Skip to main content
Log in

The timing phase affected the inconsistency of APHE subtypes of liver observations in patients at risk for HCC on the multi-hepatic arterial phase imaging

  • Hepatobiliary
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

Objective

To investigate whether liver observations in patients at risk for hepatocellular carcinoma (HCC) display inconsistent arterial phase hyperenhancement (APHE) subtypes on the multi-hepatic arterial phase imaging (mHAP) and to further investigate factors affecting inconsistent APHE subtype of observations on mHAP imaging.

Methods

From April 2018 to June 2021, a total of 141 patients at high risk of HCC with 238 liver observations who underwent mHAP MRI acquisitions were consecutively included in this retrospective study. Two experienced radiologists reviewed individual arterial phase imaging independently and assessed the enhancement pattern of each liver observation according to LI-RADS. Another two experienced radiologists identified and recorded the genuine timing phase of each phase independently. When a disagreement appeared between the two radiologists, another expert participated in the discussion to get a final decision. A separate descriptive analysis was used for all observations scored APHE by the radiologists. The Kappa coefficient was used to determine the agreement between the two radiologists. Univariate analysis was performed to investigate the factors affecting inconsistent APHE subtype of liver observations on mHAP imaging.

Results

The interobserver agreement was substantial to almost perfect agreement on the assessment of timing phase (κ = 0.712-0.887) and evaluation of APHE subtype (κ = 0.795-0.901). A total of 87.8% (209/238) of the observations showed consistent nonrim APHE and 10.2% (24/238) of the observations showed consistent rim APHE on mHAP imaging. A total of 2.1% (5/238) of the liver observations were considered inconsistent APHE subtypes, and all progressed nonrim to rim on mHAP imaging. 87.9% (124/141) of the mHAP acquisitions were all arterial phases and 12.1% (17/141) of the mHAP acquisitions obtained both the arterial phase and portal venous phase. Univariate analysis was performed and found that the timing phase of mHAP imaging affected the consistency of APHE subtype of liver observations. When considering the timing phase and excluding the portal venous phase acquired by mHAP imaging, none of the liver observations showed inconsistent APHE subtypes on mHAP imaging.

Conclusion

The timing phase which mHAP acquisition contained portal venous phase affected the inconsistency of APHE subtype of liver observations on mHAP imaging. When evaluating the APHE subtype of liver observations, it’s necessary to assess the timing of each phase acquired by the mHAP technique at first.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA: a cancer journal for clinicians. 2021; 71(3):209-49. https://doi.org/10.3322/caac.21660

    Article  PubMed  Google Scholar 

  2. American College of Radiology. Available at: https://www.acr.org/Clinical-Resources/Reporting-and-Data-Systems/LI-RADS/CT-MRI-LI-RADS-v2018.

  3. Kim JH, Yoon JH, Bae JS, Park S, Han S, Lee JM. Multiarterial Phase Acquisition in Gadoxetic Acid-Enhanced Liver MRI for the Detection of Hypervascular Hepatocellular Carcinoma in High-Risk Patients: Comparison of Compressed Sensing Versus View Sharing Techniques. Investigative radiology. 2023; 58(2):139-47. https://doi.org/10.1097/rli.0000000000000910

    Article  CAS  PubMed  Google Scholar 

  4. Yoon JH, Lee JM, Yu MH, Kim EJ, Han JK. Triple Arterial Phase MR Imaging with Gadoxetic Acid Using a Combination of Contrast Enhanced Time Robust Angiography, Keyhole, and Viewsharing Techniques and Two-Dimensional Parallel Imaging in Comparison with Conventional Single Arterial Phase. Korean J Radiol. 2016; 17(4):522-32. https://doi.org/10.3348/kjr.2016.17.4.522

    Article  PubMed  PubMed Central  Google Scholar 

  5. Haradome H, Grazioli L, Tsunoo M, et al. Can MR fluoroscopic triggering technique and slow rate injection provide appropriate arterial phase images with reducing artifacts on gadoxetic acid-DTPA (Gd-EOB-DTPA)-enhanced hepatic MR imaging? Journal of magnetic resonance imaging : JMRI. 2010; 32(2):334-40. https://doi.org/10.1002/jmri.22241

    Article  PubMed  Google Scholar 

  6. Michaely HJ, Morelli JN, Budjan J, et al. CAIPIRINHA-Dixon-TWIST (CDT)-volume-interpolated breath-hold examination (VIBE): a new technique for fast time-resolved dynamic 3-dimensional imaging of the abdomen with high spatial resolution. Investigative radiology. 2013; 48(8):590-7. https://doi.org/10.1097/RLI.0b013e318289a70b

    Article  CAS  PubMed  Google Scholar 

  7. Pietryga JA, Burke LM, Marin D, Jaffe TA, Bashir MR. Respiratory motion artifact affecting hepatic arterial phase imaging with gadoxetate disodium: examination recovery with a multiple arterial phase acquisition. Radiology. 2014; 271(2):426-34. org/https://doi.org/10.1148/radiol.13131988

    Article  PubMed  Google Scholar 

  8. Saranathan M, Rettmann DW, Hargreaves BA, Clarke SE, Vasanawala SS. DIfferential Subsampling with Cartesian Ordering (DISCO): a high spatio-temporal resolution Dixon imaging sequence for multiphasic contrast enhanced abdominal imaging. Journal of magnetic resonance imaging : JMRI. 2012; 35(6):1484-92. https://doi.org/10.1002/jmri.23602

    Article  PubMed  Google Scholar 

  9. Wei Y, Deng L, Yuan Y, et al. Gadoxetate acid disodium-enhanced MRI: Multiple arterial phases using differential sub-sampling with cartesian ordering (DISCO) may achieve more optimal late arterial phases than the single arterial phase imaging. Magnetic resonance imaging. 2019; 61:116-23. https://doi.org/10.1016/j.mri.2019.05.033

    Article  PubMed  Google Scholar 

  10. Ikram NS, Yee J, Weinstein S, et al. Multiple arterial phase MRI of arterial hypervascular hepatic lesions: improved arterial phase capture and lesion enhancement. Abdominal radiology (New York). 2017; 42(3):870-6. https://doi.org/10.1007/s00261-016-0948-8

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kazmierczak PM, Theisen D, Thierfelder KM, et al. Improved detection of hypervascular liver lesions with CAIPIRINHA-Dixon-TWIST-volume-interpolated breath-hold examination. Investigative radiology. 2015; 50(3):153-60. https://doi.org/10.1097/rli.0000000000000118

    Article  PubMed  Google Scholar 

  12. Qu J, Han S, Zhang H, et al. Improved Detection of Recurrent Hepatocellular Carcinomas in Arterial Phase With CAIPIRINHA-Dixon-TWIST-Volumetric Interpolated Breath-Hold Examination. Investigative radiology. 2016; 51(10):602-8. https://doi.org/10.1097/rli.0000000000000281

    Article  CAS  PubMed  Google Scholar 

  13. Qu J, Han S, Zhang H, et al. Arterial Phase with CAIPIRINHA-Dixon-TWIST (CDT)-Volume-Interpolated Breath-Hold Examination (VIBE) in Detecting Hepatic Metastases. Translational oncology. 2017; 10(1):46-53. https://doi.org/10.1016/j.tranon.2016.11.005

    Article  PubMed  Google Scholar 

  14. Hong S, Choi SH, Hong SB, Kim SY, Lee SS. Clinical usefulness of multiple arterial-phase images in gadoxetate disodium-enhanced magnetic resonance imaging: a systematic review and meta-analysis. European radiology. 2022; 32(8):5413-23. https://doi.org/10.1007/s00330-022-08620-x

    Article  PubMed  Google Scholar 

  15. Cunha GM, Hasenstab KA, Delgado T, et al. Multi-arterial phase MRI depicts inconsistent arterial phase hyperenhancement (APHE) subtypes in liver observations of patients at risk for hepatocellular carcinoma. European radiology. 2021; 31(10):7594-604. https://doi.org/10.1007/s00330-021-07924-8

    Article  PubMed  Google Scholar 

  16. Sofue K, Marin D, Jaffe TA, Nelson RC, Bashir MR. Can combining triple-arterial phase acquisition with fluoroscopic triggering provide both optimal early and late hepatic arterial phase images during gadoxetic acid-enhanced MRI? Journal of magnetic resonance imaging : JMRI. 2016; 43(5):1073-81. https://doi.org/10.1002/jmri.25079

    Article  PubMed  Google Scholar 

  17. EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. J Hepatol. 2018; 69(1):182-236. https://doi.org/10.1016/j.jhep.2018.03.019

    Article  Google Scholar 

  18. Narsinh KH, Cui J, Papadatos D, Sirlin CB, Santillan CS. Hepatocarcinogenesis and LI-RADS. Abdominal radiology (New York). 2018; 43(1):158-68. https://doi.org/10.1007/s00261-017-1409-8

    Article  PubMed  Google Scholar 

  19. Villanueva A. Hepatocellular Carcinoma. The New England journal of medicine. 2019; 380(15):1450-62. https://doi.org/10.1056/NEJMra1713263

    Article  CAS  PubMed  Google Scholar 

  20. Francis IR, Cohan RH, McNulty NJ, et al. Multidetector CT of the liver and hepatic neoplasms: effect of multiphasic imaging on tumor conspicuity and vascular enhancement. AJR Am J Roentgenol. 2003; 180(5):1217-24. https://doi.org/10.2214/ajr.180.5.1801217

    Article  PubMed  Google Scholar 

  21. Kim SK, Lim JH, Lee WJ, et al. Detection of hepatocellular carcinoma: comparison of dynamic three-phase computed tomography images and four-phase computed tomography images using multidetector row helical computed tomography. Journal of Computer Assisted Tomography. 2002; 26(5):691-8. https://doi.org/10.1097/00004728-200209000-00005

    Article  PubMed  Google Scholar 

  22. Gatti M, Calandri M, Bergamasco L, et al. Characterization of the arterial enhancement pattern of focal liver lesions by multiple arterial phase magnetic resonance imaging: comparison between hepatocellular carcinoma and focal nodular hyperplasia. La Radiologia medica. 2020; 125(4):348-55. https://doi.org/10.1007/s11547-019-01127-4

    Article  PubMed  Google Scholar 

  23. Laghi A, Iannaccone R, Rossi P, et al. Hepatocellular carcinoma: detection with triple-phase multi-detector row helical CT in patients with chronic hepatitis. Radiology. 2003; 226(2):543-9. https://doi.org/10.1148/radiol.2262012043

    Article  PubMed  Google Scholar 

  24. Ichikawa T, Kitamura T, Nakajima H, et al. Hypervascular hepatocellular carcinoma: can double arterial phase imaging with multidetector CT improve tumor depiction in the cirrhotic liver? AJR Am J Roentgenol. 2002; 179(3):751-8. https://doi.org/10.2214/ajr.179.3.1790751

    Article  PubMed  Google Scholar 

  25. Shetty AS, Fraum TJ, Ludwig DR, et al. Body MRI: Imaging Protocols, Techniques, and Lessons Learned. Radiographics : a review publication of the Radiological Society of North America, Inc. 2022; 42(7):2054-74. https://doi.org/10.1148/rg.220025

    Article  PubMed  Google Scholar 

  26. Kambadakone AR, Fung A, Gupta RT, et al. LI-RADS technical requirements for CT, MRI, and contrast-enhanced ultrasound. Abdominal radiology (New York). 2018; 43(1):56-74. https://doi.org/10.1007/s00261-017-1325-y

    Article  PubMed  Google Scholar 

  27. Park YS, Lee CH, Kim JW, Lee YS, Paek M, Kim KA. Application of High-Speed T1 Sequences for High-Quality Hepatic Arterial Phase Magnetic Resonance Imaging: Intraindividual Comparison of Single and Multiple Arterial Phases. Investigative radiology. 2017; 52(10):605-11. https://doi.org/10.1097/rli.0000000000000378

    Article  PubMed  Google Scholar 

  28. Ito K, Fujita T, Shimizu A, et al. Multiarterial phase dynamic MRI of small early enhancing hepatic lesions in cirrhosis or chronic hepatitis: differentiating between hypervascular hepatocellular carcinomas and pseudolesions. AJR Am J Roentgenol. 2004; 183(3):699-705. https://doi.org/10.2214/ajr.183.3.1830699

    Article  PubMed  Google Scholar 

  29. Lim JH, Choi D, Kim SH, et al. Detection of hepatocellular carcinoma: value of adding delayed phase imaging to dual-phase helical CT. AJR Am J Roentgenol. 2002; 179(1):67-73. https://doi.org/10.2214/ajr.179.1.1790067

    Article  PubMed  Google Scholar 

  30. Monzawa S, Ichikawa T, Nakajima H, Kitanaka Y, Omata K, Araki T. Dynamic CT for detecting small hepatocellular carcinoma: usefulness of delayed phase imaging. AJR Am J Roentgenol. 2007; 188(1):147-53. https://doi.org/10.2214/ajr.05.0512

    Article  PubMed  Google Scholar 

  31. Lee SE, An C, Hwang SH, Choi JY, Han K, Kim MJ. Extracellular contrast agent-enhanced MRI: 15-min delayed phase may improve the diagnostic performance for hepatocellular carcinoma in patients with chronic liver disease. European radiology. 2018; 28(4):1551-9. https://doi.org/10.1007/s00330-017-5119-y

    Article  PubMed  Google Scholar 

  32. Choi JY, Lee JM, Sirlin CB. CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part I. Development, growth, and spread: key pathologic and imaging aspects. Radiology. 2014; 272(3):635-54. https://doi.org/10.1148/radiol.14132361

    Article  PubMed  Google Scholar 

  33. Choi JY, Lee JM, Sirlin CB. CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part II. Extracellular agents, hepatobiliary agents, and ancillary imaging features. Radiology. 2014; 273(1):30-50. https://doi.org/10.1148/radiol.14132362

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (No.82071876, 82372043, 61871276, and 62171298) and Beijing Municipal Administration of Hospitals’ Youth Programme (QML20200108); Beijing Hospitals Authority Clinical Medicine Development of Special Funding Support (ZYLX202101).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Zhenghan Yang or Hui Xu.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 15 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, J., Yang, D., Yang, Z. et al. The timing phase affected the inconsistency of APHE subtypes of liver observations in patients at risk for HCC on the multi-hepatic arterial phase imaging. Abdom Radiol 49, 1092–1102 (2024). https://doi.org/10.1007/s00261-023-04096-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00261-023-04096-5

Keywords

Navigation