Khaled Fareed a, Tianming Gao b, Sherif Armanyous c, Amr Fergany a, Michael ... the mean eGFR difference was Ð10.6 ml/min (95% confidence interval Ð12.56 ...
EUO-70; No. of Pages 7 E U R O P E A N U R O L O GY O N C O L O G Y X X X ( 2 0 18 ) X X X – X X X
available at www.sciencedirect.com journal homepage: euoncology.europeanurology.com
Transperitoneal Robot-assisted Partial Nephrectomy with Minimum Follow-up of 5 Years: Oncological and Functional Outcomes from a Single Institution Riccardo Bertolo a, Juan Garisto a, Julien Dagenais a, Daniel Sagalovich a, Robert Stein a, Khaled Fareed a, Tianming Gao b, Sherif Armanyous c, Amr Fergany a, Michael Lioudis c, Jihad Kaouk a,* a
Department of Urology, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, OH, USA; b Quantitative Health Sciences, Cleveland Clinic,
Cleveland, OH, USA; c Department of Nephrology, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, OH, USA
Article info
Abstract
Article history: Accepted June 22, 2018
Background: Robot-assisted partial nephrectomy (RAPN) is an established, minimally invasive nephron-sparing technique with excellent perioperative and intermediate oncological outcomes. However, long-term oncological outcomes have not been reported to date. Objective: To report oncological and functional outcomes of RAPN among patients with minimum follow-up of 5 yr. Design, setting, and participants: Data for consecutive patients undergoing RAPN since October 2006 were extracted from a prospectively-maintained institutional PN database. Patients with benign tumors, genetic mutations, prior radical or ipsilateral PN, and those with follow-up of 25%, n (%) a No Yes
Result 206 (178–247) 200 (100–300) 20.0 (14.9–27.0) 236 (85.5) 40 (14.5) 273 (98.2) 5 (1.8) 208 (74.8) 55 (19.8) 15 (5.4) 135 (48.6) 143 (51.4) 3 (3–4) 0.96 (0.83–1.18) 1.03 (0.86–1.27) 1.00 (0.87–1.20) 77.6 (64.3–89.7) 72.5 (57.5–88.0) 76.1 (63.9–90.6) 160 (57.6) 118 (42.4) 255 (91.7) 23 (8.3) 278 (100) 0 (0)
IQR = interquartile range; POD = postoperative day; POM = postoperative month; eGFR = estimated glomerular filtration rate; CKD = chronic kidney disease. a Versus baseline eGFR.
high Fuhrman grade (grades 3–4). Twelve patients (4.3%) had PSMs. The pathological results are reported in Table 3. Twenty-eight deaths (10.1%) occurred in the study cohort during the follow-up period, with five (1.8%) related to metastatic RCC. The 5-yr and 7-yr cumulative incidence was 1.80% for RCC death, 3.61% and 4.16% for local recurrence, and 3.24% and 4.57% for metastasis, respectively. The 5-yr and 7-yr cumulative incidence of death from other cause was 6.47% and 9.30%, respectively (Fig. 1). Univariate competing-risks regression revealed that Fuhrman grade (grade 3–4 vs 1–2; hazard ratio [HR] 8.76; p = 0.051), pathological tumor size (per 1-cm increment; HR 1.67; p < 0.001), and tumor necrosis (HR 16.73; p = 0.002) were predictors of RCC death (Supplementary Fig. 1). Pathological tumor size (per 1-cm increment; HR 1.32; p < 0.001), stage >pT1a (HR 3.38; p = 0.042), and age (per 10-yr increment; HR 1.68; p = 0.018) were predictors of recurrence (Supplementary Fig. 2). Fuhrman grade (grade 3–4 vs 1–2; HR 4.00; p = 0.026), tumor size (for each 1-cm increment; HR 1.45; p = 0.0001), stage >pT1a (HR 3.43; p = 0.038) sarcomatoid pattern (HR 12.09; p = 0.038), and age (per 10-yr increment; HR 1.76; p = 0.0024) were predictors of recurrence (Supplementary Fig. 3). CCI (per 1-point increment; HR 1.40; p < 0.001),
Please cite this article in press as: Bertolo R, et al. Transperitoneal Robot-assisted Partial Nephrectomy with Minimum Follow-up of 5 Years: Oncological and Functional Outcomes from a Single Institution. Eur Urol Oncol (2018), https://doi.org/10.1016/j. euo.2018.06.012
EUO-70; No. of Pages 7 4
E U R O P E A N U R O L O GY O N C O L O GY X X X ( 2 018 ) X X X – X X X
Table 3 – Pathological and oncological outcomes Variable Median tumor size at final pathology, cm (interquartile range) pT stage, n (%) T1a T1b T2a T3a Cystic features, n (%) No Yes Clear cell histology, n (%) No Yes Sarcomatoid pattern, n (%) No Yes Necrosis, n (%) No Yes Fuhrman grade, n (%) a 1 2 3 4 Margin status, n (%) Negative Positive Median follow-up, mo (interquartile range) Local recurrence at 5 yr, n (%) No Yes Metastasis at 5 yr, n (%) No Yes Cause of death at 5 yr, n (%) Renal cell carcinoma Other a
Result 2.7 (2.0–4.0)
201 51 5 21
(72.3) (18.3) (1.8) (7.6)
258 (92.8) 20 (7.2) 96 (34.5) 182 (65.5) 275 (98.9) 3 (1.08) 266 (95.7) 12 (4.32) 9 165 75 8
(3.5) (64.2) (29.2) (3.1)
266 (95.7) 12 (4.3) 70.8 (64.5–80.0) 266 (96.0) 11 (4.0) 267 (96.0) 11 (4.0) 5 (1.8) 23 (8.3)
Assigned in 257 renal cell carcinoma cases.
age (per 10-yr increment; HR 2.51; p 60% were of moderate to high complexity. In addition, intraoperative hemostatic agents were used according to surgeon preference. Hemostatic agents, which were not measured in our study, may have had an impact on bleeding-related complications
Please cite this article in press as: Bertolo R, et al. Transperitoneal Robot-assisted Partial Nephrectomy with Minimum Follow-up of 5 Years: Oncological and Functional Outcomes from a Single Institution. Eur Urol Oncol (2018), https://doi.org/10.1016/j. euo.2018.06.012
EUO-70; No. of Pages 7 6
E U R O P E A N U R O L O GY O N C O L O GY X X X ( 2 018 ) X X X – X X X
[34]. Finally, we acknowledge that because of the small number of postoperative cancer-related events, multivariable regression was not performed.
(The RECORd 1 project). Eur J Surg Oncol 2017;43:823–30. https://doi.org/10.1016/j.ejso.2016.10.016 [5] Lane BR, Campbell SC, Gill IS. 10-Year oncologic outcomes after laparoscopic and open partial nephrectomy. J Urol 2013;190:44–9. [6] Porpiglia F, Mari A, Bertolo R, et al. Partial nephrectomy in clinical
5.
Conclusions
T1b renal tumors: multicenter comparative study of open, laparoscopic and robot-assisted approach (the RECORd project). Urology
Notwithstanding the limitations, this is the first singleinstitution study to report oncological outcomes of RAPN in a consistent population after minimum follow-up of 5 yr, confirming the excellent long-term cancer control in a selected cohort of patients with RCC. Further data on the oncological safety of RAPN in a population with tumors of greater complexity and longer follow-up are still needed. Our results confirm that the renal functional deterioration after RAPN remains stable over time after the early postoperative decrease.
2016;89:45–51. https://doi.org/10.1016/j.urology.2015.08.049 [7] Ghani KR, Sukumar S, Sammon JD, Rogers CG, Trinh QD, Menon M. Practice patterns and outcomes of open and minimally invasive partial nephrectomy since the introduction of robotic partial nephrectomy: results from the nationwide inpatient sample. J Urol 2014;191:907–12. [8] Dev HS, Sooriakumaran P, Stolzenburg JU, Anderson CJ. Is robotic technology facilitating the minimally invasive approach to partial nephrectomy? BJU Int 2012;109:760–8. [9] Minervini A, Vittori G, Antonelli A, et al. Open versus robotic-assisted partial nephrectomy: a multicenter comparison study of perioperative results and complications. World J Urol 2014;32:287–93.
Author contributions: Jihad Kaouk had full access to all the data in the study
[10] Lee S, Oh J, Hong SK, Lee SE, Byun SS. Open versus robot-assisted
and takes responsibility for the integrity of the data and the accuracy of the
partial nephrectomy: effect on clinical outcome. J Endourol
data analysis.
2011;25:1181–5.
Study concept and design: Kaouk, Bertolo.
[11] Ficarra V, Minervini A, Antonelli A, et al. A multicentre matched-
Acquisition of data: Bertolo, Garisto, Dagenais, Sagalovich.
pair analysis comparing robot-assisted versus open partial nephrec-
Analysis and interpretation of data: Bertolo, Garisto.
tomy. BJU Int 2014;113:936–41.
Drafting of the manuscript: Bertolo.
[12] Simone G, Gill IS, Mottrie A, et al. Indications, techniques, outcomes,
Critical revision of the manuscript for important intellectual content: Kaouk,
and limitations for minimally ischemic and off-clamp partial ne-
Stein, Fareed, Fergany, Lioudis.
phrectomy: a systematic review of the literature. Eur Urol
Statistical analysis: Gao.
2015;68:632–40.
Obtaining funding: None.
[13] Simhan J, Smaldone MC, Tsai KJ, et al. Perioperative outcomes of
Administrative, technical, or material support: None.
robotic and open partial nephrectomy for moderately and highly
Supervision: Kaouk.
complex renal lesions. J Urol 2012;187:2000–4.
Other (renal function analysis): Armanyous.
[14] Hennessey DB, Wei G, Moon D, et al. Strategies for success: a multi-
Financial disclosures: Jihad Kaouk certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: Jihad Kaouk has a financial relationship with Endocare and Intuitive. The remaining authors have nothing to disclose.
institutional study on robot-assisted partial nephrectomy for complex renal lesions. BJU Int 2018;121(3 Suppl):40–7. https://doi.org/ 10.1111/bju.14059 [15] Khalifeh A, Autorino R, Eyraud R, et al. Three-year oncologic and renal functional outcomes after robot-assisted partial nephrectomy. Eur Urol 2013;64:744–50. [16] Kyllo RL, Tanagho YS, Kaouk JH, et al. Prospective multi-center study of oncologic outcomes of robot-assisted partial nephrectomy for pT1 renal cell carcinoma. BMC Urol 2012;12:11. [17] Kaouk JH, Khalifeh A, Hillyer S, Haber GP, Stein RJ, Autorino R. Robot-
Funding/Support and role of the sponsor: None.
assisted laparoscopic partial nephrectomy: step-by-step contemporary technique and surgical outcomes at a single high-volume
Appendix A. Supplementary data
institution. Eur Urol 2012;62:553–61. [18] Nuttalla M, van der Meulena J, Embertona M. Charlson scores based
Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.euo.2018.06. 012.
on ICD-10 administrative data were valid in assessing comorbidity in patients undergoing urological cancer surgery. J Clin Epidemiol 2006;59:265–73. [19] Kutikov A, Uzzo RG, The RENAL. nephrometry score: a comprehensive standardized system for quantitating renal tumor size, location and depth. J Urol 2009;182:844–53.
References
[20] Bertolo RG, Zargar H, Autorino R, et al. Estimated glomerular
[1] Campbell SC, Novick AC, Belldegrun A, et al. Guideline for manage-
filtration rate, renal scan and volumetric assessment of the kidney before and after partial nephrectomy: a review of the current
ment of the clinical T1 renal mass. J Urol 2009;182:1271–9. [2] Ljungberg B, Bensalah K, Canfield S, et al. EAU guidelines on renal
literature. Minerva Urol Nefrol 2017;69:539–47. https://doi.org/ 10.23736/S0393-2249.17.02865-X
cell carcinoma: 2014 update. Eur Urol 2015;67:913–24. [3] Rassweiler J, Goezen AS. Laparoscopic partial nephrectomy in the
[21] Dindo D, Demartines N, Clavien PA. Classification of surgical com-
era of robotic surgery: there is a role! Minerva Urol Nefrol
plications: a new proposal with evaluation in a cohort of
2018;70:6–8. https://doi.org/10.23736/S0393-2249.17.03039-9
6336 patients and results of a survey. Ann Surg 2004;240:205–13.
[4] Mari A, Antonelli A, Bertolo R, et al. Predictive factors of
[22] Lopez-Beltran A, Scarpelli M, Montironi R, Kirkali Z. 2004 WHO
overall and major postoperative complications after partial ne-
classification of the renal tumors of the adults. Eur Urol
phrectomy:
2006;49:798–805.
results
from
a
multicenter
prospective
study
Please cite this article in press as: Bertolo R, et al. Transperitoneal Robot-assisted Partial Nephrectomy with Minimum Follow-up of 5 Years: Oncological and Functional Outcomes from a Single Institution. Eur Urol Oncol (2018), https://doi.org/10.1016/j. euo.2018.06.012
EUO-70; No. of Pages 7 7
E U R O P E A N U R O L O G Y O N C O L O GY X X X ( 2 0 18 ) X X X – X X X
[23] Edge S, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A. AJCC
[29] Antonelli A, Furlan M, Sodano M, et al. Features, risk factors and
cancer staging manual. ed. 7 New York, NY: Springer; 2009.
clinical outcome of “very late” recurrences after surgery for local-
[24] Patel SG, Penson DF, Pabla B, et al. National trends in the use of
ized renal carcinoma: a retrospective evaluation of a cohort with a
partial nephrectomy: a rising tide that has not lifted all boats. J Urol
minimum of 10 years of follow up. Int J Urol 2016;23:36–40.
2012;187:816–21.
https://doi.org/10.1111/iju.12962
[25] Abdel Raheem A, Alatawi A, Kim DK, et al. Outcomes of high-
[30] Becker A, Hickmann D, Hansen J, et al. Critical analysis of a simplified
complexity renal tumours with a Preoperative Aspects and Dimen-
Fuhrman grading scheme for prediction of cancer specific mortality in
sions Used for an Anatomical (PADUA) score of 10 after robot-
patients with clear cell renal cell carcinoma—impact on prognosis. Eur J
assisted partial nephrectomy with a median 46.5-month follow-up:
Surg Oncol 2016;42:419–25. https://doi.org/10.1016/j.ejso.201509.023
a tertiary centre experience. BJU Int 2016;118:770–8. https://doi.
[31] Cheung DC, Finelli A. Active surveillance in small renal masses in
org/10.1111/bju.13501 [26] Andrade HS, Zargar H, Caputo PA, et al. Five-year oncologic outcomes after transperitoneal robotic partial nephrectomy for renal
the elderly: a literature review. Eur Urol Focus 2017;3:340–51. https://doi.org/10.1016/j.euf.2017.11.005 [32] Mir MC, Ercole C, Takagi T, et al. Decline in renal function after
cell carcinoma. Eur Urol 2016;69:1149–54. https://doi.org/10.1016/
partial
j.eururo.2015.12.004
2015;193:1889–98. https://doi.org/10.1016/j.juro.2015.01.093
nephrectomy:
etiology
and
prevention.
J
Urol
[27] Vartolomei MD, Matei DV, Renne G, et al., Robot-assisted partial
[33] Porpiglia F, Fiori C, Bertolo R, et al. Long-term functional evaluation of
nephrectomy: 5-yr oncological outcomes at a single European
the treated kidney in a prospective series of patients who underwent
tertiary cancer center. Eur Urol Focus. In press. https://doi.org/
laparoscopic partial nephrectomy for small renal tumors. Eur Urol
10.1016/j.euf.2017.10.005.
2012;62:130–5. https://doi.org/10.1016/j.eururo.2012.02.001
[28] Beauval JB, Peyronnet B, Benoit T, et al. Long-term oncological
[34] Antonelli A, Minervini A, Mari A, et al. TriMatch comparison of the
outcomes after robotic partial nephrectomy for renal cell carcino-
efficacy of FloSeal versus TachoSil versus no hemostatic agents for
ma: a prospective multicentre study. World J Urol 2018;36:897–
partial nephrectomy: results from a large multicenter dataset. Int J
904. https://doi.org/10.1007/s00345-018-2208-8
Urol 2015;22:47–52. https://doi.org/10.1111/iju.1260.3
Please cite this article in press as: Bertolo R, et al. Transperitoneal Robot-assisted Partial Nephrectomy with Minimum Follow-up of 5 Years: Oncological and Functional Outcomes from a Single Institution. Eur Urol Oncol (2018), https://doi.org/10.1016/j. euo.2018.06.012