Top

European Journal of Nuclear Medicine and Molecular Imaging

Published in:

Open Access 05-09-2022 | Rectal Cancer | Original Article

Added value of quantitative, multiparametric 18F-FDG PET/MRI in the locoregional staging of rectal cancer

Authors: Alexander Herold, Christian Wassipaul, Michael Weber, Florian Lindenlaub, Sazan Rasul, Anton Stift, Judith Stift, Marius E. Mayerhoefer, Marcus Hacker, Ahmed Ba-Ssalamah, Alexander R. Haug, Dietmar Tamandl

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 1/2022

Abstract

Purpose

The purpose of this study was to determine whether multiparametric positron emission tomography/magnetic resonance imaging (mpPET/MRI) can improve locoregional staging of rectal cancer (RC) and to assess its prognostic value after resection.

Methods

In this retrospective study, 46 patients with primary RC, who underwent multiparametric 18F-fluorodeoxyglucose (FDG) PET/MRI, followed by surgical resection without chemoradiotherapy, were included. Two readers reviewed T- and N- stage, mesorectal involvement, sphincter infiltration, tumor length, and distance from anal verge. In addition, diffusion-weighted imaging (DWI) and PET parameters were extracted from the multiparametric protocol and were compared to radiological staging as well as to the histopathological reference standard. Clinical and imaging follow-up was systematically assessed for tumor recurrence and death.

Results

Locally advanced rectal cancers (LARC) exhibited significantly higher metabolic tumor volume (MTV, AUC 0.74 [95% CI 0.59–0.89], p = 0.004) and total lesion glycolysis (TLG, AUC 0.70 [95% CI 0.53–0.87], p = 0.022) compared to early tumors. T-stage was associated with MTV (AUC 0.70 [95% CI 0.54–0.85], p = 0.021), while N-stage was better assessed using anatomical MRI sequences (AUC 0.72 [95% CI 0.539–0.894], p = 0.032). In the multivariate regression analysis, depending on the model, both anatomical MRI sequences and MTV/TLG were capable of detecting LARC. Combining anatomical MRI stage and MTV/TLG led to a superior diagnostic performance for detecting LARC (AUC 0.81, [95% CI 0.68–0.94], p < 0.001). In the survival analysis, MTV was independently associated with overall survival (HR 1.05 [95% CI 1.01–1.10], p = 0.044).

Conclusion

Multiparametric PET-MRI can improve identification of locally advanced tumors and, hence, help in treatment stratification. It provides additional information on RC tumor biology and may have prognostic value.

Available only for authorised users

Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;17:209–49. https://doi.org/10.3322/caac.21660.CrossRef

Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72:7–33. https://doi.org/10.3322/caac.21708.CrossRefPubMed

Catalano OA, Coutinho AM, Sahani DV, Vangel MG, Gee MS, Hahn PF, et al. Colorectal cancer staging: comparison of whole-body PET/CT and PET/MR. Abdom Radiol (NY). 2017;42:1141–51. https://doi.org/10.1007/s00261-016-0985-3.CrossRef

Siegel RL, Miller KD, Fedewa SA, Ahnen DJ, Meester RGS, Barzi A, et al. Colorectal cancer statistics, 2017. CA Cancer J Clin. 2017;67:177–93. https://doi.org/10.3322/caac.21395.CrossRefPubMed

Suarez-Weiss KE, Herold A, Gervais D, Palmer E, Amorim B, King JD, et al. Hybrid imaging of the abdomen and pelvis. Radiologe. 2020;60:80–9. https://doi.org/10.1007/s00117-020-00661-x.CrossRefPubMed

Braendengen M, Tveit KM, Berglund A, Birkemeyer E, Frykholm G, Påhlman L, et al. Randomized phase III study comparing preoperative radiotherapy with chemoradiotherapy in nonresectable rectal cancer. J Clin Oncol. 2008;26:3687–94. https://doi.org/10.1200/jco.2007.15.3858.CrossRefPubMed

Ganeshan D, Nougaret S, Korngold E, Rauch GM, Moreno CC. Locally recurrent rectal cancer: what the radiologist should know. Abdom Radiol (NY). 2019;44:3709–25. https://doi.org/10.1007/s00261-019-02003-5.CrossRef

Conroy T, Bosset JF, Etienne PL, Rio E, François É, Mesgouez-Nebout N, et al. Neoadjuvant chemotherapy with FOLFIRINOX and preoperative chemoradiotherapy for patients with locally advanced rectal cancer (UNICANCER-PRODIGE 23): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol. 2021;22:702–15. https://doi.org/10.1016/s1470-2045(21)00079-6.CrossRefPubMed

Bahadoer RR, Dijkstra EA, van Etten B, Marijnen CAM, Putter H, Kranenbarg EM, et al. Short-course radiotherapy followed by chemotherapy before total mesorectal excision (TME) versus preoperative chemoradiotherapy, TME, and optional adjuvant chemotherapy in locally advanced rectal cancer (RAPIDO): a randomised, open-label, phase 3 trial. Lancet Oncol. 2021;22:29–42. https://doi.org/10.1016/s1470-2045(20)30555-6.CrossRefPubMed

10.

Gassert FG, Rübenthaler J, Cyran CC, Rink JS, Schwarze V, Luitjens J, et al. (18)F FDG PET/MRI with hepatocyte-specific contrast agent for M staging of rectal cancer: a primary economic evaluation. Eur J Nucl Med Mol Imaging. 2021;48:3268–76. https://doi.org/10.1007/s00259-021-05193-7.CrossRefPubMedPubMedCentral

11.

Haug U, Engel S, Verheyen F, Linder R. Estimating colorectal cancer treatment costs: a pragmatic approach exemplified by health insurance data from Germany. PLoS ONE. 2014;9:e88407. https://doi.org/10.1371/journal.pone.0088407.CrossRefPubMedPubMedCentral

12.

Benson AB, Venook AP, Al-Hawary MM, Cederquist L, Chen YJ, Ciombor KK, et al. Rectal Cancer, Version 1.2022, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2022. https://www.nccn.org/professionals/physician_gls/pdf/rectal.pdf

13.

Beets-Tan RGH, Lambregts DMJ, Maas M, Bipat S, Barbaro B, Curvo-Semedo L, et al. Magnetic resonance imaging for clinical management of rectal cancer: Updated recommendations from the 2016 European Society of Gastrointestinal and Abdominal Radiology (ESGAR) consensus meeting. Eur Radiol. 2018;28:1465–75. https://doi.org/10.1007/s00330-017-5026-2.CrossRefPubMed

14.

Tamandl D, Mang T, Ba-Ssalamah A. Imaging of colorectal cancer - the clue to individualized treatment. Innov Surg Sci. 2018;3:3–15. https://doi.org/10.1515/iss-2017-0049.CrossRefPubMedPubMedCentral

15.

Li J, Zhou Y, Wang X, Zhou M, Chen X, Luan K. An MRI-based multi-objective radiomics model predicts lymph node status in patients with rectal cancer. Abdom Radiol (NY). 2021;46:1816–24. https://doi.org/10.1007/s00261-020-02863-2.CrossRef

16.

Catana C. Principles of Simultaneous PET/MR Imaging. Magn Reson Imaging Clin N Am. 2017;25:231–43. https://doi.org/10.1016/j.mric.2017.01.002.CrossRefPubMedPubMedCentral

17.

Incoronato M, Grimaldi AM, Mirabelli P, Cavaliere C, Parente CA, Franzese M, et al. Circulating miRNAs in untreated breast cancer: an exploratory multimodality morpho-functional study. Cancers (Basel). 2019;11. https://doi.org/10.3390/cancers11060876.

18.

Catalano OA, Horn GL, Signore A, Iannace C, Lepore M, Vangel M, et al. PET/MR in invasive ductal breast cancer: correlation between imaging markers and histological phenotype. Br J Cancer. 2017;116:893–902. https://doi.org/10.1038/bjc.2017.26.CrossRefPubMedPubMedCentral

19.

Mayerhoefer ME, Prosch H, Beer L, Tamandl D, Beyer T, Hoeller C, et al. PET/MRI versus PET/CT in oncology: a prospective single-center study of 330 examinations focusing on implications for patient management and cost considerations. Eur J Nucl Med Mol Imaging. 2019. https://doi.org/10.1007/s00259-019-04452-y

20.

Park J, Pak K, Yun TJ, Lee EK, Ryoo I, Lee JY, et al. Diagnostic accuracy and confidence of [18F] FDG PET/MRI in comparison with PET or MRI alone in head and neck cancer. Sci Rep. 2020;10:9490. https://doi.org/10.1038/s41598-020-66506-8.CrossRefPubMedPubMedCentral

21.

Amorim BJ, Hong TS, Blaszkowsky LS, Ferrone CR, Berger DL, Bordeianou LG, et al. Clinical impact of PET/MR in treated colorectal cancer patients. Eur J Nucl Med Mol Imaging. 2019;46:2260–9. https://doi.org/10.1007/s00259-019-04449-7.CrossRefPubMed

22.

Delaby G, Ataeinia B, Wo J, Catalano OA, Heidari P. Impact of 18F-FDG PET/MR based tumor delineation in radiotherapy planning for cholangiocarcinoma. Abdom Radiol (NY). 2021;46:3908–16. https://doi.org/10.1007/s00261-021-03053-4.CrossRef

23.

Catalano OA, Daye D, Signore A, Iannace C, Vangel M, Luongo A, et al. Staging performance of whole-body DWI, PET/CT and PET/MRI in invasive ductal carcinoma of the breast. Int J Oncol. 2017;51:281–8. https://doi.org/10.3892/ijo.2017.4012.CrossRefPubMed

24.

Biondetti P, Vangel MG, Lahoud RM, Furtado FS, Rosen BR, Groshar D, et al. PET/MRI assessment of lung nodules in primary abdominal malignancies: sensitivity and outcome analysis. Eur J Nucl Med Mol Imaging. 2021;48:1976–86. https://doi.org/10.1007/s00259-020-05113-1.CrossRefPubMed

25.

Catalano OA, Lee SI, Parente C, Cauley C, Furtado FS, Striar R, et al. Improving staging of rectal cancer in the pelvis: the role of PET/MRI. Eur J Nucl Med Mol Imaging. 2021;48:1235–45. https://doi.org/10.1007/s00259-020-05036-x.CrossRefPubMed

26.

Singnurkar A, Poon R, Metser U. Comparison of 18F-FDG-PET/CT and 18F-FDG-PET/MR imaging in oncology: a systematic review. Ann Nucl Med. 2017;31:366–78. https://doi.org/10.1007/s12149-017-1164-5.CrossRefPubMed

27.

Glynne-Jones R, Wyrwicz L, Tiret E, Brown G, Rödel C, Cervantes A, et al. Rectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018;29:iv263. https://doi.org/10.1093/annonc/mdy161.

28.

Maas M, Lambregts DM, Lahaye MJ, Beets GL, Backes W, Vliegen RF, et al. T-staging of rectal cancer: accuracy of 3.0 Tesla MRI compared with 1.5 Tesla. Abdom Imaging. 2012;37:475–81. https://doi.org/10.1007/s00261-011-9770-5.CrossRefPubMed

29.

Merkel S, Mansmann U, Siassi M, Papadopoulos T, Hohenberger W, Hermanek P. The prognostic inhomogeneity in pT3 rectal carcinomas. Int J Colorectal Dis. 2001;16:298–304. https://doi.org/10.1007/s003840100309.CrossRefPubMed

30.

Ogawa S, Hida J-i, Ike H, Kinugasa T, Ota M, Shinto E, et al. Selection of lymph node–positive cases based on perirectal and lateral pelvic lymph nodes using magnetic resonance imaging: study of the Japanese Society for Cancer of the Colon and Rectum. Ann Surg Oncol 2016;23:1187–94. https://doi.org/10.1245/s10434-015-5021-2.

31.

Gröne J, Loch FN, Taupitz M, Schmidt C, Kreis ME. Accuracy of various lymph node staging criteria in rectal cancer with magnetic resonance imaging. J Gastrointest Surg. 2018;22:146–53. https://doi.org/10.1007/s11605-017-3568-x.CrossRefPubMed

32.

Curvo-Semedo L, Lambregts DM, Maas M, Beets GL, Caseiro-Alves F, Beets-Tan RG. Diffusion-weighted MRI in rectal cancer: apparent diffusion coefficient as a potential noninvasive marker of tumor aggressiveness. J Magn Reson Imaging : JMRI. 2012;35:1365–71. https://doi.org/10.1002/jmri.23589.CrossRefPubMed

33.

Shih IL, Yen RF, Chen CA, Cheng WF, Chen BB, Chang YH, et al. PET/MRI in cervical cancer: associations between imaging biomarkers and tumor stage, disease progression, and overall survival. J Magn Reson Imaging : JMRI. 2021;53:305–18. https://doi.org/10.1002/jmri.27311.CrossRefPubMed

34.

Malik V, Johnston C, O’Toole D, Lucey J, O’Farrell N, Claxton Z, et al. Metabolic tumor volume provides complementary prognostic information to EUS staging in esophageal and junctional cancer. Dis Esophagus. 2017;30:1–8. https://doi.org/10.1111/dote.12505.CrossRefPubMed

35.

Liu H, Ye Z, Yang T, Xie H, Duan T, Li M, et al. Predictive value of metabolic parameters derived from 18F-FDG PET/CT for microsatellite instability in patients with colorectal carcinoma. Front Immunol. 2021;12. https://doi.org/10.3389/fimmu.2021.724464.

36.

Cerny M, Dunet V, Prior JO, Hahnloser D, Wagner AD, Meuli RA, et al. Initial staging of locally advanced rectal cancer and regional lymph nodes: comparison of diffusion-weighted MRI with 18F-FDG-PET/CT. Clin Nucl Med. 2016;41:289–95. https://doi.org/10.1097/rlu.0000000000001172.CrossRefPubMedPubMedCentral

37.

Queiroz MA, Ortega CD, Ferreira FR, Capareli FC, Nahas SC, Cerri GG, et al. Value of primary rectal tumor PET/MRI in the prediction of synchronic metastatic disease. Mol Imaging Biol. 2021. https://doi.org/10.1007/s11307-021-01674-1

38.

Li Y, Mueller LI, Neuhaus JP, Bertram S, Schaarschmidt BM, Demircioglu A, et al. (18)F-FDG PET/MR versus MR alone in whole-body primary staging and restaging of patients with rectal cancer: what is the benefit of PET? J Clin Med. 2020;9. https://doi.org/10.3390/jcm9103163.

Title: Added value of quantitative, multiparametric 18F-FDG PET/MRI in the locoregional staging of rectal cancer
Authors: Alexander Herold
Christian Wassipaul
Michael Weber
Florian Lindenlaub
Sazan Rasul
Anton Stift
Judith Stift
Marius E. Mayerhoefer
Marcus Hacker
Ahmed Ba-Ssalamah
Alexander R. Haug
Dietmar Tamandl
Publication date: 05-09-2022
Publisher: Springer Berlin Heidelberg
Keywords: Rectal Cancer
Rectal Cancer
Published in: European Journal of Nuclear Medicine and Molecular Imaging / Issue 1/2022
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI: https://doi.org/10.1007/s00259-022-05936-0

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Added value of quantitative, multiparametric 18F-FDG PET/MRI in the locoregional staging of rectal cancer

Abstract

Purpose

Methods

Results

Conclusion

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2022

Imaging of heart disease in women: review and case presentation

Theranostic application of 64Cu/177Lu-labeled anti-Trop2 monoclonal antibody in pancreatic cancer tumor models

[18F]FDG brain PET findings in CLIPPERS at diagnosis and therapeutic follow-up

Quantitative PET imaging of the CD4 pool in nonhuman primates

Correction to: [18F]FAPI‑42 PET/CT versus [18F]FDG PET/CT for imaging of recurrent or metastatic gastrointestinal stromal tumors

Prognostic role of metabolic parameters (MTV and TLG) of staging PET/CT in the pediatric population with Hodgkin’s lymphoma: an open discussion