Most abundant skin organisms are likely unknown to most clinicians and operating room staff. Indeed, preoperative skin preparation and antibiotic administration should be expected to obliterate the skin microbiota but the clinical consequences of these interventions are understudied. We postulate that improved knowledge of the skin microbiome and the associated immune response, in parallel with improved knowledge of the gut microbiome and gastrointestinal surgery, could provide actionable findings about SSI pathogenesis.
The purpose of this study was to characterize changes in the cutaneous microbiome in patients undergoing major elective colorectal procedures for both benign and malignant disease. Swabs of the chest wall served as internal controls for postoperative swabs of the incision. To our knowledge, this is the largest study to date of the microbiota of surgical incisions, and the samples collected were paired with intestinal contents, stool samples, and intraoperative swabs of the subcutaneous fat in the wounds. Overall, as expected, we observed a skin microbiota marked by an abundance of Corynebacteriaceae, Propionibacterium, and Staphylococcus.
The key finding was a transient postoperative loss of the skin commensals Corynebacterium and Propionibacterium and a transient colonization by potential pathogens as well as anaerobes from the gut. This appears to be unique to the surgical site, as the observed chest microbiota was far more stable. During the period of microbial instability after surgery, skin swabs contained unusually high levels of Enterobacteriaceae and intestinal anaerobes such as Lachnospiraceae and Bacteroidaceae. Interestingly, the swabs of the subcutaneous fat from the opening incisions did not demonstrate complex microbial communities, whereas swabs at wound closure contained an intestine-like microbiota.
Because the SSI rate in this cohort was low, it was not possible to formally test the hypothesis that pathogens responsible for SSIs would be present on postoperative swabs prior to onset of infection. This lack of SSIs may reflect the large number of minimally invasive cases, which generally enjoy lower complication rates34. In the single patient with an Enterococcus wound infection, we observed a dramatic increase in abundance of Enterococcus in ileostomy effluent and concomitantly on swabs of the abdominal skin. This coincided almost perfectly with a loss of the commensals. The fact that the pathogen responsible for wound infection was not seen in the luminal contents or subcutaneous fat swabs supports the concept that wound infection may not necessarily reflect intraoperative contamination. It may be the case that Enterococcus bloomed in the setting of antibiotic exposure35, and subsequently spread to cause infection.
Although we did not observe a signal linking skin microbiome and SSI, the available literature would suggest that our findings are clinically relevant. The loss of skin commensals near the wound likely creates an opportunity for growth of pathogens and other organisms not typically found on the skin, as seen also in models of skin wounds27,31. The observed dysbiosis, like dysbiosis at other body locations, brings about two related problems. First, affected individuals acutely suffer from the loss of commensals that may be important for health and immune function. Second, with commensals absent, potential pathogens may grow in a compensatory fashion in a manner akin to loss of colonization resistance, which has been better studied in the intestine36,37. Clearly, since most subjects in this study did not suffer complications despite displaying postoperative skin dysbiosis, additional variables must be responsible for the pathogenesis of SSIs. Identifying these variables and integrating them with knowledge of postoperative dysbiosis could be useful in preventing SSI.
If larger studies in the future allow for identification of colonization patterns associated with onset of infection, then there may be actionable opportunities for improved perioperative care. First, it may be possible to identify surgical incisions at high risk of infection, and then monitor the microbiome of these incisions over time. Early identification of postoperative skin dysbiosis may then allow for preventive measures to restore a normal skin microbiota. For example, topical probiotic therapy has now been embraced as a method to optimize the skin microbiome38,39. Other available interventions to modulate the skin microbiota include topical application of honey-based ointments or the use of enteral probiotics. Proof-of-principle for perioperative manipulation of the microbiome was provided with the demonstration that administration of mupirocin for patients found to be colonized preoperatively with methicillin-resistant S. aureus improves outcomes40.
Finally, this study raises questions about the unfocused approach to obliterate the perioperative skin microbiome in the hopes of preventing SSI. Minimizing intraoperative contamination will always be important, but could be integrated with microbiome science. Ultimately, when a wound becomes infected and a causative bacterial species is isolated from culture, one might attempt to determine the origin of the offending organism. If the operating room environment is identified as the source of infection, then the focus on sterility is appropriate. If the offending organism is found to be a member of the patient’s native microbiome or the microbiome that emerges in the setting of perioperative antibiotics, then the focus on sterility may be a distraction. This is particularly true in the case of clean operations. For example, it is puzzling to see sternotomy or laminectomy incisions infected with intestinal organisms even without violation of the gastrointestinal tract41,42. Larger and more comprehensive perioperative studies of the microbiota could begin to answer these questions and, hopefully, improve patient outcomes.