Abstract
Background:
This retrospective study aimed to compare the short- and long-term surgical outcomes of laparoscopic surgery versus open surgery in elderly patients with rectal cancer.
Patients and Methods:
Elderly patients (≥70 years old) with rectal cancer who received radical surgery were retrospectively analysed. Patients were matched (1:1 ratio) using propensity score matching (PSM), with age, sex, body mass index, American Society of Anesthesiologists score and tumour-node-metastasis staging included as covariates. Baseline characteristics, post-operative complications, short- and long-term surgical outcomes and overall survival (OS) were compared between the two matched groups.
Results:
Sixty-one pairs were selected after PSM. Patients with laparoscopic surgery had a longer duration of operation time, lower estimated blood loss, shorter duration of post-operative analgesics administered, time to first flatus, time to first oral diet and post-operative hospitalisation stay than those observed in patients with open surgery (All P < 0.05). The incidence of post-operative complications in the open surgery group was numerically higher than that occurred in the laparoscopic surgery group (30.6% vs. 17.7%). Median OS was 67.0 months (95% confidence interval [CI], 62.2–71.8) in the laparoscopic surgery group and 65.0 months (95% CI, 59.9–70.1) in the open surgery group, however, Kaplan–Meier curves indicated that no significant differences in OS (Log-rank test, P = 0.535) were noted between the two matched groups.
Conclusions:
Compared with the open surgery, laparoscopic surgery had the advantages of less trauma and faster recovery, and provided similar long-term prognostic outcome in elderly patients with rectal cancer.
Keywords: Elderly patients, laparoscopic surgery, open surgery, rectal cancer, surgical outcomes
INTRODUCTION
Colorectal cancer is the third most commonly diagnosed cancer in the world. According to a survey conducted by the World Health Organization, about 1.4 million people worldwide were diagnosed with colorectal cancer in 2012, and one-third of these patients were found in the rectum.[1] Population aging has been a common phenomenon in developing countries. With the increase in the proportion of elderly and long-lived people, the proportion of elderly patients with rectal cancer is also raising.[2] Among population aged 75 years and over in China, the new cases of colorectal cancer are about 78,200/year, accounting for 18.08% of the global incidence of colorectal cancer.[3]
Radical surgical resection has been the primary option for the treatment of rectal cancer and has considered to be feasible and effective. Laparoscopic surgery for the treatment of colorectal carcinoma has been widely applied in the clinical practice for its advantages of small trauma, fast recovery and short hospitalisation.[4-6]
Several vital clinical trials and large-scale systematic reviews have demonstrated that colorectal cancer patients treated with laparoscopic surgery have the similar short-and long-term efficacy compared with those with open surgery.[7-12] Majority of elderly patients have multiple chronic diseases, such as cardiovascular disease, hypertension, diabetes mellitus and so on. These comorbidities might injure body function and significantly increased the risk of surgery. Nevertheless, whether laparoscopic surgery for exclusive elderly patients with rectal cancer could obtain long-term survival benefits or not still remains unknown. The elderly (age >70 years old) has been demonstrated to be an independent predictive factor for increased risk of post-operative complications, which represents a more fragile patient population and results in longer hospitalisation time and higher post-operative mortality.[13-15] Therefore, this study aimed to use propensity score matching (PSM) to compare the short- and long-term surgical outcomes of laparoscopic surgery and open surgery in elderly patients with rectal cancer aged 70 and older.
PATIENTS AND METHODS
Patients
This retrospective study analysed the clinical data of elderly patients with rectal cancer who underwent radical surgery in the General Surgery Department, First Hospital of Lanzhou University between February 2014 and October 2018. The inclusion criteria were: (1) age ≥70 years; (2) pathologically diagnosed as primary rectal cancer; (3) received laparoscopic surgery or open surgery for the radical treatment and (4) adequate organ function. The exclusion criteria were listed as follows: (1) emergency that required surgery for the reason such as bleeding, perforation or intestinal obstruction; (2) palliative surgery; (3) treated by pre-operative neoadjuvant therapy; (4) patients with surgical contradictions and (5) patients who converted to the open surgery during the laparoscopic surgery.
This study was approved by the ethics committee and Institutional Review Board of First Hospital of Lanzhou University and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.
Clinical data collection
The clinical data of all patients were retrospectively collected from the medical records.
The demographic baseline included age, sex, body mass index (BMI), American Society of Anesthesiologists (ASA) score, tumour distance from the anal verge (TDAV), previous abdominal surgery and comorbid diseases. Comorbidity was evaluated using the Charlson Comorbidity Index (CCI).[16]
Accordingly, the intraoperative indicators were also collected, such as the duration of operation, estimated blood loss and modes of anastomosis. The post-operative pathological staging was performed based on the 8th edition of tumor-node-metastasis (TNM) cancer staging system, developed by the International Union for Cancer Control (TNM) cancer staging system. The indicators for post-operative recovery were comprised of the duration of post-operative analgesics administrated, time to first flatus, time to first oral feeding, post-operative hospital stay, post-operative complications and post-operative 30-day mortality.
Follow-up and survival data
After surgery, all patients underwent regular outpatient follow-up visits every 3 months for the initial 3 years. During the first 3 years after surgery, the patients received consultation, physical examination, tumour biomarker examination at each scheduled visit; chest, abdominal and pelvic computed tomography/magnetic resonance imaging every 6 months; and colonoscopy every 12 months. After the initial 3 years, the patients were followed up every 6 months through outpatient visits, telephone or home visit until death due to recurrence and/or metastasis of rectal cancer.
Statistical analysis
On the basis of surgical strategy, patients were classified into the open surgery group and the laparoscopic surgery group, respectively. A multivariate logistic regression model was used to calculate the propensity score of each patient and decrease the selection bias between the two groups. The matching ratio was set as 1:1, with age, gender, BMI, ASA and TNM staging included as covariates. The distributions of continuous variables were analysed by Kolmogorov–Smirnov test. Normally distributed data were shown as mean ± standard deviation and compared by the Student’s t-test. Non-normally distributed data were indicated as median (interquartile range) and analysed using the Mann–Whitney U-test. Counting variables were shown as frequencies and were analysed using Chi-square test or Fisher’s exact test if appropriate. Survival analysis was assessed by the Kaplan–Meier method and Log-rank test. The SPSS 20.0 (IBM, Armonk, NY, USA) was used for all the statistical analyses. Two-sided P < 0.05 were considered statistically significant.
RESULTS
Patient characteristics
A total of 732 patient with rectal cancer who received radical surgery in the First Hospital of Lanzhou University were enrolled. Among them, 272 patients aged ≥70 years old, including 87 patients with open surgery and 185 patients with laparoscopic surgery. Finally, 62 pairs were selected through PSM. The clinical demographics and pathological characteristics of the open surgery group and the laparoscopic surgery group after PSM are presented in Table 1. After PSM, the clinical characteristics with respect to age, sex, BMI, ASA and TNM staging were balanced between the two groups. The mean age of patients was 5.2 ± 4.9 and 76.1 ± 3.8 years old in the open surgery and the laparoscopic group, respectively. The proportion of patients who had received previous abdominal surgery was similar between the two groups. The distribution of comorbid conditions based on CCI was also comparable in these two matched groups.
Table 1.
Clinical demographics and pathological characteristics of the elderly patients with rectal cancer after propensity score matching
| Variables | Matched cohorts | P | |
|---|---|---|---|
|
| |||
| Open surgery (n=62), n (%) | Laparoscopic surgery (n=62), n (%) | ||
| Age (years) | 75.2±4.9 | 76.1±3.8 | 0.225 |
| Sex | |||
| Female | 23 (37.1) | 23 (37.1) | 0.999 |
| Male | 39 (62.9) | 39 (62.9) | |
| BMI | 23.7±1.2 | 23.6±1.1 | 0.629 |
| ASA | |||
| 2 | 31 (50.0) | 30 (48.4) | 0.673 |
| 3 | 25 (40.3) | 23 (37.1) | |
| 4 | 5 (8.1) | 8 (12.9) | |
| TMN* | |||
| I | 5 (8.1) | 7 (11.3) | 0.832 |
| II | 26 (41.9) | 27 (43.5) | |
| III | 25 (40.3) | 24 (38.7) | |
| IV | 5 (8.1) | 3 (4.8) | |
| Previous abdominal surgery | 29 (47.5) | 26 (42.6) | 0.585 |
| CCI | |||
| 0 | 14 (22.6) | 15 (24.2) | 0.936 |
| 1 | 18 (29.0) | 19 (30.6) | |
| 2 | 21 (33.9) | 22 (35.5) | |
| 3 | 6 (9.7) | 4 (6.5) | |
| 4 | 2 (3.2) | 1 (1.6) | |
*Assessed based on the 8th edition of UICC TNM staging system. SD: Standard deviation, BMI: Body mass index, ASA: American Society of Anesthesiologists, TNM: Tumor nodes metastasis, CCI: Charlson comorbidity index, UICC: Union for International Cancer Control
Short-term surgical outcomes
Patients who received the laparoscopic group had a significantly longer duration of operation time (204 ± 18 min vs. 192 ± 25 min, P = 0.003) and lower estimated blood loss (117 ± 52 ml vs. 142 ± 43 ml, P = 0.004) than those indexes observed in patients with open surgery. Compared with the open surgery group, the duration of post-operative analgesics administered (1.28 ± 0.55 days vs. 1.80 ± 0.51 days), time to first flatus (65.12 ± 13.09 h vs. 83.51 ± 10.74 h) and time to first oral diet (3.59 ± 0.62 days vs. 4.56 ± 0.51 days) were significantly shorter than those in the laparoscopic group (All P < 0.001). The post-operative hospitalisation stay of the patients with laparoscopic surgery was 10.25 ± 1.92 days, which was significantly shorter than that reported in patients with the open surgery (11.91 ± 2.15 days) (P < 0.001). The proportion of patients receiving miles operations in the open surgery group was numerically higher than that observed in the laparoscopic surgery group (19.4% vs. 16.1%). On the other hand, the sphincter preservation rate was relatively lower in the patients with open surgery, however, there showed no significant difference between the two groups [Table 2].
Table 2.
Short-term surgical outcomes of elderly patients with rectal cancer in matched groups
| Variables | Open surgery (n=62) | Laparoscopic surgery (n=62) | P |
|---|---|---|---|
| Duration of operation time (min), mean±SD | 192±25 | 204±18 | 0.003 |
| Estimated blood loss (mL), mean±SD | 142±43 | 117±52 | 0.004 |
| Mode of anastomosis, n (%) | |||
| Miles | 12 (19.4) | 10 (16.1) | 0.823 |
| Dixon | 45 (72.6) | 48 (77.4) | |
| Hartmann | 5 (8.1) | 4 (6.5) | |
| Duration of post-operative analgesics administered (day), mean±SD | 1.80±0.51 | 1.28±0.55 | <0.001 |
| Time to first flatus (h), mean±SD | 83.51±10.74 | 65.12±13.09 | <0.001 |
| Time to first oral diet (day), mean±SD | 4.56±0.51 | 3.59±0.62 | <0.001 |
| Post-operative hospitalisation (day), mean±SD | 11.91±2.15 | 10.25±1.92 | <0.001 |
SD: Standard deviation
Post-operative complications
Overall, the incidence of post operative complications in the open surgery group was higher than that reported in the laparoscopic surgery group (30.6% vs. 17.7%), but there was no significant difference between the two groups (P = 0.093), as shown in Table 3. Compared with the laparoscopic surgery group, patients treated with open surgery had higher occurrence rats of paralytic ileus (6.5% vs. 1.6%) and wound infection (4.8% vs. 1.6%), however, the differences showed no statistically significance (All P > 0.05). Four patients (6.5%) in the open surgery group and three patients (4.8%) in the laparoscopic surgery group experienced pneumonia. Three (4.8%) patients and two (1.6%) patients occurred acute cardiac failure in the open surgery and the laparoscopic surgery group, respectively. However, the proportions of post-operative pneumonia and acute cardiac failure did not show a significant difference between the two groups.
Table 3.
Post-operative complications of elderly patients with rectal cancer in matched groups
| Post-operative complications | Open surgery (n=62), n (%) | Laparoscopic surgery (n=62), n (%) | P |
|---|---|---|---|
| Total | 19 (30.6) | 11 (17.7) | 0.093 |
| Minor complications | |||
| Paralytic ileus | 4 (6.5) | 2 (1.6) | 0.680 |
| Wound infection | 3 (4.8) | 1 (1.6) | 0.619 |
| Pneumonia | 4 (6.5) | 3 (4.8) | 0.999 |
| Acute cardiac failure | 3 (4.8) | 2 (1.6) | 0.999 |
| Major complications | |||
| Anastomotic leakage (Dixon) | 1 (1.6) | 2 (3.2) | 0.999 |
| Intraluminal bleeding (Dixon) | 2 (1.6) | 1 (1.6) | 0.999 |
| Wound dehiscence | 2 (1.6) | 0 | 0.496 |
| 30 days mortality | 0 | 0 | - |
In addition, a major complication occurred in 5 patients with open surgery (anastomotic leakage [Dixon], n = 1; intraluminal bleeding [Dixon], n = 2; wound dehiscence, n = 2) and 3 patients with laparoscopic surgery (anastomotic leakage [Dixon], n = 2; intraluminal bleeding [Dixon], n = 1), respectively. No death was reported within 30 days after the operation in either group.
Tumour location and preventative ostomy in elderly rectal cancer patients with Dixon operation
There were 45 (72.6%) and 48 (77.4%) patients received Dixon operation in the open surgery and the laparoscopic surgery group, respectively. As illustrated in the Table 4, the overall proportion of preventative ostomy in patients with laparoscopic surgery was higher than that in those with open surgery (6/45 [25.0%] vs. 12/48 [13.3%]) in elderly patients with rectal cancer who received Dixon operation, especially in those with TDAV <5 cm and TDAV 5–10 cm, however, the difference between the two groups did not show statistically significant (P = 0.155).
Table 4.
Tumour location and preventative ostomy in elderly rectal cancer patients with Dixon operation
| Open surgery (n=45), n (%) | Laparoscopic surgery (n=48), n (%) | P | |
|---|---|---|---|
| TDAV <5 cm | 10 (27.0) | 19 (39.6) | 0.079 |
| Preventive ostomy | 4 (40.0) | 10 (52.6) | 0.700 |
| TDAV 5–10 cm | 23 (51.1) | 13 (27.1) | 0.017 |
| Preventive ostomy | 2 (8.7) | 2 (15.4) | 0.609 |
| TDAV >10 cm | 12 (26.7) | 16 (33.3) | 0.484 |
| Preventive ostomy | 0 | 0 | - |
TDAV: Tumour distance from the anal verge
In those with TDAV <5 cm, 10 (27.0%) patients in the open surgery group and 19 (39.6%) patients in the laparoscopic group received Dixon operation, respectively, without significant difference between the two matched groups (P = 0.079). In addition, for those with TDAV of 5–10 cm, 23 (51.1%) patients received open surgery and 13 (27.1%) patients received laparoscopic surgery, suggesting that open surgery might be the preferred option in this patient population (P = 0.017). In elderly rectal cancer patients receiving Dixon operation, the proportion of those with TDAV >10 cm was comparable between the two matched groups (26.7% vs. 33.3%; P = 0.484).
Survival analysis
The mean follow-up period of all 124 patients was 57.6 months (range, 53.4–61.8), with 56.4 months (range, 52.1–60.7) in the open surgery group and 58.7 months (range, 54.7–62.8) in the laparoscopic surgery group. Seventy patients (56.5%; 34 patients in the laparoscopic surgery group and 36 patients in the open surgery group) died during the entire follow-up period. Median overall survival (OS) was 67.0 months (95% confidence interval [CI], 62.2–71.8) in the laparoscopic surgery group and 65.0 months (95% CI, 59.9–70.1) in the open surgery group, respectively. The Kaplan–Meier curves indicated that no significant difference (Log rank test, P = 0.535) was observed in OS between the two matched groups [Figure 1].
Figure 1.
Kaplan–Meier curves for OS in the two matched groups. OS: Overall survival
DISCUSSION
Prior studies had demonstrated that laparoscopic surgery had the comparable long-term efficacy compared with open surgery for the treatment of colorectal tumours.[4,17] Due to the small trauma of laparoscopic colorectal surgery, the post-operative stress level of patients was relatively low, and post-operative C-reactive protein and interleukin-6 levels were lower than those observed in those with open surgery.[18] Elderly patients might benefit from this minimally invasive procedure. However, considering the long operation time, the reduced cardiac output and risk of post-operative atelectasis induced by pneumoperitoneum, the application of laparoscopic surgery in elderly patients was still limited.
Radical surgery is the mainstream treatment for patients with rectal cancer. However, with the increase of age, the body’s reserve capacity gradually decreases. Devoto et al.[19] indicated that among patients who received surgery for the treatment of colorectal cancer, even if there was no obvious underlying comorbidity, the post-operative mortality and complication rate significantly increased in those aged ≥70 years old. Arenal-Vera et al.’s[20] also suggested that 30-day mortality rate of elderly patients (≥70 years old) with colorectal cancer who underwent surgery was about 6%, and approximately 20% elderly patients had at least one post-operative complication.
Prior studies had demonstrated that laparoscopic rectal surgery showed prominent advantages due to its minimally invasive nature compared with open surgery. The patients treated with laparoscopic surgery had less intraoperative blood loss and post-operative pain, faster recovery of gastrointestinal function, earlier first anal exhaust and shorter hospital lengths of stay.[21-23] The similar phenomenon was also confirmed in elderly rectal cancer patients with laparoscopic surgery in our study. However, laparoscopic surgery required a longer operation time than open surgery, and there showed a statistical difference between the two groups (204 min vs. 192 min; P = 0.003). Akiyoshi et al.[24] also found that operation time in elderly patients ≥75 years) undergoing laparoscopic rectal resection was longer than those receiving open rectal resection (256 min vs. 196 min). This indicated that surgeons still have to spend a long time to perform and complete the laparoscopic surgery, and the anaesthesia time of patients with laparoscopic surgery might be longer. However, the mean difference in operation time between the two matched groups was only 20 min in the current study. That is to say, with the development of the technology and the improvement of the surgeon’s proficiency, the operation time gap between laparoscopic surgery and open surgery has been gradually narrowing.
In our study, no significant difference in post-operative complications was observed between the two matched groups. The proportion of anastomotic leakage in the laparoscopic surgery group was numerically higher than that in the open surgery group; however, the occurrences of incision-related complications and paralytic ileus tended to be higher in the open surgery group. The proportion of cardiopulmonary complications was similar between the two matched groups. No death was reported within 30 days after the operation in either group, which was in line with previous findings in similar studies.[19,23,24] There might exist more cardiopulmonary complications after surgery in elderly patients, which is associated with the reduced cardiopulmonary reserve and fragile ability to withstand surgical strikes.
Overall, the proportion of patients with Dixon operation in the laparoscopic surgery group was higher than that in the open surgery group, and the sphincter preserving rates between the two groups were similar. However, in elderly rectal cancer patients with Dixon operation, we found that those with TDAV <5 cm were prone to receive laparoscopic surgery. The location of the tumour might be an important reason for the surgeon’s treatment choice. In patients with low tumour location, surgeons preferred to select laparoscopic surgery. The magnifying effect and fine operation in narrow space could help surgeons to complete the mission during the laparoscopic surgery. In patients with open surgery, the tumour location was relatively high, and anastomosis after resection was easy to achieve, which might be contributed to the low anastomosis-related complications in those with open surgery. However, patients with low rectal cancer made it difficult to reinforce the suture after anastomosis. The uncertainty of surgery in low rectal cancer also drove surgeons to choose preventive ostomy more often to balance and make up for the shortcomings. Thus, in our study, patients treated with laparoscopic surgery had a higher proportion of preventive ostomy than those with open surgery.
Patients in either group were followed for a long period, with an average follow-up of 57.6 months (range, 53.4–61.8 months). The Kaplan–Meier curves revealed that no significant differences in OS (Log-rank test, P = 0.535) were observed between the two matched cohort, supporting similar long-term prognosis between the two surgical strategies. Our results revealed that laparoscopic rectal cancer surgery had significant short-term advantages versus open surgery in elderly patients aged 70 and older, mainly including reduced trauma and pain, and fast recovery, which was consistent with the findings observed in younger patients.[10,25] Therefore, age is not a restricted factor for laparoscopic surgery. With the improvement of surgical techniques, the advantages of laparoscopic techniques will become more prominent. In our study, when elderly patients were classified based on tumour location, those with low rectal carcinoma were more likely to gain benefits from the laparoscopic surgery.
The current study had some potential limitations. First, this is a retrospective study conducted at a single medical centre and the sample size was limited. Second, comorbidity was not included as a covariate of PSM and the choice of laparoscopic or open surgery is subjective to surgeons’ preference or discretion, which might induce some potential bias.
CONCLUSIONS
Compared with the open surgery, laparoscopic surgery had the advantages of less trauma and faster recovery and provided similar long-term prognostic outcomes in elderly patients with rectal cancer aged 70 and older.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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