Abstract
Purpose
To compare morphological and functional MRI metrics and determine which ones perform best in assessing response to neoadjuvant chemoradiotherapy (CRT) in rectal cancer.
Materials and methods
This retrospective study included 24 uniformly-treated patients with biopsy-proven rectal adenocarcinoma who underwent MRI, including diffusion-weighted (DW) and dynamic contrast-enhanced (DCE) sequences, before and after completion of CRT. On all MRI exams, two experienced readers independently measured longest and perpendicular tumour diameters, tumour volume, tumour regression grade (TRG) and tumour signal intensity ratio on T2-weighted imaging, as well as tumour volume and apparent diffusion coefficient on DW-MRI and tumour volume and transfer constant Ktrans on DCE-MRI. These metrics were correlated with histopathological percent tumour regression in the resected specimen (%TR). Inter-reader agreement was assessed using the concordance correlation coefficient (CCC).
Results
For both readers, post-treatment DW-MRI and DCE-MRI volumetric tumour assessments were significantly associated with %TR; DCE-MRI volumetry showed better inter-reader agreement (CCC=0.700) than DW-MRI volumetry (CCC=0.292). For one reader, mrTRG, post-treatment T2 tumour volumetry and assessments of volume change made with T2, DW-MRI and DCE-MRI were also significantly associated with %TR.
Conclusion
Tumour volumetry on post-treatment DCE-MRI and DW-MRI correlated well with %TR, with DCE-MRI volumetry demonstrating better inter-reader agreement.
Key Points
• Volumetry on post-treatment DCE-/DW-MRI sequences correlated well with histopathological tumour regression.
• DCE-MRI volumetry demonstrated good inter-reader agreement.
• Inter-reader agreement was higher for DCE-MRI volumetry than for DW-MRI volumetry.
• DCE-MRI volumetry merits further investigation as a metric for evaluating treatment response.
Similar content being viewed by others
References
Habr-Gama A (2006) Assessment and management of the complete clinical response of rectal cancer to chemoradiotherapy. Colorectal Dis 8(Suppl 3):21–24
Beets-Tan RG, Beets GL (2011) Local staging of rectal cancer: a review of imaging. J Magn Reson Imaging 33(5):1012–1019
Barbaro B, Fiorucci C, Tebala C, Valentini V, Gambacorta MA, Vecchio FM et al (2009) Locally advanced rectal cancer: MR imaging in prediction of response after preoperative chemotherapy and radiation therapy. Radiology 250(3):730–739
Kuo LJ, Chern MC, Tsou MH, Liu MC, Jian JJ, Chen CM et al (2005) Interpretation of magnetic resonance imaging for locally advanced rectal carcinoma after preoperative chemoradiation therapy. Dis Colon Rectum 48(1):23–28
Patel UB, Taylor F, Blomqvist L, George C, Evans H, Tekkis P et al (2011) Magnetic resonance imaging-detected tumor response for locally advanced rectal cancer predicts survival outcomes: MERCURY experience. J Clin Oncol 29(28):3753–3760
Patel UB, Brown G, Rutten H, West N, Sebag-Montefiore D, Glynne-Jones R et al (2012) Comparison of magnetic resonance imaging and histopathological response to chemoradiotherapy in locally advanced rectal cancer. Ann Surg Oncol 19(9):2842–2852
Kluza E, Rozeboom ED, Maas M, Martens M, Lambregts DM, Slenter J et al (2013) T2 weighted signal intensity evolution may predict pathological complete response after treatment for rectal cancer. Eur Radiol 23(1):253–261
Barbaro B, Vitale R, Valentini V, Illuminati S, Vecchio FM, Rizzo G et al (2012) Diffusion-weighted magnetic resonance imaging in monitoring rectal cancer response to neoadjuvant chemoradiotherapy. Int J Radiat Oncol Biol Phys 83(2):594–599
Curvo-Semedo L, Lambregts DM, Maas M, Beets GL, Caseiro-Alves F, Beets-Tan RG (2012) Diffusion-weighted MRI in rectal cancer: apparent diffusion coefficient as a potential noninvasive marker of tumor aggressiveness. J Magn Reson Imaging 35(6):1365–1371
Elmi A, Hedgire SS, Covarrubias D, Abtahi SM, Hahn PF, Harisinghani M (2013) Apparent diffusion coefficient as a non-invasive predictor of treatment response and recurrence in locally advanced rectal cancer. Clin Radiol 68(10):e524–e531
Ha HI, Kim AY, Yu CS, Park SH, Ha HK (2013) Locally advanced rectal cancer: diffusion-weighted MR tumour volumetry and the apparent diffusion coefficient for evaluating complete remission after preoperative chemoradiation therapy. Eur Radiol 23(12):3345–3353
Jung SH, Heo SH, Kim JW, Jeong YY, Shin SS, Soung MG et al (2012) Predicting response to neoadjuvant chemoradiation therapy in locally advanced rectal cancer: diffusion-weighted 3 Tesla MR imaging. J Magn Reson Imaging 35(1):110–116
Kim SH, Lee JM, Hong SH, Kim GH, Lee JY, Han JK et al (2009) Locally advanced rectal cancer: added value of diffusion-weighted MR imaging in the evaluation of tumor response to neoadjuvant chemo- and radiation therapy. Radiology 253(1):116–125
Lambrecht M, Vandecaveye V, de Keyzer F, Roels S, Penninckx F, van Cutsem E et al (2012) Value of diffusion-weighted magnetic resonance imaging for prediction and early assessment of response to neoadjuvant radiochemotherapy in rectal cancer: preliminary results. Int J Radiat Oncol Biol Phys 82(2):863–870
Sun YS, Zhang XP, Tang L, Ji JF, Gu J, Cai Y et al (2010) Locally advanced rectal carcinoma treated with preoperative chemotherapy and radiation therapy: preliminary analysis of diffusion-weighted MR imaging for early detection of tumor histopathologic downstaging. Radiology 254(1):170–178
van der Paardt MP, Zagers MB, Beets-Tan RGH, Stoker J, Bipat S (2013) Patients Who Undergo Preoperative Chemoradiotherapy for Locally Advanced Rectal Cancer Restaged by Using Diagnostic MR Imaging: A Systematic Review and Meta-Analysis. Radiology 269(1):101–112
Cai P, Wu Y, An X, Qiu X, Kong L, Liu G et al (2014) Simple measurements on diffusion-weighted MR imaging for assessment of complete response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Eur Radiol 24(11):2962–2970
de Lussanet QG, Backes WH, Griffioen AW, Padhani AR, Baeten CI, van Baardwijk A et al (2005) Dynamic contrast-enhanced magnetic resonance imaging of radiation therapy-induced microcirculation changes in rectal cancer. Int J Radiat Oncol Biol Phys 63(5):1309–1315
Devries AF, Griebel J, Kremser C, Judmaier W, Gneiting T, Kreczy A et al (2001) Tumor microcirculation evaluated by dynamic magnetic resonance imaging predicts therapy outcome for primary rectal carcinoma. Cancer Res 61(6):2513–2516
Devries AF, Kremser C, Hein PA, Griebel J, Krezcy A, Ofner D et al (2003) Tumor microcirculation and diffusion predict therapy outcome for primary rectal carcinoma. Int J Radiat Oncol Biol Phys 56(4):958–965
Dinter DJ, Horisberger K, Zechmann C, Wenz F, Brade J, Willeke F et al (2009) Can dynamic MR imaging predict response in patients with rectal cancer undergoing cetuximab-based neoadjuvant chemoradiation? Onkologie 32(3):86–93
Oberholzer K, Menig M, Pohlmann A, Junginger T, Heintz A, Kreft A et al (2012) Rectal cancer: Assessment of response to neoadjuvant chemoradiation by dynamic contrast-enhanced MRI. J Magnet Reson Imaging 38(1):119–126
Gollub MJ, Gultekin DH, Akin O, Do RK, Fuqua JL, Gonen M et al (2012) Dynamic contrast enhanced-MRI for the detection of pathological complete response to neoadjuvant chemotherapy for locally advanced rectal cancer. Eur Radiol 22(4):821–831
Lim JS, Kim D, Baek SE, Myoung S, Choi J, Shin SJ et al (2012) Perfusion MRI for the prediction of treatment response after preoperative chemoradiotherapy in locally advanced rectal cancer. Eur Radiol 22(8):1693–1700
Curvo-Semedo L, Lambregts DM, Maas M, Thywissen T, Mehsen RT, Lammering G et al (2011) Rectal cancer: assessment of complete response to preoperative combined radiation therapy with chemotherapy--conventional MR volumetry versus diffusion-weighted MR imaging. Radiology 260(3):734–743
Nougaret S, Rouanet P, Molinari N, Pierredon MA, Bibeau F, Azria D et al (2012) MR volumetric measurement of low rectal cancer helps predict tumor response and outcome after combined chemotherapy and radiation therapy. Radiology 263(2):409–418
Nougaret S, Fujii S, Addley HC, Bibeau F, Pandey H, Mikhael H et al (2013) Neoadjuvant chemotherapy evaluation by MRI volumetry in rectal cancer followed by chemoradiation and total mesorectal excision: Initial experience. J Magn Reson Imaging 38(3):726–732
Benson AB, Bekaii-Saab T, Chan E, Chen Y, Choti MA, Cooper HS et al (2012) Rectal cancer. J Natl Compr Cancer Netw 10(12):1528–1564
Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R et al (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45(2):228–247
Miller AB, Hoogstraten B, Staquet M, Winkler A (1981) Reporting results of cancer treatment. Cancer 47(1):207–214
Kim SH, Lee JY, Lee JM, Han JK, Choi BI (2011) Apparent diffusion coefficient for evaluating tumour response to neoadjuvant chemoradiation therapy for locally advanced rectal cancer. Eur Radiol 21(5):987–995
Tofts PS, Brix G, Buckley DL, Evelhoch JL, Henderson E, Knopp MV et al (1999) Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. J Magn Reson Imaging 10(3):223–232
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675
Shia J, Guillem JG, Moore HG, Tickoo SK, Qin J, Ruo L et al (2004) Patterns of morphologic alteration in residual rectal carcinoma following preoperative chemoradiation and their association with long-term outcome. Am J Surg Pathol 28(2):215–223
Trakarnsanga A, Gönen M, Shia J, Nash GM, Temple LK, Guillem JG et al (2014) Comparison of tumor regression grade systems for locally advanced rectal cancer after multimodality treatment. J Natl Cancer Inst 106(10)
Lin LI (1989) A concordance correlation coefficient to evaluate reproducibility. Biometrics 45(1):255–268
Sauer R, Liersch T, Merkel S, Fietkau R, Hohenberger W, Hess C et al (2012) Preoperative versus postoperative chemoradiotherapy for locally advanced rectal cancer: results of the German CAO/ARO/AIO-94 randomized phase III trial after a median follow-up of 11 years. J Clin Oncol Off J Am Soc Clin Oncol 30(16):1926–1933
Lambregts, Doenja MJ, Rao S, Sassen S, Martens MH, Heijnen LA, Buijsen J et al (2014) 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. doi:10.1097/SLA.0000000000000909
Hötker AM, Garcia-Aguilar J, Gollub MJ (2014) Multiparametric MRI of rectal cancer in the assessment of response to therapy: a systematic review. Dis Colon Rectum 57(6):790–799
Chetty R, Gill P, Govender D, Bateman A, Chang HJ, Deshpande V et al (2012) International study group on rectal cancer regression grading: interobserver variability with commonly used regression grading systems. Hum Pathol 43(11):1917–1923
Vallbohmer D, Bollschweiler E, Brabender J, Wedemeyer I, Grimminger PP, Metzger R et al (2012) Evaluation of histological regression grading systems in the neoadjuvant therapy of rectal cancer: do they have prognostic impact? Int J Color Dis 27(10):1295–1301
Acknowledgments
The authors thank Ada Muellner, MS for editing the manuscript. The research of Kaitlin M. Woo and Mithat Gönen was partly supported by NIH/NCI Cancer Center Support Grant P30 CA008748. The scientific guarantor of this publication is Dr. Marc J. Gollub. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. Mithat Gönen PhD and Kaitlin M. Woo MS kindly provided statistical advice for this manuscript. Institutional Review Board approval was obtained. Written informed consent was waived by the Institutional Review Board. No study subjects or cohorts have been previously reported. Methodology: retrospective, experimental, performed at one institution.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hötker, A.M., Tarlinton, L., Mazaheri, Y. et al. Multiparametric MRI in the assessment of response of rectal cancer to neoadjuvant chemoradiotherapy: A comparison of morphological, volumetric and functional MRI parameters. Eur Radiol 26, 4303–4312 (2016). https://doi.org/10.1007/s00330-016-4283-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-016-4283-9