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Original Article
76 (
3
); 122-128
doi:
10.25259/IJMS_268_2023

Clinico-microbiological evaluation of post-cesarean surgical site infections

Department of Obstetrics and Gynaecology, Government Medical College, Patiala, Punjab, India
Department of Obstetrics and Gynaecology, Government Medical College and Hospital, Chandigarh, India.
Department of Microbiology, Government Medical College and Hospital, Chandigarh, India.

*Corresponding author: Kangan, Department of Obstetrics and Gynaecology, Government Medical College, Patiala, Punjab, India. drkangan@gmail.com

Licence
This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.

How to cite this article: Kangan, Mehra R, Gupta V, Goel P, Kaur M. Clinico-microbiological evaluation of post-cesarean surgical site infections. Indian J Med Sci. 2024;76:122-8. doi: 10.25259/IJMS_268_2023

Abstract

Objectives:

With increasing rates of cesarean section (CS), the incidence of post-operative complications is bound to increase, which includes surgical site infections (SSIs), being one of the common and distressing complication. This study was aimed to evaluate the various determinants of post-CS SSI, their clinical spectrum, prevalent microbiology, and their susceptibility and resistance patterns.

Materials and Methods:

This was a prospective longitudinal hospital-based study undertaken in Government Medical College and Hospital (GMCH), Chandigarh. Six hundred and eighty-eight patients were included from April, 2021, to September, 2022, and were followed up till 42nd day post-procedure.

Results:

The incidence of SSI in the study was 3.49%. The risk factors identified were gestational diabetes mellitus (GDM), thrombocytopenia, chorioamnionitis, prolonged labor, multiple per vaginum examinations, prolonged surgery, post-partum hemorrhage, and blood and blood product transfusions. Most patients presented on or after day 8 of surgery with discharge from the wound site being the most common presentation. Staphylococcus aureus emerged as the most prevalent organism and out of five patients having S. aureus, three had methicillin-resistant S. aureus. Linezolid was found to be the most susceptible antibiotic, whereas ciprofloxacin was mostly resistant among the prevalent isolates.

Conclusion:

Some of these determinants are modifiable such as GDM and thrombocytopenia and if detected and managed early may help in reducing the risk of developing SSI. Linezolid must be used empirically for treatment of SSI until the reporting of culture and sensitivity is done because routine antibiotics used for antibiotic prophylaxis in CS were found to be highly resistant. Periodic analysis of clinical spectrum and culture and sensitivity patterns is imperative for the early diagnosis and appropriate empirical management of SSI.

Keywords

Cesarean section
Surgical site infections
Risk factors
Staphylococcus aureus
Linezolid

INTRODUCTION

Cesarean section (CS) is a widely performed procedure in modern obstetrics aimed at enhancing maternal and neonatal outcomes when vaginal delivery is deemed risky or unfeasible. Despite its intended purpose, the global surge in CS rates, particularly in India, has raised concerns.[1] The World Health Organization suggests an optimal CS rate of 10–15%, yet India’s rates escalated from 8.5% in 2005–2006 to 21.5% in 2019–2021, as reported by the National Health Systems Resource Center (NHSN).[1-3] The escalating CS rates bring about an inevitable rise in post-operative complications, notably surgical site infections (SSIs), contributing to maternal morbidity, mortality, psychological distress, extended hospital stays, increased treatment costs, and strain on health-care facilities.[4]

Various risk factors contribute to the occurrence of SSI, encompassing maternal pre-existing comorbidities, obstetrical factors (parity, preterm rupture of membranes, prolonged labor, meconium-stained liquor, chorioamnionitis, gestational diabetes mellitus [GDM], anemia, previous CS, excessive vaginal manipulation), socioeconomic status, and illiteracy. Factors such as the type of ward, emergency or elective procedures, type of anesthesia, abdominal incision type, and overall procedure duration also impact SSI rates. Low socioeconomic status and illiteracy heighten infection risks due to overcrowded living conditions and lack of awareness regarding surgical site care.

SSI, occurring within 30 days post-CS, is categorized by the Centers for Disease Control and Prevention (CDC) into superficial incisional SSI, deep incisional SSI, and organ/space infections. It manifest with symptoms such as purulent discharge, pain, erythema, induration, local temperature elevation, and fever.[5] Common pathogens associated with SSI include Staphylococci, Streptococci, Enterococci, Lactobacilli, Diphtheroid, Escherichia coli, Anaerobic Streptococci, Bacteroides, and Fusobacterium species depending on the factors responsible for infection and prevalence of microbes in a particular health-care facility or area.[6,7]

The consequences of SSI extend beyond immediate health implications, encompassing indirect costs such as loss of productivity, patient dissatisfaction, litigation, and diminished quality of life. Preventing SSI involves addressing predisposing risk factors and understanding the microbial spectrum and antibiotic sensitivity in a healthcare setting, thereby improving prognosis and reducing morbidity associated with CS.

MATERIALS AND METHODS

This study was a prospective longitudinal hospital-based study that aimed to calculate the incidence of SSIs after CSs and evaluate the various determinants of post-CS SSI, their clinical spectrum, prevalent microbiology, and their susceptibility and resistance patterns. The study was conducted in the Department of Obstetrics and Gynecology in collaboration with the Department of Microbiology at Government Medical College and Hospital (GMCH) sector-32, Chandigarh. Optimum sample size was calculated on the basis of 7% incidence of SSI after CSs.[6] Assuming 95% confidence level and 10% precision, the sample size came out to be 385. We planned to take at least 385 subjects who complete the follow-up at 6 weeks. The study lasted 18 months from April 2021 to September 2022. Seven hundred patients were enrolled, out of which 688 patients completed the follow-up. The condition of their surgical scar/wound was assessed. The inclusion criteria for the study were patients undergoing CS at GMCH, who gave consent for the study and follow-up and SSI occurring within 42 days of CS.

The exclusion criteria were patients undergoing CS outside GMCH, patients having uterine rupture, patients undergoing peripartum hysterectomy, immunocompromised patients, and patients who refused to give consent for the study and follow-up.

Factors such as age, parity, background, socioeconomic status, education level, preterm rupture of membranes, prolonged labor, GDM, overt diabetes mellitus, anemia, previous CS, multiple vaginal examinations, emergency or elective case, post-partum hemorrhage, type of anesthesia, type of abdominal incision, meconium staining of liquor, chorioamnionitis, duration of surgery, malnutrition, obesity, hypertension, and any chronic disorders were noted. The surgical wound was examined at the time of first dressing, at 8–12 days post-cesarean, as and when required, and on day 42 of CS. Diagnosis of SSI was made according to the CDC standards, which involve infection that occurs within 30 days (extended to 42 days for this study).[5] After taking the wound swabs, where indicated, patients were treated according to ideal standard of care, which involved antibiotics, dressings, debridement, resuturing, readmission, etc. Swabs were sent for culture and sensitivity to microbiology laboratory. Isolation and susceptibility testing of culture isolates was done in our clinical microbiology laboratory using standard methods.[8] Antimicrobial susceptibility of culture isolates was done using Kirby-Bauer’s disk diffusion method according to recent Clinical and Laboratory Standards Institute (CLSI) guidelines.[9]

RESULTS

A total of 700 post-CS patients were enrolled out of which ten patients lost to follow-up and two patients expired. Hence, 688 patients were studied and follow-up was done till 42 days after CS. Twenty-four patients developed SSI making the incidence to be 3.49%. Various determinants of post-CS SSIs were studied. GDM and thrombocytopenia were among the maternal factors which had significant association with SSI. Maternal obstetric factors such as chorioamnionitis, prolonged labor, and multiple per vaginum examinations also significantly increased the risk of SSI. Prolonged surgery, post-partum hemorrhage, and blood product transfusions also were major risk factors for developing SSI. The following table depicts various determinants studied and their association with the risk of developing post-cesarean SSI [Table 1]. Mean time of detection of SSI was 11.75 ± 3.232 day. Out of 24 patients, 18 had purulent discharge whereas four had serous discharge. Fifteen patients had pain and tenderness, eight had induration and swelling, five were febrile, and two developed erythema. Only six patients developed dehiscence of wound, as evident [Table 2]. Twenty-two out of 24 were superficial SSI, whereas two patients had deep SSI.

Table 1: Various risk factors associated with SSI.
Variables Categories Post-CS SSI P-value Odds ratio
Yes No
Age group (years) ≤20 3 47 >0.05
21–25 6 230
26–30 7 236
31–35 6 116
>35 2 35
Socioeconomic status Lower 2 47 >0.05
Upper lower 2 112
Lower middle 9 284
Upper middle 9 179
Upper 2 42
Background Rural 13 341 >0.05 1.119, (95% CI, 0.494–2.535)
Urban 11 323
Education Illiterate 4 102 >0.05
Undergraduate 11 405
Graduate and above 9 157
BMI Underweight 1 4 >0.05
Normal weight 2 175
Overweight 6 193
Obese I 13 246
Obese II 2 46
Obese Yes 15 292 >0.05 2.1233, (95% CI 0.9162–4.9208)
No 9 372
Anemia Yes 6 249 >0.05 0.5556, (95% CI 0.2176–1.4183)
No 18 415
GDM Yes 5 44 <0.05 3.708, (95% CI 1.3218–10.4024)
No 19 620
Hypertensive disorders of pregnancy Gestational hypertension 0 56 >0.05
Preeclampsia 8 150
HELLP syndrome 1 4
Eclampsia 0 13
Thrombocytopenia (platelet count <1 lakh per µL) Yes 7 70 <0.05 3.494, (95% CI 1.4003–8.7188)
No 17 594
Parity Multiparous 11 346 >0.05 0.7778, (955 C1 0.3435–1.7609)
Primiparous 13 318
Previous history of CS Yes 5 227 >0.05 0.5066, (95% CI 0.1867–1.3745)
No 19 437
Past history of tuberculosis Yes 0 4 >0.05
No 24 660
Overt diabetes Yes 0 22 >0.05
No 24 642
Chronic hypertension Yes 1 26 >0.05 1.0669, (95% CI 0.1387–8.2066)
No 23 638
Thyroid disorders Yes 3 49 >0.05 1.7930, (95% CI 0.5167–6.2222)
No 21 615
Bronchial asthma Yes 1 3 >0.05 9.5797, (95% CI 0.9594–95.6531)
No 23 661
POG <32 weeks 3 41 >0.05
32–36+6 weeks 8 257
More than 37 weeks 13 366
CS done in labor Yes 14 355 >0.05 1.2186, (95% CI 0.5336–2.7827)
No 10 309
Prolonged labor Yes 7 71 <0.05 3.4391, (95% CI 1.3788–8.5779)
No 7 593
Multiple per vaginum examinations No 6 66 <0.05 3.02, (95% CI 1.1584–7.8744)
Yes 18 598
Duration of rupture of membranes Not ruptured 9 361 >0.05
<24 h 13 258
>24 h 2 45
PPROM Yes 3 114 >0.05 0.6892, (95 % CI 0.2022–2.3496)
No 21 550
MSL Yes 9 183 >0.05 1.5770, (95% CI 0.6783–3.6668)
No 15 481
Chorioamnionitis Yes 2 7 <0.05 8.5325, (95% CI 1.6753–43.4574)
No 22 657
Place of hospital stay General ward 19 627 >0.05 0.2242, (95% CI 0.0793–0.6341)
Private ward 5 37
Emergency versus elective CS Elective 5 58 >0.05 0.3637, 95% CI 0.1310–1.0099
Emergency 19 606
Type of abdominal incision Transverse 21 642 >0.05 4.168, (95% CI 1.1565–15.0270)
Vertical 3 22
Prolonged surgery >2 h 3 19 <0.05 4.8647, (95% CI 1.3352–17.7236)
<2 h 21 647
Type of anesthesia General 6 105 >0.05 1.7746, (95% CI 0.6883–4.5757)
Spinal 18 559
Post-partum hemorrhage Yes 6 62 <0.05 3.237, (95% CI 1.2390–8.4548)
No 18 602
Blood and blood products transfusion Yes 9 137 <0.05 2.308, (95% CI 0.9889–5.3866)
No 15 527
Time of start of antibiotics 30–60 min before 22 633 >0.05 1.856, (95% CI 0.4176–8.2513)
>60 min before 2 31
Ampicillin versus Ceftriaxone Ampicillin 18 394 >0.05 2.056, (95% CI 0.806–5.246)
Ceftriaxone 6 270

SSI: Surgical site infection, CS: Cesarean section, BMI: Body mass index, GDM: Gestational diabetes mellitus, CI: Confidence interval, POG: Period of gestation, PPROM: Preterm prelabor rupture of membranes, MSL: Meconium stained liquor, HELLP: Hemolysis, elevated liver enzymes, low platelet count

Table 2: Signs and symptoms of SSI.
Signs and symptoms Number of patients Percentage
Fever 5 20.83
Wound dehiscence 6 25.00
Tenderness and pain 15 62.50
Purulent discharge 18 75.00
Serous discharge 4 16.67
Induration and swelling 8 33.33
Erythema 2 8.33

SSI: Surgical site infection

Culture report

All wound swabs were subjected to antimicrobial susceptibility testing using Kirby-Bauer’s disk diffusion method according to recent CLSI guidelines wherein antibiotic panel checked was according to the kind of organism being cultured, so all organisms were not checked for similar antibiotics.[9] Eighteen organisms were isolated from wound swab. Six swabs were sterile. Out of 18, five were Staphylococcus aureus, four other Staphylococcus species, four E. coli, two Klebsiella pneumoniae, one Acinetobacter, one Citrobacter koseri, and one Enterococcus faecium. Moreover, out of five patients having S. aureus, three had methicillin resistant S. aureus [Table 3].

Table 3: Cultured isolates from wound swabs.
Culture report Number of isolates Percentage
Staphylococcus aureus 5 20.83
Acinetobacter 1 4.17
Citrobacter koseri 1 4.17
Enterococcus faecium 1 4.17
Escherichia coli 4 16.67
Klebsiella pneumoniae 2 8.33
Other Staphylococcus species 4 16.67
Sterile 6 25.00
Total 24 100

Antimicrobial susceptibility and resistance pattern

All wound swabs were subjected to antimicrobial susceptibility testing using Kirby-Bauer’s disk diffusion method according to recent CLSI guidelines wherein antibiotic panel checked was according to the kind of organism being cultured, so all organisms were not checked for similar antibiotics. Antimicrobial susceptibility and resistance among various isolates is shown in following [Table 4].

Table 4: Antimicrobial sensitivity of the cultures isolates.
Penicillin Ampicillin Erythromycin Clindamycin Doxycycline Ciprofloxacin Gentamycin Amikacin Tobramycin Ceftazidime Cefepime Sulbactam-Ampicillin Tazobactam-Piperacillin Imipenem Cefoxitin Tetracycline Cefotaxime Vancomycin Linezolid Cotrimoxazole
Staphylococcus aureus
  S 0 2 3 3 0 0 2 5 0
  R 5 3 2 2 1 1 3 0 1
Staphylococcus other
  S 3 1 2 4 0 0 4 4 1
  R 1 3 2 0 2 2 0 0 1
Escherichia coli
  S 1 3 1 0 3 1 0 1
  R 3 1 3 4 1 3 4 3
Klebsiella pneumonia
  S 0 2 0 0 1 2 0 0
  R 2 0 2 2 1 0 2 1
Acinetobacter
  S 0 0 0 0 0 0 0 0 0 1 0 0
  R 1 0 1 1 1 0 1 1 1 0 0 0
Enterococcus faecium
  S 0 0 0 0 0 0 0 1 1
  R 1 1 1 1 1 1 1 0 0
Citrobacter koseri
  S 1 1 1 1 1 1 1 0
  R 0 0 0 0 0 0 0 0

S: Sensitive, R: Resistant

DISCUSSION

The incidence of SSI in the study was 3.49% in 688 post-CS patients and it was found to be lower than some past studies due to the strict antibiotic policy and asepsis in the operation theatre of the tertiary care center where the study was conducted. The incidence of SSI has also decreased over the past decade as per the literature review.[6,7,10-12]

The study found that maternal medical factors such as obesity, GDM, and thrombocytopenia were associated with a higher risk of SSI, but the association with obesity was not statistically significant. The study did not find any association of SSI with hypertension, pre-existing medical illnesses, or anemia. The conflicting relationship with anemia could be explained by sufficient availability of blood and blood components and adequate build-up of patients in the preoperative period, which improves the general condition of the patient, and also good antibiotic coverage, which reduces the rate of bacterial proliferation. Maternal obstetric determinants such as preterm CS, previous CS, preterm pre-labor rupture of membranes, duration of rupture of membranes, and meconium-stained liquor have been found to increase the incidence of SSI as shown by Gomaa et al. but this study did not find any such correlation.[13] Chorioamnionitis emerged as a significant risk factor with 8.5 times increased risk of developing SSI. The study also found that patients with prolonged labor (>12 h duration) and multiple per vaginum (PV) examinations (≥5) had significantly higher risk of SSI. Surgery and anesthesia related factors such as use of general anesthesia, emergency procedures compared to electives, vertical skin incision, and general ward stay have been found to increase the risk of developing SSI in other studies, but this study did not find any significant association of rates of infection with these factors.[10,14] Patients with duration of surgery more than 2 h had significant increase in risk of developing SSI. The study also found that patients with post-partum hemorrhage had 3.237 times higher incidence of SSI. The study also evaluated the impact of blood transfusion and antibiotic prophylaxis on the incidence of SSI. Patients who received transfusions were found to have a 2.308 times increased risk of developing SSI, which was statistically significant. Whereas, no significant difference in incidence of SSI was found between the patients receiving antibiotics within or before 60 min of incision.

Clinical spectrum

The study found that the mean time of detection of SSI was 11.75 days and majority of the cases were diagnosed post-removal of sutures. Superficial incisional SSI was more frequent than deep incisional SSI. The most common symptom among patients with SSI was discharge from cesarean site and pain and tenderness were the second most common presentation. SSI increased the duration of hospital stay and some patients even required readmission, daily dressing, prolonged intravenous antibiotics, and re-suturing of the wound. Despite all the morbidity and burden caused by SSI, 100% survival and cure rates were observed.

Antibiotic spectrum

The most frequent isolate was S. aureus, followed by other Staphylococcal species and E. coli. The study found that linezolid had maximum susceptibility among isolates from patients developing post-CS SSI at GMCH, Chandigarh. Ten out of ten isolates tested for linezolid were susceptible to it. It was followed by doxycycline in seven patients but it is not recommended for use in post-partum patients during lactation.[10] Isolates were found to be resistant to ciprofloxacin, making it the most resistant antimicrobial. The study concluded that further studies are warranted to analyze the associated and especially modifiable risk factors and effect of thrombocytopenia on the risk of SSI as we were not able to find similar findings in literature available from the past few years. It is crucial to identify and modify the risk factors before they are able to impact maternal health negatively. Periodic analysis of the clinical spectrum of SSI and its microbial prevalence with antimicrobial sensitivity patterns is imperative for prompt diagnosis, appropriate empirical management and decelerating the emerging antimicrobial resistance.

CONCLUSION

Post-caesarean surgical site infections (SSI) present a significant challenge, with this study pinpointing risks such as gestational diabetes and thrombocytopenia, etc. Despite GMCH’s tertiary care status, a 3.49% SSI incidence is attributed to a comprehensive treatment approach. Staphylococcus aureus prevails, and linezolid is suggested as empirical treatment pending culture results. Continued research should prioritize identifying and modifying risk factors for improved maternal health, stressing routine analysis for timely diagnosis and effective SSI management.

Acknowledgments

The authors would like to thank almighty god for the blessings, the respected professors and patients for giving support in conducting this study.

Ethical approval

The research/study approved by the Institutional Review Board at Government Medical College and Hospital, Chandigarh, number GMCH/IEC/2020/500/133, dated February 24, 2021.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent.

Conflicts of interest

There are no conflicts of interest.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation

The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.

Financial support and sponsorship

Nil.

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