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Contrast-enhanced ultrasound (CEUS) imaging for active surveillance of small renal masses

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Abstract

Purpose

To assess the safety and efficacy of contrast-enhanced ultrasound (CEUS) imaging for monitoring small (< 4 cm) renal masses (SRM) in patients undergoing active surveillance (AS).

Methods

We retrospectively selected all consecutive patients with SRMs who underwent AS for at least 6 months at our Institution between January 2014 and December 2018. CEUS imaging was performed by two experienced genitourinary radiologists at established time points. The accuracy of CEUS for monitoring SRM size was compared with that of CT scan. For solid SRMs, four enhancement patterns (EP) were recorded. Radiological progression was defined as SRM growth rate ≥ 5 mm/year.

Results

Overall, 158/1049 (15.1%) patients with SRMs underwent AS. At a median follow-up of 25 months (IQR 13–39), no patient died due to renal cell carcinoma (RCC). No patients experienced CEUS-related adverse events. There was a large variability in the pattern of growth of SRMs (overall median growth rate: 0.40 mm/year), with 9.5% of SRMs showing radiological progression. The median SRM size was comparable between CEUS and CT scan examinations at all time points. The vast majority (92.7%) of SRMs did not show a change in their EP over time; and there was no association between the SRM’s EP and radiological progression or SRM size. Overall, 43 (27.2%) patients underwent delayed intervention (DI); median SRM size, and median growth rate were significantly higher in these patients as compared to those continuing AS.

Conclusion

In experienced hands, CEUS is a safe and effective strategy for active monitoring of SRMs in well-selected patients undergoing AS.

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References

  1. Capitanio U, Bensalah K, Bex A et al (2019) Epidemiology of renal cell carcinoma. Eur Urol 75(1):74–84. https://doi.org/10.1016/j.eururo.2018.08.036

    Article  PubMed  Google Scholar 

  2. Mir MC, Capitanio U, Bertolo R et al (2018) Role of active surveillance for localized small renal masses. Eur Urol Oncol 1(3):177–187. https://doi.org/10.1016/j.euo.2018.05.001

    Article  PubMed  Google Scholar 

  3. Finelli A, Ismaila N, Bro B et al (2017) Management of small renal masses: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol 35(6):668–680. https://doi.org/10.1200/JCO.2016.69.9645

    Article  PubMed  Google Scholar 

  4. Cheaib JG, Pierorazio PM (2019) How does treatment uncertainty factor into decisions to place patients on active surveillance for kidney cancer? Eur Urol Focus 5(6):946–948. https://doi.org/10.1016/j.euf.2019.07.002

    Article  PubMed  Google Scholar 

  5. Campbell S, Uzzo RG, Allaf ME et al (2017) Renal mass and localized renal cancer: AUA guideline. J Urol 198:520–529. https://doi.org/10.1016/j.juro.2017.04.100

    Article  PubMed  Google Scholar 

  6. Metcalf MR, Cheaib JG, Biles MJ et al (2020) Outcomes of active surveillance for young patients with small renal masses: prospective data from the DISSRM registry. J Urol. https://doi.org/10.1097/JU.0000000000001575 (Epub ahead of print)

    Article  PubMed  Google Scholar 

  7. Sohlberg EM, Metzner TJ, Leppert JT (2019) The harms of overdiagnosis and overtreatment in patients with small renal masses: a mini-review. Eur Urol Focus 5(6):943–945. https://doi.org/10.1016/j.euf.2019.03.006

    Article  PubMed  Google Scholar 

  8. Ristau BT, Kutikov A, Uzzo RG, Smaldone MC (2016) Active surveillance for small renal masses: when less is more. Eur Urol Focus 2(6):660–668. https://doi.org/10.1016/j.euf.2017.04.004

    Article  PubMed  Google Scholar 

  9. Campi R, Sessa F, Corti F et al (2020) Triggers for delayed intervention in patients with small renal masses undergoing active surveillance: a systematic review. Minerva Urol Nefrol 72(4):389–407. https://doi.org/10.23736/S0393-2249.20.03870-9

    Article  PubMed  Google Scholar 

  10. Pierorazio PM, Johnson MH, Ball MW et al (2015) Five-year analysis of a multi-institutional prospective clinical trial of delayed intervention and surveillance for small renal masses: the DISSRM registry. Eur Urol 68(3):408–415. https://doi.org/10.1016/j.eururo.2015.02.001

    Article  PubMed  Google Scholar 

  11. McIntosh AG, Ristau BT, Ruth K et al (2018) Active surveillance for localized renal masses: tumor growth, delayed intervention rates, and >5-yr clinical outcomes. Eur Urol 74(2):157–164. https://doi.org/10.1016/j.eururo.2018.03.011

    Article  PubMed  Google Scholar 

  12. Patel AK, Rogers CG, Johnson A et al (2021) Initial observation of a large proportion of patients presenting with clinical stage T1 renal masses: results from the MUSIC-KIDNEY statewide collaborative. Eur Urol Open Sci 23:13–19. https://doi.org/10.1016/j.euros.2020.11.002

    Article  PubMed  Google Scholar 

  13. Ljungberg B, Albiges L, Abu-Ghanem Y et al (2020) European association of urology guidelines on renal cell carcinoma: the 2019 update. Eur Urol. https://doi.org/10.1016/j.eururol.2019.02.011

    Article  PubMed  PubMed Central  Google Scholar 

  14. Rossi SH, Prezzi D, Kelly-Morland C, Goh V (2018) Imaging for the diagnosis and response assessment of renal tumors. World J Urol 36:1927–1942. https://doi.org/10.1007/s00345-018-2342-3

    Article  PubMed  PubMed Central  Google Scholar 

  15. Schoots IG, Zaccai K, Hunink MG, Verhagen PCMS (2017) Bosniak classification for complex renal cysts reevaluated: a systematic review. J Urol 198(1):12–21. https://doi.org/10.1016/j.juro.2016.09.160

    Article  PubMed  Google Scholar 

  16. Thaiss WM, Bedke J, Kruck S et al (2019) Can contrast-enhanced ultrasound and acoustic radiation force impulse imaging characterize CT-indeterminate renal masses? A prospective evaluation with histological confirmation. World J Urol 37:1339–1346. https://doi.org/10.1007/s00345-018-2520-3

    Article  PubMed  Google Scholar 

  17. Furrer MA, Spycher SCJ, Büttiker SM et al (2020) Comparison of the diagnostic performance of contrast-enhanced ultrasound with that of contrast-enhanced computed tomography and contrast-enhanced magnetic resonance imaging in the evaluation of renal masses: a systematic review and meta-analysis. Eur Urol Oncol 3(4):464–473. https://doi.org/10.1016/j.euo.2019.08.013

    Article  PubMed  Google Scholar 

  18. Sidhu PS, Cantisani V, Dietrich CF et al (2018) 2017 The EFSUMB guidelines and recommendations on the clinical practice of contrast enhanced ultrasound (CEUS) in non-hepatic applications: update. Ultraschall Med 39(2):e2–e44

    Article  Google Scholar 

  19. von Elm E, Altman DG, Egger M et al (2007) The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 370(9596):1453–1457. https://doi.org/10.1016/S0140-6736(07)61602-X

    Article  Google Scholar 

  20. Sevcenco S, Spick C, Helbich TH et al (2017) Malignancy rates and diagnostic performance of the Bosniak classification for the diagnosis of cystic renal lesions in computed tomography—a systematic review and meta-analysis. Eur Radiol 27(6):2239–2247. https://doi.org/10.1007/s00330-016-4631-9

    Article  PubMed  Google Scholar 

  21. Bertelli E, Mercatelli L, Savi E et al (2020) Surgical margin follow-up after nephron-sparing surgery: the possible role of CEUS. J Ultrasound 23(4):515–520. https://doi.org/10.1007/s40477-019-00413-1 (Epub 2019 Nov 18)

    Article  PubMed  Google Scholar 

  22. Dong X, Shen Y, Xu L et al (2009) Contrast-enhanced ultrasound for detection and diagnosis of renal clear cell carcinoma. Chin Med J (Engl) 122(10):1179–1183

    Google Scholar 

  23. Silverman SG, Pedrosa I, Ellis JH et al (2019) Bosniak classification of cystic renal masses, version 2019: an update proposal and needs assessment. Radiology 292(2):475–488. https://doi.org/10.1148/radiol.2019182646

    Article  PubMed  Google Scholar 

  24. Minervini A, Campi R, Di Maida F et al (2018) Tumor-parenchyma interface and long-term oncologic outcomes after robotic tumor enucleation for sporadic renal cell carcinoma. Urol Oncol 36(12):527.e1-527.e11. https://doi.org/10.1016/j.urolonc.2018.08.014

    Article  Google Scholar 

  25. Minervini A, Campi R, Lane BR et al (2020) Impact of resection technique on perioperative outcomes and surgical margins after partial nephrectomy for localized renal masses: a prospective multicenter study. J Urol 203(3):496–504. https://doi.org/10.1097/JU.0000000000000591

    Article  PubMed  Google Scholar 

  26. Spiesecke P, Fischer T, Friedersdorff F et al (2020) Quality assessment of CEUS in individuals with small renal masses-which individual factors are associated with high image quality? J Clin Med 9(12):4081. https://doi.org/10.3390/jcm9124081

    Article  PubMed Central  Google Scholar 

  27. Li CX, Lu Q, Huang BJ et al (2014) The value of contrast-enhanced ultrasound (CEUS) in detecting minute renal cell carcinoma. Discov Med 18(99):179–188

    PubMed  Google Scholar 

  28. Bertolotto M, Cicero C, Perrone R et al (2015) Renal masses with equivocal enhancement at CT: characterization with contrast-enhanced ultrasound. AJR Am J Roentgenol 204(5):557–565. https://doi.org/10.2214/AJR.14.13375

    Article  Google Scholar 

  29. Sun D, Wei C, Li Y et al (2016) Contrast-enhanced ultrasonography with quantitative analysis allows differentiation of renal tumor histotypes. Sci Rep 6:35081. https://doi.org/10.1038/srep35081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Xue L, Lu Q, Huang B et al (2015) Papillary renal cell carcinoma and clear cell renal cell carcinoma: differentiation of distinct histological types with contrast—enhanced ultrasonography. Eur J Radiol 84(10):1849–1856. https://doi.org/10.1016/j.ejrad.2015.06.017

    Article  PubMed  Google Scholar 

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Funding

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Author information

Authors and Affiliations

Authors

Contributions

EB: project concept and design, manuscript writing, and data collection. AP: project concept and design, data collection. FS: manuscript writing. NM, IB, SV, IG, SM, AP, AB, RN: data collection. AS, AM, MC, MG, VM: critical revision of the manuscript. SA: data collection, critical revision of the manuscript, project concept and design, supervision. SS: project concept and design, critical revision of the manuscript, supervision. RC: project concept and design, manuscript writing, statistical analysis, critical revision of the manuscript.

Corresponding author

Correspondence to Elena Bertelli.

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Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

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

Research involving human participants

All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and national research Committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 28 KB)

345_2021_3589_MOESM2_ESM.png

Supplementary file 2 Supplementary Figure 1. Graphical overview of small renal mass (SRM)-specific enhancement pattern (EP) at CEUS imaging at baseline (blue circles) and at last follow-up (red circles), stratified by renal mass growth rate (<5 mm/year vs > 5 mm/year). Overall, the baseline EP was recorded in 139/141 (98.6%) patients with solid SRMs (EP1: 27.3%; EP2: 34.5%; EP4: 38.1%). Of these, at last follow-up, 10/139 (7.2%) SRMs did show a change in their EP (EP1: 29.6%; EP2: 32.0%; EP3: 38.4%). (PNG 433 KB)

345_2021_3589_MOESM3_ESM.png

Supplementary file3 Supplementary Figure 2. Overview of the median (IQR, range) small renal mass (SRM) size at CEUS imaging at four selected time points (baseline, 6 months, 12 months, last follow-up) among patients continuing the active surveillance (AS) protocol and among those switching to delayed intervention (DI). A. The median SRM size was significantly higher among patients undergoing DI at all time points (24 mm vs 14 mm at baseline, p<0.001 (*); 25 mm vs 15mm at 6 months, p<0.001 (*); 23 mm vs 15mm at 12 months, p=0.043(**); 25 mm vs 16 mm at last follow-up, p<0.001 (*)). B. There was no association between the median SRM size (at last follow-up) and enhancement pattern (EP) (at last follow-up) in both the cohort of patients continuing AS (15.5 vs 15.0 vs 15.0 mm for EP 1, 2 and 4, respectively, p=0.7) and the cohort of patients switching to DI (28.0 vs 23.5 vs 22.5 mm for EP 1, 2 and 4, respectively, p=0.4). (PNG 530 KB)

Supplementary file4 (DOCX 14 KB)

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Bertelli, E., Palombella, A., Sessa, F. et al. Contrast-enhanced ultrasound (CEUS) imaging for active surveillance of small renal masses. World J Urol 39, 2853–2860 (2021). https://doi.org/10.1007/s00345-021-03589-6

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