Original Study
Laparoscopic Radical Cystectomy Versus Extraperitoneal Radical Cystectomy: Is the Extraperitoneal Technique Rewarding? Junjie Zhao,1,2 Shuxiong Zeng,1 Zhensheng Zhang,1 Tie Zhou,1 Bo Yang,1 Ruixiang Song,1 Yinghao Sun,1 Chuanliang Xu1 Abstract The surgical approach is an important factor in the development of postoperative ileus (POI) after radical cystectomy (RC); however, studies comparing extraperitoneal open radical cystectomy (EORC) and laparoscopic RC (LRC) are lacking. We retrospectively studied 41 LRCs and 53 EORCs performed by a single surgeon. In our experience, EORC had a POI rate similar to that of LRC, despite the presence of factors favoring LRC, and was associated with similar oncologic outcomes, indicating that extraperitoneal LRC could be a promising method for improving the perioperative results. Background: To study whether extraperitoneal radical cystectomy (EORC) accelerates the postoperative recovery of bowel function compared with laparoscopic radical cystectomy (LRC). Patients and Methods: All the patients with bladder cancer who underwent EORC or LRC with an ileal conduit by a single surgeon from January 2009 to June 2014 were investigated. The perioperative outcomes and follow-up data were analyzed, with a focus on postoperative ileus (POI). Results: A total of 41 LRCs and 53 EORCs met the inclusion criteria. LRC was associated with a significant reduction in the estimated blood loss (278 vs. 356 mL, P ¼ .017) and a shorter hospital stay (8.1 vs. 9.2 days, P ¼ .003). However, LRC was also associated with longer operative times (349 vs. 316 minutes, P ¼ .022). The incidence of paralytic POI was 7.3% (3 of 41) and 7.5% (4 of 53; P ¼ .966) and the obstructive POI rate was 4.9% (2 of 41) and 3.8% (2 of 53; P ¼ .792) for the LRC and EORC groups, respectively. No significant differences were noted in blood transfusion requirements, interval to flatus or liquid intake, or opioid dosage. No patient in either group had positive surgical margins, and no significant differences were observed in the lymph node count (P ¼ .112). At a median follow-up period of 28.7 months (range, 3-62 months), no significant differences were seen between the LRC and EORC groups in the 3-year overall, cancer-specific, or cancer-free survival rates. Conclusion: EORC resulted in a POI rate similar to that of LRC, despite factors favoring LRC. Our results suggest that extraperitoneal LRC could improve the perioperative outcomes. Clinical Genitourinary Cancer, Vol. 13, No. 4, e271-7 ª 2015 Elsevier Inc. All rights reserved. Keywords: Bladder cancer, Cystectomy, Ileus, Laparoscopy, Morbidity
Introduction J. Zhao and S. Zeng contributed equally to the present report. 1
Department of Urology, Changhai Hospital, Second Military Medical University, Shanghai, People’s Republic of China 2 Department of Urology, Yantai Yuhuangding Hospital, Shandong, People’s Republic of China Submitted: Oct 30, 2014; Revised: Jan 6, 2015; Accepted: Jan 16, 2015; Epub: Jan 21, 2015 Address for correspondence: Chuanliang Xu, MD, Department of Urology, Changhai Hospital, Second Military Medical University, 168 Changhai Road, Shanghai 200433, People’s Republic of China E-mail contact: [email protected]
1558-7673/$ - see frontmatter ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.clgc.2015.01.006
Radical cystectomy (RC) with urinary diversion remains the most aggressive surgical option in urology and has a high incidence of postoperative complications. During the early recovery period after RC, postoperative (paralytic and obstructive) ileus (POI) accounts for most postoperative complications, affecting approximately 23% of patients.1 Laparoscopic RC (LRC) and robotic-assisted RC (RARC) are characterized by reduced blood loss and postoperative pain and have emerged as minimally invasive modalities that lead to a significant improvement in intestinal function recovery. These techniques have been
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Laparoscopic Versus Extraperitoneal Radical Cystectomy increasingly used by urologists.2,3 Although minimally invasive surgery is becoming increasingly popular, POI remains the most common complication. Xylinas et al4 recently reported on 175 consecutive patients who had undergone RARC with extracorporeal urinary diversion. Of these 175 patients, 18 (10.3%) developed paralytic POI and 2 (1.1%) obstructive POI and required a second operation.4 POI is the most frequent complication occurring immediately after surgery. The paralytic POI rate after LRC has been 10.5%.5 The incidence of paralytic POI has been alarmingly high and comparable to the rate after laparoscopic colectomy (10.1%).6 Laparoscopic colectomy is considered to be the surgery most at risk of leading to the development of paralytic POI. This led us to hypothesize that other underlying causes of paralytic POI are involved after minimally invasive surgery (in addition to classic risk factors, such as increased blood loss and opioid use for postoperative pain control).7,8 Therefore, the pathogenesis of POI in the context of minimally invasive surgery should be investigated. Extraperitoneal open radical cystectomy (EORC), a modification of the conventional transperitoneal technique, results in a dramatically reduced POI risk compared with traditional open surgery.9,10 The distinguishing feature of EORC involves the total restoration of the peritoneum during the operation. LRC is different. The operative steps of LRC are basically duplicated from the transperitoneal open techniques. Thus, we have presumed that the absence of retroperitonealization during LRC is likely an important factor contributing to the development of POI. Hence, we conducted a novel retrospective study comparing EORC and LRC, both with ileal conduit (IC) diversion, to investigate whether EORC facilitates more robust postoperative intestinal function recovery than LRC. The procedures were performed by a single surgeon during a 5-year period.
Patients and Methods
demonstrating air fluid levels. In addition to POI, all other postoperative complications before discharge were recorded, including wound healing disorders (ie, any wound problems, including a sterile or an infectious fluid collection), wound dehiscence, and incisional hernias. The oncologic outcomes and survival data, including overall survival, cancer-specific survival, and cancer-free survival, were also evaluated.
Surgical Techniques LRC With Intraperitoneal IC. In the LRC cohort, bilateral pelvic lymphadenectomy and cystectomy were performed according to the technique of Matin and Gill.11 The lateral parietal peritoneum was incised above the external iliac artery and extended distally along the external iliac artery to the pubic bone. After standard pelvic lymph node dissection, a transverse incision of the peritoneum was created in the retrovesical pouch, and the bilateral vasa deferentia were divided. The Denonvilliers fascia was horizontally incised. The peritoneotomy was then extended anteriorly toward the umbilicus in an inverted-U shape, incorporating each medial umbilical ligament, and dividing the urachus high near the umbilicus. The lateral and posterior vascular pedicles of the bladder and prostate were controlled with sequential firings of a Harmonic scalpel (Johnson & Johnson, Cincinnati, OH) or LigaSure vessel sealing system (Valleylab, Tyco Healthcare Group, Boulder, CO). Hem-o-Lok clips (Weck Surgical Instruments, Teleflex Medical, Durham, NC) were occasionally used for large caliber arterioles. Both ureters were distally clipped and divided, and the left ureter was laparoscopically transferred to the right side through an incision created in the sigmoid mesentery after the bladder had been resected. The bowel work and ureteroileal anastomosis were performed extracorporeally through a 5- to 6-cm infraumbilical wound extended from the umbilical port incision. After the IC had been formed, the body of the conduit was free in the peritoneal cavity, and the wound was closed without restoring the peritoneal cavity.
Study Cohort From January 2009 to June 2014, all the patients with bladder cancer who underwent LRC or EORC with IC diversion were enrolled in the present study. We excluded those patients who had undergone robotic-assisted radical cystectomy. LRC and EORC was performed by a single surgeon (C.L.X.), who was proficient in both techniques. The clinical and follow-up data were retrospectively collected from our bladder cancer database. The clinical and pathologic parameters included age, gender, body mass index (BMI), American Society of Anesthesiologists (ASA) score, history of abdominal surgery, disease stage, tumor grade, type of bowel preparation, operative time (skin to skin), estimated blood loss (EBL), transfusion requirement, interval to flatus, interval to liquid intake, hospital stay, dosage of opioids for postoperative pain management, and other techniques used to stimulate a rapid return of bowel function (ie, chewing gum and fast-track surgery). Paralytic POI was defined as a period > 5 days before the return of normal bowel function.5 Normal bowel function was defined as the presence of bowel sounds, the passage of stool or flatus, and oral food tolerance for 24 hours. Paralytic POI was not diagnosed when small bowel obstruction (SBO) developed in patients presenting with abdominal pain, abdominal distension, and/or vomiting associated with an upright abdominal radiograph
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EORC With Extraperitoneal IC. In the EORC cohort, standard bilateral pelvic lymph node dissection and open RC were performed using a radical retrograde extraperitoneal approach through a 12- to 15-cm midline incision in the lower abdomen.12 The rectus abdominis muscles were split at the midline, and the underlying transversalis fascia was incised. A plane was created immediately superficial to the peritoneum, entering the space of Retzius inferiorly and the retroperitoneal space on either side with the help of a selfretaining retractor. Bilateral pelvic lymphadenectomy, mobilization of the bladder, suturing and division of the dorsal vein complex and division of the urethra were performed outside the peritoneal cavity, which was opened at the end of the extirpative portion. The bladder with a peritoneal flap covering the bladder dome and urachus was resected en bloc by cutting the urachus at the level of the umbilicus. Next, extracorporeal IC formation was initiated. After the procedure, the peritoneum was completely reclosed, leaving the entire IC and bilateral ureters completely out of the peritoneal cavity.
Statistical Analysis The statistical tests were performed using SPSS software, version 19.0 (SPSS Inc., Chicago, IL). Two-sided tests were used, and the significance level was set at P ¼ .05. The continuous parametric data
Junjie Zhao et al Table 1 Baseline Characteristics Characteristic Age (years) 2
BMI (kg/m )
LRC (n [ 41)
EORC (n [ 53)
P Value
65.5 10.1
66.2 9.7
.734
24.7 3.9
25.5 4.1
Gender Men Women
.341 .807
37
47
4
6
23 (56.1)
28 (52.8)
.753
2 (4.9)
5 (9.4)
.404
Ta-T1
17 (41.5)
17 (32.1)
T2-T4
24 (58.5)
36 (67.9)
Low grade
3 (7.3)
3 (5.7)
High grade
38 (92.7)
50 (94.3)
ASA score 2 Abdominal surgical history Clinical stage
.348
Tumor grade
.745
Data presented as mean standard deviation or n (%). Abbreviations: ASA ¼ American Society of Anesthesiologists; BMI ¼ body mass index; EORC ¼ extraperitoneal open radical cystectomy; LRC ¼ laparoscopic radical cystectomy.
were compared using the independent samples t test. The categorical data were compared using Pearson’s c2 test, and Fisher’s exact test was used when appropriate. The survival data were compared using Kaplan-Meier survival analysis and the log-rank test.
Results A total of 94 patients met the inclusion criteria (41 had undergone LRC and 53, EORC; Table 1). The patients in the LRC and EORC groups had comparable baseline characteristics with respect to age, gender, BMI, ASA class, surgical history, and pathologic status. The operative and postoperative characteristics are listed in Table 2. A significant difference was observed between the 2 groups in the operative time, EBL, and hospital stay. The LRC group required a significantly longer operative time (mean, 349 minutes vs. 316 minutes for the EORC group; P ¼ .022). The mean EBL was 278 mL for the LRC group and 356 mL for the EORC group (P ¼ .017). The hospital duration for the LRC group was much shorter than that for the EORC group (8.1 vs. 9.2 days, P ¼ .003). No significant differences in the other parameters, including blood transfusion, interval to flatus, interval to liquid intake, and opioid dosage, were noted. The variables regarding uniform surgical care in the 2 cohorts were not included in Table 2. Preoperatively, all 94
patients underwent the same bowel preparation and fasting technique. In brief, 2 days before surgery, all the patients began a semiliquid diet and metronidazole intake. A liquid diet was initiated 1 day before surgery. In addition, 12 hours before surgery, the patients underwent bowel preparation with 50% magnesium sulfate. During surgery, general anesthesia was administered to all patients (no epidural anesthesia or other anesthesia methods were used). Postoperatively, all the patients received intravenous patientcontrolled analgesia (PCA) for postoperative pain management. The opioid dosage using PCA was recorded and quantified as the amount of fentanyl administered per kilogram of body weight (using an equianalgesic conversion chart).13 No patient received gum-chewing therapy or participated in fast-track surgery programs. The postoperative complications are listed in Table 3. POI and wound healing morbidities were the most common early complications after surgery. The incidence of paralytic POI was 7.3% (3 of 41) and 7.5% (4 of 53) for those undergoing LRC and EORC, respectively (P ¼ .966). Of the patients with paralytic POI, total parenteral nutrition was provided until oral intake was resumed. All the patients received a warm saline enema to stimulate bowel motility and regained their normal intestinal function before the ninth postoperative day. The SBO rate was 4.9% (2 of 41) in the LRC group and 3.8% (2 of 53) in the EORC group (P ¼ .792). All
Table 2 Perioperative Results Variable Operative time (min) Estimated blood loss (mL) Blood transfusion Interval to flatus (d) Interval to liquid intake (d) Opioid dosage (mg) Hospital stay (d)
LRC (n [ 41) 349 62.6 278 133.1 2 (4.9) 3.2 1.3 4.0 1.8 9.9 0.5 8.1 1.6
EORC (n [ 53) 316 356 6 3.5 4.1 10.0 9.2
71.8 167.9 (11.3) 1.5 1.6 0.6 1.8
P Value .022 .017 .267 .311 .777 .392 .003
Data presented as mean standard deviation or n (%). Abbreviations: EORC ¼ extraperitoneal open radical cystectomy; LRC ¼ laparoscopic radical cystectomy.
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Laparoscopic Versus Extraperitoneal Radical Cystectomy Table 3 Postoperative Complications LRC (n [ 41)
EORC (n [ 53)
P Value
10 (24.4)
15 (28.3)
.670
Paralytic POI
3 (7.3)
4 (7.5)
.966
SBO
2 (4.9)
2 (3.8)
.792
Wound healing disorders
1 (2.4)
5 (9.4)
.169
Complication Total
Urine leakage
1 (2.4)
1 (1.9)
.854
Lymphorrhagia
1 (2.4)
2 (3.8)
.715
Subcutaneous emphysema
2 (4.9)
0 (0)
.104
Rapid ventricular arrhythmia
0 (0)
1 (1.9)
.377
Clavien classification Grade I
5 (12.2)
7 (13.2)
.884
Grade IIa
5 (12.2)
8 (15.1)
.686
0
0
NA
Grade III-V
Data presented as n (%). Abbreviations: EORC ¼ extraperitoneal open radical cystectomy; LRC ¼ laparoscopic radical cystectomy; NA ¼ not applicable; POI ¼ postoperative ileus; SBO ¼ small bowel obstruction. a Intraoperative blood transfusions were not included.
the patients with SBO responded to conservative care and medication; no surgical intervention was required. One patient in the LRC group experienced a wound healing disorder compared with 5 in the EORC group (P ¼ .169). One of the latter patients received antibiotics for a surgical site infection that had been confirmed by positive wound culture findings. Urine leakage and lymphorrhagia were diagnosed by an increased amount of pelvic fluid collection with or without a reduction in urine output, which was differentiated using creatinine measurements. All patients with urine leakage or lymphorrhagia were cured by simply prolonged placement of the pelvic drainage tubes. One patient with rapid ventricular arrhythmia in the EORC group required b-receptor antagonists for heart rate control on the fifth postoperative day. Two patients with local subcutaneous emphysema in the LRC group recovered spontaneously. Using the Clavien classification of surgical complications,14 no grade IIIa or higher severe morbidities were noted in
either cohort. No disparity was evident between the 2 cohorts regarding the incidence and severity of early morbidities after RC. The postoperative pathologic results in the LRC group were similar to those in the EORC group (Table 4). The positive surgical margin rate was 0% for both groups. No significant differences were observed in the lymph node count between the 2 groups. The median follow-up duration was 23.2 months (range, 3-62 months) and 32.9 months (range, 3-60 months) for the LRC and EORC groups, respectively. At the final follow-up visit, 38 and 46 patients were alive in the LRC and EORC groups, respectively. Cancerspecific death occurred in 2 of 3 and 5 of 7 patients in the LRC and EORC groups, respectively. Local recurrence developed in 1 LRC patient (2.4%) and 2 EORC patients (3.8%). Distant metastasis was observed in 4 LRC patients (9.8%) and 5 EORC patients (9.4%). The Kaplan-Meier survival curves (Figure 1) demonstrated the absence of significant differences between the
Table 4 Pathologic Outcomes Variable
LRC (n [ 41)
EORC (n [ 53)
Pathologic stage Ta-Tis
.807 5 (12.2)
6 (11.3)
T1
12 (29.2)
11 (20.7)
T2
18 (43.9)
24 (45.3)
T3
4 (9.8)
9 (17.0)
T4a
2 (4.9)
3 (5.7)
Grade
.745
Low grade
3 (7.3)
3 (5.7)
High grade
38 (92.7)
50 (94.3)
Positive lymph node involvement
4 (9.8)
6 (11.3)
.807
Lymph node number
12 3
13 3
.112
Positive surgical margins
0 (0)
0 (0)
Data presented as n (%) or mean standard deviation. Abbreviations: EORC ¼ extraperitoneal open radical cystectomy; LRC ¼ laparoscopic radical cystectomy; NA ¼ not applicable.
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P Value
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NA
Junjie Zhao et al Figure 1 Kaplan-Meier Curves for (A) Overall Survival, (B) Cancer-specific Survival, and (C) Cancer-Free Survival After Laparoscopic Radical Cystectomy (LRC) and Extraperitoneal Open Radical Cystectomy (EORC)
LRC and EORC groups in terms of the 3-year overall, cancerspecific, and cancer-free survival rates.
Discussion Laparoscopic surgery is widely accepted in the urologic field. Decades ago, laparoscopic adrenalectomy replaced open surgery and became the reference standard for the treatment of adrenal lesions.15 However, the development of laparoscopic techniques for RC has been rather slow. In addition to the steep learning curve,16 other key concerns have included occasional port site metastasis,17 debate regarding the oncologic outcomes,18 and difficulty in reducing the risk of postoperative complications, in particular, POI. Broadly, POI can be paralytic or obstructive, and the pathogenesis of paralytic POI remains equivocal. The possible mechanisms include inflammatory, neurogenic, pharmacologic, and hormonal responses.19
Laparoscopic surgery reduces bowel manipulation and tissue trauma, which also reduces the inflammatory and catabolic responses. Additionally, the smaller abdominal incisions and less postoperative pain after laparoscopic surgery could theoretically result in a lower paralytic POI rate. However, this technique has not worked in practice.20,21 Similarly, obstructive POI, known as SBO, occurs frequently in patients who have undergone RC, even in the current era of minimally invasive techniques. The etiology of SBO is multifactorial, including a variety of intrinsic and extrinsic factors. The most common cause of SBO is adhesions (accounting for 65% to 75% of all cases). Other causes include malignant tumors, hernias, Crohn’s disease, and volvulus.22 Importantly, SBO is the main cause of reoperation after EORC and LRC.23 Gupta et al24 performed 5 LRCs with intracorporeal IC diversion. One patient developed intestinal obstruction after surgery and required a
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Laparoscopic Versus Extraperitoneal Radical Cystectomy diverting ileostomy for 12 weeks. Numerous attempts have been made to reduce the incidence of gastrointestinal complications after RC, including gum chewing, medications targeting the peripheral m-opioid receptor, and fast track regimens.25-27 However, these efforts are a series of conservative measures and should serve as adjunctive therapies, because the surgery itself has a much greater affect on the occurrence and development of POI. Kulkarni et al12 first described extraperitoneal radical cystectomy using a retrograde technique in 1999. An antegrade study was reported in 2003.28 Theoretically, the extraperitoneal technique will inherently reduce the risk of POI developing. First, total retroperitonealization can localize the peritonitis arising from urine or intestinal leakage. Urinary extravasation and intestinal leakage, from either the anastomotic site or the stump suture, are not uncommon during the RC postoperative period. Some of these events will be asymptomatic. Evidence has suggested that these complications cannot be avoided using routine ureteral stenting strategies and modifications of the anastomotic technique.29 Thus, complete retroperitonealization is an effective method to minimize the undesirable outcome of urine or intestinal leakage. Second, although no such leakage complications exist, reconstruction of the peritoneal cavity can prevent the inflammatory reactions induced by the deperitonealized pelvic wall with the small bowel, which could cause adhesions and ensuing enteroparalysis or even mechanical obstruction. Finally, avoiding a de-peritonealized pelvic wall will also decrease the risk of a strangulated internal hernia developing after pelvic lymphadenectomy when the patient has tortuous, elongated external iliac arteries.30 Extraperitoneal radical cystectomy has achieved satisfactory results in clinical practice. Jentzmik et al9 documented a significantly lower paralytic POI rate in an extraperitoneal group compared with a transperitoneal group (4.1% vs. 21.2%) in a comparison study of ORC. Park et al10 also observed results favoring the extraperitoneal technique. In their study, no POI occurred in the EORC group; however, 26.7% of the patients in the transperitoneal ORC group developed POI (1 patient required reoperation for SBO management). However, whether extraperitoneal radical cystectomy accelerates bowel function recovery compared with minimally invasive surgery remains unclear. In the present study, POI was still the most common postoperative complication in either cohort. However, no significant disparities were observed between the 2 groups in regard to flatus and liquid intake. The incidence of SBO in the EORC group (3.8%) was reduced compared with that in the LRC group (4.9%). The rate of paralytic POI in the EORC group (7.5%) was very similar to that in the LRC group (7.2%), regardless of some factors that were disadvantageous, such as increased blood loss (356 mL vs. 278 mL, P ¼ .017) and increased incision healing morbidities (9.4% vs. 2.4%, P ¼ .169), which are frequently associated with prolonged bed duration. Compared with previous studies, the paralytic POI rate in the EORC group was also acceptable. Our POI rate was lower than that reported by Shabsigh et al1 (16.0%) for conventional ORC and even lower than the rate after LRC (10.5%) reported by Guillotreau et al.5 These results indicate that EORC efficaciously promotes intestinal motility restoration. No statistically significant differences were found in the pathologic results and intermediate-term oncologic outcomes between the LRC and EORC groups. Although neurovascular-sparing surgery
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and neobladder construction were not used in the present study, the functional advantage of the EORC technique is clear because of its ability to preserve a much longer urethral canal without sacrificing the oncologic outcomes. In practice, however, the extraperitoneal technique is not as popular as the traditional approach when open cystectomy is indicated. A number of surgeons believe that the idea of EORC is radical and unnecessary because the IC and ureteraleileal anastomosis can be covered during transperitoneal ORC by using the peritoneum that is adjacent to the large bowel to contain potential urine leaks. However, this reperitonealization technique will generally not be complete or watertight. Moreover, the side effects of a de-peritonealized pelvic wall are unavoidable. In addition, the possible risk of lymphorrhagia or lymphocele is an issue that occasionally precludes urologists from selecting EORC as a preferred approach. However, these risks will not necessarily be realized. In the study by Park et al,10 lymphoceles did not occur after EORC. In the present study, no lymphoceles developed, and the lymphorrhagia rate was low (3.8%, 2 of 53) and comparable to that in the LRC group (2.4%, 1 of 41). The patients who developed lymphorrhagia recovered quickly. In our experience, we concluded that the crux of lymphocele development is not the retroperitoneal approach itself but is dependent on the technique of lymph node dissection. For large-caliber lymph vessels, meticulous ligation, instead of monopolar coagulation, is more important for the prevention of lymphocele. In addition, maintaining an unobstructed drainage tube is another key factor. From our experience, we considered that in most (if not all) patients, the existence of a nonperitonealized pelvis in the LRC group adversely affected the functional recovery of the bowel, which likely counteracts the advantages of minimally invasive surgery. The EORC technique is generally rewarding, except for the increased blood loss and wound healing morbidities, for which laparoscopic surgery is superior. A combination of the 2 techniques would appear to be a better alternative. However, to our knowledge, the application of an extraperitoneal technique for LRC is still not available. However, because of the frequency of extraperitoneal laparoscopic radical prostatectomy (ELRP) and extraperitoneal robot-assisted radical prostatectomy (EP-RARP),31,32 we believe that extraperitoneal LRC (ELRC) will become a reality owing to the similar surgical approach and technique. ELRP and EP-RARP have become the standard treatment option for the management of localized and locally advanced prostate cancer. A recent meta-analysis indicated that EP-RARP yielded better results than transperitoneal RARP.31 Because of the high incidence of prostate cancer in Western countries, the extraperitoneal technique has been rapidly developed in LRP to achieve better results. However, from the findings of the present study, we believe that ELRC is a promising technique. The present study had limitations. First, ours was a retrospective study, with those inherent limitations. Next, only the opioid dosages after RC were recorded; the use of other types of narcotics, such as acetaminophen, nonsteroidal anti-inflammatory drugs, or selective inhibitors of cyclooxygenase-2, during the postoperative period were not reported. These drugs are effective analgesic options that might reduce POI by diminishing opioid consumption.33 Additionally, a single surgeon performed all the procedures, which eliminated surgeon-specific or experience-specific surgical technique
Junjie Zhao et al differences in both groups. However, this approach also limited our study to the proficiency of the individual surgeon’s techniques.
Conclusion To our knowledge, the present study is the first to compare the postoperative morbidity and oncologic outcomes between LRC and EORC, with a focus on POI. In our experience, EORC will result in a POI rate similar to that of LRC despite the factors that favor LRC. The reestablishment of the peritoneal cavity most likely plays a role in the recovery of intestinal function. Our results suggest that extraperitoneal LRC has the potential to improve the perioperative results. However, the actual effect of extraperitoneal LRC requires additional confirmation.
9. 10.
11. 12. 13. 14. 15. 16.
Clinical Practice Points Minimally invasive techniques are increasing in popularity;
however, POI still accounts for most early morbidity after RC, and the pathogenesis of POI remains obscure. In the present retrospective analysis, we report an initial comparison of LRC and EORC (performed by a single surgeon) in terms of the perioperative results and oncologic outcomes. Despite factors favoring LRC, EORC had a POI rate similar to that of LRC, and both techniques had satisfactory intermediateterm oncologic outcomes. The reestablishment of the peritoneal cavity is likely to play a role in the recovery of intestinal function. Our results suggest that extraperitoneal LRC has the potential to improve perioperative results.
17. 18. 19. 20. 21. 22. 23.
24.
Disclosure The authors have stated that they have no conflicts of interest.
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27. 28. 29.
30. 31. 32. 33.
muscle-invasive bladder cancer and reduction of the incidence of postoperative ileus. Surg Oncol 2008; 17:41-8. Jentzmik F, Schostak M, Stephan C, et al. Extraperitoneal radical cystectomy with extraperitonealization of the ileal neobladder: a comparison to the transperitoneal technique. World J Urol 2010; 28:457-63. Park DS, Gong IH, Choi DK, et al. A feasibility study of peritoneum preservation in radical cystectomy with extraperitonealization of orthotopic neobladder for invasive high-grade bladder cancer: a preliminary analysis. Int Urol Nephrol 2014; 46:1107-13. Matin SF, Gill IS. Laparoscopic radical cystectomy with urinary diversion: completely intracorporeal technique. J Endourol 2002; 16:335-41. Kulkarni JN, Gulla RI, Tongaonkar HB, et al. Radical cystoprostatectomy: an extraperitoneal retrograde approach. J Urol 1999; 161:545-8. Li JM. Pain management in the hospitalized patient. Med Clin North Am 2008; 92:371-85. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004; 240:205-13. Suzuki H. Laparoscopic adrenalectomy for adrenal carcinoma and metastases. Curr Opin Urol 2006; 16:47-53. Haber GP, Campbell SC, Colombo JR Jr, et al. Perioperative outcomes with laparoscopic radical cystectomy: “pure laparoscopic” and “open-assisted laparoscopic” approaches. Urology 2007; 70:910-5. El-Tabey NA, Shoma AM. Port site metastases after robot-assisted laparoscopic radical cystectomy. Urology 2005; 66:1110. Hautmann RE. The oncologic results of laparoscopic radical cystectomy are not (yet) equivalent to open cystectomy. Curr Opin Urol 2009; 19:522-6. Boeckxstaens GE, de Jonge WJ. Neuroimmune mechanisms in postoperative ileus. Gut 2009; 58:1300-11. Hemal AK, Kolla SB. Comparison of laparoscopic and open radical cystoprostatectomy for localized bladder cancer with 3-year oncological followup: a single surgeon experience. J Urol 2007; 178:2340-3. Akin Y, Celik O, Ates M, et al. Evaluation of open and laparoscopic radical cystoprostatectomy combined with orthotopic neobladder: a single-surgeon experience. Urol Int 2013; 90:348-53. Papadimitriou G, Marinis A, Papakonstantinou A. Primary midgut volvulus in adults: report of two cases and review of the literature. J Gastrointest Surg 2011; 15: 1889-92. Varkarakis IM, Chrisofos M, Antoniou N, et al. Evaluation of findings during re-exploration for obstructive ileus after radical cystectomy and ilealloop urinary diversion: insight into potential technical improvements. BJU Int 2007; 99:893-7. Gupta NP, Gill IS, Fergany A, et al. Laparoscopic radical cystectomy with intracorporeal ileal conduit diversion: five cases with a 2-year follow-up. BJU Int 2002; 90:391-6. Choi H, Kang SH, Yoon DK, et al. Chewing gum has a stimulatory effect on bowel motility in patients after open or robotic radical cystectomy for bladder cancer: a prospective randomized comparative study. Urology 2011; 77:884-90. Kauf TL, Svatek RS, Amiel G, et al. Alvimopan, a peripherally acting mu-opioid receptor antagonist, is associated with reduced costs after radical cystectomy: economic analysis of a phase 4 randomized, controlled trial. J Urol 2013; 191: 1721-7. Saar M, Ohlmann CH, Siemer S, et al. Fast-track rehabilitation after robot-assisted laparoscopic cystectomy accelerates postoperative recovery. BJU Int 2013; 112: E99-106. Serel TA, Sevin G, Perk H, et al. Antegrade extraperitoneal approach to radical cystectomy and ileal neobladder. Int J Urol 2003; 10:25-9. Chahal R, Sundaram SK, Iddenden R, et al. A study of the morbidity, mortality and long-term survival following radical cystectomy and radical radiotherapy in the treatment of invasive bladder cancer in Yorkshire. Eur Urol 2003; 43:246-57. Kim KM, Kim CH, Cho MK, et al. A strangulated internal hernia behind the external iliac artery after a laparoscopic pelvic lymphadenectomy. Surg Laparosc Endosc Percutan Tech 2008; 18:417-9. Lee JY, Diaz RR, Cho KS, et al. Meta-analysis of transperitoneal versus extraperitoneal robot-assisted radical prostatectomy for prostate cancer. J Laparoendosc Adv Surg Tech A 2013; 23:919-25. Verze P, Scuzzarella S, Martina GR, et al. Long-term oncological and functional results of extraperitoneal laparoscopic radical prostatectomy: one surgical team’s experience on 1,600 consecutive cases. World J Urol 2013; 31:529-34. Smith HS. Perioperative intravenous acetaminophen and NSAIDs. Pain Med 2011; 12:961-81.
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Laparoscopic Radical Cystectomy Versus Extraperitoneal Radical Cystectomy: Is the Extraperitoneal Technique Rewarding? Junjie Zhao,1,2 Shuxiong Zeng,1 Zhensheng Zhang,1 Tie Zhou,1 Bo Yang,1 Ruixiang Song,1 Yinghao Sun,1 Chuanliang Xu1 Abstract The surgical approach is an important factor in the development of postoperative ileus (POI) after radical cystectomy (RC); however, studies comparing extraperitoneal open radical cystectomy (EORC) and laparoscopic RC (LRC) are lacking. We retrospectively studied 41 LRCs and 53 EORCs performed by a single surgeon. In our experience, EORC had a POI rate similar to that of LRC, despite the presence of factors favoring LRC, and was associated with similar oncologic outcomes, indicating that extraperitoneal LRC could be a promising method for improving the perioperative results. Background: To study whether extraperitoneal radical cystectomy (EORC) accelerates the postoperative recovery of bowel function compared with laparoscopic radical cystectomy (LRC). Patients and Methods: All the patients with bladder cancer who underwent EORC or LRC with an ileal conduit by a single surgeon from January 2009 to June 2014 were investigated. The perioperative outcomes and follow-up data were analyzed, with a focus on postoperative ileus (POI). Results: A total of 41 LRCs and 53 EORCs met the inclusion criteria. LRC was associated with a significant reduction in the estimated blood loss (278 vs. 356 mL, P ¼ .017) and a shorter hospital stay (8.1 vs. 9.2 days, P ¼ .003). However, LRC was also associated with longer operative times (349 vs. 316 minutes, P ¼ .022). The incidence of paralytic POI was 7.3% (3 of 41) and 7.5% (4 of 53; P ¼ .966) and the obstructive POI rate was 4.9% (2 of 41) and 3.8% (2 of 53; P ¼ .792) for the LRC and EORC groups, respectively. No significant differences were noted in blood transfusion requirements, interval to flatus or liquid intake, or opioid dosage. No patient in either group had positive surgical margins, and no significant differences were observed in the lymph node count (P ¼ .112). At a median follow-up period of 28.7 months (range, 3-62 months), no significant differences were seen between the LRC and EORC groups in the 3-year overall, cancer-specific, or cancer-free survival rates. Conclusion: EORC resulted in a POI rate similar to that of LRC, despite factors favoring LRC. Our results suggest that extraperitoneal LRC could improve the perioperative outcomes. Clinical Genitourinary Cancer, Vol. 13, No. 4, e271-7 ª 2015 Elsevier Inc. All rights reserved. Keywords: Bladder cancer, Cystectomy, Ileus, Laparoscopy, Morbidity
Introduction J. Zhao and S. Zeng contributed equally to the present report. 1
Department of Urology, Changhai Hospital, Second Military Medical University, Shanghai, People’s Republic of China 2 Department of Urology, Yantai Yuhuangding Hospital, Shandong, People’s Republic of China Submitted: Oct 30, 2014; Revised: Jan 6, 2015; Accepted: Jan 16, 2015; Epub: Jan 21, 2015 Address for correspondence: Chuanliang Xu, MD, Department of Urology, Changhai Hospital, Second Military Medical University, 168 Changhai Road, Shanghai 200433, People’s Republic of China E-mail contact: [email protected]
1558-7673/$ - see frontmatter ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.clgc.2015.01.006
Radical cystectomy (RC) with urinary diversion remains the most aggressive surgical option in urology and has a high incidence of postoperative complications. During the early recovery period after RC, postoperative (paralytic and obstructive) ileus (POI) accounts for most postoperative complications, affecting approximately 23% of patients.1 Laparoscopic RC (LRC) and robotic-assisted RC (RARC) are characterized by reduced blood loss and postoperative pain and have emerged as minimally invasive modalities that lead to a significant improvement in intestinal function recovery. These techniques have been
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Laparoscopic Versus Extraperitoneal Radical Cystectomy increasingly used by urologists.2,3 Although minimally invasive surgery is becoming increasingly popular, POI remains the most common complication. Xylinas et al4 recently reported on 175 consecutive patients who had undergone RARC with extracorporeal urinary diversion. Of these 175 patients, 18 (10.3%) developed paralytic POI and 2 (1.1%) obstructive POI and required a second operation.4 POI is the most frequent complication occurring immediately after surgery. The paralytic POI rate after LRC has been 10.5%.5 The incidence of paralytic POI has been alarmingly high and comparable to the rate after laparoscopic colectomy (10.1%).6 Laparoscopic colectomy is considered to be the surgery most at risk of leading to the development of paralytic POI. This led us to hypothesize that other underlying causes of paralytic POI are involved after minimally invasive surgery (in addition to classic risk factors, such as increased blood loss and opioid use for postoperative pain control).7,8 Therefore, the pathogenesis of POI in the context of minimally invasive surgery should be investigated. Extraperitoneal open radical cystectomy (EORC), a modification of the conventional transperitoneal technique, results in a dramatically reduced POI risk compared with traditional open surgery.9,10 The distinguishing feature of EORC involves the total restoration of the peritoneum during the operation. LRC is different. The operative steps of LRC are basically duplicated from the transperitoneal open techniques. Thus, we have presumed that the absence of retroperitonealization during LRC is likely an important factor contributing to the development of POI. Hence, we conducted a novel retrospective study comparing EORC and LRC, both with ileal conduit (IC) diversion, to investigate whether EORC facilitates more robust postoperative intestinal function recovery than LRC. The procedures were performed by a single surgeon during a 5-year period.
Patients and Methods
demonstrating air fluid levels. In addition to POI, all other postoperative complications before discharge were recorded, including wound healing disorders (ie, any wound problems, including a sterile or an infectious fluid collection), wound dehiscence, and incisional hernias. The oncologic outcomes and survival data, including overall survival, cancer-specific survival, and cancer-free survival, were also evaluated.
Surgical Techniques LRC With Intraperitoneal IC. In the LRC cohort, bilateral pelvic lymphadenectomy and cystectomy were performed according to the technique of Matin and Gill.11 The lateral parietal peritoneum was incised above the external iliac artery and extended distally along the external iliac artery to the pubic bone. After standard pelvic lymph node dissection, a transverse incision of the peritoneum was created in the retrovesical pouch, and the bilateral vasa deferentia were divided. The Denonvilliers fascia was horizontally incised. The peritoneotomy was then extended anteriorly toward the umbilicus in an inverted-U shape, incorporating each medial umbilical ligament, and dividing the urachus high near the umbilicus. The lateral and posterior vascular pedicles of the bladder and prostate were controlled with sequential firings of a Harmonic scalpel (Johnson & Johnson, Cincinnati, OH) or LigaSure vessel sealing system (Valleylab, Tyco Healthcare Group, Boulder, CO). Hem-o-Lok clips (Weck Surgical Instruments, Teleflex Medical, Durham, NC) were occasionally used for large caliber arterioles. Both ureters were distally clipped and divided, and the left ureter was laparoscopically transferred to the right side through an incision created in the sigmoid mesentery after the bladder had been resected. The bowel work and ureteroileal anastomosis were performed extracorporeally through a 5- to 6-cm infraumbilical wound extended from the umbilical port incision. After the IC had been formed, the body of the conduit was free in the peritoneal cavity, and the wound was closed without restoring the peritoneal cavity.
Study Cohort From January 2009 to June 2014, all the patients with bladder cancer who underwent LRC or EORC with IC diversion were enrolled in the present study. We excluded those patients who had undergone robotic-assisted radical cystectomy. LRC and EORC was performed by a single surgeon (C.L.X.), who was proficient in both techniques. The clinical and follow-up data were retrospectively collected from our bladder cancer database. The clinical and pathologic parameters included age, gender, body mass index (BMI), American Society of Anesthesiologists (ASA) score, history of abdominal surgery, disease stage, tumor grade, type of bowel preparation, operative time (skin to skin), estimated blood loss (EBL), transfusion requirement, interval to flatus, interval to liquid intake, hospital stay, dosage of opioids for postoperative pain management, and other techniques used to stimulate a rapid return of bowel function (ie, chewing gum and fast-track surgery). Paralytic POI was defined as a period > 5 days before the return of normal bowel function.5 Normal bowel function was defined as the presence of bowel sounds, the passage of stool or flatus, and oral food tolerance for 24 hours. Paralytic POI was not diagnosed when small bowel obstruction (SBO) developed in patients presenting with abdominal pain, abdominal distension, and/or vomiting associated with an upright abdominal radiograph
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EORC With Extraperitoneal IC. In the EORC cohort, standard bilateral pelvic lymph node dissection and open RC were performed using a radical retrograde extraperitoneal approach through a 12- to 15-cm midline incision in the lower abdomen.12 The rectus abdominis muscles were split at the midline, and the underlying transversalis fascia was incised. A plane was created immediately superficial to the peritoneum, entering the space of Retzius inferiorly and the retroperitoneal space on either side with the help of a selfretaining retractor. Bilateral pelvic lymphadenectomy, mobilization of the bladder, suturing and division of the dorsal vein complex and division of the urethra were performed outside the peritoneal cavity, which was opened at the end of the extirpative portion. The bladder with a peritoneal flap covering the bladder dome and urachus was resected en bloc by cutting the urachus at the level of the umbilicus. Next, extracorporeal IC formation was initiated. After the procedure, the peritoneum was completely reclosed, leaving the entire IC and bilateral ureters completely out of the peritoneal cavity.
Statistical Analysis The statistical tests were performed using SPSS software, version 19.0 (SPSS Inc., Chicago, IL). Two-sided tests were used, and the significance level was set at P ¼ .05. The continuous parametric data
Junjie Zhao et al Table 1 Baseline Characteristics Characteristic Age (years) 2
BMI (kg/m )
LRC (n [ 41)
EORC (n [ 53)
P Value
65.5 10.1
66.2 9.7
.734
24.7 3.9
25.5 4.1
Gender Men Women
.341 .807
37
47
4
6
23 (56.1)
28 (52.8)
.753
2 (4.9)
5 (9.4)
.404
Ta-T1
17 (41.5)
17 (32.1)
T2-T4
24 (58.5)
36 (67.9)
Low grade
3 (7.3)
3 (5.7)
High grade
38 (92.7)
50 (94.3)
ASA score 2 Abdominal surgical history Clinical stage
.348
Tumor grade
.745
Data presented as mean standard deviation or n (%). Abbreviations: ASA ¼ American Society of Anesthesiologists; BMI ¼ body mass index; EORC ¼ extraperitoneal open radical cystectomy; LRC ¼ laparoscopic radical cystectomy.
were compared using the independent samples t test. The categorical data were compared using Pearson’s c2 test, and Fisher’s exact test was used when appropriate. The survival data were compared using Kaplan-Meier survival analysis and the log-rank test.
Results A total of 94 patients met the inclusion criteria (41 had undergone LRC and 53, EORC; Table 1). The patients in the LRC and EORC groups had comparable baseline characteristics with respect to age, gender, BMI, ASA class, surgical history, and pathologic status. The operative and postoperative characteristics are listed in Table 2. A significant difference was observed between the 2 groups in the operative time, EBL, and hospital stay. The LRC group required a significantly longer operative time (mean, 349 minutes vs. 316 minutes for the EORC group; P ¼ .022). The mean EBL was 278 mL for the LRC group and 356 mL for the EORC group (P ¼ .017). The hospital duration for the LRC group was much shorter than that for the EORC group (8.1 vs. 9.2 days, P ¼ .003). No significant differences in the other parameters, including blood transfusion, interval to flatus, interval to liquid intake, and opioid dosage, were noted. The variables regarding uniform surgical care in the 2 cohorts were not included in Table 2. Preoperatively, all 94
patients underwent the same bowel preparation and fasting technique. In brief, 2 days before surgery, all the patients began a semiliquid diet and metronidazole intake. A liquid diet was initiated 1 day before surgery. In addition, 12 hours before surgery, the patients underwent bowel preparation with 50% magnesium sulfate. During surgery, general anesthesia was administered to all patients (no epidural anesthesia or other anesthesia methods were used). Postoperatively, all the patients received intravenous patientcontrolled analgesia (PCA) for postoperative pain management. The opioid dosage using PCA was recorded and quantified as the amount of fentanyl administered per kilogram of body weight (using an equianalgesic conversion chart).13 No patient received gum-chewing therapy or participated in fast-track surgery programs. The postoperative complications are listed in Table 3. POI and wound healing morbidities were the most common early complications after surgery. The incidence of paralytic POI was 7.3% (3 of 41) and 7.5% (4 of 53) for those undergoing LRC and EORC, respectively (P ¼ .966). Of the patients with paralytic POI, total parenteral nutrition was provided until oral intake was resumed. All the patients received a warm saline enema to stimulate bowel motility and regained their normal intestinal function before the ninth postoperative day. The SBO rate was 4.9% (2 of 41) in the LRC group and 3.8% (2 of 53) in the EORC group (P ¼ .792). All
Table 2 Perioperative Results Variable Operative time (min) Estimated blood loss (mL) Blood transfusion Interval to flatus (d) Interval to liquid intake (d) Opioid dosage (mg) Hospital stay (d)
LRC (n [ 41) 349 62.6 278 133.1 2 (4.9) 3.2 1.3 4.0 1.8 9.9 0.5 8.1 1.6
EORC (n [ 53) 316 356 6 3.5 4.1 10.0 9.2
71.8 167.9 (11.3) 1.5 1.6 0.6 1.8
P Value .022 .017 .267 .311 .777 .392 .003
Data presented as mean standard deviation or n (%). Abbreviations: EORC ¼ extraperitoneal open radical cystectomy; LRC ¼ laparoscopic radical cystectomy.
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Laparoscopic Versus Extraperitoneal Radical Cystectomy Table 3 Postoperative Complications LRC (n [ 41)
EORC (n [ 53)
P Value
10 (24.4)
15 (28.3)
.670
Paralytic POI
3 (7.3)
4 (7.5)
.966
SBO
2 (4.9)
2 (3.8)
.792
Wound healing disorders
1 (2.4)
5 (9.4)
.169
Complication Total
Urine leakage
1 (2.4)
1 (1.9)
.854
Lymphorrhagia
1 (2.4)
2 (3.8)
.715
Subcutaneous emphysema
2 (4.9)
0 (0)
.104
Rapid ventricular arrhythmia
0 (0)
1 (1.9)
.377
Clavien classification Grade I
5 (12.2)
7 (13.2)
.884
Grade IIa
5 (12.2)
8 (15.1)
.686
0
0
NA
Grade III-V
Data presented as n (%). Abbreviations: EORC ¼ extraperitoneal open radical cystectomy; LRC ¼ laparoscopic radical cystectomy; NA ¼ not applicable; POI ¼ postoperative ileus; SBO ¼ small bowel obstruction. a Intraoperative blood transfusions were not included.
the patients with SBO responded to conservative care and medication; no surgical intervention was required. One patient in the LRC group experienced a wound healing disorder compared with 5 in the EORC group (P ¼ .169). One of the latter patients received antibiotics for a surgical site infection that had been confirmed by positive wound culture findings. Urine leakage and lymphorrhagia were diagnosed by an increased amount of pelvic fluid collection with or without a reduction in urine output, which was differentiated using creatinine measurements. All patients with urine leakage or lymphorrhagia were cured by simply prolonged placement of the pelvic drainage tubes. One patient with rapid ventricular arrhythmia in the EORC group required b-receptor antagonists for heart rate control on the fifth postoperative day. Two patients with local subcutaneous emphysema in the LRC group recovered spontaneously. Using the Clavien classification of surgical complications,14 no grade IIIa or higher severe morbidities were noted in
either cohort. No disparity was evident between the 2 cohorts regarding the incidence and severity of early morbidities after RC. The postoperative pathologic results in the LRC group were similar to those in the EORC group (Table 4). The positive surgical margin rate was 0% for both groups. No significant differences were observed in the lymph node count between the 2 groups. The median follow-up duration was 23.2 months (range, 3-62 months) and 32.9 months (range, 3-60 months) for the LRC and EORC groups, respectively. At the final follow-up visit, 38 and 46 patients were alive in the LRC and EORC groups, respectively. Cancerspecific death occurred in 2 of 3 and 5 of 7 patients in the LRC and EORC groups, respectively. Local recurrence developed in 1 LRC patient (2.4%) and 2 EORC patients (3.8%). Distant metastasis was observed in 4 LRC patients (9.8%) and 5 EORC patients (9.4%). The Kaplan-Meier survival curves (Figure 1) demonstrated the absence of significant differences between the
Table 4 Pathologic Outcomes Variable
LRC (n [ 41)
EORC (n [ 53)
Pathologic stage Ta-Tis
.807 5 (12.2)
6 (11.3)
T1
12 (29.2)
11 (20.7)
T2
18 (43.9)
24 (45.3)
T3
4 (9.8)
9 (17.0)
T4a
2 (4.9)
3 (5.7)
Grade
.745
Low grade
3 (7.3)
3 (5.7)
High grade
38 (92.7)
50 (94.3)
Positive lymph node involvement
4 (9.8)
6 (11.3)
.807
Lymph node number
12 3
13 3
.112
Positive surgical margins
0 (0)
0 (0)
Data presented as n (%) or mean standard deviation. Abbreviations: EORC ¼ extraperitoneal open radical cystectomy; LRC ¼ laparoscopic radical cystectomy; NA ¼ not applicable.
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P Value
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NA
Junjie Zhao et al Figure 1 Kaplan-Meier Curves for (A) Overall Survival, (B) Cancer-specific Survival, and (C) Cancer-Free Survival After Laparoscopic Radical Cystectomy (LRC) and Extraperitoneal Open Radical Cystectomy (EORC)
LRC and EORC groups in terms of the 3-year overall, cancerspecific, and cancer-free survival rates.
Discussion Laparoscopic surgery is widely accepted in the urologic field. Decades ago, laparoscopic adrenalectomy replaced open surgery and became the reference standard for the treatment of adrenal lesions.15 However, the development of laparoscopic techniques for RC has been rather slow. In addition to the steep learning curve,16 other key concerns have included occasional port site metastasis,17 debate regarding the oncologic outcomes,18 and difficulty in reducing the risk of postoperative complications, in particular, POI. Broadly, POI can be paralytic or obstructive, and the pathogenesis of paralytic POI remains equivocal. The possible mechanisms include inflammatory, neurogenic, pharmacologic, and hormonal responses.19
Laparoscopic surgery reduces bowel manipulation and tissue trauma, which also reduces the inflammatory and catabolic responses. Additionally, the smaller abdominal incisions and less postoperative pain after laparoscopic surgery could theoretically result in a lower paralytic POI rate. However, this technique has not worked in practice.20,21 Similarly, obstructive POI, known as SBO, occurs frequently in patients who have undergone RC, even in the current era of minimally invasive techniques. The etiology of SBO is multifactorial, including a variety of intrinsic and extrinsic factors. The most common cause of SBO is adhesions (accounting for 65% to 75% of all cases). Other causes include malignant tumors, hernias, Crohn’s disease, and volvulus.22 Importantly, SBO is the main cause of reoperation after EORC and LRC.23 Gupta et al24 performed 5 LRCs with intracorporeal IC diversion. One patient developed intestinal obstruction after surgery and required a
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Laparoscopic Versus Extraperitoneal Radical Cystectomy diverting ileostomy for 12 weeks. Numerous attempts have been made to reduce the incidence of gastrointestinal complications after RC, including gum chewing, medications targeting the peripheral m-opioid receptor, and fast track regimens.25-27 However, these efforts are a series of conservative measures and should serve as adjunctive therapies, because the surgery itself has a much greater affect on the occurrence and development of POI. Kulkarni et al12 first described extraperitoneal radical cystectomy using a retrograde technique in 1999. An antegrade study was reported in 2003.28 Theoretically, the extraperitoneal technique will inherently reduce the risk of POI developing. First, total retroperitonealization can localize the peritonitis arising from urine or intestinal leakage. Urinary extravasation and intestinal leakage, from either the anastomotic site or the stump suture, are not uncommon during the RC postoperative period. Some of these events will be asymptomatic. Evidence has suggested that these complications cannot be avoided using routine ureteral stenting strategies and modifications of the anastomotic technique.29 Thus, complete retroperitonealization is an effective method to minimize the undesirable outcome of urine or intestinal leakage. Second, although no such leakage complications exist, reconstruction of the peritoneal cavity can prevent the inflammatory reactions induced by the deperitonealized pelvic wall with the small bowel, which could cause adhesions and ensuing enteroparalysis or even mechanical obstruction. Finally, avoiding a de-peritonealized pelvic wall will also decrease the risk of a strangulated internal hernia developing after pelvic lymphadenectomy when the patient has tortuous, elongated external iliac arteries.30 Extraperitoneal radical cystectomy has achieved satisfactory results in clinical practice. Jentzmik et al9 documented a significantly lower paralytic POI rate in an extraperitoneal group compared with a transperitoneal group (4.1% vs. 21.2%) in a comparison study of ORC. Park et al10 also observed results favoring the extraperitoneal technique. In their study, no POI occurred in the EORC group; however, 26.7% of the patients in the transperitoneal ORC group developed POI (1 patient required reoperation for SBO management). However, whether extraperitoneal radical cystectomy accelerates bowel function recovery compared with minimally invasive surgery remains unclear. In the present study, POI was still the most common postoperative complication in either cohort. However, no significant disparities were observed between the 2 groups in regard to flatus and liquid intake. The incidence of SBO in the EORC group (3.8%) was reduced compared with that in the LRC group (4.9%). The rate of paralytic POI in the EORC group (7.5%) was very similar to that in the LRC group (7.2%), regardless of some factors that were disadvantageous, such as increased blood loss (356 mL vs. 278 mL, P ¼ .017) and increased incision healing morbidities (9.4% vs. 2.4%, P ¼ .169), which are frequently associated with prolonged bed duration. Compared with previous studies, the paralytic POI rate in the EORC group was also acceptable. Our POI rate was lower than that reported by Shabsigh et al1 (16.0%) for conventional ORC and even lower than the rate after LRC (10.5%) reported by Guillotreau et al.5 These results indicate that EORC efficaciously promotes intestinal motility restoration. No statistically significant differences were found in the pathologic results and intermediate-term oncologic outcomes between the LRC and EORC groups. Although neurovascular-sparing surgery
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and neobladder construction were not used in the present study, the functional advantage of the EORC technique is clear because of its ability to preserve a much longer urethral canal without sacrificing the oncologic outcomes. In practice, however, the extraperitoneal technique is not as popular as the traditional approach when open cystectomy is indicated. A number of surgeons believe that the idea of EORC is radical and unnecessary because the IC and ureteraleileal anastomosis can be covered during transperitoneal ORC by using the peritoneum that is adjacent to the large bowel to contain potential urine leaks. However, this reperitonealization technique will generally not be complete or watertight. Moreover, the side effects of a de-peritonealized pelvic wall are unavoidable. In addition, the possible risk of lymphorrhagia or lymphocele is an issue that occasionally precludes urologists from selecting EORC as a preferred approach. However, these risks will not necessarily be realized. In the study by Park et al,10 lymphoceles did not occur after EORC. In the present study, no lymphoceles developed, and the lymphorrhagia rate was low (3.8%, 2 of 53) and comparable to that in the LRC group (2.4%, 1 of 41). The patients who developed lymphorrhagia recovered quickly. In our experience, we concluded that the crux of lymphocele development is not the retroperitoneal approach itself but is dependent on the technique of lymph node dissection. For large-caliber lymph vessels, meticulous ligation, instead of monopolar coagulation, is more important for the prevention of lymphocele. In addition, maintaining an unobstructed drainage tube is another key factor. From our experience, we considered that in most (if not all) patients, the existence of a nonperitonealized pelvis in the LRC group adversely affected the functional recovery of the bowel, which likely counteracts the advantages of minimally invasive surgery. The EORC technique is generally rewarding, except for the increased blood loss and wound healing morbidities, for which laparoscopic surgery is superior. A combination of the 2 techniques would appear to be a better alternative. However, to our knowledge, the application of an extraperitoneal technique for LRC is still not available. However, because of the frequency of extraperitoneal laparoscopic radical prostatectomy (ELRP) and extraperitoneal robot-assisted radical prostatectomy (EP-RARP),31,32 we believe that extraperitoneal LRC (ELRC) will become a reality owing to the similar surgical approach and technique. ELRP and EP-RARP have become the standard treatment option for the management of localized and locally advanced prostate cancer. A recent meta-analysis indicated that EP-RARP yielded better results than transperitoneal RARP.31 Because of the high incidence of prostate cancer in Western countries, the extraperitoneal technique has been rapidly developed in LRP to achieve better results. However, from the findings of the present study, we believe that ELRC is a promising technique. The present study had limitations. First, ours was a retrospective study, with those inherent limitations. Next, only the opioid dosages after RC were recorded; the use of other types of narcotics, such as acetaminophen, nonsteroidal anti-inflammatory drugs, or selective inhibitors of cyclooxygenase-2, during the postoperative period were not reported. These drugs are effective analgesic options that might reduce POI by diminishing opioid consumption.33 Additionally, a single surgeon performed all the procedures, which eliminated surgeon-specific or experience-specific surgical technique
Junjie Zhao et al differences in both groups. However, this approach also limited our study to the proficiency of the individual surgeon’s techniques.
Conclusion To our knowledge, the present study is the first to compare the postoperative morbidity and oncologic outcomes between LRC and EORC, with a focus on POI. In our experience, EORC will result in a POI rate similar to that of LRC despite the factors that favor LRC. The reestablishment of the peritoneal cavity most likely plays a role in the recovery of intestinal function. Our results suggest that extraperitoneal LRC has the potential to improve the perioperative results. However, the actual effect of extraperitoneal LRC requires additional confirmation.
9. 10.
11. 12. 13. 14. 15. 16.
Clinical Practice Points Minimally invasive techniques are increasing in popularity;
however, POI still accounts for most early morbidity after RC, and the pathogenesis of POI remains obscure. In the present retrospective analysis, we report an initial comparison of LRC and EORC (performed by a single surgeon) in terms of the perioperative results and oncologic outcomes. Despite factors favoring LRC, EORC had a POI rate similar to that of LRC, and both techniques had satisfactory intermediateterm oncologic outcomes. The reestablishment of the peritoneal cavity is likely to play a role in the recovery of intestinal function. Our results suggest that extraperitoneal LRC has the potential to improve perioperative results.
17. 18. 19. 20. 21. 22. 23.
24.
Disclosure The authors have stated that they have no conflicts of interest.
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