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Management of pediatric cardiac surgery wound: a literature review

Background: Sternal wound infection is a severe complication of cardiac surgery in the pediatric population (0-18 years old) that can lead to increased morbidity, mortality, and prolonged hospitalization. Health professionals have the ability to perform some interventions during the pre, intra and post-surgery to correctly manage sternal wounds, with the goal of preventing infections. Objectives: To identify and discuss current best practice in the prevention, incidence, and treatment of infections of the cardiac surgery site in the pediatric population. Methods: Between February 20th 2021 and February 28th 2021 we consulted the PubMed database adopting full text, 20 years, Humans, English, Child aged 0 to 18 years as criteria. Twenty articles out of sixty-six were considered relevant to this study. These were divided into four themes. Results: All studies highlight the lack of standard guidelines for managing pediatric patients undergoing cardiac surgery. Some centers developed protocols for managing antibiotic prophylaxis supported by measurable interventions; others implemented infection surveillance systems involving families taking care of patients after hospital discharge. Discussions: the identification of healthcare-associated infections in the pediatric population after cardiac surgery is useful in all peri-operative phases. The limited and restricted literature connected to single centers, with relatively small sample sizes, the use of a single database. Conclusion: There is a lack of standard guidelines. The prevention of site infection ought to the goal of reducing surgical site infections. Building a network between the multidisciplinary staff and the pediatric patient’s family improves the infection surveillance system, reducing the incidence of infections. (www.actabiomedica.it)


Background
The surgical site infection (SSI) after cardiac surgery is a serious concern for both the adult and the pediatric populations. Numerous studies confirm that SSIs are a complication with significant sequelae, such as longer hospitalization, increased morbidity and mortality, and higher health care costs (1,2,3,4,5,6,7,8,9,10). The incidence of SSIs after pediatric cardiothoracic surgery in the United States is reported between 0.25% and 6%, and it has an associated mortality range between 7% and 20% (11). Pediatric recommendations for SSI management are based on expert's opinions and data extrapolated from adult guidelines (12). Adult guidelines are based on risk factors such as obesity, diabetes, and smoking. These items, however, are not the same risk factors identified for SSIs in children (13). Potential pre-operative, intra-operative, and post-operative risk factors for children include: age lower than one month, duration of surgery, presence of genetic abnormalities, prolonged extracorporeal circulation (ECMO) time, delayed sternal closure, pre-operative hospitalization and prolonged post-operative hospitalization, post-operative hemorrhage, and persistent low cardiac output (10,14). While for the adult population there are predefined measures that aim at reducing the rate of the infections connected to cardiac surgery wounds, such as the ones presented by Bratzler et al. (2013) for the use of antimicrobial agents for the prevention of SSIs, there are no standardized protocols and guidelines for the management of cardiac surgery wounds in the pediatric population (15). This led us to ask ourselves what are the possible consequences of this lack of guidelines, and whether the introduction of protocols/guidelines would improve the management of sternal wounds in the pediatric population.

Objective
To identify and analyze current best practices in the prevention, incidence, impact and treatment of cardiac site infections after cardiac surgery, focusing on sternal wounds, in neonatal/pediatric users in the pre, intra, and post-operative phases.

Materials and Methods
The structured literature systematic review was guided by Preferred Reporting Items for Systematic Reviews and Meta-Analyses Protocols (PRISMA-P) (16). We consulted the PubMed database between February 20 th 2021 and February 28 th 2021, using the following Mesh terms: "Surgical Wound Infection" and "Cardiac Surgical Procedures". We selected the studies considered in this review according to the following criteria. We selected the categories: full text articles (other categories such as abstract only were considered not enough detailed for the purpose of this study), published within the last 20 years, referring to human species only, written in English, and related to a neonatal and/or pediatric population (Infant: birth to 23 months, Child: birth to 18 years). We included both qualitative and quantitative studies, randomized controlled trials (RCTs), prospective and retrospective comparative cohort studies, regression analysis, casecontrol studies, quality improvement (QI) and survey studies. We excluded articles on patients over 18 years of age, in foreign languages other than English. Out of one hundred-sixteen articles, twenty-two articles were determined by us to be relevant and connected to our research (Image 1, Table 1). From an initial analysis of the twenty-two articles identified according to the criteria introduced above, we extrapolated four main recurring topics: 1) risk factors for developing SSIs; 2) strategies to reduce SSIs; 3) relationship between colonization and clinical infection (SSIs rate); 4) impact of SSIs in terms of costs for the healthcare system. We thus decided to structure our study and show the results around these topics, for a more accurate examination and comparison.

Results
Of the twenty-two analyzed studies, nine are retrospective (1,2,3,5,6,9,11,17,18); three are prospective studies (8,19,20); three are quasi-experimental studies (21,22,23); five are quality improvement studies (7,10,24,25,26); one article is a survey (13); and one is a regression analysis (4). Common to all the articles considered in our study is the research of defined criteria that can help the multidisciplinary staff to recognize and prevent possible sternal wound infections. In what follows, we are illustrating our findings proceeding according to the four themes introduced above (i.e., Risk Factors, Strategies to reduce SSIs, SSI rate, and impact of SSIs in terms of costs for the healthcare system).
Risk factors. Nine articles (1,2,3,4,5,6,7,8,9) argue about the possible risk factors of developing SSIs. These studies confirm that SSIs after congenital heart surgery are a complication with significant sequelae. Hence it is important to understand the risks associated with this procedure, and what treatments can positively or negatively affect the risk factors. A number of variables are associated with major infections (Table 2).
Strategies to reduce SSIs. Five studies (10,22,23,25,26) introduced the idea of a written protocol. They sustained the bundle approach, i.e., a set of evidence-based practices adopted collectively by the multidisciplinary team as a valid instrument to pursue the reduction of the SSIs. The use of a sternal (Harder et al., 2013, Murray et al., 2014a, Katayanagi 2015, Nelson-McMillan et al., 2016, Kansy et al., 2012, Costello et al., 2010, Sen et al., 2017, Lex et al., 2013, Turcotte et al., 2014.   wound prevention bundle (SWPB), where each single center in the four analyzed studies adopted different items, in pediatric cardiac patients results in both a standardizations of the peri-operative care to prevent sternal wound infection (SWI) (25) and a significant reduction in patients with delayed sternal closure (DSC) (10,22,23). Other four articles (13,19,21,24) adopted a similar approach, that is, the use of common guidelines across the multidisciplinary team, to reduce SSIs. The authors showed how the implementation of quality improvement measures, such as linkage of registry and infection control surveillance, pediatric preventive guidelines and practice bundles, are considered an effective and systematic way to deliver preventive measures for reducing the SSIs (13, 19, 21, 24).

Relationship between colonization and clinical infection (SSIs rate).
Three articles (17,18,20) show that there is no significant difference between colonized and non-colonized children regarding the SSIs rate (17,18,20).  The impact of SSIs in terms of costs for the healthcare system. One article (11) deals with this topic. The study of Sochet et al. (2017) is the first to value the hospital cost associated with SSIs following pediatric congenital heart surgery, showing an increased operational and departmental cost. The SSIs increase the length of stay (LOS) in the hospital, and this exposes children to a greater risk of catheter-associated blood infections, venous thromboembolism, accidental extubations, catheter-associated urinary tract infections, ventilator-associated pneumonia, and adverse events (11).

Discussion
The infection of the sternal wound after cardiac surgery is a serious concern. According to Woodward et al. (2011) the incidence of major infection remains a source of morbidity and mortality in postoperative pediatric cardiac patients. The identification of healthcare-associated infections (HAIs) in the pediatric population after cardiac surgery is useful in all peri-operative phases (9). The literature shows that adult standardized guidelines for cardiac surgery wound management should not be used with paediatric populations since there are substantial differences between adults and children. One important point investigated in many studies is the impact of standardized peri-operative antibiotic prophylaxis protocols for pediatric cardiac surgery. Bath et al. (2016) demonstrated that limiting antimicrobial prophylaxis to 48 hours post-operative pediatric cardiac surgery did not increase the incidence of SSIs or alter other clinical outcomes in this population (23). Murray et al. (2014) demonstrated that limiting peri-operative antibiotic prophylaxis after neonatal cardiac surgery to 48 hours in neonates with a closed sternum and to 24 hours after sternal closure is safe and does not increase the rate of SSIs. (22). Delgado-Corcoran and colleagues reported lower SWI rates caused by Staphylococcal; however, MRSA contributed to 10% of those infections. MRSA is associated with higher mortality rates, longer hospital length of stay, and higher hospital costs if compared with other infections (10). The duration of pre-operative hospitalization is important in the prevention of SSIs (17). The study of Katayanagi suggests that treatment with Mupirocin is an effective tool (3). Mupirocin should be given intranasally to all patients with documented Staphylococcus Aureus (SA) colonization (17). The pre-operative eradication of SA was proven effective in the prevention of SSIs and in the control of MRSA; however, the continuation of prophylactic antibiotic therapy in conjunction with delayed sternal closure may introduce antimicrobial resistance (8). In contrast to the reports above, the study by Macher and colleagues (2017) finds no association between SA carriage and the incidence of SSIs (20). Further studies are necessary in order to analyze this association. Previous studies (1,2,3,4,5,6,7,8,9) have evaluated risk factors for specific types of postoperative infections.
Standardized adult guidelines for cardiac surgery wound management may not be effective on the pediatric populations (13), as the first are based on different risk factors (e.g., obesity, diabetes and smoking) compared to the ones considered in the pediatric population (age lower than one month, duration of surgery, presence of genetic abnormalities, prolonged extracorporeal circulation time (ECMO), delayed sternal closure, pre-operative hospitalization and prolonged post-operative hospitalization, post-operative hemorrhage, and persistent low cardiac output) (10,14).
According to the literature, the institution of a multidisciplinary team where coworkers follow a standardized protocol improves the patients' outcomes. Galvin et al. (2009) assess that the adoption of a standardized procedure for how nurses perform skin preparation produces a positive effect on the practice over time (27). Jha et al. (2020) demonstrate that a protocol-based bundled approach reduces the incidence of SWI (28). Blasco et al. (2015) underline the importance of implementing a multidisciplinary infection control program to reduce the incidence of SSIs in children and neonates undergoing cardiac surgery. Staveski et al. (2016) describe the Asepsis Tool as a valid tool for monitoring the assessment of cardiac surgery injury in the adult population. It consists of data sheet that allows the nurse to perform an initial wound assessment and to compare the subsequent evaluations throughout observable data calculated with numerical scores. The survey of 28 children's cardiac surgery programs of Woodward et al. (2020) presents an overview of the responders' efforts to reduce infection in their DSC patients. These programs showed very different approaches and, eventually, a few indicators were collected regarding what works to decrease infection in this population (29).
The standardization of the behavior of health workers, by the use of standardized protocol and guidelines, and the education for a correct use of these instruments, can strongly influence the patient's assistance and the consequent development of infections (25). Thirty-Six percent of the SSIs are identified after the patient's discharge from the hospital (21). The education of family members and a confident/strong collaboration with them are essential to reduce this incidence. The surveillance path of Cannon et al. (2016) revealed how family involvement and multidisciplinary work, both hospital and territorial, reduced SSIs. Therefore, the collaboration between the multidisciplinary team and the patient's family is fundamental during and after hospitalization since the risk of developing a sternal wound infection persists after the patient discharge.
Limits. The limited and restricted literature connected to single centers, with relatively small sample sizes, and the use of a single database.

Conclusion
From this literature review we can observe oneway indication for the management of the pediatric cardiac surgery wound. All the studies agree that the use of validated and shared tools, as well as the establishment of standardized protocols, consent to improve the SSI management. The common goal is the adoption of prevention techniques for contrast the insurgence of infections. The threat does not end with the discharge of the patient. For this reason, the postoperative follow-up is fundamental. Therefore, it is essential to create a strong network between the multidisciplinary hospital staff and the pediatric patient family.
Further research is necessary for the realization of standardized protocols or guidelines for the management of the pediatric cardiac surgery wound.

Conflicts of interest:
Each author declares that he or she has no commercial associations (e.g. consultancies, stock ownership, equity interest, patent/licensing arrangement etc.) that might pose a conflict of interest in connection with the submitted article.