Introduction

Recently, there has been a growing body of evidence suggesting that partial nephrectomy (PN) is a viable option for treating localized renal cell carcinoma, offering oncological outcomes equivalent to those of radical nephrectomy [1]. In addition, PN is associated with better preservation of renal function, which may lower the risk of cardiovascular disease and translate into improved overall survival [2]. With the advent of robotic-assisted surgery, the conservative management of renal masses has been extended to include clinical T2 tumors with favorable oncological outcomes [3]. Despite these advantages, PN remains a challenging procedure with a non-negligible risk of perioperative complications [4]. To assess this, the RENAL nephrometry score and the Preoperative Aspects and Dimensions Used for an Anatomical (PADUA) score have been developed as assessment tools to predict surgical complexity, including postoperative complications or warm ischemic time (WIT) [5, 6]. These evaluation systems consider various factors, such as tumor size, location relative to polar lines, and exophytic/endophytic characteristics, to plan the most appropriate surgical procedure for the patient.

Over time, the surgical technique for PN has evolved from open PN (OPN) to laparoscopic PN (LPN) and then to robotic-assisted PN (RAPN), with the use of RAPN increasing steadily with the diffusion of the da Vinci Surgical System [7]. RAPN has expanded the spectrum of indications for PN, particularly in large and complex tumors, with its advantages of more convenient tumor excision and renorrhaphy [8, 9]. However, for some tumors, OPN may still be the preferred surgical method depending on the situation. Currently, there are few differences in perioperative and postoperative functional outcomes between OPN and RAPN, especially in complex renal masses.

This systematic review summarizes recent research on the differences in perioperative and functional outcomes between OPN and RAPN for complex renal masses.

Methods

This systematic review and meta-analysis were conducted as per the PRISMA statement [10] (Fig. 1).

Fig. 1
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PRISMA flow diagram for the systematic review

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Literature search strategy, study selection, and data collection

We conducted a systematic electronic literature search in March 2023 in PubMed, Embase, Web of Science, and Cochrane Library database. Intervention and patient-related search terms were combined to build the following search string: (complex renal tumor or renal mass) and (open partial nephrectomy) and (Robotic Surgical Procedures or Robotics or Robot-assisted). The search was limited to English. Inclusion criteria were defined using the PICOS approach. P (patients): All the patients were found to have renal mass or renal tumor; I (intervention): undergoing OPN; C (comparator): RAPN was performed as a comparator; O (outcome): one or more of the following outcomes: perioperative outcomes, functional outcomes; S (study type): prospective comparative, retrospective studies or randomized control trials. Exclusion criteria: (1) noncomparative studies; (2) editorial comments, meeting abstracts, case reports, book chapters, or studies reporting experimental; (3) none of the defined outcome measure analysis. (4) RENAL score < 9 or PADUA score < 10.

Two reviewers individually extracted data from the included studies. Data extracted for individual study included: (1) general information related to the article: first author, country, year of publication; (2) population characteristics: sample size, age, body massindex (BMI), tumor size, preoperative estimated glomerular filtration rate (eGFR); Charlson’s comorbidity index (CCI) score; the number of patients with solitary kidney;renal tumor surgical score (3) perioperative outcomes: operative time, blood loss, hospital stay (4) overall complications (defined as Clavien grade ≥ 1), minor complications (Clavien < 3), major complications (defined as Clavien grade ≥ 3); transfusion rate; ischemia time and ischemia type (5) functional outcomes: eGFR decline from baseline (tow studies as sessment time of postoperative eGFRs were not clear [17, 18]) (6) oncologic outcomes: Positive surgical margins (PSMs), Stage at final pathology (pT). Any dispute was resolved by consensus or consultation with a third reviewer.

Assessment of risk of bias

Among the studies, ROBINS-I was applied to determine [11] bias due to (1) confounding, (2) selection of participants, (3) classification of exposures, (4) departures from intended exposures, (5) missing data, (6) measurement of outcomes,and (7) selection of the reported result.

Statistical analysis

Meta-analyses were performed using odds ratios (ORs)for dichotomous outcomes, while weighted mean differences (WMDs) were used for continuous outcomes. The results were reported with 95% confidence intervals (CIs). Meta-analyses of dichotomous variables were pooled using the Mantel–Haenszel method, and continuous variables were performed using the inverse variance method. Taking account of predictable substantial between-trial heterogeneity, a random-effects model was used to combine all summary data. Review Manager V5.4 software (Cochrane Collaboration, Oxford, United Kingdom) was used for result synthesis. Heterogeneity across the included studies was assessed using the I2 statistic [12]. p values of < 0.05 were regarded as statistically significant. Data that could not be measured by meta-analysis were presented narratively.

Subgroup analysis

We performed a subgroup analysis based on the different ischemia type for this comparison: cold ischemia and warm ischemia. Subgroup analysis was performed on the difference between postoperative eGFR and baseline. There were two studies that included cold ischemia and warm ischemia in the literature sample [15, 16], but due to the small sample size of Beksac et al. [15]. Only the data of Garisto et al. [16] were collected.

Sensitivity analysis

We performed sensitivity analyses to assess the robustness of the estimates according to the size of the study cohort (excluding studies with < 150 patients) and applied the leave-one-out method to exclude studies one at a time from the pooled effect. However, sensitivity analyses were not performed when comparing three or fewer studies.

Publication bias

Because the test power was lacking when ten or fewer studies were included, we could not evaluate the publication bias [13, 14].

Results

Study characteristics

After preliminary screening and full-text review, we included 936 patients in 5 studies for meta-analysis (Fig. 1) [15,16,17,18,19]. Table 1 summarizes the key characteristics of the included articles, including the first author's name, publication year, geographic region, article type, sample size, surgical route, and Newcastle–Ottawa Scale (NOS) score, Table 2 summarizes the number and baseline demographics of the included patients having each intervention and their associated preoperative variables (age, BMI, gender rate, preoperative tumor size, Preoperative eGFR, CCI score, the number of patients with solitary kidney, and renal tumor surgical scoring system score). The baseline characteristics of the number of patients with solitary kidney were not relatively equal in one study (there were 10 (13.2%) patients with solitary kidney in OPN and 1 (16.%) in RAPN, respectively). However, the preoperative demographics were comparable in other studies, with similar age, BMI, gender rate, preoperative tumor size, Preoperative eGFR, CCI score observed in each of the included studies. Perioperative outcomes are summarized in Table 3.

Table 1 Characteristics of included studies
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Table 2 The number of patients included in the five original articles and their baseline demographic characteristics
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Table 3 Details of perioperative outcomes of five articles
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For pathological and functional outcomes, the positive surgical margin (PSM) and stage at final pathology (pT) were documented in four articles, with the pathological grade referring to the grade of the malignant tumor. Four studies reported on the follow-up of the eGFR after one year. The pathological and functional outcomes of all the literature reviewed have been documented in Table 3.

Assessment of quality

No prospective studies comparing OPN vs RAPN were identified. Instead, all included studies were retrospective comparative studies conducted from 2018 to 2022. Overall, these five studies had a moderate risk of bias, as assessed by the Newcastle–Ottawa Scale (NOS) score.

Outcome analysis

Perioperative outcomes and complications. In the meta-analysis, it was observed that OPN had a slightly shorter operating time than RAPN (pooled from five studies; WMD − 10.77 min, 95% CI − 18.49 to − 3.05, p = 0.006) [15,16,17,18,19] (Fig. 2A). However, OPN patients had a longer hospital stay (four studies; WMD 1.64, 95%CI 1.17–2.11, p < 0.00001) [15, 16, 18, 19] (Fig. 2B). There was no statistically significant difference in blood loss between OPN and RAPN (four studies; p = 0.08) [15, 16, 18, 19] (Fig. 2C). Additionally, the ischemia time during surgery did not show any significant difference between the two approaches (five studies; p = 0.06) [15,16,17,18,19] (Fig. 3A). When comparing only studies that reported on warm ischemia time (WIT), there was still no significant difference (three studies; p = 0.81) [15,16,17,18,19]. RAPN required less intraoperative or postoperative blood transfusion (five studies; OR 2.64, 95% CI 1.39–5.02, p = 0.003) [15,16,17,18,19] (Fig. 3B). The overall complication rates were 28.2% (118 out of 419 cases) for OPN and 21.5% (111 out of 517 cases) for RAPN, respectively. OPN had a higher incidence of complications than RAPN (five studies; OR 1.72, 95% CI 1.21–2.45, p = 0.002) [15,16,17,18,19] (Fig. 3C), and the occurrence of major complications (Clavien ≥3) was also higher in OPN (from five studies; OR 1.76, 95% CI 1.11–2.79, p = 0.02) [15,16,17,18,19] (Fig. 4A). However, no statistical significance was found in minor complications (Clavien<3) (five studies; p = 0.15) [15,16,17,18,19] (Fig. 4B).

Fig. 2
figure 2

Forest plot of meta‐analysis of the following variables: A operative time, B hospital stay, C estimated blood loss, CI confidence interval; df degrees of freedom; IV inverse varianc; SD standard deviation

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Fig. 3
figure 3

Forest plot of meta‐analysis of the following variables: A ischemia time, B transfusion, C overall complication, CI confidence interval; df degrees of freedom; IV inverse varianc; M‐H Mantel‐Haenszel; SD standard deviation

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Fig. 4
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Forest plot of meta‐analysis of the following variables: A major complications (Clavien ≥ 3), B minor complications (Clavien < 3), C PSM positive surgical margins, CI confidence interval; df degrees of freedom; M‐H Mantel‐Haenszel

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Pathological and functional outcomes In cases of warm ischemia, there was no statistical significance in the comparison of eGFR decline between OPN and RAPN (pooled from three studies; p = 0.43) [17,18,19] (Fig. 5). Similarly, there was no statistical significance in positive surgical margins (PSM) (four studies; p = 0.13) [15, 16, 18, 19] (Fig. 4C).

Fig. 5
figure 5

Forest plot of meta‐analysis of the following variables: eGFR decline from baseline, CI confidence interval; df degrees of freedom; IV inverse varianc, SD standard deviation

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Heterogeneity

Most of the outcomes exhibited moderate to high heterogeneity. Low heterogeneity was found for PSM, overall complications, major complications, and operative time. However, it may be misleading to assume that the heterogeneity of these results was low because the I2 has a substantial bias when the number of studies is small [20].

Discussion

Partial nephrectomy has been shown to reduce renal function impairment while yielding no difference in oncological outcomes, including better long-term survival, when compared to radical nephrectomy [21, 22]. When assessing the best PN approach, three objectives are considered: (a) minimizing perioperative complications, (b) completely removing the tumor, and (c) maximizing the preservation of remaining renal function. The previously proposed “trifecta”, “margin, ischemia, and complications (MIC)” and other combined outcomes were all based on these three objectives [23]. For decades, the open approach has been the standard for performing PN. However, with advancements in minimally invasive surgery, LPN has rapidly gained interest for localized renal cell carcinoma due to its reduced invasiveness. Nonetheless, given that LPN is a challenging procedure, robot-assisted surgery now represents a valuable alternative, particularly for more complex tumors. Features such as improved dexterity, three-dimensional optics, a high-definition camera, and tremor filtration allow the surgeon to perform more precise excision and renorrhaphy. A meta-analysis by Aboumarzouk et al. compared LPN to RAPN [24], and the latter was found to offer significantly reduced warm ischemia time, making it a feasible and safe alternative to its laparoscopic counterpart. Additionally, other reports have shown satisfactory outcomes in the application of RAPN for larger (> 7 cm) and more complex tumors [25, 26]. Therefore, the robotic surgical system has been able to reproduce the techniques of OPN and LPN. With the adoption of minimally invasive approaches by many tertiary care centers, RAPN has replaced OPN as the preferred technique. This change in practice pattern has compelled us to conduct a study specifically focusing on highly complex renal masses to compare the outcomes of RAPN versus OPN. Therefore, This article presents the first comparative analysis of perioperative outcomes between OPN and RAPN for complex renal masses.

In this study, we compared the perioperative, functional, and oncologic outcomes of 517 patients who underwent RARP. Operative time, blood loss, hospital stay, postoperative renal functionand and complication were the main perioperative parameters of RARP and OPN. This data analysis shows that the surgical time for OPN is slightly shorter than RAPN. Both surgical procedures were performed by experienced surgeons, but this may be related to the learning curve of robot-assisted surgery and the longer set-up time required for the robotic platform. It is believed that in the future, with continuous accumulation of experience, the surgical time for RAPN is expected to be comparable to that of OPN, and even shortened. There was no significant difference in intraoperative blood loss and ischemia time between the two, but the transfusion rate for OPN was significantly higher than RAPN. This may be due to the larger incision in open surgery and the inability to achieve the same level of precision in tissue and vascular separation during tumor resection as in robot-assisted surgery. As commonly acknowledged, the data shows that the length of hospital stay for OPN is longer than RAPN, which is consistent with the conclusions of previous studies [27, 28]. This may be related to the longer incision healing time for OPN patients, in which robot-assisted surgery has a significant advantage. Of course, complications have an inseparable relationship with the length of hospital stay. In terms of overall complications, the incidence of postoperative complications in RAPN is lower than that in open surgery, with no significant difference in minor complications, but in major complications, OPN is significantly higher than RAPN. That is to say, the severity of complications in OPN patients is higher than that in RAPN, which may significantly prolong the length of hospital stay, even though OPN mostly adopts the retroperitoneal approach.

Nephron sparing surgery (NSS) is currently the gold standard method to treat small renal masses [29]. Preserving as much residual nephron as possible is also important in complex renal masses, as patient quality of life after surgery is closely related to postoperative renal function recovery. However, ensuring the integrity of tumor resection is also necessary, resulting in the “trifecta” concept. Studies indicate that the TRIFECTA completion rate decreases with a higher tumor score, making it challenging to strike a balance between nephron preservation and complete tumor removal. Nevertheless, RAPN demonstrates a higher completion rate than OPN in most score groups [17], and robot-assisted partial nephrectomy is expected to overcome this challenge over time. Additionally, WIT can also affect renal function. The study by Patel et al. in solitary kidney partial nephrectomy, each minute of WIT was found to be associated with a 6% increased risk of acute renal failure, a 7% increased risk of acute-onset end-stage renal disease (ESRD), and a 4% increased risk of new-onset ESRD while controlling for preoperative renal function, tumor size, and surgical approach [30]. The available data presented in this article demonstrate that there is no statistically significant difference in postoperative renal function between OPN and RAPN under similar warm ischemia conditions, which is consistent with the conclusion of Xia et al. [31]. Furthermore, the same PSM was not statistically significant. However, we still need more data to support those conclusions.

The present study has some limitations which need to be mentioned for the interpretation of the results. First, the included studies are retrospective with intermediate quality; they may have been affected by selection bias and unmeasurable confounding factors, also, we used two scoring systems for tumor characteristics, which may have introduced bias. Second, some studies included more patients with only one kidney and higher preoperative chronic renal disease (CKD) stage (≥ 3), which had a potential impact on the postoperative renal function. Third, the short follow-up and the absence of standard definition limit the comparison between the surgical methods in terms of functional or oncologic outcomes.

Conclusion

The meta-analysis revealed that while the operation time for OPN is marginally shorter than that of RAPN for complex renal masses, the latter results in superior outcomes in terms of hospital stay, transfusion, overall complications, and major complications. However, there were no significant differences observed in Ischemia time, minor complications, PSM, short-term postoperative eGFR decline, or estimated blood loss between the two groups. Further well-designed randomized controlled trials (RCTs) with larger sample sizes and long-term follow-up are still necessary to validate and update the findings of this study.