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Minimally Invasive Approaches to Colon Cancer
Minimally Invasive Approaches to Colon Cancer Jennifer L. Paruch
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Todd D. Francone
L
aparoscopic colectomy was first described more than three decades ago, following the success of laparoscopic approaches to biliary surgery and appendicitis in the 1980s. Jacobs et al.1 described their first 20 laparoscopic colectomies for benign and malignant conditions. The paper was fairly modern, with operative times (170 minutes for sigmoid and 155 minutes for right colectomy) and lengths of stay (3 to 5 days for right, 3 to 8 days for sigmoid) comparable to more recent randomized trials. The authors concluded that the procedure “will become as accepted as laparoscopic cholecystectomy.” Although initial reports were promising, adoption of laparoscopic colectomy for cancer was met with early controversy. A report published by Johnstone et al. in 1996 documented 35 port site recurrences in patients undergoing laparoscopic colon cancer surgery.2 Other similar reports emerged, creating growing concerns over the safety of laparoscopic colectomy.3,4 As a result, a series of randomized trials were undertaken to compare outcomes between laparoscopic and open colectomy for cancer. These trials are described in detail later and represent one of the most comprehensive bodies of literature to evaluate the safety and efficacy of an emerging surgical technique. Despite the evidence supporting laparoscopic colectomy, widespread adoption has been slow. Moghadamyeghaneh et al.5 reviewed the National Inpatient Sample between 2009 and 2012 and found that 49% of elective colectomies for cancer were performed laparoscopically, with the rate of laparoscopy increasing over that time period. Other studies have reported similar numbers, with higher rates at academic centers, suggesting that there is still opportunity for increased utilization.6,7 Reasons for low adoption rates may include lack of specialized training, low surgeon or hospital volume, underreporting related to reliance on billing codes, or limitations of administrative data in capturing contraindications to laparoscopy. This chapter will review the trials comparing laparoscopic and open colectomy for cancer and discuss the key technical components of these procedures. It should be noted that laparoscopy is a technique and that it should be used when the surgeon has determined that an equivalent operation can be performed with regard to patient safety and oncologic outcome. Many of the trials included later excluded patients with locally advanced disease, perforation, or obstruction at the time of presentation.
SHORT-TERM OUTCOMES Many authors comparing laparoscopic to open colectomy for cancer published early papers focusing on short-term outcomes. All of these reported longer operative times for
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laparoscopic procedures (Table 170.1), with differences ranging from 30 to 84 minutes. The rate of conversion to open varies widely across studies, ranging from 3% to 25% (see Table 170.1). The CLASICC study reported the highest conversion rate (25%) but did note that the rate decreased over the course of the study, suggesting that this may be more reflective of the learning curve.10 One of the most universal advantages of laparoscopic colon resection across trials is a decreased length of stay (see Table 170.1). This difference ranges from a 1-day in the COST study9 to a 5-day difference reported by Liang et al.14 Interestingly, Basse et al.12 published a study comparing laparoscopic and open colectomy in the setting of a universal fast-track surgery protocol and showed a 2-day length of stay in both groups. This raises the question of whether some advantages of laparoscopy may be blunted as more centers adopt enhanced recovery protocols. The majority of studies did not find any significant differences in short-term morbidity or mortality between the laparoscopic and open groups (see Table 170.1). Lacy et al.8 and Braga et al.13 demonstrated lower overall rates of postoperative complications in the laparoscopic group. In both studies, this seemed to be driven primarily by lower rates of wound infection.
RETURN OF BOWEL FUNCTION Although there is heterogeneity across studies in the definition of return of bowel function (flatus, bowel movement, oral tolerance), there is a consistent earlier return of bowel function in the laparoscopic group (Table 170.2). This is hypothesized to be the result of gentler tissue handling, and to account for the consistent decrease in length in the laparoscopic group. Interestingly, the Basse et al.12 study, which compared laparoscopic and open colectomy with a fast-track protocol, found no difference in length of stay or time to return of bowel function between the groups. This further supports the hypothesis that the benefit of laparoscopy in decreasing length of stay may be related to shortened ileus.
POSTOPERATIVE PAIN Postoperative pain is measured differently across trials, likely because of the challenges with quantifying this outcome (Table 170.3). Most studies used some measure of narcotic use as a surrogate for pain and found a benefit in the laparoscopic group in either duration of narcotic use or percent of patients requiring narcotics. This difference may be more beneficial than was understood at the time of publication of these papers, as surgical fields come under increasing political pressure to decrease the prescription of opiates.17
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Minimally Invasive Approaches to Colon Cancer CHAPTER 170 2049.e1
KEYWORDS Colon cancer Mortality Morbidity Quality of life
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TABLE 170.1 Short-Term Outcomes After Colon Resection LOS (DAYS) Trial
Sample Size
Lap
Lacy et al., 20028 COST, 20049 CLASICC, 200510 COLOR, 200511 Basse et al., 200512 Braga et al., 200513 Liang et al., 200714 ALCCaS, 200815 Braga et al., 201016
219 872 794 1248 60 391 269 592 268
5.2 7.9* 5 6† No difference 8.2 9.3‡ No difference 9.4 12.7‡ 9 14† 7 8 7 8.7¶
Open
OPERATIVE TIME (MINUTES)
POSTOPERATIVE COMPLICATIONS
Lap
Lap
Open
12%
31%†
MORTALITY Lap
Open
No difference No difference No difference
Open
150 180 145 215
95† 135 115‡ 131§
224
184†
213
174†
No difference
LYMPH NODE HARVEST Conversion Rates
No difference No difference 17.9% 36.3%ǁ No difference No difference No difference
11% 21% 25% 17% 10% 4.2% 3% 14.6% 5.2%
Lap
Open
No difference No difference No difference
*P = .005 † P < .001 ‡ P < .0001 § P < .05 ǁ P = .0005 ¶ P = .002 lap, Laparoscopic; LOS, length of stay.
TABLE 170.2 Return of Bowel Function After Colon Resection DAYS TO BOWEL MOVEMENT
TIME TO FLATUS Trial 8
Lacy et al., 2002 COLOR, 200511 CLASICC, 200510 Basse et al., 200512 Liang et al., 200714 ALCCaS, 200815
Sample Size
Lap
Open
219 1248 794 60 269 592
36 h
55 h*
Lap
Open
3.6 4.6† 5 6 No difference 3 days
3 days‡
4
TIME TO PO TOLERANCE Lap
Open
54 h 2.9 days No difference
84 h* 3.8 days†
LENGTH OF ILEUS Lap
Open
48 h
96 h*
5§
*P = .001 † P < .0001 ‡ P = .27 § P < .011 PO, Per os; Lap, laparoscopic.
TABLE 170.3 Postoperative Pain Control After Colon Resection Trial
Sample Size
COST, 20049
872
COLOR, 200511
1248
Liang et al., 200714
269
Measurement
Outcome
Days of parenteral narcotics Days of oral analgesics Percent of patients using opiates POD#1-3
3 days laparoscopic vs. 4 days open (P < .001) 1 day lap vs. 2 days open (P = .02)
Visual analog scale (POD#1)
h, Hours; POD, postoperative day.
POD#1: No difference POD#2: 41% lap vs. 49% open (P = .008) POD#3: 26% lap vs. 37% open (P = .0003) 3.5 laparoscopic vs. 8.6 open (P < .001)
LONG-TERM OUTCOMES ONCOLOGIC OUTCOMES As mentioned earlier, one of the key motivating factors for these studies was to demonstrate equivalent oncologic outcomes between laparoscopic and open colectomy. Since their initial publication, several trials have continued to publish updates (out to 10 years) to provide a definitive answer to this question. Table 170.4 summarizes the results from these studies. In every case, groups found no significant difference in overall survival, disease-free survival, wound recurrence, or overall recurrence between laparoscopic and open colectomy. The only study showing any type of oncologic difference, reported by Lacy et al.,8 showed an advantage for laparoscopic colectomy group in cancer-related mortality. This collective body of data has demonstrated that laparoscopic colectomy is noninferior to open colectomy in appropriately selected cancer patients.
Minimally Invasive Approaches to Colon Cancer CHAPTER 170
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TABLE 170.4 Long-Term Outcomes After Colon Resection Trial
Follow-Up
COST, 20049 COST, 200718 CLASICC, 200719 CLASICC, 201020 CLASICC, 201021 CLASICC, 201322 COLOR, 200923 COLOR, 201124 Lacy et al., 200825
3 years 5 years 3 years 5 years 3 years 10 years 5 years 5 years Median 95 months 5 years 5 years
Braga et al, 201016 LAFA, 201426 Liang et al., 200714 ALCCaS, 201215
Overall Survival No No No No
Disease-Free Survival
Wound Recurrence
Recurrence
Incisional Hernia
Small Bowel Obstruction
No difference
No difference
difference No difference No difference difference No difference No difference difference No difference No difference No difference difference No difference No difference
No difference No difference No difference No difference
No difference No difference
No difference
No difference
No difference
No difference No difference No difference No difference No difference No difference No difference 10% lap, 17% 2.4% lap, 7.3% open (P = .022) open (P = .039) Median 40 No difference No difference months 5 years No difference No difference No difference
Lap, Laparoscopic.
INCISIONAL HERNIA AND ADHESIVE BOWEL OBSTRUCTION In addition to survival, many long-term studies included data on rates of incisional hernia and adhesive small bowel obstruction. Although one may hypothesize that smaller incisions and decreased tissue handling associated with laparoscopic surgery would decrease the risk of these complications, that has not been clearly supported by the literature (see Table 170.4). The majority of groups found no difference, with the exception being the LAFA study, which showed decreases in both outcomes in the laparoscopic group.26 It may be possible that longer-term follow-up is needed to detect differences between the groups.
QUALITY OF LIFE Quality of life (QoL) is a challenging outcome to compare between procedures. There are numerous instruments available, and their use varies widely across studies. Many trials hypothesized that QoL would be improved in the laparoscopic group and invested considerable resources into collecting these data. Overall, most found at least some short-term QoL benefit in the laparoscopic group. The COST group published two papers focusing on QoL.27,28 They used a Symptom Distress Scale (SDS), QoL index, and single-item global scale. They found slightly better global QoL rating at 2 weeks in the laparoscopic group; however, no other comparisons out to 2 months reached significance. At 18 months, they found a modest benefit in the laparoscopic group for global QoL, but no differences for activity, daily living, health, or support. Other groups have studied differences in QoL, with mixed results.10,26,19,29 Braga et al.13 looked at QoL at 12, 24, and 36 months using the Short Form-36. They found significantly better general health and physical and social
functioning in the laparoscopic group at 12 months. However, this difference disappeared at 48 months. Taken together, the literature suggests that certain QoL domains are improved in laparoscopic compared with open colectomy and that these differences are probably the most significant in the first 6 to 12 months after surgery.
COST The cost of the operation itself is higher for laparoscopic colectomy than for open colectomy. Liang et al.14 reported significantly higher overall costs for laparoscopic compared with open colectomy ($194,442 vs. $136,420; P < .001). These differences were largely driven by increased equipment and disposable instrument costs. The COLOR group reported higher cost of operation (€1171; P < .001), higher cost of admission (€1556; P = .015), and higher cost to the healthcare system (€2244; P = .018) for laparoscopic colectomy. However, when they took into account total cost to society (time off of work), they found no difference between laparoscopic and open colectomy at 12 months.30
ADDITIONAL CONSIDERATIONS ROBOTICS Early studies on robotic colectomy were published in 2002.31,32 The three-dimensional view, improved articulation, and multiinstrument platform provide an advantage for many surgical specialties performing complex minimally invasive procedures. Although robotics is gaining more attention for proctectomy,33–36 studies have been published comparing robotic with laparoscopic colectomy. Park et al.37 randomized 70 patients to robotic versus laparoscopic right colectomy for cancer. They demonstrated equivalent length of stay, pain scores, complications, margins, and lymphadenectomy for both groups. The robotic group
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had longer operative times (195 vs. 130 minutes; P < .001) and increased operative costs ($12,235 vs. $10,320; P = .013). The increased cost of robotics and who should be responsible for this (patient, hospital, surgeon) remain a limitation for robotic colectomy.
SINGLE INCISION Single-incision laparoscopic colectomy (SILC) increases the complexity of laparoscopic colectomy, with the goal of limiting the incision size to only that needed for specimen extraction. Early case reports established its feasibility as an approach for both cancer and inflammatory bowel disease.38–40 More recently, two randomized trials have been published comparing SILC with standard laparoscopic colectomy.41,42 Results from these trials have demonstrated similar operating times, complication rates, and lymph node harvests, along with a decreased length of stay by 1 day in one of the studies. This remains a promising and challenging technique, with similar outcomes to standard laparoscopy for appropriately selected patients.
COMPLETE MESOCOLIC EXCISION Complete mesocolic excision (CME) with central vascular ligation is hypothesized to provide an oncologic benefit. This is based on the premise that metastases as determined by the primary tumor with cancer progression occurs in a stepwise pattern. CME therefore improves outcomes by removing the mesocolon in one package with high ligation of the feeding vessels.43,44 Data suggest improved short- and long-term oncologic outcomes.45,46 Improved outcomes are thought to be related to strict adherence to oncologic principles including dissection through the proper plane, central vascular ligation, and length of proximal and distal margins. CME has been shown to achieve an en bloc removal of the disease lesion with increased amounts of colonic mesentery. It is a technically challenging operation due to high ligation of the vascular pedicles with dissection along the aorta and mobilization of the splenic flexure. Numerous recent publications have demonstrated the feasibility of laparoscopic CME with short-term outcomes similar to those of open surgery.47,48 Operative times are typically longer with the laparoscopy, with majority of studies demonstrating equivalent morbidity and mortality when compared with open CME groups. The conversion to an open CME ranges between 2% and 10%.
TECHNIQUE AND PEARLS OF WISDOM Minimally invasive surgery, both laparoscopic and robotic, have become increasingly used both for benign and malignant disease processes. Based on the underlying disease and sequelae of such processes, it is essential to be familiar with various approaches (i.e., medial to lateral, lateral to medial, superior to inferior, etc.) resulting in optimal exposure, as well as safer, quicker, and a more reproducible dissection. This is without a doubt facilitated by a fundamental understanding of the surgical anatomy, allowing the surgeon the ability to proceed in a safe manner, perform an appropriate oncologic resection, and allow for additional diagnostic and therapeutic maneuvering.
LAPAROSCOPIC RIGHT COLECTOMY FOR COLON CANCER With either laparoscopic or robotic techniques, the patient is in the supine position. If the location of the tumor is unclear based on prior review of diagnostic imaging, the patient should be placed in the modified lithotomy or split-leg position to facilitate an intraoperative endoscopic evaluation. The preferred laparoscopic and robotic port placements are demonstrated in Fig. 170.1. The patient is placed in a Trendelenburg position with the operating table inclined toward the left. Once pneumoperitoneum is established, a thorough evaluation of the abdomen is critical to understand the anatomy, evaluate for disseminated disease, and assess the feasibility of an R0 resection. The omentum is retracted superiorly over the transverse colon and liver, and the small bowel is mobilized out of the pelvis. Grasping either the cecum or mesentery close to the cecum anteriorly or ventrally will highlight the ileocolic artery branching off the superior mesenteric artery. A tenting or bowstringing effect will be noted, with the mesenteric vasculature acting as the scaffold (Fig. 170.2). The medial-lateral approach is our preferred approach, with early ligation of the ileocolic pedicle. This is generally first performed by creating an opening in the peritoneum parallel to the vessels and then encircling the vessels superiorly. Some mobilization of the mesocolon from the retroperitoneal structures may be necessary and can be performed with gentle blunt sweeping motions dorsally. When doing so, care must be taken both to visualize the right ureter as well as the duodenum. Once these structures are well visualized and out of harm’s way, a high ligation of the vessel can be performed. The medial-to-lateral dissection can then be continued with retroperitoneal attachments safely dissected away from the right colon and its mesentery, either sharply or with gentle brush movements. Care must be taken to stay in the appropriate plane and not injure the duodenum or more laterally, not mobilize the kidney (Fig. 170.3). For hepatic flexure and proximal transverse colon tumors, further distal dissection of the mesentery is performed to the level of the middle colic vessels. The middle colic vessel is the primary blood supply to the proximal two-thirds of the transverse colon. Care must be taken to use precise technique in this retroperitoneal space because the pancreaticoduodenal and gastroepiploic veins may cause significant hemorrhage if excess tension or shearing occurs. After the middle colic vessel is identified, the right branch of the middle colic vessel is then divided after isolation. At this point the right colon will now be held in place only by lateral avascular attachments to the abdominal sidewall, hepatic flexure, and gastrocolic attachments, including the omentum to the transverse colon. These can generally be easily divided by dissecting energy devices. Dissection is carried out proximally, dividing the hepatic flexure attachments and then distally toward the pelvis. The gastrocolic attachments to the transverse colon need to be divided oftentimes with entry into the lesser sac. For right colectomies, the distal extent of dissection is generally around the falciform ligament or in line with
Minimally Invasive Approaches to Colon Cancer CHAPTER 170
A
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B
FIGURE 170.1 (A) Four-port technique for laparoscopic right colectomy. Extraction site is through the midline or surgeon preference. (B) Four-arm technique for robotic right colectomy using the DaVinci Xi. Extraction site is through the midline or surgeon preference.
“Bowstring” Duodenum Duodenum Ileocolic pedicle
Retroperitoneum
FIGURE 170.2 Grasping the cecum or its mesentery and lifting anterolateral to the abdominal wall will create a tenting or “bowstring” effect with a distinct crease coursing parallel to the vessel.
FIGURE 170.3 Medial-to-lateral mobilization highlighting duodenum and white line of Toldt.
the middle colic vessels. It is sometimes best to start at this point and work retrograde toward the hepatic flexure. Hepatic flexure and proximal transverse colon tumors can be quite challenging due to the surrounding anatomy including the duodenum, pancreas, gallbladder, and kidney (Fig. 170.4). Potential involvement of these structures should instigate a cascade of diagnostic and endoscopic evaluations with involvement of the appropriate surgical teams, whether approaching it minimally invasive or open.
In the presence of a hepatic flexure or proximal colon tumor, the omentum may be involved and should remain attached to the colon to ensure an en bloc resection. Entry into the lesser sac can often be helpful in the event there is potential involvement of retroperitoneal structures. The lesser sac is entered, and the proximal transverse mesocolon can then be sharply dissected from the other abdominal and retroperitoneal structures (Fig. 170.5), including the duodenum and pancreas. Another point
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Left branch of MCA
Right branch of MCA
MCA
FIGURE 170.6 The classic “Y” pattern of the middle colic vessels is not always straightforward. Often both the right and left branch course to the patient’s right. The right branch courses off the head of the pancreas and the duodenum; the left branch makes a sharp upward turn and then veers to the left, as shown here. MCA, Middle colic artery.
FIGURE 170.4 Hepatic flexure tumor (arrows) involving the right kidney and duodenum.
Omentum
sometimes in a high fashion (Fig. 170.6). Rather than isolating the right branch of the middle colic vessel, the entire middle colic vessel may be divided. This can be challenging due to the truncated length of the middle colic vessels. It may be isolated by gently retracting the mesentery of the transverse colon superiorly. The middle colic artery and its right and left branches will be identified. A window can be created around the middle colic vessels and divided in a retrograde left-to-right fashion.
LAPAROSCOPIC LEFT COLECTOMY/SIGMOID RESECTION FOR COLON CANCER
Stomach
Transverse colon
FIGURE 170.5 Accessing the lesser sac through the omentum (gastrocolic ligament); early entry into the lesser sac is key to facilitating mobilization of the transverse colon.
of entry into the lesser sac will be the fusion or attachment of the gallbladder dome to the transverse colon or mesocolon. Once completely dissected, the right colon and mesentery should be able to be mobilized and expressed as a midline structure. Division of the intestines and subsequent anastomosis can now be performed either intracorporeally via laparoscopy or in an open fashion once extracorporealized through an extraction incision.
TRANSVERSE COLECTOMY AND THE MIDDLE COLIC VESSELS In cases requiring resection of the transverse colon, the middle colic vessel will need to be ligated and divided,
Left colectomy refers to resection of the descending and/ or splenic flexure with anastomosis of the distal transverse colon to the sigmoid colon, whereas sigmoid resection refers to removal of the sigmoid colon with restoration of intestinal continuity between the descending colon and the rectum. As mentioned previously, there are potentially no absolute contradictions to proceeding with an oncologic resection minimally invasive; however, those patients with a suspected T4 tumor should have the appropriate multidisciplinary surgical teams involved in the event a more extensive resection is required for an R0 oncologic resection. In particular, sigmoid colon cancers may involve the ureter or bladder, and as such a urologist should be involved for possible partial cystectomy or ureteral reimplantation. If the resection is considered extensive, the surgeon should have a low threshold for conversion to an alternative approach, such as an open procedure, to optimize exposure and facilitate the dissection. All patients are placed in modified lithotomy (legs in slight hip flexion) or split-leg position with both arms tucked at the sides. Positioning in this manner affords the surgeons numerous advantages including exposure to the anus/rectum for intraoperative colonoscopy if needed. This can be particularly useful for a tumor that may not have been preoperatively tattooed and localized. The
Minimally Invasive Approaches to Colon Cancer CHAPTER 170
1
2
2
3(C)
A
A
4
A
B
3(C)
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1
4
C
FIGURE 170.7 (A) Four-port technique for laparoscopic left colectomy. Extraction site is through the midline or Pfannenstiel incision. (B) Standard proposed port placement for a robotic sigmoidectomy using the DaVinci Xi. Notice the camera port is slightly off midline. This allows dissection of the splenic flexure and upper pelvis. (C) Our preferred port placement for a robotic sigmoid resection or low anterior resection using the DaVinci Xi. The “hockey stick” formation allows access to the splenic flexure as well as the pelvis with no need to redock the arms.
preferred laparoscopic port placement is demonstrated in Fig. 170.7A. When performing a left colectomy or sigmoid resection, it is customary to divide the bowel (and potentially the major vascular structures) with an endomechanical linear stapling device of various staple heights. For this reason, a 12-mm port is used in the right lower quadrant (RLQ). When performing a robotic approach, ports are spaced evenly in a straight line from the anterior superior iliac spine in the RLQ to the mid-clavicle in the left upper quadrant (LUQ) (see Fig. 170.7B and C). Prior to any mobilization or resection, inspect the abdominal and pelvic cavity to evaluate for any altered anatomy (phlegmon or occult metastatic processes) not previously appreciated or identified on preoperative imaging. In oncologic procedures, the liver is carefully inspected on both anterior and posterior surfaces, and the peritoneum, omentum, and mesentery are examined for metastatic studding. If the latter is identified, biopsy and surgical judgment will dictate how next to proceed—and whether any further resection is necessary or prudent. During diagnostic laparoscopy the surgeon often identifies the pathology. In the setting of a colonic neoplasm, the pathology’s location should often be marked with an endoscopic tattoo. Ideally, the location is marked in three to four quadrants such that the tattoo is clearly visible on the antimesenteric surface. Marking the lesion in only one quadrant may pose some difficulty in identification if the tattoo lies on the mesenteric border or in a difficult location such as the splenic or hepatic flexures. In this event, an intraoperative CO2 endoscopy may be performed. CO2 insufflation allows for quick resolution of bowel distention and continued laparoscopy during or following the endoscopic evaluation. Once the pathology has been localized, adjustments to the preoperative surgical plan may be required. In the setting of malignancy, the location of the tumor
will determine resection margins and vessel ligation. For cancers in the left colon, oncologic margins should be 5 cm proximal and distal to the tumor. A high ligation of the inferior mesenteric artery (IMA) pedicle is often performed to ensure adequate mobilization and appropriate lymph node harvesting. Pathology located in the proximal sigmoid colon or distal descending colon may necessitate mobilization of the splenic flexure for appropriate tension-free anastomosis. For lesions in the proximal descending colon, a high ligation of the inferior mesenteric vein (IMV) may also be necessary to allow mobilization and approximation of the proximal colon to the upper rectum to create an intestinal anastomosis without tension. Similar to a right colectomy, the initial dissection involves the development of the avascular plane between the parietal peritoneum overlying the retroperitoneum and the visceral peritoneum encompassing the mesentery of the left colon. There are multiple approaches to achieve this task including medial to lateral and lateral to medial. We prefer a medial-to-lateral approach for a left colectomy. The initial step for this approach requires initial identification of the IMA pedicle. The mesenteric fold containing the IMA can be found overlying and cephalad to the sacral promontory. Ventral retraction of the sigmoid and left colon mesentery will assist in outlining the IMA pedicle entering into the pelvis to form the superior rectal artery, in a similar bowstring effect noted with the ileocolic pedicle (Fig. 170.8). In the event that division of these adhesions does not allow for a clear “bowstring” of the IMA pedicle, then an alternative approach, such as a lateral to medial, should be considered to avoid injury to underlying structures such as the ureter, hypogastric nerves, and iliac vessels (Fig. 170.9). After the key retroperitoneal structures have been identified, the IMA may be divided to facilitate the pelvic
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IMV
IMA
Ligament of Trietz SP White line of Toldt Right common Iliac artery
FIGURE 170.8 The outline of the inferior mesenteric artery (IMA) can be visualized by gentle ventral retraction of the pedicle as it courses over the sacral promontory (SP). The space between the IMA and the SP has been termed the critical angle and marks the avascular plane between the retroperitoneum and the colon mesentery.
Left gonadal vessels
Ureter SP
FIGURE 170.9 Care is taken to identify and avoid the left ureter, left gonadal vessels, and the hypogastric nerve plexus. SP, Sacral promontory.
dissection. The medial-to-lateral mobilization is performed similar to that done on the right side. The dissection proceeds cephalad to the level of the superior pole of the kidney and may continue to the inferior aspect of the spleen. After medial-to-lateral mobilization is completed, the remaining avascular lateral attachments of the colon to the omentum, spleen, and abdominal and retroperitoneal sidewalls should be divided. Remember, when performing a resection of a tumor in the transverse colon, the omentum should be left on the colon and resected with the specimen to ensure adequate margins and an R0 resection. In the presence of a descending colon or distal transverse colon mass, splenic flexure mobilization will be required. Splenic flexure mobilization is generally performed using a combination of approaches. The patient is placed in a reverse Trendelenburg position with the table inclined toward the right. Typically, if an adequate medial-to-lateral mobilization is performed of the left colon and IMV, then mobilization of the splenic flexure is reduced to division of the lateral attachments of the phrenocolic ligaments
FIGURE 170.10 Continued medial-to-lateral mobilization between the inferior mesenteric artery (IMA) and inferior mesenteric vein (IMV) will facilitate mobilization of the splenic flexure.
(Fig. 170.10). Laterally, the attachments to the abdominal sidewall and spleen are carefully divided while being mindful not to injure the splenic capsule. A critical step in left colectomy is identification of a distal transection point. Distal transection localization is dependent upon both anatomic and physiologic entities. Appropriate mesenteric vascular supply must be accounted for, as well as distal resection margins in the setting of malignancy. For a sigmoid or distal left colectomy, division is generally performed at the level of the proximal rectum, past the splaying of the taenia coli on the antimesenteric surface. Further dissection and transection may be required to get appropriate distal margins. In general, at least a 5-cm distal margin is required for colonic malignancies. After the point of transection is selected, the mesentery is divided. Division of the upper rectum is generally performed with an endomechanical stapling device through the RLQ port. The colon is then extracted. Options for an extraction site include extension of the periumbilical incision, creation of a Pfannenstiel incision, or extension of the RLQ incision. After the abdominal wall is opened appropriately and the peritoneal cavity entered, a wound protector is inserted to protect the skin and soft tissue from contamination during externalization and creation of anastomosis. Through the wound protector, the distal stapled end of the colon and the proximal mobilized colon and mesentery are extracorporealized. The proximal dissection point is predicated upon a number of issues. In the setting of malignancy, at least a 5-cm margin is required. In all cases, appropriate maintenance of vascular supply must be ensured to minimize risk of ischemia of the anastomosis. Double-stapled end-end or end-side technique are often used during a left or sigmoid colectomy. It is recommended by the American Society of Colon and Rectal Surgeons that all left-sided anastomoses be tested for leakage. Once confident the anastomosis is secure and viable, the extraction sites and all port sites 10 mm or greater in size are closed.
COMPLETE MESOCOLIC EXCISION When performing a CME for right colon tumor located in the cecum approximately, the right branches of the middle
Minimally Invasive Approaches to Colon Cancer CHAPTER 170
colic artery and vein are ligated in addition to the ileocolic vessels. It is imperative to ligate the vessels just as they take off the superior mesenteric artery (SMA). For lesions located in the hepatic flexure and proximal transverse colons, an extended right colectomy is performed with the middle colic artery and vein ligated.49 Omentectomy is performed just below the gastroepiploic vessels and unless infiltrated by the tumor, the right gastroepiploic vessels are preserved. When performing a CME for a left colon tumor located in the proximal descending colon, the IMA is preserved and the left colic artery and superior rectal artery are ligated at their origin. For mid-descending and sigmoid colon cancers, the root of the IMA is ligated and the IMV is ligated just below the lower border of the pancreas.50
CONCLUSION Ongoing evidence supports the feasibility and safety of a minimally invasive surgery approach for colon cancer. To date, laparoscopy remains the most widely used minimally invasive technique with robotic surgery gaining momentum despite unsubstantiated evidence for cost-effectiveness in the treatment of both colon cancer and rectal cancer. It cannot be overstated that minimally invasive surgery is a technique or a “tool” that a surgeon may use to successfully remove pathology. It should be used when the surgeon has determined that an equivalent operation can be performed with regard to patient safety and oncologic outcome when compared with an open approach.
REFERENCES 1. Jacobs M, Verdeja JC, Goldstein HS. Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc. 1991;1(3):144-150. 2. Johnstone PA, Rohde DC, Swartz SE, Fetter JE, Wexner SD. Port site recurrences after laparoscopic and thoracoscopic procedures in malignancy. J Clin Oncol. 1996;14(6):1950-1956. 3. Berends FJ, Kazemier G, Bonjer HJ, Lange JF. Subcutaneous metastases after laparoscopic colectomy. Lancet. 1994;344(8914): 58. 4. Reilly WT, Nelson H, Schroeder G, Wieand HS, Bolton J, O’Connell MJ. Wound recurrence following conventional treatment of colorectal cancer. A rare but perhaps underestimated problem. Dis Colon Rectum. 1996;39(2):200-207. 5. Moghadamyeghaneh Z, Carmichael JC, Mills S, Pigazzi A, Nguyen NT, Stamos MJ. Variations in laparoscopic colectomy utilization in the United States. Dis Colon Rectum. 2015;58(10):950-956. 6. Yeo HL, Isaacs AJ, Abelson JS, Milsom JW, Sedrakyan A. Comparison of open, laparoscopic, and robotic colectomies using a large national database: outcomes and trends related to surgery center volume. Dis Colon Rectum. 2016;59(6):535-542. 7. Bardakcioglu O, Khan A, Aldridge C, Chen J. Growth of laparoscopic colectomy in the United States: analysis of regional and socioeconomic factors over time. Ann Surg. 2013;258(2):270-274. 8. Lacy AM, García-Valdecasas JC, Delgado S, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet. 2002;359(9325):2224-2229. 9. Nelson H, Sargent DJ, Wieand HS, et al. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004;350(20):2050-2059. 10. Guillou PJ, Quirke P, Thorpe H, et al. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005;365(9472):1718-1726. 11. Veldkamp R, Kuhry E, Hop WC, et al. Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol. 2005;6(7):477-484.
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12. Basse L, Jakobsen DH, Bardram L, et al. Functional recovery after open versus laparoscopic colonic resection: a randomized, blinded study. Ann Surg. 2005;241(3):416-423. 13. Braga M, Frasson M, Vignali A, Zuliani W, Civelli V, Di Carlo V. Laparoscopic vs. open colectomy in cancer patients: long-term complications, quality of life, and survival. Dis Colon Rectum. 2005;48(12):2217-2223. 14. Liang JT, Huang KC, Lai HS, Lee PH, Jeng YM. Oncologic results of laparoscopic versus conventional open surgery for stage II or III left-sided colon cancers: a randomized controlled trial. Ann Surg Oncol. 2007;14(1):109-117. 15. Hewett PJ, Allardyce RA, Bagshaw PF, et al. Short-term outcomes of the Australasian randomized clinical study comparing laparoscopic and conventional open surgical treatments for colon cancer: the ALCCaS trial. Ann Surg. 2008;248(5):728-738. 16. Braga M, Frasson M, Zuliani W, Vignali A, Pecorelli N, Di Carlo V. Randomized clinical trial of laparoscopic versus open left colonic resection. Br J Surg. 2010;97(8):1180-1186. 17. Waljee JF, Li L, Brummett CM, Englesbe MJ. Iatrogenic opioid dependence in the United States: are surgeons the gatekeepers? Ann Surg. 2017;265(4):728-730. 18. Fleshman J, Sargent DJ, Green E, et al. Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group trial. Ann Surg. 2007;246(4):655-662, discussion 662–654. 19. Jayne DG, Guillou PJ, Thorpe H, et al. Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol. 2007;25(21):3061-3068. 20. Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM, Guillou PJ. Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg. 2010;97(11):1638-1645. 21. Taylor GW, Jayne DG, Brown SR, et al. Adhesions and incisional hernias following laparoscopic versus open surgery for colorectal cancer in the CLASICC trial. Br J Surg. 2010;97(1):70-78. 22. Green BL, Marshall HC, Collinson F, et al. Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg. 2013;100(1):75-82. 23. Buunen M, Veldkamp R, Hop WC, et al. Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol. 2009;10(1):44-52. 24. Schölin J, Buunen M, Hop W, et al. Bowel obstruction after laparoscopic and open colon resection for cancer: results of 5 years of follow-up in a randomized trial. Surg Endosc. 2011;25(12):3755-3760. 25. Lacy AM, Delgado S, Castells A, et al. The long-term results of a randomized clinical trial of laparoscopy-assisted versus open surgery for colon cancer. Ann Surg. 2008;248(1):1-7. 26. Bartels SA, Vlug MS, Hollmann MW, et al. Small bowel obstruction, incisional hernia and survival after laparoscopic and open colonic resection (LAFA study). Br J Surg. 2014;101(9):1153-1159. 27. Weeks JC, Nelson H, Gelber S, Sargent D, Schroeder G, Clinical Outcomes of Surgery (COST) Study Group. Short-term quality-of-life outcomes following laparoscopic-assisted colectomy vs open colectomy for colon cancer: a randomized trial. JAMA. 2002;287(3):321-328. 28. Stucky CC, Pockaj BA, Novotny PJ, et al. Long-term follow-up and individual item analysis of quality of life assessments related to laparoscopic-assisted colectomy in the COST trial 93-46-53 (INT 0146). Ann Surg Oncol. 2011;18(9):2422-2431. 29. Basse L, Jakobsen DH, Bardram L, et al. Functional recovery after open versus laparoscopic colonic resection: a randomized, blinded study. Ann Surg. 2005;241(3):416-423. 30. Janson M, Björholt I, Carlsson P, et al. Randomized clinical trial of the costs of open and laparoscopic surgery for colonic cancer. Br J Surg. 2004;91(4):409-417. 31. Merola S, Weber P, Wasielewski A, Ballantyne GH. Comparison of laparoscopic colectomy with and without the aid of a robotic camera holder. Surg Laparosc Endosc Percutan Tech. 2002;12(1):46-51. 32. Weber PA, Merola S, Wasielewski A, Ballantyne GH. Teleroboticassisted laparoscopic right and sigmoid colectomies for benign disease. Dis Colon Rectum. 2002;45(12):1689-1694, discussion 1695–1686. 33. Bianchi PP, Ceriani C, Locatelli A, et al. Robotic versus laparoscopic total mesorectal excision for rectal cancer: a comparative analysis of oncological safety and short-term outcomes. Surg Endosc. 2010;24(11):2888-2894.
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34. Allemann P, Duvoisin C, Di Mare L, Hübner M, Demartines N, Hahnloser D. Robotic-assisted surgery improves the quality of total mesorectal excision for rectal cancer compared to laparoscopy: results of a case-controlled analysis. World J Surg. 2016;40(4):1010-1016. 35. Ghezzi TL, Luca F, Valvo M, et al. Robotic versus open total mesorectal excision for rectal cancer: comparative study of short and long-term outcomes. Eur J Surg Oncol. 2014;40(9):1072-1079. 36. Collinson FJ, Jayne DG, Pigazzi A, et al. An international, multicentre, prospective, randomised, controlled, unblinded, parallel-group trial of robotic-assisted versus standard laparoscopic surgery for the curative treatment of rectal cancer. Int J Colorectal Dis. 2012;27(2):233-241. 37. Park JS, Choi GS, Park SY, Kim HJ, Ryuk JP. Randomized clinical trial of robot-assisted versus standard laparoscopic right colectomy. Br J Surg. 2012;99(9):1219-1226. 38. Merchant AM, Lin E. Single-incision laparoscopic right hemicolectomy for a colon mass. Dis Colon Rectum. 2009;52(5):1021-1024. 39. Law WL, Fan JK, Poon JT. Single incision laparoscopic left colectomy for carcinoma of distal transverse colon. Colorectal Dis. 2010;12(7):698-701. 40. Law WL, Fan JK, Poon JT. Single-incision laparoscopic colectomy: early experience. Dis Colon Rectum. 2010;53(3):284-288. 41. Huscher CG, Mingoli A, Sgarzini G, et al. Standard laparoscopic versus single-incision laparoscopic colectomy for cancer: early results of a randomized prospective study. Am J Surg. 2012;204(1):115-120. 42. Poon JT, Cheung CW, Fan JK, Lo OS, Law WL. Single-incision versus conventional laparoscopic colectomy for colonic neoplasm: a randomized, controlled trial. Surg Endosc. 2012;26(10):27292734.
43. Klein CA. Parallel progression of primary tumours and metastases. Nat Rev Cancer. 2009;9(4):302-312. 44. Søndenaa K, Quirke P, Hohenberger W, et al. The rationale behind complete mesocolic excision (CME) and a central vascular ligation for colon cancer in open and laparoscopic surgery: proceedings of a consensus conference. Int J Colorectal Dis. 2014;29(4):419-428. 45. Bertelsen CA, Neuenschwander AU, Jansen JE, et al. Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: a retrospective, population-based study. Lancet Oncol. 2015;16(2):161-168. 46. Hohenberger W, Weber K, Matzel K, Papadopoulos T, Merkel S. Standardized surgery for colonic cancer: complete mesocolic excision and central ligation—technical notes and outcome. Colorectal Dis. 2009;11(4):354-364, discussion 364–355. 47. Bae SU, Saklani AP, Lim DR, et al. Laparoscopic-assisted versus open complete mesocolic excision and central vascular ligation for right-sided colon cancer. Ann Surg Oncol. 2014;21(7):2288-2294. 48. Kitano S, Inomata M, Mizusawa J, et al. Survival outcomes following laparoscopic versus open D3 dissection for stage II or III colon cancer (JCOG0404): a phase 3, randomised controlled trial. Lancet Gastroenterol Hepatol. 2017;2(4):261-268. 49. Cho MS, Baek SJ, Hur H, Soh Min B, Baik SH, Kyu Kim N. Modified complete mesocolic excision with central vascular ligation for the treatment of right-sided colon cancer: long-term outcomes and prognostic factors. Ann Surg. 2015;261(4):708-715. 50. Kim NK, Kim YW, Han YD, et al. Complete mesocolic excision and central vascular ligation for colon cancer: principle, anatomy, surgical technique, and outcomes. Surg Oncol. 2016;25(3):252-262.
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Todd D. Francone
L
aparoscopic colectomy was first described more than three decades ago, following the success of laparoscopic approaches to biliary surgery and appendicitis in the 1980s. Jacobs et al.1 described their first 20 laparoscopic colectomies for benign and malignant conditions. The paper was fairly modern, with operative times (170 minutes for sigmoid and 155 minutes for right colectomy) and lengths of stay (3 to 5 days for right, 3 to 8 days for sigmoid) comparable to more recent randomized trials. The authors concluded that the procedure “will become as accepted as laparoscopic cholecystectomy.” Although initial reports were promising, adoption of laparoscopic colectomy for cancer was met with early controversy. A report published by Johnstone et al. in 1996 documented 35 port site recurrences in patients undergoing laparoscopic colon cancer surgery.2 Other similar reports emerged, creating growing concerns over the safety of laparoscopic colectomy.3,4 As a result, a series of randomized trials were undertaken to compare outcomes between laparoscopic and open colectomy for cancer. These trials are described in detail later and represent one of the most comprehensive bodies of literature to evaluate the safety and efficacy of an emerging surgical technique. Despite the evidence supporting laparoscopic colectomy, widespread adoption has been slow. Moghadamyeghaneh et al.5 reviewed the National Inpatient Sample between 2009 and 2012 and found that 49% of elective colectomies for cancer were performed laparoscopically, with the rate of laparoscopy increasing over that time period. Other studies have reported similar numbers, with higher rates at academic centers, suggesting that there is still opportunity for increased utilization.6,7 Reasons for low adoption rates may include lack of specialized training, low surgeon or hospital volume, underreporting related to reliance on billing codes, or limitations of administrative data in capturing contraindications to laparoscopy. This chapter will review the trials comparing laparoscopic and open colectomy for cancer and discuss the key technical components of these procedures. It should be noted that laparoscopy is a technique and that it should be used when the surgeon has determined that an equivalent operation can be performed with regard to patient safety and oncologic outcome. Many of the trials included later excluded patients with locally advanced disease, perforation, or obstruction at the time of presentation.
SHORT-TERM OUTCOMES Many authors comparing laparoscopic to open colectomy for cancer published early papers focusing on short-term outcomes. All of these reported longer operative times for
CHAPTER
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laparoscopic procedures (Table 170.1), with differences ranging from 30 to 84 minutes. The rate of conversion to open varies widely across studies, ranging from 3% to 25% (see Table 170.1). The CLASICC study reported the highest conversion rate (25%) but did note that the rate decreased over the course of the study, suggesting that this may be more reflective of the learning curve.10 One of the most universal advantages of laparoscopic colon resection across trials is a decreased length of stay (see Table 170.1). This difference ranges from a 1-day in the COST study9 to a 5-day difference reported by Liang et al.14 Interestingly, Basse et al.12 published a study comparing laparoscopic and open colectomy in the setting of a universal fast-track surgery protocol and showed a 2-day length of stay in both groups. This raises the question of whether some advantages of laparoscopy may be blunted as more centers adopt enhanced recovery protocols. The majority of studies did not find any significant differences in short-term morbidity or mortality between the laparoscopic and open groups (see Table 170.1). Lacy et al.8 and Braga et al.13 demonstrated lower overall rates of postoperative complications in the laparoscopic group. In both studies, this seemed to be driven primarily by lower rates of wound infection.
RETURN OF BOWEL FUNCTION Although there is heterogeneity across studies in the definition of return of bowel function (flatus, bowel movement, oral tolerance), there is a consistent earlier return of bowel function in the laparoscopic group (Table 170.2). This is hypothesized to be the result of gentler tissue handling, and to account for the consistent decrease in length in the laparoscopic group. Interestingly, the Basse et al.12 study, which compared laparoscopic and open colectomy with a fast-track protocol, found no difference in length of stay or time to return of bowel function between the groups. This further supports the hypothesis that the benefit of laparoscopy in decreasing length of stay may be related to shortened ileus.
POSTOPERATIVE PAIN Postoperative pain is measured differently across trials, likely because of the challenges with quantifying this outcome (Table 170.3). Most studies used some measure of narcotic use as a surrogate for pain and found a benefit in the laparoscopic group in either duration of narcotic use or percent of patients requiring narcotics. This difference may be more beneficial than was understood at the time of publication of these papers, as surgical fields come under increasing political pressure to decrease the prescription of opiates.17
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Minimally Invasive Approaches to Colon Cancer CHAPTER 170 2049.e1
KEYWORDS Colon cancer Mortality Morbidity Quality of life
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SECTION IV Colon, Rectum, and Anus
TABLE 170.1 Short-Term Outcomes After Colon Resection LOS (DAYS) Trial
Sample Size
Lap
Lacy et al., 20028 COST, 20049 CLASICC, 200510 COLOR, 200511 Basse et al., 200512 Braga et al., 200513 Liang et al., 200714 ALCCaS, 200815 Braga et al., 201016
219 872 794 1248 60 391 269 592 268
5.2 7.9* 5 6† No difference 8.2 9.3‡ No difference 9.4 12.7‡ 9 14† 7 8 7 8.7¶
Open
OPERATIVE TIME (MINUTES)
POSTOPERATIVE COMPLICATIONS
Lap
Lap
Open
12%
31%†
MORTALITY Lap
Open
No difference No difference No difference
Open
150 180 145 215
95† 135 115‡ 131§
224
184†
213
174†
No difference
LYMPH NODE HARVEST Conversion Rates
No difference No difference 17.9% 36.3%ǁ No difference No difference No difference
11% 21% 25% 17% 10% 4.2% 3% 14.6% 5.2%
Lap
Open
No difference No difference No difference
*P = .005 † P < .001 ‡ P < .0001 § P < .05 ǁ P = .0005 ¶ P = .002 lap, Laparoscopic; LOS, length of stay.
TABLE 170.2 Return of Bowel Function After Colon Resection DAYS TO BOWEL MOVEMENT
TIME TO FLATUS Trial 8
Lacy et al., 2002 COLOR, 200511 CLASICC, 200510 Basse et al., 200512 Liang et al., 200714 ALCCaS, 200815
Sample Size
Lap
Open
219 1248 794 60 269 592
36 h
55 h*
Lap
Open
3.6 4.6† 5 6 No difference 3 days
3 days‡
4
TIME TO PO TOLERANCE Lap
Open
54 h 2.9 days No difference
84 h* 3.8 days†
LENGTH OF ILEUS Lap
Open
48 h
96 h*
5§
*P = .001 † P < .0001 ‡ P = .27 § P < .011 PO, Per os; Lap, laparoscopic.
TABLE 170.3 Postoperative Pain Control After Colon Resection Trial
Sample Size
COST, 20049
872
COLOR, 200511
1248
Liang et al., 200714
269
Measurement
Outcome
Days of parenteral narcotics Days of oral analgesics Percent of patients using opiates POD#1-3
3 days laparoscopic vs. 4 days open (P < .001) 1 day lap vs. 2 days open (P = .02)
Visual analog scale (POD#1)
h, Hours; POD, postoperative day.
POD#1: No difference POD#2: 41% lap vs. 49% open (P = .008) POD#3: 26% lap vs. 37% open (P = .0003) 3.5 laparoscopic vs. 8.6 open (P < .001)
LONG-TERM OUTCOMES ONCOLOGIC OUTCOMES As mentioned earlier, one of the key motivating factors for these studies was to demonstrate equivalent oncologic outcomes between laparoscopic and open colectomy. Since their initial publication, several trials have continued to publish updates (out to 10 years) to provide a definitive answer to this question. Table 170.4 summarizes the results from these studies. In every case, groups found no significant difference in overall survival, disease-free survival, wound recurrence, or overall recurrence between laparoscopic and open colectomy. The only study showing any type of oncologic difference, reported by Lacy et al.,8 showed an advantage for laparoscopic colectomy group in cancer-related mortality. This collective body of data has demonstrated that laparoscopic colectomy is noninferior to open colectomy in appropriately selected cancer patients.
Minimally Invasive Approaches to Colon Cancer CHAPTER 170
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TABLE 170.4 Long-Term Outcomes After Colon Resection Trial
Follow-Up
COST, 20049 COST, 200718 CLASICC, 200719 CLASICC, 201020 CLASICC, 201021 CLASICC, 201322 COLOR, 200923 COLOR, 201124 Lacy et al., 200825
3 years 5 years 3 years 5 years 3 years 10 years 5 years 5 years Median 95 months 5 years 5 years
Braga et al, 201016 LAFA, 201426 Liang et al., 200714 ALCCaS, 201215
Overall Survival No No No No
Disease-Free Survival
Wound Recurrence
Recurrence
Incisional Hernia
Small Bowel Obstruction
No difference
No difference
difference No difference No difference difference No difference No difference difference No difference No difference No difference difference No difference No difference
No difference No difference No difference No difference
No difference No difference
No difference
No difference
No difference
No difference No difference No difference No difference No difference No difference No difference 10% lap, 17% 2.4% lap, 7.3% open (P = .022) open (P = .039) Median 40 No difference No difference months 5 years No difference No difference No difference
Lap, Laparoscopic.
INCISIONAL HERNIA AND ADHESIVE BOWEL OBSTRUCTION In addition to survival, many long-term studies included data on rates of incisional hernia and adhesive small bowel obstruction. Although one may hypothesize that smaller incisions and decreased tissue handling associated with laparoscopic surgery would decrease the risk of these complications, that has not been clearly supported by the literature (see Table 170.4). The majority of groups found no difference, with the exception being the LAFA study, which showed decreases in both outcomes in the laparoscopic group.26 It may be possible that longer-term follow-up is needed to detect differences between the groups.
QUALITY OF LIFE Quality of life (QoL) is a challenging outcome to compare between procedures. There are numerous instruments available, and their use varies widely across studies. Many trials hypothesized that QoL would be improved in the laparoscopic group and invested considerable resources into collecting these data. Overall, most found at least some short-term QoL benefit in the laparoscopic group. The COST group published two papers focusing on QoL.27,28 They used a Symptom Distress Scale (SDS), QoL index, and single-item global scale. They found slightly better global QoL rating at 2 weeks in the laparoscopic group; however, no other comparisons out to 2 months reached significance. At 18 months, they found a modest benefit in the laparoscopic group for global QoL, but no differences for activity, daily living, health, or support. Other groups have studied differences in QoL, with mixed results.10,26,19,29 Braga et al.13 looked at QoL at 12, 24, and 36 months using the Short Form-36. They found significantly better general health and physical and social
functioning in the laparoscopic group at 12 months. However, this difference disappeared at 48 months. Taken together, the literature suggests that certain QoL domains are improved in laparoscopic compared with open colectomy and that these differences are probably the most significant in the first 6 to 12 months after surgery.
COST The cost of the operation itself is higher for laparoscopic colectomy than for open colectomy. Liang et al.14 reported significantly higher overall costs for laparoscopic compared with open colectomy ($194,442 vs. $136,420; P < .001). These differences were largely driven by increased equipment and disposable instrument costs. The COLOR group reported higher cost of operation (€1171; P < .001), higher cost of admission (€1556; P = .015), and higher cost to the healthcare system (€2244; P = .018) for laparoscopic colectomy. However, when they took into account total cost to society (time off of work), they found no difference between laparoscopic and open colectomy at 12 months.30
ADDITIONAL CONSIDERATIONS ROBOTICS Early studies on robotic colectomy were published in 2002.31,32 The three-dimensional view, improved articulation, and multiinstrument platform provide an advantage for many surgical specialties performing complex minimally invasive procedures. Although robotics is gaining more attention for proctectomy,33–36 studies have been published comparing robotic with laparoscopic colectomy. Park et al.37 randomized 70 patients to robotic versus laparoscopic right colectomy for cancer. They demonstrated equivalent length of stay, pain scores, complications, margins, and lymphadenectomy for both groups. The robotic group
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had longer operative times (195 vs. 130 minutes; P < .001) and increased operative costs ($12,235 vs. $10,320; P = .013). The increased cost of robotics and who should be responsible for this (patient, hospital, surgeon) remain a limitation for robotic colectomy.
SINGLE INCISION Single-incision laparoscopic colectomy (SILC) increases the complexity of laparoscopic colectomy, with the goal of limiting the incision size to only that needed for specimen extraction. Early case reports established its feasibility as an approach for both cancer and inflammatory bowel disease.38–40 More recently, two randomized trials have been published comparing SILC with standard laparoscopic colectomy.41,42 Results from these trials have demonstrated similar operating times, complication rates, and lymph node harvests, along with a decreased length of stay by 1 day in one of the studies. This remains a promising and challenging technique, with similar outcomes to standard laparoscopy for appropriately selected patients.
COMPLETE MESOCOLIC EXCISION Complete mesocolic excision (CME) with central vascular ligation is hypothesized to provide an oncologic benefit. This is based on the premise that metastases as determined by the primary tumor with cancer progression occurs in a stepwise pattern. CME therefore improves outcomes by removing the mesocolon in one package with high ligation of the feeding vessels.43,44 Data suggest improved short- and long-term oncologic outcomes.45,46 Improved outcomes are thought to be related to strict adherence to oncologic principles including dissection through the proper plane, central vascular ligation, and length of proximal and distal margins. CME has been shown to achieve an en bloc removal of the disease lesion with increased amounts of colonic mesentery. It is a technically challenging operation due to high ligation of the vascular pedicles with dissection along the aorta and mobilization of the splenic flexure. Numerous recent publications have demonstrated the feasibility of laparoscopic CME with short-term outcomes similar to those of open surgery.47,48 Operative times are typically longer with the laparoscopy, with majority of studies demonstrating equivalent morbidity and mortality when compared with open CME groups. The conversion to an open CME ranges between 2% and 10%.
TECHNIQUE AND PEARLS OF WISDOM Minimally invasive surgery, both laparoscopic and robotic, have become increasingly used both for benign and malignant disease processes. Based on the underlying disease and sequelae of such processes, it is essential to be familiar with various approaches (i.e., medial to lateral, lateral to medial, superior to inferior, etc.) resulting in optimal exposure, as well as safer, quicker, and a more reproducible dissection. This is without a doubt facilitated by a fundamental understanding of the surgical anatomy, allowing the surgeon the ability to proceed in a safe manner, perform an appropriate oncologic resection, and allow for additional diagnostic and therapeutic maneuvering.
LAPAROSCOPIC RIGHT COLECTOMY FOR COLON CANCER With either laparoscopic or robotic techniques, the patient is in the supine position. If the location of the tumor is unclear based on prior review of diagnostic imaging, the patient should be placed in the modified lithotomy or split-leg position to facilitate an intraoperative endoscopic evaluation. The preferred laparoscopic and robotic port placements are demonstrated in Fig. 170.1. The patient is placed in a Trendelenburg position with the operating table inclined toward the left. Once pneumoperitoneum is established, a thorough evaluation of the abdomen is critical to understand the anatomy, evaluate for disseminated disease, and assess the feasibility of an R0 resection. The omentum is retracted superiorly over the transverse colon and liver, and the small bowel is mobilized out of the pelvis. Grasping either the cecum or mesentery close to the cecum anteriorly or ventrally will highlight the ileocolic artery branching off the superior mesenteric artery. A tenting or bowstringing effect will be noted, with the mesenteric vasculature acting as the scaffold (Fig. 170.2). The medial-lateral approach is our preferred approach, with early ligation of the ileocolic pedicle. This is generally first performed by creating an opening in the peritoneum parallel to the vessels and then encircling the vessels superiorly. Some mobilization of the mesocolon from the retroperitoneal structures may be necessary and can be performed with gentle blunt sweeping motions dorsally. When doing so, care must be taken both to visualize the right ureter as well as the duodenum. Once these structures are well visualized and out of harm’s way, a high ligation of the vessel can be performed. The medial-to-lateral dissection can then be continued with retroperitoneal attachments safely dissected away from the right colon and its mesentery, either sharply or with gentle brush movements. Care must be taken to stay in the appropriate plane and not injure the duodenum or more laterally, not mobilize the kidney (Fig. 170.3). For hepatic flexure and proximal transverse colon tumors, further distal dissection of the mesentery is performed to the level of the middle colic vessels. The middle colic vessel is the primary blood supply to the proximal two-thirds of the transverse colon. Care must be taken to use precise technique in this retroperitoneal space because the pancreaticoduodenal and gastroepiploic veins may cause significant hemorrhage if excess tension or shearing occurs. After the middle colic vessel is identified, the right branch of the middle colic vessel is then divided after isolation. At this point the right colon will now be held in place only by lateral avascular attachments to the abdominal sidewall, hepatic flexure, and gastrocolic attachments, including the omentum to the transverse colon. These can generally be easily divided by dissecting energy devices. Dissection is carried out proximally, dividing the hepatic flexure attachments and then distally toward the pelvis. The gastrocolic attachments to the transverse colon need to be divided oftentimes with entry into the lesser sac. For right colectomies, the distal extent of dissection is generally around the falciform ligament or in line with
Minimally Invasive Approaches to Colon Cancer CHAPTER 170
A
2053
B
FIGURE 170.1 (A) Four-port technique for laparoscopic right colectomy. Extraction site is through the midline or surgeon preference. (B) Four-arm technique for robotic right colectomy using the DaVinci Xi. Extraction site is through the midline or surgeon preference.
“Bowstring” Duodenum Duodenum Ileocolic pedicle
Retroperitoneum
FIGURE 170.2 Grasping the cecum or its mesentery and lifting anterolateral to the abdominal wall will create a tenting or “bowstring” effect with a distinct crease coursing parallel to the vessel.
FIGURE 170.3 Medial-to-lateral mobilization highlighting duodenum and white line of Toldt.
the middle colic vessels. It is sometimes best to start at this point and work retrograde toward the hepatic flexure. Hepatic flexure and proximal transverse colon tumors can be quite challenging due to the surrounding anatomy including the duodenum, pancreas, gallbladder, and kidney (Fig. 170.4). Potential involvement of these structures should instigate a cascade of diagnostic and endoscopic evaluations with involvement of the appropriate surgical teams, whether approaching it minimally invasive or open.
In the presence of a hepatic flexure or proximal colon tumor, the omentum may be involved and should remain attached to the colon to ensure an en bloc resection. Entry into the lesser sac can often be helpful in the event there is potential involvement of retroperitoneal structures. The lesser sac is entered, and the proximal transverse mesocolon can then be sharply dissected from the other abdominal and retroperitoneal structures (Fig. 170.5), including the duodenum and pancreas. Another point
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Left branch of MCA
Right branch of MCA
MCA
FIGURE 170.6 The classic “Y” pattern of the middle colic vessels is not always straightforward. Often both the right and left branch course to the patient’s right. The right branch courses off the head of the pancreas and the duodenum; the left branch makes a sharp upward turn and then veers to the left, as shown here. MCA, Middle colic artery.
FIGURE 170.4 Hepatic flexure tumor (arrows) involving the right kidney and duodenum.
Omentum
sometimes in a high fashion (Fig. 170.6). Rather than isolating the right branch of the middle colic vessel, the entire middle colic vessel may be divided. This can be challenging due to the truncated length of the middle colic vessels. It may be isolated by gently retracting the mesentery of the transverse colon superiorly. The middle colic artery and its right and left branches will be identified. A window can be created around the middle colic vessels and divided in a retrograde left-to-right fashion.
LAPAROSCOPIC LEFT COLECTOMY/SIGMOID RESECTION FOR COLON CANCER
Stomach
Transverse colon
FIGURE 170.5 Accessing the lesser sac through the omentum (gastrocolic ligament); early entry into the lesser sac is key to facilitating mobilization of the transverse colon.
of entry into the lesser sac will be the fusion or attachment of the gallbladder dome to the transverse colon or mesocolon. Once completely dissected, the right colon and mesentery should be able to be mobilized and expressed as a midline structure. Division of the intestines and subsequent anastomosis can now be performed either intracorporeally via laparoscopy or in an open fashion once extracorporealized through an extraction incision.
TRANSVERSE COLECTOMY AND THE MIDDLE COLIC VESSELS In cases requiring resection of the transverse colon, the middle colic vessel will need to be ligated and divided,
Left colectomy refers to resection of the descending and/ or splenic flexure with anastomosis of the distal transverse colon to the sigmoid colon, whereas sigmoid resection refers to removal of the sigmoid colon with restoration of intestinal continuity between the descending colon and the rectum. As mentioned previously, there are potentially no absolute contradictions to proceeding with an oncologic resection minimally invasive; however, those patients with a suspected T4 tumor should have the appropriate multidisciplinary surgical teams involved in the event a more extensive resection is required for an R0 oncologic resection. In particular, sigmoid colon cancers may involve the ureter or bladder, and as such a urologist should be involved for possible partial cystectomy or ureteral reimplantation. If the resection is considered extensive, the surgeon should have a low threshold for conversion to an alternative approach, such as an open procedure, to optimize exposure and facilitate the dissection. All patients are placed in modified lithotomy (legs in slight hip flexion) or split-leg position with both arms tucked at the sides. Positioning in this manner affords the surgeons numerous advantages including exposure to the anus/rectum for intraoperative colonoscopy if needed. This can be particularly useful for a tumor that may not have been preoperatively tattooed and localized. The
Minimally Invasive Approaches to Colon Cancer CHAPTER 170
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FIGURE 170.7 (A) Four-port technique for laparoscopic left colectomy. Extraction site is through the midline or Pfannenstiel incision. (B) Standard proposed port placement for a robotic sigmoidectomy using the DaVinci Xi. Notice the camera port is slightly off midline. This allows dissection of the splenic flexure and upper pelvis. (C) Our preferred port placement for a robotic sigmoid resection or low anterior resection using the DaVinci Xi. The “hockey stick” formation allows access to the splenic flexure as well as the pelvis with no need to redock the arms.
preferred laparoscopic port placement is demonstrated in Fig. 170.7A. When performing a left colectomy or sigmoid resection, it is customary to divide the bowel (and potentially the major vascular structures) with an endomechanical linear stapling device of various staple heights. For this reason, a 12-mm port is used in the right lower quadrant (RLQ). When performing a robotic approach, ports are spaced evenly in a straight line from the anterior superior iliac spine in the RLQ to the mid-clavicle in the left upper quadrant (LUQ) (see Fig. 170.7B and C). Prior to any mobilization or resection, inspect the abdominal and pelvic cavity to evaluate for any altered anatomy (phlegmon or occult metastatic processes) not previously appreciated or identified on preoperative imaging. In oncologic procedures, the liver is carefully inspected on both anterior and posterior surfaces, and the peritoneum, omentum, and mesentery are examined for metastatic studding. If the latter is identified, biopsy and surgical judgment will dictate how next to proceed—and whether any further resection is necessary or prudent. During diagnostic laparoscopy the surgeon often identifies the pathology. In the setting of a colonic neoplasm, the pathology’s location should often be marked with an endoscopic tattoo. Ideally, the location is marked in three to four quadrants such that the tattoo is clearly visible on the antimesenteric surface. Marking the lesion in only one quadrant may pose some difficulty in identification if the tattoo lies on the mesenteric border or in a difficult location such as the splenic or hepatic flexures. In this event, an intraoperative CO2 endoscopy may be performed. CO2 insufflation allows for quick resolution of bowel distention and continued laparoscopy during or following the endoscopic evaluation. Once the pathology has been localized, adjustments to the preoperative surgical plan may be required. In the setting of malignancy, the location of the tumor
will determine resection margins and vessel ligation. For cancers in the left colon, oncologic margins should be 5 cm proximal and distal to the tumor. A high ligation of the inferior mesenteric artery (IMA) pedicle is often performed to ensure adequate mobilization and appropriate lymph node harvesting. Pathology located in the proximal sigmoid colon or distal descending colon may necessitate mobilization of the splenic flexure for appropriate tension-free anastomosis. For lesions in the proximal descending colon, a high ligation of the inferior mesenteric vein (IMV) may also be necessary to allow mobilization and approximation of the proximal colon to the upper rectum to create an intestinal anastomosis without tension. Similar to a right colectomy, the initial dissection involves the development of the avascular plane between the parietal peritoneum overlying the retroperitoneum and the visceral peritoneum encompassing the mesentery of the left colon. There are multiple approaches to achieve this task including medial to lateral and lateral to medial. We prefer a medial-to-lateral approach for a left colectomy. The initial step for this approach requires initial identification of the IMA pedicle. The mesenteric fold containing the IMA can be found overlying and cephalad to the sacral promontory. Ventral retraction of the sigmoid and left colon mesentery will assist in outlining the IMA pedicle entering into the pelvis to form the superior rectal artery, in a similar bowstring effect noted with the ileocolic pedicle (Fig. 170.8). In the event that division of these adhesions does not allow for a clear “bowstring” of the IMA pedicle, then an alternative approach, such as a lateral to medial, should be considered to avoid injury to underlying structures such as the ureter, hypogastric nerves, and iliac vessels (Fig. 170.9). After the key retroperitoneal structures have been identified, the IMA may be divided to facilitate the pelvic
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IMV
IMA
Ligament of Trietz SP White line of Toldt Right common Iliac artery
FIGURE 170.8 The outline of the inferior mesenteric artery (IMA) can be visualized by gentle ventral retraction of the pedicle as it courses over the sacral promontory (SP). The space between the IMA and the SP has been termed the critical angle and marks the avascular plane between the retroperitoneum and the colon mesentery.
Left gonadal vessels
Ureter SP
FIGURE 170.9 Care is taken to identify and avoid the left ureter, left gonadal vessels, and the hypogastric nerve plexus. SP, Sacral promontory.
dissection. The medial-to-lateral mobilization is performed similar to that done on the right side. The dissection proceeds cephalad to the level of the superior pole of the kidney and may continue to the inferior aspect of the spleen. After medial-to-lateral mobilization is completed, the remaining avascular lateral attachments of the colon to the omentum, spleen, and abdominal and retroperitoneal sidewalls should be divided. Remember, when performing a resection of a tumor in the transverse colon, the omentum should be left on the colon and resected with the specimen to ensure adequate margins and an R0 resection. In the presence of a descending colon or distal transverse colon mass, splenic flexure mobilization will be required. Splenic flexure mobilization is generally performed using a combination of approaches. The patient is placed in a reverse Trendelenburg position with the table inclined toward the right. Typically, if an adequate medial-to-lateral mobilization is performed of the left colon and IMV, then mobilization of the splenic flexure is reduced to division of the lateral attachments of the phrenocolic ligaments
FIGURE 170.10 Continued medial-to-lateral mobilization between the inferior mesenteric artery (IMA) and inferior mesenteric vein (IMV) will facilitate mobilization of the splenic flexure.
(Fig. 170.10). Laterally, the attachments to the abdominal sidewall and spleen are carefully divided while being mindful not to injure the splenic capsule. A critical step in left colectomy is identification of a distal transection point. Distal transection localization is dependent upon both anatomic and physiologic entities. Appropriate mesenteric vascular supply must be accounted for, as well as distal resection margins in the setting of malignancy. For a sigmoid or distal left colectomy, division is generally performed at the level of the proximal rectum, past the splaying of the taenia coli on the antimesenteric surface. Further dissection and transection may be required to get appropriate distal margins. In general, at least a 5-cm distal margin is required for colonic malignancies. After the point of transection is selected, the mesentery is divided. Division of the upper rectum is generally performed with an endomechanical stapling device through the RLQ port. The colon is then extracted. Options for an extraction site include extension of the periumbilical incision, creation of a Pfannenstiel incision, or extension of the RLQ incision. After the abdominal wall is opened appropriately and the peritoneal cavity entered, a wound protector is inserted to protect the skin and soft tissue from contamination during externalization and creation of anastomosis. Through the wound protector, the distal stapled end of the colon and the proximal mobilized colon and mesentery are extracorporealized. The proximal dissection point is predicated upon a number of issues. In the setting of malignancy, at least a 5-cm margin is required. In all cases, appropriate maintenance of vascular supply must be ensured to minimize risk of ischemia of the anastomosis. Double-stapled end-end or end-side technique are often used during a left or sigmoid colectomy. It is recommended by the American Society of Colon and Rectal Surgeons that all left-sided anastomoses be tested for leakage. Once confident the anastomosis is secure and viable, the extraction sites and all port sites 10 mm or greater in size are closed.
COMPLETE MESOCOLIC EXCISION When performing a CME for right colon tumor located in the cecum approximately, the right branches of the middle
Minimally Invasive Approaches to Colon Cancer CHAPTER 170
colic artery and vein are ligated in addition to the ileocolic vessels. It is imperative to ligate the vessels just as they take off the superior mesenteric artery (SMA). For lesions located in the hepatic flexure and proximal transverse colons, an extended right colectomy is performed with the middle colic artery and vein ligated.49 Omentectomy is performed just below the gastroepiploic vessels and unless infiltrated by the tumor, the right gastroepiploic vessels are preserved. When performing a CME for a left colon tumor located in the proximal descending colon, the IMA is preserved and the left colic artery and superior rectal artery are ligated at their origin. For mid-descending and sigmoid colon cancers, the root of the IMA is ligated and the IMV is ligated just below the lower border of the pancreas.50
CONCLUSION Ongoing evidence supports the feasibility and safety of a minimally invasive surgery approach for colon cancer. To date, laparoscopy remains the most widely used minimally invasive technique with robotic surgery gaining momentum despite unsubstantiated evidence for cost-effectiveness in the treatment of both colon cancer and rectal cancer. It cannot be overstated that minimally invasive surgery is a technique or a “tool” that a surgeon may use to successfully remove pathology. It should be used when the surgeon has determined that an equivalent operation can be performed with regard to patient safety and oncologic outcome when compared with an open approach.
REFERENCES 1. Jacobs M, Verdeja JC, Goldstein HS. Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc. 1991;1(3):144-150. 2. Johnstone PA, Rohde DC, Swartz SE, Fetter JE, Wexner SD. Port site recurrences after laparoscopic and thoracoscopic procedures in malignancy. J Clin Oncol. 1996;14(6):1950-1956. 3. Berends FJ, Kazemier G, Bonjer HJ, Lange JF. Subcutaneous metastases after laparoscopic colectomy. Lancet. 1994;344(8914): 58. 4. Reilly WT, Nelson H, Schroeder G, Wieand HS, Bolton J, O’Connell MJ. Wound recurrence following conventional treatment of colorectal cancer. A rare but perhaps underestimated problem. Dis Colon Rectum. 1996;39(2):200-207. 5. Moghadamyeghaneh Z, Carmichael JC, Mills S, Pigazzi A, Nguyen NT, Stamos MJ. Variations in laparoscopic colectomy utilization in the United States. Dis Colon Rectum. 2015;58(10):950-956. 6. Yeo HL, Isaacs AJ, Abelson JS, Milsom JW, Sedrakyan A. Comparison of open, laparoscopic, and robotic colectomies using a large national database: outcomes and trends related to surgery center volume. Dis Colon Rectum. 2016;59(6):535-542. 7. Bardakcioglu O, Khan A, Aldridge C, Chen J. Growth of laparoscopic colectomy in the United States: analysis of regional and socioeconomic factors over time. Ann Surg. 2013;258(2):270-274. 8. Lacy AM, García-Valdecasas JC, Delgado S, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet. 2002;359(9325):2224-2229. 9. Nelson H, Sargent DJ, Wieand HS, et al. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004;350(20):2050-2059. 10. Guillou PJ, Quirke P, Thorpe H, et al. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005;365(9472):1718-1726. 11. Veldkamp R, Kuhry E, Hop WC, et al. Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol. 2005;6(7):477-484.
2057
12. Basse L, Jakobsen DH, Bardram L, et al. Functional recovery after open versus laparoscopic colonic resection: a randomized, blinded study. Ann Surg. 2005;241(3):416-423. 13. Braga M, Frasson M, Vignali A, Zuliani W, Civelli V, Di Carlo V. Laparoscopic vs. open colectomy in cancer patients: long-term complications, quality of life, and survival. Dis Colon Rectum. 2005;48(12):2217-2223. 14. Liang JT, Huang KC, Lai HS, Lee PH, Jeng YM. Oncologic results of laparoscopic versus conventional open surgery for stage II or III left-sided colon cancers: a randomized controlled trial. Ann Surg Oncol. 2007;14(1):109-117. 15. Hewett PJ, Allardyce RA, Bagshaw PF, et al. Short-term outcomes of the Australasian randomized clinical study comparing laparoscopic and conventional open surgical treatments for colon cancer: the ALCCaS trial. Ann Surg. 2008;248(5):728-738. 16. Braga M, Frasson M, Zuliani W, Vignali A, Pecorelli N, Di Carlo V. Randomized clinical trial of laparoscopic versus open left colonic resection. Br J Surg. 2010;97(8):1180-1186. 17. Waljee JF, Li L, Brummett CM, Englesbe MJ. Iatrogenic opioid dependence in the United States: are surgeons the gatekeepers? Ann Surg. 2017;265(4):728-730. 18. Fleshman J, Sargent DJ, Green E, et al. Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group trial. Ann Surg. 2007;246(4):655-662, discussion 662–654. 19. Jayne DG, Guillou PJ, Thorpe H, et al. Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol. 2007;25(21):3061-3068. 20. Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM, Guillou PJ. Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg. 2010;97(11):1638-1645. 21. Taylor GW, Jayne DG, Brown SR, et al. Adhesions and incisional hernias following laparoscopic versus open surgery for colorectal cancer in the CLASICC trial. Br J Surg. 2010;97(1):70-78. 22. Green BL, Marshall HC, Collinson F, et al. Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg. 2013;100(1):75-82. 23. Buunen M, Veldkamp R, Hop WC, et al. Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol. 2009;10(1):44-52. 24. Schölin J, Buunen M, Hop W, et al. Bowel obstruction after laparoscopic and open colon resection for cancer: results of 5 years of follow-up in a randomized trial. Surg Endosc. 2011;25(12):3755-3760. 25. Lacy AM, Delgado S, Castells A, et al. The long-term results of a randomized clinical trial of laparoscopy-assisted versus open surgery for colon cancer. Ann Surg. 2008;248(1):1-7. 26. Bartels SA, Vlug MS, Hollmann MW, et al. Small bowel obstruction, incisional hernia and survival after laparoscopic and open colonic resection (LAFA study). Br J Surg. 2014;101(9):1153-1159. 27. Weeks JC, Nelson H, Gelber S, Sargent D, Schroeder G, Clinical Outcomes of Surgery (COST) Study Group. Short-term quality-of-life outcomes following laparoscopic-assisted colectomy vs open colectomy for colon cancer: a randomized trial. JAMA. 2002;287(3):321-328. 28. Stucky CC, Pockaj BA, Novotny PJ, et al. Long-term follow-up and individual item analysis of quality of life assessments related to laparoscopic-assisted colectomy in the COST trial 93-46-53 (INT 0146). Ann Surg Oncol. 2011;18(9):2422-2431. 29. Basse L, Jakobsen DH, Bardram L, et al. Functional recovery after open versus laparoscopic colonic resection: a randomized, blinded study. Ann Surg. 2005;241(3):416-423. 30. Janson M, Björholt I, Carlsson P, et al. Randomized clinical trial of the costs of open and laparoscopic surgery for colonic cancer. Br J Surg. 2004;91(4):409-417. 31. Merola S, Weber P, Wasielewski A, Ballantyne GH. Comparison of laparoscopic colectomy with and without the aid of a robotic camera holder. Surg Laparosc Endosc Percutan Tech. 2002;12(1):46-51. 32. Weber PA, Merola S, Wasielewski A, Ballantyne GH. Teleroboticassisted laparoscopic right and sigmoid colectomies for benign disease. Dis Colon Rectum. 2002;45(12):1689-1694, discussion 1695–1686. 33. Bianchi PP, Ceriani C, Locatelli A, et al. Robotic versus laparoscopic total mesorectal excision for rectal cancer: a comparative analysis of oncological safety and short-term outcomes. Surg Endosc. 2010;24(11):2888-2894.
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34. Allemann P, Duvoisin C, Di Mare L, Hübner M, Demartines N, Hahnloser D. Robotic-assisted surgery improves the quality of total mesorectal excision for rectal cancer compared to laparoscopy: results of a case-controlled analysis. World J Surg. 2016;40(4):1010-1016. 35. Ghezzi TL, Luca F, Valvo M, et al. Robotic versus open total mesorectal excision for rectal cancer: comparative study of short and long-term outcomes. Eur J Surg Oncol. 2014;40(9):1072-1079. 36. Collinson FJ, Jayne DG, Pigazzi A, et al. An international, multicentre, prospective, randomised, controlled, unblinded, parallel-group trial of robotic-assisted versus standard laparoscopic surgery for the curative treatment of rectal cancer. Int J Colorectal Dis. 2012;27(2):233-241. 37. Park JS, Choi GS, Park SY, Kim HJ, Ryuk JP. Randomized clinical trial of robot-assisted versus standard laparoscopic right colectomy. Br J Surg. 2012;99(9):1219-1226. 38. Merchant AM, Lin E. Single-incision laparoscopic right hemicolectomy for a colon mass. Dis Colon Rectum. 2009;52(5):1021-1024. 39. Law WL, Fan JK, Poon JT. Single incision laparoscopic left colectomy for carcinoma of distal transverse colon. Colorectal Dis. 2010;12(7):698-701. 40. Law WL, Fan JK, Poon JT. Single-incision laparoscopic colectomy: early experience. Dis Colon Rectum. 2010;53(3):284-288. 41. Huscher CG, Mingoli A, Sgarzini G, et al. Standard laparoscopic versus single-incision laparoscopic colectomy for cancer: early results of a randomized prospective study. Am J Surg. 2012;204(1):115-120. 42. Poon JT, Cheung CW, Fan JK, Lo OS, Law WL. Single-incision versus conventional laparoscopic colectomy for colonic neoplasm: a randomized, controlled trial. Surg Endosc. 2012;26(10):27292734.
43. Klein CA. Parallel progression of primary tumours and metastases. Nat Rev Cancer. 2009;9(4):302-312. 44. Søndenaa K, Quirke P, Hohenberger W, et al. The rationale behind complete mesocolic excision (CME) and a central vascular ligation for colon cancer in open and laparoscopic surgery: proceedings of a consensus conference. Int J Colorectal Dis. 2014;29(4):419-428. 45. Bertelsen CA, Neuenschwander AU, Jansen JE, et al. Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: a retrospective, population-based study. Lancet Oncol. 2015;16(2):161-168. 46. Hohenberger W, Weber K, Matzel K, Papadopoulos T, Merkel S. Standardized surgery for colonic cancer: complete mesocolic excision and central ligation—technical notes and outcome. Colorectal Dis. 2009;11(4):354-364, discussion 364–355. 47. Bae SU, Saklani AP, Lim DR, et al. Laparoscopic-assisted versus open complete mesocolic excision and central vascular ligation for right-sided colon cancer. Ann Surg Oncol. 2014;21(7):2288-2294. 48. Kitano S, Inomata M, Mizusawa J, et al. Survival outcomes following laparoscopic versus open D3 dissection for stage II or III colon cancer (JCOG0404): a phase 3, randomised controlled trial. Lancet Gastroenterol Hepatol. 2017;2(4):261-268. 49. Cho MS, Baek SJ, Hur H, Soh Min B, Baik SH, Kyu Kim N. Modified complete mesocolic excision with central vascular ligation for the treatment of right-sided colon cancer: long-term outcomes and prognostic factors. Ann Surg. 2015;261(4):708-715. 50. Kim NK, Kim YW, Han YD, et al. Complete mesocolic excision and central vascular ligation for colon cancer: principle, anatomy, surgical technique, and outcomes. Surg Oncol. 2016;25(3):252-262.