Skip to main content
SpringerLink
Log in

Diagnostic accuracy of qualitative and quantitative magnetic resonance imaging-guided contrast-enhanced ultrasound (MRI-guided CEUS) for the detection of prostate cancer: a prospective and multicenter study

  • Diagnostic Imaging in Oncology
  • Published:
La radiologia medica Aims and scope Submit manuscript

Abstract

Purpose

To evaluate the diagnostic value of MRI-guided contrast-enhanced ultrasound (CEUS) for prostate cancer (PCa) diagnosis, and characteristics of PCa in qualitative and quantitative CEUS.

Material and methods

This prospective and multicenter study included 250 patients (133 in the training cohort, 57 in the validation cohort and 60 in the test cohort) who underwent MRI, MRI-guided CEUS and prostate biopsy between March 2021 and February 2023. MRI interpretation, qualitative and quantitative CEUS analysis were conducted. Multitree extreme gradient boosting (XGBoost) machine learning-based models were applied to select the eight most important quantitative parameters. Univariate and multivariate logistic regression models were constructed to select independent predictors of PCa. Diagnostic value was determined for MRI, qualitative and quantitative CEUS using the area under receiver operating characteristic curve (AUC).

Results

The performance of quantitative CEUS was superior to that of the qualitative CEUS and MRI in predicting PCa. The AUC was 0.779 (95%CI 0.70–0.849), 0.756 (95%CI 0.638–0.874) and 0.759 (95%CI 0.638–0.879) of qualitative CEUS, and 0.885 (95%CI 0.831–0.940), 0.802 (95%CI 0.684–0.919) and 0.824 (95%CI 0.713–0.936) of quantitative CEUS in training, validation and test cohort, respectively. Compared with quantitative CEUS, MRI achieved less well performance for AUC 0.811 (95%CI 0.741–0.882, p = 0.099), 0.748 (95%CI 0.628–0.868, p = 0.539) and 0.737 (95%CI 0.602–0.873, p = 0.029), respectively. Moreover, the highest specificity of 80.6% was obtained by quantitative CEUS.

Conclusion

We developed a reliable method of MRI-guided CEUS that demonstrated enhanced performance compared to MRI. The qualitative and quantitative CEUS characteristics will contribute to improved diagnosis of PCa.

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

Access this article

Log in via an institution

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
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AUC:

Area under the curve

CEUS:

Contrast-enhanced ultrasound

csPCa:

Clinically significant prostate cancer

DCA:

Decision curve analysis

mp-MRI:

Multiparameter magnetic resonance imaging

nsPCa:

Non-clinically significant prostate cancer

PCa:

Prostate cancer

PI-RADS:

Prostate imaging reporting and data system

ROC:

Receiver operating curve

ROI:

Region of interest

TTP:

Time to peak

US:

Ultrasound

WoR:

Washout rate

References

  1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71(3):209–249

    Article  PubMed  Google Scholar 

  2. Kiebish MA, Tekumalla P, Ravipaty S, Dobi A, Srivastava S, Wu W, Patil S, Friss T, Klotz A, Srinivasan A, Cullen J, Rosner IL, Ali A, Laszlo S, Petrovic M, Fleshner N, Garren J, Miller G, Mahaveer Chand N, Rodrigues LO, Granger E, Kellogg MD, Luan S, Diamandis E, Akmaev VR, Sarangarajan R, Bountra C, Freedland SJ, McLeod DG, Narain NR (2021) Clinical utility of a serum biomarker panel in distinguishing prostate cancer from benign prostate hyperplasia. Sci Rep 11(1):15052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Butler SS, Muralidhar V, Zhao SG, Sanford NN, Franco I, Fullerton ZH, Chavez J, D’Amico AV, Feng FY, Rebbeck TR, Nguyen PL, Mahal BA (2020) Prostate cancer incidence across stage, NCCN risk groups, and age before and after USPSTF grade D recommendations against prostate-specific antigen screening in 2012. Cancer 126(4):717–724

    Article  CAS  PubMed  Google Scholar 

  4. Ahdoot M, Wilbur AR, Reese SE, Lebastchi AH, Mehralivand S, Gomella PT, Bloom J, Gurram S, Siddiqui M, Pinsky P, Parnes H, Linehan WM, Merino M, Choyke PL, Shih JH, Turkbey B, Wood BJ, Pinto PA (2020) MRI-targeted, systematic, and combined biopsy for prostate cancer diagnosis. N Engl J Med 382(10):917–928

    Article  PubMed  PubMed Central  Google Scholar 

  5. Ahmed HU, El-Shater Bosaily A, Brown LC, Gabe R, Kaplan R, Parmar MK, Collaco-Moraes Y, Ward K, Hindley RG, Freeman A, Kirkham AP, Oldroyd R, Parker C, Emberton M (2017) Diagnostic accuracy of multi-parametric MRI and TRUS biopsy in prostate cancer (PROMIS): a paired validating confirmatory study. Lancet 389(10071):815–822

    Article  PubMed  Google Scholar 

  6. Pagniez MA, Kasivisvanathan V, Puech P, Drumez E, Villers A, Olivier J (2020) Predictive factors of missed clinically significant prostate cancers in men with negative magnetic resonance imaging: a systematic review and meta-analysis. J Urol 204(1):24–32

    Article  CAS  PubMed  Google Scholar 

  7. Annamalai A, Fustok JN, Beltran-Perez J, Rashad AT, Krane LS, Triche BL (2022) Interobserver agreement and accuracy in interpreting mpMRI of the prostate: a systematic review. Curr Urol Rep 23(1):1–10

    Article  PubMed  Google Scholar 

  8. Borofsky S, George AK, Gaur S, Bernardo M, Greer MD, Mertan FV, Taffel M, Moreno V, Merino MJ, Wood BJ, Pinto PA, Choyke PL, Turkbey B (2018) What are we missing? False-negative cancers at multiparametric MR imaging of the prostate. Radiology 286(1):186–195

    Article  PubMed  Google Scholar 

  9. Zhang J, Xu L, Zhang G, Zhang X, Bai X, Sun H, Jin Z (2023) Effects of dynamic contrast enhancement on transition zone prostate cancer in prostate imaging reporting and data system version 2.1. Radiol Oncol

  10. Salib A, Halpern E, Eisenbrey J, Chandrasekar T, Chung PH, Forsberg F, Trabulsi EJ (2022) The evolving role of contrast-enhanced ultrasound in urology: a review. World J Urol

  11. Yang G, Ruan L (2022) Imaging findings of prostate tuberculosis by transrectal contrast-enhanced ultrasound and comparison with 2D ultrasound and pathology. Br J Radiol 95(1129):20210713

    Article  PubMed  Google Scholar 

  12. Jung EM, Wertheimer T, Putz FJ, Jung F, Kammerer S, Pregler B, Luerken L, Stroszczynski C, Beyer L (2020) Contrast enhanced ultrasound (CEUS) with parametric imaging and time intensity curve analysis (TIC) for evaluation of the success of prostate arterial embolization (PAE) in cases of prostate hyperplasia. Clin Hemorheol Microcirc 76(2):143–153

    Article  CAS  PubMed  Google Scholar 

  13. Wink M, Frauscher F, Cosgrove D, Chapelon JY, Palwein L, Mitterberger M, Harvey C, Rouvière O, de la Rosette J, Wijkstra H (2008) Contrast-enhanced ultrasound and prostate cancer; a multicentre European research coordination project. Eur Urol 54(5):982–992

    Article  PubMed  Google Scholar 

  14. Sidhu PS, Cantisani V, Dietrich CF, Gilja OH, Saftoiu A, Bartels E, Bertolotto M, Calliada F, Clevert DA, Cosgrove D, Deganello A, D’Onofrio M, Drudi FM, Freeman S, Harvey C, Jenssen C, Jung EM, Klauser AS, Lassau N, Meloni MF, Leen E, Nicolau C, Nolsoe C, Piscaglia F, Prada F, Prosch H, Radzina M, Savelli L, Weskott HP, Wijkstra H (2018) The EFSUMB guidelines and recommendations for the clinical practice of contrast-enhanced ultrasound (CEUS) in non-hepatic applications: update 2017 (Long Version). Ultraschall Med 39(2):e2–e44

    Article  PubMed  Google Scholar 

  15. Turkbey B, Rosenkrantz AB, Haider MA, Padhani AR, Villeirs G, Macura KJ, Tempany CM, Choyke PL, Cornud F, Margolis DJ, Thoeny HC, Verma S, Barentsz J, Weinreb JC (2019) Prostate imaging reporting and data system version 2.1: 2019 update of prostate imaging reporting and data system version 2. Eur Urol 76(3):340–351

    Article  PubMed  Google Scholar 

  16. Epstein JI, Egevad L, Amin MB, Delahunt B, Srigley JR, Humphrey PA (2016) The 2014 international society of urological pathology (ISUP) consensus conference on gleason grading of prostatic carcinoma: definition of grading patterns and proposal for a new grading system. Am J Surg Pathol 40(2):244–252

    Article  PubMed  Google Scholar 

  17. Sano F, Terao H, Kawahara T, Miyoshi Y, Sasaki T, Noguchi K, Kubota Y, Uemura H (2011) Contrast-enhanced ultrasonography of the prostate: various imaging findings that indicate prostate cancer. BJU Int 107(9):1404–1410

    Article  PubMed  Google Scholar 

  18. Wildeboer RR, Mannaerts CK, van Sloun RJG, Budäus L, Tilki D, Wijkstra H, Salomon G, Mischi M (2020) Automated multiparametric localization of prostate cancer based on B-mode, shear-wave elastography, and contrast-enhanced ultrasound radiomics. Eur Radiol 30(2):806–815

    Article  PubMed  Google Scholar 

  19. Liu G, Wu S, Huang L (2020) Contrast-enhanced ultrasound evaluation of the prostate before transrectal ultrasound-guided biopsy can improve diagnostic sensitivity: a STARD-compliant article. Medicine 99(19):e19946

    Article  PubMed  PubMed Central  Google Scholar 

  20. Grey ADR, Scott R, Shah B, Acher P, Liyanage S, Pavlou M, Omar R, Chinegwundoh F, Patki P, Shah TT, Hamid S, Ghei M, Gilbert K, Campbell D, Brew-Graves C, Arumainayagam N, Chapman A, McLeavy L, Karatziou A, Alsaadi Z, Collins T, Freeman A, Eldred-Evans D, Bertoncelli-Tanaka M, Tam H, Ramachandran N, Madaan S, Winkler M, Arya M, Emberton M, Ahmed HU (2022) Multiparametric ultrasound versus multiparametric MRI to diagnose prostate cancer (CADMUS): a prospective, multicentre, paired-cohort, confirmatory study. Lancet Oncol 23(3):428–438

    Article  PubMed  Google Scholar 

  21. Kunz P, Kiesl S, Groß S, Kauczor HU, Schmidmaier G, Fischer C (2020) Intra-observer and device-dependent inter-observer reliability of contrast-enhanced ultrasound for muscle perfusion quantification. Ultrasound Med Biol 46(2):275–285

    Article  PubMed  Google Scholar 

  22. Postema AW, Frinking PJ, Smeenge M, De Reijke TM, De la Rosette JJ, Tranquart F, Wijkstra H (2016) Dynamic contrast-enhanced ultrasound parametric imaging for the detection of prostate cancer. BJU Int 117(4):598–603

    Article  PubMed  Google Scholar 

  23. Weinreb JC, Barentsz JO, Choyke PL, Cornud F, Haider MA, Macura KJ, Margolis D, Schnall MD, Shtern F, Tempany CM, Thoeny HC, Verma S (2016) PI-RADS prostate imaging-reporting and data system: 2015, Version 2. Eur Urol 69(1):16–40

    Article  PubMed  Google Scholar 

  24. Pang X, Zhang J, Chen L, Yuan Y, Xu D (2022) Study on the diagnostic value of contrast-enhanced ultrasound and magnetic resonance imaging in prostate cancer. Evid Based Complement Alternat Med 2022:7983530

    Article  PubMed  PubMed Central  Google Scholar 

  25. Sato T, Isoda H, Fujimoto K, Furuta A, Fujimoto M, Ito K, Kobayashi T, Nakamoto Y (2021) Evaluation of weighted diffusion subtraction for detection of clinically significant prostate cancer. J Magn Reson Imag 54(6):1979–1988

    Article  Google Scholar 

  26. Maxeiner A, Fischer T, Schwabe J, Baur ADJ, Stephan C, Peters R, Slowinski T, von Laffert M, Marticorena Garcia SR, Hamm B, Jung EM (2019) Contrast-enhanced ultrasound (CEUS) and quantitative perfusion analysis in patients with suspicion for prostate cancer. Ultraschall Med 40(3):340–348

    Article  PubMed  Google Scholar 

  27. Jung EM, Wiggermann P, Greis C, Eder F, Ehrich J, Jung W, Schreyer AG, Stroszczynski C, Ganzer R (2012) First results of endocavity evaluation of the microvascularization of malignant prostate tumors using contrast enhanced ultrasound (CEUS) including perfusion analysis: first results. Clin Hemorheol Microcirc 52(2–4):167–177

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank all the participants in this study.

Funding

This study has received funding by National Natural Science Foundation of China (Grants No. 82171942, 82371971, 82202153 and 82202154) and the foundations of National Key R&D Program of China (Grant No. 2022YFF0606304).

Author information

Authors and Affiliations

  1. Department of Medical Ultrasound, Center of Minimally Invasive Treatment for Tumor, School of Medicine, Shanghai Tenth People’s Hospital, Tongji University, Shanghai, 200072, China

    Yunyun Liu, Guang Xu, Shuai Wang, Bangguo Zhou, Ying Zhang, Beibei Ye, Lihua Xiang & Yifeng Zhang

  2. Clinical Research Center for Interventional Medicine, School of Medicine, Ultrasound Research and Education Institute, Tongji University, Shanghai, 200072, China

    Yunyun Liu, Guang Xu, Shuai Wang, Bangguo Zhou, Ying Zhang, Beibei Ye, Lihua Xiang & Yifeng Zhang

  3. Department of Ultrasound, Chongming Hospital Affiliated to Shanghai University of Health & Medicine Sciences, Shanghai, China

    Dianyuan Lu

  4. Department of Ultrasound, Institute of Ultrasound in Medicine and Engineering, Zhongshan Hospital, Fudan University, Shanghai, 200032, China

    Huixiong Xu

Authors
  1. Yunyun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dianyuan Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shuai Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bangguo Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Beibei Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lihua Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yifeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Huixiong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lihua Xiang or Yifeng Zhang.

Ethics declarations

Conflict of interest

The authors disclose no conflicts of interest.

Ethical approval

Institutional Review Board approval was obtained.

Informed consent

Written informed consent was only obtained from prospectively enrolled patients in this study.

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 (DOCX 218 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

Liu, Y., Lu, D., Xu, G. et al. Diagnostic accuracy of qualitative and quantitative magnetic resonance imaging-guided contrast-enhanced ultrasound (MRI-guided CEUS) for the detection of prostate cancer: a prospective and multicenter study. Radiol med 129, 585–597 (2024). https://doi.org/10.1007/s11547-024-01758-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11547-024-01758-2

Keywords

Search

Navigation