Curr Urol Rep (2016) 17:7 DOI 10.1007/s11934-015-0560-4
KIDNEY DISEASES (G CIANCIO, SECTION EDITOR)
Simple Enucleation for Renal Tumors: Indications, Techniques, and Results Adolfo García García 1 & Tania González León 2
# Springer Science+Business Media New York 2016
Abstract Kidney cancer is the 13th most common malignancy worldwide with significant increase in Stage I renal cell cancer (RCC). Surgical excision by nephron sparing surgery (NSS) remains the treatment of choice for small renal masses (SRMs). One of the variants of partial nephrectomy is simple enucleation (SE) or tumor enucleation (TE). The present review comments on the indications and technical aspects of SE as well as its outcomes. SE/TE has shown both perioperative and oncologic satisfactory results, comparable to partial nephrectomy (PN). It is a valid technique for SRMs and achieves maximum renal parenchymal preservation with an insignificant impact on renal function. Keywords Renal simple enucleation . Renal tumor enucleation . Renal tumor . Partial nephrectomy . Nephron sparing surgery . Small renal mass
Introduction Kidney cancer is the 13th most common malignancy worldwide; over 90 % of renal tumors were renal cell cancer (RCC),
This article is part of the Topical Collection on Kidney Diseases * Tania González León
[email protected];
[email protected] 1
Department of Urology, Hermanos Ameijeiras Hospital, San Lázaro y Belascoain, Centro Habana, 10800 La Habana, Cuba
2
Department of Urology, National Center of Minimal Invasive Surgery, Párraga 215 e/ San Mariano y Vista Alegre, Víbora CP, 10700 La Habana, Cuba
accounting for 2–3 % of all cancers in adults. There were a total of 342,501 newly diagnosed cases in the USA in the period 2001–2010 [1, 2, 3•, 4]. There has been an increase in the global incidence of RCC, with the highest rise in rates seen for localized stage tumors. The incidence of RCC in men is 1.5–2.0 times greater; the peak age of incidence is 60–70 years. A significant increase in Stage I RCC with a decrease in Stage II–IV RCC has been reported. Most RCCs are sporadic; 20–30 % of patients with RCC present with metastatic disease [1, 2, 5, 6]. The increased incidence of RCC has been attributed to the incidental diagnosis of small, asymptomatic renal masses due to more frequent usage of CT scan. But, early detection of localized renal masses is yet to translate into any notable impact on RCC-related mortality [1]. Small renal mass (SRM) is defined as any enhancing solid renal mass 50 % of endophytic renal masses. Other advantage of HA are as follows: the tactile feedback during enucleation allows complete removal along the natural cleavage planes of the renal parenchyma. On the other hand, there is no need for vascular clamping, and this permits the correct view of the tumor thus allowing its examination at different angles, facilitating manual mobilization of the tumor bed. Another advantage is the possibility to explore the tumor bed without specific time constraint and to obtain margins of the specimen and the tumor bed prior to the reconstruction of the renal parenchyma [30, 39, 41]. Retroperitoneal approach or lumboscopy allows a direct and faster identification of the artery. This approach offers advantages in obese patients and in patients who had previous abdominal surgery, and avoids contamination of the abdominal cavity with the blood and urine improving transoperative results [9, 52]. Robotic-assisted retroperitoneal approach without pedicle clamping has been described. An important series of RA-PN was reported, but none with zero ischemia time, although there are few reports in medical literature of robotic-assisted renal enucleation, even less without pedicle ischemia [40]. Endoscopic robotic-assisted simple enucleation (ERASE), which represents the transposition of open SE to robotic surgery and is becoming the standard technique of NSS, has been described. The disadvantage of retroperitoneal approach when robotic-assisted is the restricted space to position the robot’s arms [14•, 40].
Results SE reports show encouraging oncologic, renal function, and transoperative results. To assess this, we may apply the new concept of a Btrifecta^ of outcomes of robotic or laparoscopic PN that implies negative cancer margin, functional preservation, and no urologic complications [9, 18, 53]. Renal TE has oncologic outcomes comparable with both laparoscopic and open PN. No significant differences between PN and TE have been reported in relation to morbidity and
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mortality. It has currently been considered impossible to design comparable studies between RN and TE. It is clear that RN is not a suitable option to treat well-encapsulated tumors so as to improve the preservation of renal function. It has been reported that the incidence of PSM is similar in laparoscopic PN (LPN) and open PN (OPN). Even in comparative studies, the risk of PSM was significantly lower in SE compared to PN, with a 4.7-fold increased risk of PSM for PN when a multi-varied study was carried out. The proximity between the margins of the tumor and healthy parenchyma during tumor resection explains the fear of having a higher risk of PSM [9, 54••, 55•]. The rate of PSM has been reported as 0–7 %. In published studies, they have varied: 5.5, 1.6, 2.8, and 0 %, respectively, although further studies with a higher level of evidence are necessary to confirm this outcome. Nevertheless, in series of patients with imperative indications for SE, the incidence of PSM has been considered high. An elevated incidence of PSM has also been observed when the tumor is smaller because in small tumors, it is more difficult to estimate the extension of the tumor, and the absence or incomplete development of the pseudocapsule can contribute to these results; besides, there is a higher potential of accidentally destroying the specimen during enucleation when the technique is tried with SRM [25, 56]. Many investigations have demonstrated that the rates of local recurrence-free survival and cancer-specific survival are comparable to NP, at least for renal tumors with clinical diameter up to 7 cm [12•, 16]. Rates of 0.6 % local recurrence have been considered acceptable because the reports, in general, waver between 0 and 45 % against 0–6 % in NSS. The relation of local recurrence has been considered by means of Fuhrman grade and RCC histologic subtype, as well as with metachronous multifocal RCC or synchronous multifocal RCC undiagnosed in imaging studies previous to surgery [24]. There is no evidence of statistical differences in reference to progression-free survival, cancer-specific survival estimates, and local recurrence rate between PN and SE, even in the only published multicenter study which we have consulted, which reports at 5 and 10 years, a progressionfree survival estimates of 88.9 and 82 % after PN, and 91.4 and 90.8 % after SE and the 5- and 10-year cancer-specific survival estimates of 93.9 and 91.6 % in PN, and 94.3 and 93.2 % in SE. PN has been compared with SE, cancer-specific survival in a 10-year follow-up was similar, but, likewise, further studies with higher levels of evidence are required to confirm these results [12•]. The outcome has also been satisfactory in relation to renal function. It is obvious that the minimal impact of this technique on RF is related to less loss of healthy renal parenchyma.
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In reported studies about SE, malignant tumors and RCC histologic type with Fuhrman grade 1–2 and stage p T1a prevailed. In a multi-varied study, the worst prognosis was linked to nuclear grade [55•]. The surgical outcome and complication rate of tumor enucleation are comparable to LPN. The most common reported complications in TE, which would require reintervention, are urinary fistula, which would entail a JJ stent, and postoperative bleeding, which has been reported between 0 and 7 %; whereas PN reports 4.4 % of urinary fistula and 3.1 % of severe postoperative bleeding [16, 54••]. Current evidence shows few complications, particularly of urinary fistula in SE. The measurement of the tumor, the grade of intrarenal growth, and the relation with the urinary collecting system (UCS) increase the risk of complications. It has been reported in a rate of 0.5 and 2 % of cases, respectively. The possible explanation that these excellent transoperative outcomes in SE with low complication rates could be due to the fact that not resecting healthy parenchyma around the tumor results in less theoretical risk of postoperative bleeding and damage of the UCS which is the cause of urinary fistula. There is evidence of a strong correlation among nephrometric characteristics of the lesion and severe bleeding and urinary fistula. Comparative studies between TE and laparoscopic PN will be necessary to investigate which tumors, taking into consideration their anatomical characteristics, will have a better outcome with TE than with PN. The correlation was confirmed in a study that correlated PADUA score with surgical complications. An unfavorable nephrometry is directly related to the occurrence of these complications. Each increasing point in PADUA score was associated to a higher risk of surgical complications and Clavein Dindo complexity grade [16, 34•, 57]. Low complication rates have also been reported when robotic assistance (RASE) has been used. RAPN, at least in T1a tumors, has not only shown oncologic results equivalents to LPN, but with more advantages over some transoperative outcomes. RAPN has improved LPN surgical outcome, especially by reducing the WIT, EBL, and among other parameters. Besides, it requires less pedicle clamping. RASE has been considered a feasible technique with WIT rates and complications similar to the open approach, with the advantages of mini-invasiveness. Enucleation offers the benefits of reduced surgical entry into the renal sinus, operative time, favorable impact on renal function, and satisfactory oncologic outcomes which is why it has been considered a useful technique for patients that require minimally invasive PN [14•, 18]. Encouraging results have also been reported in tumors that are considered complex [58].
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Conclusions TE is an arduous technique that requires trained surgeons especially when performed by minimal invasion: laparoscopically or robotic-assisted, which have shown both perioperative and oncologic satisfactory results, comparable to PN. It is a valid surgical variant for SRMs and achieves maximum renal parenchymal preservation with an insignificant impact on renal function; nevertheless, other studies are required that contribute to improve the levels of evidence of the results shown today.
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Compliance with Ethical Standards Conflict of Interest The authors declare that they have no competing interests. Human and Animal Rights and Informed Consent This article does not contain any studies with human or animal subjects performed by any of the authors.
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References 15.
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance 1.
2. 3.•
4.
5.
6.
7.•
8.
Kenney PA, Wszolek MF, Libertino JA. Open partial nephrectomy. In: Libertino JA editor. Renal cancer: contemporary management, 211. doi:10.1007/978-1-4614-7236-0_13, © Springer Science + Business Media New York; 2013. Bhatt JR, Finelli A. Landmarks in the diagnosis and treatment of renal cell carcinoma. Nat Rev Urol. 2014;11(9):517–25. González J, Cózar JM, Gómez A, Fernández-Pérez C, Esteban M. Nephron-sparing surgery in renal cell carcinoma: current perspectives on technical issues. Curr Urol Rep. 2015;16(2):6. This paper is an excellent update review about the current status of nephron-sparing surgery for solid renal masses with an emphasis on indications, preoperative assessment, and operative technical issues. King SC, Pollack LA, Li J, King JB, Master VA. Continued increase in incidence of renal cell carcinoma, especially in young patients and high grade disease: United States 2001 to 2010. J Urol. 2014;191(6):1665–70. Simard EP, Ward EM, Siegel R, Jemal A. Cancers with increasing incidence trends in the United States: 1999 through 2008. CA Cancer J Clin. 2012;62(2):118–28. Ginzburg S, Uzzo RG, Kutikov A. The role of minimally invasive surgery in multifocal renal cell carcinoma. Curr Urol Rep. 2012;13(3):202–10. Alasker A, Williams SK, Ghavamian R. Small renal mass: to treat or not to treat. Curr Urol Rep. 2013;14(1):13–8. This paper is an update review of the treatment of SRMs. Karam JA, Wood CG. Management of small renal masses: watch, cut, freeze, or fry? Eur Urol. 2012;61(5):905–6.
16.
17.•
18.
19.
20. 21.
22.
23.
24.
Pansadoro A, Cochetti G, D’amico F, Barillaro F, Del Zingaro M, Mearini E. Retroperitoneal laparoscopic renal tumour enucleation with local hypotension on demand. World J Urol. 2015;33(3):427–32. Campbell SC, Novick AC, Belldegrun A, Blute ML, Chow GK, Derweesh IH, et al. Guideline for management of the clinical T1 renal mass. J Urol. 2009;182(4):1271–9. Scosyrev E, Messing EM, Sylvester R, Campbell S, Van Poppel H. Renal function after nephron-sparing surgery versus radical nephrectomy: results from EORTC randomized trial 30904. Eur Urol. 2014;65(2):372–7. This paper reported the results of EORTC 30904: an important international randomized trial. It had the objective to examine the impact of NSS on kidney function, in relation to RN. Minervini A, Ficarra V, Rocco F, Antonelli A, Bertini R, Carmignani G, et al. Simple enucleation is equivalent to traditional partial nephrectomy for renal cell carcinoma: results of a nonrandomized, retrospective, comparative study. J Urol. 2011;185(5):1604–10. The authors present the first multicenter results in 537 patients, who had undergone simple enucleation for localized renal cell carcinoma at 16 academic centers. Bratslavsky G, Linehan WM. Long-term management of bilateral, multifocal, recurrent renal carcinoma. Nat Rev Urol. 2010;7(5): 267–75. Minervini A, Tuccio A, Masieri L, Veneziano D, Vittori G, Siena G, et al. Endoscopic robot-assisted simple enucleation (ERASE) for clinical T1 renal masses: description of the technique and early postoperative results. Surg Endosc. 2015;29(5):1241–9. It is an uncommon study that compared the results of robotic-assisted simple enucleation with pure laparoscopic simple enucleation. Minervini A, di Cristofano C, Lapini A, Marchi M, Lanzi F, Giubilei G, et al. Histopathologic analysis of peritumoral pseudocapsule and surgical margin status after tumor enucleation for renal cell carcinoma. Eur Urol. 2009;55(6):1410–8. Minervini A, Vittori G, Salvi M, Sebastianelli A, Tuccio A, Siena G, et al. Analysis of surgical complications of renal tumor enucleation with standardized instruments and external validation of PADUA classification. Ann Surg Oncol. 2013;20(5):1729–36. Laryngakis NA, Guzzo TJ. Tumor enucleation for small renal masses. Curr Opin Urol. 2012;22(5):365–71. It is a good review of tumor enucleation as an alternative for renal masses in specific cases. Leslie S, Goh AC, Gill IS. Partial nephrectomy-contemporary indications, techniques and outcomes. Nat Rev Urol. 2013;10(5):275– 83. Mir MC, Campbell RA, Sharma N, Remer EM, Simmons MN, Li J, et al. Parenchymal volume preservation and ischemia during partial nephrectomy: functional and volumetric analysis. Urology. 2013;82(2):263–8. Van Poppel H, Becker F, Cadeddu JA, et al. Treatment of localised renal cell carcinoma. Eur Urol. 2011;60:662–72. Thompson RH, Lane BR, Lohse CM, Leibovich BC, Fergany A, Frank I, et al. Every minute counts when the renal hilum is clamped during partial nephrectomy. Eur Urol. 2010;58(3):340–5. Ficarra V, Galfano A, Cavalleri S. Is simple enucleation a minimal partial nephrectomy responding to the EAU guidelines’ recommendations? Eur Urol. 2009;55(6):1315–8. Lane BR, Russo P, Uzzo RG, Hernandez AV, Boorjian SA, Thompson RH, et al. Comparison of cold and warm ischemia during partial nephrectomy in 660 solitary kidneys reveals predominant role of nonmodifiable factors in determining ultimate renal function. J Urol. 2011;185(2):421–7. Minervini A, Serni S, Tuccio A, Raspollini MR, Di Cristofano C, Siena G, et al. Local recurrence after tumour enucleation for renal cell carcinoma with no ablation of the tumour bed: results of a prospective single-centre study. BJU Int. 2011;107(9):1394–9.
Curr Urol Rep (2016) 17:7 25.
26.
27.
28.
29.
30.
31.
32.
33.
34.•
35.
36.
37.
38.
39.
40.
41. 42.
43.•
Marszalek M, Carini M, Chlosta P, Jeschke K, Kirkali Z, Knüchel R, et al. Positive surgical margins after nephron-sparing surgery. Eur Urol. 2012;61(4):757–63. Ljungberg B, Cowan NC, Hanbury DC, et al. European Association of Urology Guideline Group. EAU guidelines on renal cell carcinoma: the 2010 update. Eur Urol. 2010;58:398–406. Lifshitz DA, Shikanov SA, Deklaj T, et al. Laparoscopic partial nephrectomy: a single-center evolving experience. Urology. 2010;75:282–7. Laryngakis NA, Van Arsdalen KN, Guzzo TJ, Malkowicz SB. Tumor enucleation: a safe treatment alternative for renal cell carcinoma. Expert Rev Anticancer Ther. 2011;11(6):893–9. Minervini A, Rosaria Raspollini M, Tuccio A, Di Cristofano C, Siena G, Salvi M, et al. Pathological characteristics and prognostic effect of peritumoral capsule penetration in renal cell carcinoma after tumor enucleation. Urol Oncol. 2014;32(1):50. Liatsikos E, Kallidonis P, Do M, Dietel A, Al-Aown A, Constantinidis C, et al. Laparoscopic radical and partial nephrectomy: technical issues and outcome. World J Urol. 2013;31(4):785– 91. Minervini A, Tuccio A, Lapini A, Lanzi F, Vittori G, Siena G. Review of the current status of tumor enucleation for renal cell carcinoma. Arch Ital Urol Androl. 2009;81(2):65–71. Cheng X, He J, Gan W, Fan X, Yang J, Zhu B, et al. Pseudocapsule of renal cell carcinoma associated with Xp11.2 translocation/TFE3 gene fusion: a clue for tumor enucleation? Int J Clin Exp Pathol. 2015;8(5):5403–10. Jacob JM, Williamson SR, Gondim DD, Leese JA, Terry C, Grignon DJ et al. Characteristics of the peritumoral pseudocapsule vary predictably with histologic subtype of t1 renal neoplasms. Urology. 2015. Serni S, Vittori G, Frizzi J, Mari A, Siena G, Lapini A, et al. Simple enucleation for the treatment of highly complex renal tumors: perioperative, functional and oncological results. Eur J Surg Oncol. 2015;41(7):934–40. It is an interesting paper about simple enucleation as treatment for highly-complex renal tumors. Talarico F, Buli P, Iusco D, Sangiorgi A. Synchronous right nephrectomy, left kidney tumorectomy, right lateral hepatic sectorectomy and inferior vena cava thrombectomy for metastastic clear cell renal carcinoma. Report of a case and review of the literature. Ann Ital Chir. 2013;84(2):209–12. Cienfuegos-Belmonte I, León-Dueñas E, Pérez-Valdivia MA, Medina-López RA. Conservative treatment of de novo renal carcinoma on kidney graft. Actas Urol Esp. 2015. Cortés-González JR, Arratia-Maqueo JA, Ortiz-Lara GE, Escobedo M, Gutiérrez-González A. Extracorporeal tumorectomy and autotransplantation in a patient with a single kidney and a multicentric clear cell carcinoma. Arch Esp Urol. 2008;61(5): 621–3. Kutikov A, Uzzo RG. The R.E.N.A.L. nephrometry score: a comprehensive standardized system for quantitating renal tumor size, location and depth. J Urol. 2009;182(3):844–53. Engel JD, Williams SB. Unclamped hand-assisted laparoscopic partial nephrectomy for predominantly endophytic renal tumors. Urol J. 2013;10(1):767–73. Crisan N, Ivan C, Gherman V, Neiculescu C, Coman I. Tumor enucleation with zero ischemia for renal cell carcinoma by robotic retroperitoneal approach. Urol J. 2014;11(3):1721–3. Gill IS, Kamoi K, Aron M, Desai MM. 800 Laparoscopic partial nephrectomies: a single surgeon series. J Urol. 2010;183(1):34–41. Ng CK, Gill IS, Patil MB, Hung AJ, Berger AK, de Castro Abreu AL, et al. Anatomic renal artery branch microdissection to facilitate zero-ischemia partial nephrectomy. Eur Urol. 2012;61(1):67–74. Lista G, Buffi NM, Lughezzani G, Lazzeri M, Abrate A, Mistretta A, et al. Margin, ischemia, and complications system to report
Page 7 of 7 7 perioperative outcomes of robotic partial nephrectomy: a European Multicenter Observational Study (EMOS project). Urology. 2015;85(3):589–95. It is a multicenter study in patients who underwent robot assisted partial nephrectomy for cT1 renal tumors; it analyzes three important issues of this technique: margin, ischemia and complications. 44. Polascik TJ, Meng MV, Epstein JI, Marshall FF. Intraoperative sonography for the evaluation and management of renal tumors: experience with 100 patients. J Urol. 1995;154(5):1676–80. 45. Tobis S, Knopf J, Silvers C, Yao J, Rashid H, Wu G, et al. Near infrared fluorescence imaging with robotic assisted laparoscopic partial nephrectomy: 46. Teber D, Guven S, Simpfendörfer T, Baumhauer M, Güven EO, Yencilek F, et al. Augmented reality: a new tool to improve surgical accuracy during laparoscopic partial nephrectomy? Preliminary in vitro and in vivo results. Eur Urol. 2009;56(2):332–8. 47. Hagemann IS, Lewis Jr JS. A retrospective comparison of 2 methods of intraoperative margin evaluation during partial nephrectomy. J Urol. 2009;181(2):500–5. 48. Sundaram V, Figenshau RS, Roytman TM, Kibel AS, Grubb 3rd RL, Bullock A, et al. Positive margin during partial nephrectomy: does cancer remain in the renal remnant? Urology. 2011;77(6): 1400–3. 49. Ramanathan R, Leveillee RJ. A review of methods for hemostasis and renorrhaphy after laparoscopic and robot-assisted laparoscopic partial nephrectomy. Curr Urol Rep. 2010;11(3):208–20. 50. Floridi C, De Bernardi I, Fontana F, Muollo A, Ierardi AM, Agostini A, et al. Microwave ablation of renal tumors: state of the art and development trends. Radiol Med. 2014;119(7):533–40. 51. Xu L, Yang R, Wang W, Zhang Y, Gan W. Laparoscopic radiofrequency ablation-assisted enucleation of Xp11.2 translocation renal cell carcinoma: a case report. Oncol Lett. 2014;8(3):1237–9. 52. Hughes-Hallett A, Patki P, Patel N, Barber NJ, Sullivan M, Thilagarajah R. Robot-assisted partial nephrectomy: a comparison of the transperitoneal and retroperitoneal approaches. J Endourol. 2013;27(7):869–74. 53. Lane BR, Gill IS. 7-year oncological outcomes after laparoscopic and open partial nephrectomy. J Urol. 2010;183(2):473–9. 54.•• Van Poppel H, Da Pozzo L, Albrecht W, Matveev V, Bono A, Borkowski A, et al. A prospective, randomised EORTC intergroup phase 3 study comparing the oncologic outcome of elective nephron-sparing surgery and radical nephrectomy for low-stage renal cell carcinoma. Eur Urol. 2011;59(4):543–52. This paper presents interesting overall survival results in a randomized trial that compared NSS and RN. 55.• Minervini A, Serni S, Tuccio A, Siena G, Vittori G, Masieri L, et al. Simple enucleation versus radical nephrectomy in the treatment of pT1a and pT1b renal cell carcinoma. Ann Surg Oncol. 2012;19(2): 694–700. It is a paper in which oncologic outcomes are compared between TE and RN in pT1 RCCs; even when its retrospective methodological design is a limitation. 56. Raz O, Mendlovic S, Shilo Y, Leibovici D, Sandbank J, Lindner A, et al. Positive surgical margins with renal cell carcinoma have a limited influence on long-term oncological outcomes of nephron sparing surgery. Urology. 2010;75(2):277–80. 57. Minervini A, Vittori G, Lapini A, Tuccio A, Siena G, Serni S, et al. Morbidity of tumour enucleation for renal cell carcinoma (RCC): results of a single-centre prospective study. BJU Int. 2012;109(3): 372–7. 58. Mukkamala A, Allam CL, Ellison JS, Hafez KS, Miller DC, Montgomery JS, et al. Tumor enucleation vs sharp excision in minimally invasive partial nephrectomy: technical benefit without impact on functional or oncologic outcomes. Urology. 2014;83(6): 1294–9.
