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Effect of interventions in reducing the

rate of infection after cesarean delivery


Raed Salim, MD,a,b Meirav Braverman, MD,a Ilanit Berkovic, RM,a Abeer Suliman, MD,a Nava Teitler, RNMA,c
and Eliezer Shalev, MDa,b
Afula and Haifa, Israel

Background: Post–cesarean delivery (CD) surgical site infections can cause considerable maternal morbidity. We aimed to estimate
the efficacy of a medical personnel education program in aseptic and scrub techniques on the rate of infectious morbidity after CD.
Methods: A prospective, 2-period cohort intervention study was performed at a single institution. The first era, which included all
CDs performed between September 2006 and August 2007, was used to obtain baseline infection rates. During this period, prophy-
lactic antibiotics were given only to women undergoing elective CD. In era 2, July 2009 through June 2010, prophylactic antibiotics
were given to all women. In addition, medical personnel underwent an education program, refresher course, and retraining in
aseptic and scrub techniques. The study’s primary outcome included any infectious morbidity related to the CD within 30 days
from the operation.
Results: The 1,616 CDs analyzed included 751 performed in era 1 and 865 performed in era 2. The incidence of any infectious
morbidity dropped from 6.4% in era 1 to 2.5% in era 2 (P 5 .001). The incidence of any infectious morbidity in women undergoing
elective CD fell from 5.3% to 0.9% (P 5 .001). Among women undergoing nonelective CD, the difference between the first and
second eras was not statistically significant (7.5% vs 4.5%; P 5 .09). However, the rate of incisional surgical site infection fell sig-
nificantly, from 4% in era 1 to 1.5% in era 2 (P 5 .05).
Conclusions: The interventions implemented at our institution led to a considerable decline in post-CD infectious morbidity.
Key Words: Personnel education program; post-cesarean surgical site infection.
Copyright ª 2011 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights
reserved. (Am J Infect Control 2011;39:e73-8.)

Post–cesarean delivery (CD) surgical site infections strategy is recommended by the American College of
(SSIs) may cause considerable morbidity and have Obstetricians and Gynecologists4 and other consensus
other significant consequences in terms of prolonged panels.3,5 Contradictory findings regarding the efficacy
maternal length of hospital stay, socioeconomic impli- of perioperative antibiotics in women undergoing CD
cations, and increased health care costs. Estimates of while not in labor have been reported.6-9 A meta-
post-CD SSI rates range from 7% to 20%, depending analysis of prophylactic antibiotic therapy in nonlabor-
on demographic and obstetric variables and on the cri- ing CD reported a reduced risk for endometritis and
teria used to diagnose infection.1,2 The incidence might postoperative fever but only a trend toward a reduced
be underestimated when SSIs are not defined in accor- risk for incisional SSI.10 The use of staff education and
dance with the US Centers for Disease Control and retraining in scrub technique and appropriate skin
Prevention criterion of an infection occurring up to preparation is another intervention aimed at reducing
30 days after the surgical procedure.3 the incidence of SSI. The superior protection afforded
Several strategies to reduce the incidence of SSI have by appropriate skin preparation is attributed primarily
been proposed. The efficacy of perioperative antibiotics to a reduced rate of incisional SSI rather than to a re-
in reducing SSIs after CD in women in labor has duced rate of organ infection. Regardless, contradictory
been documented in a number of studies, and this results regarding the efficacy of this intervention in
women undergoing CD have been reported.11,12
From the Department of Obstetrics and Gynecology, Emek Medical The present study was undertaken to first document
Center, Afula, Israela; Rappaport Faculty of Medicine, Technion, Haifa, the true incidence of post-CD SSI according to the Cen-
Israelb; and Infectious Diseases Unit, Emek Medical Center, Afula, Israel.c ters for Disease Control and Prevention’s criterion at
Address correspondence to Raed Salim, MD, Department of Obstetrics our institution, and then to estimate the efficacy of
and Gynecology, Emek Medical Center, Afula 18101, Israel. E-mail: medical personnel education and retraining in aseptic
salim_ra@clalit.org.il.
and scrub techniques in addition to antibiotic prophy-
Conflict of interest: None to report. laxis in reducing that incidence.
0196-6553/$36.00
Copyright ª 2011 by the Association for Professionals in Infection
Control and Epidemiology, Inc. Published by Elsevier Inc. All rights METHODS
reserved.
This was a prospective, 2-period cohort interven-
doi:10.1016/j.ajic.2011.05.001
tion study of women who underwent CD at a single

e73
e74 Salim et al. American Journal of Infection Control
December 2011

academic institution. The study’s first era included all X-ray). Other infections included necrotizing fasciitis,
CDs performed between September 2006 and August pelvic abscess, and septic pelvic thrombophlebitis. A
2007. Up to the end of this period, prophylactic anti- composite postpartum infectious morbidity was de-
biotic therapy (cefalotin 1 g as a single intravenous fined as the presence of any postpartum infection
[IV] dose) after umbilical cord clamping was given outcome.
only to women undergoing nonelective CD. Women All procedures in both eras were performed jointly
presumed to be allergic to cefalotin were instead given by a senior physician and a resident. Technically, the
clindamycin 600 mg as a single IV dose after umbilical procedure was performed similarly in both eras. A
cord clamping. Data from era 1 were analyzed to ob- skin stapler (Royal AutoSuture; Covidien, Mansfield,
tain baseline infection rates. MA) was used to approximate the skin edges.
Before the beginning of era 2, which included all Data on demographic characteristics, medical and
CDs performed between July 2009 and June 2010, obstetric history, course of labor and delivery, and post-
medical personnel underwent a refresher course in operative maternal complications were collected. Data
aseptic and scrub techniques by the infection con- on infectious complications in each era were collected
trol nurse. This education and retraining included during the in-hospital stay and in the community set-
review of aseptic practices in the operating room to- ting on postoperative day 30-35. In-hospital, infectious
gether with scrubbing, room setup, proper attire, complications were diagnosed by a surgeon or infec-
and surgical preparation technique.11,13 The specific tious disease specialist and recorded on a standard
steps for skin preparation with chlorhexidine gluco- data collection form. Postdischarge surveillance was
nate (CHG) 4% scrub for 2 minutes, followed by based on telephone contacts with the women and per-
2 minutes of disinfection with CHG 0.5% in alcohol formed using a standard questionnaire format. All
70%, and letting the skin air-dry for 1 minute was women were contacted by telephone at 30-35 days af-
also emphasized. The theatre nursing team under- ter surgery and were asked to answer a brief question-
went a refresher team session with the infection naire regarding their general health, fever and other
control nurse, discussing hand hygiene, urinary potential symptoms of infection, antibiotic use, and
catheter insertion, patient preparation, and aseptic emergency department visits. In cases of readmission,
principles. Observation and feedback took place dur- surveillance was expanded using hospital databases
ing the intervention period. In addition, prophylactic that included data on administrative claims and
antibiotics after cord clamping were given to all treatments.
women undergoing CD. The same protocol as in The study’s primary outcome was a comparison of
era 1 was applied in era 2 for both elective and non- the incidence of composite postpartum infectious mor-
elective CDs. bidity in era 2 (study group) and in era 1 (control
A CD was defined as elective if the woman had intact group). Secondary outcomes included comparisons of
membranes, did not have regular uterine contractions the rate of any infectious morbidity between the 2
regardless of membrane status, and was in a fasting eras, as well as between women with elective CD and
state for a period of 6-8 hours before the procedure, those with nonelective CD. The study was approved
and as nonelective otherwise. Women who had an ac- by the local Institutional Review Board before each era.
tive infection within 1 week of admission or during la-
bor were excluded, as were women who had placenta Statistical analysis
accreta or a cesarean hysterectomy.
Although deep incisional infections involving the As appropriate, x2 or Fisher’s exact test was used to
fascial and muscle layers rarely occur after CD,14 for compare categorical data across the 2 eras. An inde-
the purpose of this study SSIs were classified as either pendent sample t test, or the Mann-Whitney U test in
incisional or organ (endometritis). Postpartum endo- the case of nonnormally distributed data, was used to
metritis was defined as a postpartum temperature of compare continuous data across the 2 eras. Logistic
388C or higher measured on 2 separate occasions ac- regression was used to adjust the infection rate for var-
companied by abnormal uterine tenderness or puru- iables that were significant in a univariate analysis of
lent drainage from the uterus requiring postpartum the 2 eras. Poisson regression was used to adjust the
antibiotic therapy. Criteria for defining incisional SSI infection rate in women undergoing elective CD with
included pain or tenderness, localized swelling, red- urinary tract infection, because of the small number
ness, or heat with or without purulent drainage. Other of cases. Statistical significance was set at P , .05. An
infectious complications recorded included urinary analysis of the data from era 1 showed that a total of
tract infection (diagnosed clinically and confirmed 749 women in each era would be required to provide
by positive urinary culture) and pneumonia (diag- 80% power to detect a 50% reduction in the incidence
nosed clinically and confirmed by positive chest of composite postpartum infectious morbidity in the
www.ajicjournal.org Salim et al. e75
Vol. 39 No. 4

Table 1. Demographic and obstetric characteristics of all women who underwent CD during eras 1 and 2
Era 1 (n 5 751) Era 2 (n 5 865) P

Ethnicity, n (%) .63


Jewish 399 (53.1) 454 (52.5)
Arab 352 (46.9) 411 (47.5)
Maternal age, years, mean 6 SD 31.9 6 5.4 31.7 6 5.6 .42
Gestational age, weeks, mean 6 SD 38.1 6 2.5 37.9 6 2.5 .14
Parity, mean 6 SD 2.75 6 1.7 2.68 6 1.5 .38
Body mass index, kg/m2, mean 6 SD 30.9 6 5.3 31.3 6 5.8 .19
Body mass index .35 kg/m2, n (%) 158 (21.0) 208 (24.0) .14
Diabetes, n (%) 98 (13.1) 97 (11.2) .25
Previous cesareans, mean 6 SD 1.76 6 0.9 1.76 6 0.9 .98
Nonelective cesareans, n (%) 373 (49.7) 400 (46.2) .17
Internal monitoring, n (%) 38 (5.1) 46 (5.3) .81
Vaginal examinations, mean 6 SD 1.9 6 3.3 2.1 6 3.5 .38
Time in delivery ward, hours, mean 6 SD (range) 2.2 6 6.0 (0-70) 2.2 6 5.4 (0-36) ,.99
Rupture of membranes, n (%) 179 (23.8) 163 (18.8) .01
Duration of membrane rupture, hours, mean 6 SD (median; range) 16.3 6 29.7 (8; 0.4-288) 26.7 6 95.2 (8; 0.5-840) .58
Hospital days before cesarean, mean 6 SD (median; range) 0.9 6 1.7 (1; 0-25) 1.0 6 2.4 (1; 0-36) .14
Anesthesia, n (%) .65
General 121 (16.1) 125 (14.5)
Spinal 573 (76.3) 674 (77.9)
Epidural 57 (7.6) 66 (7.6)
Skin cleansing, n (%) .67
Yes 748 (99.6) 863 (99.8)
No 3 (0.4) 2 (0.2)
GBS prophylaxis, n (%) 7 (0.9) 8 (0.9) .99
Duration of operation, minutes mean 6 SD 31 6 15 34 6 15 .001
,30 minutes, n (%) 386 (51.4) 364 (42.1)
30-60 minutes, n (%) 341 (45.4) 462 (53.4)
.60 minutes, n (%) 24 (3.2) 39 (4.5)
Blood loss .1,000 mL, n (%) 16 (2.1) 29 (3.4) .14
Days of hospitalization after cesarean, mean 6 SD (median; range) 4.5 6 1.4 (4; 2-21) 4.4 6 1.2 (4; 1-14) .39
CI, confidence interval; GBS, Group B Streptococcus.

study group compared with the control group (ie, first although the proportion of patients with an operation
era) with 95% confidence. time .1 hour was similar in the 2 eras (P 5 .20).
The interventions significantly decreased the inci-
RESULTS dence of composite postpartum infectious morbidity
in era 2 compared with era 1, with the most significant
Among the 4,105 women who gave birth during era decrease seen in incisional SSI (Table 2).
1, 761 (18.5%) underwent CD. Ten women were ex- There was a statistically significant reduction in
cluded from the analysis because of intrapartum fever overall infectious morbidity among elective CDs
(n 5 6) or placenta accreta (n 5 4). Of the remaining (Table 2), notably in incisional SSI and urinary tract in-
751 CDs, 378 (50.3%) were elective and 373 (49.7%) fection. Although the incidence of organ SSI was re-
were nonelective. Among the 4,129 women who gave duced by 70%, this reduction was not statistically
birth during era 2, 875 (21.2%) underwent CD. Again, significant.
10 women were excluded because of intrapartum fever Among the nonelective CDs, the reduction in overall
(n 5 8) or placenta accreta (n 5 2). Of the remaining infectious morbidity was not statistically significant;
865 CDs, 465 (53.8%) were elective and 400 were non- however, the incidence of incisional SSI was signifi-
elective (46.2%). In total, 1,616 women were included cantly reduced. Adjustment of incisional SSI for rup-
and analyzed in the 2 eras. Demographic and obstetric ture of membranes or duration of operation did not
characteristics were similar in the 2 eras (Table 1), ex- change the results (Table 2).
cept that the rate of rupture of membranes was signif- We were able to contact 99.1% of the women in era
icantly higher in era 1 than in era 2 (23.8% vs 18.8%; 1 and 99.2% of those in era 2 at 30-35 days after sur-
P 5 .01). In addition, the mean operation time was lon- gery. Out of all women with any infectious morbidity
ger in era 2 (34 minutes vs 31 minutes; P 5 .001), during era 1, 17 (34%) were diagnosed after discharge;
e76 Salim et al. American Journal of Infection Control
December 2011

Table 2. Incidence of infectious morbidity in eras 1 and 2


All CDs Elective CDs Nonelective CDs
Era 1 Era 2 P* OR Era 1 Era 2 P* OR Era 1 Era 2 P* OR
Variables (n 5 751) (n 5 865) (95% CI) (n 5 378) (n 5 465) (95% CI) (n 5 373) (n 5 400) (95% CI)

Composite infectious 48 (6.4) 22 (2.5) 0.001 20 (5.3) 4 (0.9) .001 28 (7.5) 18 (4.5) .09
morbidity, n (%) .38 (0.23-0.64) 0.14 (0.05-0.42) 0.59 (0.32-1.09)
SSI, n (%) 37 (4.9) 18 (2.1) 0.002 16 (4.2) 4 (0.8) .002 21 (5.6) 14 (3.5) .17
.40 (0.23-0.72) 0.18 (0.06-0.53) 0.61 (0.30-1.23)
Incisional SSI 26 (3.5)y 8 (0.9) 0.001 11 (2.9) 2 (0.4) .009 15 (4.0)y 6 (1.5) .05
.27 (0.12-0.59) 0.13 (0.03-0.61) 0.38 (0.14-0.99)
Organ SSI 12 (1.6)y 10 (1.2) 0.52 5 (1.3) 2 (0.4) .12 7 (1.9)y 8 (2.0) .99
.67 (0.28-1.56) 0.27 (0.05-1.44) 1.01 (0.36-2.84)
Pneumonia, n (%) 2 (0.3) 1 (0.1) 0.36 0 (0.0) 0 (0.0) - 2 (0.5) 1 (0.3) .37
.31 (0.02-3.96) 0.31 (0.02-4.00)
Urinary tract infection, n (%) 9 (1.2) 3 (0.3) 0.08 4 (1.1) 0 (0.0) .003z 5 (1.3) 3 (0.8) .49
.31 (0.08-1.17) 0.80 (0.71-0.93) 0.60 (0.14-2.55)
CI, confidence interval; OR, odds ratio.
*Adjusted for rupture of membranes and duration of operation.
y
One woman had both organ SSI and incisional SSI.
z
Poisson regression.

all were related to incisional SSI. In era 2, 8 women .5% incidence of infectious morbidity among nonla-
(32%) were diagnosed after discharge, 6 with inci- boring women undergoing CD. Hunt et al16 also rec-
sional SSI and 2 with organ SSI. There were no cases ommended the use of antibiotic prophylaxis when
of necrotizing fasciitis, pelvic abscess, or septic pelvic the rate of SSI exceeds 5%. According to these recom-
thrombophlebitis. mendations, we implemented perioperative antibi-
otics after documenting an infectious morbidity rate
DISCUSSION of 5.3% in women undergoing elective CD in era 1.
Nonetheless, it has been reported that up to two-
This study demonstrates that a staff education pro- thirds of SSIs are confined to the incision,3,17,18 and
gram and a refresher course in effective and proper optimizing skin antisepsis before surgery could have
skin antisepsis in addition to antimicrobial prophylaxis a significant clinical benefit.
after cord clamping significantly reduced the incidence Antiseptics act mainly against organisms that re-
of post-CD infectious morbidity. Although the main re- side on the patient’s integument, and the overall su-
duction in this study was attributed to a reduced inci- perior protection afforded by CHG likely can be
dence of incisional SSI and urinary tract infection, a attributed primarily to a reduced rate of incisional
trend toward a reduction in organ SSI was also observed SSI rather than to a reduction in organ SSI. In addi-
among the elective procedures. Although the reduction tion, implementation of an intensive surveillance
from 1.3% in era 1 to 0.4% in era 2 was not significant program with engaged clinicians and infection con-
among the elective CDs, it was calculated that ;4,000 trol personnel is known to contribute to a reduced
women in each era would be required to provide 80% incidence of health care–associated infections.19
power with an a of 0.05 to detect a 50% reduction Identified barriers to adhering to clinical guidelines
from a relatively low baseline rate of 1.3%. include lack of awareness of guidelines, lack of famil-
The fundamental cornerstones in any program iarity with the guidelines, lack of agreement, lack of
aimed at reducing the incidence of SSI include exqui- self-efficacy, lack of outcome expectancy, and inertia
site surgical technique, timely and appropriate anti- of previous practice.20 Compliance to clinical guide-
microbial prophylaxis, and effective and persistent lines could be improved by educating staff on the im-
skin antisepsis.15 Contradictory findings have been portance of their contributions in reducing infection
published regarding the efficacy of perioperative anti- rates.21 Accordingly, we implemented a program of
biotics in nonlaboring CD.6-9 A meta-analysis of pro- medical personnel education before the start of era
phylactic antibiotic regimens for nonlaboring CDs 2 that included a refresher course in aseptic and scrub
found reduced risks for endometritis and postopera- techniques. Compared with Kaimal et al,12 who re-
tive fever, but only a trend toward a reduced risk of in- ported no effect of policy changes to improve aseptic
cisional SSI.10 Based on those results, the authors technique, we found a significant reduction in the in-
recommended prophylaxis in populations with a cidence of incisional SSI. This effect was obvious in
www.ajicjournal.org Salim et al. e77
Vol. 39 No. 4

the women who underwent nonelective CD, in whom CONCLUSIONS


only staff education differed between the 2 eras. In
the group with elective CD, in whom staff education In the present study, the interventions of the multidis-
was implemented in addition to perioperative antibi- ciplinary health care providers led to a considerable de-
otics in era 2, reductions in both composite infectious cline in post-CD infectious morbidity. Direct health care
morbidity and incidence of incisional SSI were ob- providers are responsible for ensuring that appropriate
served. Whereas Chelmow et al10 reported only a infection prevention and control practices are consis-
trend toward a reduced rate of incisional SSI with tently applied. Future studies are needed to investigate
the use of perioperative antibiotics in elective CD, whether the consequences of staff education and inten-
our results point to an additive effect of staff educa- sive surveillance program have long-lasting effects.
tion in reducing the incidence of incisional SSI in We thank Paula S. Herer, biostatistician at the Emek Medical Center, for assisting with
elective CD. the statistical analysis.
The wide variation in the reported incidence of post-
CD SSI of 7%-20%1,2 likely can be attributed to several
factors, including whether or not postdischarge data References
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