J Infect Chemother (2012) 18:8389

DOI 10.1007/s10156-011-0298-y

ORIGINAL ARTICLE

Preventing surgical-site infections after colorectal surgery

Mao Hagihara Mieko Suwa Yumi Ito
Yuki Muramatsu Yukiko Kato Yuka Yamagishi
Hiroshige Mikamo

Received: 16 March 2011 / Accepted: 16 August 2011 / Published online: 9 September 2011
Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases 2011

Abstract Surgical-site infection (SSI) is a major contributor to patient mortality rates and health care costs. Due to the
high risk of bacterial contamination, colorectal surgery is
associated with a particularly high risk of postoperative
infection. The surveillance reported here was conducted at
Aichi Medical University Hospital on 304 patients who
underwent elective colorectal resectiontotal or partial
from June 2006 to May 2009. To determine risk factors for
SSI, multivariate analysis was used. Forty-six (15.1%)
patients were diagnosed with SSI. Patients who received
cefotiam for prophylaxis showed the highest incidence of SSI
(26.6%), and patients who were administered omoxef
showed the lowest incidence (8.1%). Patients who developed
SSI were more likely to intraoperative blood loss
(308.1 29.8 vs. 153.9 12.2; p \ 0.05), longer postoperative antimicrobial administration (5.3 2.2 vs. 4.5 1.5;
p \ 0.05), and longer operative time (3.3 1.6 vs.
2.7 1.2; p \ 0.05). Intraoperative bleeding, antimicrobial
choices to cover both anaerobic and aerobic bacteria, and
length of antimicrobial administration were independently
predictive of SSI development according to multivariate
logistic regression analysis. These results suggest that the
degree of operative invasion and anaerobic bacteria contribute to SSI following colorectal surgery.

M. Hagihara (&)
M. Suwa
Y. Muramatsu
Y. Kato

Y. Yamagishi
H. Mikamo
Department of Infection Control and Prevention,
Aichi Medical University School of Medicine,
Nagakute-cho, Aichi-gun, Aichi 480-1195, Japan
e-mail: hagimao@hotmail.com
Y. Ito
Department of Pharmacy, Aichi Medical University School
of Medicine, Nagakute-cho, Aichi-gun, Aichi 480-1195, Japan

Keywords Surgical-site infection (SSI)
Colorectal

surgery
Antimicrobial prophylaxis

Introduction
Surgical-site infection (SSI) is dened as infections
occurring within 30 daysor within 1 year in the case of
implantation of a foreign bodyafter surgery and
affecting either the incision (supercially or deeply),
organs, or body spaces at the site of operation [1]. In
2002, the US Centers for Medicare and Medicaid Services
implemented the National Surgical Infection Prevention
Project. This project builds on experience that the US
Centers for Disease Control and Prevention (CDC) have
gained from implementing the National Nosocomial
Infections Surveillance System (CDC-NNIS). According
to data from the system, SSI accounts for 1416% of
reported nosocomial infections among all hospitalized
patients and 38% among surgical patients [1, 2]. In Europe,
available data show that the incidence of SSI can be as high
as 20% depending on surgical procedure, surveillance
criteria, and study design.
As for patient resistance, intrinsic patient characteristics
strictly correlating with an increased risk of SSI include
advanced age, an American Society of Anesthesiologists
(ASA) score of III, obesity, pre-existing illness, and hostdefense deciency [38]. Moreover, risk factors for SSI
related to the surgical procedure include quality of surgical
care, diabetes mellitus, surgery type and duration, emergency procedure, blood transfusion, intraoperative hypothermia, and systemic hypoxemia [912]. Additionally, SSI
is a major contributor to patient mortality rates and health
care costs. Mortality rates were two to three times higher in
patients in whom SSI developed compared with uninfected

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patients, and hospital readmission rates were signicantly

increased [5, 1315].
In large-bowel surgery, the predominant isolates are
Bacteroides fragilis and Escherichia coli [16]. Due to the
high risk of bacterial contamination, colorectal surgery is
associated with a particularly high risk of postoperative
infection. SSI rates of up to 40% and of about 25% have
been found in patients not receiving or receiving perioperative antibiotic prophylaxis, respectively [3, 17]. Indeed,
the efcacy of perioperative systemic antimicrobial agents
is mainly related to suppression of bacterial growth in the
tissues of the operative eld once contamination occurrs.
As previous studies demonstrate, inappropriate timing of
antimicrobial administration and inappropriate selection of
the antimicrobial agent extend patient admission [1822].
It is universally accepted that antibiotic prophylaxis, i.e.,
perioperative administration of suitable antimicrobial
agents, must be considered one of the most important
measures for preventing SSI [2329]. However, the use of
antimicrobial prophylaxis is often suboptimal. Therefore,
we performed a retrospective SSI surveillance focusing on
patients undergoing colorectal surgery at the Aichi Medical
University Hospital. The aim of the study was to determine
the actual incidence of SSI and to identify risk factors for
developing SSI in patients undergoing colorectal surgery.

J Infect Chemother (2012) 18:8389

conrm patients case record; cases with no explicitly

documented incision time or antimicrobial administration
time; infection, including peritonitis and perforation, documented intraoperatively or within 48 h after the end of
surgery; obstruction of the small bowel; stomal or bypass
surgery; preoperative infectious diseases; and oral antibiotic or steroid administration before surgery. Antimicrobials were considered prophylactic if given before surgery,
intraoperatively, or within 24 h after the end of surgery.
Statistical analysis
Statistical analysis was performed using JMP software
(5.1.1 SAS Institute). The univariate relation between each
independent variable and SSI was evaluated using a t test
for continuous variables. Pearsons v2 test for categorical
variables or Fishers exact test, used when variables were
\5, was used to analyze categorized variables. In multivariate analysis, logistic regression analysis with a Wald
statistic step-forward selection was used. One-way analysis
of variance (ANOVA) was used to compare SSI risk factors in each group (cefmetazole, cephamycin and a secondgeneration cephalosporin; cefotiam, a second-generation
cephalosporin; omoxef, oxacephem and identied thirdgeneration piperacillin). Signicance was dened as
p \ 0.05.

Patients and methods

Results
Patients
Patient characteristics
This survey was conducted at the Aichi Medical University
Hospital. Patients who underwent elective colorectal
resection, total or partial, between June 2006 and May
2009 were identied for inclusion. Patients hospital
records, clinical charts, operating room records, and
information during admission were reviewed.
Methods
Demographic and clinical variables were recorded. Specic
intake variables were age, gender, ASA score, medical
history, preoperative antibiotics (general name and
administration timing) and intraoperative redosing, term of
postoperative administration of antimicrobial agents,
intraoperative hypothermia, postoperative hypothermia,
postoperative blood sugar level, operative procedure,
operative time, and operative blood loss.
Data analysis
Denition of SSI was according to NNSH manual. Cases
were excluded if results of the medical chart review did not

123

Patient demographic characteristic are summarized in

Table 1. During the 3 years, 407 patients were identied
who underwent colorectal resection; 304 patients [209
colonic surgeries (68.8%) and 95 (31.3%) rectal surgeries]
met inclusion criteria. Mean patient age was 66 (range
1991) years; 59.5% was male. Three hundred and two
patients received antimicrobial prophylaxis (99.4%).
Almost all surgeries were for malignant tumors (300/304;
98.7%); four (1.3%) were for other reasons.
ASA scores are shown in Table 1. During the study, 46
(15.1%) patients were diagnosed with SSI. Most patients
received their rst antimicrobial prophylaxis within 1 h
before incision (90.8%); 42 (13.8%) patients received an
intraoperative redosing, although mean operation time was
2.8 h. The distribution of SSI incidence for each antimicrobial group is demonstrated in Table 1. During the
investigation, there were no denitive criteria for antimicrobial choice in this hospital. Therefore, all antimicrobials
were selected based on the surgeons decision. The most
commonly prescribed agent was omoxef (45%), followed
by cefotiam (21%), piperacillin (17%), cefmetazole (12%),

J Infect Chemother (2012) 18:8389

85

Table 1 Patient demographics

Characteristics
The number of operations
(colon/rectal)

304 (209/95)

Age (year)

66 12
(19 to 91)

Sex (male/female)

181/123

Diabetic mellitus (yes/no)

51/253

Operation time (h)

2.8 1.3
(0.41 to 8.52)

Blood loss (ml)

191.8 252.1
(3.0 to 920.0)

Intraoperative body temperature (C)

36.4 2.8
(35.8 to 38.9)

Postoperation body temperature (C)

37.1 0.6
(35.1 to 40.0)

Blood sugar (mg/dl) (day 0)

125.9 29.3
(119.5 to 192.0)

Blood sugar (mg/dl) (day 1)

138.9 35.8
(74.8 to 258.0)

Blood sugar (mg/dl) (day 2)

158.9 36.6
(151.1 to 231.0)

ASA score
1

73 (24.0%)

194 (63.8%)

26 (8.6%)

1 (0.3%)

Antimicrobial prophylaxis
(yes/no) (case)

302/2

Cefmetazole

36 (11.9%)

Cefotiam

64 (21.2%)

Flomoxef

136 (45.0%)

Piperacillin

51 (16.9%)

Other

15 (5.0%)

SSI incidence (yes/no)

Cefmetazole

5/46 (9.8%)

Cefotiam

17/47 (26.6%)

Flomoxef

11/125 (8.1%)

Piperacillin

5/31 (13.9%)

First antimicrobial dosing (min)a

14.9 17.1
(-109.0 to 86.0)

Term of postoperative administration of

antimicrobial agents (day)

4.6 1.7
(1.0 to 14.0)

Intraoperative redosing (case)

42 (13.8%)

Laparoscopic surgery (yes/no)

41/263

ASA American Society of Anesthesiologists, SSI surgical-site

infection
a

The time from antimicrobial dosing to incision

and 5% other antimicrobials. Moreover, patients who

received cefotiam showed the highest incidence of SSI
(26.6%), followed by piperacillin (13.7%), cefmetazole
(9.6%), and omoxef (8.1%). Most patients were continued

on some antimicrobial based on clinical symptoms and data

(fever and inammation markers). Consequently, mean
term of postoperative antimicrobial administration for
prophylaxis was 4.6 days.
Univariate analysis
Table 2 summarizes comparisons of patient characteristics.
In the univariate analysis, patients were divided into those
with or without SSI. When we evaluated perioperative and
operative characteristics, patients who developed SSI were
more likely to have intraoperative blood loss (308.1 29.8
vs. 153.9 12.2; p \ 0.05), longer postoperative antimicrobial administration (5.3 2.2 vs. 4.5 1.5; p \ 0.05),
and longer operative time (3.3 1.6 vs. 2.7 1.2;
p \ 0.05). The prolonged length of time from incision to
antimicrobial dosing in the piperacillin group was signicantly associated with the development of SSI (25.4 5.2
vs. 12.2 2.1; p \ 0.05). However, none of the other
factors recorded were statistically associated with the
development of incision SSI.
Comparison of SSI risk factors in each antimicrobial
group
Table 3 summarized results of the comparison of risk
factors in each antimicrobial group. There were signicant
differences between piperacillin and omoxef groups in
diabetes mellitus (p \ 0.05), blood sugar level (day 0)
(p \ 0.05), blood sugar level (day 2) (p \ 0.05), term of
postoperative administration of antimicrobial agents
(p \ 0.05); there were signicant differences between
piperacillin and cefmetazole groups in terms of postoperative administration of antimicrobial agents (p \ 0.05).
Multivariable analysis
Table 4 summarizes results from the multivariate analysis.
Following the univariate analysis, variables, operative
blood loss, selection of cefotiam for prophylaxis, and
length of administration of postoperative antimicrobials
were selected with stepwise logistic regression analysis.

Discussion
Antimicrobial prophylaxis to prevent SSI is one of the most
widely accepted practices in surgery. Our results showed
that 99.4% of all patients who received elective colorectal
surgery were administered antimicrobial prophylaxis. SSI
incidence in for colorectal resections during the study
period was 15.1%, which was in range with a general
review of the literature [26, 30, 31].

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J Infect Chemother (2012) 18:8389

Table 2 Comparison between surgical-site infection (SSI) group and non-SSI group
SSI

Non-SSI

Number of operations (colon/rectal)

28/18

181/77

Age (year)

66.9 1.8

66.0 0.7

NS

Sex (male/female)

27/19

154/104

NS

Diabetic mellitus (yes/no)

6/40

44/214

NS

Operation time (h)

3.3 1.6

2.7 1.2

\0.05

Blood loss (ml)

308.1 29.8

153.9 12.2

\0.05

Intraperation body temperature (C)

37.3 0.7

36.9 2.4

NS

Postoperation body temperature (C)

37.1 0.8

36.0 5.1

NS

Blood sugar level (mg/dl) (day 0)

124.3 7.09

126.0 10.1

NS

Blood sugar level (mg/dl) (day 1)

136.8 37.5

139.3 35.6

NS

Blood sugar level (mg/dl) (day 2)

ASA score

175.5 40.3
1.84 0.08

158.2 36.7
1.84 0.03

NS
NS

16.7 2.5

14.8 1.0

NS

24.0 8.2

12.7 2.5

NS

Antimicrobial dose timing (min)a

Cefmetazole

NS

Cefotiam

18.9 3.9

19.3 2.1

NS

Flomoxef

10.3 4.3

15.2 1.4

NS

25.4 5.2

12.2 2.1

\0.05

Term of postoperative antimicrobial administration (day)

5.3 2.2

4.5 1.5

\0.05

Intraoperative redosing (yes/no)

7/39

35/223

NS

Laparoscopic surgery (yes/no)

3/43

38/220

NS

Piperacillin

Pearsons v test for categorical variables or Fisher exact test, which was used when the variables were \5, was used to analyze categorized
variables. The t test was used to analyze continuous variables
2

ASA American Society of Anesthesiologists

a

Time from antimicrobial dosing to incision

As previous studies demonstrated inappropriate timing

of antimicrobial administration, inappropriate selection of
antimicrobial agent extended patient admission [1822].
Optimal prophylaxis requires application in appropriate
types of operations, selection of safe and effective antimicrobials, initial administration and redosing to maintain
effective serum and tissue levels throughout the operation,
and discontinuation when the patient is no longer receiving
a benet [1]. Stone et al. [26] showed that the lowest rates
of SSI in abdominal operations were associated with prophylaxis started within 1 h before incision [29]. However,
our results showed that 90.8% patients received antimicrobial prophylaxis within 1 h before incision. In patients
who received prophylactic piperacillin and developed SSI,
the time from antimicrobial dosing to incision were signicantly longer than for other patients. Piperacillin has a
shorter half-life than other antimicrobials. Therefore, our
result suggest the necessity of considering an antimicrobial
blood concentration based on antimicrobial half-time and
operation time, even though all antimicrobials we used
were within 1 h prior to operation.
As choosing an antimicrobial agent for prophylaxis in
colorectal surgery, there is general agreement that antimicrobials that cover both anaerobic and aerobic bacteria

123

attain the best results. Indeed, Nelson et al. [32], in a

systemic review on antibiotic prophylaxis in colorectal
surgery, studied 182 randomized controlled trials and
found that the addition of an anaerobic to an aerobic coverage resulted in a statistically signicant reduction in the
incidence of SSI. In our study, 45% of patients received
omoxef, 21% cefotiam, 17% piperacillin, and 12% cefmetazole. Patients administered cefotiam showed the
highest incidence of SSI among all patients during the
study period. Cefotiam is not sold in Western countries,
and many drugs in this study, except cefotiam, are thought
to be effective for anaerobic bacteria. Our results also
suggest that antimicrobial prophylaxis needs to cover both
aerobic and anaerobic bacteria to prevent SSI. Indeed, the
colon and distal small intestines contain an enormous reservoir of facultative and anaerobic bacteria, which is separated from the rest of the body by the mucous membrane.
Hence, colorectal surgery might have a higher risk for SSI
development. Furthermore, although intraoperative redosing is generally recommended only when the operation
lasts longer than 23 h, Song and Glenny [33] showed a
single-dose or short-term regimen is as effective as longterm postoperative administration and that no signicant
difference in the incidence of SSI can be found between a

J Infect Chemother (2012) 18:8389

87

Table 3 Comparison of surgical-site infection (SSI) risk factors in each antimicrobial group
Cefmetazole

Cefotiam

Flomoxef

Piperacillin

Number of operations (colon/rectal)

26/10

39/25

98/38

33/18

Age (year)

65.0 12.33

68.21 10.13

64.86 11.08

66.25 12.78

20/16

37/27

82/54

33/18

Sex (male/female)
Diabetic mellitus (yes/no)

Operation time (h)a

5/31

10/54

29/107

3/48

2.6 1.2

2.8 1.3

3.0 1.3

3.2 1.6

Blood loss (ml)

180.0 33.7

168.1 25.1

161.7 17.2

209.5 27.9

Intraoperative body temperature (C)

37.3 0.4

37.1 0.3

36.7 0.2

37.1 0.3

Postoperation body temperature (C)

34.9 0.8

36.9 0.6

35.9 0.4

36.8 0.7

Blood sugar (mg/dl) (day 0)a

121.8 15.4

125.5 32.9

127.7 27.5

116.6 37.5
136.5 32.6

Blood sugar (mg/dl) (day 1)

142.0 33.6

138.5 32.0

136.0 37.4

Blood sugar (mg/dl) (day 2)a

179.5 37.0

168.5 40.5

155.5 35.6

148.0 1.73

ASA score

1.83 0.59

1.87 0.46

1.78 0.68

1.85 0.61

Antimicrobial dose timing (min)

13.6 2.6

19.1 2.0

14.4 1.3

4.4 2.2

Term of postoperative antimicrobial administration (day)a,b

4.8 1.6

4.4 1.6

5.0 1.6

4.1 1.4

Intraoperative redosing (case)

5/31

10/54

12/124

16/35

Laparoscopic surgery (yes/no)

5/31

12/52

11/125

10/41

One-way analysis of variance

ASA American Society of Anesthesiologists
a

Signicant difference between piperacillin and omoxef groups (p \ 0.05)

Signicant difference between the piperacillin and cefmetazole groups (p \ 0.05)

Table 4 Multivariate analysis

Risk factor

Odds ratio

95% CI

P value

Blood loss (ml)

0.06

0.020.22

\0.05

Duration of prophylaxis (day)

0.06

0.0040.76

\0.05

Cefotiam

0.32

0.150.70

\0.05

Stepwise method (step-forward). Coefcients: number of operations (colon/rectal), age, sex, diabetes mellitus (yes/no), operation time (h), blood
loss (ml), intraoperative body temperature (C), postoperative body temperature (C), blood sugar level (mg/dl) (day 0), blood sugar level (mg/dl)
(day 1), blood sugar level (mg/dl) (day 2), American society of Anesthesiologists score, antimicrobial prophylaxis (cefmetazole, cefotium,
omoxef, piperacillin), term of postoperative administration of antimicrobial agents, intraoperative redosing (case), laparoscopic surgery (yes/no)
CI condence interval

single-dose regimen and a multidose regimen. In our study,

13.8% of all patients received intraoperative redosing,
although mean operation time was 2.8 h; 75.0% patients
received postoperative prophylaxis, although prophylactic
antibiotics are recommended to be given for \24 h after
operation. Patients with longer operative time and longer
postoperative antimicrobial prophylaxis had a higher incidence of SSI. These results reect the degree of invasion
for patients undergoing colorectal surgery.
Previous studies suggest that SSI rates might not be the
same between colon and rectum surgery [34, 35]. Although
our results showed no signicant difference in SSI incidence between colon and rectum surgery groups, there was
a trend to SSI development in the rectum surgery group. In
addition, the reason ASA score did not selected as a risk
factor of SSI in our study is the NNIS Risk Index has been

criticized as being unsuitable for risk evaluation in colorectal surgery because most patients undergoing such the
procedure have an ASA score of 1 or 2 and a wound
classication of cleancontaminated.
There are several important limitations to this study.
First, this was retrospective analysis and not a randomized
controlled study to examine the signicance of specic risk
factors for SSI. Therefore, there was some variability
among practices [the use of antimicrobial-coated sutures,
mechanical bowel preparation (glycolelectrolyte solution
or 2-Hydroxy-1,2,3-propanetricarboxylic acid magnesium
salt)]. Second, we did not take into account stratication by
surgeon because this study was conducted in a hospital.
Although the term of investigation was 3 years, a few
surgeons in a group conducted colorectal surgeries. Additionally, SSI is categorized into incisional and organ/space

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SSI; organ/space SSI caused by anastomotic leakage or

suture failure occurred from poor wound healing at the
anastomotic site and cannot be prevented by antimicrobial
agents. In this study, although most SSIs were incisional,
we included some cases that could not be identied as
incisional and/or organ/space SSI. Therefore, we may
have included organ/space SSI. However, in generally, the
incidence of organ/space SSI is around 34% in colorectal
surgery patients, which means that less than ten organ/
space SSI patients may have been included [36]. Because
our study was retrospective, prospective study is needed
that clearly divides incisional and organ/space SSI.
Moreover, data regarding other suggested risk factors are
lacking (inspired concentration of oxygen; subcutaneous
oxygen concentrations during surgery). Some studies
evaluated SSI risk factors in elective colorectal surgery by
ve surgical types: conventional; colectomy, anterior
resection, abdominoperineal resection, and laparoscopy;
colectomy, anterior resection. However, in our study, the
number of patients who developed SSI following laparoscopic surgery was not large enough to show signicantly
difference in this analysis. Furthermore, to the best of our
knowledge, no study has evaluated these types of surgery
in regard to SSI, except for conventional or laparoscopic
surgery. Therefore, logistic regression analysis took into
account conventional and laparoscopic surgery only.
Finally, some studies show that the incidence of diarrhea
due to Clostridium difcile and methicillin-resistant
Staphylococcus aureus (MRSA) enterocolitis after colorectal surgery is approximately 3% [37]. In our study,
these occurred in fewer than ten patients, a number too
small to compare their incidence with statistical analysis
in each antibiotic group. Despite these limitations, few
studies analyzed temperatures and control of glucose
levels in relation to antimicrobial medications SSI. Our
data suggested that, at least for colorectal surgery, antimicrobial choice and how it is used are more important
than ASA score, pre- and postoperative body temperature,
and blood sugar levels, which are recognized as important
risk factor of SSI in general.
In conclusion, our study showed that blood loss during
operation and the term of postoperative antimicrobial
prophylaxis were risk factor of SSI, as they reect the
degree of operative invasion. Moreover, our results show
that patients who received omoxef as prophylaxis demonstrated the lowest incidence of SSI infection and cefotiam the highest. These results suggest that the degree of
operational invasion and anaerobic bacteria contribute to
SSI following colorectal surgery.
Acknowledgments We thank all clinicians, nurses, and pharmacists
who assisted with the provision of data for this project.

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J Infect Chemother (2012) 18:8389

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