Analysis of the Transperitoneal Approach to Robot-Assisted Laparoscopic Partial Nephrectomy for the Treatment of Anterior and Posterior Renal Masses

Abstract

Objective:

Few studies have directly assessed the impact of tumor anterior/posterior location during transperitoneal robotic-assisted laparoscopic partial nephrectomy (TPRPN). The present study sought to assess perioperative and pathological outcomes associated with TPRPN among patients with anterior versus posterior tumors.

Patients and Methods:

The Institutional Review Board–approved Mount Sinai Kidney Cancer database was used to identify 123 patients who underwent TPRPN from May 2011 to April 2015. Perioperative outcomes, including operative time, warm ischemia time (WIT), estimated blood loss (EBL), hospital length of stay (LOS), surgical margin status, complications, and reduction in estimated glomerular filtration rate (eGFR) at discharge and at last follow-up, were compared between those with anterior and posterior masses while controlling for clinical and pathological variables (i.e., age, gender, body mass index, tumor size, tumor laterality, malignancy, hilar location, and R.E.N.A.L. nephrometry score).

Results:

Clinical and pathological characteristics were comparable between groups; mean tumor size was 3.1 cm anterior versus 2.8 cm posterior (P = .187). Tumor complexity (i.e., nephrometry scores, 6.9 versus 6.3; P = .097) and proportion of malignancy (74.5% versus 73.1%; P = .799) were also similar between posterior and anterior masses. In multivariable analyses, perioperative outcomes, including operative time, WIT, EBL, LOS, surgical margin status, reduction in eGFR, and postoperative complication rates, did not significantly differ between groups.

Conclusions:

The transperitoneal approach to partial nephrectomy for posterior tumors resulted in no difference in operative time, WIT, EBL, LOS, positive surgical margins, reduction in eGFR, or postoperative complications. The TPRPN approach to treat a posterior tumor is reasonable and is the preferred technique at our institution.

Introduction

Several contemporary studies have championed the benefits of the retroperitoneal (RP) approach to minimally invasive and robotic partial nephrectomy (PN) for posterior tumors. Compared with the transperitoneal (TP) approach, the RP approach in minimally invasive PN has been reported to have significantly better perioperative outcomes, including reduced estimated blood loss (EBL) (100–307 mL),^1–4 operative time (35–114 minutes),^1–8 length of stay (LOS) (0.5–1.3 days),^1–7 re-admission rates,¹ warm ischemia time (WIT) (3–3.6 minutes),^7,8 collecting system injury (22%),⁷ time to resuming a regular diet (0.5 days), and time to catheter removal (1.1 days).⁴

Other studies of minimally invasive PN have demonstrated equivalent perioperative outcomes between TP and RP approaches, including EBL,^5–9 blood transfusion rates,^6,9 perioperative complication rates (e.g., abdominal visceral injuries, renal vascular injuries, pleural entry),^1,5–7,9 adverse events,¹⁰ positive surgical margin rates,⁹ ischemia time,^1,2,4,5,10 operative time,^1,10 postoperative estimated glomerular filtration rate (eGFR),¹ postoperative serum creatinine,^2,7 analgesic requirement,⁷ LOS,⁹ urinary fistula rates, and 3-year recurrence-free survival rates.⁶ Among these studies comparing TP and RP approaches to PN, those in which robotic PN was performed found the RP approach to result in significantly better perioperative outcomes, including reduced EBL,^1,3 operative time,^1,3,8 LOS,^1,3 re-admission rates,¹ and WIT⁸ but no difference in perioperative complication rates and postoperative eGFR.¹

The evidence to support either approach is inconsistent and may be subject to selection bias based on tumor size and location. Specifically, in these direct comparisons of TP and RP approaches to minimally invasive PN, TP tumors were either significantly larger (0.7 cm; P < .001)^1,7 or trended toward being larger (0.58 cm [P = .08], 0.3 cm [P = .09], or 1.15 cm [P = .053]).^4,9,10 Some centers advocate use of a TP approach for the treatment of both anterior and posterior renal tumors, given greater instrument maneuverability/range of motion and larger working space.^11,12

Only one study to date has compared outcomes associated with treatment of anterior and posterior renal tumors with the TP approach to robotic PN.¹² A significant limitation of this study was the failure to control for confounding variables (i.e., body mass index [BMI], tumor size, R.E.N.A.L. nephrometry score, etc.) associated with their outcomes of interest. The present study builds on this analysis by controlling for important confounding variables and by including additional outcomes of hospital LOS and postoperative change in renal function (eGFR) after TP robotic-assisted laparoscopic PN (TPRPN) for anterior and posterior tumors.

Materials and Methods

Patients

Using the Institutional Review Board–approved Mount Sinai Kidney Cancer database, we retrospectively identified patients who underwent TPRPN from May 2011 to April 2015. All surgeries were performed by a single surgeon using the Da Vinci^® Surgical System (Intuitive Surgical, Sunnyvale, CA). Demographic, clinical, tumor, operative, and postoperative data were extracted from electronic medical records and manually entered into the Institutional Review Board–approved online Research Electronic Data Capture (REDCap) system. Tumor size (largest diameter in centimeters), R.E.N.A.L. nephrometry score, clinical stage, malignancy, and tumor location were also collected. Nephrometry scores were calculated for all patients using preoperative abdominal/pelvic computed tomography and/or magnetic resonance imaging images and were independently cross-validated by two researchers. Tumors were classified as anterior or posterior tumors according to the R.E.N.A.L. nephrometry scoring system. Specifically, tumors were classified as anterior if the tumor was anterior to the coronal plane of the kidney and posterior if the tumor was posterior to the coronal plane of the kidney.¹³ Lateral tumors (i.e., those neither anterior nor posterior) were excluded from analysis.

Surgical technique

TPRPN was performed via the “First Assistant Sparing Technique” (FAST), which has been previously described by Berg et al.¹⁴ In brief, the patient is placed in the flank position, and trocars are placed for the camera, three robotic arms, assistant port, and an additional port for liver retraction for right-sided tumors. After medial reflection of the colon along the white line of Toldt, the renal hilum is dissected, the kidney is defatted, and the tumor is exposed for margin delineation using intraoperative ultrasonography. Posterior tumors require full mobilization and medial reflection of the kidney. The FAST approach specifically involves placement of all sutures and bulldog clamps intracorporeally prior to warm ischemia and tumor excision and has been demonstrated to significantly reduce WIT and total operative time.¹⁴ After tumor excision, running, unidirectional-barbed sutures are used to close any collecting system injuries and to oversew venous bleeding. Renorrhaphy is then performed with interrupted 0 polyglactin 910 (Vicryl™; Ethicon, Somerville, NJ) sutures using the “sliding-clip” technique¹⁵ and reinforced with hemostatic agents (collagen microspheres and thrombin + fibrinogen). Hemostasis is visually confirmed while reducing the pressure of the pneumoperitoneum.

Statistical analysis

Patient-specific characteristics and tumor-specific characteristics were compared between anterior and posterior tumors using the independent-samples t test for continuous variables and the chi-squared test for categorical variables. Primary outcomes included WIT, EBL, operative time, reduction in eGFR (from baseline to discharge and from baseline to last follow-up), surgical margin status, postoperative complication rates, and hospital LOS. Any complication within 30 days of surgery was recorded. These outcomes were compared between anterior and posterior tumors while controlling for age, gender, BMI, tumor size, tumor laterality, hilar location, and R.E.N.A.L. nephrometry score in multivariable logistic and linear regression models. R.E.N.A.L. nephrometry score was treated as a continuous variable and calculated as the sum of the radius, exophytic/endophytic, nearness of the tumor to the collecting system, and location relative to the polar lines components.¹³ Reduction in eGFR at discharge/last follow-up was calculated using the following formula: (eGFR₂ [discharge or last follow-up] – preoperative eGFR)/preoperative eGFR. Statistical analyses were performed with SPSS version 20 software (IBM Corp., Armonk, NY) and R version 3.1.2 software (R Foundation for Statistical Computing, Vienna, Austria). Significance was identified using two-tailed P < .05.

Results

Of the 162 patients in our institutional database, in total, 123 patients undergoing TPRPN were included in the analysis, and mean follow-up was 13 months. Posterior location was more common than anterior in our cohort (63% versus 37%, respectively). Results from univariate independent-samples t tests and chi-squared tests indicate that patients with posterior tumors had significantly longer follow-up (15.2 versus 10.3 months; P = .039) and that significantly more anterior tumors were cT1b (25.5% versus 7.7%; P = .013). The two groups did not significantly differ on any other patient- or tumor-specific characteristics, including baseline eGFR, tumor size, proportion of malignancy, or nephrometry score (Table 1). Results from univariate independent-samples t tests and chi-squared tests indicate that operative time was significantly longer for patients with posterior versus anterior renal masses (167.48 versus 153.19 minutes; P = .043). The two groups did not significantly differ on any other perioperative outcomes, including WIT, EBL, LOS, complications, positive surgical margins, and reduction in eGFR at discharge and at last follow-up (Table 2).

Table 1.

Patient- and Tumor-Specific Characteristics of Patients Who Underwent Transperitoneal Robot-Assisted Laparoscopic Partial Nephrectomy

Characteristic	Anterior	Posterior	P value
Patients	46 (37%)	77 (63%)
Age (years)	62.67 (14.13)	59.74 (14.25)	.269
Gender
Male	33 (71.7%)	50 (64.9%)	.436
Female	13 (28.3%)	27 (35.1%)
BMI (kg/m²)	29.35 (5.93)	28.97 (5.71)	.733
ASA score	2.41 (0.52)	2.35 (0.54)	.618
Serum creatinine (mg/dL)	0.98 (0.28)	1.09 (0.41)	.092
Baseline eGFR (mL/minute/1.73 m²)	78.28 (19.77)	71.24 (19.87)	.061
Serum creatinine at discharge (mg/dL)	1.07 (0.27)	1.17 (0.47)	.126
eGFR (mL/minute/1.73 m²) at
Discharge	70.69 (18.28)	66.82 (19.95)	.285
Most recent follow-up	67.78 (16.45)	64.06 (19.92)	.300
Most recent follow-up (months)	10.28 (11.74)	15.22 (12.11)	.039^a
Nephrometry score	6.86 (1.74)	6.28 (1.65)	.097
Hilar	8 (17%)	8 (10.3%)	.264
Clinical stage
cT1a	34 (73.9%)	69 (89.6%)	.013^a
cT1b	12 (26.1%)	6 (7.8%)
cT2a	0 (0%)	2 (2.6%)
Tumor laterality
Right	21 (45.7%)	38 (49.4%)	.745
Left	25 (54.3%)	39 (50.6%)
Tumor size (cm)	3.14 (1.36)	2.8 (1.43)	.187
Malignancy	35 (74.5%)	57 (73.1%)	.799

For categorical variables, frequencies are given with percentages in parentheses, and to calculate statistical significance, chi-squared tests were performed. For continuous variables, means are given with standard deviations in parentheses, and to calculate statistical significance, independent-samples t tests were performed.

Statistically significant difference at the P < .05 level.

ASA, American Society of Anesthesiologists; BMI, body mass index; eGFR, estimated glomerular filtration rate.

Table 2.

Perioperative Outcomes of Patients Who Underwent Transperitoneal Robot-Assisted Laparoscopic Partial Nephrectomy

Characteristic	Anterior	Posterior	P value
Warm ischemia time (minutes)	15.25 (4.37)	16.48 (4.28)	.131
Estimated blood loss (mL)	89.13 (75.21)	82.01 (55.38)	.579
Length of hospitalization (days)	1.4 (0.62)	1.49 (0.71)	.485
Operative time (minutes)	153.19 (30.84)	167.48 (41.54)	.043^a
Postoperative complication	2 (4.3%)	4 (5.2%)	.833
Positive surgical margin	3 (6.4%)	1 (1.23%)	.114
Reduction in eGFR (mL/minute/1.73 m²) at
Discharge	−8.38 (16.50)	−5.30 (16.94)	.338
Most recent follow-up	−11.06 (20.42)	−11.89 (22.65)	.187

Statistically significant difference at the P < .05 level.

eGFR, estimated glomerular filtration rate.

Results for all multivariable linear regression models of perioperative outcomes are displayed in Tables 3 and 4. After controlling for age, gender, tumor laterality, BMI, tumor size, R.E.N.A.L. nephrometry score, malignancy, and hilar location, results from multivariable linear regression demonstrate no significant differences in WIT (P = .053), EBL (P = .417), operative time (P = .059), reduction in eGFR from baseline to discharge (P = .921), reduction in eGFR from baseline to a mean follow-up of 13 months (P = .854), and hospital LOS (P = .903) among those with anterior versus posterior renal masses. Tumor size (β = 1.08, P < .001) and R.E.N.A.L. nephrometry score (β = 0.59, P = .025) were independently associated with longer WIT. WIT was independently associated with longer operative time (β = 4.14, P < .001) and longer hospital LOS (β = 0.05, P = .001). Age was independently associated with longer hospital LOS (β = 0.01, P = .037). BMI (β = −0.72, P = .034) and baseline eGFR were independently associated with decreased eGFR at discharge (β = −0.21, P = .031). EBL was lower in patients with left compared with right renal tumors (β = −29.0, P = .035).

Table 3.

Multiple Regression Analyses Predicting Warm Ischemia Time, Estimated Blood Loss, and Operative Time

	Warm ischemia time			Estimated blood loss			Operative time
	β	95% CI	P	β	95% CI	P	β	95% CI	P
Controls
Age	−0.01	(−6.87, 9.20)	.706	0.62	(−0.34, 1.57)	.204	0.33	(−0.17, 0.84)	.194
Gender	0.49	(−1.07, 2.05)	.535	22.1	(−6.72, 50.85)	.131	7.18	(−8.05, 22.42)	.351
BMI	0.09	(−0.04, 0.21)	.180	1.00	(−1.33, 3.34)	.396	1.14	(−0.11, 2.39)	.073
Tumor size	1.08	(0.55, 1.61)	.000^a	6.58	(−3.22, 16.39)	.186	−0.20	(−6.03, 5.63)	.945
Nephrometry score	0.59	(0.08, 1.11)	.025^a	−0.71	(−10.29, 8.87)	.884	2.77	(−2.43, 7.98)	.293
Hilar	1.08	(−1.53, 3.69)	.414	8.94	(−39.22, 57.11)	.713	−12.9	(−38.16, 12.30)	.311
Malignancy	1.59	(−0.17, 3.37)	.076	15.7	(−16.95, 48.32)	.342	−0.15	(−17.66, 17.37)	.987
Tumor laterality	0.11	(−1.35, 1.57)	.880	−29.0	(−55.89, −2.15)	.035^a	−6.80	(−20.92, 7.31)	.340
Warm ischemia time							4.14	(2.09, 6.19)	.000^a
Primary comparison
Tumor location	1.47	(−0.02, 2.97)	.053	−11.3	(−38.84, 16.25)	.417	14.4	(−0.56, 29.34)	.059

Statistically significant difference at the P < .05 level.

BMI, body mass index; CI, confidence interval.

Table 4.

Multiple Regression Analyses Predicting Length of Hospitalization and Estimated Glomerular Filtration Rate Reduction at Discharge and at Most Recent Follow-Up

	Hospital length of stay			eGFR reduction (at discharge)			eGFR reduction (at most recent follow-up)
	β	95% CI	P	β	95% CI	P	β	95% CI	P
Controls
Age	0.01	(0.00, 0.02)	.037^a	0.07	(−0.21, 0.34)	.628	0.09	(−0.29, 0.47)	.650
Gender	0.08	(−0.19, 0.39)	.512	3.35	(−4.20, 10.90)	.380	1.81	(−8.43, 12.04)	.726
BMI	0.01	(−0.02, 0.03)	.566	−0.72	(−1.39, −0.06)	.034^a	−0.12	(−0.96, 0.72)	.779
Tumor size	−0.08	(−0.19, 0.03)	.152	−1.38	(−4.17, 1.41)	.329	−0.99	(−4.99, 3.02)	.625
Nephrometry score	−0.01	(−0.11, 0.09)	.905	−0.79	(−3.35, 1.75)	.535	−2.42	(−5.81, 0.96)	.157
Hilar	−0.24	(−0.75, 0.26)	.340	−5.42	(−18.58, 7.75)	.416	−1.32	(−18.14, 15.49)	.876
Malignancy	0.23	(−0.11, 0.56)	.187	−1.06	(−9.63, 7.75)	.805	1.23	(−10.68, 13.15)	.837
Tumor laterality	0.02	(−0.26, 0.29)	.907	−2.24	(−9.17, 4.69)	.523	3.77	(−5.88, 13.42)	.439
Warm ischemia time	0.05	(0.01, 0.09)	.001^a	−0.24	(−1.23, 0.74)	.624	−0.03	(−1.62, 1.57)	.974
Baseline eGFR				−0.21	(−0.39, −0.12)	.031^a	−0.14	(−0.39, 0.12	.279
Primary comparison
Tumor location	−0.02	(−0.31, 0.27)	.903	−0.38	(−8.07, 7.29)	.921	−0.99	(−11.7, 9.72)	.854

Statistically significant difference at the P < .05 level.

BMI, body mass index; CI, confidence interval; eGFR, estimated glomerular filtration rate.

Predictors of postoperative complications and positive surgical margins are presented in Table 5. Multivariable logistic regression demonstrated no significant differences in surgical margin status (P = .873) and postoperative complication rates (P = .517) between anterior and posterior tumors. The six complications in the series were all Clavien Grade 2 or less, and there were no open conversions. The four cases of complication in the posterior group included urinary tract infection, deep vein thrombosis, urinary retention requiring a Foley catheter at an outside emergency room, and a urethral stricture. The two complications in the anterior group included hematuria and rectal bleeding from hemorrhoids requiring a hospital visit.

Table 5.

Multivariable Logistic Regression Analyses Predicting Postoperative Complication Rates and Positive Surgical Margin Rates

	Postoperative complication			Surgical margin status
Variable	OR	95% CI	P	OR	95% CI	P
Controls
Age	1.07	(0.99, 1.21)	.144	0.99	(0.94, 1.05)	.628
Gender	0.26	(0.01, 3.43)	.377	2.05	(0.40, 10.56)	.375
BMI	1.26	(1.02, 1.68)	.062	0.90	(0.76, 1.04)	.185
Tumor size	1.91	(0.56, 2.45)	.621	0.93	(0.47, 1.59)	.812
Nephrometry score	1.16	(0.53, 2.47)	.693	1.19	(0.67, 2.13)	.543
Hilar	0.00	(0.00, 1190)	.996	1.55	(0.16, 13.01)	.686
Malignancy	0.94	(0.07, 24.5)	.967	1.26	(0.22, 10.65)	.808
Tumor laterality	5.11	(0.39, 228.0)	.279	0.49	(0.09, 2.26)	.364
Primary comparison
Tumor location	2.39	(0.22, 56.54)	.517	1.14	(0.24, 6.28)	.873

BMI, body mass index; CI, confidence interval; OR, odds ratio.

Discussion

The present study compared perioperative outcomes between patients with anterior and posterior renal masses treated exclusively with TPRPN. In multivariable analyses, we found no significant difference in operative time, WIT, EBL, hospital LOS, reduction in eGFR, postoperative complication rates, and surgical margin status between patients with anterior and posterior tumors when controlling for age, gender, BMI, tumor size, R.E.N.A.L. nephrometry score, hilar location, and tumor laterality. Several studies have been published examining the impact of TP versus RP approach to minimally invasive PN and have reached divergent conclusions.^1–10 Only one study has specifically examined the TP approach for anterior versus posterior tumors in robotic surgery.¹² In this study no significant differences were found in EBL, WIT, hospital LOS, operative time, surgical margin status, and complication rates. The analysis did not control for confounding variables such as tumor size, R.E.N.A.L. nephrometry score, age, BMI, and gender, which could influence the outcomes assessed and result in a biased estimated of the difference in perioperative outcomes between the two groups. Increasing R.E.N.A.L. nephrometry score in particular has been found to be associated with increased hospital LOS, EBL, WIT, and major complication rates.^16,17 In addition, increasing tumor size has been found to significantly correlate with operative time, hospital LOS, and WIT.¹⁷

In univariable independent-samples t tests and chi-squared tests, our findings corroborate the findings by Harris et al.¹²—similar EBL, WIT, positive surgical margins, and complication rates. Although we found longer operative time for posterior tumors in univariable analysis, results from more robust analyses (i.e., multivariable logistic and linear regression) adjusting for variables not included in univariable analyses (i.e., independent-samples t test and chi-squared tests) demonstrate no difference in operative time, WIT, EBL, postoperative complications, and positive surgical margins. These findings confirm the findings by Harris et al.¹² and furthermore demonstrate the importance of controlling for confounding variables. Our findings in multivariable analyses additionally show that a TP approach to anterior and posterior renal masses results in no difference in hospital LOS, reduction in eGFR from baseline to discharge, and reduction in eGFR from baseline to a mean follow-up of 13 months.

The choice to approach PN with a TP or RP approach depends on tumor location and surgeon preference and experience, along with patient comorbidities, as well as the complication profile associated with each approach.¹¹ A purported advantage of the RP approach in obese patients is avoidance of the pannus and copious intraabdominal adipose tissue. The clinical significance of this advantage is controversial, however, with one study involving 202 patients (n = 46 with BMI ≥30 kg/m²) reporting improved outcomes in RP for EBL, operative time, LOS, and complications¹⁸ and another study involving 51 morbidly obese (BMI ≥40 kg/m²) patients reporting no statistical difference.¹⁹ It is likely that the key to minimizing the morbidity of any operative approach is surgeon experience and comfortableness with the approach, which is reflected in hospital surgical volume. Indeed, it has been reported that complication rates for robotic-assisted PN are lower at high-volume centers.²⁰ WIT has also been found to inversely correlate with surgeon volume, across multiple surgeons and institutions.²¹

TPRPN is a more familiar modality for many surgeons¹² and is the preferred approach for anterior tumors.^1,6–8 In several studies examining the impact of tumor location on surgical approach, it was found that anterior tumors were treated more often with the TP approach with rates of 62%–97%,^1,6–8 but even posterior tumors were treated transperitoneally in 17%–30%.^1,6–8 Also, given the relative unfamiliarity with the RP approach by many urologic surgeons,¹² the learning curve to master the RP approach may outweigh any purported operative benefits. In fact, the learning curve for TPRPN itself has been reported to be 20–30 cases.²² Our study demonstrates that this additional skill set may be unnecessary, as the TP approach is equally effective with equivalent perioperative outcomes between anterior and posterior renal masses. Therefore, although other patient factors may drive the choice of surgical approach (i.e., prior abdominal or ipsilateral renal surgery, BMI), tumor location should not.

A limitation of our study is that it is a single-center, single-surgeon experience. In addition, our results are limited by a retrospective methodology that is not as generalizable as a randomized design. There are also additional potential confounding variables that were not controlled for, such as prior abdominal surgery, prior renal biopsy, the use of selective clamping, patient comorbidities, and amount of perinephric fat. Also, the lack of an RP group renders us unable to comment on the suitability of this approach for anterior and posterior tumors compared with the TP approach, which is our preferred approach.

In conclusion, the TP approach to robotic-assisted PN for posterior tumors results in no difference in operative time, WIT, EBL, LOS, positive surgical margins, reduction in eGFR, or postoperative complications. Because perioperative outcomes are equivalent using a TP approach to PN for anterior and posterior renal masses, the decision regarding surgical approach should not be based on tumor location alone. Posterior tumors may be successfully accessed and treated using a TP approach without additional morbidity.

Footnotes

Disclosure Statement

No competing financial interests exist.

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