Abstract
Background/Aim: Different nephrometry scoring systems (NSSs) are used to evaluate the surgical complexity and outcomes of partial nephrectomy (PN) in patients with small renal tumors. This study aimed to assess the validity of nephrometry scoring systems towards aiding the preoperative planning of laparoscopic partial nephrectomy (PN). Patients and Methods: Data of 77 patients who underwent partial nephrectomy at the Puerto Real University Hospital between January 2011 and December 2017 were retrospectively analyzed. Statistical analyses were carried out to determine whether there was an association between the complexity of the surgical procedure and the assigned nephrometry scores. Results: Operative complications (bleeding volume, conversion to open surgery, perioperative bleeding, and postoperative fistula) were significantly associated with independent variables (age, sex, body mass index, radiological tumor size, and operative ischemia time) and with the classification of patients using arterial-based complexity (ABC) and radius endophytic/exophytic nearness anterior-posterior location (RENAL) scores. There was also a strong correlation between the RENAL and ABC scores [Cramer’s V coefficient (0.682) and Fisher’s test (p<0.0001)]. Conclusion: The RENAL and ABC scores are associated with the risk of the complexity of partial nephrectomy for T1 renal tumors, even for ≥T1b tumors and/or with complex anatomical features.
In recent years, renal cell carcinomas (RCCs) cases have increased worldwide due to improved imaging and an increasingly aging population. In this regard, the curative approach for most T1 RCCs remains surgical (1). Partial nephrectomy (PN) is the standard reference technique most commonly used for the management of T1 renal tumors, including T1a (≤4 cm) or even those larger than T1b, when technically possible (2). However, for RCCs above T1b, the choice of PN remains controversial (3). PN provides oncological and functional outcomes comparable to radical nephrectomy (RN). PN enables better preservation of renal function and a low risk of chronic kidney disease (4). However, PN is a procedure with high complication rates ranging from 4.5% to 28%, even higher in patients undergoing complex PN (5).
Different nephrometry scoring systems (NSSs) have been developed for clinical practice. The most widespread systems are the radius endophytic/exophytic nearness anterior-posterior location (RENAL) score (6) and preoperative aspects and dimensions used for anatomy (PADUA) score (7). These systems can quantify relevant anatomical features of renal tumors, providing rigorous information on surgical complexity. Therefore, these scales provide PN surgeons with standardized and easily reproducible tools that help predict the risk of intra- and perioperative complications. This leads to improved preoperative surgical planning, specialist communication, and patient counselling (8). However, these NSSs have several limitations concerning their ability to predict clinical outcomes (9). In this regard, it has been displayed that the variability associated with different observers applying these NSSs is reduced as clinical and radiological experience increases. In this case, only tumor size and distance to intrarenal structures are clinically relevant (10). Hence, other new NSSs have been developed, such as the arterial-based complexity (ABC) score, which considers the tumor’s vascular involvement (11). Specifically, the ABC score relates to the depth of the renal tumors and the size of the renal arterial branches to be sectioned during PN. This score is intuitive and easy to use in clinical practice (12, 13) establishing an appropriate association with perioperative morbidity (11). However, the acceptance of all these NSSs in daily clinical practice and their current predictive value is still unclear. Hence, it is critical to assess and validate the possible correlations between these NSSs and surgical difficulties that patients may experience during PN (12). Thus, the main objective of this study was to evaluate the validity of NSSs towards aiding preoperative planning of laparoscopic PNs in patients with T1a and even bigger T1b renal tumors.
Patients and Methods
Study population. This was a retrospective, observational, descriptive, including the study of 77 patients with renal tumors with a mean size of 3.95 cm (median=3.7 cm; range=1.3-7.3 cm) who underwent laparoscopic PN between January 2011 and December 2017 at the Puerto Real University Hospital (Cadiz, Spain). Two urologists independently scored the patients’ tumors using the ABC and RENAL NSSs.
Ethical standards. This study complied with the ethical recommendations of the Declaration of Helsinki (World Medical Association, 2013). The Puerto Real University Hospital Reviewer Board approved the research protocol, and its number is PEIBA 2161-N-21, nº187.21. All participants were provided and signed a written informed consent form with guarantees of confidentiality, and they also gave their consent for publication. Data processed in an excel file are available on reasonable request. The availability of data is subject to the restrictions of the Spanish Data Protection Act.
Clinical features, variables, and data acquisition. Data were obtained from the patient electronic medical record and were peer-reviewed. The patients’ features, their corresponding tumors, and the surgical results were gathered. Dependent variables were categorized into surgical complications (bleeding volume during surgery (ml) and conversion to hand-assisted laparoscopy, also called open surgery during laparoscopic PN) and postoperative complications (postoperative bleeding and postoperative fistula formation). The independent variables were classified as preoperative [age defined as patient’s age at the time of surgery (years); sex defined as patient’s sex; body mass index (BMI, kg/m2); radiological tumor size (cm); ABC score and RENAL score] and as intraoperative (time in min for surgery and warm ischemia, 15 min of cut-off value).
Nephrometry scoring systems (NSSs). ABC score: this NSS allowed assigning scores of 1, 2, 3S or 3H to tumors requiring transection of the interlobular and arcuate arteries, interlobular arteries, segmental arteries or proximal to the renal hilum, respectively, during laparoscopic PN (14). RENAL score: This NSS classified tumor complexity as low, moderate, and high if the RENAL score was 4-6, 7-9, or 10-12, respectively (12).
Statistical analysis. The distribution of data was analyzed by the Shapiro-Wilks test. Continuous quantitative variables were expressed as the mean and range, non-Gaussian quantitative variables as range and median and qualitative variables as frequencies. An analysis of the association between surgical complications and the independent variables was carried out using Pearson’s correlation coefficient for quantitative variables with normal distribution, Spearman’s Rho rank correlation coefficient for non-Gaussian quantitative variables; Pearson’s Chi-square test for qualitative variables; the Mann-Whitney U-test for dichotomous qualitative variables as well as quantitative ones with non-Gaussian distribution; the ANOVA test for qualitative variables with more than two categories and quantitative variables with normal distribution; and finally, the Kruskal-Wallis test for qualitative variables with more than two categories and quantitative variables with the non-Gaussian distribution. In addition, a collinearity study was performed between the RENAL and ABC scores by calculating Cramer’s V coefficient and Fisher’s test. The level of significance was set at p<0.05. All statistical analyses were performed using the SPSS Statistic v 24 software.
Results
Patient characteristics. We analyzed 77 patients with renal tumors who underwent laparoscopic PN. Their age ranged from 39 to 78 years (median=64 years); 21 patients were females (27.3%), and 56 were males (72.7%). Of note, 50% of operated patients had tumors ≥T1b and/or complex anatomical features. Table I shows the frequencies of tumor pathologic stage and histologic type for each patient.
Tumor histopathology and staging of patients (n=77).
Pre-, intra- and postoperative outcomes. The descriptive statistics of the intra- and postoperative complications (dependent variables) observed in patients with renal tumors who underwent laparoscopic PN are shown in Table II. It is worth noting that the quantitative variables analyzed followed a non-Gaussian distribution. The analysis results indicated that most patients did not require hand-assisted laparoscopic PN (71.74%), nor did they present postoperative complications (61.0% for perioperative bleeding and 85.7% for fistula formation). In addition, half of the patients bled less than 180 ml during the operation. Regarding demographic data, descriptive statistical analysis of independent variables (Table III) exhibited that most patients were men over 60 years of age. Half of the patients had a radiological tumor size ≤3.7 cm. Categories 2 on the ABC score and moderate complexity (7-9) on the RENAL score were the most frequent. In half of the patients, the operative and the warm ischemia time was ≤180 and ≤22 min, respectively (Table III).
Intra- and postoperative complications (dependent variables) of patients with renal tumors undergoing laparoscopic PN (n=77).
Demographic characteristics and descriptive statistics of the independent variables studied in patients undergoing laparoscopic PN (n=77).
Correlation analysis. Statistical correlation analysis (Table IV) showed that intraoperative bleeding volume significantly correlated directly with age, radiological tumor size, and surgery and ischemia times. Furthermore, conversion to open surgery (hand-assisted laparoscopic PN) was significantly associated with operative and ischemia times. Indeed, 90% of patients with an operative time >220 min or an ischemia time >26 min needed a hand-assisted laparoscopic PN. Perioperative bleeding was significantly associated with age, detected in 90% of patients >70 years. It was also significantly associated with radiological tumor size, with 90% of patients with tumor size >4.6 cm experiencing bleeding. Finally, it was associated with surgery and ischemia times, with 90% of patients with an operation time >210 min or an ischemia time >25 min also bleeding. Ultimately, fistula formation was significantly associated with radiological tumor size, forming in 90% of patients with tumor size >5.5 cm, and with surgery and ischemia times, with fistula formation in 90% of patients with operation time >245 min or ischemia time >27 min. However, no significant associations were found between the observed surgical complications and tumor histopathology.
Statistical correlation between independent variables and surgical complications.
On the other hand, significant differences were obtained following comparison between all observed surgical complications and the groups of patients classified by both the ABC score (Table V) and the RENAL score (Table VI). No significant differences were found by comparing ABC score classification with open surgery. It is worth noting that according to the ABC score, patients in category 3H were those with more surgical complications. Specifically, 71.4% of patients in category 3H exhibited perioperative bleeding and conversion to open surgery (Table V). While when using the RENAL score, the patients classified in the high complexity group (with a score between 10 and 12) were those who exhibited more surgical complications (Table V). Operative and ischemia times were significantly longer in patients classified in the 3H category of the ABC scale (medians=235 and 26 min, p<0.001 linear model ANOVA; p<0.003 Kruskal-Wallis test, respectively) and in the high complexity category according to the RENAL scale (medians=235 and 25 min, p<0.01 and p=0.003 Kruskal-Wallis test, respectively). Notably, both scores showed no significant differences in the association analysis between tumor histopathology and patient classification. A collinearity study was performed to determine if there is a correlation between the RENAL and ABC scores in our study. To address this, we used Cramer’s V coefficient, obtaining a value of 0.682, indicating a strong association between both scores. In fact, Fisher’s test showed that both scales are significantly associated and are not independent (p<0.0001).
Surgical complications classified according to the arterial-based complexity (ABC) score.
Surgical complications classified according to the radius endophytic/exophytic nearness anterior-posterior location (RENAL) score.
Discussion
The development of more accurate imaging techniques and improvements in preoperative staging and surgical techniques have made PN an alternative to radical RN in surgical therapy of T1 renal tumors. However, in many cases, PN involves operative complications. A direct relationship between morbidity and the degree of complexity of PN surgery has been demonstrated. Small and peripherally located tumors require less technically complex procedures; therefore, their morbidity rates are similar to those observed in patients undergoing RN (15). In contrast, complication rates are higher in extensive tumor resections closer to the renal hilum. The intervention involves extensive manipulation of the renal vasculature (longer ischemia time) and the collecting system. NSSs work as standardized procedures to predict surgical complexity and outcomes in this context. However, these NSSs have several limitations regarding their prognostic ability (13). Therefore, further studies comparing different NSSs are needed.
In this study, the RENAL and ABC scores were correlated with perioperative morbidity of the PN determined by bleeding volume, conversion to open surgery, perioperative bleeding, and postoperative fistula formation, including operative and ischemia times. There were no significant differences between ABC and RENAL scores, and they were found to similarly predict surgical complications. Our results related to the ABC score align with previous reports (11, 14). Specifically, the ABC score also predicted persistent warm ischemia time and operative time, as well as additional estimated bleeding as our study. However, in contrast to our study, the ABC score did not predict the occurrence of complications or postoperative renal function (14). Regarding our results on the RENAL score, this NSS was previously endorsed as a predictor of renal function impairment (16). Similar results to ours were also found in the assessment of PADUA and RENAL scores (17). A recent study evaluated the associations between the PADUA, RENAL, ABC, and Mayo Adhesive Probability (MAP) NSSs. In this study, surprisingly, the ABC score was not relevant. Only the MAP score, which appraised adherent peripheral fat, correlated with surgical difficulties and operative time. It is noteworthy that, as in our study, tumor diameter influenced surgical time (12). Ultimately, our data mainly confirmed the impact of the assessment of these two NSSs on PN. The recent therapeutic advances in technological procedures, such as thermal ablation or robotic-assisted PN have increased the possibilities of T1 renal tumor treatment (18, 19). Despite this, the ultimate choice of treatment is still depending on the anatomical characteristics of the tumor as well as the urologists’ experience. The intraoperative and postoperative risk of bleeding in patients suffering laparoscopic PN and/or robotics is relatively high, according to data from different cohorts (5-25% and 1-15%, respectively). Reducing this risk is essential for PN surgeons, so it is critical to identify these risk factors (18).
In our study, the risk of bleeding was related to the operation and ischemia times, with bleeding being observed in 90% of patients with an intervention time >210 min or ischemia >25 min. The most frequent complication was perioperative bleeding, present in almost 40% of the studied cases. Age was significantly related to this complication, being observed in 90% of patients >70 years of age. Likewise, radiological tumor size was a predictor of bleeding, present in 90% of patients with a size >4.6 cm. Similar to our results, tumor size and bleeding were found to be significantly related in a study of 283 patients undergoing robotic-assisted PN (tumor ≥7 cm was associated with mean bleeding of 168 ml, which was higher than for tumors >4 cm) (19). Patients with greater bleeding volume during surgery or who required conversion to open surgery had longer operative and ischemia times. Surgical duration longer than 210 min or ischemia time longer than 25 min was associated with postoperative complications. Sex, BMI, or tumor histopathology were not associated with surgical complications. Patients classified in category 3H according to the ABC scale or with a score between 10-12 according to the RENAL score (high complexity) were those who displayed a higher percentage of surgical complications.
The most important finding of our study is that the ABC and RENAL scores were not only strongly associated with each other, but also helped predict surgical complications of PN in patients with T1 renal tumors, even ≥T1b tumors, and/or with complex anatomical features, as previously described in another study (2). In this regard, laparoscopic PN assisted with thermal ablation was also validated as a safe, effective nephron-sparing treatment for cT1b renal tumors (20). Hence, these two NSSs may successfully identify suitable cases among patients with ≥T1b renal tumors who could benefit from PN. Predicting the surgical complications may facilitate the schedule of laparoscopic PNs more efficiently and, ultimately, ensure the success of more delicate procedures.
Despite the promising results, our study has certain limitations. The main limitation is its retrospective design and the fact that two urology surgeons performed laparoscopic PN with different experience levels, which may have affected the perioperative outcomes. However, in our study, no surgical complications occurred in most cases, indicating that surgical experience has overcome the learning curve. Further studies with a more extensive series of patients could help validate our results.
Acknowledgements
Regarding financial disclosure, the authors declare that this study has not been funded by any specific project, apart from the resources of the involved hospitals. The authors kindly acknowledge Patricia García-Sanz from BioMed Targets for her medical writing contributions and logistical support in preparing this manuscript.
Footnotes
Authors’ Contributions
Miguel E. Jiménez Romero: conceptualization, methodology, design of the study, surgical procedure, collecting data, data analysis, drafting, writing, editing, and reviewing manuscript. Isabel Bueno González: supervision. Miguel A. Sánchez Hurtado: conceptualization. José Carlos Rodríguez Bocanegra: supervision. Jose D. Santotoribio: data curation, formal analysis, and critical reviewing. All authors revised the final version of the manuscript and take responsibility for its content.
Conflicts of Interest
The Authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
- Received October 10, 2022.
- Revision received October 26, 2022.
- Accepted November 8, 2022.
- Copyright © 2022 International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved.
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