Abstract
Purpose:
We retrospectively reviewed the preoperative radiologic findings and operational videos of a group of patients who were undergoing laparoscopic nephron-sparing surgery (NSS), to determine whether we should decide the operational approach (laparoscopic vs open or radical nephrectomy) on the basis of only the preoperative aspects and dimensions used for an anatomic (PADUA) classification.
Patients and Methods:
In total, 41 laparoscopic NSS operations were performed during a 34-month period for suspicious solid renal lesions. Clinicopathologic variables, PADUA scores, operative parameters, and renal functional outcomes were prospectively recorded and analyzed. Meanwhile, a similar classification (intraoperative aspects and dimensions used for an anatomic [IADUA] classification) was used to compare the preoperative imaging modality findings with intraoperative findings.
Results:
There was a 73.2% difference between PADUA and IADUA scores. Sixteen (39%) patients had PADUA scores >IADUA scores, 14 (34%) had PADUA scores <IADUA scores, and only 11 (27%) had similar PADUA and IADUA scores. For the study cohort, the mean operative time (OT) was 128 minutes (range 50–250) min, the mean estimated blood loss (EBL) was 199 mL (range 10–1000 mL), the mean warm ischemia time was 35.2 minutes (range 15–60 min), and the mean change in glomerular filtration rate was 8.17 mL/min/1.73m2 (range −41–26 mL/min/1.73m2). The mean pathologic tumor size was 32.7±12.3 mm. Thirteen complications were recorded according to the modified Clavien system. PADUA and IADUA were not correlated with EBL and OT, and higher scores failed to predict perioperative complications.
Conclusions:
Reproducible standardized classification systems are necessary for renal masses. Intraoperative findings for renal masses, however, may differ from the preoperative radiologic evaluation. Thus, the decision for the type of surgical approach should not be based solely on preoperative assessment, such as the PADUA score.
Introduction
A lesion that one clinician may deem impossible for partial nephrectomy because of its central, hilar, or endophytic location may be typically operable for another clinician, depending on training patterns, biases, comfort levels, and individual experiences. 8,9 The preoperative aspects and dimensions used for an anatomic (PADUA) classification score, RENAL nephrometry score (NS), and centrality index (C-index) are the three different scoring systems that have been developed to improve clinical and radiologic assessment of renal tumors. 8,10,11 Among these, the PADUA score, a classification system of renal tumors in patients who are candidates for NSS, provides detailed and objective information on how to select patients who are suitable for NSS and predict the risk of complications, regardless of clinical tumor size.
When using PADUA classification, a relatively easy scoring system to apply, patients are staged preoperatively using CT or MRI to define the characteristics of the tumor, such as size, polar and rim location, relationship with renal sinus or urinary collecting system (UCS), and deepening of the tumor into the renal parenchyma. 10 Similarly, preoperative CT or MRI is used when assessing RENAL-NS or defining tumor size, polar location, renal sinus/collecting system relationship, and endophytic properties, whereas the C-Index uses the distance from the tumor center to the kidney center, which is a relatively difficult score to calculate. All three scoring systems enhance radiologic evaluation, surgical planning, and academic reporting.
We believe, however, that the surgeon's grading of the difficulty of the operation or preoperative determination of the PADUA score may not always correlate with the operational findings, such as UCS involvement, longitudinal location of the renal mass, and degree of endophysis. In the present study, we aimed to compare preoperative PADUA classification with a similar classification performed intraoperatively (intraoperative aspects and dimensions used for an anatomic [IADUA] classification) and to assess the importance of this difference by retrospectively reviewing the preoperative radiologic findings and operational videos of a group of patients who were undergoing laparoscopic NSS to determine whether we should decide the operational approach (laparoscopic vs open or radical nephrectomy) only by considering the PADUA classification. Meanwhile, we also assessed the complications according to the modified Clavien system. 12
Patients and Methods
From February 2008 through December 2010, 41 patients who had a diagnosis of renal masses underwent laparoscopic partial nephrectomy (LPN) that was performed or mentored by a single surgeon (OS). An institutional collected database is maintained prospectively for laparoscopic procedures and contains demographic, operative, and follow-up information on more than 400 patients who have been treated at our institution. Information on laparoscopic NSS was reviewed from the above-mentioned database. Preoperative workups included complete blood cell count (CBC), kidney function tests, and coagulation tests (such as prothrombin time, partial thromboplastin time, and international normalized ratio), and estimated glomerular filtration rate (eGFR; based on serum creatinine level, age, sex, and race). Patients were preoperatively evaluated using an American Society of Anesthesiologists (ASA) score, with ASA grades 1, 2, 3, and 4 representing healthy patients and those with mild, severe systemic, and life-threatening disease, respectively. Early withdrawal of drugs that affect platelet function, such as acetylsalicylic acid or anticoagulants, was ensured.
Preoperative CT/MRI images were also assessed, and the PADUA score was recorded by evaluating the radiologic characteristics of the renal mass, such as (a) longitudinal location, (b) renal rim location, (c) relationship with the renal sinus, (d) relationship with the UCS, (e) percentage of the tumor deepening into the kidney, and (f) maximal diameter in cm. Images from CT or MRI were independently reviewed by two final-year residents (TT and AM) and a consultant urologist (VG) who did not have knowledge of the clinical details of the cases but who had sufficient clinical and surgical experience in laparoscopic upper urinary tract surgery. Invariably, the residents/urologist who evaluated the imaging were blinded to the patients' outcomes. Generally, scores were more than two-thirds consistent between reviewers, and disagreements (for 29% of the cases) were rereviewed and decided by consensus. Moreover, all recorded NSS operative videos were overviewed with the same principles, and the IADUA was calculated similarly for each of the patients by the same urology residents and consultant urologist using the same a, b, c, d, e, and f parameters, with the only difference being the “f” parameter, for which the maximal renal mass diameter was measured after its intact extraction at the pathology department. Notably, the surgeons scoring PADUA and IADUA were independent from the surgeon who was performing or mentoring NSS. Laterality of the patients and the methods of approach (transperitoneal or retroperitoneal) were evaluated. Mean warm ischemia time (WIT), mean operative time (OT), and insufflation time were also recorded.
The patients were divided into two groups in each preoperative and postoperative PADUA classification, according to low (PADUA ≤7 [group 1] and IADUA ≤7 [group 3]) and intermediate-high (PADUA >7 [group 2] and IADUA >7 [group 4]) scores. 10 Complications within 30 days of the procedure were recorded prospectively and graded according to the modified Clavien classification system.
Exposure of the entire kidney, dissection of the renal hilum, and identification of the tumor were performed laparoscopically in all cases. The decision for application of renal ischemia was made according to the surgeon's preference. Methods of clamping, such as Satinsky (n=7, 17.1%) or bulldog clamping (n=21, 51.2%), were used for application of warm ischemia. For small exophytic tumors, warm ischemia was not applied, and partial nephrectomy (PN) was performed under perfused conditions (n=13, 31.7%). In these cases, however, the renal hilum was dissected and prepared for urgent occlusion in case of bleeding by vessel loop suspension fixed with Hem-o-lok clips (Weck Closure Systems, Research Triangle Park, NC). Venous occlusion was performed at the surgeon's preference (Satinsky [n=6, 14.6%] or bulldog [n=11, 26.8%] clamp).
The proposed line of the parenchymal incision was circumferentially scored with an electrocauterizing J-hook, maintaining a safe margin around the tumor, and the tumor was excised with round-tipped scissors. The base of the resection was biopsied, and frozen sectioning was performed, as needed. Collecting system defects were repaired with intracorporeal 3-0 polyglactin suturing, whereas renal parenchymal reconstruction was performed with 2-0 polyglactin sutures over a rolled cellulose bolster and secured with Hem-o-lok clips. Argon beam coagulation of the incised renal surface was applied at the surgeon's preference.
Serum creatinine (sCr) levels and CBC recorded preoperatively were followed postoperatively. Functional renal preservation was assessed through the comparison of preoperative and postoperative eGFR, which was calculated using the Chronic Kidney Disease (CKD) Epidemiology Collaboration formulae (
For comparison of parameters, statistical analyses, using the Mann-Whitney U test, Student t test, and chi-square test, were performed as appropriate. The statistical significance was defined as P<0.05.
Results
Demographic and operative parameteters of the 41 patients who were recruited to the present study appear in Table 1. The preoperative mean tumor size that was detected radiologically was 34.1±11.5 (18–60) mm. The mean OT was 128±39 (50–250) minutes, the mean estimated blood loss (EBL) was 199±203 mL (range 10–1000 mL), and the mean reduction in hemoglobin level was 1.4±1.3 (range −2–4). The mean hospitalization time and drain removal time were 3.6±2.7 days (range 1–18 d) and 2.6±2.1 days (range 1–15 d), respectively.
ASA=American Society of Anesthesiologists; BMI=body mass index; ECOG: Eastern Cooperative Oncology Group; eGFR=estimated glomerular filtration rate.
Six, 12, 12, 6, 4, and 1 patients were assigned PADUA scores of 6, 7, 8, 9, 10, and 11, respectively, whereas, 12, 5, 6, 10, 5, and 3 patients were assigned IADUA scores of 6, 7, 8, 9, 10, and 11, respectively. Thus, disagreement between PADUA and IADUA scores was found to occur in 73.2% of the cases. The difference between the two scoring systems was statistically significant (P=0.001) (Table 2). Sixteen (39%) patients had PADUA >IADUA, and 14 (34%) had PADUA <IADUA, whereas only 11 (27%) had similar PADUA and IADUA scores. The detailed distribution of PADUA and IADUA scores is shown in Table 3.
Student t test: P=0.001.
PADUA classification=preoperative aspects and dimensions used for anatomic classification; IADUA classification=intraoperative aspects and dimensions used for anatomic classification.
PADUA classification=preoperative aspects and dimensions used for anatomic classification; IADUA classification=intraoperative aspects and dimensions used for anatomic classification; NS=not scored.
The peak sCr, peak eGFR, last follow-up sCr and last follow-up eGFR (obtained an average of 14±10 months [range 0–34 mos] after LPN) are summarized in Table 1. As expected, the peak eGFR and last follow-up eGFR values were significantly lower than the preoperative eGFR (P=0.009 and P=0.008). The WIT, eGFR, and last follow-up eGFR in patients who were receiving WIT (n=28) were similar in group 1 vs 2 and group 3 vs 4 (Table 4). EBL and OT were similar among groups (EBL: group 1 vs 2 [P=0.275], group 3 vs 4 [P=0.413]; OT: group 1 vs 2 [P=0.56], group 3 vs 4 [P=0.831]). Modified Clavien complications related to PADUA and IADUA are shown in Table 5. No statistical significance was found between group 1 vs 2 and group 3 vs 4 regarding complications (P=0.091 and P=0.98, respectively).
Rate in groups 1, 2, 3, and 4 (mean±standard deviation, [range])
PADUA classification=preoperative aspects and dimensions used for anatomic classification; IADUA classification=intraoperative aspects and dimensions used for anatomic classification; eGFR=estimated glomerular filtration rate.
PADUA classification=preoperative aspects and dimensions used for anatomic classification; IADUA classification=intraoperative aspects and dimensions used for anatomic classification.
The mean pathologic tumor size was 32.7±12.3 mm (range 15–65 mm) in 36, 3, 1, and 1 patients with RCC, oncocytoma, angiomyolipoma, and cystic nephroma, respectively. Histologic subtypes of RCC were clear-cell in 24 (67%), papillary in 10 (28%), and chromophobe in 2 (5%) patients. Fuhrman nuclear grades were 1, 2, and 3 in 2 (5%), 28 (78%), and 6 (17%) patients, respectively. Only one patient had a positive surgical margin, and a second LPN operation is planned for that patient. After a mean follow-up of 14±10 months (range 0–34 mos), the recurrence-free and overall survival rates were 97.6% and 100%, respectively.
Discussion
NSS aims for the complete extirpation of the tumor and the maximal preservation of the renal functional unit. Cancer control in NSS is equivalent to that achieved with RN in patients with T1 renal tumors. 2 Moreover, there is a clear benefit from NSS related to cardiovascular events, which may explain the improved overall survival in these patients and may have provided added incentive for its increased use in recent years. 17 PN is a challenging procedure, and laparoscopic NSS is even more so, because it has been associated with increased morbidity, compared with traditional open NSS. 18
The novel aspect of this article is the exploration of the relationship between preoperative and intraoperative scoring. Generally, a standardized reporting of renal tumor size, location, and depth is needed for decision making and effective comparisons with respect to anatomy, pathology, and prognosis. 8 Imaging modalities, such as CT and MRI, remain the most appropriate modalities to differentiate benign from malignant lesions. Although these imaging modalities are the crucial elements for preoperative evaluation and decision making, the intraoperative evaluation of renal masses may differ from preoperative evaluation. As would be expected, this discrepancy can be prominent in cases in which detailed evaluation is performed. For instance, a surgeon may plan PN in a patient with preoperative imaging but may shift to RN intraoperatively. It is impossible to neglect intraoperative evaluation, which means that part of the IADUA score is used in every NSS surgery. This is also valid for preoperative assessment and the “unaware” use of part of the PADUA score. In this study, the concordance of PADUA and IADUA scores was evaluated, and a 73.2% significant difference (P=0.001) was found among scores, meaning that “what we found” may not be equal to “what we see.”
In addition, case complexity in renal masses may change the surgical approach. 8 Complex cases may undergo open NSS, laparoscopic RN, or open RN. Higher PADUA scores, denoting complexity of resectability, may lead surgeons to approach renal masses with open NSS or RN. We found a 73.2% discordance rate between PADUA and IADUA scores, signifying that the decision of approach (open, laparoscopic, radical, or partial) should not be based only on preoperative parameters. Higher PADUA scores should not prevent surgeons from initializing the cases laparoscopically. Thus, we plan to perform a future study aimed at delineating the method of approach in renal masses; efforts to validate PADUA scores are currently under way.
The difference between PADUA and IADUA scores may have several justifications. Interpreting IADUA scores with respect to the polar location might not be as accurate as examining the radiologic images of the patients. Regarding the exophytic and endophytic properties of the tumor, in PADUA, the radiologic measurements are clear, whereas in IADUA, the perirenal fat tissue around the renal mass may mislead the IADUA interpreter. Furthermore, while performing LPN, the surgeon clears the suspicious kidney mass from perirenal fat and mobilizes the kidney. The patient's position is no longer supine, as in the radiologic setting, and this change may lead to erroneous rim localization in the intraoperative setting, resulting in different scores between PADUA and IADUA.
In addition, UCS involvement and dislocation produces a score of 2 points in PADUA. In the radiologic image, a dislocation would thus mean 2 points in the scoring system. In the intraoperative setting, for the same patient, there could be a clear image of incised renal parenchyma, no image of the UCS at all, or no image of the wall of the UCS, resulting in a score of 1 point. On the contrary, in a case without UCS involvement, based on the radiologic image of a patient, the surgeon might prefer a deep resection, leading to exposure/opening of the UCS and necessitating further suturing of the UCS. This could mislead the IADUA interpreter into scoring 2 points for UCS involvement. Moreover, the radiologic renal mass size may differ from the pathologically determined tumor measurements. We believe that all of the aforementioned causes led to the 73.2% discordance between PADUA and IADUA scores in the current study.
The other two established tools for prediction of complications were C-index and RENAL-NS. 8,11 The former tool is not suitable for the present study instead of IADUA, because it needs an exact measurement between the kidney center (hilar axial reference point) to the tumor center, and this cannot be performed by just overviewing the operational videos. So, C-index is considered as an impractical intraoperative scoring system. On the other hand, despite many similarities with PADUA, RENAL-NS again needs the exact distance between the deepest portion of the tumor to the collecting system or sinus, which is also not possible to measure intraoperatively. PADUA classification uses “presence or absence of relationship” between UCS and renal sinus, a relative intraoperative evaluable parameter’ thus, PADUA classification was used for comparison of parameters.
The prediction of surgical and medical perioperative complications for both PADUA and IADUA was also evaluated. We did not find significant differences related to complications when comparing patients with low PADUA scores (PADUA ≤7, group 1) and intermediate-high PADUA scores (PADUA >7, group 2) (P=0.091), as in the study of Ficarra and associates. 10 We also did not find any significant difference between group 3 (IADUA ≤7) and group 4 (IADUA >7) with respect to complications (P=0.98). We believe that the relatively low number of patients (n=41) in our study might be an obstacle to determining the relationship between high-risk/high-PADUA scores and the prediction of complications. The PADUA score was originally used for open PNs. To our knowledge, no reports have validated PADUA scores to date, as with “urine leak” validation in RENAL-NS. 19 The prediction of complications that are applicable for open NSS might not apply for laparoscopic NSS. Further studies with larger numbers of patients are needed to validate the accuracy of PADUA scores in laparoscopic series, as stated in the original article. 10
Deterioration of renal function after NSS is related to old age, male sex, lower preoperative GFR, larger tumor size, postoperative complications, increased resection size, solitary kidney, and increased ischemia time. 20 In this study, postoperative eGFR and last follow-up eGFR were significantly lower than the preoperative values (P=0.009 and P=0.008, respectively), despite the fact that the lack of significant complications and the relatively small radiologic tumor size (34.1±11.5 [range 18–60] mm), male predominance (66%), low preoperative eGFR (chronic kidney disease [CKD] stage 4 [eGFR <60 mL/min/1.73 m2] in 5 patients and CKD stage 2 [eGFR <90 mL/min/1.73 m2] in 23 patients] and increased WIT (35.2±13.9 [15–60] min) may have contributed to the low postoperative eGFR in this study. 20,21 We believe that modifiable factors, such as the learning curve, can overcome the significant decrease in renal function after the operation.
Conclusions
Standardized classification systems are needed for renal masses to allow comparison between groups of patients who are undergoing different surgical approaches. The PADUA scoring system seems to be an easily applicable, standardized tool. The present study, however, revealed that intraoperative evaluation of renal masses may be different from preoperative findings. Consequently, the decision regarding which surgical approach to use should not be based solely on preoperative scores, such as the PADUA scoring system.
Footnotes
Disclosure Statement
No competing financial interests exist.
