Skip to main content

Advertisement

Log in

The efficiency of acoustic radiation force impulse imaging for the staging of liver fibrosis: a meta-analysis

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

Abstract

Objectives

Acoustic radiation force impulse (ARFI) imaging is an ultrasound-based elastography method that is integrated into a conventional ultrasound machine. A meta-analysis based on original and abstract publications was performed to evaluate the overall performance of ARFI for the diagnosis of liver fibrosis.

Methods

Literature databases and conference abstracts were searched from 2007 up to February 2012. A random effects meta-analysis of the area under the receiver operating characteristic (ROC) curve (AUROC) and the diagnostic odds ratio (DOR) was performed as well as summary ROC curve techniques. Quality analyses were conducted to assess sources of heterogeneity.

Results

The systematic literature search revealed 36 studies, with 3,951 patients overall. The mean diagnostic accuracy of ARFI expressed as the AUROC was 0.84 (DOR, 11.54) for the diagnosis of significant fibrosis (F ≥ 2), 0.89 (DOR, 33.54) for the diagnosis of severe fibrosis (F ≥ 3) and 0.91 (DOR, 45.35) for the diagnosis of liver cirrhosis (F = 4). Subgroup analyses showed sources of heterogeneity between the different underlying liver diseases for F ≥ 3 and F = 4. The mean body mass index had a significant influence for F ≥ 2.

Conclusions

The meta-analysis revealed good diagnostic accuracy of the ARFI imaging for the staging of F ≥ 2 and F ≥ 3, and excellent diagnostic accuracy for F = 4.

Key Points

• Acoustic radiation force impulse (ARFI) imaging adds important information over conventional ultrasound.

• ARFI imaging provides good diagnostic performance for assessing significant/severe hepatic fibrosis.

• ARFI imaging shows excellent diagnostic accuracy and odds ratio for cirrhosis staging.

• Body mass index significantly influences the assessment of significant fibrosis.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ARFI:

Acoustic radiation force impulse

AUROC:

Area under the ROC curve

CLD:

Chronic liver disease

DOR:

Diagnostic odds ratio

F:

Fibrosis stage

HBV:

Chronic hepatitis B

HCV:

Chronic hepatitis C

IPD:

Individual patient data

ROC:

Receiver operating characteristic curve

SROC:

Summary ROC

TE:

Transient elastography

References

  1. Lauer GM, Walker BD (2001) Hepatitis C virus infection. N Engl J Med 345:41–52

    Article  PubMed  CAS  Google Scholar 

  2. Strader DB, Wright T, Thomas DL, Seeff LB, American Association for the Study of Liver Diseases (2004) Diagnosis, management, and treatment of hepatitis C. Hepatology 39:1147–1171

    Article  PubMed  Google Scholar 

  3. Lok AS, McMahon BJ (2007) Chronic hepatitis B. Hepatology 45:507–539

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  6. Friedrich-Rust M, Ong MF, Martens S, Sarrazin C, Bojunga J, Zeuzem S et al (2008) Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology 134:960–974

    Article  PubMed  Google Scholar 

  7. Talwalkar JA, Kurtz DM, Schoenleber SJ, West CP, Montori VM (2007) Ultrasound-based transient elastography for the detection of hepatic fibrosis: systematic review and meta-analysis. Clin Gastroenterol Hepatol 5:1214–1220

    Article  PubMed  Google Scholar 

  8. Stebbing J, Farouk L, Panos G, Anderson M, Jiao LR, Bower M et al (2010) A meta-analysis of transient elastography for the detection of hepatic fibrosis. J Clin Gastroenterol 44:214–219

    Article  PubMed  Google Scholar 

  9. Shaheen AA, Wan AF, Myers RP (2007) FibroTest and FibroScan for the prediction of hepatitis C-related Fibrosis: a systematic review of diagnostic test accuracy. Am J Gastroenterol 102:2589–2600

    Article  PubMed  Google Scholar 

  10. Smith JO, Sterling RK (2009) Systematic review: non-invasive methods of fibrosis analysis in chronic hepatitis C. Aliment Pharmacol Ther 30:557–576

    Article  PubMed  CAS  Google Scholar 

  11. European Association For The Study Of The Liver, European Organisation For Research And Treatment Of Cancer (2012) EASL–EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56:908–943

    Google Scholar 

  12. Nightingale K, Soo MS, Nightingale RL, Trahey G (2002) Acoustic radiation force impulse imaging: in vivo demonstration of clinical feasibility. Ultrasound Med Biol 28:227–235

    Article  PubMed  Google Scholar 

  13. Nightingale KR, Zhai L, Dahl JJ, Frinkley KD, Palmeri ML (2006) Shear wave velocity estimation using acoustic radiation force impulsive excitation in liver in vivo. Proceedings of IEEE Ultrasonics Symposium 2006. Institute of Electrical and Electronics Engineers, Vancouver, pp 1156–1160

    Google Scholar 

  14. Kasai C, Namekawa K, Koyano A, Omoto R (1985) Real-time two-dimensional blood flow imaging using an auto-correlation technique. IEEE Trans Son Ultrason 32:458–464

    Article  Google Scholar 

  15. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    Article  PubMed  CAS  Google Scholar 

  16. Friedrich-Rust M, Nierhoff J, Lupsor M, Sporea I, Fierbinteanu-Braticevici C, Strobel D et al (2012) Performance of acoustic radiation force impulse imaging for the staging of liver fibrosis: a pooled meta-analysis. J Viral Hepat 19:212–219

    Article  Google Scholar 

  17. Arends LR, Hamza TH, van Houwelingen JC, Heijenbrok-Kal MH, Hunink MGM, Stijnen T (2008) Bivariate random effects meta-analysis of ROC curves. Med Decis Making 621–638

  18. Deeks JJ, Macaskill P, Irwig L (2005) The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol 58:882–893

    Article  PubMed  Google Scholar 

  19. Begg CB, Mazumdar M (1994) Operating characteristics of rank correlation test for publication bias. Biometrics 50:1088–1101

    Article  PubMed  CAS  Google Scholar 

  20. Duval S, Tweedie R (2000) A nonparametric “Trim and Fill” method of accounting for publication bias in meta-analysis. J Am Stat Assoc 95:89–98

    Google Scholar 

  21. Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J (2003) The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol 3:25

    Article  PubMed  Google Scholar 

  22. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 62:e1–e34

    Article  PubMed  Google Scholar 

  23. Fierbinteanu-Braticevici C, Andronescu D, Usvat R, Cretoiu D, Baicus C, Martinoschi G (2009) Acoustic Radiation Force Imaging Sonoelastography for noninvasive staging of liver fibrosis. World J Gastroenterol 15:5525–5532

    Article  PubMed  Google Scholar 

  24. Friedrich-Rust M, Wunder K, Kriener S, Sotoudeh F, Richter S, Bojunga J et al (2009) Liver fibrosis in viral hepatitis: noninvasive assessment with acoustic radiation force impulse imaging versus transient elastography. Radiology 252:595–604

    Article  PubMed  Google Scholar 

  25. Lupsor M, Badea R, Stefanescu H, Sparchez Z, Branda H, Serban A et al (2009) Performance of a new elastographic method (ARFI technology) compared to unidimensional transient elastography in the noninvasive assessment of chronic hepatitis C. Preliminary results. J Gastrointestin Liver Dis 18:303–310

    PubMed  Google Scholar 

  26. Goertz RS, Zopf Y, Jugl V, Heide R, Janson C, Strobel D et al (2010) Measurement of liver elasticity with acoustic radiation force impulse (ARFI) technology: an alternative noninvasive method for staging liver fibrosis in viral hepatitis. Ultraschall Med 31:151–155

    Article  PubMed  CAS  Google Scholar 

  27. Haque M, Robinson C, Owen D, Yoshida EM, Harris A (2010) Comparison of Acoustic Radiation Force Impulse Imaging (ARFI) to liver biopsy histologic scores in the evaluation of chronic liver disease: a pilot study. Ann Hepatol 9:289–293

    PubMed  Google Scholar 

  28. Kuroda H, Kakisaka K, Tatemichi Y, Sawara K, Miyamoto Y, Oikawa K et al (2010) Non-invasive evaluation of liver fibrosis using acoustic radiation force impulse imaging in chronic hepatitis patients with hepatitis C virus infection. Hepatogastroenterology 57:1203–1207

    PubMed  Google Scholar 

  29. Osaki A, Kubota T, Suda T, Igarashi M, Nagasaki K, Tsuchiya A et al (2010) Shear wave velocity is a useful marker for managing nonalcoholic steatohepatitis. World J Gastroenterol 16:2918–25

    Article  PubMed  Google Scholar 

  30. Takahashi H, Ono N, Eguchi Y, Eguchi T, Kitajima Y, Kawaguchi Y et al (2010) Evaluation of acoustic radiation force impulse elastography for fibrosis staging of chronic liver disease: a pilot study. Liver Int 30:538–545

    Article  PubMed  Google Scholar 

  31. Yoneda M, Suzuki K, Kato S, Fujita K, Nozaki Y, Hosono K et al (2010) Nonalcoholic fatty liver disease: US-based acoustic radiation force impulse elastography. Radiology 256:640–647

    Article  PubMed  Google Scholar 

  32. Ebinuma H, Saito H, Komuta M, Ojiro K, Wakabayashi K, Usui S et al (2011) Evaluation of liver fibrosis by transient elastography using acoustic radiation force impulse: comparison with Fibroscan(®). J Gastroenterol 46:1238–1248

    Article  PubMed  Google Scholar 

  33. Grgurevic I, Cikara I, Horvat J, Lukic IK, Heinzl R, Banic M et al (2011) Noninvasive assessment of liver fibrosis with acoustic radiation force impulse imaging: increased liver and splenic stiffness in patients with liver fibrosis and cirrhosis. Ultraschall Med 32:160–166

    Article  PubMed  CAS  Google Scholar 

  34. Karlas T, Pfrepper C, Wiegand J, Wittekind C, Neuschulz M, Mössner J et al (2011) Acoustic radiation force impulse imaging (ARFI) for non-invasive detection of liver fibrosis: examination standards and evaluation of interlobe differences in healthy subjects and chronic liver disease. Scand J Gastroenterol 46:1458–1467

    Article  PubMed  Google Scholar 

  35. Palmeri ML, Wang MH, Rouze NC, Abdelmalek MF, Guy CD, Moser B et al (2011) Noninvasive evaluation of hepatic fibrosis using acoustic radiation force-based shear stiffness in patients with nonalcoholic fatty liver disease. J Hepatol 55:666–672

    Article  PubMed  Google Scholar 

  36. Piscaglia F, Salvatore V, Di Donato R, D’Onofrio M, Gualandi S, Galotti A et al (2011) Accuracy of Virtual Touch Acoustic Radiation Force Impulse (ARFI) imaging for the diagnosis of cirrhosis during liver ultrasonography. Ultraschall Med 32:167–175

    Article  PubMed  CAS  Google Scholar 

  37. Rifai K, Cornberg J, Mederacke I, Bahr MJ, Wedemeyer H, Malinski P et al (2011) Clinical feasibility of liver elastography by acoustic radiation force impulse imaging (ARFI). Dig Liver Dis 43:491–497

    Article  PubMed  Google Scholar 

  38. Rizzo L, Calvaruso V, Cacopardo B, Alessi N, Attanasio M, Petta S et al (2011) Comparison of transient elastography and acoustic radiation force impulse for non-invasive staging of liver fibrosis in patients with chronic hepatitis C. Am J Gastroenterol 106:2112–2120

    Article  PubMed  CAS  Google Scholar 

  39. Sporea I, Badea R, Sirli R, Lupsor M, Popescu A, Danila M et al (2011) How efficient is acoustic radiation force impulse elastography for the evaluation of liver stiffness? Hepat Mon 11:532–538

    Article  PubMed  Google Scholar 

  40. Sporea I, Sirli R, Deleanu A, Popescu A, Focsa M, Danila M et al (2011) Acoustic radiation force impulse elastography as compared to transient elastography and liver biopsy in patients with chronic hepatopathies. Ultraschall Med 32:S46–S52

    Article  PubMed  Google Scholar 

  41. Toshima T, Shirabe K, Takeishi K, Motomura T, Mano Y, Uchiyama H et al (2011) New method for assessing liver fibrosis based on acoustic radiation force impulse: a special reference to the difference between right and left liver. J Gastroenterol 46:705–711

    Article  PubMed  Google Scholar 

  42. Colombo S, Buonocore M, Del Poggio A, Jamoletti C, Elia S, Mattiello M et al (2012) Head-to-head comparison of transient elastography (TE), real-time tissue elastography (RTE) and acoustic radiation force impulse imaging (ARFI) in the diagnosis of liver fibrosis. J Gastroenterol 47:461–469

    Article  PubMed  Google Scholar 

  43. Friedrich-Rust M, Romen D, Vermehren J, Kriener S, Sadet D, Herrmann E et al (2012) Acoustic radiation force impulse imaging and transient elastography for non-invasive assessment of liver fibrosis and steatosis in NAFLD. Eur J Radiol 81:e325–e331

    Article  PubMed  Google Scholar 

  44. Hsu SJ, Liu CH, Kao JH, Chen DS (2009) Acoustic radiation force impulse imaging predicts advanced fibrosis and cirrhosis in chronic hepatitis C patients. Hepatology 50:S1055A–S1056A

    Google Scholar 

  45. Crespo G, Fernández-Varo G, Martínez SM, Miquel R, Gilabert R, Forns X et al (2010) Non-invasive assessment of liver fibrosis using acoustic radiation force impulse imaging (ARFI): a prospective comparison with transient elastography and serum markers. Hepatology 52:S962A

    Google Scholar 

  46. Ferlitsch A, Salzl P, Reiberger T, Homoncik M, Payer B, Schwengerer B (2010) Comparison of liver stiffness assessment by Fibroscan® and Acoustic Radiation Force Impulse Imaging® for the evaluation of liver fibrosis and cirrhosis. Wien Klin Wochenschr 122:A11

    Google Scholar 

  47. Rossini A, Cabassa P, Gatti E, Contessi GB, Morone M, Maroldi R (2010) Assessment of liver fibrosis by Acoustic Radiation Force Impulse Elastography in healthy subjects and patients with chronic hepatitis C. Hepatology 52:S1234A–S1234A

    Google Scholar 

  48. Song C, Hiramatsu N, Inoue Y, Kurokawa M, Oze T, Yakushijn T et al (2010) Non-invasive evaluation of liver fibrosis by using Virtual Touch Tissue Quantification in patients with chronic hepatitis C. Hepatology 52:S1124A–S1124A

    Google Scholar 

  49. Sporea I, Sirli R, Popescu A, Danila M, Bota S (2010) The value of Acoustic Radiation Force Impulse Elastography (ARFI) for the evaluation of liver fibrosis. J Hepatol 52:S173

    Google Scholar 

  50. Yoon KT, Heo J, Woo HY, Cho M (2010) Liver stiffness measurement using Acoustic Radiation Force Impulse Imaging in chronic liver disease. J Hepatol 52:S175A

    Google Scholar 

  51. Fierbinteanu-Braticevici C, Tribus L, Petrisor A, Usvat R, Stan I, Busegeanu C (2011) Role of noninvasive tests for assessing liver fibrosis in patients with chronic hepatitis C. J Hepatol 54:S132

    Article  Google Scholar 

  52. Friedrich-Rust M, Buggisch P, de Knegt RJ, Shi Y, Matschenz K, Schneider MD et al (2011) Acoustic Radiation Force Impulse Imaging for noninvasive assessment of liver fibrosis in chronic hepatitis B. Hepatology 54:S1085A

    Google Scholar 

  53. Kandiah K, Sangwaiya MJ, Tadrous P, Shorvon P, Sherman D (2011) Role of Acoustic Radiation Force Impulse (ARFI) Elastography in the non-invasive assessment of liver fibrosis in chronic viral hepatitis: a simultaneous comparison with liver histology in a secondary care setting. Hepatology 54:S905A

    Google Scholar 

  54. Pfeifer L, Goertz RS, Bernatik T, Neurath MF, Strobel D (2011) Acoustic radiation force impulse versus high-frequency ultrasound for the diagnosis of liver cirrhosis. Ultrasound Med Biol 37:S57A

    Article  Google Scholar 

  55. Sporea I, Sirli R, Bota S, Tanaka H, Iijima H, Badea R et al (2011) Is ARFI Elastography useful for fibrosis evaluation in patients with chronic HCV Hepatitis in our clinical practice? A multicenter international study. Hepatology 54:S559A–S560A

    Google Scholar 

  56. Tanaka H, Iijima H, Yoshida M, Iwai T, Takashima T, Aizawa N et al (2011) Usefulness of virtual touch tissue quantification to diagnose the severity of fibrosis. Ultrasound Med Biol 37:S58A–S59A

    Article  Google Scholar 

  57. Yoshioka K, Nishikawa T, Hashimoto S, Kawabe N, Harata M, Nitta Y et al (2011) Acoustic radiation force impulse elastography for evaluation of fibrosis stage and prediction of hepatocellular carcinoma in chronic HCV infection. Hepatology 54:570A

    Google Scholar 

  58. Young JJ, Kim SG, Kim YS, Lim JH, Min SK, Lee SH et al (2011) The usefulness of transient elastography, acoustic radiation force impulse elastography and real time elastography for the evaluation of liver fibrosis. Hepatology 54:S1230A

    Google Scholar 

  59. Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293

    Article  PubMed  CAS  Google Scholar 

  60. Ebell MH (2003) Probability of cirrhosis in patients with hepatitis C. Am Fam Physician 68:1831–1833

    PubMed  Google Scholar 

  61. Riley RD, Lambert PC, Abo-Zaid G (2010) Meta-analysis of individual participant data: rationale, conduct, and reporting. BMJ 340:c221

    Article  PubMed  Google Scholar 

  62. McAuley L, Pham B, Tugwell P, Moher D (2000) Does the inclusion of grey literature influence estimates of intervention effectiveness reported in meta-analyses? Lancet 356:1228–1231

    Article  PubMed  CAS  Google Scholar 

  63. Fraquelli M, Rigamonti C, Casazza G, Conte D, Donato MF, Ronchi G et al (2011) Etiology-related determinants of liver stiffness values in chronic viral hepatitis B or C. J Hepatol 54:621–628

    Article  PubMed  Google Scholar 

  64. De Lédinghen V, Wong VW, Vergniol J, Wong GLH, Foucher J, Chu SHT et al (2012) Diagnosis of liver fibrosis and cirrhosis using liver stiffness measurement: comparison between M and XL probe of FibroScan. J Hepatol 56:833–839

    Article  PubMed  Google Scholar 

  65. Petta S, Di Marco V, Cammà C, Butera G, Cabibi D, Craxì A (2011) Reliability of liver stiffness measurement in non-alcoholic fatty liver disease: the effects of body mass index. Aliment Pharmacol Ther 33:1350–1360

    Article  PubMed  CAS  Google Scholar 

  66. Gaia S, Carenzi S, Barilli AL, Bugianesi E, Smedile A, Brunello F et al (2011) Reliability of transient elastography for the detection of fibrosis in non-alcoholic fatty liver disease and chronic viral hepatitis. J Hepatol 54:64–71

    Article  PubMed  Google Scholar 

  67. Jaffer OS, Lung PF, Bosanac D, Patel VM, Ryan SM, Heneghan MA et al (2012) Acoustic radiation force impulse quantification: repeatability of measurements in selected liver segments and influence of age, body mass index and liver capsule-to-box distance. Br J Radiol 85:e858–e863

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julia Nierhoff.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure S1

Forest Plots from meta-analysis of the DOR. Forest plots for F ≥ 2 (a), F ≥ 3 (b) and F = 4 (c) using the random effects model. The size of squares is shown proportional to the weight that the respective study contributes to the estimator of the overall DOR. Studies with a larger sample size get more weight than studies with a small sample size. (JPEG 273 kb)

High resolution image (TIFF 1686 kb)

Figure B

(JPEG 282 kb)

High resolution image (TIFF 1680 kb)

Figure C

(JPEG 288 kb)

High resolution image (TIFF 1495 kb)

Figure S2

Funnel Plots. Assessment of publication bias using the funnel plots of the log diagnostic odds ratio for F < 2 vs. F ≥ 2 (A), F < 3 vs. F ≥ 3 (B) and F < 4 vs. F = 4 (C) against a sample size dependent term, where root(ess) describes the root of the effective sample size [18]. The funnel plots are trimmed and filled to adjust for a possible asymmetry arising from publication bias [20]. While the funnel plot for F ≥ 2 indicates asymmetry (p = 0.0094), the funnel plots for F ≥ 3 (p = 0.1955) and F = 4 (p = 0.95) do not seem to deviate from symmetry. (JPEG 64 kb)

High resolution image (TIFF 1321 kb)

Figure B

(JPEG 61 kb)

High resolution image (TIFF 1321 kb)

Figure C

(JPEG 61 kb)

High resolution image (TIFF 1321 kb)

Figure S3

QUADAS criteria. Proportion of studies rated as yes, no or unclear for each of the QUADAS items. In the right columns it is specified for each QUADAS item if there was a significant reduction of heterogeneity for the AUROC estimates. For three QUADAS items (appropriate reference standard, partial verification bias, incorporation bias) a p-value cannot be calculated because of missing values to be needed for the estimation of the standard error of the AUROC. (JPEG 108 kb)

High resolution image (TIFF 119 kb)

Table S1

Quality Assessment Using QUADAS Questionnaire (DOCX 26 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nierhoff, J., Chávez Ortiz, A.A., Herrmann, E. et al. The efficiency of acoustic radiation force impulse imaging for the staging of liver fibrosis: a meta-analysis. Eur Radiol 23, 3040–3053 (2013). https://doi.org/10.1007/s00330-013-2927-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-013-2927-6

Keywords

Navigation