Abstract
Background and Objectives:
The applications of laparoscopic surgery are expanding, but there is still controversy about its application in patients with peritonitis resulting from diverticulitis perforation. This study aimed to investigate the factors affecting the postoperative mortality rate in patients undergoing surgery for perforated diverticulitis. Further, we compared the recovery courses of patients between open and laparoscopic surgeries.
Methods:
We analyzed the medical records of adult patients with peritonitis caused by perforated diverticulitis from six hospitals of Hallym University Medical Center from January 2006 to December 2016.
Results:
A total of 166 patients were identified. In the univariate analysis, the statistically significant factors associated with postoperative mortality were age ≥ 60 years, body mass index ≥ 23 kg/m2, American Society of Anesthesiologists score ≥ 3, hypertension, serum blood urea nitrogen ≥ 23 mg/dL, creatinine ≥ 1.2 mg/dL, albumin < 3.0 g/dL, modified Hinchey score ≥ grade III, formation of stoma, and laparoscopic surgery. In multivariate analysis, serum albumin < 3.0 g/dL was the only factor associated with mortality. After case-control matching, we compared postoperative hospital course and prognosis between open and laparoscopic surgery groups. There was no significant difference in the clinical course between the groups. No significant difference was observed in the complication rate, reoperation rate, readmission rate, and mortality.
Conclusion:
Low preoperative serum albumin level (<3.0 g/dL) affects the mortality rate of patients after surgery. The hospital course and prognosis after laparoscopic surgery and conventional open surgery are comparable in patients with peritonitis caused by diverticulitis perforation.
Keywords: Laparoscopic Surgery, Diverticular Diseases, Colonic Diverticulum
INTRODUCTION
Colonic diverticular disease is common in the Western population but is rare among Asians.1 The incidence of this disease is highly related to a high-protein and low-fiber diet, and the occurrence rate is gradually increasing in Korea based on the westernization of diet.2
The treatment of acute diverticulitis depends on the severity of the disease.3 Simple diverticulitis can be sufficiently treated with antibiotics, but perforated diverticulitis with peritonitis requires surgery. Of the patients with diverticulitis, 25% require surgery,4 and various surgical procedures such as ostomy, stepped bowel resection, and simple peritoneal lavage are used for treatment.5
The applications of laparoscopic surgery are gradually increasing. However, laparoscopic surgery for peritonitis is still controversial. This is because of the theoretical background that bacteremia and endotoxemia can get worse if air is introduced into the abdomen causing aeroperitonia.6,7
In this study, therefore, we were going to evaluate the stability of laparoscopic surgery in patients with peritonitis caused by perforated diverticulitis. This study aimed to determine the preoperative factors affecting mortality after surgery in patients with perforated diverticulitis requiring surgical treatment to determine whether laparoscopic surgery affects the outcome, and to compare the recovery courses of patients after open surgery and laparoscopic surgery to check if they produce similar results.
PATIENTS AND METHODS
Research Design
We retrospectively reviewed the medical records of patients who underwent surgery for peritonitis caused by perforated diverticulitis at six hospitals of Hallym University Medical Center (Hallym University Sacred Heart Hospital, Kangnam Sacred Heart Hospital, Chuncheon Sacred Heart Hospital, Hangang Sacred Heart Hospital, Dongtan Sacred Heart Hospital, Kangdong Sacred Heart Hospital) between January 2006 and December 2016. The Institutional Review Board of Dongtan Sacred Heart Hospital approved this study.
Inclusion Criteria
Patients who were diagnosed with peritonitis caused by perforated diverticulitis were hospitalized and underwent surgery were included.
Exclusion Criteria
Patients aged < 19 years or ≥ 91 years, expectant mothers, and patients with postoperative pathologic findings were excluded if the perforation of the diverticulum was not confirmed.
Number of Patients
This study was a retrospective, observational study where no specific hypothesis testing was performed. A total of 524 patients were recruited. Of them, 358 patients were excluded due to exclusion criteria. As a result, 166 patients were examined without the need for a separate sample count calculation.
Assessment Methods
We analyzed the age, sex, underlying disease, medical history, social history, body mass index, and American Society of Anesthesiologists scores of patients who underwent peritonitis surgery because of perforated diverticulitis. We analyzed the history such as previous abdominal surgery, history of diverticulitis, and history of constipation, as well as social history concerning smoking and drinking. Further, we analyzed the body temperature and levels of white blood cell, serum C-reactive protein, blood urea nitrogen, creatinine, total bilirubin, direct bilirubin, and albumin at the time of admission. Modified Hinchey score, perforation location, operation method, and duration of operation were analyzed in patients who underwent surgery. The modified Hinchey score was referenced in 1999 by Wasvary et al.8 with the following classification (Hinchey classification (Wasvary Modification):
0 Mild clinical diverticulitis
Ia Confined pericolic inflammation or phlegmon
Ib Pericolic or mesocolic abscess
II Pelvic, distant intra-abdominal or retroperitoneal abscess
III Generalized purulent peritonitis
IV Generalized fecal peritonitis
For determining location of perforation, cecum, ascending colon, and hepatic flexure were classified as the right side and splenic flexure, descending colon, and S colon were classified as the left side.
Surgical procedures were classified based on the choice of open or laparoscopic procedures, bowel resection requirement, and formation of ostomy. Because this study was a retrospective study, there were no clear criteria for determining the surgical procedure. Therefore, the surgical procedure was determined by the physician according to the patient's condition.
We analyzed patients who underwent surgery for peritonitis resulting from perforated diverticulitis for recovery time of bowel movements, time to drinking, time to ingestion of soft meal, duration of hospitalization, complication, reoperation, and death. The recovery time was the first time the patient farted after surgery. Complications were defined as enteritis, enteroplegia, anastomotic leakage, wound infection, pneumonia, cardiovascular disease (such as heart failure and pulmonary embolism), acute renal failure, and sepsis. Reoperation was defined as an operation performed to treat complications appearing within 1 month after surgery. Finally, death was defined as death occurring within 1 month after surgery.
Univariate and multivariate analyses were performed to find predictors in patients who died after surgery. Case-control matching was performed to compare open and laparoscopic surgeries for postoperative outcome and prognosis of patients who underwent surgery. Matching was performed based on factors that were significant in univariate and multivariate analyses to find predictors in patients who died after surgery. As a result, 40 patients were selected from each group and compared.
Statistical Processing
The results were expressed as mean (standard deviation) paired-sample t-test was performed for the comparison of continuous variables. The discontinuous variables were expressed as the number of patients and percentage (%), or number of patients after crossover analysis. Univariate analysis was performed using Fisher's exact test. Multivariate analysis was performed using logistic regression to analyze factors that predict postoperative complications. Case-control matching was performed based on factors significantly associated with multivariate and univariate analyses. Statistical analysis was performed using SPSS version 21.0 (Chicago, Illinois, USA) and P < .05 was used for statistical significance.
RESULTS
Patient Characteristics
During the 11-year study period, 524 patients were included. Of them, 358 patients were excluded due to exclusion criteria. As a result, 166 patients were included, of whom, 107 and 59 underwent open laparoscopic surgeries, respectively. The mean age of the patients was 54.8 years. There were 99 males and 67 females. The distribution of Modified Hinchey score was as follows: 27.7% in Ia, 24.7% in Ib, 23.5% in II, 21.7% in III, and 2.4% in IV. With regard to the location of perforation, right side perforations were observed in 91 patients and left side in 75 patients, with more patients having right side perforations. Most patients underwent bowel resection (90.4%) and 50 patients (30.1%) developed ostomy (Table 1).
Table 1.
Patient's Demographics and Clinical Manifestation
| No (%) | |
|---|---|
| Age (years) | 54.8 (17.8) |
| Male:female | 99:67 |
| BMI (kg/m2) | 23.9 (3.6) |
| ASA, n (%) | |
| 1 | 58 (34.9) |
| 2 | 65 (39.2) |
| 3 | 40 (24.1) |
| 4 | 2 (1.2) |
| 5 | 1 (0.6) |
| Hypertension, n (%) | 45 (27.1) |
| Hepatitis, n (%) | 4 (2.4) |
| DM, n (%) | 20 (12.0) |
| Tuberculosis, n (%) | 3 (1.8) |
| Abdominal operation history, n (%) | 45 (27.1) |
| Constipation, n (%) | 13 (7.8) |
| Smoking, n (%) | 49 (29.5) |
| Alcohol, n (%) | 22 (13.3) |
| History of diverticulitis, n (%) | 13 (7.8) |
| Body temperature (°C) | 37.4 (1.0) |
| WBC (×103/μL) | 12.9 (5.0) |
| Serum CRP (mg/L) | 117.1 (91.5) |
| Serum BUN (mg/dL) | 17.1 (11.6) |
| Serum creatinine (mg/dL) | 1.04 (0.87) |
| Serum total bilirubin (mg/dL) | 1.3 (1.4) |
| Serum direct bilirubin (mg/dL) | 0.5 (1.1) |
| Serum albumin (g/dL) | 3.9 (0.7) |
| Modified hinchey score, n (%) | |
| Ia | 46 (27.7) |
| Ib | 41 (24.7) |
| II | 39 (23.5) |
| III | 36 (21.7) |
| IV | 4 (2.4) |
| Perforation site, n (%) | |
| Right | 91 (54.8) |
| Left | 75 (45.2) |
| Operation method, n (%) | |
| Laparoscopy | 59 (35.5) |
| Open | 107 (64.5) |
| Bowel resection, n (%) | 150 (90.4) |
| Laparoscopy | 55 |
| Open | 95 |
| Stoma formation, n (%) | 50 (30.1) |
| Laparoscopy | 4 |
| Open | 46 |
| Operation time (min) | 172.9 (67.6) |
Data are presented as the number of patients (%) or mean (standard deviation) unless otherwise stated.
ASA, American Society of Anesthesiologists; BMI, body mass index; BUN, blood urea nitrogen; CRP, C-reactive protein; DM, diabetes mellitus; WBC, white blood cell.
Rehospitalization and reoperation rates were 5.4% and 4.8%, respectively. The complication and mortality rates were 43.4% and 8.4%, respectively (Table 2).
Table 2.
Patient's Clinical Course After Surgery
| No (%) | |
|---|---|
| Time to gas passing (days) | 3.6 (2.0) |
| Time to drinking water (days) | 4.9 (2.9) |
| Time to soft diet (days) | 6.4 (3.2) |
| Length of hospital stay (days) | 18.2 (12.0) |
| Post-operation hospital stay (days) | 14.7 (11.4) |
| Complication, n (%) | 72 (43.4) |
| Re-admission, n (%) | 9 (5.4) |
| Re-operation, n (%) | 8 (4.8) |
| Mortality, n (%) | 14 (8.4) |
Data are presented as the number of patients (%) or mean (standard deviation) unless otherwise stated.
Predictors of Postoperative Death
Univariate and multivariate analysis for various factors were performed to determine the factors that predicted postoperative death. A serum albumin level of less than 3.0 g/dL was the only factor that significantly associated with mortality (P = .011; Table 3).
Table 3.
Univariate and Multivariate Analyses of Mortality
| Variable | Univariate Analysis |
Multivariate Analysis |
||
|---|---|---|---|---|
| OR (95% CI) | P | OR (95% CI) | P | |
| Age ≥ 60 years | 19.393 (2.473–152.107) | .005 | 5.403 (0.464–62.985) | .178 |
| Males | 0.652 (0.218–1.953) | .445 | ||
| BMI ≥ 23 kg/m2 | 0.192 (0.040–0.924) | .040 | 0.570 (0.043–7.589) | .670 |
| ASA ≥ 3 | 4.457 (1.449–13.713) | .009 | 0.665 (0.102–4.318) | .669 |
| Hypertension | 8.357 (2.469–28.292) | .001 | 3.687 (0.633–21.454) | .147 |
| DM | 1.241 (0.257–5.998) | .788 | ||
| Hepatitis | 3.821 (0.371–39.388) | .260 | ||
| Tuberculosis | 2.020 (0.243–16.783) | .515 | ||
| Abdominal operation history | 3.000 (0.989–9.104) | .052 | ||
| Constipation | 0.897 (0.108–7.459) | .920 | ||
| Smoking | 0.167 (0.021–1.311) | .089 | ||
| Alcohol | 0.442 (0.055–3.541) | .442 | ||
| History of diverticulitis | 0.897 (0.108–7.459) | .920 | ||
| Body temperature ≥ 38.3°C | 0.373 (0.047–2.976) | .352 | ||
| WBC ≥ 10 × 103/μL | 0.492 (0.161–1.506) | .214 | ||
| Serum CRP ≥ 40 mg/L | 0.493 (0.141–1.715) | .266 | ||
| Serum BUN ≥ 23 mg/dL | 4.432 (1.402–14.009) | .011 | 1.010 (0.169–6.060) | .991 |
| Serum creatinine ≥ 1.2 mg/dL | 6.238 (1.986–19.592) | .002 | 6.320 (0.976–40.945) | .053 |
| Serum total bilirubin ≥ 1.2 mg/dL | 0.955 (0.194–6.199) | .961 | ||
| Serum direct bilirubin ≥ 1.2 mg/dL | 0.356 (0.100–1.276) | .113 | ||
| Serum albumin < 3.0 g/dL | 16.000 (3.135–81.665) | .001 | 22.811 (2.068–251.587) | .011 |
| Modified Hinchey score ≥ III | 5.000 (1.618–15.448) | .005 | 2.186 (0.320–14.933) | .425 |
| Left side perforation | 2.345 (0.751–7.329) | .142 | ||
| Bowel resection | 1.423 (0.174–11.654) | .742 | ||
| Stoma formation | 3.492 (1.143–10.666) | .028 | 0.332 (0.046–2.404) | .275 |
| Laparoscopy | 8.021 (1.022–62.942) | .048 | 2.480 (0.157–39.161) | .519 |
| Operation time ≥ 180 min | 2.685 (0.859–8.399) | .090 | ||
ASA, American Society of Anesthesiologists; BMI, body mass index; BUN, blood urea nitrogen; CI, confidence interval; CRP, C-reactive protein; DM, diabetes mellitus; OR, odds ratio; WBC, white blood cell.
Comparison Between Open Surgery and Laparoscopic Surgery After Case Matching
Case-control matching was performed to compare the open surgery group and laparoscopic group after reducing the differences in factors that may affect the recovery process. In all, 40 patients were selected for performing case-control matching with different variables (age, body mass index, American Society of Anesthesiologists score, hypertension, serum blood urea nitrogen level, creatinine level, albumin level, modified Hinchey score, formation of ostomy, and laparoscopic surgery), which were significantly associated with postoperative mortality in the univariate analysis. There were no statistically significant differences between the two groups in terms of factors that could affect the prognosis (Table 4 and Table 5).
Table 4.
Patients' Demographics and Clinical Manifestation According to the Type of Surgery (Case-Control Matching)
| Open (n = 40) | Laparoscopy (n = 40) | P | |
|---|---|---|---|
| Age (years) | 43.2 (17.1) | 47.4 (16.0) | .263 |
| Male, n (%) | 29 (72.5) | 27 (67.5) | .807 |
| BMI (kg/m2) | 24.4 (4.4) | 24.4 (3.3) | .981 |
| ASA (%) | .765 | ||
| 1 | 19 (47.5) | 20 (50.0) | |
| 2 | 17 (42.5) | 15 (37.5) | |
| 3 | 4 (10.0) | 4 (10.0) | |
| 4 | 0 (0.0) | 1 (2.5) | |
| 5 | 0 (0.0) | 0 (0.) | |
| Underlying disease, n (%) | 10 (25.0) | 12 (30.0) | .802 |
| Hypertension | 5 | 9 | .239 |
| DM | 1 | 4 | .359 |
| Abdominal operation history, n (%) | 12 (30.0) | 10 (25.0) | .802 |
| Constipation, n (%) | 0 (0.0) | 1 (2.5) | 1.000 |
| Alcohol, n (%) | 6 (15.0) | 10 (25.0) | .402 |
| Smoking, n (%) | 20 (50.0) | 13 (32.5) | .173 |
| History of diverticulitis, n (%) | 4 (10.0) | 4 (10.0) | 1.000 |
| Body temperature (°C) | 37.4 (0.83) | 37.6 (0.84) | .281 |
| WBC (×103/μL) | 14.9 (5.8) | 13.1 (4.3) | .116 |
| Serum CRP (mg/L) | 122.9 (91.5) | 98.0 (64.7) | .321 |
| Serum BUN (mg/dL) | 14.0 (12.9) | 12.9 (5.5) | .615 |
| Serum creatinine (mg/dL) | 0.84 (0.16) | 0.89 (0.20) | .194 |
| Serum total bilirubin (mg/dL) | 1.2 (1.0) | 1.2 (0.6) | .919 |
| Serum direct bilirubin (mg/dL) | 0.3 (0.2) | 0.4 (0.3) | .153 |
| Serum albumin (g/dL) | 4.0 (0.6) | 4.1 (0.4) | .460 |
| Modified Hinchey score, n (%) | .575 | ||
| Ia | 14 (35.0) | 14 (35.0) | |
| Ib | 16 (40.0) | 10 (25.0) | |
| II | 7 (17.5) | 12 (30.0) | |
| III | 2 (5.0) | 3 (7.5) | |
| IV | 1 (2.5) | 1 (2.5) | |
| Perforation site, n (%) | .401 | ||
| Right | 28 (70.0) | 30 (75.0) | |
| Left | 12 (30.0) | 10 (25.0) |
Data are presented as the number of patients (%) or mean (standard deviation) unless otherwise stated.
ASA, American Society of Anesthesiologists; BMI, body mass index; BUN, blood urea nitrogen; CRP, C-reactive protein; DM, diabetes mellitus; WBC, white blood cell.
Table 5.
Comparison Between Open and Laparoscopy Group (Case-Control Matching)
| Open (n = 40) | Laparoscopy (n = 40) | P | |
|---|---|---|---|
| Bowel resection, n (%) | 36 (90.0) | 36 (90.0) | 1.000 |
| Stoma formation, n (%) | 7 (17.5) | 4 (10.0) | .518 |
Data are presented as the number of patients (%) or mean (standard deviation) unless otherwise stated.
There was no statistically significant difference in prognosis (Table 6).
Table 6.
Clinical Recovery Course According to the Type of Surgery (Case-Control Matching)
| Open (n = 40) | Laparoscopy (n = 40) | P | |
|---|---|---|---|
| Time to gas passing (days) | 3.2 (1.4) | 3.0 (1.7) | .776 |
| Time to drinking water (days) | 4.6 (2.2) | 3.8 (1.4) | .067 |
| Time to soft diet (days) | 5.9 (2.3) | 5.2 (1.5) | .080 |
| Length of hospital stay (days) | 15.8 (8.9) | 14.0 (6.0) | .279 |
| Postoperative hospital stay (days) | 12.1 (7.5) | 10.7 (6.0) | .361 |
| Complication, n (%) | 14 (35.0) | 13 (32.6) | 1.000 |
| Re-admission, n (%) | 2 (5.0) | 4 (10.0) | .675 |
| Re-operation, n (%) | 2 (5.0) | 0 (0.0) | .464 |
| Mortality, n (%) | 1 (2.5) | 1 (2.5) | 1.000 |
Data are presented as the number of patients (%) or mean (standard deviation) unless otherwise stated.
DISCUSSION
Colonic diverticular disease is a condition where in small sacs protrude abnormally from the colon wall. It can be classified as a true diverticulum in which the entire layer of the colon is pushed out and a false diverticulum in which there are mucosa or submucosal protrusions through the weakened wall of the colon due to degenerative changes.1–3 The Western population is more likely to have false diverticulum of the S colon, while Asian patients have frequent occurrences of appendicitis and true diverticulum of the ascending colon.2,3
The diverticulum of the large intestine is mostly symptomless, but it causes various problems depending on the progression. Among them, diverticulitis is a common condition. The feces enter the diverticulum and form feces stones that cause erosion of the mucous membrane of the diverticula. If this condition persists, inflammation becomes more severe and spreads to other tissues around the diverticulum. Western and Oriental sex ratios of diverticulitis differ slightly. In the case of the West, the ratio of male to female is similar, or 1:1.5∼2, with a higher occurrence in females.9 In Korea and Asia, however, the male to female ratio is 1.5:1, with a higher occurrence in males.10 In this study, the male to female incidence was 1.47:1, which was higher in males.
If inflammation of the diverticulum gets worse, about 15% patients have complications such as perforation.11 In most cases, perforation with peritonitis requires emergency surgery.1,3–5 Although the incidence of perforating peritonitis is low, once it occurs, the mortality rate is 4% to 26% regardless of the treatment method.12–15 In our study, mortality after surgery was observed in 14 of 166 patients (8.4%).
Many studies have suggested that poor preoperative nutritional status adversely affects recovery after surgery,16,17 and postoperative complications and mortality are likely to increase.18–20 Serum albumin acts as a carrier of various minerals, hormones, and fatty acids and plays an important role in maintaining the osmotic pressure between blood vessels and tissues,21 and albumin levels are used as one of the various measures for assessing the nutritional status in patients.22–24 In this study, serum albumin levels below 3.0 g/dL were associated with postoperative mortality (OR, 22.811; 95% CI, 2.068–251.587; P = .011). This suggests that a low serum albumin level reflects poor nutritional status before surgery and this affects postoperative mortality.
Laparoscopic colonic surgery has been shown not to be inferior to open surgery in terms of postoperative recovery in several studies.25–27 In this study, according to the prognosis of the two groups after case matching, there was no significant difference between the laparoscopic surgery group and the open surgery group with regard to the time to recovery (3.2 days vs. 3.0 days; P = .776), time to drinking (4.6 days vs. 3.8 days; P = .067), time to ingestion of soft meal (5.9 days vs. 5.2 days; P = .080), total duration of hospitalization (15.8 days vs. 14.0 days; P = .279), and postoperative duration of hospitalization (12.1 days vs. 10.7 days; P = .361). In addition, there were no statistically significant differences in the complication rate (35.0% vs. 32.6%; P = 1.000), reoperation rate (5.0% vs. 10.0%; P = .675), readmission rate (5.0% vs. 0.0%; P = .464), and mortality (2.5% vs. 2.5%; P = 1.000) between groups. Based on this, we believe that the recovery and prognosis after laparoscopic surgery in peritonitis patients with perforated diverticulitis are not inferior to those after open surgery.
This study has some limitations. First, because this study is a retrospective study, there could be selection bias. The process of determining the surgical procedure in the course of treatment was not recorded in the medical record and could not be evaluated. Second, because this study was conducted for multiple institutions rather than a single institution, it is possible that the operation method changed according to the doctor's experience and preference. Third, the number of patients in the laparoscopic surgery group was lower than that in the open surgery group, and high-risk patients in the open surgery group were excluded from case-matching. Although these limitations exist, this study is significant and confirms the factors affecting postoperative mortality, and laparoscopic surgery may be a good choice in peritonitis cause by perforated diverticulitis. We believe that a prospective study is required with a higher number of cases in the future.
CONCLUSION
In cases where the preoperative serum albumin level is low, postoperative mortality is high. On comparing the open surgery group and laparoscopic surgery group after case-control matching, postoperative recovery progress in the laparoscopic surgery group was not bad compared with that in the open surgery group for patients with peritonitis caused by perforated diverticulitis.
Contributor Information
Sung Bak An, Department Of Surgery, Hallym University Medical Center, Dongtan Sacred Heart Hospital, Hwaseong, Republic of Korea.
Byung Chun Kim, Department Of Surgery, Hallym University Medical Center, Kangnam Sacred Heart Hospital, Seoul, Republic of Korea.
Jeong Yeon Kim, Department Of Surgery, Hallym University Medical Center, Dongtan Sacred Heart Hospital, Hwaseong, Republic of Korea.
Jong Wan Kim, Department Of Surgery, Hallym University Medical Center, Dongtan Sacred Heart Hospital, Hwaseong, Republic of Korea.
Sang-Jeon Lee, Department of Surgery, College of Medicine, Chungbuk National University and Hospital, Cheongju, Republic of Korea.
References:
- 1. Almy TP, Howell DA. Medical progress. Diverticular disease of the colon. N Engl J Med. 1980;302:324–331. [DOI] [PubMed] [Google Scholar]
- 2. Kim SH, Byun CG, Cha JW, Choi SH, Kho YT, Seo DY. Comparative study of the clinical features and treatment for right and left colonic diverticulitis. J Korean Soc Coloproctol. 2010;26:407–412. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. Etzioni DA, Mack TM, Beart RW, Jr, Kaiser AM. Diverticulitis in the United States: 1998–2005: changing patterns of disease and treatment. Ann Surg. 2009;249:210–217. [DOI] [PubMed] [Google Scholar]
- 4. Law WL, Lo CY, Chu KW. Emergency surgery for colonic diverticulitis: differences between right-sided and left-sided lesions. Int J Colorectal Dis. 2001;16:280–284. [DOI] [PubMed] [Google Scholar]
- 5. Vermeulen J, Lange JF. Treatment of perforated diverticulitis with generalized peritonitis: past, present, and future. World J Surg. 2010;34:587–593. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Ozmen MM, Cöl C, Aksoy AM, Tekeli FA, Berberoglu M. Effect of CO(2) insufflation on bacteremia and bacterial translocation in an animal model of peritonitis. Surg Endosc. 1999;13:801–803. [DOI] [PubMed] [Google Scholar]
- 7. Horattas MC, Haller N, Ricchiuti D. Increased transperitoneal bacterial translocation in laparoscopic surgery. Surg Endosc. 2003;17:1464–1467. [DOI] [PubMed] [Google Scholar]
- 8. Wasvary H, Turfah F, Kadro O. Same hospitalization resection for acute diverticulitis. Am Surg. 1999;65:632–635; discussion 636. [PubMed] [Google Scholar]
- 9. Weizman AV, Nguyen GC. Diverticular disease: epidemiology and management. Can J Gastroenterol. 2011;25:385–389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Song JH, Kim YS, Lee JH, et al. Clinical characteristics of colonic diverticulosis in Korea: a prospective study. Korean J Intern Med. 2010;25:140–146. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Parks TG. Natural history of diverticular disease of the colon. Clin Gastroenterol. 1975;4:53–69. [PubMed] [Google Scholar]
- 12. Vermeulen J, Gosselink MP, Hop WCJ, et al. Hospital mortality after emergency surgery for perforated diverticulitis. Ned Tijdschr Geneesk. 2009;153:1209–1214. [PubMed] [Google Scholar]
- 13. Morris CR, Harvey IM, Stebbings WS, Hart AR. Incidence of perforated diverticulitis and risk factors for death in a UK population. Br J Surg. 2008;95:876–881. [DOI] [PubMed] [Google Scholar]
- 14. Salem L, Flum DR. Primary anastomosis or Hartmann's procedure for patients with diverticular peritonitis? A systematic review. Dis Colon Rectum. 2004;47:19531964. [DOI] [PubMed] [Google Scholar]
- 15. Constantinides VA, Tekkis PP, Senapati A. Prospective multicentre evaluation of adverse outcomes following treatment for complicated diverticular disease. Br J Surg. 2006;93:1503–1513. [DOI] [PubMed] [Google Scholar]
- 16. Correia MI, Waitzberg DL. The impact of malnutrition on morbidity, mortality, length of hospital stay and costs evaluated through a multivariate model analysis. Clin Nutr. 2003;22:235–239. [DOI] [PubMed] [Google Scholar]
- 17. Sullivan DH, Bopp MM, Roberson PK. Protein energy undernutrition and life-threatening complications among the hospitalized elderly. J Gen Intern Med. 2002;17:923–932. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Giner M, Laviano A, Meguid MM, Gleason JR. In 1995 a correlation between malnutrition and poor outcome in critically ill patients still exists. Nutrition. 1996;12:23–29. [DOI] [PubMed] [Google Scholar]
- 19. Sungurtekin H, Sungurtekin U, Balci C, Zencir M, Erdem E. The influence of nutritional status on complications after major intraabdominal surgery. J Am Coll Nutr. 2004;23:227–232. [DOI] [PubMed] [Google Scholar]
- 20. Lumbers M, Driver LT, Howland RJ, Older MW, Williams CM. Nutritional status and clinical outcome in elderly female surgical orthopaedic patients. Clin Nutr. 1996;15:101–107. [DOI] [PubMed] [Google Scholar]
- 21. Bharadwaj S, Ginoya S, Tandon P, et al. Malnutrition: laboratory markers vs nutritional assessment. Gastroenterol Rep (Oxf). 2016;4:272–280. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. Prenner G, Wasler A, Fahrleinter-Pammer A. The role of serum albumin in the prediction of malnutrition in patients at least five yr after heart transplantation. Clin Transplant. 2014;28:737–742. [DOI] [PubMed] [Google Scholar]
- 23. Cross MB, Yi PH, Thomas CF. Evaluation of malnutrition in orthopaedic surgery. J Am Acad Orthop Surg. 2014;22:193–199. [DOI] [PubMed] [Google Scholar]
- 24. Gama-Axelsson T, Heimbürger O, Stenvinkel P, Bárány P, Lindholm B, Qureshi AR. Serum albumin as predictor of nutritional status in patients with ESRD. Clin J Am Soc. Nephrol 2012;7:1446–1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Zheng MH, Feng B, Lu AG, et al. Laparoscopic versus open right hemicolectomy with curative intent for colon carcinoma. World J Gastroenterol. 2005;21:11:323–326. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. Desiderio J, Trastulli S, Ricci F, et al. Laparoscopic versus open left colectomy in patients with sigmoid colon cancer: prospective cohort study with long-term follow-up. Int J Surg. 2014;12:745–750. [DOI] [PubMed] [Google Scholar]
- 27. Nussbaum DP, Speicher PJ, Ganapathi AM, et al. Laparoscopic versus open low anterior resection for rectal cancer: results from the national cancer data base. J Gastrointest Surg. 2015;19:124–131; discussion 131–132. [DOI] [PMC free article] [PubMed] [Google Scholar]