Pediatric antimicrobial stewardship program in a low- and middle-income country: pre- and post-implementation to improve surgical prophylaxis

Introduction

Surgical site infections (SSIs) are concerning complications in hospitalized patients, including children, undergoing surgeries. In the United States, SSI contributed to 30% of morbidity in pediatric surgeries (1). In terms of SSI rate, a meta-analysis on the burden of healthcare-associated infections in Southeast Asia from 2000 to 2012 reported the pooled SSI rate was 7.8%, which was 2.9% higher than that of developing countries from Asia, Europe, Africa and Latin America surveyed from 2005 to 2010 (2). Surgical site infections can lead to prolonged hospital stay, an increase in treatment cost and mortality (3).

Surgical antibiotic prophylaxis (SAP) is an effective measure to prevent SSI, with guidelines published by the Centers for Disease Control and Prevention and World Health Organization (3-5). The use of antibiotics can prevent perioperative infection, effectively reducing 50% of serious SSI (6,7). Consequently, the development and implementation of SAP is prudent to prevent SSI, especially in children, and may also help control the growth of antimicrobial resistance. According to the American Society of Health-System Pharmacists (ASHP), four criteria are considered when determining the appropriateness of SAP: antibiotic timing, selection, dosing and duration (6).

The development and implementation of SAP guidelines for hospitals in low- and middle-income countries (LMICs) are prudent since these hospitals usually have limited sources for effective infection control. Despite the availability of SAP guidelines, adherence varies among hospitals in Qatar, Malaysia and Greece, ranging from 20.7% to 64% (8-10). Recommendations and research on SAP have mainly focused on adults, with minimal effort for pediatrics; therefore, SAP guidelines for pediatric use are extrapolated from the adults (1,3). Antimicrobial stewardship (AMS) programs within hospitals provide a framework to support successful implementation of SAP guidelines, yet efforts are limited in pediatric hospitals especially in LMICs. Previously, at the Vietnam National Children’s Hospital (VNCH), antibiotic prophylaxis was only routinely performed under the orders of surgeons or anesthesiologists, without close intervention from the AMS team. The use of antibiotic prophylaxis was only controlled by the World Health Organization (WHO) surgical checklist, which only counted whether or not antibiotic prophylaxis had been used before surgery, without going into details that could affect the results of surgical prophylaxis. Therefore, we aimed to evaluate adherence to SAP guidelines developed within our pediatric AMS program performed in a hospital of Vietnam—a LMIC. We present this article in accordance with the STROBE reporting checklist (available at https://pm.amegroups.com/article/view/10.21037/pm-25-49/rc).

Methods

This was a retrospective pre- and post-implementation observational study conducted at VNCH in Hanoi, Vietnam. After development of SAP guidelines within our pediatric AMS program, we implemented and monitored adherence to our guidelines. Intensive education and implementation of our SAP guidelines were executed from May 2019 to March 2021. We provided training to all surgeons, anesthesiologists and nurses involved in the operations. Then, AMS teams periodically observed the implementation of antibiotic prophylaxis during the operations. Errors were noted and addressed in subsequent meetings. The pre-implementation period was from January 2017 to September 2017, and the post-implementation period was from April 2021 to June 2023. A time gap from October 2017 to April 2019 was used to develop SAP guidelines specifically for each surgical department.

Our study included patients less than 18 years of age who underwent the following surgical services of which wounds were classified as clean and clean-contaminated: urology, general surgery, orthopedics, craniofacial and plastic surgery, whereas general surgery is defined to include thoracic, gastrointestinal, hepatobiliary and pancreatic surgery. We excluded patients who were hospitalized for more than 14 days, or patients who received antibiotics 48 hours prior to skin incision. Patients who experienced multiple surgeries within less than 24 hours, emergency surgeries, those without full medical records and those who died within 24 hours after surgery were also excluded. Patients on mechanical ventilation, had comorbidities, and/or received immunosuppressive agents were also excluded.

Demographic and clinical data (i.e., surgery and antibiotic use with timing, dosing and duration) were collected for all subjects. For each surgery, timing of skin incision and prophylactic antibiotic administration were directly documented by the AMS team in operating rooms. Other information was collected according to paper medical records, including surgery duration, antibiotic selection, dosage, and duration of antibiotic therapy.

SAP adherence was evaluated according to four criteria defined by ASHP. Indications were classified as adherent if the selected antibiotics concordant with our SAP guideline that was based on wound classification and surgery type (Table 1, Appendix 1). Dosing adherence was defined as less than 10% difference compared to the recommended dose in the ASHP’s Guidelines for Antimicrobial Prophylaxis in Surgery (4). Based on WHO’s recommendations, timing prior to skin incision within 60 minutes were considered adherent. This criterion was assessed according to WHO guidelines due to its broad applicability and practical relevant. Adherent duration of SAP was defined using the ASHP guidelines; however, for certain cases in which devices (e.g., Kirschner wire, drills) were implanted into the body, the duration of SAP was reviewed and determined by surgeons of specific specialties in collaboration with our AMS team.

Guidelines implementation

From January 2017 to September 2017, the AMS team consisted of physicians, clinical pharmacists, and quality control executives of VNCH who completed an assessment survey on the use of SAP in urology and general surgery. From 2019 to 2021, SAP guidelines were developed by our AMS team with surgeons and implemented for urology surgery, orthopedics, general surgery, craniofacial and plastic surgery. Intensive SAP guidelines education was conducted for surgeons, anesthesiologists, and nurses in all surgical departments before full guidelines implementation. Audit and feedback were conducted through different channels, including direct communication of inappropriate practice to clinical staff involved in the surgery department, and periodic hospital meetings to review deviations from guidelines and best practice for SAP.

Our primary study outcome was the composite adherence to our local SAP guidelines. Our secondary outcomes included: total adherence, partial adherence and the adherence assessed by each ASHP criterion. Total adherence was defined if all four ASHP criteria were met, and partial adherence was achieved if indication and timing were met. A composite adherence was defined as achieving either partial or total adherence. Non-adherence was defined if either total or partial adherence was absent.

Statistical analysis

Statistical analyses were performed using R software (version 4.3.1). Continuous data (e.g., age and weight) were presented as means and standard deviations, and categorical data (e.g., gender and adherence rates), as number and percentages. The two-sided student t (or unpaired Wilcoxon for non-normal distribution) and χ² tests were used to compare continuous and categorical variables, respectively, during the pre- and post-implementation periods. Statistical significance was set with P<0.05.

Ethical considerations

This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by institutional ethics committee of Vietnam National Children’s Hospital number 1600/BVNTW-HDDD (IRB - VN01037/IRB00011976/FWA00028418) and individual consent for this retrospective analysis was waived.

Results

Among 355 subjects who met the inclusion criteria at the VNCH from January 2017 to June 2023, 65 were excluded. The remaining 289 subjects were analyzed, with 96 cases in the pre-implementation and 193 cases in the post-implementation periods (Figure 1). The mean [standard deviation (SD)] age was 5.0±4.0 and most were male gender (69.2%). There were 2 infants <1 month of age in the post-implementation period. There was no statistical difference in wound classification between the pre- and post-implementation periods (P=0.37) (Table 2). Most subjects underwent urology and general surgery before SAP guidelines implementation. Diverse types of surgeries were performed after SAP guideline implementation.

Figure 1 Study flowchart.

The composite adherence to SAP guidelines significantly increased from 33.3% to 80.3% in the pre- and post-implementation periods (P<0.001) (Figure 2). Both the total and partial adherence also significantly increased during the post-implementation period. In contrast, non-adherence to SAP guidelines significantly decreased during the post-implementation period (66.7% vs. 19.7%, P<0.001) (Figure 2). Adherence to all four ASHP criteria also increased significantly during the post-implementation period (P<0.001) (Table 3).

Figure 2 Adherence to surgical antibiotic prophylaxis guidelines (%).

Discussion

SSI has always been an important issue to surgeons, especially in vulnerable populations such as pediatrics. One-third of surgical complications in children are SSIs in high-income countries, yet data are lacking and potentially variable in LMICs (11). A report from Nigeria provided the overall pediatric SSI rate at 23.6% (12), whereas Vietnam showed data of SSI incidence among 7 hospitals was 5.5% (13). Appropriate use of SAP is one of the infection prevention and control strategies for LMICs (11). However, guidelines on SAP for pediatrics are often extrapolated from adults, lending to the need for robust research on SAP in children.

We conducted this study to evaluate the adherence rate of surgeons to a local guideline on SAP in a tertiary pediatric hospital in Vietnam. Notably, this was the first study, to our knowledge, assessing SAP adherence in pediatric surgeries in a low and middle-income country. Using a framework of intensive implementations from our hospital’s AMS program, we demonstrated that the total and partial adherence significantly improved between the pre- and post-implementation periods (P<0.001), with similar results to the study by So et al. (14). In fact, the non-adherence from pre- to post-implementation periods successfully decreased from 66.7% to 19.7% (P<0.001). This improvement in adherence was evident in all 4 criteria of our SAP guidance.

In the pre-implementation period, timing was the least adherent criterion to prescribers with 38.5%. Our result was similar to several studies, of which correct timing was considered to be “the most problematic indicator” (1,15,16,17). However, in our study, for the post period, administration time adherence significantly improved to 99.5% (P<0.001). Tourmousoglou et al. also reported 100% for time adherence in a Greece hospital (10). This result was achieved likely from the collaborative efforts of healthcare professionals at our hospital who participated in the surgery, including pre-operative nurses, anesthesiologists, surgeons, and surgical nurses who held each step accountable for implementing prophylactic antibiotics at the right time. Furthermore, the effort of the AMS team impacted this improvement since members actively intervened in the operating room to discuss and inform surgeons and nurses of our SAP guidelines, gradually creating habits in practice.

The adherence rates to SAP guidelines by indication and dosing were similar in trend from pre- to post-implementation periods. While correct indication improved from 41.7% to 82.4% (P<0.001), dosage adherence rate surged from 41.7% to 84.5% (P<0.001). Appropriate antibiotic choice had the highest rate of adherence in published studies (1,9,15,16). In our study, cases were deemed inadequate based on the wound classification by surgeons, which led to inaccurate antibiotic selection, and their prescribing habits of dose rounding by vial availability, which was easily memorized for surgeons and offered convenience for nurses to execute medication orders.

Duration of SAP is the most difficult factor to intervene and improve among the 4 criteria. This issue has been acknowledged by many studies, even when AMS implementations were carried out (1,9,10,14,16-18). Prolonged use of SAP was attributed to multiple concerns for SSI development, including discontinuation of antibiotic, prosthetic device placement in patients after surgery and the lack of unified guidelines among surgeries. Periodic meetings with discussions on continuous quality improvement between AMS team and surgical team showed the ability to help gradually solve the problem and improve the duration adherence from 74% to 91.2% (P<0.001). To reach consensus between the AMS team and the surgical departments, coupled to the epidemiology of bacteria in LMICs, we required surgeons to clarify the reason for prolonged SAP exceeding 24 hours after skin incision in the medical records, especially if any abnormalities were identified during the operation.

Our study had several limitations. First, we collected data focusing on urology and general surgery in the pre-implementation period since these were most common at our hospital. Notably, our SAP guidelines implementation was conducted throughout our entire hospital, which impacted all surgeons and surgical departments. As such, during the post-implementation period, we captured SAP adherences for other types of surgeries, in addition to the common ones during pre-implementation. The evaluation method was similar among different types of surgery, in accordance with ASHP guidelines. Second, we were not able to evaluate three important data since they were not documented in our medical record system: (I) repeated SAP dosing in surgeries lasting longer than 2 hours; (II) antibiotics prescribed after hospital discharge; and (III) SSIs were not documented in all operations. Lastly, the sample size was small as we were not able to apply electronic medical record to assess the SAP guidelines adherence of surgeons. Future research is needed to address areas that were deficient in documentation, especially with a large sample size. Nonetheless, we believe that our study was informative and demonstrated the importance of implementing SAP guidelines to improve SSI in children, especially those residing in LMICs where efforts and research are limited.

Conclusions

The composite, including total and partial adherence, significantly improved after implementation of an intensive SAP program. However, it is imperative to continue to develop guideline specific for each type of operation, especially incorporating limitation on the prolonged use of SAP. Further efforts are prudent to reach full adherence in all four criteria, potentially with the integration of technology to assess SAP adherence in real-time.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://pm.amegroups.com/article/view/10.21037/pm-25-49/rc

Data Sharing Statement: Available at https://pm.amegroups.com/article/view/10.21037/pm-25-49/dss

Peer Review File: Available at https://pm.amegroups.com/article/view/10.21037/pm-25-49/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://pm.amegroups.com/article/view/10.21037/pm-25-49/coif). J.L. participates on a Data Safety Monitoring Board or Advisory Board of Innovia Specialty Therapeutics and serves as an unpaid editorial board member of Pediatric Medicine from January 2024 to December 2025. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by institutional ethics committee of Vietnam National Children’s Hospital number 1600/BVNTW-HDDD (IRB - VN01037/IRB00011976/FWA00028418) and individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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