Feasibility and Safety of Laparoscopic Right Colectomy in Oldest-Old Patients with Colon Cancer: Results of the CLIMHET Study Group

Abstract

Background:

Laparoscopy for colorectal cancer treatment is widely accepted. However, there is no consensus as to whether or not laparoscopy can be considered the preferred treatment strategy in octogenarian and nonagenarian patients with colon cancer. The aim of this study was to compare operative and postoperative outcomes of laparoscopic right colectomy between oldest-old (≥80 years) and younger (<80 years) patients with colon cancer.

Methods:

The study population was sampled from the CLIMHET Study Group cohort. Between January 2005 and December 2015, data were retrieved for all patients who had undergone elective laparoscopic right colectomy for colon cancer in five University Hospital centers in France (CHU of Clermont-Ferrand, Hôpital Civil of Strasbourg—IRCAD, Hôpital Henri-Mondor of Créteil, Hôpital Européen Georges Pompidou of Paris, and CHRU of Tours).

Results:

Overall, 473 cancer patients were selected and analyzed. There were 156 oldest-old patients (median age: 84.1 years, range: 80–96) and 317 younger patients (median age: 67 years, range: 25–79). After adjusting based on propensity score on gender, obesity, American Society of Anesthesiologists score, smoking, arteriopathy, coronaropathy, comorbidity, and American Joint Committee on Cancer staging, no significant difference was found in operative and postoperative outcomes, except for time to resume a regular diet (3.6 days versus 3.0 days, P = .008) and length of hospital stay (12.1 days versus 9.1 days, P = .03), which were longer for oldest-old patients. Overall and disease-free survival rates were also equivalent between groups.

Conclusion:

These findings support that laparoscopic right colectomy can be safely performed in cancer patients aged 80 and older, and its outcomes are similar in oldest-old and younger patients.

Introduction

In developed countries, colorectal cancer is the second leading cause of cancer-related death in men and the third cause in women,¹ with a risk that increases with age and an incidence that peaks between the seventh and eighth decade.^2–4

The proportion of oldest-old people has substantially increased over recent years worldwide, and this growth is expected to accelerate in the coming decades. In particular, the group of individuals aged 80 and older, namely the “oldest-old” people, is increasing even faster than the number of old persons overall, with a projection of 202 million oldest-old people in 2030 and 434 million ones in 2050.^5,6 Consequently, an increasing number of individuals aged 80 and older are diagnosed with cancer and non-cancer pathologies, requiring surgical treatments every year,⁷ and an increasing number of surgical operations are performed in octogenarian and nonagenarian patients. However, an advanced age is associated with a higher American Society of Anesthesiologists (ASA) score, a higher cardiac and pulmonary comorbidity rate, a poorer nutritional status, and a reduced physiological reserve to cope with major surgery.^8–10

Several studies have reported the benefits of laparoscopic colorectal surgery compared to open surgery in elderly patients,^11–16 with recent reports describing good outcomes in octogenarians^17–19 and in very old patients with colorectal cancer.²⁰ However, despite a growing body of evidence supporting that laparoscopic outcomes in elderly patients with colorectal cancer are similar to those observed in younger patients,²¹ further studies are required to establish the optimal care strategy for the oldest-old population.^22–24

Because laparoscopy requires the induction of a pneumoperitoneum and often longer operative times, laparoscopic colorectal resection is not always recommended for oldest-old patients,²⁵ and the feasibility and safety of the whole procedure should be carefully considered.²⁶ In particular, the patient's general status and performance, the underlying pathology (e.g., malignant or benign), and the type of surgical procedure required (e.g., right or left colectomy) are the main factors to be taken into consideration before performing laparoscopic surgery in oldest-old patients.

This study aimed to describe the operative and postoperative outcomes of laparoscopic right colectomy performed in octogenarian and nonagenarian patients with colon cancer. To assess the feasibility and safety of laparoscopy, the outcomes observed in the oldest-old group (≥80 years old) were compared with those observed in younger patients (<80 years old) undergoing laparoscopic right colectomy for the same indication.

Materials and Methods

The study population was retrieved from the CLIMHET Study Group database, which includes patients undergoing laparoscopic right colectomy between January 2005 and December 2015 in five University Hospital centers in France (CHU of Clermont-Ferrand, Hôpital Civil of Strasbourg—IRCAD, Hôpital Henri-Mondor of Créteil, Hôpital Européen Georges Pompidou of Paris, and CHRU of Tours). Data were extracted from a retrospective database concerning exclusively the laparoscopic approach in right colectomies for benign and malignant pathologies. The study was conducted in accordance with the ethical principles ascertained in the Declaration of Helsinki.

For these analyses, we selected all patients who underwent an elective laparoscopic right colectomy for histologically proven colon cancer located in the ascending colon (from the ileocecal valve to the right colonic flexure). Patients with synchronous colon cancers, metastatic disease, locally advanced cancer requiring multivisceral resections, or who underwent reoperations for tumor recurrence were excluded. Based upon the patient's age at the time of surgery, the study population was divided into two groups: the oldest-old group (including patients aged 80 or older) and the younger group (including patients aged 79 or less).

Perioperative antiembolic stockings were applied for deep vein thrombosis prophylaxis. Laparoscopic right colectomies were performed as previously reported using a medial-to-lateral approach for radical operations.^27–30 The ileocolic anastomosis was performed either intracorporeally or extracorporeally.³¹ Conversion was defined as the completion of the right colectomy procedure through either an enlarged incision or an abdominal incision of ≥6 cm.

The following variables were analyzed: age, gender, body mass index (BMI), obesity (BMI >30), ASA score, smoking, diabetes, arteriopathy, coronaropathy, previous laparotomy, previous laparoscopy, comorbidity score in elderly patients (as described by Covinsky et al.³²), American Joint Committee on Cancer (AJCC) staging, lesion localization (e.g., cecum, ascending colon, right colonic flexure ( = hepatic flexure), and ileocecal valve), operative time, conversion rate, anastomotic characteristics (e.g., manual and extracorporeal), perioperative antibiotics, perioperative transfusion, and perioperative intravenous fluids. Postoperative morbidity and mortality were defined as events occurring during hospital stay or within 90 days after resection. Postoperative complications were categorized according to the Dindo–Clavien classification.³³ Surgical complications included prolonged ileus (>5 days with nasogastric tube), anastomotic leakage, anastomotic hemorrhage, wound infection, intra-abdominal abscess, bleeding, and evisceration. Nonsurgical complications included cardiac, vascular, and pulmonary ones. All complications were assessed by a clinician and were prospectively registered into databases at discharge or during the first outpatient visit. Postoperative outcomes included the following: reoperation rate, time to resume a regular diet, time before ambulation, time to flatus, time to the first stools, time before cessation of intravenous fluids l, intensive care unit (ICU) stay, length of hospital stay, and number of lymph nodes harvested.

Statistical analysis

For descriptive statistics, continuous variables are presented as median (range) and categorical variables as numbers and percentages. For bivariate two-sided comparisons between oldest-old and younger groups, a Mann–Whitney U test, a chi-squared test, or a Fisher's exact test was used. Binary, multimodal, and linear regression analyses were performed to control the effects of covariates on operative and postoperative outcomes, including, in the multivariate analysis, those variables that reached a significant P value in the univariate analyses. In addition, a multivariate analysis of demographic, clinical, and pathological variables was used to identify independent factors associated with the incidence of postoperative complications. Overall survival (OS) and disease-free survival (DFS) rates were computed using the Kaplan-Meier method and compared between groups using the log rank (Mantel–Cox) test. A P value <.05 was considered significant. Statistics were performed using the R software (version 3.2.0, R Core Team, R Foundation for Statistical Computing, Vienna, Austria).

Results

Out of a total of 637 patients of the CLIMHET Study Group database, 473 patients were selected and included in these analyses. All patients underwent an elective laparoscopic right colectomy for colon cancer. Demographic and clinical characteristics are reported in Table 1. The oldest-old groups presented with a lower proportion of male patients (45.5% versus 57.1%, P = .01), a higher ASA score (P = .0002), fewer smoking patients (5.1% versus 16.7%, P = .0002), and more arteriopathy and coronaropathy compared to the younger patients' group. Comorbidity score and AJCC staging were also significantly different between the two groups.

Table 1.

Demographic and Clinical Characteristics of Oldest-Old (≥80 Years) and Younger (<80 Years) Patients Undergoing a Laparoscopic Right Colectomy for Colon Cancer

	Oldest-old patients (n = 156)	Younger patients (n = 317)	P
Age, years, median (range)	84.1 (80–96)	67(25–79)	.0001
Male gender, n (%)	71 (45.5)	181(57.1)	.01
BMI, mean (SD)	24.4(3.4)	25.6(4.6)	.05
Obesity (BMI >30), n (%)	12 (7.7)	43 (13.6)	.06
ASA score, n (%)			.0002
I	0	44 (13.9)
II	23 (14.8)	234 (73.8)
III	111 (71.1)	36 (11.3)
IV	22 (14.1)	3 (1)
Smoking, n (%)	8 (5.1)	53 (16.7)	.0002
Diabetes, n (%)	34 (21.8)	60 (18.9)	.46
Arteriopathy, n (%)	64 (41.0)	97 (30.6)	.03
Coronaropathy, n (%)	49 (31.4)	53 (16.7)	.001
Previous laparotomy, n (%)	57 (36.5)	98 (30.9)	.25
Previous laparoscopy, n (%)	17 (10.9)	52 (16.4)	.11
Comorbidity score, n (%)			.0001
0	0 (0)	16 (5.0)
1	15 (9.6)	79 (24.9)
2–4	110 (70.5)	216 (68.1)
≥5	31 (19.9)	6 (1.9)
AJCC staging, n (%)			.01
0	5 (3.2)	38 (12.0)
I	40 (25.6)	74 (23.3)
IIa	64 (41.0)	103 (32.5)
IIb	7 (4.5)	9 (2.8)
IIc	3 (1.9)	3 (0.9)
IIIa	0 (0)	6 (1.9)
IIIb	31 (19.9)	64 (20.2)
IIIc	6 (3.8)	20 (6.3)
Lesion location, n (%)			.70
Cecum	64 (41.0)	122 (38.5)
Ascending colon	45 (28.8)	84 (26.5)
Hepatic flexure	33 (21.2)	73 (23.0)
Ileocecal valve	14 (9.0)	38 (12.0)

Values shown in bold denote a statistically significant value.

AJCC, American Joint Committee for Cancer; ASA, American Society of Anesthesiologists; BMI, body mass index.

Operative variables are outlined in Table 2. Both groups had similar operative times. No significant difference was found in the conversion rate and in the technical details of the surgical procedure, such as ileocolic anastomosis, perioperative antibiotics, transfusion, and administration of intravenous fluids. No significant difference was found when adjusting the P value for gender, obesity, ASA score, smoking, arteriopathy, coronaropathy, comorbidity score, and AJCC staging.

Table 2.

Operative Outcomes of Oldest-Old (≥80 Years) and Younger (<80 Years) Patients Undergoing a Laparoscopic Right Colectomy for Colon Cancer

	Oldest-old patients (n = 156)	Younger patients (n = 317)	P	Adjusted P value
Operative time, minutes, median (range)	207 (75–380)	210 (80–660)	.94	0.45
Conversion, n (%)	8 (5.1)	20 (6.3)	.68	0.70
Extracorporeal anastomosis, n (%)	120 (76.9)	238 (75.1)	.73	0.97
Perioperative antibiotic, n (%)	154 (98.7)	316 (99.7)	.25	0.50
Perioperative transfused patients, n (%)	8 (5.1)	12 (3.8)	.47	0.27
Perioperative blood transfusion, RBC unit, median (range)	0.09 (0–2)	0.07 (0–3)	.51	0.34
Perioperative intravenous fluids, mL, median (range)	1234 (750–5500)	1264 (500–5000)	.50	0.81

Adjusted for gender, obesity, ASA score, smoking, arteriopathy, coronaropathy, comorbidity score, and AJCC staging.

AJCC, American Joint Committee on Cancer; ASA, American Society of Anesthesiologists.

Postoperative outcomes are displayed in Table 3. Surgical complication rates were not different between the two groups (28.2% for oldest-old patients versus 20.8% for younger patients, P = .08). The most common complication in both groups was prolonged ileus (8.3% for the oldest-old group and 7.3% for the younger group). A significant difference was found in the incidence of nonsurgical complications, with a greater incidence of cardiac, vascular, and pulmonary complications in the oldest-old group (14.7% versus 7.6%, P = .02). However, this difference was no longer significant in the preoperative risk-adjusted analysis. The younger patients' group showed a shorter time to resume a regular diet (3.0 days versus 3.6 days, P = .007), a reduced time to first flatus (3.0 days versus 3.3 days, P = .02), and a reduced time before cessation of intravenous fluids (5.5 days versus 6.1 days, P = .004) compared to the oldest-old group. In addition, a shorter ICU stay (0.62 days versus 1.2 days, P = .04) and a shorter hospital stay (9.1 days versus 12.1 days, P = .0001) were observed in younger patients compared to oldest-old ones. However, only the time to resume a regular diet and the length of hospital stay remained significantly different in favor of the younger patients group in preoperative risk-adjusted analysis. A trend toward statistical significance was noted for the Dindo–Clavien classification of postoperative complications (P = .06). However, no group difference was noted when adjusting for covariates. The 90-day mortality and the number of lymph nodes harvested were also similar between groups.

Table 3.

Postoperative Outcomes in Oldest-Old (≥80 Years) and Younger (<80 Years) Patients Undergoing a Laparoscopic Right Colectomy for Colon Cancer

	Oldest-old patients (n = 156)	Younger patients (n = 317)	P	Adjusted P value^a
Surgical complications, n (%)	44 (28.2)	66 (20.8)	.08	.28
Ileus	13 (8.3)	23 (7.3)
Anastomotic leakage	6 (3.8)	10 (3.2)
Wound abscess	9 (5.8)	14 (4.4)
Intra-abdominal abscess	3 (1.9)	3 (0.9)
Bleeding	7 (4.5)	9 (2.8)
Evisceration	2 (1.3)	1 (0.3)
Nonsurgical complications, n (%)	23 (14.7)	24 (7.6)	.02	.54
Cardiac	15 (9.6)	12 (3.8)
Vascular	4 (2.6)	3 (0.9)
Pulmonary	12 (7.7)	11 (3.5)
Reoperation, n (%)	12 (7.7)	14 (4.4)	.16	.52
Time to resume regular diet, days mean (range)	3.6 (0–22)	3.0(0–17)	.007	.008
Time to resume ambulation, days mean (range)	1.5 (0–5)	1.2 (0–8)	.05	.90
Time to flatus, days mean (range)	3.3 (0–8)	3 (1–14)	.04	.51
Time to first stools, days mean (range)	4.5 (1–10)	4.4 (1–16)	.21	.20
Time before infusion therapy removal, days mean (range)	6.1 (1–18)	5.5 (1–23)	.004	.90
Intensive care unit stay, days [mean mean (range)	1.2 (0–26)	0.62 (0–16)	.04	.83
Length of hospital stay, days mean (range)	12.1 (4–56)	9.1 (3–39)	.0001	.03
Dindo–Clavien classification of complications, n (%)			.06	.71
0	64 (41.0)	166 (52.4)
I	42 (26.9)	86 (27.1)
II	32 (20.5)	40 (12.6)
III	9 (5.8)	17 (5.4)
IV	2 (1.3)	3 (0.9)
90-day mortality, n (%)	7 (4.5)	5 (1.6)	.07	.94
Lymph nodes harvested mean (range)	22 (6–57)	22 (3–77)	.89	.95

Values shown in bold denote a statiscially significant value.

Adjusted for gender, obesity, ASA score, smoking, arteriopathy, coronaropathy, comorbidity score, and AJCC staging.

AJCC, American Joint Committee on Cancer; ASA, American Society of Anesthesiologists.

Results of the univariate and multivariate analyses of factors associated with the incidence of postoperative surgical and nonsurgical complications are shown in Table 4. Diabetes, arteriopathy, operative times longer than 240 minutes, and transfusion were significantly associated with the incidence of postoperative surgical complications. Multivariate logistic regression analysis showed that all these factors were significant predictors of the incidence of postoperative surgical complications. Coronaropathy, comorbidity score, and AJCC staging were significantly associated with postoperative nonsurgical complications. On the contrary, the oldest age did not appear as an independent prognostic factor associated with postoperative surgical or nonsurgical complication.

Table 4.

Univariate and Multivariate Analysis of Factors Associated with Postoperative Complications

	Surgical complications				Nonsurgical complications
Factors	Incidence of complications (n)	P value of univariate analysis	P value of multivariate analysis	Odds ratio (95% CI)	Incidence of complications (n)	P value of univariate analysis	P value of multivariate analysis	Odds ratio (95% CI)
Age		.08				.02
<80 years (reference)	66				24
≥80 years	44				23
Gender		.12				.76
Male (reference)	66				24
Female	44				23
ASA score		.11				.65
I, II (reference)	63				27
III, IV	47				20
Obesity		.99				.80
BMI ≤30 (reference)	97				6
BMI >30	12				40
Smoking		.74				.07
No (reference)	95				45
Yes	15				2
Diabetes		.01	.05	2.21 (1.18–4.13)		.08
No (reference)	97				14
Yes	13				33
Arteriopathy		.004	.03	1.62 (1.16–3.35)		.19
No (reference)	85				20
Yes	25				27
Coronaropathy		.99				.008	.04	2 (1.02–4)
No (reference)	86				18
Yes	24				29
Previous laparotomy		.99				.25
No (reference)	74				19
Yes	36				28
Previous laparoscopy	91	.36			42	.51
No (reference)	19				5
Yes
Comorbidity score		.15				.0001	.01	5.7 (1.3–24.2)
0–1 (reference)	19				2
≥2	91				45
AJCC staging		.20				.02	.01	2.17 (1.16–4.16)
0-I (reference)	42				23
II-III	68				24
Conversion		.11
No (reference)	100
Yes	10
Operative time		.002	.02	1.85 (1.11–2.95)		.99
<240 minutes (reference)	67				34
≥240 minutes	43				13
Perioperative transfused patients		.02	.03	2.85 (1.19–6.6)	46	.34
No (reference)	101				1
Yes	9

Values shown in bold denote a significant result.

AJCC, American Joint Committee on Cancer; BMI, body mass index; CI, confidence interval.

Median follow-up time for the whole study population was 36 months (range: 1–121). OS and DFS are displayed in Figures 1 and 2. OS of the oldest-old group was comparable to the one of the younger patients' group. Survival rates were as follows: 98% at 1 year, 95% at 3 years in the oldest-old group versus 97% at 1 year, and 93% at 3 years in the younger patients' group (P = .15), respectively. DFS rates were as follows: 94% at 1 year, 89% at 3 years in the oldest-old group versus 96% at 1 year, and 92% at 3 years in the younger patients' group (P = .29), respectively.

FIG. 1.

Overall survival.

FIG. 2.

Disease-free survival.

Discussion

In a large cohort of patients with colon cancer, this study shows that laparoscopic right colectomy can be safely performed in oldest-old patients as in younger ones. Operative and postoperative variables are comparable between the two groups of age, although time to resume regular diet and length of hospital stay are longer in the oldest-old patients' group. However, being octogenarian or nonagenarian does not appear to be a predictor of postoperative surgical and nonsurgical complications.

Nowadays, laparoscopic surgery is considered the gold standard approach for colon cancers and it is also gaining widespread application for rectal cancers.^34–37 However, in elderly patients, laparoscopy is still a matter of controversy,³⁸ and several studies indicated that an increasing age is an independent predictor of increased surgical mortality,^39–43 whereas other studies supported that age per se has a minimal effect on surgical morbidity and mortality risks.^{20,26,39–42,44}

Due to the global aging process and particularly to the fact that people aged 80 and older are growing faster than any younger segment of the population, abdominal surgeons deal with oldest-old patients almost everyday.⁵ Octogenarian and nonagenarian patients undergo an increasing number of surgical operations performed every year,^7,26,45 and they represent a surgical challenge because of the association with multiple comorbidities and with reduced physiological reserves and tolerance to stress.^26,38,43 In addition, the use of laparoscopy has been associated with the risk of adverse hemodynamic effects related to pneumoperitoneum induction in patients with limited cardiopulmonary reserve. At present, this drawback seems to be limited. Recent studies observed an improved OS in elderly patients operated on with laparoscopy as opposed to open surgery,^46,47 and the possibility to work with low intra-abdominal pressures may contribute to minimize this risk.³⁸

This study confirms that the oldest-old population is more vulnerable than younger patients, presenting with a higher comorbidity score and particularly with more cardiovascular pathologies (e.g., arteriopathy and coronaropathy). However, the operative outcomes of laparoscopic right colectomy are not different between groups, supporting the feasibility and safety of laparoscopy even in octogenarian and nonagenarian patients. Of note, the conversion rate was similar in both age groups and no conversion to open surgery was required due to anesthesia problems related to the pneumoperitoneum.

Overall postoperative morbidity, including surgical and nonsurgical complications, and 90-day mortality were equivalent between the oldest-old patients' group and the younger patients' group when adjusting for gender, obesity, ASA score, smoking, AJCC staging, and comorbidities. Independent predictors significantly associated with postoperative surgical complications were as follows: diabetes, arteriopathy, operative time ≥240 minutes, and perioperative blood transfusion. For nonsurgical complications, the significant predictors were as follows: coronaropathy, high comorbidity score, and advanced AJCC staging. These predictors were already observed in previous studies,^{9,20,45,48,49} while age was not significantly associated with postoperative morbidity.⁴⁸ This highlights the critical concept that the age factor cannot be simply considered the chronological age of the patient, rather, it should include the complete evaluation of the patient's physical, mental, and functional health to assess the related risk for postoperative adverse events. Similarly, the age threshold to define the elderly population has been a matter of debate and has been progressively increased over the last decades.^{19,39,43,49–55} In this study, we decided to evaluate the feasibility and safety of laparoscopic right colectomy in oldest-old patients, a specific age category, which necessarily emerged from the global increase in life expectancy. As observed in other studies conducted in elderly populations (75 years and older),^20,48,49 also in this study, the quality of the aging process (e.g., presence of comorbidity), rather than the chronological age of the patient, appears to be the critical factor predicting surgical outcomes.

With respect to short-term postoperative outcomes, the oldest-old patients' group showed significantly longer times to resume a regular diet and a longer length of hospital stay compared to the younger patients' group. These longer times may result from a slower return to gastrointestinal functions, a more intense postoperative pain and fatigue, and a lower physical reserve, which can be expected in octogenarian and nonagenarian patients. Conversely, long-term outcomes showed similar overall and DFS rates.

This study has strengths and limitations. The study population is a homogeneous cohort of patients operated on for colon cancer using laparoscopic right colectomy only. This is rarely found in the literature where most studies evaluated colon and rectal cancer together, which, however, require different treatments (e.g., chemoradiotherapy) and surgical interventions. Notwithstanding, caution should be taken to interpret and generalize these findings. The CLIMHET database involved five University Hospitals and included patients who underwent a laparoscopic right colectomy only. No comparative evaluation with open surgery for colon cancer in oldest-old patients could be performed. In addition, due to the long time interval considered, the impact of therapeutic protocols, such as adjuvant chemotherapy, could not be assessed and selection bias cannot be ruled out. All surgeons involved in the study were highly experienced in laparoscopic surgery, and for every patient, indication for surgery was determined after discussion in multidisciplinary meetings. As a result, operative and postoperative outcomes cannot be directly generalized to low-volume, nontertiary, or nonuniversity centers. Further studies should be conducted to assess the impact of specific therapeutic protocols in combination with laparoscopic colectomy in the specific subset of elderly patients.

Conclusion

Laparoscopic right colectomy can be safely performed in oldest-old patients with colon cancer with operative outcomes that are comparable to those observed in younger patients. Postoperatively, the oldest-old patients' group recovers more slowly than the younger patients' group. However, age per se does not appear to be a significant predictor of postoperative surgical and nonsurgical complications. Nevertheless, the presence of comorbidities, especially cardiovascular ones, and their severity impact on postoperative outcomes should be attentively evaluated preoperatively to assess the patient's risk.

Footnotes

Disclosure Statement

No competing financial interest exists.

References

Rosso

, Malvezzi

, Bosetti

, Bertuccio

, Negri

, La Vecchia

. Cancer mortality in Europe, 1970–2009: An age, period, and cohort analysis. Eur J Cancer Prev, 2018; 27:88–102.

Yamauchi

, Lochhead

, Morikawa

, et al. Colorectal cancer: A tale of two sides or a continuum?. Gut, 2012; 61:794–797.

Stepien

, Gluszek

, Koziel

, Kaczmarczyk

. The risk of surgical treatment in patients aged 85+, with special consideration of colorectal cancer. Pol Przegl Chir, 2014; 86:132–140.

Hermans

, van Schaik

, Prins

, Ernst

, Dautzenberg

, Bosscha

. Outcome of colonic surgery in elderly patients with colon cancer. J Oncol, 2010; 2010:865908.

Wimo

, Winblad

, Aguero-Torres

, von Strauss

. The magnitude of dementia occurrence in the world. Alzheimer Dis Assoc Disord, 2003; 17:63–67.

United Nations, Department of Economic and Social Affairs, Population Division. World Population Ageing 2015 (ST/ESA/SER.A/390). 2015. Available at: http://www.un.org/en/development/desa/population/publications/pdf/ageing/WPA2015_Report.pdf (last accessed September 10, 2018).

Hamel

, Henderson

, Khuri

, Daley

. Surgical outcomes for patients aged 80 and older: Morbidity and mortality from major noncardiac surgery. J Am Geriatr Soc, 2005; 53:424–429.

Senagore

, Madbouly

, Fazio

, Duepree

, Brady

, Delaney

. Advantages of laparoscopic colectomy in older patients. Arch Surg, 2003; 138:252–256.

Manceau

, Karoui

, Werner

, Mortensen

, Hannoun

. Comparative outcomes of rectal cancer surgery between elderly and non-elderly patients: A systematic review. Lancet Oncol, 2012; 13:e525–e536.

10.

Frasson

, Braga

, Vignali

, Zuliani

, Di Carlo

. Benefits of laparoscopic colorectal resection are more pronounced in elderly patients. Dis Colon Rectum, 2008; 51:296–300.

11.

Tuech

, Pessaux

, Rouge

, Regenet

, Bergamaschi

, Arnaud

. Laparoscopic vs open colectomy for sigmoid diverticulitis: A prospective comparative study in the elderly. Surg Endosc, 2000; 14:1031–1033.

12.

Stocchi

, Nelson

, Young-Fadok

, Larson

, Ilstrup

. Safety and advantages of laparoscopic vs. open colectomy in the elderly: Matched-control study. Dis Colon Rectum, 2000; 43:326–332.

13.

Stewart

, O'Suilleabhain

, Madhavan

, Wigmore

, Parks

, Garden

. The extent of resection influences outcome following hepatectomy for colorectal liver metastases. Eur J Surg Oncol, 2004; 30:370–376.

14.

Kurian

, Wang

, Grunkemeier

, Bhayani

, Swanstrom

. Defining “the elderly” undergoing major gastrointestinal resections: Receiver operating characteristic analysis of a large ACS-NSQIP cohort. Ann Surg, 2013; 258:483–489.

15.

Keller

, Lawrence

, Nobel

, Delaney

. Optimizing cost and short-term outcomes for elderly patients in laparoscopic colonic surgery. Surg Endosc, 2013; 27:4463–4468.

16.

Vignali

, Di Palo

, Tamburini

, Radaelli

, Orsenigo

, Staudacher

. Laparoscopic vs. open colectomies in octogenarians: A case-matched control study. Dis Colon Rectum, 2005; 48:2070–2075.

17.

Soma

, Sugano

, Kawasaki

, Tsuji

, Fukui

. Colorectal resection in nonagenarians: Effectiveness of laparoscopic surgery. Asian J Endosc Surg, 2014; 7:222–226.

18.

Seshadri

, Mamazza

, Schlachta

, Cadeddu

, Poulin

. Laparoscopic colorectal resection in octogenarians. Surg Endosc, 2001; 15:802–805.

19.

Cheung

, Chung

, Fung

, Wong

, Yau

, Li

. Laparoscopic resection for colorectal cancer in octogenarians: Results in a decade. Dis Colon Rectum, 2007; 50:1905–1910.

20.

Lim

, Kim

. Laparoscopic surgery for colorectal cancer in patients over 80 years of age: The morbidity outcomes. Ann Surg Treat Res, 2017; 92:423–428.

21.

Devoto

, Celentano

, Cohen

, Khan

, Chand

. Colorectal cancer surgery in the very elderly patient: A systematic review of laparoscopic versus open colorectal resection. Int J Colorectal Dis, 2017; 32:1237–1242.

22.

Sundararajan

, Mitra

, Jacobson

, Grann

, Heitjan

, Neugut

. Survival associated with 5-fluorouracil-based adjuvant chemotherapy among elderly patients with node-positive colon cancer. Ann Intern Med, 2002; 136:349–357.

23.

Pallis

, Papamichael

, Audisio

, et al. EORTC Elderly Task Force experts' opinion for the treatment of colon cancer in older patients. Cancer Treat Rev, 2010; 36:83–90.

24.

Ades

. Adjuvant chemotherapy for colon cancer in the elderly: Moving from evidence to practice. Oncology (Williston Park), 2009; 23:162–167.

25.

Hatakeyama

, Nakanishi

, Murayama

, et al. Laparoscopic resection for colorectal cancer improves short-term outcomes in very elderly colorectal cancer patients. Surg Laparosc Endosc Percutan Tech, 2013; 23:532–535.

26.

, Wang

, Gao

, Yang

, Guo

. Laparoscopic colorectal resection versus open colorectal resection in octogenarians: A systematic review and meta-analysis of safety and efficacy. Tech Coloproctol, 2016; 20:153–162.

27.

Clinical Outcomes of Surgical Therapy Study

, Nelson

, Sargent

, et al. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med, 2004; 350:2050–2059.

28.

Croce

, Olmi

, Azzola

, Russo

, Di Bonifacio

. Laparoscopic colectomy: Indications, standardized technique and results after 6 years experience. Hepatogastroenterology, 2000; 47:683–691.

29.

de'Angelis

, Lizzi

, Azoulay

, Brunetti

. Robotic versus laparoscopic right colectomy for colon cancer: Analysis of the initial simultaneous learning curve of a surgical fellow. J Laparoendosc Adv Surg Tech A, 2016; 26:882–892.

30.

Deo

, Puntambekar

. Laparoscopic right radical hemicolectomy. J Minim Access Surg, 2012; 8:21–24.

31.

Shapiro

, Keler

, Segev

, Sarna

, Hatib

, Hazzan

. Laparoscopic right hemicolectomy with intracorporeal anastomosis: Short- and long-term benefits in comparison with extracorporeal anastomosis. Surg Endosc, 2016; 30:3823–3829.

32.

Covinsky

, Kahana

, Kercher

, Schumacher

, Justice

. History and mobility exam index to identify community-dwelling elderly persons at risk of falling. J Gerontol A Biol Sci Med Sci, 2001; 56:M253–M259.

33.

Dindo

, Demartines

, Clavien

. Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg, 2004; 240:205–213.

34.

Martinez-Perez

, Carra

, Brunetti

, de'Angelis

. Pathologic outcomes of laparoscopic vs open mesorectal excision for rectal cancer: A systematic review and meta-analysis. JAMA Surg, 2017; 152:e165665.

35.

de'Angelis

, Vitali

, Brunetti

, et al. Laparoscopic vs. open surgery for T4 colon cancer: A propensity score analysis. Int J Colorectal Dis, 2016; 31:1785–1797.

36.

de'Angelis

, Landi

, Vitali

, et al. Multicentre propensity score-matched analysis of laparoscopic versus open surgery for T4 rectal cancer. Surg Endosc, 2017; 31:3106–3121.

37.

Lacy

, Garcia-Valdecasas

, Delgado

, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: A randomised trial. Lancet, 2002; 359:2224–2229.

38.

Panis

, Maggiori

, Caranhac

, Bretagnol

, Vicaut

. Mortality after colorectal cancer surgery: A French survey of more than 84,000 patients. Ann Surg, 2011; 254:738–743; discussion 743–734.

39.

Al-Refaie

, Parsons

, Habermann

, et al. Operative outcomes beyond 30-day mortality: Colorectal cancer surgery in oldest old. Ann Surg, 2011; 253:947–952.

40.

Page

, Poritz

, Kunselman

, Koltun

. Factors affecting surgical risk in elderly patients with inflammatory bowel disease. J Gastrointest Surg, 2002; 6:606–613.

41.

Rutten

, den Dulk

, Lemmens

, van de Velde

, Marijnen

. Controversies of total mesorectal excision for rectal cancer in elderly patients. Lancet Oncol, 2008; 9:494–501.

42.

Vemuri

, Wainess

, Dimick

, et al. Effect of increasing patient age on complication rates following intact abdominal aortic aneurysm repair in the United States. J Surg Res, 2004; 118:26–31.

43.

Duron

, Duron

, Dugue

, et al. Risk factors for mortality in major digestive surgery in the elderly: A multicenter prospective study. Ann Surg, 2011; 254:375–382.

44.

Ballesta Lopez

, Cid

, Poves

, Bettonica

, Villegas

, Memon

. Laparoscopic surgery in the elderly patient. Surg Endosc, 2003; 17:333–337.

45.

Turrentine

, Wang

, Simpson

, Jones

. Surgical risk factors, morbidity, and mortality in elderly patients. J Am Coll Surg, 2006; 203:865–877.

46.

Hinoi

, Kawaguchi

, Hattori

, et al. Laparoscopic versus open surgery for colorectal cancer in elderly patients: A multicenter matched case-control study. Ann Surg Oncol, 2015; 22:2040–2050.

47.

Rinaldi

, Ouaissi

, Barabino

, et al. Laparoscopy could be the best approach to treat colorectal cancer in selected patients aged over 80 years: Outcomes from a multicenter study. Dig Liver Dis, 2017; 49:84–90.

48.

Manceau

, Hain

, Maggiori

, Mongin

, Prost

AlDJ

, Panis

. Is the benefit of laparoscopy maintained in elderly patients undergoing rectal cancer resection? An analysis of 446 consecutive patients. Surg Endosc, 2017; 31:632–642.

49.

Tan

, Konishi

, Kawamura

, et al. Laparoscopic colorectal surgery in elderly patients: A case-control study of 15 years of experience. Am J Surg, 2011; 201:531–536.

50.

Fiscon

, Portale

, Frigo

, Migliorini

. Laparoscopic resection of colorectal cancer: Matched comparison in elderly and younger patients. Tech Coloproctol, 2010; 14:323–327.

51.

Kunitake

, Zingmond

, Ryoo

, Ko

. Caring for octogenarian and nonagenarian patients with colorectal cancer: What should our standards and expectations be?. Dis Colon Rectum, 2010; 53:735–743.

52.

Law

, Chu

, Tung

. Laparoscopic colorectal resection: A safe option for elderly patients. J Am Coll Surg, 2002; 195:768–773.

53.

Pinto

, Ruiz

, Edden

, Weiss

, Nogueras

, Wexner

. How reliable is laparoscopic colorectal surgery compared with laparotomy for octogenarians?. Surg Endosc, 2011; 25:2692–2698.

54.

Altomare

, Di Lena

, Porcelli

, et al. Effects of curative colorectal cancer surgery on exhaled volatile organic compounds and potential implications in clinical follow-up. Ann Surg, 2015; 262:862–866.

55.

Rotelli

, Bocale

, De Fazio

, et al. IN-VITRO evidence for the protective properties of the main components of the Mediterranean diet against colorectal cancer: A systematic review. Surg Oncol, 2015; 24:145–152.