During 2004 to 2011, 81, 420, and 166 patients with colorectal cancer (CRC), epithelial appendiceal neoplasm (APN), and gastric cancer (GC) with PC were treated with cytoreductive surgery (CRS) plus perioperative chemotherapy. CRS was performed by peritonectomy techniques using an aqua dissection.
The current state-of-the-art treatment for the peritoneal carcinomatosis (PC) from colorectal, appendiceal, and gastric cancers consists of a comprehensive management strategy using cytoreductive surgery (CRS) and perioperative intraperitoneal chemotherapy (PIC) [
However, complete cytoreduction is sometimes difficult in patients with deep invasion into the liver hilum, lesser omentum, pelvic structures, liver parenchyma, or diffuse involvement of the mesentery and serosa of small bowel. Even by the most experienced surgeons in the world, the incidences of complete cytoreduction are reported 77% (617/802) [
Between June, 2004, and January, 2011, a total of 667 patients underwent CRS combined with PIC for peritoneal carcinomatosis from colorectal origin (
Preoperatively, the tumor volume was quantified according to computed tomography (CT) scans using the Peritoneal Cancer Index (PCI, Washington Cancer Institute) [
CRS consists of numerous surgical procedures depending on the extent of peritoneal tumor manifestation. Surgery may include parietal and visceral peritonectomy, greater and lesser omentectomy, splenectomy, cholecystectomy, resection of the liver capsule, small bowel resections, colonic and rectal resections, gastrectomy, pancreatic resection, hysterectomy, ovariectomy, and urine bladder resection [
Patients who had the following criteria are excluded as candidates for peritonectomy: (1) evidence of lymph node involvement and distant hematogenous metastasis confirmed by computed tomography (CT), magnetic resonance imaging (MRI), or 18Fluorodeoxyglucose positron emission tomography (PET/CT), (2) progressive disease after preoperative chemotherapy, and (3) severe comorbidities or poor general condition.
Under general anesthesia, midline incision was made from the xiphoid to the pubis, and PCI score was calculated in each case [
For the tissue dissection, electrosurgical techniques are used. In electrosurgery, a generator delivers high frequency current greater than 200 kHz under high power electricity (100 Watt), and the tissue impedance converts electric current into thermal energy, resulting in the localized tissue heating and coagulation. We use the electrosurgical generator (Valleylab Inc., Boulder, CO, USA), on pure cut and adjusted to the maximum electrical power. The mainly used handpiece is the ball-tipped type. The 2 mm ball-tip electrode is used for dissecting on visceral surfaces, including stomach, small bowel, and colon. When more rapid tumor destruction is required, the 5 mm ball-tip can be used.
Before the tissue dissection with electrosurgery, a 5% dextran solution plus adrenaline (a concentration of 10−6) is injected into the dissection plane to separate the layers properly and to decrease bleeding. The technique is named the
The skin incision deepened through the
The peritoneum of the Morrison pouch and paracolic gutters on both sides is completely freed from retroperitoneum and is removed with the anterior parietal peritoneum. The ureters and gonadal vessels are identified and taped. In males, the gonadal vessels should be preserved but are removed with the ovary in females.
The dissected parietal peritoneum is opened in the midline, and extensive wash and aspiration of the peritoneal cavity ten times using one liter of normal saline each time is done. The purpose of the washing is to remove peritoneal free cancer cells and mucinous materials from the peritoneal cavity. During the washing surgeons decide the operation plan.
If the undersurface of the diaphragm is involved, stripping of peritoneum from the right and left hemidiaphragm is done. The falciform and round ligament are taken down and resected completely. Bleeding from diaphragmatic muscle is stopped by argon beam coagulation (ABC) which has a penetration depth of coagulation limited to a few millimeters. Advantages of ABC include the ability to coagulate broad surface areas and larger vessels.
Figure
Cancer cells tend to invade the muscle layer of the encircled area of the right hemidiaphragm, where is the boundary of bare area and peritoneal reflection. Bare area below the invaded.
Partial resection of the diaphragm by using a linear stapler.
A greater omentectomy is performed with combination of splenectomy and the resection of anterior leaf of mesocolon. If the omentum is free of disease, gastroepiploic arcade is preserved after taping the root of the vessels. Greater omentum is removed with the right gastroepiploic vessels if it is involved with bulky tumor. Splenic artery and vein are identified and ligated at the splenic hilum. If the right gastroepiploic vessels and spleen are removed, left gastric artery and vein should be preserved. After the left lobe of the liver is freed from the left triangular ligament, resection of the lesser omentum along the Arantius duct is started. Next the small incisions are made on the peritoneal attachment to the stomach wall, and the 5% dextran solution is injected through the incision (
A 5% dextrose solution is injected in the incision site on the lesser curvature, and the left gastric vessels are identified and taped. Aqua dissection technique.
Preservation of the left gastric vessels and whole stomach. Surgical techniques of the removal of lesser omental tumors.
Except for gastric cancer, gastrectomy may be sometimes indicated in patients with peritoneal carcinomatosis from PMP, colorectal cancer, ovarian cancer, and mesothelioma [
The parts of gastric wall liable to involvement by the disease process (dotted line): (1) the posterior wall of the antrum in the vestibule of the omental bursa, (2) the mid-lesser curvature, which are invaded from the metastasis of lesser omentum, and (3) the upper greater curvature by the invasion from splenic hilar metastasis. Region 4 is named as superior omental recessus, which is frequently involved in pseudomyxoma peritonei.
In PC from PMP and mucinous ovarian tumors, hepatoduodenal ligament and liver hilar plate are frequently involved (Figures
Enhanced CT scan shows tumor located in the hilar, cystic, and umbilical plate, and tumor extended in Glisson’s capsule.
The view of the hilar plate after complete eradication of the infiltrating tumor. The right portal pedicle is tapped by blue tape. The oozing blood from the liver surface is controlled by ABC. Dissection of mucinous tumor from the hilar plate after taping the right portal pedicle branches. This excision only involves surgical removal of Glisson’s capsule bearing tumor and approximately 1-2 cm in depth of hepatic parenchyma.
Figure
The only efficient procedure for hilar metastases is excision, which is followed by complementary treatment. Surgery should start with the dissection of the hepatoduodenal ligament, to identify the limits of the tumor, its mobility, or infiltration of adjacent planes and elements, confirming the existence or absence of infiltration of vascular elements and, in particular, of the portal vein or its branches. Dissection of the hepatic pedicle usually begins with isolation of the artery followed by the biliary tract and portal vein. Aqua dissection enables to identify the second branches of the portal triads (Figure
As shown in Figure
Axial contrast-enhanced CT scan of the upper abdomen demonstrates multiple low attenuated cystic lesions with rim-like calcifications scalloping the liver margin, infiltrating the spleen, and compressing the bowel, pancreas, and left kidney.
The operative view after enucleating of a large cystic lesion indenting the liver deeply. The resected specimen of the lesion described in Figure
Peritoneum of the superior omental recess (region 4 in Figure
Figure
Coronal enhanced CT scan shows tumor located between the inferior vena cava, caudate lobe, and left crus of diaphragm.
Morrison’s pouch and the paracolic gutter are the common sites of tumor implantation. The peritoneum covering Morrison’s pouch is removed with the peritoneum on the right paracolic gutter, right subdiaphragm, and right abdominal wall (Figures
Dissection of the tumor in the superior omental recessus. By traction of tumors to the left side, the capsule of the caudate lobe is cut and the tumors with liver capsule and retroperitoneum are dissected from the caudate lobe, left crural muscle, and vena cave.
Dissection line of Morrison’s pouch. The peritoneum covering Morrisons’s pouch is removed with the peritoneum on the right paracolic gutter, right subdiaphragm, and right abdominal wall.
Large tumors attach on the ascending colon and hepatic flexure, and tumors on the paracolic gutter and Morrison’s pouch are removed in combination with extended right hemicolectomy.
The entire pelvic peritoneum is dissected from the anterior inferior abdominal wall, urinary bladder, and retroperitoneum. The peritoneum covering the urinary bladder is dissected, and the rectovesical pouch is completely freed from the urinary bladder and rectum. In males, the space between the seminal vesicle and peritoneum of rectovesical pouch is dissected, lifting the vas deferens off. In females, blood vessels around the uterus are dissected and cut with Ligasure (Valleylab Inc., Boulder, CO, USA). Amputation of the vagina is done at a plane 1 cm below the peritoneal reflection of the Douglass pouch to ensure removal of all tumors occupying the cul-de-sac.
If the tumor invades the anterior rectal wall, the rectum is cut at 1 cm below the peritoneal reflection. Reasonable length of the rectum should be preserved for the anastomosis with the colon or ileum.
The entire small bowel and its mesentery are traced from the duodenojejunal flexure to the ileocecal junction. There are often tumor nodules at paraduodenal recesses covering the ligament of Treitz, and these are easily dissected by the
Complete cytoreduction is aimed by removing all macroscopic tumors by peritonectomy combined with laser or electric fulguration and HIPEC for microscopic PC.
The aim of CRS was to obtain complete macroscopic cytoreduction as a precondition for the application of HIPEC. The residual disease was classified intraoperatively using the completeness of cytoreduction (CC) score [
All patients were followed up and no patients were lost to follow up. Outcome data were obtained from medical records and patients’ interviews. All statistical analyses were performed using the SPSS software statistical computer package version 17 (SPSS Inc., Chicago, USA).
CC-0,-1 resections were done in 62/81 (76.5%), 228/420 (54.3%), and 101/166 (60.8%) of patients with colorectal cancer, appendiceal neoplasm, and gastric cancer (Table
Correlation of CC scores and PCI scores.
Total | |||||
---|---|---|---|---|---|
colorectal cancer | |||||
CC-0,-1 | 43 (95.5%) | 16 (76.2%) | 3 (30.0%) | 0 (0.0%) | 62 (76.5%) |
CC-2,-3 | 2 | 5 | 7 | 5 | 19 |
Appendiceal neoplasm | |||||
CC-0,-1 | 111 (97.4%) | 57 (0.3%) | 39 (36.4%) | 21 (17.8%) | 228 (54.3%) |
CC-2,-3 | 3 | 24 | 68 | 97 | 192 |
Gastric cancer | |||||
CC-0,-1 | 95 (79.2%) | 5 (21.7%) | 0 (0.0%) | 1 (25.0%) | 101 (60.8%) |
CC-2,-3 | 25 | 23 | 14 | 3 | 66 |
The reasons of CC-2,-3 resections are listed in Table
The causes of CC-2,-3 resections.
Colorectal cancer | Appendiceal neoplasm | Gastric cancer | |
---|---|---|---|
Involvement of all peritoneal regions | 7 | 71 (22 + old age) | 11 |
Diffuse small bowel involvement | 5 (2 + LB#, 1 + PH$) | 86 (15 + LB, 3 + PH,1 + ST&) | 22 (1 + LG) |
Bleeding | 0 | 10 | 0 |
Old age | 1 | 5 | 0 |
Comorbidity | 0 | 4 | 0 |
Positive histologic margin | 0 | 0 | 6 |
Local invasion | 0 | 2 | 3 |
Lymph node metastasis | 0 | 0 | 3 |
Perihepatic involvement | 0 | 6 | 0 |
Emergency | 1 | 2 | 0 |
others | 1 | 4 | 1 |
#LB: large bowel involvement, $PH: perihepatic involvement, and &ST: stomach involvement.
Regarding the correlation between PCI scores of small bowel (SB-PCI) and CC scores in colorectal cancer patients, CC-0,-1 resection was done in 36 of 38 (95%) patients with SB-PCI ≤ 3, but only in 12 of 24 (50%) patients with SBPCI ≥ 4.
In gastric cancer patients, 65 of 78 (83%) of patients with SB-PCI ≤ 3 and 43/83 (52%) of those with SBPCI ≥ 4 underwent CC-0,-1 resections.
In PMP patients, CC-0,-1 resection rate was significantly higher in patients with SB-PCI ≤ 6 (209/265, 79%) than that in those with SB-PCI ≥ 7 (19/155, 12%).
Before December, 2007 (first 3 years), CC-0,-1 resection was done in 82 (42%) of 197 patients. After January, 2008 (next 3 years), when the aqua dissection method was introduced, it was done in 302 (64.3%) of 470 patients, and there was a significant difference (
A total of 41 (6.1%) among 667 patients died postoperatively. Mortality rate (3.6%, 14/391) after CC-0,-1 resections was significantly lower than that (8.7%, 24/276) after CC-1,-2 resections (Table
Postoperative mortality and morbidity after cytoreductive surgery.
No complication | Grades 1-2 | Grade 3 | Reoperation | Hospital deaths | |
---|---|---|---|---|---|
Colorectal cancer | |||||
CC-0,-1 | 35 (56.5%) | 19 (30.1%) | 3 (4.8%) | 3 (4.8%) | 2 (3.2%) |
CC-2,-3 | 10 (52.6%) | 3 (15.8%) | 4 (21.0%) | 0 | 2 (10.6%) |
Appendiceal neoplasm | |||||
CC-0,-1 | 128 (56.1%) | 44 (19.3%) | 32 (14.0%) | 19 (8.3%) | 5 (2.2%) |
CC-2,-3 | 98 (51.0%) | 26 (13.5%) | 38 (19.8%) | 10 (5.2%) | 20 (10.4%) |
Gastric cancer | |||||
CC-0,-1 | 76 (75.2%) | 8 (7.9%) | 9 (8.9%) | 2 (2.0%) | 7 (6.9%) |
CC-2,-3 | 45 (68%) | 10 (15.2%) | 4 (6.1%) | 2 (3.0%) | 5 (7.6%) |
Major complication (grade 3-4 complications) occurred in 126 patients (18.9%). A reoperation was necessary in 36 patients (5.4%). The experienced complications were abdominal abscess (
The overall 1-year, 3-year, and 5-year survival rates and median survivals of the three groups are shown in Table
Survival after CRS in terms of CC score and PCI score.
Median survivals | 1-year survival | 3-year survival | 5-year survival | Log-rank test ( | |
months | (%) | (%) | (%) | ||
Colorectal cancer | |||||
CC-0,-1 ( | 38.4 | 93 | 51 | 28 | |
CC-2,-3 ( | 19.2 | 33 | 16 | 0 | |
NR | 95 | 59 | 59 | ||
18.2 | 83 | 37 | 0 | ||
Appendiceal neoplasm | |||||
CC-0,-1 ( | NR | 99 | 93 | 84 | |
CC-2,-3 ( | NR | 91 | 69 | 50 | |
NR | 99 | 89 | 76 | ||
49.2 | 87 | 63 | 55 | ||
Gastric cancer | |||||
CC-0,-1 ( | 21.5 | 70 | 26 | 17 | |
CC-2,-3 ( | 13.6 | 59 | 8 | 2 | |
21.5 | 76 | 23 | 14 | ||
13.6 | 57 | 21 | 3 |
The 5-year survival rate of colorectal cancer patients with PCI score ≤ 10 was significantly better than that with PCI score ≥ 11 (
By the multivariate analysis, PCI scores were capable of serving as thresholds for favorable versus poor prognosis in each group and CC scores demonstrated as the significant independent prognostic factors after CRS. In colorectal cancer patients, CC score (CC-0,1 versus CC-2,-3) and PCI score (PCI ≤ 10 versus PCI ≥ 11) emerged as the independent prognostic factors (
Current surgical management of the PC can be performed with curative intent and potential long-term survival when a strategy of CRS combined with HIPEC is used to select patients.
Adequate patient selection and the improvement of surgical skills of surgeons are crucial to obtain a complete macroscopic cytoreduction, which is a leading predictor of patient outcome. Adequate patient selection is sometimes difficult for surgeons with experience of small number of cases with PC. Many criteria have to be assessed in each patient: performance status, response to chemotherapies, existence of lymph node and/or hematogenous metastasis, histologic grading, PCI, and comorbidities. Patients with poor performance status, severe comorbidities, and PC already spread to the entire peritoneal cavity are not indicated for complete cytoreduction. In gastric cancer, response after neoadjuvant chemotherapy is one of the selection criteria for CRS [
In the surgical treatment of patients with PC from colorectal cancer, appendiceal neoplasm, and gastric cancer, complete cytoreduction is believed as an essential factor for a good prognosis. In the present data, CC-0,-1 and the PCI scores of less than the threshold values for each disease clearly were demonstrated as independent prognostic factors after CRS plus perioperative chemotherapy. Peritonectomy techniques improved the incidence of complete cytoreduction, as compared with the ordinary surgical techniques [
We developed an aqua dissection technique to guide surgeons to perform a safe tumor dissection through the correct dissection plane, to avoid injury of the important vessels, and to reduce the blood loss. Using this technique, the dissection around the hepatic hilar plate and lateral dissection of the pelvic spaces can be done in a safer and easier manner.
Diffuse small bowel involvement is the most frequent cause of incomplete cytoreduction. Tumor nodules from colorectal and gastric cancer often invade the mesentery where the blood vessels enter the small bowel and this can be especially problematic to resect the tumor nodules without full-thickness injury to the bowel. Once the small bowel is inspected completely, a decision is made to perform resections while leaving adequate bowel length for normal nutritional function and minimizing the number of anastomoses. In colorectal and gastric cancer, the present data demonstrated that the complete cytoreduction rate in patients with SB-PCI ≤ 3 was significantly higher (85.6%, 15/118) than that in patients with SB-PCI ≤ 4 (32.3%, 20/42). In appendiceal neoplasm patients, CC-0,-1 resection rate was significantly higher in patients with SB-PCI ≤ 6 (209/265, 79%) than that in those with SB-PCI ≥ 7 (19/155, 12%). Accordingly, the SB-PCI thresholds for the complete cytoreduction were ≥3 for colorectal and gastric cancer and ≥6 for appendiceal neoplasm. Esquivel et al. reported that there is no surgical option to remove all affected sites of small bowel even if there is evidence of intestinal obstruction at more than one site [
PCI score demonstrated its significant influence on survival, and a PCI score capable of serving as a threshold for favorable versus poor prognosis has been reported. In colorectal cancer, the survival results were significantly better when the PCI was lower than 16 [
Recently, neoadjuvant intraperitoneal/systemic chemotherapy improves survival results in gastric cancer. Patients who progress or develop extra-abdominal metastases during neoadjuvant chemotherapy may be excluded from an aggressive CRS [
The authors have no financial interest related to the contents of this paper to disclose.