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Portal hypertension may influence the registration of hypointensity of small hepatocellular carcinoma in the hepatobiliary phase in gadoxetic acid MR

Carla Caparroz

Carla Caparroz

Radiology Department, Barcelona Clinic Liver Cancer (BCLC) Group, Hospital Clinic Barcelona, University of BarcelonaBarcelona, Spain
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Caparroz, Carla
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Alejandro Forner

Alejandro Forner

  • Liver Unit, Barcelona Clinic Liver Cancer (BCLC) Group, Hospital Clinic Barcelona. IDIBAPS, University of BarcelonaBarcelona, Spain
  • Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd)Barcelona, Spain
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Forner, Alejandro
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Jordi Rimola

Jordi Rimola

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Rimola, Jordi
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Anna Darnell

Anna Darnell

Radiology Department, Barcelona Clinic Liver Cancer (BCLC) Group, Hospital Clinic Barcelona, University of BarcelonaBarcelona, Spain
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Darnell, Anna
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Ángeles García-Criado

Ángeles García-Criado

Radiology Department, Barcelona Clinic Liver Cancer (BCLC) Group, Hospital Clinic Barcelona, University of BarcelonaBarcelona, Spain
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García-Criado, Ángeles
, 
Juan Ramón Ayuso

Juan Ramón Ayuso

Radiology Department, Barcelona Clinic Liver Cancer (BCLC) Group, Hospital Clinic Barcelona, University of BarcelonaBarcelona, Spain
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Ayuso, Juan Ramón
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María Reig

María Reig

  • Liver Unit, Barcelona Clinic Liver Cancer (BCLC) Group, Hospital Clinic Barcelona. IDIBAPS, University of BarcelonaBarcelona, Spain
  • Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd)Barcelona, Spain
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Reig, María
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Jordi Bruix

Jordi Bruix

  • Liver Unit, Barcelona Clinic Liver Cancer (BCLC) Group, Hospital Clinic Barcelona. IDIBAPS, University of BarcelonaBarcelona, Spain
  • Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd)Barcelona, Spain
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Bruix, Jordi
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Carmen Ayuso

Carmen Ayuso

  • Radiology Department, Barcelona Clinic Liver Cancer (BCLC) Group, Hospital Clinic Barcelona, University of BarcelonaBarcelona, Spain
  • Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd)Barcelona, Spain
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Ayuso, Carmen
  
14. Aug. 2022
Portal hypertension may influence the registration of hypointensity of small hepatocellular carcinoma in the hepatobiliary phase in gadoxetic acid MR's Cover Image
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Artikel-Kategorie: research article
Online veröffentlicht: 14. Aug. 2022
Seitenbereich: 292 - 302
Eingereicht: 04. Feb. 2022
Akzeptiert: 24. Apr. 2022
DOI: https://doi.org/10.2478/raon-2022-0024
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© 2022 Carla Caparroz, Alejandro Forner, Jordi Rimola, Anna Darnell, Ángeles García-Criado, Juan Ramón Ayuso, María Reig, Jordi Bruix, Carmen Ayuso, published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Figure 1

Non-adequate quality in the liver uptake of Gadolinium-ethoxybenzyl-diethylenetriamine penta-acetic acid (Gd-EOB-DTPA) in the 20 minutes hepatobiliary phase. (A) and (B): patient with liver cirrhosis Child-Pugh B and clinically significant portal hypertension. (A): Baseline T1w-3D VIBE sequence. (B): the liver showed poor or non-apparent contrast uptake compared to the liver before contrast injection. (C) and (D): patient with liver cirrhosis Child-Pugh A 5 points with no clinically significant portal hypertension. (C): Baseline T1w-3D VIBE sequence. (D): the liver parenchyma showed very heterogeneous uptake of the contrast media, especially in the periphery of the right hepatic lobe.
Non-adequate quality in the liver uptake of Gadolinium-ethoxybenzyl-diethylenetriamine penta-acetic acid (Gd-EOB-DTPA) in the 20 minutes hepatobiliary phase. (A) and (B): patient with liver cirrhosis Child-Pugh B and clinically significant portal hypertension. (A): Baseline T1w-3D VIBE sequence. (B): the liver showed poor or non-apparent contrast uptake compared to the liver before contrast injection. (C) and (D): patient with liver cirrhosis Child-Pugh A 5 points with no clinically significant portal hypertension. (C): Baseline T1w-3D VIBE sequence. (D): the liver parenchyma showed very heterogeneous uptake of the contrast media, especially in the periphery of the right hepatic lobe.

Figure 2

Location of the 6 regions of interest (ROIs) in the liver parenchyma, to calculate the liver signal intensity (LSI) in the pre-contrast sequence (LSIpre) (A), at 10 minutes (LSI10) (B) and at 20 minutes (LSI20) hepatobiliary phase (C). Four of the ROIs were located in the anterior and posterior segments respectively of the right hepatic lobe, and two more were placed in the lateral and medial segments of the left lobe respectively. ROIs were drawn avoiding the inclusion of vascular structures and possible focal liver lesions.
Location of the 6 regions of interest (ROIs) in the liver parenchyma, to calculate the liver signal intensity (LSI) in the pre-contrast sequence (LSIpre) (A), at 10 minutes (LSI10) (B) and at 20 minutes (LSI20) hepatobiliary phase (C). Four of the ROIs were located in the anterior and posterior segments respectively of the right hepatic lobe, and two more were placed in the lateral and medial segments of the left lobe respectively. ROIs were drawn avoiding the inclusion of vascular structures and possible focal liver lesions.

Figure 3

Location of the region of interest in the 20 minutes hepatobiliary phase in the spleen (A), in the right paravertebral muscle (B), and in the upper pole of the right kidney (C) to calculate the different quantitative parameters of contrast liver uptake: spleen-liver intensity (SLI) and liver-spleen contrast ratio (LSCR), muscle-liver intensity (MLI) and the liver-muscle contrast ratio (LMCR) and kidney-liver intensity (KLI) and the liver-kidney contrast ratio (LKCR), respectively.
Location of the region of interest in the 20 minutes hepatobiliary phase in the spleen (A), in the right paravertebral muscle (B), and in the upper pole of the right kidney (C) to calculate the different quantitative parameters of contrast liver uptake: spleen-liver intensity (SLI) and liver-spleen contrast ratio (LSCR), muscle-liver intensity (MLI) and the liver-muscle contrast ratio (LMCR) and kidney-liver intensity (KLI) and the liver-kidney contrast ratio (LKCR), respectively.

Quantitative assessment of liver uptake of Gadolinium-ethoxybenzyl-diethylenetriamine penta-acetic acid (Gd-EOB-DTPA) during hepatobiliary phase (HPB) at 10 and 20 minutes in the study group considering the presence of clinically significant portal hypertension (CSPH)_ On the left, including all study cohort and on the right, considering only cirrhotic patients with preserved liver function (Child-Pugh A 5 points)_ Variables described as median and interquartile range

INDEX No CSPH (all CP A-5 points) CSPH P value No CSPH (all CP A-5 points) CP A-5 points and CSPH P value
N 19 43 19 25
RLE10 0.73 [0.52-0.89] 0.57 [0.47-0.69] 0.027 0.73 [0.52-0.89] 0.65 [0.51-0.77] NS
RLE20 0.73 [0.56-0.85] 0.59 [0.47-0.74] NS 0.73 [0.56-0.85] 0.66 [0.54-0.77] NS
LSCR10 1.54 [1.37-1.67] 1.23 [1.15-1.39] < 0.001 1.54 [1.37-1.67] 1.29 [1,15-1.51] 0.014
LSCR20 1.68 [1.53-1.84] 1.35 [1.20-1.57] 0.003 1.68 [1.53-1.84] 1.37 [1.26-1.74] 0.036
LMCR10 2.41 [2.12-2.83] 2.06 [1.75-2.45] 0.006 2.41 [2.12-2.83] 1.88 [1.76-2.50] 0.034
LMCR20 2.49 [2.24-2.96] 1.95 [1.77-2.39] 0.005 2.49 [2.24-2.96] 1.92 [1.78-2.6] 0.036
LKCR10 1.15 [0.98-1.34] 0.93 [0.81-1.13] 0.001 1.15 [0.98-1.34] 1.01 [0.84-1.21] 0.032
LKCR20 1.25 [1.16-1.43] 0.98 [0.88-1.28] 0.001 1.25 [1.16-1.43] 1.05 [0.88-1.03] 0.017
CEI10 1.46 [1.34-1.59] 1.36 [1.26-1.52] NS 1.46 [1.34-1.59] 1.47 [1.31-1.58] NS
CEI20 1.50 [1.38-1.71] 1.41 [1.24-1.54] NS 1.50 [1.38-1.71] 1.48 [1.33-1.65] NS
HUI10 609.7 [501.4-970.3] 327.8 [191.7-511.8] 0.004 609.7 [501.4-970.3] 411.4 [223.4-1210.7] NS
HUI20 803.6 [678.7-1091.2] 450.5 [274.8-864.4] 0.033 803.6 [678.7-1091.2] 569.0 [341.8-987.1] NS

Quantitative parameters evaluating the liver uptake in the 20 minutes hepatobiliary phase (HPB) of Gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid (Gd-EOB-DTPA) according to the quality of the HBP_ In one patient the HBP at 20 minutes was not available (n = 61)_ Variables described as median and interquartile range

INDEX Qualitative assessment adequate Qualitative assessment Non-adequate P value
N 49 12
RLE20 0.68 [0.57-0.83] 0.40 [0.31-0.51] < 0.001
LSCR20 1.53 [1.34-1.78] 1.19 [1.06-1.22] < 0.001
LMCR20 2.34 [1.88-2.78] 1.91 [1.50-2.11] 0.002
LKCR20 1.20 [0.95-1.35] 0.89 [0.78-0.98] 0.001
CEI20 1.23 [1.09-1.32] 1.00 [0.90-1.10] 0.001
HUI20 744.1 [444.8-1024.1] 251.5 [65-4-331.0] < 0.001

Formulas used for qualitative assessment of liver uptake of Gadolinium-ethoxybenzyl-diethylenetriamine penta-acetic acid (Gd-EOB-DTPA) in the hepatobiliary phase (HPB)

Formula Variables definition
Relative Liver Enhancement (RLE) RLE10=( LSI10 − LSIPRE)  LSIPRE  $RLE10=\frac{(\text{ }\!\!~\!\!\text{ LSI10 }\!\!~\!\!\text{ }-\text{ }\!\!~\!\!\text{ LSIPRE) }\!\!~\!\!\text{ }}{\text{ }\!\!~\!\!\text{ LSIPRE }\!\!~\!\!\text{ }}$ RLE10 and RLE20: RLE at 10- and 20-min HBP
RLE20=( LSI20 - LSIPRE ) LSIPRE  $RLE20=\frac{(\text{ }\!\!~\!\!\text{ LSI20 - LSIPRE }\!\!~\!\!\text{ })}{\text{ }\!\!~\!\!\text{ LSIPRE }\!\!~\!\!\text{ }}$ LSIpre, LSI10 and LSI20: Liver signal intensity pre-contrast, at 10- and 20-min HBP, respectively
Liver to Spleen Contrast Ratio (LSCR) LSCRpre = LSIPRE  SSIPRE  $LSCRpre\text{ }\!\!~\!\!\text{ }=\frac{\text{ }\!\!~\!\!\text{ LSIPRE }\!\!~\!\!\text{ }}{\text{ }\!\!~\!\!\text{ SSIPRE }\!\!~\!\!\text{ }}$ LSCRpre LSCR10 and LSCR20r: LSCR pre-contrast, at 10- and 20- min HBP, respectively
LSCR10=LSI10SSI10 $LSCR10=\frac{\text{LSI}10}{\text{SSI}10}$ LSIpre, LSI10 and LSI20: Liver signal intensity pre-contrast, at 10- and 20- min HBP, respectively
LSCR20 = LSI20  SSI20  $LSCR\text{20 }\!\!~\!\!\text{ }=\frac{\text{ }\!\!~\!\!\text{ LSI20 }\!\!~\!\!\text{ }}{\text{ }\!\!~\!\!\text{ SSI20 }\!\!~\!\!\text{ }}$ SSIpre, SSI10 and SSI20: Spleen signal intensity pre-contrast, at 10- and 20- min HBP, respectively
Liver to muscle Contrast Ratio (LMCR) LMCRpre = LSIPRE  MSIPRE  $LMCRpre\text{ }\!\!~\!\!\text{ }=\frac{\text{ }\!\!~\!\!\text{ LSIPRE }\!\!~\!\!\text{ }}{\text{ }\!\!~\!\!\text{ MSIPRE }\!\!~\!\!\text{ }}$ LMCRpre, LMCR10 and LMCR20r: LMCR pre-contrast, at 10- and 20- min HBP, respectively
LMCR10=LSI10MSI10 $LMCR10=\frac{\text{LSI}10}{\text{MSI}10}$ LSIpre, LSI10 and LSI20: Liver signal intensity pre-contrast, at 10- and 20- min HBP, respectively
LMCR20 =LSI20MSI20 $LMCR\text{20 }\!\!~\!\!\text{ }=\frac{\text{LSI}20}{\text{MSI}20}$ MSIpre, MSI10 and MSI20: Muscle signal intensity pre-contrast, at 10- and 20- min HBP, respectively
Liver to Kidney Contrast Ratios (LKCR) LKCRpre = LSIPRE  KSIPRE  $LKCRpre\text{ }\!\!~\!\!\text{ }=\frac{\text{ }\!\!~\!\!\text{ LSIPRE }\!\!~\!\!\text{ }}{\text{ }\!\!~\!\!\text{ KSIPRE }\!\!~\!\!\text{ }}$ LKCR LKCR and LKCR: LKCR pre-contrast, at 10- and 20- min HBP, respectively pre, 10 20r
LKCR10= LSI10  KSI10  $LKCR10=\frac{\text{ }\!\!~\!\!\text{ LSI10 }\!\!~\!\!\text{ }}{\text{ }\!\!~\!\!\text{ KSI10 }\!\!~\!\!\text{ }}$ LSIpre, LSI10 and LSI20: Liver signal intensity pre-contrast, at 10- and 20- min HBP, respectively
LKCR20 = LSI20  KSI20  $LKCR\text{20 }\!\!~\!\!\text{ }=\frac{\text{ }\!\!~\!\!\text{ LSI20 }\!\!~\!\!\text{ }}{\text{ }\!\!~\!\!\text{ KSI20 }\!\!~\!\!\text{ }}$ KSIpre, KSI10 and KSI20: Kidney signal intensity pre-contrast, at 10- and 20- min HBP, respectively
Contrast Enhancement Index (CEI) CEI10 = LMCR10  LMCRPRE  $\text{CEI10 }\!\!~\!\!\text{ }=\frac{\text{ }\!\!~\!\!\text{ }LMCR\text{10 }\!\!~\!\!\text{ }}{\text{ }\!\!~\!\!\text{ LMCRPRE }\!\!~\!\!\text{ }}$ - LMCRpre, LMCR10 and LMCR20r: LMCR pre-contrast, at 10- and 20- min HBP, respectively
CEI20 =LMCR20 LMCRPRE  $\text{CEI20 }\!\!~\!\!\text{ }=\frac{LMCR20}{\text{ }\!\!~\!\!\text{ LMCRPRE }\!\!~\!\!\text{ }}$ - CEI10 and CEI20: Contrast Enhancement Index at 10- and 20- min HBP, respectively
Hepatic Uptake index (HUI) HUI10=VOLLIVER ( LSI10  SSI10)−1 $\text{HU}{{\text{I}}_{10}}=\text{VO}{{\text{L}}_{\text{LIVER }\!\!~\!\!\text{ }}}\left( \frac{\text{ }\!\!~\!\!\text{ LSI10 }\!\!~\!\!\text{ }}{\text{ }\!\!~\!\!\text{ SSI10}} \right)-1$ - HUI10 and HUI20: Hepatic Uptake index at 10- and 20- min HBP, respectively
HUL20=VOLLIVER (512058120)=1 $\text{HU}{{\text{L}}_{20}}=\text{VO}{{\text{L}}_{\text{LIVER }\!\!~\!\!\text{ }}}\left( \frac{5120}{58120} \right)=1$ LSI10 and LSI20: Liver signal intensity at 10- and 20- min HBP, respectively
SSI10 and SSI20: Spleen signal intensity at 10- and 20- min HBP, respectively

Quantitative assessment of liver uptake of Gadolinium-ethoxybenzyl-diethylenetriamine penta-acetic acid (Gd-EOB-DTPA) during the hepatobiliary phase (HPB) at 10 and 20 minutes considering the degree of liver function impairment according to Child-Pugh classification_ Variables described as median and interquartile range

INDEX Study group Child-Pugh A Child-Pugh B P value Child-Pugh A-5 points Child-Pugh A-6 points + B P value
N 62 53 9 44 18
RLE10 0.65 [0.49-0.75] 0.68 [0.51-0.81] 0.41 [0.30-0.52] <0.001 0.68 [0.52-0.82] 0.50 [0.40-0.58] 0.005
RLE20 0.63 [0.51-0.78] 0.67 [0.55-0.82] 0.41 [0.30-0.52] <0.001 0.68 [0.56-0.83] 0.52 [0.40-0.61] 0.006
LSCR10 1.32 [1.17-1.55] 1.35 [1.11-1.59] 1.20 [0.99-1.28] 0.016 1.43 [1.19-1.61] 1.20 [1,11-1.28] 0.001
LSCR20 1.48 [1.23-1.71] 1.51 [1.30-1.80] 1.20 [1.01-1.43] 0.006 1.54 [1.32-1.81] 1.25 [1.17-1.53] 0.008
LMCR10 2.14 [1.78-2.51] 2.16 [1.81-2.62] 1.78 [1.52-2.13] 0.030 2.26 [1.81-2.71] 2.08 [1.73-2.16] NS
LMCR20 2.25 [1.86-2.63] 2.29 [1.89-2.69] 1.79 [1.52-2.23] 0.030 2.34 [1.88-2.70] 2.05 [1.75-2.31] NS
LKCR10 1.02 [0.85-1.17] 1.04 [0.89-1.21] 0.83 [0.74-0.90] 0.005 1.06 [0.91-1.25] 0.87 [0.76-1.05] 0.008
LKCR20 1.14 [0.90-1.13] 1.19 [0.96-1.33] 0.89 [0.80-0.96] 0.009 1.20 [0.96-1.38] 0.91 [0.81-1.22] 0.012
CEI10 1.39 [1.27-1.57] [1.341.43 -1.1.58] 1.26 [1.22-1.32] 0.006 1.47 [1.34-1.58] 1.33 [1.25-1.38] 0.003
CEI20 1.43 [1.30-1.61] 1.45 [1.35-1.63] 1.32 [1.19-1.37] 0.007 1.50 [1.39-1.66] 1.35 [1.19-1.42] 0.001
HUI10 407.3 [223.7-640.9] 486.2 [235.3-845.4] 312.4 [-3.31- 400] 0.022 522.4 [284.9-1036.4] 265.7 [130.5-383.7] <0.001
HUI20 660.5 [301.5-956.5] 697.8 [367.1-1028.9] 265 [72.5-620.4] 0.009 720.1 [450.5-1062.4] 327.2 [198.1-772.2] 0.004

Quantitative assessment of liver uptake of Gadolinium-ethoxybenzyl-diethylenetriamine penta-acetic acid (Gd-EOB-DTPA) during hepatobiliary phase (HPB) at 10 minutes in patients with normal liver (control group) compared with all Child-Pugh (CP) A 5 points patients (left panel) and with patients Child-Pugh A 5 points patients without clinically significant portal hypertension (CSPH)_ Variables described as median and interquartile range

INDEX Control group Child-Pugh A-5 points P value Control group No CSPH (all CP A-5 points) P value
N 20 44 20 19
RLE10 1.06 [0.82-2.16] 0.68 [0.52-0.82] < 0.001 1.06 [0.82-2.16] 0.73 [0.52-0.89] < 0.001
LSCR10 2,27 [2.06-2.88] 1.43 [1.19-1.61] < 0.001 2,27 [2.06-2.88] 1.54 [1.37-1.67] < 0.001
LMCR10 3.11 [2.90-3.55] 2.26 [1.81-2.71] < 0.001 3.11 [2.90-3.55] 2.41 [2.12-2.83] < 0.001
LKCR10 1.82 [1.51-1.99] 1.06 [0.91-1.25] < 0.001 1.82 [1.51-1.99] 1.15 [0.98-1.34] < 0.001
CEI10 1.71 [1.55-1.85] 1.47 [1.34-1.58] 0.001 1.71 [1.55-1.85] 1.46 [1.34-1.59] 0.007
HUI10 1449.6 [1259-1717.7] 522.4 [284.9-1036.4] < 0.001 1449.6 [1259-1717.7] 609.7 [501.4-970.3] < 0.001
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