Safety of Laparoscopic Oncologic Resection in Elderly Patients with Colorectal Cancer: A Multicenter Retrospective Study Based on Perioperative Short-Term Outcomes

Abstract

Objectives:

Over the last century, unthinkable goals have been achieved in health care and medical sciences, leading to longer life expectancy. Although cancer affects all ages, it disproportionately targets older individuals. Thus, surgical oncologists are confronted with increasing numbers of older patients presenting with multiple chronic conditions. We intended to investigate the safety of oncologic resection in older patients with colorectal cancer (CRC) based on perioperative outcomes.

Materials and Methods:

We retrospectively collected and analyzed data from older patients (>85 years) who underwent curative resection for stage II or III CRC between January 2007 and August 2017 at four hospitals (St. Vincent's Hospital, Incheon St. Mary's Hospital, Seoul St. Mary's Hospital, and Yeouido St. Mary's Hospital).

Results:

A total of 140 patients were enrolled in this study. The mean age was 87.1, the mean stay in the intensive care unit after surgery was 1.6 ± 3.8 days, and the mean postoperative hospital stay was 10.5 ± 3.8 days, D3 lymph node dissection was performed in 67.0% of patients, and D2 lymph node dissection was performed in 33.0%. Postoperative complications occurred in 38 patients (27.9%). In the univariate analysis, the risk factors for postoperative complications were the omission of mechanical bowel preparation (P = .039) and open surgery (P = .031).

Conclusions:

Oncologic resection in selected older patients with CRC might be a relatively safe treatment option. In particular, a laparoscopic approach might be a safer surgical method than open surgery in older patients with CRC.

Introduction

Colorectal cancer (CRC) is the third most common cancer worldwide and has the same incidence in Korea.^1,2 Currently, human lifespan has increased, and the proportion of the world's population older than 60 will double from ∼11% to 22% between 2000 and 2050.³ The number of elderly patients with CRC has increased gradually over the past decade.⁴ In the United States, about 40% of CRC occurred in patients aged 65–79 years and 19% of those in patients older than 80 years.⁵

Surgery is still the main treatment for CRC whenever possible. In older patients, surgery is associated with a higher rate of postoperative morbidity and mortality depending on the patient's reserve capacity and presence of underlying diseases, therefore, the clinicians must weigh the benefits of oncologic resection and the risks of postoperative morbidity and mortality that might be worse in terms of patient survival and quality of life. There is some conflict about the treatment of CRC in older patients. Several studies have concluded that old age is a negative prognostic factor.^6,7 In contrast, several studies have demonstrated surgery can be performed safely in selected elderly patients with acceptable morbidity and cancer-specific survival.^8–10

Laparoscopic surgery for CRC was first performed in 1991.¹¹ Since then, laparoscopic surgery has been widely used to treat CRC patients. Currently, it is accepted that laparoscopic surgery for CRC has the advantage of less blood loss, earlier bowel movement, shorter hospital stay, and lower complication rates than open approaches with similar oncologic outcomes.^12,13 There are several studies that have compared the outcomes of laparoscopic surgery with those of open surgery in older patients.^14–17 Most of these studies concluded that laparoscopic surgery for CRC can be performed safely in older patients. However, most previous studies defined older patients as those >65 or 80 years.

Older patients can be classified into three categories: (1) patients between 65 and 75 years of age; (2) patients between 76 and 85 years of age; and (3) patients older than 85 years of age.¹⁸ According to the data from the Life Tables of the United States in 2014, the life expectancies of patients who are older than 85 years were reported to be 7.1 years in women and 6.0 years in men.¹⁹ Therefore, considering life expectancy, short-term perioperative outcomes may be more important after oncologic resection for patients older than 85 years. Additionally, it needs to be clarified whether oncologic resection is necessary in these patients. In our studies, we focused on patients with CRC older than 85 years to evaluate the safety of oncologic resection based on short-term perioperative outcomes and to evaluate the safety of laparoscopic surgery in these patients.

Methods

Patient enrollment

We retrospectively reviewed medical records from four medical centers at Catholic University of Korea (Seoul St. Mary's Hospital, Yeouido St. Mary's Hospital, Incheon St. Mary's Hospital and St. Vincent's Hospital) from January 2007 to December 2017. A total of 140 patients were enrolled in this study. The eligibility criteria included patients over the age of 85 who underwent oncologic resection for stage II and III CRC.

Ethics

After obtaining Review Board approval from the Catholic University of Korea Catholic Medical Center CMC Clinical Research Coordination Center (IRB No. XC18REDI0030K), we retrospectively analyzed the data and clinical information from these 140 patients.

Definitions

Tumor location was classified into three groups: right-sided colon, left-sided colon, and rectum. A right-sided colon tumor was defined as a tumor located in the appendix, cecum, ascending colon, hepatic flexure colon, or proximal transverse colon; a left-sided colon tumor as a tumor was defined as a tumor located in the distal transverse colon, splenic flexure colon, descending colon, sigmoid colon, or rectosigmoid junction colon; and a rectal tumor was defined as a tumor located within 12 cm from anal verge. Colon obstruction by a tumor was clinically defined as symptoms including abdominal pain, distension, and no stool or flatus passage and was radiologically defined as severe dilatation of the colon proximal to the obstructive lesion. Emergency surgery was defined as surgery performed within 24 hours after patient's first visit to our hospital. In addition, complete preoperative bowel preparation was defined as the patient taking 4 L of polyethylene glycol (PEG) electrolyte solution and without complaint of any gastrointestinal symptoms afterward. Minimally invasive surgery included a single port or multiple ports for laparoscopic surgery and robotic surgery, and combined resection was defined as resection of an adjacent organ during the resection of the primary lesion, regardless of en bloc resection. In terms of lymph node dissection, ligation of the central vessel root around superior mesenteric artery in right-sided colon cancer or the aorta in left-sided colon cancer or rectal cancer was defined as D3 lymph node dissection, and limited vessel ligation was defined as D2 lymph node resection. The 7th edition of the AJCC was applied for description of pathological staging. Recovery time was defined as the earliest postoperative day on which all of the following criteria were met: tolerance of diet for 24 hours, free ambulation, afebrile status without major complications (>37.2°C axillary temperature), and a drain-free state. The Clavien-Dindo scale was used to evaluate the severity of postoperative complications.²⁰ Urinary retention was defined as a patient requiring reinsertion of an indwelling urinary catheter after previous removal during routine postoperative care. Surgical site infections were evaluated by the CDC classification of surgical wound infections.²¹

Data collection

Data collected included patient demographics, individual past history of other malignancy, tumor location, surgical approach (laparoscopy or open), postoperative morbidity and mortality, postoperative recovery time, pathological findings, and postoperative hospital stay.

Outcomes

The primary outcome was the safety of oncologic resection for patients older than 85 years based on short-term perioperative outcomes. In addition, we secondarily intended to identify the differences in perioperative outcomes between open and minimally invasive surgery (MIS) approaches and to determine the patterns and risk factors related to postoperative morbidity in these patients.

Statistical analysis

To compare the variables, pair t-tests were used for continuous variables, and the chi-square test was used for categorical variables. Statistical significance was defined as P ≤ .05. All statistical analyses were performed using the Statistical Package of the Social Sciences (SPSS) version 15.0 for Windows (SPSS, Inc., Chicago, IL).

Results

The mean age was 87.1 ± 2.3 years. Most patients (73.6%) had an American Society of Anesthesiologist (ASA) classification of class II. Eighteen patients (12.9%) underwent emergency surgery. Primary tumors were located in the right colon in 53 (37.9%) patients, in the left colon in 54 (38.6%) patients, and in the rectum in 28 (20%) patients. One hundred and nineteen patients (73.6%) underwent MIS, and 3 (2.1%) of these patients underwent conversion to open surgery. D3 lymphadenectomy was performed in 60 patients (42.9%), and 15 patients (10.7%) underwent combined resection. Intraoperative complications occurred in 7 patients; 5 patients had massive bleeding from injury to major vessels, one minimal burn of the left ureter, and one small bowel injury. Severe complications greater than Clavien-Dindo grade 3 after surgery occurred in 9 (6.4%) patients. The mean stay in the intensive care unit (ICU) after surgery was 1.6 ± 3.8 days, and the mean postoperative hospital stay was 10.5 ± 6.1 days. Three patients (2.1%) died within 30 days after surgery.

In the univariate analysis, the risk factors for postoperative complication were the omission of mechanical bowel preparation (47.9% versus 23.9%, P = .039), emergency surgery (50% versus 24.6%, P = .045), obstruction (48.0% versus 28.1%, P = .031), and open surgery (46.7% versus 22.9%, P = .034). In this study, the range of lymph node dissection, combined resection with adjacent organs, and the location of the tumor were not risked factors for postoperative complications (Table 1). When comparing the postoperative complications according to surgical approach, we found that open surgery tended to be associated with more frequent postoperative complications than MIS, and the difference was statistically significant (46.7% versus 22.6%, P = .020). In particular, postoperative pulmonary complications (10% versus 0.9%) and severe complications greater than grade III Clavien-Dindo complications occurred more frequently after open surgery than after MIS (16.7% versus 3.8%, P = .025). In terms of postoperative complications, postoperative ileus (9.3%) and urinary retention (7.9%) were the most common complications. In particular, postoperative cardiopulmonary complications occurred more frequently after open surgery than after MIS (10.0% versus 0.9%) (Table 2).

Table 1.

Univariate Analysis for Morbidity in Patients Aged 85 Years or Older with Colorectal Cancer Who Underwent Surgery

	Complication (−), N = 98	Complication (+), N = 38	P
Age (years)
Mean ± SD	87.13 ± 2.26	86.95 ± 2.37	.674
Sex
Male	34 (69.4%)	15 (30.6%)
Female	64 (73.6%)	23 (26.4%)	.691
ASA classification
1	11 (73.3%)	4 (26.7%)
2	74 71.8%)	29 (28.2%)
3	12 (75.0%)	4 (25.0%)
4	1 (50.0%)	1 (50.0%)	.83
BMI (kg/m²)
Mean ± SD	22.38 ± 3.44	21.84 ± 3.65	.433
Cancer history
No	85 (69.7%)	37 (30.3%)
Yes	9 (90.0%)	1 (10.0%)	.28
Tumor location
Right-sided colon	34 (66.7%)	17 (33.3%)
Left-sided colon	39 (73.6%)	14 (26.4%)
Rectum	21 (75.0%)	7 (25.0%)
Multiple	4 (100%)	0	.182
Obstruction
No	82 (75.9%)	26 (24.1%)
Yes	13 (52.0%)	12 (48.0%)	.031
Perforation
No	93 (72.7%)	35 (27.3%)
Yes	5 (62.5%)	3 (37.5%)	.686
Emergency surgery
No	89 (75.4%)	29 (24.6%)
Yes	9 (50.0%)	9 (50.0%)	.045
Preoperative bowel preparation
No	12 (52.2%)	11 (47.8%)
Yes	86 (76.1%)	27 (23.9%)	.039
Operation method
Open	16 (53.3%)	14 (46.7%)
MIS	81 (77.1%)	24 (22.9%)	.034
Lymph node dissection
D2	19 (67.9%)	9 (32.1%)
D3	46 (76.7%)	14 (23.3%)	.439
Combined resection
No	88 (72.7%)	33 (27.3%)
Yes	10 (66.7%)	5 (33.3%)	.761
Intraoperative complications
No	93 (72.1%)	36 (27.9%)
Yes	5 (71.4%)	2 (28.6%)	1
Postoperative stay in the ICU (days)
Mean ± SD	1.14 ± 1.20	2.65 ± 6.71	.037
Foley catheter removal
Yes	93 (73.8%)	33 (26.2%)
No	0	2 (100%)	.073
Postoperative hospital stay (POD)
Mean ± SD	9.42 ± 4.59	13.36 ± 8.35	.001
Pathologic TNM stage
1	16 (88.9%)	2 (11.1%)
2	41 (64.1%)	23 (35.9%)
3	41 (75.9%)	13 (24.1%)	.083

ASA, American Society of Anesthesiologist; BMI, body mass index; ICU, intensive care unit; MIS, minimally invasive surgery; POD, postoperative days; SD, standard deviation.

Table 2.

Postoperative Complications According to the Surgical Approach

	Open (N = 14)	Laparoscopy (N = 24)	Total (N = 38)
Ileus	4 (13.3%)	9 (8.5%)	13 (9.3%)
Urinary retention	4 (13.3%)	7 (6.6%)	11 (7.9%)
Bleeding	2 (6.7%)	3 (2.8%)	5 (3.5%)
Cardiopulmonary	3 (10.0%)	1 (0.9%)	4 (2.8%)
Anastomosis leakage	1 (3.3%)	2 (1.9%)	3 (2.1%)
Neurologic	1 (3.3%)	1 (0.9%)	2 (1.4%)
Surgical site infection	0	2 (1.9%)	2 (1.4%)

When comparing the postoperative outcomes of open surgery and MIS (Table 3), patients who were treated with open surgery had a longer stay in the ICU after surgery (3.46 versus 1.02, P = .002) and a longer hospital stay (14.21 versus 9.39, P < .001). All 3 patients who died within 30 days after surgery were in the open surgery group. The pathological characteristics of the tumor and pathological stage, which are surrogate factors for long-term outcomes, were not different in both groups. The resection margins and number of harvested lymph nodes were adequate in both groups, but patients in the open approach group had more harvested lymph node than those in the MIS group (29.81 versus 22.25, P = .04).

Table 3.

Comparison of Patient Demographics and Postoperative Outcomes According to the Surgical Approach

	Open (N = 33)	Laparoscopy (N = 107)	P
Age	87.19 ± 1.61	87.03 ± 2.44	.729
Sex
Male	10 (20.4%)	39 (79.6%)
Female	23 (25.3%)	68 (74.7%)	.659
ASA classification
1	3 (20.0%)	12 (80.0%)
2	19 (18.4%)	84 (81.6%)
3	8 (47.1%)	9 (52.9%)
4	1 (50.0%)	1 (50.0%)	.052
BMI (kg/m²)	22.27 ± 3.3	22.23 ± 3.5	.78
Cancer history
No	26 (21.1%)	97 (78.9%)
Yes	4 (40.0%)	6 (60.0%)	.232
Preoperative bowel preparation
No	16 (69.6%)	7 (30.4%)
Yes	15 (13.2%)	99 (86.8%)	<.001
Lymph node dissection
D2	11 (35.5%)	20 (64.5%)
D3	18 (30.0%)	42 (70.0%)	.639
Combined resection
No	28 (22.4%)	97 (77.6%)
Yes	5 (33.3%)	10 (66.7%)	.567
Intraoperative complication
No	30 (23.1%)	100 (76.9%)
Yes	1 (14.3%)	6 (85.7%)	1.000
TNM stage
1	5 (26.3%)	14 (73.7%)
2	15 (23.1%)	50 (76.9%)
3	12 (21.8%)	43 (78.2%)	.922
Harvested lymph nodes	29.81 ± 15.89	22.25 ± 11.35	.004
Metastatic lymph nodes	3.16 ± 9.91	1.10 ± 2.25	.049
PRM (cm)	21.48 ± 26.22	14.76 ± 11.46	.043
DRM (cm)	8.73 ± 6.54	10.25 ± 7.66	<.001
Postoperative ICU stay (days)	3.46 ± 7.44	1.02 ± 1.08	.002
Flatus passing (POD)	3.69 ± 2.05	2.97 ± 1.64	.21
Recovery of time (POD)	6.36 ± 1.96	5.67 ± 3.59	.555
Foley catheter removal
Yes	25 (19.7%)	102 (80.3%)
No	1 (50.0%)	1 (50.0%)	.364
Postoperative complications
No	16 (16.3%)	82 (83.7%)
Yes	14 (36.8%)	24 (63.2%)	.002
Clavien-Dindo scale
I and II	25 (19.7%)	102 (80.3%)
III or more	5 (55.6%)	4 (44.4%)	.025
Reoperation within 30 days after surgery
No	16 (14.8%)	92 (85.2%)
Yes	2 (50.0%)	2 (50.0%)	.121
Mortality within 30 days after surgery
No	16 (14.5%)	94 (85.5%)
Yes	3 (100%)	0	.004
Postoperative hospital stay (POD)	14.21 ± 8.6	9.39 ± 4.61	<.001

ASA, American Society of Anesthesiologist; BMI, body mass index; DRM, distal resection margin; ICU, intensive care unit; POD, postoperative days; PRM, proximal resection margin.

Discussion

Due to the increase in the number of older patients with CRC, many studies have reported the outcomes of surgery in these patients. However, the criteria for defining the age of these older patients are not clear, and many studies used cutoff ages of 65–75 years. Our study focused on the age group of patients older than 85 years. It is true that elderly patients often have multiple comorbidities, and they face increased risks of postoperative morbidity and mortality. Large-scaled studies from France and the Netherlands showed that comorbidities and old age (more than 85 years and more 75 years, respectively) are risk factors for postoperative death.^6,7 In particular, a systematic review of rectal cancer surgery in elderly patients (>75 years old) showed significantly higher 30-day mortality risk in the elderly patients.⁹ Postoperative death affects the survival of older patients, especially during the first year. If older patients survive for 1 year after surgery, they may have the same overall cancer-related survival as younger patients.²² In a systematic review, the postoperative mortality rates in older patients (>85 years old) with CRC varied from 7.7% to 48.8%, which was ∼6.2 times the mortality rates of younger patients (<65 years old).²³ The common postoperative complications were pulmonary and cardiovascular complications, which occurred in ∼15% and 4% of patients, respectively. The authors demonstrated that about 3% of anastomosis leakage rate had no significant difference compared with younger patients. Postoperative complications occurred in ∼40% of older patients, and this complication rate was not significantly higher than that in younger patients. However, when complications occurred in older patients, they were more severe than in younger patients. In our study, the mortality rate was 2.1%. The overall postoperative complication rate was 27.1% but the severe complication rate, which was above grade III Clavien-Dindo classification, was only 6.4%. The most common complications were ileus (9.3%) and urinary retention (7.9%). Cardiopulmonary complications occurred in only 2.8% of patients, and anastomotic leakage occurred in 2.1% of patients. When compared to the results of previous studies, our results were the same but the rates of postoperative mortality and morbidity tended to be lower. However, there was a higher cardiopulmonary complication rate resulting from open surgery in our study. This might be due to the large abdominal incision needed for open surgery, which may have interfered in cardiopulmonary recovery and rehabilitation, such as deep breathing and early ambulation. Therefore, sufficient pain control and appropriate rehabilitation programs should be implemented for elderly patients undergoing oncologic resection for CRC, especially in patients undergoing open surgery.

In general, age is not the primary determining factor for surgical risk, although the physiologic status of the patient needs to be assessed.²⁴ However, patients should be made aware that emergency surgery carries an increased risk of complications.²⁵ Some reports have demonstrated that elderly patients who present with symptoms requiring emergent surgery have higher complication rates.^26,27 In the present study, obstructive symptoms, the omission of bowel preparation, emergency surgery, and open surgery were related to postoperative complications. However, obstruction was one of the indications for emergency surgery and a contraindication for bowel preparation; thus, both of these factors were related to postoperative complications. We may be able to conclude that emergency surgery and open surgery are risk factors for postoperative complications. This suggests that rehabilitation and preoperative resuscitation may be important, and bridges to surgery after preoperative resuscitation, such as metallic stent placement for obstructive colon cancer, should be considered in older patients with CRC.

Since laparoscopic colorectal surgery was first performed in 1990,¹¹ today laparoscopy is widely used and has become standardized. Laparoscopic surgery for CRC has advantages in terms of less blood loss, earlier bowel movements, shorter hospital stays, and lower complication rates than open approaches without compromising long-term oncologic outcomes. However, laparoscopic surgery was associated with a longer operative time than open surgery, which may have impacted the postoperative outcomes, especially in older patients. Several studies have evaluated the outcomes of laparoscopy compared to open surgery in older patients (older than 80 years) with CRC.^14–17 The results from these studies were similar to the abovementioned results. The median operative time in the laparoscopic group was longer than that in the open group, and blood loss in the laparoscopic group was less than that in the open group. The time to recovery (return of bowel function, ICU stay, and hospital stay) were shorter in the laparoscopic group. Patients in the open group tended to have more postoperative morbidity than those in the laparoscopic group. Some studies reported that the long-term outcomes, overall survival, and disease-free survival were not different between the laparoscopic and the open group.^14–16 However, most of these studies are retrospective and involve patients older than 80 years. Atsushi Ishibe and colleagues conducted a randomized study that compared laparoscopic surgery and conventional open surgery in patients 75 years or older with CRC (n = 200). Their results were similar to those of most studies in terms of the short-term and long-term outcomes.²⁸

In our study, when comparing the postoperative outcomes between the MIS group and the open group, patients in the MIS group had shorter recovery times (postoperative ICU stay, time to return of bowel function, and hospital stay) than those in the open group, and the differences were statistically significant. The postoperative complication rate, including severe complication greater than Clavien-Dindo grade III complications, was lower in the MIS group. In this study, long-term oncologic outcomes were not analyzed because the authors thought that in considering the life expectancy of this group of patients, the short-term perioperative outcomes might be more important in oncologic surgery. However, oncologic resection should be considered for these patients because patients can suffer from recurrence of disease. Therefore, we analyzed pathological finding as a surrogate of long-term oncologic outcomes. The pathological stage, appropriate number of harvested lymph nodes and length of the resection margins were not different between the open surgery and MIS groups.

There are several limitations of our study. First, this study did not provide details on the comorbidities of the patients, which is an important factor that affects postoperative morbidity. Second, this study did not directly compare the postoperative outcomes with those of younger patients; however, when compared with the results of previous studies the morbidity and mortality rates in this study were acceptable. Additionally, there was a considerable amount of missing data due to the nature of this retrospective study. However, to the best of our knowledge, this is the first analysis of the safety of oncologic resection in patients 85 years or older with CRC.

In conclusion, from our data, oncologic resection for patients 85 years old or older with CRC can be performed safely in selected patients. Additionally, minimally invasive surgery can be performed with better outcome in terms of faster recovery and lower postoperative morbidity than open surgery. We suggest that oncologic surgery should be considered as the first-line treatment approach for a selected older patient group with CRC.

Footnotes

Disclosure Statement

The authors have no conflict of interest or financial ties to disclose.

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