Share this content in WeChat
Research progress in imaging evaluation of liver metastases in colorectal cancer
TIAN Yihe  LIU Hong  BAI Liangcai 

Cite this article as: TIAN Y H, LIU H, BAI L C. Research progress in imaging evaluation of liver metastases in colorectal cancer[J]. Chin J Magn Reson Imaging, 2023, 14(2): 191-196. DOI:10.12015/issn.1674-8034.2023.02.034.

[Abstract] Colorectal cancer is the third most common malignant tumor in the world, with a high incidence and mortality of liver metastasis. The key to improve the prognosis of colorectal cancer patients with liver metastases is early diagnosis and reasonable treatment of liver metastases. Imaging methods such as CT, MRI, positron emission tomography (PET) and ultrasound (US) can be used to evaluate liver metastases from colorectal cancer. This article reviews the imaging evaluation methods of colorectal cancer liver metastases to provide a reference for the clinical diagnosis and treatment strategy of colorectal cancer liver metastases.
[Keywords] colorectal neoplasms;colorectal cancer liver metastasis;radiography;computer tomography;magnetic resonance imaging;positron emission tomography;ultrasound

TIAN Yihe1   LIU Hong1, 2   BAI Liangcai1, 2*  

1 The Second School of Clinical Medicine, Lanzhou University, Lanzhou 730000, China

2 Department of Radiology, Lanzhou University Second Hospital, Key Laboratory of Medical Imaging of Gansu Province, Gansu International Science and Technology Cooperation Base for Artificial Intelligence in Medical Imaging, Lanzhou 730030, China

*Correspondence to: Bai LC, E-mail:

Conflicts of interest   None.

Received  2022-09-06
Accepted  2023-01-12
DOI: 10.12015/issn.1674-8034.2023.02.034
Cite this article as: TIAN Y H, LIU H, BAI L C. Research progress in imaging evaluation of liver metastases in colorectal cancer[J]. Chin J Magn Reson Imaging, 2023, 14(2): 191-196. DOI:10.12015/issn.1674-8034.2023.02.034.

LI M Y, LI X Y, GUO Y, et al. Development and assessment of an individualized nomogram to predict colorectal cancer liver metastases[J]. Quant Imaging Med Surg, 2020, 10(2): 397-414. DOI: 10.21037/qims.2019.12.16.
QIN H, WU Y Q, LIN P, et al. Ultrasound image-based radiomics: an innovative method to identify primary tumorous sources of liver metastases[J]. J Ultrasound Med, 2021, 40(6): 1229-1244. DOI: 10.1002/jum.15506.
LEE S, CHOE E K, KIM S Y, et al. Liver imaging features by convolutional neural network to predict the metachronous liver metastasis in stage Ⅰ-Ⅲ colorectal cancer patients based on preoperative abdominal CT scan[J/OL]. BMC Bioinformatics, 2020, 21(13): 382 [2022-09-10]. DOI: 10.1186/s12859-020-03686-0.
WIERING B, RUERS T J, KRABBE P F, et al. Comparison of multiphase CT, FDG-PET and intra-operative ultrasound in patients with colorectal liver metastases selected for surgery[J]. Ann Surg Oncol, 2007, 14(2): 818-826. DOI: 10.1245/s10434-006-9259-6.
BENOIST S, BROUQUET A, PENNA C, et al. Complete response of colorectal liver metastases after chemotherapy: does it mean cure?[J]. J Clin Oncol, 2006, 24(24): 3939-3945. DOI: 10.1200/JCO.2006.05.8727.
TSILIMIGRAS D I, BRODT P, CLAVIEN P A, et al. Liver metastases[J/OL]. Nat Rev Dis Primers, 2021, 7(1): 27 [2022-12-04]. DOI: 10.1038/s41572-021-00261-6.
VAN KESSEL C S, BUCKENS C F, VAN DEN BOSCH M A, et al. Preoperative imaging of colorectal liver metastases after neoadjuvant chemotherapy: a meta-analysis[J]. Ann Surg Oncol, 2012, 19(9): 2805-2813. DOI: 10.1245/s10434-012-2300-z.
STURESSON C, NILSSON J, LINDELL G, et al. Disappearing liver metastases from colorectal cancer: impact of modern imaging modalities[J]. HPB (Oxford), 2015, 17(11): 983-987. DOI: 10.1111/hpb.12476.
TIRUMANI S H, KIM K W, NISHINO M, et al. Update on the role of imaging in management of metastatic colorectal cancer[J]. Radiographics, 2014, 34(7): 1908-1928. DOI: 10.1148/rg.347130090.
VAN CAMP L, DEAK P, HASPESLAGH M, et al. A prospective clinical study using a dynamic contrast-enhanced CT-protocol for detection of colorectal liver metastases[J/OL]. Eur J Radiol, 2018, 107: 143-148 [2022-09-10]. DOI: 10.1016/j.ejrad.2018.08.022.
ABDEL MONEIM CHALABI N, BASSIOUNY R H, SEDEK M A EL. FDG-PETCT versus contrast-enhanced computed tomography in diagnosis of post-therapeutic colorectal cancer recurrence and metastases[J/OL]. Egypt J Radiol Nucl Med, 2020, 51(1): 3 [2022-09-10]. DOI: 10.1186/s43055-019-0083-y.
MALEUX G, IZAMIS M L, WERBROUCK C, et al. Characterization of Liver Metastases During Catheter-Directed Liver Interventions: A Comparison between Dual Phase Cone-Beam Computed Tomography and Conventional Contrast-Enhanced Computed Tomography[J/OL]. J Belg Soc Radiol, 2020, 104(1): 41 [2022-09-10]. DOI: 10.5334/jbsr.2052.
FANG T Q, CHEN Y Y, BIN G, et al. An overview on the research of spectral CT in liver cancer[J]. Int J Med Radiol, 2017, 40(2): 165-169. DOI: 10.19300/j.2017.Z4260.
YE X H, ZHOU C, WU G G, et al. Primary study on the detection of hepatic tumors with spectral CT monochromatic imaging[J]. Chin J Radiol, 2011, 45(8): 718-722. DOI: 10.3760/cma.j.issn.1005-1201.2011.08.003.
CECCO C N D, WICHMANN J L, MUSCOGIURI G, et al. Dual energy CT in Oncology[M]. Berlin: Springer, 2015: 59-73.
DUAN H F, MA G M, REN Z L, et al. Value of energy spectrum CT plain scan imaging in differentiating small hepatic cysts from small metastatic tumors[J]. Shaanxi Med J, 2016, 45(5): 568-569. DOI: 10.3969/j.issn.1000-7377.2016.05.024.
LUO N B, LI W Z, XIE J S, et al. Preoperative normalized iodine concentration derived from spectral CT is correlated with early recurrence of hepatocellular carcinoma after curative resection[J]. Eur Radiol, 2021, 31(4): 1872-1882. DOI: 10.1007/s00330-020-07330-6.
WANG N, JU Y, WU J, et al. Differentiation of liver abscess from liver metastasis using dual-energy spectral CT quantitative parameters[J/OL]. Eur J Radiol, 2019, 113: 204-208 [2022-09-09]. DOI: 10.1016/j.ejrad.2019.02.024.
TAGHAVI M, STAAL F, GOMEZ MUNOZ F, et al. CT-Based Radiomics Analysis Before Thermal Ablation to Predict Local Tumor Progression for Colorectal Liver Metastases[J/OL]. Cardiovasc Intervent Radiol, 2021, 44(6): 913-920 [2022-12-06]. DOI: 10.1007/s00270-020-02735-8.
TAGHAVI M, TREBESCHI S, SIMÕES R, et al. Machine learning-based analysis of CT radiomics model for prediction of colorectal metachronous liver metastases[J]. Abdom Radiol (NY), 2021, 46(1): 249-256. DOI: 10.1007/s00261-020-02624-1.
GHADIMI M, PANDEY P, REZVANI HABIBABADI R, et al. Role of volumetric multiparametric MRI in distinguishing between intraductal papillary mucinous neoplasms and serous cystadenoma[J]. Abdom Radiol (NY), 2021, 46(4): 1629-1639. DOI: 10.1007/s00261-020-02792-0.
ZHANG Y P, LI X H, WANG F, et al. Quantitative diagnosis of non-contrast-enhanced T1 mapping in hemangioma, hepatocellular carcinoma and hepatic metastases[J]. Chin J Med Imaging, 2021, 29(12): 1216-1221. DOI: 10.3969/j.issn.1005-5185.2021.12.010.
HUANG J Y, LU Z J, LIU B. Diagnostic significance of MRI combined with DWI for colorectal cancer[J]. China Med Pharm, 2019, 9(17): 158-161. DOI: 10.3969/j.issn.2095-0616.2019.17.046.
YU Z Z, HUANG J Y, ZHOU Z M, et al. Development of magnetic resonance imaging contrast agents[J]. Shandong Chem Ind, 2019, 48(21): 60-62, 67. DOI: 10.19319/j.cnki.issn.1008-021x.2019.21.023.
D'SILVA M, CHO J Y, HAN H S, et al. Association between oncological outcomes of patients with colorectal liver metastasis and additional gadoxetic acid-enhanced magnetic resonance imaging[J]. Ann Palliat Med, 2021, 10(10): 10213-10221. DOI: 10.21037/apm-21-1470.
GRANATA V, FUSCO R, DE LUTIO DI CASTELGUIDONE E, et al. Diagnostic performance of gadoxetic acid-enhanced liver MRI versus multidetector CT in the assessment of colorectal liver metastases compared to hepatic resection[J/OL]. BMC Gastroenterol, 2019, 19(1): 129 [2022-09-08]. DOI: 10.1186/s12876-019-1036-7.
KIM C, KIM S Y, KIM M J, et al. Clinical impact of preoperative liver MRI in the evaluation of synchronous liver metastasis of colon cancer[J]. Eur Radiol, 2018, 28(10): 4234-4242. DOI: 10.1007/s00330-018-5422-2.
CHOI S H, KIM S Y, PARK S H, et al. Diagnostic performance of CT, gadoxetate disodium-enhanced MRI, and PET/CT for the diagnosis of colorectal liver metastasis: systematic review and meta-analysis[J]. J Magn Reson Imaging, 2018, 47(5): 1237-1250. DOI: 10.1002/jmri.25852.
SHU Z, FANG S, DING Z, et al. MRI-based Radiomics nomogram to detect primary rectal cancer with synchronous liver metastases[J/OL]. Sci Rep, 2019, 9(1): 3374 [2022-12-06]. DOI: 10.1038/s41598-019-39651-y.
GRANATA V, FUSCO R, DE MUZIO F, et al. Radiomics and Machine Learning Analysis Based on Magnetic Resonance Imaging in the Assessment of Colorectal Liver Metastases Growth Pattern[J/OL]. Diagnostics (Basel), 2022, 12(5) [2022-12-07]. DOI: 10.3390/diagnostics12051115.
HONG J P, ZUO C J, ZHANG J, et al. The value of PET/CT in metastatic liver cancer[J]. J Pract Med Imaging, 2013, 14(2): 119-121. DOI: 10.16106/j.cnki.cn14-1281/r.2013.02.035.
MAFFIONE A M, LOPCI E, BLUEMEL C, et al. Diagnostic accuracy and impact on management of (18)F-FDG PET and PET/CT in colorectal liver metastasis: a meta-analysis and systematic review[J]. Eur J Nucl Med Mol Imaging, 2015, 42(1): 152-163. DOI: 10.1007/s00259-014-2930-4.
LOPEZ-LOPEZ V, ROBLES R, BRUSADIN R, et al. Role of 18F-FDG PET/CT vs CT-scan in patients with pulmonary metastases previously operated on for colorectal liver metastases[J/OL]. Br J Radiol, 2018, 91(1081): 20170216 [2022-12-06]. DOI: 10.1259/bjr.20170216.
JONSSON J, HEMMINGSSON O, STRENGBOM R, et al. Does (18)F-FDG PET/CT change the surgical management of potentially resectable colorectal liver metastases?[J/OL]. Scand J Surg, 2022, 111(1): 14574969221083144 [2022-06-24]. DOI: 10.1177/14574969221083144.
OZIS S E, SOYDAL C, AKYOL C, et al. The role of 18F-fluorodeoxyglucose positron emission tomography/computed tomography in the primary staging of rectal cancer[J/OL]. World J Surg Oncol, 2014, 12: 26 [2022-09-10]. DOI: 10.1186/1477-7819-12-26.
MIRSHAHVALAD S A, HINZPETER R, KOHAN A, et al. Diagnostic performance of [(18)F]-FDG PET/MR in evaluating colorectal cancer: a systematic review and meta-analysis[J/OL]. Eur J Nucl Med Mol Imaging, 2022, 49(12): 4205-4217 [2022-09-10]. DOI: 10.1007/s00259-022-05871-0.
AKHURST T, GÖNEN M, BASER R E, et al. Prospective evaluation of 18F-FDG positron emission tomography in the preoperative staging of patients with hepatic colorectal metastases[J]. Hepatobiliary Surg Nutr, 2022, 11(4): 539-554. DOI: 10.21037/hbsn-19-357.
DONATI O F, HANY T F, REINER C S, et al. Value of retrospective fusion of PET and MR images in detection of hepatic metastases: comparison with 18F-FDG PET/CT and Gd-EOB-DTPA-enhanced MRI[J]. J Nucl Med, 2010, 51(5): 692-699. DOI: 10.2967/jnumed.109.068510.
COENEGRACHTS K, DE GEETER F, BEEK L TER, et al. Comparison of MRI (including SS SE-EPI and SPIO-enhanced MRI) and FDG-PET/CT for the detection of colorectal liver metastases[J]. Eur Radiol, 2009, 19(2): 370-379. DOI: 10.1007/s00330-008-1163-y.
LAM C S N, BHARWANI A A, CHAN E H Y, et al. A machine learning model for colorectal liver metastasis post-hepatectomy prognostications[J/OL]. Hepatobiliary Surg Nutr, 2022 [2022-12-06]. DOI: 10.21037/hbsn-21-453
HAGOPIAN E J. Liver ultrasound: a key procedure in the surgeon's toolbox[J]. J Surg Oncol, 2020, 122(1): 61-69. DOI: 10.1002/jso.25908.
CLAUDON M, DIETRICH C F, CHOI B I, et al. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) in the liver: update 2012: a WFUMB-EFSUMB initiative in cooperation with representatives of AFSUMB, AIUM, ASUM, FLAUS and ICUS[J]. Ultraschall Med, 2013, 34(1): 11-29. DOI: 10.1055/s-0032-1325499.
PISCAGLIA F, LENCIONI R, SAGRINI E, et al. Characterization of focal liver lesions with contrast-enhanced ultrasound[J]. Ultrasound Med Biol, 2010, 36(4): 531-550. DOI: 10.1016/j.ultrasmedbio.2010.01.004.
FANG C, ANUPINDI S A, BACK S J, et al. Contrast-enhanced ultrasound of benign and malignant liver lesions in children[J/OL]. Pediatr Radiol, 2021, 51(12): 2181-2197 [2022-09-10]. DOI: 10.1007/s00247-021-04976-2.
NTOULIA A, ANUPINDI S A, BACK S J, et al. Contrast-enhanced ultrasound: a comprehensive review of safety in children[J/OL]. Pediatr Radiol, 2021, 51(12): 2161-2180 [2022-09-10]. DOI: 10.1007/s00247-021-05223-4.
SAWATZKI M, GULLER U, GUSEWELL S, et al. Contrast-enhanced ultrasound can guide the therapeutic strategy by improving the detection of colorectal liver metastases[J/OL]. J Hepatol, 2021, 74(2): 419-427 [2022-09-10]. DOI: 10.1016/j.jhep.2020.09.036.
TSILI A C, ALEXIOU G, NAKA C, et al. Imaging of colorectal cancer liver metastases using contrast-enhanced US, multidetector CT, MRI, and FDG PET/CT: a meta-analysis[J]. Acta Radiol, 2021, 62(3): 302-312. DOI: 10.1177/0284185120925481.
ZHANG L N, ZHANG L, WANG H, et al. Diagnostic performance of contrast-enhanced ultrasound and magnetic resonance imaging for detecting colorectal liver metastases: a systematic review and meta-analysis[J]. Dig Liver Dis, 2019, 51(9): 1241-1248. DOI: 10.1016/j.dld.2019.06.004.
CHEN J Y, DAI H Y, LI C Y, et al. Improved sensitivity and positive predictive value of contrast-enhanced intraoperative ultrasound in colorectal cancer liver metastasis: a systematic review and meta-analysis[J]. J Gastrointest Oncol, 2022, 13(1): 221-230. DOI: 10.21037/jgo-21-881.
STAVROU G A, STANG A, RAPTIS D A, et al. Intraoperative (Contrast-Enhanced) Ultrasound Has the Highest Diagnostic Accuracy of Any Imaging Modality in Resection of Colorectal Liver Metastases[J/OL]. J Gastrointest Surg, 2021, 25(12): 3160-3169 [2022-09-10]. DOI: 10.1007/s11605-021-04925-2.
CANTISANI V, GRAZHDANI H, FIORAVANTI C, et al. Liver metastases: contrast-enhanced ultrasound compared with computed tomography and magnetic resonance[J]. World J Gastroenterol, 2014, 20(29): 9998-10007. DOI: 10.3748/wjg.v20.i29.9998.
MEHDORN A S, BECKMANN J H, BRAUN F, et al. Usability of Indocyanine Green in Robot-Assisted Hepatic Surgery[J/OL]. J Clin Med, 2021, 10(3) [2022-09-08]. DOI: 10.3390/jcm10030456.
PEYRAT P, BLANC E, GUILLERMET S, et al. HEPATOFLUO: a prospective monocentric study assessing the benefits of indocyanine green (ICG) fluorescence for hepatic surgery[J]. J Surg Oncol, 2018, 117(5): 922-927. DOI: 10.1002/jso.25011.
KOSE E, KAHRAMANGIL B, AYDIN H, et al. A comparison of indocyanine green fluorescence and laparoscopic ultrasound for detection of liver tumors[J]. HPB (Oxford), 2020, 22(5): 764-769. DOI: 10.1016/j.hpb.2019.10.005.
LIM H J, CHIOW A K H, LEE L S, et al. Novel method of intraoperative liver tumour localisation with indocyanine green and near-infrared imaging[J]. Singapore Med J, 2021, 62(4): 182-189. DOI: 10.11622/smedj.2019137.
PICCOLO G, BARABINO M, PESCE A, et al. Role of indocyanine green fluorescence imaging in minimally invasive resection of colorectal liver metastases[J]. Surg Laparosc Endosc Percutan Tech, 2022, 32(2): 259-265. DOI: 10.1097/SLE.0000000000001037.
ACHTERBERG F B, SIBINGA MULDER B G, MEIJER R P J, et al. Real-time surgical margin assessment using ICG-fluorescence during laparoscopic and robot-assisted resections of colorectal liver metastases[J/OL]. Ann Transl Med, 2020, 8(21): 1448 [2022-09-08]. DOI: 10.21037/atm-20-1999.

PREV Research progress of different MRI techniques in young women breast tumors
NEXT Advances in clinical research in urologic neoplasms with machine learning-based radiomics technology

Tel & Fax: +8610-67113815    E-mail: