Skip to main content
SpringerLink
Log in

Liver MRI with amide proton transfer imaging: feasibility and accuracy for the characterization of focal liver lesions

  • Gastrointestinal
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objective

To investigate the feasibility of using amide proton transfer (APT) magnetic resonance imaging (MRI) in the liver and to evaluate its ability to characterize focal liver lesions (FLLs).

Methods

A total of 203 patients with suspected FLLs who underwent APT imaging at 3T were included. APT imaging was obtained using a single-slice turbo spin-echo sequence to include FLLs through five breath-holds, and its acquisition time was approximately 1 min. APT signals in the background liver and FLL were measured with magnetization transfer ratio asymmetry (MTRasym) at 3.5 ppm. The technical success rate of APT imaging and the reasons for failure to obtain meaningful MTRasym values were assessed. The Mann Whitney U test was used to compare MTRasym values between different FLLs.

Results

The technical success rate of APT imaging in the liver was 62.1% (126/203). The reasons for failure were a too large B0 inhomogeneity (n = 43), significant respiratory motion (n = 12), and these two factors together (n = 22), respectively. Among 59 FLLs with analyzable APT images, MTRasym values were compared between 27 patients with liver metastases and 23 patients with hepatocellular carcinomas (HCCs). The MTRasym values of metastases were significantly higher than those of HCC (0.13 ± 2.15% vs. − 1.41 ± 3.68%, p = 0.027).

Conclusions

APT imaging could be an imaging biomarker for the differentiation of FLLs. However, further technical improvement is required before APT imaging can be clinically applied to liver MRI.

Key Points

• Liver APT imaging was technically feasible, but with a relatively low success rate (62.1%).

• Liver metastases showed higher APT values than hepatocellular carcinomas.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

APT:

Amide proton transfer

CEST:

Chemical exchange saturation transfer

CoV:

Coefficient of variation

FLL:

Focal liver lesion

FNH:

Focal nodular hyperplasia

HCC:

Hepatocellular carcinoma

MRI:

Magnetic resonance imaging

MTR asym :

Magnetization transfer ratio asymmetry

RF:

Radiofrequency

ROI:

Region of interest

TSE:

Turbo spin-echo

References

  1. van Zijl PC, Yadav NN (2011) Chemical exchange saturation transfer (CEST): what is in a name and what isn’t? Magn Reson Med 65:927–948

    PubMed  PubMed Central  Google Scholar 

  2. Ward KM, Aletras AH, Balaban RS (2000) A new class of contrast agents for MRI based on proton chemical exchange dependent saturation transfer (CEST). J Magn Reson 143:79–87

    CAS  PubMed  Google Scholar 

  3. Zhou J, Payen JF, Wilson DA, Traystman RJ, van Zijl PC (2003) Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat Med 9:1085–1090

    CAS  PubMed  Google Scholar 

  4. Jones KM, Pollard AC, Pagel MD (2018) Clinical applications of chemical exchange saturation transfer (CEST) MRI. J Magn Reson Imaging 47:11–27

    PubMed  Google Scholar 

  5. Park JE, Lee JY, Kim HS et al (2018) Amide proton transfer imaging seems to provide higher diagnostic performance in post-treatment high-grade gliomas than methionine positron emission tomography. Eur Radiol 28:3285–3295

    PubMed  Google Scholar 

  6. Jeong HK, Han K, Zhou J et al (2017) Characterizing amide proton transfer imaging in haemorrhage brain lesions using 3T MRI. Eur Radiol 27:1577–1584

    PubMed  Google Scholar 

  7. Jones CK, Schlosser MJ, van Zijl PC, Pomper MG, Golay X, Zhou J (2006) Amide proton transfer imaging of human brain tumors at 3T. Magn Reson Med 56:585–592

    PubMed  Google Scholar 

  8. Joo B, Han K, Choi YS et al (2018) Amide proton transfer imaging for differentiation of benign and atypical meningiomas. Eur Radiol 28:331–339

    PubMed  Google Scholar 

  9. Zhou J, Heo HY, Knutsson L, van Zijl PCM, Jiang S (2019) APT-weighted MRI: techniques, current neuro applications, and challenging issues. J Magn Reson Imaging 50:347–364

    PubMed  PubMed Central  Google Scholar 

  10. Deng M, Chen SZ, Yuan J, Chan Q, Zhou J, Wang YX (2016) Chemical exchange saturation transfer (CEST) MR technique for liver imaging at 3.0 Tesla: an evaluation of different offset number and an after-meal and over-night-fast comparison. Mol Imaging Biol 18:274–282

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Chen SZ, Yuan J, Deng M, Wei J, Zhou J, Wang YX (2016) Chemical exchange saturation transfer (CEST) MR technique for in-vivo liver imaging at 3.0 tesla. Eur Radiol 26:1792–1800

    PubMed  Google Scholar 

  12. Lin Y, Luo X, Yu L et al (2019) Amide proton transfer-weighted MRI for predicting histological grade of hepatocellular carcinoma: comparison with diffusion-weighted imaging. Quant Imaging Med Surg 9:1641–1651

    PubMed  PubMed Central  Google Scholar 

  13. Choi YS, Ahn SS, Lee SK et al (2017) Amide proton transfer imaging to discriminate between low- and high-grade gliomas: added value to apparent diffusion coefficient and relative cerebral blood volume. Eur Radiol 27:3181–3189

    PubMed  PubMed Central  Google Scholar 

  14. Zhou J, Lal B, Wilson DA, Laterra J, van Zijl PC (2003) Amide proton transfer (APT) contrast for imaging of brain tumors. Magn Reson Med 50:1120–1126

    PubMed  Google Scholar 

  15. Chung SR, Lee SS, Kim N et al (2015) Intravoxel incoherent motion MRI for liver fibrosis assessment: a pilot study. Acta Radiol 56:1428–1436

    PubMed  Google Scholar 

  16. Kim HC, Seo N, Chung YE, Park MS, Choi JY, Kim MJ (2019) Characterization of focal liver lesions using the stretched exponential model: comparison with monoexponential and biexponential diffusion-weighted magnetic resonance imaging. Eur Radiol 29:5111–5120

    PubMed  Google Scholar 

  17. Danet IM, Semelka RC, Leonardou P et al (2003) Spectrum of MRI appearances of untreated metastases of the liver. AJR Am J Roentgenol 181:809–817

    PubMed  Google Scholar 

  18. Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology 53:1020–1022

    PubMed  PubMed Central  Google Scholar 

  19. Seale MK, Catalano OA, Saini S, Hahn PF, Sahani DV (2009) Hepatobiliary-specific MR contrast agents: role in imaging the liver and biliary tree. Radiographics 29:1725–1748

    PubMed  Google Scholar 

  20. Zhou J (2011) Amide proton transfer imaging of the human brain. Methods Mol Biol 711:227–237

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhu H, Jones CK, van Zijl PC, Barker PB, Zhou J (2010) Fast 3D chemical exchange saturation transfer (CEST) imaging of the human brain. Magn Reson Med 64:638–644

    PubMed  PubMed Central  Google Scholar 

  22. Zhou J, Zhu H, Lim M et al (2013) Three-dimensional amide proton transfer MR imaging of gliomas: initial experience and comparison with gadolinium enhancement. J Magn Reson Imaging 38:1119–1128

    PubMed  Google Scholar 

  23. Wen Z, Hu S, Huang F et al (2010) MR imaging of high-grade brain tumors using endogenous protein and peptide-based contrast. Neuroimage 51:616–622

    PubMed  PubMed Central  Google Scholar 

  24. Zhou J, Blakeley JO, Hua J et al (2008) Practical data acquisition method for human brain tumor amide proton transfer (APT) imaging. Magn Reson Med 60:842–849

    PubMed  PubMed Central  Google Scholar 

  25. Yuan J, Chen S, King AD et al (2014) Amide proton transfer-weighted imaging of the head and neck at 3 T: a feasibility study on healthy human subjects and patients with head and neck cancer. NMR Biomed 27:1239–1247

    PubMed  PubMed Central  Google Scholar 

  26. Wei W, Jia G, Flanigan D, Zhou J, Knopp MV (2014) Chemical exchange saturation transfer MR imaging of articular cartilage glycosaminoglycans at 3 T: accuracy of B0 field inhomogeneity corrections with gradient echo method. Magn Reson Imaging 32:41–47

    CAS  PubMed  Google Scholar 

  27. Kuai ZX, Sang XQ, Yao YF, Chu CY, Zhu YM (2019) Evaluation of non-monoexponential diffusion models for hepatocellular carcinoma using b values up to 2000 s/mm(2): a short-term repeatability study. J Magn Reson Imaging 50:297–304

    PubMed  Google Scholar 

  28. Barnhart HX, Barboriak DP (2009) Applications of the repeatability of quantitative imaging biomarkers: a review of statistical analysis of repeat data sets. Transl Oncol 2:231–235

    PubMed  PubMed Central  Google Scholar 

  29. Hallgren KA (2012) Computing inter-rater reliability for observational data: an overview and tutorial. Tutor Quant Methods Psychol 8:23–34

    PubMed  PubMed Central  Google Scholar 

  30. Sun PZ, Benner T, Kumar A, Sorensen AG (2008) Investigation of optimizing and translating pH-sensitive pulsed-chemical exchange saturation transfer (CEST) imaging to a 3T clinical scanner. Magn Reson Med 60:834–841

    PubMed  Google Scholar 

  31. Kim J, Wu Y, Guo Y, Zheng H, Sun PZ (2015) A review of optimization and quantification techniques for chemical exchange saturation transfer MRI toward sensitive in vivo imaging. Contrast Media Mol Imaging 10:163–178

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Wang QB, Zhu H, Liu HL, Zhang B (2012) Performance of magnetic resonance elastography and diffusion-weighted imaging for the staging of hepatic fibrosis: a meta-analysis. Hepatology 56:239–247

    PubMed  Google Scholar 

  33. Lee JB, Park JE, Jung SC et al (2020) Repeatability of amide proton transfer-weighted signals in the brain according to clinical condition and anatomical location. Eur Radiol 30:346–356

    PubMed  Google Scholar 

  34. Feng L, Benkert T, Block KT, Sodickson DK, Otazo R, Chandarana H (2017) Compressed sensing for body MRI. J Magn Reson Imaging 45:966–987

    PubMed  Google Scholar 

  35. Heo HY, Zhang Y, Lee DH, Jiang S, Zhao X, Zhou J (2017) Accelerating chemical exchange saturation transfer (CEST) MRI by combining compressed sensing and sensitivity encoding techniques. Magn Reson Med 77:779–786

    CAS  PubMed  Google Scholar 

  36. Seo N, Chung YE, Park YN, Kim E, Hwang J, Kim MJ (2018) Liver fibrosis: stretched exponential model outperforms mono-exponential and bi-exponential models of diffusion-weighted MRI. Eur Radiol 28:2812–2822

    PubMed  Google Scholar 

  37. Ohno Y, Yui M, Koyama H et al (2016) Chemical exchange saturation transfer MR imaging: preliminary results for differentiation of malignant and benign thoracic lesions. Radiology 279:578–589

    PubMed  Google Scholar 

  38. Nishie A, Asayama Y, Ishigami K et al (2019) Amide proton transfer imaging to predict tumor response to neoadjuvant chemotherapy in locally advanced rectal cancer. J Gastroenterol Hepatol 34:140–146

    CAS  PubMed  Google Scholar 

  39. Ray KJ, Simard MA, Larkin JR et al (2019) Tumor pH and protein concentration contribute to the signal of amide proton transfer magnetic resonance imaging. Cancer Res 79:1343–1352

    CAS  PubMed  PubMed Central  Google Scholar 

  40. van Zijl PC, Zhou J, Mori N, Payen JF, Wilson D, Mori S (2003) Mechanism of magnetization transfer during on-resonance water saturation. A new approach to detect mobile proteins, peptides, and lipids. Magn Reson Med 49:440–449

    PubMed  Google Scholar 

  41. Heo HY, Xu X, Jiang S et al (2019) Prospective acceleration of parallel RF transmission-based 3D chemical exchange saturation transfer imaging with compressed sensing. Magn Reson Med 82:1812–1821

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The authors state that this work has not received any funding.

Author information

Author notes

  1. Ha-Kyu Jeong

    Present address: Clinical Research Group, Business of Healthcare and Medical Equipment, Samsung Electronics Co., Ltd., Suwon-si, South Korea

Authors and Affiliations

  1. Department of Radiology, Severance Hospital, Yonsei University College of Medicine, 50-1 Yonsei-ro, Seodaemun-gu, Seoul, 03722, South Korea

    Nieun Seo, Jin-Young Choi, Mi-Suk Park, Myeong-Jin Kim & Yong Eun Chung

  2. Clinical Science MR, Philips Healthcare, Seoul, South Korea

    Ha-Kyu Jeong

Authors
  1. Nieun Seo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ha-Kyu Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jin-Young Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mi-Suk Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Myeong-Jin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yong Eun Chung
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yong Eun Chung.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Yong Eun Chung.

Conflict of interest

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.

Statistics and biometry

Nieun Seo performed statistical analysis, who is one of the coauthors.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• diagnostic or prognostic study

• performed at one institution

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 516 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seo, N., Jeong, HK., Choi, JY. et al. Liver MRI with amide proton transfer imaging: feasibility and accuracy for the characterization of focal liver lesions. Eur Radiol 31, 222–231 (2021). https://doi.org/10.1007/s00330-020-07122-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-020-07122-y

Keywords

Search

Navigation