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Postdischarge surveillance following
  cesarean section: The incidence of
  surgical site infection and associated
  factors
  Meire Celeste Cardoso Del Monte, RN,a and Aarao Mendes Pinto Neto, MD, PhDb
                                               ˜
       ˜
      Sao Paulo, Brazil


      Background: The rate of surgical site infections (SSI) and their associated risk factors was identified by performing postdischarge
      surveillance following cesarean section at a public university teaching hospital in Brazil.
      Methods: The study was conducted at the Center for Women’s Integrated Health Care in Brazil between May 2008 and March 2009.
      Women were contacted by telephone 15 and 30 days after cesarean section. During hospitalization, a form was completed on
      factors associated with post-cesarean SSI. The x2 test and Fisher exact test were used to analyze categorical variables and the
      Mann-Whitney test for numerical variables. Relative risks (RR) and their respective 95% confidence intervals (95% CI) were
      calculated for factors associated with SSI. P values , .05 were considered significant.
      Results: The final sample consisted of 187 women. SSI was detected in 44 cases (23.5%). In 42 of 44 women (95%), SSI appeared
      following discharge from hospital, becoming evident within the first 15 days following surgery. Number of prenatal consultations
      #7 (RR, 2.09; 95% CI: 1.26-3.48) and hypertension (RR, 2.07; 95% CI: 1.25-3.43) were significantly associated with SSI in the bivariate
      analysis. In the multivariate analysis, only hypertension (RR, 2.47; 95% CI: 1.21-5.04) remained significant.
      Conclusion: Postdischarge surveillance is essential for ensuring accurate estimates of post-cesarean section SSI. A 15-day
      postdischarge follow-up was shown to be sufficient. Hypertension was a factor associated with SSI.
      Key Words: Postdischarge surveillance; cesarean section; surgical site infection; hospital infection; infection control nurse.
      Copyright ª 2010 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights
      reserved. (Am J Infect Control 2010;38:467-72.)


   Surgical site infections (SSI) are common postoperative                   their statistics to those patients in whom infection
complications, constituting a major clinical problem in                      becomes apparent prior to discharge or those who re-
terms of morbidity and mortality,1 duration of hospitali-                    turn spontaneously to the hospital for treatment. Vari-
zation, and hospital costs.2,3                                               ous studies have been published showing a consensus
   Most SSIs only become apparent after the patient is                       on the need to perform postdischarge surveillance of
discharged from hospital.4-13 Different studies that                         patients submitted to C-sections to obtain more
included postdischarge surveillance have reported                            accurate statistics on the frequency of SSI.7-13
infection rates varying from 27.6%4 to 84%,5 particu-                           In Brazil, Couto et al (1998)12 reported post-C-section
larly following surgeries such as cesarean sections                          SSI rates of 1.6% when surveillance was limited to
(C-sections) for which the hospitalization period is brief.6                 hospitalized patients and 9.6% when postdischarge sur-
   Few Brazilian hospitals conduct surveillance after                        veillance was implemented. Another study carried out
the patient has been discharged from hospital, limiting                                                                 ˜
                                                                             in a maternity hospital in the state of Sao Paulo found
                                                                             a post-C-section SSI rate of 1.2% when surveillance
 From the Department of Infection Controla and Department of                 was limited to hospitalized patients versus 14.4%
 Obstetrics and Gynecology,b Women’s Hospital, School of Medical             when these rates were obtained from postdischarge sur-
                                                        ˜
 Sciences, University of Campinas (UNICAMP), Campinas, Sao Paulo,            veillance.13 The study was conducted at the Center for
 Brazil.                                                                     Women’s Integrated Health Care, a tertiary, 142-bed,
 Address correspondence to Meire Celeste Cardoso Del Monte, RN,              university teaching and public hospital situated in the
                                    ´                      ˜
 Rua Dr. Liraucio Gomes, 257 Cambuı, 13.024-490 Campinas, Sao Paulo,
 Brazil. E-mail: meiredelmonte@yahoo.com.
                                                                                        ˜
                                                                             state of Sao Paulo, Brazil. A mean of 100 C-sections are
                                                                             performed in this hospital monthly. This study was car-
 Conflicts of interest: None to report.
                                                                             ried out between May 2008 and March 2009. There has
 0196-6553/$36.00
                                                                             been a hospital infection control committee (HICC) in
 Copyright ª 2010 by the Association for Professionals in Infection          this institute since 1986, and this committee currently
 Control and Epidemiology, Inc. Published by Elsevier Inc. All rights
 reserved.
                                                                             recommends prophylactic antibiotic therapy following
                                                                             all C-section deliveries. This protocol determines the
 doi:10.1016/j.ajic.2009.10.008
                                                                             use of cefazolin, 2 g intravenously, after the umbilical

                                                                                                                                                467
468   Cardoso Del Monte and Pinto Neto                                                  American Journal of Infection Control
                                                                                                                August 2010


cord has been clamped or 900 mg of clindamycin for            Review Board of the institute prior to initiation of the
patients who are allergic to penicillin.                      study. If the woman agreed to participate, she then
   A recent systematic review of the methods used to          signed the informed consent form, was given a copy,
identify SSI following discharge from hospital                and was admitted to the study.
concluded that existing studies on the subject have so           Diagnosis of SSI was defined according to the criteria
far failed to identify a valid, reliable method for identi-   standardized by the Centers for Disease Control and Pre-
fying such infections postdischarge. On a local level,        vention, Atlanta, GA, determining superficial incisional
the method used to identify postdischarge SSI is likely       SSI, deep incisional SSI, or organ/space SSI.15 The inves-
to be dependent on existing resources, on the objective       tigator made a questionnaire, based in this criteria, from
of surveillance, and on the nature of the data routinely      which questions about purulent discharge, identification
available.14 In this study, the researcher contacted the      of an isolated organism, signs and symptoms of infection
patients by telephone following discharge and estab-          (fever, pain or tenderness, localized swelling, redness,
lished the occurrence of a SSI by having the patients         heat), an abscess or other evidence of infection involving
confirm the presence or absence of symptoms associ-            the deep incision, or diagnosis of SSI by attending physi-
ated with a SSI. Therefore, the methodology used to           cian were applied by telephone interview.
determine postdischarge SSI should be considered as              The following data were obtained from the patient’s
a potential limitation of the study.                          chart: age, gestational age, whether the patient had
   The objectives of the present study were to evaluate       undergone prenatal care and the number of prenatal
the incidence of SSI following discharge of the patient       consultations she had attended, weight and height,
from hospital through the use of telephone interviews         parity, presence of community infection, ruptured
and to identify factors associated with the presence of       membranes at admission and the time of membrane
these infections in a tertiary Brazilian university           rupture, presence of diabetes or arterial hypertension,
teaching hospital that is a regional referral hospital for    duration of labor, indication for C-section, surgical
maternal and child health care.                               wound classification (clean, clean contaminated, con-
                                                              taminated and dirty/infected), use of general anesthe-
METHODS                                                       sia or other type of anesthesia, the American Society
                                                              of Anesthesiologists (ASA) physical status classification
   This is an observational, longitudinal, cohort study       score, whether the C-section represented an emer-
carried out using data collected from patient charts          gency or elective surgery, duration of the surgery,
and from interviews with patients with the objective          volume of intrasurgical blood loss as calculated by
of identifying post-C-section SSI. Sample size calcula-       the anesthesiologist, whether any other procedures
tion was based on the SSI rate of 0.7% registered by          were carried out, and whether there was compliance
the HICC in 2006, established according to the epide-         with the institutional protocol of prophylactic antibi-
miologic surveillance of patients up to the time of their     otic therapy. The intraoperative nursing chart was
discharge from hospital, and the estimated SSI                used to detect whether electrocauterization was per-
incidence of around 23.5% obtained in a previously            formed. To evaluate obesity, body mass index (BMI)
conducted pilot study that included postdischarge             was calculated for each patient and classified according
surveillance. A significance level of 5% and a sampling        to the following categories: BMI ,20, underweight; BMI
error of 8% were adopted; therefore, a minimum                20 to 24.9, ideal weight; BMI 25 to 29.9, overweight;
sample of 108 women was required, with an estimated           BMI .30, obese. C-sections were classified according
confidence interval (CI) of 15.5% to 31%.                      to the risk of SSI as 0, 1, 2, or 3 in accordance with
   The inclusion criteria consisted of having been            the NNIS system.16
submitted to a C-section after April 2008 and having             A postdischarge telephone interview was conducted
a telephone for contact. Exclusion criteria consisted         by the investigator herself or by a student nurse specif-
of death in the immediate postoperative period or the         ically trained for this task. A structured questionnaire
presence of any form of impairment that would ham-            was used, and the estimated duration of the interview
per the patient’s ability to consent to participate in        was 5 minutes. The questions were specifically de-
the proposed study or affect postdischarge telephone          signed to identify any signs of a SSI following the pa-
contact. The criterion for discontinuation consisted of       tient’s discharge from hospital. An initial contact was
being unable to contact the woman within the 30-day           made 15 days after the C-section and a second contact
follow-up period, except if she had already reported          30 days after the surgery. A maximum of 3 attempts
an SSI at first contact. The investigator approached           were made to establish contact on both occasions.
women who had undergone a C-section while they                Patients who could not be contacted for the second in-
were still in hospital and read them the informed con-        terview were discontinued from the study unless an SSI
sent form, which had been approved by the Internal            was identified at the first interview.
www.ajicjournal.org                                                                       Cardoso Del Monte and Pinto Neto                                  469
Vol. 38 No. 6

Table 1. Infections based on hospital surveillance and                                        204 women admitted to the study
infection postdischarge, 2008-2009
                                                                       17 were discontinued                                     187 final sample – follow
                              Forms of surveillance                                                                              up 30 days after surgery

                         In-hospital      Post-discharge
                                                                                                                             44 SSI                   143 no SSI
                        n         %        n          %    P value
                                                                                                          42 postdischarge     02 while in hospital
No infection            185      98.9     145      77.54                                                        95%                    5%
Infection present         2       1.06     42      22.45   ,.0001
Total                   187     100       187     100
                                                                                                  39 in 1st contact         03 in 2nd contact
                    2                                                                                   93%                       07%
NOTE. McNemar x test.
                                                                                         In 4 patients in whom the infection became evident within
                                                                                        the first 15 days, symptoms persisted 30 days after surgery


   Statistical analysis was performed using the Statisti-                                                             Fig 1. Selected sample.
cal Analysis System, a statistical software program, ver-
sion 9.02 (SAS Institute, Cary, NC). The McNemar x2 test
and Fisher exact test were used, as applicable, for cate-
gorical variables, and the Mann-Whitney test for numer-              calculated from the date of the woman’s last menstrual
ical variables. Cox proportional hazards regression                  period or by ultrasonography when this date was
model was used to identify the risk factors associated               unavailable, was 38.8 weeks (range, 27.2-45.4 weeks).
with the occurrence of SSI. Relative risks and their                 Thirteen women in the sample had a community infec-
respective 95% confidence intervals were calculated,                  tion: 4 cases of diverse infections, 3 cases of urinary
P values ,.05 being considered statistically significant.             infections, 2 cases of chorioamnionitis, 2 cases of hep-
                                                                     atitis C, 1 case of HIV, and 1 case of HIV and concomi-
RESULTS                                                              tant hepatitis C. There was no statistically significant
                                                                     difference in the SSI rate in these patients. In the study
   A total of 204 women were admitted to the study. Of               sample, 185 women (98.9%) had undergone prenatal
these, 17 were discontinued principally because of                   care, 130 (70.3%) of whom had attended more than
difficulty in establishing contact; therefore, the final               7 prenatal consultations. With respect to BMI, 88
sample consisted of 187 women. Of these, 44 (23.5%)                  women (47.05%) were classified as obese, 77
developed a SSI. In 42 of 44 women (95.4%), the SSI ap-              (41.17%) as overweight, and 17 (9%) as being of ideal
peared after the patient was discharged from hospital                weight or underweight. In 5 cases (2.7%), this informa-
(Table 1). In 39 of 42 cases (93.9%), the infection was              tion was unavailable. With respect to parity, 96 patients
diagnosed during the first telephone contact with the                 (51.3%) were nulliparas and 49 (26.2%) primiparas,
patient (15 days after the C-section), whereas, in 3                 whereas 26 patients (13.9%) had already had 2 chil-
cases (7.1%), diagnosis was only made at the second                  dren, and 16 patients (8.5%) had given birth 3 or
contact (30 days after the C-section) (Fig 1). In 4 of 44            more times previously. In 98 cases (52.4%), the women
patients (9%) in whom the infection became evident                   had intact membranes when surgery began; whereas,
within the first 15 days, symptoms persisted 30 days                  in 60 patients (32.1%), membrane rupture occurred
after surgery. In 3 cases, the patient was readmitted                12 hours or less prior to surgery; and, in 29 patients
to hospital for treatment. Infections classified as super-            (15.5%), membranes ruptured more than 12 hours
ficial incisional SSI involving the skin and subcutane-               prior to C-section. In 147 cases (78.6%), the women
ous region occurred in 43 patients (97.7% of cases).                 went into labor in hospital, and, in these cases, labor
Most of these cases were treated with 500 mg of first-                lasted for a mean of 14.6 hours (median, 9.3 hours;
generation cephalosporin every 6 hours for 7 to 10                   range, 1-76.3 hours). The principal characteristics of
days, as prescribed by physicians at basic health care               the study population are summarized in Table 2. The
units. In one case, the infection, classified as an or-               primary reasons for indicating C-section were as
gan/space SSI, progressed in the form of an abscess                  follows: fetal distress in 47 cases (25.1%), repeat C-sec-
that began in the pelvis and extended to the right hypo-             tion in 26 cases (13.9%), functional dystocia in 26
chondrium, and a subtotal hysterectomy had to be per-                cases (13.9%), cephalopelvic disproportion in 22 cases
formed. In this case, the patient required prolonged                 (11.8%), and breech presentation in 19 cases (10.2%).
hospitalization for 20 days, including 6 days in an                  Of the women in this study, 40 were hypertensive
intensive care unit. This treatment was carried out at               (21.4%), and 14 were diabetic (7.5%) individuals. Re-
the Center for Women’s Integrated Health Care.                       garding the potential for contamination during surgery,
   The mean age of the women in this study was 27.3                  only 2 cases were classified as infected following detec-
years (range, 13-44 years). Mean gestational age,                    tion of chorioamnionitis during the C-section. The
470      Cardoso Del Monte and Pinto Neto                                                                        American Journal of Infection Control
                                                                                                                                         August 2010


Table 2. Selected characteristics of the study sample
Variables                                               No.                Mean       6SD           Median           Minimum               Maximum

Age, yr                                                 187                27.38       6.85          27                 13                    44
Gestational age (wk)                                    185                38.81       2.39          39                 27.71                 45.43
BMI (kg/m2)                                             182                31.04       6.4           29.75              18.91                 58.14
Number of prenatal consultations                        184                 9.06       2.81           9                  2                    16
Parity                                                  187                 0.83       1.07           0                  0                     5
Time of membrane rupture*                                89                13.71      29.24           6.42               0.58                264
Duration of labor*                                      147                14.6       14.6            9.3                1                    76.3
Duration of surgery*                                    179                 1.25       0.41           1.17               0.58                  3.5
SD, standard deviation.
*Hours.




Table 3. Variables significantly associated with surgical site infection in the bivariate analysis
Variables                                                     Category             SSI, %            P value              RR                  95% CI

Number of prenatal consultations                                 #7                 37.0             .0047*               2.09               1.26-3.48
                                                                 .7                 17.7
Arterial hypertension                                            Yes                40               .0065*               2.07               1.25-3.43
                                                                 No                 19.3
CI, confidence interval; RR, relative risk; SSI, surgical site infection.
*P , .05, x2 test.




most commonly used type of anesthesia was a spinal                                    in SSI between surgeries classified as 1 and 2; however,
block in 107 cases (57.2%), followed by an epidural                                   this calculation could not be made for a risk score of
in 56 cases (29.9%) and spinal block plus epidural in                                 3 because there was only 1 patient with this score. In
20 cases (10.7%). Only 4 patients were submitted to                                   the bivariate analysis, factors found to be significantly
general anesthesia (2.1%). According to the ASA phys-                                 associated with SSI were the number of prenatal
ical status classification, 82 women were classified as                                 consultations and the presence of hypertension
ASA 1 and 82 as ASA 2, constituting 87.7% of the sam-                                 (Table 3); however, only arterial hypertension remained
ple. In addition, 16 women (8.6%) were classified as                                   significant in the multivariate analysis (Table 4).
ASA 3 and 1 (0.5%) as ASA 4. In 6 patients, ASA classi-
fication was not recorded. Of the 187 C-sections per-
                                                                                      DISCUSSION
formed, 128 (68.4%) were elective surgeries, and 53
(28.3%) were emergency. In 6 cases, there was no                                         This study clearly shows that neglecting to perform
record of whether the surgery had been elective or                                    postdischarge surveillance of women undergoing to a
emergency. The mean duration of surgery was 1 hour                                    C-section leads to under-notification of SSI with respect
25 minutes (range, 34.8 minutes to 3.5 hours). In the                                 to this type of surgery. The fact that most of the cases
majority of cases in which the duration of surgery                                    were detected after the patient was discharged from
was longer than the mean, it was found to have been                                   hospital is probably due to the brief period of hospitali-
associated with another procedure (tubal ligation,                                    zation (72 hours) associated with this type of surgery
total abdominal hysterectomy, or repair of bladder                                    during which time the infection is not yet apparent.
laceration). With respect to intrasurgical blood loss,                                This finding is consistent with data published by other
107 patients (57.2%) lost #700 mL of blood, whereas                                   investigators in the international literature, citing
67 patients (35.8%) lost more than 700 mL. In 13 cases                                postdischarge infection rates following C-sections that
(6.9%), there was no record of blood loss. Electrocau-                                varied depending on the type of postdischarge surveil-
terization was used during surgery in 112 cases                                       lance implemented.5-14 It is important to say that the cri-
(60%). Compliance with the institute’s protocol for pro-                              teria used for diagnosis for SSI in these studies was that
phylactic antibiotic therapy was confirmed in 181                                      from the Centers for Disease Control and Prevention.
cases (96.8%). With respect to the NNIS basic SSI risk                                   A study carried out by Ferraz et al17 in 1995, involv-
index, 116 cases were classified as 2 and 70 as 1,                                     ing outpatients who had recently been submitted to
whereas only 1 patient was classified as 3 and none                                    surgery in Brazil, reported a postdischarge SSI rate of
as 0. There was no statistically significant difference                                91.4% following C-section. An interesting finding of
www.ajicjournal.org                                                                                    Cardoso Del Monte and Pinto Neto                        471
Vol. 38 No. 6

Table 4. Variable significantly associated with surgical site                            Multiple factors contribute to post-C-section SSI. In
infection in multivariate analysis                                                  the present study, factors classically associated with
                                                                                    post-C-section SSI such as obesity, premature rupture
Variable                                 P value           RR            95% CI
                                                                                    of membranes, diabetes, and emergency C-sections
Presence of arterial                     .01*              2.47         1.21-5.04   were not found to be significantly associated.19
  hypertension                                                                          With respect to the number of prenatal consultations
CI, confidence interval; RR, relative risk.                                          attended by the patient, similar findings have been
*P , .05, Cox proportional hazards regression with stepwise variable selection.     reported by Killian et al (2001),19 whose study showed
                                                                                    that having attended fewer than 7 prenatal consulta-
the present study that deserves particular mention is                               tions was a factor that significantly increased the risk
that, in 93% of the women who developed an SSI,                                     of post-C-section endometritis. More prenatal consulta-
the infection became apparent in the first 15 days fol-                              tions are a guarantee that primary prevention methods
lowing C-section. This finding corroborates data from                                are instituted that will consequently avoid many perina-
similar studies carried out in Brazil. Ferraz et al17                               tal complications including postsurgical infection.
reported that post-C-section SSI becomes evident after                              Women should be counseled to control their weight
a mean of 8.6 days following surgery; Couto et al12                                 and blood pressure. The increased risk of infection
showed that 95% of cases of post-C-section SSI                                      following a C-section in hypertensive women may be
occurred between the tenth and fifteenth days follow-                                explained by the chronic alteration in peripheral blood
ing surgery; and Dantas13 stated that 95% of these                                  supply as a result of increased vascular resistance. This
infections became apparent within 14 days following                                 finding was also reported in a study with a large sample
surgery. Therefore, a 30-day follow-up period may be                                size (19,416 C-sections) carried out to identify risk
unnecessary for the detection of post C-section SSI.                                factors for early SSIs in C-sections (diagnosed prior to
   The SSI rate found in the present study (23.5%) is                               discharge from hospital).20 The present study also
higher than rates found in other studies in which postdi-                           sought to evaluate electrocauterization, which is
scharge surveillance was performed. Although no con-                                commonly used in this institute, as a factor associated
sensus has yet been reached on the best methodology                                 with SSI; however, no such association was found.
for implementing postdischarge surveillance, telephone                                  In conclusion, it is our belief that accurate knowledge
contact would appear to represent a low-cost technique                              of infection rates will help develop and implement mea-
that requires minimal resources and is widely used. Nev-                            sures for the prevention and control of these infections.
ertheless, Whitby et al18 found a low positive predictive                           In view of the relevance of the data obtained, the postdi-
value (28.7%) for diagnoses made according to patient                               scharge surveillance methodology used in the present
telephone reports, although the negative predictive                                 study will be incorporated by this institute’s HICC. Quar-
value was high (98.2%) compared with diagnosis made                                 terly data analyses will continue, and feedback will be
by an infection control nurse through direct examina-                               provided to those responsible for the area with the
tion of the surgical incision in the patient following                              objective of stimulating a review of current practices
discharge from hospital.                                                            and reducing SSI rates.
   Postdischarge surveillance involving telephone
contact with patients and using a well-defined script
of questions has been shown to constitute a very useful                             References
instrument for the detection of SSI. It is important to
                                                                                    1. Astagneau P, Rioux C, Golliot F, Brucker G. INCISO Network Study
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emphasize that this model of surveillance was possible                                 Group. Morbity and mortality associated with surgical site infections:
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                                                                                                                                                  August 2010


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Acr 3 en fama

  • 1. Postdischarge surveillance following cesarean section: The incidence of surgical site infection and associated factors Meire Celeste Cardoso Del Monte, RN,a and Aarao Mendes Pinto Neto, MD, PhDb ˜ ˜ Sao Paulo, Brazil Background: The rate of surgical site infections (SSI) and their associated risk factors was identified by performing postdischarge surveillance following cesarean section at a public university teaching hospital in Brazil. Methods: The study was conducted at the Center for Women’s Integrated Health Care in Brazil between May 2008 and March 2009. Women were contacted by telephone 15 and 30 days after cesarean section. During hospitalization, a form was completed on factors associated with post-cesarean SSI. The x2 test and Fisher exact test were used to analyze categorical variables and the Mann-Whitney test for numerical variables. Relative risks (RR) and their respective 95% confidence intervals (95% CI) were calculated for factors associated with SSI. P values , .05 were considered significant. Results: The final sample consisted of 187 women. SSI was detected in 44 cases (23.5%). In 42 of 44 women (95%), SSI appeared following discharge from hospital, becoming evident within the first 15 days following surgery. Number of prenatal consultations #7 (RR, 2.09; 95% CI: 1.26-3.48) and hypertension (RR, 2.07; 95% CI: 1.25-3.43) were significantly associated with SSI in the bivariate analysis. In the multivariate analysis, only hypertension (RR, 2.47; 95% CI: 1.21-5.04) remained significant. Conclusion: Postdischarge surveillance is essential for ensuring accurate estimates of post-cesarean section SSI. A 15-day postdischarge follow-up was shown to be sufficient. Hypertension was a factor associated with SSI. Key Words: Postdischarge surveillance; cesarean section; surgical site infection; hospital infection; infection control nurse. Copyright ª 2010 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. (Am J Infect Control 2010;38:467-72.) Surgical site infections (SSI) are common postoperative their statistics to those patients in whom infection complications, constituting a major clinical problem in becomes apparent prior to discharge or those who re- terms of morbidity and mortality,1 duration of hospitali- turn spontaneously to the hospital for treatment. Vari- zation, and hospital costs.2,3 ous studies have been published showing a consensus Most SSIs only become apparent after the patient is on the need to perform postdischarge surveillance of discharged from hospital.4-13 Different studies that patients submitted to C-sections to obtain more included postdischarge surveillance have reported accurate statistics on the frequency of SSI.7-13 infection rates varying from 27.6%4 to 84%,5 particu- In Brazil, Couto et al (1998)12 reported post-C-section larly following surgeries such as cesarean sections SSI rates of 1.6% when surveillance was limited to (C-sections) for which the hospitalization period is brief.6 hospitalized patients and 9.6% when postdischarge sur- Few Brazilian hospitals conduct surveillance after veillance was implemented. Another study carried out the patient has been discharged from hospital, limiting ˜ in a maternity hospital in the state of Sao Paulo found a post-C-section SSI rate of 1.2% when surveillance From the Department of Infection Controla and Department of was limited to hospitalized patients versus 14.4% Obstetrics and Gynecology,b Women’s Hospital, School of Medical when these rates were obtained from postdischarge sur- ˜ Sciences, University of Campinas (UNICAMP), Campinas, Sao Paulo, veillance.13 The study was conducted at the Center for Brazil. Women’s Integrated Health Care, a tertiary, 142-bed, Address correspondence to Meire Celeste Cardoso Del Monte, RN, university teaching and public hospital situated in the ´ ˜ Rua Dr. Liraucio Gomes, 257 Cambuı, 13.024-490 Campinas, Sao Paulo, Brazil. E-mail: meiredelmonte@yahoo.com. ˜ state of Sao Paulo, Brazil. A mean of 100 C-sections are performed in this hospital monthly. This study was car- Conflicts of interest: None to report. ried out between May 2008 and March 2009. There has 0196-6553/$36.00 been a hospital infection control committee (HICC) in Copyright ª 2010 by the Association for Professionals in Infection this institute since 1986, and this committee currently Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. recommends prophylactic antibiotic therapy following all C-section deliveries. This protocol determines the doi:10.1016/j.ajic.2009.10.008 use of cefazolin, 2 g intravenously, after the umbilical 467
  • 2. 468 Cardoso Del Monte and Pinto Neto American Journal of Infection Control August 2010 cord has been clamped or 900 mg of clindamycin for Review Board of the institute prior to initiation of the patients who are allergic to penicillin. study. If the woman agreed to participate, she then A recent systematic review of the methods used to signed the informed consent form, was given a copy, identify SSI following discharge from hospital and was admitted to the study. concluded that existing studies on the subject have so Diagnosis of SSI was defined according to the criteria far failed to identify a valid, reliable method for identi- standardized by the Centers for Disease Control and Pre- fying such infections postdischarge. On a local level, vention, Atlanta, GA, determining superficial incisional the method used to identify postdischarge SSI is likely SSI, deep incisional SSI, or organ/space SSI.15 The inves- to be dependent on existing resources, on the objective tigator made a questionnaire, based in this criteria, from of surveillance, and on the nature of the data routinely which questions about purulent discharge, identification available.14 In this study, the researcher contacted the of an isolated organism, signs and symptoms of infection patients by telephone following discharge and estab- (fever, pain or tenderness, localized swelling, redness, lished the occurrence of a SSI by having the patients heat), an abscess or other evidence of infection involving confirm the presence or absence of symptoms associ- the deep incision, or diagnosis of SSI by attending physi- ated with a SSI. Therefore, the methodology used to cian were applied by telephone interview. determine postdischarge SSI should be considered as The following data were obtained from the patient’s a potential limitation of the study. chart: age, gestational age, whether the patient had The objectives of the present study were to evaluate undergone prenatal care and the number of prenatal the incidence of SSI following discharge of the patient consultations she had attended, weight and height, from hospital through the use of telephone interviews parity, presence of community infection, ruptured and to identify factors associated with the presence of membranes at admission and the time of membrane these infections in a tertiary Brazilian university rupture, presence of diabetes or arterial hypertension, teaching hospital that is a regional referral hospital for duration of labor, indication for C-section, surgical maternal and child health care. wound classification (clean, clean contaminated, con- taminated and dirty/infected), use of general anesthe- METHODS sia or other type of anesthesia, the American Society of Anesthesiologists (ASA) physical status classification This is an observational, longitudinal, cohort study score, whether the C-section represented an emer- carried out using data collected from patient charts gency or elective surgery, duration of the surgery, and from interviews with patients with the objective volume of intrasurgical blood loss as calculated by of identifying post-C-section SSI. Sample size calcula- the anesthesiologist, whether any other procedures tion was based on the SSI rate of 0.7% registered by were carried out, and whether there was compliance the HICC in 2006, established according to the epide- with the institutional protocol of prophylactic antibi- miologic surveillance of patients up to the time of their otic therapy. The intraoperative nursing chart was discharge from hospital, and the estimated SSI used to detect whether electrocauterization was per- incidence of around 23.5% obtained in a previously formed. To evaluate obesity, body mass index (BMI) conducted pilot study that included postdischarge was calculated for each patient and classified according surveillance. A significance level of 5% and a sampling to the following categories: BMI ,20, underweight; BMI error of 8% were adopted; therefore, a minimum 20 to 24.9, ideal weight; BMI 25 to 29.9, overweight; sample of 108 women was required, with an estimated BMI .30, obese. C-sections were classified according confidence interval (CI) of 15.5% to 31%. to the risk of SSI as 0, 1, 2, or 3 in accordance with The inclusion criteria consisted of having been the NNIS system.16 submitted to a C-section after April 2008 and having A postdischarge telephone interview was conducted a telephone for contact. Exclusion criteria consisted by the investigator herself or by a student nurse specif- of death in the immediate postoperative period or the ically trained for this task. A structured questionnaire presence of any form of impairment that would ham- was used, and the estimated duration of the interview per the patient’s ability to consent to participate in was 5 minutes. The questions were specifically de- the proposed study or affect postdischarge telephone signed to identify any signs of a SSI following the pa- contact. The criterion for discontinuation consisted of tient’s discharge from hospital. An initial contact was being unable to contact the woman within the 30-day made 15 days after the C-section and a second contact follow-up period, except if she had already reported 30 days after the surgery. A maximum of 3 attempts an SSI at first contact. The investigator approached were made to establish contact on both occasions. women who had undergone a C-section while they Patients who could not be contacted for the second in- were still in hospital and read them the informed con- terview were discontinued from the study unless an SSI sent form, which had been approved by the Internal was identified at the first interview.
  • 3. www.ajicjournal.org Cardoso Del Monte and Pinto Neto 469 Vol. 38 No. 6 Table 1. Infections based on hospital surveillance and 204 women admitted to the study infection postdischarge, 2008-2009 17 were discontinued 187 final sample – follow Forms of surveillance up 30 days after surgery In-hospital Post-discharge 44 SSI 143 no SSI n % n % P value 42 postdischarge 02 while in hospital No infection 185 98.9 145 77.54 95% 5% Infection present 2 1.06 42 22.45 ,.0001 Total 187 100 187 100 39 in 1st contact 03 in 2nd contact 2 93% 07% NOTE. McNemar x test. In 4 patients in whom the infection became evident within the first 15 days, symptoms persisted 30 days after surgery Statistical analysis was performed using the Statisti- Fig 1. Selected sample. cal Analysis System, a statistical software program, ver- sion 9.02 (SAS Institute, Cary, NC). The McNemar x2 test and Fisher exact test were used, as applicable, for cate- gorical variables, and the Mann-Whitney test for numer- calculated from the date of the woman’s last menstrual ical variables. Cox proportional hazards regression period or by ultrasonography when this date was model was used to identify the risk factors associated unavailable, was 38.8 weeks (range, 27.2-45.4 weeks). with the occurrence of SSI. Relative risks and their Thirteen women in the sample had a community infec- respective 95% confidence intervals were calculated, tion: 4 cases of diverse infections, 3 cases of urinary P values ,.05 being considered statistically significant. infections, 2 cases of chorioamnionitis, 2 cases of hep- atitis C, 1 case of HIV, and 1 case of HIV and concomi- RESULTS tant hepatitis C. There was no statistically significant difference in the SSI rate in these patients. In the study A total of 204 women were admitted to the study. Of sample, 185 women (98.9%) had undergone prenatal these, 17 were discontinued principally because of care, 130 (70.3%) of whom had attended more than difficulty in establishing contact; therefore, the final 7 prenatal consultations. With respect to BMI, 88 sample consisted of 187 women. Of these, 44 (23.5%) women (47.05%) were classified as obese, 77 developed a SSI. In 42 of 44 women (95.4%), the SSI ap- (41.17%) as overweight, and 17 (9%) as being of ideal peared after the patient was discharged from hospital weight or underweight. In 5 cases (2.7%), this informa- (Table 1). In 39 of 42 cases (93.9%), the infection was tion was unavailable. With respect to parity, 96 patients diagnosed during the first telephone contact with the (51.3%) were nulliparas and 49 (26.2%) primiparas, patient (15 days after the C-section), whereas, in 3 whereas 26 patients (13.9%) had already had 2 chil- cases (7.1%), diagnosis was only made at the second dren, and 16 patients (8.5%) had given birth 3 or contact (30 days after the C-section) (Fig 1). In 4 of 44 more times previously. In 98 cases (52.4%), the women patients (9%) in whom the infection became evident had intact membranes when surgery began; whereas, within the first 15 days, symptoms persisted 30 days in 60 patients (32.1%), membrane rupture occurred after surgery. In 3 cases, the patient was readmitted 12 hours or less prior to surgery; and, in 29 patients to hospital for treatment. Infections classified as super- (15.5%), membranes ruptured more than 12 hours ficial incisional SSI involving the skin and subcutane- prior to C-section. In 147 cases (78.6%), the women ous region occurred in 43 patients (97.7% of cases). went into labor in hospital, and, in these cases, labor Most of these cases were treated with 500 mg of first- lasted for a mean of 14.6 hours (median, 9.3 hours; generation cephalosporin every 6 hours for 7 to 10 range, 1-76.3 hours). The principal characteristics of days, as prescribed by physicians at basic health care the study population are summarized in Table 2. The units. In one case, the infection, classified as an or- primary reasons for indicating C-section were as gan/space SSI, progressed in the form of an abscess follows: fetal distress in 47 cases (25.1%), repeat C-sec- that began in the pelvis and extended to the right hypo- tion in 26 cases (13.9%), functional dystocia in 26 chondrium, and a subtotal hysterectomy had to be per- cases (13.9%), cephalopelvic disproportion in 22 cases formed. In this case, the patient required prolonged (11.8%), and breech presentation in 19 cases (10.2%). hospitalization for 20 days, including 6 days in an Of the women in this study, 40 were hypertensive intensive care unit. This treatment was carried out at (21.4%), and 14 were diabetic (7.5%) individuals. Re- the Center for Women’s Integrated Health Care. garding the potential for contamination during surgery, The mean age of the women in this study was 27.3 only 2 cases were classified as infected following detec- years (range, 13-44 years). Mean gestational age, tion of chorioamnionitis during the C-section. The
  • 4. 470 Cardoso Del Monte and Pinto Neto American Journal of Infection Control August 2010 Table 2. Selected characteristics of the study sample Variables No. Mean 6SD Median Minimum Maximum Age, yr 187 27.38 6.85 27 13 44 Gestational age (wk) 185 38.81 2.39 39 27.71 45.43 BMI (kg/m2) 182 31.04 6.4 29.75 18.91 58.14 Number of prenatal consultations 184 9.06 2.81 9 2 16 Parity 187 0.83 1.07 0 0 5 Time of membrane rupture* 89 13.71 29.24 6.42 0.58 264 Duration of labor* 147 14.6 14.6 9.3 1 76.3 Duration of surgery* 179 1.25 0.41 1.17 0.58 3.5 SD, standard deviation. *Hours. Table 3. Variables significantly associated with surgical site infection in the bivariate analysis Variables Category SSI, % P value RR 95% CI Number of prenatal consultations #7 37.0 .0047* 2.09 1.26-3.48 .7 17.7 Arterial hypertension Yes 40 .0065* 2.07 1.25-3.43 No 19.3 CI, confidence interval; RR, relative risk; SSI, surgical site infection. *P , .05, x2 test. most commonly used type of anesthesia was a spinal in SSI between surgeries classified as 1 and 2; however, block in 107 cases (57.2%), followed by an epidural this calculation could not be made for a risk score of in 56 cases (29.9%) and spinal block plus epidural in 3 because there was only 1 patient with this score. In 20 cases (10.7%). Only 4 patients were submitted to the bivariate analysis, factors found to be significantly general anesthesia (2.1%). According to the ASA phys- associated with SSI were the number of prenatal ical status classification, 82 women were classified as consultations and the presence of hypertension ASA 1 and 82 as ASA 2, constituting 87.7% of the sam- (Table 3); however, only arterial hypertension remained ple. In addition, 16 women (8.6%) were classified as significant in the multivariate analysis (Table 4). ASA 3 and 1 (0.5%) as ASA 4. In 6 patients, ASA classi- fication was not recorded. Of the 187 C-sections per- DISCUSSION formed, 128 (68.4%) were elective surgeries, and 53 (28.3%) were emergency. In 6 cases, there was no This study clearly shows that neglecting to perform record of whether the surgery had been elective or postdischarge surveillance of women undergoing to a emergency. The mean duration of surgery was 1 hour C-section leads to under-notification of SSI with respect 25 minutes (range, 34.8 minutes to 3.5 hours). In the to this type of surgery. The fact that most of the cases majority of cases in which the duration of surgery were detected after the patient was discharged from was longer than the mean, it was found to have been hospital is probably due to the brief period of hospitali- associated with another procedure (tubal ligation, zation (72 hours) associated with this type of surgery total abdominal hysterectomy, or repair of bladder during which time the infection is not yet apparent. laceration). With respect to intrasurgical blood loss, This finding is consistent with data published by other 107 patients (57.2%) lost #700 mL of blood, whereas investigators in the international literature, citing 67 patients (35.8%) lost more than 700 mL. In 13 cases postdischarge infection rates following C-sections that (6.9%), there was no record of blood loss. Electrocau- varied depending on the type of postdischarge surveil- terization was used during surgery in 112 cases lance implemented.5-14 It is important to say that the cri- (60%). Compliance with the institute’s protocol for pro- teria used for diagnosis for SSI in these studies was that phylactic antibiotic therapy was confirmed in 181 from the Centers for Disease Control and Prevention. cases (96.8%). With respect to the NNIS basic SSI risk A study carried out by Ferraz et al17 in 1995, involv- index, 116 cases were classified as 2 and 70 as 1, ing outpatients who had recently been submitted to whereas only 1 patient was classified as 3 and none surgery in Brazil, reported a postdischarge SSI rate of as 0. There was no statistically significant difference 91.4% following C-section. An interesting finding of
  • 5. www.ajicjournal.org Cardoso Del Monte and Pinto Neto 471 Vol. 38 No. 6 Table 4. Variable significantly associated with surgical site Multiple factors contribute to post-C-section SSI. In infection in multivariate analysis the present study, factors classically associated with post-C-section SSI such as obesity, premature rupture Variable P value RR 95% CI of membranes, diabetes, and emergency C-sections Presence of arterial .01* 2.47 1.21-5.04 were not found to be significantly associated.19 hypertension With respect to the number of prenatal consultations CI, confidence interval; RR, relative risk. attended by the patient, similar findings have been *P , .05, Cox proportional hazards regression with stepwise variable selection. reported by Killian et al (2001),19 whose study showed that having attended fewer than 7 prenatal consulta- the present study that deserves particular mention is tions was a factor that significantly increased the risk that, in 93% of the women who developed an SSI, of post-C-section endometritis. More prenatal consulta- the infection became apparent in the first 15 days fol- tions are a guarantee that primary prevention methods lowing C-section. This finding corroborates data from are instituted that will consequently avoid many perina- similar studies carried out in Brazil. Ferraz et al17 tal complications including postsurgical infection. reported that post-C-section SSI becomes evident after Women should be counseled to control their weight a mean of 8.6 days following surgery; Couto et al12 and blood pressure. The increased risk of infection showed that 95% of cases of post-C-section SSI following a C-section in hypertensive women may be occurred between the tenth and fifteenth days follow- explained by the chronic alteration in peripheral blood ing surgery; and Dantas13 stated that 95% of these supply as a result of increased vascular resistance. This infections became apparent within 14 days following finding was also reported in a study with a large sample surgery. Therefore, a 30-day follow-up period may be size (19,416 C-sections) carried out to identify risk unnecessary for the detection of post C-section SSI. factors for early SSIs in C-sections (diagnosed prior to The SSI rate found in the present study (23.5%) is discharge from hospital).20 The present study also higher than rates found in other studies in which postdi- sought to evaluate electrocauterization, which is scharge surveillance was performed. Although no con- commonly used in this institute, as a factor associated sensus has yet been reached on the best methodology with SSI; however, no such association was found. for implementing postdischarge surveillance, telephone In conclusion, it is our belief that accurate knowledge contact would appear to represent a low-cost technique of infection rates will help develop and implement mea- that requires minimal resources and is widely used. Nev- sures for the prevention and control of these infections. ertheless, Whitby et al18 found a low positive predictive In view of the relevance of the data obtained, the postdi- value (28.7%) for diagnoses made according to patient scharge surveillance methodology used in the present telephone reports, although the negative predictive study will be incorporated by this institute’s HICC. Quar- value was high (98.2%) compared with diagnosis made terly data analyses will continue, and feedback will be by an infection control nurse through direct examina- provided to those responsible for the area with the tion of the surgical incision in the patient following objective of stimulating a review of current practices discharge from hospital. and reducing SSI rates. Postdischarge surveillance involving telephone contact with patients and using a well-defined script of questions has been shown to constitute a very useful References instrument for the detection of SSI. It is important to 1. 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