Abstract
Background/Aim: Previous studies have shown that laparoscopic colorectal cancer surgery is highly safe and effective compared to laparotomy. However, whether laparoscopic colorectal cancer surgery can be safely performed in patients with severe comorbidities remains unclear. The aim of this study was to evaluate the safety of laparoscopic colorectal cancer surgery in patients with severe comorbidities. Patients and Methods: A total of 82 consecutive patients with colorectal cancer who underwent laparoscopic surgery were retrospectively divided into two groups according to whether they had severe comorbidity (50 patients) or non-severe comorbidity (32 patients). An age-adjusted Charlson comorbidity index of ≥6 was defined as severe comorbidity. Results: Operative time, blood loss, and rate of conversion to laparotomy did not differ between the groups. Postoperative complications and the length of the postoperative hospital stay also did not differ significantly between the groups. Conclusion: Laparoscopic colorectal cancer surgery is feasible and safe, even in patients with severe comorbidities.
The safety of laparoscopic colorectal cancer surgery has been demonstrated by randomized controlled trials (RCTs) over the past 20 years (1-3). Laparoscopic surgery is characterized by less postoperative pain, reducing the need for analgesic agents, fewer wound-related complications, and a shorter hospital stay than laparotomy (1, 3). The indications for laparoscopic colorectal cancer surgery have gradually been expanded to include advanced cancer as well as early cancer (1, 4, 5), obese patients (6), and patients with a history of laparotomy (7). Laparoscopic surgery is now widely recognized as a very safe and effective standard treatment for colorectal cancer as compared with laparotomy (8). However, the safety of laparoscopic colorectal cancer surgery in patients with severe comorbidities remains unclear.
Because laparoscopic surgery is generally performed with pneumoperitoneum in patients in the Trendelenburg position, adverse hemodynamic and respiratory effects, such as increased systemic vascular resistance, decreased ejection fraction, and increased respiratory compliance have been reported (9). Patients with severe comorbidities were, therefore, generally excluded from randomized controlled studies (1, 2), and adequate evidence supporting the safety of laparoscopic surgery in such patients is lacking. Our group recently obtained similar short-term results for laparoscopic surgery and laparotomy in patients with severe comorbidities (10). The question, therefore, arises whether the good short-term results obtained after laparoscopic surgery in patients without severe comorbidity are retained in patients with severe comorbidity.
The Charlson Comorbidity Index (CCI) is based on 19 comorbid conditions, each of which is assigned a weighted score (11) and has been validated as an effective predictor of outcomes in patients with colorectal cancer (12, 13). The age-adjusted CCI (ACCI) is a modification that considers age as an additional comorbid factor (14) (Table I). Several studies have shown that it is a useful tool for predicting both short- and long-term outcomes in patients with various types of cancer (15-18). A previous study reported that an ACCI score of ≥6 indicates severe comorbidity (10, 15, 16).
In the present study, the safety and outcomes of laparoscopic surgery in patients with colorectal cancer who had severe comorbidities were compared with those in a similar cohort of patients without severe comorbidities who underwent surgery during the same period. ACCI was used to categorize the patients according to the severity of comorbidity.
Age-adjusted Charlson Comorbidity Index.
Patients and Methods
Patient enrollment. The study group comprised consecutive patients with colorectal cancer who had severe comorbidities and underwent primary surgical resection in a university teaching hospital from April 2004 through March 2016. A total of 317 patients underwent primary resection of their colorectal tumors during that period. A total of 233 patients were excluded because they underwent laparotomy, and 2 patients were excluded because of multiple organ resection. The 82 remaining patients were then divided into two groups according to whether the ACCI was ≥6, which was considered to indicate severe comorbidity (50 patients, 61.0%), or <6, considered to indicate non-severe comorbidity (32 patients, 39.0%) (Figure 1).
The indications for performing laparoscopic surgery rather than laparotomy were not standardized, but were generally based on surgical experience, patient preference, and tumor size. Patient data, which included information on the preoperative assessment, operative outcomes, and postoperative complications, were entered into a prospective database and reviewed retrospectively.
All study protocols were approved by our institutional review board (No. B170700003). The details of the study protocol were provided to the patients by means of a notice board in the hospital and were published in the hospital website.
Perioperative management. The perioperative management of patients was similar in both groups. The patients underwent bowel preparation with polyethylene glycol electrolyte solution and began an oral diet on the third day after surgery. All patients received intravenous cefmetazole from immediately before starting the operation until the day after the operation. Deep venous thrombosis prophylaxis included a perioperative antiembolic stocking and intraoperative pneumatic calf compression for patients without peripheral vascular disease. Postoperative complications were evaluated according to the Clavien-Dindo classification (19). The criteria for patient discharge in both groups included tolerance of an oral diet without nausea or vomiting, passage of flatus and stool, and sufficient recovery from any postoperative complications.
Consort diagram. ACCI: Age-adjusted Charlson Comorbidity Index.
Operative techniques. All operations were performed or directly supervised by any of 6 experienced colorectal surgeons. For the laparoscopic procedures, first access to the abdomen was usually achieved via the umbilical port. Once pneumoperitoneum was established, 4 additional ports were placed. Vessel ligation with lymph-node dissection was performed, followed by mobilization of the colon. The specimen was extracted via a 4- to 6 cm umbilical incision. Bowel anastomosis was performed intracorporeally with the double-staple technique for colorectal anastomosis, and extracorporeally at the extraction site for ileocolic and colo-colonic anastomoses. For open colorectal resection, a midline laparotomy was the access point of choice. Mobilization of the colon was followed by ligation of the vessels, bowel resection, and bowel anastomosis. Any incision longer than >8 cm was considered a conversion to open surgery in this study.
Statistical analysis. Patient characteristics, operative findings, and postoperative results were compared between the two groups. Comparisons between the laparoscopic and laparotomy group were made on an intent-to-treat basis. Chi-square and Fisher's exact tests were used to compare categorical variables. Student's t-test was used to compare continuous variables. All statistical analyses were performed using the EZR software program (20) (Jichi Medical University, Saitama, Japan). All p-values are 2-sided, and p-values less than 0.05 were considered to indicate statistical significance.
Results
The demographic characteristics of the two groups are presented in Table II. There were significant differences in age (75 vs. 67 years, p<0.01), the American Society of Anesthesiologists (ASA) physical status classification (p<0.01), cardiovascular disease (27 vs. 9, p=0.04), diabetes mellitus (12 vs. 1, p=0.03), and serum albumin levels (4.1 vs. 4.4 g/dl, p<0.01) between the two groups.
Demographic characteristics (n=82).
The operative outcomes of the two groups are summarized in Table III. Operative time (250 min vs. 239 min, p=0.71) and blood loss (42 g vs. 60 g, p=0.21) did not differ between the groups. The rate of conversion to laparotomy was 8.0% (4 patients) in the severe comorbidity group and 6.3% (2 patients) in the non-severe comorbidity group (p=1.00). The reasons for conversion to laparotomy were tumor invasion to an adjacent structure in 3 patients, and severe intra-abdominal adhesion in 1 patient in the severe comorbidity group and tumor invasion to an adjacent structure in 1 patient, and severe intra-abdominal adhesion in 1 patient in the non-severe comorbidity group. There was no conversion to laparotomy caused by physiological intolerance to pneumoperitoneum or the Trendelenburg position in either group. There were no significant differences in postoperative complications (10% vs. 16%, p=0.50), the details of complications, or the length of the postoperative hospital stay (10 days vs. 10 days, p=0.18) between the two groups. There was no mortality in either group.
Discussion
Several RCTs have demonstrated that laparoscopic colorectal cancer surgery is superior to laparotomy in terms of short-term outcomes (1, 2, 8, 21, 22), and laparoscopic colorectal cancer surgery is regarded as a standard procedure. However, the number of RCTs is limited, and the literature lacks sufficient information on the outcomes of patients with severe comorbidities who underwent laparoscopic surgery. Patients with severe comorbidities, such as circulatory and pulmonary impairment (1, 22), liver and renal dysfunction, advanced age (≥76 years) (1), high BMI, distant metastasis (2), and severe medical illness (21) were excluded from previous RCTs. Laparoscopic colorectal cancer surgery was safe in patients with severe comorbidities and was associated with a lower rate of overall operative complications than laparotomy (10). However, the safety of laparoscopic colorectal cancer surgery in patients with severe comorbidities as compared with patients without severe comorbidities remains to be fully evaluated. The aim of the present study was to clarify the safety of laparoscopic colorectal cancer surgery in patients who have severe comorbidities as compared with patients who have non-severe comorbidities.
Operative outcomes (n=82).
Few studies have compared the safety of laparoscopic colorectal cancer surgery between patients with severe comorbidities and patients with non-severe comorbidities. Some studies reported that the short-term results of laparoscopic colorectal cancer surgery were similar in patients with severe comorbidities and patients with non-severe comorbidities. Ichikawa et al. (23) used the ASA score to assess the severity of comorbidities in patients who underwent resection of colorectal cancer and then compared the complication rates among 3 groups: a laparoscopic surgery group with an ASA score of 3 (LAP3), a laparoscopic surgery group with an ASA score of <2 (LAP2), and an open surgery group with an ASA score of 3 (OP3). They found that the total complication rate in the LAP3 group was similar to that in the LAP2 group and concluded that laparoscopic colorectal resection can be performed safely in patients with severe comorbidities. Tashiro et al. (24) stratified patient comorbidity according to the ASA score (ASA1, ASA2-3, or ASA4) and compared the short-term results after laparoscopic resection for colorectal cancer. They reported that the incidence of postoperative complications did not differ significantly among the groups. Kazama et al. (25) classified patients who underwent laparoscopic surgery for colorectal cancer into two age groups and demonstrated that postoperative complications and the length of the hospital stay were similar in patients who were 75 years or older and non-elderly patients who were younger than 75 years. Thus, few previous studies have shown that the short-term results of laparoscopic colorectal cancer surgery in patients with severe comorbidities are similar to those in patients with non-severe comorbidities, and the short-term results in patients with severe comorbidities have not been fully evaluated. In addition, previous studies selected patients with severe comorbidities on the basis of only age or only ASA. It is necessary to assess severe comorbidities with the use of a tool that reflects the general conditions of the study group.
The ACCI is not just a weighted measure that reflects the severity of the comorbidity, but it also considers age as an important risk factor that can be used to evaluate the patient's general physical condition. The present study used the ACCI to quantify baseline comorbidities and showed that the short-term results of laparoscopic colorectal cancer surgery in patients with severe comorbidities were as favorable as those in patients with non-severe comorbidities. The usefulness of ACCI has been reported by several previous studies. Park et al. (17) demonstrated that patients with an ACCI of ≥3 were at greater risk for systemic complications, which suggests that ACCI is a useful predictor of systemic complications after laparoscopic-assisted distal gastrectomy and can be used routinely for the perioperative care of elderly patients who have comorbidities. Tian et al. (16) suggested that the ACCI score positively correlates with the risk of prolonged postoperative ileus in colon cancer as well as rectal cancer. To the best of our knowledge, no previous study has used the ACCI to categorize preoperative comorbidities and compare the short-term results after laparoscopic colorectal cancer surgery between patients with higher and lower ACCI scores.
The short-term results of laparoscopic colorectal cancer surgery in patients with higher ACCI scores were similar to those in patients with lower ACCI scores, indicating that the safety of the procedure is not affected by the presence or absence of comorbidities. There were no significant differences in the rates of postoperative complications, the details of postoperative complications, or and the length of the postoperative hospital stay between the two groups. There was also no mortality in either group. However, several previous studies have shown that after laparotomy patients who were elderly and had severe comorbidities had more postoperative complications than patients without severe comorbidities (26, 27) in contrast to the results obtained in our laparoscopic cohort. Because laparoscopic surgery is a minimally invasive procedure, it could be safely performed regardless of the presence of systemic preoperative comorbidities. A meta-analysis of laparoscopically assisted colorectal surgery in elderly patients (28) reported that laparoscopic surgery reduced the rates of postoperative pneumonia, cardiac complications, and wound infection. There are several possible explanations for these results: tissue trauma, as reflected in the systemic cytokine response, has been reported to be milder after laparoscopic colorectal surgery than after laparotomy (29). Furthermore, reduced pain in the early postoperative period might improve ventilator status, lessen cardiac afterload, and enhance the resumption of normal activities. The decreased surgical stress associated with laparoscopic surgery is a factor contributing to a reduction in systemic complications in the early postoperative period (30).
Our study has several potential limitations. First, this study was retrospective and non-randomized in design. The choice of laparoscopic surgery or laparotomy was determined by an informed consultation between the surgeon and the patient. Therefore, the results of this study may not be generally applicable to all patients with severe comorbidities, but only to selected patients. The second limitation was the sample size. The present study collected data from a university teaching hospital over a 12-year period and identified 82 patients. Combined data from multiple centers are needed to confirm the results of the present study.
In conclusion, laparoscopic colorectal cancer surgery was considered feasible and safe, even in patients with severe comorbidities. A randomized retrospective study or large case-matched analysis is needed to confirm our results.
- Received April 23, 2018.
- Revision received May 15, 2018.
- Accepted May 16, 2018.
- Copyright© 2018, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved
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