Drs. Mitt and Maimets are from the Departments of Internal Medicine and Infection Control, and Dr. Peri is from the Women’s Clinic, Tartu University Hospital, Tartu, Estonia. Dr. Lang is from the Department of Public Health, University of Tartu, Tartu, Estonia.
Address reprint requests to Piret Mitt, MD, Department of Infection Control, Tartu University Hospital, Lina 6, 51004 Tartu, Estonia. Piret.Mitt@kliinikum.ee
The authors thank Fred Kirss, MD, head of the Department of Obstetrics, Women’s Clinic, Tartu University Hospital, for supporting the study and Kristiina Rull, MD, Women’s Clinic, Tartu University Hospital, for critical review of the manuscript.
Piret Mitt, MD; Katrin Lang, MD, MPH; Aira Peri, MD; Matti Maimets, MD, PhD
OBJECTIVES: To evaluate a multi-method approach to postdischarge surveillance of surgical-site infections (SSIs) and to identify infection rates and risk factors associated with SSI following cesarean section.
DESIGN: Cross-sectional survey.
SETTING: Academic tertiary-care obstetric and gynecol-ogy center with 54 beds.
PATIENTS: All women who delivered by cesarean sec-tion in Tartu University Women’s Clinic during 2002.
METHODS: Infections were identiﬁed during hospital stay or by postdischarge survey using a combination of tele-phone calls, healthcare worker questionnaire, and outpatient medical records review. SSI was diagnosed according to the cri-teria of the Centers for Disease Control and Prevention National Nosocomial Infections Surveillance System.
RESULTS: The multi-method approach gave a follow-up rate of 94.8%. Of 305 patients, 19 (6.2%; 95% conﬁdence interval [CI95], 3.8–9.6) had SSIs. Forty-two percent of these SSIs were detected during postdischarge surveillance. We found three variables associated with increased risk for developing SSI: in-ternal fetal monitoring (odds ratio [OR], 16.6; CI95, 2.2–125.8;
P = .007), chorioamnionitis (OR, 8.8; CI95, 1.1–69.6; P = .04), and surgical wound classes III and IV (OR, 3.8; CI95, 1.2–11.8;
P = .02).
CONCLUSIONS: The high response rate validated the effectiveness of this kind of surveillance method and was most suitable in current circumstances. A challenge exists to de-crease the frequency of internal fetal monitoring and to treat chorioamnionitis as soon as possible (Infect Control Hosp Epide-miol 2005;26:449-454).
The single most important risk factor for postpartum maternal infection is delivery by cesarean section.1 Mater-nal morbidity related to infections has been shown to be eightfold higher after cesarean section than after vaginal delivery.2 Reducing the number of deliveries by cesarean section and identifying risk factors for post-cesarean surgi-cal-site infections (SSIs) could contribute to a decrease in maternal morbidity.
The reported incidence of SSI following cesarean section varies widely, ranging from 0.3% in Turkey3 to 17% in Australia.4 Among hospitals reporting to the National Nosocomial Infections Surveillance (NNIS) System, the rate of SSI after cesarean section was 2.8% to 6.7% de-pending on the risk index category.5 The incidence rate depends on the following: the deﬁnition of SSI adopted, the intensity of surveillance, the prevalence of risk factors for SSI in the patient group being audited, and whether the survey contains postdischarge data.6 SSI may not be detected for several weeks after discharge and may not require admission to the operating hospital. Because the length of postoperative hospitalization continues to
decrease, the increasing number of SSIs is not detected through the standard surveillance method; therefore, postdischarge surveillance has become increasingly im-portant to obtain accurate rates of SSI. Several methods for postdischarge surveillance of SSI have been evaluated for efﬁciency, including direct examination of patients’ wounds during follow-up visits to either surgery clinics or physicians’ ofﬁces, review of medical records of surgery clinic patients, and patient and healthcare worker surveys by mail or telephone.4,7 Automated data, especially from pharmacy and administrative claims, might substantially improve both inpatient and postdischarge surveillance for SSI while reducing the resources required8; however, this method is not available everywhere. Nevertheless, there is no universally accepted strategy for monitoring these infections.6,7,9,10 When choosing a surveillance method, in-fection control personnel must consider not only the sen-sitivity and the sources for data, but also the human and ﬁnancial resources allotted for SSI surveillance.10
Various factors affect infection rates in different set-tings; those most frequently cited in the literature include
extremes of maternal weight (being underweight or obese), prolonged labor or rupture of membranes, long duration of surgery, multiple procedures, manual removal of the pla-centa, young maternal age, maternal preoperative condi-tion, procedure-related blood loss, and absence of antibiotic prophylaxis.11-17 It is important to identify these factors to target high-risk patients who need speciﬁc prevention mea-sures.
Despite recent progress in developing a medical in-frastructure, some of its components, such as a national system for nosocomial infections surveillance, have not yet been established in Estonia. In Estonia, only a few studies have been conducted on healthcare-associated infections.18 The aims of this descriptive study were to evaluate a multi-method approach to postdischarge surveillance of SSI and to identify infection rates and risk factors associated with SSI following cesarean section by comparing patients with and without SSI.
Tartu University Women’s Clinic is a 54-bed (2002 data) academic, tertiary-care obstetric and gynecology cen-ter that serves mainly the population of southern Estonia,
which accounts for approximately one-third of the Estonian population, and has an average of 2,000 deliveries per year.
The study population consisted of women who de-livered by cesarean section in Tartu University Women’s Clinic during 2002. The purpose of the study was explained to patients, and their verbal consent to participate was ob-tained.
Infections were identiﬁed during hospital stay or within 30 days following cesarean section by readmission to the hospital or by postdischarge survey using the cri-teria of the Centers for Disease Control and Prevention (CDC) NNIS System.7 The postdischarge survey was per-formed according to the modiﬁed methodology developed by Stockley et al.19 The patient received a questionnaire (Figure) to be given to the physician (ie, obstetrician or general practitioner) to complete if problems developed regarding the wound or if endometritis developed after discharge. All study subjects were contacted at home by telephone 30 to 35 days after surgery (including those patients who had been diagnosed as having SSI during admission). The patients were asked about their general health and the state of their surgical wound using a stan-dard format based on the physician’s questionnaire. If a patient’s complaints referred to a possible infection and the questionnaire had not been received, the investigator contacted the physician for verbal conﬁrmation of SSI or the medical chart was reviewed to determine whether the patient had attended the outpatient department for the treatment of SSI or had been admitted to the hospital. If it was not possible to contact the patient, the outpatient med-ical records of those patients who were known to have re-turned to Tartu University Women’s Clinic were reviewed. When the completed questionnaire arrived and the CDC criteria were met, no further contact with the physician was established.
All surveillance data were collected by a single inves-tigator. Demographic information, potential risk factors, and surgical indications were recorded. Host-related vari-ables included age, nationality, parity, existing comorbidi-ties (eg, diabetes, preeclampsia, anemia, or chorioamnion-itis), bacterial vaginosis during pregnancy, a preoperative condition assessed by American Society of Anesthesiolo-gists (ASA) score, number of prenatal care visits, duration of ruptured membranes, duration of labor, preoperative stay, length of hospital stay, use of internal fetal monitor-ing, and number of vaginal examinations prior to cesarean section at the hospital. Surgery-related variables included emergency nature of the operation, indications for cesar-ean section, duration of the operation, manual removal of the placenta, volume of blood loss, and antibiotic prophy-laxis. The study subjects were postoperatively monitored for temperature, SSI, wound and endocervical culture, and antibiotic treatment.
Inpatient surveillance (including gathering surveil-FIGURE. Questionnaire given to patients to deliver to their physician if
lance data and explaining the purpose of the study) took approximately 20 minutes per patient; telephone follow-up took an average of 3 to 5 minutes per patient.
According to the modiﬁed wound classiﬁcation, ce-sarean section deliveries were classiﬁed as follows: class I if there was no rupture of membranes or labor, class II if there was less than 2 hours of membrane rupture without labor or labor of any length with intact membranes, class III for rupture of membranes greater than 2 hours, and class IV for purulent amniotic ﬂuid.11,12 Currently practiced hos-pital policy for surgical antibiotic prophylaxis in Tartu Uni-versity Women’s Clinic recommends intravenous adminis-tration of 1 g of cefazolin as soon as the umbilical cord is clamped for all patients undergoing non-elective cesarean section and for patients undergoing elective cesarean sec-tion for rupture of membranes more than 4 hours or with bacterial vaginosis diagnosed during pregnancy. Elective cesarean section was deﬁned as a planned procedure and performed when scheduled (patient did not have active la-bor or rupture of membranes prior to surgery), whereas all other instances of cesarean section were deﬁned as emer-gency procedures.
All comparisons were unpaired, and all tests of signiﬁ-cance were two-tailed. For all categorical variables, Fisher’s exact test or chi-square was used. For continuous variables, Student’s t test was performed. Odds ratios (ORs) and 95% conﬁdence intervals (CI95) were calculated using standard methods. A P value of .05 or less was considered to indicate statistical signiﬁcance. Multiple logistic regression analysis was performed to obtain adjusted estimates of OR and to identify independent risk factors. Data were analyzed using Stata statistical software (version 8.0; StataCorp, College Station, TX).
There were 310 cesarean sections performed among 2,092 deliveries (14.8%; CI95, 13.3 to 16.4) during the study period. Three hundred ﬁve patients were enrolled in the study (4 patients refused to participate, and 1 patient died during the operation due to a complication of underlying disease, rupture of an aortic aneurysm). Among the study patients, there were 192 (63%) emergency and 113 (37%) elective cesarean sections performed. Indications for cesar-ean section are provided in Table 1.
During the study period, 19 SSIs were identiﬁed: 14 patients developed incisional (2 deep and 12 superﬁcial) infections, 4 developed endometritis, and 1 developed in-tra-abdominal abscess. The overall infection rate was 6.2% (CI95, 3.8 to 9.6). Of the 19 SSIs identiﬁed, 11 (57.9%) were diagnosed before and 8 (42.1%) after discharge. Of the lat-ter, 2 patients were readmitted to the hospital and 6 had SSIs that were detected by multi-method postdischarge surveillance.
During the postdischarge surveillance, 280 patients
were contacted by telephone. Fifteen of them described a possible infection but only 6 cases were ﬁnally conﬁrmed by the physician (4 with the questionnaire and 2 with personal contact). Information was obtained on chart review for 9 study subjects who could not be contacted by telephone nor from whom a completed questionnaire was received. No SSI was detected. In this study, 16 of the 305 eligible patients were not available for any infor-mation during the postdischarge period. A combination of healthcare worker questionnaires, telephone calls, and chart reviews gave a postdischarge follow-up rate of 94.8%.
Two patients were excluded from the study during risk factor analysis because SSI developed more than 30 days after their cesarean sections. The characteristics of the sample are given in Table 2. Variables such as national-ity, diabetes, preeclampsia, anemia, bacterial vaginosis dur-ing pregnancy, manual removal of the placenta, and volume of blood loss did not show signiﬁcant association between patients with and without SSI (data not shown). Univariate analysis identiﬁed that chorioamnionitis, duration of labor, internal fetal monitoring, and surgical wound classes III and IV were associated with SSI (Table 2). Multiple logistic regression analysis found three variables that were inde-pendently associated with increased risk for developing SSI: internal fetal monitoring (OR, 16.6; CI95, 2.2 to 125.8;
P = .007), chorioamnionitis (OR, 8.8; CI95, 1.1 to 69.6; P = .04), and surgical wound classes III and IV (OR, 3.8; CI95, 1.2 to 11.8; P = .02).
Analysis of the use of antibiotic prophylaxis re-vealed that 163 (84.9%) of the emergency cesarean sec-tion deliveries and 37 (32.7%) of the elective cesarean section deliveries received prophylaxis. Two hundred twenty-three (73.1%) of the patients had followed the guidelines according to the current policy for hospital antibiotic prophylaxis. Seventy-ﬁve patients received an-tibacterial treatment without any conﬁrmed diagnosis of infection after the operation.
Patients with SSI had a longer mean hospitalization
INDICATIONSFOR CESAREAN SECTION
No. of Patients (%)
Fetal distress 72 (23.6)
Breech and malpresentation 63 (20.7)
Cephalopelvic disproportion 41 (13.4) Previous delivery by cesarean section 39 (12.8)
Preeclampsia 25 (8.2)
Dystocia 13 (4.3)
Placenta previa, placenta increta, or placental abruption
Other* 40 (13.1)
Total 305 (100.0)
time than did noninfected patients (5.8 ± 0.3 vs 7.9 ± 1.5 days; P < .03).
To our knowledge, this is the ﬁrst extensive SSI surveillance study performed in Estonia. The main goals of our study were to evaluate a multi-method approach to postdischarge surveillance of SSI and to identify infection rates after cesarean section.
The overall SSI rate of 6.2% in our hospital is low-er than rates from othlow-er studies that have used postdis-charge surveillance. Rates have varied from 9.6% in Bra-zil9 to 17% in Australia.4 The comparison of our SSI rates with NNIS System benchmarks is not meaningful because postdischarge surveillance is not required by the NNIS System, but any comparison of SSI rates must take into account whether case-ﬁnding included the detection of SSI after discharge. Twelve percent to 84% of SSIs are detected after patients are discharged from the hospital.7 During postdischarge surveillance in our study, 42.1% of SSIs were detected; however, the numbers were relatively small and may therefore have been affected by a random error. The data suggest the necessity to perform postdis-charge surveillance to obtain more accurate SSI rates. Noy and Creedy4 recommended in their study that when the rate is being calculated, the number of responders, rather
than the number of the total sample, should be used. As in-creasingly more infections emerge after discharge and in cases of a low response rate, inclusion of nonresponders may lower the infection rate and produce inaccuracies when compared with other healthcare facilities. Thus, when these comparisons are being made, the denomina-tor has to be taken into consideration. In our study, the re-sponse rate was high and the exclusion of nonresponders from the denominator would not have changed the results signiﬁcantly (6.2% vs 6.6%).
However, the best way to conduct postdischarge surveillance is still a matter of dispute according to the literature. The ideal methodology should have a high fol-low-up rate, be cost-effective, and have high sensitivity and speciﬁcity.4,6-8,10 The follow-up rate in our study was 94.8%; in a study conducted by Stockley et al.,19 a combi-nation of different postdischarge surveillance methods gave a follow-up rate of 92.7%. In the study performed by Taylor et al.,20 patients were contacted only by telephone. The compliance rate was 93.3%, and it was concluded that this method of contact is feasible and effective. Stockley et al.19 found that the combination of different methods is relatively simple to use and causes minimal inconvenience to patients and healthcare workers. We agree with this be-cause most of the patients were interested in participating in the surveillance and because given that approximately
ANALYSISOF RISK FACTORSFOR SURGICAL-SITE INFECTIONS FOLLOWING CESAREAN SECTION
Mean ± SD or No. (%)
Risk Factor SSI (n = 19) No SSI (n = 284) OR CI95 P
Age, y 27.7 ± 6.5 28.5 ± 5.9 .59
Gestational age, wk 39.2 ± 2.6 38.6 ± 2.6 .38
Prenatal care visits 9.4 ± 2.2 9.6 ± 2.7 .75
Preoperative stay, d 1.2 ± 1.2 1.1 ± 1.7 .08
Vaginal examination 2.6 ± 1.7 1.9 ± 1.8 .06
Duration of labor, h 6.0 ± 8.5 2.8 ± 4.7 .008
Duration of ruptured membranes, h 10.5 ± 18.2 5.4 ± 21.2 .31
ASA score 1.3 ± 0.5 1.5 ± 0.8 .18
Duration of surgery, min 40.7 ± 6.8 40.6 ± 15.0 .97
Repeat cesarean section 4 (21) 62 (21) 0.95 0.32–2.85 1.00
Emergency 14 (74) 178 (63) 1.67 0.61–4.57 .46
Chorioamnionitis 2 (11) 2 (1) 16.58 2.75–100.29 .02
Nulliparity 11 (58) 133 (47) 1.56 0.63–3.89 .35
Internal fetal monitoring 2 (11) 3 (1) 11.02 1.72–70.43 .03
Absence of prophylaxis 7 (37) 96 (34) 1.14 0.44–2.99 .79
Surgical wound class* 12 (63) 84 (30) 4.08 1.55–10.73 .002
SD = standard deviation; SSI = surgical-site infection; OR = odds ratio; CI95 = 95% conﬁdence interval; ASA score = American Society of Anesthesiologists preoperative assessment score. *Contaminated or dirty.
65% of the population owns a mobile phone, the telephone questionnaire is a suitable method.21 The method we used is not very time consuming. It is also more acceptable to patients because only those who have a problematic wound area need to go to the hospital for checkups. The data collection was simpliﬁed by the fact that most of the women returned to our clinic for postdischarge care. The same applies to the physicians; only physicians whose patients have problems should take part in the study. In the study by Stockley et al.,19 the medical records of patients who could not be contacted by phone were not reviewed. In contrast, we performed chart reviews and re-ceived information regarding nine more patients, a meth-od also practiced by Noy and Creedy.4 The high response rate validates the effectiveness of this kind of surveillance method.
The literature suggests that direct observation of surgical sites by trained professionals (eg, infection con-trol practitioners) is the most accurate method to detect SSI.6,7 However, in our study this was not possible because we had to consider human and ﬁnancial resources allotted for SSI surveillance. It could be one of the reasons why our infection rate is lower than those from other studies. The validity of the information obtained from patients and physicians and whether the diagnosis of SSI can be based on this is a matter of dispute in several research studies. Seaman and Lammers22 found that patients, despite using verbal or printed instructions, were unable to recognize infections. They reported that patients correctly identi-ﬁed their infections in only 11 cases, whereas medical examiners diagnosed infection in 21 wounds, and called into question the validity of data obtained using patient-returned questionnaires or telephone surveys. A recent study,23 however, demonstrated that patients can accurate-ly diagnose the absence of a wound complication but are less accurate in diagnosing the presence of an infection. Patients frequently confuse serous discharge with pus and, therefore, this marker may overestimate infection rates. The results of the current study also support the latter because nine of the patients self-reported the SSIs, which were not conﬁrmed by a physician. Conﬁdence in the results should be improved by gathering information from patient records, microbiologic ﬁndings, and discus-sions with the physician. The current data were collected from several sources, and SSIs were always conﬁrmed by the physician. All of the SSI diagnoses were determined by the investigator to have met the CDC criteria.
Multi-method postdischarge surveillance has been described as cost-effective in several studies.4,19,20 The cur-rent study included the costs of labor, postage, and tele-phone calls. Sands et al.24 evaluated the use of automated ambulatory diagnosis, testing, and pharmacy code screen-ing combined with discharge diagnosis to identify SSI in non-obstetric patients undergoing surgery. They found that ambulatory code screening was a sensitive method for de-tecting patients with SSI. Yokoe et al.8 screened automated ambulatory medical records, hospital and emergency de-partment claims, and pharmacy records and found that this
method allows efﬁcient identiﬁcation of postpartum infec-tions not detected by conventional surveillance. Computer-ized systems could reduce the time and costs required to perform surveillance, but electronic medical records do not exist yet on a large scale in Estonia.
Studies have indicated that antibiotic exposure is a sensitive indicator of an infection because relatively few serious infections are managed without antibiotics. Poor speciﬁcity (too many false-positive results) has been a ma-jor problem because antibiotics are so widely used after sur-gery for extended prophylaxis, empiric therapy of suspect-ed infection, and treatment of infections other than SSI.10,25 In our study, 75 patients without any conﬁrmed infection diagnosis received antimicrobial treatment after cesarean section. Therefore, we cannot use therapy as an indicator of SSI. Inappropriate use of antimicrobial agents not only adds to the cost of medical care, but also needlessly exposes the patient to potential toxicity and risks that promote the de-velopment and spread of antimicrobial resistance in health-care facilities.26
Our postdischarge surveillance system was most suitable in the current circumstances.
The second aim of this study was to identify the risk factors that contribute to SSI following cesarean section. In contrast to the NNIS System results, age, ASA score, dura-tion of labor, and duradura-tion of surgery were not signiﬁcant risk factors in our study sample.17 The average age of the patients in the infected group was younger than that of the noninfected group, but not signiﬁcantly younger. However, our rate estimates could have been affected by a random er-ror caused by the small number of infections observed. The multiple logistic regression revealed three variables inde-pendently associated with post-cesarean SSI. Other studies have also reported a contaminated or dirty operation as a risk factor.17,27 Internal fetal monitoring and chorioamnion-itis, although they occurred in only a few cases, appeared to predispose women strongly to SSI. A challenge exists to de-crease the frequency of internal fetal monitoring and treat chorioamnionitis as soon as possible.
There were no signiﬁcant differences regarding infec-tions between elective and non-elective groups or between those receiving and not receiving appropriate antibiotic phylaxis. A Cochrane Review from 2002 recommends pro-phylactic antibiotics to all women undergoing cesarean sec-tion.1 According to our current hospital policy, antibiotics should be given to only high-risk groups. Because for 73% of the patients our current hospital antibiotic prophylaxis policy was followed, we cannot conclude whether selective prophylactics is a better alternative than routine prophylac-tics. The results of this study indicate the need for interven-tion to improve the rainterven-tional use of antibiotic prophylaxis in consonance with the hospital guidelines.
It has been proved in several studies that a signiﬁcant increase in hospital stay occurs when a patient acquires SSI.13,19 A signiﬁcantly longer hospital stay also occurred in the current study once SSI was identiﬁed.
Healthcare-associated infection control is a relatively new ﬁeld in Estonia, and we have to develop a surveillance
system and propose a control strategy for nosocomial infec-tions. The baseline quantiﬁcation of nosocomial infection rates and their comparisons with external rates enable hos-pitals to direct infection surveillance and control programs. The next step in our hospital would be to inform physicians about the results and set up further follow-up of SSIs. As greater efforts are made to quantify and describe the char-acteristics of healthcare-associated infections in Estonia, active surveillance, application of prevention interventions, and judicious antimicrobial use should greatly improve patient outcomes.
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