Laparoscopic surgery improves postoperative outcomes in high-risk patients with colorectal cancer
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- Feroci, F., Baraghini, M., Lenzi, E. et al. Surg Endosc (2013) 27: 1130. doi:10.1007/s00464-012-2559-y
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Patients with significant comorbidities often are denied laparoscopic colorectal resections, because they are thought to be too “high-risk.” This study was designed to examine the feasibility and safety of laparoscopic colorectal resections in high-risk colorectal cancer patients and to compare them with a similar cohort of patients undergoing open resections in the same time period.
This was a single-center, prospective, cohort study conducted at a high-volume, nonuniversity, tertiary care hospital. From a database of 616 patients submitted to elective colorectal surgery for cancer within a fast-track protocol (January 2005 to November 2011), 188 patients who met at least one minor (age >80 years and body mass index (BMI) >30 m/kg2) and one major (cardiac, pulmonary, renal or liver disease, diabetes mellitus) criterion were classified as high-risk. Differences in baseline characteristics, intraoperative outcomes, and short-term (30-day) postoperative outcomes, as well as the pathology findings and the readmission and reoperation rates, were compared between the open and laparoscopic cohorts in both high- and low-risk groups and between high- and low-risk groups.
During the study period, 68 high-risk patients underwent laparoscopic resections and 120 had open surgeries. A shorter length of postoperative stay (6 vs. 9 days, p < 0.0001) and fewer postoperative nonsurgical complications (4 % vs. 19 %, p = 0.003) were observed among the laparoscopic group. Postoperative major (p = 0.774) and minor complications (p = 0.3) and reoperations (p = 0.196) were similar between the two groups, and a significantly lower rate of mortality (1.5 vs. 7.5 %, p = 0.038) was observed in the laparoscopic group than in the open group.
Laparoscopic colorectal resection can be safely performed on “high-risk” surgical patients with better results than a similar group of high-risk patients undergoing open colon resections.
KeywordsLaparoscopic colorectal surgeryHigh-risk patientsColorectal cancer
The feasibility of laparoscopic colectomy procedures, in terms of both safety and oncological radicality, has been reported since 1991 with data from several randomized trials [1–5]. These trials demonstrated that improvements in short-term postoperative results could be achieved without compromising long-term oncological results. The percentage of elective colectomies performed laparoscopically has increased over time; however, almost 90 % of cases are still performed open, and utilization continues to be influenced by several factors . In the western world, the percentage of laparoscopic colectomies among colectomies for benign diseases increased from 6.2 % in 2001–2003 to 11.8 % in 2005–2007, whereas those for colon cancer increased by a larger percentage, from 2.3 % to 8.9 % .
Patients with significant comorbidities often are denied laparoscopic colorectal resections, because they are thought to be too “high-risk” to tolerate abdominal insufflation, the extreme Trendelenburg position, and potentially lengthy surgery . Unfortunately, only 10–26 % of patients from previous, randomized, controlled trials [2–5] were categorized as ASA III or ASA IV, and no specific analyses were conducted on that subset of patients. There is a lack of information in the literature regarding the outcomes of high-risk patients undergoing laparoscopic colorectal surgery, and only a limited number of studies have tried to address the problem. Furthermore, risk factors have been defined differently, and no consensus on what constitutes risk factors has been reached [8–14].
In this study, we examined the feasibility and safety of elective laparoscopic colorectal resections in high-risk colorectal cancer patients and to compare them with a similar cohort of patients undergoing open resections during the same time period.
Population and study objectives
Institutional review board approval was obtained before the review of any patient materials. Our high-risk patient classification was defined by two minor criteria (patient age older than 80 years and body mass index (BMI) >30 m/kg2) and five major criteria (cardiac, pulmonary, renal or liver disease, and diabetes mellitus) . Patients who met at least one minor and one major criterion were classified as high-risk.
A prospectively maintained, divisional database of 616 consecutive R0 colorectal resections for cancer was used to identify high-risk patients between January 2005 and November 2011. The exclusion criteria included patients who were medically unfit for surgery, had undergone a nonresective procedure (i.e., transanal resection, colostomy, or bypass procedure), had any nonelective admission or preoperative evidence of distant metastases, were aged younger than 18 years, or were pregnant. For each patient, 92 parameters capturing patient demographics, preoperative diagnosis, intraoperative events, postoperative course, and follow-up assessment were documented on a standardized form.
Three colorectal fellowship-trained surgeons performed or supervised both the open and laparoscopic procedures, and these surgeons were involved in all of the operations. Surgical interventions were conducted as described previously . A right-sided hemicolectomy was performed through a right horizontal incision above the umbilicus (surgeon’s choice) in the open group. All other procedures were performed through a midline vertical incision that was extended as necessary. Laparoscopic right hemicolectomy with a total intracorporeal side-to-side anastomosis was performed using three 12-mm trocars in the left hemi-abdomen. The specimen was extracted from a 3-cm Pfannenstiel incision and protected by a plastic drape. A laparoscopic left hemicolectomy was executed using three 12-mm trocars in the right hemi-abdomen; however, a fourth 5-mm trocar was used for the anterior resection of the rectum (RAR). The colon was extracted from a 3-cm transverse laparotomy in the right abdomen. A loop ileostomy was executed at the end of low RARs using a 3-cm extraction laparotomy in the right hemi-abdomen. A 19-French suction drain was positioned at the surgeon’s discretion. The operating surgeon determined each patient’s suitability for a laparoscopic-assisted resection on a case-by-case basis, depending on his/her practice or the patient’s preference. Due to the current lack of consensus regarding the definition of conversion in laparoscopic colon surgery, we defined a laparoscopic-converted colon resection as the abortion of the laparoscopic approach and the performance of a conventional abdominal incision for completion of the operation. Any incision >6 cm also was considered a conversion to an open procedure.
Postoperative management and discharge criteria
Since the introduction of laparoscopic colon surgery at our institution, we have been using a “fast-track surgery” protocol, as previously published . The primary objective of this protocol is to reduce nonsurgical morbidity and to hasten patient recovery. A detailed protocol was prepared and distributed to all patients, department doctors (surgeons, anesthesiologists, and nutritionists), and nurses to standardize the treatment. A mechanical bowel preparation using a single dose of phosphate magnesium was administered only in patients who underwent rectal surgery. All patients were allowed clear liquids up to 4 h before surgery, and no premedication was administered. An antithrombotic prophylaxis was administered 12 h before the intervention and continued until 30 days after discharge. Antibiotic (cephazolin 2 g and metronidazole 500 mg, i.v.) prophylaxis was administered 30 min before interventions and repeated after 3 h if necessary. The nasogastric tube was always removed at the end of surgery, and hypothermia was prevented using a Bair Hugger and warmed intravenous fluids. Open surgery patients were given thoracic epidural catheters. All patients received 12 ml of 0.5 % bupivacaine followed by 4 ml per hour and an epidural dose of morphine (2 mg <70 years and 1 mg >70 years) intraoperatively. The epidural analgesia was continued during surgery and for 48 h with 0.25 % bupivacaine and morphine 0.05 mg/ml, 4 ml per hour. Laparoscopic surgery patients received Tramadol (300 mg), Ketorolac Tromethamine (90 mg), and Ondansetron (10 mg) using an intravenous elastomeric infusion pump with a constant flow (2 ml/h) for 48 h. Both groups received Paracetamol (2 g) every 12 h. Ketorolac Tromethamine (30 mg) was administered up to 3 times within 24 h when visual analog scale measurements were >50. The bladder catheter was removed from RAR patients on the second postoperative day in the absence of surgical complications and on the first postoperative day for all other cases. The suction drain was removed on the second postoperative day in the absence of surgical complications. After the procedure, patients were moved to an armchair in the evening. The next day, they were mobilized to the bathroom and were seated in an armchair for at least 2 h. On the second postoperative day, patients were encouraged to ambulate out of the room and to sit in an armchair for at least 8 h. Patients were allowed to drink water 3 to 6 h after the intervention and to take a semisolid diet on the first postoperative day. A solid diet was allowed on the second postoperative day.
Patients were discharged to home on day 3 postoperatively if the following criteria were met: no complications arose, the ability to tolerate at least three solid meals daily, a bowel movement and/or flatus, the ability to ambulate independently, and adequate pain control with the use of oral pain medication only.
All patients were given detailed postoperative instructions and a 24-hr contact phone number for a physician at the hospital. Patients residing more than 100 km from the hospital were advised to stay close to the hospital for at least 24 h after discharge. All patients had follow-up outpatient clinic visits 8 days after discharge, and at this visit, their pathology results were reviewed with them. Patients who developed fever, abdominal pain, vomiting, or other pertinent symptoms were readmitted for a workup.
Two different authors independently reviewed demographic, treatment, and outcome variables for accuracy. Differences in clinically important baseline characteristics, intraoperative outcomes, and short-term (30-day) postoperative outcomes, as well as the pathology findings (tumor characteristics, lymph node retrieval), and the readmission and reoperation rates were compared between the open and laparoscopic cohorts in both high- and low-risk groups and between the high- and low-risk groups. Major surgical morbidities included anastomotic leaks, anastomotic strictures, internal hernias, and a fascial dehiscence with evisceration. Minor surgical complications included a transient partial small-bowel obstruction, an ileus, minor anastomotic bleeding, wound infections, wound hematomas, and hernias.
A univariate analysis was performed by using the Mann–Whitney U test for continuous variables, and the χ2 test was used for categorical variables. For all analyses, p values <0.05 were considered statistically significant, and all tests were two-sided. Univariate results are reported as the median (interquartile range) or the frequency (percent); only the ml of transfused blood result is reported as the mean (range). The data were analyzed on an intention-to-treat basis. The data were tabulated on a Microsoft® Excel spreadsheet (Excel for Windows®; Microsoft Corporation, Redmond, WA) and then processed with SPSS© 16.0 for Windows (SPSS Inc., Chicago, IL). p < 0.05 was considered statistically significant.
Baseline characteristics of high-risk patients
(n = 120)
(n = 68)
Sex ratio (M:F)
Previous abdominal operation
AJCC 2002 staging
Classification of high-risk patients
(n = 120)
(n = 68)
Age >80 year
BMI (kg/m2) >30
Major factors (comorbidity)
1 minor + 1 major
1 minor + 2 major
1 minor + 3 major
2 minor + 1 major
2 minor + 2 major
2 minor + 3 major
(n = 120)
(n = 68)
Splenic flexure resection
Gastric GIST removal
Lymph nodes harvested
Duration of surgery
Blood transfusion (ml)
Postoperative outcomes in the high-risk group: laparoscopic vs. open surgery
Short-term (30 days) outcome in all groups
High risk vs. low risk
(n = 120)
(n = 68)
(n = 168)
(n = 261)
First bowel movement pod
First flatus pod
First stool pod
Liquid diet toleration pod
Solid diet toleration pod
Drain removal pod
Bladder catheter removal pod
NGT tube reinsertion
Bladder catheter reinsertion
Analgesic administration (oral or IV) pod
Postoperative outcomes in laparoscopic patients: low-risk vs. high-risk patients
High-risk patients had a longer LOS (6 vs. 5 days, p = 0.015), more postoperative complications (35.3 vs. 17.2 %, p = 0.006), including anastomotic leakages (5.8 vs. 1.5 %, p = 0.046) and minor surgical morbidity (19.1 vs. 9.9 %, p = 0.003), and a higher reoperation rate (8.8 vs. 2.7 %, p = 0.007). Later stool canalization (4 vs. 3 days, p = 0.015), later bladder catheter removal (2 vs. 1 days, p = 0.001), and higher nasogastric tube reintroduction (11.7 vs. 3.8 %, p = 0.008) were observed in laparoscopic high-risk patients.
Postoperative outcomes in open patients: low-risk vs. high-risk patients
The outcomes in the two groups were similar except for a higher rate of nonsurgical morbidity for the high-risk patients (15.8 vs. 8.9 %, p = 0.006).
The major findings in this study are that laparoscopic resection for colorectal cancer can be performed with lower rates of mortality and morbidity than open surgery, both in low- and high-risk patient groups. These results show a significantly reduced length of hospital stay and a significantly enhanced recovery of patients’ mobility and feeding and gastrointestinal functions in the laparoscopic group compared with the open group.
High-risk patients will continue to represent an increasing percentage of a surgeon’s colorectal practice. Too often, however, laparoscopic colorectal procedures are not considered for this patient population due to fears about the safety of this minimally invasive approach, because the creation of the pneumoperitoneum with carbon dioxide is associated with potentially adverse pathophysiological changes, including hypercapnia, reduced venous return, increased peak airway pressure, and decreased pulmonary compliance [12, 17]. Although there are an increasing number of reports concerning laparoscopic colon surgery in the literature, only a limited number of studies address high-risk patients. Generally, most of the literature has shown that high-risk patients benefited from laparoscopic surgery more than from open surgery [8–14]. Considering these results, colorectal surgeons should not deny a laparoscopic approach to patients solely because of their high-risk status; they also should consider that previous reports have included only 20 to 70 patients with a mixture of both benign and malignant diseases and that different definitions were adopted for high-risk patients. For example, in those studies, age (>60, or between 70 and 80 years), obesity (BMI >30 kg/m2), radiotherapy, and ASA status were selected as high-risk criteria [8–14]. Although conventional elective procedures can be performed with acceptable mortality rates in octogenarians (although mortality rates are higher than in younger patients), the morbidity rates from major surgery remain considerable [18–20]. In previous studies, laparoscopy improved short-term postoperative outcomes more in the elderly than in younger patients. Patients with a body mass index (BMI) >30 have increased rates of wound and cardiorespiratory complications, anastomotic leaks, and prolonged hospital stays after conventional colorectal surgery and higher rates of conversion with laparoscopic colorectal surgery [21–24]. Laparoscopy also improved short-term postoperative outcomes more in elderly than in younger patients [25, 26], and BMI increased operative times without affecting short-term outcomes . In our laparoscopic patients, we observed only a slightly longer length of stay for patients older than 80 years, whereas a BMI >30 influenced the length of intervention only.
The ASA classification is a standard element of the anesthesiologist’s preoperative assessment of surgical patients worldwide . The goal of the system is to assess the overall physical status of the patient before surgery and not to assess surgical risk per se, because it neglects the impact of the surgery itself on the patient’s outcomes . The definitions of the six physical status classes are relatively straightforward and simple; the simplicity of these definitions is both the classification system’s strength and its weakness. It is easily applied and communicated, which makes it practical to use; however, the ASA Physical Status classification lacks specificity, which leads to inconsistent ratings between anesthesiologists and imprecise clinical interpretations [29–31]. For these reasons, the ASA classification was not used in this study.
Several aspects of our study merit discussion. First, the most important weakness of this study is the nonrandomization of cases; thus, this study has the same limitations of the majority of similar studies. Second, information about anesthetic complications during surgery in this group of high-risk patients was not available for comparison, and there was no information on whether some of the postoperative cardiopulmonary complications were the consequence of adverse anesthetic events. Third, we are aware that our fast-track protocol can influence results, but previous studies from our group suggest that within an enhanced recovery program, laparoscopic resections may provide the best short-term clinical outcomes for patients with resectable colorectal cancer . Fourth, our study reflects the experiences of only three practiced surgeons from the same unit; previous research has demonstrated that a surgeon’s skill, particularly in advanced laparoscopic surgery, has a significant impact on patient outcomes, and improved results are achieved after surgeons have completed a learning curve [24, 32–34]. As in a similar study , one of the strengths of this study is that it reports the total experience and results of the unit over a selected time period (high- and low-risk, open and laparoscopic).
Our results show that in experienced hands, laparoscopic colorectal resection can be performed safely on “high-risk” surgical patients. This subset of patients seems to have better results when treated laparoscopically than a similar group of high-risk patients undergoing open colon resections.
Francesco Feroci, Maddalena Baraghini, Elisa Lenzi, Alessia Garzi, Andrea Vannucchi, Stefano Cantafio, and Marco Scatizzi have no conflict of interest or financial ties to disclose.
There was no financial support for this study.