+Model MEDMAL-3432; No. of Pages 7 ARTICLE IN PRESS Disponible en ligne sur www.sciencedirect.com Médecine et maladies infectieuses xxx (2013) xxx–xxx General review Epidemiology and prevention of surgical site infections after cardiac surgery Épidémiologie et prévention des infections du site opératoire après chirurgie cardiaque D. Lepelletier a,∗,d , C. Bourigault a , J.C. Roussel b , C. Lasserre a , B. Leclère a , S. Corvec a,d , S. Pattier b , T. Lepoivre e , O. Baron b,c , P. Despins b,c a Service de bactériologie et d’hygiène hospitalière, unité de gestion du risque infectieux, CHU de Nantes, bâtiment Le Tourville, 5, rue du Pr-Yves-Boquien, 44093 Nantes cedex 01, France b Service de chirurgie thoracique et cardiovasculaire, CHU de Nantes, 44000 Nantes, France c Inserm UMR S 1087, université de Nantes, institut du thorax, 44000 Nantes, France d UFR médecine, université de Nantes, EA 3826, Nantes, France e Département d’anesthésie-réanimation, 44000 Nantes, France Received 14 September 2012; received in revised form 20 June 2013; accepted 19 July 2013 Abstract Deep sternal wound infection is the major infectious complication in patients undergoing cardiac surgery, associated with a high morbidity and mortality rate, and a longer hospital stay. The most common causative pathogen involved is Staphylococcus spp. The management of post sternotomy mediastinitis associates surgical revision and antimicrobial therapy with bactericidal activity in blood, soft tissues, and the sternum. The pre-, per-, and postoperative prevention strategies associate controlling the patient’s risk factors (diabetes, obesity, respiratory insufficiency), preparing the patient’s skin (body hair, preoperative showering, operating site antiseptic treatment), antimicrobial prophylaxis, environmental control of the operating room and medical devices, indications and adequacy of surgical techniques. Recently published scientific data prove the significant impact of decolonization in patients carrying nasal Staphylococcus aureus, on surgical site infection rate, after cardiac surgery. © 2013 Elsevier Masson SAS. All rights reserved. Keywords: Cardiac surgery; Surgical site infection; Risk factors; Prevention Résumé Les infections du site opératoires profondes représentent la complication infectieuse majeure de la chirurgie cardiaque. Essentiellement staphylococciques, elles nécessitent une reprise chirurgicale précoce et une antibiothérapie rapidement bactéricide au niveau du sang, des tissus mous et du sternum. Leurs conséquences sont sévères en termes de morbidité et d’allongement de la durée de séjour hospitalier. Les stratégies de prévention pré, per- et postopératoire associent le contrôle des facteurs liés aux patients (obésité, diabète, insuffisance respiratoire), la préparation cutanée corporelle (traitement des pilosités, douche préopératoire, antisepsie du site opératoire), l’antibioprophylaxie, la maîtrise de l’environnement du bloc opératoire et des dispositifs médicaux mais aussi les indications et la qualité des techniques opératoires. Les données récentes de la littérature scientifique montrent un impact significatif de la décolonisation des patients porteurs de staphylocoques doré au niveau nasal sur le taux d’infection du site opératoire après chirurgie cardiaque. © 2013 Elsevier Masson SAS. Tous droits réservés. Mots clés : Chirurgie cardiaque ; Infection du site opératoire ; Facteurs de risque ; Prévention 1. Introduction ∗ Corresponding author. E-mail address: [email protected] (D. Lepelletier). More than 40,000 cardiac surgery procedures are performed every year in France. Deep sternal wound infection (mediastinitis) is the most severe complication and surgical site infection 0399-077X/$ – see front matter © 2013 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.medmal.2013.07.003 Please cite this article in press as: Lepelletier D, et al. Epidemiology and prevention of surgical site infections after cardiac surgery. Med Mal Infect (2013), http://dx.doi.org/10.1016/j.medmal.2013.07.003 +Model MEDMAL-3432; No. of Pages 7 2 ARTICLE IN PRESS D. Lepelletier et al. / Médecine et maladies infectieuses xxx (2013) xxx–xxx (SSI) in cardiac surgery performed mainly by median sternotomy [1]. Its incidence is relatively low and has remained for several years, but it concerns 4000 to 8000 increasingly fragile patients every year, whose risk of mortality is increased from 10 to 40% [2–4]. All cardiac surgery units in France are concerned by the occurrence of mediastinitis and confronted to its severity at short or long term, to its difficult management, and to significant over-cost [5]. The surgical teams in these units have developed SSI prevention strategies in collaboration with hygienists, anesthesiologists, and critical care specialists, based on recent recommendations, particularly those concerning antibiotic prophylaxis [6] and patient preparation [7]. Besides these recommendations, choosing preventive measures relies on the knowledge and management of risk factors related to patients, to the surgery, and to the operating room environment [8]. The prognosis depends on the delay before diagnosis and treatment, on the therapeutic method, and on the effectiveness of antibiotherapy. The definition, the incidence, and the risk factors for SSI after cardiac surgery are presented in this review. We have summarized the main strategic orientations currently recommended for the prevention of these sometimes devastating infectious complications. 2. Definition and classification of surgical site infection after cardiac surgery SSI include superficial infections of the postoperative scar and deep wound infections such as sternal osteitis, mediastinitis, and endocarditis. The definitions of postoperative SSI are adapted from those issued by the National Technical Committee on Nosocomial Infections and Care Related Infections (French acronym CTINILS 2007) [9], which had been adapted from those issued by the centers for disease control and prevention (CDC) [10]. 2.1. Superficial wound infections Superficial wound infections concern the skin and subcutaneous tissue. The signs (redness, fluid collection, disunion) are always local. The sternum is not involved, stable, and painless on bi-manual palpation. Most of the time, it requires only local (disinfection, warm pads) and oral (antibiotics) treatment. But it may extend to deeper layers at any time. 2.2. Deep infection or of hemoculture (or both in case of germs commensal of the cutaneous flora). Only surgical exploration can document the true nature, the extent, and the prognosis of infection. Despite the helpfulness of these definitions, the use of different terms to define SSI may account for the difficulty to clearly define and measure its incidence [11]. Sternal wound complications range from sterile dehiscence to suppurative mediastinitis, and the terms of sternitis or sternal osteitis (surgical revision without sternal opening) and mediastinitis (surgical revision with sternal opening) are used to define deep infection. Some definitions published in the 2000s are author specific such as El Oakley’s or Gardlund’s [12,13]. Furthermore, the reproducibility of SSI diagnosis may vary according to the depth of infection [11,14]; the medical specialty of the physician also has an impact (surgeon, anesthesiologist, infectious disease specialist, bacteriologist, hygienist), stressing the need for a multidisciplinary approach [14]. 3. Incidence of surgical site infection in cardiac surgery The rate of SSI varies according to the quality of the local epidemiological surveillance [15] or of surveillance networks, of the SSI definition used (superficial, deep), of the patient’s profile, and of the type surgical procedure [16,17]. The true global incidence of infection in cardiac surgery is thus difficult to assess. In France, the alert, investigation, and surveillance of nosocomial infections (French acronym RAISIN) network data concerning cardiac surgery is made on too small samples to be representative [16]. According to some authors and to simplify data collection, the surveillance of patients reviewed surgically (with or without sternal re-opening) from the operating room and onward, would allow measuring reliably and easily the incidence of deep SSI [3]. The incidence of mediastinitis after the 1990s has not decreased compared to the 1970–1980s, ranging between 0.5% and 4.4% [18]. Various scores have been built and used to stratify the incidence of postoperative SSI according to risk factors. The American score of the National Nosocomial Infections Surveillance (NNIS) System integrates the ASA physical status score, the Altemeier contamination classification, and the length of surgery [19]. Other scores have been proposed for prediction based on factors more specifically associated to the risk of mediastinitis identified by comparatives studies in multivariate analysis [20–22]. Deep infection includes the previously mentioned lesions and is defined by the involvement of tissue below the subcutaneous layer with at least one of the following criteria: 4. Physiopathology of surgical site infection after cardiac surgery • positive culture of tissue samples or mediastinal fluid; • typical presentation of mediastinitis on revision surgery or anatomopathological examination; • presence of one of the following elements: fever superior to 38 ◦ C, thoracic pain or sternal instability, with either pus in the mediastinum, or positive culture of peroperative samples The contamination of the operative site may be due to the patient’s endogenous flora or to the surgical team’s or operating room exogenous flora, and is often peri-operative. Some factors promote the occurrence of SSI from this contamination, such as tissue necrosis, hematoma, foreign body, of a prosthesis or of an implant, and bad vascularization. Please cite this article in press as: Lepelletier D, et al. Epidemiology and prevention of surgical site infections after cardiac surgery. Med Mal Infect (2013), http://dx.doi.org/10.1016/j.medmal.2013.07.003 +Model ARTICLE IN PRESS MEDMAL-3432; No. of Pages 7 D. Lepelletier et al. / Médecine et maladies infectieuses xxx (2013) xxx–xxx 4.1. The impact of endogenous flora The impact of endogenous flora is essential in the physiopathology of SSI. Since the late 1990s it was acknowledged that nasal colonization by Staphylococcus aureus was a risk factor for S. aureus SSI after cardiac surgery [23,24] with a great similitude of colonization and infection strains. 4.2. The exogenous contamination The exogenous contamination of the operative site is either handborne or airborne. The airborne contamination requires two associated phenomena, the presence of microorganisms (air biocontamination) and of inert particles (air contamination) some of which are used as support by bacteria. The microorganisms often come from the usual saprophyte flora of air (rarely pathogenic) and from the commensal human flora (mostly S. aureus, coagulase negative staphylococci, sometimes Gram-negative bacteria) released by human bodies (patients and surgical team) [8,25]. The particles are released by individuals (cutaneous squamous cells, skin appendages, respiratory droplets, and droplet nuclei), and textiles (surgical team’s clothes and operative field drapes); the quantity is proportional to the number of individuals present in the room and to their movements and moving around, as well as to the quality of textiles used (no-woven and polycoton drapes emit less particles than cotton drapes and more particle proof) [26]. The surgical team’s flora is rarely the cause. Contamination by soiled material, very rare, has now become exceptionally rare because of the recent strengthening of sterilization and disinfection guidelines for materials, and the use of disposable sterile material. Other rare modes of postoperative contamination may be mentioned, particularly hematogenous ones from an infection occurring in postoperative critical care (catheter bacteremias [27] or pneumonia) or by direct bacterial inoculation of the operative site when changing wound dressing in patients presenting with scarring abnormalities. Three major hypotheses can be considered concerning the chronology. The infection is localized after contamination, responsible secondarily for localized sternal osteomyelitis, inducing the disunion of fasciae. Other authors believe there is first a separation of sternal margins leading to the disunion of fasciae secondarily colonized by bacteria. The last admitted hypothesis is that of the poor drainage, with a large stagnant collection, favoring bacterial development [28]. 5. Microbiology Staphylococci are the main bacteria responsible for postoperative SSI, even if their proportion may vary according to reports. S. aureus accounts for 40 to 60% of strains causing mediastinitis. Coagulase negative staphylococci are involved in 20 to 30% of cases (Table 1). 20 to 30% of mediastinitis cases are caused by Gram-negative bacilli and rarely by yeasts [28]. Some authors have described various types and times of bacterial contamination (pre-, per-, and postoperative) according to microbiological documentation [13]. 3 Table 1 Microbiological documentation of mediastinitis after cardiac surgery. Documentation microbiologique des médiastinites après chirurgie cardiaque. Microbiology of mediastinitis Gram positive Cocci Staphylococcus aureus Coagulase negative Staphylococcus 40% 30% Gram negative Bacilli Escherichia coli Enterobacter spp. Klebsiella spp. Proteus spp. Pseudomonas spp. 5% 10% 3% 2% 2% Other Candida Polymicrobial < 2% 10–40% From [29]. 6. Risk factors associated with mediastinitis Many authors, over the last 20 last years, have well described the risk factors for mediastinitis, especially in patients having undergone coronary bypass, which often overlap. The patients may be contaminated before, during, or after surgery, and any reoperation exposes to the risk of SSI. The risk factors are related to the patient (age, sex, obesity, diabetes, respiratory insufficiency), to surgery (context of emergency, type of surgery, operative time, early surgical revision for bleeding) and to hospitalization and its environment (duration of preoperative stay, patient preparation) [8,29,30]. The main risk factors associated with postoperative SSI are listed in Table 2. 6.1. Risk factors related to patients Obesity was identified as an independent risk factor for mediastinitis by many authors. The severely obese patients Table 2 Main risk factors for mediastinitis after cardiac surgery. Principaux facteurs de risque pour une médiastinite après chirurgie cardiaque. Main risk factors of mediastinitis References Related to patients Age Sex Obesity Diabetes COBP Nasal Staphylococcus aureus carriage [31] [29,31] [30–32] [31,33] [15,29,31] [24,34] Related to hospitalization Duration of preoperative hospitalization [30] Related to surgery Surgical time Coronary bypass Use of internal mammary arteries Early revision for bleeding [1,33] [15] [1,15,35–38] [15] Other NNIS infectious risk score ≥ 2 [15] Please cite this article in press as: Lepelletier D, et al. Epidemiology and prevention of surgical site infections after cardiac surgery. Med Mal Infect (2013), http://dx.doi.org/10.1016/j.medmal.2013.07.003 +Model ARTICLE IN PRESS MEDMAL-3432; No. of Pages 7 4 D. Lepelletier et al. / Médecine et maladies infectieuses xxx (2013) xxx–xxx [BMI > 35 kg/m2 ] had increased risks for comorbidity because of a longer hospital stay than non-obese patients, and a lower 5year survival rate with a Kaplan Meier analysis and multivariate analysis using Cox’s regression model [32]. The peri-operative antibiotic doses administrated to obese patients, not adapted to their distribution volume, and the difficulties to implement an operative field could account for this risk [39]. Diabetes, and especially peri-operative hyperglycemia, also increases the infectious risk after cardiac surgery. More precisely, elevated glycemia (> 200 mg/dL) on the first and second postoperative days could be associated to an increase of sternal infections in diabetic patients and peroperative control of glycemia could decrease the morbidity [33]. 6.2. Risk factors related to the procedure Some surgical techniques may also be associated with the risk of mediastinitis. This is why using either of the two internal thoracic arteries (ITA) in patients for coronary bypass remains quite controversial [35]. Using the two ITA results in a significant improvement of survival and of postoperative outcome. Man authors have reported a decrease revision surgery rate for revascularization compared to patients whose bypass was made with the great saphenous vein. These assets are counterbalanced by the significantly increased risk of SSI, especially in obese and diabetic patients who should benefit the most from the double internal thoracic vascularization [36]. There are alternative procedures for these patients including the strict control of perioperative glycemia [37] and the skeletonization of arterial grafts, minimizing sternal devascularization [38]. The other risk factors related to surgery are, early revision surgery, the more often for postoperative hemorrhage, often mentioned as a risk factor for sternal infection, especially when the initial surgery was long and complicated [15,40]. A mediastinal hematoma may develop, because of the bad hemostatic quality of sternal closure, favoring serous fluid collection and necrotic material in which bacteria may proliferate [41]. 7. Prevention strategy The occurrence of a postoperative SSI is due to several factors and its prevention relies on the control of risk factors related to patients, to the procedure, and to hospital environment, during the pre, per, and postoperative periods. The French Society for Hospital Hygiene (French acronym SFHH) issued recommendations for the prevention of SSI in 2004, “Preoperative management of the infectious risk” in partnership with all surgery learned societies [7], “Air management in the operating room” [42], and more recently in 2010 “Monitor and prevent care related infections” in collaboration with the French National Authority for Health (French acronym HAS) [8]. The 2004 recommendations are currently being reviewed to take into account the evolution of published scientific data on nasal S. aureus decolonization to decrease the rate of S. aureus SSI and on the patient’s skin preparation. The 1999 CDC recommendations [10] in the USA have been completed more recent publications, specifically adapted to cardiac surgery [43], especially postoperatively at home [44]. These measures are classified by levels of recommendations and of evidence (Table 3). They especially concern the preoperative period and include the patient’s body skin preparation (body hair removal, preoperative shower, antisepsis of the operative site with an alcohol based antiseptic), preparation and dressing of the surgical team, and environment control of the operating room and devices. These prevention measures were completed by recommendations on surgical antibioprophylaxis issued by the French Society of Anesthesiology and Critical Care [6] and specific cardiac surgery data [45]. The decolonization of nasal S. aureus carriage is currently the most debated prevention measure related to the patient. Many authors, between 2000 and 2010, reported no significant impact of decolonization on the rate of S. aureus SSI because of differences in the methodological approach of decolonization strategies and types of procedures studied [24,34]. The authors of a randomized, double blind, placebo controlled study made in 2010, in the context of a multicentric clinical trial, reported the effectiveness of rapid S. aureus screening on admission and nasal decolonization with mupirocine only in patients identified as S. aureus carriers, associated to body showering with chlorhexidine gluconate antiseptic soap, and oro-pharyngeal decolonization, on the rate of deep S. aureus infections, essentially in cardiac surgery (the study also included other types of surgery but in smaller samples) compared to the placebo control group including patients carrying S. aureus (79% decrease, OR 0.21. CI95% 0.07–0.62) [46]. The trial results will soon be integrated in the new recommendations of the French Society for Hospital Hygiene, to be issued in 2013. Nevertheless, the implementation mode of this decolonization strategy (with or without: prior nasal screening, screening method, decolonization period) must still be evaluated and the occurrence of SSI due to other microorganisms must be monitored. Using a sponge impregnated with local diffusion antibiotics on the operative site (gentamycin) is debated as a peroperative prevention measure; recent scientific publications on this issue are often contradictory [47,48]. This measure has not sufficiently demonstrated its effectiveness, even if some cardiac surgery units use it successfully. The authors of recent studies have reported the contribution of education programs and of prevention focusing on some measures grouped as “bundles”, set of measures, which observed and assessed at the same time, allow obtaining a decrease of SSI rates, demonstrating the multimodal aspect of prevention strategies. These interventional programs include some measures such as the patient’s skin preparation, nasal screening of patients, nasal decolonization with mupirocine, evaluation and switch of antibioprophylaxis, especially for patients carrying methicillin resistant S. aureus (MRSA), barrier measures in the operating room (gloves), and compression devices to prevent mechanical postoperative scar disunion (obese patients, patients presenting with chronic bronchitis), [49,50]. A prevention program implemented at the Nantes hospital center during more than 10 years, allowed to decrease the rate of mediastinitis 100 cardiac surgery procedures from 2.1% in 2001 to 1.1% in Please cite this article in press as: Lepelletier D, et al. Epidemiology and prevention of surgical site infections after cardiac surgery. Med Mal Infect (2013), http://dx.doi.org/10.1016/j.medmal.2013.07.003 +Model ARTICLE IN PRESS MEDMAL-3432; No. of Pages 7 D. Lepelletier et al. / Médecine et maladies infectieuses xxx (2013) xxx–xxx 5 Table 3 Prevention of surgical site infections (level and proof of guidelines 2004 and number of recommendation 2010). Principales mesures de prévention des infections du site opératoire (niveau de recommandation et de preuve 2004 et référence de la recommandation 2010). Prevention measures Preoperative Surveillance of surgical site infections Delayed surgery in case of intercurrent infection Nasal Staphylococcus aureus decolonization No shaving or hair removal At least one preoperative shower with antiseptic soap Mouthwash with antiseptic solution Patient dressed with no-woven or micro-fiber fabric Peroperative (intra-operating room) Disinfection of hands with hydro-alcoholic gel Detergence with antiseptic soap followed by broad disinfection of the operative site Brushing with an alcoholic antiseptic solution 100% cotton patient drapes Adequate surgical garb, operating room discipline and use of a check-list Quality of air the operating room Postoperative Maintaining glycemia < 2 g/L Mouthwash with antiseptic solution Traceability of the following Surgical program planning Antibioprophylaxis Patient’s cutaneous preparation Identification of operators Elements of the NNIS infectious risk score Medical material and devices used Cleaning procedures Chronology of events a Recommendations 2004 [7] Recommendations 2010 [8] – Yes (A2) No (E-2)a Yes (B-1) Yes (A-1)a R91 Yes (B-1) Yes (B-3) R93 – Yes (A-1)a Yes (B-3)a No (E-3) – – R94 R96 R94 R97 R98 Yes (A-1) Yes (B-1) Yes (B-3) R97 R95 Under revision 2013. 2011 (P = 0.05) (Fig. 1). During this period, the number of procedures in adults with extra corporeal circulation increased from 1100 to 1486, including 590 coronary bypass and 780 valvular surgery procedures. This prevention program chronologically integrated several measures: retrospective analysis of SSI and direct observation of the patient’s skin preparation (2001), prospective surveillance of SSI (2002), drafting and implementation of a new operating mode for the patient’s skin preparation Fig. 1. Incidence of mediastinitis/100 cardiac surgery procedures and chronology of key prevention measures implemented from 2001 to 2011 at the Nantes university hospital. Évolution du taux d’incidence des médiastinites/100 interventions en chirurgie cardiaque et chronologie des principales mesures de prévention implémentées sur une période de 11 ans (2001–2011) au centre hospitalier universitaires de Nantes. Please cite this article in press as: Lepelletier D, et al. Epidemiology and prevention of surgical site infections after cardiac surgery. Med Mal Infect (2013), http://dx.doi.org/10.1016/j.medmal.2013.07.003 +Model MEDMAL-3432; No. of Pages 7 6 ARTICLE IN PRESS D. Lepelletier et al. / Médecine et maladies infectieuses xxx (2013) xxx–xxx including two preoperative showers, preparation of the operative site in four steps with antiseptic soap detergence and applying the double alcoholic antiseptic protocol (2003), using sutures impregnated with antiseptics and oropharyngeal decolonization (2005), a second direct observation of the patient’s skin preparation (2007), surveillance and control of peri-operative glycemia, and using a thoracic compression device for obese patients (2008), drafting a protocol for a 24 or 48 hours antibioprophylaxis according to risk factors (2009), temporary use of a sponge impregnated with antibiotics (2009 and 2010), training new interns on brush techniques, case studies of mediastinitis cases (presented as case-vignettes ([17]) every trimester during multidisciplinary meetings associating cardiac surgeons, hygienists, and cardiologists following patients in the cardiac surgery unit (2012). During this 10-year period, the rate of S. aureus mediastinitis decreased from 50 to 25%, with a single MRSA strain responsible for mediastinitis. No mupirocine nasal decolonization strategy was initiated during the study period. There were 26 cases of mediastinitis after 2858 cardiac surgical procedures in 2010 and 2011, 47% of patients having presented with mediastinitis were diabetic, 40% had a BMI superior to 30. Thirty-three percent had an NNIS risk score superior or equal to 2.43% underwent emergency surgery, and 50% of operations lasted more than 240 minutes (75th percentile). Twenty patients (77%) presented two or more of these five risk factors. 8. Conclusion Despite their relatively low incidence, mediastinitis remains a fearful and feared postoperative infections associated with high morbidity and mortality and important costs. Optimizing their prevention with surveillance and education programs, through a multidisciplinary approach is a true challenge. 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