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A prospective comparison of three ultrasound-based techniques in quantitative diagnosis of hepatic steatosis in NAFLD

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

Abstract

Purpose

To investigate the correlation between different ultrasound attenuation-based techniques and to compare their diagnostic performances using proton magnetic resonance spectroscopy (1H-MRS) as a reference standard.

Methods

Participants who had clinical suspicion of nonalcoholic fatty liver disease (NAFLD) were prospectively recruited. Each subject had ultrasound with attenuation imaging (ATI) or quantitative ultrasound including tissue attenuation imaging (TAI) and tissue scatter-distribution imaging (TSI), and controlled-attenuation parameter (CAP) and 1H-MRS if available. The technical success rates, intra-observer repeatabilities of attenuation and backscattering coefficient were evaluated. ATI, TAI and CAP were three attenuation-based techniques. Spearman coefficient was used to test correlations among them and 1H-MRS. In addition, the diagnostic performances of these parameters for detecting ≥ 5% or 10% hepatic steatosis were evaluated.

Results

130 participants had ultrasound scanning. Among them, 67 had CAP and 48 had 1H-MRS. The technical success rates were all 100%. The intra-observer repeatabilities of them were also excellent (ICCs > 0.90) and AC-ATI correlated well with AC-TAI (r = 0.752). AC-ATI, AC-TAI showed moderate correlation with CAP, (rATI = 0.623, 95% CI 0.446–0.752, P < 0.001; rTAI = 0.573, 95% CI 0.377–0.720, P < 0.001). For correlation with 1H-MRS, ATI and TAI performed better than CAP(rATI = 0.587; rTAI = 0.712; r CAP = 0.485). The AUCs of ATI, TAI, TSI and CAP for detecting ≥ 5% hepatic steatosis were 0.883, 0.862, 0.870 and 0.868, respectively. The AUC improved to 0.907 when TAI and TSI were combined (P < 0.05). When detecting ≥ 10% hepatic steatosis, the AUCs were 0.855, 0.702, 0.822 and 0.838, respectively.

Conclusion

Different ultrasound attenuation-based techniques were well correlated and exhibited good diagnostic performances in quantitative diagnosis of hepatic steatosis, however, the threshold values were different. Combinations of multiple parameters may improve the diagnostic performance in detecting hepatic steatosis.

Trial registration

The study has been registered online (https://www.chictr.org.cn; unique identifier: ChiCTR2300069459).

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Abbreviations

NAFLD:

Nonalcoholic fatty liver disease

NASH:

Nonalcoholic steatohepatitis

1H-MRS:

Proton magnetic resonance spectroscopy

MRI-PDFF:

MRI-proton density fat fraction

AC:

Attenuation coefficient

BC:

Backscatter coefficient

BMI:

Body mass index

CAP:

Controlled-attenuation parameter

ATI:

Attenuation imaging

QUS:

Quantitative ultrasound techniques

RF:

Raw radiofrequency

TAI:

Tissue attenuation imaging

TSI:

Tissue scatter-distribution imaging

References

  1. Tamaki N, Ajmera V, Loomba R (2022) Non-invasive methods for imaging hepatic steatosis and their clinical importance in NAFLD. Nature Reviews Endocrinology 18:55-66

    Article  CAS  PubMed  Google Scholar 

  2. Ferraioli G, Berzigotti A, Barr RG et al (2021) Quantification of liver fat content with ultrasound: a WFUMB position paper. Ultrasound Med Biol 47:2803-2820.

    Article  PubMed  Google Scholar 

  3. Guan X, Chen YC, Xu HX (2022) New horizon of ultrasound for screening and surveillance of non-alcoholic fatty liver disease spectrum. Eur J Radiol 154:110450

    Article  PubMed  Google Scholar 

  4. Li J, Zou B, Yeo YH et al (2019) Prevalence, incidence, and outcome of non-alcoholic fatty liver disease in Asia, 1999-2019: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol 4:389-398

    Article  PubMed  Google Scholar 

  5. Younossi Z, Anstee QM, Marietti M et al (2018) Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol 15:11-20

    Article  PubMed  Google Scholar 

  6. Davison BA, Harrison SA, Cotter G et al (2020) Suboptimal reliability of liver biopsy evaluation has implications for randomized clinical trials. Journal of hepatology 73:1322-1332

    Article  CAS  PubMed  Google Scholar 

  7. Barr RG (2019) Ultrasound of diffuse liver disease including elastography. Radiol Clin North Am 57:549-562

    Article  PubMed  Google Scholar 

  8. Lu ZF, Zagzebski JA, Lee FT (1999) Ultrasound backscatter and attenuation in human liver with diffuse disease. Ultrasound in Medicine & Biology 25:1047-1054

    Article  CAS  Google Scholar 

  9. Wan YL, Tai DI, Ma HY, et al (2015) Effects of fatty infiltration in human livers on the backscattered statistics of ultrasound imaging. Proc Inst Mech Eng H 229:419-428

    Article  PubMed  Google Scholar 

  10. Caussy C, Alquiraish MH, Nguyen P et al (2018) Optimal threshold of controlled attenuation parameter with MRI‐PDFF as the gold standard for the detection of hepatic steatosis. Hepatology 67:1348-1359

    Article  CAS  PubMed  Google Scholar 

  11. Ferraioli G, Tinelli C, Lissandrin R et al (2014) Interobserver reproducibility of the controlled attenuation parameter (CAP) for quantifying liver steatosis. Hepatol Int 8:576-581

    Article  PubMed  Google Scholar 

  12. Karlas T, Petroff D, Sasso M et al (2017) Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol 66:1022-1030

    Article  PubMed  Google Scholar 

  13. Eddowes PJ, Sasso M, Allison M et al (2019) Accuracy of FibroScan controlled attenuation parameter and liver stiffness measurement in assessing steatosis and fibrosis in patients with nonalcoholic fatty liver disease. Gastroenterology 156:1717-1730

    Article  PubMed  Google Scholar 

  14. Ferraioli G, Maiocchi L, Raciti MV et al (2019) Detection of liver steatosis with a novel ultrasound-based technique: a pilot study using MRI-derived proton density fat fraction as the gold standard. Clinical and Translational Gastroenterology 10:e00081

    Article  PubMed  PubMed Central  Google Scholar 

  15. Ferraioli G, Maiocchi L, Savietto G et al (2021) Performance of the attenuation imaging technology in the detection of liver steatosis. J Ultrasound Med 40:1325-1332

    Article  PubMed  Google Scholar 

  16. Jeon SK, Lee JM, Joo I, Park S-J (2021) Quantitative ultrasound radiofrequency data analysis for the assessment of hepatic steatosis in nonalcoholic fatty liver disease using magnetic resonance imaging proton density fat fraction as the reference standard. Korean journal of radiology 22:1077

    Article  PubMed  PubMed Central  Google Scholar 

  17. Jeon SK, Joo I, Kim SY et al (2021) Quantitative ultrasound radiofrequency data analysis for the assessment of hepatic steatosis using the controlled attenuation parameter as a reference standard. Ultrasonography 40:136

    Article  PubMed  Google Scholar 

  18. Chalasani N, Younossi Z, Lavine JE et al (2018) The diagnosis and management of nonalcoholic fatty liver disease: Practice guidance from the American Association for the Study of Liver Diseases. Hepatology 67:328-357

    Article  PubMed  Google Scholar 

  19. Vuppalanchi R, Siddiqui MS, Van Natta ML et al (2018) Performance characteristics of vibration-controlled transient elastography for evaluation of nonalcoholic fatty liver disease. Hepatology 67:134-144

    Article  PubMed  Google Scholar 

  20. Xia MF, Yan HM, He WY et al (2012) Standardized ultrasound hepatic/renal ratio and hepatic attenuation rate to quantify liver fat content: an improvement method. Obesity (Silver Spring) 20:444-452

    Article  CAS  PubMed  Google Scholar 

  21. DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics:837-845

  22. Procopet B, Berzigotti A, Abraldes JG et al (2015) Real-time shear-wave elastography: applicability, reliability and accuracy for clinically significant portal hypertension. J Hepatol 62:1068-1075

    Article  PubMed  Google Scholar 

  23. Jeon SK, Lee JM, Joo I, Yoon JH, Lee G (2023) Two-dimensional convolutional neural network using quantitative US for noninvasive assessment of hepatic steatosis in NAFLD. Radiology. https://doi.org/10.1148/radiol.221510:221510

    Article  PubMed  Google Scholar 

  24. Labyed Y, Milkowski A (2020) Novel method for ultrasound-derived fat fraction using an integrated phantom. J Ultrasound Med 39:2427-2438

    Article  PubMed  Google Scholar 

  25. Petroff D, Blank V, Newsome PN et al (2021) Assessment of hepatic steatosis by controlled attenuation parameter using the M and XL probes: an individual patient data meta-analysis. Lancet Gastroenterol Hepatol 6:185-198

    Article  PubMed  Google Scholar 

  26. Jang JK, Choi SH, Lee JS, Kim SY, Lee SS, Kim KW (2022) Accuracy of the ultrasound attenuation coefficient for the evaluation of hepatic steatosis: a systematic review and meta-analysis of prospective studies. Ultrasonography 41:83-92

    Article  PubMed  Google Scholar 

  27. Bae JS, Lee DH, Lee JY et al (2019) Assessment of hepatic steatosis by using attenuation imaging: a quantitative, easy-to-perform ultrasound technique. Eur Radiol 29:6499-6507

    Article  PubMed  Google Scholar 

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Funding

This work was supported by the Science and Technology Commission of Shanghai Municipality [19DZ2251100]; Shanghai Municipal Health Commission [2019LJ21 and SHSLCZDZK 03502], Pilot Medical Construction Project of Fudan University (Grant IDF 152076), Scientific Research and Development Fund of Zhongshan Hospital of Fudan University [2022ZSQD07] and Health Commission Health Sector Clinical Research Special Clinical Project [202340087].

Author information

Author notes

  1. Yuli Zhu, Haohao Yin and Da Zhou have contributed equally to this work.

Authors and Affiliations

  1. Department of Ultrasound, Zhongshan Hospital, Fudan University, No. 180 Fenglin Road, Shanghai, 200032, China

    Yuli Zhu, Haohao Yin, Qiannan Zhao, Kun Wang, Yunling Fan, Kailing Chen, Hong Han & Huixiong Xu

  2. Shanghai Institute of Medical Imaging, Fudan University, Shanghai, 200032, China

    Haohao Yin

  3. Institute of Ultrasound in Medicine and Engineering, Fudan University, Shanghai, 200032, China

    Haohao Yin

  4. Department of Gastroenterology, Zhongshan Hospital, Fudan University, Shanghai, 200032, China

    Da Zhou

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  1. Yuli Zhu
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Contributions

The authors thank the research participants for making this study possible, HX: conceptualization, funding acquisition, supervision, resources, writing-review & editing. HH: supervision, funding acquisition, writing-review & editing. YZ, HY, DZ: methodology, data curation, resources, writing—original draft, writing—review & editing. QZ, KW, YF, KC: methodology, data curation, resources.

Corresponding authors

Correspondence to Hong Han or Huixiong Xu.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the Ethics Committee of Zhongshan Hospital, Fudan University (B2021-0921R). Informed consent was obtained from all individual participants included in the study and patients signed informed consent regarding publishing their data and photographs.

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Zhu, Y., Yin, H., Zhou, D. et al. A prospective comparison of three ultrasound-based techniques in quantitative diagnosis of hepatic steatosis in NAFLD. Abdom Radiol 49, 81–92 (2024). https://doi.org/10.1007/s00261-023-04078-7

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