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Infection Prevention in Practice logoLink to Infection Prevention in Practice
. 2020 Sep 9;2(4):100090. doi: 10.1016/j.infpip.2020.100090

Overview of risk factor and bacterial pattern in patient with surgical site infection after caesarean section in Ciptomangunkusumo Hospital from 2016 to 2018

Achmad Kemal Harzif a, Muhammad Dwi Wicaksono a, Annissa Kallista a,, Malvin Emeraldi b, Gita Pratama a
PMCID: PMC8336288  PMID: 34368724

Summary

Background

Caesarean section is one of the most commonly performed surgeries both in the hospital. The incidence of infections in cesarean section varies greatly around the world at 3–15%. SSI on is a multifactorial process that starts from the perioperative preparation, the patient, the type of surgery, the type of germ and other factors.

Aims

To determine the characteristics of patients, bacterial patterns, and risk factors for the incidence of SSI in Cipto Mangunkusumo National General Hospital in 2016–2018.

Method

This study was an observational study using a retrospective cohort method. The subject of this study were patients undergoing cesarean section in Cipto Mangunkusumo National General Hospital in 2016–2018 recruited using consecutive sampling method. Based on the data obtained, bivariate and multivariate analysis were conducted to determine the factors affecting post-caesarean SSI.

Results

A total of 2052 subjects were included in the study. There were 85 cases of surgical site infection (SSI) out of 2052 operations (4.14 %). A total of 85 SSI cases and 1967 control groups were included in the risk factor analysis. The most common bacteria found in surgical site infection culture were Staphylococcus aureus (16,5%), Klebsiella pneumoniae (12,9%), Escherichia coli (9,4%), Enterococcus faecalis (9,4%), and others (21,2%). Variables associated with SSI in this study is fetal distress (p=0,002; AOR = 2,265 CI 95 % 1,350–3,801) and BMI ≥30 kg/m2 (p=0,028; AOR 1,824 CI 95% 1,066–3,121).

Conclusion

Factors influencing the incidence of SSI post cesarean section was fetal distress (p=0,002; AOR = 2,265 CI 95 % 1,350–3,801) and BMI ≥30 kg/m2 (p=0,028; AOR 1,824 CI 95% 1,066–3,121).

Keywords: Surgical site infection, c-section, Bacterial pattern

Background

Cesarean section is one of the most frequent actions performed in the field of obstetrics within a hospital and may continue given the high incidence of cesarean section. In the last thirteen years the incidence of cesarean section has risen to 41% [1]. This is a global phenomenon, as cesarean section is now performed on 32% of total births in the United States, which concludes about 1.3 million operations yearly, while in the UK and Australia the number of cesarean section operation reached 26.5% and 32.3%. Furthermore, data in Indonesia showed that the number of cesarean sections in 2012 was 15.3% [1,2]. Like any other operation, cesarean section may be followed by various complications, one of which a surgical site infection (SSI) [1] (Figure 1).

Figure 1.

Figure 1

Research Flow.

Several risk factors associated with the occurrence of surgical site infection after cesarean section have been identified. The identification of these factors plays an important role in determining the methods that can be used to reduce the risk of SSI. Risk factors can be divided into three categories. 1) factors related to host, 2) factors related to pregnancy and intrapartum and 3) factors related to surgery [2].

Factors related to the host include too old or too young maternal age, obesity, living in rural areas (compared to living in urban area), gestational diabetes mellitus, history of previous cesarean section, recurrent miscarriage, preoperative maternal conditions (American Society of Anesthesiologist (ASA) score >3) [[2], [3], [4]]. While factors related to pregnancy include hypertension, gestational diabetes, multiple pregnancies, premature rupture of membranes, greater number of internal examinations, prolonged parturition of the trial before surgery, use of epidural anesthetics, use of internal fetal monitoring, and chorioamnionitis [4]. Meanwhile, factors related to cesarean section itself are emergency surgeries, no antibiotic prophylaxis, cases related to uterine rupture, cesarean section with hysterectomy, need for transfusion, and longer operative time. Operating time of more than 1 hour is associated with up to two times the risk of SSI [5].

Various studies have been performed in order to determine factors affecting the rate of surgical site infection in post caesarean patients. However, few of the studies were performed in a tertiary care hospital, which has more severe cases and therefore complications. In order to reduce the rate of surgical site infection in caesarean section patients, a study investigating the risk factors was performed.

Methods

An analytic observational study using cohort retrospective method was done. The population were all women undergoing caesarean section within the course of the study. In the study period, a sample of 2,052 women undergoing caesarean section were included. Patients with an incomplete medical record, not attending postnatal care, or died within 30 days of birth were excluded from the study. The data were then analyzed by two groups (surgical site infection group vs. control group). Ethical clearance was issued from ethical committee in Faculty of Medicine, Universitas Indonesia with ethical clearance number of 19/06/0736.

Results and discussion

In this study, there were 85 cases of surgical site infections (SSI) out of 2052 surgeries (4.14%) (Table 1). This figure is not much different from the results of similar studies in Israel with a percentage of 3.7% SSI and in North America with a percentage of 2.7% [4,6]. This figure is lower than similar studies conducted in other Southeast Asia countries such as Thailand which had a rate of 5.9% [7]. Previous research shows that the post caesarean SSI rate in developed countries ranges from 1.5% - 7.0% while the rate for developing countries is about 6% [6,8].

Table 1.

Baseline characteristics of subjects

Variables N = 2052
Maternal Age 30 (13–47)
Gestational age
 Preterm 1.159 (56,5%)
 Term 893 (43,5%)
Gravid
 Primigravid 702 (34,2%)
 Multigravid 1.350 (65,8%)
Parity
 Primiparous 809 (39,4%)
 Multiparous 1.243 (60,6%)
Abortion history
 Yes 446 (21,7%)
 No 1606 (78,3%)
Operation type
 Elective 183 (9,0%)
 Emergency 1867 (91,0%)
Previous Caesarean Section history
 Yes 560 (27,3%)
 No 1492 (72,7%)
Body mass index 25,28 (16,89–50,59)
Hemoglobin level 11,7 (6,4–17,7)
Premature Rupture of Membrane (PROM)
 Yes 771 (37,6%)
 No 1281 (62,4%)
Gestational Hypertension
 Yes 682 (33,2%)
 No 1370 (66,8%)
Fetal distress
 Yes 397 (19,3%)
 No 1655 (80,7%)
Antepartum hemorrhage
 Yes 143 (7%)
 No 1909 (93%)
Dystocia
 Yes 75 (3,7%)
 No 1977 (96,3%)
Diabetes mellitus
 Yes 71 (4,0%)
 No 1724 (96%)
Intrauterine infection
 Yes 141 (6,9%)
 No 1911 (93,1%)
HIV
 Yes 41 (2,0%)
 No 2011 (98%)
Glucose blood level 105,8 (43,99)
Leucocyte level 14.197 (13.110)
Serum albumin level 4,01 (6,75)

Samples for culture in this study were taken from the wound base, discharge, or lochia. However, cultures that were considered representative of SSI were cultures that taken from the wound base, but not all patients had samples taken for bacterial culture in this study, due to the financial cost, for some patients. The bacteria most often found in this study were Staphylococcus aureus (16.5%), followed by Klebsiella pneumoniae (12.9%), Escherichia coli (9.4%), Enterococcus faecalis (9.4%), and other pathogens like Streptococcus epidermidis and Acinetobacter baumanii (Table 2).

Table 2.

Characteristics of SSI

Characteristics N = 85
SSI classification
 Incisional superficial 79 (92,9%)
 Incisional deep 4 (4,7%)
 Organ/space 2 (2,4%)
Culture result
 Klebsiella pneumoniae ss. Pneumoniae 11 (12,9%)
 Escherichia coli 8 (9,4%)
 Enterococcus faecalis 8 (9,4%)
 Pseudomonas sp. 2 (2,4%)
 Staphylococcus aureus 14 (16,5%)
 Others 18 (21,2%)
 Sterile 6 (7,1%)
Treatment
 Wound care 65 (76,5%)
 Re-operation 20 (23,5%)

Culture results of this study were consistent with similar studies such as a study in Tanzania showing that Staphylococcus aureus as one of the most common bacterium causing SSI in post-caesarean patients, and particular superficial infections [2,9]. In addition, the study found that S. aureus in post cesarean section SSI cultures were resistant to ampicillin, co-trimoxazole, and erythromycin. In this study antibiotic resistance tests were not included in the study. In addition, the results showed that Klebsiella pneumoniae was the second most prevalent bacteria in SSI post cesarean section, especially in internal and organ infections [9]. In research conducted in Israel, Escherichia coli is one of the organisms that are often found in post caesarean SSI [2]. In another study in Tanzania, E. coli obtained from the post-Caesarean SSI culture had high resistance to ampicillin, a combination of amoxicillin/clavulanate, tetracycline, and co-trimoxazole [9].

Besides the normal flora of the skin, vagina, and the gastrointestinal tract, there are bacteria that originate from opportunistic bacteria originating from hospital-caused infections (HCAI/Healthcare Associated Infection), namely Acinetobacter spp. In this study, it was found that 8 (9.41%) research subjects having Acinetobacter sp in cultures. Acinetobacter spp. is recognized to be a nosocomial pathogen found in healthcare enviroments, often causing hospital-acquired pneumonia (HAP) with associated significant resistance to antibiotics [10].

In the patients with SSI, 65 cases (76.5%) were treated with standard wound care, while 20 other cases needed re-operation (23.5%). SSI is generally considered as one of the causes of prolongation of the duration of postoperative hospitalization and additional costs for patients with various types of surgery, including cesarean section [11]. Uniquely, a study in the UK shows that the stitching method used in caesarean section affects the rate of SSI, with the smallest percentage of SSI occuring in subcuticular sutures and the largest percentage obtained in interrupted sutures [12].

In this study, high body mass index (BMI), BMI ≥ 30 kg/m2 was associated with increased risk of SSI (p = 0.028; OR 1.824 CI95% 1.066–3.121) (Table 3, Table 4). This is consistent with previous studies in the UK where BMI >30 kg/m2 was known as a risk factor for complications in surgery [13]. Obesity as a risk factor for SSI is due to an increase in relatively avascular adipose tissue, increase in the area of the surgical wound and reduced prophylactic antibiotic penetration into the adipose tissue [14].

Table 3.

Bivariate analysis of SSI risk factors

Variables Study groups
P OR CI 95%
SSI (n=85) Control (n=1967)
Age 29 (17–43) 30 (17–49) 0,240
Gravid 2 (1–6) 2 (0–12) 0,839
Parity 1 (0–4) 1 (0–10) 0,887
Abortion history 0 (0–3) 0 (0–10) 0,212
Gestational age 0,635 1,86 1,19–2,9
 Preterm 49 (57,6%) 858 (43,6%)
 Term 34 (42,4%) 1110 (56,4%)
Maternal age 0,428 0,81 0,481–1,365
 < 35 64 (77,1%) 1441 (73,1%)
 ≥ 35 19 (22,9% 528 (26,9%)
Operation type 0,816 1,092 0,518–2,302
 Emergency 75 (90,6%) 1792 (91,1%)
 Elective 8 (9,4%) 75 (8,9%)
History of diabetes 0,173 1,90 0,74–4,88
 Yes 5 (7,1%) 66 (3,4%)
 No 66 (92,9%) 1658 (96,6%)
Hemoglobin level 11,6 ± 1,88 11,5 ± 1,87 0,836
 Hb < 11 g/dL 28 (36,5%) 721 (36,7%) 0,644 0,89 0,56–1,43
 Hb ≥ 11 g/dL 54 (63,5%) 1246 (63,3%)
PROM 0,461 0,84 0,52–1,33
 Yes 28 (35,3%) 743 (37,7%)
 No 55 (64,7%) 1226 (62,3%)
Hypertension 0,417 1,20 0,76–1,90
 Yes 31 (38,8%) 651 (33,0%)
 No 52 (61,2%) 1318 (67,0%)
Fetal distress 0,001 2,09 1,3-3,33
 Yes 28 (32,9%) 369 (18,7%)
 No 55 (64,7%) 1600 (81,3%)
Intrauterine infection 0,822 1,08 0,46–2,53
 Yes 6 (11,8%) 135 (7,3%)
 No 75 (88,2%) 1823 (92,7%)
History of previous CS 0,930 6,95 4,2–11,4
 Yes 23 (29,42%) 537 (27,2%)
 No 60 (70,58%) 1432 (72,8%)
Antepartum hemorrhage 0,513 0,97 0,44–2,15
 Yes 7 (8,2%) 136 (6,9%)
 No 76 (91,8%) 1833 (95,1%)
Dystocia 0,543 1,35 0,48–3,80
 Yes 4 (4,7%) 71 (3,5%)
 No 79 (95,3%) 1898 (96,5%)
HIV history 1,000 0,59 0,07–4,33
 Yes 1 (1,1%) 40 (2,0%)
 No 82 (98,9%) 1929 (98,0%)
Additional operation 0,04 1,97 1,019–3,792
 Yes 11 142
 No 72 1827
BMI ≥ 30 0,035 1,767 1,035–3,017
 Yes 48 (70,6%) 343 (19,1%)
 No 20 (29,4% 1455 (80,9%)

Significance P<0,005.

PROM = premature rupture of membrane, CS = caesarean section, HIV = human immunodeficiency virus.

Table 4.

Risk factors of SSI

Variables P Value OR CI 95%
Fetal distress 0,002 2,265 1,350–3,801
BMI ≥ 30 kg/m2 0,028 1,824 1,066–3,121

Significance P<0,005.

Fetal distress was also considered to be one of the risk factors for SSI events in postoperative caesarean patients (p= 0.001, OR = 2.09, CI95% 1.3–3.33) (Table 4). Fetal distress is one of the indications of a cesarean section, in fact it is one of the three most frequent reasons for cesarean section [6]. One study that showed fetal distress as a risk factor for SSI was carried out by Moulton and colleagues [15]. Caesarean section due to fetal distress as a risk factor for SSI have not been widely discussed in other studies. One possible reason is the lack of optimal preparation of caesarean section in cases of fetal distress, but this requires further research.

Conclusions

This study found that the variables that played a role in the incidence of SSI were caesarean section due to fetal distress and BMI ≥ 30 kg/m2. Other variables, although clinically significant, are not considered to have statistical significance. The incidence of surgical site infection after caesarean section in this study was 4.14%.

Ethics approval and consent to participate

This study was acknowledged by Ethical Committee for Medical Research of Faculty of Medicine, University of Indonesia.

Conflict of interest statement

None declared.

Authors' contributions

MDW extracted, analyzed, and interpreted the data. AKH analyzed the data and interpreted the results. Both authors wrote, read and approved the final manuscript.

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