Journal List > Ann Clin Microbiol > v.18(4) > 1078523

Kim and Lee: Active Surveillance of Multidrug-Resistant Organisms with Rapid Detection Methods for Infection Control

초록

Antibiotic-resistant bacteria have become an increas-ingly serious problem in Korea, and multidrug-resistant organisms (MDROs) such as methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococcus (VRE), and multidrug-resistant Pseudomonas aeruginosa and Acinetobacter baumannii have increased over the recent years. More seriou-sly, the recent emergence of carbapenem resistance among Enterobacteriaceae is thought to be an urgent worldwide threat. Active surveillance have been identified as an important tool as an intensified infection control intervention for the control of MRSA and VRE and may be also an effective strategy for multi-drug-resistant Gram-negative bacilli. Rapid detection using molecular methods could aid in the timely detection of MDRO carriers, and adequate application of infection control strategy could reduce the transmission of MDROs within hospital settings.

REFERENCES

1.CDC. CDC web sites on Antibiotic Resistance Threats in the United States, 2013. www.cdc.gov/drugresistance/threat-report-2013/. [Online] (last visited on 16 September 2015).
2.Martín-Loeches I., Diaz E., Vallés J. Risks for multidrug-resistant pathogens in the ICU. Curr Opin Crit Care. 2014. 20:516–24.
crossref
3.DeLeo FR., Chambers HF. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J Clin Invest. 2009. 119:2464–74.
4.DiazGranados CA., Jernigan JA. Impact of vancomycin resistance on mortality among patients with neutropenia and en-terococcal bloodstream infection. J Infect Dis. 2005. 191:588–95.
crossref
5.Esterly JS., Griffith M., Qi C., Malczynski M., Postelnick MJ., Scheetz MH. Impact of carbapenem resistance and receipt of active antimicrobial therapy on clinical outcomes of Acinetobacter baumannii bloodstream infections. Antimicrob Agents Chemother. 2011. 55:4844–9.
6.Patel G., Huprikar S., Factor SH., Jenkins SG., Calfee DP. Outcomes of carbapenem-resistant Klebsiella pneumoniae infection and the impact of antimicrobial and adjunctive therapies. Infect Control Hosp Epidemiol. 2008. 29:1099–106.
7.Korea Centers for Disease Control and Prevention. Infection Control Guidelines for Multidrug Resistant Microorganisms in Healthcare Facilities. http://www.cdc.go.kr/CDC/together/CdcKrTogether0302.jsp?menuIds=HOME001-MNU1154-MNU0004-MN U0088&fid=51&q_type=title&q_value=%EB%8B%A4%EC%A0%9C%EB%82%B4%EC%84%B1%EA%B7%A0&cid=18712&page Num=/. [Online] (last visited on 16 September 2015).
8.Backman C., Taylor G., Sales A., Marck PB. An integrative review of infection prevention and control programs for multidrug- resistant organisms in acute care hospitals: a socio-ecological perspective. Am J Infect Control. 2011. 39:368–78.
9.Diekema DJ., Pfaller MA. Rapid detection of antibiotic-re-sistant organism carriage for infection prevention. Clin Infect Dis. 2013. 56:1614–20.
crossref
10.Lee Y., Kim YA., Song W., Lee H., Lee HS., Jang SJ, et al. Recent trends in antimicrobial resistance in intensive care units in Korea. Korean J Nosocomial Infect Control. 2014. 19:29–36.
crossref
11.Xu J., Duan X., Wu H., Zhou Q. Surveillance and correlation of antimicrobial usage and resistance of Pseudomonas aeruginosa: a hospital population-based study. PLoS One. 2013. 8:e78604.
12.Korea Centers for Disease Control and Prevention. Emergence and characteristics of carbapenemase-producing Enterobacteriaceae (CPE) in Korea, 2012. www.cdc.go.kr/CDC/contents/CdcKrContentLink.jsp?fid=31&cid=20994&ctype=6/. [Online] (last visited on 16 September 2015).
13.Cho SY., Huh HJ., Baek JY., Chung NY., Ryu JG., Ki CS, et al. Klebsiella pneumoniae co-producing NDM-5 and OXA-181 carbapenemases, South Korea. Emerg Infect Dis. 2015. 21:1088–9.
14.Sader HS., Farrell DJ., Flamm RK., Jones RN. Antimicrobial susceptibility of Gram-negative organisms isolated from patients hospitalized in intensive care units in United States and European hospitals (2009-2011). Diagn Microbiol Infect Dis. 2014. 78:443–8.
crossref
15.Cantón R. Role of the microbiology laboratory in infectious disease surveillance, alert and response. Clin Microbiol Infect. 2005. 11(Suppl 1):3–8.
crossref
16.Muto CA., Jernigan JA., Ostrowsky BE., Richet HM., Jarvis WR., Boyce JM, et al. SHEA. SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and Enterococcus. Infect Control Hosp Epidemiol. 2003. 24:362–86.
17.Tsiatsiou O., Iosifidis E., Katragkou A., Dimou V., Sarafidis K., Karampatakis T, et al. Successful management of an outbreak due to carbapenem-resistant Acinetobacter baumannii in a neonatal intensive care unit. Eur J Pediatr. 2015. 174:65–74.
18.Giuffrè M., Bonura C., Geraci DM., Saporito L., Catalano R., Di Noto S, et al. Successful control of an outbreak of colonization by Klebsiella pneumoniae carbapenemase-producing K. pneumoniae sequence type 258 in a neonatal intensive care unit, Italy. J Hosp Infect. 2013. 85:233–6.
19.Matheson A., Christie P., Stari T., Kavanagh K., Gould IM., Master-ton R, et al. Nasal swab screening for methicillin-resistant Staphylococcus aureus-how well does it perform? A cross-sectional study. Infect Control Hosp Epidemiol. 2012. 33:803–8.
20.Warren DK., Kollef MH., Seiler SM., Fridkin SK., Fraser VJ. The epidemiology of vancomycin-resistant Enterococcus colonization in a medical intensive care unit. Infect Control Hosp Epidemiol. 2003. 24:257–63.
21.Marlowe EM., Bankowski MJ. Conventional and molecular methods for the detection of methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2011. 49:S53–6.
crossref
22.Lee S., Park YJ., Park KG., Jekarl DW., Chae H., Yoo JK, et al. Comparative evaluation of three chromogenic media combined with broth enrichment and the real-time PCR-based Xpert MRSA assay for screening ofmethicillin-resistant Staphylococcus aureus in nasal swabs. Ann Lab Med. 2013. 33:255–60.
23.Buchan BW., Ledeboer NA. Identification of two borderline oxacillin-resistant strains of Staphylococcus aureus from routine nares swab specimens by one of three chromogenic agars evalua-ted for the detection of MRSA. Am J Clin Pathol. 2010. 134:921–7.
24.Yang HY., Suh JT., Lee HJ. Evaluation of commercial selective agars in screening for methicillin-resistant Staphylococcus aureus. Ann Clin Lab Sci. 2010. 40:252–6.
25.Denys GA., Renzi PB., Koch KM., Wissel CM. Three-way comparison of BBL CHROMagar MRSA II, MRSASelect, and spectra MRSA for detection of methicillin-resistant Staphylococcus aureus isolates in nasal surveillance cultures. J Clin Microbiol. 2013. 51:202–5.
26.Suwantarat N., Roberts A., Prestridge J., Seeley R., Speser S., Harmon C, et al. Comparison of five chromogenic media for recovery of vancomycin-resistant enterococci from fecal samples. J Clin Microbiol. 2014. 52:4039–42.
crossref
27.Ledeboer NA., Tibbetts RJ., Dunne WM. A new chromogenic agar medium, chromID VRE, to screen for vancomycin-resistant Enterococcus faecium and Enterococcus faecalis. Diagn Microbiol Infect Dis. 2007. 59:477–9.
28.Anderson NW., Buchan BW., Young CL., Newton DW., Brenke C., Lapsley L, et al. Multicenter clinical evaluation of VRESelect agar for identification of vancomycin-resistant Enterococcus faecalis and Enterococcus faecium. J Clin Microbiol. 2013. 51:2758–60.
29.Jenkins SG., Raskoshina L., Schuetz AN. Comparison of perfor-mance of the novel chromogenic spectra VRE agar to that of bile esculin azide and Campylobacter agars for detection of vancomy-cin-resistant enterococci in fecal samples. J Clin Microbiol. 2011. 49:3947–9.
30.Uzun B., Karataş Ş ener AG., Güngör S., Afş ar I., Yüksel Ergin O., Demirci M. Comparison of cefoxitin disk diffusion test, automated system and chromogenic medium for detection of methicillin resistance in Staphylococcus aureus isolates. Mikrobiyol Bul. 2013. 47:11–8.
31.Dalpke AH., Hofko M., Zimmermann S. Comparison of the BD Max methicillin-resistant Staphylococcus aureus (MRSA) assay and the BD GeneOhm MRSA achromopeptidase assay with direct- and enriched-culture techniques using clinical specimens for detection of MRSA. J Clin Microbiol. 2012. 50:3365–7.
crossref
32.Patel PA., Ledeboer NA., Ginocchio CC., Condon S., Bouchard S., Qin P, et al. Performance of the BD GeneOhm MRSA achromopeptidase assay for real-time PCR detection of methicillin-resistant Staphylococcus aureus in nasal specimens. J Clin Microbiol. 2011. 49:2266–8.
33.Arcenas RC., Spadoni S., Mohammad A., Kiechle FL., Walker K., Fader RC, et al. Multicenter evaluation of the LightCycler MRSA advanced test, the Xpert MRSA Assay, and MRSASelect directly plated culture with simulated workflow comparison for the detection of methicillin-resistant Staphylococcus aureus in nasal swabs. J Mol Diagn. 2012. 14:367–75.
34.Diederen BM. Comparison of the Cepheid Xpert TM MRSA assay with culture in a low prevalence setting in The Netherlands. J Infect. 2010. 61:509–10.
35.Patel PA., Schora DM., Peterson KE., Grayes A., Boehm S., Peterson LR. Performance of the Cepheid XpertⓇ SA Nasal Complete PCR assay compared to culture for detection of methicillin-sensitive and methicillin-resistant Staphylococcus aureus colonization. Diagn Microbiol Infect Dis. 2014. 80:32–4.
36.Kim MH., Lee WI., Kang SY. Detection of methicillin-resistant Staphylococcus aureus in healthcare workers using real-time poly-merase chain reaction. Yonsei Med J. 2013. 54:1282–4.
37.Tacconelli E., De Angelis G., de Waure C., Cataldo MA., La Torre G., Cauda R. Rapid screening tests for meticillin-resistant Staphylococcus aureus at hospital admission: systematic review and meta-analysis. Lancet Infect Dis. 2009. 9:546–54.
38.Yam WC., Siu GK., Ho PL., Ng TK., Que TL., Yip KT, et al. Evaluation of the LightCycler methicillin-resistant Staphylococcus aureus (MRSA) advanced test for detection of MRSA nasal colonization. J Clin Microbiol. 2013. 51:2869–74.
39.Polisena J., Chen S., Cimon K., McGill S., Forward K., Gardam M. Clinical effectiveness of rapid tests for methicillin resistant Staphylococcus aureus (MRSA) in hospitalized patients: a systematic review. BMC Infect Dis. 2011. 11:336.
crossref
40.Roisin S., Laurent C., Denis O., Dramaix M., Nonhoff C., Hallin M, et al. Impact of rapid molecular screening at hospital admission on nosocomial transmission of methicillin-resistant Staphylococcus aureus: cluster randomised trial. PLoS One. 2014. 9:e96310.
41.Malhotra-Kumar S., Haccuria K., Michiels M., Ieven M., Poyart C., Hryniewicz W, et al. MOSAR WP2 Study Team. Current trends in rapid diagnostics for methicillin-resistant Staphylococcus aureus and glycopeptide-resistant Enterococcus species. J Clin Microbiol. 2008. 46:1577–87.
42.Lee SY., Park KG., Lee GD., Park JJ., Park YJ. Comparison of Seeplex VRE detection kit with ChromID VRE agar for detection of vancomycin-resistant enterococci in rectal swab specimens. Ann Clin Lab Sci. 2010. 40:163–6.
43.Kim DH., Lee JH., Ha JS., Ryoo NH., Jeon DS., Kim JR. Evaluation of the usefulness of selective chromogenic agar medium (chromID VRE) and multiplex PCR method for the detection of vancomycin- resistant enterococci. Korean J Lab Med. 2010. 30:631–6.
44.Werner G., Serr A., Schütt S., Schneider C., Klare I., Witte W, et al. Comparison of direct cultivation on a selective solid medium, polymerase chain reaction from an enrichment broth, and the BD GeneOhm TM VanR Assay for identification of vancomycin-resistant enterococci in screening specimens. Diagn Microbiol Infect Dis. 2011. 70:512–21.
45.Usacheva EA., Ginocchio CC., Morgan M., Maglanoc G., Mehta MS., Tremblay S, et al. Prospective, multicenter evaluation of the BD GeneOhm VanR assay for direct, rapid detection of van-comycin-resistant Enterococcus species in perianal and rectal specimens. Am J Clin Pathol. 2010. 134:219–26.
46.Gazin M., Lammens C., Goossens H., Malhotra-Kumar S. MOSAR WP2 Study Team. Evaluation of GeneOhm VanR and Xpert vanA/vanB molecular assays for the rapid detection of vancomy-cin-resistant enterococci. Eur J Clin Microbiol Infect Dis. 2012. 31:273–6.
crossref
47.Sloan LM., Uhl JR., Vetter EA., Schleck CD., Harmsen WS., Manahan J, et al. Comparison of the Roche LightCycler vanA/vanB detection assay and culture for detection of vancomycin- resistant enterococci from perianal swabs. J Clin Microbiol. 2004. 42:2636–43.
48.Bourdon N., Bérenger R., Lepoultier R., Mouet A., Lesteven C., Borgey F, et al. Rapid detection of vancomycin-resistant entero-cocci from rectal swabs by the Cepheid Xpert vanA/vanB assay. Diagn Microbiol Infect Dis. 2010. 67:291–3.
crossref
49.The Korean Society of Clinical Microbiology. Guideline of diagnostic method of CPE. http://kscm.or.kr/xe/kscmnotice/71241. [Online] (last visited on 16 September 2015).
50.Wilkinson KM., Winstanley TG., Lanyon C., Cummings SP., Raza MW., Perry JD. Comparison of four chromogenic culture media for carbapenemase-producing Enterobacteriaceae. J Clin Microbiol. 2012. 50:3102–4.
51.Dortet L., Poirel L., Nordmann P. Rapid identification of carbape-nemase types in Enterobacteriaceae and Pseudomonas spp. by using a biochemical test. Antimicrob Agents Chemother. 2012. 56:6437–40.
52.Dortet L., Poirel L., Errera C., Nordmann P. CarbAcineto NP test for rapid detection of carbapenemase-producing Acinetobacter spp. J Clin Microbiol. 2014. 52:2359–64.
53.Bush K. Alarming β -lactamase-mediated resistance in multidrug- resistant Enterobacteriaceae. Curr Opin Microbiol. 2010. 13:558–64.
54.Szabó D., Silveira F., Hujer AM., Bonomo RA., Hujer KM., Marsh JW, et al. Outer membrane protein changes and efflux pump ex-pression together may confer resistance to ertapenem in Enterobacter cloacae. Antimicrob Agents Chemother. 2006. 50:2833–5.
55.Yang FC., Yan JJ., Hung KH., Wu JJ. Characterization of erta-penem-resistant Enterobacter cloacae in a Taiwanese university hospital. J Clin Microbiol. 2012. 50:223–6.
56.Lee Y., Choi H., Yum JH., Kang G., Bae IK., Jeong SH, et al. Molecular mechanisms of carbapenem resistance in Enterobacter cloacae clinical isolates from Korea and clinical outcome. Ann Clin Lab Sci. 2012. 42:281–6.
57.Naas T., Cuzon G., Bogaerts P., Glupczynski Y., Nordmann P. Evaluation of a DNA microarray (Check-MDR CT102) for rapid detection of TEM, SHV, and CTX-M extended-spectrum β - lactamases and of KPC, OXA-48, VIM, IMP, and NDM-1 carbapenemases. J Clin Microbiol. 2011. 49:1608–13.
58.Nijhuis R., Samuelsen O., Savelkoul P., van Zwet A. Evaluation of a new real-time PCR assay (Check-Direct CPE) for rapid detection of KPC, OXA-48, VIM, and NDM carbapenemases using spiked rectal swabs. Diagn Microbiol Infect Dis. 2013. 77:316–20.
crossref
59.Tenover FC., Canton R., Kop J., Chan R., Ryan J., Weir F, et al. Detection of colonization by carbapenemase-producing Gram- negative bacilli in patients by use of the Xpert MDRO assay. J Clin Microbiol. 2013. 51:3780–7.

Table 1.
Antimicrobial susceptibility of clinically important Gram-negative bacteria from intensive care units in Korea, United States and Europe
Antimicrobial agents E. coli Klebsiella spp.* P. aeruginosa Acinetobacter spp.
Region K U E K U E K U E K U E
Susceptibility R% NS% NS% R% NS% NS% R% NS% NS% R% NS% NS%
3 rd Cephalosporin 38 12 17 45 13 37 26 24 25 86 61 -
Carbapenem - - - - 4 10 32 30 31 83 56 62
Fluoroquinolone 52 39 28 39 15 38 38 27 28 87 63 68
Gentamicin 37 13 15 24 8 21 27 - - 84 - -

Klebsiella spp. in Korea was K. pneuumoniae.

Abbreviations: K, Korea; U, United States; E, Europe (Belgium, France, Germany, Ireland, Italy, Portugal, Spain, Sweden, and United Kingdom); R%, resistance rate; NS%, non-susceptibility rate; Susceptibiity data modified from KONSAR surveillance [10] and from SENTRY surveillance [14]; -, no reported data.

Table 2.
Performance of chromogenic media for detection of methicillin-resistant S. aureus and vancomycin-resistant enterococcus
Media % Sensitivity % Specificity % PPV % NPV Reference
ChromID MRSA 95.6 (24 hr) 95.8 (24 hr) 82.3 (24 hr) 99.1 (24 hr) 22
 (bioMérieux) 100 (48 hr) 92.5 (48 hr) 73.1 (48 hr) 100 (48 hr)  
  58 (18 hr) 100 (18 hr) 100 (18 hr) 93.7 (18 hr) 23
  88 (24 hr) 99.7 (24 hr) 97.8 (24 hr) 98.1 (24 hr)  
  96 (48 hr) 98.7 (48 hr) 92.3 (48 hr) 99.4 (48 hr)  
  80.8 (18 hr) 98.7 (18 hr) 93 (18 hr) 96.1 (18 hr) 24
  90.9 (24 hr) 98.1 (24 hr) 90.9 (24 hr) 98.1 (24 hr)  
  99 (48 hr) 97.9 (48 hr) 90.7 (48 hr) 99.8 (48 hr)  
CHROMagar MRSA II 87.7 98.6 91.4 98 25
 (BD Diagnostics) 84.8 (18 hr) 99.8 (18 hr) 98.8 (18 hr) 97 (18 hr) 24
  91.9 (24 hr) 99.5 (24 hr) 97.9 (24 hr) 98.4 (24 hr)  
  99 (48 hr) 99 (48 hr) 95.2 (48 hr) 99.8 (48 hr)  
MRSASelect 89 93.4 69.1 98.1 25
(Bio-Rad Laboratories) 86 (18 hr) 100 (18 hr) 100 (18 hr) 97.8 (18 hr) 23
  96 (24 hr) 100 (24 hr) 100 (24 hr) 99.4 (24 hr)  
  96 (48 hr) 82.5 (48 hr) 46.6 (48 hr) 99.2 (48 hr)  
  87.9 (18 hr) 99 (18 hr) 94.6 (18 hr) 97.5 (18 hr) 24
  94.9 (24 hr) 98.5 (24 hr) 93.1 (24 hr) 99 (24 hr)  
  100 (48 hr) 97.7 (48 hr) 90 (48 hr) 100 (48 hr)  
Spectra MRSA 83.6 92.1 63.5 97.1 25
 (Remel) 82 (18 hr) 100 (18 hr) 100 (18 hr) 97.2 (18 hr) 23
  96 (24 hr) 99.7 (24 hr) 98 (24 hr) 99.4 (24 hr)  
  100 (48 hr) 80.3 (48 hr) 44.6 (48 hr) 100 (48 hr)  
ChromID VRE 94.9 99.7 98.9 98.3 26
 (bioMérieux) 86.3 (24 hr) 100 (24 hr) 100 (24 hr) 90.8 (24 hr) 27
  88.2 (48 hr) 98.6 (48 hr) 97.8 (48 hr) 90.7 (48 hr)  
VRESelect 91.9 99.7 98.9 97.4 26
 (Bio-Rad Laboratories) 98.7 99 96.9 99.6 28
Spectra VRE 93.9 99.7 98.9 98 26
 (Remel) 98.3 (24 hr) 95.2 (24 hr) 93.4 (24 hr) 98.8 (24 hr) 29
  100 (48 hr) 95.2 (48 hr) 93.5 (48 hr) 100 (48 hr)  

Abbreviations: PPV, positive predictive value; NPV, negative predictive value.

Table 3.
Performance of molecular methods for detection of methicillin-resistant S. aureus and vancomycin-resistant enterococcus
Diagnostics Comparators % Sensitivity % Specificity % PPV % NPV Reference
GeneOhm MRSA ACP Culture 93.8 98.3 69.8 99.7 31
 (BD Diagnostics) Culture 92 94.6 75.4 98.5 32
Xpert MRSA Culture 92.6 96.7 85.1 98.5 22
 (Cepheid) Culture 99 95.5     33
  Culture 91.6 97 54.3 99.7 34
  Culture 92.6 96.7 85.1 98.5 22
Xpert SA Nasal Culture 91.8 97.6 94.6 96.3 35
 Complete (Cepheid)            
LightCycler MRSA Culture 95.2 95.5     33
 (Roche Diagnostics) Culture 100 90.1 45.8 100 36
GeneOhm VanR Culture 93.1 87 43.4 99.1 44
 (BD Diagnostics) Culture 93.2 81.9 54.4 98.1 45
  VRE culture isolates 40 (vanA) 93.3 (vanA) 80 (vanA) 70 (vanA) 46
  (van +) 100 (vanB) 14.9 (vanB) 7 (vanB) 100 (vanB)  
  Direct van PCR 43.5 (vanA) 100 (vanA) 100 (vanA) 67.5 (vanA) 46
  in stool 100 (vanB) 20.6 (vanB) 37.2 (vanB) 100 (vanB)  
LightCycler vanA/ vanB Culture (V-MIC 6) 100 97 42 100 47
 (Roche Diagnostics) Culture (V-MIC 8) 100 95 32 100 47
Xpert vanA/ vanB assay Culture 100 85.4 8.7 100 48
 (Cepheid) VRE culture isolates 70 (vanA) 83.3 (vanA) 73.7 (vanA) 80.6 (vanA) 46
  (van +) 66.7 (vanB) 12.8 (vanB) 4.7 (vanB) 85.7 (vanB)  
  Direct van PCR 73.9 (vanA) 92.6 (vanA) 89.5 (vanA) 80.6 (vanA) 46
  in stool 87.5 (vanB) 14.7 (vanB) 32.6 (vanB) 71.4 (vanB)  

Abbreviations: PPV, positive-predictive value; NPV, negative-predictive value; V-MIC, vancomycin minimal inhibitory concentration (μ g/mL).

TOOLS
Similar articles