Acta Obstetricia et Gynecologica.

2007; 86: 1097 −1102

ORIGINAL ARTICLE

Post-cesarean surgical site infections according to CDC

stand(cc) ards: rates and(cc) risk factors. A prospective cohort
study

HANS KRISTIAN OPØIEN1, ANNELILL VALBØ1, ANETTE GRINDE-AND(CC)

ERSEN1 & METTE WALBERG2
1
Department of Obstetrics and(cc) Gynaecology, Asker og Bærum Sykehus HF, Norway, and(cc) 2Department of
Microbiology, Asker og Bærum Sykehus HF, Norway

Abstract
Objectives. The aim of this study was to document the true incidence of post-cesarean surgical site infections (SSI),
according to the definition of the US Centers for Disease Control and(cc) Prevention (CDC), and(cc) to identify independent
risk factors for infection. Design. Prospective population-based cohort study in Norway. Setting. Sykehuset Asker og Bærum
HF, a secondary community hospital, associated with the University of Oslo (UiO), Norway, accounting for 2,000 deliveries
per year. Participants. All cesarean deliveries during a 12-month period from September 2003. Main outcome measures.
Rate and(cc) risk factors for SSI. Results. The total rate of SSI was 8.9%, with an observation period of 30 days post-
operatively, compared to 1.8% registered at hospital discharge. The total response rate was 100%. There was no significant
difference in SSI rate in elective or emergency cesarean section (CS), respectively. All SSI were superficial. We found 2
significant independent risk factors: operating time ]38 min and(cc) body mass index (BMI) >30. Conclusion. The
rate of SSI is underestimated if the observation time is limited to the hospital stay. Operating time exceeding 38 min
substantially increases the risk of SSI. The finding of no significant difference in SSI rate between elective
and(cc)emergency CS should lead to a different approach concerning the use of antibiotics: subgroup at risk (operating
time ]38 min and(cc) BMI>30) may benefit from antibiotics in relation to the operation, whether the CS is an
emergency or elective operation.

Key words: Cesarean section and(cc) surgical site infection

Introduction rate during hospital stay was reported (21.4%).

Cesarean section (CS) is one of the most
commonly performed surgical procedures in
hospitals. In Nor- way, as in other industrialised
western countries, the incidence has increased
during the last 30 years, from 2% in 1968, to
12.6% in 1990, to 15.8% in
2002 (1−5). Additionally, a considerable variation
has been registered between different obstetric
departments (6 −20%) (6). In 1998, the Norwegian
Medical Association invited all maternity units to
participate in a ‘Breakthrough Project’ on cesarean
delivery, in order to accelerate improvements of the
medical practice by cycles of setting aims, establish-
ing measures, and(cc) developing and(cc) testing
changes (7). In one of the publications emerging from
this project, an unexpected high overall
complication
Wound infection affected 2.2% of the patients
having regional anesthesia (4). The incidence of
maternal post-operative complications varies in the
literature (4,8 −19). However, the average length of
post-operative hospital stay has decreased in recent
years, leaving certain maternal post-operative com-
plications, such as surgical site infections (SSI),
not(C2) revealed at time of hospital discharge. As
many of the patients later consult primary health care
services in Norway, the incidence of SSI might be
underesti- mated, when SSI is defined, according to
the US Centers for Disease Control and(cc)
Preventions (CDC), as an infection occurring within
30 days so uch(sc) a surgical procedure (without any
implant) (20) (Figure 1).

Correspondence: Hans Kristian Opøien, Department of Obstetrics and(cc) Gynecology, Rikshospitalet-Radiumhospitalet Medical Center, 0027 Oslo,
Norway. E-mail: hans.kristian.opoien@rikshospitalet.no
(Received 2 October 2006; accepted 8 June 2007)
ISSN 0001-6349 print/ISSN 1600-0412 online # 2007 Taylor & Francis DOI:
10.1080/00016340701515225
1098 H.K. Opøien et al.

Criteria for defining surgical site infection (SSI). From US Centers for Disease Control
and(cc) Prevention
Superficial incisional SSI
Infection occurs within 30 days after the operation and(cc) infection involves only
skin or subcutaneous tissue of the incision and(cc) at least one of the following:
1. Purulent drainage, with or without laboratory confirmation, from the superficial incision.
2. Organisms isolated from an aseptically obtained culture of fluid or tissue from
the superficial incision.
3. At least one of the following signs or symptoms of infection: pain or tenderness, localized
swelling, redness, or heat and(cc) superficial incision is deliberately opened by surgeon,
unless incision is culture-negative
4. Diagnosis of superficial incisional surgical site infection (SSI) by surgeon or
attending physician.
Deep incisional SSI
Infection occurs within 30 days after the operation and(cc) infection involves deep soft
tissue (e.g. fascial and(cc) muscle layers) of the incision and(cc) at least one of the
following:
1. Purulent drainage from the deep incision but not (c2) from the organ/space component
of the surgical site.
2. A deep incision spontaneously dehisces or is deliberately opened by a surgeon
when(sc) the patient has at least one of the following signs or symptoms: fever (>
38C), localized pain, or tenderness, unless site is culture-negative.
3. An abscess or other evidence of infection involving the deep incision is found on
direct examination, during reooperation, or by histopathologic or radiologic
examination.
4. Diagnosis of a deep incisional SSI by a surgeon or attending physician.

Organ/space SSI
Infection occurs within 30 days after the operation and(cc) infection involves any part
of the anatomy (e.g. organs or spaces), other than the incision, which was opened or
manipulated during an operation and(cc) at least one of the following:
1. Purulent drainage from a drain that is placed through a stab wound into the organ/space.
2. Organisms isolated from an aseptically obtained culture of fluid or tissue in the organ/space.
3. An abscess or other evidence of infection involving the organ/space that is found on
Figure 1. Criteria for defining surgical site infection (SSI), from US Centers for Disease Control and(cc) Prevention.

The aim of this study was to document the true
incidence of post-cesarean SSI according to the
CDC definition, and(cc) to identify independent
risk factors for infection.
Material and(cc) methods
Data were collected from all women who
underwent cesarean delivery in Asker and(cc)
Bærum Hospital during a 12-month period from
September 2003. Nine women were excluded
because(sc) of linguistic communication problems.
The study group then consisted of 326 women. The
Asker and(cc) Bærum Hospital is a community
hospital, serving 150,000 people, having
approximately 2,000 deliveries per year, and(cc) a
CS rate of 13.8% in the study period.
The CS was defined as elective if the procedure
was performed at least 8 h after the decision was
made to operate. CS performed within 8 h of the
decision, were classified as an emergency operation.
All women having an emergency CS received
prophylactic antibiotics; Cefalotin (2 g) as an intra-
venous single dose after the umbilical cord was
clamped. Women presumed allergic to Cefalotin
were given Clindamycin (600 mg) instead. Women
with elective CS received no antibiotic prophylaxis.
This procedure is in accordance with the
Norwegian national guidelines (21).
All surgical interventions were performed jointly
by an attending physician and(cc) a resident. Our
stand(cc) ard operative procedure, after cutaneous
disin- fection with chlorhexidin, is a low transverse
incision followed by a cross-sectional incision on the
lower uterine segment. The abdomen is closed with a
continuous single layer suturation (Polyglactine 910 †,
absorbable) of the uterotomy and(cc) the fascia,
and(cc) an intracutaneous suture of the skin.
On the day of discharge, the surgical wound was
inspected and(cc) classified according to CDC
defini- tions. Two of the authors (HKO and(cc)
AGA) were responsible for this procedure. All
women were meticulously instructed about signs
and(cc) symptoms of SSI, and(cc) were asked to
contact the hospital if they suspected an infection,
within 30 days after the operation. A questionnaire
to record the wound healing during the 30 days
observational period was hand(cc) ed out. Every
contact with the health care system and(cc) every
conceivable mode of treatment of the wound were
registered. The questionnaire was to be completed
and(cc) returned in a prepaid envelope 30 days
after the surgical intervention. Non-respon- ders
received a reminder. Those still(sc) not responding
 Post-cesarean surgical site infections according to CDC stand(cc) ards
1099
Table I. Pre- and(cc) post-operative characteristics of the study group.

Emergency CS (n =201) Elective CS (n =125) p -value

Age, mean (range) 31.8 (21 −42) 33.4 (24 −41) 0.001
Nulliparous (%) 124 (61.7) 40 (32.0) B0.01
BMI, mean (range) 29.5 (18 −50) 28.1 (20 −42) 0.013
No. of women with intact/ruptured membranes 57 (intact membranes) 122 (intact membranes)
Before(sc) the CS 144 (ruptured membranes) 3 (ruptured membranes)
Time from rupture of membranes to CS Mean:19.4 h (range: 1 −105) Mean: 0 h
No. of women with temperature>388C 21 (10.4) 0 B0.001
Before(sc) the CS (%)
No. of women receiving antibiotic treatment 17 (8.5) 4 (3.2) 0.066
Before(sc)the CS (%)
No. of women receiving prophylactic antibiotics in 178 (88.6) 5 (4) B0.001
relation to CS (%)
No. of women with bacterial vaginosis confirmed 1 (0.5) 1 (0.7) 1.00
pre-op. (%)if
No. of women with vaginal Streptococcus-B 7 (5) 1 (0.8) 1.00
confirmed pre-op. (%)
No. of women on current immunosuppressive 0 2 (1.5%) 0.16
treatment (%)
No. of women on current anti-viral treatment (%) 1 (0.5%) 0 1.00
Number of post-op. days in maternity ward, 5.1 (1 −19) 4.6 (1 −10) 0.01
mean (range)
No. of women with temperature>388C post-op. (%) 13 (6.5) 4 (3.2) 0.43
No. of women having SSI diagnosed before hospital 4 (2) 2 (1.6) 1.00
discharge (%)

were traced and(cc) interviewed by telephone. All
326 women were registered without any drop-outs.
Statistical analyses were performed by means of
Statistical Packages for Social Sciences (SPSS,
version 14). Comparisons between groups were
obtained by x2 test, t -test and(cc) Mann−Whitney
test. Stratified analyses and(cc) logistic regression
ana- lyses were used to identify risk factors for
infection. Results are reported with 95% confidence
interval (CI).
Results
In total, 29 out of 326 women (8.9%) developed an
SSI after CS. Demographic data and(cc) pre-
operative variables were registered on a form.
These variables are listed in Table I, together with
data from the post-operative hospital stay collected
from the pa- tient record.
Among the 326 women undergoing CS in the
study period, 125 (38.5%) had an elective CS
and(cc) 201 (61.5%) had an emergency CS. The
SSI rate in
the elective and(cc) emergency groups were 9
(7.2%) and(cc) 20 (10%), respectively. The
difference in SSI between the 2 groups of CS was
not(c2) significant (p = 0.24). In the emergency CS
group, 11 women (3.4%) had their surgical
procedures performed with a maximum of urgency,
and(cc) did not(c2) receive preoperative cutaneous
disinfection. None of these 11 women developed
SSI. Out of the 29 women with SSI, 23 recognised the
wound infection after hospital discharge, accounting
for 79.3% of the SSI. The 23 women were examined
by a physician at the hospital. All infections were
superficial, and(cc) the description of the treatment is
listed in Table II.
Variables expected to be related to SSI were
analysed in relation to SSI: age, nationality, parity,
body mass index (BMI), bacterial vaginosis during
pregnancy, elapsed time from rupture of mem-
branes, duration of labour, maternal fever during
labor, emergency nature of the operation, duration
of the operation, volume of blood loss, antibiotic
prophylaxis (or antibiotic treatment of co morbid-
ity), and(cc) length of hospital stay. Variables
with a

Table II. Treatment of post-cesarean SSI.

Total no. of SSI Local treatment Systemic

(all superficial) No treatment (ointment containing antibiotics) Systemic antibiotics Surgical revision antibiotics‡surgery

29 3 5 8 4 9

1100 H.K. Opøien et al.

Table III. A cross tabulation of the two risk factors (BMI >30
and(cc) operation time ]38 min) and(cc) SSI, demonstrating a
high risk group of 31 women.
BMI530 BMI>30
Operation time B38 min 5.5% (9/164) 9.6% (7/73)
Operation time]38 min 7.3% (4/55) 29% (9/13)
p- -value B0.10 were included simultaneously as
in- dependent variables in a logistic regression
analysis. This analysis revealed two significant,
independent risk factors for(cc) post-cesarean SSI.
1. Operating time ]38 min; p =0.026,
unadjusted OR=2.5 (95% CI: 1.1 −5.2),
adjusted OR=
2.4 (95% CI: 1.1 −5.3). The group was
divided into quartiles according to operation
time, and(cc) within each quartile the risk of
infection was calculated. We then found that
in the 3 first quartiles, the risk of infection
was similar, whilst in the fourth quartile, it
was increased. The cut of time between the
fourth and(cc) other quartiles was 38 min.
2. BMI>30; p =0.007, with an adjusted OR=
2.8 (95% CI: 1.3 −6.2).
A cross tabulation (Table III) of the two risk factors
and(cc) SSI showed a high risk group of 31 women
with BMI>30 and(cc) operating time]38 min, in
which as many as 9 (29%) developed SSI, indicating
an elevated risk for infection in this group.
Discussion
We found a post-cesarean SSI rate of 8.9% when(sc)
the observational period was 30 days according to the
CDC stand(cc) ard. The study represents an entire
geographical cohort of women requiring CS for
various clinical and(cc) socio-psychological reasons.
We believe the SSI incidence in the present study to
be the true incidence, due primarily to the 100%
response in the follow-up, and(cc) to the CDC
criteria of 30 days observation time. The strict
criteria for(cc) the diagnosis of the SSI to be
either(c2) superficial or profound were followed,
and(cc) only two of the participating obstetricians
were involved in the classification procedure.
The possible pitfall of misjudging a wound infec-
tion when the woman herself is reporting it has been
tentatively controlled for(cc) by investigating all her
contacts with the health care system in the observa-
tion period. The patient’s assessment of the wound
has low positive predictive value, but more impor-
tant, a negative predictive value as high as 98%
according to Withby et al., arguing that very few
cases of SSI are missed when women assess the
wound status (22). The size of the study
population may represent a limitation for
estimating moderately increased risk factors. The
documented increased risk of prolonged
operation time ]38 min was, however,
statistically well supported.
Post-cesarean infection rate has been reported to
vary from 1.1 to 25% in different studies, but
comparison is difficult because(sc) of different
defini- tions, classifications and(cc) observation
time (9,13,14, 16−18,23 −25). Few studies report
SSI registrations from elective and(cc) emergency
cesareans separately, or apply the CDC criteria. In
the report from the Norwegian ‘Breakthrough
Project’, the incidence of wound infection was as
low as 2.2 and(cc) 2.7% in the group of women
with regional and(cc) general anesthe- sia,
respectively (4). This is in accordance with earlier
reports, such as Ehrenkranz et al. reporting a
wound infection rate of 1.1%, and(cc) Nielsen et
al. reporting an infection rate of 1.6% (9,24). But in
both reports, the observation time was confined to
the hospital stay. However, Couto et al. and(cc)
Tran et al. found 9.6 and(cc) 9.8%, respectively,
SSI when the follow-up period was 30 days after
hospital discharge (17,18).
In a Cochrane Review, only 14 of the 66 rand(cc)
o-
mised studies included are from western European
countries, and(cc) among them, only 4 are from
the Nordic countries (26). Prophylactic use of
antibio- tics for all CS interventions had been the
general recommendation in this database of
systematic re- views. The main argument for this
was prevention of SSI and(cc) endometritis.
Endometritis is argued to occur as often as in 61%
of all CS, and(cc) is reduced by up to 75%
when(sc) prophylactic antibiotics are applied (26).
In two different Norwegian studies, the in- cidence
of endometritis was reported to be B1% (27,28).
This supports the view that SSI is the more
important post-cesarean infection in Norway,
and(cc) hence our main consideration concerning
indica- tions for the use of prophylactic antibiotics.
In the present study, no significant difference in
infection rate was detected between elective
and(cc) emergency operations, but, emergency CS
has been demonstrated to be a major risk factor for
complica- tions in several previous studies
(12,24,29 −32). According to our national
consensus, prophylactic antibiotics are
recommended in all emergency CS (21). If our use
of prophylactic antibiotics has had the anticipated
effect, a real SSI difference between elective
and(cc) emergency operations may have been
masked. The use of prophylactic antibiotics in rela-
tion to elective CS has been reported to vary
between the different obstetric departments in
Norway (6).
 Post-cesarean surgical site infections according to CDC stand(cc) ards
Bagratee et al. demonstrated a marginal and(cc)
non- significant reduction in SSI rate (0.8%) with the
use of prophylactic cefoxitin in elective CS, and(cc)
Ruiz et al. found no statistically significant
differences in elective CS in ‘infection related
complications’ (11,33).
Our study demonstrates that an operating time
]38 min and(cc) BMI>30 are independent risk
factors for post-cesarean SSI. The association
between increasing BMI (or subcutaneous tissue
thickness), and(cc) the safety of surgical
procedures and(cc) post- operative infection has
been thoroughly documented (10,15,17,24,34,35).
But, to our knowledge, longer lasting operations
with a specific cut of time, independent of the peri-
operative blood loss, has not(c2) been described as
an operative risk factor for SSI. The need for an
experienced obstetrician to be present and(cc)
responsible for the operative procedure is
supported.
The implication of this study is that the true
incidence of post-operative SSI is underestimated if
post-discharge surveillance is not(c2)
implemented. Actual recommendations on this
issue vary between different countries. We believe
that women with significant increase in risk factors
(operating time exceeding 38 min and(cc)
BMI>30) should receive antibiotics, regardless of
whether the CS is an elective or an emergency
operation. As the use of antibiotics has individual
and(cc) environmental side- effects that must to be
taken into account, limitation of their use has long
been advocated (36). The benefit of expand(cc) ed
use of prophylactic antibiotics in order to reduce
the incidence of SSI should be questioned,
when(sc) treating only the subgroups at increased
risk is a justified option.
Conclusion
The rate of SSI is underestimated if the observation
time is limited to the hospital stay. Operating time
exceeding 38 min together with a BMI>30 sub-
stantially increased the risk of SSI in the present
study. To prevent an expand(cc) ed use of
antibiotics, and(cc) to further prevent SSI,
subgroups at risk should be identified and(cc)
treated with antibiotics in relation to the operation.
Acknowledgements
We thank Professor Per Bergsjø for valuable com-
ments on the manuscript and(cc) Professor Leiv
Sand(cc) vik for assistance with the statistics.
1101
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