Comparison of Hand-Assisted Laparoscopic vs Robot-Assisted Laparoscopic vs Open Partial Nephrectomy in Patients with T1 Renal Masses

Abstract

Purpose:

To evaluate the validity of hand-assisted laparoscopic partial nephrectomy (HALPN) for small renal masses, patients who underwent HALPN, robot-assisted laparoscopic partial nephrectomy (RALPN), or open partial nephrectomy (OPN) at a single medical institution were compared in terms of perioperative outcomes.

Patients and Methods:

In this retrospective cohort study, all 590 consecutive patients who underwent HALPN (n=89), RALPN (n=147), or OPN (n=354) between July 2011 and April 2014 in a single institute were compared in terms of perioperative outcomes, including the mean operative time, warm ischemia time (WIT), length of the hospital stay, change in the estimated glomerulofiltration rate (eGFR), duration of analgesic use, surgical margins, and adverse events. The patient groups were compared by a multivariate regression model, in which adjustments were made for differences in baseline demographic and tumor characteristics.

Results:

OPN associated with a significantly longer mean operative time (187 minutes) than RALPN (162 minutes; p<0.001) or HALPN (172 minutes; p=0.013), a longer hospital stay (7.3, 5.3, and 5.9 days, respectively; p<0.001 and <0.001, respectively), and a longer duration of analgesic use (6.6, 4.6, and 5.4 days, respectively; p<0.001 and <0.001, respectively). HALPN and RALPN were equivalent in terms of operative time. RALPN had a significantly longer WIT than HALPN and OPN (p<0.001 and <0.001, respectively). HALPN had a significantly longer hospital stay than RALPN (p=0.026). The three methods differed in terms of eGFR change (p=0.028), but multivariate analysis found that the surgical method was not a significant factor for eGFR. The three methods did not differ in terms of complication rates.

Conclusions:

HALPN associated with shorter operative and convalescence times compared with OPN. HALPN was generally not inferior to RALPN in terms of perioperative outcomes, although it associated with a longer convalescence.

Introduction

The American Urological Association (AUA) guidelines recommend partial nephrectomy (PN), when feasible, as a standard treatment for patients presenting with T1 renal cell carcinoma.¹ However, whether this approach really is the best method for treating a small renal mass was initially thrown in doubt when a prospective randomized study comparing the oncologic outcomes of elective nephron-sparing surgery and radical nephrectomy for low-stage renal cell carcinoma suggested that nephron-sparing surgery may not confer overall survival benefits.² Nevertheless, subsequent evidence indicated that compared with radical nephrectomy, PN indeed associates with a lower renal function impairment, better overall patient survival, and equivalent oncologic survival.^3
–5

A number of minimally invasive technologies have been made recently. There are two different endoscopic approaches for PN, namely, the laparoscopic transperitoneal and retroperitoneoscopic approaches. For both approaches, hand-assisted and robotic-assisted techniques are available. Since the principal advantage of the retroperitoneoscopic approach is the absence of intra-abdominal manipulation, this technique is favored mostly in patients who have undergone previous abdominal surgery or who have a posteriorly located tumor.⁶ Therefore, at present, there are three different laparoscopic PN (LPN) techniques, namely, pure LPN, hand-assisted LPN (HALPN), and robot-assisted LPN (RALPN). HALPN has one marked advantage over LPN and RALPN; it allows the surgeon to perform laparoscopic procedures with his or her hand inside the patient's abdominal cavity, thus maintaining tactile feedback.⁷ Moreover, since RALPN has largely overcome the technical difficulties of LPN, it is increasingly being performed instead of LPN.⁸

Despite these advances in minimally invasive PN, open PN (OPN) is still predominantly used at present to treat small renal masses.⁹ All this technical diversity has spawned debate about which of the three PN techniques (OPN, HALPN, and RALPN) yields the best outcomes in terms of warm ischemia times (WIT), positive surgical margins, perioperative complications, and renal functional outcomes. To address these issues, the contemporary PN series between 2011 and 2014 at a single medical center was analyzed to compare the perioperative outcomes of HALPN, RALPN, and OPN for T1 renal tumor.

Patients and Methods

Study population

This retrospective cohort study was based on all consecutive patients with T1 renal tumor who underwent HALPN, OPN, or RALPN between July 2011 and April 2014 in a single medical institute. Thus, the medical charts of 590 consecutive patients who underwent HALPN (n=89), RALPN (n=147), or OPN (n=354) were reviewed. All patient data were obtained from our Institutional Review Board-approved database, which prospectively registers all baseline patient characteristics.

Surgical technique

The HALPN procedure that is performed in our institution is similar to the method described by Strup et al.¹⁰ Thus, an 8-cm vertical incision is made for a hand port and the Gel Port system (Applied Medical, Rancho Santa Margarita, CA) is applied. An additional two 12-mm trocars are then placed. Occasionally, a third (5-mm) trocar is used. For dissection, the Harmonic Ace scalpel (Endo Surgery; Ethicon, Cincinnati, OH) is generally used instead of electrocautery laparoscopic scissors. The RALPN procedure that is used in our institution is similar to the method described by Gettman et al.¹¹ Thus, the da Vinci S robot (Intuitive Surgical Systems, Sunnyvale, CA) with a four-arm technique and a transperitoneal approach is employed. Hilar control is obtained through bulldog clamping. OPN is performed using a subcostal or flank approach. Most of the present cases involved the retroperitoneal approach. The renal pedicle is generally clamped by using a bulldog clamp. Occasionally, when tumor is superficial and peripheral, the pedicle is not clamped. Depending on the operator's preference, ice is used during pedicle clamping. Opened calices and bleeding sites are always carefully repaired.

Statistical considerations

For all patients, the tumor localization was determined by reviewing the radiographic images and the RENAL nephrometry scores were calculated. The three groups were compared in terms of perioperative outcomes by using a multivariate regression model, in which adjustments were made for potential confounders, namely, baseline demographic and tumor characteristics. Comparisons involving categorical and continuous variables were made by using the chi-square test and ANOVA, respectively. All reported p-values were two sided, and a value of p<0.05 was considered to indicate statistical significance. SPSS version 18.0 (IBM Corp., Armonk, NY) was used for statistical analyses.

Results

The demographic data are summarized in Table 1. Regarding the perioperative outcomes, the average operative times of the HALPN, RALPN, and OPN groups were 173, 162, and 187 minutes, respectively (p<0.001). The HALPN and RALPN groups did not differ significantly in terms of this variable (p=0.18). The RALPN group had the longest mean WIT (24.7 minutes). However, the HALPN and OPN groups did not differ significantly in terms of WIT (19.4 vs19.6 minutes, p=0.85). The OPN group had the longest average hospitalization stay (7.3 days). Moreover, the HALPN group stayed significantly longer in hospital than the RALPN group (5.9 vs 5.3 days, p=0.026). The OPN group also had a significantly longer duration of analgesic use (6.6 days) than the RALPN (4.6 days) or HALPN (5.4 days) group (p<0.001). The three groups differed significantly in terms of estimated glomerular filtration rate (eGFR) decrease; it was 3.20, 2.40, and 4.34 mL/minute/1.73 m² for the HALPN, RALPN, and OPN groups, respectively (p=0.028) (Table 2). However, multivariate regression model analysis did not find that the operation type associated significantly with the eGFR decrease. By contrast, age, American Society of Anesthesiologists score (ASA score), solitary kidney status, and the RENAL nephrometry score all associated significantly with the eGFR decrease. However, multivariate regression model analysis showed that OPN associated significantly with a long operation time. Gender also associated significantly regardless of the operation type; PN took about 15 minutes longer in men than in women. Body mass index also associated significantly with operative time; the higher the body mass index (BMI), the longer the operation time (Table 3).

Table 1.

Demographic and Tumor Characteristics of Entire Cohort

	HALPN (n=89)	RALPN (n=147)	OPN (n=354)	Total (n =590)	p-Value
Patient age, year, mean (SD)	53.6 (9.7)	52.5 (11.9)	55.3 (12.4)	54.4 (11.9)	0.05
Male gender, n (%)	62 (69.7)	108 (73.5)	270 (76.3)	440 (74.6)	0.41
BMI (SD)	25.8 (3.1)	25.56 (3.2)	24.5 (3.0)	24.9 (4.1)	0.02
ASA score (SD)	1.66 (0.5)	1.51 (0.52)	1.40 (0.49)	1.47 (0.51)	<0.001
Baseline eGFR (SD, mL/minute/1.73 m²)	82.1 (10.4)	82.3 (9.9)	80.1 (13.3)	80.9 (12.1)	0.12
Prior abdominal surgery, n (%)	4 (4.5)	16 (10.9)	33 (9.3)	53 (9.0)	0.24
Solitary kidney, n (%)	1 (1.1)	1 (0.6)	10 (1.1)	12 (2.8)	0.24
Right/left	53/36	79/68	177/177	309/281	0.25
(R) Tumor size (SD, cm)	2.39 (0.95)	2.58 (1.13)	2.80 (1.35)	2.68 (1.25)	0.08
(E) Exophytic/endophytic properties					0.007
≥50%	24 (27%)	68 (46.3%)	143 (40.4%)	235 (39.8%)
<50%	48 (53.9%)	60 (40.8%)	134 (37.9%)	242 (41.0%)
Entirely endophytic	17 (19.1%)	19 (12.9%)	77 (21.8%)	113 (19.2%)
(N) Nearness of tumor to the collecting system					0.13
≥7	44 (49.4%)	74 (50.3%)	205 (57.9%)	323 (54.7%)
>4 but <7	16 (18%)	37 (25.2%)	64 (18.1%)	117 (19.8%)
≤4	29 (32.6%)	36 (24.5%)	85 (24%)	150 (25.4%)
(A) Anterior/posterior					0.23
Anterior	31 (34.8%)	71 (48.3%)	149 (42.1%)	251 (42.5%)
Posterior	41 (46.1%)	52 (35.4%)	130 (36.7%)	223 (37.8%)
Neither	17 (19.1%)	24 (16.3%)	75 (21.2%)	116 (19.7%)
(L) Location relative to polar lines					0.002
Upper and lower pole	34 (38.2%)	75 (51.0%)	112 (31.6%)	221 (37.4%)
Cross polar line	28 (31.5%)	39 (26.5%)	134 (37.9%)	201 (34.1%)
Entirely between polar line	27 (30.3%)	33 (22.5%)	108 (30.5%)	168 (28.5%)
RENAL nephrometry score (SD)	6.21 (1.61)	6.58 (1.80)	6.72 (1.63)	6.51 (1.73)	0.07

ANOVA, chi-square test, Kruscal–Wallis test.

ASA score=American Society of Anesthesiologists score; BMI=body mass index; eGFR=estimated glomerulofiltration rate; HALPN=hand-assisted laparoscopic partial nephrectomy; OPN=open partial nephrectomy; RALPN=robot-assisted laparoscopic partial nephrectomy; SD=standard deviation.

Table 2.

Perioperative Outcomes in the Three Cohorts

	HALPN (n=89)	RALPN (n=147)	OPN (n=354)	p-Value
Operative time (SD, minute)	172.9 (42.3)	162.3 (32.2)	187.2 (43.8)	<0.0001
WIT (SD, minute)	19.4 (6.7)	24.7 (7.3)	19.6 (6.7)	<0.0001
Length of hospitalization (SD, day)	5.9 (1.66)	5.3 (1.41)	7.3 (2.06)	<0.0001
Decrease in eGFR (SD, mL/minute/1.73 m²)	3.20 (5.44)	2.40 (6.70)	4.34 (8.34)	0.028
Resection margin (SD, cm)	0.35 (0.24)	0.36 (0.26)	0.46 (0.36)	0.0007
Duration of analgesic (SD, day)	5.40 (1.24)	4.65 (1.26)	6.61 (1.66)	<0.0001
Postoperative complications (%)	4 (4.49)	5 (3.4)	28 (7.91)	0.13

ANOVA, chi-square test.

WIT=warm ischemia time.

Table 3.

Linear Regression Model of Perioperative Outcomes

	Multivariate analysis
Variable	Estimate (95% CI)	p-Value
Operative time
RALPN/HALPN	−8.91 (−19.5, 1.70)	0.09
OPN/HALPN	15.11 (5.67, 24.56)	0.002
Gender M/F	15.05 (7.66, 22.45)	<0.001
BMI	1.66 (0.60, 2.72)	0.002
RENAL nephrometry score	3.24 (1.38, 5.09)	0.001
WIT
RALPN/HALPN	6.01 (4.21, 7.81)	<0.001
OPN/HALPN	0.42 (−1.17, 2.01)	0.60
RENAL nephrometry score	0.88 (0.56, 1.20)	<0.001
Length of hospitalization (log)
RALPN/HALPN	−0.11 (−0.17, −0.05)	0.001
OPN/HALPN	0.20 (0.14, 0.25)	<0.001
Duration of analgesic (log)
RALPN/HALPN	−0.15 (−0.21,0.10)	<0.001
OPN/HALPN	0.20 (0.15, 0.24)	<0.001
Decrease in eGFR
RALPN/HALPN	−0.11 (−2.05, 1.82)	0.90
OPN/HALPN	1.13 (−0.60, 2.87)	0.20
Age	0.11 (0.06, 0.16)	<0.001
ASA score	1.87 (0.59, 3.14)	0.004
Solitary kidney	5.13 (0.91, 9.35)	0.01
RENAL nephrometry score	0.72 (0.38, 1.06)	<0.001

CI=confidence intervals.

The complications included hematuria, urine leak, hypoxia, transfusion, pesudoaneurysm, and wound dehiscence. The overall complication rates for the HALPN, RALPN, and OPN groups were 4.5%, 3.4%, and 7.9%, respectively (Tables 2 and 4). The three groups did not differ in terms of complication rates (p=0.13). Multivariate regression analysis revealed that only the RENAL nephrometry score was a significant factor for complication rate (odds ratio 1.49, 95% confidence intervals 1.22, 1.81) (Table 5). The surgical margins in all patients were negative.

Table 4.

Complications

	HALPN 4 (4.5%)	RALPN 5 (3.4%)	OPN 28 (7.9%)
Clavien grade I	Hematuria (1)	Hypoxia (1), hematuria (1)	Ileus (4)
Clavien grade II	—	Blood transfusion (1)	Blood transfusion (17)
Clavien grade III-IV	Pseudoaneurysm (1), urine leak (1), wound dehiscence (1)	Pseudoaneurysm (1), urine leak (1)	Pseudoaneurysm (2), urine leak (2), wound dehiscence (3)

Table 5.

Independent Predictor of Complication

	Univariate		Multivariable
	OR (95% CI)	p-Value	OR (95% CI)	p-Value
Group
RALPN/HALPN	0.75 (0.20, 2.86)	0.67	0.96 (0.25, 3.77)	0.95
OPN/HALPN	1.83 (0.62, 5.35)	0.27	1.74 (0.58, 5.21)	0.32
Age	1.01 (0.98, 1.04)	0.47
Gender M/F	1.50 (0.64, 3.48)	0.35
BMI	0.97 (0.95, 0.99)	0.64
ASA score	1.12 (0.58, 2.19)	0.73
Prior abdominal surgery	0.89 (0.26, 2.99)	0.85
Solitary kidney	1.37 (0.17, 10.9)	0.76
Right/left	0.85 (0.44, 1.66)	0.64
RENAL nephrometry score	1.52 (1.25, 1.85)	<0.001	1.49 (1.22, 1.81)	<0.001

OR=odds ratio.

Discussion

HALPN was introduced by Jordan and Winslow in 1993 and is a practical option for small (<4 cm) renal masses.^12,13 While two studies have compared HALPN with RALPN or OPN,^14,15 they are disadvantaged by a small sample size or by differences between the groups in terms of tumor characteristics. Therefore, to determine whether these three methods differ in terms of perioperative outcomes and complications, we designed the present study, which was reasonably sized and involved covariant-adjusted group comparisons.

Although the retroperitoneal approach has several advantages that allow direct access to the renal artery, thus reducing the chance of organ injury, this approach is complicated by the small working space and relative paucity of distinct anatomical landmarks.^6,16 Therefore, unless patients are not eligible for the transperitoneal approach, we prefer to employ the transperitoneal approach rather than the retroperitoneal approach. By contrast, most of the OPN surgeries in the present study involved the retroperitoneal approach. Moreover, there was variability in terms of whether ice was used when the pedicle was clamped in OPN; 22.8% of the OPN cases involved the use of ice. There was also some variability in terms of whether the nonclamp technique was used, if the tumor was superficial and peripheral clamping was not performed. This applied in four HALPN cases, one RALPN case, and 21 OPN cases.

OPN is considered to be the gold standard treatment for small renal tumors as its renal functional outcomes and disease-specific survival are superior and equivalent to those of radical nephrectomy, respectively.^17,18 However, compared with LPN, OPN associates with an increased convalescence time because it involves a large incision that produces intense pain. By contrast, LPN reduces recovery time while yielding similar oncologic and nephrologic outcomes. Indeed, one study of 1800 consecutive patients who underwent either OPN or LPN reported that the LPN group had shorter operative times, less intraoperative blood loss, and a shorter length of hospital stay. However, it should be noted that the patients who underwent LPN were more likely than the patients undergoing OPN to have more peripheral and smaller tumors. Moreover, due to the greater number of surgical steps involved in LPN compared with OPN, LPN associated with longer WITs and a significant increase in the postoperative complication rate.¹⁹ To reduce the problems associated with such a difficult laparoscopic technique, RALPN was developed. It reduces surgeon fatigue and shortens the learning curve of LPN and has as a result largely replaced LPN.²⁰ HALPN is also another traditional minimally invasive approach for PN. Thus, the three most commonly used PN techniques in our medical institution in the study period were HALPN, RALPN, and OPN.

A previous study showed that HALPN associates with a shorter mean operation time than OPN (161 vs 191 minutes; p=0.027). It also associates with less blood loss (120 vs 353 cc; p=0.0003), a shorter WIT (27.0 vs 33.0 minutes; p=0.035), and a smaller overall complication rate (18.3% vs 32.5%, p=0.10).¹⁴ The present study also showed that HALPN associated with better outcomes than OPN in terms of most perioperative variables. This may reflect the fact that although HALPN is still a minimally invasive approach, it also allows tactile feedback that aids tumor perception and dissection and specimen extraction and reduces the WIT.²¹ The present study showed that HALPN associated with a shorter convalescence time than OPN. However, HALPN did not differ from OPN in terms of complication rates or eGFR decrease. Moreover, the WITs of these groups did not differ (19.4 vs 19.6 minutes, p=0.85). However, this contrasts with a previous study, which showed that HALPN has superior WIT compared with OPN.¹⁴

The present study also compared HALPN with RALPN. Unlike the equivalence of HALPN and OPN in terms of WIT, HALPN is associated with a shorter WIT (19.4 minutes) than RALPN (24.7 minutes; p<0.001). This is significant because Thompson et al.²² showed that a high WIT associates with an acute risk of postoperative renal failure and an increased risk of postoperative stage IV chronic kidney disease (CKD). Thus, WIT is an important predictor of renal function preservation. However, the present study could not demonstrate a relationship between WIT and postoperative renal failure. Another study also found that RALPN does not yield remarkable benefits in terms of perioperative outcomes relative to HALPN; moreover, RALPN is associated with increased cost.¹⁵

Most of the advantages of HALPN over other laparoscopic techniques stem from the surgeon being able to use his or her hand during the surgery. When resecting a tumor after positioning a hilar clamp, a fingertip can bluntly dissect a mass, similar to what is achieved by using a blade handle in open surgery. Moreover, using the hand to enclose a defect can be both effective and prompt. Grasping and folding a kidney by hand is also helpful for approximating the defect surface. Moreover, unlike OPN, HALPN is performed in our institute by using a high-definition laparoscopic monitor that facilitates the meticulousness of the technique.

It should, however, be noted that HALPN is more invasive than LPN or RALPN and can lead to wound problems and hernias. Furthermore, the hand can hinder laparoscopic vision during surgery. However, these problems are compensated by the great advantages yielded by the tactile feedback in HALPN. Moreover, although the open surgical technique is still considered to be the gold standard treatment in terms of renal function outcomes and disease-specific survival relative to radical nephrectomy,^17,18 HALPN is also amenable to oncologic principles. The present study suggested that HALPN may achieve the superior outcomes of OPN relative to radical nephrectomy, while tending to reduce complications.

This study has some limitations. First, there was a selection bias due to the use of different surgeons. Only HALPN was performed by one surgeon. Furthermore, although a multivariate regression model was employed, the study was not a randomized prospective study and thus it is subject to the inherent limitations of a retrospective analysis of observational data.

Conclusions

Compared to OPN, HALPN associated with a shorter operative time and convalescence period. Compared to RALPN, HALPN generally did not have inferior perioperative outcomes; however, it did associate with a significantly longer convalescence period. The three approaches did not differ in terms of the complication rate.

Footnotes

Author Disclosure Statement

The authors have no conflicts of interest to disclose.

Abbreviations Used

References

Campbell

, et al. Guideline for management of the clinical T1 renal mass. J Urol, 2009; 182:1271–1279.

Van Poppel

, et al. A prospective, randomised EORTC intergroup phase 3 study comparing the oncologic outcome of elective nephron-sparing surgery and radical nephrectomy for low-stage renal cell carcinoma. Eur Urol, 2011; 59:543–552.

MacLennan

, et al. Systematic review of oncological outcomes following surgical management of localised renal cancer. Eur Urol, 2012; 61:972–993.

Antonelli

, et al. Elective partial nephrectomy is equivalent to radical nephrectomy in patients with clinical T1 renal cell carcinoma: Results of a retrospective, comparative, multi-institutional study. BJU Int, 2012; 109:1013–1018.

Ficarra

, et al. A multicentre matched-pair analysis comparing robot-assisted versus open partial nephrectomy. BJU Int, 2014; 113:936–941.

Ren

, et al. Transperitoneal approach versus retroperitoneal approach: A meta-analysis of laparoscopic partial nephrectomy for renal cell carcinoma. PLoS One, 2014; 9:e91978.

Wolf

Jr . Hand-assisted laparoscopy: Pro. Urology, 2001; 58:310–312.

Benway

, et al. Robot assisted partial nephrectomy versus laparoscopic partial nephrectomy for renal tumors: A multi-institutional analysis of perioperative outcomes. J Urol, 2009; 182:866–872.

Kowalczyk

, et al. Comparative effectiveness, costs and trends in treatment of small renal masses from 2005 to 2007. BJU Int, 2013; 112:E273–E280.

10.

Strup

, et al. Laparoscopic partial nephrectomy: Hand-assisted technique. J Endourol, 2005; 19:456–459; discussion 459–460.

11.

Gettman

, et al. Robotic-assisted laparoscopic partial nephrectomy: Technique and initial clinical experience with DaVinci robotic system. Urology, 2004; 64:914–918.

12.

Jordan

, Winslow

. Laparoendoscopic upper pole partial nephrectomy with ureterectomy. J Urol, 1993; 150:940–943.

13.

, et al. A propensity-score matched comparison of perioperative and early renal functional outcomes of robotic versus open partial nephrectomy. PLoS One, 2014; 9:e94195.

14.

DeVoe

, et al. Hand-assisted laparoscopic partial nephrectomy after 60 cases: Comparison with open partial nephrectomy. Surg Endosc, 2009; 23:1075–1080.

15.

Elsamra

, et al. Hand-assisted laparoscopic versus robot-assisted laparoscopic partial nephrectomy: Comparison of short-term outcomes and cost. J Endourol, 2013; 27:182–188.

16.

Marszalek

, et al. Laparoscopic partial nephrectomy: A matched-pair comparison of the transperitoneal versus the retroperitoneal approach. Urology, 2011; 77:109–113.

17.

Mabjeesh

, Avidor

, Matzkin

. Emerging nephron sparing treatments for kidney tumors: A continuum of modalities from energy ablation to laparoscopic partial nephrectomy. J Urol, 2004; 171(2 Pt 1):553–560.

18.

Fergany

, Hafez

, Novick

. Long-term results of nephron sparing surgery for localized renal cell carcinoma: 10-year followup. J Urol, 2000; 163:442–445.

19.

Gill

, et al. Comparison of 1,800 laparoscopic and open partial nephrectomies for single renal tumors. J Urol, 2007; 178:41–46.

20.

Haber

, et al. Robotic versus laparoscopic partial nephrectomy: Single-surgeon matched cohort study of 150 patients. Urology, 2010; 76:754–758.

21.

Wolf

Jr. , Seifman

, Montie

. Nephron sparing surgery for suspected malignancy: Open surgery compared to laparoscopy with selective use of hand assistance. J Urol, 2000; 163:1659–1664.

22.

Thompson

, et al. Every minute counts when the renal hilum is clamped during partial nephrectomy. Eur Urol, 2010; 58:340–345.