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Laparoscopic Partial Nephrectomy: A Matched-pair Comparison of the Transperitoneal Versus the Retroperitoneal Approach
Laparoscopy and Robotics Laparoscopic Partial Nephrectomy: A Matched-pair Comparison of the Transperitoneal Versus the Retroperitoneal Approach Martin Marszalek, Thomas Chromecki, Badereddin Mohamad Al-Ali, Herbert Meixl, Stephan Madersbacher, Klaus Jeschke, Karl Pummer, and Richard Zigeuner OBJECTIVES
METHODS
RESULTS
CONCLUSIONS
To compare surgical and functional results of both surgical approaches to endoscopic partial nephrectomy. It is currently performed either by the transperitoneal (t) or the retroperitoneal (r) approach. This was a retrospective, matched-pair comparison of 105 patients who underwent either transperitoneal laparoscopic (Graz) or retroperitoneoscopic (Klagenfurt) partial nephrectomy for clinical T1a renal masses. A total of 35 patients after transperitoneal laparoscopic and 70 patients after retroperitoneoscopic partial nephrectomy were included to this analysis after matching for age (T: 59.3 vs R: 60.1 a), preoperative glomerular filtration rate (GFR) (T: 93.2 vs R: 96.1 mL/min) and tumor size (T: 2.4 vs R: 2.5 cm). Nephrometry scores were comparable between groups and were low, medium, and high in 54.3%, 45.7%, and 0% (t) and 55.7%, 42.9%, and 1.4% (r) of patients (P ⫽ .9). Operative time (T: 139.3 minutes vs. R: 83.9 minutes; P ⬍ .001) and hospitalization (T: 7 days, R: 5 days; P ⬍ .001) were shorter in the retroperitoneoscopic group. Ischemia time (T: 24.3 minutes, R: 22.6 minutes) and postsurgical GFR (T: 86.6 vs R: 90.0 mL/min), postsurgical GFR-decrease (T: 7.1%, R: 6.2%, P ⫽ .9) and decline of hemoglobin (T: 17.1%, R: 16.6%) were comparable. Complications were 4 nephrectomies (T: n ⫽ 1, R: n ⫽ 3), 2 revisions for hemorrhage (R: n ⫽ 2), 4 pneumothorax (R: n ⫽ 4), and 2 urinary fistulas (T: n ⫽ 2). The positive surgical margin rate was comparable between groups (T: n ⫽ 3, R: n ⫽ 5). Transperitoneal laparoscopic and retroperitoneoscopic partial nephrectomy provide comparable surgical and functional results. One advantage of the retroperitoneoscopic access seems to be a shorter total surgical time. UROLOGY 77: 109 –113, 2011. © 2011 Elsevier Inc.
E
ndoscopic partial nephrectomy (PN) is increasingly offered as an alternative to the open approach for T1a renal masses. To ensure proper outcomes in terms of ischemia and surgical margin status, accessibility of the tumor and renal hilum are essential. Localization of the renal mass and experience of the surgeon will predict the use of the transperitoneal or retroperitoneal approach in most cases.1,2 As select tumors may be accessible by either route, specific advantages and limitations of both approaches have to be considered, and differences in working space, port placement, and the corresponding angulation of laparoscopic
instruments accounted for by diligent patient selection.3 The respective benefits and disadvantages of laparoscopic and retroperitoneoscopic approach to renal masses have been addressed before.4-6 However, these 3 studies available to date are hampered by a small sample size4 or differences in tumor size.5,6 We have therefore performed a matched-pair comparison to provide more reliable information on surgical and clinical outcomes and particular complications that can be expected with either approach.
MATERIAL AND METHODS Patients
From the Department of Urology, Klagenfurt General Hospital, Klagenfurt, Austria; Department of Urology and Andrology, Danube Hospital, Vienna, Austria and Department of Urology, Medical University of Graz, Graz, Austria Reprint requests: Martin Marszalek, M.D., Department of Urology and Andrology, Donauspital, Langobardenstrasse 122, A-1220 Vienna, Austria. E-mail: [email protected] Submitted: December 16, 2009, accepted (with revisions): February 16, 2010
© 2011 Elsevier Inc. All Rights Reserved
In total, 105 patients who underwent endoscopic partial nephrectomy for incidentally discovered renal masses were included to this matched-pair analysis. All transperitoneal procedures were performed at the Department of Urology of the Graz Medical University, Styria, Austria by 1 experienced surgeon over a period of 4 years. All retroperitoneal procedures were 0090-4295/11/$36.00 doi:10.1016/j.urology.2010.02.057
109
performed at the Department of Urology of the Klagenfurt General Hospital, Carinthia, Austria by 2 experienced surgeons over a period of 5 years; some of these cases have been part of a previous analysis.7 In both groups, renal sonography, chest x-ray, and abdominal contrast medium– enhanced computed tomographic scans were included in the preoperative workup of each patient. In select cases not elegible for contrast medium application, magnetic resonance imaging studies were performed. Pre- and postoperatively, blood sample analyses, including serum creatinine, blood urea nitrogen, and hemoglobin serum levels were performed. Institutional review board approval was obtained.
Surgical Technique The technique of retroperitoneoscopic partial nephrectomy has been described previously.7 In brief, with the patient in a full flank position, a retroperitoneal cavity was formed from a small incision in the lumbar triangle and a Hasson trocar introduced. Two additional ports (12 and 5 mm) were placed at the discretion of the surgeon. Renal arteries were clamped with endobulldog clamps followed by excision of the tumor with a choledochotom (Karl Storz, Tuttlingen, Germany) and scissors. Hemostasis was achieved by central suturing with application of fibrin glue (Baxter International, Deerfield, IL) and 3-5 additional parenchymal sutures. An endobag was used to retrieve the specimen. The technique of transperitoneal partial nephrectomy has also been described previously.8 In brief, pneumoperitoneum was established by insertion of a 12-mm camera trocar via a mini-laparotomy. With the patient in a 30-degree elevated flank position, this port was placed supraumbilical, or paramedian in obese patients. Consecutively, 2 12-mm working ports were introduced at the discretion of the surgeon. For right-sided partial nephrectomies, an additional 5-mm port was introduced below the xyphoid for retraction of the liver. Dissection of the ascending and descending colon and the kidney was performed by an Ultracision device (Ethicon Endo-Surgery, Cincinnati, OH). Renal arteries were clamped by endobulldog clamps and excision of the tumor was performed with scissors. Hemostasis was also achieved by central suturing, autologous fibrin glue (Vivostat; Vivostat A/S, Alleroed, Denmark)8 and parenchymal sutures and the specimen retrieved by an endobag. A perirenal drain was placed routinely in all patients of both cohorts. No intraoperative frozen section analysis was performed with either procedure. As no intracorporal cooling method was used, all procedures were performed in warm ischemia.
Perioperative and Renal Function Analysis Perioperative blood loss was determined by change in serum hemoglobin levels. Renal function was assessed by pre- and postoperative assessment of serum creatinine and estimation of respective glomerular filtration rates (GFR) using the Mayo Clinic Quadratic Equation (MCQE).9 Intra- and postoperative complications and surgical revisions are reported.
Statistical Analysis A matched-pair analysis was performed comparing data for 35 patients after endoscopic transperitoneal and 70 patients after endoscopic retroperitoneal partial nephrectomy. The population available for the matching process consisted of 2 consecutive series of patients who underwent endoscopic PN for 110
clinical T1a renal masses (transperitoneal: n ⫽ 52, retroperitoneal: n ⫽ 150). Each patient in the transperitoneal group was matched to 2 corresponding patients of the retroperitoneoscopic group, with regard to age, preoperative glomerular filtration rate, and tumor size. Clinical stage of renal cell cancer was T1a in all cases. Tumor localization was compared between groups by calculation of the recently developed RENAL nephrometry scores.10 Both groups were compared regarding surgical and clinical outcome variables. Continuous variables were compared by t test or Wilcoxon rank-sum test, with results presented as means and standard error (SE) when the t test was used and as median and quartiles (25th and 75th percentiles) when the Wilcoxon rank-sum test was used. Comparison of categorical variables was performed by Person chi-square test and Fisher exact test. All statistical analysis were performed using the Statistical Package for the Social Sciences 16 (SPSS Inc., Chicago, IL), with a two-tailed value of P ⬍ .05 considered to indicate statistical significance.
RESULTS Patient Characteristics A total of 105 patients who underwent transperitoneal or retroperitoneal partial nephrectomy were matched for age, preoperative glomerular filtration rate, and tumor size. Mean age at surgery was 59.3 ⫾ 1.9 years in the transperitoneal and 60.1 ⫾ 1.3 years in the open group (P ⫽ .8). Gender distribution was identical in both series (P ⫽ .8) (Table 1). Mean tumor size was 2.4 ⫾ 0.1 cm (range: 1.2-4.0 cm) in the transperitoneal and 2.4 ⫾ 0.1 (range: 1.2-4.0 cm) in the retroperitoneal group (P ⫽ .8). Nephrometry scores were comparable in both groups (P ⫽ .8), such as for the laterality of the affected kidney (P ⫽ .2) (Table 1). Surgical Outcomes Total surgical time (skin incision to skin closure) was shorter in the retroperitoneal compared with the transperitoneal group (P ⬍ .001). Arterial occlusion time was comparable in both groups (P ⫽ .2). Ischemia time was similar in malignant and benign tumors in transperitoneal (23.4 ⫾ 1.2 minutes [range: 12-43 minutes] vs 27.0 ⫾ 3.5 minutes [range: 16-45 minutes]; P ⫽ .2) and retroperitoneal PN (22.8 ⫾ 0.6 minutes [range: 13-37 minutes] vs 21.3 ⫾ 0.9 minutes [range: 15-27 minutes]; P ⫽ .5). After retroperitoneal PN, hospitalization was shorter compared with the transperitoneal approach (5 days [IQR: 5-6 days] vs 7 day [IQR: 5.8-8.3 days]; P ⬍ .001). Serum hemoglobin declined after transperitoneal PN by 17.1 ⫾ 1.4% from 14.6 ⫾ 0.2 g/dL (range: 12.0-17.8 g/dL) before surgery to 12.1 ⫾ 1.8 g/dL (range: 8.1-16.1 g/dL) after surgery (24 hours after surgery; P ⬍ .001); after retroperitoneal PN hemoglobin declined by 16.6 ⫾ 1.0% from 14.6 ⫾ 0.2 g/dL (range: 9.2-17.8 g/dL) to 12.1 ⫾ 0.2 g/dL (range: 8.2-14.8 g/dL) (P ⬍ .001). These changes from pre-to postoperative serum hemoglobin levels were comparable in both groups (P ⫽ .8). Transfusion rate was 5.7% in the transperitoneal and 5.1% in the retroperitoneal group (P ⫽ .9) (Table 2). UROLOGY 77 (1), 2011
Table 1. Principal characteristics of the study population
Mean age, yrs (range) Sex (male/female), % Mean patient BMI, kg/m2 (range) Laterality (right/left), % Nephrometry scoresⴱ Median tumor size cm, (IQR) Endophytic/exophytic tumors Exophytic (⬎50%), % Exophytic (⬍50%), % Entirely endophytic, % Nearness of tumor to sinus/calyx ⱖ7 mm, % ⬎4 mm but ⬍7 mm, % ⱕ4 mm, % Anterior/posterior tumors Anterior, % Posterior, % Location relative to upper/lower polar line Entirely above/below upper/lower polar line, % Crosses polar line, % ⬎50% across polar line or crosses axial midline or tumor entirely between polar lines, % Contact to first-order vessel in the renal hilum, % Total scoreⴱ (range) Complexity of surgical procedure according to nephrometry score Low, % Medium, % High, %
Transperitoneal (n ⫽ 35)
Retroperitoneal (n ⫽ 70)
59.3 (43.8/78.0) 65.7/34.3 27.9 (22.1/40.0) 48.6/51.4
60.1 (41.5/80.6) 62.9/37.1 27.1 (20.0/36.3) 57.1/42.9
2.4 (1.7/3.0)
2.5 (1.8/3.0)
62.8 (n ⫽ 22) 34.3 (n ⫽ 12) 2.9 (n ⫽ 1)
65.7 (n ⫽ 46) 31.4 (n ⫽ 22) 2.9 (n ⫽ 2)
34.3 (n ⫽ 12) 31.4 (n ⫽ 11) 34.3 (n ⫽ 12)
35.7 (n ⫽ 25) 32.9 (n ⫽ 23) 31.4 (n ⫽ 22)
54.3 (n ⫽ 19) 45.7 (n ⫽ 16)
65.7 (n ⫽ 46) 34.3 (n ⫽ 24)
37.1 (n ⫽ 13) 28.6 (n ⫽ 10) 34.3 (n ⫽ 12)
44.3 (n ⫽ 31) 24.3 (n ⫽ 17) 31.4 (n ⫽ 22)
2.9 (n ⫽ 1) 6.33 (4-9)
0 (n ⫽ 0) 6.25 (4-10)
54.3 (n ⫽ 19) 45.7 (n ⫽ 16) 0 (n ⫽ 0)
55.7 (n ⫽ 39) 42.9 (n ⫽ 30) 1.4 (n ⫽ 1)
P Value .8 .3 .2 .8 .9
.9
.3 .6
.8 .9
BMI, body mass index; IQR, interquartile range; RENAL, nephrometry score.10
Table 2. Perioperative results
Median hospitalization, days (IQR) Mean operative time, min (range) Mean arterial occlusion time, min (range) Blood loss, % (mean decline in % of baseline hemoglobin) Overall complication rate, %
Transperitoneal (n ⫽ 35)
Retroperitoneal (n ⫽ 70)
P Value
7 (5.8/8.3) 139.3 (90/190) 24.3 (12/45) 17.1 8.6
5 (5.0/6.0) 83.9 (50/165) 22.6 (13/37) 16.6 14.3
⬍.001 ⬍.001 .2 .8 .5
IQR, interquartile range.
Table 3. Renal function outcomes in patients after endoscopic partial nephrectomy
2
Mean preoperative (GFR ml/min/1.72 m ) Mean postoperative (GFR ml/min/1.72 m2) Decline in GFR from pre- to postoperative (GFR ml/min/1.72 m2) Relative decline in GFR from pre- to postoperative %
Transperitoneal
Retroperitoneal
P Value
93.2 ⫾ 3.7 (50.7-128.6) 86.6 ⫾ 3.2 (46.6-123.9) 6.6 ⫾ 2.3
96.1 ⫾ 2.3 (52.5-134.0) 90.0 ⫾ 2.9 (42.7-130.8) 6.1 ⫾ 2.3
.5 .5 .9
7.1 ⫾ 3.0
6.3 ⫾ 2.7
.9
GFR, glomerular filtration rate. Values are mean ⫾ standard error (range).
Renal Function Preoperative glomerular filtration rate was similar in both groups (P ⫽ .5), as was postoperative GFR (24 hours after surgery; P ⫽ .5) (Table 3). A significant decline from pre-to postoperative GFR was observed in the transperitoneal (7.1%, P ⫽ .007) and retroperitoneoscopic group UROLOGY 77 (1), 2011
(6.2%, P ⫽ .01). This decline was comparable in both groups (P ⫽ .9) (Fig. 1). Pathologic Outcomes and Surgical Margin Status In the final histopathologic evaluation, 25.7% of tumors in the transperitoneal group and 18.6% in the retroperitoneal 111
Figure 1. Pre- and postoperative glomerular filtration rate (mL/min/1.73 m2) in patients undergoing endoscopic partial nephrectomy. Results are given for the transperitoneal and the retroperitoneal group.
group were benign (P ⫽ .5). All malignant tumors were pT1a stage renal cell carcinomas except 1 metastasis of malignant melanoma in the transperitoneal group. The rate of positive surgical margins in the matched population was comparable between groups (transperitoneal PN: 8.6% [n ⫽ 3]; retroperitoneal PN: 7.1% [n ⫽ 5], P ⫽ .8). However, the positive margin rate in the overall consecutive series of unmatched patients was 5.8% after transperitoneal and 4.7% after retroperitoneal PN. Complications Three patients undergoing transperitoneal (t) PN developed 3 complications (overall complication rate: 8.6%). In the retroperitoneal (r) group, 8 patients experienced a total of 10 complications (overall complication rate: 14.3%, P ⫽ .5). Complications were pneumothorax (T: n ⫽ 0, R: n ⫽ 4), urinary leakage (T: n ⫽ 2, R: n ⫽ 0) and postoperative development of subcutaneous hematoma (T: n ⫽ 0, R: n ⫽ 1). In the transperitoneal group, postoperative bleeding was managed conservatively in 1 patient (2.9%) by transfusion of 2 U of packed red blood cells. Another patient underwent revision for severe hemorrhage, resulting in nephrectomy. After retroperitoneoscopic PN, 5 patients underwent revision for severe hemorrhage, 3 (4.3%) of which resulted in nephrectomy. The underlying cause of severe hemorrhage prompting acute surgical reintervention was arterial bleeding as confirmed on emergently performed abdominal CT scan in all cases.
COMMENT The principal finding of this matched-pair analysis was a comparable surgical and functional outcome after transperitoneal laparoscopic and retroperitoneoscopic PN. Endoscopic PN can be performed via transperitoneal and retroperitoneal approach, each providing specific advantages and disadvantages.4 Arguments in favor of the 112
transperitoneal route are the larger working space, allowing for wider angulation and maneuverability with laparoscopic instruments, and the more accustomed orientation by familiar anatomic landmarks.4,5 Intra-abdominal adhesions, which might develop as result of laparoscopic surgical procedures, usually appear to be of minor clinical significance.11 Retroperitoneoscopy, by avoiding bowel mobilization, seems to provide a more direct access to the kidney and the renal hilum.4 Drawbacks are the spatial limitations of the narrow retroperitoneal working space, the lack of view, and the risk of disorientation.12 Select tumors may be approached by either route, according to the surgeon’s preference. However, similar to open surgery, indication and patient selection for either access have to be carefully considered by the endoscopic surgeon, with tumor localization as most important decisive factor: this fact also obviates a randomized study design, which, besides the limited sample size and the lack of long-term follow-up, is recognized as shortcoming of the present retrospective analysis. Furthermore, transperitoneal and retroperitoneal PN were performed by experienced laparoscopic surgeons, but at different institutions, a limitation of the present study that has to be considered when interpreting the data provided. As indicated by the results presented by the Cleveland Clinic Foundation, 1 advantage of the retroperitoneal route seems to be a shorter total operative time; Ng et al reported an operative time of 3.5 hours for laparoscopic PN compared with 2.9 hours for the retroperitoneoscopic procedure6 However, patients in this analysis were not pair matched, and transperitoneally accessed tumors were significantly larger (3.1 vs 2.6 cm; P ⫽ .004). Although retroperitoneoscopic PN was also the less time-consuming procedure, operative times of both, the trans- and retroperitoneal group, were shorter in our series when compared with the results of Ng et al..6 This may in part reflect the interim refinement of the surgical technique and, at least with the retroperitoneal approach, the extensive expertise of the respective surgeons. Also, others reported comparable results, in terms of shorter retroperitoneoscopic operative time, in line with our findings.4,5 It has been consistently shown that prolonged arterial occlusion time exceeding 30 minutes of warm ischemia will exert a significant negative influence on renal function.13,14 Furthermore, recent data recommend even shorter ischemic periods of 20 minutes to prevent persistent renal damage.15 Therefore, it is crucial to keep ischemia short, even more as local hypothermia in endoscopic PN remains a sophisticated challenge.16 Ng et al. observed longer ischemia times of 31 minutes with the transperitoneal approach compared with 28 minutes with the retroperitoneal approach.6 As mentioned before, tumors in their analysis were larger in the transperitoneal group, which might well have contributed to these results. We did not observe an advantage for either approach, trans- or retroperitoneal, considering ischemia time. This is underlined by the work of Wright et al, who UROLOGY 77 (1), 2011
observed similar ischemia times of 32 minutes in both groups.4 In another comparative study, Kieran et al, also found comparable arterial occlusion times in patients undergoing endoscopic trans- or retroperitoneal PN (25.6 vs 22.7 minutes; P ⫽ .3).5 Again, tumors in their study were larger in the transperitoneal group (2.7 vs 2.1 cm; P ⫽ .03). Besides ischemia, compelling evidence suggests a negative impact of pneumoperitoneum and pneumoretroperitoneum on hemodynamic and ventilatory parameters as well as intraoperative renal blood flow and renal function.7,17,18 Although present with either route of access, these negative effects seem to be less pronounced with the retroperitoneal approach.17 We observed a significant pre- to postoperative decrease of glomerular filtration rate of roughly 5% in both groups. This similar decrease suggests a comparable clinical impact of gas insufflation on renal function, regardless of the approach chosen. Kieran et al found a postoperative increase of serum creatinine levels (⫹ 0.11 mg/dL) after both, transand retroperitoneoscopic PN (P ⫽ .96),5 an observation that is in line with our findings. In a recent analysis, Kieran et al presented perioperative complications of trans- and retroperitoneal PN,5 revealing comparable overall complication rates of 22% and 19%, respectively. We were able to confirm their results of similar overall complication rates for either surgical approach, however we experienced different types of complications: Kieran et al mainly observed postoperative hemorrhage in both groups (transperitoneal: 13.3%, retroperitoneal: 11.1%) as well as bowel related complications in the transperitoneal group (6.7%).5 Whereas postoperative hemorrhage was also prevalent with both approaches, we did not find bowelrelated complications in our analysis. However, pneumothorax in the retroperitoneal and urinary leakage prompting ureteral stenting in the transperitoneal group were additional complications observed in our study. Pleural entry was also reported in the comparative analysis of the Cleveland Clinic group (1% with the transperitoneal route) as well as urinary leakage rates of 4% and 3% after laparoscopic and retroperitoneoscopic PN.6 At least the higher pleural entry rates that we observed with the retroperitoneoscopic approach may in part reflect the surgeons’ need to compensate the limitations of the narrow retroperitoneal space. In our series, intercostal port placement may well acount for this particular complication.
CONCLUSIONS According to our experience, transperitoneal and retroperitoneal endoscopic PN provide similar surgical and functional results. Appropriate selection of surgical access facilitates tumor resection, resulting in comparable
UROLOGY 77 (1), 2011
ischemia times for either approach. The specific challenges of the retroperitoneal route must not be underestimated by the endoscopic surgeon. However, 1 particular advantage of this approach seems to be a shorter total surgical time. References 1. Winfield HN, Donovan JF, Lund GO, et al. Laparoscopic partial nephrectomy: initial experience and comparison to the open surgical approach. J Urol. 1995;153:1409-1414. 2. Gill IS, Delworth MG, Munch LC. Laparoscopic retroperitoneal partial nephrectomy. J Urol. 1994;152:1539-1542. 3. Singh D, Rubenstein M, Gill IS. Laparoscopic partial nephrectomy. J Endourol. 2005;19:451-455. 4. Wright JL, Porter JR. Laparoscopic partial nephrectomy: comparison of transperitoneal and retroperitoneal approaches. J Urol. 2005; 174:841-845. 5. Kieran K, Montgomery JS, Daignault S, et al. Comparison of intraoperative parameters and perioperative complications of retroperitoneal and transperitoneal approaches to laparoscopic partial nephrectomy: support for a retroperitoneal approach in selected patients. J Endourol. 2007;21:754-759. 6. Ng CS, Gill IS, Ramani AP, et al. Transperitoneal versus retroperitoneal laparoscopic partial nephrectomy: patient selection and perioperative outcomes. J Urol. 2005;174:846-849. 7. Marszalek M, Meixl H, Polajnar M, et al. Laparoscopic and open partial nephrectomy: a matched-pair comparison of 200 patients. Eur Urol. 2009;55:1171-1178. 8. Schips L, Dalpiaz O, Cestari A, et al. Autologous fibrin glue using the Vivostat system for hemostasis in laparoscopic partial nephrectomy. Eur Urol. 2006;50:801-805. 9. Lippi G, Montagnana M, Banfi G, et al. Comparison of 2 methods for the calculation of estimated glomerular filtration rate. Lab Med. 2008;39:35-37. 10. Kutikov A, Uzzo RG, The RENAL Nephrometry Score: A comprehensive standardized system for quantitating renal tumor size, location and depth. J Urol. 2009;182:844-853. 11. Pattaras JG, Moore RG, Landman J, et al. Incidence of postoperative adhesion formation after transperitoneal genitourinary laparoscopic surgery. Urology. 2002;59:37-41. 12. McAllister M, Bhayani SB, Ong A, et al. Vena caval transection during retroperitoneoscopic nephrectomy: report of the complication and review of the literature. J Urol. 2004;172:183-185. 13. Porpiglia F, Renard J, Billia M, et al. Is renal warm ischemia over 30 minutes during laparoscopic partial nephrectomy possible? Oneyear results of a prospective study. Eur Urol. 2007;52:1170-1178. 14. Desai MM, Gill IS, Ramani AP, et al. The impact of warm ischemia on renal function after laparoscopic partial nephrectomy. BJU Int. 2005;95:377-383. 15. Thompson RH, Blute ML. At what point does warm ischemia cause permanent renal damage during partial nephrectomy? Eur Urol. 2007;52:961-963. 16. Becker F, Van Poppel H, Hakenberg OW, et al. Assessing the impact of ischemia time during partial nephrectomy. Eur Urol. 2009;56:625-635. 17. Nadu A, Ekstein P, Szold A, et al. Ventilatory and hemodynamic changes during retroperitoneal and transperitoneal laparoscopic nephrectomy: a prospective real-time comparison. J Urol. 2005;174: 1013-1017. 18. Cisek LJ, Gobet RM, Peters CA. Pneumoperitoneum produces reversible renal dysfunction in animals with normal and chronically reduced renal function. J Endourol. 1998;12:95-100.
113
METHODS
RESULTS
CONCLUSIONS
To compare surgical and functional results of both surgical approaches to endoscopic partial nephrectomy. It is currently performed either by the transperitoneal (t) or the retroperitoneal (r) approach. This was a retrospective, matched-pair comparison of 105 patients who underwent either transperitoneal laparoscopic (Graz) or retroperitoneoscopic (Klagenfurt) partial nephrectomy for clinical T1a renal masses. A total of 35 patients after transperitoneal laparoscopic and 70 patients after retroperitoneoscopic partial nephrectomy were included to this analysis after matching for age (T: 59.3 vs R: 60.1 a), preoperative glomerular filtration rate (GFR) (T: 93.2 vs R: 96.1 mL/min) and tumor size (T: 2.4 vs R: 2.5 cm). Nephrometry scores were comparable between groups and were low, medium, and high in 54.3%, 45.7%, and 0% (t) and 55.7%, 42.9%, and 1.4% (r) of patients (P ⫽ .9). Operative time (T: 139.3 minutes vs. R: 83.9 minutes; P ⬍ .001) and hospitalization (T: 7 days, R: 5 days; P ⬍ .001) were shorter in the retroperitoneoscopic group. Ischemia time (T: 24.3 minutes, R: 22.6 minutes) and postsurgical GFR (T: 86.6 vs R: 90.0 mL/min), postsurgical GFR-decrease (T: 7.1%, R: 6.2%, P ⫽ .9) and decline of hemoglobin (T: 17.1%, R: 16.6%) were comparable. Complications were 4 nephrectomies (T: n ⫽ 1, R: n ⫽ 3), 2 revisions for hemorrhage (R: n ⫽ 2), 4 pneumothorax (R: n ⫽ 4), and 2 urinary fistulas (T: n ⫽ 2). The positive surgical margin rate was comparable between groups (T: n ⫽ 3, R: n ⫽ 5). Transperitoneal laparoscopic and retroperitoneoscopic partial nephrectomy provide comparable surgical and functional results. One advantage of the retroperitoneoscopic access seems to be a shorter total surgical time. UROLOGY 77: 109 –113, 2011. © 2011 Elsevier Inc.
E
ndoscopic partial nephrectomy (PN) is increasingly offered as an alternative to the open approach for T1a renal masses. To ensure proper outcomes in terms of ischemia and surgical margin status, accessibility of the tumor and renal hilum are essential. Localization of the renal mass and experience of the surgeon will predict the use of the transperitoneal or retroperitoneal approach in most cases.1,2 As select tumors may be accessible by either route, specific advantages and limitations of both approaches have to be considered, and differences in working space, port placement, and the corresponding angulation of laparoscopic
instruments accounted for by diligent patient selection.3 The respective benefits and disadvantages of laparoscopic and retroperitoneoscopic approach to renal masses have been addressed before.4-6 However, these 3 studies available to date are hampered by a small sample size4 or differences in tumor size.5,6 We have therefore performed a matched-pair comparison to provide more reliable information on surgical and clinical outcomes and particular complications that can be expected with either approach.
MATERIAL AND METHODS Patients
From the Department of Urology, Klagenfurt General Hospital, Klagenfurt, Austria; Department of Urology and Andrology, Danube Hospital, Vienna, Austria and Department of Urology, Medical University of Graz, Graz, Austria Reprint requests: Martin Marszalek, M.D., Department of Urology and Andrology, Donauspital, Langobardenstrasse 122, A-1220 Vienna, Austria. E-mail: [email protected] Submitted: December 16, 2009, accepted (with revisions): February 16, 2010
© 2011 Elsevier Inc. All Rights Reserved
In total, 105 patients who underwent endoscopic partial nephrectomy for incidentally discovered renal masses were included to this matched-pair analysis. All transperitoneal procedures were performed at the Department of Urology of the Graz Medical University, Styria, Austria by 1 experienced surgeon over a period of 4 years. All retroperitoneal procedures were 0090-4295/11/$36.00 doi:10.1016/j.urology.2010.02.057
109
performed at the Department of Urology of the Klagenfurt General Hospital, Carinthia, Austria by 2 experienced surgeons over a period of 5 years; some of these cases have been part of a previous analysis.7 In both groups, renal sonography, chest x-ray, and abdominal contrast medium– enhanced computed tomographic scans were included in the preoperative workup of each patient. In select cases not elegible for contrast medium application, magnetic resonance imaging studies were performed. Pre- and postoperatively, blood sample analyses, including serum creatinine, blood urea nitrogen, and hemoglobin serum levels were performed. Institutional review board approval was obtained.
Surgical Technique The technique of retroperitoneoscopic partial nephrectomy has been described previously.7 In brief, with the patient in a full flank position, a retroperitoneal cavity was formed from a small incision in the lumbar triangle and a Hasson trocar introduced. Two additional ports (12 and 5 mm) were placed at the discretion of the surgeon. Renal arteries were clamped with endobulldog clamps followed by excision of the tumor with a choledochotom (Karl Storz, Tuttlingen, Germany) and scissors. Hemostasis was achieved by central suturing with application of fibrin glue (Baxter International, Deerfield, IL) and 3-5 additional parenchymal sutures. An endobag was used to retrieve the specimen. The technique of transperitoneal partial nephrectomy has also been described previously.8 In brief, pneumoperitoneum was established by insertion of a 12-mm camera trocar via a mini-laparotomy. With the patient in a 30-degree elevated flank position, this port was placed supraumbilical, or paramedian in obese patients. Consecutively, 2 12-mm working ports were introduced at the discretion of the surgeon. For right-sided partial nephrectomies, an additional 5-mm port was introduced below the xyphoid for retraction of the liver. Dissection of the ascending and descending colon and the kidney was performed by an Ultracision device (Ethicon Endo-Surgery, Cincinnati, OH). Renal arteries were clamped by endobulldog clamps and excision of the tumor was performed with scissors. Hemostasis was also achieved by central suturing, autologous fibrin glue (Vivostat; Vivostat A/S, Alleroed, Denmark)8 and parenchymal sutures and the specimen retrieved by an endobag. A perirenal drain was placed routinely in all patients of both cohorts. No intraoperative frozen section analysis was performed with either procedure. As no intracorporal cooling method was used, all procedures were performed in warm ischemia.
Perioperative and Renal Function Analysis Perioperative blood loss was determined by change in serum hemoglobin levels. Renal function was assessed by pre- and postoperative assessment of serum creatinine and estimation of respective glomerular filtration rates (GFR) using the Mayo Clinic Quadratic Equation (MCQE).9 Intra- and postoperative complications and surgical revisions are reported.
Statistical Analysis A matched-pair analysis was performed comparing data for 35 patients after endoscopic transperitoneal and 70 patients after endoscopic retroperitoneal partial nephrectomy. The population available for the matching process consisted of 2 consecutive series of patients who underwent endoscopic PN for 110
clinical T1a renal masses (transperitoneal: n ⫽ 52, retroperitoneal: n ⫽ 150). Each patient in the transperitoneal group was matched to 2 corresponding patients of the retroperitoneoscopic group, with regard to age, preoperative glomerular filtration rate, and tumor size. Clinical stage of renal cell cancer was T1a in all cases. Tumor localization was compared between groups by calculation of the recently developed RENAL nephrometry scores.10 Both groups were compared regarding surgical and clinical outcome variables. Continuous variables were compared by t test or Wilcoxon rank-sum test, with results presented as means and standard error (SE) when the t test was used and as median and quartiles (25th and 75th percentiles) when the Wilcoxon rank-sum test was used. Comparison of categorical variables was performed by Person chi-square test and Fisher exact test. All statistical analysis were performed using the Statistical Package for the Social Sciences 16 (SPSS Inc., Chicago, IL), with a two-tailed value of P ⬍ .05 considered to indicate statistical significance.
RESULTS Patient Characteristics A total of 105 patients who underwent transperitoneal or retroperitoneal partial nephrectomy were matched for age, preoperative glomerular filtration rate, and tumor size. Mean age at surgery was 59.3 ⫾ 1.9 years in the transperitoneal and 60.1 ⫾ 1.3 years in the open group (P ⫽ .8). Gender distribution was identical in both series (P ⫽ .8) (Table 1). Mean tumor size was 2.4 ⫾ 0.1 cm (range: 1.2-4.0 cm) in the transperitoneal and 2.4 ⫾ 0.1 (range: 1.2-4.0 cm) in the retroperitoneal group (P ⫽ .8). Nephrometry scores were comparable in both groups (P ⫽ .8), such as for the laterality of the affected kidney (P ⫽ .2) (Table 1). Surgical Outcomes Total surgical time (skin incision to skin closure) was shorter in the retroperitoneal compared with the transperitoneal group (P ⬍ .001). Arterial occlusion time was comparable in both groups (P ⫽ .2). Ischemia time was similar in malignant and benign tumors in transperitoneal (23.4 ⫾ 1.2 minutes [range: 12-43 minutes] vs 27.0 ⫾ 3.5 minutes [range: 16-45 minutes]; P ⫽ .2) and retroperitoneal PN (22.8 ⫾ 0.6 minutes [range: 13-37 minutes] vs 21.3 ⫾ 0.9 minutes [range: 15-27 minutes]; P ⫽ .5). After retroperitoneal PN, hospitalization was shorter compared with the transperitoneal approach (5 days [IQR: 5-6 days] vs 7 day [IQR: 5.8-8.3 days]; P ⬍ .001). Serum hemoglobin declined after transperitoneal PN by 17.1 ⫾ 1.4% from 14.6 ⫾ 0.2 g/dL (range: 12.0-17.8 g/dL) before surgery to 12.1 ⫾ 1.8 g/dL (range: 8.1-16.1 g/dL) after surgery (24 hours after surgery; P ⬍ .001); after retroperitoneal PN hemoglobin declined by 16.6 ⫾ 1.0% from 14.6 ⫾ 0.2 g/dL (range: 9.2-17.8 g/dL) to 12.1 ⫾ 0.2 g/dL (range: 8.2-14.8 g/dL) (P ⬍ .001). These changes from pre-to postoperative serum hemoglobin levels were comparable in both groups (P ⫽ .8). Transfusion rate was 5.7% in the transperitoneal and 5.1% in the retroperitoneal group (P ⫽ .9) (Table 2). UROLOGY 77 (1), 2011
Table 1. Principal characteristics of the study population
Mean age, yrs (range) Sex (male/female), % Mean patient BMI, kg/m2 (range) Laterality (right/left), % Nephrometry scoresⴱ Median tumor size cm, (IQR) Endophytic/exophytic tumors Exophytic (⬎50%), % Exophytic (⬍50%), % Entirely endophytic, % Nearness of tumor to sinus/calyx ⱖ7 mm, % ⬎4 mm but ⬍7 mm, % ⱕ4 mm, % Anterior/posterior tumors Anterior, % Posterior, % Location relative to upper/lower polar line Entirely above/below upper/lower polar line, % Crosses polar line, % ⬎50% across polar line or crosses axial midline or tumor entirely between polar lines, % Contact to first-order vessel in the renal hilum, % Total scoreⴱ (range) Complexity of surgical procedure according to nephrometry score Low, % Medium, % High, %
Transperitoneal (n ⫽ 35)
Retroperitoneal (n ⫽ 70)
59.3 (43.8/78.0) 65.7/34.3 27.9 (22.1/40.0) 48.6/51.4
60.1 (41.5/80.6) 62.9/37.1 27.1 (20.0/36.3) 57.1/42.9
2.4 (1.7/3.0)
2.5 (1.8/3.0)
62.8 (n ⫽ 22) 34.3 (n ⫽ 12) 2.9 (n ⫽ 1)
65.7 (n ⫽ 46) 31.4 (n ⫽ 22) 2.9 (n ⫽ 2)
34.3 (n ⫽ 12) 31.4 (n ⫽ 11) 34.3 (n ⫽ 12)
35.7 (n ⫽ 25) 32.9 (n ⫽ 23) 31.4 (n ⫽ 22)
54.3 (n ⫽ 19) 45.7 (n ⫽ 16)
65.7 (n ⫽ 46) 34.3 (n ⫽ 24)
37.1 (n ⫽ 13) 28.6 (n ⫽ 10) 34.3 (n ⫽ 12)
44.3 (n ⫽ 31) 24.3 (n ⫽ 17) 31.4 (n ⫽ 22)
2.9 (n ⫽ 1) 6.33 (4-9)
0 (n ⫽ 0) 6.25 (4-10)
54.3 (n ⫽ 19) 45.7 (n ⫽ 16) 0 (n ⫽ 0)
55.7 (n ⫽ 39) 42.9 (n ⫽ 30) 1.4 (n ⫽ 1)
P Value .8 .3 .2 .8 .9
.9
.3 .6
.8 .9
BMI, body mass index; IQR, interquartile range; RENAL, nephrometry score.10
Table 2. Perioperative results
Median hospitalization, days (IQR) Mean operative time, min (range) Mean arterial occlusion time, min (range) Blood loss, % (mean decline in % of baseline hemoglobin) Overall complication rate, %
Transperitoneal (n ⫽ 35)
Retroperitoneal (n ⫽ 70)
P Value
7 (5.8/8.3) 139.3 (90/190) 24.3 (12/45) 17.1 8.6
5 (5.0/6.0) 83.9 (50/165) 22.6 (13/37) 16.6 14.3
⬍.001 ⬍.001 .2 .8 .5
IQR, interquartile range.
Table 3. Renal function outcomes in patients after endoscopic partial nephrectomy
2
Mean preoperative (GFR ml/min/1.72 m ) Mean postoperative (GFR ml/min/1.72 m2) Decline in GFR from pre- to postoperative (GFR ml/min/1.72 m2) Relative decline in GFR from pre- to postoperative %
Transperitoneal
Retroperitoneal
P Value
93.2 ⫾ 3.7 (50.7-128.6) 86.6 ⫾ 3.2 (46.6-123.9) 6.6 ⫾ 2.3
96.1 ⫾ 2.3 (52.5-134.0) 90.0 ⫾ 2.9 (42.7-130.8) 6.1 ⫾ 2.3
.5 .5 .9
7.1 ⫾ 3.0
6.3 ⫾ 2.7
.9
GFR, glomerular filtration rate. Values are mean ⫾ standard error (range).
Renal Function Preoperative glomerular filtration rate was similar in both groups (P ⫽ .5), as was postoperative GFR (24 hours after surgery; P ⫽ .5) (Table 3). A significant decline from pre-to postoperative GFR was observed in the transperitoneal (7.1%, P ⫽ .007) and retroperitoneoscopic group UROLOGY 77 (1), 2011
(6.2%, P ⫽ .01). This decline was comparable in both groups (P ⫽ .9) (Fig. 1). Pathologic Outcomes and Surgical Margin Status In the final histopathologic evaluation, 25.7% of tumors in the transperitoneal group and 18.6% in the retroperitoneal 111
Figure 1. Pre- and postoperative glomerular filtration rate (mL/min/1.73 m2) in patients undergoing endoscopic partial nephrectomy. Results are given for the transperitoneal and the retroperitoneal group.
group were benign (P ⫽ .5). All malignant tumors were pT1a stage renal cell carcinomas except 1 metastasis of malignant melanoma in the transperitoneal group. The rate of positive surgical margins in the matched population was comparable between groups (transperitoneal PN: 8.6% [n ⫽ 3]; retroperitoneal PN: 7.1% [n ⫽ 5], P ⫽ .8). However, the positive margin rate in the overall consecutive series of unmatched patients was 5.8% after transperitoneal and 4.7% after retroperitoneal PN. Complications Three patients undergoing transperitoneal (t) PN developed 3 complications (overall complication rate: 8.6%). In the retroperitoneal (r) group, 8 patients experienced a total of 10 complications (overall complication rate: 14.3%, P ⫽ .5). Complications were pneumothorax (T: n ⫽ 0, R: n ⫽ 4), urinary leakage (T: n ⫽ 2, R: n ⫽ 0) and postoperative development of subcutaneous hematoma (T: n ⫽ 0, R: n ⫽ 1). In the transperitoneal group, postoperative bleeding was managed conservatively in 1 patient (2.9%) by transfusion of 2 U of packed red blood cells. Another patient underwent revision for severe hemorrhage, resulting in nephrectomy. After retroperitoneoscopic PN, 5 patients underwent revision for severe hemorrhage, 3 (4.3%) of which resulted in nephrectomy. The underlying cause of severe hemorrhage prompting acute surgical reintervention was arterial bleeding as confirmed on emergently performed abdominal CT scan in all cases.
COMMENT The principal finding of this matched-pair analysis was a comparable surgical and functional outcome after transperitoneal laparoscopic and retroperitoneoscopic PN. Endoscopic PN can be performed via transperitoneal and retroperitoneal approach, each providing specific advantages and disadvantages.4 Arguments in favor of the 112
transperitoneal route are the larger working space, allowing for wider angulation and maneuverability with laparoscopic instruments, and the more accustomed orientation by familiar anatomic landmarks.4,5 Intra-abdominal adhesions, which might develop as result of laparoscopic surgical procedures, usually appear to be of minor clinical significance.11 Retroperitoneoscopy, by avoiding bowel mobilization, seems to provide a more direct access to the kidney and the renal hilum.4 Drawbacks are the spatial limitations of the narrow retroperitoneal working space, the lack of view, and the risk of disorientation.12 Select tumors may be approached by either route, according to the surgeon’s preference. However, similar to open surgery, indication and patient selection for either access have to be carefully considered by the endoscopic surgeon, with tumor localization as most important decisive factor: this fact also obviates a randomized study design, which, besides the limited sample size and the lack of long-term follow-up, is recognized as shortcoming of the present retrospective analysis. Furthermore, transperitoneal and retroperitoneal PN were performed by experienced laparoscopic surgeons, but at different institutions, a limitation of the present study that has to be considered when interpreting the data provided. As indicated by the results presented by the Cleveland Clinic Foundation, 1 advantage of the retroperitoneal route seems to be a shorter total operative time; Ng et al reported an operative time of 3.5 hours for laparoscopic PN compared with 2.9 hours for the retroperitoneoscopic procedure6 However, patients in this analysis were not pair matched, and transperitoneally accessed tumors were significantly larger (3.1 vs 2.6 cm; P ⫽ .004). Although retroperitoneoscopic PN was also the less time-consuming procedure, operative times of both, the trans- and retroperitoneal group, were shorter in our series when compared with the results of Ng et al..6 This may in part reflect the interim refinement of the surgical technique and, at least with the retroperitoneal approach, the extensive expertise of the respective surgeons. Also, others reported comparable results, in terms of shorter retroperitoneoscopic operative time, in line with our findings.4,5 It has been consistently shown that prolonged arterial occlusion time exceeding 30 minutes of warm ischemia will exert a significant negative influence on renal function.13,14 Furthermore, recent data recommend even shorter ischemic periods of 20 minutes to prevent persistent renal damage.15 Therefore, it is crucial to keep ischemia short, even more as local hypothermia in endoscopic PN remains a sophisticated challenge.16 Ng et al. observed longer ischemia times of 31 minutes with the transperitoneal approach compared with 28 minutes with the retroperitoneal approach.6 As mentioned before, tumors in their analysis were larger in the transperitoneal group, which might well have contributed to these results. We did not observe an advantage for either approach, trans- or retroperitoneal, considering ischemia time. This is underlined by the work of Wright et al, who UROLOGY 77 (1), 2011
observed similar ischemia times of 32 minutes in both groups.4 In another comparative study, Kieran et al, also found comparable arterial occlusion times in patients undergoing endoscopic trans- or retroperitoneal PN (25.6 vs 22.7 minutes; P ⫽ .3).5 Again, tumors in their study were larger in the transperitoneal group (2.7 vs 2.1 cm; P ⫽ .03). Besides ischemia, compelling evidence suggests a negative impact of pneumoperitoneum and pneumoretroperitoneum on hemodynamic and ventilatory parameters as well as intraoperative renal blood flow and renal function.7,17,18 Although present with either route of access, these negative effects seem to be less pronounced with the retroperitoneal approach.17 We observed a significant pre- to postoperative decrease of glomerular filtration rate of roughly 5% in both groups. This similar decrease suggests a comparable clinical impact of gas insufflation on renal function, regardless of the approach chosen. Kieran et al found a postoperative increase of serum creatinine levels (⫹ 0.11 mg/dL) after both, transand retroperitoneoscopic PN (P ⫽ .96),5 an observation that is in line with our findings. In a recent analysis, Kieran et al presented perioperative complications of trans- and retroperitoneal PN,5 revealing comparable overall complication rates of 22% and 19%, respectively. We were able to confirm their results of similar overall complication rates for either surgical approach, however we experienced different types of complications: Kieran et al mainly observed postoperative hemorrhage in both groups (transperitoneal: 13.3%, retroperitoneal: 11.1%) as well as bowel related complications in the transperitoneal group (6.7%).5 Whereas postoperative hemorrhage was also prevalent with both approaches, we did not find bowelrelated complications in our analysis. However, pneumothorax in the retroperitoneal and urinary leakage prompting ureteral stenting in the transperitoneal group were additional complications observed in our study. Pleural entry was also reported in the comparative analysis of the Cleveland Clinic group (1% with the transperitoneal route) as well as urinary leakage rates of 4% and 3% after laparoscopic and retroperitoneoscopic PN.6 At least the higher pleural entry rates that we observed with the retroperitoneoscopic approach may in part reflect the surgeons’ need to compensate the limitations of the narrow retroperitoneal space. In our series, intercostal port placement may well acount for this particular complication.
CONCLUSIONS According to our experience, transperitoneal and retroperitoneal endoscopic PN provide similar surgical and functional results. Appropriate selection of surgical access facilitates tumor resection, resulting in comparable
UROLOGY 77 (1), 2011
ischemia times for either approach. The specific challenges of the retroperitoneal route must not be underestimated by the endoscopic surgeon. However, 1 particular advantage of this approach seems to be a shorter total surgical time. References 1. Winfield HN, Donovan JF, Lund GO, et al. Laparoscopic partial nephrectomy: initial experience and comparison to the open surgical approach. J Urol. 1995;153:1409-1414. 2. Gill IS, Delworth MG, Munch LC. Laparoscopic retroperitoneal partial nephrectomy. J Urol. 1994;152:1539-1542. 3. Singh D, Rubenstein M, Gill IS. Laparoscopic partial nephrectomy. J Endourol. 2005;19:451-455. 4. Wright JL, Porter JR. Laparoscopic partial nephrectomy: comparison of transperitoneal and retroperitoneal approaches. J Urol. 2005; 174:841-845. 5. Kieran K, Montgomery JS, Daignault S, et al. Comparison of intraoperative parameters and perioperative complications of retroperitoneal and transperitoneal approaches to laparoscopic partial nephrectomy: support for a retroperitoneal approach in selected patients. J Endourol. 2007;21:754-759. 6. Ng CS, Gill IS, Ramani AP, et al. Transperitoneal versus retroperitoneal laparoscopic partial nephrectomy: patient selection and perioperative outcomes. J Urol. 2005;174:846-849. 7. Marszalek M, Meixl H, Polajnar M, et al. Laparoscopic and open partial nephrectomy: a matched-pair comparison of 200 patients. Eur Urol. 2009;55:1171-1178. 8. Schips L, Dalpiaz O, Cestari A, et al. Autologous fibrin glue using the Vivostat system for hemostasis in laparoscopic partial nephrectomy. Eur Urol. 2006;50:801-805. 9. Lippi G, Montagnana M, Banfi G, et al. Comparison of 2 methods for the calculation of estimated glomerular filtration rate. Lab Med. 2008;39:35-37. 10. Kutikov A, Uzzo RG, The RENAL Nephrometry Score: A comprehensive standardized system for quantitating renal tumor size, location and depth. J Urol. 2009;182:844-853. 11. Pattaras JG, Moore RG, Landman J, et al. Incidence of postoperative adhesion formation after transperitoneal genitourinary laparoscopic surgery. Urology. 2002;59:37-41. 12. McAllister M, Bhayani SB, Ong A, et al. Vena caval transection during retroperitoneoscopic nephrectomy: report of the complication and review of the literature. J Urol. 2004;172:183-185. 13. Porpiglia F, Renard J, Billia M, et al. Is renal warm ischemia over 30 minutes during laparoscopic partial nephrectomy possible? Oneyear results of a prospective study. Eur Urol. 2007;52:1170-1178. 14. Desai MM, Gill IS, Ramani AP, et al. The impact of warm ischemia on renal function after laparoscopic partial nephrectomy. BJU Int. 2005;95:377-383. 15. Thompson RH, Blute ML. At what point does warm ischemia cause permanent renal damage during partial nephrectomy? Eur Urol. 2007;52:961-963. 16. Becker F, Van Poppel H, Hakenberg OW, et al. Assessing the impact of ischemia time during partial nephrectomy. Eur Urol. 2009;56:625-635. 17. Nadu A, Ekstein P, Szold A, et al. Ventilatory and hemodynamic changes during retroperitoneal and transperitoneal laparoscopic nephrectomy: a prospective real-time comparison. J Urol. 2005;174: 1013-1017. 18. Cisek LJ, Gobet RM, Peters CA. Pneumoperitoneum produces reversible renal dysfunction in animals with normal and chronically reduced renal function. J Endourol. 1998;12:95-100.
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