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Keywords:

  • laparoscopy;
  • partial nephrectomy;
  • renal ischaemia;
  • renal scintigraphy

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Objectives

  • To present our laparoscopic partial nephrectomy (LPN) results according to the margin, ischaemia and complications (MIC) system recently proposed for the standardized reporting of partial nephrectomy (PN) outcomes.
  • To assess the role of learning curve and tumour anatomical characteristics on the outcomes by using MIC system.

Patients and Methods

  • Data were obtained from our prospectively maintained LPN database, including only patients who underwent LPN performed with vascular clamping.
  • According to the MIC system definition, the goal of LPN was reached (i.e. MIC was achieved) when surgical margins were negative, warm ischaemia time (WIT) was <20 min and no major complications occurred.
  • Patients were stratified by quartiles of distribution, named LPN eras 1–4, and MIC rates in different LPN eras were compared, evaluating the impact of learning curve and tumour anatomical characteristics (as assessed by Preoperative Aspects and Dimensions Used for an Anatomical [PADUA] score on the outcomes.

Results

  • The study population consisted of 206 patients.
  • The overall MIC rate was 63.1%: it progressively increased along the learning curve, reaching 84.9% in LPN era 4 (P < 0.001).
  • PADUA-score risk group categories were inversely correlated with MIC score (P = 0.001).
  • When simultaneously considering the effects of both LPN eras and PADUA-score risk group categories, a trend towards a higher MIC rate was found in the latest series, regardless of tumour anatomical characteristics.
  • When MIC score components were separately analysed, WIT decreased significantly from LPN era 1 to LPN era 4 (P < 0.001) and from PADUA-score risk group categories 3 to 1 (P = 0.001)
  • A trend towards a decrease in the complication rate along the learning curve was observed (P = 0.251), while LPN era and PADUA score together significantly influenced the complications rate (P < 0.001). The positive surgical margin rate was very low (2.9% overall) and stable throughout the case study.

Conclusion

  • The MIC rate increased with surgeon's experience and decreased when complex lesions were treated.
  • The MIC system was found to be an easy, useful and reproducible tool to report LPN data series.

Abbreviations
LPN

laparoscopic partial nephrectomy

MIC

margin, ischaemia and complications

PN

partial nephrectomy

PADUA score

Preoperative Aspects and Dimensions Used for an Anatomical score

WIT

warm ischaemia time

LRF

loss of renal function

PSM

positive surgical margin

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

The treatment of kidney cancer has seen significant advances in recent years, and we observed a dramatic shift from radical nephrectomy to nephron-sparing procedures. This is because partial nephrectomy (PN) achieves the same oncological results as radical nephrectomy and reduces the loss of renal function (LRF) after surgery [1]. Thus PN has become the ‘gold standard’ treatment for renal tumours <7 cm [2]. To reduce the invasiveness of traditional open surgery, laparoscopic PN (LPN) and, more recently, robot-assisted PN have been developed. PN, especially when performed with minimally invasive techniques, is technically demanding and has a higher risk of complications compared with radical nephrectomy [3, 4]. This greater risk of complications is counterbalanced by the preservation of functioning renal parenchyma, leading to the chance of longer ‘kidney survival’ and a lower incidence of cardiovascular diseases [5]. In this scenario, standardizing the reporting of PN outcomes, not only in terms of oncology, but also in terms of functional results and complications, is critical for the comparison of different techniques. Combining surgical margin status, complications according to the Clavien system and the duration of ischaemia, some authors have recently proposed a novel ‘margin, ischaemia, and complications’ (MIC) [6] binary system, with the aim of standardizing the reporting of PN results. This idea is similar to that of ‘trifecta’, which was proposed in 2005 in the literature and is commonly used for the evaluation of the results of radical prostatectomy [7]. According to the MIC system, the goal of PN is reached (i.e. MIC is achieved) when surgical margins are negative, the warm ischaemia time (WIT) is <20 min, and no major complications (grade III–IV according to the Clavien classification) are observed. Subsequently, Mottrie [8] suggested that the use of the MIC system in evaluating early outcomes of PN would have to be supported by the scientific community; furthermore, he supported the use of the MIC system to evaluate PN outcomes in patients stratified by characteristics of renal mass. To contribute to this field, in the present study, we aimed to report our LPN outcomes and to assess the role of the learning curve and tumour anatomical characteristics in a standardized manner, using the MIC system.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

After institutional review board approval, data from 302 consecutive patients, who had undergone LPN by the same surgeon (F.P.) at our institution between September 2001 and September 2012, were obtained from our prospectively maintained database. Specifically, for the purpose of the study, patients were stratified by quartiles of distribution, named ‘LPN eras’ 1, 2, 3 and 4, to report the impact of the learning curve on the outcome.

All patients who had been diagnosed with a single, organ-confined, contrast-enhancing renal mass suspected to be a malignant lesion were included in the present study. The indications for surgery for tumours suspected to be an angiomyolipoma included tumour size >4 cm, chronic flank pain attributable to the renal mass and previous spontaneous haemorrhage.

Patients with a solitary kidney, who underwent open PN, robot-assisted PN or who underwent clampless LPN (without clamping of renal artery) according to a previously described technique [9] were excluded.

The following variables were evaluated: demographic data (age, gender and body mass index), preoperative data (American Society of Anesthesiologists score, Charlson's comorbidity index [10], lesion size on CT, tumour side and tumour anatomical characteristics, as classified by Preoperative Aspects and Dimensions Used for an Anatomical [PADUA]-score risk group categories [11]: PADUA scores <7, low risk; scores 8–9, intermediate risk; and scores >10, high risk), peri-operative data (laparoscopic approach on the basis of tumour location [retro-/transperitoneal], operating time, WIT, estimated blood loss, use of haemostatic agents) and postoperative data (duration of hospitalization). In addition, surgery-related complications (either intra- or postoperative) were analysed. Postoperative complications were classified according to the modified Clavien classification system [12]. Concerning functional data, serum creatinine and estimated GFR were assessed by serial measurements preoperatively and 3 months after surgery. Learning curve (LPN eras) and tumour anatomical characteristics (PADUA-score risk group categories) were tested, either alone or together, to evaluate their influence on the MIC rate.

A dedicated uropathologist analysed fresh tissue specimens from the operating room and determined the extension of the primary tumour according to the 2009 version of TNM classification [13]. After fixation in a 10% formalin solution, all specimens were step-sectioned at 5-mm intervals, and the entire specimen was analysed, including the distance between the inked margin and the tumour, to assign the mean value of the thickness of the peri-tumoural healthy tissue [14]. Histological subtypes and nuclear grade were defined according to the WHO classification [15] and Fuhrman classification [16] systems, respectively. Positive surgical margins (PSMs) were defined as cancer cells at the level of the inked parenchymal excision surface [14, 17].

Patients with a final diagnosis of RCC were generally observed every 3–4 months for the first year after LPN and every 6 months from the second to the fifth years. Oncological follow-up consisted of a history, a physical examination and an abdominal evaluation using ultrasonography or CT, according to the risk of recurrence. Elective bone scan, chest CT and MRI were performed when clinically indicated.

Mean (sd) values were used to report continuous variables. Frequencies and proportions were used for categorical variables. The means of continuous variables were compared using the Mann–Whitney U-test. Kruskall–Wallis anova was used to compare the means of more than two groups. A one-way anova was used to test the effect of a single categorical variable on the dependent variable. Factorial anova was used to analyse the simultaneous interactive effects of multiple categorical variables on the considered dependent variable. All tests were two-sided, and a P value <0.05 was considered to indicate statistical significane. All statistical analyses were performed using Statistic 8 (Statsoft Inc., Tulsa, OK, USA).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

In all, 96 patients who did not meet the inclusion/exclusion criteria were excluded from the analysis (two because they had a solitary kidney, 10 because they had undergone a robot-assisted procedure and 84 because they had undergone a clampless procedure); thus, the study consisted of 206 patients who underwent conventional LPN. According to quartiles distribution, patients #1–51 were in LPN era 1 (September 2001 to April 2006), patients #52–102 were in LPN era 2 (May 2006 to July 2008), patients #103–153 were in LPN era 3 (June 2008 to October 2010) and patients #154–206 were in LPN era 4 (November 2010 to September 2012). Demographic, preoperative, peri-operative and postoperative data are shown in Table 1. Complications and pathological results are shown in Table 2. The overall PSM and complication rates were 2.9% (6/206 patients) and 16.5% (34/206 patients), respectively, while the major (Clavien grade > II) complication rate was 5.8% (12/206 patients). The mean (sd) WIT was 22.6 (8.6) min, and a WIT duration >20 min was found in 34.0% of patients (70/206). The demographic and peri-operative data were very similar across different LPN eras. The use of haemostatic agents was systematically introduced from LPN era 2 as shown in Table 1, regardless of tumour anatomical characteristics. The most frequently used haemostatic agent was Floseal (Baxter, Deerfield, IL, USA).

Table 1. Demographic, preoperative, peri-operative and postoperative results
 OverallLPN era 1LPN era 2LPN era 3LPN era 4P
N = 206N = 51N = 51N = 51N = 53
  1. ASA, American Society of Anesthesiologists.

Mean (sd) age, years60.3 (14.0)63.2 (11.0)57.5 (15.0)58.2 (14.0)62.1 (12.0)0.166
Males, n (%)132 (64.0)29 (56.9)29 (56.9)38 (74.5)36 (67.9)0.058
Mean (sd) body mass index, kg/m226.6 (3.8)27.1 (4.1)27.0 (4.3)26.6 (4.5)25.8 (3.7)0.221
ASA score ≥3, n (%)112 (54.4)25 (49.0)28 (54.9)30 (58.8)29 (54.7)0.313
Mean (sd) Charlson comorbidity index score1.1 (1.5)1.1 (1.2)1.0 (1.3)1.1 (1.6)0.9 (1.5)0.465
Mean (sd) CT scan size, cm3.3 (1.4)3.2 (1.2)3.2 (1.3)3.2 (1.8)3.5 (1.4)0.101
Right-sided lesions, n (%)108 (52.4)26 (51.0)29 (56.9)21 (41.2)32 (60.4)0.053
Mean (sd) PADUA score7.2 (1.6)6.4 (0.6)6.7 (1.0)7.3 (1.8)8.3 (1.8)<0.001
PADUA-score risk group categories, n (%)      
1155 (75.2)47 (92.2)45 (88.2)38 (74.6)25 (47.2)<0.001
224 (11.7)4 (7.8)5 (9.8)4 (7.8)11 (20.7)0.065
327 (13.1)0 (0.0)1 (2.0)9 (17.6)17 (32.1)<0.001
Retroperitoneal approaches, n (%)126 (61.2)24 (47.0)32 (62.7)32 (62.7)38 (71.7)0.012
Mean (sd) operating time, min119.6 (32.0)117.0 (32.2)123.9 (29.3)119.2 (34.9)118.4 (31.8)0.217
Mean (sd) WIT, min22.6 (8.6)29.1 (8.3)23.7 (8.9)19.8 (6.7)18.1 (5.9)<0.001
Mean (sd) estimated blood loss, mL174.8 (122.8)188.8 (87.9)169.1 (139.2)126.5 (112.3)217.5 (131.4)0.003
No. use of haemostatic agents (%)152 (73.8)7/51 (13.7)42/51 (82.3)50/51 (98.0)53/53 (100.0)<0.001
Mean (sd) duration of hospitalization, days6.0 (1.8)6.1 (0.9)6.5 (2.8)5.9 (1.4)5.3 (0.9)0.085
Table 2. Complications and pathological results
 OverallLPN era 1LPN era 2LPN era 3LPN era 4P
N = 206N = 51N = 51N = 51N = 53
Complications, n (%)34 (16.5)12 (23.5)10 (19.6)4 (7.8)9 (16.9)0.032
Clavien > II, n (%)12 (5.8)3 (5.9)5 (9.8)2 (3.9)2 (3.8)0.241
Death from respiratory illness11 
Acute bleeding73311 
Peri-renal haematoma11 
Urine leakage111 
Management of Clavien > II      
Embolization 2 (Clavien III)2 (Clavien III)1 (Clavien III)1 (Clavien III) 
Reoperation 1 (Clavien IV)2 
JJ stenting 11 (Clavien III) 
Malignant, n (%)143 (69.4)28 (54.9)36 (70.6)43 (84.3)36 (67.9)0.002
PSM, n (%)6 (2.9)2 (3.9)1 (1.9)1 (1.9)2 (3.8)0.548
Mean (sd) thickness of peri-tumoural healthy tissue, mm2.6 (1.9)2.5 (1.3)2.5 (1.5)2.4 (2.3)2.7 (2.2)0.415

Patients were similar across LPN eras in terms of baseline serum creatinine and eGFR, and no differences in these variables were found postoperatively either (Table 3). The overall MIC rate was 63.1% (130/206 patients). The MIC rate was significantly correlated with the LPN era (P < 0.001, Fig. 1A): it increased progressively along the learning curve: 15/51 patients (29.4%), 30/51 patients (58.8%) 40/51 patients (78.4%) and 45/53 patients (84.9%) in LPN eras 1, 2, 3 and 4, respectively. Seven, three, two and three patients did not achieve two goals included in the MIC system in LPN eras 1, 2, 3 and 4, respectively. An inverse correlation between MIC score and PADUA-score risk categories was observed (P = 0.001, Fig. 1B). When simultaneously considering the effects of both LPN era and PADUA-score risk group categories, a trend towards an increased MIC rate was found (Fig. 1C). When MIC score components were analysed separately, WIT decreased significantly from LPN era 1 to LPN era 4 (P < 0.001, Fig. 2A) and from PADUA-score risk group categories 3 to 1 (P = 0.001, Fig. 2B). Interestingly, WIT decreased in proportion to more recent LPN eras regardless of PADUA score when simultaneously considering both variables, but this correlation was not significant (P = 0.401, Fig. 2C).

figure

Figure 1. anova performed on MIC rate and A, LPN eras (one-way anova), B, PADUA-score risk group categories (one-way anova) and C, both LPN eras and PADUA-score riskgroup categories.

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figure

Figure 2. anova performed on: WIT and A, LPN eras (one-way anova), B PADUA-score risk group categories (one-way anova) and C, both LPN eras and PADUA-score risk group categories (the effect of LPN eras and PADUA-score risk group categories are considered simultaneously); complications rate and D, LPN eras (one-way anova), E, PADUA-score risk groups categories (one-way anova) and F, both LPN eras and PADUA-score risk group categories (the effect of LPN eras and PADUA-score risk group categories are considered simultaneously); and PSM rate and G, LPN eras (one-way anova), H, PADUA-score risk group categories (one-way anova) and I, both LPN eras and PADUA-score risk group categories (the effect of LPN eras and PADUA score risk-group categories are considered simultaneously).

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Table 3. Functional results
 OverallLPN era 1LPN era 2LPN era 3LPN era 4P
N = 206N = 51N = 51N = 51N = 53
Mean (sd) serum creatinine, mg/dL      
Baseline0.96 (0.21)0.98 (0.23)0.95 (0.18)0.93 (0.19)0.94 (0.20)0.450
(t-test P value)(0.532)(0.301)(0.586)(0.614)(0.234)
3 months after LPN0.94 (0.19)0.93 (0.15)0.95 (0.16)0.91 (0.19)0.93 (0.18)0.308
Mean (sd) estimated GFR, mL/min      
Baseline91.9 (21.7)93.3 (21.1)91.5 (24.3)89.6 (22.5)91.4 (18.5)0.194
(t-test P value)(0.375)(0.293)(0.199)(0.275)(0.578)
3 months after LPN90.3 (22.7)91.7 (25.0)90.9 (20.2)88.6 (19.4)90.2 (18.3)0.326

A trend towards a decrease in the complication rate along the learning curve was observed, although it was not significant (P = 0.251, Fig. 2D). Conversely, complications were significantly correlated with PADUA-score risk group categories (P < 0.001, Fig. 2E). In the simultaneous analysis, LPN era and PADUA score together significantly influenced the complications rate (P < 0.001, Fig. 2F). PSMs were not correlated with LPN era (P = 0.213, Fig. 2G) or PADUA-score risk group categories (P = 0.863, Fig. 2H), and the same result was observed when both predictive variables were analysed together (P = 0.319, Fig. 2I).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

When different approaches are available for a single procedure, standardized outcome reporting is of critical importance for evaluating and comparing the efficacy of these different approaches. This is especially true for PN, which has become the gold standard treatment of small, localized tumours, leading to the same oncological results and less LRF compared with radical nephrectomy [7, 18-20]. Three major issues are widely used to report PN outcomes (oncological results, complications and functional results), but these variables have always been considered separately, which makes the comparison of the results of the different techniques (and different surgeons) more difficult. Commonly, the surgical margin status has been considered an early good surrogate of oncological outcomes. A negative surgical margin, defined as the absence of cancer cells at the level of the inked parenchymal excision surface, is the first goal of PN. Nevertheless, intermediate follow-up data indicate that the majority of patients with PSMs will not experience local or distant tumour recurrence, while the combination of a highly malignant tumour and PSM status seems to increase the risk of local recurrence [21]. Regarding the safety profile, the Clavien system seemed to be an appropriate tool to standardize the reporting of complications after the vast majority of surgical interventions, and it has already been successfully used for PN [6, 9, 12, 22]. In this system, major complications (grade III, which require surgical, endoscopic or radiological intervention, and grade IV, which are considered life-threatening complications) are clearly identified and fit well with the possible complications of LPN. The reporting of functional results after PN is still a challenge for researchers. LRF after PN is a multifactorial, complex process, and it is related to unmodifiable (age, comorbidities, preoperative renal function) and modifiable (duration of ischaemia, sacrifice of unaffected nephrons) factors. Furthermore, the measurement of LRF is difficult after PN. Serum creatinine and estimated GFR are commonly used, but the functioning contralateral may influence the results. By contrast, renal scintigraphy is the most reliable tool, but it is rarely used in clinical practice [22-24]. Because WIT, together with quality and quantity of renal parenchyma, is among the most important factors in determining LRF and because it is easily measurable, the duration of ischaemia is commonly used as an ‘index’ of renal damage. Although every minute is crucial in determining postoperative renal ischaemic damage, many authors, including our group, have suggested that the critical threshold for WIT is ∼20–25 min [22, 25].

In an effort to achieve the standardization of reporting PN results, and using a single variable rather than three different ones, the combined binary evaluation of MIC has recently been introduced [6]. Because we believed that the MIC rate could potentially be helpful in a research setting, we retrospectively reviewed our LPN database and re-classified and analysed our data on the basis of this new system to report these data in a standardized manner. Overall, we analysed the data of 206 patients treated with a conventional LPN technique. Because all of the procedures were performed by the same surgeon, we avoided the bias of different surgeons. Furthermore, to limit the bias of different techniques, we excluded all patients treated with robot-assisted PN and those treated with a clampless technique, in which the goal of ischaemia <20 min would be reached by definition. Based on these criteria, we believe that our data were homogeneous. We then divided the population of the study on the basis of chronological criteria (LPN eras) to evaluate the effects of the surgeon's experience on the MIC rate. Overall, the MIC rate was 63.1%, and it progressively increased along the learning curve to 84.9% in LPN era 4, which was consistent with published data on robot-assisted PN [6]. Because the MIC rate could be affected by anatomical and topographic features of treated tumours (i.e. more complex tumours should have a lower MIC rate than less complex ones), we stratified the MIC rates according to PADUA-score risk group categories; our results showed that the MIC is not achieved as often with higher PADUA scores (P < 0.001). When the three components included in the MIC system were analysed separately, PSMs were not correlated with LPN era or PADUA score. This result means that, at least in our experience, once the technique has been standardized, PSM rates are not an important factor during LPN, and they are established at acceptable levels and are similar to PSM rates with open surgery. The complication rate increased significantly with an increase in PADUA score, and we observed a trend towards a reduction in complications beginning from the third LPN era. This result confirmed that LPN is a challenging technique that requires a long learning curve to significantly improve its safety; however, interestingly, complications were associated with both LPN era and PADUA score: they showed a reduction throughout the learning curve regardless of the more challenging cases treated. WIT was significantly correlated with both LPN era and PADUA score (P < 0.001), and it seemed to play a crucial role in discriminating whether the ‘kidney trifecta’ was achieved in the vast majority of cases. Overall, MIC seems to be simple to use and reproducible, and could allow easy comparison among different case studies from different centres and surgeons.

Although the MIC system is simple, it has limitations. Like all binary systems, the threshold chosen by the authors is arbitrary. For example, the chosen threshold for WIT could be a matter of debate. Indeed, the MIC rate changes radically if the threshold for WIT is increased to 25 min, which many authors consider safe in terms of LRF [22, 25]. In addition, the use of the MIC system when a clampless technique is performed is questionable. Buffi et al. [6] highlighted that in these settings, ‘the ischaemia goal’ of the system would be reached by definition, and this could imply a distortion of the MIC system. Nevertheless, the primary potential drawbacks of the clampless technique are a higher complication rate (i.e. bleeding) and higher PSM rate resulting from the loss of visualization of the resection bed during mass excision and so the advantage of reaching one goal by definition (ischaemia) would be counterbalanced by the potential risk of not reaching the other goals (margins and complications). On the basis of these considerations, we believe that the MIC can be used even when a clampless approach is selected. In addition, using WIT itself as surrogate of LRF is questionable. The same durations of WIT can lead to different post-PN outcomes in different patients. Theoretically, to assess PN outcomes, the amount of LRF should be assessed rather than the duration of WIT, but in the present case study, patients who underwent LPN with WIT <20 min did not experience a significant postoperative decrease in either serum creatinine or estimated GFR. Furthermore, as more complex tumours should have a lower MIC rate than less complex ones, the MIC score should always be ‘corrected’ by risk group categories based on standardized classification systems (PADUA/RENAL/C-index scores). Finally, the introduction of the MIC system raised the question of the recommended score. For example, if we consider a MIC score >80% as adequate, in our experience, this result is reached after 150 procedures.

The present study has some limitations. Although extracted from a prospectively maintained database, the data were analysed in a retrospective fashion. Furthermore, like all single-centre single-surgeon studies, it does not reflect a real-life situation and has limited reproducibility, especially in terms of the learning curve.

In our experience, the MIC system was an easy, useful and reproducible tool for reporting the results of our data series. The MIC rate increased with the surgeon's experience and decreased when complex lesions were treated. Using the MIC system as a tool for the assessment of LPN outcomes, we confirm that LPN is a technically challenging procedure requiring a long learning curve, and ∼150 procedures are required to obtain an acceptable (>80%) MIC rate, regardless of tumour anatomical characteristics. Despite its intrinsic limitations, we believe that the MIC system will be effective in more appropriately comparing the early results of different approaches and surgical techniques currently used to perform PN. With this aim in mind, we think that it could be a helpful tool to assess PN outcomes.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References
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