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 contrib-
utor 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 postop-
erative 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 contrib-
ute 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 host-
defense deciency [38]. Moreover, risk factors for SSI
related to the surgical procedure include quality of surgical
care, diabetes mellitus, surgery type and duration, emer-
gency procedure, blood transfusion, intraoperative hypo-
thermia, 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
123
84
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 periop-
erative 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.
Patients and methods
Patients
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
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, doc-
umented intraoperatively or within 48 h after the end of
surgery; obstruction of the small bowel; stomal or bypass
surgery; preoperative infectious diseases; and oral antibi-
otic or steroid administration before surgery. Antimicro-
bials 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 multi-
variate 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 fac-
tors in each group (cefmetazole, cephamycin and a second-
generation cephalosporin; cefotiam, a second-generation
cephalosporin; omoxef, oxacephem and identied third-
generation piperacillin). Signicance was dened as
p \ 0.05.
Results
Patient characteristics
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 antimi-
crobial group is demonstrated in Table 1. During the
investigation, there were no denitive criteria for antimi-
crobial 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 on some antimicrobial based on clinical symptoms and data
Characteristics
(fever and inammation markers). Consequently, mean
term of postoperative antimicrobial administration for
The number of operations 304 (209/95) prophylaxis was 4.6 days.
(colon/rectal)
Age (year) 66 12 Univariate analysis
(19 to 91)
Sex (male/female) 181/123
Table 2 summarizes comparisons of patient characteristics.
Diabetic mellitus (yes/no) 51/253
In the univariate analysis, patients were divided into those
Operation time (h) 2.8 1.3
(0.41 to 8.52)
with or without SSI. When we evaluated perioperative and
Blood loss (ml) 191.8 252.1
operative characteristics, patients who developed SSI were
(3.0 to 920.0) more likely to have intraoperative blood loss (308.1 29.8
Intraoperative body temperature (C) 36.4 2.8 vs. 153.9 12.2; p \ 0.05), longer postoperative antimi-
(35.8 to 38.9) crobial administration (5.3 2.2 vs. 4.5 1.5; p \ 0.05),
Postoperation body temperature (C) 37.1 0.6 and longer operative time (3.3 1.6 vs. 2.7 1.2;
(35.1 to 40.0) p \ 0.05). The prolonged length of time from incision to
Blood sugar (mg/dl) (day 0) 125.9 29.3 antimicrobial dosing in the piperacillin group was signi-
(119.5 to 192.0)
cantly associated with the development of SSI (25.4 5.2
Blood sugar (mg/dl) (day 1) 138.9 35.8 vs. 12.2 2.1; p \ 0.05). However, none of the other
(74.8 to 258.0)
factors recorded were statistically associated with the
Blood sugar (mg/dl) (day 2) 158.9 36.6
(151.1 to 231.0) development of incision SSI.
ASA score
1 73 (24.0%)
Comparison of SSI risk factors in each antimicrobial
2 194 (63.8%)
group
3 26 (8.6%)
Table 3 summarized results of the comparison of risk
4 1 (0.3%)
factors in each antimicrobial group. There were signicant
Antimicrobial prophylaxis 302/2
(yes/no) (case) differences between piperacillin and omoxef groups in
Cefmetazole 36 (11.9%) diabetes mellitus (p \ 0.05), blood sugar level (day 0)
Cefotiam 64 (21.2%) (p \ 0.05), blood sugar level (day 2) (p \ 0.05), term of
Flomoxef 136 (45.0%) postoperative administration of antimicrobial agents
Piperacillin 51 (16.9%) (p \ 0.05); there were signicant differences between
Other 15 (5.0%)
piperacillin and cefmetazole groups in terms of postoper-
SSI incidence (yes/no)
ative administration of antimicrobial agents (p \ 0.05).
Cefmetazole 5/46 (9.8%)
Multivariable analysis
Cefotiam 17/47 (26.6%)
Flomoxef 11/125 (8.1%)
Table 4 summarizes results from the multivariate analysis.
Piperacillin 5/31 (13.9%)
Following the univariate analysis, variables, operative
First antimicrobial dosing (min)a 14.9 17.1
(-109.0 to 86.0) blood loss, selection of cefotiam for prophylaxis, and
Term of postoperative administration of 4.6 1.7 length of administration of postoperative antimicrobials
antimicrobial agents (day) (1.0 to 14.0) were selected with stepwise logistic regression analysis.
Intraoperative redosing (case) 42 (13.8%)
Laparoscopic surgery (yes/no) 41/263
Discussion
ASA American Society of Anesthesiologists, SSI surgical-site
infection
a
The time from antimicrobial dosing to incision
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
and 5% other antimicrobials. Moreover, patients who surgery were administered antimicrobial prophylaxis. SSI
received cefotiam showed the highest incidence of SSI incidence in for colorectal resections during the study
(26.6%), followed by piperacillin (13.7%), cefmetazole period was 15.1%, which was in range with a general
(9.6%), and omoxef (8.1%). Most patients were continued review of the literature [26, 30, 31].

123
86 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 NS

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) 175.5 40.3 158.2 36.7 NS
ASA score 1.84 0.08 1.84 0.03 NS
Antimicrobial dose timing (min)a 16.7 2.5 14.8 1.0 NS
Cefmetazole 24.0 8.2 12.7 2.5 NS
Cefotiam 18.9 3.9 19.3 2.1 NS
Flomoxef 10.3 4.3 15.2 1.4 NS
Piperacillin 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
Pearsons v test for categorical variables or Fisher exact test, which was used when the variables were \5, was used to analyze categorized
2

variables. The t test was used to analyze continuous variables

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 anti-
microbials, 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 pro-
phylaxis started within 1 h before incision [29]. However,
our results showed that 90.8% patients received antimi-
crobial prophylaxis within 1 h before incision. In patients
who received prophylactic piperacillin and developed SSI,
the time from antimicrobial dosing to incision were sig-
nicantly 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 antimi-
crobials that cover both anaerobic and aerobic bacteria
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 cov-
erage 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% cef-
metazole. 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 res-
ervoir of facultative and anaerobic bacteria, which is sep-
arated from the rest of the body by the mucous membrane.
Hence, colorectal surgery might have a higher risk for SSI
development. Furthermore, although intraoperative redos-
ing 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 long-
term postoperative administration and that no signicant
difference in the incidence of SSI can be found between a

123
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
Sex (male/female) 20/16 37/27 82/54 33/18
a
Diabetic mellitus (yes/no) 5/31 10/54 29/107 3/48
Operation time (h)a 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
Blood sugar (mg/dl) (day 1) 142.0 33.6 138.5 32.0 136.0 37.4 136.5 32.6
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)
b
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 inci-
dence 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 inci-
dence 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 colo-
rectal 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. Addi-
tionally, SSI is categorized into incisional and organ/space

123
88
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 laparo-
scopic 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 colo-
rectal 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, anti-
microbial 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 dem-
onstrated the lowest incidence of SSI infection and cefot-
iam 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.
123
J Infect Chemother (2012) 18:8389
References
1. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR.
Guideline for prevention of surgical site infection, 1999. Hospital
Infection Control Practices Advisory Committee. Infect Control
Hosp Epidemiol. 1999;20:25078.
2. Emori TG, Gaynes RP. An overview of nosocomial infections,
including the role of the microbiology laboratory. Clin Microbiol
Rev. 1993;6:42842.
3. Smith RL, Bohl JK, McElearney ST, Friel CM, Barclay MM,
Sawyer RG, et al. Wound infection after elective colorectal
resection. Ann Surg. 2004;239:599605.
4. Kaye KS, Schmit K, Pieper C, Sloane R, Caughlan KF, Sexton
DJ, et al. The effect of increasing age on the risk of surgical site
infection. J Infect Dis. 2005;191:105662.
5. Garibaldi RA, Cushing D, Lerer T. Risk factors for postoperative
infection. Am J Med. 1991;91:158S63S.
6. Woodeld JC, Beshay NM, Pettigrew RA, Plank LD, van Rij
AM. American Society of Anesthesiologists classication of
physical status as a predictor of wound infection. ANZ J Surg.
2007;77:73841.
7. Choban PS, Heckler R, Burge JC, Flancbaum L. Increased inci-
dence of nosocomial infections in obese surgical patients. Am
Surg. 1995;61:10015.
8. Haley RW, Culver DH, Morgan WM, White JW, Emori TG,
Hooton TM. Identifying patients at high risk of surgical wound
infection. A simple multivariate index of patient susceptibility
and wound contamination. Am J Epidemiol. 1985;121:20615.
9. Allen DB, Maguire JJ, Mahdavian M, Wicke C, Marcocci L,
Scheuenstuhl H, et al. Wound hypoxia and acidosis limit neu-
trophil bacterial killing mechanisms. Arch Surg. 1997;132:9916.
10. Kurz A, Sessler DI, Lenhardt R. Perioperative normothermia to
reduce the incidence of surgical-wound infection and shorten
hospitalization. Study of Wound Infection and Temperature
Group. N Engl J Med. 1996;334:120915.
11. Gottrup F, Firmin R, Rabkin J, Halliday BJ, Hunt TK. Directly
measured tissue oxygen tension and arterial oxygen tension
assess tissue perfusion. Crit Care Med. 1987;15:10306.
12. Hopf HW, Hunt TK, West JM, Blomquist P, Goodson WH 3rd,
Jensen JA, et al. Wound tissue oxygen tension predicts the risk of
wound infection in surgical patients. Arch Surg. 1997;132:
9971004.
13. Astagneau P, Rioux C, Golliot F, Brucker G, INCISO Network
Study Group. Morbidity and mortality associated with surgical
site infections: results from the 19971999 INCISO surveillance.
J Hosp Infect. 2001;48:26774.
14. Engemann JJ, Carmeli Y, Cosgrove SE, Fowler VG, Bronstein
MZ, Trivette SL, et al. Adverse clinical and economic outcomes
attributable to methicillin resistance among patients with Staph-
ylococcus aureus surgical site infection. Clin Infect Dis.
2003;36:5928.
15. Kirkland KB, Briggs JP, Trivette SL, Wilkinson WE, Sexton DJ.
The impact of surgical-site infections in the 1990s: attributable
mortality, excess length of hospitalization, and extra costs. Infect
Control Hosp Epidemiol. 1999;20:72530.
16. Sutter VL. Frequency of occurrence and antimicrobial suscepti-
bility of bacterial isolates from the intestinal and female genital
tracts. Rev Infect Dis. 1983;5:S849.
17. Baum ML, Anish DS, Chalmers TC, Sacks HS, Smith H Jr,
Fagerstrom RM. A survey of clinical trials of antibiotic prophy-
laxis in colon surgery: evidence against further use of no-treat-
ment controls. N Engl J Med. 1981;305:7959.
18. Silver A, Eichorn A, Kral J, Pickett G, Barie P, Pryor V, et al.
Timeliness and use of antibiotic prophylaxis in selected inpatient
J Infect Chemother (2012) 18:8389
surgical procedures. The Antibiotic Prophylaxis Study Group.
Am J Surg. 1996;171:54852.
19. Matuschka PR, Cheadle WG, Burke JD, Garrison RN. A new
standard of care: administration of preoperative antibiotics in the
operating room. Am Surg. 1997;63:5003.
20. Gorecki P, Schein M, Rucinski JC, Wise L. Antibiotic adminis-
tration in patients undergoing common surgical procedures in a
community teaching hospital: the chaos continues. World J Surg.
1999;23:42932.
21. Trick WE, Scheckler WE, Tokars JI, Jones KC, Reppen ML,
Smith EM, et al. Modiable risk factors associated with deep
sternal site infection after coronary artery bypass grafting.
J Thorac Cardiovasc Surg. 2000;119(1):10814.
22. Burke JP. Maximizing appropriate antibiotic prophylaxis for
surgical patients: an update from LDS Hospital, Salt Lake City.
Clin Infect Dis. 2001;33(Suppl 2):S7883.
23. Miles AA, Miles EM, Burke J. The value and duration of defence
reactions of the skin to the primary lodgement of bacteria. Br J
Exp Pathol. 1957;38(1):7996.
24. Burke JF. The effective period of preventive antibiotic action in
experimental incisions and dermal lesions. Surgery. 1961;
50:1618.
25. Polk HC Jr, Lopez-Mayor JF. Postoperative wound infection: a
prospective study of determinant factors and prevention. Surgery.
1969;66:97103.
26. Stone HH, Hooper CA, Kolb LD, Geheber CE, Dawkins EJ.
Antibiotic prophylaxis in gastric, biliary and colonic surgery. Ann
Surg. 1976;184:44352.
27. Polk HC Jr, Trachtenberg L, Finn MP. Antibiotic activity in
surgical incisions. The basis of prophylaxis in selected opera-
tions. JAMA. 1980;244:13534.
28. DiPiro JT, Vallner JJ, Bowden TA Jr, Clark B, Sisley JF. Intra-
operative serum concentrations of cefazolin and cefoxitin
89
administered preoperatively at different times. Clin Pharm.
1984;3:647.
29. Classen DC, Evans RS, Pestotnik SL, Horn SD, Menlove RL,
Burke JP. The timing of prophylactic administration of antibiotics
and the risk of surgical-wound infection. N Engl J Med.
1992;326:2816.
30. Clarke JS, Condon RE, Bartlett JG, Gorbach SL, Nichols RL,
Ochi S. Preoperative oral antibiotics reduce septic complications
of colon operations: results of prospective, randomized, double-
blind clinical study. Ann Surg. 1977;186:2519.
31. Goldring J, McNaught W, Scott A, Gillespie G. Prophylactic oral
antimicrobial agents in elective colonic surgery. A controlled
trial. Lancet. 1975;2:9971000.
32. Nelson RL, Glenny AM, Song F. Antimicrobial prophylaxis for
colorectal surgery. Cochrane Database Syst Rev. 2009;21:
CD001181.
33. Song F, Glenny AM. Antimicrobial prophylaxis in colorectal
surgery: a systematic review of randomised controlled trials.
Health Technol Assess. 1998;2:1110.
34. Nichols RL, Choe EU, Weldon CB. Mechanical and antibacterial
bowel preparation in colon and rectal surgery. Chemotherapy.
2005;51:S11521.
35. Coppa GF, Eng K. Factors involved in antibiotic selection in
elective colon and rectal surgery. Surgery. 1988;104:8538.
36. Eagye KJ, Nicolau DP. Deep and organ/space infections in
patients undergoing elective colorectal surgery: incidence and
impact on hospital length of stay and costs. Am J Surg.
2009;198:35967.
37. de Lalla F. Antimicrobial prophylaxis in colorectal surgery: focus
on ertapenem. Ther Clin Risk Manag. 2009;5:82939.
123