Surgical innovation revisited: A historical narrative of the minimally invasive “Agarwal sliding‐clip renorrhaphy” technique for partial nephrectomy and its application to an Australian cohort

Abstract Objective To evaluate local clinical outcomes of sliding clip renorrhaphy, from inception to current utilization for open, laparoscopic, and robotically assisted partial nephrectomy. Methods We reviewed prospectively maintained databases of three surgeons performing partial nephrectomies with the sliding‐clip technique at teaching hospitals between 2005 and 2019. Baseline characteristics, operative parameters, including surgical approach, RENAL Nephrometry Score, and post‐operative outcomes, including Clavien‐Dindo classification of complications, were recorded for 76 consecutive cases. We compared perioperative and 90‐day events with patient and tumor characteristics, stratified by operative approach and case complexity, using Wilcoxon rank‐sum test for continuous variables and the Chi‐squared or Fisher's exact test, for binary and categorical variables, respectively. Results Open surgery (n = 15) reduced ischemia time and operative time, but increased hospital admission time. Pre‐ and post‐operative estimated glomerular filtration rates did not change significantly by operative approach. Older patients (P = .007) and open surgery (P = .003) were associated with a higher rate of complications (any‐grade). Six grade ≥3 complications occurred: these were associated with higher RENAL Nephrometry Score (P = .016) and higher pathological tumor stage (P = .045). Limits include smaller case volumes which incorporate the learning curve cases; therefore, these data are most applicable to lower volume teaching hospitals. Conclusion The sliding‐clip technique for partial nephrectomy was first described by Agarwal et al and has low complication rates, acceptable operative time, and preserves renal function across open and minimally invasive surgeries. This series encompasses the initial learning curve with developing the technique through to present‐day emergence as a routine standard of practice.


| INTRODUC TI ON
In 1870, Gustav Simon performed the first partial nephrectomy. 1 For the next century, the procedure was confined to obscurity, largely reserved for patients with solitary kidneys, compromised renal function, and bilateral renal masses. This was due to concerns regarding local recurrence from multifocal malignant renal tumors and morbidity associated with intraoperative and delayed hemorrhage. 2 The advent of computed tomography (CT) increased the incidence of asymptomatic small renal masses, aided pre-operative planning, and increased the utilization of the partial nephrectomy. 3 The only randomized control trial comparing partial and radical nephrectomy between 1992 to 2003 demonstrated that partial nephrectomy had improved long term renal function, reducing the incidence of stage 3a and 3b chronic kidney disease; however, for patients with renal cell carcinoma (RCC), there was no difference in local recurrence, cancer-specific survival or overall survival. 4,5 Notably, severe hemorrhages and reoperations were significantly higher in the partial nephrectomy arm. 6  The technique prevents the cheese-wire effect (when parenchyma is lacerated as sutures are placed under tension), maintains tension on the suture material to ensure sustained parenchymal compression and hemostasis, and negates the need for slower intracorporeal knot tying. An initial clip is slid down the outer layer suture with a second clip then applied at the hinge aspect to lock it in place.
The sliding-clip technique for renorrhaphy has become widely utilized in open, laparoscopic, and robotic approaches. [8][9][10] The technique has been adapted, but the fundamental sliding and clipping technique remain common throughout all operative approaches as first described by Agarwal et al. 7 Today, partial nephrectomy is the recommended surgical approach for T1 renal tumors, particularly those <4 cm (T1a), and is increasingly favored for managing complex renal masses. [11][12][13] Herein, we describe an Australian experience of partial nephrectomy using the sliding-clip renorrhaphy technique, from inception to present-day utilization. Patient demographics, perioperative sequelae, and pre-operative and post-operative estimated glomerular filtration rate (eGFR) were all recorded. All patients underwent an abdominal CT scan with 3-mm axial slices to delineate characteristics of tumor location, depth, and proximity to the collecting system. Tumor complexity was defined as low (4-6 points), intermediate (7-9 points) or high (10-12 points), using the RENAL Nephrometry Score. 14 A thorough chart review was undertaken for each patient to identify 90-day complications. As Australian patients are both operated on and managed postoperatively in the same health network, most postoperative complications were likely to be identified. Postoperative complications were then graded using the Clavien-Dindo classification. 15

| Intervention
Across the cohort, the surgical approach varied depending upon tumor size and location. Pre-operatively, each case was discussed at a multidisciplinary team meeting, where urologists formed a consensus on the indication and strategy for excising the tumor.
Tumors located anteriorly and antero-laterally were approached by transperitoneal laparoscopic approach. Posterior tumors were approached with a retroperitoneal laparoscopic approach. An open approach was used in select patients where laparoscopic approach was considered difficult. Over time, robotically assisted surgeries were used more frequently.
Nonetheless, the principles of surgery were the same in all approaches: first, the hilum and tumor were exposed. The tumor was circumscribed with a safe normal renal parenchymal margin using diathermy, and intraoperative ultrasound was used for all lesions to help identify an adequate excision margin. Next, the renal artery and, in select cases, the renal vein, were clamped using bull dog clamps   The only independent covariates associated with any-Clavien-Dindo grade complications were older patients (P = .007), open surgery (P = .003), and longer total length of stay (P < .001) (Figure 2). Blood transfusions were associated with older patients (P = .033) and lower day one post-operative eGFR (P = .043), likely reflecting intraoperative volume depletion. Major complications were associated with a higher median RENAL Nephrometry Score (9 vs 6; P = .016) and, among the malignant tumors, major complications were also associated with a higher proportion of pT stage > T1a tumors (50% vs 13%; P = .045), also likely reflecting the greater intraoperative complexity.

| D ISCUSS I ON
Our case series encompasses the initial learning curve through to present-day routine standard of practice using the sliding-clip technique for renorrhaphy partial nephrectomy. Presently, partial nephrectomy is the gold standard for excising pT1a renal tumors and increasingly larger, more complex renal masses. 13 Aside from the debate about oncological equivalency to radical nephrectomy, the main concern previously restricting the uptake of partial nephrectomy was morbidity associated with achieving hemostasis and urinary leaks. The sliding-clip renorrhaphy technique and its variations have assisted in improving safety and outcomes therein. Despite including the first-in-human cases, we report low overall rates of transfusions when utilizing the sliding-clip. Only   or non-bolstered horizontal mattress closure of the capsule 26 or even omitting to close the cortex. 27 A trial randomising patients to double-layer or medullary renorrhaphy alone is currently accruing with preliminary results potentially suggesting that the closure of the deep-layer alone may be superior. 28 Furthermore, these variations may also impact longer term total renal volume loss. 29 Incorporation of these elements when undertaking sliding-clip renorrhaphy may further improve the safety and utility of partial nephrectomy for managing renal masses. Nonetheless, each of these adaptions retains the central sliding and clipping component.

| CON CLUS ION
After 150 years of incremental improvement, the partial nephrectomy for T1 renal tumors has emerged as the gold standard treatment. The widespread adoption of nephron-sparing surgery is predominantly due to reduced perioperative morbidity and preserved long-term renal function. While larger partial nephrectomy studies in the literature describe how the sliding-clip technique for renorrhaphy facilitates effective hemostasis and shortens ischemia time, this paper serves to provide a historical perspective by describing the first-in-human experience. Furthermore, the study demonstrates how the technique, which is steadily being promulgated within the urology community, was safely applied in lower volume teaching hospitals. Finally, this experience demonstrates that ingenuity from a single institution can lead to changes in practices worldwide.

ACK N OWLED G EM ENTS
Nicholas Howard: Clinical Research Coordinator, Department of Urology, Royal Melbourne Hospital.