Log in

Ultrasound attenuation imaging: a reproducible alternative for the noninvasive quantitative assessment of hepatic steatosis in children

  • Original Article
  • Published:
Pediatric Radiology Aims and scope Submit manuscript

Abstract

Background

Pediatric hepatic steatosis is a global public health concern, as an increasing number of children are affected by this condition. Liver biopsy is the gold standard diagnostic method; however, this procedure is invasive. Magnetic resonance imaging (MRI)-derived proton density fat fraction has been accepted as an alternative to biopsy. However, this method is limited by cost and availability. Ultrasound (US) attenuation imaging is an upcoming tool for noninvasive quantitative assessment of hepatic steatosis in children. A limited number of publications have focused on US attenuation imaging and the stages of hepatic steatosis in children.

Objective

To analyze the usefulness of ultrasound attenuation imaging for the diagnosis and quantification of hepatic steatosis in children.

Material and methods

Between July and November 2021, 174 patients were included and divided into two groups: group 1, patients with risk factors for steatosis (n = 147), and group 2, patients without risk factors for steatosis (n = 27). In all cases, age, sex, weight, body mass index (BMI), and BMI percentile were determined. B-mode US (two observers) and US attenuation imaging with attenuation coefficient acquisition (two independent sessions, two different observers) were performed in both groups. Steatosis was classified into four grades (0: absent, 1: mild, 2: moderate and 3: severe) using B-mode US. Attenuation coefficient acquisition was correlated with steatosis score according to Spearman’s correlation. Attenuation coefficient acquisition measurements’ interobserver agreement was assessed using intraclass correlation coefficients (ICC).

Results

All attenuation coefficient acquisition measurements were satisfactory without technical failures. The median values for group 1 for the first session were 0.64 (0.57–0.69) dB/cm/MHz and 0.64 (0.60–0.70) dB/cm/MHz for the second session. The median values for group 2 for the first session were 0.54 (0.51–0.56) dB/cm/MHz and 0.54 (0.51–0.56) dB/cm/MHz for the second. The average attenuation coefficient acquisition was 0.65 (0.59–0.69) dB/cm/MHz for group 1 and 0.54 (0.52–0.56) dB/cm/MHz for group 2. There was excellent interobserver agreement at 0.94 (95% CI 0.92–0.96). There was substantial agreement between both observers (κ = 0.77, with a P < 0.001). There was a positive correlation between ultrasound attenuation imaging and B-mode scores for both observers (r = 0.87, P < 0.001 for observer 1; r = 0.86, P < 0.001 for observer 2). Attenuation coefficient acquisition median values were significantly different for each steatosis grade (P < 0.001). In the assessment of steatosis by B-mode US, the agreement between the two observers was moderate (κ = 0.49 and κ = 0.55, respectively, with a P < 0.001 in both cases).

Conclusion

US attenuation imaging is a promising tool for the diagnosis and follow-up of pediatric steatosis, which provides a more repeatable form of classification, especially at low levels of steatosis detectable in B-mode US.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Tzifi F, Fretzayas A, Chrousos G, Kanaka-Gantenbein C (2019) Non-alcoholic fatty liver infiltration in children: an underdiagnosed evolving disease. Hormones 18:255–265

    Article  PubMed  Google Scholar 

  2. Draijer L, Benninga M, Koot B (2019) Pediatric NAFLD: an overview and recent developments in diagnostics and treatment. Expert Rev Gastroenterol Hepatol 13:447–461

    Article  CAS  PubMed  Google Scholar 

  3. Mencin AA, Lavine JE (2011) Nonalcoholic fatty liver disease in children. Curr Opin Clin Nutr Metab Care 14:151–157

    CAS  PubMed  Google Scholar 

  4. Lee SS, Park SH, Kim HJ et al (2010) Non-invasive assessment of hepatic steatosis: prospective comparison of the accuracy of imaging examinations. J Hepatol 52:579–585

    Article  CAS  PubMed  Google Scholar 

  5. Shannon A, Alkhouri N, Carter-Kent C et al (2011) Ultrasonographic quantitative estimation of hepatic steatosis in children with NAFLD. J Pediatr Gastroenterol Nutr 53:190–195

    Article  PubMed  PubMed Central  Google Scholar 

  6. Permutt Z, Le TA, Peterson MR et al (2012) Correlation between liver histology and novel magnetic resonance imaging in adult patients with non-alcoholic fatty liver disease - MRI accurately quantifies hepatic steatosis in NAFLD. Aliment Pharmacol Ther 36:22–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Schwimmer JB, Middleton MS, Behling C et al (2015) Magnetic resonance imaging and liver histology as biomarkers of hepatic steatosis in children with nonalcoholic fatty liver disease. Hepatology 61:1887–1895

    Article  CAS  PubMed  Google Scholar 

  8. Ferraioli G, Calcaterra V, Lissandrin R et al (2017) Noninvasive assessment of liver steatosis in children: the clinical value of controlled attenuation parameter. BMC Gastroenterol 17:61

    Article  PubMed  PubMed Central  Google Scholar 

  9. Desai NK, Harney S, Raza R et al (2016) Comparison of controlled attenuation parameter and liver biopsy to assess hepatic steatosis in pediatric patients. J Pediatr 173:160–164

    Article  PubMed  PubMed Central  Google Scholar 

  10. Shin J, Kim MJ, Shin HJ et al (2019) Quick assessment with controlled attenuation parameter for hepatic steatosis in children based on MRI-PDFF as the gold standard. BMC Pediatr 19:112

    Article  PubMed  PubMed Central  Google Scholar 

  11. Dioguardi Burgio M, Ronot M, Reizine E et al (2020) Quantification of hepatic steatosis with ultrasound: promising role of attenuation imaging coefficient in a biopsy-proven cohort. Eur Radiol 30:2293–2301

    Article  PubMed  Google Scholar 

  12. 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 

  13. 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. Clin Transl Gastroenterol 10:e00081

    Article  PubMed  PubMed Central  Google Scholar 

  14. Jeon SK, Lee JM, Joo I et al (2019) Prospective evaluation of hepatic steatosis using ultrasound attenuation imaging in patients with chronic liver disease with magnetic resonance imaging proton density fat fraction as the reference standard. Ultrasound Med Biol 45:1407–1416

    Article  PubMed  Google Scholar 

  15. Tada T, Iijima H, Kobayashi N et al (2019) Usefulness of attenuation imaging with an ultrasound scanner for the evaluation of hepatic steatosis. Ultrasound Med Biol 45:2679–2687

    Article  PubMed  Google Scholar 

  16. Yoo J, Lee JM, Joo I et al (2020) Reproducibility of ultrasound attenuation imaging for the noninvasive evaluation of hepatic steatosis. Ultrasonography 39:121–129

    Article  PubMed  Google Scholar 

  17. Tada T, Kumada T, Toyoda H et al (2020) Attenuation imaging based on ultrasound technology for assessment of hepatic steatosis: a comparison with magnetic resonance imaging-determined proton density fat fraction. Hepatol Res 50:1319–1327

    Article  CAS  PubMed  Google Scholar 

  18. Hsu PK, Wu LS, Yen HH et al (2021) Attenuation imaging with ultrasound as a novel evaluation method for liver steatosis. J Clin Med 10:965

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kwon EY, Kim YR, Kang DM et al (2021) Usefulness of US attenuation imaging for the detection and severity grading of hepatic steatosis in routine abdominal ultrasonography. Clin Imaging 76:53–59

    Article  PubMed  Google Scholar 

  20. Lee DH, Cho EJ, Bae JS et al (2021) Accuracy of two-dimensional shear wave elastography and attenuation imaging for evaluation of patients with nonalcoholic steatohepatitis. Clin Gastroenterol Hepatol 19(4):797-805.e7

    Article  PubMed  Google Scholar 

  21. Sugimoto K, Moriyasu F, Oshiro H et al (2020) The role of multiparametric US of the liver for the evaluation of nonalcoholic steatohepatitis. Radiology 296:532–540

    Article  PubMed  Google Scholar 

  22. Cailloce R, Tavernier E, Brunereau L et al (2021) Liver shear wave elastography and attenuation imaging coefficient measures: prospective evaluation in healthy children. Abdom Radiol (NY) 46:4629–4636

    Article  PubMed  Google Scholar 

  23. Song K, Son NH, Chang DR et al (2022) Feasibility of ultrasound attenuation imaging for assessing pediatric hepatic steatosis. Biology (Basel) 11:1087

    PubMed  Google Scholar 

  24. Dr. Hiroko Iijima (2020) Assessment of non-alcoholic fatty liver disease with Attenuation Imaging (ATI) https://us.medical.canon/download/ul-wp-fatty-liver-disease-ati.pdf consultation date 12/16/2022

  25. Canon (2021–2022) Canon Operation Manual. 12:391–398

  26. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  CAS  PubMed  Google Scholar 

  27. Koo TK, Li M, Y, (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15:155–163

    Article  PubMed  PubMed Central  Google Scholar 

  28. Alves VPV, Dillman JR, Tkach JA et al (2022) Comparison of quantitative liver US and MRI in patients with liver disease. Radiology 304:660–669

    Article  PubMed  Google Scholar 

  29. D’Hondt A, Rubesova E, **e H et al (2021) Liver fat quantification by ultrasound in children: a prospective study. AJR Am J Roentgenol 217:996–1006

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Esteban P. Dardanelli.

Ethics declarations

Ethics approval

Approval was obtained from the ethics committee of Garrahan Hospital. The procedures used in this study adhere to the tenets of the Declaration of Helsinki.

Consent for publication

Informed consent was obtained from all individual participants included in this study.

Conflicts of interest

None.

Additional information

Publisher's Note

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

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

Dardanelli, E.P., Orozco, M.E., Oliva, V. et al. Ultrasound attenuation imaging: a reproducible alternative for the noninvasive quantitative assessment of hepatic steatosis in children. Pediatr Radiol 53, 1618–1628 (2023). https://doi.org/10.1007/s00247-023-05601-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00247-023-05601-0

Keywords

Navigation