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SURGICAL INFECTIONS

Volume X, Number X, 2015


Mary Ann Liebert, Inc.
DOI: 10.1089/sur.2014.148

Epidemiology and Microbiology of Secondary


Peritonitis Caused by Viscus Perforation:
A Single-Center Retrospective Study
Ji Young Jang,1 Seung Hwan Lee,2 Hongjin Shim,1 Jun Yong Choi,4 Dongeun Yong,3 and Jae Gil Lee 2

Abstract

Background: Complicated intra-abdominal infections are serious conditions that require urgent source control
and antibiotic treatment. The purpose of this study was to evaluate the epidemiology and bacterial causation of
such infections using blood and peritoneal cultures of Korean patients with peritonitis originating from viscus
perforation.
Methods: The medical records of 419 consecutive patients who underwent emergency surgery because of bowel
perforation from January 2007 to December 2011 were analyzed. Clinical characteristics, peri-operative conditions, perforation sites, and mortality data were obtained. Bacterial distributions and antibiotic resistance were
evaluated using blood and peritoneal culture reports.
Results: The most common perforation site was the colon (165; 39.4%), and the overall mortality rate was
11.2%. Blood cultures were performed in 182 patients, and 20 patients (11.0%) had a positive culture. Blood
culture positivity was significantly higher for colon perforations (17.7%) than perforations elsewhere
(p = 0.039). A peritoneal culture was performed for each of 210 patients (50.1%), and 145 of those patients
(69.0%) had a positive culture. Enterococcus faecium (35.2%) was the most common gram-positive bacterium,
and Escherichia coli was the most common gram-negative organism. There were 276 community-acquired
infections (CAI) (65.9%) and 143 hospital-acquired infections (HAI) (34.1%). Escherichia coli producing
extended-spectrum b-lactamases were more common in the HAI than in the CAI group (p = 0.016).
Conclusions: The compositions and antibiotic resistances of micro-organisms found in this study are similar to
those reported previously. A multicenter prospective study is needed of this disease state in South Korea.

are needed. During the initial stages, broad-spectrum antibiotics are selected empirically. Accordingly, knowledge of
the microbial distribution is essential, because physicians
must understand the regional distributions and characteristics
of bacteria to ensure an optimal empirical choice of antibiotic. In this context, a number of research studies have been
performed on bacteria resistant to newly developed antimicrobial agents [6,7]. After antimicrobial susceptibilities have
been determined, de-escalation or escalation of antibiotics is
desirable [3,8].
Although some guidelines on empiric antibiotics for IAIs
have been published, most studies on causative bacteria were
performed before the 2000s [13,5]. Furthermore, few studies have been published on peritonitis in Korean populations.

ntra-abdominal infections (IAIs) have clinical presentations that range from localized peritonitis to diffuse
inflammation of the abdominal cavity. Peritonitis may be
primary, secondary, or tertiary [1]; and secondary peritonitis
is the common form of intraperitoneal infection originating
from bowel injuries, such as perforation, strangulation, or
infection. Complicated intra-abdominal infections (cIAIs)
are defined as those extending beyond the original injury into
the peritoneal space with associated abscess formation or
peritonitis [2]. The most important treatment for patients with
secondary peritonitis attributable to hollow viscus perforation is removing the contamination source as soon as possible
[35]. In addition, fluid resuscitation, electrolyte supplementation, and the administration of appropriate antibiotics

Department of Surgery, Yonsei University Wonju College of Medicine, Wonju, Republic of Korea.
Departments of Surgery, 3Laboratory Medicine, and 4Internal Medicine and AIDS Research Institute, Yonsei University College of
Medicine, Seoul, Republic of Korea.
2

The purpose of this study was to evaluate the epidemiology


and bacterial distribution, as identified from blood and peritoneal cultures, of secondary peritonitis caused by hollow
viscus perforation in Korean patients who had undergone an
emergency operation.
Patients and Methods

This study was approved by the Severance Hospital Institutional Review Board (approval no. 4-2013-0802).
Patients

The medical records of 419 consecutive patients with


hollow viscus perforation who underwent emergency surgery
from January 2007 to December 2011 were reviewed retrospectively. Patients with perforated appendicitis or cholecystitis were excluded because peritoneal cultures were not
obtained routinely during laparoscopic surgery. The following data were extracted: Underlying disease, presence of perioperative hypotension (systolic blood pressure < 90 mm Hg),
systemic inflammatory response status (including sepsis,
severe sepsis, and septic shock as defined in the American
College of Chest Physicians/Society of Critical Care Medicine guidelines [9]), pre-operative antibiotics, post-operative
laboratory tests, re-operation, length of stay (LOS) in an intensive care unit (ICU), LOS in a hospital, days on mechanical ventilation, and date of death if relevant.
Pathology and culture data

Information about perforation sites was obtained from


the operative notes or pathology reports, and the sites were
classified as follows: Stomach or duodenum, small bowel, or
colon (including rectum). Results of peritoneal and blood cultures were collected by reviewing microbial culture studies.
Infections were classified as community-acquired (CAI) or
hospital-acquired (HAI) based on the timing of the diagnosis of
the IAI using a 48-h post-hospitalization cut-off to distinguish between the two [10,11]. Infections diagnosed after
48 h of hospitalization, such as with perforation during chemotherapy or other therapeutic intervention besides intraperitoneal infections, were classified as HAI.
A peritoneal culture was defined as a test performed on
aspirated or swabbed intraperitoneal fluid during surgery or
on drainage fluid after the immediate post-operative period.
When patients had suspected sepsis (temperature > 38.3C or
shock), a blood culture was performed from more than two sites
pre-operatively. When three bottles of blood samples were
obtained, the occurrence of an organism in two was interpreted
as a positive finding, and when two bottles of blood were
drawn, the occurrence of an organism in one was considered a
positive finding.
Microbiological tests

Antibiotic-resistant organisms were defined as follows:


Vancomycin-resistant Enterococcus (VRE), methicillinresistant Staphylococcus spp. (MRS), Escherichia coli producing an extended-spectrum beta-lactamase (ESBL), Klebsiella
pneumoniae with ESBL, carbapenem-resistant Pseudomonas
aeruginosa (CRPA), and carbapenem-resistant Acinetobacter
baumannii (CRAB).

JANG ET AL.

The isolates were identified using conventional biochemical methods (VITEK systems; bioMerieux, Hazelwood,
MO). Antimicrobial susceptibilities were measured using
disk-diffusion methods or the VITEK-2 N131 card (bioMerieux). Results were interpreted using the guidelines issued by the Clinical and Laboratory Standards Institute
(CLSI) in 2009 [12].
Statistical analysis

Continuous variables are expressed as means standard


deviations or medians (ranges). The w2 or Fisher exact test, as
appropriate, was used to compare categorical variables.
Statistical analysis was performed using SPSS version 20.0
(IBM, Inc., Armonk, NY), and two-sided p values < 0.05
were considered significant.

Table 1. Patient Demographics


No. (%)
Gender (male)/total
Age
Underlying diseasea
Cardiologic
Pulmonary
Endocrinologic
Nephrologic
Immunosuppression
Pre-operative hypotension (ED)
Pre-operative status (ED)
SIRS
Sepsis
Severe sepsis
Septic shock
Post-operative hypotension
Post-operative status
SIRS
Sepsis
Severe sepsis
Septic shock
Post-operative laboratory findings
WBC ( 103)
Hemoglobin
Platelets ( 103)
Base excess
Lactate
Reoperation
Community-acquired infection
Hospital-acquired infection
Hospital stay (d)
ICU admission
ICU stay (d)
Duration of MV (d)
Death

270 (64.4)/419
59.0 15.9
64
41
59
44
114
40/270

(15.3)
( 9.8)
(14.1)
(10.5)
(27.2)
(14.8)

52
127
34
20
96

(12.4)
(30.3)
( 8.1)
( 4.8)
(22.9)

99
180
63
50

(25.3)
(45.9)
(16.1)
(12.8)

10.8 7.5
11.6 4.4
207 (266,002)
- 7.1 5.7
2.6 2.3
46 (11.0)
276 (65.9)
143 (34.1)
17 ( 0201)
312 (74.5)
2 ( 0102)
1 ( 059)
47 (11.2)

a
Cardiologic disease: hypertensive disease, ischemic disease,
heart failure, cardiac dysrhythmias, valvular disease. Pulmonary
disease: chronic obstructive disease, pulmonary tuberculosis, pneumothorax, interstitial lung disease. Endocrine disease: diabetes
mellitus, hyperthyroidism, hypothyroidism, adrenal disease. Nephrologic disease: chronic renal dysfunction, end-stage renal
disease, nephrotic syndrome, nephritic syndrome. Immunosuppression: taking immunosuppressant or corticosteroid or receiving
chemotherapy within one year from the operation.
ED = emergency department; ICU = intensive care unit; MV = mechanical ventilation; SIRS = systemic inflammatory response syndrome.

PERITONITIS WITH VISCUS PERFORATION

Results
Demographics and clinical characteristics

Of the 419 study subjects, 270 (64.4%) were male, and the
mean age was 59.3 15.9 y. One hundred fourteen patients
(27.2%) had received a corticosteroid or chemotherapy
within one year of the operation. Fifty-nine (14.1%) had
endocrine disease. In the emergency room, 40 (14.8%) had
hypotension, 127 (30.3%) sepsis, 34 (8.1%) severe sepsis,
and 20 (4.8%) septic shock.
Monotherapy was given to 166 patients (39.6%) and
combination therapy to 253 patients (60.4%). Piperacillintazobactam (116; 69.9%) was the single agent most
frequently used, followed by a carbapenem (18; 10.8%)
and a second- (16; 9.6%) or third-generation (8; 4.8%)
cephalosporin. For combination therapy, a triple regimen
(second-or third-generation cephalosporin + aminoglycoside +
metronidazole) (90; 35.6%) was most common. Regimens
such as a third-generation cephalosporin plus metronidazole
(30; 11.9%), piperacillin-tazobactam plus metronidazole
(30), and a third-generation cephalosporin in combination
with aminoglycoside (23; 9.1%) also were prescribed. When
the appropriateness of antibiotic use was analyzed, an inappropriate antibiotic was found to have been used in 36 patients (8.6%). Post-operative hypotension developed in 96
patients (22.9%). The mean LOS in the hospital was 17 d
(range 1201 d), and 46 patients (11%) underwent re-operation. Two hundred seventy-six patients (65.9%) had a CAI
and 143 (34.1%) an HAI. Forty-seven patients (11.2%) died
in the hospital (Table 1).
The most common site of perforation was the colon or
rectum (n = 165), followed by the stomach or duodenum
(n = 136) and the small bowel (n = 105). Thirteen patients had
one or more perforations in multiple sites. In the CAI group,
perforation of the stomach or duodenum (74.3%) was more
common than perforation of the small bowel (62.9%), large
bowel (61.8%), or multiple sites (53.8%) (p = 0.081).
A peritoneal culture was performed in 210 patients
(50.1%), and microorganisms were identified in 145 (69%).
Blood cultures were performed in 182 patients (43.4%), and
microorganisms were found in 20 (11.0%). Blood culture

positivity was significantly more common in cases of colon


perforation (17.7%) than in the others (p = 0.039). Enterococcus spp. and E. coli were identified more often in
patients with perforation of the lower gastrointestinal tract
(p = 0.002 and 0.030, respectively). Klebsiella spp. also were
found more frequently in patients with small bowel perforation (p = 0.009). However, there was no influence of perforation site on mortality rate, peritoneal culture positivity, or
antibiotic resistance rate (p = 0.911, 0.331, and 0.151, respectively) (Table 2).
Microbiology of blood cultures

A blood culture was positive in 20 patients. The grampositive bacteria identified were Streptococcus spp. (5; 25%),
Staphylococcus epidermidis (4; 20%), E. faecium (3; 15%),
and E. avium (1; 5%). The gram-negative bacteria were E.
coli (7; 35%), P. aeruginosa (2; 10%), and Bacillus spp. and
Micrococcus spp. (1 each; 5%). The anaerobes were Bacteroides spp. (4; 20%), with one being B. fragilis. Candida
albicans was identified in one patient (Table 3).
Microbiology of peritoneal cultures

A peritoneal culture was positive in 145 patients (69.0%).


The most common organism was E. faecium (51; 35.2%),
followed by E. coli (29; 20%), Candida albicans (25; 17.2%),
and P. aeruginosa (17; 11.7%). The gram-positive bacteria
identified were E. faecium (51; 35.2%), E. faecalis (12;
8.3%), and other enterococci (14; 9.7%). The staphylococcal
species identified were S. aureus (10; 6.9%) and coagulasenegative staphylococci (13; 9.0%). Streptococcus spp. were
identified in 11 patients (7.6%). The gram-negative bacteria
were E. coli (29; 20%), P. aeruginosa (17; 11.7%), K.
pneumoniae (16; 11%), Enterobacter aerogenes (7; 4.8%),
and A. baumannii (12; 8.3%). For anaerobic organisms,
Bacteroides spp. were isolated from eight patients (5.5%),
and two patients (1.4%) had B. fragilis. Twenty-five patients
(17.2%) had C. albicans, which was the most frequent yeast,
and non-albicans Candida was identified in 11 patients
(7.6%) (Tables 4 and 5).

Table 2. Patient Characteristics and Microbiology by Perforation Site


Stomach/duodenum
Community-acquired infection (276)
Hospital-acquired infection (143)
Positive blood culture (20)
Positive peritoneal culture (145)
Staphylococcus spp. (22)
Enterococcus spp. (74)
Escherichia coli (29)
Klebsiella spp.(16)
Pseudomonas aeruginosa (16)
Acinetobacter baumannii (12)
Antibiotic resistant (43)
Deaths (45)
a

Linear by linear association.

101
35
5
42
8
12

(74.3)
(25.7)
(10.0)
(65.6)
(12.5)
(18.8)

2 ( 3.1)
3
4
5
12
14

( 4.7)
( 6.2)
( 7.8)
(18.8)
(10.3)

Small bowel
66
39
1
35
6
21

(62.9)
(37.1)
( 2.1)
(74.5)
(12.8)
(44.7)

8 (17.0)
9
4
2
8
11

(19.1)
( 8.5)
( 4.3)
(17.0)
(10.5)

Colon
102
63
14
63
8
38

(61.8)
(38.2)
(17.9)
(67.0)
( 8.5)
(39.4)

Other
7
6
0
5
0
4

( 53.8)
( 46.2)
(100)
( 80.0)

18 (19.1)

1 ( 20.0)

4
9
4
20
20

0
0
1 ( 20.0)
3 ( 60.0)
2 ( 15.4)

( 4.3)
( 8.5)
( 4.3)
(21.3)
(12.1)

p
0.081
0.036
0.331
0.679
0.002
0.001a
0.030
0.004a
0.009
0.863
0.396
0.151
0.911

JANG ET AL.

Table 3. Organisms Recovered in Blood


Cultures of 182 Patients
No. (%)
Gram-positive cocci
Enterococcus faecium
E. avium
Staphylococcus aureus
Coagulase-negative staphylococci
S. epidermidis
Streptococcus spp.
Gram-negative bacilli
Escherichia coli
Pseudomonas aeruginosa
Bacillus spp.
Micrococcus spp.
Anaerobes
Bacteroides spp.
B. fragillis
Yeasts
Candida albicans

3
1
0
3
4
5

(15.0)
( 5.0)
(15.0)
(20.0)
(25.0)

7
2
1
1

(35.0)
(10.0)
( 5.0)
( 5.0)

4 (20.0)
1 ( 5.0)
1 ( 5.0)

Streptococcus spp. (9; 11.3%) in the CAI group and E. faecalis (7; 10.8%) in the HAI group.
Regarding gram-negative bacteria, in the CAI group, E.
coli (20; 25%) was the most common pathogen, followed by
K. pneumoniae (8; 10%) and P. aeruginosa (6; 7.5%). In the
HAI group, P. aeruginosa (11; 16.9%) and E. coli (9; 13.8%)
were the most common pathogens, and ESBL-producing E.
coli was significantly more common in this group than in the
CAI group (p = 0.016). The positivities for VRE, MRS, ESBL
Klebsiella pneumoniae, CRPA, and CRAB in the two groups
were not significantly different (Table 5).
Clinical outcomes according to antibiotic resistance

Among 210 patients who underwent a peritoneal culture,


43 patients with resistant organisms had longer durations of
hospitalization, ICU stay, and mechanical ventilation than
the others (p < 0.001, < 0.001, and 0.021, respectively), but
there was no significant difference in the mortality rate. Patients with CRAB had more post-operative shock and a
higher mortality rate than patients without (Table 6).
Discussion

Difference between community-acquired


and hospital-acquired infections

A blood culture was performed for 152 of the 276 patients


in the CAI group and in 30 of the 143 patients in the HAI
group. There was no statistically significant difference in the
culture execution rate between the groups (11.8% vs. 6.7%;
p = 0.536).
The peritoneal culture positivity rates were 65.0% and
74.7% in the CAI and HAI groups, respectively, which was
not a significant difference (p = 0.173). Antibiotic-resistant
organisms were more common in the HAI group (15.4% vs.
27.6%; p = 0.032), and the mortality rate was higher in this
group (16.1% vs. 8.7%; p = 0.023) (see Table 4). Enterococcus faecium was the gram-positive bacterium detected most commonly in both groups (31.3% and 40%). The
second most common organisms were other enterococci and

Table 4. Differences between Community-Acquired


and Hospital-Acquired Infections
Community
acquired
(%)
Blood culture
Positive
Negative
Peritoneal culture
Positive
Negative
Antibiotic resistanta
Deaths
Total
a

152
18
134
123
80
43
19
24
276

(11.8)
(88.2)
(65.0)
(35.0)
(15.4)
( 8.7)

Hospital
acquired
(%)
30
2
28
87
65
22
24
23
143

( 6.7)
(93.3)

0.536

(74.7)
(25.3)
(27.6)
(16.1)

0.173
0.032
0.023

Antibiotic resistance is described as vancomycin-resistant


Enterococcus, methicillin-resistant Staphylococcus spp., Escherichia coli with extended-spectrum b-lactamase (ESBL), Klebsiella
pneumoniae with ESBL, carbapenem-resistant Pseudomonas aeruginosa, and carbapenem-resistant Acinetobacter baumannii.

Intra-abdominal infections are classified as complicated or


uncomplicated and are defined as infections that extend beyond the originating viscus perforation and lead to more
diffuse peritonitis or abscess formation [13]. In this study,
appendicitis and biliary tract disease cIAIs were excluded. In
patients with a cIAI, E. coli was the most common gramnegative pathogen, followed by K. pneumoniae, Enterobacter spp., and P. aeruginosa, whereas Streptococcus
spp., Enterococcus spp., and Staphylococcus were the major
gram-positive pathogens [13]. Among anaerobe or yeast
isolates, Bacteroides and Candida spp. are most frequent
[4,1419]. In the present study, Enterococcus spp. and E. coli
were the most common pathogens isolated from peritoneal
cultures, which is consistent with the results of previous
studies.
Blood culture positivity was higher after colon than other
perforations, which probably is related to the normal gastrointestinal flora of the colon [20]. The number of anaerobes
increases rapidly beginning in the distal ileum, which increases the likelihood of bacterial translocation and bacteremia [1,20,21]. Accordingly, the early use of proper
antibiotics is more important in patients with secondary
peritonitis caused by colon perforation.
Several etiologic studies on cIAIs reported that the most
common infecting organism was E. coli (18%71%), and that
the prevalence of K. pneumoniae, Streptococcus spp., and B.
fragilis was 7%11%, 14%38%, and 6%35%, respectively. In addition, patients with an HAI had similar isolation rates for E. coli (19%42%) and K. pneumoniae (7%
10%), but a higher prevalence of Enterococcus spp. (21%
35%) and yeast (13%33%). Furthermore, some studies
found that Enterococcus and yeast were related to a higher
mortality rate in patients with secondary peritonitis [3,22
24]. In the present study, the prevalence of these organisms was higher in the HAI than in the CAI group, and
patients with an HAI had a high prevalence of P. aeruginosa
(16.9%) [13].
Somewhat surprisingly, the isolation rate of Enterococcus
was greater in the present study than in other studies (51.7%

PERITONITIS WITH VISCUS PERFORATION

Table 5. Differences between Infecting Organism of Community-Acquired and Hospital-Acquired


Infections as Determined by Peritoneal Culture
CAI (%)
Gram-positive
Enterococcus faecium
Ent. faecalis
Enterococcus (other)
VRE
Staphylococcus aureus
Coagulase-negative staphylococci
Staphylococcus epidermidis
MRS
Streptococcus spp.
Gram-negative bacilli
Escherichia coli
ESBL
Klebsiella pneumoniae
ESBL
Klebsiella (spp.)
Pseudomonas aeruginosa
CRPA
Enterobacter aerogenes
Enterobacter (spp.)
Acinetobacter baumannii
CRAB
Other
Anaerobes
Bacteroides spp.
Clostridium spp.
Yeasts
Candida albicans
Non-albicans Candida
Patients with positive culture (total culture)

HAI (%)

Total (%)

25
5
9
7/39
5
7
1
4/13
9

(
(
(
(
(
(
(
(
(

31.3)
6.3)
11.3)
17.9)
6.3)
8.8)
1.3)
30.8)
11.3)

26
7
5
9/38
5
3
1
5/9
2

(40)
(10.8)
( 7.7)
(23.7)
( 7.7)
( 4.6)
( 1.5)
(55.6)
( 3.1)

51
12
14
16/77
10
10
2
9/22
11

20
2/20
8
3/8
3
6
2/6
4
4
7
5/7
10

(
(
(
(
(
(
(
(
(
(
(
(

25)
10)
10)
37.5)
3.8)
7.5)
33.3)
5)
5)
8.8)
71.4)
12.5)

9
5/9
8
3/8
1
11
4/11
3
3
5
1/5
8

(13.8)
(55.6)
(12.3)
(37.5)
( 1.5)
(16.9)
(36.4)
( 4.6)
( 4.6)
( 7.7)
(20)
(12.3)

29
7/29
16
6/16
4
17
6/17
7
7
12
6/12
18

5(
1(

6.3)
1.3)

3 ( 4.6)
0

12 ( 15)
7 ( 8.8)
80 (123)

13 (20)
4 ( 6.2)
65 (87)

( 35.2)
( 8.3)
( 9.7)
( 20.8)
( 6.9)
( 6.9)
( 1.4)
( 40.9)
( 7.6)
(
(
(
(
(
(
(
(
(
(
(
(

20)
24.1)
11.0)
37.5)
2.8)
11.7)
35.3)
4.8)
4.8)
8.3)
50)
12.4)

8(
1(

5.5)
0.7)

pa

0.407

0.384

0.016
1.000
1.000

0.242

25 ( 17.2)
11 ( 7.6)
145 (210)

a
Fisher exact test.
CAI = community-acquired infection; CRAB = carbapenem-resistant Acinetobacter baumannii; CRPA = carbapenem-resistant Pseudomonas aeruginosa; ESBL = extended-spectrum b-lactamase; HAI = hospital-acquired infection; MRS = methicillin-resistant Staphylococcus
spp.; VRE = vancomycin-resistant Enterococcus.

Table 6. Clinical Outcomes According


to Antibiotic Resistance
With
antibiotic
resistance
(n = 43)

Without
antibiotic
resistance
(n = 167)

Postoperative
19 (44.2)
48 (28.7)
0.066
shock (%)
Hospital stay (d)
59.1 37.3 27.8 23.4 < 0.001a
ICU stay (d)
5 ( 1102) 2 ( 059) < 0.001a
Mechanical
2 ( 040)
1 ( 059)
0.021a
ventilation (d)
Deaths (%)
10 (23.3)
23 (13.8)
0.128
CRAB patients (n = 6) (%)
Postoperative shock
5 (83.3)
0.013b
Deaths
3 (50.0)
0.051b
a

Mann-Whitney U test.
Fisher exact test.
CRAB = carbapenem-resistant Acinetobacter baumannii.

vs. 5.5%21.5%) [2426]. Ruiter et al. reported that the more


severe secondary peritonitis is, the longer the ICU stay and
the greater the risk of Enterococcus spp. colonization; consequentially, the presence of Enterococcus implies tertiary
peritonitis [23,27]. Although our patients had cIAIs, complicated appendicitis or complicated cholecystitis cases were
excluded. In fact, only cases of peritonitis secondary to hollow viscus perforation were included. Thus, Enterococcus
infections were identified more frequently because the proportion of pre-operative peritonitis was higher than in previous reports, which was about 56% post-operatively
compared with 100% in the present study [25].
Regarding the rate of resistance to antibiotics, VRE accounted for 20.8% of all Enterococcus, MRS for 40.9% of all
Staphylococcus, ESBL-producing E. coli 24.1% of all E. coli,
and ESBL-producing K. pneumoniae 37.5% of all of this
genus, whereas CRPA and CRAB accounted for 35.3% and
50% among P. aeruginosa and A. baumannii, respectively.
Furthermore, the prevalence of ESBL-producing E. coli was
significantly higher in the HAI group, but the prevalence of
other antibiotic-resistant organisms was non-significantly
different in the two groups. In the Study for Monitoring
Antimicrobial Resistance Trends (SMART), the in vitro

activities of several antimicrobial agents on gram-negative


bacilli have been examined since 2002 [28]. According to the
report issued by the Asia-Pacific SMART Group, the rates of
ESBL-producing E. coli and K. pneumoniae were 34.0% and
22.3% of all these organisms, respectively. More specifically,
resistance rates in one university hospital in South Korea
were 30.4% and 25.0%, respectively. Isolation rates of
ESBL-producing E. coli and K. pneumoniae also were higher
in the HAI group than in the CAI group [29]. Our results
showed similar peritoneal microbiology and antibiotic resistance patterns in patients with cIAIs.
Several previous studies published in South Korea attest
that the five most prevalent organisms in general patients are
E. coli (19.3%21.1%), S. aureus (16.6%17.8%), coagulase-negative staphylococci (13.1%13.8%), P. aeruginosa
(9.7%11.7%), and K. pneumoniae (9.4%10.0%). The
proportions of VRE, MRSA, ESBL-producing E. coli, ESBLproducing K. pneumoniae, CRPA, and CRAB were 21%
29%, 64%69%, 12%20%, 29%33%, 23%29%, and
22%56%, respectively [6,7]. The resistance rates and the
proportions of peritoneal organisms found in the present
study concur with those in previous reports, with the exception of enterococci, which were the most common bacterium
in the present study.
The mortality rates of cIAIs depend on the source of infection. Several studies of secondary peritonitis in the 1980s
and 1990s reported a mortality rate of 3%28% in cases of
stomach or duodenal perforation, 20%38% for small bowel
perforation, and 20%45% for colon perforation [16]. In the
Complicated Intra-abdominal Infection Observational
Worldwide (CIAOW) study [19], a mortality rate of 10.1%
was reported, which is similar to the 10.3%15.3% observed
in the present study.

JANG ET AL.

4.
5.
6.

7.

8.

9.

10.
11.

12.

Conclusion

Although this study is limited by its single location and


retrospective design, it provides meaningful information
because of the relatively large number of patients enrolled
and the lack of a previous report on the epidemiology or
bacteriology of secondary peritonitis in South Korea. Further
prospective multicenter studies on this topic are needed.

13.
14.
15.

Author Disclosure Statement and Contributions

The authors have no competing interest to declare.


JGL designed the study. SHL and HS collected and analyzed the data. JYJ analyzed the results and wrote the manuscript. JYC and DY took part in critical revision of the
manuscript. All authors read and approved the final manuscript.

16.
17.
18.

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Address correspondence to:


Dr. Jae Gil Lee
Department of Surgery
Yonsei University College of Medicine
50-1 Yonsei-ro
Seodaemun-gu
Seoul 120-752, Republic of Korea
E-mail: jakii@yuhs.ac

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