Predictors of Positive Surgical Margins after Robot-Assisted Partial Nephrectomy for Localized Renal Tumors: Insights from a Large Multicenter International Prospective Observational Project (The Surface-Intermediate-Base Margin Score Consortium)
Abstract
:1. Introduction
2. Materials and Methods
2.1. Patient and Dataset
2.2. Objectives of the Study
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Campbell, S.; Uzzo, R.G.; Allaf, M.E.; Bass, E.; Cadeddu, J.A.; Chang, A.; Clark, P.E.; Davis, B.; Derweesh, I.H.; Giambarresi, L.; et al. Renal Mass and Localized Renal Cancer: AUA Guideline. J. Urol. 2017, 198, 520–529. [Google Scholar] [CrossRef] [Green Version]
- Ljungberg, B.; Albiges, L.; Abu-Ghanem, Y.; Bensalah, K.; Dabestani, S.; Fernandez-Pello, S.; Giles, R.H.; Hofmann, F.; Hora, M.; Kuczyk, M.A.; et al. European Association of Urology Guidelines on Renal Cell Carcinoma: The 2019 Update. Eur. Urol. 2019, 75, 799–810. [Google Scholar] [CrossRef] [PubMed]
- Citamak, B.; Haberal, H.B.; Akdogan, B. Assessing the Association of Surface-Intermediate-Base Margin Score with Perioperative Outcomes and Parenchymal Volume Preserved during Partial Nephrectomy. Urol. Int. 2020, 104, 781–788. [Google Scholar] [CrossRef] [PubMed]
- Klingler, M.J.; Babitz, S.K.; Kutikov, A.; Campi, R.; Hatzichristodoulou, G.; Sanguedolce, F.; Brookman-May, S.; Akdogan, B.; Capitanio, U.; Roscigno, M.; et al. Assessment of volume preservation performed before or after partial nephrectomy accurately predicts postoperative renal function: Results from a prospective multicenter study. Urol. Oncol. Semin. Orig. Investig. 2018, 37, 33–39. [Google Scholar] [CrossRef] [PubMed]
- Minervini, A.; Campi, R.; Sessa, F.; Derweesh, I.; Kaouk, J.H.; Mari, A.; Rha, K.H.; Sessa, M.; Volpe, A.; Carini, M.; et al. Positive surgical margins and local recurrence after simple enucleation and standard partial nephrectomy for malignant renal tumors: Systematic review of the literature and meta-analysis of prevalence. Minerva Urol. e Nefrol. Ital. J. Urol. Nephrol. 2017, 69, 523–538. [Google Scholar] [CrossRef] [PubMed]
- Schiavina, R.; Mari, A.; Bianchi, L.; Amparore, D.; Antonelli, A.; Artibani, W.; Brunocilla, E.; Capitanio, U.; Fiori, C.; Di Maida, F.; et al. Predicting positive surgical margins in partial nephrectomy: A prospective multicentre observational study (the RECORd 2 project). Eur. J. Surg. Oncol. (EJSO) 2020, 46, 1353–1359. [Google Scholar] [CrossRef]
- Borghesi, M.; Brunocilla, E.; Schiavina, R.; Martorana, G. Positive Surgical Margins After Nephron-Sparing Surgery for Renal Cell Carcinoma: Incidence, Clinical Impact, and Management. Clin. Genitourin. Cancer 2013, 11, 5–9. [Google Scholar] [CrossRef]
- Schiavina, R.; Serni, S.; Mari, A.; Antonelli, A.; Bertolo, R.; Bianchi, G.; Brunocilla, E.; Borghesi, M.; Carini, M.; Longo, N.; et al. A Prospective, Multicenter Evaluation of Predictive Factors for Positive Surgical Margins After Nephron-Sparing Surgery for Renal Cell Carcinoma: The RECORd1 Italian Project. Clin. Genitourin. Cancer 2014, 13, 165–170. [Google Scholar] [CrossRef]
- Dagenais, J.; Bertolo, R.; Garisto, J.; Maurice, M.J.; Mouracade, P.; Kara, O.; Chavali, J.; Li, J.; Nelson, R.; Fergany, A.; et al. Variability in Partial Nephrectomy Outcomes: Does Your Surgeon Matter? Eur. Urol. 2018, 75, 628–634. [Google Scholar] [CrossRef]
- Minervini, A.; Carini, M.; Uzzo, R.G.; Campi, R.; Smaldone, M.C.; Kutikov, A. Standardized Reporting of Resection Technique During Nephron-sparing Surgery: The Surface—Intermediate—Base Margin Score. Eur. Urol. 2014, 66, 803–805. [Google Scholar] [CrossRef]
- Minervini, A.; Campi, R.; Lane, B.R.; De Cobelli, O.; Sanguedolce, F.; Hatzichristodoulou, G.; Antonelli, A.; Noyes, S.; Mari, A.; Rodriguez-Faba, O.; et al. Impact of Resection Technique on Perioperative Outcomes and Surgical Margins after Partial Nephrectomy for Localized Renal Masses: A Prospective Multicenter Study. J. Urol. 2020, 203, 496–504. [Google Scholar] [CrossRef] [PubMed]
- Ficarra, V.; Novara, G.; Secco, S.; Macchi, V.; Porzionato, A.; De Caro, R.; Artibani, W. Preoperative Aspects and Dimensions Used for an Anatomical (PADUA) Classification of Renal Tumours in Patients who are Candidates for Nephron-Sparing Surgery. Eur. Urol. 2009, 56, 786–793. [Google Scholar] [CrossRef] [PubMed]
- Kutikov, A.; Uzzo, R.G. The RENAL Nephrometry Score: A Comprehensive Standardized System for Quantitating Renal Tumor Size, Location and Depth. J. Urol. 2009, 182, 844–853. [Google Scholar] [CrossRef]
- Bertolo, R.; Pozzi, L. From PADUA to RENAL Score and Vice Versa: Development and Validation of a Mathematical Converter. J. Urol. 2019, 201, 674–675. [Google Scholar] [CrossRef] [PubMed]
- Brierley, J.D.; Gospodarowicz, M.K.; Wittekind, C. TNM Classification of Malignant Tumours, 8th ed.; John Wiley & Sons: Hoboken, NJ, USA, 2017. [Google Scholar] [CrossRef]
- Delahunt, B.; Cheville, J.C.; Martignoni, G.; Humphrey, P.A.; Magi-Galluzzi, C.; McKenney, J.; Egevad, L.; Algaba, F.; Moch, H.; Grignon, D.J.; et al. The International Society of Urological Pathology (ISUP) Grading System for Renal Cell Carcinoma and Other Prognostic Parameters. Am. J. Surg. Pathol. 2013, 37, 1490–1504. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gupta, G.N.; Boris, R.S.; Campbell, S.C.; Zhang, Z. Tumor Enucleation for Sporadic Localized Kidney Cancer: Pro and Con. J. Urol. 2015, 194, 623–625. [Google Scholar] [CrossRef]
- Cao, D.-H.; Liu, L.-R.; Fang, Y.; Tang, P.; Li, T.; Bai, Y.; Wang, J.; Wei, Q. Simple tumor enucleation may not decrease oncologic outcomes for T1 renal cell carcinoma: A systematic review and meta-analysis. Urol. Oncol. Semin. Orig. Investig. 2017, 35, 661.e15–661.e21. [Google Scholar] [CrossRef]
- Azhar, R.A.; Abreu, A.L.D.C.; Broxham, E.; Sherrod, A.; Ma, Y.; Cai, J.; Gill, T.S.; Desai, M.; Gill, I.S. Histological Analysis of the Kidney Tumor-Parenchyma Interface. J. Urol. 2015, 193, 415–422. [Google Scholar] [CrossRef]
- Minervini, A.; Campi, R.; Di Maida, F.; Mari, A.; Montagnani, I.; Tellini, R.; Tuccio, A.; Siena, G.; Vittori, G.; Lapini, A.; et al. Tumor–parenchyma interface and long-term oncologic outcomes after robotic tumor enucleation for sporadic renal cell carcinoma. Urol. Oncol. Semin. Orig. Investig. 2018, 36, 527.e1–527.e11. [Google Scholar] [CrossRef]
- Carini, M.; Campi, R.; Mari, A.; Minervini, A. Oncologic Safety of Robotic Partial Nephrectomy: Setting Tiles in the Mosaic of Evidence While Designing Future Research Projects. Eur. Urol. Focus 2019, 5, 357–360. [Google Scholar] [CrossRef]
- Campi, R.; Di Maida, F.; Lane, B.R.; De Cobelli, O.; Sanguedolce, F.; Hatzichristodoulou, G.; Antonelli, A.; Noyes, S.; Mari, A.; Grosso, A.A.; et al. Impact of surgical approach and resection technique on the risk of Trifecta Failure after partial nephrectomy for highly complex renal masses. Eur. J. Surg. Oncol. (EJSO) 2021, 48, 687–693. [Google Scholar] [CrossRef] [PubMed]
- Mari, A.; Di Maida, F.; Tellini, R.; Campi, R.; Sforza, S.; Cocci, A.; Siena, G.; Vittori, G.; Tuccio, A.; Masieri, L.; et al. Oncologic outcomes in patients treated with endoscopic robot assisted simple enucleation (ERASE) for renal cell carcinoma: Results from a tertiary referral center. Eur. J. Surg. Oncol. (EJSO) 2019, 45, 1977–1982. [Google Scholar] [CrossRef] [PubMed]
- Dong, W.; Chen, X.; Huang, M.; Chen, X.; Gao, M.; Ou, D.; Li, K.; Wang, C.; Wu, S.; Liu, H.; et al. Long-Term Oncologic Outcomes After Laparoscopic and Robotic Tumor Enucleation for Renal Cell Carcinoma. Front. Oncol. 2021, 10, 595457. [Google Scholar] [CrossRef] [PubMed]
- Mari, A.; Morselli, S.; Sessa, F.; Campi, R.; Di Maida, F.; Greco, I.; Siena, G.; Tuccio, A.; Vittori, G.; Serni, S.; et al. Impact of the off-clamp endoscopic robot-assisted simple enucleation (ERASE) of clinical T1 renal tumors on the postoperative renal function: Results from a matched-pair comparison. Eur. J. Surg. Oncol. (EJSO) 2018, 44, 853–858. [Google Scholar] [CrossRef] [PubMed]
- Bertolo, R.; Simone, G.; Garisto, J.; Nakhoul, G.; Armanyous, S.; Agudelo, J.; Costantini, M.; Tuderti, G.; Gallucci, M.; Kaouk, J. Off-clamp vs on-clamp robotic partial nephrectomy: Perioperative, functional and oncological outcomes from a propensity-score matching between two high-volume centers. Eur. J. Surg. Oncol. (EJSO) 2019, 45, 1232–1237. [Google Scholar] [CrossRef]
- Anceschi, U.; Brassetti, A.; Bertolo, R.; Tuderti, G.; Ferriero, M.C.; Mastroianni, R.; Flammia, R.S.; Costantini, M.; Kaouk, J.; Leonardo, C.; et al. On-clamp versus purely off-clamp robot-assisted partial nephrectomy in solitary kidneys: Comparison of perioperative outcomes and chronic kidney disease progression at two high- volume centers. Minerva Urol. Nephrol. 2020, 73, 739–745. [Google Scholar] [CrossRef]
- Mellouki, A.; Bentellis, I.; Morrone, A.; Doumerc, N.; Beauval, J.-B.; Roupret, M.; Nouhaud, F.-X.; Lebacle, C.; Long, J.-A.; Chevallier, D.; et al. Evaluation of oncological outcomes of robotic partial nephrectomy according to the type of hilar control approach (On-clamp vs. Off-clamp), a multicentric study of the French network of research on kidney cancer—UROCCR 58-NCT03293563. World J. Urol. 2021, 1–8. [Google Scholar] [CrossRef]
- Porpiglia, F.; Amparore, D.; Checcucci, E.; Manfredi, M.; Stura, I.; Migliaretti, G.; Autorino, R.; Ficarra, V.; Fiori, C. Three-dimensional virtual imaging of renal tumours: A new tool to improve the accuracy of nephrometry scores. Br. J. Urol. 2019, 124, 945–954. [Google Scholar] [CrossRef]
- Bianchi, L.; Schiavina, R.; Bortolani, B.; Cercenelli, L.; Gaudiano, C.; Carpani, G.; Rustici, A.; Droghetti, M.; Mottaran, A.; Boschi, S.; et al. Interpreting nephrometry scores with three-dimensional virtual modelling for better planning of robotic partial nephrectomy and predicting complications. Urol. Oncol. Semin. Orig. Investig. 2021, 39, 836.e1–836.e9. [Google Scholar] [CrossRef]
- DI Maida, F.; Vittori, G.; Campi, R.; Mari, A.; Tellini, R.; Sforza, S.; Sessa, F.; Lucarini, S.; Miele, V.; Vignozzi, L.; et al. Clinical predictors and significance of adherent perinephric fat assessed with Mayo Adhesive Probability (MAP) score and Perinephric Fat Surface Density (PnFSD) at the time of partial nephrectomy for localized renal mass. A single high-volume referral centre experience. Minerva Urol. Nephrol. 2020, 73, 225–232. [Google Scholar] [CrossRef]
Preoperative Features | ||
---|---|---|
Age, Median (IQR) | 61 (53–69) | |
Gender, n (%) | Male | 154 (53.3%) |
Female | 135 (46.7%) | |
BMI, median (IQR) | 26.3 (24.0–30.0) | |
ASA score, median (IQR) | 2 (2–2) | |
ASA score ≥ 3, n (%) | 48 (16.6%) | |
Charlson Score, median (IQR) | 1 (1–2) | |
Tumour diameter (cm), median (IQR) | 3.0 (2.3–4.2) | |
Tumor side, n (%) | Right | 154 (53.3) |
Left | 135 (46.7) | |
cT stage, n (%) | T1a | 198 (68.5) |
T1b-T2 | 91 (31.5) | |
PADUA score, median (IQR) | 8 (7–9) | |
Preoperative eGFR, median (IQR) | 87.8 (72.8–97.4) | |
Intraoperative features | ||
Approach, n. % | Transperitoneal | 264 (91.3) |
Retroperitoneal | 25 (8.7) | |
Hilar clamping, n. % | 234 (80.9%) | |
Warm Ischemia Time (min), median (IQR) | 16 (14–21) | |
EBL (cc), median (IQR) | 150 (90–210) | |
Operative time, median (IQR) | 140 (115–190) | |
SIB score, n. % | SIB score 0–2 | 154 (53.3) |
SIB score 3–4 | 79 (27.3) | |
SIB score 5 | 56 (19.4) |
Postoperative and Anathomopathological Features | ||
---|---|---|
Pathological diameter (cm), median (IQR) | 3.0 (2.2–4.0) | |
Tumor nature, n. (%) | Benign | 72 (24.9) |
Malignant | 217 (75.1) | |
pT stage, n. (%) (among malignant tumors, n = 217) | pT1a | 158 (72.8) |
pT1b | 43 (19.8) | |
pT2 | 5 (2.3) | |
pT3a | 11 (5.1) | |
Positive Surgical Margins, n. (%) | 18 (6.2) | |
Positive Surgical Margins rate according to resection technique, n. (%) | SIB score 0–2 | 7/154 (4.5) |
SIB score 3–4 | 9/79 (11.4) | |
SIB score 5 | 2/56 (3.6) | |
RCC Histotype, n. (%) | Clear Cell (cc-RCC) | 149 (51.6) |
Papillary (p-RCC) | 34 (11.8) | |
Chromofobe (ch-RCC) | 22 (7.6) | |
Oncocytoma | 46 (15.9) | |
Angiomyolipoma | 26 (9.0) | |
Other RCC subtypes | 12 (4.2) |
Preoperative Features | NSM (n = 271) | PSM (n = 18) | p Value | |
---|---|---|---|---|
Age, median (IQR) | 61 (54–69) | 64 (52–68) | 0.99 | |
Gender, n (%) | Male | 170 (62.7) | 13 (72.2) | 0.41 |
Female | 101 (37.3) | 5 (27.8) | ||
BMI, median (IQR) | 26.3 (24–30) | 25.8 (23.7–32.6) | 0.19 | |
ASA score, median (IQR) | 2 (2–2) | 2 (2–3) | 0.26 | |
ASA score ≥ 3, n (%) | 43 (15.9) | 5 (27.8%) | 0.20 | |
Charlson Score, median (IQR) | 1 (1–2) | 1 (1–2) | 0.43 | |
Tumour diameter, median (IQR) | 3.0 (2.3–4.2) | 2.8 (1.9–3.9) | 0.42 | |
cT stage, n (%) | T1a | 184 | 14 | 0.38 |
T1b-T2 | 87 | 4 | ||
PADUA score, median (IQR) | 8 (7–9) | 8 (7–9) | 0.31 | |
Contact with urinary collecting system, n (%) | 74 (27.3) | 10 (55.6) | <0.001 | |
Preoperative eGFR, median (IQR) | 87.8 (73.2–98.2) | 86.5 (67.4–93.5) | 0.39 | |
Intraoperative Features | NSN (n = 271) | PSM (n = 18) | p Value | |
Approach, n. % | Transperitoneal | 246 | 18 | 0.18 |
Retroperitoneal | 25 | 0 | ||
Hilar clamping, n. % | 217 (80.1) | 16 (88.9) | 0.37 | |
Warm Ischemia Time (min), median IQR | 16 (13–20) | 22 (16–26) | 0.02 | |
EBL (cc), median IQR | 150 (90–210) | 160 (95–220) | 0.63 | |
Operative Time, median IQR | 140 (115–190) | 145 (120–200) | 0.58 | |
SIB score, n. % | SIB score 0–2 | 147 (54.2) | 7 (38.9) | 0.08 |
SIB score 3–4 | 70 (25.8) | 9 (50) | ||
SIB score 5 | 54 (19.9) | 2 (11.1) | ||
Postoperative Features | NSN (n = 271) | PSM (n = 18) | p Value | |
Pathological diameter (cm), median (IQR) | 3.0 (2.2–4.0) | 2.9 (1.8–4.0) | 0.74 | |
Tumor nature, n. (%) | Bening | 70 (25.8) | 2 (11.1) | 0.08 |
Malignant | 201 (74.2) | 16 (88.9) | ||
pT stage, n. (%) (among malignant tumors, n = 217) | pT1a | 146 (72.6) | 12 (75) | 0.47 |
pT1b | 41 (20.4) | 2 (12.5) | ||
pT2 | 5 (2.5) | 0 (0.0) | ||
pT3a | 9 (4.5) | 2 (12.5) | ||
RCC Histotype, n. (%) | Clear Cell (cc–RCC) | 137 (50.6) | 12 (66.7) | 0.59 |
Papillary (p–RCC) | 31 (11.4) | 3 (16.7) | ||
Chromophobe (ch–RCC) | 21 (7.7) | 1 (5.6) | ||
Oncocytoma | 45 (16.6) | 1 (5.6) | ||
Angiomyolipoma | 25 (9.2) | 1 (5.6) | ||
Other RCC subtypes | 12 (4.4) | 0 (0.0) |
z | Univariable Analysis | Multivariable Analysis | ||||||
---|---|---|---|---|---|---|---|---|
OR | 95% CI | p Value | Standard Error | OR | 95% CI | p Value | ||
Pathological diameter (continuous) | 1.26 | 1.10–1.44 | 0.001 | 0.22 | 0.81 | 0.54–1.25 | 0.36 | |
Ischemia | Clampless | 1.74 | 1.14–4.79 | 0.02 | 0.79 | 0.55 | 0.12–2.58 | 0.45 |
Clamp (ref) | - | - | - | - | - | - | - | |
Contact with urinary collecting system | Yes | 1.22 | 1.11–1.52 | 0.001 | 0.74 | 1.33 | 0.78–2.49 | 0.21 |
No (ref) | - | - | - | - | - | - | - | |
PADUA score | ≥10 | 2.17 | 1.37–3.44 | 0.001 | 0.78 | 0.74 | 0.16–3.41 | 0.69 |
8–9 | 1.46 | 0.88–2.41 | 0.14 | 0.57 | 1.53 | 0.49–4.67 | 0.45 | |
6–7 (ref) | - | - | - | - | - | - | - | |
SIB score | 5 | 0.92 | 0.83–1.01 | 0.09 | 0.84 | 1.56 | 0.30–8.09 | 0.62 |
3–4 | 3.11 | 1.76–5.51 | <0.001 | 0.54 | 2.68 | 1.25–7.63 | 0.04 | |
0–2 (ref) | - | - | - | - | - | - | - |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Di Maida, F.; Campi, R.; Lane, B.R.; De Cobelli, O.; Sanguedolce, F.; Hatzichristodoulou, G.; Antonelli, A.; Grosso, A.A.; Noyes, S.; Rodriguez-Faba, O.; et al. Predictors of Positive Surgical Margins after Robot-Assisted Partial Nephrectomy for Localized Renal Tumors: Insights from a Large Multicenter International Prospective Observational Project (The Surface-Intermediate-Base Margin Score Consortium). J. Clin. Med. 2022, 11, 1765. https://doi.org/10.3390/jcm11071765
Di Maida F, Campi R, Lane BR, De Cobelli O, Sanguedolce F, Hatzichristodoulou G, Antonelli A, Grosso AA, Noyes S, Rodriguez-Faba O, et al. Predictors of Positive Surgical Margins after Robot-Assisted Partial Nephrectomy for Localized Renal Tumors: Insights from a Large Multicenter International Prospective Observational Project (The Surface-Intermediate-Base Margin Score Consortium). Journal of Clinical Medicine. 2022; 11(7):1765. https://doi.org/10.3390/jcm11071765
Chicago/Turabian StyleDi Maida, Fabrizio, Riccardo Campi, Brian R. Lane, Ottavio De Cobelli, Francesco Sanguedolce, Georgios Hatzichristodoulou, Alessandro Antonelli, Antonio Andrea Grosso, Sabrina Noyes, Oscar Rodriguez-Faba, and et al. 2022. "Predictors of Positive Surgical Margins after Robot-Assisted Partial Nephrectomy for Localized Renal Tumors: Insights from a Large Multicenter International Prospective Observational Project (The Surface-Intermediate-Base Margin Score Consortium)" Journal of Clinical Medicine 11, no. 7: 1765. https://doi.org/10.3390/jcm11071765
APA StyleDi Maida, F., Campi, R., Lane, B. R., De Cobelli, O., Sanguedolce, F., Hatzichristodoulou, G., Antonelli, A., Grosso, A. A., Noyes, S., Rodriguez-Faba, O., Keeley, F. X., Langenhuijsen, J., Musi, G., Klatte, T., Roscigno, M., Akdogan, B., Furlan, M., Simeone, C., Karakoyunlu, N., ... SIB International Consortium. (2022). Predictors of Positive Surgical Margins after Robot-Assisted Partial Nephrectomy for Localized Renal Tumors: Insights from a Large Multicenter International Prospective Observational Project (The Surface-Intermediate-Base Margin Score Consortium). Journal of Clinical Medicine, 11(7), 1765. https://doi.org/10.3390/jcm11071765