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Current Microbiology of Surgical Site Infections in Patients with Cancer: A Retrospective Review

Background Patients with solid tumors frequently undergo surgical procedures and develop procedure-related infections. We sought to describe the current microbiologic spectrum of infections at various sites following common surgical procedures. Methods This was a retrospective review of microbiologic data between January 2011 and February 2012. The sites studied were those associated with breast cancer surgery, thoracotomy, craniotomy, percutaneous endoscopic gastrostomy (PEG) tube insertion, and abdominal/pelvic surgery. Only patients with solid tumors were included. Results A total of 368 surgical site infections (SSIs) were identified (68 breast cancer related; 91 thoracotomy related; 45 craniotomy related; 75 PEG-tube insertion related; and 89 abdominal/pelvic surgery related). Of these, 58% were monomicrobial and 42% were polymicrobial. Overall, 85% of the 215 monomicrobial infections were caused by Gram-positive organisms and 13% by Gram-negative bacilli (GNB). Staphylococcus aureus was the predominant pathogen in monomicrobial infections (150 of 215, 70%). Sixty (40%) of these staphylococcal isolates were methicillin resistant (MRSA), and 65% had a vancomycin minimal inhibitory concentration (MIC) ≥1.0 µg/ml. Pseudomonas aeruginosa was the predominant GNB pathogen (19 of 27, 70%). Staphylococci were also the predominant pathogens in polymicrobial infections, while P. aeruginosa and Escherichia coli were the predominant GNB. Overall, 35% of isolates from polymicrobial infections were GNB. Cephalosporins (e.g., cefazolin) or amoxicillin/clavulanate was used most often for surgical prophylaxis, and 47% of organisms from monomicrobial infections (MRSA, P. aeruginosa) were resistant to them. A similar resistance pattern was observed in polymicrobial infections. Conclusion Staphylococcus species were isolated most often from the sites studied. Polymicrobial infections (42%) and GNB monomicrobial infections (13%) were relatively frequent causes of SSIs. Many of these infections were caused by organisms that are resistant to agents commonly used for surgical prophylaxis. Additionally, 65% of staphylococcal isolates had a vancomycin MIC ≥1.0 µg/ml, suggesting the need for alternative therapeutic agents. Electronic supplementary material The online version of this article (doi:10.1007/s40121-014-0048-4) contains supplementary material, which is available to authorized users.

frequently, both as a result of the underlying malignancy, and its treatment [1]. Whereas infections in patients with hematologic malignancies and in recipients of hematopoietic stem cell transplantation have been well studied, data on infections in patients with solid tumors who are not neutropenic are scarce [2,3]. Our institution has been designated a Comprehensive Cancer Center by the National Cancer Institute, and cares exclusively for patients with cancer. As part of our infection control and antimicrobial stewardship initiatives, we conduct periodic surveillance studies to determine the most current epidemiology/microbiology of infections in our patients [4]. These surveys help us determine the most appropriate antimicrobial agents for prophylaxis, empiric therapy, and targeted therapy for various patient subgroups at our institution [5].
Specific recommendations are included in institutional guidelines and pathways, which are updated periodically. In contrast to patients with hematologic malignancies, patients with solid tumors frequently undergo various diagnostic and therapeutic surgical procedures, and surgical site infections (SSIs) are among the most common infections seen in such patients [6].
Consequently, peri-operative antimicrobial prophylaxis is administered to the majority of patients undergoing these procedures. Many of the agents (e.g., first-or second-generation cephalosporins) commonly used for prophylaxis were selected for this indication several decades ago, and are probably outdated due to recent epidemiologic changes and alterations in susceptibility/resistance patterns globally [7][8][9][10]. Additionally, if a postsurgical infection develops, patients are often given empiric antimicrobial therapy designed to provide coverage against anticipated pathogens, prior to culture results being available. These empiric regimens are adjusted once culture results become available. We recently conducted a survey of the current microbiology of infections associated with common surgical procedures performed at our institution. This information is useful in determining whether our guidelines for prophylaxis and empiric therapy are adequate or need updating. Our findings form the basis of this report. We did not look at treatment and outcomes of these patients, since this was purely a microbiologic survey, and no specific treatment algorithms were being evaluated.

PEG-tube Insertion Site Infections
A total of 75 episodes of PEG-tube insertion SSIs were identified during the study period (

Abdominal and Pelvic Wound Infections
A total of 89 episodes of infection associated with abdominal/pelvic surgery were identified (         Consequently, infection prevention is important and antimicrobial prophylaxis is recommended for most of these surgical procedures [7-9, 18, 19]. The agents commonly used for prophylaxis (e.g., first-or second-generation cephalosporins; amoxicillin/ clavulanate) were selected several decades ago, based on microbiologic data available then [20]. In the past, methicillin-susceptible S. aureus and, to a lesser extent, beta-hemolytic streptococci were the predominant organisms causing SSIs [21]. Data from our study provide confirmation that Gram-positive bacteria remain the most frequently isolated pathogens in SSIs in cancer patients, regardless of the specific site of infection. Of the 157 monomicrobial infections, 129 (82%) were caused by Gram-positive pathogens. However, streptococci accounted for only 8% (12 of 157) of these infections, possibly because current prophylactic regimens are still effective against these organisms. In contrast, staphylococci accounted for 109 of 157 episodes of monomicrobial infections (70%), suggesting that prophylaxis was not particularly effective. Of concern is the fact that 40% of S. aureus isolates were methicillin resistant, and that 67% of staphylococcal isolates had a vancomycin MIC C1.0 lg/ml. Although there is some variability with susceptibility test results using different methods (E-test, which we used, usually gives higher MIC values than other methods), such organisms have been shown to cause infections that respond slowly, or not at all, to therapy with vancomycin [22][23][24]. Also of concern is the fact that such isolates are now almost as common among MSSA as they are among MRSA strains. These data have therapeutic implications and suggest that vancomycin might no longer be the agent of choice for the treatment of staphylococcal SSIs at our institution.
We were surprised to find that Gramnegative bacilli caused a substantial proportion (23 of 157 episodes, 15%) of monomicrobial infections, with P. aeruginosa (16 of 23 episodes, 70%) being the predominant pathogen.
Although not frequent, the isolation of multidrug-resistant P. aeruginosa and other Gram-negative organisms is of some concern. While this epidemiologic shift does not justify the administration of prophylaxis with broadspectrum and/or anti-pseudomonal agents on a routine basis to all patients undergoing surgical procedures (particularly since institutional/ geographic differences do occur), it should not be ignored. Other investigators have also reported an increase in the frequency of SSIs caused by Gram-negative organisms (49% in one study), and have suggested that alternatives to cefazolin or similar agents, be considered for prophylaxis [25,26]. We believe that individual institutions performing substantial numbers of these surgical procedures should generate their own data, and assess their own clinical needs. Since many of these procedures are elective, determining the presence of colonization with problem organisms such as MRSA or P. aeruginosa prior to surgery, and administering targeted prophylaxis to patients who are colonized, might be one approach in this setting. Based on our data, and on some clinical experience, we have instituted a change in our clinical practice in our breast cancer cohort by providing empiric coverage against Gram-negative organisms including P.
aeruginosa until microbiologic data become available. We strongly recommend discontinuation of anti-pseudomonal coverage if subsequent cultures do not confirm it as a pathogen.
We were even more surprised to find a high proportion of polymicrobial infections at all surgical sites studied. The combined frequency of polymicrobial infections was 43.3%, ranging from a low of 37.7% for craniotomy site infections, to a high of 48% for PEG-tube insertion site infections. We realize that when multiple pathogens are isolated, it is often not possible to determine the exact role played by individual organisms in the pathogenesis of polymicrobial infections. Nevertheless, it is striking that the organisms isolated most frequently from such infections (Staphylococcus species including MRSA and P. aeruginosa) are the same as those isolated most frequently from monomicrobial infections, probably reflecting the inadequacy of the agents used for prophylaxis as well. We have documented an increase in the overall frequency of polymicrobial infections in cancer patients, including patients with and without neutropenia [27]. Based on our current microbiologic data and guidelines provided by our antimicrobial stewardship initiative and on some recent clinical experience, we have instituted changes in our clinical practice by providing broad-spectrum empiric therapy, followed by de-escalation if possible, once microbiologic data become available [28]. We recommend this approach in other institutions that are experiencing epidemiologic changes similar to ours.

CONCLUSION
Although Gram-positive bacteria continue to be isolated more frequently from SSIs than Gram-negative bacteria, our data from cancer patients indicate that there have been significant changes in the epidemiology of these infections in recent times. The overall frequency of monomicrobial infections has declined, and the incidence of polymicrobial infections has increased considerably.