J Korean Med Assoc.  2018 Jan;61(1):26-35. 10.5124/jkma.2018.61.1.26.

Management of multi-drug resistant organisms in healthcare settings

• Park SH

• KMID: 2405133
• DOI: http://doi.org/10.5124/jkma.2018.61.1.26

Abstract

Antimicrobial resistance is an important global threat to public health. Hospitals, in particular, are increasingly faced with the emergence and transmission of multidrug-resistant organisms (MDROs). In hospitals, MDROs are transmitted via the hands of healthcare workers, from the contaminated environment, or directly from person to person. Although the transmission of MDROs is frequently recognized in acute care facilities, all healthcare settings are affected by MDROs. Given the evolving epidemiology of MDROs and the complexity of managing them across heterogeneous healthcare settings, multimodal strategies should be adopted to control and prevent the transmission of MDROs. It is fundamental to ensure adherence to evidence-based healthcare-associated infection prevention strategies, including hand hygiene, antimicrobial stewardship, and adequate environmental cleaning, and to ensure the reliable performance of basic infection prevention practices known to mitigate the transmission of MDROs. Healthcare-associated infections and MDROs should be surveilled in a standardized manner in order to detect outbreaks and newly introduced MDROs in healthcare facilities. When epidemiologically important pathogens newly emerge in healthcare facilities or to control outbreaks of specific pathogens, active surveillance cultures combined with preemptive isolation and contact precautions can also be implemented. Healthcare facilities should make sure that appropriate strategies are fully implemented, regularly evaluated for effectiveness, and adjusted as needed. Successful prevention and control of MDROs can be accomplished by administrative leadership, financial and human resource commitments by individual healthcare facilities, and continuous governmental efforts to make resources available for infection prevention and control.

Keyword

Drug resistance, multiple, bacterial; Prevention & control; Healthcare facilities

MeSH Terms

Delivery of Health Care*
Disease Outbreaks
Drug Resistance, Multiple, Bacterial
Epidemiology
Hand
Hand Hygiene
Humans
Leadership
Public Health

Reference

1. World Health Organization. WHO global strategy for containment of antimicrobial resistance [Internet]. Geneva: World Health Organization;2001. [cited 2017 Dec 15]. Available from:. http://www.who.int/drugresistance/WHO_Global_Strategy_English.pdf.

2. Kim HS, Kim JI, Park C. Monitoring of antimicrobial resistance on non-tertiary hospitals in Korea, 2007-2014. Public Health Wkly Rep. 2015; 9:405–408.

3. Korea Centers for Disease Control and Prevention. Epidemic investigation report for imported CRE outbreak in Korea [Internet]. Cheongju: Korea Centers for Disease Control and Prevention;2013. [cited 2017 Dec 15]. Available from:. http://cdc.go.kr/CDC/cms/content/mobile/61/21361_view.html.

4. Jayol A, Poirel L, Dortet L, Nordmann P. National survey of colistin resistance among carbapenemase-producing Enterobacteriaceae and outbreak caused by colistin-resistant OXA-48-producing Klebsiella pneumoniae, France, 2014. Euro Surveill. 2016; 21.

5. Jeong SH, Kim HS, Kim JS, Shin DH, Kim HS, Park MJ, Shin S, Hong JS, Lee SS, Song W. Prevalence and molecular characteristics of carbapenemase-producing enterobacteriaceae from five hospitals in Korea. Ann Lab Med. 2016; 36:529–535.

6. Siegel JD, Rhinehart E, Jackson M, Chiarello L. Healthcare Infection Control Practices Advisory Committee. Management of multidrug-resistant organisms in health care settings, 2006. Am J Infect Control. 2007; 35(10 Suppl 2):S165–S193.

7. World Health Organization. WHO guidelines on hand hygiene in health care [Internet]. Geneva: World Health Organization;2009. [cited 2017 Dec 15]. Available from:. http://www.who.int/gpsc/5may/tools/9789241597906/en/.

8. Kim YA, Lee H, Lee K. Contamination of the hospital environmental by pathogenic bacteria and infection control. Korean J Nosocomial Infect Control. 2015; 20:1–6.

9. Dancer SJ. Controlling hospital-acquired infection: focus on the role of the environment and new technologies for decontamination. Clin Microbiol Rev. 2014; 27:665–690.

10. Teerawattanapong N, Kengkla K, Dilokthornsakul P, Saokaew S, Apisarnthanarak A, Chaiyakunapruk N. Prevention and control of multidrug-resistant gram-negative bacteria in adult intensive care units: a systematic review and network metaanalysis. Clin Infect Dis. 2017; 64(Suppl 2):S51–S60.

11. Goodman ER, Platt R, Bass R, Onderdonk AB, Yokoe DS, Huang SS. Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms. Infect Control Hosp Epidemiol. 2008; 29:593–599.

12. Kim D, Ahn JY, Lee CH, Jang SJ, Lee H, Yong D, Jeong SH, Lee K. Increasing resistance to extended-spectrum cephalosporins, fluoroquinolone, and carbapenem in gram-negative bacilli and the emergence of carbapenem non-susceptibility in Klebsiella pneumoniae: analysis of Korean Antimicrobial Resistance Monitoring System (KARMS) Data From 2013 to 2015. Ann Lab Med. 2017; 37:231–239.

13. Choi JY, Kwak YG, Yoo H, Lee SO, Kim HB, Han SH, Choi HJ, Kim HY, Kim SR, Kim TH, Lee H, Chun HK, Kim JS, Eun BW, Kim DW, Koo HS, Cho EH, Lee K. Korean Nosocomial Infections Surveillance System. Trends in the distribution and antimicrobial susceptibility of causative pathogens of device-associated infection in Korean intensive care units from 2006 to 2013: results from the Korean Nosocomial Infections Surveillance System (KONIS). J Hosp Infect. 2016; 92:363–371.

14. Hong SK, Yong D, Kim K, Hong SS, Hong SG, Khosbayar T, Song W, Roh KH, Jeong SH, Lee K, Chong Y. First outbreak of KPC-2-producing Klebsiella pneumoniae sequence type 258 in a hospital in South Korea. J Clin Microbiol. 2013; 51:3877–3879.

15. Park JW, Lee E, Lee SJ, Lee H. Status of carbapenemase-producing enterobacteriaceae incidences in Korea, 2015-2016. Public Health Wkly Rep. 2017; 10:1243–1247.

16. Sievert DM, Ricks P, Edwards JR, Schneider A, Patel J, Srinivasan A, Kallen A, Limbago B, Fridkin S. National Healthcare Safety Network (NHSN) Team and Participating NHSN Facilities. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009-2010. Infect Control Hosp Epidemiol. 2013; 34:1–14.

17. Korea Centers for Disease Control and Prevention. Standard guidelines for infection prevention and control 2017 [Internet]. Cheongju: Korean Centers for Disease Control and Prevention;2017. [cited 2017 Dec 15]. Available from:. http://cdc.go.kr/CDC/together/CdcKrTogether0302.jsp?menuIds=HOME001-MNU1154-MNU0005-MNU0088&fid=51&q_type=title&q_value=%ED%91%9C%EC%A4%80&cid=75626&pageNum=.

18. Tacconelli E, De Angelis G, Cataldo MA, Pozzi E, Cauda R. Does antibiotic exposure increase the risk of methicillin-resistant Staphylococcus aureus (MRSA) isolation? A systematic review and metaanalysis. J Antimicrob Chemother. 2008; 61:26–38.

19. Tinelli M, Cataldo MA, Mantengoli E, Cadeddu C, Cunietti E, Luzzaro F, Rossolini GM, Tacconelli E. Epidemiology and genetic characteristics of extended-spectrum β-lactamase-producing Gram-negative bacteria causing urinary tract infections in longterm care facilities. J Antimicrob Chemother. 2012; 67:2982–2987.

20. Tacconelli E, De Angelis G, Cataldo MA, Mantengoli E, Spanu T, Pan A, Corti G, Radice A, Stolzuoli L, Antinori S, Paradisi F, Carosi G, Bernabei R, Antonelli M, Fadda G, Rossolini GM, Cauda R. Antibiotic usage and risk of colonization and infection with antibiotic-resistant bacteria: a hospital population-based study. Antimicrob Agents Chemother. 2009; 53:4264–4269.

21. Barlam TF, Cosgrove SE, Abbo LM, MacDougall C, Schuetz AN, Septimus EJ, Srinivasan A, Dellit TH, Falck-Ytter YT, Fishman NO, Hamilton CW, Jenkins TC, Lipsett PA, Malani PN, May LS, Moran GJ, Neuhauser MM, Newland JG, Ohl CA, Samore MH, Seo SK, Trivedi KK. Implementing an antibiotic stewardship program: guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin Infect Dis. 2016; 62:e51–e77.

22. Kim HI, Kim SW, Chang HH, Kim HB. A survey of antimicrobial stewardship programs in Korean hospitals. Korean J Med. 2014; 87:173–181.

23. Huang SS, Rifas-Shiman SL, Warren DK, Fraser VJ, Climo MW, Wong ES, Cosgrove SE, Perl TM, Pottinger JM, Herwaldt LA, Jernigan JA, Tokars JL, Diekema DJ, Hinrichsen VL, Yokoe DS, Platt R. Centers for Disease Control and Prevention Epicenters Program. Improving methicillin-resistant Staphylococcus aureus surveillance and reporting in intensive care units. J Infect Dis. 2007; 195:330–338.

24. Huskins WC, Huckabee CM, O'Grady NP, Murray P, Kopetskie H, Zimmer L, Walker ME, Sinkowitz-Cochran RL, Jernigan JA, Samore M, Wallace D, Goldmann DA. STAR∗ICU Trial Investigators. Intervention to reduce transmission of resistant bacteria in intensive care. N Engl J Med. 2011; 364:1407–1418.

25. Septimus E, Weinstein RA, Perl TM, Goldmann DA, Yokoe DS. Approaches for preventing healthcare-associated infections: go long or go wide? Infect Control Hosp Epidemiol. 2014; 35:797–801.

26. Weber SG, Huang SS, Oriola S, Huskins WC, Noskin GA, Harriman K, Olmsted RN, Bonten M, Lundstrom T, Climo MW, Roghmann MC, Murphy CL, Karchmer TB. Legislative mandates for use of active surveillance cultures to screen for methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci: position statement from the Joint SHEA and APIC Task Force. Am J Infect Control. 2007; 35:73–85.

27. Vos MC, Behrendt MD, Melles DC, Mollema FP, de Groot W, Parlevliet G, Ott A, Horst-Kreft D, van Belkum A, Verbrugh HA. 5 Years of experience implementing a methicillin-resistant Staphylococcus aureus search and destroy policy at the largest university medical center in the Netherlands. Infect Control Hosp Epidemiol. 2009; 30:977–984.

28. Hayden MK, Lin MY, Lolans K, Weiner S, Blom D, Moore NM, Fogg L, Henry D, Lyles R, Thurlow C, Sikka M, Hines D, Weinstein RA. Centers for Disease Control and Prevention Epicenters Program. Prevention of colonization and infection by Klebsiella pneumoniae carbapenemase-producing enterobacteriaceae in longterm acute-care hospitals. Clin Infect Dis. 2015; 60:1153–1161.

29. Schwaber MJ, Lev B, Israeli A, Solter E, Smollan G, Rubino-vitch B, Shalit I, Carmeli Y. Israel Carbapenem-Resistant Enterobacteriaceae Working Group. Containment of a countrywide outbreak of carbapenem-resistant Klebsiella pneumoniae in Israeli hospitals via a nationally implemented intervention. Clin Infect Dis. 2011; 52:848–855.

30. Kim NH, Han WD, Song KH, Seo HK, Shin MJ, Kim TS, Park KU, Ahn S, Yoo JS, Kim ES, Kim HB. Successful containment of carbapenem-resistant Enterobacteriaceae by strict contact precautions without active surveillance. Am J Infect Control. 2014; 42:1270–1273.

31. Ben-David D, Maor Y, Keller N, Regev-Yochay G, Tal I, Shachar D, Zlotkin A, Smollan G, Rahav G. Potential role of active surveillance in the control of a hospital-wide outbreak of carbapenem-resistant Klebsiella pneumoniae infection. Infect Control Hosp Epidemiol. 2010; 31:620–626.

32. World Health Organization. Guidelines for the prevention and control of carbapenem-resistant Enterobacteriaceae, Acinetobacter baumannii and Pseudomonas aeruginosa in health care facilities [Internet]. Geneva: World Health Organization;2017. [cited 2017 Dec 15]. Available from:. http://www.who.int/infection-prevention/publications/guidelines-cre/en/.

33. Tacconelli E, Cataldo MA, Dancer SJ, De Angelis G, Falcone M, Frank U, Kahlmeter G, Pan A, Petrosillo N, Rodriguez-Bano J, Singh N, Venditti M, Yokoe DS, Cookson B. European Society of Clinical Microbiology. ESCMID guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients. Clin Microbiol Infect. 2014; 20(Suppl 1):1–55.

34. Korea Centers for Disease Control and Prevention. Guidelines for Healthcare Associated Infection Prevention and Control (VRSA, CRE) [Internet]. Cheongju: Korea Centers for Disease Control and Prevention;2017. [cited 2017 Dec 15]. Available from:. http://cdc.go.kr/CDC/cms/content/mobile/74/74974_view.html.

35. Santos RP, Mayo TW, Siegel JD. Healthcare epidemiology: active surveillance cultures and contact precautions for control of multidrug-resistant organisms: ethical considerations. Clin Infect Dis. 2008; 47:110–116.

36. Diekema DJ, Pfaller MA. Rapid detection of antibiotic-resistant organism carriage for infection prevention. Clin Infect Dis. 2013; 56:1614–1620.

37. Anderson DJ, Chen LF, Weber DJ, Moehring RW, Lewis SS, Triplett PF, Blocker M, Becherer P, Schwab JC, Knelson LP, Lokhnygina Y, Rutala WA, Kanamori H, Gergen MF, Sexton DJ. CDC Prevention Epicenters Program. Enhanced terminal room disinfection and acquisition and infection caused by multidrug-resistant organisms and Clostridium difficile (the Benefits of Enhanced Terminal Room Disinfection study): a cluster-randomised, multicentre, crossover study. Lancet. 2017; 389:805–814.

38. O'Fallon E, Gautam S, D'Agata EM. Colonization with mul-tidrug-resistant gram-negative bacteria: prolonged duration and frequent cocolonization. Clin Infect Dis. 2009; 48:1375–1381.