The Role of the Gut Microbiome on the Development of Surgical Site Infections

Abstract Despite advances in antisepsis techniques, surgical site infection remains the most common and most costly reason for hospital readmission after surgery. Wound infections are conventionally thought to be directly caused by wound contamination. However, despite strict adherence to surgical site infection prevention techniques and bundles, these infections continue to occur at high rates. The contaminant theory of surgical site infection fails to predict and explain most postoperative infections and still remains unproven. In this article we provide evidence that the process of surgical site infection development is far more complex than what can be explained by simple bacterial contamination and hosts' ability to clear the contaminating pathogen. We show a link between the intestinal microbiome and distant surgical site infections, even in the absence of intestinal barrier breach. We discuss the Trojan-horse mechanisms by which surgical wounds may become seeded by pathogens from within one's own body and the contingencies that need to be met for an infection to develop.

[1]  J. V. van Dijl,et al.  Staphylococcal trafficking and infection—from ‘nose to gut’ and back , 2021, FEMS microbiology reviews.

[2]  H. Fukuda,et al.  Healthcare resources attributable to methicillin-resistant Staphylococcus aureus orthopedic surgical site infections , 2020, Scientific Reports.

[3]  Hanqiang Jin,et al.  Intestinal methicillin-resistant Staphylococcus aureus causes prosthetic infection via ‘Trojan Horse’ mechanism: Evidence from a rat model , 2020, Bone & joint research.

[4]  Á. Soriano,et al.  Prevalence and Impact of Positive Intraoperative Cultures in Partial Hip or Knee Revision. , 2020, The Journal of arthroplasty.

[5]  J. Alverdy,et al.  Re-examining causes of surgical site infections following elective surgery in the era of asepsis. , 2020, The Lancet. Infectious diseases.

[6]  W. V. van Wamel,et al.  Dendritic Cells Internalize Staphylococcus aureus More Efficiently than Staphylococcus epidermidis, but Do Not Differ in Induction of Antigen-Specific T Cell Proliferation , 2019, Microorganisms.

[7]  A. Rosinski,et al.  Selection pressures of vancomycin powder use in spine surgery: a meta-analysis. , 2019, The spine journal : official journal of the North American Spine Society.

[8]  U. Völker,et al.  Metabolic niche adaptation of community- and hospital-associated methicillin-resistant Staphylococcus aureus. , 2019, Journal of proteomics.

[9]  A. Milby,et al.  The impact of prophylactic intraoperative vancomycin powder on microbial profile, antibiotic regimen, length of stay, and reoperation rate in elective spine surgery. , 2019, The spine journal : official journal of the North American Spine Society.

[10]  Marie A. Bashaw,et al.  Perioperative Strategies for Surgical Site Infection Prevention , 2019, AORN journal.

[11]  M. Fraunholz,et al.  Inside job: Staphylococcus aureus host-pathogen interactions. , 2017, International journal of medical microbiology : IJMM.

[12]  A. Zaborin,et al.  Can Methicillin-resistant Staphylococcus aureus Silently Travel From the Gut to the Wound and Cause Postoperative Infection? Modeling the “Trojan Horse Hypothesis” , 2017, Annals of surgery.

[13]  C. Edmiston,et al.  Environment of care: Is it time to reassess microbial contamination of the operating room air as a risk factor for surgical site infection in total joint arthroplasty? , 2017, American journal of infection control.

[14]  F. Lucht,et al.  Epidemiology and clinical relevance of Staphylococcus aureus intestinal carriage: a systematic review and meta-analysis , 2017, Expert review of anti-infective therapy.

[15]  Christine S. M. Lau,et al.  Bundles Prevent Surgical Site Infections After Colorectal Surgery: Meta-analysis and Systematic Review , 2017, Journal of Gastrointestinal Surgery.

[16]  K. Guyton,et al.  The gut microbiota and gastrointestinal surgery , 2017, Nature Reviews Gastroenterology &Hepatology.

[17]  D. Hurley,et al.  Survey of Intraoperative Bacterial Contamination in Dogs Undergoing Elective Orthopedic Surgery. , 2016, Veterinary surgery : VS.

[18]  A. Ko,et al.  Predictors of infection after 754 cranioplasty operations and the value of intraoperative cultures for cryopreserved bone flaps. , 2016, Journal of neurosurgery.

[19]  K. Forde,et al.  Combined preoperative mechanical bowel preparation with oral antibiotics significantly reduces surgical site infection, anastomotic leak, and ileus after colorectal surgery. , 2015, Annals of surgery.

[20]  D. Missiakas,et al.  Staphylococcal manipulation of host immune responses , 2015, Nature Reviews Microbiology.

[21]  J. Faith,et al.  Neutrophil ageing is regulated by the microbiome , 2015, Nature.

[22]  J. Scarborough,et al.  Combined Mechanical and Oral Antibiotic Bowel Preparation Reduces Incisional Surgical Site Infection and Anastomotic Leak Rates After Elective Colorectal Resection: An Analysis of Colectomy-Targeted ACS NSQIP. , 2015, Annals of surgery.

[23]  T. Trikalinos,et al.  Oral Mechanical Bowel Preparation for Colorectal Surgery: Systematic Review and Meta-Analysis , 2015, Diseases of the colon and rectum.

[24]  J. Cavanaugh,et al.  Association of a bundled intervention with surgical site infections among patients undergoing cardiac, hip, or knee surgery. , 2015, JAMA.

[25]  M. Hawn,et al.  Oral Antibiotic Bowel Preparation Significantly Reduces Surgical Site Infection Rates and Readmission Rates in Elective Colorectal Surgery. , 2015, Annals of surgery.

[26]  S. Awad,et al.  Effect of a preoperative decontamination protocol on surgical site infections in patients undergoing elective orthopedic surgery with hardware implantation. , 2015, JAMA Surgery.

[27]  Mallary C Greenlee-Wacker,et al.  How methicillin-resistant Staphylococcus aureus evade neutrophil killing , 2015, Current opinion in hematology.

[28]  Sean M. Kearney,et al.  Microbial Symbionts Accelerate Wound Healing via the Neuropeptide Hormone Oxytocin , 2013, PloS one.

[29]  R. Cofield,et al.  Clinical meaning of unexpected positive cultures (UPC) in revision shoulder arthroplasty. , 2013, Journal of shoulder and elbow surgery.

[30]  James C. Cox,et al.  Risk factors for 30-day hospital readmission among general surgery patients. , 2012, Journal of the American College of Surgeons.

[31]  M. Makary,et al.  An evaluation of surgical site infections by wound classification system using the ACS-NSQIP. , 2012, The Journal of surgical research.

[32]  I. Gelalis,et al.  Bacterial wound contamination during simple and complex spinal procedures. A prospective clinical study. , 2011, The spine journal : official journal of the North American Spine Society.

[33]  V. Gant,et al.  Are bloodstream leukocytes Trojan Horses for the metastasis of Staphylococcus aureus? , 2011, Nature Reviews Microbiology.

[34]  N. Groot,et al.  Intestinal carriage of Staphylococcus aureus: how does its frequency compare with that of nasal carriage and what is its clinical impact? , 2009, European Journal of Clinical Microbiology & Infectious Diseases.

[35]  E. Bouza,et al.  Cultures of sternal wound and mediastinum taken at the end of heart surgery do not predict postsurgical mediastinitis. , 2006, Diagnostic microbiology and infectious disease.

[36]  E. Ayello,et al.  Increased Bacterial Burden and Infection: The Story of NERDS and STONES , 2006, Advances in skin & wound care.

[37]  R. Roumen,et al.  Bacteriology of abdominal wounds in elective open colon surgery: a prospective study of 100 surgical wounds. , 2005, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[38]  K. Slim,et al.  Meta‐analysis of randomized clinical trials of colorectal surgery with or without mechanical bowel preparation , 2004, The British journal of surgery.

[39]  O. Zmora,et al.  Colon and Rectal Surgery Without Mechanical Bowel Preparation: A Randomized Prospective Trial , 2003, Annals of surgery.

[40]  R. Gaynes,et al.  Surgical site infection (SSI) rates in the United States, 1992-1998: the National Nosocomial Infections Surveillance System basic SSI risk index. , 2001, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[41]  B. Wilson,et al.  Survival of Staphylococcus aureus Inside Neutrophils Contributes to Infection1 , 2000, The Journal of Immunology.

[42]  R. Garibaldi,et al.  Predictors of intraoperative-acquired surgical wound infections. , 1991, The Journal of hospital infection.

[43]  R. Simmons,et al.  Enteric bacteria and ingested inert particles translocate to intraperitoneal prosthetic materials. , 1991, Archives of surgery.

[44]  E. J. Poth Historical development of intestinal antisepsis , 1982, World journal of surgery.

[45]  D. Burdon,et al.  Influence of bowel preparation and antimicrobials on colonic microflora , 1978, The British journal of surgery.

[46]  J. S. Clarke,et al.  Preoperative Oral Antibiotics Reduce Septic Complications of Colon Operations: Results of Prospective, Randomized, Double‐blind Clinical Study , 1977, Annals of surgery.

[47]  J. T. Mcclintock,et al.  INTESTINAL OBSTRUCTION : II. A STUDY OF THE FACTORS INVOLVED IN THE PRODUCTION AND ABSORPTION OF TOXIC MATERIAIS FROM THE INTESTINE. , 1919 .