Skip to main content

Technical feasibility and correlations between shear-wave elastography and histology in kidney fibrosis in children

Abstract

Background

Ultrasound elastography has been suggested for assessing organ fibrosis.

Objective

To study the feasibility of shear-wave elastography in children with kidney disease and the correlation between elasticity and kidney fibrosis in order to reduce the indications for kidney biopsy and its complications.

Materials and methods

Four operators measured kidney elasticity in children with kidney diseases or transplants, all of whom also had a renal biopsy. We assessed the feasibility and the intraobserver variability of the elasticity measurements for each probe used and each kidney explored. Then we tested the correlation between elasticity measurements and the presence of fibrosis.

Results

Overall, we analyzed 95 children and adolescents, 31 of whom had renal transplant. Measurements with the convex probe were possible in 100% of cases. Linear probe analysis was only possible for 20% of native kidneys and 50% of transplants. Intraobserver variabilities ranged from moderate to high, depending on the probe and kidney studied. Elasticity was higher with the linear probe than with the convex probe (P<0.001 for left kidney and P=0.03 for right kidney). Measurements did not differ from one kidney to another in the same child. Elasticity and fibrosis were both higher in transplant patients (P=0.02 with convex probe; P=0.01 with linear probe; P=0.04 overall). There was no correlation between elasticity and fibrosis.

Conclusion

Of the devices used in this work, kidney elastography was more accurately analyzed with a convex probe. Our study did not identify any correlation between elasticity and kidney fibrosis.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. 1.

    European Association for Study of Liver, Asociacion Latinoamericana para el Estudio del Higado (2015) EASL-ALEH clinical practice guidelines: non-invasive tests for evaluation of liver disease severity and prognosis. J Hepatol 63:237–264

    Article  Google Scholar 

  2. 2.

    Barr RG, Ferraioli G, Palmeri ML et al (2015) Elastography assessment of liver fibrosis: Society of Radiologists in Ultrasound consensus conference statement. Radiology 276:845–861

    PubMed  PubMed Central  Article  Google Scholar 

  3. 3.

    Ferraioli G, Filice C, Castera L et al (2015) WFUMB guidelines and recommendations for clinical use of ultrasound elastography: part 3: liver. Ultrasound Med Biol 41:1161–1179

    PubMed  Article  PubMed Central  Google Scholar 

  4. 4.

    Pariente D, Franchi-Abella S (2010) Paediatric chronic liver diseases: how to investigate and follow up? Role of imaging in the diagnosis of fibrosis. Pediatr Radiol 40:906–919

    PubMed  Article  PubMed Central  Google Scholar 

  5. 5.

    Franchi-Abella S, Corno L, Gonzales E et al (2015) Feasibility and diagnostic accuracy of supersonic shear-wave elastography for the assessment of liver stiffness and liver fibrosis in children: a pilot study of 96 patients. Radiology 278:554–562

    PubMed  Article  PubMed Central  Google Scholar 

  6. 6.

    Kotlyar DS, Blonski W, Rustgi VK (2008) Noninvasive monitoring of hepatitis C fibrosis progression. Clin Liver Dis 12:557–571

    PubMed  Article  PubMed Central  Google Scholar 

  7. 7.

    Chen S, Liao B, Zhong Z et al (2016) Supersonic shearwave elastography in the assessment of liver fibrosis for postoperative patients with biliary atresia. Sci Rep 6:31057

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 8.

    Peride I, Rădulescu D, Niculae A et al (2016) Value of ultrasound elastography in the diagnosis of native kidney fibrosis. Med Ultrason 18:362–369

    PubMed  Article  PubMed Central  Google Scholar 

  9. 9.

    Wang L (2016) Applications of acoustic radiation force impulse quantification in chronic kidney disease: a review. Ultrasonography 35:302–308

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Yoo MG, Jung DC, Oh YT et al (2017) Usefulness of multiparametric ultrasound for evaluating structural abnormality of transplanted kidney: can we predict histologic abnormality on renal biopsy in advance? AJR Am J Roentgenol 209:139–144

    Article  Google Scholar 

  11. 11.

    Grenier N, Poulain S, Lepreux S et al (2012) Quantitative elastography of renal transplants using supersonic shear imaging: a pilot study. Eur Radiol 22:2138–2146

    PubMed  Article  PubMed Central  Google Scholar 

  12. 12.

    Stock KF, Klein BS, Cong MT et al (2011) ARFI-based tissue elasticity quantification and kidney graft dysfunction: first clinical experiences. Clin Hemorheol Microcirc 49:527–535

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. 13.

    Arndt R, Schmidt S, Loddenkemper C et al (2010) Noninvasive evaluation of renal allograft fibrosis by transient elastography — a pilot study. Transpl Int 23:871–877

    PubMed  PubMed Central  Google Scholar 

  14. 14.

    Ghonge NP, Mohan M, Kashyap V, Jasuja S (2018) Renal allograft dysfunction: evaluation with shear-wave sonoelastography. Radiology 288:146–152

    PubMed  Article  PubMed Central  Google Scholar 

  15. 15.

    Ma MK, Law HK, Tse KS et al (2018) Non-invasive assessment of kidney allograft fibrosis with shear wave elastography: a radiological–pathological correlation analysis. Int J Urol 25:450–455

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  16. 16.

    Chiocchini ALC, Sportoletti C, Comai G et al (2017) Correlation between renal cortical stiffness and histological determinants by point shear-wave elastography in patients with kidney transplantation. Prog Transplant 27:346–353

    PubMed  Article  PubMed Central  Google Scholar 

  17. 17.

    Kim BJ, Kim CK, Park JJ (2018) Non-invasive evaluation of stable renal allograft function using point shear-wave elastography. Br J Radiol 91:20170372

    PubMed  Article  PubMed Central  Google Scholar 

  18. 18.

    Lee J, Oh YT, Joo DJ et al (2015) Acoustic radiation force impulse measurement in renal transplantation. A prospective, longitudinal study with protocol biopsies. Medicine 94:e1590

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. 19.

    He WY, Jin YJ, Wang WP et al (2014) Tissue elasticity quantification by acoustic radiation force impulse for the assessment of renal allograft function. Ultrasound Med Biol 40:322–329

    PubMed  Article  PubMed Central  Google Scholar 

  20. 20.

    Early HM, Cheang EC, Aguilera JM et al (2018) Utility of shear wave elastography for assessing allograft fibrosis in renal transplant recipients: a pilot study. J Ultrasound Med 37:1455–1465

    PubMed  Article  PubMed Central  Google Scholar 

  21. 21.

    Syversveen T, Brabrand K, Midtvedt K et al (2010) Assessment of renal allograft fibrosis by acoustic radiation force impulse quantification — a pilot study. Transplant Int 24:100–105

    Article  Google Scholar 

  22. 22.

    Radulescu D, Peride I, Petcu LC et al (2018) Supersonic shear wave ultrasonography for assessing tissue stiffness in native kidney. Ultrasound Med Biol 44:2556–2568

    PubMed  Article  PubMed Central  Google Scholar 

  23. 23.

    Habibi HA, Cicek RY, Kandemirli SG et al (2017) Acoustic radiation force impulse (ARFI) elastography in the evaluation of renal parenchymal stiffness in patients with ureteropelvic junction obstruction. J Medic Ultrason 44:167–172

    Article  Google Scholar 

  24. 24.

    Sohn B, Kim MJ, Han SW et al (2014) Shear wave velocity measurements using acoustic radiation force impulse in young children with normal kidneys versus hydronephrotic kidneys. Ultrasonography 33:116–121

    PubMed  PubMed Central  Article  Google Scholar 

  25. 25.

    Gennisson JL, Grenier N, Combe C, Tanter M (2012) Supersonic shear wave elastography of in vivo pig kidney: influence of blood pressure, urinary pressure and tissue anisotropy. Ultrasound Med Biol 38:1559–1567

    PubMed  Article  PubMed Central  Google Scholar 

  26. 26.

    Derieppe M, Delmas Y, Gennisson J-L et al (2012) Detection of intrarenal microstructural changes with supersonic shear wave elastography in rats. Eur Radiol 22:243–250

    PubMed  Article  PubMed Central  Google Scholar 

  27. 27.

    Liu X, Li N, Xu T et al (2012) Detection of intrarenal microstructural changes with supersonic shear wave elastography in rats. Eur Radiol 22:243–250

    Article  Google Scholar 

  28. 28.

    Bercoff J, Tanter M, Fink M (2004) Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control 51:396–409

    PubMed  PubMed Central  Article  Google Scholar 

  29. 29.

    Grenier N, Gennisson JL, Cornelis F et al (2013) Renal ultrasound elastography. Diagn Interv Imaging 94:545–550

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  30. 30.

    Bruno C, Minniti S, Bucci A et al (2016) ARFI: from basic principles to clinical applications in diffuse chronic disease. Insights Imaging 7:735–746

    PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

    Correas JM, Anglicheau D, Gennisson JL, Tanter M (2016) Renal elastography. Nephrol Therap 12:S25–S34

    Article  Google Scholar 

  32. 32.

    Grass L, Szekely N, Alrajab A et al (2017) Point shear wave elastography (pSWE) using acoustic radiation force impulse (ARFI) imaging: a feasibility study and norm values for renal parenchymal stiffness in healthy children and adolescents. Med Ultrason 19:366–373

    PubMed  Article  PubMed Central  Google Scholar 

  33. 33.

    Lee MJ, Kim MJ, Han KH, Yoon CS (2013) Age-related changes in liver, kidney, and spleen stiffness in healthy children measured with acoustic radiation force impulse imaging. Eur J Radiol 82:e290–e294

    PubMed  Article  PubMed Central  Google Scholar 

  34. 34.

    Franchi-Abella S, Elie C, Correas JM (2013) Ultrasound elastography: advantages, limitations and artefacts of the different techniques from a study on a phantom. Diagn Interv Imaging 94:497–501

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  35. 35.

    Chang S, Kim MJ, Kim J, Lee MJ (2013) Variability of shear wave velocity using different frequencies in acoustic radiation force impulse (ARFI) elastography: a phantom and normal liver study. Ultraschall Med 34:260–265

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Göya C, Hamidi C, Ece A et al (2015) Acoustic radiation force impulse (ARFI) elastography for detection of renal damage in children. Pediatr Radiol 45:55–61

    PubMed  Article  PubMed Central  Google Scholar 

  37. 37.

    Saglam D, Bilgici MC, Kara C et al (2017) Acoustic radiation force impulse elastography in determining the effects of type 1 diabetes on pancreas and kidney elasticity in children. AJR Am J Roentgenol 209:1143–1149

    PubMed  Article  PubMed Central  Google Scholar 

  38. 38.

    Bota S, Bob F, Sporea I et al (2015) Factors that influence kidney shear wave speed assessed by acoustic radiation force impulse elastography in patients without kidney pathology. Ultrasound Med Biol 41:1–6

    PubMed  Article  PubMed Central  Google Scholar 

  39. 39.

    Asano K, Ogata A, Tanaka K et al (2014) Acoustic radiation force impulse elastography of the kidneys: is shear wave velocity affected by tissue fibrosis or renal blood flow? J Ultrasound Med 33:793–801

    PubMed  Article  PubMed Central  Google Scholar 

  40. 40.

    Guo L-H, Xu H-X, Fu H-J et al (2013) Acoustic radiation force impulse imaging for noninvasive evaluation of renal parenchyma elasticity: preliminary findings. PLoS One 8:e68925

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. 41.

    Singh H, Biju Panta O, Khanal U, Kumar Ghimire R (2017) Renal cortical elastography: normal values and variations. J Med Ultrasound 25:215–220

    PubMed  PubMed Central  Article  Google Scholar 

  42. 42.

    Bob F, Bota S, Sporea I et al (2014) Kidney shear wave speed values in subjects with and without renal pathology and inter-operator reproducibility of acoustic radiation force impulse elastography (ARFI) — preliminary results. PLoS One 9:e113761

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  43. 43.

    Bota S, Sporea I, Sirli R et al (2012) Intra- and interoperator reproducibility of acoustic radiation force impulse (ARFI) elastography — preliminary results. Ultrasound Med Biol 38:1103–1108

    PubMed  Article  PubMed Central  Google Scholar 

  44. 44.

    Dillman JR, Smith EA, Davenport MS et al (2015) Can shear-wave elastography be used to discriminate obstructive hydronephrosis from nonobstructive hydronephrosis in children? Radiology 277:259–267

    PubMed  Article  PubMed Central  Google Scholar 

  45. 45.

    Bruno C, Caliari G, Zaffanello M et al (2013) Acoustic radiation force impulse (ARFI) in the evaluation of the renal parenchymal stiffness in paediatric patients with vesicoureteral reflux: preliminary results. Eur Radiol 23:3477–3484

    PubMed  Article  PubMed Central  Google Scholar 

  46. 46.

    Kalyoncu Ucar A, Cicek RY, Alis D et al (2019) Shear wave elastography in the evaluation of the kidneys in pediatric patients with unilateral vesicoureteral reflux. J Ultrasound Med 38:379–385

    PubMed  Article  PubMed Central  Google Scholar 

  47. 47.

    Xu B, Jiang G, Ye J et al (2016) Research on pediatric glomerular disease and normal kidney with shear wave based elastography point quantification. Jpn J Radiol 34:738–746

    PubMed  Article  PubMed Central  Google Scholar 

  48. 48.

    Bilgici MC, Bekci T, Genc G et al (2017) Acoustic radiation force impulse quantification in the evaluation of renal parenchyma elasticity in pediatric patients with chronic kidney disease: preliminary results. J Ultrasound Med 36:1555–1561

    PubMed  Article  PubMed Central  Google Scholar 

  49. 49.

    Goya C, Kilinc F, Hamidi C et al (2015) Acoustic radiation force impulse imaging for evaluation of renal parenchyma elasticity in diabetic nephropathy. AJR Am J Roentgenol 204:324–329

    PubMed  Article  PubMed Central  Google Scholar 

  50. 50.

    Samir AE, Allegretti AS, Zhu Q et al (2015) Shear wave elastography in chronic kidney disease: a pilot experience in native kidneys. BMC Nephrol 16:119

    PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

    el Nahas AM, Muchaneta-Kubara EC, Essawy M, Soylemezoglu O (1997) Renal fibrosis: insights into pathogenesis treatment. Int J Biochem Cell Biol 29:55–62

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  52. 52.

    Urban MW, Chen S, Fatemi M (2012) A review of shearwave dispersion ultrasound vibrometry (SDUV) and its applications. Med Imaging Rev 8:27–36

    Article  Google Scholar 

  53. 53.

    Chen S, Sanchez W, Callstrom MR et al (2013) Assessment of liver viscoelasticity by using shear waves induced by ultrasound radiation force. Radiology 266:964–970

    PubMed  PubMed Central  Article  Google Scholar 

  54. 54.

    Warner L, Yin M, Glaser KJ et al (2011) Noninvasive in vivo assessment of renal tissue elasticity during graded renal ischemia using MR elastography. Investig Radiol 46:509–514

    Article  Google Scholar 

  55. 55.

    Syversveen T, Midtvedt K, Berstad AE et al (2012) Tissue elasticity estimated by acoustic radiation force impulse quantification depends on the applied transducer force: an experimental study in kidney transplant patients. Eur Radiol 10:2130–2137

    Article  Google Scholar 

  56. 56.

    Gennisson J-L, Renier M, Catheline S et al (2007) Acoustoelasticity in soft solids: assessment of the nonlinear shear modulus with the acoustic radiation force. J Acoust Soc Am 122:3211–3219

    PubMed  Article  PubMed Central  Google Scholar 

  57. 57.

    Naesens M, Kuypers DRJ, De Vusser K et al (2014) The histology of kidney transplant failure: a long-term follow-up study. Transplantation 98:427–435

    PubMed  Article  PubMed Central  Google Scholar 

  58. 58.

    Dillman JR, Chen S, Davenport MS et al (2015) Superficial ultrasound shear wave speed measurements in soft and hard elasticity phantoms: repeatability and reproducibility using two ultrasound systems. Pediatr Radiol 45:376–385

    PubMed  Article  PubMed Central  Google Scholar 

Download references

Acknowledgments

The study was funded by Assistance Publique Hôpitaux de Marseille (Délégation de la Recherche Clinique et Innovation-Unité Coordination et Contrôle Qualité).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Guillaume Gorincour.

Ethics declarations

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

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Desvignes, C., Dabadie, A., Aschero, A. et al. Technical feasibility and correlations between shear-wave elastography and histology in kidney fibrosis in children. Pediatr Radiol 51, 1879–1888 (2021). https://doi.org/10.1007/s00247-021-05068-x

Download citation

Keywords

  • Adolescents
  • Children
  • Fibrosis
  • Kidney
  • Shear-wave elastography
  • Transplant
  • Ultrasound