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Table 1. 
Demographic Characteristics for the 4 Patient Cohorts*
Demographic Characteristics for the 4 Patient Cohorts*
Table 2. 
Distribution of Operative Procedures and Pathologic Findings Among the Patient Cohorts
Distribution of Operative Procedures and Pathologic Findings Among the Patient Cohorts
Table 3. 
Distribution of All Complications Among the Patient Cohorts*
Distribution of All Complications Among the Patient Cohorts*
Table 4. 
Reasons for Readmission Within 30 Days of Discharge*
Reasons for Readmission Within 30 Days of Discharge*
Table 5. 
Ratios of POSSUM Observed to Expected Morbidity and Mortality for the 4 Patient Cohorts
Ratios of POSSUM Observed to Expected Morbidity and Mortality for the 4 Patient Cohorts
1.
Pearson  SDGoulart-Fisher  DLee  TH Critical pathways as a strategy for improving patient care. Ann Intern Med. 1995;123941- 948Article
2.
Archer  SBBurnett  RJFlesch  LV  et al.  Implementation of a clinical pathway decreases length of stay and hospital charges for patients undergoing total colectomy and ileal pouch/anal anastomosis. Surgery. 1997;122699- 705Article
3.
Kehlet  H Multimodal approach to control postoperative pathophysiology and rehabilitation. Br J Anaesth. 1997;78606- 617Article
4.
Kehlet  HMogensen  T Hospital stay of 2 days after open sigmoidectomy with a multimodal rehabilitation programme. Br J Surg. 1999;86227- 230Article
5.
Basse  LJakobsen  DHBillesbolle  P  et al.  A clinical pathway to accelerate recovery after colonic resection. Ann Surg. 2000;23251- 57Article
6.
Bardram  LFunch-Jensen  PJensen  P  et al.  Recovery after laparoscopic colonic surgery with epidural analgesia and early oral nutrition and mobilisation. Lancet. 1995;345763- 764Article
7.
Binderow  SRCohen  SMWexner  SDNogueras  JJ Must early postoperative oral intake be limited to laparoscopy? Dis Colon Rectum. 1994;37584- 589Article
8.
Reissman  PTeoh  TACohen  SMWeiss  EGNogueras  JJWexner  SD Is early feeding safe after elective colorectal surgery? a prospective randomized trial. Ann Surg. 1995;22273- 77Article
9.
Di Fronzo  LACymerman  JO'Connell  TX Factors affecting early postoperative feeding following elective open colon resection. Arch Surg. 1999;134941- 946Article
10.
Bradshaw  BCGLiu  SSThirlby  RC Standardized perioperative care protocols and reduced length of stay after colon surgery. J Am Coll Surg. 1998;186501- 506Article
11.
Behrns  KEKircher  APGalanko  JA  et al.  Prospective randomized trial of early initiation and hospital discharge on a liquid diet following elective intestinal surgery. J Gastrointest Surg. 2000;4217- 221Article
12.
Senagore  AJLuchtefeld  MAMackeigan  JM What is the learning curve for laparoscopic colectomy? Am Surg. 1995;61681- 685
13.
Simons  AJAnthone  GJOrtega  AE  et al.  Laparoscopic-assisted colectomy learning curve. Dis Colon Rectum. 1995; Jun38 ((6)) 600- 603Article
14.
Bennett  CLStryker  SJFerreira  MRAdams  JBeart Jr  RW The learning curve for laparoscopic colorectal surgery: preliminary results from a prospective analysis of 1194 laparoscopic-assisted colectomies. Arch Surg. 1997;13241- 44Article
15.
Senagore  AJWhalley  DDelaney  CPMekhail  NDuepree  HJFazio  VW Epidural anesthesia-analgesia shortens length of stay after laparoscopic segmental colectomy for benign pathology. Surgery. 2001;129672- 676Article
16.
Bardram  LFunch-Jensen  PKehlet  H Rapid rehabilitation in elderly patients after laparoscopic colonic resection. Br J Surg. 2000;871540- 1545Article
17.
Delaney  CPFazio  VWSenagore  AJRobinson  BHalverson  ALRemzi  FH "Fast track" postoperative management protocol for patients with high co-morbidity undergoing complex abdominal and pelvic colorectal surgery. Br J Surg. 2001;881533- 1538Article
18.
Whitely  MSPrytherch  DHiggins  BWeaver  PCProut  WG Comparative audit of colorectal resection with the POSSUM scoring system. Br J Surg. 1995;82425- 426Article
19.
Kragelund  EBalslev  IBardram  L  et al.  Resectability, operative mortality, and survival of patients in old age with carcinoma of colon and rectum. Dis Colon Rectum. 1974;17617- 621Article
20.
Chiappa  AZbar  APBertani  EBiella  FAudisio  RAStaudacher  C Surgical outcomes for colorectal cancer patients including the elderly. Hepatogastroenterology. 2001;48440- 444
21.
Hobler  KE Colon surgery for cancer in the very elderly: cost and 3-year survival. Ann Surg. 1986;203129- 131Article
22.
Wise  WEPadmanabhan  AMessig  DM  et al.  Abdominal colon and rectal operations in the elderly. Dis Colon Rectum. 1991;34959- 963Article
23.
Sunouchi  KNamiki  KMori  MShimizu  TTadokoro  M How should patients 80 years of age and older with colorectal carcinoma be treated? long-term and short-term outcome and postoperative cytokine levels. Dis Colon Rectum. 2000;43233- 241Article
24.
Greenburg  AGSaik  RPPridham  D Influence of age on mortality of colon surgery. Am J Surg. 1985;15065- 70Article
25.
Boyd  JBBradford Jr  BWatne  AL Operative risk factors of colon resection in the elderly. Ann Surg. 1980;192743- 746Article
26.
Stewart  BTStitz  RWLumley  JW Laparoscopically assisted colorectal surgery in the elderly. Br J Surg. 1999;86938- 941Article
27.
Reissman  PAgachan  FWexner  SD Outcome of laparoscopic colorectal surgery in older patients. Am Surg. 1996;621060- 1063
28.
Delgado  SLacy  AMGarcia Valdecasas  JC  et al.  Could age be an indication for laparoscopic colectomy in colorectal cancer? Surg Endosc. 2000;1422- 26Article
29.
Stocchi  LNelson  HYoung-Fadok  TMLarson  DRIlstrup  DM Safety and advantages of laparoscopic vs open colectomy in the elderly: matched-control study. Dis Colon Rectum. 2000;43326- 332Article
30.
Schwandner  OSchiedeck  THBruch  HP Advanced age: indication or contraindication for laparoscopic colorectal surgery? Dis Colon Rectum. 1999;42356- 362Article
31.
Whiteley  MSPrytherch  DRHiggins  BWeaver  PCProut  WG An evaluation of the POSSUM surgical scoring system. Br J Surg. 1996;83812- 815Article
32.
Prytherch  DRWhiteley  MSHiggins  BWeaver  PCProut  WG POSSUM and Portsmouth POSSUM for predicting mortality. Br J Surg. 1998;851217- 1220Article
33.
Tekkis  PPKocher  HMBentley  AJE  et al.  Operative mortality rates among surgeons. Dis Colon Rectum. 2000;431528- 1534Article
34.
Copeland  GPJones  DWalters  M POSSUM: a scoring system for surgical audit. Br J Surg. 1991;78355- 360Article
Original Article
March 2003

Advantages of Laparoscopic Colectomy in Older Patients

Author Affiliations

From the Department of Colorectal Surgery, Minimally Invasive Surgery Center, The Cleveland Clinic Foundation, Cleveland, Ohio.

Arch Surg. 2003;138(3):252-256. doi:10.1001/archsurg.138.3.252
Abstract

Hypothesis  Few data describe the relative benefits of an expedited recovery program and laparoscopic technique in older vs younger patients undergoing colectomy. We compared short-term outcomes in age-matched cohorts of patients undergoing laparoscopic vs open segmental colectomy managed with the Controlled Rehabilitation With Early Ambulation and Diet program.

Design  Four age-matched cohorts of patients were compared: (1) patients 70 years or older undergoing laparoscopic colectomy (group 1), (2) those 70 or older undergoing open colectomy (group 2), (3) those younger than 60 undergoing laparoscopic colectomy (group 3), and (4) those younger than 60 undergoing open colectomy (group 4).

Methods  Data collected included age, sex, body mass index, Physiologic and Operative Severity Score for the Enumeration of Morbidity and Mortality, American Society of Anesthesiologists' score, estimated blood loss, operative duration in minutes, pathologic findings, type of segmental colectomy, complications, mortality, length of hospital stay, and 30-day readmission rate.

Results  Four hundred seventy-six patients fulfilled the inclusion criteria and had complete data available for collection (group 1, 50 patients; group 2, 123 patients; group 3, 181 patients; and group 4, 122 patients). Demographic data, operative procedures, and pathologic findings were similar among the cohorts. The mean ± SEM length of hospital stay was significantly shorter with laparoscopic surgery in both age cohorts (group 1, 4.2 ± 3.0 days; group 2, 9.3 ± 7.6 days; group 3, 3.9 ± 5.9 days; and group 4, 6.1 ± 3.0 days). The mean ± SEM direct hospital costs were significantly lower only with laparoscopic colectomy in the older cohorts. Using the Physiologic and Operative Severity Score for the Enumeration of Morbidity and Mortality, it was noted that group 2 experienced an observed rate of morbidity similar to that predicted. Conversely, groups 1, 3, and 4 had rates that were significantly lower than expected. Mean ± SEM readmission rates were comparable in the older cohorts (group 1, 6.0%, and group 2, 6.5%) but significantly different in the younger cohorts (group 3, 9.4%, and group 4, 4.1%).

Conclusions  The Controlled Rehabilitation With Early Ambulation and Diet program in combination with laparoscopic segmental colectomy can be safely performed in all age groups. The technique offers particular advantages to older patients because of reductions in length of hospital stay, morbidity and mortality rates, and direct cost of care.

THE CLINICAL BENEFITS of accelerated recovery after colorectal surgery have been increasingly appreciated during the last 5 years.111 Changes in perioperative care plans and laparoscopic techniques have aimed at reducing perioperative stress, decreasing morbidity and mortality, and lowering the overall resource consumption for patients of all ages.114 The major emphasis of these programs is to encourage earlier resumption of oral intake to reduce ileus and to provide adequate analgesia so that ambulation can be expedited.

Most evidence suggests that laparoscopic colectomy can be performed safely for several pathologic conditions.1214 The resulting advantages of smaller wounds, shorter ileus, earlier resumption of dietary intake, and reductions in length of hospital stay are associated with this approach.1215 Bardram and colleagues16 applied a rapid rehabilitation program to a small cohort of older (median age, 81 years) patients and demonstrated a median length of hospital stay of 2.5 days, despite a 22% rate of conversion to an open procedure.

To our knowledge, there are no substantial data that compare the relative risks and benefits of operative intervention and expedited recovery programs in patients undergoing open vs laparoscopic colectomy or, in particular, that assess whether equivalent benefits are obtained by older and younger patients. The objective of this study was to compare short-term outcomes in 4 cohorts of patients managed with a rapid postoperative recovery program: (1) patients 70 years or older undergoing laparoscopic colectomy (group 1), (2) those 70 or older undergoing open colectomy (group 2), (3) those younger than 60 undergoing laparoscopic colectomy (group 3), and (4) those younger than 60 undergoing open colectomy (group 4).

METHODS

Data on all patients undergoing elective segmental colectomy for any pathologic condition without prior major abdominal surgery between March 1, 1999, and December 31, 2001, were evaluated. All open surgery cases were evaluated for exclusion criteria that would have precluded a laparoscopic approach by us: body mass index greater than 36 (calculated as weight in kilograms divided by the square of height in meters) and prior major laparotomy, excluding cholecystectomy, abdominal hysterectomy, and appendectomy. The 4 cohorts of patients already described were compared.

The perioperative care plan used for these patients, Controlled Rehabilitation With Early Ambulation and Diet (CREAD), has been separately evaluated in patients undergoing laparoscopic and open colectomy.15,17 None of the patients accepted in the present study were specifically included in either of those studies. Before surgery, the patient was instructed regarding the components of the care plan and was provided an information sheet highlighting the expected milestones. Based on patient preference, an intravenous patient-controlled anesthesia system or patient-controlled epidural anesthesia consisting of fentanyl citrate and bupivacaine hydrochloride regimen was used. Analgesia was supplemented with 30 mg intravenous ketorolac tromethamine every 6 hours, if needed. Orogastric tubes were placed after induction of anesthesia and removed before endotracheal extubation. Ambulation was encouraged the evening of surgery and at least 5 times per day starting on the first postoperative day. The first meal offered was clear liquids as soon as the patient was free of nausea and had recovered from the anesthetic. Patients were allowed to advance to a general diet as tolerated. Oral analgesia was started once the patient tolerated solids, generally on the first postoperative day for patients who underwent laparoscopic colectomy and on the second day for those who underwent open colectomy. The catheter was removed from the bladder on day 1 or 2, depending on the need for epidural analgesia. Before discharge, all patients passed flatus or stool, tolerated at least 3 solid meals, and had adequate oral analgesia.

Data collected included age, sex, Physiologic and Operative Severity Score for the Enumeration of Morbidity and Mortality (POSSUM), American Society of Anesthesiologists' score, estimated blood loss, operative duration in minutes (defined as time from incision to wound closure), pathologic findings, type of segmental colectomy, complications, mortality, length of hospital stay, and 30-day readmission rate. The POSSUM is a validated scoring system used to predict outcome after colon resection.18 The system uses 12 physiologic variables and 6 operative variables to predict expected mortality and morbidity. Direct cost per case was assessed using data provided by Stanford University's (Palo Alto, Calif) integrated hospital cost management and decision software (Transition Systems, Inc, Boston, Mass). This software provided direct cost per case for charges associated with laboratory services, the pharmacy, radiology, anesthesia, the operating room, and hospitalization. Acquisition costs were applied for disposable operative equipment. There was no attempt to address total cost per case, as indirect fixed and variable indirect costs were not included. Data on professional charges were not included in the study.

Data are presented as mean ± SEM for parametric data and median (interquartile range) for nonparametric data. Statistical analysis consisted of the Wilcoxon rank sum test, χ2 test, and analysis of variance as appropriate, with significance set at P<.05. The study was performed using data from institutional review board–approved databases. All laparoscopic conversions to open procedures were included in the respective laparoscopic groups, based on intention to treat.

RESULTS

Four hundred seventy-six patients fulfilled the inclusion criteria and had complete data available for collection. The numbers in each cohort were as follows: group 1, 50 patients; group 2, 123 patients; group 3, 181 patients; and group 4, 122 patients. Based on the research design, there was a significant difference in mean age between the cohorts; however, there was no significant age difference between groups 1 and 2 or between groups 3 and 4 (Table 1). Other demographic data are given in Table 1. The distribution of operative procedures among the cohorts is given in Table 2.

The length of hospital stay was significantly shorter in the laparoscopic groups (Table 1). Among patients who underwent open surgery, group 2 had a significantly longer hospital stay compared with that of group 4.

In the older groups, those who underwent laparoscopic surgery incurred significantly lower direct hospital costs. Total direct costs were similar for the 2 operative approaches in the younger cohorts, indicating that a laparoscopic approach is not necessarily associated with high costs. The direct costs were similar between the 2 laparoscopic cohorts, whereas costs in group 2 were significantly higher than those in group 4 (Table 1).

The specific morbidities experienced by the groups are given in Table 3 and Table 4. Using the POSSUM, the only group that had an observed rate of morbidity similar to that predicted was group 2. This rate was significantly higher than those in the other 3 cohorts, who experienced similar complication rates that were significantly lower than predicted rates (Table 5). Among all patient cohorts, the mortality rates were significantly lower than predicted, as there were only 2 mortalities, both occurring in group 2 (Table 5).

Readmission rates within 30 days were comparable in the older groups (group 1, 6.0%, and group 2, 6.5%). In the younger cohorts, those who underwent laparoscopic surgery had a significantly higher readmission rate (group 3, 9.4%, and group 4, 4.1%). There were no significant differences in the reoperation rates among the cohorts (group 1, 0%; group 2, 0.8%; group 3, 1.6%; and group 4, 0%).

COMMENT

In the not-so-distant past, advanced age was considered a contraindication for major colectomy because of the significant risk of postoperative morbidity and mortality.18 Operative morbidity and mortality in older patients is closely tied to the number and severity of comorbid illnesses.1923 Greenburg et al24 reported an operative mortality of 4% in a group of patients undergoing open colectomy who preoperatively had normal chest x-ray films, renal function, and white blood cell counts and an absence of cardiomegaly. The presence of at least 2 significant comorbidities has a substantial effect in patients older than 70 years, with Boyd et al25 describing a mortality of 16.2% in an older cohort compared with 8.6% in a younger one.

Several authors have evaluated the outcomes of patients undergoing laparoscopic colectomy. Stewart et al26 recently reported results of a cohort study of patients older than 80 years undergoing open or laparoscopic colectomy; they identified a 41% reduction in the length of hospital stay and a greater percentage of patients achieving normal activity within 1 month after surgery in the laparoscopic group. Reissman et al27 compared a group of older patients with a high incidence of comorbid illnesses with a younger patient cohort and found similar lengths of hospital stay and postoperative morbidity in the 2 age groups undergoing colorectal surgery. Bardram et al16 used a rapid rehabilitation program of epidural anesthesia, early feeding, and aggressive ambulation and achieved a median length of hospital stay of 2.5 days in older patients who underwent laparoscopic colonic resection. Delgado et al28 presented data from a prospective colon cancer trial that demonstrated a higher morbidity in patients older than 70 years who underwent open surgery vs patients of similar age who underwent laparoscopic procedures. In addition to shorter hospital stays and lower morbidity rates, laparoscopic colectomy may allow for a more frequent and earlier return to independent living.28,29 Schwandner et al,30 however, found a longer operative duration, greater consumption of intensive care resources, and an overall longer hospital stay in patients older than 70 undergoing laparoscopic colectomy compared with those younger than 70. This was a German study, and cultural influences and practice patterns may have affected the outcomes.

In typical series,14 the postoperative length of hospital stay after major gastrointestinal surgery is between 5 and 10 days. Longer length of hospital stay in older patients may be the result of postoperative pain, slow return of gastrointestinal function, physical deconditioning and fatigue, or postoperative complications.3 Kehlet and Mogensen3,4 attempted to address these issues by evaluating the benefits of a rapid rehabilitation program and described a median postoperative stay of 2 days after elective open sigmoid colectomy. His group found similar results in a group of patients older than 80 years using the program following laparoscopic colonic resection.16

Several multimodal care plans that successfully reduce the length of hospital stay for colorectal surgery have been advocated, although most exclude the use of epidural analgesia, oral cathartics, and prokinetic agents.711 Unfortunately, a common sequela of these programs is substantial readmission, despite differences in discharge criteria (eg, tolerating a clear liquid diet with or without evidence of gastrointestinal function).9,11 With the CREAD program, significant reductions in length of hospital stay were obtained for patients undergoing open and laparoscopic colectomies.15,17

Our data demonstrate that laparoscopic colectomy in combination with the CREAD program safely reduced the length of hospital stay by 54.9% in older patients and by 36.1% in younger patients. There was an associated significant reduction in the direct cost of caring for patients in group 1 ($3920) vs group 2 ($6448). In addition, laparoscopic colectomy reduced the postoperative morbidity in group 1 well below the POSSUM predicted rates and significantly lower than that of group 2. Two surrogates for operative stress, operative duration and estimated blood loss, were also significantly reduced in both laparoscopic groups.

The limitation of this study is the use of cohort methods. We attempted to reduce bias by including all index cases performed by open and laparoscopic techniques. To minimize selection bias in the laparoscopic group, we also did not include open surgery cases that represented significant reoperative abdominal surgery, as only 2 surgeons performed laparoscopic procedures. The American Society of Anesthesiologists' score and POSSUM were used in an attempt to assess the risk of the patient groups. As expected, the 2 older cohorts of patients appeared to be at greater risk, as demonstrated by a higher percentage of patients with an American Society of Anesthesiologists' score of 3 or 4 and a higher predicted morbidity and mortality rate by POSSUM.3034

CONCLUSIONS

Our data demonstrate that a combination of the CREAD program and laparoscopic segmental colectomy can be safely performed in all age groups. The laparoscopic technique is particularly advantageous for older patients, as it reduces the length of hospital stay, morbidity and mortality rates, and direct cost of care compared with those associated with open colectomy.

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Article Information

Corresponding author: Anthony J. Senagore, MD, MS, MBA, Department of Colorectal Surgery, Minimally Invasive Surgery Center, The Cleveland Clinic Foundation, 9500 Euclid Ave, Desk A-30, Cleveland, OH 44195 (e-mail: Senagoa@ccf.org).

Accepted for publication October 25, 2002.

References
1.
Pearson  SDGoulart-Fisher  DLee  TH Critical pathways as a strategy for improving patient care. Ann Intern Med. 1995;123941- 948Article
2.
Archer  SBBurnett  RJFlesch  LV  et al.  Implementation of a clinical pathway decreases length of stay and hospital charges for patients undergoing total colectomy and ileal pouch/anal anastomosis. Surgery. 1997;122699- 705Article
3.
Kehlet  H Multimodal approach to control postoperative pathophysiology and rehabilitation. Br J Anaesth. 1997;78606- 617Article
4.
Kehlet  HMogensen  T Hospital stay of 2 days after open sigmoidectomy with a multimodal rehabilitation programme. Br J Surg. 1999;86227- 230Article
5.
Basse  LJakobsen  DHBillesbolle  P  et al.  A clinical pathway to accelerate recovery after colonic resection. Ann Surg. 2000;23251- 57Article
6.
Bardram  LFunch-Jensen  PJensen  P  et al.  Recovery after laparoscopic colonic surgery with epidural analgesia and early oral nutrition and mobilisation. Lancet. 1995;345763- 764Article
7.
Binderow  SRCohen  SMWexner  SDNogueras  JJ Must early postoperative oral intake be limited to laparoscopy? Dis Colon Rectum. 1994;37584- 589Article
8.
Reissman  PTeoh  TACohen  SMWeiss  EGNogueras  JJWexner  SD Is early feeding safe after elective colorectal surgery? a prospective randomized trial. Ann Surg. 1995;22273- 77Article
9.
Di Fronzo  LACymerman  JO'Connell  TX Factors affecting early postoperative feeding following elective open colon resection. Arch Surg. 1999;134941- 946Article
10.
Bradshaw  BCGLiu  SSThirlby  RC Standardized perioperative care protocols and reduced length of stay after colon surgery. J Am Coll Surg. 1998;186501- 506Article
11.
Behrns  KEKircher  APGalanko  JA  et al.  Prospective randomized trial of early initiation and hospital discharge on a liquid diet following elective intestinal surgery. J Gastrointest Surg. 2000;4217- 221Article
12.
Senagore  AJLuchtefeld  MAMackeigan  JM What is the learning curve for laparoscopic colectomy? Am Surg. 1995;61681- 685
13.
Simons  AJAnthone  GJOrtega  AE  et al.  Laparoscopic-assisted colectomy learning curve. Dis Colon Rectum. 1995; Jun38 ((6)) 600- 603Article
14.
Bennett  CLStryker  SJFerreira  MRAdams  JBeart Jr  RW The learning curve for laparoscopic colorectal surgery: preliminary results from a prospective analysis of 1194 laparoscopic-assisted colectomies. Arch Surg. 1997;13241- 44Article
15.
Senagore  AJWhalley  DDelaney  CPMekhail  NDuepree  HJFazio  VW Epidural anesthesia-analgesia shortens length of stay after laparoscopic segmental colectomy for benign pathology. Surgery. 2001;129672- 676Article
16.
Bardram  LFunch-Jensen  PKehlet  H Rapid rehabilitation in elderly patients after laparoscopic colonic resection. Br J Surg. 2000;871540- 1545Article
17.
Delaney  CPFazio  VWSenagore  AJRobinson  BHalverson  ALRemzi  FH "Fast track" postoperative management protocol for patients with high co-morbidity undergoing complex abdominal and pelvic colorectal surgery. Br J Surg. 2001;881533- 1538Article
18.
Whitely  MSPrytherch  DHiggins  BWeaver  PCProut  WG Comparative audit of colorectal resection with the POSSUM scoring system. Br J Surg. 1995;82425- 426Article
19.
Kragelund  EBalslev  IBardram  L  et al.  Resectability, operative mortality, and survival of patients in old age with carcinoma of colon and rectum. Dis Colon Rectum. 1974;17617- 621Article
20.
Chiappa  AZbar  APBertani  EBiella  FAudisio  RAStaudacher  C Surgical outcomes for colorectal cancer patients including the elderly. Hepatogastroenterology. 2001;48440- 444
21.
Hobler  KE Colon surgery for cancer in the very elderly: cost and 3-year survival. Ann Surg. 1986;203129- 131Article
22.
Wise  WEPadmanabhan  AMessig  DM  et al.  Abdominal colon and rectal operations in the elderly. Dis Colon Rectum. 1991;34959- 963Article
23.
Sunouchi  KNamiki  KMori  MShimizu  TTadokoro  M How should patients 80 years of age and older with colorectal carcinoma be treated? long-term and short-term outcome and postoperative cytokine levels. Dis Colon Rectum. 2000;43233- 241Article
24.
Greenburg  AGSaik  RPPridham  D Influence of age on mortality of colon surgery. Am J Surg. 1985;15065- 70Article
25.
Boyd  JBBradford Jr  BWatne  AL Operative risk factors of colon resection in the elderly. Ann Surg. 1980;192743- 746Article
26.
Stewart  BTStitz  RWLumley  JW Laparoscopically assisted colorectal surgery in the elderly. Br J Surg. 1999;86938- 941Article
27.
Reissman  PAgachan  FWexner  SD Outcome of laparoscopic colorectal surgery in older patients. Am Surg. 1996;621060- 1063
28.
Delgado  SLacy  AMGarcia Valdecasas  JC  et al.  Could age be an indication for laparoscopic colectomy in colorectal cancer? Surg Endosc. 2000;1422- 26Article
29.
Stocchi  LNelson  HYoung-Fadok  TMLarson  DRIlstrup  DM Safety and advantages of laparoscopic vs open colectomy in the elderly: matched-control study. Dis Colon Rectum. 2000;43326- 332Article
30.
Schwandner  OSchiedeck  THBruch  HP Advanced age: indication or contraindication for laparoscopic colorectal surgery? Dis Colon Rectum. 1999;42356- 362Article
31.
Whiteley  MSPrytherch  DRHiggins  BWeaver  PCProut  WG An evaluation of the POSSUM surgical scoring system. Br J Surg. 1996;83812- 815Article
32.
Prytherch  DRWhiteley  MSHiggins  BWeaver  PCProut  WG POSSUM and Portsmouth POSSUM for predicting mortality. Br J Surg. 1998;851217- 1220Article
33.
Tekkis  PPKocher  HMBentley  AJE  et al.  Operative mortality rates among surgeons. Dis Colon Rectum. 2000;431528- 1534Article
34.
Copeland  GPJones  DWalters  M POSSUM: a scoring system for surgical audit. Br J Surg. 1991;78355- 360Article
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