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Predicting Multidrug-Resistant Gram-Negative Bacterial Colonization and Associated Infection on Hospital Admission

  • Wen-Pin Tseng (a1), Yee-Chun Chen (a2) (a3), Bey-Jing Yang (a4), Shang-Yu Chen (a1), Jr-Jiun Lin (a1), Ya-Huei Huang (a3) (a4), Chia-Ming Fu (a1), Shan-Chwen Chang (a2) and Shey-Ying Chen (a1) (a5)...



Isolation of multidrug-resistant gram-negative bacteria (MDR-GNB) from patients in the community has been increasingly observed. A prediction model for MDR-GNB colonization and infection risk stratification on hospital admission is needed to improve patient care.


A 2-stage, prospective study was performed with 995 and 998 emergency department patients enrolled, respectively. MDR-GNB colonization was defined as isolates resistant to 3 or more classes of antibiotics, identified in either the surveillance or early (≤48 hours) clinical cultures.


A score-assigned MDR-GNB colonization prediction model was developed and validated using clinical and microbiological data from 995 patients enrolled in the first stage of the study; 122 of these patients (12.3%) were MDR-GNB colonized. We identified 5 independent predictors: age>70 years (odds ratio [OR], 1.84 [95% confidence interval (CI), 1.06–3.17]; 1 point), assigned point value in the model), residence in a long-term-care facility (OR, 3.64 [95% CI, 1.57–8.43); 3 points), history of cerebrovascular accidents (OR, 2.23 [95% CI, 1.24–4.01]; 2 points), hospitalization within 1 month (OR, 2.63 [95% CI, 1.39–4.96]; 2 points), and recent antibiotic exposure (OR, 2.18 [95% CI, 1.16–4.11]; 2 points). The model displayed good discrimination in the derivation and validation sets (area under ROC curve, 0.75 and 0.80, respectively) with the best cutoffs of<4 and ≥4 points for low- and high-risk MDR-GNB colonization, respectively. When applied to 998 patients in the second stage of the study, the model successfully stratified the risk of MDR-GNB infection during hospitalization between low- and high-risk groups (probability, 0.02 vs 0.12, respectively; log-rank test, P<.001).


A model was developed to optimize both the decision to initiate antimicrobial therapy and the infection control interventions to mitigate threats from MDR-GNB.

Infect Control Hosp Epidemiol 2017;38:1216–1225


Corresponding author

Address correspondence to Shey-Ying Chen, MD, Department of Emergency Medicine, National Taiwan University Hospital, College of Medicine, National Taiwan University. No. 7, Zhongshan S Rd, Zhongzheng District, Taipei City 100, Taiwan (


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PREVIOUS PRESENTATION: This study was presented in part at the 51st Interscience Conference on Antimicrobial Agents and Chemotherapy, Chicago, Illinois, on September 19, 2011, and at the 7th Asian Conference on Emergency Medicine in Tokyo, Japan, on October 24, 2013.



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1. Pop-Vicas, AE, D’Agata, EMC. The rising influx of multidrug-resistant gram-negative bacilli into a tertiary care hospital. Clin Infect Dis 2005;40:17921798.
2. Arias, CA, Murray, BE. Antibiotic-resistant bugs in the 21st century—a clinical super-challenge. N Engl J Med 2009;360:439443.
3. Pitout, JD, Nordmann, P, Laupland, KB, Poirel, L. Emergence of Enterobacteriaceae producing extended-spectrum beta-lactamases (ESBLs) in the community. J Antimicrob Chemother 2005;56:5259.
4. Ben-Ami, R, Rodríguez-Baño, J, Arslan, H, et al. A multinational survey of risk factors for infection with extended-spectrum beta-lactamase-producing enterobacteriaceae in nonhospitalized patients. Clin Infect Dis 2009;49:682690.
5. Cosgrove, SE. The relationship between antimicrobial resistance and patient outcomes: mortality, length of hospital stay, and health care costs. Clin Infect Dis 2006;42(Suppl 2):S82S89.
6. Evans, HL, Lefrak, SN, Lyman, J, et al. Cost of gram-negative resistance. Crit Care Med 2007;35:8995.
7. Roberts, RR, Hota, B, Ahmad, I, et al. Hospital and societal costs of antimicrobial-resistant infections in a Chicago teaching hospital: implications for antibiotic stewardship. Clin Infect Dis 2009;49:11751184.
8. Schwaber, MJ, Carmeli, Y. Mortality and delay in effective therapy associated with extended-spectrum beta-lactamase production in Enterobacteriaceae bacteraemia: a systematic review and meta-analysis. J Antimicrob Chemother 2007;60:913920.
9. Vallés, J, Rello, J, Ochagavía, A, Garnacho, J, Alcalá, MA. Community-acquired bloodstream infection in critically ill adult patients: impact of shock and inappropriate antibiotic therapy on survival. Chest 2003;123:16151624.
10. Mammina, C, Di Carlo, P, Cipolla, D, et al. Surveillance of multidrug-resistant gram-negative bacilli in a neonatal intensive care unit: prominent role of cross transmission. Am J Infect Control 2007;35:222230.
11. Giuffrè, M, Geraci, DM, Bonura, C, et al. The increasing challenge of multidrug-resistant gram-negative bacilli: results of a 5-year active surveillance program in a neonatal intensive care unit. Medicine (Baltimore) 2016;95:e3016.
12. Reddy, P, Malczynski, M, Obias, A, et al. Screening for extended-spectrum beta-lactamase-producing Enterobacteriaceae among high-risk patients and rates of subsequent bacteremia. Clin Infect Dis 2007;45:846852.
13. Otter, JA, Mutters, NT, Tacconelli, E, Gikas, A, Holmes, AH, et al. Controversies in guidelines for the control of multidrug-resistant gram-negative bacteria in EU countries. Clin Microbiol Infect 2015;21:10571066.
14. Tumbarello, M, Trecarichi, EM, Bassetti, M, et al. Identifying patients harboring extended-spectrum-beta-lactamase-producing Enterobacteriaceae on hospital admission: derivation and validation of a scoring system. Antimicrob Agents Chemother 2011;55:34853490.
15. Johnson, SW, Anderson, DJ, May, DB, Drew, RH. Utility of a clinical risk factor scoring model in predicting infection with extended-spectrum β-lactamase-producing enterobacteriaceae on hospital admission. Infect Control Hosp Epidemiol 2013;34:385392.
16. Augustine, MR, Testerman, TL, Justo, JA, et al. Clinical risk score for prediction of extended-spectrum β-lactamase-producing Enterobacteriaceae in bloodstream Isolates. Infect Control Hosp Epidemiol 2017;38:266272.
17. Kengkla, K, Charoensuk, N, Chaichana, M, et al. Clinical risk scoring system for predicting extended-spectrum β-lactamase-producing Escherichia coli infection in hospitalized patients. J Hosp Infect 2016;93:4956.
18. Tacconelli, E, Cataldo, MA, De Pascale, G, et al. Prediction models to identify hospitalized patients at risk of being colonized or infected with multidrug-resistant Acinetobacter baumannii calcoaceticus complex. J Antimicrob Chemother 2008;62:11301137.
19. Ruppé, E, Pitsch, A, Tubach, F, et al. Clinical predictive values of extended-spectrum beta-lactamase carriage in patients admitted to medical wards. Eur J Clin Microbiol Infect Dis 2012;31:319325.
20. Platteel, TN, Leverstein-van Hall, MA, Cohen Stuart, JW, et al. Predicting carriage with extended-spectrum beta-lactamase-producing bacteria at hospital admission: a cross-sectional study. Clin Microbiol Infect 2015;21:141146.
21. Vasudevan, A, Mukhopadhyay, A, Li, J, Yuen, EG, Tambyah, PA. A prediction tool for nosocomial multi-drug resistant gram-negative bacilli infections in critically ill patients—prospective observational study. BMC Infect Dis 2014;14:615.
22. Snyder, GM, D’Agata, EM. Diagnostic accuracy of surveillance cultures to detect gastrointestinal colonization with multidrug-resistant gram-negative bacteria. Am J Infect Control 2012;40:474476.
23. Siegel, JD, Rhinehart, E, Jackson, M, Chiarello, L. Management of multidrug-resistant organisms in health care settings, 2006. Am J Infect Control 2007;35(Suppl 2):165193.
24. McNeil, BJ, Hanley, JA. Statistical approaches to the analysis of receiver operating characteristic (ROC) curves. Med Decis Making 1984;4:137150.
25. Laupacis, A, Sekar, N, Stiell, IG. Clinical prediction rules. A review and suggested modifications of methodological standards. JAMA 1997;277:488494.
26. Diagnosis. In Fletcher, RH, Fletcher, SW, Wagner, EG, eds. Clinical Epidemiology: the Essentials. 3rd ed. Philadelphia: Lippincott Williams & Wilkins; 1996:4850.
27. Falagas, ME, Karageorgopoulos, ED. Extended-spectrum beta-lactamase-producing organisms. J Hosp Infect 2009;73:345354.
28. Friedmann, R., Raveh, D, Zartzer, E, et al. Prospective evaluation of colonization with extended-spectrum beta-lactamase (ESBL)-producing enterobacteriaceae among patients at hospital admission and of subsequent colonization with ESBL-producing enterobacteriaceae among patients during hospitalization. Infect Control Hosp Epidemiol 2009;30:534542.
29. Hawser, SP, Bouchillon, SK, Hoban, DJ, Badal, RE, Cantón, R, Baquero, F. Incidence and antimicrobial susceptibility of Escherichia coli and Klebsiella pneumoniae with extended-spectrum beta-lactamases in community- and hospital-associated intra-abdominal infections in Europe: results of the 2008 Study for Monitoring Antimicrobial Resistance Trends (SMART). Antimicrob Agents Chemother 2010;54:30433046.
30. Sands, KE, Bates, DW, Lanken, PN, et al. Epidemiology of sepsis syndrome in 8 academic medical centers. JAMA 1997;278:234240.
31. Lautenbach, E, Patel, JB, Bilker, WB, Edelstein, PH, Fishman, NO. Extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae: risk factors for infection and impact of resistance on outcomes. Clin Infect Dis 2001;32:11621171.
32. Tacconelli, E. Screening and isolation for infection control. J Hosp Infect 2009;73:371377.
33. Wassenberg, MW, Kluytmans, JA, Bosboom, RW, et al. Rapid diagnostic testing of methicillin-resistant Staphylococcus aureus carriage at different anatomical sites: costs and benefits of less extensive screening regimens. Clin Microbiol Infect 2011;17:17041710.
34. Murthy, A, De Angelis, G, Pittet, D, Schrenzel, J, Uckay, I, Harbarth, S. Cost-effectiveness of universal MRSA screening on admission to surgery. Clin Microbiol Infect 2010;16:17471753.
35. O’Fallon, E, Gautam, S, D’Agata, EM. Colonization with multidrug-resistant gram-negative bacteria: prolonged duration and frequent cocolonization. Clin Infect Dis 2009;48:13751381.
36. Villar, HE, Baserni, MN, Jugo, MB. Faecal carriage of ESBL-producing Enterobacteriaceae and carbapenem-resistant gram-negative bacilli in community settings. J Infect Dev Ctries 2013;7:630634.
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