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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
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(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
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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
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[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
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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
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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. All cardiac
surgery units in France are concerned by the management of
a few cases of mediastinitis every year. Each center must plan
its prevention strategy according to national recommendations
and adapt it to its surgical activity, its patients, and its ecology.
The permanent and strict observance of all mentioned measures
pre-, per- and postoperatively should ensure a quality and safety
approach of healthcare, aimed at decreasing the infectious risk
as much as possible and allowing informing patients.
Disclosure of interest
The authors declare that they have no conflicts of interest
concerning this article.
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