Defining post-sternotomy mediastinitis for clinical evidence-based studies

Abstract

Background

Considerable advances have already been made in the treatment of deep thoracic wound infections following a median sternotomy for cardiac surgery. Further improvement in diagnosis, treatment, and outcome will require a targeted approach by multidisciplinary teams. Clear communication and synergy between the various clinical and supportive disciplines would assist in removing the last barriers to standardized evidence-based studies and the development of improved evidence-based guidelines.

Methods

An extensive literature search without language restrictions was carried out on PubMed (Medline), EMBASE, and Web of Science, covering the period 1988 to week 16, 2014, and a manual search of the reference lists was performed regarding all possible definitions and classifications of post-sternotomy mediastinitis. Two hundred and eighteen papers describing post-sternotomy infections in a multitude of terms were identified, and the strengths and weaknesses of the most popular definitions and terms relating specifically to post-sternotomy infections were examined.

Results

This study revealed that clinicians use a multitude of terms to describe post-sternotomy infections without defining the condition under treatment. Occasionally, older epidemiological (surveillance) definitions were used. It also shows that supportive disciplines have their own definitions, or interpretations of existing definitions, to describe these infections.

Conclusion

The outcome of this study is that clinicians have adopted no single definition, which is essential for further improvement for evidence-based studies. We suggest that it is possible to adopt a single term for thoracic infection after a sternotomy (and only sternotomy), and propose a clinical definition for this purpose.

Keywords

Mediastinitis Mediastinum Sternotomy Surgical wound infection

Introduction

Very recently, the editors of the leading cardiovascular journals (the HEART Group) issued a statement urging all investigators and editors to very carefully select language (descriptive or declarative) that is appropriate to evidence-based studies.¹ Prior to embarking on any evidence-based study, albeit observational, case control, or randomized controlled trial, to evaluate the outcome of an intervention, the terminology and description of the disease or condition to be studied has to be widely accepted and preferably standardized. This also holds true but is not yet the case for the severe thoracic wound infection that could follow a median sternotomy. As broadly as it is known, as widely as it is dreaded, just as prolific are the terms used. “Postoperative mediastinitis”,^2–5 “postoperative sternomediastinitis”,⁶ “post-sternotomy mediastinitis”,^7–12 “post-sternotomy wound infection”,¹³ “deep sternal infection”,¹⁴ or “deep mediastinal wound infection”¹⁵ are some of the many terms used interchangeably with “deep sternal wound infection” (DSWI).^16–23 Still others prefer to use “sternal osteomyelitis” as a synonym.^24–27 Both the American and European Centers for Disease Control (CDC) have meritoriously proffered descriptors and definitions.^28–30 Both of these CDC definitions were developed by epidemiologists for the purpose of surveillance of “health care-associated infections”.^28,29 The latter generic term replaced the term “nosocomial” in 2008.²⁹

When navigating the clinical and surgical literature, it is noticeable that the CDC nomenclature has failed to gain popularity among clinicians dealing with this vexatious condition. The main reasons for this are that surveillance criteria, which are population-based and applied exactly in the same fashion each time, differ from clinical criteria, which are patient-centered and used for therapeutic decisions. Surveillance definitions are thus not always suitable for surgeons. The other members of the multidisciplinary team dealing with these cases (among others, microbiologists, intensivists, radiologists, and cardiologists) all have their own interpretations or definitions, creating further important interdisciplinary differences in understanding. This short article aims to review the practicality of applying surveillance definitions for clinical purposes and to reconcile the nomenclature and definitions. Synergy should facilitate clear interdisciplinary communication and future research, and result in improved evidence-based guidelines as well as recommendations. The purpose of this paper is to critically review all previously proposed definitions and propose a single definition for surgeons and other clinicians

Methods

An extensive literature search without language restrictions was carried out on PubMed (Medline), EMBASE, and Web of Science covering the period 1988 to week 16, 2014, and a manual search of the reference lists was performed in an effort to identify all possible definitions referring to a severe thoracic wound infection following a median sternotomy. Descending or other causes of mediastinitis were excluded. Furthermore, possible classifications of post-sternotomy mediastinitis and related terminology were sought. Initially, publications related to sternal/thoracic wound infections, published since 1974, were screened. As it became obvious that no specific single definition was retrieved from publications before 1988, the study period was commenced to include peer reviewed studies focusing on all aspects (diagnosis and treatment, surgical and nonsurgical) of severe thoracic wound infections following a median sternotomy from that year. Participants in these studies were adult patients (>18 years).

Results

The search strategy resulted in 233 citations. Two hundred and eighteen papers dealing with post-sternotomy wound infections were identified through PubMed, EMBASE, and the Web of Science, and the rest by hand searching or citation tracking. A multitude of terms to describe post-sternotomy infections were identified. In more than 78% of papers, no specific definition was offered. Three specific epidemiological (surveillance) definitions were identified.^28–30 Where clinicians, even in papers of the last five years, mentioned a definition, the older epidemiological (surveillance) definition was preferentially directly or obliquely referred to.²⁸ No alternative clinical definitions were identified, and more recent epidemiological definitions are not mentioned in papers dealing with treatment.^29,30 Other supportive disciplines (assisting in diagnosis) either presented their own definitions or interpretations of existing definitions describing these infections.

The oldest term, namely deep sternal wound infection (DSWI), which is still popular today, evolved from a definition of deep surgical wound infection published by the Centers for Disease Control and Prevention (CDC) in Atlanta, United States in 1988.²⁸ DSWI is defined in Table 1. Two criteria of a DSWI refer to a “fascial layer”.²⁸ One, a main criterion, specifies that the tissues or spaces involved are located “beneath fascial layer” (sic). Another supportive criterion specifies that the purulent drainage should originate from a drain placed “beneath fascial layer” (sic). Purists may have pointed to the well-known absence of a natural protective (fascial) barrier between the sternum and the anterior mediastinum.³¹ It is not known whether this point was taken into consideration by the CDC when they reviewed the definition 20 years later and replaced the term “deep surgical wound infection” with “deep incisional surgical site infection” (DIP).²⁹ DIP is defined in Table 2.

Table 1.

Center for Disease Control definition of a deep surgical wound infection (1988).

Deep surgical wound infection must meet the following criteria:

Infection occurs at operative site:

- within 30 days after surgery if no implant is left in place or

- within 1 year if implant is in place

AND infection appears related to surgery

AND infection involves tissues or spaces at or beneath fascial layer

AND any of the following:

1. Purulent drainage from drain placed beneath fascial layer.

2. Wound spontaneously dehisces or is deliberately opened by surgeon when patient has fever (>38℃) and/or localized pain or tenderness, unless wound is culture-negative.

3. An abscess or other evidence of infection seen on direct examination, during surgery, or by histopathologic examination.

4. Surgeon’s diagnosis of infection.

Table 2.

CDC/NHSN definition of a deep incisional surgical site infection (2008).

Deep incisional surgical site infection must meet the following criteria:

Infection occurs:

- within 30 days after the operative procedure if no implant is left in place or

- within 1 year if implant is in place

AND infection appears related to the operative procedure

AND infection involves deep soft tissues (e.g. fascial and muscle layers) of the incision

AND at least 1 of the following:

1. Purulent drainage from the deep incision, but not from the organ/space component of the surgical site.

2. Deep incision spontaneously dehisces or is deliberately opened by surgeonAND is culture-positive or not cultured

(AND)* when patient has at least 1 of the following:

• fever (>38℃) or

• localized pain or

• tenderness. A culture-negative finding does not meet this criterion.

3. An abscess or other evidence of infection seen on direct examination, during surgery, or by histopathologic examination.

4. Diagnosis of a deep incisional surgical site infection by a surgeon or attending physician.

*(AND) was added to the original definition by the author (JJvW) for purposes of clarity.²⁹ CDC: Center for Disease Control; NHSN: National Healthcare Safety Network.

Three similarities between the 1998 and 2008 CDC definitions are worth highlighting. First, the interval between surgery and presentation specified in both definitions is limited to 30 days in the absence of an implant, or within 1 year if an implant was left in place. Second, wound cultures are not absolutely necessary to confirm the diagnosis (they constitute a minor criterion). Third, note the apparent significance attributed to the fascia in both. In the old definition, the infection had to be “beneath” [sic] the fascia; in the “new” definition of a DIP,²⁹ the fascia itself, among others, has to be involved. However, it is important to pause to draw attention to the addition of the minor criterion (1) in the 2008 CDC definition, which reads: “… but not from the organ/space component of the surgical site”.²⁹ The CDC suggests that following cardiac surgery, once the mediastinum is involved, neither “deep surgical wound infection” nor “deep incisional surgical site infection” is appropriate. It proposed here that the term “organ/space surgical site infection (SSI) of the mediastinum (SSI-MED)”, as defined in Table 3, be adopted instead.

Table 3.

Center for Control definition of an organ/space surgical site infection of the mediastinum (2008).

Mediastinitis (in adults) must meet at least 1 of the following criteria:

1. Patient has organisms cultured from mediastinal tissue or fluid obtained during a surgical operation or needle aspiration.

2. Patient has evidence of mediastinitis seen during a surgical operation or histopathologic examination.

3. Patient has at least 1 of the following signs or symptoms with no other recognized cause: fever (>38℃), chest pain, or sternal instability.

AND at least 1 of the following:

• purulent discharge from mediastinal area

• organisms cultured from blood or discharge from mediastinal area

• mediastinal widening on radiography

As mentioned previously, some clinicians still favor the term “sternal osteomyelitis”.^24–27 Careful perusal of the data of these studies shows that it was always used to include mediastinitis or used as a synonym. A separate definition, other than in those rare cases where bone biopsies of the sternum only were taken, was seldom proffered in these studies. The European Centre for Disease Prevention and Control (ECDC) does make such a distinction; it recommends “mediastinitis following cardiac surgery that is accompanied by osteomyelitis”, and only then is reported as an organ/space SSI (SSI-O).³⁰ The ECDC guideline thus seems to distinguish between mediastinitis following cardiac surgery, which occurs without involvement of the sternum, and that which does (Table 4). The American CDC is quite clear in its current recommendation that after cardiac surgery, their definition of SSI-MED rather than SSI-BONE (which osteomyelitis implies) would apply.²⁹ By recommending that mediastinitis that develops after cardiac surgery be reported as an SSI-O, the ECDC clearly takes a different position from the American CDC. These are two different definitions and the reason for this is not clear, more so as the ECDC has a separate definition for reporting mediastinitis, which apart from being a different term (Cardiovascular System Infection-Mediastinitis, or CVS-MED for short), is almost a mirror image of the CDC definition of an SSI-MED (Table 5).³⁰

Table 4.

European Centre for Disease Prevention and Control definition of an organ/space surgical site infection.

Infection occurs

- within 30 days after the operative procedure if no implant is left in place or

- within 1 year if implant is in place

AND infection appears related to the operation

AND infection involves any part of the anatomy (e.g. organs and spaces) other than the incision, which was opened or manipulated during an operation

AND at least 1 of the following:

• purulent drainage from a drain that is placed through a stab wound into the organ/space

• organisms isolated from an aseptically obtained culture of fluid or tissue in the organ/space

• an abscess or other evidence of infection involving the organ/space that is found on direct examination

• diagnosis of organ/space surgical site infection made by the surgeon or attending physician

Table 5.

Surveillance definitions: advantages and disadvantages.

Definition	Institution	Year introduced	Advantages	Disadvantages
Deep surgical wound infection²⁸	ACDC	1988	Broad, includes “tissues or spaces”	Short time-span (<30 days), anatomically incorrect (beneath fascial layer)
Deep incisional surgical site infection²⁹	ACDC	2008	Includes “tissues” (fascia ± muscle)	Excludes “spaces” (including mediastinum)
Organ/space surgical site infection of the mediastinum²⁹	ACDC	2008	Broad, anatomically correct	Short time-span (<30 days), radiologically too narrow
Organ/space surgical site definition³⁰	ECDC	2012	Includes “organs and spaces”	Short time-span (<30 days), anatomically confusing: includes infections “limited” to the sternum; excludes incisions into “spaces”
Cardiovascular system infection of the mediastinum³⁰	ECDC	2012	Broad, similar to surgical site infection of the mediastinum	Short time-span (<30 days), anatomically confusing: includes infections of the mediastinum; excludes sternum

ACDC: United States Centers for Disease Control and Prevention; ECDC: European Centre for Disease Prevention and Control.

Discussion

The first question that should be addressed is whether a single term can be considered for describing an infection following a sternotomy that extends beyond the subcutaneous soft tissue of the wound, i.e. once bone (the sternum) is involved, can be considered. The various terms for a non-superficial wound infection following a sternotomy seem to suggest that unique disease entities exist. This may not necessarily be so for several reasons: first, there is no natural barrier between the sternum and the mediastinum;³¹ second, results from several studies suggest that swabs and cultures from the superficial tissue alone have a high predictive value and for staphylococci, they almost always match those of the mediastinal (deep) soft tissues;^23,24 and finally, clinical experience has shown that the progression of disease may be halted by early diagnosis and application of negative-pressure therapy.^9,11 The clinical appearance at the time of diagnosis may thus, more likely, simply represent a stage in the spectrum of the same disease process rather than a particular disease entity.

When looking at the suitability of adapting one of the surveillance (epidemiological) definitions for clinical purposes, each criterion has to be carefully considered. One of the core criteria in both the American CDC guidelines of 2008 and the ECDC guidelines of 2012 for the diagnosis of an SSI, whether a (deep) incisional or organ/space SSI, is timing of the presentation: infection should “occur” (sic) in the operative field within 30 days following surgery when no permanent implant was used, or within a year when an implant was left in place.^29,30 There is currently a considerable body of evidence pointing towards a rising number of post-sternotomy infections that present later than 30 days after cardiac surgery in patients in whom an implant had not been placed.^27,32,33 Why is this and what is the significance? There has been an alarming and significant increase in the incidence of post-sternotomy mediastinitis (PSM) due to slower-growing pathogens such as (the deceptive) coagulase-negative staphylococcus (CoNS) and certain fungi since 1997.^2,11,34,41 This shift in the spectrum of causative pathogens has been reported and may have accelerated in recent years.⁴² Up to 2007, Staphylococcus aureus and/or CoNS were the most prevalent pathogens encountered in PSM.^43,44 In a study covering 15 years, Matros and colleagues¹⁸ found CoNS to be the most prevalent pathogen in 49% of 285 patients with PSM, and Baillot and colleagues⁴⁵ found the same in 49,6% of 267 patients. One recent study reported an incidence of CoNS of 62%.⁴⁶ The subtle change is well illustrated in a study by Steingrimsson and colleagues⁴⁷ who identified CoNS as the sole pathogen in 70% of cases of PSM between the years 2005 and 2010, compared with only 30% between 2000 and 2005 (p = 0.01). In addition, a recent study revealed a remarkably high clonal colonization of Staphylococcus epidermidis across cardiac centers in the United States, with 48% of the typed isolates belonging to 1 of 7 clonal types, as defined by pulsed-field gel electrophoresis.⁴⁸ These 7 were the most commonly shared clusters, not restricted to particular clinical centers, and were more likely to be resistant to methicillin and a number of other antimicrobials. In another study, the isolates from patients with CoNS-related PSM produced biofilms significantly more frequently when compared with contaminants (p < 0.001).⁴⁹ The recent advance in slow-growing pathogens has to be taken into consideration in any definition of PSM.

Some have warned of the emerging role of candida, another slow-growing pathogen, in the development of PSM.^50–54 Whereas candidal mediastinitis following cardiac surgery used to be exceedingly rare,⁵⁰ an incidence reaching 20% has recently been reported.⁵¹ Why may this be of importance? A significant change in the cardiac surgical patient population in terms of age and other comorbidities as well as improved surgical techniques and intensive care management has contributed to a rise in surgery for the more infirm (and susceptible). In addition, some candida species are survivors, by their ability to form a hypoxic biofilm in deeper structures, despite conventional antifungal therapy.⁵⁵ Furthermore, elegant studies indicate that in mixed-species biofilms of candida and Staphylococcus epidermidis (CoNS), the fungal cells can protect staphylococci against vancomycin. Conversely, biofilm produced by staphylococci may inhibit fluconazole penetration.⁵⁶ In addition, staphylococci may assist in inhibiting phagocytosis of candida cells.

Strict application of the 30-day criterion in the current era could thus lead to the exclusion of a significant number of patients suffering from a serious post-sternotomy infection. In a protocol edit published in July 2013, the American CDC recommended increasing the period of surveillance following coronary artery bypass graft surgery to 90 days.⁵⁷ We believe that this is a step in the right direction: regardless of the specifics of the definition used, increasing the surveillance period to one year for all (whether an implant was used or not) would reduce miscalculation and simplify reporting. It could be fairly argued that this may lead to an increase in diagnosis. However, since both the cost and complexity of treating a PSM are significantly cheaper and simpler when diagnosed earlier rather than later,^58,59 it is defendable. It would be economically wiser to identify those patients with an increased risk of CoNS-related PSM early than to adhere strictly to the suggested interval of 30 days between surgery and presentation. Patients particularly at risk for CoNS-related PSM are those afflicted by diabetes mellitus,³⁵ by chronic obstructive pulmonary disease, or obese patients, especially when a prolonged preoperative stay was required or where an incision drape was used during a lengthy operation.^41,60

Finally, recent data confirm that biofilms more frequently accumulate on sternal wires in PSM.^49,61 The sternal wires are the first to be removed in PSM, not only to gain access to the infected mediastinum but also because clinically, they behave no differently from other biomedical implants. Surgeons treat them no differently. Surveillance (CDC) definitions of PSM incorporate the increased risk of using implants and advise the period of surveillance to be increased from 30 to 365 days (1 year). If the behavior of sternal wires (especially once covered by a biofilm) is regarded as similar to that of other implants, it would almost automatically (even from an epidemiological point of view) strengthen the argument for a 1-year (instead of the 30 days) surveillance period.

DSWI is still a universally popular term with surgeons. However, the definition of a DSWI, as published by the CDC in 1988 and from which DSWI derived, indicates that the infection involves “tissues or spaces” (Table 1). The definition continues by specifying that these tissues or spaces are to be found at or beneath a fascial layer, which anatomists and surgeons alike know does not exist between the sternum and the anterior mediastinum. This, and the fact that the definition of DSWI has since been replaced by the Centers, make good arguments for dropping the term DSWI altogether. The new definition, introduced by the CDC in 2008,²⁹ suggests that fascia should be involved. Theoretically, this could refer to the fascia surrounding some of the deeper vital structures in the mediastinum, which in turn would allow for the interpretation that the definition of a DIP is applicable to post-sternotomy mediastinitis.²⁹ However, the DIP definition continues in point (1) to specify that “the organ/space (Table 2) component of the surgical site” is excluded. Thus neither the nomenclature of DIP nor the contents of its definition is applicable for a clinical definition of PSM.

The critical appraisal of the various (CDC) surveillance definitions above suggests that, but for two criteria, the SSI-MED definition, with the wording given in the American CDC guideline of 2008,²⁹ could be suitable as a clinical definition of PSM. Our recommendation (Table 6) is that the definition be adopted as a clinical definition with two changes: prolong the interval between (cardiac) surgery and presentation to 1 year, for the reasons given above; and replace “mediastinal widening on X-ray” with “radiological evidence of an infective process in the mediastinum”. The reason for the latter change is to encompass the rapidly increasing evidence provided by advanced radiological investigations (specifically, computed tomography and scintigraphy) that has become available of late.^62–65 Novel biomarkers and proxies are certain to follow in the near future.⁶⁶ One advantage of adopting the larger part of an existing definition is that verification only, rather than validation, is necessary. Verification is slightly different from validation. Only verification through the provision of new data, ideally from multiple clinical investigators, will confirm (or refute) whether the objectives of the currently proposed clinical definition have been met. Thereafter, the clinical definition is subjected to a process of continuous validation.

Table 6.

Amsterdam definition of post-sternotomy mediastinitis.

Post-sternotomy mediastinitis (in adults) must meet the following criteria:

Infection occurs within 1 year, regardless of whether an implant is in place or not

AND infection appears related to the operative procedure

AND at least 1 of the following criteria:

1. Patient has organisms cultured from mediastinal tissue or fluid obtained during a surgical operation or needle aspiration.

2. Patient has evidence of mediastinitis seen during a surgical operation or histopathologic examination.

3. Patient has at least 1 of the following signs or symptoms with no other recognized cause: fever (>38℃), chest pain, or sternal instability

AND at least 1 of the following:

a. Purulent discharge from mediastinal area

b. Organisms cultured from blood or discharge from mediastinal area

c. Radiological evidence of an infective process in the mediastinum.

If the premise that the mediastinum, due to its unique location, is exposed to what Jones and colleagues⁶⁷ have so eloquently described as a “continuum of clinical entities” is embraced by all disciplines, a single definition for PSM should suffice. The clinical appearance at the time of diagnosis is a reflection of the stage of the disease, which in turn is dependent on the severity of the infective process. The severity of the affliction is determined by the virulence of the causative microorganism and the ability of the patient to combat its progress. Why the term post-sternotomy mediastinitis? Building on a further premise that all surgical disciplines share, a single term for the spectrum of clinical entities just described will provide the necessary clarity. This is that the mediastinum is always (to a greater or a lesser extent) involved in any thoracic wound infection after a sternotomy, and the debridement thereof is taken as seriously as that of the more superficial bone and soft tissue. Compartmentalization is unnecessary.

For post-sternotomy cases specifically (on which this paper focuses), terms such as postoperative or postsurgical mediastinitis could be misleading. In this context, their use should preferably be discouraged. Descending necrotizing or fulminating mediastinitis originating from an iatrogenic perforation during central venous catheterization, endoscopic treatment of a Zenker diverticulum, transcervical spinal surgery, or tracheal bougienage are all postoperative and postsurgical. Such mediastinitis is not uncommon,⁶⁸ but is in many ways different from post-sternotomy mediastinitis following cardiac surgery. The term PSM is compact, concise, and popular.^7–12 It is not controversial. The mediastinitis is clearly linked to a recent surgical procedure (post-) and the procedure is specified (sternotomy). Universal acceptance of the proposed clinical definition and terminology would allow standardization. Tools such as computerized data entry forms and classification are developed from the standardized descriptors and terminology necessary for evidence-based studies. To this purpose, we propose that PSM be adopted as the preferred term for describing an infection following a sternotomy, which extends beyond the subcutaneous soft tissue of the wound, i.e. once bone (the sternum) is clearly involved.

This extensive review of 218 peer-reviewed papers published between 1988 until the beginning of 2014, dealing with all aspects (diagnosis and treatment, surgical and non-surgical) of severe thoracic wound infections following a median sternotomy, shows that no single definition has been universally adopted by all clinicians, and surgeons in particular. It furthermore shows why definitions developed for surveillance purposes are not completely appropriate for clinical purposes but could serve as an important framework from which a clinically suitable definition could be developed.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

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