Clinical impact of PET/MRI in oligometastatic colorectal cancer

Felipe S Furtado, Krista E Suarez-Weiss, Mark Vangel, Jeffrey W Clark, James C Cusack, Theodore Hong, Lawrence Blaszkowsky, Jennifer Wo, Robin Striar, Lale Umutlu, Heike E Daldrup-Link, David Groshar, Ricciardi Rocco, Liliana Bordeianou, Mark A Anderson, Amirkasra Mojtahed, Motaz Qadan, Cristina Ferrone, Onofrio A Catalano, Felipe S Furtado, Krista E Suarez-Weiss, Mark Vangel, Jeffrey W Clark, James C Cusack, Theodore Hong, Lawrence Blaszkowsky, Jennifer Wo, Robin Striar, Lale Umutlu, Heike E Daldrup-Link, David Groshar, Ricciardi Rocco, Liliana Bordeianou, Mark A Anderson, Amirkasra Mojtahed, Motaz Qadan, Cristina Ferrone, Onofrio A Catalano

Abstract

Background: Oligometastatic colorectal cancer (CRC) is potentially curable and demands individualised strategies.

Methods: This single-centre retrospective study investigated if positron emission tomography (PET)/magnetic resonance imaging (MR) had a clinical impact on oligometastatic CRC relative to the standard of care imaging (SCI). Adult patients with oligometastatic CRC on SCI who also underwent PET/MR between 3/2016 and 3/2019 were included. The exclusion criterion was lack of confirmatory standard of reference, either surgical pathology, intraoperative gross confirmation or imaging follow-up. SCI consisted of contrast-enhanced (CE) computed tomography (CT) of the chest/abdomen/pelvis, abdominal/pelvic CE-MR, and/or CE whole-body PET/CT with diagnostic quality (i.e. standard radiation dose) CT. Follow-up was evaluated until 3/2020.

Results: Thirty-one patients constituted the cohort, 16 (52%) male, median patient age was 53 years (interquartile range: 49-65 years). PET/MR and SCI results were divergent in 19% (95% CI 9-37%) of the cases, with PET/MR leading to management changes in all of them. The diagnostic accuracy of PET/MR was 90 ± 5%, versus 71 ± 8% for SCI. In a pairwise analysis, PET/MR outperformed SCI when compared to the reference standard (p = 0.0412).

Conclusions: These findings suggest the potential usefulness of PET/MR in the management of oligometastatic CRC.

Conflict of interest statement

The authors declare no competing interests.

© 2021. The Author(s), under exclusive licence to Springer Nature Limited.

Figures

Fig. 1. Peritoneal disease detected at PET/MR…
Fig. 1. Peritoneal disease detected at PET/MR only.
Axial CE-CT (a), PET/MR axial T2-weighted high resolution (b), and fused PET/MR (c), from a 55-year-old female patient with oligometastatic rectal cancer, who had already undergone rectal surgery. The axial CT shows a presacral soft-tissue nodule, inseparable from the anastomosis, suspicious for tumour recurrence (arrow in a). On the PET/MR, the same lesion did not demonstrate increased FDG uptake (short arrow in b, c). There is, however, unexpected peritoneal disease involving the serosa of the sigmoid colon that was not seen on CT (long arrow in b, c). Both scans were performed 19 days apart. Due to the demonstration of peritoneal metastases by PET/MR, the patient was placed on chemotherapy instead of the original surgical approach which included liver metastasectomy and pelvic recurrence resection. The findings were confirmed by follow-up CE-MR performed 73 days later.
Fig. 2. Viable metastasis diagnosed by PET/MR.
Fig. 2. Viable metastasis diagnosed by PET/MR.
Axial fused PET/CT (a), axial fused PET/MR (b), PET/MR contrast-enhanced VIBE (c), low b-value diffusion-weighted imaging (DWI) (d), and apparent diffusion coefficient (ADC) map (e). 50-year-old female patient with oligometastatic rectal cancer. PET/CT did not show residual hepatic metastases. However, a residual metastasis in segment VI/VII (arrow) was diagnosed by PET/MR. The lesion is harder to call a metastasis on PET/CT. Compared to PET/CT, the longer PET acquisition time along with the combined information from restricted diffusion and enhancement pattern on PET/MR allowed lesion detection and characterisation. Therefore, the patient underwent a liver metastasectomy in addition to the already planned chemoradiation therapy. Both scans were performed on the same day, and the pathology report from the liver metastasectomy specimen confirmed the PET/MR finding.

References

    1. Ferlay J, Colombet M, Soerjomataram I, Mathers C, Parkin DM, Piñeros M, et al. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer. 2019;144:1941–53. doi: 10.1002/ijc.31937.
    1. Siegel RL, Miller KD, Fuchs H, Jemal A. Cancer statistics, 2021. CA Cancer J Clin. 2021;71:7–33. doi: 10.3322/caac.21654.
    1. Aigner F, Pratschke J, Schmelzle M. Oligometastatic disease in colorectal cancer—how to proceed? Vis Med. 2017;33:23–8.
    1. Van Cutsem E, Cervantes A, Nordlinger B, Arnold D; ESMO Guidelines Working Group. Metastatic colorectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2014;25 (Suppl 3):iii1–iii9.
    1. Van der Pool AEM, Damhuis RA, Ijzermans JNM, de Wilt JHW, Eggermont AMM, Kranse R, et al. Trends in incidence, treatment and survival of patients with stage IV colorectal cancer: a population-based series. Colorectal Dis. 2012;14:56–61. doi: 10.1111/j.1463-1318.2010.02539.x.
    1. Sadahiro S, Suzuki T, Tanaka A, Okada K, Kamata H. Hematogenous metastatic patterns of curatively resected colon cancer were different from those of stage IV and autopsy cases. Jpn J Clin Oncol. 2013;43:444–7. doi: 10.1093/jjco/hyt002.
    1. Manfredi S, Lepage C, Hatem C, Coatmeur O, Faivre J, Bouvier A-M. Epidemiology and management of liver metastases from colorectal cancer. Ann. Surg. 2006;244:254–9. doi: 10.1097/.
    1. Tomlinson JS, Jarnagin WR, DeMatteo RP, Fong Y, Kornprat P, Gonen M, et al. Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol. 2007;25:4575–80. doi: 10.1200/JCO.2007.11.0833.
    1. House MG, Ito H, Gönen M, Fong Y, Allen PJ, DeMatteo RP, et al. Survival after hepatic resection for metastatic colorectal cancer: trends in outcomes for 1,600 patients during two decades at a single institution. J Am Coll Surg. 2010;210:744–52. doi: 10.1016/j.jamcollsurg.2009.12.040.
    1. Adam R, Wicherts DA, de Haas RJ, Ciacio O, Lévi F, Paule B, et al. Patients with initially unresectable colorectal liver metastases: is there a possibility of cure? J Clin Oncol. 2009;27:1829–35. doi: 10.1200/JCO.2008.19.9273.
    1. Weichselbaum RR, Hellman S. Oligometastases revisited. Nat Rev Clin Oncol. 2011;8:378–82. doi: 10.1038/nrclinonc.2011.44.
    1. Palma DA, Salama JK, Lo SS, Senan S, Treasure T, Govindan R, et al. The oligometastatic state—separating truth from wishful thinking. Nat Rev Clin Oncol. 2014;11:549. doi: 10.1038/nrclinonc.2014.96.
    1. Weiser MR, Jarnagin WR, Saltz LB. Colorectal cancer patients with oligometastatic liver disease: what is the optimal approach? Oncology. 2013;27:1074–8.
    1. Martin R, Paty P, Fong Y, Grace A, Cohen A, DeMatteo R, et al. Simultaneous liver and colorectal resections are safe for synchronous colorectal liver metastasis. J Am Coll Surg. 2003;197:233–41. doi: 10.1016/S1072-7515(03)00390-9.
    1. Onkologie L. S3-Leitlinie Kolorektales Karzinom. Langversion. 2014;1:2014.
    1. Monteil J, Le Brun-Ly V, Cachin F, Zasadny X, Seitz J-F, Mundler O, et al. Comparison of 18FDG-PET/CT and conventional follow-up methods in colorectal cancer: A randomised prospective study. Dig Liver Dis. 2021;53:231–7. doi: 10.1016/j.dld.2020.10.012.
    1. Atkinson W, Catana C, Abramson JS, Arabasz G, McDermott S, Catalano O, et al. Hybrid FDG-PET/MR compared to FDG-PET/CT in adult lymphoma patients. Abdom Radio (NY) 2016;41:1338–48. doi: 10.1007/s00261-016-0638-6.
    1. Pace L, Nicolai E, Aiello M, Catalano OA, Salvatore M. Whole-body PET/MRI in oncology: current status and clinical applications. Clin Transl Imaging. 2013;1:31–44. doi: 10.1007/s40336-013-0012-4.
    1. Wetter A, Grueneisen J, Umutlu L. PET/MR imaging of pelvic malignancies. Eur J Radio. 2017;94:A44–51. doi: 10.1016/j.ejrad.2017.02.026.
    1. Catalano OA, Rosen BR, Sahani DV, Hahn PF, Guimaraes AR, Vangel MG, et al. Clinical impact of PET/MR imaging in patients with cancer undergoing same-day PET/CT: initial experience in 134 patients—a hypothesis-generating exploratory study. Radiology. 2013;269:857–69. doi: 10.1148/radiol.13131306.
    1. 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. doi: 10.1038/bjc.2017.26.
    1. Furtado FS, Ferrone CR, Lee SI, Vangel M, Rosman DA, Weekes C, et al. Impact of PET/MRI in the Treatment of Pancreatic Adenocarcinoma: a Retrospective Cohort Study. Mol Imaging Biol. 2021;23:456–66. doi: 10.1007/s11307-020-01569-7.
    1. 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. doi: 10.3892/ijo.2017.4012.
    1. Ferrone C, Goyal L, Qadan M, Gervais D, Sahani DV, Zhu AX, et al. Management implications of fluorodeoxyglucose positron emission tomography/magnetic resonance in untreated intrahepatic cholangiocarcinoma. Eur J Nucl Med Mol Imaging. 2020;47:1871–84. doi: 10.1007/s00259-019-04558-3.
    1. 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. doi: 10.1007/s00259-019-04449-7.
    1. 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 Radio (NY) 2017;42:1141–51. doi: 10.1007/s00261-016-0985-3.
    1. Kang B, Lee JM, Song YS, Woo S, Hur BY, Jeon JH, et al. Added value of integrated whole-body PET/MRI for evaluation of colorectal cancer: comparison with contrast-enhanced MDCT. AJR Am J Roentgenol. 2016;206:W10–20. doi: 10.2214/AJR.14.13818.
    1. Catalano OL, 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. doi: 10.1007/s00259-020-05036-x.
    1. Niibe Y, Chang JY. Novel insights of oligometastases and oligo-recurrence and review of the literature. Pulm Med. 2012;2012:261096. doi: 10.1155/2012/261096.
    1. Reyes DK, Pienta KJ. The biology and treatment of oligometastatic cancer. Oncotarget. 2015;6:8491–524. doi: 10.18632/oncotarget.3455.
    1. Benson AB, Venook AP, Al-Hawary MM, Cederquist L, Chen Y-J, Ciombor KK, et al. NCCN Guidelines insights: colon cancer, Version 2.2018. J Natl Compr Canc Netw. 2018;16:359–69. doi: 10.6004/jnccn.2018.0021.
    1. Ottaiano A, Circelli L, Lombardi A, Scala S, Martucci N, Galon J, et al. Genetic trajectory and immune microenvironment of lung-specific oligometastatic colorectal cancer. Cell Death Dis. 2020;11:275. doi: 10.1038/s41419-020-2480-6.
    1. Petre EN, Sofocleous C. Thermal ablation in the management of colorectal cancer patients with oligometastatic liver disease. Visc Med. 2017;33:62–8. doi: 10.1159/000454697.
    1. Pitroda SP, Khodarev NN, Huang L, Uppal A, Wightman SC, Ganai S, et al. Integrated molecular subtyping defines a curable oligometastatic state in colorectal liver metastasis. Nat Commun. 2018;9:1793. doi: 10.1038/s41467-018-04278-6.
    1. Weiser MR. AJCC 8th edition: colorectal cancer. Ann Surg Oncol. 2018;25:1454–5. doi: 10.1245/s10434-018-6462-1.
    1. Van Cutsem E, Cervantes A, Adam R, Sobrero A, Van Krieken JH, Aderka D, et al. ESMO consensus guidelines for the management of patients with metastatic colorectal cancer. Ann Oncol. 2016;27:1386–422. doi: 10.1093/annonc/mdw235.
    1. Delso G, Fürst S, Jakoby B, Ladebeck R, Ganter C, Nekolla SG, et al. Performance measurements of the Siemens mMR integrated whole-body PET/MR scanner. J Nucl Med. 2011;52:1914–22. doi: 10.2967/jnumed.111.092726.
    1. Gassert FG, Rübenthaler J, Cyran CC, Rink JS, Schwarze V, Luitjens J, et al. 18F 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; 10.1007/s00259-021-05193-7. [Epub ahead of print].
    1. Benson AB III, Venook AP, Al-Hawary MM, Arain MA, Chen Y-J, Ciombor KK, et al. NCCN guidelines version 1.2021 rectal cancer [Internet]. J Natl Compr Cancer Netw. 2020 [cited 2021 Mar 3]. Available from: .
    1. Zhang C, O’Shea A, Parente CA, Amorim BJ, Caravan P, Ferrone CR, et al. Evaluation of the diagnostic performance of positron emission tomography/magnetic resonance for the diagnosis of liver metastases. Invest Radiol. [Internet]. 2021. Available from: 10.1097/RLI.0000000000000782. [Epub ahead of print].
    1. Queiroz MA, Ortega CD, Ferreira FR, Nahas SC, Cerri GG, Buchpiguel CA. Diagnostic accuracy of FDG-PET/MRI versus pelvic MRI and thoracic and abdominal CT for detecting synchronous distant metastases in rectal cancer patients. Eur. J. Nucl. Med Mol. Imaging. 2021;48:186–95. doi: 10.1007/s00259-020-04911-x.
    1. 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. doi: 10.1007/s00259-020-05113-1.
    1. Moses WW. Fundamental limits of spatial resolution in PET. Nucl Instrum Methods Phys Res A. 2011;648:S236–40. doi: 10.1016/j.nima.2010.11.092.
    1. Sandhu J, Lavingia V, Fakih M. Systemic treatment for metastatic colorectal cancer in the era of precision medicine. J Surg Oncol. 2019;119:564–82. doi: 10.1002/jso.25421.
    1. Dercle L, Lu L, Schwartz LH, Qian M, Tejpar S, Eggleton P, et al. Radiomics response signature for identification of metastatic colorectal cancer sensitive to therapies targeting EGFR pathway. J Natl Cancer Inst. 2020;112:902–12. doi: 10.1093/jnci/djaa017.
    1. Yang L, Dong D, Fang M, Zhu Y, Zang Y, Liu Z, et al. Can CT-based radiomics signature predict KRAS/NRAS/BRAF mutations in colorectal cancer? Eur Radio. 2018;28:2058–67. doi: 10.1007/s00330-017-5146-8.
    1. Paspulati RM, Partovi S, Herrmann KA, Krishnamurthi S, Delaney CP, Nguyen NC. Comparison of hybrid FDG PET/MRI compared with PET/CT in colorectal cancer staging and restaging: a pilot study. Abdom Imaging. 2015;40:1415–25. doi: 10.1007/s00261-015-0474-0.
    1. Brendle C, Schwenzer NF, Rempp H, Schmidt H, Pfannenberg C, la Fougère C, et al. Assessment of metastatic colorectal cancer with hybrid imaging: comparison of reading performance using different combinations of anatomical and functional imaging techniques in PET/MRI and PET/CT in a short case series. Eur J Nucl Med Mol Imaging. 2016;43:123–32. doi: 10.1007/s00259-015-3137-z.

Source: PubMed

3
S'abonner