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Original Article |

Dramatic Decreases in Mortality From Laparoscopic Colon Resections Based on Data From the Nationwide Inpatient Sample FREE

Molly M. Cone, MD; Daniel O. Herzig, MD; Brian S. Diggs, PhD; James P. Dolan, MD; Jennifer D. Rea, MD; Karen E. Deveney, MD; Kim C. Lu, MD
[+] Author Affiliations

Author Affiliations: Department of Surgery, Oregon Health and Science University, Portland.


Arch Surg. 2011;146(5):594-599. doi:10.1001/archsurg.2011.79.
Text Size: A A A
Published online

Objective  To determine the mortality rate and associated factors for laparoscopic and open colectomy as derived from the Nationwide Inpatient Sample database.

Design  Retrospective cohort.

Setting  Nationwide Inpatient Sample database.

Patients  Between 2002 and 2007, the Nationwide Inpatient Sample estimated 1 314 696 patients underwent colectomy in the United States. Most (n = 1 231 184) were open, but 83 512 were laparoscopic. Patients who underwent a laparoscopic procedure that was converted to open were analyzed within the laparoscopic group on an intention-to-treat basis.

Main Outcome Measure  Mortality rate. Using a logistic regression model, patient and institutional characteristics were analyzed and evaluated for significant associations with in-hospital mortality.

Results  In a multivariate analysis, significant predictors of increased mortality included older age, male sex, lower socioeconomic status, comorbidities, and emergency or transfer admission. Additionally, a laparoscopic approach was an independent predictor of decreased mortality when compared with open colectomy (relative risk, 0.51; P < .001).

Conclusion  Even when controlling for comorbidities, socioeconomic status, practice setting, and admission type, laparoscopy is an independent predictor of decreased mortality for colon resection.

Colon resection is a common operation that is associated with a mortality rate of 2% to 6%.16 Multiple studies have evaluated factors related to mortality after colectomy, including surgeon factors or hospital volume,79 while others have derived risk stratification models using patient comorbidities.6,10 Other models select colectomies for specific disease processes such as Clostridium difficile colitis,11,12 ischemic colitis,13 and colon cancer5,14 or by patient factors, including age or socioeconomic status.15 In this study, we sought to examine individual predictors of increased mortality among all colectomies, inclusive of all admission status, diagnosis, age, surgical approach, and socioeconomic class using a large national database.

STUDY POPULATION

The patient data were extracted from the Nationwide Inpatient Sample (NIS) compiled by the Healthcare Cost and Utilization Project for 2002 to 2007. This sample represents the all-payer inpatient experience via a 20% stratified probability sample of American nonmilitary, nonfederal hospitals for each year under consideration. Each individual discharge abstract for this population of patients is statistically weighted to provide a national representation of diagnoses and procedure volume. The NIS database includes inpatient data only, so deaths after hospital discharge were not included in this analysis.

DATA EXTRACTION

Using the appropriate procedure and diagnosis codes as defined by the International Classification of Diseases, Ninth Revision, Clinical Modification, patients undergoing right, left, transverse, sigmoid, partial, multiple-segment, or total colectomy (codes 45.71-45.8) for each year under review were identified and their data were extracted from the overall data set. Cases were further classified as laparoscopic (additional procedure code 54.21 with or without diagnosis code V64.4 for conversion) or open (neither procedure code 54.21 nor diagnosis code V64.4 also present). Cases were included for analysis if they had any of the following diagnosis codes: 008.45 (C difficile colitis), 555.1 (Crohn colitis), 556 (ulcerative colitis), 558.9 (microscopic colitis), 560.2 (sigmoid or cecal volvulus), 562.1 (colon diverticulitis), 564.01 (constipation), 578.9 (acute gastrointestinal bleed), 235.5 (neoplasm of uncertain behavior), 211.3 (colon polyp), and 153 (colon cancer). Patient comorbidities were analyzed individually using a subset of the comprehensive list defined by the Elixhauser Comorbidity Index, which was developed by the Agency for Health Research and Quality for use with the NIS database.16 Comorbidities present in at least 5% of cases and those deemed clinically relevant (anemia, congestive heart failure, chronic pulmonary disease, diabetes mellitus, hypertension, fluid and electrolyte disorders, and obesity) were included. For the purpose of our analysis, converted cases were considered to be part of our laparoscopic cohort on an intent-to-treat basis.

DATA ANALYSIS

Data extraction for the primary procedures, calculation of the national averages, and statistical analysis were performed using SAS/STAT software (release 9.1; SAS Institute Inc, Cary, North Carolina), taking into account the sampling weights and sampling structure of the data. Variables felt to be clinically relevant were included in a multivariate logistic regression model with mortality as the dependent variable. Because this is a nonrandomized study, we also evaluated the data with propensity matching to confirm findings from our multivariate analysis. To correct for potential confounding, we tested for effect measure modification with interaction terms.

Over the 6-year period between 2002 and 2007, a weighted estimate of 1 314 696 patients underwent a colectomy. Table 1 shows patient demographics. Of the 11 International Classification of Diseases, Ninth Revision diagnosis codes used as indications for undergoing a colectomy, colon cancer was the single most common diagnosis (43.8%), followed by diverticulitis (32.6%), and benign neoplasm (11.5%). Overall mortality was 3.7% (n = 48 637). In the open group, 3.9% died (n = 47 863), and mortality in the laparoscopic group was 0.9% (n = 774).

Table Graphic Jump LocationTable 1. Demographics of Patients Who Underwent Colectomy Between 2002 and 2007 in the NIS

The multivariate mortality analysis is reported in Table 2. We found a substantially lower risk of death for all undergoing laparoscopic colectomy when compared with open colectomy (odds ratio [OR], 0.51; 95% confidence interval [CI], 0.43-0.60). Since this was nonrandomized, we used propensity matching to evaluate each decile of patients with the same likelihood of receiving a laparoscopic approach. In each decile, the mortality was lower for a laparoscopic approach. From this analysis, the overall mortality from laparoscopy carried an OR of 0.512 (95% CI, 0.43-0.60) compared with open.

Table Graphic Jump LocationTable 2. Multivariate Analysis of In-Hospital Mortality Following Colectomy Between 2002 and 2007a

Other factors associated with increased survival include younger age, female sex (OR, 0.82; 95% CI, 0.78-0.86), and hospitalization at a rural hospital (OR, 0.87; 95%, CI 0.81-0.95). Medicare and Medicaid insurance coverage were associated with decreased survival (OR, 1.85; 95% CI, 1.70-2.02 and OR, 2.07; 95% CI, 1.82-2.36, respectively). With respect to diagnoses, hemorrhage involving the colon (OR, 3.48; 95% CI, 3.06-3.94) and C difficile colitis (OR, 3.70; 95% CI, 3.32-4.12) had the most notable increased risk of death.

To further evaluate confounding, we looked carefully at effect measure modification. For in-hospital mortality, the multivariate model did not show any clinically significant interactions between approach (laparoscopic vs open) and diagnosis, age, or segment resected.

In this study, we used a national database to evaluate mortality-related outcomes for all patients undergoing a colectomy during 2002 to 2007. Laparoscopic colectomy was shown to be an independent predictor of a markedly decreased mortality rate when compared with open colectomy. Additionally, several factors were found to be associated with an increased risk of death, including older age, male sex, nonelective admission, diagnosis, Medicare insurance, lower income, and operations done at a teaching facility.

In establishing laparoscopic colectomy as a beneficial operation, perioperative mortality must be one of the first factors considered. Several large randomized trials evaluated laparoscopic treatment of colon cancer, including the Clinical Outcomes of Surgical Therapy Study Group (COST) trial, the multicenter European Colon Cancer Laparoscopic or Open Resection Study Group (COLOR) trial, the multicenter UK trial supported by the Medical Research Council (CLASSIC), and the Barcelona trial. None found a significant difference in early mortality between the open and laparoscopic groups.1720 Several other studies evaluated an existing database to look at mortality as a primary outcome, but the results vary from no difference to improved perioperative survival in the laparoscopic group.3,2124 These database studies, however, limited their patient selection by colon cancer, diverticulitis, nonemergent cases, or single institutions. Our analysis differs from these previous reports in that it reviews a national patient sample of all patients who underwent a colectomy during a 6-year period for all diagnoses, all admission types, and all levels of surgeon experience. These demographics allow conclusions to be made about laparoscopic colectomy as a whole, and the results are widely generalizable.

Our results show a significantly decreased risk of death with laparoscopic colectomy. The OR of 0.51 and a tight 95% CI (0.43-0.60) support the validity of this finding, even after accounting for comorbidities, demographics, and institutional characteristics in a multivariate analysis. These results are powered by the substantial patient numbers from NIS, the largest all-payer, inpatient care database,25 which may account for the lack of significance in the smaller studies. Also, the inclusion of emergency admissions in this data set may explain the higher mortality than what has been reported from the various randomized controlled trials. Our findings support a marked reduction of mortality in patients who are treated with a laparoscopic approach.

Other studies have looked at different operations and found similar outcomes with mortality. A recent publication by Dolan et al26 looked at laparoscopic vs open cholecystectomy and found laparoscopy to be an independent predictor of decreased mortality in all age groups younger than 80 years. Singla et al27 also looked at outcomes in complex laparoscopic abdominal operations and found decreased mortality in laparoscopic nephrectomy and colectomy groups compared with open.

The reason for our findings of a dramatic reduction in mortality in the laparoscopic colectomy group is difficult to elucidate. Confounding factors may exist within the database itself, including our inability to account for unmeasured comorbidities or assess cause of death. However, there is some evidence supporting the conclusion that laparoscopy itself is the factor associated with the lower mortality. Major open abdominal surgery is associated with a period of relative immunosuppression, while laparoscopic procedures minimize this cytokine response.28,29 Whether this decrease could lead to a mortality difference has yet to be shown. Another argument, as suggested by a recent National Surgical Quality Improvement Program study, is that the patients chosen for laparoscopic colectomy were overall at lower risk.30 The authors of that study did not, however, examine the relationship between mortality and patient variables in a multivariate model. The mortality reduction reported in our study persists after taking into account recorded comorbidities and other patient and institutional factors in a multivariate analysis.

Female sex was associated with a decreased risk of perioperative death when undergoing colectomy. In contrast, a study looking at the outcomes of sigmoid colectomy showed no difference in survival by sex, and a second study of colon cancer resections found no early survival difference by sex but found improved long-term survival in women.31,32 Dent et al33 found poorer survival in men undergoing colectomy for stage II cancer. They postulated that men experience greater postoperative morbidity than women because of clinical factors, such as comorbidities, or lack of protective biologic characteristics that women possess, including immunologic, hormonal, and molecular factors. There may also be unrecognized comorbidities in the male group or the severity of comorbidities is worse, which cannot be accounted for in this administrative database.

Another factor associated with improved survival was undergoing colectomy in rural hospitals. Similar findings were shown in a National Surgical Quality Improvement Program study looking at surgical outcomes between teaching and nonteaching centers. These findings were attributed to the fact that risk adjustment did not completely eliminate the differences in the patient populations, including a higher prevalence of comorbidities, longer operation times, and more complex operations in teaching institutions.34

There are several limitations to this study. The NIS is an administrative database and may be subject to coding errors. Selection bias is also difficult to eliminate without using randomization. Although we included comorbidities in our multivariate analysis, there is no way to quantify disease severity. We also cannot account for surgeon experience with laparoscopy, which undoubtedly contributed to the choice of surgical approach and to the conversion rate. Finally, this is a nonrandomized prospective cohort study. We attempted to compensate for that with our propensity matching analysis.

In conclusion, this article demonstrates that laparoscopic colectomy is an independent factor predictive of decreased mortality based on a representative sample of the US patient population representing all types of admissions, all payers, all income levels, and all types of treating institutions.

Correspondence: Kim C. Lu, MD, Oregon Health and Science University, 3181 SW Sam Jackson Park Rd, L223, Portland, OR 97239 (luk@ohsu.edu).

Accepted for Publication: April 15, 2010.

Author Contributions:Study concept and design: Cone, Herzig, Dolan, Rea, Deveney, and Lu. Acquisition of data: Cone. Analysis and interpretation of data: Cone, Herzig, Diggs, Rea, and Lu. Drafting of the manuscript: Cone, Herzig, and Lu. Critical revision of the manuscript for important intellectual content: Herzig, Diggs, Dolan, Rea, Deveney, and Lu. Statistical analysis: Diggs. Administrative, technical, and material support: Cone, Herzig, and Rea. Study supervision: Herzig, Dolan, Deveney, and Lu.

Financial Disclosure: None reported.

Previous Presentation: This paper was presented as a poster at the 81st Annual Meeting of the Pacific Coast Surgical Association; February 14, 2010; Maui, Hawaii.

Callahan  MAChristos  PJGold  HTMushlin  AIDaly  JM Influence of surgical subspecialty training on in-hospital mortality for gastrectomy and colectomy patients. Ann Surg 2003;238 (4) 629- 636
PubMed
Cohen  MEBilimoria  KYKo  CYRichards  KHall  BL Effect of subjective preoperative variables on risk-adjusted assessment of hospital morbidity and mortality. Ann Surg 2009;249 (4) 682- 689
PubMed Link to Article
Kemp  JAFinlayson  SR Outcomes of laparoscopic and open colectomy: a national population-based comparison. Surg Innov 2008;15 (4) 277- 283
PubMed Link to Article
Varela  JEAsolati  MHuerta  SAnthony  T Outcomes of laparoscopic and open colectomy at academic centers. Am J Surg 2008;196 (3) 403- 406
PubMed Link to Article
Longo  WEVirgo  KSJohnson  FE  et al.  Risk factors for morbidity and mortality after colectomy for colon cancer. Dis Colon Rectum 2000;43 (1) 83- 91
PubMed Link to Article
Ragg  JLWatters  DAGuest  GD Preoperative risk stratification for mortality and major morbidity in major colorectal surgery. Dis Colon Rectum 2009;52 (7) 1296- 1303
PubMed Link to Article
Muscari  FSuc  BMsika  S  et al. French Federation for Surgical Research, Surgeon-dependent predictive factors for mortality after elective colorectal resection and immediate anastomosis for cancer or nonacute diverticular disease: multivariable analysis of 2,605 patients. J Am Coll Surg 2008;207 (6) 888- 895
PubMed Link to Article
Karanicolas  PJDubois  LColquhoun  PHSwallow  CJWalter  SDGuyatt  GH The more the better?: the impact of surgeon and hospital volume on in-hospital mortality following colorectal resection. Ann Surg 2009;249 (6) 954- 959
PubMed Link to Article
Kwan  TLLai  FLam  CM  et al.  Population-based information on emergency colorectal surgery and evaluation on effect of operative volume on mortality. World J Surg 2008;32 (9) 2077- 2082
PubMed Link to Article
Cohen  MEBilimoria  KYKo  CYHall  BL Development of an American College of Surgeons National Surgery Quality Improvement Program: morbidity and mortality risk calculator for colorectal surgery. J Am Coll Surg 2009;208 (6) 1009- 1016
PubMed Link to Article
Pepin  JVo  TTBoutros  M  et al.  Risk factors for mortality following emergency colectomy for fulminant Clostridium difficile infection. Dis Colon Rectum 2009;52 (3) 400- 405
PubMed Link to Article
Sailhamer  EACarson  KChang  Y  et al.  Fulminant Clostridium difficile colitis: patterns of care and predictors of mortality. Arch Surg 2009;144 (5) 433- 439
PubMed Link to Article
Antolovic  DKoch  MHinz  U  et al.  Ischemic colitis: analysis of risk factors for postoperative mortality. Langenbecks Arch Surg 2008;393 (4) 507- 512
PubMed Link to Article
Vibert  EBretagnol  FAlves  APocard  MValleur  PPanis  Y Multivariate analysis of predictive factors for early postoperative death after colorectal surgery in patients with colorectal cancer and synchronous unresectable liver metastases. Dis Colon Rectum 2007;50 (11) 1776- 1782
PubMed Link to Article
Birkmeyer  NJGu  NBaser  OMorris  AMBirkmeyer  JD Socioeconomic status and surgical mortality in the elderly. Med Care 2008;46 (9) 893- 899
PubMed Link to Article
Elixhauser  ASteiner  CHarris  DRCoffey  RM Comorbidity measures for use with administrative data. Med Care 1998;36 (1) 8- 27
PubMed Link to Article
Clinical Outcomes of Surgical Therapy Study Group, A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 2004;350 (20) 2050- 2059
PubMed Link to Article
Veldkamp  RKuhry  EHop  WC  et al. COlon cancer Laparoscopic or Open Resection Study Group (COLOR), Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 2005;6 (7) 477- 484
PubMed Link to Article
Guillou  PJQuirke  PThorpe  H  et al. MRC CLASICC trial group, Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet 2005;365 (9472) 1718- 1726
PubMed Link to Article
Lacy  AMGarcía-Valdecasas  JCDelgado  S  et al.  Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 2002;359 (9325) 2224- 2229
PubMed Link to Article
Steele  SRBrown  TARush  RMMartin  MJ Laparoscopic vs open colectomy for colon cancer: results from a large nationwide population-based analysis. J Gastrointest Surg 2008;12 (3) 583- 591
PubMed Link to Article
Guller  UJain  NHervey  SPurves  HPietrobon  R Laparoscopic vs open colectomy: outcomes comparison based on large nationwide databases. Arch Surg 2003;138 (11) 1179- 1186
PubMed Link to Article
Kennedy  GDHeise  CRajamanickam  VHarms  BFoley  EF Laparoscopy decreases postoperative complication rates after abdominal colectomy: results from the National Surgical Quality Improvement Program. Ann Surg 2009;249 (4) 596- 601
PubMed Link to Article
Law  WLLee  YMChoi  HKSeto  CLHo  JW Impact of laparoscopic resection for colorectal cancer on operative outcomes and survival. Ann Surg 2007;245 (1) 1- 7
PubMed Link to Article
 Overview of the Nationwide Inpatient Sample (NIS). HCUP Web site. http://www.hcup-us.ahrq.gov/nisoverview.jsp. Accessed January 5, 2010
Dolan  JPDiggs  BSSheppard  BCHunter  JG The national mortality burden and significant factors associated with open and laparoscopic cholecystectomy: 1997 -2006. J Gastrointest Surg 2009;13 (12) 2292- 2301
PubMed Link to Article
Singla  ALi  YNg  SCCsikesz  NGTseng  JFShah  SA Is the growth in laparoscopic surgery reproducible with more complex procedures? Surgery 2009;146 (2) 367- 374
PubMed Link to Article
Whelan  RLFranklin  MHolubar  SD  et al.  Postoperative cell mediated immune response is better preserved after laparoscopic vs open colorectal resection in humans. Surg Endosc 2003;17 (6) 972- 978
PubMed Link to Article
Gitzelmann  CAMendoza-Sagaon  MTalamini  MAAhmad  SAPegoli  W  JrPaidas  CN Cell-mediated immune response is better preserved by laparoscopy than laparotomy. Surgery 2000;127 (1) 65- 71
PubMed Link to Article
Senagore  AJStulberg  JJByrnes  JDelaney  CP A national comparison of laparoscopic vs open colectomy using the National Surgical Quality Improvement Project data. Dis Colon Rectum 2009;52 (2) 183- 186
PubMed Link to Article
Oomen  JLEngel  AFCuesta  MA Outcome of elective primary surgery for diverticular disease of the sigmoid colon: a risk analysis based on the POSSUM scoring system. Colorectal Dis 2006;8 (2) 91- 97
PubMed Link to Article
McArdle  CS McMillan  DCHole  DJ Male gender adversely affects survival following surgery for colorectal cancer. Br J Surg 2003;90 (6) 711- 715
PubMed Link to Article
Dent  OFChapuis  PHRenwick  AABokey  EL The importance of tumor stage and relative survival analysis for the association between sex and survival after resection of colorectal cancer. Ann Surg 2009;249 (3) 402- 408
PubMed Link to Article
Khuri  SFNajjar  SFDaley  J  et al. VA National Surgical Quality Improvement Program, Comparison of surgical outcomes between teaching and nonteaching hospitals in the Department of Veterans Affairs. Ann Surg 2001;234 (3) 370- 382
PubMed Link to Article

Figures

Tables

Table Graphic Jump LocationTable 1. Demographics of Patients Who Underwent Colectomy Between 2002 and 2007 in the NIS
Table Graphic Jump LocationTable 2. Multivariate Analysis of In-Hospital Mortality Following Colectomy Between 2002 and 2007a

References

Callahan  MAChristos  PJGold  HTMushlin  AIDaly  JM Influence of surgical subspecialty training on in-hospital mortality for gastrectomy and colectomy patients. Ann Surg 2003;238 (4) 629- 636
PubMed
Cohen  MEBilimoria  KYKo  CYRichards  KHall  BL Effect of subjective preoperative variables on risk-adjusted assessment of hospital morbidity and mortality. Ann Surg 2009;249 (4) 682- 689
PubMed Link to Article
Kemp  JAFinlayson  SR Outcomes of laparoscopic and open colectomy: a national population-based comparison. Surg Innov 2008;15 (4) 277- 283
PubMed Link to Article
Varela  JEAsolati  MHuerta  SAnthony  T Outcomes of laparoscopic and open colectomy at academic centers. Am J Surg 2008;196 (3) 403- 406
PubMed Link to Article
Longo  WEVirgo  KSJohnson  FE  et al.  Risk factors for morbidity and mortality after colectomy for colon cancer. Dis Colon Rectum 2000;43 (1) 83- 91
PubMed Link to Article
Ragg  JLWatters  DAGuest  GD Preoperative risk stratification for mortality and major morbidity in major colorectal surgery. Dis Colon Rectum 2009;52 (7) 1296- 1303
PubMed Link to Article
Muscari  FSuc  BMsika  S  et al. French Federation for Surgical Research, Surgeon-dependent predictive factors for mortality after elective colorectal resection and immediate anastomosis for cancer or nonacute diverticular disease: multivariable analysis of 2,605 patients. J Am Coll Surg 2008;207 (6) 888- 895
PubMed Link to Article
Karanicolas  PJDubois  LColquhoun  PHSwallow  CJWalter  SDGuyatt  GH The more the better?: the impact of surgeon and hospital volume on in-hospital mortality following colorectal resection. Ann Surg 2009;249 (6) 954- 959
PubMed Link to Article
Kwan  TLLai  FLam  CM  et al.  Population-based information on emergency colorectal surgery and evaluation on effect of operative volume on mortality. World J Surg 2008;32 (9) 2077- 2082
PubMed Link to Article
Cohen  MEBilimoria  KYKo  CYHall  BL Development of an American College of Surgeons National Surgery Quality Improvement Program: morbidity and mortality risk calculator for colorectal surgery. J Am Coll Surg 2009;208 (6) 1009- 1016
PubMed Link to Article
Pepin  JVo  TTBoutros  M  et al.  Risk factors for mortality following emergency colectomy for fulminant Clostridium difficile infection. Dis Colon Rectum 2009;52 (3) 400- 405
PubMed Link to Article
Sailhamer  EACarson  KChang  Y  et al.  Fulminant Clostridium difficile colitis: patterns of care and predictors of mortality. Arch Surg 2009;144 (5) 433- 439
PubMed Link to Article
Antolovic  DKoch  MHinz  U  et al.  Ischemic colitis: analysis of risk factors for postoperative mortality. Langenbecks Arch Surg 2008;393 (4) 507- 512
PubMed Link to Article
Vibert  EBretagnol  FAlves  APocard  MValleur  PPanis  Y Multivariate analysis of predictive factors for early postoperative death after colorectal surgery in patients with colorectal cancer and synchronous unresectable liver metastases. Dis Colon Rectum 2007;50 (11) 1776- 1782
PubMed Link to Article
Birkmeyer  NJGu  NBaser  OMorris  AMBirkmeyer  JD Socioeconomic status and surgical mortality in the elderly. Med Care 2008;46 (9) 893- 899
PubMed Link to Article
Elixhauser  ASteiner  CHarris  DRCoffey  RM Comorbidity measures for use with administrative data. Med Care 1998;36 (1) 8- 27
PubMed Link to Article
Clinical Outcomes of Surgical Therapy Study Group, A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 2004;350 (20) 2050- 2059
PubMed Link to Article
Veldkamp  RKuhry  EHop  WC  et al. COlon cancer Laparoscopic or Open Resection Study Group (COLOR), Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 2005;6 (7) 477- 484
PubMed Link to Article
Guillou  PJQuirke  PThorpe  H  et al. MRC CLASICC trial group, Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet 2005;365 (9472) 1718- 1726
PubMed Link to Article
Lacy  AMGarcía-Valdecasas  JCDelgado  S  et al.  Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 2002;359 (9325) 2224- 2229
PubMed Link to Article
Steele  SRBrown  TARush  RMMartin  MJ Laparoscopic vs open colectomy for colon cancer: results from a large nationwide population-based analysis. J Gastrointest Surg 2008;12 (3) 583- 591
PubMed Link to Article
Guller  UJain  NHervey  SPurves  HPietrobon  R Laparoscopic vs open colectomy: outcomes comparison based on large nationwide databases. Arch Surg 2003;138 (11) 1179- 1186
PubMed Link to Article
Kennedy  GDHeise  CRajamanickam  VHarms  BFoley  EF Laparoscopy decreases postoperative complication rates after abdominal colectomy: results from the National Surgical Quality Improvement Program. Ann Surg 2009;249 (4) 596- 601
PubMed Link to Article
Law  WLLee  YMChoi  HKSeto  CLHo  JW Impact of laparoscopic resection for colorectal cancer on operative outcomes and survival. Ann Surg 2007;245 (1) 1- 7
PubMed Link to Article
 Overview of the Nationwide Inpatient Sample (NIS). HCUP Web site. http://www.hcup-us.ahrq.gov/nisoverview.jsp. Accessed January 5, 2010
Dolan  JPDiggs  BSSheppard  BCHunter  JG The national mortality burden and significant factors associated with open and laparoscopic cholecystectomy: 1997 -2006. J Gastrointest Surg 2009;13 (12) 2292- 2301
PubMed Link to Article
Singla  ALi  YNg  SCCsikesz  NGTseng  JFShah  SA Is the growth in laparoscopic surgery reproducible with more complex procedures? Surgery 2009;146 (2) 367- 374
PubMed Link to Article
Whelan  RLFranklin  MHolubar  SD  et al.  Postoperative cell mediated immune response is better preserved after laparoscopic vs open colorectal resection in humans. Surg Endosc 2003;17 (6) 972- 978
PubMed Link to Article
Gitzelmann  CAMendoza-Sagaon  MTalamini  MAAhmad  SAPegoli  W  JrPaidas  CN Cell-mediated immune response is better preserved by laparoscopy than laparotomy. Surgery 2000;127 (1) 65- 71
PubMed Link to Article
Senagore  AJStulberg  JJByrnes  JDelaney  CP A national comparison of laparoscopic vs open colectomy using the National Surgical Quality Improvement Project data. Dis Colon Rectum 2009;52 (2) 183- 186
PubMed Link to Article
Oomen  JLEngel  AFCuesta  MA Outcome of elective primary surgery for diverticular disease of the sigmoid colon: a risk analysis based on the POSSUM scoring system. Colorectal Dis 2006;8 (2) 91- 97
PubMed Link to Article
McArdle  CS McMillan  DCHole  DJ Male gender adversely affects survival following surgery for colorectal cancer. Br J Surg 2003;90 (6) 711- 715
PubMed Link to Article
Dent  OFChapuis  PHRenwick  AABokey  EL The importance of tumor stage and relative survival analysis for the association between sex and survival after resection of colorectal cancer. Ann Surg 2009;249 (3) 402- 408
PubMed Link to Article
Khuri  SFNajjar  SFDaley  J  et al. VA National Surgical Quality Improvement Program, Comparison of surgical outcomes between teaching and nonteaching hospitals in the Department of Veterans Affairs. Ann Surg 2001;234 (3) 370- 382
PubMed Link to Article

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The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
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For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
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