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Risk Factors for Surgical Site Infection After Low Transverse Cesarean Section
Author(s): By Margaret A. Olsen,, PhD, MPH; Anne M. Butler,, MS; Denise M. Willers,, MD;
Preetishma Devkota,, MBBS; Gilad A. Gross,, MD; Victoria J. Fraser,, MD
Source: Infection Control and Hospital Epidemiology, Vol. 29, No. 6 (June 2008), pp. 477-484
Published by: The University of Chicago Press on behalf of The Society for Healthcare Epidemiology of
America
Stable URL: http://www.jstor.org/stable/10.1086/587810 .
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                            This content downloaded from 150.214.230.47 on Sun, 31 Mar 2013 09:45:24 AM
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infection control and hospital epidemiology                  june 2008, vol. 29, no. 6


                                                          original article

                          Risk Factors for Surgical Site Infection After
                               Low Transverse Cesarean Section

         Margaret A. Olsen, PhD, MPH; Anne M. Butler, MS; Denise M. Willers, MD; Preetishma Devkota, MBBS;
                                     Gilad A. Gross, MD; Victoria J. Fraser, MD


(See the commentary by Lee on pages 485– 486)
background. Independent risk factors for surgical site infection (SSI) after cesarean section have not been well documented, despite the
large number of cesarean sections performed and the relatively common occurrence of SSI.
objective.      To determine independent risk factors for SSI after low transverse cesarean section.
design.     Retrospective case-control study.
setting.      Barnes-Jewish Hospital, a 1,250-bed tertiary care hospital.
patients.      A total of 1,605 women who underwent low transverse cesarean section during the period from July 1999 to June 2001.
methods. Using the International Classification of Diseases, Ninth Revision, Clinical Modification diagnosis codes for SSI or wound compli-
cation and/or data on antibiotic use during the surgical hospitalization or at readmission to the hospital or emergency department, we identified
potential cases of SSI in a cohort of patients who underwent a low transverse cesarean section. Cases of SSI were verified by chart review using
the definitions from the Centers for Disease Control and Prevention’s National Nosocomial Infections Surveillance System. Control patients
without SSI or endomyometritis were randomly selected from the population of patients who underwent cesarean section. Independent risk
factors for SSI were determined by logistic regression.
results. SSIs were identified in 81 (5.0%) of 1,605 women who underwent low transverse cesarean section. Independent risk factors for SSI
included development of subcutaneous hematoma after the procedure (adjusted odds ratio [aOR], 11.6 [95% confidence interval {CI}, 4.1–
33.2]), operation performed by the university teaching service (aOR, 2.7 [95% CI, 1.4 –5.2]), and a higher body mass index at admission (aOR,
1.1 [95% CI, 1.0 –1.1]). Cephalosporin therapy before or after the operation was associated with a significantly lower risk of SSI (aOR, 0.2 [95%
CI, 0.1– 0.5]). Use of staples for skin closure was associated with a marginally increased risk of SSI.
conclusions.        These independent risk factors should be incorporated into approaches for the prevention and surveillance of SSI after surgery.
                                                                                                       Infect Control Hosp Epidemiol 2008; 29:477– 484


Surgical site infection (SSI) after a cesarean section increases              atively high. We performed a large case-control study to deter-
maternal morbidity and medical costs.1 The rates of SSI after                 mine clinically relevant independent risk factors for SSI after
cesarean section reported in the literature range from 3% to                  low transverse cesarean section. A low transverse uterine inci-
15%, depending on the surveillance methods used to identify                   sion is the preferred type of incision for cesarean section, be-
infections, the patient population, and the use of antibiotic                 cause it is associated with less blood loss and lower risk of sub-
prophylaxis.2-11 The pooled mean rate of SSI after cesarean sec-              sequent uterine rupture than a vertical incision. It is used for
tion for US hospitals participating in the Centers for Disease                the vast majority of cesarean section deliveries in the United
Control and Prevention’s National Nosocomial Infections                       States, whereas a vertical incision (alone or in combination
Surveillance System is 3.15%.12                                               with a low transverse incision) is typically used for a minority
   Expanding our knowledge of the risk factors associated with                of cesarean section deliveries, for selected obstetric reasons or
SSI is essential to developing targeted prevention strategies to              when there is need for rapid delivery.14
reduce the risk of SSI. Independent risk factors for SSI after
cesarean section have not been well documented, despite the                   methods
fact that it is the most commonly performed surgical proce-                   This study was conducted at Barnes-Jewish Hospital, a 1,250-
dure in the United States,13 and the reported rate of SSI is rel-             bed tertiary care hospital. It is the academic hospital for the

  From Division of Infectious Diseases (M.A.O., A.M.B., P.D., V.J.F.) and Department of Obstetrics and Gynecology (D.M.W., G.A.G.), Washington University
School of Medicine, St. Louis, Missouri.
  Received December 7, 2007; accepted February 24, 2008; electronically published May 30, 2008.
© 2008 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2008/2906-0001$15.00. DOI: 10.1086/587810




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                                                    All use subject to JSTOR Terms and Conditions
478   infection control and hospital epidemiology           june 2008, vol. 29, no. 6


Washington University School of Medicine and has a referral            within 24 hours before incision and within 48 hours after in-
base of patients from metropolitan St. Louis and within a 200-         cision. Additional postoperative variables included receipt of
mile radius of the city. At the hospital, the obstetrics service       blood transfusion (after incision during the cesarean section
performs approximately 4,000 deliveries per year and provides          admission) and development of a subcutaneous hematoma.
a full range of care, including high-risk maternal and fetal med-
icine. Obstetric care is provided by a full-time faculty in the        Definitions
department of obstetrics and gynecology at the Washington
University School of Medicine and by an adjunct obstetric fac-         Cohort patients were identified by an International Classifica-
ulty in private practice.                                              tion of Diseases, Ninth Revision, Clinical Modification (ICD-9-
   We performed a case-control study nested within a cohort            CM) procedure code for low transverse cesarean section (74.1)
of 1,605 women who underwent low transverse cesarean sec-              and were included only if the operative note indicated that a
tion during the period from July 1999 to June 2001. Demo-              low transverse uterine incision had been used. Screening for
graphic, pharmacy, and laboratory data were obtained from              wound complications was done during the surgical hospital-
the Barnes-Jewish Hospital Medical Informatics database. Risk          ization or rehospitalization (inpatient, emergency department,
factor data were collected from the medical records of each            or outpatient surgery admission) within 60 days after opera-
patient’s surgical hospitalization, including all notes by physi-      tion with use of ICD-9-CM discharge diagnosis codes for inci-
cians and/or nurses concerning the hospitalization.                    sional infection, dehiscence, wound necrosis, seroma, or he-
   Patient-related variables included age, race, marital status,       matoma (998.5, 998.51, 998.59, 674.32, or 674.34) and/or data
type of insurance, body mass index (BMI) at admission, weight          on excess use of antibiotics after operation.11,15 We reviewed all
gain during pregnancy, presence of diabetes mellitus, gesta-           of the hospital medical records of patients who met the screen-
tional diabetes, systemic lupus erythematosis, sexually trans-         ing criteria, to determine if they met the case definition for SSI
mitted diseases during pregnancy (eg, gonorrhea, chlamydia,            using the definitions from the Centers for Disease Control and
bacterial vaginosis, Trichomonas vaginalis infection, herpes           Prevention’s National Nosocomial Infections Surveillance Sys-
simplex virus infection, or human immunodeficiency virus in-            tem.16 We included case patients with SSI identified during the
fection), group B Streptococcus (GBS) colonization, and use of         surgical hospitalization or during an inpatient rehospitaliza-
alcohol, tobacco, illicit street drugs, and/or corticosteroids.        tion, emergency department visit, or outpatient surgery with
   For the mother, obstetrics-related variables included the
                                                                       signs and/or symptoms of SSI within 30 days after operation.
number of prior pregnancies, prior births, abortions, and pre-
                                                                       Questionable cases were verified by an obstetrician and gyne-
vious cesarean sections; presence of cervical incompetence; the
                                                                       cologist (D.M.W.). Control patients without SSI or endomyo-
number of vaginal exams before cesarean section; presence of
                                                                       metritis were randomly selected from the women who under-
vaginal discharge at admission; the number of prenatal care
visits; presence of preeclampsia, chorioamnionitis, maternal           went low transverse cesarean section during the study period.
fever, fundal tenderness before delivery, maternal and fetal
tachycardia, and/or vaginal bleeding; malpresentation; spon-           Statistical Analysis
taneous or assisted rupture of membranes; interval since rup-          Comparisons for categorical variables were performed using
ture of membranes; duration of labor; use of internal fetal            the ␹2 or Fisher exact test. Continuous variables were com-
monitors; use of Foley bulb for cervical ripening; receipt of          pared using the Student t or Mann-Whitney U tests. Linearity
amnioinfusion; and presence of meconium. For the infant,               assessments were performed on the variables of age and BMI.
obstetrics-related variables included gestational age at delivery,     Fractional polynomials were used to determine the best fit for
birth weight, and Apgar score.                                         BMI.17 Independent risk factors for SSI were determined by
   Operation-related variables included the American Society           multivariate logistic regression. All variables with P Ͻ .20 in
of Anesthesiologists score, urgency of operation, type of skin
                                                                       the univariate analysis or with a priori clinical significance were
and uterine incision, exteriorization of the uterus, manual re-
                                                                       evaluated by stepwise logistic regression for inclusion in the
moval of placenta, presence of drains, receipt of shave with
                                                                       final model. The variable for lack of private insurance (ie, reli-
razor, use of staples for skin closure, receipt of an additional
                                                                       ance on Medicaid or Medicare) was forced into the logistic
operative procedure, duration of time between hospital admis-
sion and operation, type of service (university teaching or pri-       regression model as a proxy for socioeconomic status. Interac-
vate), volume of blood loss, and receipt of antibiotic therapy.        tions between the type and the timing of antibiotic prophylaxis
   Cesarean sections were classified as elective, urgent, or            were tested in the multivariate models, but they did not meet
emergent according to standardized criteria by the operative           the criteria for inclusion (P Ͻ .05 for interaction terms). Model
team. True emergent procedures were classified as emergent              fit was assessed using the C statistic. All tests were 2-tailed, and
and did not include full surgical preparation. Hemoglobin and          P Ͻ .05 was considered significant. Statistical analyses were
hematocrit levels were determined within 24 hours before in-           performed with SPSS version 14.0 (SPSS). Approval for this
cision and within 48 hours after incision. The highest serum           study was obtained from the Washington University Human
glucose level, if available, was determined from blood obtained        Research Protection Office.




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risk factors for ssi after cesarean section                 479


results                                                                        table 1. Characteristics of 391 Patients Who Under-
                                                                               went Low Transverse Cesarean Section at Barnes-Jewish
During the 2-year study period, 1,759 patients underwent ce-
                                                                               Hospital During the Period From July 1999 to June 2001
sarean section in our academic tertiary care medical center. Of
those patients, 1,605 (91%) underwent a low transverse uterine                 Characteristic                                      Value
incision, and 81 (5.0%) of those 1,605 patients met the case                   Age, years                                      26.5 (15–43)
definition for SSI with onset of infection within 30 days after                 Body mass index at admission                    32.3 (17–65)
low transverse cesarean section. Seventy-five (92.6%) of those                  Race
81 patients had SSIs that were classified as superficial inci-                     Black                                          239 (61.1)
sional, 4 (4.9%) had deep incisional SSI, and 2 (2.5%) had                       White                                          127 (32.5)
organ space infection. Forty-eight (59.3%) of the 81 patients                    Other                                           25 (6.4)
                                                                               Tobacco use
had SSI diagnosed during surgical hospitalization, 27 (33.3%)
                                                                                 Never                                          294 (75.2)
during rehospitalization, and 6 (7.4%) during an emergency                       Prior use, quit during pregnancy                26 (6.6)
department visit. A total of 310 control patients without en-                    Current use                                     71 (18.2)
domyometritis were randomly selected for comparison with                       Had gonorrhea or Chlamydia infection
the 81 case patients with SSI.                                                     during pregnancy                              34 (8.7)
   The characteristics of the 81 case and 310 control patients                 HIV infection                                      4 (1.0)
are described in Table 1. Of these 391 patients, 239 (61.1%)                   Type of insurance
were black, 71 (18.2%) smoked during their pregnancy, 34                         Private                                        155 (39.6)
(8.7%) had gonorrhea or chlamydial infection during their                        Medicaid and/or Medicare                       236 (60.4)
pregnancy, 129 (33.0%) had 1 or more cesarean sections                         Service performing operation
                                                                                 University teaching                            226 (57.8)
previously, and 226 (57.8%) were admitted to the university
                                                                                 Private                                        165 (42.2)
teaching service. More than half of the patients were cov-                     No. of prior cesarean sections
ered by either Medicaid or Medicare, or had no health in-                        0                                              262 (67.0)
surance.                                                                         1                                               87 (22.3)
   In the univariate analysis, SSI occurred significantly more                    2                                               32 (8.2)
often among women with the following risk factors: presence                      3                                               10 (2.6)
of chorioamnionitis, induction of labor, use of staples for skin               Onset of labor
closure, development of subcutaneous hematoma after opera-                       Spontaneous                                    121 (30.9)
tion, and admission to the university teaching service (Table                    Induced                                         85 (21.7)
                                                                                 No labor                                       185 (47.3)
2). There was a significant association between a higher BMI at
                                                                               Type of cesarean section
admission and SSI (median BMI, 36.4 for case patients vs 31.8                    Elective                                       114 (29.2)
for control patients; P ϭ .003). Patients who had skin closure                   Urgent                                         215 (55.0)
with staples had a significantly higher median BMI than pa-                       Emergent                                        62 (15.9)
tients who had skin closure with sutures (33.1 vs 29.6; P ϭ                    Type of skin incision
.004). Patients admitted to the university teaching service were                 Vertical                                        10 (2.6)
significantly more likely to have skin closure with staples than                  Transverse                                     381 (97.4)
patients admitted to the private service (216 [95.6%] of 226 vs                note.     Data are no. (%) of patients or median value (range).
130 [78.8%] of 165 patients of patients; P Ͻ .001). There was a                Body mass index is defined as the weight in kilograms divided by
marginal association between longer duration of operation                      the square of the height in meters.
and SSI (mean duration, 63.1 minutes for case patients vs 57.9
minutes for control patients; P ϭ .090). Only 83% of patients           gentamycin or tobramycin, or ampicillin-sulbactam, 35 (60.0%)
had the duration of operation recorded, and, for this reason, it        had chorioamnionitis diagnosed.
was not included in further analyses.                                      Patients who were not given intravenous antibiotics before
   Antibiotics were administered intravenously to 178 (45.5%) of        or after incision were significantly more likely to have under-
391 patients before incision, including 109 (27.9%) who were            gone an elective operation than patients who were given anti-
given ampicillin, penicillin, or clindamycin, presumably for anti-      biotics (19 [42.2%] of 45 vs 95 [27.6%] of 346 patients; P ϭ
GBS prophylaxis, and 58 (14.8%) who received antibiotics for            .040). Twenty-two (48.9%) of the 45 patients who were not
chorioamnionitis or fever (Table 3). Of the 109 women who re-           given antibiotics were attended by a private physician (P ϭ
ceived ampicillin, penicillin, or clindamycin, 36 (33.0%) had GBS       .334). For 20 patients who did not receive antibiotic prophy-
colonization, and 55 (50.5%) had risk factors for GBS coloniza-         laxis, the operation was classified as urgent; for 6 patients who
tion (ie, urinary tract infection during pregnancy, fever, rupture of   did not receive antibiotic prophylaxis, the operation was clas-
membranes 18 hours or more before incision, and/or preterm              sified as emergent. When the analysis of the categories of anti-
labor [before week 37 of gestation]18) without documented posi-         biotics and the SSI risk was repeated using only the patients
tive culture results. Of the 58 women who received ampicillin plus      who underwent elective surgery without antibiotic prophylaxis




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                                                 All use subject to JSTOR Terms and Conditions
480   infection control and hospital epidemiology                  june 2008, vol. 29, no. 6


        table 2. Univariate Comparisons of Risk Factors for Surgical Site Infection (SSI) in Patients With and Patients Without
        SSI After Low Transverse Cesarean Section at Barnes-Jewish Hospital, July 1999 to June 2001
                                                                                       No. (%) of patients
                                                                                  Case group      Control group
        Risk factor                                                                (n ϭ 81)        (n ϭ 310)            OR (95% CI)        P
        Demographic factors
          Age Ͻ18 years                                                              6 (7.4)          17 (5.5)           1.4 (0.5–3.6)     .514
          Race
             White                                                                 27 (33.3)        100 (32.3)                1.0          ...
             Black                                                                 49 (60.5)        190 (61.3)           1.0 (0.6–1.6)     .865
             Other                                                                  5 (6.2)          20 (6.5)            0.9 (0.3–2.7)     .888
          Had diabetes mellitus or gestational diabetes                             8 (9.9)          30 (9.7)            1.0 (0.4–2.3)     .957
          Had gonorrhea or Chlamydia infection during pregnancy                    10 (12.3)         24 (7.7)            1.7 (0.8–3.7)     .194
          Had Trichomonas infection during pregnancy                               11 (13.6)         27 (8.6)            1.6 (0.8–3.5)     .191
          Had documented GBS colonization                                          15 (18.5)         46 (14.8)           1.3 (0.7–2.5)     .417
          Tobacco use (past or present)                                            25 (30.9)         72 (23.2)           1.5 (0.9–2.5)     .158
          Type of insurance
             Private                                                               30 (37.0)        125 (40.3)                1.0          ...
             Medicaid and/or Medicare                                              51 (63.0)        185 (59.7)           1.1 (0.7–1.9)     .590
          Type of service
             Private                                                               18 (22.2)        147 (47.4)                1.0          ...
             University teaching                                                   63 (77.8)        163 (52.6)           3.2 (1.8–5.6)    Ͻ.001
        Obstetric factors
          Use of internal monitors                                                 40 (49.4)        118 (38.1)           1.6 (1.0–2.6)     .066
          Had chorioamnionitisa                                                    21 (25.9)         41 (13.2)           2.3 (1.3–4.2)     .006
          No. of vaginal examinations
             0                                                                     12 (14.8)         63 (20.3)                1.0          ...
             1–6                                                                   49 (60.5)        192 (61.9)           1.3 (0.7–2.7)     .408
             ୑7                                                                    20 (24.7)         55 (17.7)           1.9 (0.9–4.3)     .114
          Induction of labor                                                       45 (55.6)        123 (39.7)           1.9 (1.2–3.1)     .011
          Duration of labor
             No labor                                                              35 (43.2)        150 (48.4)                1.0          ...
             Ͻ6 hours                                                              11 (13.6)         59 (19.0)           0.8 (0.4–1.7)     .553
             6–12 hours                                                            11 (13.6)         47 (15.2)           1.0 (0.5–2.1)     .994
             Ͼ12 hours                                                             24 (29.6)         54 (17.4)           1.9 (1.0–3.5)     .037
        Surgical factors
          Use of drains                                                            10 (12.3)         20 (6.5)            2.0 (0.9–4.6)     .081
          Use of staples for skin closure                                          79 (97.5)        267 (86.1)           6.4 (1.5–26.8)    .012
          Type of cesarean section
             Elective                                                              19 (23.5)         95 (30.6)                1.0          ...
             Urgent                                                                50 (61.7)        165 (53.2)           1.5 (0.8–2.7)     .164
             Emergent                                                              12 (14.8)         50 (16.1)           1.2 (0.5–2.7)     .655
        Postoperative factors
          Transfusion after incision during the surgical hospitalization           11 (13.6)          22 (7.1)           2.1 (1.0–4.4)     .066
          Development of subcutaneous hematoma after operation                     16 (19.8)           6 (1.9)          12.5 (4.7–33.1)   Ͻ.001
        note.      CI, confidence interval; GBS, group B Streptococcus; OR, odds ratio.
        a
            Determined by the symptoms of fever during labor and/or fundal tenderness, and/or by physician diagnosis.


as the reference group, there were no significant differences in                with a 2.1-fold increased odds of SSI, compared with receipt of
risk of SSI associated with the various categories of antibiotics              standard surgical prophylaxis at the time the umbilical cord
(all P Ͼ .100). This analysis was limited by the small number of               was clamped (Table 3). The patients who received antibiotics
patients in the reference group; there were only 19 patients                   more than 1 hour before incision were much more likely to
who underwent elective surgery without antibiotic prophy-                      have a diagnosis of chorioamnionitis than patients who re-
laxis.                                                                         ceived antibiotics within 1 hour before or after incision (61
   Suboptimal timing of antibiotic prophylaxis was also asso-                  [48%] of 128 vs 45 [21%%] of 218 patients; P Ͻ .001).
ciated with a higher risk of SSI in univariate analysis. Receipt of               Independent risk factors for SSI identified in the multivari-
antibiotics more than 1 hour before incision was associated                    ate logistic regression analysis included higher BMI, admission




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risk factors for ssi after cesarean section            481


          table 3. Univariate Comparisons of Antibiotic Therapy Given to Patients With and Patients Without Surgical Site
          Infection (SSI) After Low Transverse Cesarean Section at Barnes-Jewish Hospital, July 1999 to June 2001
                                                                                 No. (%) of patients
          Antibiotic therapy                                      Case group (n ϭ 81)      Control group (n ϭ 310)        OR (95% CI)         P
          Category or indication
            No intravenous antibioticsa                                15 (18.5)                    30 (9.7)                    1.00          ...
            Cephalosporin surgical prophylaxisb                        24 (29.6)                   155 (50.0)              0.3 (0.1–0.7)     .002
            Anti-GBS agentsc                                           16 (19.8)                    36 (11.6)              0.9 (0.4–2.1)     .787
            Surgical prophylaxis plus anti-GBS agentsd                 11 (13.6)                    46 (14.8)              0.5 (0.2–1.2)     .110
            Therapy for chorioamnionitis or fevere                     15 (18.5)                    43 (13.9)              0.7 (0.3–1.6)     .409
          Timing of administration
            Only after incision                                        23 (28.4)                   145 (46.8)                   1.0           ...
            Within 1 hour before incisiona                             11 (13.6)                    39 (12.6)              1.8 (0.8–4.0)     .159
            Between 1 and 8 hours before incision                      32 (39.5)                    96 (31.0)              2.1 (1.2–3.8)     .014
          note.      CI, confidence interval; GBS, group B Streptococcus; OR, odds ratio.
          a
            Three patients received oral antibiotics within 8 hours before incision (2 between 4 and 6 hours before incision and 1 Ͼ7 hours before
          incision). The remaining 42 patients received no antibiotics before incision.
          b
            Cefazolin or cefotetan.
          c
            Ampicillin, penicillin, or clindamycin (1 patient received vancomycin alone within 1 hour before incision).
          d
            Ampicillin, penicillin, or clindamycin, plus cefazolin or cefotetan.
          e
            Ampicillin plus gentamycin or tobramycin, or ampicillin-sulbactam.



to the university teaching service, and development of subcu-                   for other independent risk factors, we found that skin closure
taneous hematoma after operation (Table 4). Receipt of ceph-                    with staples was associated with marginally increased odds of
alosporin prophylaxis before or during operation was associ-                    SSI. GBS colonization and risk factors for GBS colonization did
ated with a 77% lower odds of SSI, compared with no receipt of                  not confound the relationship between type of antibiotic and
antibiotics before or after incision (P Ͻ .001). After adjusting                SSI when these variables were forced into the logistic regression
                                                                                model. In addition, there was no effect modification by receipt
                                                                                of antibiotic more than 1 hour before incision on the type of
table 4. Multivariate Model of Risk Factors for Surgical Site In-
fection (SSI) After Low Transverse Cesarean Section at Barnes-Jewish
                                                                                antibiotic used (P Ͼ .50 for all interaction terms).
Hospital, July 1999 to June 2001
                                                                                discussion
Risk factor                                     aORa (95% CI)          P
                                                                                This is, to our knowledge, the largest study to date examining
Body mass index at admission                      1.1 (1.0–1.1)        .003     independent risk factors for SSI after low transverse cesarean
Service performing operation                                                    section in the United States that has used definitions from the
  Private                                              1.0            ...
                                                                                Centers for Disease Control and Prevention’s National Noso-
  University teaching                             2.7 (1.4–5.2)       .003
Use of staples for skin closure                   3.3 (0.7–14.7)      .118      comial Infections Surveillance System and 30-day hospital-
Development of subcutaneous hematoma                                            based surveillance to identify patients with SSI. Independent
    after operation                             11.6 (4.1–33.2) Ͻ.001           risk factors for SSI after low transverse cesarean section in-
Antibiotic therapy                                                              cluded a higher BMI at admission, admission to the university
  None                                                 1.00           ...       teaching service, absence of cephalosporin prophylaxis before
  Cephalosporin surgical prophylaxisb             0.2 (0.1–0.5)      Ͻ.001      or during operation, and development of subcutaneous hema-
  Anti-GBS agentsc                                0.5 (0.2–1.4)       .215      toma after operation. The rate of SSI after low transverse ce-
  Surgical prophylaxis plus anti-GBS
                                                                                sarean during this 2-year study section was 5.0%, which is con-
    agentsd                                       0.3 (0.1–0.8)        .018
                                                                                sistent with estimates from other studies.
  Therapy for chorioamnionitis or fevere          0.4 (0.2–1.2)        .095
                                                                                   Previous studies that had sufficient sample sizes and that
note.     Two patients were excluded from the multivariate regression model
                                                                                used multivariate analysis to identify independent risk factors
because their height measurements, which are necessary for calculation of
BMI, were missing (model C-statistic, 0.781). aOR, adjusted odds ratio; CI,     for SSI after cesarean section identified the following factors
confidence interval; GBS, group B Streptococcus.                                 associated with increased risk of SSI: younger age; obesity;
a
  Model adjusted for type of insurance (private vs. Medicaid and/or Medi-       presence of hypertension or preeclampsia; diabetes mellitus;
care).                                                                          chorioamnionitis; preoperative infection at a remote body site;
b
  Cefazolin or cefotetan.
c
  Ampicillin, penicillin, or clindamycin.
                                                                                high preoperative severity of illness; nulliparity; fewer than 7
d
  Ampicillin, penicillin, or clindamycin, plus cefazolin or cefotetan.          prenatal visits; longer interval since rupture of membranes;
e
  Ampicillin plus gentamycin or tobramycin, or ampicillin-sulbactam.            premature rupture of membranes; emergency delivery; ab-




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482   infection control and hospital epidemiology            june 2008, vol. 29, no. 6


sence of antibiotic prophylaxis; longer duration of operation;          of cephalosporins before or after incision independently de-
use of staples for skin closure; and twin delivery.3,7,8,19 The wide    creased the odds of SSI by 77%, compared with no administra-
variety of reported independent risk factors for SSI may be due         tion of antibiotics before or after incision. Interestingly, the
to the variability in potential risk factors selected for analysis.     adjusted OR for SSI was very similar for the group who re-
Killian et al.3 included only a very small number of potential          ceived anti-GBS prophylaxis and a cephalosporin before or af-
risk factors, whereas other studies included a more compre-             ter incision and for the group who received a cephalosporin
hensive collection.7,8 Also, of the 4 studies that used multivar-       only (0.3 vs 0.2). In contrast, patients given anti-GBS prophy-
iate analysis with sufficient sample size, 1 study conducted SSI         laxis alone during labor had a higher adjusted OR for SSI (0.5).
surveillance only during the original surgical admission.7              This suggests the possible benefit of either the addition of ceph-
   Our study of a university-affiliated tertiary care hospital ob-       alosporin therapy or antibiotic administration within 1 hour
stetrics population undergoing low transverse cesarean section          before or after incision, although we were unable to detect a
included women from a wide spectrum of society with regard              significant interaction between timing of administration and
to socioeconomic and health status. More than half the deliv-           type of antibiotic given as prophylaxis.
eries were performed by the university teaching service, in-               Our adjusted estimate of the protective effect of cephalospo-
cluding patients with low socioeconomic status and/or with              rin surgical prophylaxis closely reflects the 59% reduction in
severe maternal or fetal health conditions. Compared with pa-           the incidence of wound infection reported in a Cochrane meta-
tients with private insurance, patients without private insur-          analysis comparing prophylaxis with an antibiotic and with
ance had a relatively higher number of high-risk characteris-           placebo during cesarean section.30 The reference group for our
tics, increasing their underlying risk of SSI; therefore, we            analysis included all patients who did not receive antibiotics.
included an indicator of socioeconomic status in the analysis.          During the study period, the American College of Obstetri-
Our finding of increased risk of SSI among patients admitted to          cians and Gynecologists recommended antibiotic prophylaxis
the university teaching service is consistent with previous re-         only for high-risk cesarean sections but did not recommend
ports of increased risk of SSI associated with operation by             routine administration of antibiotic prophylaxis for low-risk
trainee or inexperienced surgeons.20,21 In our institution, house       surgeries.31
staff members in the university teaching service are actively              The relationship between use of staples for skin closure and
involved in surgery, with faculty supervision, and this likely          SSI after cesarean section remains unresolved. Of 5 very small
contributes to the increased risk of postoperative infection.           randomized controlled trials in cardiovascular surgery that
   Obesity is a well-known risk factor for SSI.3,7,8,22 Possible bi-    compared use of staples with use of sutures for skin closure, 3
ological explanations for this association include the relative         reported higher infection rates with use of staples, and 2 re-
avascularity of adipose tissue,8,23 the increase in wound area,24       ported no difference.32 Our estimate is similar to the findings of
and the poor penetration of prophylactic antibiotics in adipose         Johnson et al.,19 who report that skin closure with staples dou-
tissue.25 Our study calculated the BMI of patients from their           bled the risk of SSI after cesarean section. In our study, patients
weight and height at admission, because the prepregnancy                with staples had a significantly higher BMI than patients with
BMI was not available for all patients. In addition, given the          sutures. Interestingly, Trick et al.27 reported that use of staples
range of weight change during pregnancy in our study (ranging           for skin closure was significantly associated with deep inci-
from 11.8 kg in weight loss to 54.4 kg weight gain), we hypoth-         sional sternal SSI after coronary artery bypass surgery in
esized that the BMI at admission was a better indicator of body         normal-weight or overweight patients, but not in obese pa-
mass during the at-risk time for development of SSI than was            tients (BMI, Ͼ30). We were unable to assess the effect modifi-
the prepregnancy BMI.                                                   cation of BMI on the relationship between use of staples and
   We did not detect an association between diabetes and SSI in         risk of SSI because 97.5% of the patients with SSI had staples
this study. It is possible that the perioperative serum glucose         used for skin closure.
level, which has been associated with increased risk of SSI after          A unique strength of this study is the examination of post-
cardiac surgery,26-29 may be a more sensitive predictor of SSI          operative risk factors for SSI, particularly the development of
than is diabetes. Although we attempted to assess this relation-        subcutaneous hematoma. Previous cesarean section studies
ship, only 17% of patients had documented perioperative                 have generally omitted postoperative maternal factors from
blood glucose levels measured during the surgical hospitaliza-          their analyses. To our knowledge, this is the first multivariate
tion. Evaluating the association between hyperglycemia and              study to establish the development of subcutaneous hematoma
SSI will require a much larger study with systematic collection         as an independent risk factor for SSI after cesarean section,
of perioperative blood glucose levels.                                  despite awareness that hematomas may provide a medium for
   Estimating the protective effect of antibiotics is problematic       bacterial growth.25,33-35 Notably, development of a subcutane-
because they are used both therapeutically and prophylacti-             ous hematoma was the strongest independent risk factor for
cally in this patient population. In the case of cephalosporin          SSI in our model.
therapy, patients treated with a cephalosporin had an a priori             The limitations of this study include the potential for mis-
lower risk of SSI than patients who received other antibiotics          classification of the outcome. Our SSI rate is most likely an
during labor for suspected chorioamnionitis. Administration             underestimate, because the surveillance strategy we used only




                                 This content downloaded from 150.214.230.47 on Sun, 31 Mar 2013 09:45:24 AM
                                                 All use subject to JSTOR Terms and Conditions
risk factors for ssi after cesarean section                    483


captured data on infections managed in the hospital or diag-                     Presented in part: 15th Annual Scientific Meeting of the Society for Health-
nosed during an emergency department visit. The infections                     care Epidemiology of America; Los Angeles, CA; April 9 –12, 2005 (Abstract
                                                                               266).
that were missed by our surveillance strategy were most likely
superficial incisional SSI treated with oral antibiotics. In addi-              references
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Arc 5

  • 1. Risk Factors for Surgical Site Infection After Low Transverse Cesarean Section Author(s): By Margaret A. Olsen,, PhD, MPH; Anne M. Butler,, MS; Denise M. Willers,, MD; Preetishma Devkota,, MBBS; Gilad A. Gross,, MD; Victoria J. Fraser,, MD Source: Infection Control and Hospital Epidemiology, Vol. 29, No. 6 (June 2008), pp. 477-484 Published by: The University of Chicago Press on behalf of The Society for Healthcare Epidemiology of America Stable URL: http://www.jstor.org/stable/10.1086/587810 . Accessed: 31/03/2013 09:45 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. . The University of Chicago Press and The Society for Healthcare Epidemiology of America are collaborating with JSTOR to digitize, preserve and extend access to Infection Control and Hospital Epidemiology. http://www.jstor.org This content downloaded from 150.214.230.47 on Sun, 31 Mar 2013 09:45:24 AM All use subject to JSTOR Terms and Conditions
  • 2. infection control and hospital epidemiology june 2008, vol. 29, no. 6 original article Risk Factors for Surgical Site Infection After Low Transverse Cesarean Section Margaret A. Olsen, PhD, MPH; Anne M. Butler, MS; Denise M. Willers, MD; Preetishma Devkota, MBBS; Gilad A. Gross, MD; Victoria J. Fraser, MD (See the commentary by Lee on pages 485– 486) background. Independent risk factors for surgical site infection (SSI) after cesarean section have not been well documented, despite the large number of cesarean sections performed and the relatively common occurrence of SSI. objective. To determine independent risk factors for SSI after low transverse cesarean section. design. Retrospective case-control study. setting. Barnes-Jewish Hospital, a 1,250-bed tertiary care hospital. patients. A total of 1,605 women who underwent low transverse cesarean section during the period from July 1999 to June 2001. methods. Using the International Classification of Diseases, Ninth Revision, Clinical Modification diagnosis codes for SSI or wound compli- cation and/or data on antibiotic use during the surgical hospitalization or at readmission to the hospital or emergency department, we identified potential cases of SSI in a cohort of patients who underwent a low transverse cesarean section. Cases of SSI were verified by chart review using the definitions from the Centers for Disease Control and Prevention’s National Nosocomial Infections Surveillance System. Control patients without SSI or endomyometritis were randomly selected from the population of patients who underwent cesarean section. Independent risk factors for SSI were determined by logistic regression. results. SSIs were identified in 81 (5.0%) of 1,605 women who underwent low transverse cesarean section. Independent risk factors for SSI included development of subcutaneous hematoma after the procedure (adjusted odds ratio [aOR], 11.6 [95% confidence interval {CI}, 4.1– 33.2]), operation performed by the university teaching service (aOR, 2.7 [95% CI, 1.4 –5.2]), and a higher body mass index at admission (aOR, 1.1 [95% CI, 1.0 –1.1]). Cephalosporin therapy before or after the operation was associated with a significantly lower risk of SSI (aOR, 0.2 [95% CI, 0.1– 0.5]). Use of staples for skin closure was associated with a marginally increased risk of SSI. conclusions. These independent risk factors should be incorporated into approaches for the prevention and surveillance of SSI after surgery. Infect Control Hosp Epidemiol 2008; 29:477– 484 Surgical site infection (SSI) after a cesarean section increases atively high. We performed a large case-control study to deter- maternal morbidity and medical costs.1 The rates of SSI after mine clinically relevant independent risk factors for SSI after cesarean section reported in the literature range from 3% to low transverse cesarean section. A low transverse uterine inci- 15%, depending on the surveillance methods used to identify sion is the preferred type of incision for cesarean section, be- infections, the patient population, and the use of antibiotic cause it is associated with less blood loss and lower risk of sub- prophylaxis.2-11 The pooled mean rate of SSI after cesarean sec- sequent uterine rupture than a vertical incision. It is used for tion for US hospitals participating in the Centers for Disease the vast majority of cesarean section deliveries in the United Control and Prevention’s National Nosocomial Infections States, whereas a vertical incision (alone or in combination Surveillance System is 3.15%.12 with a low transverse incision) is typically used for a minority Expanding our knowledge of the risk factors associated with of cesarean section deliveries, for selected obstetric reasons or SSI is essential to developing targeted prevention strategies to when there is need for rapid delivery.14 reduce the risk of SSI. Independent risk factors for SSI after cesarean section have not been well documented, despite the methods fact that it is the most commonly performed surgical proce- This study was conducted at Barnes-Jewish Hospital, a 1,250- dure in the United States,13 and the reported rate of SSI is rel- bed tertiary care hospital. It is the academic hospital for the From Division of Infectious Diseases (M.A.O., A.M.B., P.D., V.J.F.) and Department of Obstetrics and Gynecology (D.M.W., G.A.G.), Washington University School of Medicine, St. Louis, Missouri. Received December 7, 2007; accepted February 24, 2008; electronically published May 30, 2008. © 2008 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2008/2906-0001$15.00. DOI: 10.1086/587810 This content downloaded from 150.214.230.47 on Sun, 31 Mar 2013 09:45:24 AM All use subject to JSTOR Terms and Conditions
  • 3. 478 infection control and hospital epidemiology june 2008, vol. 29, no. 6 Washington University School of Medicine and has a referral within 24 hours before incision and within 48 hours after in- base of patients from metropolitan St. Louis and within a 200- cision. Additional postoperative variables included receipt of mile radius of the city. At the hospital, the obstetrics service blood transfusion (after incision during the cesarean section performs approximately 4,000 deliveries per year and provides admission) and development of a subcutaneous hematoma. a full range of care, including high-risk maternal and fetal med- icine. Obstetric care is provided by a full-time faculty in the Definitions department of obstetrics and gynecology at the Washington University School of Medicine and by an adjunct obstetric fac- Cohort patients were identified by an International Classifica- ulty in private practice. tion of Diseases, Ninth Revision, Clinical Modification (ICD-9- We performed a case-control study nested within a cohort CM) procedure code for low transverse cesarean section (74.1) of 1,605 women who underwent low transverse cesarean sec- and were included only if the operative note indicated that a tion during the period from July 1999 to June 2001. Demo- low transverse uterine incision had been used. Screening for graphic, pharmacy, and laboratory data were obtained from wound complications was done during the surgical hospital- the Barnes-Jewish Hospital Medical Informatics database. Risk ization or rehospitalization (inpatient, emergency department, factor data were collected from the medical records of each or outpatient surgery admission) within 60 days after opera- patient’s surgical hospitalization, including all notes by physi- tion with use of ICD-9-CM discharge diagnosis codes for inci- cians and/or nurses concerning the hospitalization. sional infection, dehiscence, wound necrosis, seroma, or he- Patient-related variables included age, race, marital status, matoma (998.5, 998.51, 998.59, 674.32, or 674.34) and/or data type of insurance, body mass index (BMI) at admission, weight on excess use of antibiotics after operation.11,15 We reviewed all gain during pregnancy, presence of diabetes mellitus, gesta- of the hospital medical records of patients who met the screen- tional diabetes, systemic lupus erythematosis, sexually trans- ing criteria, to determine if they met the case definition for SSI mitted diseases during pregnancy (eg, gonorrhea, chlamydia, using the definitions from the Centers for Disease Control and bacterial vaginosis, Trichomonas vaginalis infection, herpes Prevention’s National Nosocomial Infections Surveillance Sys- simplex virus infection, or human immunodeficiency virus in- tem.16 We included case patients with SSI identified during the fection), group B Streptococcus (GBS) colonization, and use of surgical hospitalization or during an inpatient rehospitaliza- alcohol, tobacco, illicit street drugs, and/or corticosteroids. tion, emergency department visit, or outpatient surgery with For the mother, obstetrics-related variables included the signs and/or symptoms of SSI within 30 days after operation. number of prior pregnancies, prior births, abortions, and pre- Questionable cases were verified by an obstetrician and gyne- vious cesarean sections; presence of cervical incompetence; the cologist (D.M.W.). Control patients without SSI or endomyo- number of vaginal exams before cesarean section; presence of metritis were randomly selected from the women who under- vaginal discharge at admission; the number of prenatal care visits; presence of preeclampsia, chorioamnionitis, maternal went low transverse cesarean section during the study period. fever, fundal tenderness before delivery, maternal and fetal tachycardia, and/or vaginal bleeding; malpresentation; spon- Statistical Analysis taneous or assisted rupture of membranes; interval since rup- Comparisons for categorical variables were performed using ture of membranes; duration of labor; use of internal fetal the ␹2 or Fisher exact test. Continuous variables were com- monitors; use of Foley bulb for cervical ripening; receipt of pared using the Student t or Mann-Whitney U tests. Linearity amnioinfusion; and presence of meconium. For the infant, assessments were performed on the variables of age and BMI. obstetrics-related variables included gestational age at delivery, Fractional polynomials were used to determine the best fit for birth weight, and Apgar score. BMI.17 Independent risk factors for SSI were determined by Operation-related variables included the American Society multivariate logistic regression. All variables with P Ͻ .20 in of Anesthesiologists score, urgency of operation, type of skin the univariate analysis or with a priori clinical significance were and uterine incision, exteriorization of the uterus, manual re- evaluated by stepwise logistic regression for inclusion in the moval of placenta, presence of drains, receipt of shave with final model. The variable for lack of private insurance (ie, reli- razor, use of staples for skin closure, receipt of an additional ance on Medicaid or Medicare) was forced into the logistic operative procedure, duration of time between hospital admis- sion and operation, type of service (university teaching or pri- regression model as a proxy for socioeconomic status. Interac- vate), volume of blood loss, and receipt of antibiotic therapy. tions between the type and the timing of antibiotic prophylaxis Cesarean sections were classified as elective, urgent, or were tested in the multivariate models, but they did not meet emergent according to standardized criteria by the operative the criteria for inclusion (P Ͻ .05 for interaction terms). Model team. True emergent procedures were classified as emergent fit was assessed using the C statistic. All tests were 2-tailed, and and did not include full surgical preparation. Hemoglobin and P Ͻ .05 was considered significant. Statistical analyses were hematocrit levels were determined within 24 hours before in- performed with SPSS version 14.0 (SPSS). Approval for this cision and within 48 hours after incision. The highest serum study was obtained from the Washington University Human glucose level, if available, was determined from blood obtained Research Protection Office. This content downloaded from 150.214.230.47 on Sun, 31 Mar 2013 09:45:24 AM All use subject to JSTOR Terms and Conditions
  • 4. risk factors for ssi after cesarean section 479 results table 1. Characteristics of 391 Patients Who Under- went Low Transverse Cesarean Section at Barnes-Jewish During the 2-year study period, 1,759 patients underwent ce- Hospital During the Period From July 1999 to June 2001 sarean section in our academic tertiary care medical center. Of those patients, 1,605 (91%) underwent a low transverse uterine Characteristic Value incision, and 81 (5.0%) of those 1,605 patients met the case Age, years 26.5 (15–43) definition for SSI with onset of infection within 30 days after Body mass index at admission 32.3 (17–65) low transverse cesarean section. Seventy-five (92.6%) of those Race 81 patients had SSIs that were classified as superficial inci- Black 239 (61.1) sional, 4 (4.9%) had deep incisional SSI, and 2 (2.5%) had White 127 (32.5) organ space infection. Forty-eight (59.3%) of the 81 patients Other 25 (6.4) Tobacco use had SSI diagnosed during surgical hospitalization, 27 (33.3%) Never 294 (75.2) during rehospitalization, and 6 (7.4%) during an emergency Prior use, quit during pregnancy 26 (6.6) department visit. A total of 310 control patients without en- Current use 71 (18.2) domyometritis were randomly selected for comparison with Had gonorrhea or Chlamydia infection the 81 case patients with SSI. during pregnancy 34 (8.7) The characteristics of the 81 case and 310 control patients HIV infection 4 (1.0) are described in Table 1. Of these 391 patients, 239 (61.1%) Type of insurance were black, 71 (18.2%) smoked during their pregnancy, 34 Private 155 (39.6) (8.7%) had gonorrhea or chlamydial infection during their Medicaid and/or Medicare 236 (60.4) pregnancy, 129 (33.0%) had 1 or more cesarean sections Service performing operation University teaching 226 (57.8) previously, and 226 (57.8%) were admitted to the university Private 165 (42.2) teaching service. More than half of the patients were cov- No. of prior cesarean sections ered by either Medicaid or Medicare, or had no health in- 0 262 (67.0) surance. 1 87 (22.3) In the univariate analysis, SSI occurred significantly more 2 32 (8.2) often among women with the following risk factors: presence 3 10 (2.6) of chorioamnionitis, induction of labor, use of staples for skin Onset of labor closure, development of subcutaneous hematoma after opera- Spontaneous 121 (30.9) tion, and admission to the university teaching service (Table Induced 85 (21.7) No labor 185 (47.3) 2). There was a significant association between a higher BMI at Type of cesarean section admission and SSI (median BMI, 36.4 for case patients vs 31.8 Elective 114 (29.2) for control patients; P ϭ .003). Patients who had skin closure Urgent 215 (55.0) with staples had a significantly higher median BMI than pa- Emergent 62 (15.9) tients who had skin closure with sutures (33.1 vs 29.6; P ϭ Type of skin incision .004). Patients admitted to the university teaching service were Vertical 10 (2.6) significantly more likely to have skin closure with staples than Transverse 381 (97.4) patients admitted to the private service (216 [95.6%] of 226 vs note. Data are no. (%) of patients or median value (range). 130 [78.8%] of 165 patients of patients; P Ͻ .001). There was a Body mass index is defined as the weight in kilograms divided by marginal association between longer duration of operation the square of the height in meters. and SSI (mean duration, 63.1 minutes for case patients vs 57.9 minutes for control patients; P ϭ .090). Only 83% of patients gentamycin or tobramycin, or ampicillin-sulbactam, 35 (60.0%) had the duration of operation recorded, and, for this reason, it had chorioamnionitis diagnosed. was not included in further analyses. Patients who were not given intravenous antibiotics before Antibiotics were administered intravenously to 178 (45.5%) of or after incision were significantly more likely to have under- 391 patients before incision, including 109 (27.9%) who were gone an elective operation than patients who were given anti- given ampicillin, penicillin, or clindamycin, presumably for anti- biotics (19 [42.2%] of 45 vs 95 [27.6%] of 346 patients; P ϭ GBS prophylaxis, and 58 (14.8%) who received antibiotics for .040). Twenty-two (48.9%) of the 45 patients who were not chorioamnionitis or fever (Table 3). Of the 109 women who re- given antibiotics were attended by a private physician (P ϭ ceived ampicillin, penicillin, or clindamycin, 36 (33.0%) had GBS .334). For 20 patients who did not receive antibiotic prophy- colonization, and 55 (50.5%) had risk factors for GBS coloniza- laxis, the operation was classified as urgent; for 6 patients who tion (ie, urinary tract infection during pregnancy, fever, rupture of did not receive antibiotic prophylaxis, the operation was clas- membranes 18 hours or more before incision, and/or preterm sified as emergent. When the analysis of the categories of anti- labor [before week 37 of gestation]18) without documented posi- biotics and the SSI risk was repeated using only the patients tive culture results. Of the 58 women who received ampicillin plus who underwent elective surgery without antibiotic prophylaxis This content downloaded from 150.214.230.47 on Sun, 31 Mar 2013 09:45:24 AM All use subject to JSTOR Terms and Conditions
  • 5. 480 infection control and hospital epidemiology june 2008, vol. 29, no. 6 table 2. Univariate Comparisons of Risk Factors for Surgical Site Infection (SSI) in Patients With and Patients Without SSI After Low Transverse Cesarean Section at Barnes-Jewish Hospital, July 1999 to June 2001 No. (%) of patients Case group Control group Risk factor (n ϭ 81) (n ϭ 310) OR (95% CI) P Demographic factors Age Ͻ18 years 6 (7.4) 17 (5.5) 1.4 (0.5–3.6) .514 Race White 27 (33.3) 100 (32.3) 1.0 ... Black 49 (60.5) 190 (61.3) 1.0 (0.6–1.6) .865 Other 5 (6.2) 20 (6.5) 0.9 (0.3–2.7) .888 Had diabetes mellitus or gestational diabetes 8 (9.9) 30 (9.7) 1.0 (0.4–2.3) .957 Had gonorrhea or Chlamydia infection during pregnancy 10 (12.3) 24 (7.7) 1.7 (0.8–3.7) .194 Had Trichomonas infection during pregnancy 11 (13.6) 27 (8.6) 1.6 (0.8–3.5) .191 Had documented GBS colonization 15 (18.5) 46 (14.8) 1.3 (0.7–2.5) .417 Tobacco use (past or present) 25 (30.9) 72 (23.2) 1.5 (0.9–2.5) .158 Type of insurance Private 30 (37.0) 125 (40.3) 1.0 ... Medicaid and/or Medicare 51 (63.0) 185 (59.7) 1.1 (0.7–1.9) .590 Type of service Private 18 (22.2) 147 (47.4) 1.0 ... University teaching 63 (77.8) 163 (52.6) 3.2 (1.8–5.6) Ͻ.001 Obstetric factors Use of internal monitors 40 (49.4) 118 (38.1) 1.6 (1.0–2.6) .066 Had chorioamnionitisa 21 (25.9) 41 (13.2) 2.3 (1.3–4.2) .006 No. of vaginal examinations 0 12 (14.8) 63 (20.3) 1.0 ... 1–6 49 (60.5) 192 (61.9) 1.3 (0.7–2.7) .408 ୑7 20 (24.7) 55 (17.7) 1.9 (0.9–4.3) .114 Induction of labor 45 (55.6) 123 (39.7) 1.9 (1.2–3.1) .011 Duration of labor No labor 35 (43.2) 150 (48.4) 1.0 ... Ͻ6 hours 11 (13.6) 59 (19.0) 0.8 (0.4–1.7) .553 6–12 hours 11 (13.6) 47 (15.2) 1.0 (0.5–2.1) .994 Ͼ12 hours 24 (29.6) 54 (17.4) 1.9 (1.0–3.5) .037 Surgical factors Use of drains 10 (12.3) 20 (6.5) 2.0 (0.9–4.6) .081 Use of staples for skin closure 79 (97.5) 267 (86.1) 6.4 (1.5–26.8) .012 Type of cesarean section Elective 19 (23.5) 95 (30.6) 1.0 ... Urgent 50 (61.7) 165 (53.2) 1.5 (0.8–2.7) .164 Emergent 12 (14.8) 50 (16.1) 1.2 (0.5–2.7) .655 Postoperative factors Transfusion after incision during the surgical hospitalization 11 (13.6) 22 (7.1) 2.1 (1.0–4.4) .066 Development of subcutaneous hematoma after operation 16 (19.8) 6 (1.9) 12.5 (4.7–33.1) Ͻ.001 note. CI, confidence interval; GBS, group B Streptococcus; OR, odds ratio. a Determined by the symptoms of fever during labor and/or fundal tenderness, and/or by physician diagnosis. as the reference group, there were no significant differences in with a 2.1-fold increased odds of SSI, compared with receipt of risk of SSI associated with the various categories of antibiotics standard surgical prophylaxis at the time the umbilical cord (all P Ͼ .100). This analysis was limited by the small number of was clamped (Table 3). The patients who received antibiotics patients in the reference group; there were only 19 patients more than 1 hour before incision were much more likely to who underwent elective surgery without antibiotic prophy- have a diagnosis of chorioamnionitis than patients who re- laxis. ceived antibiotics within 1 hour before or after incision (61 Suboptimal timing of antibiotic prophylaxis was also asso- [48%] of 128 vs 45 [21%%] of 218 patients; P Ͻ .001). ciated with a higher risk of SSI in univariate analysis. Receipt of Independent risk factors for SSI identified in the multivari- antibiotics more than 1 hour before incision was associated ate logistic regression analysis included higher BMI, admission This content downloaded from 150.214.230.47 on Sun, 31 Mar 2013 09:45:24 AM All use subject to JSTOR Terms and Conditions
  • 6. risk factors for ssi after cesarean section 481 table 3. Univariate Comparisons of Antibiotic Therapy Given to Patients With and Patients Without Surgical Site Infection (SSI) After Low Transverse Cesarean Section at Barnes-Jewish Hospital, July 1999 to June 2001 No. (%) of patients Antibiotic therapy Case group (n ϭ 81) Control group (n ϭ 310) OR (95% CI) P Category or indication No intravenous antibioticsa 15 (18.5) 30 (9.7) 1.00 ... Cephalosporin surgical prophylaxisb 24 (29.6) 155 (50.0) 0.3 (0.1–0.7) .002 Anti-GBS agentsc 16 (19.8) 36 (11.6) 0.9 (0.4–2.1) .787 Surgical prophylaxis plus anti-GBS agentsd 11 (13.6) 46 (14.8) 0.5 (0.2–1.2) .110 Therapy for chorioamnionitis or fevere 15 (18.5) 43 (13.9) 0.7 (0.3–1.6) .409 Timing of administration Only after incision 23 (28.4) 145 (46.8) 1.0 ... Within 1 hour before incisiona 11 (13.6) 39 (12.6) 1.8 (0.8–4.0) .159 Between 1 and 8 hours before incision 32 (39.5) 96 (31.0) 2.1 (1.2–3.8) .014 note. CI, confidence interval; GBS, group B Streptococcus; OR, odds ratio. a Three patients received oral antibiotics within 8 hours before incision (2 between 4 and 6 hours before incision and 1 Ͼ7 hours before incision). The remaining 42 patients received no antibiotics before incision. b Cefazolin or cefotetan. c Ampicillin, penicillin, or clindamycin (1 patient received vancomycin alone within 1 hour before incision). d Ampicillin, penicillin, or clindamycin, plus cefazolin or cefotetan. e Ampicillin plus gentamycin or tobramycin, or ampicillin-sulbactam. to the university teaching service, and development of subcu- for other independent risk factors, we found that skin closure taneous hematoma after operation (Table 4). Receipt of ceph- with staples was associated with marginally increased odds of alosporin prophylaxis before or during operation was associ- SSI. GBS colonization and risk factors for GBS colonization did ated with a 77% lower odds of SSI, compared with no receipt of not confound the relationship between type of antibiotic and antibiotics before or after incision (P Ͻ .001). After adjusting SSI when these variables were forced into the logistic regression model. In addition, there was no effect modification by receipt of antibiotic more than 1 hour before incision on the type of table 4. Multivariate Model of Risk Factors for Surgical Site In- fection (SSI) After Low Transverse Cesarean Section at Barnes-Jewish antibiotic used (P Ͼ .50 for all interaction terms). Hospital, July 1999 to June 2001 discussion Risk factor aORa (95% CI) P This is, to our knowledge, the largest study to date examining Body mass index at admission 1.1 (1.0–1.1) .003 independent risk factors for SSI after low transverse cesarean Service performing operation section in the United States that has used definitions from the Private 1.0 ... Centers for Disease Control and Prevention’s National Noso- University teaching 2.7 (1.4–5.2) .003 Use of staples for skin closure 3.3 (0.7–14.7) .118 comial Infections Surveillance System and 30-day hospital- Development of subcutaneous hematoma based surveillance to identify patients with SSI. Independent after operation 11.6 (4.1–33.2) Ͻ.001 risk factors for SSI after low transverse cesarean section in- Antibiotic therapy cluded a higher BMI at admission, admission to the university None 1.00 ... teaching service, absence of cephalosporin prophylaxis before Cephalosporin surgical prophylaxisb 0.2 (0.1–0.5) Ͻ.001 or during operation, and development of subcutaneous hema- Anti-GBS agentsc 0.5 (0.2–1.4) .215 toma after operation. The rate of SSI after low transverse ce- Surgical prophylaxis plus anti-GBS sarean during this 2-year study section was 5.0%, which is con- agentsd 0.3 (0.1–0.8) .018 sistent with estimates from other studies. Therapy for chorioamnionitis or fevere 0.4 (0.2–1.2) .095 Previous studies that had sufficient sample sizes and that note. Two patients were excluded from the multivariate regression model used multivariate analysis to identify independent risk factors because their height measurements, which are necessary for calculation of BMI, were missing (model C-statistic, 0.781). aOR, adjusted odds ratio; CI, for SSI after cesarean section identified the following factors confidence interval; GBS, group B Streptococcus. associated with increased risk of SSI: younger age; obesity; a Model adjusted for type of insurance (private vs. Medicaid and/or Medi- presence of hypertension or preeclampsia; diabetes mellitus; care). chorioamnionitis; preoperative infection at a remote body site; b Cefazolin or cefotetan. c Ampicillin, penicillin, or clindamycin. high preoperative severity of illness; nulliparity; fewer than 7 d Ampicillin, penicillin, or clindamycin, plus cefazolin or cefotetan. prenatal visits; longer interval since rupture of membranes; e Ampicillin plus gentamycin or tobramycin, or ampicillin-sulbactam. premature rupture of membranes; emergency delivery; ab- This content downloaded from 150.214.230.47 on Sun, 31 Mar 2013 09:45:24 AM All use subject to JSTOR Terms and Conditions
  • 7. 482 infection control and hospital epidemiology june 2008, vol. 29, no. 6 sence of antibiotic prophylaxis; longer duration of operation; of cephalosporins before or after incision independently de- use of staples for skin closure; and twin delivery.3,7,8,19 The wide creased the odds of SSI by 77%, compared with no administra- variety of reported independent risk factors for SSI may be due tion of antibiotics before or after incision. Interestingly, the to the variability in potential risk factors selected for analysis. adjusted OR for SSI was very similar for the group who re- Killian et al.3 included only a very small number of potential ceived anti-GBS prophylaxis and a cephalosporin before or af- risk factors, whereas other studies included a more compre- ter incision and for the group who received a cephalosporin hensive collection.7,8 Also, of the 4 studies that used multivar- only (0.3 vs 0.2). In contrast, patients given anti-GBS prophy- iate analysis with sufficient sample size, 1 study conducted SSI laxis alone during labor had a higher adjusted OR for SSI (0.5). surveillance only during the original surgical admission.7 This suggests the possible benefit of either the addition of ceph- Our study of a university-affiliated tertiary care hospital ob- alosporin therapy or antibiotic administration within 1 hour stetrics population undergoing low transverse cesarean section before or after incision, although we were unable to detect a included women from a wide spectrum of society with regard significant interaction between timing of administration and to socioeconomic and health status. More than half the deliv- type of antibiotic given as prophylaxis. eries were performed by the university teaching service, in- Our adjusted estimate of the protective effect of cephalospo- cluding patients with low socioeconomic status and/or with rin surgical prophylaxis closely reflects the 59% reduction in severe maternal or fetal health conditions. Compared with pa- the incidence of wound infection reported in a Cochrane meta- tients with private insurance, patients without private insur- analysis comparing prophylaxis with an antibiotic and with ance had a relatively higher number of high-risk characteris- placebo during cesarean section.30 The reference group for our tics, increasing their underlying risk of SSI; therefore, we analysis included all patients who did not receive antibiotics. included an indicator of socioeconomic status in the analysis. During the study period, the American College of Obstetri- Our finding of increased risk of SSI among patients admitted to cians and Gynecologists recommended antibiotic prophylaxis the university teaching service is consistent with previous re- only for high-risk cesarean sections but did not recommend ports of increased risk of SSI associated with operation by routine administration of antibiotic prophylaxis for low-risk trainee or inexperienced surgeons.20,21 In our institution, house surgeries.31 staff members in the university teaching service are actively The relationship between use of staples for skin closure and involved in surgery, with faculty supervision, and this likely SSI after cesarean section remains unresolved. Of 5 very small contributes to the increased risk of postoperative infection. randomized controlled trials in cardiovascular surgery that Obesity is a well-known risk factor for SSI.3,7,8,22 Possible bi- compared use of staples with use of sutures for skin closure, 3 ological explanations for this association include the relative reported higher infection rates with use of staples, and 2 re- avascularity of adipose tissue,8,23 the increase in wound area,24 ported no difference.32 Our estimate is similar to the findings of and the poor penetration of prophylactic antibiotics in adipose Johnson et al.,19 who report that skin closure with staples dou- tissue.25 Our study calculated the BMI of patients from their bled the risk of SSI after cesarean section. In our study, patients weight and height at admission, because the prepregnancy with staples had a significantly higher BMI than patients with BMI was not available for all patients. In addition, given the sutures. Interestingly, Trick et al.27 reported that use of staples range of weight change during pregnancy in our study (ranging for skin closure was significantly associated with deep inci- from 11.8 kg in weight loss to 54.4 kg weight gain), we hypoth- sional sternal SSI after coronary artery bypass surgery in esized that the BMI at admission was a better indicator of body normal-weight or overweight patients, but not in obese pa- mass during the at-risk time for development of SSI than was tients (BMI, Ͼ30). We were unable to assess the effect modifi- the prepregnancy BMI. cation of BMI on the relationship between use of staples and We did not detect an association between diabetes and SSI in risk of SSI because 97.5% of the patients with SSI had staples this study. It is possible that the perioperative serum glucose used for skin closure. level, which has been associated with increased risk of SSI after A unique strength of this study is the examination of post- cardiac surgery,26-29 may be a more sensitive predictor of SSI operative risk factors for SSI, particularly the development of than is diabetes. Although we attempted to assess this relation- subcutaneous hematoma. Previous cesarean section studies ship, only 17% of patients had documented perioperative have generally omitted postoperative maternal factors from blood glucose levels measured during the surgical hospitaliza- their analyses. To our knowledge, this is the first multivariate tion. Evaluating the association between hyperglycemia and study to establish the development of subcutaneous hematoma SSI will require a much larger study with systematic collection as an independent risk factor for SSI after cesarean section, of perioperative blood glucose levels. despite awareness that hematomas may provide a medium for Estimating the protective effect of antibiotics is problematic bacterial growth.25,33-35 Notably, development of a subcutane- because they are used both therapeutically and prophylacti- ous hematoma was the strongest independent risk factor for cally in this patient population. In the case of cephalosporin SSI in our model. therapy, patients treated with a cephalosporin had an a priori The limitations of this study include the potential for mis- lower risk of SSI than patients who received other antibiotics classification of the outcome. Our SSI rate is most likely an during labor for suspected chorioamnionitis. Administration underestimate, because the surveillance strategy we used only This content downloaded from 150.214.230.47 on Sun, 31 Mar 2013 09:45:24 AM All use subject to JSTOR Terms and Conditions
  • 8. risk factors for ssi after cesarean section 483 captured data on infections managed in the hospital or diag- Presented in part: 15th Annual Scientific Meeting of the Society for Health- nosed during an emergency department visit. The infections care Epidemiology of America; Los Angeles, CA; April 9 –12, 2005 (Abstract 266). that were missed by our surveillance strategy were most likely superficial incisional SSI treated with oral antibiotics. In addi- references tion, there is also the potential for information bias in our 1. Cooper NJ, Sutton AJ, Abrams KR. Decision analytical economic model- study, because information for some confounders may also ling within a Bayesian framework: application to prophylactic antibiotics have been incompletely captured (eg, for subcutaneous hema- use for caesarean section. Stat Methods Med Res 2002;11:491–512. toma, since small hematomas that developed after hospital dis- 2. Chaim W, Bashiri A, Bar-David J, Shoham-Vardi I, Mazor M. 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The use of fractional polynomials to for their assistance with data collection and management. We also thank the model continuous risk variables in epidemiology. Int J Epidemiol 1999;28: reviewers for their insightful comments. 964 –974. Financial support. Centers for Disease Control and Prevention (grant 18. Prevention of perinatal group B streptococcal disease: a public health per- UR8/CCU715087) and the National Institutes of Health (grant K01AI065808 spective. Centers for Disease Control and Prevention (published correc- to M.A.O. and grant K24AI06779401 to V.J.F.). tion appears in MMWR Morb Mortal Wkly Rep 1996;45:679). MMWR Potential conflicts of interest. The authors report no conflict of interest Recomm Rep 1996;45(RR-7):1–24. relevant to this article. 19. Johnson A, Young D, Reilly J. Caesarean section surgical site infection surveillance. J Hosp Infect 2006;64:30 –35. 20. Miller PJ, Searcy MA, Kaiser DL, Wenzel RP. 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