Skip to main content

Advertisement

Log in

Comparison between CT volumetry, technetium99m galactosyl-serum-albumin scintigraphy, and gadoxetic-acid-enhanced MRI to estimate the liver fibrosis stage in preoperative patients

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

Abstract

Objectives

To compare the efficacy of computed tomography volumetry (CTV), technetium99m galactosyl-serum-albumin (99mTc-GSA) scintigraphy, and gadolinium-ethoxybenzyl-diethylenetriamine-pentaacetic-acid-enhanced MRI (EOB-MRI) in estimating the liver fibrosis (LF) stage in patients undergoing liver resection.

Methods

This retrospective study included 91 consecutive patients who had undergone preoperative dynamic CT and 99mTc-GSA scintigraphy. EOB-MRI was performed in 76 patients. CTV was used to measure the total liver volume (TLV), spleen volume (SV), normalised to the body surface area (BSA), and liver-to-spleen volume ratio (TLV/SV). 99mTc-GSA scintigraphy provided LHL15, HH15, and GSA indices. The liver-to-spleen ratio (LSR) was calculated in the hepatobiliary phase of EOB-MRI. Hyaluronic acid and type 4 collagen levels were measured in 65 patients. Logistic regression and receiver operating characteristic (ROC) analyses were performed to identify useful parameters for estimating the LF stage and laboratory data.

Results

According to the multivariable logistic regression analysis, SV/BSA (odds ratio [OR], 1.01; 95% confidence interval [CI], 1.003–1.02; p = 0.011), LSR (OR, 0.06; 95%CI, 0.004–0.70; p = 0.026), and hyaluronic acid (OR, 1.01; 95%CI, 1.001–1.02; p = 0.024) were independent variables for severe LF (F3–4). Combined SV/BSA, LSR, and hyaluronic acid correctly estimated severe LF, with an AUC of 0.91, which was significantly larger than the AUCs of the GSA index (AUC = 0.84), SV/BSA (AUC = 0.83), or LSR (AUC = 0.75) alone.

Conclusions

Combined CTV, EOB-MRI, and hyaluronic acid analyses improved the estimation accuracy of severe LF compared to CTV, EOB-MRI, or 99mTc-GSA scintigraphy individually.

Clinical relevance statement

The combined analysis of spleen volume on CT volumetry, liver-to-spleen ratio on gadolinium-ethoxybenzyl-diethylenetriamine-pentaacetic-acid-enhanced MRI, and hyaluronic acid can identify severe liver fibrosis associated with a high risk of liver failure after hepatectomy and recurrence in patients with hepatocellular carcinoma.

Key Points

• Spleen volume of CT volumetry normalised to the body surface area, liver-to-spleen ratio of EOB-MRI, and hyaluronic acid were independent variables for liver fibrosis.

• CT volumetry and EOB-MRI enable the detection of severe liver fibrosis, which may correlate with post-hepatectomy liver failure and complications.

• Combined CT volumetry, gadolinium-ethoxybenzyl-diethylenetriamine-pentaacetic-acid-enhanced MRI (EOB-MRI), and hyaluronic acid analyses improved the estimation of severe liver fibrosis compared to technetium99m galactosyl-serum-albumin scintigraphy.

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

Similar content being viewed by others

Abbreviations

ALT:

Alanine aminotransferase

APRI:

Aspartate aminotransferase-platelet ratio index

AST:

Aspartate aminotransferase

BMI:

Body mass index

BSA:

Body surface area

CI:

Confidence interval

Cr:

Creatinine

EOB-MRI:

Gadolinium-ethoxybenzyl-diethylenetriamine-pentaacetic-acid-enhanced MRI

FIB-4:

Fibrosis index based on four factors; fibrosis-4 score

CTV:

CT volumetry

Gd:

Gadolinium

Gd-EOB-DTPA:

Gadolinium-ethoxybenzyl-diethylenetriamine-pentaacetic acid

HH15:

Uptake ratio of the heart at 15 min to that at 3 min

HCC:

Hepatocellular carcinoma

ICC:

Intraclass correlation

ICG:

Indocyanine green

ICG-R15:

Indocyanine green retention rates at 15 min after injection

INR:

International normalised ratio

LF:

Liver fibrosis

LHL15:

Uptake ratio of the liver to the liver plus heart at 15 min

LSR:

Liver-to-spleen ratio

MDCT:

Multidetector computed tomography

MELD:

Model for end-stage liver disease score

OR:

Odds ratio

Plt:

Platelet count

SI:

Signal intensity

SPECT:

Single-photon emission computed tomography

SV:

Splenic volume

TLV:

Total liver volume

TLV/SV:

Ratio of TLV to SV

99 mTc-GSA:

Technetium99m galactosyl-serum-albumin

References

  1. Abe H, Midorikawa Y, Mitsuka Y et al (2017) Predicting postoperative outcomes of liver resection by magnetic resonance elastography. Surgery 162:248–255

    Article  PubMed  Google Scholar 

  2. Liu P, Li P, He W, Zhao LQ (2009) Liver and spleen volume variations in patients with hepatic fibrosis. World J Gastroenterol 15:3298–3302

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bedossa P, Dargere D, Paradis V (2003) Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology 38:1449–1457

    Article  PubMed  Google Scholar 

  4. Bravo AA, Sheth SG, Chopra S (2001) Liver biopsy. N Engl J Med 344:495–500

    Article  CAS  PubMed  Google Scholar 

  5. Standish RA (2006) An appraisal of the histopathological assessment of liver fibrosis. Gut 55:569–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lurie Y, Webb M, Cytter-Kuint R, Shteingart S, Lederkremer GZ (2015) Non-invasive diagnosis of liver fibrosis and cirrhosis. World J Gastroenterol 21:11567–11583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pickhardt PJ, Malecki K, Hunt OF et al (2017) Hepatosplenic volumetric assessment at MDCT for staging liver fibrosis. Eur Radiol 27:3060–3068

    Article  PubMed  Google Scholar 

  8. Sato H, Takase S, Takada A (1989) Changes in liver and spleen volumes in alcoholic liver disease. J Hepatol 8:150–157

    Article  CAS  PubMed  Google Scholar 

  9. Iguchi T, Sato S, Kouno Y et al (2003) Comparison of Tc-99m-GSA scintigraphy with hepatic fibrosis and regeneration in patients with hepatectomy. Ann Nucl Med 17:227–233

    Article  PubMed  Google Scholar 

  10. Tokorodani R, Sumiyoshi T, Okabayashi T et al (2019) Liver fibrosis assessment using 99mTc-GSA SPECT/CT fusion imaging. Jpn J Radiol 37:315–320

    Article  CAS  PubMed  Google Scholar 

  11. Nishikawa H, Osaki Y, Komekado H et al (2015) Clinical implication of the preoperative GSA index in 99mTc-GSA scintigraphy in hepatitis C virus-related hepatocellular carcinoma. Oncol Rep 33:1071–1078

    Article  CAS  PubMed  Google Scholar 

  12. Watanabe H, Kanematsu M, Goshima S et al (2011) Staging hepatic fibrosis: comparison of gadoxetate disodium-enhanced and diffusion-weighted MR imaging–preliminary observations. Radiology 259:142–150

    Article  PubMed  Google Scholar 

  13. Nishie A, Asayama Y, Ishigami K et al (2012) MR prediction of liver fibrosis using a liver-specific contrast agent: superparamagnetic iron oxide versus Gd-EOB-DTPA. J Magn Reson Imaging 36:664–671

    Article  PubMed  Google Scholar 

  14. Tamada T, Ito K, Higaki A et al (2011) Gd-EOB-DTPA-enhanced MR imaging: evaluation of hepatic enhancement effects in normal and cirrhotic livers. Eur J Radiol 80:e311-316

    Article  PubMed  Google Scholar 

  15. Motosugi U, Ichikawa T, Oguri M et al (2011) Staging liver fibrosis by using liver-enhancement ratio of gadoxetic acid-enhanced MR imaging: comparison with aspartate aminotransferase-to-platelet ratio index. Magn Reson Imaging 29:1047–1052

    Article  CAS  PubMed  Google Scholar 

  16. Furusato Hunt OM, Lubner MG, Ziemlewicz TJ, Muñoz Del Rio A, Pickhardt PJ (2016) The liver segmental volume ratio for noninvasive detection of cirrhosis: comparison with established linear and volumetric measures. J Comput Assist Tomogr 40:478–484

    Article  PubMed  Google Scholar 

  17. Son JH, Lee SS, Lee Y et al (2020) Assessment of liver fibrosis severity using computed tomography-based liver and spleen volumetric indices in patients with chronic liver disease. Eur Radiol 30:3486–3496

    Article  PubMed  Google Scholar 

  18. Hwang EH, Taki J, Shuke N et al (1999) Preoperative assessment of residual hepatic functional reserve using 99mTc-DTPA-galactosyl-human serum albumin dynamic SPECT. J Nucl Med 40:1644–1651

    CAS  PubMed  Google Scholar 

  19. Kwon AH, Ha-Kawa SK, Uetsuji S, Kamiyama Y, Tanaka Y (1995) Use of technetium 99m diethylenetriamine-pentaacetic acid-galactosyl-human serum albumin liver scintigraphy in the evaluation of preoperative and postoperative hepatic functional reserve for hepatectomy. Surgery 117:429–434

    Article  CAS  PubMed  Google Scholar 

  20. Makuuchi M, Kosuge T, Takayama T et al (1993) Surgery for small liver cancers. Semin Surg Oncol 9:298–304

    Article  CAS  PubMed  Google Scholar 

  21. Wai CT, Greenson JK, Fontana RJ et al (2003) A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology 38:518–526

    Article  PubMed  Google Scholar 

  22. Vallet-Pichard A, Mallet V, Nalpas B et al (2007) FIB-4: an inexpensive and accurate marker of fibrosis in HCV infection. Comparison with liver biopsy and fibrotest. Hepatology 46:32–36

    Article  CAS  PubMed  Google Scholar 

  23. Malinchoc M, Kamath PS, Gordon FD, Peine CJ, Rank J, ter Borg PC (2000) A model to predict poor survival in patients undergoing transjugular intrahepatic portosystemic shunts. Hepatology 31:864–871

    Article  CAS  PubMed  Google Scholar 

  24. Yamashita Y, Komohara Y, Takahashi M et al (2000) Abdominal helical CT: evaluation of optimal doses of intravenous contrast material–a prospective randomized study. Radiology 216:718–723

    Article  CAS  PubMed  Google Scholar 

  25. Du Bois D, Du Bois EF (1989) A formula to estimate the approximate surface area if height and weight be known. 1916. Nutrition 5:303–311; discussion 312–303

  26. Ichida F, Tsuji T, Omata M et al (1996) New Inuyama classification; new criteria for histological assessment of chronic hepatitis^1. Int Hepatol Commun 6:112–119

    Article  Google Scholar 

  27. Ngu S, Lebron-Zapata L, Pomeranz C et al (2016) Inter-observer agreement on the assessment of relative liver lesion signal intensity on hepatobiliary phase imaging with gadoxetate (Gd-EOB-DTPA). Abdom Radiol (NY) 41:50–55

    Article  PubMed  Google Scholar 

  28. Prassopoulos P, Daskalogiannaki M, Raissaki M, Hatjidakis A, Gourtsoyiannis N (1997) Determination of normal splenic volume on computed tomography in relation to age, gender and body habitus. Eur Radiol 7:246–248

    Article  CAS  PubMed  Google Scholar 

  29. Horowitz JM, Venkatesh SK, Ehman RL et al (2017) Evaluation of hepatic fibrosis: a review from the society of abdominal radiology disease focus panel. Abdom Radiol (NY) 42:2037–2053

    Article  PubMed  Google Scholar 

  30. Katsube T, Okada M, Kumano S et al (2011) Estimation of liver function using T1 mapping on Gd-EOB-DTPA-enhanced magnetic resonance imaging. Invest Radiol 46:277–283

    Article  PubMed  Google Scholar 

  31. Nishie A, Ushijima Y, Tajima T et al (2012) Quantitative analysis of liver function using superparamagnetic iron oxide- and Gd-EOB-DTPA-enhanced MRI: comparison with Technetium-99m galactosyl serum albumin scintigraphy. Eur J Radiol 81:1100–1104

    Article  PubMed  Google Scholar 

  32. Lubner MG, Dustin Pooler B, del Rio AM, Durkee B, Pickhardt PJ (2014) Volumetric evaluation of hepatic tumors: multi-vendor, multi-reader liver phantom study. Abdom Imaging 39:488–496

    PubMed  Google Scholar 

  33. Gudowska M, Cylwik B, Chrostek L et al (2017) The role of serum hyaluronic-acid determination in the diagnosis of liver fibrosis. Acta Biochim Pol 64:451–457

    Article  CAS  PubMed  Google Scholar 

  34. Laurent TC, Laurent UB, Fraser JR et al (1996) Serum hyaluronan as a disease marker. Ann Med 28:241–253

    Article  CAS  PubMed  Google Scholar 

  35. Tago K, Tsukada J, Sudo N et al (2022) Comparison between CT volumetry and extracellular volume fraction using liver dynamic CT for the predictive ability of liver fibrosis in patients with hepatocellular carcinoma. Eur Radiol 32:7555–7565

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank all the medical staff involved in this study.

Funding

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

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masahiro Okada.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Masahiro Okada.

Conflict of interest

The authors have no conflicts of interest to declare.

Statistics and biometry

We consulted statistical experts in the preparation of this manuscript.

Hirotsugu Yasuda, statistician Kondo P.P. Inc.

Informed consent

Informed consent was waived by the Institutional Review Board, given the study’s retrospective nature.

Ethical approval

Institutional Review Board approval was obtained (Nihon University, Itabashi Hospital, RK-201110-12).

Study subjects or cohorts overlap

Two of the 91 patients in this study have been previously reported in Tago K et al (2022) European Radiology. 32:7555–7565. https://doi.org/10.1007/s00330-022-08852-x

Methodology

• Retrospective

• Observational 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.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 120 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

Nakazawa, Y., Okada, M., Hyodo, T. et al. Comparison between CT volumetry, technetium99m galactosyl-serum-albumin scintigraphy, and gadoxetic-acid-enhanced MRI to estimate the liver fibrosis stage in preoperative patients. Eur Radiol 34, 2212–2222 (2024). https://doi.org/10.1007/s00330-023-10219-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-023-10219-9

Keywords

Navigation