1. INTRODUCTION

The increased use of imaging studies has led to an increase in the incidental diagnosis of renal masses. The 2019 European Association of Urology Guidelines on Renal Cell Carcinoma currently recommended partial nephrectomy (PN) as the standard of care for T1a lesions and most T1b lesions.1 PN minimizes the risk of chronic kidney disease and is associated with favorable oncologic outcomes, including excellent local control.2,3 Advances in minimally invasive surgery, including laparoscopic partial nephrectomy (LPN) and robotic-assisted partial nephrectomy (RAPN), have resulted in shorter hospital stay, improved cosmesis, and faster convalescence.4–6 Complication rates of PN range between 10% and 50%.7–12 The most frequent and potentially life-threatening adverse events associated with PN are hemorrhagic complications (HCs), which may require blood transfusion, angioembolization, and/or reoperation that can increase morbidity and the length of hospital stay as well as delay the patient’s return to normal activities.

The aim of this study was to analyze the risk factors for HCs after PN in patients who undergo RAPN.

2. METHODS 2. 1. Patient selection

We retrospectively reviewed the medical records of 260 patients who underwent RAPN between January 2010 and July 2018. RAPN was performed by a single urologist who had experience with performing more than 100 RAPNs. All patients were followed up for 1 month after the surgery. The study protocol was reviewed and approved by the ethics committee of Taipei Veterans General Hospital, Taiwan (IRB number: TPEVGH-IRB 2020-06-015AC). The decision to perform RAPN was based on the patient’s tumor characteristics, performance status, comorbidities, and surgical history.

Patients with renal angiomyolipoma, as diagnosed using preoperative imaging studies, were excluded. All patients received preoperative assessments of their hemoglobin and creatinine levels as well as estimated glomerular filtration rate using the modification of diet in renal disease formula. Concerning high bleeding risk in PN, all the patients with a history of cardiovascular disease were referred to the cardiovascular clinic for evaluation. The protocol for anticoagulant and antiplatelet discontinuation and resumption was according to the European Society of Cardiology (ESC) guideline.13 Patients with HCs resumed medication after resolution of HCs according to the surgeon’s decision. Antiplatelet medications and anticoagulants were not used in the perioperative period. Tumor characteristics, including tumor size, location, and vessel anatomy, were evaluated using preoperative imaging studies. Both the RENAL nephrometry score and PADUA score is a simple anatomical system that can be used to predict the risk of surgical and medical perioperative complications in patients undergoing open NSS (PADUA score) were calculated for analyses. Tumor complexity was classified using the RENAL nephrometry score: low complexity (Radius-scores tumor size as maximal diameter exophytic/endophytic properties of the tumor nearness of the deepest portion of the tumor to the collecting system or renal sinus anterior (a)/posterior (p) descriptor location relative to the polar line [RENAL score] between four and six), moderate complexity (RENAL score between seven and nine), and high complexity (RENAL score greater than nine or presence of hilar tumors).14 Postoperative hemoglobin level was recorded in the HC group. All patients underwent sonography and computerized tomography at 3 and 6 months, respectively, after the surgery for evaluation.

2. 2. Operative method

Several different techniques for RAPN have been reported.15 In this study, RAPN was performed via a transperitoneal or retroperitoneal approach depending on the tumor location or previous abdominal operation history. The principles of tumor resection were the same as those for open surgical methods. Briefly, the renal hilum was identified, allowing individual clamping of the renal artery and vein using bulldog clamps. In some cases, the renal artery was clamped alone. Intraoperative ultrasonography was used to identify the tumor margins. Cold scissor excision of the renal tumor was performed with minimal margins of the healthy renal parenchyma. The frozen sections were examined in case of any doubt.

Hemostasis with bolster sutures was performed after tumor resection, and gelatin-based sealants (FloSeal®, Baxter, floseal hemostatic matrix, North Largo, FL, USA) were applied to the renorrhaphy site. All intraoperative data, including the surgical approach, the decision on pedicle control, whether to clamp the renal artery and vein or the artery alone, the warm ischemic time, intraoperative estimated blood loss, and console time, were documented.

2. 3. Definition of HCs

HCs were defined as bleeding, hematoma, or arteriovenous fistula requiring hemostatic medication, blood transfusion, or therapeutic interventions. HCs were divided into the following three categories according to their time of onset: intraoperative (from the beginning of anesthesia to the end of the operation), postoperative (after the operation but during the hospital stay), or delayed (within one month after discharge). The severity of the HCs was graded according to the modified Clavien classification system,16 and only HCs with Clavien grade II or higher were included in the HC group. The management of all HCs was also documented. We also analyzed preoperative evaluation data, comorbidities, and perioperative outcomes as potential risk factors for HCs after RAPN.

2. 4. Statistical analysis

We used the Mann–Whitney U test to compare the continuous variables between groups and the chi-squared test to compare categorical variables. Multiple logistic regression analysis was used to identify the risk factors for HCs. Odds ratios (ORs) and 95% confidence intervals (CIs) were determined. Variables with p values <0.05 on the univariate analysis were included in the multivariate logistic regression model. A p value <0.05 was set as the threshold for statistical significance.

3. RESULTS

Of the 260 patients included in this study, 32 (12.3%) had HCs, which were intraoperative in 16 (6.2%), postoperative in six (2.3%), and delayed in 10 (3.8%). Overall, six HCs (2.3%) were treated using hemostatic medication, 17 (6.5%) required blood transfusion, two (0.7%) were treated using cystoscopic bladder irrigation, six (2.3%) were treated via angiographic embolization because of arteriovenous fistula formation, and one (0.4%) was treated using surgical reintervention to check for bleeding. All patients with intraoperative bleeding were treated using blood transfusion, and no conversion to open surgery or radical nephrectomy was necessary. According to the modified Clavien classification system, 23 HCs were grade II (8.8%), eight were grade IIIa (3.1%), and one was grade IIIb (0.4%). However, no complication-related deaths occurred. The HC group had significantly more essential blood loss (712.5 ± 518.4 vs 229.6 ± 212.3 mL; p < 0.001) and a significantly longer length of hospital stay (7.0 ± 2.2 days vs 5.6 ± 1.8 days; p < 0.001) than did the non-HC group. On comparing the preoperative and postoperative hemoglobin levels of the HC group, the postoperative hemoglobin level was significantly lower (13.4 ± 1.6 vs 11.7 ± 1.8 g/dL; p = 0.001). None of the patients showed any evidence of tumor recurrence during the imaging follow-up at 3 and 6 months after the surgery.

Table 1 summarizes the patient demographics and tumor characteristics. Patients were comparable for age, body mass index, preoperative hemoglobin level, renal function, and PADUA score. A preoperative history of diabetes mellitus was significantly associated with the occurrence of HCs (31.2% vs 16.2%; p = 0.04) and the HC group had significantly more complex tumors and a higher renal score than did the non-HC group (8.4 ± 1.7 vs 7.5 ± 1.7; p = 0.002). In addition, the sum of the renal size plus renal sinus involvement in the PADUA score was significantly higher in the HC group (p = 0.045).

Table 1 - Patient demographics and tumor characteristics No HCs (n = 228) HCs (n = 32) p Male 162 23 0.92 Female 66 9 Age (y) 59.6 ± 12.8 55.2 ± 14.0 0.07 BMI 26.0 ± 3.71 26.6 ± 4.7 0.54 Diabetes mellitus 37 (16.4%) 10 (31.2%) 0.04 Hypertension 104 (46.0%) 15 (46.9%) 0.93 Heart disease 18 (8.0%) 3 (9.4%) 0.73 Hemoglobin level (g/dL) 13.5 ± 1.5 13.6 ± 1.8 0.63 Creatine level (mg/dL) 1.1 ± 1.0 0.9 ± 0.3 0.51 eGFR (mL/min/1.73 m2) 82.3 ± 21.8 85.8 ± 21.9 0.44 Side 0.71  Left 110 (48.2%) 14 (43.8%)  Right 118 (51.8%) 18 (56.2%) Tumor size (mm) 36.7 ± 15.6 41.0 ± 13.6 0.13 PADUA score 8.8 ± 1.6 9.4 ± 1.6 0.08 RENAL score 7.5 ± 1.7 8.4 ± 1.7 0.002 Complexity 0.009  Low 59 (25.9%) 2 (6.3%)  Medium 147 (64.5%) 23 (71.9%)  High 22 (9.6%) 7 (21.8%)

Mann–Whitney U test was used to compare the continuous variables between groups while the chi-squared test was used to compare categorical variables.

BMI = body mass index; eGFR = estimated glomerular filtration rate; HCs = hemorrhagic complications; RENAL score = radius-scores tumor size as maximal diameter exophytic/endophytic properties of the tumor nearness of the deepest portion of the tumor to the collecting system or renal sinus anterior (a)/posterior (p) descriptor location relative to the polar line; PADUA score = simple anatomical system that can be used to predict the risk of surgical and medical perioperative complications in patients undergoing open NSS.

Table 2 lists the operative factors. The HC group had significantly longer console times (229.8 ± 94.7 vs 187.7 ± 65.9; p = 0.03) and warm ischemic times (22.4 ± 15.4 vs 34.4 ± 20.2; p < 0.0001) than did the non-HC group. The method of pedicle control was significantly associated with the occurrence of HCs (p = 0.014). However, no significant difference was observed in the surgical approach (transperitoneal or retroperitoneal) or the method of collecting system entry during the surgery between the two groups.

Table 2 - Operative factors No HCs (n = 228) HCs (n = 32) p Approach 0.62  Transperitoneal 218 (95.6%) 32 (100%)  Retroperitoneal 10 (4.4%) 0 Pedicle control 0.014  No 31 (13.6%) 1 (3.1%)  Artery 109 (47.8%) 12 (37.5%)  Artery + vein 88 (38.6%) 19 (59.4%) Collecting system entry 113 (49.8%) 19 (59.4%) 0.31 Console time (min) 187.7 ± 65.9 229.8 ± 94.7 0.03 Warm ischemic time (min) 22.4 ± 15.4 34.4 ± 20.2 <0.0001

Mann–Whitney U test was used to compare the continuous variables between groups while the chi-squared test was used to compare categorical variables.

HCs = hemorrhagic complications.

The results of the multivariate logistic regression analysis are shown in Table 3. The analysis revealed that a warm ischemic time >25 minutes was the only significant independent risk factor for HCs in patients who underwent RAPN (OR, 3.51; 95% CI, 1.28-9.59; p = 0.01).

Table 3 - Multivariate logistic regression analysis OR (95% CI) p Diabetes mellitus 2.17 (0.87–5.42) 0.10 Console time > 180 min 1.02 (0.40–2.59) 0.97 Warm ischemic time > 25 min 3.51 (1.28–9.59) 0.01 Complexity  Low - -  Medium 2.04 (0.41–10.31) 0.39  High 2.99 (0.45–19.74) 0.26 Pedicle control  No - -  Artery 1.40 (0.15–13.23) 0.77  Artery + vein 1.63 (0.17–15.89) 0.68

Multiple logistic regression analysis was used to identify the risk factors for hemorrhagic complications.

CI = confidence interval; OR = odds ratio.

4. DISCUSSION

PN is the standard treatment for clinical T1 renal tumors. Its oncological outcomes are comparable to those of radical nephrectomy and it reduces mortality associated with cardiovascular accidents.17 Owing to the advances in minimally invasive surgical techniques over the past decade, RAPN has become the mainstream surgical method for localized renal tumors because it has a relatively shorter learning curve than that required for LPN.18 RAPN also yields oncological outcomes comparable to those of open approaches or LPN.3–6,19–21 Previous studies have investigated the utility of RAPN in managing various characteristics of renal tumors and have reported good clinical outcomes.19,22,23

As the number of RAPNs performed increases, HCs remain the most common and potentially life-threatening adverse events. A review of the literature revealed that the incidence of HCs ranged from 0% to 30%.9,11,24 This wide variation in the incidence of HCs is probably due to the varying definitions of hemorrhage used in different studies. Some studies defined HCs as bleeding that required a blood transfusion,25 whereas some defined HCs as bleeding that necessitated therapeutic intervention.26 Some authors defined HCs on the basis of decreases in hemoglobin levels,27 and some included both clinical and biological hemorrhages.12 In addition, the time of HC occurrence was different, because while some studies included perioperative hemorrhage, some did not.28 These multiple definitions of HCs make it difficult to perform comparisons across studies.

In the present study, we defined HCs as bleeding, hematoma, or arteriovenous fistula requiring hemostatic medication, blood transfusion, or therapeutic intervention. The rate of HCs was 12.3% (n = 32). Fardoun et al12 reported a higher rate of HCs up to 20%. Their patient group included those who underwent both open and minimally invasive PN. Notably, their definition of HCs also included a decrease in hemoglobin level >3 g/dL. In the present study, we focused only on RAPN and HCs were defined on the basis of an unstable hemodynamic status or clinical symptoms indicating bleeding. Moreover, we only included HCs with Clavien grade II or higher. Postoperative hemoglobin levels significantly decreased in the HC group, and this was compatible with the clinical finding. This may be considered a better reflection of the actual conditions in the clinical setting.

The influence of comorbidities on HCs remains controversial. Most previous studies investigated the association between comorbidities and overall complication rates. Some studies demonstrated that complications after RAPN are associated with comorbidities or the performance status.29,30 Conversely, other studies did not find such an association.11,12 Khene et al29 found that Charlson’s comorbidity index was significantly associated with overall complications in a multivariable analysis, but cardiovascular disease was the only significant factor associated with major complications (Clavien score ≥ 3). Bauman et al30 demonstrated that cerebrovascular disease and chronic obstructive pulmonary disease could predict complications after RAPN. Fardoun et al12 found that comorbidities did not correlate with HCs in patients who underwent PN. In the present study, patients were comparable for age, body mass index, preoperative hemoglobin level, and renal function, and a preoperative history of diabetes mellitus was significantly associated with the occurrence of HCs (31.2% vs 16.2%; p = 0.04). However, in our multivariate analysis, no significant differences were observed in comorbidities between patients with HCs and those without. The explanation for this remains unclear.

Tumor characteristics may also impact the outcomes of RAPN. Previous studies have reported conflicting results regarding the influence of tumor complexity, as represented by the RENAL nephrometry scores. While some studies found an association between nephrometry scores and complications after RAPN,7,11 others failed to demonstrate this association.12,24,31,32 Previous studies also investigated tumor features included in the RENAL nephrometry scores, such as tumor size and tumor growth pattern, which may be independently associated with HCs. Cacciamani et al31 conducted a meta-analysis to evaluate the impact of host factors on RAPN outcomes and found that neither tumor size nor the presence of a hilar tumor could predict overall complications. In their study, although the endophytic tumor group had less postoperative complications, the exophytic tumor group had a larger tumor size and older age. Komninos et al32 reported no significant difference in the complication rates between patients with complete endophytic renal tumors and those without. Mari et al24 conducted a multicenter prospective study to assess predictors of complications after PN, but they found that none of the nephrometry tumor features significantly predicted surgical complications. Instead, they found that comorbidities and the surgical approach played a significant role in the occurrence of postoperative complications. Fardoun et al12 also analyzed the predictive factors for HCs and reported that tumor complexity was not an independent factor associated with HCs. In the present study, the univariate analysis showed that the HC group had significantly higher RENAL nephrometry scores, while in the multivariate analysis, no significant difference was observed in the RENAL nephrometry scores between patients with and without HCs. We postulated that the higher RENAL nephrometry scores implied that the surgical techniques were more challenging during the RAPN, but these could not directly affect the occurrence of HCs.

Several studies investigated the effect of surgical factors on RAPN-associated complications. Tanagho et al11 reviewed complications of RAPN at five centers in the United States and found that the complication group had significantly increased warm ischemic times and increased operative times, but the hilar clamping method made no significant difference. However, operative factors were not significant in the multiple logistic regression analysis. Cacciamani et al21 conducted a comprehensive meta-analysis to critically evaluate the impact of surgical factors on the operative, perioperative, functional, oncologic, and survival outcomes in patients undergoing RAPN. They found that RAPN had outcomes mostly superior, and at a minimum equivalent, to those of open and laparoscopic PN. In their analyses of surgical factors, they found that the transperitoneal and retroperitoneal approaches had similar complication rates. They also found that the various techniques of hilar control, including off-clamp, selective or superselective clamp, and early unclamp, had complication rates and oncological outcomes similar to those of main artery clamping. Fardoun et al12 also reported that the clamping method and warm ischemic time were not associated with HCs and that the surgical technique used had no effect on HCs. In contrast, the present study only focused on HCs in patients who underwent RAPN. Our multivariate analysis revealed that a warm ischemic time >25 minutes was the only significant risk factor for HCs, which may imply that prolonged warm ischemic time may indicate more challenging or difficult surgical techniques.

The current study had some limitations. First, it had a retrospective and single-center design, which may have resulted in the selection of patients with more complex tumors or comorbidities and may reflect the experience of the single operator. Second, we only used the RENAL nephrometry scores to evaluate tumor complexity. Third, only HCs with Clavien grade II or higher were included in the HC group, and the postoperative hemoglobin level was checked only when the patient experienced HCs. The absence of postoperative hemoglobin level measurements from all patients may have resulted in the exclusion of patients with HCs who are not symptomatic. Additionally, our study only followed patients for 1 month after their RAPN and imaging follow-up was performed only at 3 and 6 months after the surgery. Further studies evaluating long-term complications are warranted.

Patients who undergo RAPN with a warm ischemic time >25 minutes are significantly more likely to have HCs and should hence be carefully monitored during their perioperative follow-up.

ACKNOWLEDGMENTS

The authors thank Howard En-Hao Tien for his valuable statistical assistance.

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