Renal Transposition During Minimally Invasive Partial Nephrectomy: A Safe Technique for Excision of Upper Pole Tumors

Abstract

Minimally invasive partial nephrectomy (MIPN) for upper pole masses, particularly for those located posteriorly, is challenging because of difficult visualization during tumor resection and renorrhaphy. Complete renal transposition facilitates access to and excision of upper pole renal masses during MIPN. Sixteen patients with upper pole renal masses underwent laparoscopic or robot-assisted partial nephrectomy with renal transposition from October 2009 to March 2012 with a mean follow-up of 22 months. Mean operative time was 242.6 minutes, and mean warm ischemic time was 14.7 minutes. No patient needed an intraoperative or postoperative blood transfusion. Five (31%) patients had a postoperative complication (four Clavien grade I, one Clavien grade II). There were no delayed complications, positive surgical margins, or tumor recurrences. Mean postoperative eGFR change within 3 months was −9.4%. These results show that complete renal transposition can be safely used to facilitate excision of upper pole tumors.

Introduction

P artial nephrectomy is the standard of care for the treatment of patients with clinical T₁ renal masses, offering cancer outcomes equivalent to radical nephrectomy and a decreased risk of short- and long-term deficits in renal function.^1
–3 Laparoscopic partial nephrectomy (LPN) and robot-assisted partial nephrectomy (RAPN) follow the established surgical oncologic principles of open partial nephrectomy (OPN), appear to have comparable cancer outcomes to OPN, and offer the potential of improved quality-of-life outcomes. These less invasive approaches, however, have been associated with longer warm ischemia time (WIT) and a higher complication rate in recent retrospective comparisons.^4,5 Although the rates of minimally invasive partial nephrectomy (MIPN) have been increasing,⁶ the technical challenges of MIPN largely limit its performance to surgeons performing a high volume of these procedures at tertiary care centers.^2,7

Even in skilled hands, certain tumor positions can increase the difficulty of MIPN. In particular, upper pole masses, especially those positioned posteriorly, present significant challenges in visualization during tumor resection and renorrhaphy. The few existing studies focusing on minimally invasive surgical treatment of upper pole tumors suggest that the open approach remains the standard of care because of the difficulty and high complication rate associated with laparoscopy.^8,9

We sought to develop a safe technique to better access and more easily excise difficult-to-reach upper pole tumors in patients undergoing transperitoneal MIPN. After mobilizing the entire kidney and ureter, we perform complete renal transposition, flipping the upper pole posterior aspect of the kidney to the lower pole anterior position. In this study, we present our technique and outcomes. A detailed demonstration of RAPN using complete renal transposition is in the accompanying video.* The technique of renal transposition in LPN is unchanged from RAPN, and therefore applicable to all MIPN.

Technique

We use a three-arm robotic approach employing a 0-degree lens and two robotic working arms.

With the patient in a modified 30-degree lateral position with all pressure points padded, we establish pneumoperitoneum with a Veress needle and place trocars under direct visualization.^10,11 We reflect the colon medially and develop a plane posterior to the ureter and anterior to the psoas muscle. We then isolate the renal hilum. Intraoperative ultrasonography is used to identify the tumor boundaries in all patients.

We use the transposition technique only if complete circumferential access to the tumor remains compromised after adequate mobilization and medial rotation of the kidney. To allow for complete transposition, (1) all attachments to the kidney must be dissected free outside of the Gerota fascia; (2) all fatty vascular tissue superior to the renal hilum must be dissected free, including complete separation of the adrenal gland from the upper pole; (3) the ureter must be dissected away from the lower pole of the kidney to the level of the renal pelvis. This ensures an adequately narrow hilum to allow for complete kidney rotation around the hilar axis. Patients with multiple renal vessels are not candidates for transposition because polar vessels prohibit complete transposition and hilums with multiple vessels cannot be narrowed adequately to allow for complete transposition.

Once all renal attachments except the hilum are freed, we perform transposition by rotating the upper pole of the kidney anteriorly and inferiorly while simultaneously displacing the lower pole posteriorly and superiorly, placing upper pole posterior tumors into a more accessible lower pole-anterior position (Fig. 1).

FIG. 1.

Complete renal transposition during minimally invasive partial nephrectomy. (a) A renal tumor is located on the superomedial aspect of the upper pole. (b) The kidney, freed of all its attachments, is rotated 180 degrees anterior-posteriorly around its hilar axis by pulling the upper pole anteriorly and inferiorly while simultaneously pushing the lower pole posteriorly and superiorly. (c) The renal hilum is clamped en bloc after transposition and resection of the tumor proceeds with improved visualization and ergonomics.

After the perirenal fat overlying the tumor is removed, we use ultrasound to demarcate tumor margins and score the renal capsule circumferentially around the tumor. We apply a laparoscopic bulldog clamp to the renal artery or the entire hilum en bloc, and sharply excise the tumor. We perform an early unclamping technique in all patients, first oversewing the base of the excision defect with a running 3-0 barbed absorbable suture to close collecting system defects and larger central vessels, then removing the bulldog clamp and individually ligating any remaining bleeding end arteries with figure of eight 3-0 absorbable barbed or polyglactin braided sutures.¹¹

To reapproximate the renal cortical edges, we use a sliding clip renorrhaphy technique using a series of 0-polyglactin absorbable braided sutures with Weck (Teleflex, Research Triangle Park, NC) Hem-o-lok^® and LAPRA-TY^® clips (Ethicon Endo-Surgery, Somerville, NJ) clips.¹² No fibrin bolsters or biologic glue products are used. The kidney is returned to its native position and secured to the abdominal sidewall using a 3-0 running absorbable braided suture.

Equipment

• da Vinci^® Surgical System S or Si HD

• Fenestrated bipolar forceps, Prograsp™ forceps, curved scissors, and large needle drivers

• Laparoscopic 0-degree and da Vinci^® 0-degree lenses

• Two 12-mm trocars

• Two 8-mm robotic trocars and one or two 5-mm trocars

• Laparoscopic suction-irrigator, scissors, locking grasper, and bulldog clamp applier for assistant

• Flexible laparoscopic or “drop-in” robotically controlled ultrasound transducer

• Two long, straight (25 mm) laparoscopic bulldog clamps

• Sutures: 3-0 barbed Vicryl™ suture for deep running repair of renal defect, 0 Vicryl (CT-1 needle) for renorrhaphy, 3-0 Vicryl (SH-needle) for reapproximation of the Gerota fascia

• Hem-o-lok^® Clips, Lapry-Ty^® suture clips, and clip appliers

• Endoscopic specimen bag, 10 mm

Role in Urologic Practice

Results

From October 2009 to July 2012, a total of 16 patients underwent complete renal transposition during MIPN at our institution (2 LPN, 14 RAPN). The transposition technique was performed only if visualization of the tumor was initially insufficient to ensure safe and complete excision and reconstruction. Cohort data was collected prospectively with Institutional Review Board approval.

Table 1 summ arizes patient demographics and preoperative characteristics. Mean age was 49.9 years, and 69% of patients had a Charlson Comorbidity score of 2 or lower. All tumors were clinical stage T_1a, with a mean tumor size of 2.9 cm. Most patients who needed renal transposition had upper pole tumors; one had a midpolar posterior tumor that was medially located just above and adjacent to the hilum. There were 63% of patients who had nephrometry scores consistent with tumors of moderate to high complexity.¹³

Table 1.

Patient Demographics and Preoperative Characteristics (N=16)

Sex
Male (N, %)	10, 63%
Female (N, %)	6, 37%
Mean age (range)	49.9 (29–71)
Mean kg/m² body mass index (range)	29.7 (21.6–40.1)
Mean ASA score (range)	2.38 (2–3)
Charlson Comorbidity Index
0–2 (N, %)	11, 69%
3+ (N, %)	5, 31%
Mean cm preoperative tumor size (range)	2.9 (1.4–4.0)
Side
Left (N, %)	10, 63%
Right (N, %)	6, 37%
Pole
Upper (N, %)	15, 94%
Midpolar (N, %)	1, 6%
Lower (N, %)	0, 0%
Total nephrometry score (N)
4	3
5	1
6	2
7	9
8	0
9	0
10	1
11	0
12	0
Mean mL/min per 1.73m² preoperative eGFR (range)	97.1 (70.1–132.6)

ASA=American Society of Anesthesiologists; eGFR=estimated glomerular filtration rate.

The mean operative time was 242.6 minutes, mean warm ischemia time was 14.7 minutes, and mean estimated blood loss was 440 mL (Table 2). No patient needed a blood transfusion, and all cases were completed without conversion to open surgery. One patient had a small colonic thermal injury recognized intraoperatively that was oversewn with a single figure-of-eight silk suture without sequelae.

Table 2.

Intraoperative and Perioperative Outcomes (N=16)

Mean operative minutes (range)	242.6 (159–455)
Mean mL EBL (range)	440.0 (50–1000)
Mean minutes WIT (range)	14.7 (9–23)
Mean days LOS (range)	2.9 (2–6)
Intraoperative complications (N, %)	1, 6%
Complications ≤30 days postoperatively (N, %)	5, 31%
	Clavien Grade:
	I: 4
	II: 1
	IIIa: 0
	IIIb: 0
	IV: 0
	V: 0
Intraoperative or postoperative blood transfusions (N)	0, 0%
Mean postoperative eGFR change ≤3 months (%)	≤3 months: −9.4% (−42.0–4.9)
Mean cm postoperative tumor size (range)	2.8 (1.2–4.1)
Mean nuclear Fuhrman grade (range)	2.0 (1–3)
Pathology
Clear-cell (N, %)	7, 44%
Papillary (N, %)	3, 19%
Oncocytoma (N, %)	3, 19%
AML (N, %)	2, 13%
Other benign (N, %)	1, 6%
PSM (N, %)	0, 0%

EBL=estimated blood loss; WIT=warm ischemia time; LOS length of stay; eGFR=estimated glomerular filtration rate; AML=angiomyolipoma; PSM=positive surgical margin.

Mean length of stay was 2.9 days. Five (31%) patients experienced a minor postoperative complication within 30 days of surgery, four of which were Clavien grade I and one of which was Clavien grade II. With a mean follow-up of 22 months, no patients had a delayed complication. Pathologic data were available for all patients. There were no positive surgical margins.

Discussion

Nearly two decades ago, LPN was described as an alternative to OPN for the resection of small renal masses.¹⁴ Subsequent studies established improved convalescence and equivalent oncologic outcomes.^5,15
–17 Further advances have allowed safe application of minimally invasive techniques for partial nephrectomy including robot assistance, sliding-clip renorrhaphy,¹⁸ intraoperative ultrasonography,¹⁹ early unclamping,^11,20 and off-clamp laparoscopic partial nephrectomy (PN.)²¹ The American Urological Association now recognizes PN (any approach) as the standard of care for T_1a renal masses and recommends that “patients with small peripheral lesions who meet criteria for open partial nephrectomy should be considered for laparoscopic partial nephrectomy.”²²

Only 32% of stage 1 tumors included in The National Cancer Data Base as of 2007 were excised using PN, however.²³ The causes for this low implementation are multifactorial and may include financial considerations,²⁴ pressure to perform minimally invasive radical nephrectomy rather than OPN, and surgical technical complexity inherent to certain tumor locations. In particular, upper pole posterior tumors are challenging during LPN because the patients' ribs necessitate positioning the camera inferomedially, mandating an inferomedial approach to the renal hilum and tumor. This makes visualization, resection, and reconstruction more difficult.

The challenges that upper pole tumors present are reflected in the outcomes for MIPN reported in the current literature. In a retrospective review of 123 cases of LPN, upper pole tumors were associated with the greatest blood loss and complication rate compared with tumors in other locations.²⁵ Another retrospective review studied differences in intraoperative and perioperative outcomes between upper pole LPN, lower pole LPN, and upper pole OPN, and found that upper pole LPN had a significantly higher transfusion rate than lower pole LPN and upper pole OPN (25%, 6%, and 4%, respectively).⁸ Upper pole LPN also trended toward a higher intraoperative major complication rate than upper pole OPN (17% vs 4%, P=0.17) and a higher postoperative major complication rate than lower pole LPN (22% vs 6%, P=0.07), although these differences did not reach statistical significance. Recently presented data highlighted the inherent difficulty in MIPN for upper pole tumors, reporting an 8% intraoperative complication rate and a >90% low-grade delayed postoperative complication rate using the Clavien-Dindo classification.⁹ For each of the above studies, authors suggested that the open approach should be strongly considered for tumors in the upper pole location.

The literature is sparse in regard to describing surgical techniques to perform nephron-sparing resection of upper pole tumors. Chien and colleagues²⁶ described using a suspension traction suture to more optimally position the kidney for transperitoneal LPN, but did not report patient demographics nor complication rates. A case report from Japan described using a gauze sling and a flexible laparoscope to approach two upper pole apical tumors, but did not describe any intraoperative or perioperative outcomes.²⁷ One recent study comparing single-port laparoscopy (SPL) to single-port robot-assisted laparoscopy in seven patients acknowledged the reduced maneuverability and visibility of upper pole masses and recommended that upper pole masses be excluded from SPL PN.²⁸

A small retrospective study described renal transposition during LPN; however, there was a higher complication and transfusion rate than in the current series.²⁹ Retroperitoneoscopic LPN is also a viable approach to upper pole posterior tumors, and its use was encouraged for tumors in that location in a study by Ng and associates³⁰ from the Cleveland Clinic, although outcomes were not stratified by tumor position. Most urologists, however, are less familiar with the retroperitoneal approach to minimally invasive surgery than the more traditional transperitoneal approach.

Robot assistance was used in the majority of the patients in our series, but robotic technology is not essential to the transposition technique. There are, however, several crucial technical considerations that should be understood before performing renal transposition.

First, the extensive mobilization of the ureter up to the level of the renal hilum ensures adequate freedom-of-motion with which to rotate the kidney and is inherent and critical to renal transposition. We have not observed any early or late ureteral complications in our series associated with this dissection.

Second, renal transposition raises considerations regarding clamping of the renal hilum. In our cohort, we clamped the renal hilum after transposition, because it is our belief that additional shearing forces during the flipping process could cause trauma to the hilum if it is clamped before transposition. Also, we found that twisting of the renal artery with the kidney can make separate arterial clamping difficult; therefore, we often clamped the entire hilum en bloc after transposition using a single laparoscopic bulldog placed by the bedside assistant.

Third, the surgeon should be prepared for increased venous back-bleeding with renal transposition, especially after early unclamping and before sliding clip renorrhaphy, as a result of partial compression of the renal vein because of the rotation inherent to complete transposition. This phenomenon is observed even if early unclamping is not performed and would likely be accentuated in the setting of off-clamp MIPN. In our experience, although increased back-bleeding was noticeable, it did not interfere with visualization during tumor excision or renal reconstruction, and no blood transfusions were needed intraoperatively or postoperatively.

Finally, it should be noted that patients with large amounts of adherent perirenal fat can still undergo transposition and, in fact, we have found that transposing the kidney makes for a more straightforward dissection of the fat around the tumor because it is more easily visible. In addition, renal transposition does not crowd the surgeon's view as can be an issue with simple medial reflection of the kidney; transposition maintains the kidney in the renal fossa while rotating it around the hilum, and thus the effective working distance is similar to that when the kidney is in its native orientation.

This study describes the experience of a single fellowship-trained surgeon at a tertiary care institution with a high volume of laparoscopic and robot-assisted kidney surgeries. A multi-institutional evaluation would validate the generalizability of our technique.

Conclusions

Renal transposition is a safe technique that facilitates nephron-sparing transperitoneal laparoscopic resection of difficult-to-reach upper pole tumors. Adoption of this technique may increase the proportion of small renal masses that can be resected using minimally invasive approaches.

Footnotes

Acknowledgments

The authors would like to thank Tom Laws for his expertise in video editing and Ryan Cauley, MD, for his illustrative talents.

Disclosure Statement

No competing financial interests exist.

Abbreviations Used

References

Patard

, Shvarts

, Lam

et al. Safety and efficacy of partial nephrectomy for all T1 tumors based on an international multicenter experience. J Urol, 2004; 171:2181–2185.

Zini

, Patard

, Capitanio

et al. The use of partial nephrectomy in European tertiary care centers. Eur J Surg Oncol, 2009; 35:636–642.

Donin

, Suh

, Barlow

et al. Tumour diameter and decreased preoperative estimated glomerular filtration rate are independently correlated in patients with renal cell carcinoma. BJU Int, 2012; 109:379–383.

Lane

, Novick

, Babineau

et al. Comparison of laparoscopic and open partial nephrectomy for tumor in a solitary kidney. J Urol, 2008; 179:847–852.

Gill

, Kavoussi

, Lane

et al. Comparison of 1,800 laparoscopic and open partial nephrectomies for single renal tumors. J Urol, 2007; 178:41–46.

Smaldone

, Kutikov

, Egleston

et al. Assessing performance trends in laparoscopic nephrectomy and nephron-sparing surgery for localized renal tumors. Urology, 2012; 80:286–291.

Thompson

, Kaag

, Vickers

et al. Contemporary use of partial nephrectomy at a tertiary care center in the United States. J Urol, 2009; 181:993–997.

Zorn

, Gong

, Mendiola

et al. Operative outcomes of upper pole laparoscopic partial nephrectomy: Comparison of lower pole laparoscopic and upper pole open partial nephrectomy. Urology, 2007; 70:28–34.

Narayanan

, O'Malley

, Mehedint

, Schwaab

. Upper pole kidney tumors: Open or laparoscopic partial nephrectomy? J Clin Oncol, 2012; 30,suppl 5Abstract 429http://www.asco.org/ascov2/Meetings/Abstracts?&vmview=abst_detail_view&confID=116&abstractID=89709. 2012 July 5.

10.

Benway

, Bhayani

, Rogers

et al. Robot-assisted partial nephrectomy: An international experience. Eur Urol, 2010; 57:815–820.

11.

San Francisco

, Sweeney

, Wagner

. Robot-assisted partial nephrectomy: Early unclamping technique. J Endourol, 2011; 25:305–308.

12.

Haber

, White

, Crouzet

et al. Robotic versus laparoscopic partial nephrectomy: Single-surgeon matched cohort study of 150 patients. Urology, 2010; 76:754–758.

13.

Kutikov

, Uzzo

. The R.E.N.A.L. nephrometry score: A comprehensive standardized system for quantitating renal tumor size, location and depth. J Urol, 2009; 182:844–853.

14.

Winfield

, Donovan

, Godet

, Clayman

. Laparoscopic partial nephrectomy: Initial case report for benign disease. J Endourol, 1993; 7:521–526.

15.

Koenig

, Aron

, Kaouk

, Gill

. The case for laparoscopic partial nephrectomy. J Endourol, 2008; 22:1917–19191925, 1929.

16.

Simmons

, Chung

, Gill

. Perioperative efficacy of laparoscopic partial nephrectomy for tumors larger than 4 cm. Eur Urol, 2009; 55:199–207.

17.

Gong

, Orvieto

, Zorn

et al. Comparison of laparoscopic and open partial nephrectomy in clinical T1a renal tumors. J Endourol, 2008; 22:953–957.

18.

Benway

, Wang

, Cabello

, Bhayani

. Robotic partial nephrectomy with sliding-clip renorrhaphy: Technique and outcomes. Eur Urol, 2009; 55:592–599.

19.

Sun

, Wagner

, San Francisco

et al. Need for intraoperative ultrasound and surgical recommendation for partial nephrectomy: Correlation with tumor imaging features and urologist practice patterns. Ultrasound Q, 2012; 28:21–27.

20.

Nguyen

, Gill

. Halving ischemia time during laparoscopic partial nephrectomy. J Urol, 2008; 179:627–632.

21.

Kaczmarek

, Tanagho

, Hillyer

et al. Off-clamp robot-assisted partial nephrectomy preserves renal function: A multi-institutional propensity score analysis. Eur Urol, 2012Epub ahead of print.

22.

Novick

, Campbell

, Belldegrun

et al. American Urological Association Education and Research (AUA) Guidelines: Guideline for Management of the Clinical Stage 1 Renal Mass. http://www.auanet.org/content/GUidelines-and-quality-care/clinical-guidelines/main-reports/renalmass09.pdf. 2012 July 5.

23.

Cooperberg

, Mallin

, Kane

, Carroll

. Treatment trends for stage I renal cell carcinoma. J Urol, 2011; 186:394–399.

24.

Tanagho

, Figenshau

, Sandhu

, Bhayani

. Is there a financial disincentive to perform partial nephrectomy? J Urol, 2012; 187:1995–1999.

25.

Venkatesh

, Weld

, Ames

et al. Laparoscopic partial nephrectomy for renal masses: Effect of tumor location. Urology, 2006; 67:1169–1174.

26.

Chien

, Orvieto

, Chuang

et al. Use of suspension traction system for renal positioning during laparoscopic partial nephrectomy. J Endourol, 2005; 19:406–409.

27.

Kim

, Hattori

, Yoshino

et al. Laparoscopic partial nephrectomy in upper-pole apical renal tumor using gauze sling and flexible laparoscope. J Endourol, 2007; 21:879–882.

28.

Kaouk

, Goel

. Single-port laparoscopic and robotic partial nephrectomy. Eur Urol, 2009; 55:1163–1169.

29.

Nouralizadeh

, Ziaee

, Basiri

et al. Transperitoneal laparoscopic partial nephrectomy using a new technique. Urol J, 2009; 6:176–181.

30.

, Gill

, Ramani

et al. Transperitoneal versus retroperitoneal laparoscopic partial nephrectomy: Patient selection and perioperative outcomes. J Urol, 2005; 174:846–849.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

42.81 MB