadjuvant chemoradiotherapy in rectal cancer patients studied with 3-T magnetic resonance. Invest Radiol 2015; 50(4): 239-45.
[http://dx.doi.org/10.1097/RLI.0000000000000116] [PMID: 25501017]
[27]
Liu Z, Wang S, Dong D, et al. The applications of radiomics in precision diagnosis and treatment of oncology: Opportunities and challeng-es. Theranostics 2019; 9(5): 1303-22.
[http://dx.doi.org/10.7150/thno.30309] [PMID: 30867832]
[28]
Choi MH, Oh SN, Rha SE, et al. Diffusion-weighted imaging: Apparent diffusion coefficient histogram analysis for detecting pathologic complete response to chemoradiotherapy in locally advanced rectal cancer. J Magn Reson Imaging 2016; 44(1): 212-20.
[http://dx.doi.org/10.1002/jmri.25117] [PMID: 26666560]
[29]
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(9): 1042-50.
[http://dx.doi.org/10.1177/0284185114550193] [PMID: 25270374]
[30]
Aker M, Ganeshan B, Afaq A, Wan S, Groves AM, Arulampalam T. Magnetic resonance texture analysis in identifying complete pathologi-cal response to neoadjuvant treatment in locally advanced rectal cancer. Dis Colon Rectum 2019; 62(2): 163-70.
[http://dx.doi.org/10.1097/DCR.0000000000001224] [PMID: 30451764]
[31]
Jalil O, Afaq A, Ganeshan B, et al. Magnetic resonance based texture parameters as potential imaging biomarkers for predicting long-term survival in locally advanced rectal cancer treated by chemoradiotherapy. Colorectal Dis 2017; 19(4): 349-62.
[http://dx.doi.org/10.1111/codi.13496] [PMID: 27538267]
[32]
De Cecco CN, Ciolina M, Caruso D, et al. Performance of diffusion-weighted imaging, perfusion imaging, and texture analysis in predicting tumoral response to neoadjuvant chemoradiotherapy in rectal cancer patients studied with 3T MR: Initial experience. Abdom Radiol (NY) 2016; 41(9): 1728-35.
[http://dx.doi.org/10.1007/s00261-016-0733-8] [PMID: 27056748]
[33]
Shu Z, Fang S, Ye Q, et al. Prediction of efficacy of neoadjuvant chemoradiotherapy for rectal cancer: The value of texture analysis of mag-netic resonance images. Abdom Radiol (NY) 2019; 44(11): 3775-84.
[http://dx.doi.org/10.1007/s00261-019-01971-y] [PMID: 30852633]
[34]
Kluza E, Rozeboom ED, Maas M, et al. T2 weighted signal intensity evolution may predict pathological complete response after treatment for rectal cancer. Eur Radiol 2013; 23(1): 253-61.
[http://dx.doi.org/10.1007/s00330-012-2578-z] [PMID: 22777621]
[35]
Crimì F, Capelli G, Spolverato G, et al. MRI T2-weighted sequences-based Texture Analysis (TA) as a predictor of response to neoadjuvant chemo-radiotherapy (nCRT) in patients with Locally Advanced Rectal Cancer (LARC). Radiol Med (Torino) 2020; 125(12): 1216-24.
[http://dx.doi.org/10.1007/s11547-020-01215-w] [PMID: 32410063]
[36]
Mueller MM, Fusenig NE. Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 2004; 4(11): 839-49.
[http://dx.doi.org/10.1038/nrc1477] [PMID: 15516957]
[37]
Eberhard A, Kahlert S, Goede V, Hemmerlein B, Plate KH, Augustin HG. Heterogeneity of angiogenesis and blood vessel maturation in human tumors: Implications for antiangiogenic tumor therapies. Cancer Res 2000; 60(5): 1388-93.
[PMID: 10728704]
[38]
Kim SH, Lee JY, Lee JM, Han JK, Choi BI. Apparent diffusion coefficient for evaluating tumour response to neoadjuvant chemoradiation therapy for locally advanced rectal cancer. Eur Radiol 2011; 21(5): 987-95.
[http://dx.doi.org/10.1007/s00330-010-1989-y] [PMID: 20978768]
[39]
Napoletano M, Mazzucca D, Prosperi E, et al. Locally advanced rectal cancer: Qualitative and quantitative evaluation of diffusion-weighted magnetic resonance imaging in restaging after neoadjuvant chemo-radiotherapy. Abdom Radiol (NY) 2019; 44(11): 3664-73.
[http://dx.doi.org/10.1007/s00261-019-02012-4] [PMID: 31004202]
[40]
Foti PV, Privitera G, Piana S, et al. Locally advanced rectal cancer: Qualitative and quantitative evaluation of diffusion-weighted MR imaging in the response assessment after neoadjuvant chemo-radiotherapy. Eur J Radiol Open 2016; 3: 145-52.
[http://dx.doi.org/10.1016/j.ejro.2016.06.003] [PMID: 27489868]
[41]
Amodeo S, Rosman AS, Desiato V, et al. MRI-based apparent diffusion coefficient for predicting pathologic response of rectal cancer after neoadjuvant therapy: Systematic review and meta-analysis. AJR Am J Roentgenol 2018; 211(5): W205-16.
[http://dx.doi.org/10.2214/AJR.17.19135] [PMID: 30240291]
[42]
Enkhbaatar NE, Inoue S, Yamamuro H, et al. MR imaging with apparent diffusion coefficient histogram analysis: Evaluation of locally advanced rectal cancer after chemotherapy and radiation therapy. Radiology 2018; 288(1): 129-37.
[http://dx.doi.org/10.1148/radiol.2018171804] [PMID: 29558294]
[43]
Kim NK, Baik SH, Min BS, et al. A comparative study of volumetric analysis, histopathologic downstaging, and tumor regression grade in evaluating tumor response in locally advanced rectal cancer following preoperative chemoradiation. Int J Radiat Oncol Biol Phys 2007; 67(1): 204-10.
[http://dx.doi.org/10.1016/j.ijrobp.2006.08.020] [PMID: 17084555]
[44]
Neri E, Guidi E, Pancrazi F, et al. MRI tumor volume reduction rate vs. tumor regression grade in the pre-operative re-staging of locally advanced rectal cancer after chemo-radiotherapy. Eur J Radiol 2015; 84(12): 2438-43.
[http://dx.doi.org/10.1016/j.ejrad.2015.08.008] [PMID: 26462793]
[45]
Blazic IM, Lilic GB, Gajic MM. Quantitative assessment of rectal cancer response to neoadjuvant combined chemotherapy and radiation therapy: Comparison of three methods of positioning region of interest for ADC measurements at diffusion-weighted MR imaging. Radiology 2017; 282(2): 615.
[http://dx.doi.org/10.1148/radiol.2017164040] [PMID: 28099105]