Surgical margin follow-up after nephron-sparing surgery: the possible role of CEUS

  • Elena BertelliEmail author
  • Laura Mercatelli
  • Elena Savi
  • Alessandro Pili
  • Silvia Verna
  • Alberto Palombella
  • Davide Caramella
  • Andrea Minervini
  • Sergio Serni
  • Simone Agostini
  • Vittorio Miele
Original Article



To evaluate the possible role of CEUS in the management of patients who underwent nephron-sparing surgery (NSS) and presented questionable findings on the surgical margins at the CECT follow-up exam.


In our retro-prospective study, we included 952 patients with small renal masses (SRMs) treated with NSS between 2012 and 2015 and followed with CECT for at least 3 years at Careggi University Hospital. Twenty-two of them presented solid masses on the site of surgery with questionable enhancement at CECT and were further studied with CEUS. This examination was followed by a quantitative analysis of the enhancement pattern.


Out of the 22 masses, 18 were considered possible granulomas, presenting slow wash-in and low enhancement peaks compared to the surrounding parenchyma and persistent delayed wash-out at CEUS. Four lesions presented a suspicious malignant enhancement pattern, with rapid wash-in, high peak and rapid wash-out. In accordance with instructions from the urologist, the first group of 18 patients was strictly monitored, revealing that the mass dimensions and enhancement pattern were stable for at least 3 years of follow-up, while the other 4 patients underwent a second intervention and their masses were confirmed as tumor recurrence at the histopathological evaluation.


CEUS can play a key role in the surgical margin follow-up after NSS when a suspicious enhancing mass is detected by CECT, giving an accurate depiction of the enhancement pattern and thus helping the clinician in the management of the patient.


CEUS Nephron-sparing surgery (NSS) Small renal masses (SRM) Kidney Cancer Granuloma 



No funding was used for this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

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


  1. 1.
    Ljungberg B, Albiges L, Abu-Ghanem Y et al (2019) European association of urology guidelines on renal cell carcinoma: the 2019 update. Eur Urol 75(5):799–810CrossRefGoogle Scholar
  2. 2.
    Bjornsson J, Short MP, Kwiatkowski DJ et al (1996) Tuberous sclerosis-associated renal cell carcinoma: clinical, pathological, and genetic features. Am J Pathol 149:1201–1208PubMedPubMedCentralGoogle Scholar
  3. 3.
    Ng CS, Wood CG, Silverman PM et al (2008) Renal cell carcinoma: diagnosis, staging, and surveillance. AJR Am J Roentgenol 191(4):1220–1232CrossRefGoogle Scholar
  4. 4.
    Kim JK, Kim TK, Ahn HJ et al (2002) Differentiation of subtypes of renal cell carcinoma on helical CT scans. AJR Am J Roentgenol 178(6):1499–1506CrossRefGoogle Scholar
  5. 5.
    Oliva MR, Glickman JN, Zou KH et al (2009) Renal cell carcinoma: T1 and T2 signal intensity characteristics of papillary and clear cell types correlated with pathology. AJR Am J Roentgenol 192(6):1524–1530CrossRefGoogle Scholar
  6. 6.
    Pantuck AJ, Zisman A, Belldegrun AS (2001) The changing natural history of renal cell carcinoma. J Urol 166:1611–1623CrossRefGoogle Scholar
  7. 7.
    Kopka L, Fischer U, Zoeller G et al (1997) Dual-phase helical CT of the kidney: value of the corticomedullary and nephrographic phase for evaluation of renal lesions and preoperative staging of renal cell carcinoma. AJR Am J Roentgenol 169(6):1573–1578CrossRefGoogle Scholar
  8. 8.
    Bechtold RE, Zagoria RJ (1997) Imaging approach to staging of renal cell carcinoma. Urol Clin North Am 24:507–522CrossRefGoogle Scholar
  9. 9.
    Sheth S, Scatarige JC, Horton KM et al. (2001) Current concepts in the diagnosis and management of renal cell carcinoma: role of multidetector ct and three-dimensional CT. Radiographics. 21 Spec No: S237–54Google Scholar
  10. 10.
    Hertzberg BS, Middleton WD (2015) Ultrasound: the Requisites, 3rd edn. Elsevier, NetherlandsGoogle Scholar
  11. 11.
    Dinney CPN, Awad SA, Gajewski JB et al (1992) Analysis of imaging modalities, staging systems, and prognostic indicators for renal cell carcinoma. Urology 36:22–29Google Scholar
  12. 12.
    O’Connor SD, Silverman SG, Ip IK et al (2013) Simple cyst-appearing renal masses at unenhanced CT: can they be presumed to be benign? Radiology 269(3):793–800CrossRefGoogle Scholar
  13. 13.
    Gill IS, Aron M, Gervais DA et al (2010) Clinical practice. Small renal mass. N Engl J Med 362:624–634CrossRefGoogle Scholar
  14. 14.
    Almassi N, Gill BC, Rini B et al (2017) Management of the small renal mass. Transl Androl Urol 6(5):923–930CrossRefGoogle Scholar
  15. 15.
    Jonisch AI, Rubinowitz AN, Mutalik PG et al (2007) Can high-attenuation renal cysts be differentiated from renal cell carcinoma at unenhanced CT? Radiology 243(2):445–450CrossRefGoogle Scholar
  16. 16.
    Zhao Y, Wu Y, Zuo Z et al (2017) CT angiography of the kidney using routine CT and the latest Gemstone Spectral Imaging combination of different noise indexes: image quality and radiation dose. Radiol Med 122(5):327–336CrossRefGoogle Scholar
  17. 17.
    Jain Y, Liew S, Taylor MB et al (2011) Is dual-phase abdominal CT necessary for the optimal detection of metastases from renal cell carcinoma? Clin Radiol 66(11):1055–1059CrossRefGoogle Scholar
  18. 18.
    Zhong Y, Shen Y, Pan J et al (2017) Renal epithelioid angiomyolipoma: MRI findings. Radiol Med 122(11):814–821CrossRefGoogle Scholar
  19. 19.
    Tedeschi E, Caranci F, Giordano F et al (2017) Gadolinium retention in the body: what we know and what we can do. Radiol Med 122(8):589–600CrossRefGoogle Scholar
  20. 20.
    Dabestani S, Beisland C, Stewart GD et al (2018) Long-term outcomes of follow-up for initially localised clear cell renal cell carcinoma: RECUR database analysis. Eur Urol Focus S2405–4569(18):30072–30075Google Scholar
  21. 21.
    Antonelli A, Ficarra V, Bertini R et al (2012) Elective partial nephrectomy is equivalent to radical nephrectomy in patients with clinical T1 renal cell carcinoma: results of a retrospective, comparative, multi-institutional study. BJU Int 109(7):1013–1018CrossRefGoogle Scholar
  22. 22.
    Weight CJ, Larson BT, Fergany AF et al (2010) Nephrectomy induced chronic renal insufficiency is associated with increased risk of cardiovascular death and death from any cause in patients with localized cT1b renal masses. J Urol 183(4):1317–1323CrossRefGoogle Scholar
  23. 23.
    Barbiero G, Groff S, Battistel M et al (2018) Are iatrogenic renal artery pseudoaneurysms more challenging to embolize when associated with an arteriovenous fistula? Radiol Med 123(10):742–752CrossRefGoogle Scholar
  24. 24.
    Antic T, Taxy JB (2015) Partial nephrectomy for renal tumors: lack of correlation between margin status and local recurrence. Am J Clin Pathol 143(5):645–651CrossRefGoogle Scholar
  25. 25.
    Comai A, Trenti M, Mayr R et al (2015) Computed Tomography after nephron sparing surgery. Abdom Imaging 40(7):2424–2431CrossRefGoogle Scholar
  26. 26.
    Pozza S, De Marchi A, Albertin C et al (2018) Technical and clinical feasibility of contrast-enhanced ultrasound evaluation of long bone non-infected nonunion healing. Radiol Med 123(9):703–709CrossRefGoogle Scholar
  27. 27.
    Faccioli N, Foti G, Casagranda G et al (2018) CEUS versus CT Angiography in the follow-up of abdominal aortic endoprostheses: diagnostic accuracy and activity-based cost analysis. Radiol Med 123(12):904–909CrossRefGoogle Scholar
  28. 28.
    Tagliati C, Argalia G, Polonara G et al (2019) Contrast-enhanced ultrasound in delayed splenic vascular injury and active extravasation diagnosis. Radiol Med 124(3):170–175CrossRefGoogle Scholar
  29. 29.
    Putz FJ, Erlmeier A, Wiesinger I et al (2017) Contrast-enhanced ultrasound (CEUS) in renal imaging at an interdisciplinary ultrasound centre: possibilities of dynamic microvascularisation and perfusion. Clin Hemorheol Microcirc 66(4):293–302CrossRefGoogle Scholar
  30. 30.
    Le O, Wood C, Vikram R et al (2017) Feasibility of contrast-enhanced intraoperative ultrasound for detection and characterization of renal mass undergoing open partial nephrectomy. J Ultrasound Med 36(8):1547–1553CrossRefGoogle Scholar
  31. 31.
    Drudi FM, Cantisani V, Granata A et al (2019) Multiparametric ultrasound in the evaluation of kidney disease in elderly. J Ultrasound. [Epub ahead of print]CrossRefPubMedGoogle Scholar
  32. 32.
    Nestola M, De Matthaeis N, Ferraro PM et al (2018) Contrast-enhanced ultrasonography in chronic glomerulonephritides: correlation with histological parameters of disease activity. J Ultrasound 21(2):81–87CrossRefGoogle Scholar
  33. 33.
    Sidhu PS, Cantisani V, Dietrich CF et al (2018) The EFSUMB guidelines and recommendations for the clinical practice of contrast-enhanced ultrasound (CEUS) in non-hepatic applications: update 2017 (Short Version). Ultraschall Med 39(2):154–180CrossRefGoogle Scholar
  34. 34.
    Meloni MF, Smolock A, Cantisani V et al (2015) Contrast enhanced ultrasound in the evaluation and percutaneous treatment of hepatic and renal tumors. Eur J Radiol 84(9):1666–1674CrossRefGoogle Scholar
  35. 35.
    Singh A, Jai S, Ganpule S et al (2016) Bolster material granuloma masquerading as recurrent renal cell carcinoma following partial nephrectomy. Indian J Radiol Imaging 26(3):352–355CrossRefGoogle Scholar
  36. 36.
    Agarval MM, Mandal AK, Agarwal S et al (2010) Surgicel granuloma unusual case of “recurrent” mass lesion after laparoscopic nephron sparing surgery for renal cell carcinoma. Urology 76(2):334–335CrossRefGoogle Scholar
  37. 37.
    Tonolini M, Ierardi AM, Varca V et al (2015) Multidetector CT imaging of complications after laparoscopic nephron sparing surgery. Insight Imaging 6(4):465–478CrossRefGoogle Scholar
  38. 38.
    Álvarez Rodríguez S, Hevia Palacios V, Sanz Mayayo E et al (2017) The usefulness of contrast-enhanced ultrasound in the assessment of early kidney transplant function and complications. Diagnostics (Basel). CrossRefGoogle Scholar
  39. 39.
    Mueller-Peltzer K, Rübenthaler J, Fischereder M et al (2017) The diagnostic value of contrast-enhanced ultrasound (CEUS) as a new technique for imaging of vascular complications in renal transplants compared to standard imaging modalities. Clin Hemorheol Microcirc 67(3–4):407–413CrossRefGoogle Scholar

Copyright information

© Società Italiana di Ultrasonologia in Medicina e Biologia (SIUMB) 2019

Authors and Affiliations

  • Elena Bertelli
    • 1
    • 2
    Email author
  • Laura Mercatelli
    • 1
  • Elena Savi
    • 1
  • Alessandro Pili
    • 3
  • Silvia Verna
    • 1
  • Alberto Palombella
    • 1
  • Davide Caramella
    • 4
  • Andrea Minervini
    • 3
  • Sergio Serni
    • 3
  • Simone Agostini
    • 1
  • Vittorio Miele
    • 1
  1. 1.Department of RadiologyCareggi University HospitalFlorenceItaly
  2. 2.Clinical and Translational SciencesUniversity of PisaFlorenceItaly
  3. 3.Department of Urologic Robotic Surgery and Renal TransplantationCareggi Hospital, University of FlorenceFlorenceItaly
  4. 4.Diagnostic and Interventional RadiologyUniversity of PisaFlorenceItaly

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