Preventing Surgical Site Infections

Ilker Uçkay; Stephan Harbarth; Robin Peter; Daniel Lew; Pierre Hoffmeyer; Didier Pittet


Expert Rev Anti Infect Ther. 2010;8(6):657-670. 

In This Article

Preventing SSI


Most SSIs are believed to be acquired during surgery.[48] This is supported by the success of SSI prevention measures directed towards activities in the operating theater and a few reports demonstrating matching strains of pathogens from the surgeon's fingers and postoperative infection.[49,50] However, despite much research on SSI, there are currently no data on the actual proportion acquired in the operating theater versus post-operative care on wards. Similarly, within the subgroup of SSIs acquired during surgery, the proportion originating from the patient versus that transmitted by the surgical staff, operating theater procedure or the environment remains unknown.

Independent Risk Factors for Surgical Site Infection

Over the past decades, identified risk factors have been assessed through epidemiological studies due to a lack of knowledge of the detailed pathogenesis of SSIs. The literature reports dozens of independent risk factors, mostly assessed by retrospective case–control (Table 3) or before–after quasi-experimental studies. In this article, we only discuss the risk factors that have been shown to be independent determinants by multivariate analysis. Among the most frequently cited are diabetes mellitus,[11] age,[10] obesity[9] and incorrect or lack of antibiotic prophylaxis;[51] other mentioned factors, such as low socioeconomic status[52] or postoperative pain,[53] have not been thoroughly investigated.[54] It is likely that with the construction of large databases for nationwide surveillance programs, new and as yet unidentified risk factors will emerge from research. Data on the clinical impact related to both endogenous and exogenous independent risk factors reveal risk indices oscillating between 1.3[10] and 4.5[11] (Table 3). Approximately half of all identified risk factors are endogenous and difficult to modify in the immediate preoperative and perioperative phase. For exogenous risk factors, past experience has identified those with the best and least costly chance to decrease SSIs (Table 4).

Evidence-based Preventive Measures

At present, four preventive measures are considered as having a high level of evidence (grade IA) according to major evidence-based guidelines:[1,12] surgical hand preparation;[55] appropriate antibiotic prophylaxis;[1,3] and postponing of an elective operation in the case of active remote infection.[1] Although hair clipping before surgery was considered grade IA evidence in the 1999 CDC guidelines,[1] this high grading is now a matter of debate.[56–58]

Surgical Hand Preparation Surgical hand preparation[55] is probably the most important SSI prevention strategy, although there is no strict randomized study comparing surgery with and without previous hand antisepsis preparation sensu strictu. Its importance is supported by expert opinion,[16,55,59,60] experimental studies[61] and success stories of SSI reduction via mere hand hygiene promotion campaigns.[60,62] However, owing to their multimodal design, most hand hygiene campaigns cannot distinguish between SSI reduction due to improved antisepsis in the operating theater versus better patient and wound care on the ward. Few interventions have targeted the operating theater as in the seminal intervention of Ignaz Semmelweis (1818–1865) who recognized that the incidence of puerperal fever was high in his obstetric clinic. After the compulsory introduction of hand antisepsis for obstetricians using chlorinated lime, he succeeded in lowering the incidence of this life-threatening, postpartum maternal infection.[63] A cluster-randomized, crossover trial recently reported the equivalence of surgical hand preparation with unmedicated soap and water versus alcohol-based handrub on postoperative SSI rates.[64] Parienti et al. reported the equivalence of a handrubbing protocol with a 75% alcohol-based solution versus a handscrubbing protocol containing 4% povidone-iodine or 45% chlorhexidine gluconate in terms of SSI prevention.[65] A Cochrane review also addressed the issue of preoperative surgical hand preparation.[66] Hand rubbing with an alcohol-based formulation was considered as effective as scrubbing, for which the ideal duration remains unknown,[67] although it is probable that the minimum duration is 2–3 min for both techniques.[55] Either alcohol-based hand rubs or aqueous antiseptic scrubs can then be subsequently used between patients, provided hands are not visibly soiled.[16,55] However, the rapid antimicrobial action, wider spectrum of activity, lower side effects and the absence of the risk of hand contamination by rinsing water in resource-poor areas might favor alcohol-based solutions.[16,55,64] Brushes are not recommended for surgical hand preparation.[16,55,67]

Antibiotic Prophylaxis The effectiveness of the administration of preoperative antibiotic agents can be assumed,[1,3,12,51,68–70] at least for most surgical interventions. Exceptions are clean elective surgery without foreign material, for example, hernia repair, removal of implant material, dermatologic surgery[71] and some foot and ankle surgery,[3] where the number-to-treat needed to prevent one SSI episode might be too small to justify routine administration for a few superficial easy-to-treat SSIs. In orthopedic implant surgery, prophylaxis helps in reducing SSI rates from 4–8% without antibiotics to 1–3%, according to trials performed in the 1970s and 1980s.[3,51,72–77]

Successful and adequate prophylactic antibiotic use depends on a number of key principles: the patient's individual history of allergy must be considered; first- or second-generation cephalosporins are sufficient for most types of surgery.[3,68] The proportional distribution of SSI pathogens has remained stable over the last two decades,[1] even if the recent challenge of community-acquired methicillin-resistant Staphylococcus aureus (MRSA) and other resistant pathogens might become a threat in the future.[68] In the case of skin colonization with methicillin-resistant staphylococci, a glycopeptide antibiotic is recommended.[1,3,68] Some experts advocate that general vancomycin prophylaxis may be appropriate in settings with more than 20% MRSA prevalence,[68] but from an epidemiologic standpoint, there is no threshold for routine glycopeptide prophylaxis in settings with endemicity for methicillin-resistant staphylococci.[78,79] Furthermore, there is no evidence that a glycopeptide would be superior to cephalosporins for patients without MRSA carriage.[3] With a few exceptions, such as dermatologic or cataract surgery,[39] antibiotics have to be administered parenterally without adaptation of the recommended dose for renal insufficiency. Suboptimal dosing is a risk factor for SSI.[6,68] An additional benefit of antibiotics in irrigation fluid[3] or of antibiotic-loaded cements in primary arthroplasty surgery[80] has not yet been proven. Timing is of the utmost importance[6,68,81] and prophylaxis should be within 1 h before incision.[81] Recent reports attempted to further define the optimal time frame for administration of antibiotic prophylaxis, but showed contrasting results. While two studies identified the best time window as between 0 and 30 min before incision,[37,82] another from Switzerland identified a delay of 30–60 min to be superior in terms of SSI reduction.[83] Undoubtedly, this debate will continue until definitive research is conducted, ideally using a cluster-randomized crossover trial. One dose is sufficient.[84] For operating procedures longer than 4 h or in the case of significant blood loss, redosing may be justified,[3,82] but this recommendation depends on the half-life of the antimicrobial agent. At present, it remains unknown if a repeated administration should use the same or a reduced dosage, but there is no advantage of a continuous versus intermittent infusion in the case of redosing.[78,84] In any case, a prolongation of prophylaxis beyond 24 h postoperative is of little benefit (except for surgery of large burn wounds where pre-emptive administration of antibiotics may be beneficial beyond 24 h)[3,68,85] and favors the acquisition of antibiotic resistance, particularly among Gram-negative pathogens.[86] When a tourniquet is used, the entire dose should be administered prior to its inflation.[3,87] At present, it remains unknown whether standard doses should be routinely enhanced for obese patients, for instance, patients with a BMI of more than 30 kg/m2 or higher. Different experts recommend a higher prophylactic dose for selected pathogens or infections,[88] but this is an empirical opinion and no clinical trials have demonstrated the advantage of this approach so far.

Postponing Elective Surgery in the Case of Symptomatic Remote Infection This issue is regarded as high evidence in the CDC guidelines,[1] although there are no randomized trials on the topic of postponing to the best of our knowledge. However, a number of case series and retrospective studies exist reporting a hematogenous origin for total joint arthroplasty infections and secondary infections of other orthopedic implants. Although the incidence of true hematogenous arthroplasty infections in the case of active remote infection is probably lower than formerly believed,[28,89] most experts agree that elective surgery should be postponed until the remote infection is cured. The necessity to postpone in the case of asymptomatic bacteriuria[90] or even urinary tract infection[91] in elective orthopedic surgery or nonimplant-related surgery is less certain. Common sources of hematogenous implant infections are often the skin, the GI tract or the lungs.[28]

Other Measures with High Efficacy

Expertise of the Surgeon The surgeon's expertise and surgical technique is probably very important, although subjective and difficult to analyze.[12] Furthermore, it is almost impossible to perform a randomized trial on this subject. An excellent surgical technique is believed to reduce SSI by: maintaining effective hemostasis while preserving adequate blood supply; gentle handling of tissue; removal of devitalized tissue; eradication of dead space; and appropriate management of the postoperative incision.[1] These techniques can be learned and it has been suggested since the mid-1980s that surgical simulation has a beneficial impact on surgeons' experience and performance.[92]

Active Surveillance with Feedback

Decreases in SSI rates have been observed in national surveillance networks in European countries, such as France,[10,22,93,94] Germany[35,95] and The Netherlands.[24,25,96] An active surveillance programme may decrease SSI rates by merely reporting data without any other formal interventions.[22] Some experts question whether studies using data from national surveillance networks can be used to support the effectiveness of surveillance with feedback as there is no information about other interventions implemented in the many hospitals that have contributed to the data. However, the reports do not mention these theoretical aspects. In 1985, the Study on the Efficacy of Nosocomial Infection Control (SENIC) showed that the presence of a dedicated infection control team, together with surveillance and feedback of observed data, resulted in a 38% decrease of SSIs among participating hospitals.[97] However, the structural mechanism of implementing such a strategy is complex and requires engineering changes in behavioral[98] as well as system aspects. In addition, it differs according to the setting and takes several years to develop gradually to its full effectiveness,[35,94] although the impact can be very powerful, with reports ranging from a 25[35] to 50% decrease in SSI rates[94] within 4–6 years following implementation.

Multimodal Intervention Instead of targeting single risk factors, it is advised to target several at the same time, although they are usually based on pre–post intervention studies and not randomized trials or meta-analyses. Multimodal interventions, sometimes in the form of so-called 'bundles', have become very popular in recent years.[99] A variant are safety checklists[15] that have been inspired from the airline industry. The multimodal approach does not need to cover all potential risk factors. Local,[7,11] nationwide ('100k lives' campaign'[13] and Surgical Care Improvement Project[6,14]) and global (World Health Organization Global Patient Safety Challenges 'Clean Care is Safer Care' and 'Safe Surgery Saves Lives'[15,17]) intervention programs rely on only three to six key targets and have achieved substantial results. For example, Trussell et al. implemented a quality care initiative including peri-incisional antibiotic prophylaxis, close glucose control and hair clipping and reported 1.5% SSIs in the intervention group compared with 3.5% in the comparator arm.[11] The USA's 100k lives program recommended correct antibiotic prophylaxis, glucose control and intraoperative normothermia, and achieved a 27% reduction in SSI rates.[13,202] Globally, the WHO strategies are effective through education programs, use of alcohol-based hand rub and access to safe surgical care. Multimodal interventions based on bundles or checklists are the strategy with the highest impact in terms of SSI prevention.

Preventing SSI: Promising Avenues of Research

The recent literature offers promising new measures for the prevention of SSI. Although they may appear to be contradictory to some extent at the present time, these measures represent possibilities for future research and development.

Screening for MRSA Carriage on Admission The rationale behind this approach is to detect MRSA skin carriage before incision, identify carriers and administer glycopeptide prophylaxis in the case of known carriage.[1] However, the results of several outstanding prospective trials in recent years are inconclusive. While some before–after studies[100–102] report a benefit, other crossover design trials[103,104] fail to show a reduction in SSI rates (or at least in SSI rates due to MRSA). Therefore the final outcome of this debate remains open.

Screening for Nasal S. aureus Colonization & Decolonization An observational study in patients undergoing cardiac surgery found a higher incidence of SSI in S. aureus nasal carriers than in noncarriers (12.5 vs 5%).[105] Subsequent studies were inconclusive. Some demonstrated that although the intranasal use of mupirocin reduced the overall incidence of S. aureus infection, a reduction in overall SSIs was not observed.[106] Others attributed a reduction in S. aureus nasal carriage only, but not in SSIs.[107] For general surgery, a large trial[108] and a meta-analysis[109] failed to reveal a benefit of nasal decolonization in terms of SSI decrease. Other reports claimed that preoperative S. aureus decolonization reduces SSIs,[110,111] including a meta-analysis of eight randomized trials (relative risk: 0.6; 95% CI: 0.4–0.7).[106] Very recently, a multicenter, double-blind prospective trial assessing S. aureus carriage at admission by PCR and subsequent nasal and total body decolonization during 5 days found significantly reduced hospital-acquired S. aureus among surgical and medical S. aureus carriers. However, results for SSIs due to non-S. aureus were not reported.[112] Further randomized trials are required to assess the usefulness of this preventive measure for surgery in general, or to identify subpopulations of patients in whom this approach would be beneficial.[3]

Avoidance of Intraoperative Hypothermia The intraoperative period is important in terms of SSI prevention and leaves room for measures not targeting the transmission of pathogens, but rather enhancing patient immunity. Perioperative hypothermia is common and is estimated to occur in about half of all surgical patients.[113] Several trials and a systematic review[114] reported the importance of maintaining normothermia during anesthesia (above 36°C). This requires close collaboration with anesthesiologists and is not easy to implement, but the benefits seem to be substantial.[115] The primary beneficial effects of warming are mediated through increased blood flow and oxygen tension at the tissue level,[113] but there are also other mechanisms. Many biological systems in warm-blooded animals are temperature-dependent. Hypothermia has been shown to affect molecular interactions and cellular functions in a number of systems, including coagulation, viscosity and the hematocrit, and the immune and endocrine systems. These effects, either alone or in combination, have also been shown to translate into serious clinical consequences.[113] In clinical practice, Melling et al. performed a randomized study among 421 patients undergoing clean surgery; one group with perioperative warming, and the other group without. While SSI risk was 14% in the non-warmed patient group, it was only 5% among the warmed patients. This difference was highly significant.[116]

Avoidance of Intraoperative Hyperglycemia Similar to the avoidance of hypothermia, maintaining intraoperative normoglycemia (<200 mg/dl) throughout surgery and some hours beyond is regarded to be of benefit,[8,117,118] although the evidence surrounding glycemic control is of mixed opinion in the literature.[119] A Cochrane review identified five randomized trials on this topic. None evaluated strict glycemic control in the immediate preoperative period or outside the intensive care unit. Owing to heterogeneity in patient populations, glycemic target and definitions, a combination of the results into a meta-analysis was not appropriate.[119] Nevertheless, glycemic control is used as a cornerstone of SSI prevention in many trials or settings. For example, the USA's 100k lives campaign incorporated normothermia and normoglycemia as the cornerstones of their surgical intervention bundle.[13,202] Normoglycemic patients do not only carry a lower risk for SSI, but are also at lower risk for stroke, urinary tract infection, ileus, postoperative hemorrhage and death.[118] The benefit of normoglycemia seems to be independent of HbA1c values or pre-existent diabetes mellitus.[117] Nevertheless, insulin should not be routinely given to all patients for the purpose of reducing the risk of SSI. This is another area where further research is required.[12]

Supplemental Oxygen Intraoperative-administered fraction of inspired oxygen of less than 50% was identified as an independent risk factor for SSI.[120] A randomized, double-blinded multicenter trial allocated patients to receive either 80 or 30% oxygen throughout surgery and 6 h postoperatively[121] and showed a 39% reduction of SSI rates in the 80% arm. Conversely, another study among cesarean delivery patients showed no benefit,[122] while a third study had to be terminated early because the frequency of infection increased with supplemental oxygen.[123] Some later studies advocate the benefit of supplemental oxygen in colorectal surgery[121,124] and a recent meta-analysis of five articles attributed a preventive effect, at least in colorectal surgery (SSI reduction of 25%).[125] However, another recent study involving general surgery patients failed to yield a benefit in terms of SSI reduction or atelectasis prevention and the debate continues.[126] From a physiological point of view, SSI reduction with supplemental oxygen is believed to be related to low oxygen partial pressure (tension) in surgical wounds and enhanced oxidative killing of leukocytes with oxygen supply.[127]

Other Measures yet to be Confirmed in Future Trials Several new approaches show promising results in randomized trials, but have been reported only once or on very few occasions. As an example, Dutch investigators reported that naso- and oropharynx decontamination with chlorhexidine before cardiac surgery significantly lowered deep SSIs, bacteremia and lower respiratory tract infections.[128] This needs confirmation in further trials as a similar approach failed to show any benefit for ventilator-associated pneumonia.[129] Further concerns about the potential for chlorhexidine resistance, in particular among staphylococci, require further study and explanation.[130] The future will show if continuous, positive airway pressure during anesthesia significantly lowers the risk for several HAIs by avoidance of postoperative hypoxemia.[131] Another debate concerns whether minimal invasive surgery or the use of laparoscopy versus laparotomy may lower SSI risk.[35,99,132]

SSI Prevention: Widespread Measures with Low Evidence

Some measures used in daily practice are profoundly embedded in our medical culture, but nevertheless lack evidence as to their real efficacy. Substantial new evidence is needed to upgrade these recommendations.

Preoperative Bathing or Showering There is currently no evidence that preoperative showering with an antiseptic agent reduces SSI rates, despite the fact that it has been shown to reduce skin colonization.[1] The CDC recommends that patients shower or bathe with an antiseptic agent prior to surgery,[1] while NICE recommends the use of soap only.[12] A Cochrane review including six trials with 10,000 participants found no evidence for the superiority of preoperative bathing and showering versus placebo.[133]

Preoperative Skin Preparation Skin preparation in the operating theater immediately before surgery is routinely implemented in daily clinical practice worldwide, based on expert opinion.[1] However, even with optimal preparation, true sterilization of the skin is impossible. To the best of our knowledge, there is no consensus on the best antiseptic agent to be used, although, very recently, a prospective randomized nonblinded study revealed a superiority of 2% chlorhexidine combined with 70% isopropyl alcohol versus 10% povidone-iodine for preventing SSI after clean-contaminated surgery.[134] For several decades, povidone-iodine[135] or chlorhexidine[130] have been generally used for skin antisepsis. The development of bacterial resistance (mostly among staphylococci and Pseudomonas aeruginosa) to chlorhexidine has been acknowledged and its clinical impact is the subject of ongoing studies.[130] Skin preparation in concentric circles versus a back-and-forth motion has no significant impact on SSI,[136] and surgical site marking does not affect antisepsis of the surgical field.[137]

Gloves & Adhesive Drapes Sterile gloves and adhesive drapes are almost always used in the operating theater. They contribute to prevent site contamination, but also reduce blood-borne pathogen transmission from patients to surgeons.[55] However, many gloves reveal tiny punctures after use that mostly go unnoticed by the operating team[55,138] and may double the SSI risk.[55,139] Hence, the use of sterile gloves does not render surgical hand preparation unnecessary.[55] Double-gloving or glove-changing might reduce the risk of punctures,[55,140] but does not guarantee their absence.[55,141] A Cochrane review of 26 trials conducted on the practice of double gloving as a barrier precaution was inconclusive in terms of SSI reduction.[141] Similarly, the use of adhesive drapes failed to yield a protective effect on postoperative SSI rates.[142] Regarding the use of gowns, there are limited data to understand the relationship with SSI risk.[1] Extended antisepsis measures within the operating theater, such as routine glove changing, use of iodine-impregnated foils, and ear and neck caps, failed to provide an additional benefit.[54] Many will continue to be used, or even recommended, despite the lack of evidence to prove the appropriateness of their application.

Preoperative Hair Removal Clipping versus shaving in case of hair removal is classified as grade 1A evidence in the 1999 CDC guidelines,[1] but has been questioned in a recent meta-analysis[56] and additional publications.[57,58,143] If hair removal is performed, this should be carried out with clippers and not razors[38] immediately before surgery and not the previous evening.[1,38,56] A Cochrane review in 2006 identified 11 publications on this subject. Three trials involving 625 patients compared hair removal using either depilatory cream or razors with no hair removal and found no statistically significant difference between the groups in terms of SSI. No trials were identified that compared clipping with no hair removal. Three trials involving 3193 patients compared shaving with clipping and found that there were statistically significantly more SSIs when individuals were shaved rather than clipped. Seven trials involving 1420 patients compared shaving with hair removal using a depilatory cream, but found no statistically significant difference in SSI rates between the two groups. No trials were found that compared clipping with a depilatory cream. The evidence found no difference in SSIs among patients who have had hair removed prior to surgery and those who have not.[58]

Laminar Airflow in the Operating Theater In 2008, several drawbacks of laminar air flow in the operating theater were identified. Many hospitals in resource-rich countries are equipped with relatively expensive vertical or horizontal laminar airflow systems that reduce the bacterial burden in the air.[67,72,144,145] A previous study questioned its use in terms of SSI reduction,[44] while other reports suggested a benefit for some types of surgery.[67,76,145] A retrospective analysis of the German national HAI surveillance system recently showed no reduction of SSI with laminar airflow versus no laminar airflow.[146] However, this study has some limitations, such as a lack of information on individual antibiotic prophylaxis, and presence of obesity or normothermia, and requires confirmation by other large-scale studies.[147]

Oral Mechanical & Antibiotic Bowel Preparation A recent meta-analysis including 14 trials and 4859 patients failed to demonstrate a benefit of mechanical bowel preparation before colorectal surgery in terms of reduction of SSI or anastomotic leakage.[148] Of note, the NICE guidelines do not recommend mechanical bowel preparation.[12] The use of oral antibiotics during preparation is also under debate, with preliminary results hinting at a possible effectiveness,[69] but further trials are needed to provide more definitive evidence.

Other Practices This review would be incomplete without mention of the use of staples versus sutures[149,150] or the use of drains;[130] both are reported to be similar in terms of SSI risk. Some studies concluded that primary closure in dirty abdominal surgery leads to less SSIs than delayed primary closure,[151] whereas others report the opposite.[152] Microbial sealing (with mechanical blockage of pathogen migration to the surgical wound) may be a new approach to reduce wound contamination,[153] but this has yet to prove its effectiveness in reducing SSI rates. A prospective randomized study[154] on postoperative pin care and a Cochrane review including six trials reported that no regimen (daily vs weekly, cleansing vs no cleansing) is superior to others.[155]

Postsurgical Wound Care There is a paucity of literature on surgical wound care and SSI prevention, in contrast to the many reports on the care of central lines after insertion.[31,156] Clearly, hands must be cleaned before and after wound care.[16,59] A randomized trial in Togo assessed the need for surgical wound care after abdominal surgery.[157] After wound closure, patients were randomized to either a group undergoing dressing change every 2 days or a group whose wounds were left open to the air after a first dressing change at 48 h. There was no difference in the occurrence of SSIs, even under warm and humid climatic conditions.[157] More than a mere decrease of SSIs, dressings might influence the avoidance of blistering.[158] A Cochrane review assessed the effectiveness of various dressings and topical agents on surgical wound healing (and infection) and concluded that the quality of the trials was insufficient to determine any superiority of one protocol or one topical agent over another.[159] Other randomized studies comparing occlusive versus gauze dressings equally failed to detect superiority in terms of SSI reduction or wound healing.[160–162] To the best of our knowledge, the potential preventive role of silver-coated antimicrobial barrier dressings for noninfected surgical wounds is currently unknown.

Public (mandatory) Reporting of HAI & SSI Rates Public reporting of HAIs or SSIs is mandatory or under discussion in several states[163] or private institutes[164] in the USA, but less so in Europe. The scientific basis for such reporting is scarce and a CDC review of ten studies could not identify any studies having investigated SSI reduction as an outcome, nor comparing associated costs.[163,165,166] Nevertheless, the United States Healthcare Infection Control Practices Advisory Committee envisages possible public reporting of antibiotic prophylaxis-related parameters and SSI of selected surgical procedures.[165] So far, it remains unknown how such a reporting method might influence healthcare workers' motivation or how to handle possible unexpected consequences.[166]


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