Decolonization to Prevent Healthcare-Associated Infections 2024 State-of-the-Art Review

Main Article Content

Edward J. Septimus, MD

Abstract

Colonization with health care-associated pathogens such as Staphylococcus aureus, enterococci, Gram-negative organisms, and Clostridioides difficile is associated with increased risk of infection. Decolonization is an evidence-based intervention that can be used to prevent health care-associated infections. This review evaluates agents used for nasal topical decolonization, topical (e.g., skin) decolonization, oral decolonization, and selective digestive or oropharyngeal decontamination. Although the majority of studies performed to date have focused on S. aureus decolonization, there is increasing interest in how to apply decolonization strategies to reduce infections due to Gram-negative organisms, especially those that are multidrug resistant. Nasal topical decolonization agents reviewed include mupirocin, povidone-iodine, alcohol-based nasal antiseptic, and photodynamic therapy.


Topical decolonization agents reviewed included chlorhexidine gluconate, and povidone-iodine. Of these, CHG is the skin decolonization agent that has the strongest evidence base. There is also evidence to support the use of selective digestive decontamination and selective oropharyngeal decontamination, but additional studies are needed to assess resistance to these agents, especially selection for resistance. Small studies have shown some effect of fecal microbiota transplant against multidrug resistant gram-negative organisms. Some of the strongest evidence for decolonization is to prevent surgical site infections in high-risk procedures primarily cardiac and orthopedic procedures.

Keywords: nasal decolonization, skin decolonization, healthcare-associated infections, selective digestive decontamination

Article Details

How to Cite
SEPTIMUS, Edward J.. Decolonization to Prevent Healthcare-Associated Infections 2024 State-of-the-Art Review. Medical Research Archives, [S.l.], v. 12, n. 10, oct. 2024. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/5782>. Date accessed: 22 dec. 2024. doi: https://doi.org/10.18103/mra.v12i10.5782.
Section
Review Articles

References

1. Magill SS, Edwards JR, Bamberg W, et al. Multistate point-prevalence survey of health care-associated infections. The New England journal of medicine. Mar 27 2014;370(13):1198-208. doi:10. 1056/NEJMoa1306801

2. Zimlichman E, Henderson D, Tamir O, et al. Health care-associated infections: a meta-analysis of costs and financial impact on the US health care system. JAMA internal medicine. Dec 9-23 2013;17 3(22):2039-46. doi:10.1001/jamainternmed.2013.9763

3. WHO Global report on the epidemiology and burden of sepsis. accesseed September 16, 2024 doi:https://iris.who.int/bitstream/handle/10665/334216/9789240010789-eng.pdf?sequence=1

4. Schreiber PW, Sax H, Wolfensberger A, Clack L, Kuster SP. The preventable proportion of healthcare-associated infections 2005-2016: Systematic review and meta-analysis. Infection control and hospital epidemiology. Nov 2018;39 (11):1277-1295. doi:10.1017/ice.2018.183

5. National Action Plan. Accessed June 19, 2024. https://health.gov/about-odphp/previous-initiatives#SSI

6. Magill SS, O'Leary E, Janelle SJ, et al. Changes in Prevalence of Health Care-Associated Infections in U.S. Hospitals. The New England journal of medicine. Nov 1 2018;379(18):1732-1744. doi:10. 1056/NEJMoa1801550

7. EU HAI Report 2022/3. Accessed June 19, 2024. https://www.ecdc.europa.eu/sites/default/files/documents/healthcare-associated-point-prevalence-survey-acute-care-hospitals-2022-2023.pdf

8. Lastinger LM, Alvarez CR, Kofman A, et al. Continued increases in the incidence of healthcare-associated infection (HAI) during the second year of the coronavirus disease 2019 (COVID-19) pandemic. Infection Control & Hospital Epidemiology. 2022:1-5. doi:10.1017/ice.2022.116

9. 2022 National and State Healthcare-Associated Infections Progress Report. Accessed June 19, 2024. https://www.cdc.gov/healthcare-associated-infections/php/data/progress-report.html?CDC_AAref_Val=https://www.cdc.gov/hai/data/portal/progress-report.html

10. Ammerlaan HS, Kluytmans JA, Wertheim HF, Nouwen JL, Bonten MJ. Eradication of methicillin-resistant Staphylococcus aureus carriage: a systematic review. Clin Infect Dis. Apr 1 2009;48 (7):922-30. doi:10.1086/597291

11. Oostdijk EAN, Smet AMGAd, Blok HEM, et al. Ecological Effects of Selective Decontamination on Resistant Gram-negative Bacterial Colonization. American journal of respiratory and critical care medicine. 2010;181(5):452-457. doi:10.1164/rccm. 200908-1210OC

12. D'Amico R, Pifferi S, Torri V, Brazzi L, Parmelli E, Liberati A. Antibiotic prophylaxis to reduce respiratory tract infections and mortality in adults receiving intensive care. Cochrane Database of Systematic Reviews. 2009;(4)doi:10.1002/1465185 8.CD000022.pub3

13. Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nature Reviews Immunology. 2013/11/01 2013;13 (11):790-801. doi:10.1038/nri3535

14. Wertheim HF, Melles DC, Vos MC, et al. The role of nasal carriage in Staphylococcus aureus infections. The Lancet Infectious diseases. Dec 2005;5(12):751-62. doi:10.1016/s1473-3099(05)70295-4

15. VandenBergh MF, Yzerman EP, van Belkum A, Boelens HA, Sijmons M, Verbrugh HA. Follow-up of Staphylococcus aureus nasal carriage after 8 years: redefining the persistent carrier state. Journal of clinical microbiology. Oct 1999;37 (10):3133-40.

16. Sim BL, McBryde E, Street AC, Marshall C. Multiple site surveillance cultures as a predictor of methicillin-resistant Staphylococcus aureus infections. Infection control and hospital epidemiology. Aug 2013;34(8):818-24. doi:10.1086/671273

17. Szumowski JD, Wener KM, Gold HS, et al. Methicillin-Resistant Staphylococcus aureus Colonization, Behavioral Risk Factors, and Skin and Soft-Tissue Infection at an Ambulatory Clinic Serving a Large Population of HIV-Infected Men Who Have Sex with Men. Clinical Infectious Diseases. 2009;49(1):118-121. doi:10.1086/599608

18. Russell DL, Flood A, Zaroda TE, et al. Outcomes of colonization with MRSA and VRE among liver transplant candidates and recipients. Am J Transplant. Aug 2008;8(8):1737-43. doi:10. 1111/j.1600-6143.2008.02304.x

19. Montecalvo MA, Shay DK, Gedris C, et al. A Semiquantitative Analysis of the Fecal Flora of Patients with Vancomycin-Resistant Enterococci: Colonized Patients Pose an Infection Control Risk. Clinical Infectious Diseases. 1997;25(4):929-930. doi:10.1086/597643

20. Wang X, Liu J, Li A. Incidence and risk factors for subsequent infections among rectal carriers with carbapenem-resistant Klebsiella pneumoniae: a systematic review and meta-analysis. The Journal of hospital infection. Mar 2024;145:11-21. doi:10. 1016/j.jhin.2023.12.002

21. Almohaya A, Fersovich J, Weyant RB, et al. The impact of colonization by multidrug resistant bacteria on graft survival, risk of infection, and mortality in recipients of solid organ transplant: systematic review and meta-analysis. Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases. Apr 10 2024;doi:10. 1016/j.cmi.2024.03.036

22. McKinnell JA, Singh RD, Miller LG, et al. The SHIELD Orange County Project: Multidrug-resistant Organism Prevalence in 21 Nursing Homes and Long-term Acute Care Facilities in Southern California. Clinical Infectious Diseases. 2019;69(9):1566-1573. doi:10.1093/cid/ciz119

23. Mody L, Foxman B, Bradley S, et al. Longitudinal Assessment of Multidrug-Resistant Organisms in Newly Admitted Nursing Facility Patients: Implications for an Evolving Population. Clinical Infectious Diseases. 2018;67(6):837-844. doi:10.1093/cid/ciy194

24. Nelson RE, Hatfield KM, Wolford H, et al. National Estimates of Healthcare Costs Associated With Multidrug-Resistant Bacterial Infections Among Hospitalized Patients in the United States. Clinical Infectious Diseases. 2021;72(Supplement_ 1):S17-S26. doi:10.1093/cid/ciaa1581

25. Gussin GM, McKinnell JA, Singh RD, et al. Reducing Hospitalizations and Multidrug-Resistant Organisms via Regional Decolonization in Hospitals and Nursing Homes. Jama. May 14 2024;331 (18):1544-1557. doi:10.1001/jama.2024.2759

26. Kalmeijer MD, Nieuwland-Bollen Ev, Bogaers-Hofman D, Baere GAJd, Kluytmans JAJW. Nasal Carriage of Staphylococcus aureus: Is a Major Risk Factor for Surgical-Site Infections in Orthopedic Surgery. Infection Control & Hospital Epidemiology. 2000;21(5):319-323. doi:10.1086/501763

27. Wenzel RP, Edmond MB. Infection control: the case for horizontal rather than vertical interventional programs. Int J Infect Dis. Oct 2010;14 Suppl 4:S3-5. doi:10.1016/j.ijid.2010.05.002

28. Septimus E, Weinstein RA, Perl TM, Goldmann DA, Yokoe DS. Approaches for preventing healthcare-associated infections: go long or go wide? Infection control and hospital epidemiology. Sep 2014;35 Suppl 2:S10-4.

29. Septimus EJ, Hayden MK, Kleinman K, et al. Does chlorhexidine bathing in adult intensive care units reduce blood culture contamination? A pragmatic cluster-randomized trial. Infection control and hospital epidemiology. Oct 2014;35 Suppl 3:S17-22. doi:10.1086/677822

30. Lee BY, Wiringa AE, Bailey RR, et al. Screening cardiac surgery patients for MRSA: an economic computer model. Am J Manag Care. Jul 1 2010;16(7):e163-73.

31. Immerman I, Ramos NL, Katz GM, Hutzler LH, Phillips MS, Bosco JA, 3rd. The persistence of Staphylococcus aureus decolonization after mupirocin and topical chlorhexidine: implications for patients requiring multiple or delayed procedures. The Journal of arthroplasty. Jun 2012; 27(6):870-6. doi:10.1016/j.arth.2012.01.010

32. Holton DL, Nicolle LE, Diley D, Bernstein K. Efficacy of mupirocin nasal ointment in eradicating Staphylococcus aureus nasal carriage in chronic haemodialysis patients. The Journal of hospital infection. Feb 1991;17(2):133-7. doi:10.1016/0195 -6701(91)90177-a

33. Loeb MB, Main C, Eady A, Walker-Dilks C. Antimicrobial drugs for treating methicillin-resistant Staphylococcus aureus colonization. The Cochrane database of systematic reviews. 2003;(4): Cd003340. doi:10.1002/14651858.Cd003340

34. Bommer J, Vergetis W, Andrassy K, Hingst V, Borneff M, Huber W. Elimination of Staphylococcus aureus in Hemodialysis Patients. ASAIO Journal. 1995;41(1):127-131.

35. Ward A, Campoli-Richards DM. Mupirocin. A review of its antibacterial activity, pharmacokinetic properties and therapeutic use. Drugs. Nov 1986; 32(5):425-44. doi:10.2165/00003495-198632050-00002

36. Perl TM, Cullen JJ, Wenzel RP, et al. Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N Engl J Med. Jun 13 2002;34 6(24):1871-7. doi:10.1056/NEJMoa003069

37. van Rijen M, Bonten M, Wenzel R, Kluytmans J. Mupirocin ointment for preventing Staphylococcus aureus infections in nasal carriers. The Cochrane database of systematic reviews. Oct 8 2008;(4):Cd 006216. doi:10.1002/14651858.CD006216.pub2

38. Schweizer M, Perencevich E, McDanel J, et al. Effectiveness of a bundled intervention of decolonization and prophylaxis to decrease Gram positive surgical site infections after cardiac or orthopedic surgery: systematic review and meta-analysis. Bmj. Jun 13 2013;346:f2743. doi:10.113 6/bmj.f2743

39. Kallen AJ, Wilson CT, Larson RJ. Perioperative intranasal mupirocin for the prevention of surgical-site infections: systematic review of the literature and meta-analysis. Infection control and hospital epidemiology. Dec 2005;26(12):916-22. doi:10.10 86/505453

40. Perez-Fontan M, Rosales M, Rodriguez-Carmona A, Falcon TG, Valdes F. Mupirocin resistance after long-term use for Staphylococcus aureus colonization in patients undergoing chronic peritoneal dialysis. American journal of kidney diseases: the official journal of the National Kidney Foundation. Feb 2002;39(2):337-41.

41. Vasquez JE, Walker ES, Franzus BW, Overbay BK, Reagan DR, Sarubbi FA. The epidemiology of mupirocin resistance among methicillin-resistant Staphylococcus aureus at a Veterans' Affairs hospital. Infection control and hospital epidemiology. Jul 2000;21(7):459-64. doi:10.1086/501788

42. Walker ES, Vasquez JE, Dula R, Bullock H, Sarubbi FA. Mupirocin-resistant, methicillin-resistant Staphylococcus aureus: does mupirocin remain effective? Infection control and hospital epidemiology. May 2003;24(5):342-6. doi:10.1086/502218

43. Fawley WN, Parnell P, Hall J, Wilcox MH. Surveillance for mupirocin resistance following introduction of routine peri-operative prophylaxis with nasal mupirocin. The Journal of hospital infection. Mar 2006;62(3):327-32. doi:10.1016/j.jhi n.2005.09.022

44. Hayden MK, Lolans K, Haffenreffer K, et al. Chlorhexidine and Mupirocin Susceptibility of Methicillin-Resistant Staphylococcus aureus Isolates in the REDUCE-MRSA Trial. Journal of clinical microbiology. Nov 2016;54(11):2735-2742. doi:10.1128/jcm.01444-16

45. Dadashi M, Hajikhani B, Darban-Sarokhalil D, van Belkum A, Goudarzi M. Mupirocin resistance in Staphylococcus aureus: A systematic review and meta-analysis. Journal of Global Antimicrobial Resistance. 2020/03/01/ 2020;20:238-247. doi:https://doi.org/10.1016/j.jgar.2019.07.032

46. Semret M, Miller MA. Topical mupirocin for eradication of MRSA colonization with mupirocin-resistant strains. Infection control and hospital epidemiology. Sep 2001;22(9):578-80. doi:10.108 6/501956

47. Huang SS, Septimus EJ, Kleinman K, et al. Nasal Iodophor Antiseptic vs Nasal Mupirocin Antibiotic in the Setting of Chlorhexidine Bathing to Prevent Infections in Adult ICUs: A Randomized Clinical Trial. JAMA. 2023;330(14):1337-1347. doi: 10.1001/jama.2023.17219

48. Huang SS, Septimus E, Kleinman K, et al. Targeted versus universal decolonization to prevent ICU infection. The New England journal of medicine. Jun 13 2013;368(24):2255-65. doi:10.10 56/NEJMoa1207290

49. Hill RL, Casewell MW. The in-vitro activity of povidone-iodinecream against Staphylococcus aureus and its bioavailability in nasal secretions. The Journal of hospital infection. Jul 2000;45(3) :198-205. doi:10.1053/jhin.2000.0733

50. Rezapoor M, Nicholson T, Tabatabaee RM, Chen AF, Maltenfort MG, Parvizi J. Povidone-Iodine-Based Solutions for Decolonization of Nasal Staphylococcus aureus: A Randomized, Prospective, Placebo-Controlled Study. The Journal of arthroplasty. Sep 2017;32(9):2815-2819. doi:10.10 16/j.arth.2017.04.039

51. Phillips M, Rosenberg A, Shopsin B, et al. Preventing surgical site infections: a randomized, open-label trial of nasal mupirocin ointment and nasal povidone-iodine solution. Infection control and hospital epidemiology. Jul 2014;35(7):826-32. doi:10.1086/676872

52. Saidel-Odes L, Yosipovich R, Benkovich V, et al. Getting the drop on Staphylococcus aureus: Semiquantitative Staphylococcus aureus nasal colony reduction in orthopedic surgery reduces surgical site infection. American journal of infection control. 2024;52(7):785-789. doi:10.1016/j.ajic.2024.02.014

53. Harrison C, Zent R, Schneck E, Flynn CE, Drees M. Infection prevention versus antimicrobial stewardship: Does nasal povidone-iodine interfere with methicillin-resistant Staphylococcus aureus (MRSA) screening? Infection Control & Hospital Epidemiology. 2022;43(7):945-947. doi:10.1017/ ice.2021.152

54. Boyce JM, Pittet D. Guideline for Hand Hygiene in Health-Care Settings. Recommendations of the Healthcare Infection Control Practices Advisory Committee and the HIPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. American journal of infection control. Dec 2002;30(8):S1-46.

55. Steed LL, Costello J, Lohia S, Jones T, Spannhake EW, Nguyen S. Reduction of nasal Staphylococcus aureus carriage in health care professionals by treatment with a nonantibiotic, alcohol-based nasal antiseptic. American journal of infection control. Aug 2014;42(8):841-6. doi:10.1 016/j.ajic.2014.04.008

56. Kanwar A, Kumar JA, Ng-Wong YK, et al. Evaluation of an alcohol-based antiseptic for nasal decolonization of methicillin-resistant Staphylococcus aureus in colonized patients. Infection Control & Hospital Epidemiology. 2019;40(12):1436-1437. doi:10.1017/ice.2019.266

57. Street CN, Pedigo L, Gibbs A, Loebel NG. Antimicrobial photodynamic therapy for the decolonization of methicillin-resistant Staphylococcus aureus from the anterior nares. SPIE; 2009:16.

58. Bryce E, Wong T, Forrester L, et al. Nasal photodisinfection and chlorhexidine wipes decrease surgical site infections: a historical control study and propensity analysis. The Journal of hospital infection. Oct 2014;88(2):89-95. doi:10.1 016/j.jhin.2014.06.017

59. Embleton ML, Nair SP, Cookson BD, Wilson M. Antibody-Directed Photodynamic Therapy of MethicillinResistant Staphylococcus aureus. Microbial Drug Resistance. 2004/06/01 2004;10 (2):92-97. doi:10.1089/1076629041310000

60. Bezerra DT, La Selva A, Cecatto RB, et al. Antimicrobial Photodynamic Therapy in the Nasal Decolonization of Maintenance Hemodialysis Patients: A Pilot Randomized Trial. American journal of kidney diseases : the official journal of the National Kidney Foundation. May 2023;81(5):528-536.e1. doi:10.1053/j.ajkd.2022.09.013

61. Weinstein RA, Milstone AM, Passaretti CL, Perl TM. Chlorhexidine: Expanding the Armamentarium for Infection Control and Prevention. Clinical Infectious Diseases. 2008;46(2):274-281. doi:10.1 086/524736

62. Maki DG, Alvarado CJ, Ringer M. Prospective randomised trial of povidone-iodine, alcohol, and chlorhexidine for prevention of infection associated with central venous and arterial catheters. The Lancet. 1991;338(8763):339-343. doi:10.1016/0140-6736(91)90479-9

63. Vernon MO, Hayden MK, Trick WE, et al. Chlorhexidine Gluconate to Cleanse Patients in a Medical Intensive Care Unit: The Effectiveness of Source Control to Reduce the Bioburden of Vancomycin-Resistant Enterococci. Archives of internal medicine. 2006;166(3):306-312. doi:10.10 01/archinte.166.3.306

64. Bleasdale SC, Trick WE, Gonzalez IM, Lyles RD, Hayden MK, Weinstein RA. Effectiveness of Chlorhexidine Bathing to Reduce Catheter-Associated Bloodstream Infections in Medical Intensive Care Unit Patients. Archives of internal medicine. 2007;167(19):2073-2079. doi:10.1001/a rchinte.167.19.2073

65. Borer A, Gilad J, Porat N, et al. Impact of 4% chlorhexidine whole-body washing on multidrug-resistant Acinetobacter baumannii skin colonisation among patients in a medical intensive care unit. Journal of Hospital Infection. 2007;67(2):149-155. doi:10.1016/j.jhin.2007.07.023

66. Climo MW, Yokoe DS, Warren DK, et al. Effect of daily chlorhexidine bathing on hospital-acquired infection. The New England journal of medicine. Feb 7 2013;368(6):533-42. doi:10.1056/NEJMoa 1113849

67. Milstone AM, Elward A, Song X, et al. Daily chlorhexidine bathing to reduce bacteraemia in critically ill children: a multicentre, cluster-randomised, crossover trial. Lancet (London, England). 2013;381(9872):1099-1106. doi:10.1016 /S0140-6736(12)61687-0

68. Huang SS, Septimus E, Platt R. Targeted decolonization to prevent ICU infections. The New England journal of medicine. Oct 10 2013;369( 15):1470-1. doi:10.1056/NEJMc1309704

69. Septimus E, Hickok J, Moody J, et al. Closing the Translation Gap: Toolkit-based Implementation of Universal Decolonization in Adult Intensive Care Units Reduces Central Line-associated Bloodstream Infections in 95 Community Hospitals. Clin Infect Dis. Jul 15 2016;63(2):172-7. doi:10.1093/cid/ciw282

70. Derde LPG, Cooper BS, Goossens H, et al. Interventions to reduce colonisation and transmission of antimicrobial-resistant bacteria in intensive care units: an interrupted time series study and cluster randomised trial. The Lancet Infectious Diseases. 2014;14(1):31-39. doi:10.101 6/S1473-3099(13)70295-0

71. Noto MJ, Domenico HJ, Byrne DW, et al. Chlorhexidine Bathing and Health Care–Associated Infections: A Randomized Clinical Trial. JAMA. 2015;313(4):369-378. doi:10.1001/jama.20 14.18400

72. Huang SS, Septimus E, Kleinman K, et al. Chlorhexidine versus routine bathing to prevent multidrug-resistant organisms and all-cause bloodstream infections in general medical and surgical units (ABATE Infection trial): a cluster-randomised trial. Lancet (London, England). 2019;393(10177):1205-1215. doi:10.1016/S0140-6736(18)32593-5

73. Tien KL, Sheng WH, Shieh SC, et al. Chlorhexidine Bathing to Prevent Central Line-Associated Bloodstream Infections in Hematology Units: A Prospective, Controlled Cohort Study. Clin Infect Dis. Jul 27 2020;71(3):556-563. doi:10.109 3/cid/ciz874

74. Denkel LA, Schwab F, Clausmeyer J, et al. Effect of antiseptic bathing with chlorhexidine or octenidine on central line–associated bloodstream infections in intensive care patients: a cluster-randomized controlled trial. Clinical Microbiology and Infection. 2022;28(6):825-831. doi:10.1016/ j.cmi.2021.12.023

75. Sturm L, Service N, Bufalino A, et al. Is Hospital-Onset Bloodstream Infection (HOBSI) a Useful Measure to Evaluate Infection Prevention Progress? Infection Control & Hospital Epidemiology. 2020;41(S1):s307-s308. doi:10.101 7/i ce.2020.894

76. Page B, Klompas M, Chan C, et al. Surveillance for Healthcare-Associated Infections: Hospital-Onset Adult Sepsis Events Versus Current Reportable Conditions. Clinical Infectious Diseases. 2021;73(6 ):1013-1019. doi:10.1093/cid/ciab217

77. Yu KC, Jung M, Ai C. Characteristics, costs, and outcomes associated with central-line-associated bloodstream infection and hospital-onset bacteremia and fungemia in US hospitals. Infection control and hospital epidemiology. Dec 2023;44(12):1920-1926. doi:10.1017/ice.2023.132

78. Blauw M, Foxman B, Wu J, Rey J, Kothari N, Malani AN. Risk Factors and Outcomes Associated With Hospital-Onset Peripheral Intravenous Catheter–Associated Staphylococcus aureus Bacteremia. Open forum infectious diseases. 2019; 6(4)doi:10.1093/ofid/ofz111

79. Garcia R, Septimus EJ, LeDonne J, et al. Prevention of Vascular Access Device-Associated Hospital Onset Bacteremia and Fungemia: A Review of Emerging Perspectives and Synthesis of Technical Aspects. Clinical Infectious Diseases. 2024;doi:10.1093/cid/ciae245

80. Buetti N, Marschall J, Drees M, et al. Strategies to prevent central line-associated bloodstream infections in acute-care hospitals: 2022 Update. Infection control and hospital epidemiology. May 2022;43(5):553-569. doi:10.1017/ice.2022.87

81. Block C, Robenshtok E, Simhon A, Shapiro M. Evaluation of chlorhexidine and povidone iodine activity against methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus faecalis using a surface test. Journal of Hospital Infection. 2000;46(2):147-152. doi:10.1053/jhin.2000.0805

82. Smylie HG, Logie JRC, Smith G. From Phisohex to Hibiscrub. British Medical Journal. 1973;4(5892):586-589. doi:10.1136/bmj.4.5892.586

83. null n. Skin Antisepsis before Surgical Fixation of Extremity Fractures. New England Journal of Medicine. 2024/01/31 2024;390(5):409-420. doi:1 0.1056/NEJMoa2307679

84. Widmer AF, Atkinson A, Kuster SP, et al. Povidone Iodine vs Chlorhexidine Gluconate in Alcohol for Preoperative Skin Antisepsis: A Randomized Clinical Trial. JAMA. 2024;doi:10.100 1/jama.2024.8531

85. Calderwood MS, Anderson DJ, Bratzler DW, et al. Strategies to prevent surgical site infections in acute-care hospitals: 2022 Update. Infection control and hospital epidemiology. May 2023;44 (5):695-720. doi:10.1017/ice.2023.67

86. Chan EY, Ruest A, Meade MO, Cook DJ. Oral decontamination for prevention of pneumonia in mechanically ventilated adults: systematic review and meta-analysis. BMJ. 2007;334(7599):889. doi:1 0.1136/bmj.39136.528160.BE

87. Smet AMGAd, Kluytmans JAJW, Cooper BS, et al. Decontamination of the Digestive Tract and Oropharynx in ICU Patients. New England Journal of Medicine. 2009;360(1):20-31. doi:10.1056/NEJ Moa0800394

88. de Smet AMGA, Kluytmans JAJW, Blok HEM, et al. Selective digestive tract decontamination and selective oropharyngeal decontamination and antibiotic resistance in patients in intensive-care units: an open-label, clustered group-randomised, crossover study. The Lancet Infectious Diseases. 2011;11(5):372-380. doi:10.1016/S1473-3099(11)70035-4

89. Oostdijk EAN, Kesecioglu J, Schultz MJ, et al. Effects of Decontamination of the Oropharynx and Intestinal Tract on Antibiotic Resistance in ICUs: A Randomized Clinical Trial. JAMA. 2014;312(14) :1429-1437. doi:10.1001/jama.2014.7247

90. Price R, MacLennan G, Glen J. Selective digestive or oropharyngeal decontamination and topical oropharyngeal chlorhexidine for prevention of death in general intensive care: systematic review and network meta-analysis. BMJ : British Medical Journal. 2014;348:g2197. doi:10.1136/bmj.g2197

91. Klompas M, Branson R, Cawcutt K, et al. Strategies to prevent ventilator-associated pneumonia, ventilator-associated events, and nonventilator hospital-acquired pneumonia in acute-care hospitals: 2022 Update. Infection Control & Hospital Epidemiology. 2022;43(6):687-713. doi:10.1017/ice.2022.88

92. Daneman N, Sarwar S, Fowler RA, Cuthbertson BH. Effect of selective decontamination on antimicrobial resistance in intensive care units: a systematic review and meta-analysis. The Lancet Infectious Diseases. 2013;13(4):328-341. doi:10.10 16/S1473-3099(12)70322-5

93. Plantinga NL, de Smet A, Oostdijk EAN, et al. Selective digestive and oropharyngeal decontamination in medical and surgical ICU patients: individual patient data meta-analysis. Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases. May 2018; 24(5):505-513. doi:10.1016/j.cmi.2017.08.019

94. Hammond NE, Myburgh J, Seppelt I, et al. Association Between Selective Decontamination of the Digestive Tract and In-Hospital Mortality in Intensive Care Unit Patients Receiving Mechanical Ventilation: A Systematic Review and Meta-analysis. JAMA. 2022;328(19):1922-1934. doi:10.1 001/jama.2022.19709

95. Huttner B, Haustein T, Uçkay I, et al. Decolonization of intestinal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae with oral colistin and neomycin: a randomized, double-blind, placebo-controlled trial. Journal of Antimicrobial Chemotherapy. 2013;68(10):2375-2382. doi:10.1093/jac/dkt174

96. Saidel-Odes L, Polachek H, Peled N, et al. A Randomized, Double-Blind, Placebo-Controlled Trial of Selective Digestive Decontamination Using Oral Gentamicin and Oral Polymyxin E for Eradication of Carbapenem-Resistant Klebsiella pneumoniae Carriage. Infection Control & Hospital Epidemiology. 2012;33(1):14-19. doi:10.1086/663206

97. Oren I, Sprecher H, Finkelstein R, et al. Eradication of carbapenem-resistant Enterobacteriaceae gastrointestinal colonization with nonabsorbable oral antibiotic treatment: A prospective controlled trial. American journal of infection control. 2013;41(12):1167-1172. doi:10. 1016/j.ajic.2013.04.018

98. Bilsen MP, Lambregts MMC, van Prehn J, Kuijper EJ. Faecal microbiota replacement to eradicate antimicrobial resistant bacteria in the intestinal tract – a systematic review. Current Opinion in Gastroenterology. 2022;38(1):15-25. doi:10.1097/mog.0000000000000792

99. Macareño-Castro J, Solano-Salazar A, Dong LT, Mohiuddin M, Espinoza JL. Fecal microbiota transplantation for Carbapenem-Resistant Enterobacteriaceae: A systematic review. Journal of Infection. 2022;84(6):749-759. doi:10.1016/ j.jinf.2022.04.028

100. Huttner BD, de Lastours V, Wassenberg M, et al. A 5-day course of oral antibiotics followed by faecal transplantation to eradicate carriage of multidrug-resistant Enterobacteriaceae : a randomized clinical trial. Clinical Microbiology and Infection. 2019;25(7):830-838. doi:10.1016/j.cmi.2018.12.009

101. Woodworth MH, Conrad RE, Haldopoulos M, et al. Fecal microbiota transplantation promotes reduction of antimicrobial resistance by strain replacement. Science Translational Medicine. 2023 ;15(720):eabo2750. doi:doi:10.1126/scitranslmed. abo2750

102. Bode LGM, Kluytmans JAJW, Wertheim HFL, et al. Preventing Surgical-Site Infections in Nasal Carriers of Staphylococcus aureus. New England Journal of Medicine. 2010;362(1):9-17. doi:10.10 56/NEJMoa0808939

103. Cimochowski GE, Harostock MD, Brown R, Bernardi M, Alonzo N, Coyle K. Intranasal mupirocin reduces sternal wound infection after open heart surgery in diabetics and nondiabetics. The Annals of thoracic surgery. May 2001;71(5) :1572-8; discussion 1578-9.

104. Schweizer ML, Chiang HY, Septimus E, et al. Association of a bundled intervention with surgical site infections among patients undergoing cardiac, hip, or knee surgery. Jama. Jun 2 2015;313 (21):2162-71. doi:10.1001/jama.2015.5387

105. Bebko SP, Green DM, Awad SS. Effect of a preoperative decontamination protocol on surgical site infections in patients undergoing elective orthopedic surgery with hardware implantation. JAMA surgery. May 2015;150(5):390-5. doi:10.100 1/jamasurg.2014.3480

106. Mullen A, Wieland HJ, Wieser ES, Spannhake EW, Marinos RS. Perioperative participation of orthopedic patients and surgical staff in a nasal decolonization intervention to reduce Staphylococcus spp surgical site infections. American journal of infection control. May 1 2017; 45(5):554-556. doi:10.1016/j.ajic.2016.12.021

107. Bostian PA, Vaida J, Brooks WC, et al. A Novel Protocol for Nasal Decolonization Using Prolonged Application of an Alcohol-Based Nasal Antiseptic Reduces Surgical Site Infections in Total Joint Arthroplasty Patients: A Retrospective Cohort Study. Surg Infect (Larchmt). Sep 2023;24(7):651-656. doi:10.1089/sur.2022.344

108. Sławiński G, Lewicka E, Kempa M, Budrejko S, Raczak G. Infections of cardiac implantable electronic devices: Epidemiology, classification, treatment, and prognosis. Adv Clin Exp Med. Feb 2019;28(2):263-270. doi:10.17219/acem/80665

109. Sandoe JA, Barlow G, Chambers JB, et al. Guidelines for the diagnosis, prevention and management of implantable cardiac electronic device infection. Report of a joint Working Party project on behalf of the British Society for Antimicrobial Chemotherapy (BSAC, host organization), British Heart Rhythm Society (BHRS), British Cardiovascular Society (BCS), British Heart Valve Society (BHVS) and British Society for Echocardiography (BSE). The Journal of antimicrobial chemotherapy. Feb 2015;70(2):325-59. doi:10.1093/jac/dku383