Abstract

•Surgical site infections are among the most common hospital-acquired infections in the United States.•Surgical site infections are classified by extent of involvement: superficial incisional, deep incisional, and organ/space surgical site infections.•Guidelines for prevention of surgical site infections include parental antimicrobial prophylaxis, alcohol-based skin preparation, perioperative glycemic control, and maintenance of normothermia. •Surgical site infections are among the most common hospital-acquired infections in the United States.•Surgical site infections are classified by extent of involvement: superficial incisional, deep incisional, and organ/space surgical site infections.•Guidelines for prevention of surgical site infections include parental antimicrobial prophylaxis, alcohol-based skin preparation, perioperative glycemic control, and maintenance of normothermia. The work of Louis Pasteur, Joseph Lister, and Robert Koch in the late nineteenth century has informed the role of infection on surgical outcomes and ultimately served as the foundation for the transformation of surgical medicine. Louis Pasteur was a French scientist whose studies in fermentation, anthrax, silkworm disease, chicken cholera, and rabies led to the development of the germ theory of fermentation and subsequently the germ theory of disease.1Toledo-Pereyra L.H. Louis pasteur surgical revolution.J Invest Surg. 2009; 22: 82-87Crossref PubMed Scopus (8) Google Scholar, 2Bulander R.E. Dunn D.L. Beilman G.J. Surgical infections.in: Brunicardi F.C. Andersen D.K. Billiar T.R. Schwartz's principles of surgery, 11e. McGraw-Hill Education, New York (NY)2019Google Scholar, 3Gaynes R.P. Germ theory medical pioneers in infectious diseases. In. Washington, DC. ASM Press, Washington, DC2011Crossref Google Scholar In his early fermentation studies, he proposed that microorganisms caused fermentation and decomposition during a time when it was widely believed to be solely a chemical reaction. He developed techniques of sterilizing equipment in the laboratory that later would translate into similar applications in the surgical setting. British surgeon Joseph Lister brought his experience and observations as a surgeon and his belief in the germ theory of disease to his development of aseptic techniques using carbolic acid in the surgical setting.4Lister J. Antiseptic principle of the practice of surgery. Hoboken (NJ): Generic NL Freebook Publisher; 1867.Google Scholar He developed a set of principles in asepsis to be used in approach to surgery and surgical wounds: (1) destroy germs on the patient’s skin, the surgeon’s hands, the instruments, and the area surrounding the surgical site; (2) prevent germs from the air from entering the wound during surgery; and (3) prevent germs from entering the wound after surgery.3Gaynes R.P. Germ theory medical pioneers in infectious diseases. In. Washington, DC. ASM Press, Washington, DC2011Crossref Google Scholar, 4Lister J. Antiseptic principle of the practice of surgery. Hoboken (NJ): Generic NL Freebook Publisher; 1867.Google Scholar, 5Pitt D. Aubin J.-M. Joseph Lister: Father Of Modern Surgery.Can J Surg. 2012; 55: E8-E9Crossref PubMed Scopus (26) Google Scholar, 6Lister J. On a new method of treating compound fracture, abscess, etc.: with observations on the conditions of suppuration.Lancet. 1867; 89: 326-329Abstract Scopus (81) Google Scholar Robert Koch was a German physician who had experience with wound infections during his service at a battlefield hospital. His research working with anthrax and his discovery of Mycobacterium tuberculosis would serve as a foundation for what came to be known as Koch postulates. These postulates would establish a causal relationship between a specific microorganism and disease.3Gaynes R.P. Germ theory medical pioneers in infectious diseases. In. Washington, DC. ASM Press, Washington, DC2011Crossref Google Scholar,7Koch R. Brock T.D. Fred E.B. The etiology of tuberculosis.Rev Infect Dis. 1982; 4: 1270-1274Crossref PubMed Scopus (50) Google Scholar In the era prior to these discoveries and the development and implementation of the principles of asepsis, infection after surgery was an expected outcome. Purulence that was localized to the surgical wound was considered a favorable outcome. A local infection could be treated successfully, but a widespread infection likely would be fatal. Morbidity and mortality due to surgical wound infections decreased with the implementation of surgical asepsis. These discoveries and innovations of the late nineteenth century marked the beginning of the evolution of surgical care and remain at the core of knowledge of surgical site infections (SSIs).1Toledo-Pereyra L.H. Louis pasteur surgical revolution.J Invest Surg. 2009; 22: 82-87Crossref PubMed Scopus (8) Google Scholar, 2Bulander R.E. Dunn D.L. Beilman G.J. Surgical infections.in: Brunicardi F.C. Andersen D.K. Billiar T.R. Schwartz's principles of surgery, 11e. McGraw-Hill Education, New York (NY)2019Google Scholar, 3Gaynes R.P. Germ theory medical pioneers in infectious diseases. In. Washington, DC. ASM Press, Washington, DC2011Crossref Google Scholar A surgical wound infection involves an infection at the surgical incision site after an operation. Use of the term, surgical wound infection, has been modified to SSI, to better represent infections at the surgical site and not just the incision.8Horan T.C. Gaynes R.P. Martone W.J. et al.CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgical wound infections.Am J Infect Control. 1992; 20: 271-274Abstract Full Text PDF PubMed Scopus (578) Google Scholar The Centers for Disease Control and Prevention (CDC) define SSI as any infection after surgery the involves the surgical wound (incision) or organ/space that was manipulated during the procedure that occurs within 30 days of surgery or within 1 year with prosthetic material implantation. SSIs are classified as superficial incisional SSI, deep incisional SSI, or organ/space SSI (see Table 1 for criteria).8Horan T.C. Gaynes R.P. Martone W.J. et al.CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgical wound infections.Am J Infect Control. 1992; 20: 271-274Abstract Full Text PDF PubMed Scopus (578) Google Scholar A suture abscess or stitch abscess is an abscess at the suture site only and is not considered an SSI. Remote infections resulting from surgery but not involving the surgical site are called surgical patient infections.8Horan T.C. Gaynes R.P. Martone W.J. et al.CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgical wound infections.Am J Infect Control. 1992; 20: 271-274Abstract Full Text PDF PubMed Scopus (578) Google Scholar An example of a surgical patient infection is pneumonia or a urinary tract infection in a patient who underwent an appendectomy.Table 1Surgical site infections are classified into 3 categories: superficial incisional, deep incisional (fascia and muscle), and organ/space criteria for surgical site infection8Horan T.C. Gaynes R.P. Martone W.J. et al.CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgical wound infections.Am J Infect Control. 1992; 20: 271-274Abstract Full Text PDF PubMed Scopus (578) Google ScholarSurgical Site Infection General CriteriaClassificationStructuresCriteria•Infection related to an operative procedure•Occurs at or near surgical site•Within 30 d of procedurebWithin 1 y if prosthetic material is implanted and seems associated with operative site for deep incisional or organ/space SSI.Superficial incisionalSSISkinSubcutaneous tissueGeneral criteria AND 1 of the following:•Purulent drainage from superficial incision (not deep)•Organisms isolated from aseptically obtained culture•≥1 sign or symptom pain/tenderness, localized swelling, erythema, warmth, or superficial incision deliberately opened (unless culture is negative)Deep incisionalSSIDeep soft tissue (fascia and muscle)General criteria AND 1 of the following:•Purulent drainage from deep incision (not organ space)•Spontaneous dehisces or deliberately opened with fever and/or pain/tenderness (unless culture is negative)•Abscess or evidence of infection on direct examination, during reoperation, or by histologic or radiologic examinationOrgan/spaceSSIOrgan/spaceGeneral criteria and involves any part of the anatomy (organ or space) opened or manipulated during the procedure (specific sites assigned to identify locationaSpecific sites of organ/space SSI: arterial or venous infection, breast abscess or mastitis, disc space, ear/mastoid, endometritis, endocarditis, eye (not conjunctivitis), gastrointestinal tract, intra-abdominal, intracranial, brain, dural infections abscesses, joint or bursa, mediastinitis, meningitis or ventriculitis, myocarditis or pericarditis, oral cavity (mouth, tongue, or gums), osteomyelitis, other lower respiratory tract infection, other urinary tract infections, other male or female reproductive tract, spinal abscess without meningitis, sinusitis, upper respiratory tract, pharyngitis, and vaginal cuff (episiotomy, circumcision, and burn wounds are excluded).) AND 1 of the following:•Purulent drainage from a drain placed through stab wound into the organ/space•Organisms isolated from aseptically obtained culture of fluid or tissue•Abscess or evidence of infection involving organ/space on direct on direct examination, during reoperation, or by histologic or radiologic examinationa Specific sites of organ/space SSI: arterial or venous infection, breast abscess or mastitis, disc space, ear/mastoid, endometritis, endocarditis, eye (not conjunctivitis), gastrointestinal tract, intra-abdominal, intracranial, brain, dural infections abscesses, joint or bursa, mediastinitis, meningitis or ventriculitis, myocarditis or pericarditis, oral cavity (mouth, tongue, or gums), osteomyelitis, other lower respiratory tract infection, other urinary tract infections, other male or female reproductive tract, spinal abscess without meningitis, sinusitis, upper respiratory tract, pharyngitis, and vaginal cuff (episiotomy, circumcision, and burn wounds are excluded).b Within 1 y if prosthetic material is implanted and seems associated with operative site for deep incisional or organ/space SSI. Open table in a new tab Surgical manipulation of tissue causes changes in host (patient) defense mechanisms against infection. Skin and mucous membranes provide a physical barrier to pathogens and bacteria entering a patient’s tissues.2Bulander R.E. Dunn D.L. Beilman G.J. Surgical infections.in: Brunicardi F.C. Andersen D.K. Billiar T.R. Schwartz's principles of surgery, 11e. McGraw-Hill Education, New York (NY)2019Google Scholar Additionally, the skin and mucous membranes of normal healthy individuals are colonized with bacteria collectively known as normal microbial flora. Normal microbial flora varies slightly between individual people, but there are common types of bacteria found in specific anatomic locations (Table 2).9Riedel S. Hobden J.A. Miller S. et al.Normal human microbiota.in: Weitz M. Thomas C.M. Jawetz, melnick, & adelberg's medical microbiology. 28th edition. McGraw-Hill Education, New York2019Google Scholar, 10Davis CP. Normal flora. In: Baron S, editor. Medical microbiology. 4th edition. Galveston: University of Texas Medical Branch at Galveston; 1996.Google Scholar, 11Gillespie S. Bamford K. Medical microbiology and infection at a glance. John Wiley & Sons, Hoboken, (United Kingdom)2012Google Scholar Disruption of this barrier during surgical procedures can allow normal microbial flora and other pathogens to enter the surrounding tissues, which can lead to infection. Further manipulation of tissue or organs in the surgical site during the operation can expose the surgical site to bacterial flora typically present at the specific site. Introduction of bacteria can occur from external sources of contamination during the procedure or after the procedure. Exposure to microorganisms stimulates an immune response in the patient. If the microbes are not eliminated by a patient’s immune response, an infection develops. The resulting infection can be contained, locoregional, or systemic2Bulander R.E. Dunn D.L. Beilman G.J. Surgical infections.in: Brunicardi F.C. Andersen D.K. Billiar T.R. Schwartz's principles of surgery, 11e. McGraw-Hill Education, New York (NY)2019Google Scholar (Box 1). Although most SSIs are bacterial, infections can be fungal or viral in origin.2Bulander R.E. Dunn D.L. Beilman G.J. Surgical infections.in: Brunicardi F.C. Andersen D.K. Billiar T.R. Schwartz's principles of surgery, 11e. McGraw-Hill Education, New York (NY)2019Google Scholar Common bacterial pathogens involved in SSIs are listed in Table 3. The most common bacterial pathogens involved are Staphylococcus aureus (methicillin-resistant Staphylococcus aureus [MRSA] and methicillin-sensitive Staphylococcus aureus [MSSA]), coagulase-negative staphylococci, and enterococci.12Miller J.M. Binnicker M.J. Campbell S. et al.A guide to utilization of the microbiology laboratory for diagnosis of infectious diseases: 2018 update by the infectious diseases society of america and the american society for microbiologya.Clin Infect Dis. 2018; 67: e1-e94Crossref PubMed Scopus (92) Google Scholar,13Hidron A.I. Edwards J.R. Patel J. et al.NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National healthcare safety network at the centers for disease control and prevention, 2006-2007.Infect Control Hosp Epidemiol. 2008; 29: 996Crossref PubMed Scopus (1546) Google ScholarTable 2Normal microbial flora: the normal microbial flora commonly is called microbiotaAnatomic LocationGram PositiveGram NegativeCocciRodsCocciRodsSkinStaphylococcus epidermidisStaphylococcus aureusMicrococcusα-Hemolytic streptococci Nonhemolytic streptococciPeptostreptococcus speciesPropionibacterium speciesCorynebacterium speciesPropionibacterium acnesEnteric bacilli (some sites)Acinetobacter species (coccobacilli)Nasopharynxα-Hemolytic streptococciStaphylococcus epidermidis Nonhemolytic streptococciMicrococcusAnaerobesCorynebacteriumNeisseria species (nonpathogenic)Haemophilus speciesPrevotella speciesAnaerobesGastrointestinal tract (stomach)Small flora∗ (undetectable to 103/g of contents)∗Limited to bacteria swallowed with foodLactobacillus speciesGastrointestinal tract (ileum)Moderate mixed flora (106/g to 108/g of contents)EnterococciEnterobacteriaceaeGastrointestinal tract (large intestine)Dense flora (109/g to 1011/g of contents)StreptococcusEnterococciα-Hemolytic streptococci non-hemolytic streptococciAnaerobesPeptostreptococcus speciesLactobacillus speciesClostridium speciesDiphtheroidsEnterobacteriaceaeBacteroidesEnteric bacilliAnaerobesGenitaliaStreptococcusα-Hemolytic streptococci Nonhemolytic streptococciLactobacillus speciesCorynebacterium speciesNeisseria species (nonpathogenic)BacteroidesAnaerobesThis is a small representation of some of the most common bacteria in the microbiota of specific anatomic locations.9Riedel S. Hobden J.A. Miller S. et al.Normal human microbiota.in: Weitz M. Thomas C.M. Jawetz, melnick, & adelberg's medical microbiology. 28th edition. McGraw-Hill Education, New York2019Google Scholar, 10Davis CP. Normal flora. In: Baron S, editor. Medical microbiology. 4th edition. Galveston: University of Texas Medical Branch at Galveston; 1996.Google Scholar, 11Gillespie S. Bamford K. Medical microbiology and infection at a glance. John Wiley & Sons, Hoboken, (United Kingdom)2012Google Scholar∗ the Small flora is limited to the bacteria swallowed with food. Open table in a new tab Box 1Degree of infectionContained infection•Local purulence•Furuncle•AbscessLocoregional with or without distant spread•Cellulitis•Lymphangitis•Aggressive soft tissue infection•Metastatic abscessSystemic infection•Bacteremia•Fungemia•Systemic inflammatory response syndrome•Sepsis•Septic shockTable 3Common bacterial surgical pathogens: most surgical site infections are bacterial2Bulander R.E. Dunn D.L. Beilman G.J. Surgical infections.in: Brunicardi F.C. Andersen D.K. Billiar T.R. Schwartz's principles of surgery, 11e. McGraw-Hill Education, New York (NY)2019Google Scholar,14Stevens D.L. Bisno A.L. Chambers H.F. et al.Practice guidelines for the diagnosis and management of skin and soft tissue infections: 2014 update by the infectious diseases society of America.Clin Infect Dis. 2014; 59: e10-e52Crossref PubMed Scopus (824) Google ScholarGram PositiveGram NegativeCocciRodsCocciRodsAerobicStaphylococcus aureusCoagulase-negative staphylococciStaphylococcus epidermidisStreptococcus pyogenesStreptococcus pneumoniaeEnterococcus faeciumEnterococcus faecalisEscherichia coliHaemophilus influenzae (coccobacilli)Klebsiella pneumoniaeProteus mirabilisEnterobacter cloacaeEnterobacter aerogenesSerratia marcescensAcinetobacter calcoacetisus (coccobacilli)Citrobacter freundiiPseudomonas aeruginosaStenotrophomonas maltophiliaAnaerobesPeptostreptococcus speciesClostridium difficileClostridium perfringensClostridium tetaniClostridium septicumBacteroides fragilisFusobacterium speciesOtherMycobacterium avium-intracellulareMycobacterium tuberculosisNocardia asteroidsLegionella pneumophiliaListeria monocytogenes Open table in a new tab This is a small representation of some of the most common bacteria in the microbiota of specific anatomic locations.9Riedel S. Hobden J.A. Miller S. et al.Normal human microbiota.in: Weitz M. Thomas C.M. Jawetz, melnick, & adelberg's medical microbiology. 28th edition. McGraw-Hill Education, New York2019Google Scholar, 10Davis CP. Normal flora. In: Baron S, editor. Medical microbiology. 4th edition. Galveston: University of Texas Medical Branch at Galveston; 1996.Google Scholar, 11Gillespie S. Bamford K. Medical microbiology and infection at a glance. John Wiley & Sons, Hoboken, (United Kingdom)2012Google Scholar ∗ the Small flora is limited to the bacteria swallowed with food. Contained infection•Local purulence•Furuncle•AbscessLocoregional with or without distant spread•Cellulitis•Lymphangitis•Aggressive soft tissue infection•Metastatic abscessSystemic infection•Bacteremia•Fungemia•Systemic inflammatory response syndrome•Sepsis•Septic shock There are many risk factors for developing an SSI, including microbe-related factors, patient factors, and procedure-related factors (Box 2).2Bulander R.E. Dunn D.L. Beilman G.J. Surgical infections.in: Brunicardi F.C. Andersen D.K. Billiar T.R. Schwartz's principles of surgery, 11e. McGraw-Hill Education, New York (NY)2019Google Scholar,15Pessaux P. Msika S. Atalla D. et al.Risk factors for postoperative infectious complications in noncolorectal abdominal surgery: a multivariate analysis based on a prospective multicenter study of 4718 patients.Arch Surg. 2003; 138: 314-324Crossref PubMed Scopus (197) Google Scholar, 16Nolan M.B. Martin D.P. Thompson R. et al.Association between smoking status, preoperative exhaled carbon monoxide levels, and postoperative surgical site infection in patients undergoing elective surgery.JAMA Surg. 2017; 152: 476-483Crossref PubMed Scopus (45) Google Scholar, 17Hollenbeak C.S. Lave J.R. Zeddies T. et al.Factors associated with risk of surgical wound infections.Am J Med Qual. 2006; 21: 29S-34SCrossref PubMed Scopus (16) Google Scholar, 18Sørensen L.T. Wound healing and infection in surgery: the pathophysiological impact of smoking, smoking cessation, and nicotine replacement therapya systematic review.Ann Surg. 2012; 255: 1069-1079Crossref PubMed Scopus (301) Google Scholar, 19Culver D.H. Horan T.C. Gaynes R.P. et al.Surgical wound infection rates by wound class, operative procedure, and patient risk index.Am J Med. 1991; 91: S152-S157Abstract Full Text PDF Scopus (1160) Google Scholar, 20Haley R.W. Culver D.H. Morgan W.M. et al.Identifying patients at high risk of surgical wound infection: a simple multivariate index of patient susceptibility and wound contamination.Am J Epidemiol. 1985; 121: 206-215Crossref PubMed Scopus (570) Google Scholar Degree of wound contamination has been shown to be a risk factor for development of SSI; a classification of wound by degree of contamination is found in Table 4.21Ortega G. Rhee D.S. Papandria D.J. et al.An evaluation of surgical site infections by wound classification system using the ACS-NSQIP.J Surg Res. 2012; 174: 33-38Abstract Full Text Full Text PDF PubMed Scopus (130) Google Scholar, 22Martone W.J. Nichols R.L. Recognition, prevention, surveillance, and management of surgical site infections: introduction to the problem and symposium overview.Clin Infect Dis. 2001; 33: S67-S68Crossref PubMed Scopus (82) Google Scholar, 23CDC guidelines for the prevention and control of nosocomial infections. Guidelines for prevention of surgical wound infections, 1985.Am J Infect Control. 1986; 14: 71Abstract Full Text PDF PubMed Scopus (38) Google ScholarBox 2The risk factors for surgical site infection (SSI) fall in three categories2Bulander R.E. Dunn D.L. Beilman G.J. Surgical infections.in: Brunicardi F.C. Andersen D.K. Billiar T.R. Schwartz's principles of surgery, 11e. McGraw-Hill Education, New York (NY)2019Google Scholar,15Pessaux P. Msika S. 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Surgical wound infection: epidemiology, pathogenesis, diagnosis and management.BMC Infect Dis. 2006; 6: 171Crossref PubMed Scopus (38) Google Scholar,25Tang R. Chen H.H. Wang Y.L. et al.Risk factors for surgical site infection after elective resection of the colon and rectum: a single-center prospective study of 2,809 consecutive patients.Ann Surg. 2001; 234: 181-189Crossref PubMed Scopus (383) Google ScholarMICROBE RELATED•Degree of wound contamination•Virulence of pathogen•Prolonged hospitalization prior to surgeryPATIENT RELATED•Index of disease•Morbid obesity•Advanced age•Protein-calorie malnutrition•Age•Immunosuppressants•Diabetes mellitus•Smoking•Cancer•Systemic infectionOPERATION RELATED•Duration of operation (>2 hours)•Tissue trauma•Poor hemostasis•Presence of foreign material•Intra-abdominal procedure•TechniqueTable 4Wound classification according to degree of contamination21Ortega G. Rhee D.S. Papandria D.J. et al.An evaluation of surgical site infections by wound classification system using the ACS-NSQIP.J Surg Res. 2012; 174: 33-38Abstract Full Text Full Text PDF PubMed Scopus (130) Google ScholarContamination ClassificationDefinitionaClassifications as defined by ACS National Surgical Quality Improvement Program.21Surgical Site Infection Rates21Ortega G. Rhee D.S. Papandria D.J. et al.An evaluation of surgical site infections by wound classification system using the ACS-NSQIP.J Surg Res. 2012; 174: 33-38Abstract Full Text Full Text PDF PubMed Scopus (130) Google ScholarCleanThese are uninfected operative wounds in which no inflammation is encountered and the respiratory, alimentary, genital, or uninfected urinary tracts are not entered.1.76% Superficial incisional0.54% Deep incisional0.28% Organ/spaceClean/contaminatedThese are operative wounds in which the respiratory, alimentary, genital, or urinary tract is entered under controlled conditions and without unusual contamination.3.94% Superficial incisional0.86% Deep incisional1.87% Organ/spaceContaminatedThese include open, fresh, accidental wounds; operations with major breaks in sterile technique or gross spillage from the gastrointestinal tract; and incisions in which acute, nonpurulent inflammation is encountered.4.75% Superficial incisional1.31% Deep incisional2.55% Organ/spaceDirtyThese include old traumatic wounds with retained devitalized tissue and those that involve existing clinical infection or perforated viscera.5.16% Superficial incisional2.1% Deep incisional4.54% Organ/apacea Classifications as defined by ACS National Surgical Quality Improvement Program.21Ortega G. Rhee D.S. Papandria D.J. et al.An evaluation of surgical site infections by wound classification system using the ACS-NSQIP.J Surg Res. 2012; 174: 33-38Abstract Full Text Full Text PDF PubMed Scopus (130) Google Scholar Open table in a new tab MICROBE RELATED•Degree of wound contamination•Virulence of pathogen•Prolonged hospitalization prior to surgeryPATIENT RELATED•Index of disease•Morbid obesity•Advanced age•Protein-calorie malnutrition•Age•Immunosuppressants•Diabetes mellitus•Smoking•Cancer•Systemic infectionOPERATION RELATED•Duration of operation (>2 hours)•Tissue trauma•Poor hemostasis•Presence of foreign material•Intra-abdominal procedure•Technique SSIs remain a significant burden, with approximately 2% to 5% of patients undergoing inpatient surgery developing an SSI.2Bulander R.E. Dunn D.L. Beilman G.J. Surgical infections.in: Brunicardi F.C. Andersen D.K. Billiar T.R. Schwartz's principles of surgery, 11e. McGraw-Hill Education, New York (NY)2019Google Scholar,14Stevens D.L. 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