Intraoperative imaging techniques for robotic-assisted partial nephrectomy: where do we stand?

Abstract

Robot-assisted partial nephrectomy is currently the gold standard treatment for localized selected cT1 and cT2 renal tumors. This narrative review aims to analyze the technologies employed in this procedure to increase the precision and accuracy of the surgeon, in order to obtain adequate oncological radicality, negative surgical margins, and good preservation of renal function. In this scenario, new technologies are developing, from three-dimensional reconstructions to artificial intelligence up to the new concept of metaverse.

Keywords

Partial nephrectomy / renal cancer / robotic surgery / 3D imaging / augmented reality / artificial intelligence

References

[1] Ljungberg B,Abu-Ghanem Y.European Association of Urology Guidelines on renal cell carcinoma: the 2022 update.Eur Urol2022;82:399-410

[2] Benway BM,Rogers CG.Robot assisted partial nephrectomy versus laparoscopic partial nephrectomy for renal tumors: a multi-institutional analysis of perioperative outcomes.J Urol2009;182:866-72

[3] Kim DK,Raheem AA.Comparison of trifecta and pentafecta outcomes between T1a and T1b renal masses following robot-assisted partial nephrectomy (RAPN) with minimum one year follow up: can RAPN for T1b renal masses be feasible?.PLoS One2016;11:e0151738 PMCID:PMC4795597

[4] Marszalek M,Chlosta P.Positive surgical margins after nephron-sparing surgery.Eur Urol2012;61:757-63

[5] Kaczmarek BF,Petros F.Robotic ultrasound probe for tumor identification in robotic partial nephrectomy: initial series and outcomes.Int J Urol2013;20:172-6

[6] Zhang Y,Wu B.Robot-assisted partial nephrectomy with a standard laparoscopic ultrasound probe in treating endophytic renal tumor.Asian J Surg2020;43:423-7

[7] Puliatti S,Checcucci E.New imaging technologies for robotic kidney cancer surgery.Asian J Urol2022;9:253-62 PMCID:PMC9399539

[8] Di Cosmo G,Silvestri T.Intraoperative ultrasound in robot-assisted partial nephrectomy: state of the art.Arch Ital Urol Androl2018;90:195-8

[9] Correas JM,Joly D,Tanter M.Ultrasound-based imaging methods of the kidney-recent developments.Kidney Int2016;90:1199-210

[10] Hyams ES,Stifelman MD.A prospective evaluation of the utility of laparoscopic Doppler technology during minimally invasive partial nephrectomy.Urology2011;77:617-20

[11] Greis C. Technology overview: SonoVue (Bracco, Milan).Eur Radiol2004;14:11-15

[12] Rosiello G,Puliatti S.Simplified PADUA renal (SPARE) nephrometry score validation and long-term outcomes after robot-assisted partial nephrectomy.Urol Oncol2022;40:65.e1-9

[13] Hsu TH,Chon C.Laparoscopic radical nephrectomy incorporating intraoperative ultrasonography for renal cell carcinoma with renal vein tumor thrombus.Urology2003;61:1246-8

[14] Campbell SC,Novick AC.Intraoperative evaluation of renal cell carcinoma: a prospective study of the role of ultrasonography and histopathological frozen sections.J Urol1996;155:1191-5

[15] Polascik TJ,Epstein JI.Intraoperative sonography for the evaluation and management of renal tumors: experience with 100 patients.J Urol1995;154:1676-80

[16] Alenezi AN.Role of intra-operative contrast-enhanced ultrasound (CEUS) in robotic-assisted nephron-sparing surgery.J Robot Surg2015;9:1-10 PMCID:PMC4333307

[17] Keereweer S,Snoeks TJA.Optical image-guided cancer surgery: challenges and limitations.Clin Cancer Res2013;19:3745-54

[18] Gadus L,Chmelik F,Heracek J.Robotic partial nephrectomy with indocyanine green fluorescence navigation.Contrast Media Mol Imaging2020;2020:1287530 PMCID:PMC7204372

[19] Bjurlin MA,Stifelman MD.Near-infrared fluorescence imaging with intraoperative administration of indocyanine green for robotic partial nephrectomy.Curr Urol Rep2015;16:20

[20] Diana P,Lughezzani G.The role of intraoperative indocyanine green in robot-assisted partial nephrectomy: results from a large, multi-institutional series.Eur Urol2020;78:743-9

[21] McClintock TR,Wysock JS.Can selective arterial clamping with fluorescence imaging preserve kidney function during robotic partial nephrectomy?.Urology2014;84:327-32 PMCID:PMC4683014

[22] Mattevi D,Mantovani W.Fluorescence-guided selective arterial clamping during RAPN provides better early functional outcomes based on renal scan compared to standard clamping.J Robot Surg2019;13:391-6

[23] Abdel Raheem A,Capitanio U.Warm ischemia time length during on-clamp partial nephrectomy: does it really matter?.Minerva Urol Nephrol2022;74:194-202

[24] Simone G,Papalia R,Guaglianone S.Zero-ischemia minimally invasive partial nephrectomy.Curr Urol Rep2013;14:465-70

[25] Sentell KT,Abaza R.Near-infrared fluorescence imaging for intraoperative margin assessment during robot-assisted partial nephrectomy.BJU Int2020;126:259-64

[26] Simone G,Anceschi U.“Ride the green light”: indocyanine green-marked off-clamp robotic partial nephrectomy for totally endophytic renal masses.Eur Urol2019;75:1008-14

[27] Autorino R,Laydner H.Robot-assisted partial nephrectomy (RAPN) for completely endophytic renal masses: a single institution experience.BJU Int2014;113:762-8

[28] Tuderti G,Mastroianni R.Expanding the limits of nephron-sparing surgery: surgical technique and mid-term outcomes of purely off-clamp robotic partial nephrectomy for totally endophytic renal tumors.Int J Urol2022;29:282-8

[29] Sulek JE,Bahler CD.Folate-targeted intraoperative fluorescence, OTL38, in robotic-assisted laparoscopic partial nephrectomy.Scand J Urol2021;55:331-6

[30] Povoski SP,Murrey DA Jr.Multimodal imaging and detection strategy with 124 I-labeled chimeric monoclonal antibody cG250 for accurate localization and confirmation of extent of disease during laparoscopic and open surgical resection of clear cell renal cell carcinoma.Surg Innov2013;20:59-69 PMCID:PMC3758170

[31] Hekman MC,de Weijert M.Targeted dual-modality imaging in renal cell carcinoma: an ex vivo kidney perfusion study.Clin Cancer Res2016;22:4634-42

[32] Phung MC,Pangilinan J.Investigation of confocal microscopy for differentiation of renal cell carcinoma versus benign tissue. Can an optical biopsy be performed?.Asian J Urol2020;7:363-8 PMCID:PMC7498942

[33] Su LM,Allan RW.Fiber-optic confocal laser endomicroscopy of small renal masses: toward real-time optical diagnostic biopsy.J Urol2016;195:486-92

[34] Gordetsky J,Canner J.Frozen section during partial nephrectomy: does it predict positive margins?.BJU Int2015;116:868-72

[35] Puliatti S,Pirola GM.Ex vivo fluorescence confocal microscopy: the first application for real-time pathological examination of prostatic tissue.BJU Int2019;124:469-76

[36] Mir MC,Calatrava A.Ex-vivo confocal fluorescence microscopy for rapid evaluation of renal core biopsy.Minerva Urol Nefrol2020;72:109-13

[37] Prata F,Taffon C.Real-time urethral and ureteral assessment during radical cystectomy using ex-vivo optical imaging: a novel technique for the evaluation of fresh unfixed surgical margins.Curr Oncol2023;30:3421-31 PMCID:PMC10047830

[38] Linehan JA,Hariri LP.Feasibility of optical coherence tomography imaging to characterize renal neoplasms: limitations in resolution and depth of penetration.BJU Int2011;108:1820-4

[39] Hekman MCH,Langenhuijsen JF,Oosterwijk E.Intraoperative imaging techniques to support complete tumor resection in partial nephrectomy.Eur Urol Focus2018;4:960-8

[40] Esperto F,Autrán-Gómez AM.New technologies for kidney surgery planning 3D, impression, augmented reality 3D, reconstruction: current realities and expectations.Curr Urol Rep2021;22:35 PMCID:PMC8143991

[41] Sun Z.Insights into 3D printing in medical applications.Quant Imaging Med Surg2019;9:1-5 PMCID:PMC6351810

[42] Papalia R,Mastroianni R.Accuracy of magnetic resonance imaging to identify pseudocapsule invasion in renal tumors.World J Urol2020;38:407-15

[43] Kim JH,Hwang J.Diagnostic accuracy of contrast-enhanced computed tomography and contrast-enhanced magnetic resonance imaging of small renal masses in real practice: sensitivity and specificity according to subjective radiologic interpretation.World J Surg Oncol2016;14:260 PMCID:PMC5059933

[44] Moldovanu CG,Buruian MM.A systematic review of the clinical value and applications of three-dimensional virtual reconstructions in renal tumors.Med Pharm Rep2022;95:11-23 PMCID:PMC9177088

[45] Bertolo R,Fiori C.Expanding the indications of robotic partial nephrectomy for highly complex renal tumors: urologists’ perception of the impact of hyperaccuracy three-dimensional reconstruction.J Laparoendosc Adv Surg Tech A2019;29:233-9

[46] Porpiglia F,Checcucci E.Three-dimensional virtual imaging of renal tumours: a new tool to improve the accuracy of nephrometry scores.BJU Int2019;124:945-54

[47] Tuderti G,Anceschi U.Assessing the trade-off between the safety and effectiveness of off-clamp robotic partial nephrectomy for renal masses with a high RENAL score: a propensity score-matched comparison of perioperative and functional outcomes in a multicenter analysis.Eur Urol Focus2023;9:1037-43

[48] Liu J,Wang S.Three-dimensional nephrometry scoring system: a precise scoring system to evaluate complexity of renal tumors suitable for partial nephrectomy.PeerJ2020;8:e8637 PMCID:PMC7049461

[49] Yoshitomi KK,Yamamoto T.Improving accuracy, reliability, and efficiency of the RENAL nephrometry score with 3D reconstructed virtual imaging.Urology2022;164:286-92

[50] Huang Q,Zhu J.A three-dimensional, anatomy-based nephrometry score to guide nephron-sparing surgery for renal sinus tumors.Cancer2020;126:2062-72

[51] Mitsui Y,Araki M.The 3-D volumetric measurement including resected specimen for predicting renal function afterrobot-assisted partial nephrectomy.Urology2019;125:104-10

[52] Meyer A,Weinberg AC.Predicting renal parenchymal loss after nephron sparing surgery.J Urol2015;194:658-63

[53] Porpiglia F,Checcucci E.for ESUT Research GroupCurrent use of three-dimensional model technology in urology: a road map for personalised surgical planning.Eur Urol Focus2018;4:652-6

[54] Tang SL,Teo MY,Ling KV.Augmented reality systems for medical applications.IEEE Eng Med Biol Mag1998;17:49-58

[55] Checcucci E,Fiori C.3D imaging applications for robotic urologic surgery: an ESUT YAUWP review.World J Urol2020;38:869-81

[56] Hughes-Hallett A,Marcus HJ.Augmented reality partial nephrectomy: examining the current status and future perspectives.Urology2014;83:266-73

[57] Altamar HO,Glisson CL.Kidney deformation and intraprocedural registration: a study of elements of image-guided kidney surgery.J Endourol2011;25:511-7

[58] Hughes-Hallett A,Mayer E.Intraoperative ultrasound overlay in robot-assisted partial nephrectomy: first clinical experience.Eur Urol2014;65:671-2

[59] Kowalewski KF, Egen L, Fischetti CE, et al; Young Academic Urologists (YAU)-Urotechnology-Group. Artificial intelligence for renal cancer: from imaging to histology and beyond.Asian J Urol2022;9:243-52 PMCID:PMC9399557

[60] Hameed BMZ,Raza SZ.Artificial intelligence and its impact on urological diseases and management: a comprehensive review of the literature.J Clin Med2021;10:1864 PMCID:PMC8123407

[61] Feng Z,Cao P.Machine learning-based quantitative texture analysis of CT images of small renal masses: differentiation of angiomyolipoma without visible fat from renal cell carcinoma.Eur Radiol2018;28:1625-33

[62] Shah M,Somani BK.Artificial intelligence (AI) in urology-current use and future directions: an iTRUE study.Turk J Urol2020;46:S27-39 PMCID:PMC7731952

[63] Kocak B,Bektas CT.Textural differences between renal cell carcinoma subtypes: machine learning-based quantitative computed tomography texture analysis with independent external validation.Eur J Radiol2018;107:149-57

[64] Ding J,Jiang Z.CT-based radiomic model predicts high grade of clear cell renal cell carcinoma.Eur J Radiol2018;103:51-6

[65] Li P,Zhang Y.Fifteen-gene expression based model predicts the survival of clear cell renal cell carcinoma.Medicine2018;97:e11839 PMCID:PMC6113007

[66] Kocak B,Ates E.Radiogenomics in clear cell renal cell carcinoma: machine learning-based high-dimensional quantitative CT texture analysis in predicting PBRM1 mutation status.AJR Am J Roentgenol2019;212:W55-63

[67] Nakawala H,Pescatori LE,Ferrigno G.“Deep-Onto” network for surgical workflow and context recognition.Int J Comput Assist Radiol Surg2019;14:685-96

[68] Amir-Khalili A,Peyrat JM.Automatic segmentation of occluded vasculature via pulsatile motion analysis in endoscopic robot-assisted partial nephrectomy video.Med Image Anal2015;25:103-10

[69] Amparore D, Piramide F, De Cillis S, et al; Renal Cancer Working Group of the Young Academic Urologists (YAU) and European Association of Urology (EAU). Robotic partial nephrectomy in 3D virtual reconstructions era: is the paradigm changed?.World J Urol2022;40:659-70

[70] Veneziano D, Amparore D, Cacciamani G, Porpiglia F; Uro-technology; SoMe Working Group of the Young Academic Urologists Working Party of the European Association of Urology; European Section of Uro-technology. Climbing over the barriers of current imaging technology in urology.Eur Urol2020;77:142-3

[71] Checcucci E,Amparore D.The metaverse in urology: ready for prime time. The ESUT, ERUS, EULIS, and ESU perspective.Eur Urol Open Sci2022;46:96-8 PMCID:PMC9647430