Surg Endosc DOI 10.1007/s00464-015-4382-8
and Other Interventional Techniques
Laparoscopic partial nephrectomy without intracorporeal suturing Ching-Chia Li1,2,3,4 • Hsin-Chih Yeh1,2,3,4 • Hsiang-Ying Lee1,2 • Wei-Ming Li1,3,4 • Hung-Lung Ke1,3,4 • Allen Herng Shouh Hsu1,2 • Mei Hui Lee1 • Chia-Chun Tsai1,2 • Kuang-Shun Chueh1,2 • Chun-Nung Huang1,4 • Yii-Her Chou1,4 • Chien-Feng Li4,5,6 • Wen-Jeng Wu1,4,7
Received: 28 May 2015 / Accepted: 26 June 2015 Ó Springer Science+Business Media New York 2015
Abstract Background Partial nephrectomy has gained wider acceptance as a surgical technique in treating small renal tumors. Laparoscopic partial nephrectomy (LPN) still remains a technically demanding surgery to this day. We present our technique of laparoscopic partial nephrectomy, one that is performed without intracorporeal suturing. Methods We performed LPN on 31 patients with localized renal parenchymal tumor (stage T1). The procedures were done from September 2009 to March 2015 at the Kaohsiung Medical University Hospital and the Kaohsiung Municipal Ta-Tung Hospital. Our technique involves the covering of renal defect layer by layer with FloSeal, Tisseel and a fat pad after monopolar coagulation. Results Thirty-one patients were included in this study. Mean patient age was 53 years old (range 39–70). Mean
& Wen-Jeng Wu [email protected] 1
Department of Urology, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
2
Department of Urology, Kaohsiung Municipal Ta-Tung Hospital, Kaohsiung, Taiwan
3
Graduate Institute of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
4
Department of Urology, Faculty of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
5
Department of Pathology, Chi Mei Foundation Medical Center, Tainan, Taiwan
6
Department of Biotechnology, Southern Taiwan University of Science and Technology, Tainan, Taiwan
7
Department of Urology, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
tumor size was 2.9 cm (range 1.8–6.3). Mean RENAL nephrometry score was 5.3 (range 4–7). The average operation time was 188 min (range 120–290), and the average warm ischemic time was 19.0 min (range 9–26). Mean estimated blood loss was 171 ml (range 10–650), with no postoperative bleeding among the total 31 patients. No recurrent tumors were identified at a mean follow-up of 29 months postoperatively. The mean change in eGFR was 6.5 (ml/min/m2). Conclusion Laparoscopic partial nephrectomy is a feasible surgical method for most patients with stage 1 tumor. Our technique has shown to reduce warm ischemic time significantly and provide patients with excellent functional outcomes without affecting oncological results. With this technique, surgeons can perform LPN with more efficiency and with fewer complications. Keywords Partial nephrectomy LPN Suturing Ischemic time Tisseel
The incidence rate and mortality rate of renal cancer are currently increasing, with an expected 270,000 newly diagnosed cases and 110,000 deaths worldwide according to a 2008 GLOBOCAN estimation [1]. Many minimally invasive procedures have been adopted for the treatment of this disease, including cryotherapy, HIFU, radiofrequency and oral target therapy. To date, surgical excision still remains the only curative treatment and the optimal management for most patients with localized renal cancer. In the past, radical nephrectomy has been the standard management of renal cancer; partial nephrectomy was only performed on patients with chronic renal insufficiency or solitary kidney. In the last decade, the indication of partial nephrectomy has expanded to include patients with a tumor
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size smaller than 4 cm, regardless of the contralateral kidney function. Literatures have noted the excellent oncological outcomes of partial nephrectomy in comparison with radical nephrectomy [2, 3]. The first laparoscopic renal surgeries performed by Clayman [4] in 1991 have included partial nephrectomy [5, 6]. Laparoscopic partial nephrectomy (LPN) is a technically demanding surgery even when performed under robot assistance. Some challenges met during this procedure include: preventing perioperative bleeding, achieving renal hypothermia after renal artery clamping, reducing warm ischemic time and accomplishing laparoscopic intracorporeal suturing. Although renal hypothermia can be achieved by injecting cold saline into the renal pelvis, the cooling effect is not optimal. Gill et al. [7] reported a novel method of placing ice slush around the kidney; however, this cooling method was not easily replicated during laparoscopic surgery. With the difficulty of achieving renal hypothermia while performing a LPN, it is therefore crucial to reduce warm ischemic time. Huang et al. [8] highlighted the issue of renal function preservation by minimizing warm ischemic time in patients undergoing PN. A traditional LPN has a significant warm ischemic time partly due to the suturing process. In this study, we present our technique of laparoscopic partial nephrectomy performed without intracorporeal suturing. Our method has shown to reduce warm ischemic time and has alleviated some common challenges of LPN.
Materials and methods We performed LPN on 31 patients with localized renal parenchymal tumor (stage T1N0M0). The procedures were done from September 2009 to March 2015 at the Kaohsiung Medical University Hospital and Kaohsiung Municipal Ta-Tung Hospital. All patients were informed of the potential complications and risks of this surgery. Patients with suspected lymph node(s) or distal metastasis before the operation were excluded from this study. Patients with endophytic tumor and tumor locating less than 4 mm from the collecting system were also excluded from this study. In total, 31 patients underwent LPN without intracorporeal suturing. Transperitoneal approach was performed for 12 patients with tumor located at the anterior aspect of the kidney, while retroperitoneal approach was performed for the other 19 patients with tumor located at the lateral or posterior aspect of the kidney. In regard to hilar control, nine patients did not undergo renal pedicle clamping due to relatively small tumor sizes or had tumors of exophytic locations. We used endo-Satinsky or bulldog clamps to occlude the renal artery in the remaining 22 patients. The decision to renal
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pedicle clamping was made by surgeons based on preoperative imaging and intraoperative findings. No renal cooling procedure was carried out throughout the study.
Technique The basic laparoscopic surgical method has been described in our previous article [9]. Patients were placed in flank position for the retroperitoneal approach with the lesion side up. The transperitoneal approach required patients to be in a modified flank position (table flexion of 45°). We used the multiple instrument access port—LagiPort (Lagis, Taiwan)—for the laparoendoscopic single-site partial nephrectomy. After entering the retroperitoneal cavity, we identified the kidney, renal artery and primary tumor. Before the tumor was excised, we obtained a fat pad from the peri-renal space (Fig. 1). The origin of the fat pad should be located as far away as possible from tumor. In surgical candidates with renal artery non-clamping, tumor excision was performed slowly with a harmonic scalpel leaving a 0.5- to 1-cm safety margin. In renal artery clamping via endo-Satinsky or bulldog clamps, tumor excision was performed with laparoscopic scissors, keeping in mind of the warm ischemic nature of artery clamping. Excisions causing vascular disruptions were extensively fulgurated. If any disruptions in the collecting system were identified, the cross section of renal calyx or pelvis was sealed off by monopolar coagulation via laparoscopic scissors. A hemostatic matrix—FloSeal (Baxter, Zurich, Switzerland)—was placed into the space antecedently (Fig. 2B), and a fibrin sealant—Tisseel (Baxter, Zurich, Switzerland)—was injected to cover the entire hemostatic matrix and the surrounding normal renal tissue (Fig. 2C). Finally, the fat pad previously prepared was placed over the areas coated with the fibrin sealant. The process of placing fat pad should be completed in less than 20 s, as fibrin sealant has a short solidifying time. Accomplishing the
Fig. 1 Obtain a fat pad from perirenal space
Surg Endosc
Drainage tube was placed in 28 of the 31 patients; the three patients without drainage tube had characteristics of small exophytic renal tumor.
Results
Fig. 2 A A defect after tumor was excised. B FloSeal was placed into the defect of kidney. C Tisseel was injected to cover whole the hemostatic matrix and surrounding normal renal surface. D Fat pad was then placed on the top of the field covered with Tisseel. FloSeal swell in the airtight space, like a ‘‘pressure cooker’’
aforementioned steps, this fat pad will adhere to the periphery of our incision field (Fig. 3) and hemostatic matrix will be closed off underneath. Hemostatic matrix is a combination of gelatin matrix and thrombin component where its volume will increase approximately 20 % upon contacting blood or urine. This chemical reaction will begin soon after the endo-Satinsky or bulldog clamps have been removed from the renal artery. Being sealed off by fat pad, the hemostatic matrix engorges within the airtight space acting like a ‘‘pressure cooker’’ (Fig. 2D), providing extra external pressure for the prevention of postoperative bleeding. The tumor specimen was removed through one extended port using the laparoscopic sac in the traditional laparoscopic procedure. Specimen was withdrawn directly via laparoscopic grasper in the laparoendoscopic single-site procedure.
Fig. 3 Fat pad stick together on the periphery of our incision field
All 31 patients underwent the surgical procedure with complete success, and none required a conversion to an open surgery. Mean patient age was 53 years (range 39–70), and the male-to-female ratio was 1.6–1. Mean BMI was 25.2 (range 20.3–35.9). Mean tumor size was 2.9 cm (range 1.8–6.3). Mean RENAL nephrometry score was 5.3 (range 4–7) (Table 1). Perioperative and pathological data are given in Table 2. The retroperitoneal approach was performed in 20 patients, where the tumor was located at the posterior and lateral aspect of kidney. The transperitoneal approach was performed only in patients with tumor located at the anterior aspect of kidney. For the latter 1 year during the surgical procedures performed in this study, we began the use of the laparoendoscopic single-site (LESS) partial nephrectomy technique. This study includes six patients that underwent the LESS surgery; these patients received the retroperitoneal approach. In regard to the renal pedicle control during tumor excision, renal artery non-clamping was performed in 11 patients that had tumors of relatively smaller size or of exophytic characteristics. In the total 31 surgeries, the average operation time was 188 min (range 120–290). The average warm ischemic time was 19.0 min (range 9–26). Mean estimated blood loss was 171 ml (range 10–650), and average hospital stay was 6.2 days (range 3–13). There were eight patients whom encountered collecting system disruption during tumor excision while only one patient needed blood transfusion. Overall, postoperative complications occurred in two patients (6.5 %), including one patient with post-operation lung infection needing extended antibiotics treatment (Clavien grade 2) and one patient with urine leakage managed by conservative treatment (Clavien grade 1). The final histopathology confirmed the diagnosis of renal cell carcinoma in 21 patients, oncocytoma in 4, angiomyolipoma in 4, metanephric adenoma in 1 and infected cyst in one patient. Stage pT1a was given in 19 patients and stage pT1b in the remaining two patients. One patient with positive surgical margin in this study received close follow-up by ultrasound and CT scan. Neither residual nor recurrent tumors were identified by image studies after a 25-month follow-up time frame. Among all 31 patients, neither recurrent nor metastatic tumor was identified at a mean follow-up of 29 months postoperatively. The mean change of eGFR was decreased by 6.5 (ml/min/m2).
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Surg Endosc Table 1 Patient characteristics
Overall population (n = 31) Gender Male
19
Female
12
Age (years), mean (range)
53 (39–70)
BMI (kg/m2), mean (range)
25.2 (20.3–35.9)
ASA classification ASA I
12
ASA II
17
ASA III
2
Tumor side Right
18
Left
2.9 (1.8–6.3)
RENAL nephrometry score, mean (range)
5.3 (4–7)
Discussion Previous literature has shown that partial nephrectomy is equivalent to radical nephrectomy in terms of long-term outcome in patients with malignant tumors less than 4 cm [2, 3]. Partial nephrectomy is a procedure that has gained wider acceptance in the recent decades. Since LPN was first performed in 1993 [5], it has become the most popular procedure for treating small renal tumor because of its minimally invasive advantages. However, laparoscopic partial nephrectomy is a technically more demanding surgery than laparoscopic nephrectomy. During a traditional open partial nephrectomy which involves renal pedicle clamping and suturing post-tumor excision, renal hypothermia can be easily achieved by instilling ice slush around the kidney and bleeding can be controlled under a larger field of operation. Under a laparoscopic setting, such challenges are more difficult to overcome. In LPN intracorporeal suturing, operation time is further extended even under robot assistance, a step which prolongs warm ischemic time. Some authors proposed that deep medullary suture may cause partial devascularization of the remaining renal parenchyma, affecting renal preservation [10]. However, the application of hemostatic matrix and fibrin sealant has shown to allow us to perform LPN without renal artery clamping and without intracorporeal suturing. FloSeal is a hemostatic agent composed of a gelatin matrix and human thrombin. The efficacy of hemostasis had been confirmed during partial nephrectomy in previous literatures [11–13]. Tisseel, a fibrin sealant, has also been used for partial nephrectomy; however, the effect of such products in the sealing of the collecting system remains controversial [13, 14]. Recently, Ploussard et al. [15] reported that the combination of FloSeal and Tisseel has shown in their study to safely control parenchymal
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13
Tumor size (cm), mean (range)
bleeding and replace the conventional suture without compromising operative outcomes during LPN on a swine experimental surgery. According to the experiences of reviewed authors, we modified their methods to develop a technique of performing LPN with ease and with satisfactory results. At our institution, we started laparoscopic radical nephrectomy in 2000 and began the laparoscopic partial nephrectomy program in 2003. Our experience with LESS partial nephrectomy began in 2013. In recent years, we evaluated our evolution from traditional partial nephrectomy to LESS partial nephrectomy using this technique to minimize wound length without compromising surgical outcomes. In this study, we included only six patients that received LESS partial nephrectomy; the initial results are encouraging. We plan to report on detailed surgical outcome of LESS partial nephrectomy in the future. LPN can be carried out either via the transperitoneal route or via the retroperitoneal route. To date, there is no significant evidence showing the optimal technique for LPN. Previous literature has shown that retroperitoneoscopy is associated with more complications and conversions compared to traditional laparoscopy [16, 17]. In this study, we show no difference in conversion and complication rates between the two techniques. Two postoperative complications occurred in this study: One patient that received the transperitoneal approach suffered from postoperative pneumonia. She was the oldest patient in the patient population and was able to make a full recovery after receiving 1 week of antibiotics treatment. Another patient that received the retroperitoneal approach suffered from persistent urine leakage for 6 days post-operation. This patient was noted to have had the largest collecting system disruption compared to all other patients (approximately 1 cm in length). This defect had been
Surg Endosc Table 2 Perioperative parameters
No = 31 Approach Transperitoneal
11 (35 %)
Retroperitoneal
20 (65 %)
Method Traditional laparoscopy
25 (81 %)
Laparoendoscopic single-site (LESS)
6 (19 %)
Renal artery control Clamped
20 (65 %)
Non-clamped
11 (35 %)
Warm ischemic time (minute), mean (range)
19.0 (9–26)
Operation time (minute), mean (range)
188 (120–290)
Blood loss (ml), mean (range)
171 (10–650)
Hospital stay (day), mean (range)
6.2 (3–13)
Blood transfusion Yes No
1 (3.2 %) 30 (96.8 %)
Histology RCC
21 (67.7 %)
Oncocytoma
4 (12.9 %)
AML
4 (12.9 %)
Metanephric adenoma
1 (3.2 %)
Infected cyst
1 (3.2 %)
Stage of RCC PT1a
19 (90.5 %)
PT1b
2 (9.5 %)
Complications Pneumonia
1 (3.2 %)
Prolong urine leakage
1 (3.2 %)
Positive margin Yes
1 (3.2 %)
No Cancer recurrence
30 (96.8 %)
Yes
0 (0 %)
No
21 (100 %)
Duration of follow-up (month), mean (range)
29 (3–70)
Change of eGFR (ml/min/m2), mean (range)
-6.5 (-26.3 to ?15.1)
initially sealed off by cauterization and covered by FloSeal, Tisseel and fat pad layer by layer consecutively. Persistent urine leakage (about 200–400 ml/day) from the JacksonPratt drainage tube was noted for 6 days but was spontaneously resolved 1 week after the surgery without additional management. We noticed that collecting system disruption occurred in 8 of the 31 patients. One patient as mentioned above had massive urine leakage; two patients had minor urine leakage (less than 100 ml/day) for 3 days postoperatively. There was no urine leakage noted in the other five patients. Our results are consistent with previous studies. L’Esperance et al. [11] also reported a high rate of
urine leakage when Tisseel was used for collecting duct repair, regardless of the addition of FloSeal use. One novel technique we propose is using the Tisseel to bind a fat pad to the outer layer. The fat pad encapsulated the FloSeal within the tumor-excised cavity, supplementing structural support of the expanding and swelling action of FloSeal after it interacts with blood or urine from within. The space within the fat pad acts in theory like a ‘‘pressure cooker,’’ providing an extra external pressure in preventing postoperative bleeding. We did not perform any renal parenchymal suturing after tumor excision, and none of our patients suffered from postoperative bleeding. Although urine
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leakage occurred in three patients, only conservative management was required. Aboumarzouk et al. [18] and Zhang et al. [19] conducted systematic reviews on the outcomes of robotic and LPN; they concluded that the robotic approach had significantly shorter warm ischemic time [18, 19]. Warm ischemic time is the major factor for renal function preservation after LPN. Our technique facilitates shorter renal defect repair time and therefore reduces the ischemic time. The results of this study show that our procedure is an excellent alternative to LPN specifically in patients with stage 1 renal tumors. We show a significantly shorter warm ischemic time, lower risk of postoperative bleeding and high feasibility for surgeons. Operative time in this study was longer compared to other study groups due to the inclusion of LESS procedure and also due to some lessexperienced surgeons that performed the LPN. If we exclude patients whom were operated by less-experienced surgeons as well as those that received the LESS surgery, the mean warm ischemic time would be 16 min. For patients that underwent the LESS method, the warm ischemic time was nevertheless convincing. The mean warm ischemic time of the six patients was 23 min (range 19–27). Shorter warm ischemic time in our study was significantly compared to that of other studies where LPN was performed under robot assistance [20–22]. We believe that this technique should be adopted in LESS partial nephrectomy to improve not only the warm ischemic time but also the learning curve of surgeons. This technique will shorten the learning curve in accomplishing LPN, robotic PN or LESS PN for urologists who lack the experience of intracorporeal suturing. We also believed that this technique is suitable for other surgeries in the field of hepatobiliary surgery, for example, using the omentum as an adhesive encapsulation for liver surface after tumor excision. There are still some limitations to this design. We used a relatively small cohort group, and we did not have a prospective randomized controlled group. Most patients included in this study had characteristics of exophytic tumor. The efficacy of this technique for patients with endophytic tumor still needs to be explored.
Conclusion Although LPN is a challenging procedure, we have shown that our LPN technique reduces the warm ischemic time significantly and provides excellent functional outcomes. This method allows surgeons to perform LPN more easily and more effectively with fewer complications. In our initial experience, suturing was not necessary during collecting system disruption of less than 1 cm in length.
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We are currently continuing long-term follow-up and documentation of associated outcomes in order to confirm the long-term efficacy of this surgical management. Acknowledgments This study was supported by a grant from Health and welfare surcharge of tobacco products, Ministry of Health and Welfare (MOHW104-TDU-B-212-124-003); Kaohsiung Medical University Hospital (KMUH103-3R46); Ministry of Science and Technology (MOST 103-2320-B-037-010). Compliance with Ethical Standards Disclosures Ching-Chia Li, Hsin-Chih Yeh, Hsiang-Ying Lee, WeiMing Li, Hung-Lung Ke, Allen Herng Shouh Hsu, Mei Hui Lee, Chia-Chun Tsai, Kuang-Shun Chueh, Chun-Nung Huang, Yii-Her Chou, Chien-Feng Li and Wen-Jeng Wu declare they have no conflict of interest. Ethical standard This study was approved by the appropriate institutional review board at Kaohsiung Medical University Hospital (KMUH-IRB-20130082) and performed according to the ethical standards laid down by the 1964 Declaration of Helsinki.
References 1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917 2. Van Poppel H, Becker F, Cadeddu JA, Gill IS, Janetschek G, Jewett MA, Laguna MP, Marberger M, Montorsi F, Polascik TJ, Okimura O, Zhu G (2011) Treatment of localised renal cell carcinoma. Eur Urol 60(4):662–672 3. Antonelli A, Ficarra V, Bertini R, Carini M, Carmignani G, Corti S, Longo N, Martorana G, Minervini A, Mirone V, Novara G, Serni S, Simeone C, Simonato A, Siracusano S, Volpe A, Zattoni F, Cunico SC (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):1013–1018 4. Clayman RV, Kavoussi LR, Soper NJ, Dierks SM, Meretyk S, Darcy MD, Roemer FD, Pingleton ED, Thomson PG, Long SR (1991) Laparoscopic nephrectomy: initial case report. J Urol 146(2):278–282 5. Winfield HN, Donovan JF, Lund GO, Kreder KJ, Stanley KE, Brown BP, Loening SA, Clayman RV (1995) Laparoscopic partial nephrectomy: initial experience and comparison to the open surgical approach. J Urol 153(5):1409–1414 6. McDougall EM, Elbahnsay AM, Clayman RV (1998) Laparoscopic wedge resection and partial nephrectomy: the Washington University experience and review of the literature. J Soc Laparoendosc Surg 2(1):15–23 7. Gill IS, Abreu SC, Desai MM, Steinberg AP, Ramani AP, Ng C, Banks K, Novick AC, Kaouk JH (2003) Laparoscopic ice slush renal hypothermia for partial nephrectomy: the initial experience. J Urol 170(1):52–56 8. Huang WC, Levey AS, Serio AM, Snyder M, Vickers AJ, Raj GV, Scardino PT, Russo P (2006) Chronic kidney disease after nephrectomy in patients with renal cortical tumours: a retrospective cohort study. Lancet Oncol 7(9):735–740 9. Li CC, Chou YH, Wu WJ, Shih MC, Juan YS, Shen JT, Liu CC, Huang SP, Huang CH (2007) Laparoscopic partial nephrectomy: the effect of preoperative tumor embolization. Kaohsiung J Med Sci 23(12):624–630
Surg Endosc 10. L’Esperance JO, Marguet CG, Walters RC, Sung JC, Auge BK, Stroup SP, L’esperance AH, Albala DM (2010) Do nonspecific deep corticomedullary sutures performed during partial nephrectomy adequately control major vascular and collecting system injury? BJU Int 105(3):411–415 11. L’Esperance JO, Sung JC, Marguet CG, Maloney ME, Springhart WP, Preminger GM, Albala DM (2005) Controlled survival study of the effects of Tisseel or a combination of FloSeal and Tisseel on major vascular injury and major collecting-system injury during partial nephrectomy in a porcine model. J Endourol 19(9):1114–1121 12. User HM, Nadler RB (2003) Applications of FloSeal in nephronsparing surgery. Urology 62(2):342–343 13. Rouach Y, Delongchamps NB, Patey N, Fontaine E, Timsit MO, Thiounn N, Me´jean A (2009) Suture or hemostatic agent during laparoscopic partial nephrectomy? A randomized study using a hypertensive porcine model. Urology 73(1):172–177 14. Pick DL, Kolla SB, Mucksavage P, Louie MK, Sountoulides P, Kaufmann O, Olamendi S, Kaplan A, Huynh V, Ortiz-Vanderdys C, Truong HP, Said SA, Andrade L, Tongson-Ignacio J, McDougall EM, Clayman RV (2011) Sprayed fibrin sealant as the sole hemostatic agent for porcine laparoscopic partial nephrectomy. J Urol 185(1):291–297 15. Ploussard G, Haddad R, Loutochin O, Bera R, Cabrera T, Malibari N, Scarlata E, Derbekyan V, Bladou F, Anidjar M (2015) A combination of hemostatic agents may safely replace deep medullary suture during laparoscopic partial nephrectomy in a pig model. J Urol 193(1):318–324 16. El Ghoneimi A, Farhat W, Bolduc S, Bagli D, Mclorie G, Khoury A (2003) Retroperitoneal laparoscopic vs open partial nephroureterectomy in children. BJU Int 91(6):532–535
17. Le Clair MD, Vidal I, Suply E, Podevin G, Heloury Y (2009) Retroperitoneal laparoscopic heminephrectomy in duplex kidney in infants and children: a 15-year experience. Eur Urol 56(2):385–389 18. Aboumarzouk OM, Stein RJ, Eyraud R, Haber GP, Chlosta PL, Somani BK, Kaouk JH (2012) Robotic versus laparoscopic partial nephrectomy: a systematic review and meta analysis. Eur Urol 62(6):1023–1033 19. Zhang X, Shen Z, Zhong S, Zhu Z, Wang X, Xu T (2013) Comparison of perioperative outcomes of robot-assisted vs laparoscopic partial nephrectomy: a meta-analysis. BJU Int 112(8):1133–1142 20. Wu Z, Li M, Song S, Ye H, Yang Q, Liu B, Cai C, Yang B, Xiao L, Chen Q, Lu¨ C, Gao X, Xu C, Gao X, Hou J, Wang L, Sun Y (2014) Propensity-score matched analysis comparing robot-assisted with laparoscopic partial nephrectomy. BJU Int 115(3):437–445 21. Khalifeh A, Autorino R, Hillyer SP, Laydner H, Eyraud R, Panumatrassamee K, Long JA, Kouk JH (2013) Comparative outcomes and assessment of trifecta in 500 robotic and laparoscopic partial nephrectomy cases: a single surgeon experience. J Urol 189(4):1236–1242 22. Wang AJ, Bhayani SB (2009) Robotic partial nephrectomy versus laparoscopic partial nephrectomy for renal cell carcinoma: singlesurgeon analysis of [100 consecutive procedures. Urology 73(2):306–310
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and Other Interventional Techniques
Laparoscopic partial nephrectomy without intracorporeal suturing Ching-Chia Li1,2,3,4 • Hsin-Chih Yeh1,2,3,4 • Hsiang-Ying Lee1,2 • Wei-Ming Li1,3,4 • Hung-Lung Ke1,3,4 • Allen Herng Shouh Hsu1,2 • Mei Hui Lee1 • Chia-Chun Tsai1,2 • Kuang-Shun Chueh1,2 • Chun-Nung Huang1,4 • Yii-Her Chou1,4 • Chien-Feng Li4,5,6 • Wen-Jeng Wu1,4,7
Received: 28 May 2015 / Accepted: 26 June 2015 Ó Springer Science+Business Media New York 2015
Abstract Background Partial nephrectomy has gained wider acceptance as a surgical technique in treating small renal tumors. Laparoscopic partial nephrectomy (LPN) still remains a technically demanding surgery to this day. We present our technique of laparoscopic partial nephrectomy, one that is performed without intracorporeal suturing. Methods We performed LPN on 31 patients with localized renal parenchymal tumor (stage T1). The procedures were done from September 2009 to March 2015 at the Kaohsiung Medical University Hospital and the Kaohsiung Municipal Ta-Tung Hospital. Our technique involves the covering of renal defect layer by layer with FloSeal, Tisseel and a fat pad after monopolar coagulation. Results Thirty-one patients were included in this study. Mean patient age was 53 years old (range 39–70). Mean
& Wen-Jeng Wu [email protected] 1
Department of Urology, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
2
Department of Urology, Kaohsiung Municipal Ta-Tung Hospital, Kaohsiung, Taiwan
3
Graduate Institute of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
4
Department of Urology, Faculty of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
5
Department of Pathology, Chi Mei Foundation Medical Center, Tainan, Taiwan
6
Department of Biotechnology, Southern Taiwan University of Science and Technology, Tainan, Taiwan
7
Department of Urology, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
tumor size was 2.9 cm (range 1.8–6.3). Mean RENAL nephrometry score was 5.3 (range 4–7). The average operation time was 188 min (range 120–290), and the average warm ischemic time was 19.0 min (range 9–26). Mean estimated blood loss was 171 ml (range 10–650), with no postoperative bleeding among the total 31 patients. No recurrent tumors were identified at a mean follow-up of 29 months postoperatively. The mean change in eGFR was 6.5 (ml/min/m2). Conclusion Laparoscopic partial nephrectomy is a feasible surgical method for most patients with stage 1 tumor. Our technique has shown to reduce warm ischemic time significantly and provide patients with excellent functional outcomes without affecting oncological results. With this technique, surgeons can perform LPN with more efficiency and with fewer complications. Keywords Partial nephrectomy LPN Suturing Ischemic time Tisseel
The incidence rate and mortality rate of renal cancer are currently increasing, with an expected 270,000 newly diagnosed cases and 110,000 deaths worldwide according to a 2008 GLOBOCAN estimation [1]. Many minimally invasive procedures have been adopted for the treatment of this disease, including cryotherapy, HIFU, radiofrequency and oral target therapy. To date, surgical excision still remains the only curative treatment and the optimal management for most patients with localized renal cancer. In the past, radical nephrectomy has been the standard management of renal cancer; partial nephrectomy was only performed on patients with chronic renal insufficiency or solitary kidney. In the last decade, the indication of partial nephrectomy has expanded to include patients with a tumor
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size smaller than 4 cm, regardless of the contralateral kidney function. Literatures have noted the excellent oncological outcomes of partial nephrectomy in comparison with radical nephrectomy [2, 3]. The first laparoscopic renal surgeries performed by Clayman [4] in 1991 have included partial nephrectomy [5, 6]. Laparoscopic partial nephrectomy (LPN) is a technically demanding surgery even when performed under robot assistance. Some challenges met during this procedure include: preventing perioperative bleeding, achieving renal hypothermia after renal artery clamping, reducing warm ischemic time and accomplishing laparoscopic intracorporeal suturing. Although renal hypothermia can be achieved by injecting cold saline into the renal pelvis, the cooling effect is not optimal. Gill et al. [7] reported a novel method of placing ice slush around the kidney; however, this cooling method was not easily replicated during laparoscopic surgery. With the difficulty of achieving renal hypothermia while performing a LPN, it is therefore crucial to reduce warm ischemic time. Huang et al. [8] highlighted the issue of renal function preservation by minimizing warm ischemic time in patients undergoing PN. A traditional LPN has a significant warm ischemic time partly due to the suturing process. In this study, we present our technique of laparoscopic partial nephrectomy performed without intracorporeal suturing. Our method has shown to reduce warm ischemic time and has alleviated some common challenges of LPN.
Materials and methods We performed LPN on 31 patients with localized renal parenchymal tumor (stage T1N0M0). The procedures were done from September 2009 to March 2015 at the Kaohsiung Medical University Hospital and Kaohsiung Municipal Ta-Tung Hospital. All patients were informed of the potential complications and risks of this surgery. Patients with suspected lymph node(s) or distal metastasis before the operation were excluded from this study. Patients with endophytic tumor and tumor locating less than 4 mm from the collecting system were also excluded from this study. In total, 31 patients underwent LPN without intracorporeal suturing. Transperitoneal approach was performed for 12 patients with tumor located at the anterior aspect of the kidney, while retroperitoneal approach was performed for the other 19 patients with tumor located at the lateral or posterior aspect of the kidney. In regard to hilar control, nine patients did not undergo renal pedicle clamping due to relatively small tumor sizes or had tumors of exophytic locations. We used endo-Satinsky or bulldog clamps to occlude the renal artery in the remaining 22 patients. The decision to renal
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pedicle clamping was made by surgeons based on preoperative imaging and intraoperative findings. No renal cooling procedure was carried out throughout the study.
Technique The basic laparoscopic surgical method has been described in our previous article [9]. Patients were placed in flank position for the retroperitoneal approach with the lesion side up. The transperitoneal approach required patients to be in a modified flank position (table flexion of 45°). We used the multiple instrument access port—LagiPort (Lagis, Taiwan)—for the laparoendoscopic single-site partial nephrectomy. After entering the retroperitoneal cavity, we identified the kidney, renal artery and primary tumor. Before the tumor was excised, we obtained a fat pad from the peri-renal space (Fig. 1). The origin of the fat pad should be located as far away as possible from tumor. In surgical candidates with renal artery non-clamping, tumor excision was performed slowly with a harmonic scalpel leaving a 0.5- to 1-cm safety margin. In renal artery clamping via endo-Satinsky or bulldog clamps, tumor excision was performed with laparoscopic scissors, keeping in mind of the warm ischemic nature of artery clamping. Excisions causing vascular disruptions were extensively fulgurated. If any disruptions in the collecting system were identified, the cross section of renal calyx or pelvis was sealed off by monopolar coagulation via laparoscopic scissors. A hemostatic matrix—FloSeal (Baxter, Zurich, Switzerland)—was placed into the space antecedently (Fig. 2B), and a fibrin sealant—Tisseel (Baxter, Zurich, Switzerland)—was injected to cover the entire hemostatic matrix and the surrounding normal renal tissue (Fig. 2C). Finally, the fat pad previously prepared was placed over the areas coated with the fibrin sealant. The process of placing fat pad should be completed in less than 20 s, as fibrin sealant has a short solidifying time. Accomplishing the
Fig. 1 Obtain a fat pad from perirenal space
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Drainage tube was placed in 28 of the 31 patients; the three patients without drainage tube had characteristics of small exophytic renal tumor.
Results
Fig. 2 A A defect after tumor was excised. B FloSeal was placed into the defect of kidney. C Tisseel was injected to cover whole the hemostatic matrix and surrounding normal renal surface. D Fat pad was then placed on the top of the field covered with Tisseel. FloSeal swell in the airtight space, like a ‘‘pressure cooker’’
aforementioned steps, this fat pad will adhere to the periphery of our incision field (Fig. 3) and hemostatic matrix will be closed off underneath. Hemostatic matrix is a combination of gelatin matrix and thrombin component where its volume will increase approximately 20 % upon contacting blood or urine. This chemical reaction will begin soon after the endo-Satinsky or bulldog clamps have been removed from the renal artery. Being sealed off by fat pad, the hemostatic matrix engorges within the airtight space acting like a ‘‘pressure cooker’’ (Fig. 2D), providing extra external pressure for the prevention of postoperative bleeding. The tumor specimen was removed through one extended port using the laparoscopic sac in the traditional laparoscopic procedure. Specimen was withdrawn directly via laparoscopic grasper in the laparoendoscopic single-site procedure.
Fig. 3 Fat pad stick together on the periphery of our incision field
All 31 patients underwent the surgical procedure with complete success, and none required a conversion to an open surgery. Mean patient age was 53 years (range 39–70), and the male-to-female ratio was 1.6–1. Mean BMI was 25.2 (range 20.3–35.9). Mean tumor size was 2.9 cm (range 1.8–6.3). Mean RENAL nephrometry score was 5.3 (range 4–7) (Table 1). Perioperative and pathological data are given in Table 2. The retroperitoneal approach was performed in 20 patients, where the tumor was located at the posterior and lateral aspect of kidney. The transperitoneal approach was performed only in patients with tumor located at the anterior aspect of kidney. For the latter 1 year during the surgical procedures performed in this study, we began the use of the laparoendoscopic single-site (LESS) partial nephrectomy technique. This study includes six patients that underwent the LESS surgery; these patients received the retroperitoneal approach. In regard to the renal pedicle control during tumor excision, renal artery non-clamping was performed in 11 patients that had tumors of relatively smaller size or of exophytic characteristics. In the total 31 surgeries, the average operation time was 188 min (range 120–290). The average warm ischemic time was 19.0 min (range 9–26). Mean estimated blood loss was 171 ml (range 10–650), and average hospital stay was 6.2 days (range 3–13). There were eight patients whom encountered collecting system disruption during tumor excision while only one patient needed blood transfusion. Overall, postoperative complications occurred in two patients (6.5 %), including one patient with post-operation lung infection needing extended antibiotics treatment (Clavien grade 2) and one patient with urine leakage managed by conservative treatment (Clavien grade 1). The final histopathology confirmed the diagnosis of renal cell carcinoma in 21 patients, oncocytoma in 4, angiomyolipoma in 4, metanephric adenoma in 1 and infected cyst in one patient. Stage pT1a was given in 19 patients and stage pT1b in the remaining two patients. One patient with positive surgical margin in this study received close follow-up by ultrasound and CT scan. Neither residual nor recurrent tumors were identified by image studies after a 25-month follow-up time frame. Among all 31 patients, neither recurrent nor metastatic tumor was identified at a mean follow-up of 29 months postoperatively. The mean change of eGFR was decreased by 6.5 (ml/min/m2).
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Surg Endosc Table 1 Patient characteristics
Overall population (n = 31) Gender Male
19
Female
12
Age (years), mean (range)
53 (39–70)
BMI (kg/m2), mean (range)
25.2 (20.3–35.9)
ASA classification ASA I
12
ASA II
17
ASA III
2
Tumor side Right
18
Left
2.9 (1.8–6.3)
RENAL nephrometry score, mean (range)
5.3 (4–7)
Discussion Previous literature has shown that partial nephrectomy is equivalent to radical nephrectomy in terms of long-term outcome in patients with malignant tumors less than 4 cm [2, 3]. Partial nephrectomy is a procedure that has gained wider acceptance in the recent decades. Since LPN was first performed in 1993 [5], it has become the most popular procedure for treating small renal tumor because of its minimally invasive advantages. However, laparoscopic partial nephrectomy is a technically more demanding surgery than laparoscopic nephrectomy. During a traditional open partial nephrectomy which involves renal pedicle clamping and suturing post-tumor excision, renal hypothermia can be easily achieved by instilling ice slush around the kidney and bleeding can be controlled under a larger field of operation. Under a laparoscopic setting, such challenges are more difficult to overcome. In LPN intracorporeal suturing, operation time is further extended even under robot assistance, a step which prolongs warm ischemic time. Some authors proposed that deep medullary suture may cause partial devascularization of the remaining renal parenchyma, affecting renal preservation [10]. However, the application of hemostatic matrix and fibrin sealant has shown to allow us to perform LPN without renal artery clamping and without intracorporeal suturing. FloSeal is a hemostatic agent composed of a gelatin matrix and human thrombin. The efficacy of hemostasis had been confirmed during partial nephrectomy in previous literatures [11–13]. Tisseel, a fibrin sealant, has also been used for partial nephrectomy; however, the effect of such products in the sealing of the collecting system remains controversial [13, 14]. Recently, Ploussard et al. [15] reported that the combination of FloSeal and Tisseel has shown in their study to safely control parenchymal
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13
Tumor size (cm), mean (range)
bleeding and replace the conventional suture without compromising operative outcomes during LPN on a swine experimental surgery. According to the experiences of reviewed authors, we modified their methods to develop a technique of performing LPN with ease and with satisfactory results. At our institution, we started laparoscopic radical nephrectomy in 2000 and began the laparoscopic partial nephrectomy program in 2003. Our experience with LESS partial nephrectomy began in 2013. In recent years, we evaluated our evolution from traditional partial nephrectomy to LESS partial nephrectomy using this technique to minimize wound length without compromising surgical outcomes. In this study, we included only six patients that received LESS partial nephrectomy; the initial results are encouraging. We plan to report on detailed surgical outcome of LESS partial nephrectomy in the future. LPN can be carried out either via the transperitoneal route or via the retroperitoneal route. To date, there is no significant evidence showing the optimal technique for LPN. Previous literature has shown that retroperitoneoscopy is associated with more complications and conversions compared to traditional laparoscopy [16, 17]. In this study, we show no difference in conversion and complication rates between the two techniques. Two postoperative complications occurred in this study: One patient that received the transperitoneal approach suffered from postoperative pneumonia. She was the oldest patient in the patient population and was able to make a full recovery after receiving 1 week of antibiotics treatment. Another patient that received the retroperitoneal approach suffered from persistent urine leakage for 6 days post-operation. This patient was noted to have had the largest collecting system disruption compared to all other patients (approximately 1 cm in length). This defect had been
Surg Endosc Table 2 Perioperative parameters
No = 31 Approach Transperitoneal
11 (35 %)
Retroperitoneal
20 (65 %)
Method Traditional laparoscopy
25 (81 %)
Laparoendoscopic single-site (LESS)
6 (19 %)
Renal artery control Clamped
20 (65 %)
Non-clamped
11 (35 %)
Warm ischemic time (minute), mean (range)
19.0 (9–26)
Operation time (minute), mean (range)
188 (120–290)
Blood loss (ml), mean (range)
171 (10–650)
Hospital stay (day), mean (range)
6.2 (3–13)
Blood transfusion Yes No
1 (3.2 %) 30 (96.8 %)
Histology RCC
21 (67.7 %)
Oncocytoma
4 (12.9 %)
AML
4 (12.9 %)
Metanephric adenoma
1 (3.2 %)
Infected cyst
1 (3.2 %)
Stage of RCC PT1a
19 (90.5 %)
PT1b
2 (9.5 %)
Complications Pneumonia
1 (3.2 %)
Prolong urine leakage
1 (3.2 %)
Positive margin Yes
1 (3.2 %)
No Cancer recurrence
30 (96.8 %)
Yes
0 (0 %)
No
21 (100 %)
Duration of follow-up (month), mean (range)
29 (3–70)
Change of eGFR (ml/min/m2), mean (range)
-6.5 (-26.3 to ?15.1)
initially sealed off by cauterization and covered by FloSeal, Tisseel and fat pad layer by layer consecutively. Persistent urine leakage (about 200–400 ml/day) from the JacksonPratt drainage tube was noted for 6 days but was spontaneously resolved 1 week after the surgery without additional management. We noticed that collecting system disruption occurred in 8 of the 31 patients. One patient as mentioned above had massive urine leakage; two patients had minor urine leakage (less than 100 ml/day) for 3 days postoperatively. There was no urine leakage noted in the other five patients. Our results are consistent with previous studies. L’Esperance et al. [11] also reported a high rate of
urine leakage when Tisseel was used for collecting duct repair, regardless of the addition of FloSeal use. One novel technique we propose is using the Tisseel to bind a fat pad to the outer layer. The fat pad encapsulated the FloSeal within the tumor-excised cavity, supplementing structural support of the expanding and swelling action of FloSeal after it interacts with blood or urine from within. The space within the fat pad acts in theory like a ‘‘pressure cooker,’’ providing an extra external pressure in preventing postoperative bleeding. We did not perform any renal parenchymal suturing after tumor excision, and none of our patients suffered from postoperative bleeding. Although urine
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leakage occurred in three patients, only conservative management was required. Aboumarzouk et al. [18] and Zhang et al. [19] conducted systematic reviews on the outcomes of robotic and LPN; they concluded that the robotic approach had significantly shorter warm ischemic time [18, 19]. Warm ischemic time is the major factor for renal function preservation after LPN. Our technique facilitates shorter renal defect repair time and therefore reduces the ischemic time. The results of this study show that our procedure is an excellent alternative to LPN specifically in patients with stage 1 renal tumors. We show a significantly shorter warm ischemic time, lower risk of postoperative bleeding and high feasibility for surgeons. Operative time in this study was longer compared to other study groups due to the inclusion of LESS procedure and also due to some lessexperienced surgeons that performed the LPN. If we exclude patients whom were operated by less-experienced surgeons as well as those that received the LESS surgery, the mean warm ischemic time would be 16 min. For patients that underwent the LESS method, the warm ischemic time was nevertheless convincing. The mean warm ischemic time of the six patients was 23 min (range 19–27). Shorter warm ischemic time in our study was significantly compared to that of other studies where LPN was performed under robot assistance [20–22]. We believe that this technique should be adopted in LESS partial nephrectomy to improve not only the warm ischemic time but also the learning curve of surgeons. This technique will shorten the learning curve in accomplishing LPN, robotic PN or LESS PN for urologists who lack the experience of intracorporeal suturing. We also believed that this technique is suitable for other surgeries in the field of hepatobiliary surgery, for example, using the omentum as an adhesive encapsulation for liver surface after tumor excision. There are still some limitations to this design. We used a relatively small cohort group, and we did not have a prospective randomized controlled group. Most patients included in this study had characteristics of exophytic tumor. The efficacy of this technique for patients with endophytic tumor still needs to be explored.
Conclusion Although LPN is a challenging procedure, we have shown that our LPN technique reduces the warm ischemic time significantly and provides excellent functional outcomes. This method allows surgeons to perform LPN more easily and more effectively with fewer complications. In our initial experience, suturing was not necessary during collecting system disruption of less than 1 cm in length.
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We are currently continuing long-term follow-up and documentation of associated outcomes in order to confirm the long-term efficacy of this surgical management. Acknowledgments This study was supported by a grant from Health and welfare surcharge of tobacco products, Ministry of Health and Welfare (MOHW104-TDU-B-212-124-003); Kaohsiung Medical University Hospital (KMUH103-3R46); Ministry of Science and Technology (MOST 103-2320-B-037-010). Compliance with Ethical Standards Disclosures Ching-Chia Li, Hsin-Chih Yeh, Hsiang-Ying Lee, WeiMing Li, Hung-Lung Ke, Allen Herng Shouh Hsu, Mei Hui Lee, Chia-Chun Tsai, Kuang-Shun Chueh, Chun-Nung Huang, Yii-Her Chou, Chien-Feng Li and Wen-Jeng Wu declare they have no conflict of interest. Ethical standard This study was approved by the appropriate institutional review board at Kaohsiung Medical University Hospital (KMUH-IRB-20130082) and performed according to the ethical standards laid down by the 1964 Declaration of Helsinki.
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