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Open Access 12-04-2024 | Hepatobiliary

Combining T1rho and advanced diffusion MRI for noninvasively staging liver fibrosis: an experimental study in rats

Authors: Yiwan Guo, Tingting Guo, Chen Huang, Peng Sun, Zhigang Wu, Ziwei Jin, Chuansheng Zheng, Xin Li

Published in: Abdominal Radiology

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Abstract

Purpose

To investigate the value of imaging parameters derived from T1 relaxation times in the rotating frame (T1ρ or T1rho), diffusion kurtosis imaging (DKI) and intravoxel incoherent motion (IVIM) in assessment of liver fibrosis in rats and propose an optimal diagnostic model based on multiparametric MRI.

Methods

Thirty rats were divided into one control group and four fibrosis experimental groups (n = 6 for each group). Liver fibrosis was induced by administering thioacetamide (TAA) for 2, 4, 6, and 8 weeks. T1ρ, mean kurtosis (MK), mean diffusivity (MD), perfusion fraction (f), true diffusion coefficient (D), and pseudo-diffusion coefficient (D*) were measured and compared among different fibrosis stages. An optimal diagnostic model was established and the diagnostic efficiency was evaluated by receiver operating characteristic (ROC) curve analysis.

Results

The mean AUC values, sensitivity, and specificity of T1ρ and MD derived from DKI across all liver fibrosis stages were comparable but much higher than those of other imaging parameters (0.954, 92.46, 91.85 for T1ρ; 0.949, 92.52, 91.24 for MD). The model combining T1ρ and MD exhibited better diagnostic performance with higher AUC values than any individual method for staging liver fibrosis (≥ F1: 1.000 (0.884–1.000); ≥ F2: 0.935 (0.782–0.992); ≥ F3: 0.982 (0.852–1.000); F4: 0.986 (0.859–1.000)).

Conclusion

Among the evaluated imaging parameters, T1ρ and MD were superior for differentiating varying liver fibrosis stages. The model combining T1ρ and MD was promising to be a credible diagnostic biomarker to detect and accurately stage liver fibrosis.

Graphical abstract

Literature
1.
go back to reference Parola M, Pinzani M. Liver fibrosis: Pathophysiology, pathogenetic targets and clinical issues. Mol Aspects Med. 2019;65:37-55CrossRefPubMed Parola M, Pinzani M. Liver fibrosis: Pathophysiology, pathogenetic targets and clinical issues. Mol Aspects Med. 2019;65:37-55CrossRefPubMed
2.
3.
4.
go back to reference Kisseleva T, Brenner D. Molecular and cellular mechanisms of liver fibrosis and its regression. Nat Rev Gastroenterol Hepatol. 2021;18(3):151-166CrossRefPubMed Kisseleva T, Brenner D. Molecular and cellular mechanisms of liver fibrosis and its regression. Nat Rev Gastroenterol Hepatol. 2021;18(3):151-166CrossRefPubMed
5.
go back to reference Tapper EB, Lok AS. Use of Liver Imaging and Biopsy in Clinical Practice. N Engl J Med. 2017;377(8):756-768CrossRefPubMed Tapper EB, Lok AS. Use of Liver Imaging and Biopsy in Clinical Practice. N Engl J Med. 2017;377(8):756-768CrossRefPubMed
6.
go back to reference Srinivasa Babu A, Wells ML, Teytelboym OM, et al. Elastography in Chronic Liver Disease: Modalities, Techniques, Limitations, and Future Directions. Radiographics. 2016;36(7):1987-2006CrossRefPubMed Srinivasa Babu A, Wells ML, Teytelboym OM, et al. Elastography in Chronic Liver Disease: Modalities, Techniques, Limitations, and Future Directions. Radiographics. 2016;36(7):1987-2006CrossRefPubMed
7.
go back to reference Kotowski K, Kucharski D, Machura B, et al. Detecting liver cirrhosis in computed tomography scans using clinically-inspired and radiomic features. Comput Biol Med. 2023;152:106378CrossRefPubMed Kotowski K, Kucharski D, Machura B, et al. Detecting liver cirrhosis in computed tomography scans using clinically-inspired and radiomic features. Comput Biol Med. 2023;152:106378CrossRefPubMed
8.
go back to reference Singh S, Venkatesh SK, Wang Z, et al. Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol. 2015;13(3):440-451.e6CrossRefPubMed Singh S, Venkatesh SK, Wang Z, et al. Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol. 2015;13(3):440-451.e6CrossRefPubMed
9.
go back to reference Le Bihan D, Ichikawa S, Motosugi U. Diffusion and Intravoxel Incoherent Motion MR Imaging-based Virtual Elastography: A Hypothesis-generating Study in the Liver. Radiology. 2017;285(2):609-619CrossRefPubMed Le Bihan D, Ichikawa S, Motosugi U. Diffusion and Intravoxel Incoherent Motion MR Imaging-based Virtual Elastography: A Hypothesis-generating Study in the Liver. Radiology. 2017;285(2):609-619CrossRefPubMed
10.
go back to reference Shi Y, Qi YF, Lan GY, et al. Three-dimensional MR Elastography Depicts Liver Inflammation, Fibrosis, and Portal Hypertension in Chronic Hepatitis B or C. Radiology. 2021;301(1):154-162CrossRefPubMed Shi Y, Qi YF, Lan GY, et al. Three-dimensional MR Elastography Depicts Liver Inflammation, Fibrosis, and Portal Hypertension in Chronic Hepatitis B or C. Radiology. 2021;301(1):154-162CrossRefPubMed
11.
go back to reference Seo N, Chung YE, Park YN, et al. Liver fibrosis: stretched exponential model outperforms mono-exponential and bi-exponential models of diffusion-weighted MRI. Eur Radiol. 2018;28(7):2812-2822CrossRefPubMed Seo N, Chung YE, Park YN, et al. Liver fibrosis: stretched exponential model outperforms mono-exponential and bi-exponential models of diffusion-weighted MRI. Eur Radiol. 2018;28(7):2812-2822CrossRefPubMed
12.
go back to reference Lu Y, Wang Q, Zhang T, et al. Staging Liver Fibrosis: Comparison of Native T1 Mapping, T2 Mapping, and T1ρ: An Experimental Study in Rats With Bile Duct Ligation and Carbon Tetrachloride at 11.7 T MRI. J Magn Reson Imaging. 2022;55(2):507-517CrossRefPubMed Lu Y, Wang Q, Zhang T, et al. Staging Liver Fibrosis: Comparison of Native T1 Mapping, T2 Mapping, and T1ρ: An Experimental Study in Rats With Bile Duct Ligation and Carbon Tetrachloride at 11.7 T MRI. J Magn Reson Imaging. 2022;55(2):507-517CrossRefPubMed
13.
go back to reference Tosun M, Onal T, Uslu H, et al. Intravoxel incoherent motion imaging for diagnosing and staging the liver fibrosis and inflammation. Abdom Radiol (NY). 2020;45(1):15-23CrossRefPubMed Tosun M, Onal T, Uslu H, et al. Intravoxel incoherent motion imaging for diagnosing and staging the liver fibrosis and inflammation. Abdom Radiol (NY). 2020;45(1):15-23CrossRefPubMed
14.
go back to reference Sheng RF, Jin KP, Yang L, et al. Histogram Analysis of Diffusion Kurtosis Magnetic Resonance Imaging for Diagnosis of Hepatic Fibrosis. Korean J Radiol. 2018;19(5):916-922CrossRefPubMedPubMedCentral Sheng RF, Jin KP, Yang L, et al. Histogram Analysis of Diffusion Kurtosis Magnetic Resonance Imaging for Diagnosis of Hepatic Fibrosis. Korean J Radiol. 2018;19(5):916-922CrossRefPubMedPubMedCentral
15.
go back to reference Yang L, Rao S, Wang W, et al. Staging liver fibrosis with DWI: is there an added value for diffusion kurtosis imaging?. Eur Radiol. 2018;28(7):3041-3049CrossRefPubMed Yang L, Rao S, Wang W, et al. Staging liver fibrosis with DWI: is there an added value for diffusion kurtosis imaging?. Eur Radiol. 2018;28(7):3041-3049CrossRefPubMed
16.
17.
go back to reference Petitclerc L, Sebastiani G, Gilbert G, et al. Liver fibrosis: Review of current imaging and MRI quantification techniques. J Magn Reson Imaging. 2017;45(5):1276-1295CrossRefPubMed Petitclerc L, Sebastiani G, Gilbert G, et al. Liver fibrosis: Review of current imaging and MRI quantification techniques. J Magn Reson Imaging. 2017;45(5):1276-1295CrossRefPubMed
18.
go back to reference Vilaseca M, García-Calderó H, Lafoz E, et al. The anticoagulant rivaroxaban lowers portal hypertension in cirrhotic rats mainly by deactivating hepatic stellate cells. Hepatology. 2017;65(6):2031-2044CrossRefPubMed Vilaseca M, García-Calderó H, Lafoz E, et al. The anticoagulant rivaroxaban lowers portal hypertension in cirrhotic rats mainly by deactivating hepatic stellate cells. Hepatology. 2017;65(6):2031-2044CrossRefPubMed
19.
go back to reference Zhang X, Guo Q, Shi Y, et al. 99mTc-3PRGD2 scintigraphy to stage liver fibrosis and evaluate reversal after fibrotic stimulus withdrawn. Nucl Med Biol. 2017;49:44-49CrossRefPubMed Zhang X, Guo Q, Shi Y, et al. 99mTc-3PRGD2 scintigraphy to stage liver fibrosis and evaluate reversal after fibrotic stimulus withdrawn. Nucl Med Biol. 2017;49:44-49CrossRefPubMed
20.
go back to reference Sheng RF, Wang HQ, Yang L, et al. Diffusion kurtosis imaging and diffusion-weighted imaging in assessment of liver fibrosis stage and necroinflammatory activity. Abdom Radiol (NY). 2017;42(4):1176-1182CrossRefPubMed Sheng RF, Wang HQ, Yang L, et al. Diffusion kurtosis imaging and diffusion-weighted imaging in assessment of liver fibrosis stage and necroinflammatory activity. Abdom Radiol (NY). 2017;42(4):1176-1182CrossRefPubMed
21.
go back to reference Lv J, Xu Y, Xu L, et al. Quantitative Functional Evaluation of Liver Fibrosis in Mice with Dynamic Contrast-enhanced Photoacoustic Imaging. Radiology. 2021;300(1):89-97CrossRefPubMed Lv J, Xu Y, Xu L, et al. Quantitative Functional Evaluation of Liver Fibrosis in Mice with Dynamic Contrast-enhanced Photoacoustic Imaging. Radiology. 2021;300(1):89-97CrossRefPubMed
22.
go back to reference Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology. 1996;24(2):289-293 Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology. 1996;24(2):289-293
24.
go back to reference Anstee QM, Reeves HL, Kotsiliti E, et al. From NASH to HCC: current concepts and future challenges. Nat Rev Gastroenterol Hepatol. 2019;16(7):411-428CrossRefPubMed Anstee QM, Reeves HL, Kotsiliti E, et al. From NASH to HCC: current concepts and future challenges. Nat Rev Gastroenterol Hepatol. 2019;16(7):411-428CrossRefPubMed
25.
go back to reference Takayama Y, Nishie A, Ishimatsu K, et al. Diagnostic potential of T1ρ and T2 relaxations in assessing the severity of liver fibrosis and necro-inflammation. Magn Reson Imaging. 2022;87:104-112CrossRefPubMed Takayama Y, Nishie A, Ishimatsu K, et al. Diagnostic potential of T1ρ and T2 relaxations in assessing the severity of liver fibrosis and necro-inflammation. Magn Reson Imaging. 2022;87:104-112CrossRefPubMed
26.
go back to reference Wáng YX, Zhang Q, Li X, Chen W, Ahuja A, Yuan J. T1ρ magnetic resonance: basic physics principles and applications in knee and intervertebral disc imaging. Quant Imaging Med Surg. 2015;5(6):858-885PubMedPubMedCentral Wáng YX, Zhang Q, Li X, Chen W, Ahuja A, Yuan J. T1ρ magnetic resonance: basic physics principles and applications in knee and intervertebral disc imaging. Quant Imaging Med Surg. 2015;5(6):858-885PubMedPubMedCentral
27.
go back to reference Dixon WT, Oshinski JN, Trudeau JD, Arnold BC, Pettigrew RI. Myocardial suppression in vivo by spin locking with composite pulses. Magn Reson Med. 1996;36(1):90-94CrossRefPubMed Dixon WT, Oshinski JN, Trudeau JD, Arnold BC, Pettigrew RI. Myocardial suppression in vivo by spin locking with composite pulses. Magn Reson Med. 1996;36(1):90-94CrossRefPubMed
28.
go back to reference Kettunen MI, Sierra A, Närväinen MJ, et al. Low spin-lock field T1 relaxation in the rotating frame as a sensitive MR imaging marker for gene therapy treatment response in rat glioma. Radiology. 2007;243(3):796-803CrossRefPubMed Kettunen MI, Sierra A, Närväinen MJ, et al. Low spin-lock field T1 relaxation in the rotating frame as a sensitive MR imaging marker for gene therapy treatment response in rat glioma. Radiology. 2007;243(3):796-803CrossRefPubMed
29.
go back to reference Togao O, Keupp J, Hiwatashi A, et al. Amide proton transfer imaging of brain tumors using a self-corrected 3D fast spin-echo dixon method: Comparison With separate B0 correction. Magn Reson Med. 2017;77(6):2272-2279CrossRefPubMed Togao O, Keupp J, Hiwatashi A, et al. Amide proton transfer imaging of brain tumors using a self-corrected 3D fast spin-echo dixon method: Comparison With separate B0 correction. Magn Reson Med. 2017;77(6):2272-2279CrossRefPubMed
30.
go back to reference Rosenkrantz AB, Padhani AR, Chenevert TL, et al. Body diffusion kurtosis imaging: Basic principles, applications, and considerations for clinical practice. J Magn Reson Imaging. 2015;42(5):1190-1202CrossRefPubMed Rosenkrantz AB, Padhani AR, Chenevert TL, et al. Body diffusion kurtosis imaging: Basic principles, applications, and considerations for clinical practice. J Magn Reson Imaging. 2015;42(5):1190-1202CrossRefPubMed
31.
go back to reference Granata V, Fusco R, Belli A, et al. Diffusion weighted imaging and diffusion kurtosis imaging in abdominal oncological setting: why and when. Infect Agent Cancer. 2022;17(1):25CrossRefPubMedPubMedCentral Granata V, Fusco R, Belli A, et al. Diffusion weighted imaging and diffusion kurtosis imaging in abdominal oncological setting: why and when. Infect Agent Cancer. 2022;17(1):25CrossRefPubMedPubMedCentral
32.
go back to reference Cheng Z, Yang Q, He H, et al. Intravoxel incoherent motion diffusion-weighted imaging and shear wave elastography for evaluating peritumoral liver fibrosis after transarterial chemoembolization in a VX2 rabbit liver tumor model. Front Physiol. 2022;13:893925CrossRefPubMedPubMedCentral Cheng Z, Yang Q, He H, et al. Intravoxel incoherent motion diffusion-weighted imaging and shear wave elastography for evaluating peritumoral liver fibrosis after transarterial chemoembolization in a VX2 rabbit liver tumor model. Front Physiol. 2022;13:893925CrossRefPubMedPubMedCentral
33.
go back to reference Ma Y, Dong D, Gong Z, et al. Novel imaging-based approaches for predicting the hepatic venous pressure gradient in a porcine model of liver cirrhosis and portal hypertension. Life Sci. 2021;264:118710CrossRefPubMed Ma Y, Dong D, Gong Z, et al. Novel imaging-based approaches for predicting the hepatic venous pressure gradient in a porcine model of liver cirrhosis and portal hypertension. Life Sci. 2021;264:118710CrossRefPubMed
34.
go back to reference Ye Z, Wei Y, Chen J, et al. Value of intravoxel incoherent motion in detecting and staging liver fibrosis: A meta-analysis. World J Gastroenterol. 2020;26(23):3304-3317CrossRefPubMedPubMedCentral Ye Z, Wei Y, Chen J, et al. Value of intravoxel incoherent motion in detecting and staging liver fibrosis: A meta-analysis. World J Gastroenterol. 2020;26(23):3304-3317CrossRefPubMedPubMedCentral
35.
go back to reference Liu B, Zeng Q, Huang J, et al. IVIM using convolutional neural networks predicts microvascular invasion in HCC. Eur Radiol. 2022;32(10):7185-7195CrossRefPubMed Liu B, Zeng Q, Huang J, et al. IVIM using convolutional neural networks predicts microvascular invasion in HCC. Eur Radiol. 2022;32(10):7185-7195CrossRefPubMed
36.
go back to reference Liang J, Song X, Xiao Z, et al. Using IVIM-MRI and R2⁎ Mapping to Differentiate Early Stage Liver Fibrosis in a Rat Model of Radiation-Induced Liver Fibrosis. Biomed Res Int. 2018;2018:4673814CrossRefPubMedPubMedCentral Liang J, Song X, Xiao Z, et al. Using IVIM-MRI and R2⁎ Mapping to Differentiate Early Stage Liver Fibrosis in a Rat Model of Radiation-Induced Liver Fibrosis. Biomed Res Int. 2018;2018:4673814CrossRefPubMedPubMedCentral
37.
go back to reference Ichikawa S, Motosugi U, Morisaka H, et al. MRI-based staging of hepatic fibrosis: Comparison of intravoxel incoherent motion diffusion-weighted imaging with magnetic resonance elastography. J Magn Reson Imaging. 2015;42(1):204-210CrossRefPubMed Ichikawa S, Motosugi U, Morisaka H, et al. MRI-based staging of hepatic fibrosis: Comparison of intravoxel incoherent motion diffusion-weighted imaging with magnetic resonance elastography. J Magn Reson Imaging. 2015;42(1):204-210CrossRefPubMed
38.
go back to reference Gilani IA, Sepponen R. Quantitative rotating frame relaxometry methods in MRI. NMR Biomed. 2016;29(6):841-861CrossRefPubMed Gilani IA, Sepponen R. Quantitative rotating frame relaxometry methods in MRI. NMR Biomed. 2016;29(6):841-861CrossRefPubMed
Metadata
Title
Combining T1rho and advanced diffusion MRI for noninvasively staging liver fibrosis: an experimental study in rats
Authors
Yiwan Guo
Tingting Guo
Chen Huang
Peng Sun
Zhigang Wu
Ziwei Jin
Chuansheng Zheng
Xin Li
Publication date
12-04-2024
Publisher
Springer US
Published in
Abdominal Radiology
Print ISSN: 2366-004X
Electronic ISSN: 2366-0058
DOI
https://doi.org/10.1007/s00261-024-04327-3
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