Introduction

Partial nephrectomy (PN) is typically recommended for the management of localized T1 renal tumors [1]. In the long term, PN may potentially reduce the occurrence of cardiovascular disease, slow the progression to end-stage renal disease (ESRD), and decrease the necessity for hemodialysis [2, 3]. An essential step in conventional PN is renal artery control. However, transient interruption of arterial blood flow might lead to ischemic renal parenchymal injury [4]. Studies have shown a correlation between extended warm ischemia time (WIT) and both the amount of conserved renal tissue and the onset of postoperative renal damage after PN with segmental artery clamping [5, 6]. Under the guidance of dual-source computed tomography (DSCT) angiography, the precision of the segmental artery clamping technique has been enhanced in tumor removal and preservation of normal renal parenchyma [6]. However, this approach requires microdissection of the renal hilum, leading to increased bleeding volume and a high conversion rate [5].

Endovascular balloon occlusion is an effective modality to ensure a bloodless operative field distal to the plane of occlusion, thereby enhancing the efficacy of various surgical interventions [7, 8]. PN with endovascular balloon occlusion has been previously reported [9, 10]. Nevertheless, the occlusion procedure is typically performed under digital subtraction angiography (DSA) guidance and therefore relies on the utilization of intricate digital subtraction angiography equipment. Subsequently, patients are required to be transformed to the laparoscopic or robotic operation room for the surgical procedure, which entails the potential hazard of balloon displacement [9]. The ultrasound-guided renal artery balloon catheter occlusion hybrid partial nephrectomy (UBo-HPN) technique allows for arterial occlusion and tumor excision in the same robotic operating room without the need for dissection of the renal hilum’s vascular structures(unpublished). This method is particularly beneficial for patients with a history of prior surgery, as it circumvents the need for renal hilum dissection, thus minimizing surgical complexity and the associated risks of vascular damage [11]. UBo-HPN with branch renal artery occlusion could skip the most difficult and risky stage of renal artery branch microdissection. In this single-arm prospective trial, we aimed to evaluate the clinical data of patients underwent UBo-HPN with branch renal artery occlusion.

Materials and methods

Subjects

The study design was a single-arm pilot design. The inclusion and exclusion criteria are set as follows: Inclusion Criteria: (a) Patients with renal tumors at T1N0M0 stage, as confirmed by imaging examination, according to the 2007 renal cell carcinoma guideline [12]; (b) Patients aged between 20 and 85 years; (c) CTA imaging reveals that the tumor is vascularized by a single branch of the renal artery. Exclusion Criteria: (a) Patients with renal tumors near the renal hilus or invading the renal sinus area, which may require simultaneous blockade of the renal vein during tumor resection; (b) Patients whose tumor is supplied by multiple arteries and is difficult to occluded with a single balloon; (c) Patients with severe underlying cardiovascular and cerebrovascular diseases, particularly those with large vascular lesions, aneurysms, or severe atherosclerosis in the renal arteries. From August 2021 to July 2023, 20 patients diagnosed with renal tumors underwent robotic-assisted partial nephrectomy (RAPN) with the application of the renal artery branch occlusion technique. Clinical data for patients who underwent UBo-HPN with branch renal artery occlusion were prospectively collected. The research was granted approval by the ethical committee of Tongji hospital of Tongji medical college and was registered on chictr.org.cn (registration number ChiCTR2100050808). All participants grovided informed consent. All surgeries were performed by an experienced surgeon (H.L.). Computed tomography angiography (CTA) was performed preoperatively to determine the segmentation of the renal vasculature. The artery identified by CTA was designated as the target artery, which is the first-order branch of the renal artery supplying the tumor.

Surgical methods

  1. 1)

    The surgical procedures were performed employing the Intuitive Surgical DaVinci Si or Xi system (Intuitive Surgical, Sunnyvale, CA, USA). After the administration of general anesthesia, patients were positioned in the conventional lateral decubitus position, adjusted to an approximate 70-degree tilt. Transperitoneal approach was applied in all cases. Five ports (12 mm port for the optic, two 8 mm ports for robotic instruments, one 10 mm and one 5 mm ports for the assistant) are placed in a classical configuration.

  2. 2)

    The tumor was routinely localized using laparoscopic ultrasound (LUS) (UST-5550, Hitachi Aloka Medical, Japan). After the perirenal fat surrounding the renal tumor was dissected under robotic laparoscopy, a 5.5 F guiding catheter was inserted into the femoral artery through a puncture channel. Under continuous real-time monitoring with laparoscopic ultrasound, the catheter was advanced through the external iliac artery, iliac artery, and abdominal aorta until it reached the opening of the renal artery.

    With the aid of the guiding catheter, a 0.035-inch ultraslippery guidewire was placed into the renal artery or its specific branches, which were preliminarily identified via CTA and confirmed intraoperatively using laparoscopic ultrasound. The guidewire was then advanced into the target artery under continuous laparoscopic ultrasound monitoring. Following this, a Fogarty balloon catheter was inserted along the guidewire until the balloon reached the target location. The balloon was inflated with an appropriate amount of saline to occlude the renal blood supply. Unlike conventional partial nephrectomy, this procedure did not require dissection of the renal hilum.

  3. 3)

    Ensuring safety and mitigating the risk of significant hemorrhage were crucial components of this process. Confirmation of successful occlusion included: (A) continuous monitoring showing the disappearance of the CDFI blood flow signal; (B) CE-LUS showing no enhancement compared to the pre-inflation image (this step is optional). When branch occlusion was inadequate to fully occluded the tumor’s blood supply, the balloon can be withdrawn to the main renal artery to ensure complete occlusion.

  4. 4)

    The tumor border was subsequently dissected using cold scissors without the need for dissection of the renal hilum vessels. Additionally, a vacuum aspirator was introduced between the tumor and the tumor bed to facilitate blood aspiration. Following the thorough removal of the tumor, sutures were routinely employed for both the renal medulla and parenchyma.

  5. 5)

    Following the deflation of the balloon catheter, renal blood flow was successfully reinstated, and further inspection of the kidney was conducted to assess hemostasis. Subsequently, the arterial sheath was retracted, and a vascular closure device, Angio-Seal, was employed to effectively occlude the puncture site in the femoral artery. Protamine was administered in appropriate quantities based on the predicted volume of remaining heparin.

Postoperative management and follow-up

Postoperative blood routine and biochemical tests were performed, and the patients’ vital signs and abdominal drainage were observed and documented. The levels of estimated glomerular filtration rate (eGFR) were routinely assessed at two time points: 48 h post-operation and one month following the patient’s discharge. A subset of patients continued to be examined at follow-up visits. Thereafter, the patients underwent regular follow-up examinations, including renal computed tomography (CT) or magnetic resonance imaging (MRI), and blood biochemistry analysis, which were conducted at three-month intervals.

Results

Surgical success rate and perioperative outcomes

Table 1 summarizes patient/tumor characteristics. The mean age of patients was 55 yrs, and the mean BMI was 23.63 kg/m2, with a median R.E.N.A.L. score of 6 (range: 5–7). All 20 patients underwent successful surgeries. No patients required simultaneous occlusion of multiple segmental renal arteries. In 19 out of 20 cases (95%), satisfactory ischemic regions were achieved with ultrasound-guided renal artery branch balloon catheter occlusion. In one patient, after occlusion of branch artery and before surgical resection, CDFI showed that blood supply still existed in the tumor area. Therefore, the balloon catheter was retreated to the main renal artery for occlusion. Recheck of CTA confirmed the presence of a tiny accessory renal artery supplying the tumor area. In addition, none of the cases required conversion to open surgery.

Table 1 Patients and tumors characteristics
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Perioperative characteristics are listed in Table 2. The mean total operative time was 95.8 min. The mean operative time for vascular intervention was 21.25 min and mean WIT was 20.35 min. None of the patients developed postoperative acute renal injury. The median eGFR preservation percentage at postoperative 48 h, 30 days, and the latest follow-up were 87.52%, 91.47%, and 92.2%, respectively. Median EBL was 50 ml (range: 20–300 ml).

Table 2 Surgical and pathological outcomes
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Perioperative complications and follow-up

The incidence of complications overall was 5%. One patient experienced skin bruising at the femoral artery puncture site, which resolved spontaneously within a week. No patients experienced substantial bleeding, acute renal failure, or other severe complications. In all cases, no vascular complications, including dissection, thrombosis, or occlusion of the artery were observed.

Discussion

During PN, the preservation of as much renal function as possible assumes paramount significance [13, 14]. Therefore, the adverse effect of warm ischemia (WI) injury on renal function continues to be a core concern [4, 15, 16]. Although clamping of the renal artery can provide better intraoperative visualization, bleeding control, this approach inevitably results in global renal WI injury [17]. In light of this, researchers have implemented several strategies to mitigate WI injury. The strategy of segmental artery clamping could minimize post-PN renal function decline while achieving a relatively bloodless surgical field [18,19,20,21,22]. However, this strategy resulted in a higher rate of vascular injury [6]. In addition, the dissection of the renal hilum during this procedure increased the possibility of elevated intraoperative hemorrhage, And the extent of bleeding was directly proportional to the number of branches that were clamped [6]. Hence, its applicability and generalizability were limited.

In consideration of this, we have developed a novel renal artery branch occlusion technique. The primary distinction from traditional renal artery branch clamping methods was that it did not require the dissection of renal hilum vessel branches. Herein, we presented the preliminary results of a single-arm cohort study, which includes the initial 20 cases.

Previous findings indicated that for RAPN, the complication rate of Clavien-Dindo Grade III or higher varied from 2.6–5.8% [23, 24], with an overall frequency as high as 26% [25]. In comparison, the results of our study showed a significantly lower complication rate. Only one case of interventional complication with localized bruising occurred and was resolved with conservative treatment.

All 20 cases in this study were completed successfully with one balloon catheter, with only one case requiring conversion to balloon occlusion of the main renal artery. Notably, there were no instances of conversion to open or radical nephrectomy. The conversion rate was lower than the reported rate of 6.6% for open conversion and 8% for radical resection in the context of selective or super-selective clamping, which indicated a higher technical success rate for renal artery branch occlusion in UBo-HPN.

A lower EBL was also demonstrated by our research compared to previous reports, primarily attributed to the technical advantage of UBo-HPN renal artery branch artery with circumvent of the renal hilum dissection [26,27,28,29]. Notably, when dealing with renal tumors on the anterior side of the kidney, tumor resection can be achieved by minimizing or partially repositioning the colon. This technique can minimize the inherent intraperitoneal trauma caused by traditional clamping method. Consistent with previous reports, our study revealed an average WIT of 20.35 min. The surgical process also demonstrated effective branch occlusion. Although UBo-HPN did not exhibit a significant advantage in reducing warm ischemia time, it can be considered, at the very least, non-inferior to selective clamping [30]. In addition, the eGFR preservation rates at 48 h, 30 days, and the latest follow-up after the operation were 87.52%, 91.47%, and 92.2%, respectively. These reductions were comparable to previously reported decreases in eGFR. However, this may be due to the inclusion of cases with smaller tumor size in this study and the use of eGFR as the metric for assessing renal function [31].

In comparison to branch clamping of RAPN, UBo-HPN with branch occlusion of the renal artery provided a renal function preserving maneuver for patients with a solitary kidney or impaired renal function. This is attributed not only to the selective interruption of blood flow enabled by segmental artery occlusion, preserving the blood supply to other segments, but also to the fact that the absence of renal hilum dissection virtually eliminates the risk of damage to the renal hilum. Overall, UBo-HPN can serve as an effective alternative to RAPN in certain scenarios.

Several limitations are inherent in our research. Firstly, our study lacked a parallel control group. Secondly, eGFR was used to assess changes in renal function of patients [32]. Future study with increasing the number of participants and extending follow-up period was expected.

Conclusion

UBo-HPN with branch occlusion of the renal artery proved to be a safe and efficient technique for RAPN, leading to decreased intraoperative hemorrhage. Incidences of vascular intervention-related complications were diminished. The incidence of complications was decreased in comparison to selective clamping technique. Functional and oncologic outcomes required further investigation.