Skip to main content Accessibility help

Readmissions With Multidrug-Resistant Infection in Patients With Prior Multidrug Resistant Infection

  • Jason P. Burnham (a1), Jennie H. Kwon (a1), Margaret A. Olsen (a1), Hilary M. Babcock (a1) and Marin H. Kollef (a2)...



To determine incidence of and risk factors for readmissions with multidrug-resistant organism (MDRO) infections among patients with previous MDRO infection.


Retrospective cohort of patients admitted between January 1, 2006, and October 1, 2015.


Barnes-Jewish Hospital, a 1,250-bed academic tertiary referral center in St Louis, Missouri.


We identified patients with MDROs obtained from the bloodstream, bronchoalveolar lavage (BAL)/bronchial wash, or other sterile sites. Centers for Disease Control and prevention (CDC) and European CDC definitions of MDROs were utilized. All readmissions ≤1 year from discharge from the index MDRO hospitalization were evaluated for bloodstream, BAL/bronchial wash, or other sterile site cultures positive for the same or different MDROs.


In total, 4,429 unique patients had a positive culture for an MDRO; 3,453 of these (78.0%) survived the index hospitalization. Moreover, 2,127 patients (61.6%) were readmitted ≥1 time within a year, for a total of 5,849 readmissions. Furthermore, 512 patients (24.1%) had the same or a different MDRO isolated from blood, BAL/bronchial wash, or another sterile site during a readmission. Bone marrow transplant, end-stage renal disease, lymphoma, methicillin-resistant Staphylococcus aureus, or carbapenem-resistant Pseudomonas aeruginosa during index hospitalization were factors associated with increased risk of having an MDRO isolated during a readmission. MDROs isolated during readmissions were in the same class of MDRO as the index hospitalization 9%–78% of the time, with variation by index pathogen.


Readmissions among patients with MDRO infections are frequent. Various patient and organism factors predispose to readmission. When readmitted patients had an MDRO, it was often a pathogen in the same class as that isolated during the index admission, with the exception of Acinetobacter (~9%).

Infect Control Hosp Epidemiol 2018;39:12–19


Corresponding author

Address correspondence to Jason P. Burnham, MD, Division of Infectious Diseases, Washington University School of Medicine, 4523 Clayton Avenue, Campus Box 8051, St Louis, MO 63110 ( or to Marin H. Kollef, MD, Division of Pulmonary and Critical Care Medicine, Washington University School of Medicine, 4523 Clayton Avenue, Campus Box 8052, St Louis, MO 63110 (


Hide All

PREVIOUS PRESENTATION: Portions of this manuscript were presented in a preliminary form at the SHEA Spring 2017 conference on March 31, 2017, in St Louis, Missouri.



Hide All
1. Pearson, S, Stewart, S, Rubenach, S. Is health-related quality of life among older, chronically ill patients associated with unplanned readmission to hospital? Aust N Z J Med 1999;29:701706.
2. Rodriguez-Artalejo, F, Guallar-Castillon, P, Pascual, CR, et al. Health-related quality of life as a predictor of hospital readmission and death among patients with heart failure. Arch Intern Med 2005;165:12741279.
3. Hu, Y, McMurry, TL, Stukenborg, GJ, Kozower, BD. Readmission predicts 90-day mortality after esophagectomy: analysis of Surveillance, Epidemiology, and End Results Registry linked to Medicare outcomes. J Thorac Cardiovasc Surg 2015;150:12541260.
4. Hicks, CW, Tosoian, JJ, Craig-Schapiro, R, et al. Early hospital readmission for gastrointestinal-related complications predicts long-term mortality after pancreatectomy. Am J Surg 2015;210:636642.
5. Gohil, SK, Datta, R, Cao, C, et al. Impact of hospital population case-mix, including poverty, on hospital all-cause and infection-related 30-day readmission rates. Clin Infect Dis 2015;61:12351243.
6. Prescott, HC, Langa, KM, Iwashyna, TJ. Readmission diagnoses after hospitalization for severe sepsis and other acute medical conditions. JAMA 2015;313:10551057.
7. Sun, A, Netzer, G, Small, DS, et al. Association between index hospitalization and hospital readmission in sepsis survivors. Crit Care Med 2016;44:478487.
8. Prescott, HC, Langa, KM, Liu, V, Escobar, GJ, Iwashyna, TJ. Increased 1-year healthcare use in survivors of severe sepsis. Am J Respir Crit Care Med 2014;190:6269.
9. Liu, V, Lei, X, Prescott, HC, Kipnis, P, Iwashyna, TJ, Escobar, GJ. Hospital readmission and healthcare utilization following sepsis in community settings. J Hosp Med 2014;9:502507.
10. Ortego, A, Gaieski, DF, Fuchs, BD, et al. Hospital-based acute care use in survivors of septic shock. Crit Care Med 2015;43:729737.
11. Wang, T, Derhovanessian, A, De Cruz, S, Belperio, JA, Deng, JC, Hoo, GS. Subsequent infections in survivors of sepsis: epidemiology and outcomes. J Intensive Care Med 2014;29:8795.
12. Donnelly, JP, Hohmann, SF, Wang, HE. Unplanned readmissions after hospitalization for severe sepsis at academic medical center-affiliated hospitals. Crit Care Med 2015;43:19161927.
13. Goodwin, AJ, Rice, DA, Simpson, KN, Ford, DW. Frequency, cost, and risk factors of readmissions among severe sepsis survivors. Crit Care Med 2015;43:738746.
14. Jones, TK, Fuchs, BD, Small, DS, et al. Post-acute care use and hospital readmission after sepsis. Ann Am Thorac Soc 2015;12:904913.
15. Chang, DW, Tseng, CH, Shapiro, MF. Rehospitalizations following sepsis: common and costly. Crit Care Med 2015;43:20852093.
16. Mayr, FB, Talisa, VB, Balakumar, V, Chang, CH, Fine, M, Yende, S. Proportion and cost of unplanned 30-day readmissions after sepsis compared with other medical conditions. JAMA 2017;317:530531.
17. Nathwani, D, Raman, G, Sulham, K, Gavaghan, M, Menon, V. Clinical and economic consequences of hospital-acquired resistant and multidrug-resistant Pseudomonas aeruginosa infections: a systematic review and meta-analysis. Antimicrob Resist Infect Control 2014;3:32.
18. Andruska, A, Micek, ST, Shindo, Y, et al. Pneumonia pathogen characterization Is an independent determinant of hospital readmission. Chest 2015;148:103111.
19. Datta, R, Brown, S, Nguyen, VQ, et al. Quantifying the exposure to antibiotic-resistant pathogens among patients discharged from a single hospital across all California healthcare facilities. Infect Control Hosp Epidemiol 2015;36:12751282.
20. Emerson, CB, Eyzaguirre, LM, Albrecht, JS, Comer, AC, Harris, AD, Furuno, JP. Healthcare-associated infection and hospital readmission. Infect Control Hosp Epidemiol 2012;33:539544.
21. Micek, ST, Heard, KM, Gowan, M, Kollef, MH. Identifying critically ill patients at risk for inappropriate antibiotic therapy: a pilot study of a point-of-care decision support alert. Crit Care Med 2014;42:18321838.
22. Neuner, EA, Yeh, JY, Hall, GS, et al. Treatment and outcomes in carbapenem-resistant Klebsiella pneumoniae bloodstream infections. Diagn Microbiol Infect Dis 2011;69:357362.
23. Quezada Joaquin, NM, Diekema, DJ, Perencevich, EN, Bailey, G, Winokur, PL, Schweizer, ML. Long-term risk for readmission, methicillin-resistant Staphylococcus aureus (MRSA) infection, and death among MRSA-colonized veterans. Antimicrob Agents Chemother 2013;57:11691172.
24. Chopra, T, Neelakanta, A, Dombecki, C, et al. Burden of Clostridium difficile infection on hospital readmissions and its potential impact under the Hospital Readmission Reduction Program. Am J Infect Control 2015;43:314317.
25. Duggal, A, Barsoum, W, Schmitt, SK. Patients with prosthetic joint infection on IV antibiotics are at high risk for readmission. Clin Orthop Relat Res 2009;467:17271731.
26. Unusual Susceptibility Profiles Alert. Centers for Disease Control and Prevention website. Accessed July 19, 2016.
27. Multidrug-Resistant Organism and Clostridium difficile Infection (MDRO/CDI) Module. Centers for Disease Control and Prevention website. 12pscMDRO_CDA Dcurrent.pdf. Published 2016. Accessed July 19, 2016.
28. Magiorakos, AP, Srinivasan, A, Carey, RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268281.
29. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement. CLSI document M100-S25. Vol. 25. Wayne, PA: CLSI; 2015.
30. Messina, JA, Cober, E, Richter, SS, et al. Hospital readmissions in patients with Carbapenem-resistant Klebsiella pneumoniae . Infect Control Hosp Epidemiol 2016;37:281288.
31. Allison, GM, Muldoon, EG, Kent, DM, et al. Prediction model for 30-day hospital readmissions among patients discharged receiving outpatient parenteral antibiotic therapy. Clin Infect Dis 2014;58:812819.
32. Yaw, LK, Robinson, JO, Ho, KM. A comparison of long-term outcomes after meticillin-resistant and meticillin-sensitive Staphylococcus aureus bacteraemia: an observational cohort study. Lancet Infect Dis 2014;14:967975.
33. Safdar, N, Maki, DG. The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant Staphylococcus aureus, enterococcus, gram-negative bacilli, Clostridium difficile, and Candida . Ann Intern Med 2002;136:834844.
34. Butler, AM, Olsen, MA, Merz, LR, et al. Attributable costs of enterococcal bloodstream infections in a nonsurgical hospital cohort. Infect Control Hosp Epidemiol 2010;31:2835.
35. Palacios-Baena, ZR, Gutierrez-Gutierrez, B, De Cueto, M, et al. Development and validation of the INCREMENT-ESBL predictive score for mortality in patients with bloodstream infections due to extended-spectrum-beta-lactamase-producing Enterobacteriaceae. J Antimicrob Chemother 2017;72:906913.
Type Description Title
Supplementary materials

Burnham et al. supplementary material
Figure S1

 Unknown (615 KB)
615 KB
Supplementary materials

Burnham et al. supplementary material
Tables S1-S6

 Word (65 KB)
65 KB


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed