Open partial nephrectomy with kidney split: Effective surgical approach to resect completely endophytic tumors

Abstract

Objectives:

To review perioperative, renal functional, and oncological outcomes of the kidney split technique in performing partial nephrectomy (PN) to resect completely endophytic renal tumors.

Methods:

All consecutive patients who underwent open PN with kidney split between 2015–2019 at our institution were included. In this approach the kidney is incised along Brodel’s line in an avascular plane to locate and then resect the endophytic tumor. Clinicopathologic data, perioperative metrics, complications, renal function, recurrence, and mortality were analyzed using descriptive statistics.

Results:

42 open PN with kidney split were performed in 40 patients. No patients required conversion to radical nephrectomy. Most tumors were pT1a renal cell carcinoma (76%), with no recurrences or deaths after a median follow-up of 15 months. All patients had tumors of moderate or high complexity by R.E.N.A.L. nephrometry score. Median cold ischemia time, operative time, estimated blood loss, and inpatient length-of-stay were 34 minutes, 152 minutes, 225 mL, and 2 days, respectively. No patients experienced any Clavien-Dindo grade 4 or 5 complications. Post-operative estimated glomerular filtration rate (eGFR) at last follow-up was >30 mL/min/1.73m² in all but one patient, and no patients required dialysis.

Conclusions:

The kidney split represents an effective PN technique to resect complex, endophytic renal tumors. In our experience, this technique affords acceptable perioperative outcomes, preserved renal function, and no short-term recurrences or mortality events. Our series highlights the importance of adapting classical surgical techniques, using cold ischemia, and relying on preoperative and intraoperative ultrasonography to effectively guide this complex kidney-sparing operation.

INTRODUCTION

The American Urological Association (AUA) guidelines strongly advocate the use of partial nephrectomy (PN) over radical nephrectomy (RN) in surgically managing clinically localized renal masses, when technically feasible, in order to minimize the risk of chronic kidney disease (CKD) and achieve similar oncological outcomes to RN.¹ Traditionally restricted to stage T1a tumors, PN for even stage T1b-T3a tumors can also yield similar oncologic control to RN in appropriately selected patients.^2–5 Nephron preservation is critical for patients with tumors in a solitary kidney, bilateral tumors, and for those with preexisting CKD in an attempt to delay or prevent the need for renal replacement therapy. However, completely endophytic, renal sinus, multifocal, and perihilar tumors pose technical challenges and lower the threshold for many surgeons to perform RN due to increased complexity, bleeding risk, risk of renal loss, or inability to repair the collecting system. Centrally located tumors may also be associated with higher stage or recurrence risk.⁶

Over the last 15 years, minimally-invasive surgical techniques have been widely implemented with robotic-assisted PN supplanting laparoscopic and open PN as the most common approach utilized.⁷ At our center, we have found comparable perioperative, functional, and oncologic outcomes between open and minimally-invasive PN.^8–11 For impalpable, completely endophytic tumors, intraoperative ultrasound enables real-time visualization for surgical planning.¹² One approach to these endophytic tumors is an en bloc removal of that portion of the tumor-bearing kidney with subsequent nephron loss and a large defect necessitating repair of the kidney and collecting system. Robotic-assisted techniques have also been described.^13–15 In this technical paper we would like to present an effective alternative approach to resect these completely endophytic tumors utilizing a classical open surgical technique originally described for anatrophic nephrolithotomies.¹⁶ A vertical renal cortical incision in Brodel’s line takes advantage of an avascular surgical plane to minimize blood loss and spare the benign renal parenchyma overlying the tumor. Herein, we review our contemporary series of utilizing this open surgical approach to resect complex endophytic renal tumors, which we term the kidney split, and report our perioperative outcomes as they relate to complications, renal function, and survival using this technique.

METHODS

Following institutional review board approval, all patients who underwent attempted PN, including those who were converted to RN, at our institution were queried. All consecutive patients who underwent open PN with kidney split by two high-volume kidney surgeons (P.R. or A.A.H.) between 2015 and 2019 comprised our final cohort. Although the kidney split approach was utilized prior to 2015, it was not routinely described as such in the operative reports, and outcomes data could not be reliably collected until 2015 when computer forms were introduced and consistently allowed for recording all surgical details. Representative preoperative CT and renal ultrasound imaging shown in Supplementary Figure 1 provides the basis of our surgical planning.

With respect to our surgical approach (Figure 1 and Supplementary Figure 2), patients are placed in the standard flank position, and access to the kidney is obtained via a previously described mini-flank supra-11^th rib incision, which is usually 8–10 cm in length.^{17, 18} Following complete kidney mobilization and its delivery into the incision, the renal artery, vein and ureter are isolated. Intraoperative ultrasound is used to confirm the precise location and depth of the tumor and to identify any satellite lesions or invasion into a branch renal vein or collecting system. Renal artery occlusion with a bulldog clamp is performed to limit blood loss and improve visibility. The renal vein is not routinely clamped. We routinely apply ice slush hypothermia for renoprotection. Based on our published randomized trial, mannitol for renoprotection is no longer used.¹⁹

Figure 1.

Kidney split surgical technique illustrated. (A) Following initiation of cold ischemia, a cortical incision along Brodel’s line enables entry into an avascular plane. (B) The endophytic tumor is identified and dissected. The use of stay sutures to control vessels and provide traction, a metal suction, a Penfield dissector, and/or Singley forceps provide assistance with excision of the tumor.

With the assistance of intraoperative ultrasound, the renal cortex is vertically incised close to, but not right over, the endophytic tumor along Brodel’s line.²⁰ This approach allows access into the renal sinus through the renal cortex in a relatively avascular plane. The surgeon carefully probes the renal cortex with its reddish hue until the lateral border of the tumor is identified often with a strikingly different color from the cortex. Usually the tumor is floating freely within the renal sinus fatty tissue and can splay vascular and collecting system elements but rarely invades them. Careful dissection with the Penfield dissector or Cobb elevator is done with special care not to violate the tumor or its pseudo-capsule in the process. The tumor is gently delivered out of the sinus and detached sharply from the renal cortex, which always serves as its point of attachment, with at least a 1 cm margin. Any rents in the collecting system or opened renal vessels are closed with 3–0 absorbable sutures. The argon beam coagulator is used to cauterize any exposed renal cortical tissue. Any available perinephric fat and absorbable clotting matrix (Surgicel®, Arista™) are placed in the resection cavity to fill the space. The renal capsule is then reapproximated with Surgicel-pledgeted 0 chromic liver sutures. The renal artery is then unclamped, and iced slush removed from the wound. Careful inspection of the kidney, which assumes its normal pink and well perfused appearing color, is done for 5–8 minutes. Gentle pressure is applied to the resection site to promote hemostasis of any small venous channels within the resection bed. This waiting period also allows any small arterial vessels that may have been in spasm to manifest bleeding while the patient is still in the operating room. On rare occasion, brisk bright red bleeding may emanate from the surgical resection bed. This type of arterial bleeding will not respond to pressure and necessitates the opening of renorrhaphy renal capsular sutures allowing for direct inspection of the surgical bed and suture ligation of the bleeding artery. We avoid, if possible, re-clamping of the renal artery to prevent reperfusion injury to the kidney. Surgical drains are rarely utilized in this setting.²¹ Once hemostasis is achieved, the flank incision is closed in two layers with #1 PDS, and the skin is closed with a 4–0 subcuticular absorbable suture.

Patients are followed post-operatively according to AUA guidelines,²² with history and physical, laboratory testing to include renal function, and an initial cross-sectional scan of the abdomen (CT or MRI) along with chest imaging obtained within 3 months of surgery. Thereafter, patients are followed by renal CT or ultrasound, chest imaging, and laboratory testing at 6-month intervals for 2 years and then yearly thereafter.

Clinicopathologic data, perioperative outcomes (including cold ischemia time, estimated blood loss (EBL), inpatient length-of-stay (LOS), blood transfusions, complications according to the Clavien-Dindo classification, and readmissions), renal functional outcomes, and oncologic outcomes (including recurrence and mortality) were collected. The data were analyzed using descriptive statistics in SPSS version 25.0 (IBM, Armonk, NY).

RESULTS

Among 1,410 total PN performed at our institution between 2015 and 2019, 743 (53%) were performed open and included 42 (3%) kidney split PN in 40 patients. Median age was 55 years and our cohort consisted of 50% males and 50% females. Most patients (81%) had a Charlson comorbidity index <2. No patient had a solitary kidney. All but one patient had renal cell carcinoma, with benign histology noted in the remaining patient. Median tumor size was 2.5 cm (range 0.9–5.5 cm), and pathologic stage was pT1a in 32 cases (76%), pT1b in 2 cases (5%), and pT3a in 7 cases (17%). The mean R.E.N.A.L. nephrometry score was 9.2 (range 7–11), and no patients harbored tumors of low complexity (nephrometry score between 4–6), while 45% of tumors were of high complexity (nephrometry score between 10–12).²³ Positive surgical margins were present in 2 cases (5%). After a median follow-up of 15.0 (IQR 6.9–28.5) months, no patient experienced recurrence, and all patients remain alive and free of disease. Clinical and pathologic data across the cohort are summarized in Supplementary Tables 1 and 2, respectively.

Median cold ischemia time was 34 minutes (range 17–82 minutes), and median operative time was 152 minutes (range 87–281 minutes). PN was performed successfully in all 42 cases, and no patient required conversion to RN. Two cases (5%) required a packed red blood cell transfusion intraoperatively, and 2 (5%) required a transfusion postoperatively. Median EBL was 225 mL (range 50–1550), and median LOS was 2 days (range 1–9). There were 12 patients (30%) who experienced any complication, all of which were Clavien-Dindo grades 1–3 (no grade 4 or 5 complications were observed), and all of which occurred within the first 30 days of their operation. The most common complication was urinary leak in 7 cases (17%), successfully managed with surveillance (1 case), percutaneous drain placement only (4 cases), or placement of both a percutaneous drain and a ureteral stent (2 cases). Two patients required readmission within 30 days of surgery, both for management of symptomatic urinary leaks. All leaks ultimately resolved. Perioperative outcomes are summarized in Table 1.

Table 1.

Perioperative outcomes of patients undergoing kidney split procedure.

Cases requiring intraoperative blood transfusion	2 (5%)
Cases requiring postoperative blood transfusion	2 (5%)
Median inpatient length-of-stay (IQR), days	2 (2–3)
Median operative time (IQR), mins.	152 (130–171)
Median cold ischemia time (IQR), mins.	33.9 (38.3–46.9)
Median estimated blood loss (IQR), mL	225 (100–500)
Cases requiring readmissions*	2 (5%)
Number of complications (Clavien-Dindo classification)*	Total patients with any complication: 12 (30%)
-Grade 1	6
-Grade 2	2
-Grade 3	10
-Grade 4	0
-Grade 5	0
Complication type (number of cases)
-Urine leak	7
-Infection/fever	3
-Pulmonary	2
-Arteriovenous fistula/pseudoaneurysm	1
-Anemia	1
-Cardiac	1
-Thromboembolic	1
-Gastrointestinal	1
-Hematuria	1

^*Both readmissions and all complications occurred within 30 days of surgery

Preoperatively all patients had eGFR ≥30 mL/min/1.73m², and after surgery, only one patient had eGFR <30 mL/min/1.73m² at last follow-up, with median eGFR 73 mL/min/1.73m². Median overall decrease in eGFR at last follow-up was 14%. No patients required dialysis. Median time to most recent eGFR was 14.5 (IQR 6.3–28.1) months. Renal functional outcomes are summarized in Table 2.

Table 2.

Renal functional outcomes of patients undergoing kidney split procedure. No patients required dialysis. eGFR, estimated glomerular filtration rate.

Median preoperative eGFR (IQR), mL/min/1.73m2	85.9 (76.0–96.8)
Preoperative eGFR
-≥60 mL/min/1.73m2	37 (88%)
−45–59 mL/min/1.73m2	2 (5%)
−30–44 mL/min/1.73m2	37 (88%)
-<30 mL/min/1.73m2	0 (0%)
Median eGFR at last follow-up (IQR), mL/min/1.73m2	73.0 (58.0–87.4)
Postoperative eGFR
-≥60 mL/min/1.73m2	29 (69%)
−45–59 mL/min/1.73m2	10 (24%)
−30–44 mL/min/1.73m2	2 (5%)
-<30 mL/min/1.73m2	1 (2%)
Median absolute decrease in eGFR at last follow-up (IQR), mL/min/1.73m2	11.3 (0.6–17.8)
Median % decrease in eGFR at last follow-up (IQR)	14.0 (0.6–22.5)
Median time to last eGFR (IQR), months	14.5 (6.3–28.1)

DISCUSSION

In this technical paper, we report our recent experience utilizing the kidney split approach during open PN to resect complex endophytic tumors. We spared the kidney in all cases and report favorable perioperative, functional, and oncological outcomes. Patients were discharged at a median of 2 days postoperatively, with acceptable intraoperative EBL and no grade 4–5 complications. Renal function was well-preserved with no patients requiring dialysis. Across a median follow-up of 15 months, we observed no recurrences or deaths. Together, our data support an important role for the kidney split approach as an effective operation for resecting complex, endophytic tumors.

The kidney split approach to endophytic tumors relies on classical surgical principles described originally by Dr. William H. Boyce over 50 years ago for removing staghorn calculi using open, trans-renal surgery.¹⁶ This anatrophic nephrolithotomy capitalized on the avascular plane between the anterior and posterior segmental branches of the renal artery, referred to as Brodel’s line,²⁰ which lies slightly posterior to the sagittal midline of the kidney. Accurately entering this plane via a cortical incision enables a relatively bloodless approach to the endophytic tumor situated in the renal sinus without sacrificing functional nephron volume. Earlier, smaller series have reported on the successful use of this approach to access and excise completely intraparenchymal renal tumors.^{24, 25}

Minimally-invasive approaches have been widely embraced for renal surgery,⁷ and it is our hope that the open surgical principles described herein may similarly be adopted for minimally-invasive techniques, particularly for these more complex endophytic tumors. Over the time period queried in the present study (2015–2019), a total of 647 minimally-invasive PN were performed at our institution, of which only 3 were performed using the kidney split technique, limiting a direct comparison of outcomes between open and minimally-invasive kidney split. Nevertheless, we have previously reported comparable perioperative, renal functional, and oncologic outcomes between open and minimally-invasive PN.^8–10 Recently, we also reported that, in a retrospective population-based cohort analysis of the Surveillance, Epidemiology, and End Results (SEER) database linked to Medicare claims, the use of minimally-invasive surgery for early-stage kidney cancer was not associated with differences in overall or disease-specific survival compared to open surgery.¹¹ The use of ice slush in open surgery also provides the advantage of prolonging ischemia time without compromising long-term renal function.^26–28 We routinely use ice slush during open PN regardless of tumor complexity, though its utility may be particularly valuable in these more complex cases.

We also want to highlight the importance of preoperative and intraoperative ultrasonography in guiding the kidney split surgical resection. In addition to CT or MRI cross-sectional imaging for clinical staging and delineation of the hilar anatomy, we also routinely obtain a preoperative renal ultrasound which effectively provides an imaging template and, coupled with intraoperative ultrasound, allows for real-time spatial information and precise access to the endophytic tumor through Brodel’s line. We and others have also found that intraoperative ultrasound during open PN may reveal additional findings such as satellite tumors, invasion into collecting system, or branched renal vein, not appreciated by preoperative cross-sectional imaging that may alter surgical management, minimize positive surgical margins,^{12, 29, 30} and facilitate a complete tumor resection.

Our series is limited by its relatively short oncological follow-up. However, we experienced no short-term recurrences or mortalities using the kidney split technique. We also note that the intent of our technical paper is simply to describe our outcomes using this open technique for complex endophytic renal tumors, rather than to directly compare the technique against other approaches, particularly given that only 3 kidney split procedures were performed using minimally-invasive approaches over the queried time period. Furthermore, although our analysis was limited to a contemporary cohort of patients who underwent the kidney split starting in 2015, our experience with the kidney split spans a considerably longer time frame. Prior to 2015, the use of this technique was not reliably reported in our renal cancer surgical database, and hence we did not include the earlier cases in this series. The decision to pursue PN over RN was based on a combination of factors including patient comorbidities, anticipated renal functional reserve, subjective assessment of renal parenchymal volume as a surrogate for ipsilateral function, and shared decision-making with the patient.

CONCLUSION

The kidney split through the avascular plane of Brodel’s line during open PN represents an effective approach to resect complex, endophytic renal tumors. In our series, this technique afforded acceptable perioperative outcomes with no Clavien-Dindo grade 4–5 complications, preserved renal function without the need for dialysis, and resulted in no short-term recurrences or mortality. Our experience also highlights the importance of adapting classical surgical techniques, using cold ischemia, and relying on preoperative and intraoperative ultrasonography to guide an effective and complex operation.

Supplementary Material

1

Supplementary Figure 1. Representative preoperative images illustrating a 2.4 × 1.9 x. 2.2 cm right-sided, solid, enhancing, completely endophytic, interpolar mass abutting the renal sinus fat, excised successfully using a kidney split open partial nephrectomy. Shown on computed tomography scan in (A) axial and (B) coronal views (black arrowheads). (C) Seen as a complex cystic lesion on renal ultrasound (white arrowheads).

2

Supplementary Figure 2. Intraoperative photographs of kidney split surgical technique. (A) Anatrophic kidney split through Brodel’s line, followed by (B) dissection of the tumor within the renal sinus and (C) further dissection of the tumor with the point of renal cortical attachment visualized.

HIGHLIGHTS.

• The kidney split represents an effective technique to resect complex, endophytic renal tumors.

• The kidney split affords acceptable perioperative outcomes, preserved renal function, and no short-term recurrences or mortality events.

• Classical surgical techniques, cold ischemia, and use of ultrasonography effectively guide this complex kidney-sparing operation.