1887

Abstract

Surgical site infection (SSI) remains one of the most important causes of healthcare-associated infections, accounting for ~17 % of all hospital-acquired infections. Although short-term perioperative treatment with high fraction of inspired oxygen (FiO) has shown clinical benefits in reducing SSI in colorectal resection surgeries, the true clinical benefits of FiO therapy in reducing SSI remain unclear because randomized controlled trials on this topic have yielded disparate results and inconsistent conclusions. To date, no animal study has been conducted to determine the efficacy of short-term perioperative treatments with high (FiO>60 %) versus low (FiO<40 %) oxygen in reducing SSI. In this report, we designed a rat model for muscle surgery to compare the effectiveness of short-term perioperative treatments with high (FiO=80 %) versus a standard low (FiO=30 %) oxygen in reducing SSI with – one of the most prevalent Gram-negative pathogens, responsible for nosocomial SSIs. Our data demonstrate that 5 h perioperative treatment with 80 % FiO is significantly more effective in reducing SSI with compared to 30 % FiO treatment. We further show that whilst 80 % FiO treatment does not affect neutrophil infiltration into infected muscles, neutrophils in the 80 % FiO-treated and infected animal group are significantly more activated than neutrophils in the 30 % FiO-treated and infected animal group, suggesting that high oxygen perioperative treatment reduces SSI with by enhancing neutrophil activation in infected wounds.

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2016-08-01
2024-12-13
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References

  1. Al-Niaimi A., Safdar N. 2009; Supplemental perioperative oxygen for reducing surgical site infection: a meta-analysis. J Eval Clin Pract 15:360–365 [View Article][PubMed]
    [Google Scholar]
  2. Allen D. B., Maguire J. J., Mahdavian M., Wicke C., Marcocci L., Scheuenstuhl H., Chang M., Le A. X., Hopf H. W., Hunt T. K. 1997; Wound hypoxia and acidosis limit neutrophil bacterial killing mechanisms. Arch Surg 132:991–996 [View Article][PubMed]
    [Google Scholar]
  3. Anderson D. J. 2011; Surgical site infections. Infect Dis Clin North Am 25:135–153 [View Article][PubMed]
    [Google Scholar]
  4. Arsalan A., Alam M., Naqvi S. B. S., Ahmad I., Anwar Z. 2014; Oxygen as a facilitator in the reduction of surgical site infections. Sri Lanka J Surg 31: [View Article]
    [Google Scholar]
  5. Awad S. S. 2012; Adherence to surgical care improvement project measures and post-operative surgical site infections. Surg Infect 13:234–237 [View Article][PubMed]
    [Google Scholar]
  6. Belda F. J., Aguilera L., García de la Asunción J., Alberti J., Vicente R., Ferrándiz L., Rodríguez R., Company R., Sessler D. I. et al. 2005; Supplemental perioperative oxygen and the risk of surgical wound infection: a randomized controlled trial. JAMA 294:2035–2042 [View Article][PubMed]
    [Google Scholar]
  7. Belda F. J., Catalá-López F., Greif R., Canet J. 2014; Benefits and risks of intraoperative high inspired oxygen therapy: firm conclusions are still far off. Anesthesiology 120:1051–1052 [View Article][PubMed]
    [Google Scholar]
  8. Björnsdottir H., Welin A., Michaëlsson E., Osla V., Berg S., Christenson K., Sundqvist M., Dahlgren C., Karlsson A., Bylund J. 2015; Neutrophil NET formation is regulated from the inside by myeloperoxidase-processed reactive oxygen species. Free Radic Biol Med 89:1024–1035 [View Article][PubMed]
    [Google Scholar]
  9. Brar M. S., Brar S. S., Dixon E. 2011; Perioperative supplemental oxygen in colorectal patients: a meta-analysis. J Surg Res 166:227–235 [View Article][PubMed]
    [Google Scholar]
  10. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D. S., Weinrauch Y., Zychlinsky A. 2004; Neutrophil extracellular traps kill bacteria. Science 303:1532–1535 [View Article][PubMed]
    [Google Scholar]
  11. Chura J. C., Boyd A., Argenta P. A. 2007; Surgical site infections and supplemental perioperative oxygen in colorectal surgery patients: a systematic review. Surg Infect 8:455–461 [View Article][PubMed]
    [Google Scholar]
  12. Dovi J., Szpaderska A. M., DiPietro L. A. 2004; Neutrophil function in the healing wound: adding insult to injury?. Thromb Haemost 92:275–280 [View Article][PubMed]
    [Google Scholar]
  13. Garrity-Ryan L., Shafikhani S., Balachandran P., Nguyen L., Oza J., Jakobsen T., Sargent J., Fang X., Cordwell S. et al. 2004; The ADP ribosyltransferase domain of Pseudomonas aeruginosa ExoT contributes to its biological activities. Infect Immun 72:546–558 [View Article][PubMed]
    [Google Scholar]
  14. Giacometti A., Cirioni O., Schimizzi A. M., Del Prete M. S., Barchiesi F., D'Errico M. M., Petrelli E., Scalise G. 2000; Epidemiology and microbiology of surgical wound infections. J Clin Microbiol 38:918–922[PubMed]
    [Google Scholar]
  15. Gjødsbøl K., Christensen J. J., Karlsmark T., Jørgensen B., Klein B. M., Krogfelt K. A. 2006; Multiple bacterial species reside in chronic wounds: a longitudinal study. Int Wound J 3:225–231 [View Article][PubMed]
    [Google Scholar]
  16. Goldufsky J., Wood S., Hajihossainlou B., Rehman T., Majdobeh O., Kaufman H. L., Ruby C. E., Shafikhani S. H. 2015a; Pseudomonas aeruginosa exotoxin T induces potent cytotoxicity against a variety of murine and human cancer cell lines. J Med Microbiol 64:164–173 [View Article]
    [Google Scholar]
  17. Goldufsky J., Wood S. J., Jayaraman V., Majdobeh O., Chen L., Qin S., Zhang C., DiPietro L. A., Shafikhani S. H. 2015b; Pseudomonas aeruginosa uses T3SS to inhibit diabetic wound healing. Wound Repair Regen 23:557–564 [View Article]
    [Google Scholar]
  18. Greif R., Laciny S., Rapf B., Hickle R. S., Sessler D. I. 1999; Supplemental oxygen reduces the incidence of postoperative nausea and vomiting. Anesthesiology 91:1246–1252 [View Article][PubMed]
    [Google Scholar]
  19. Greif R., Akça O., Horn E. P., Kurz A., Sessler D. I. Outcomes Research Group 2000; Supplemental perioperative oxygen to reduce the incidence of surgical-wound infection. N Engl J Med 342:161–167 [View Article][PubMed]
    [Google Scholar]
  20. Halbert A. R., Stacey M. C., Rohr J. B., Jopp-McKay A. 1992; The effect of bacterial colonization on venous ulcer healing. Australas J Dermatol 33:75–80[PubMed] [CrossRef]
    [Google Scholar]
  21. Hopf H. W., Hunt T. K., West J. M., Blomquist P., Goodson W. H., Jensen J. A., Jonsson K., Paty P. B., Rabkin J. M. et al. 1997; Wound tissue oxygen tension predicts the risk of wound infection in surgical patients. Arch Surg 132:997–1004 discussion 1005 [View Article][PubMed]
    [Google Scholar]
  22. Hovaguimian F., Lysakowski C., Elia N., Tramèr M. R. 2013; Effect of intraoperative high inspired oxygen fraction on surgical site infection, postoperative nausea and vomiting, and pulmonary function: systematic review and meta-analysis of randomized controlled trials. Anesthesiology 119:303–316 [View Article][PubMed]
    [Google Scholar]
  23. Hunt T. K., Linsey M., Grislis H., Sonne M., Jawetz E. 1975; The effect of differing ambient oxygen tensions on wound infection. Ann Surg 181:35–39 [View Article][PubMed]
    [Google Scholar]
  24. Klebanoff S. J., Kettle A. J., Rosen H., Winterbourn C. C., Nauseef W. M. 2013; Myeloperoxidase: a front-line defender against phagocytosed microorganisms. J Leukoc Biol 93:185–198 [View Article][PubMed]
    [Google Scholar]
  25. Klevens R. M., Edwards J. R., Richards C. L., Horan T. C., Gaynes R. P., Pollock D. A., Cardo D. M. 2007; Estimating health care-associated infections and deaths in U.S. hospitals, 2002. Public Health Rep 122:160–166[PubMed]
    [Google Scholar]
  26. Knighton D. R., Halliday B., Hunt T. K. 1984; Oxygen as an antibiotic. Arch Surg 119:199–204 [View Article]
    [Google Scholar]
  27. Knighton D. R., Halliday B., Hunt T. K. 1986; Oxygen as an antibiotic. Arch Surg 121:191–195 [View Article]
    [Google Scholar]
  28. Kroin J. S., Buvanendran A., Li J., Moric M., Im H. J., Tuman K. J., Shafikhani S. H., Moric H. J., Im K. J. T. 2015; Short-term glycemic control is effective in reducing surgical site infection in diabetic rats. Anesth Analg 120:1289–1296 [View Article][PubMed]
    [Google Scholar]
  29. Lin W. Y., Tsai S. C., Hung G. U., Kwan P. C., Lin C. F., Yuan C. S., Lin Y. C. 2005; Comparison of animal models with soft tissue infection by different bacilli. J Vet Med Sci 67:43–49 [View Article][PubMed]
    [Google Scholar]
  30. Madsen S. M., Westh H., Danielsen L., Rosdahl V. T. 1996; Bacterial colonization and healing of venous leg ulcers. APMIS 104:895–899 [View Article][PubMed]
    [Google Scholar]
  31. Magill S. S., Hellinger W., Cohen J., Kay R., Bailey C., Boland B., Carey D., de Guzman J., Dominguez K. et al. 2012; Prevalence of healthcare-associated infections in acute care hospitals in Jacksonville, Florida. Infect Control Hosp Epidemiol 33:283–291 [View Article][PubMed]
    [Google Scholar]
  32. Malik A., Mohammad Z., Ahmad J. 2013; The diabetic foot infections: biofilms and antimicrobial resistance. Diabetes Metab Syndr 7:101–107 [View Article][PubMed]
    [Google Scholar]
  33. Martin P. 1997; Wound healing – aiming for perfect skin regeneration. Science 276:75–81 [View Article][PubMed]
    [Google Scholar]
  34. Nauseef W. M., Borregaard N. 2014; Neutrophils at work. Nat Immunol 15:602–611 [View Article][PubMed]
    [Google Scholar]
  35. Ohman D. E., Sadoff J. C., Iglewski B. H. 1980; Toxin A-deficient mutants of Pseudomonas aeruginosa PA103: isolation and characterization. Infect Immun 28:899–908[PubMed]
    [Google Scholar]
  36. Qadan M., Akça O., Mahid S. S., Polk H. C. 2009; Perioperative supplemental oxygen therapy and surgical site infection: a meta-analysis of randomized controlled trials. Arch Surg 144:359–366 discussion 366–357 [View Article][PubMed]
    [Google Scholar]
  37. Ramakant P., Verma A. K., Misra R., Prasad K. N., Chand G., Mishra A., Agarwal G., Agarwal A., Mishra S. K. 2011; Changing microbiological profile of pathogenic bacteria in diabetic foot infections: time for a rethink on which empirical therapy to choose?. Diabetologia 54:58–64 [View Article][PubMed]
    [Google Scholar]
  38. Scott R. 2009 The Direct Medical Costs of Healthcare-Associated Infections in US Hospitals and the Benefits of Prevention Atlanta, GA: Centers for Disease Control and Prevention;
    [Google Scholar]
  39. Shafikhani S. H., Engel J. 2006; Pseudomonas aeruginosa type III-secreted toxin ExoT inhibits host-cell division by targeting cytokinesis at multiple steps. Proc Natl Acad Sci U S A 103:15605–15610 [View Article][PubMed]
    [Google Scholar]
  40. Shafikhani S. H., Morales C., Engel J. 2008; The Pseudomonas aeruginosa type III secreted toxin ExoT is necessary and sufficient to induce apoptosis in epithelial cells. Cell Microbiol 10:994–1007 [View Article][PubMed]
    [Google Scholar]
  41. Sjöberg F., Singer M. 2013; The medical use of oxygen: a time for critical reappraisal. J Intern Med 274:505–528 [View Article][PubMed]
    [Google Scholar]
  42. Togioka B., Galvagno S., Sumida S., Murphy J., Ouanes J. P., Wu C. 2012; The role of perioperative high inspired oxygen therapy in reducing surgical site infection: a meta-analysis. Anesth Analg 114:334–342 [View Article][PubMed]
    [Google Scholar]
  43. Tsai W. C., Strieter R. M., Mehrad B., Newstead M. W., Zeng X., Standiford T. J. 2000; CXC chemokine receptor CXCR2 is essential for protective innate host response in murine Pseudomonas aeruginosa pneumonia. Infect Immun 68:4289–4296 [View Article][PubMed]
    [Google Scholar]
  44. Winstanley C., Kaye S. B., Neal T. J., Chilton H. J., Miksch S., Hart C. A. Microbiology Ophthalmic Group 2005; Genotypic and phenotypic characteristics of Pseudomonas aeruginosa isolates associated with ulcerative keratitis. J Med Microbiol 54:519–526 [View Article][PubMed]
    [Google Scholar]
  45. Winterbourn C. C., Kettle A. J., Hampton M. B. 2016; Reactive oxygen species and neutrophil function. Annu Rev Biochem 85:765–792 [View Article][PubMed]
    [Google Scholar]
  46. Wood S., Pithadia R., Rehman T., Zhang L., Plichta J., Radek K. A., Forsyth C., Keshavarzian A., Shafikhani S. H. 2013; Chronic alcohol exposure renders epithelial cells vulnerable to bacterial infection. PLoS One 8:e54646 [View Article][PubMed]
    [Google Scholar]
  47. Wood S., Jayaraman V., Huelsmann E. J., Bonish B., Burgad D., Sivaramakrishnan G., Qin S., DiPietro L. A., Zloza A. et al. 2014; Pro-inflammatory chemokine CCL2 (MCP-1) promotes healing in diabetic wounds by restoring the macrophage response. PLoS One 9:e91574 [View Article][PubMed]
    [Google Scholar]
  48. Wood S., Goldufsky J., Shafikhani S. H. 2015a; Pseudomonas aeruginosa ExoT induces atypical anoikis apoptosis in target host cells by transforming crk adaptor protein into a cytotoxin. PLoS Pathog 11:e1004934 [View Article]
    [Google Scholar]
  49. Wood S. J., Goldufsky J. W., Bello D., Masood S., Shafikhani S. H. 2015b; Pseudomonas aeruginosa ExoT induces mitochondrial apoptosis in target host cells in a manner that depends on its GAP domain activity. J Biol Chem 27:29063–29073 [CrossRef]
    [Google Scholar]
  50. Zhao G., Hochwalt P. C., Usui M. L., Underwood R. A., Singh P. K., James G. A., Stewart P. S., Fleckman P., Olerud J. E. 2010; Delayed wound healing in diabetic (db/db) mice with Pseudomonas aeruginosa biofilm challenge: a model for the study of chronic wounds. Wound Repair Regen 18:467–477 [View Article][PubMed]
    [Google Scholar]
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