Notes from the Field: Large Cluster of Verona Integron-Encoded Metallo-Beta-Lactamase–Producing Carbapenem-Resistant Pseudomonas aeruginosa Isolates Colonizing Residents at a Skilled Nursing Facility — Chicago, Illinois, November 2016–March 2018

Whitney J. Clegg, MD1; Massimo Pacilli, MS, MPH1; Sarah K. Kemble, MD1; Janna L. Kerins, VMD1,2; Ahmed Hassaballa, MBBCH1; Alexander J. Kallen, MD3; Maroya S. Walters, PhD3; Alison Laufer Halpin, PhD3; Richard A. Stanton, PhD3; Sandra Boyd3; Paige Gable3; Jonathan Daniels, MS3; Michael Y. Lin, MD4; Mary K. Hayden, MD4; Karen Lolans4; Deb P. Burdsall, PhD5; Mary Alice Lavin, MJ5; Stephanie R. Black, MD1 (View author affiliations)

View suggested citation
Article Metrics
Related Materials

On November 1, 2016, a point prevalence survey conducted at a Chicago skilled nursing facility with ventilated residents (vSNF A) to understand the prevalence of carbapenemase-producing organisms in health care facilities in the Chicago region identified 20 patients with Verona integron-encoded metallo-beta-lactamase–producing carbapenem-resistant Pseudomonas aeruginosa (VIM-CRPA) colonization. To determine the extent of VIM-CRPA colonization at vSNF A and provide infection control recommendations, the Chicago Department of Public Health conducted an investigation.

The first VIM-CRPA outbreak reported in the United States occurred in a Chicago acute care hospital in 2003 (1). Other outbreaks have been described; however, none was associated with a single skilled nursing facility (25). Carbapenemase-producing CRPA are uncommon in the United States; a surveillance pilot for CRPA at five U.S. sites identified only two carbapenemase-producing CRPA among 129 isolates tested (CDC, unpublished data, 2017).

To determine whether ongoing transmission was occurring at vSNF A, the Chicago Department of Public Health conducted 10 additional point prevalence surveys during November 2016–March 2018. Rectal specimens were collected from all residents, and tracheostomy site specimens were collected from residents with tracheostomies. vSNF A is a licensed 312-bed facility; point prevalence surveys were conducted on a floor with standard skilled nursing (SN floor) and on a floor housing residents with a tracheostomy or who were mechanically ventilated (VT floor).

During November 2016–March 2018, collection of 903 screening swabs from 209 residents identified 38 residents with VIM-CRPA colonization. One additional colonized resident was identified by a rectal screening culture collected on admission to an acute care hospital. Among the 39 residents, four (10%) resided on the SN floor and 35 (90%) on the VT floor. Thirty (77%) had positive rectal swabs, four (10%) had positive tracheostomy swabs, and five (13%) had positive swabs from both sites.

Floor prevalence was calculated by dividing the number of VIM-CRPA–positive residents present on the day of the point prevalence survey by the total number of residents present. Prevalences ranged from 0% to 6% on the SN floor and 21% to 43% on the VT floor during November 2016–March 2018 (Table). Among the 18 additional residents with VIM-CRPA identified after the November 2016 point prevalence survey, 17 (94%) previously had screened negative at vSNF A, representing probable incident transmission events (Table). No additional residents with VIM-CRPA were identified during the last two consecutive point prevalence surveys on the SN floor and the last four on VT floors.

During November 2016–July 2017, point prevalence surveys were conducted at six other vSNFs and six long-term acute care hospitals in the Chicago region. Twelve additional VIM-CRPA positive patients were identified at five vSNFs and one long-term acute care hospital; facility prevalences ranged from 1% to 4%.

Whole genome sequencing performed on 26 isolates from five different facilities, including 19 from vSNF A, and two historical isolates from 2003 found that all contained the VIM-2 allelic variant, and 25 were multilocus sequence type (ST) 233 (others were ST 277, 708, and 875).* The ST233 isolates were identified across the five facilities and, using a core genome multilocus sequence typing analysis, clustered separately from epidemiologically unlinked ST233 isolates from CDC’s reference collection. In addition, clusters of highly related isolates (differences ranging from one to 10 single nucleotide polymorphisms) were consistent with transmission in vSNF A. These results suggest that a common strain of VIM-CRPA has had a longstanding presence in this region, with recent transmission in vSNF A.

The Chicago Department of Public Health provided ongoing on-site assessments to monitor infection control practices. Improvements were made in hand hygiene and isolation precautions compliance, resident cohorting, bathing practices, and environmental cleaning. The facility also stopped rinsing respiratory equipment with tap water in sinks in residents’ rooms.

This is the largest health care–associated cluster of VIM-CRPA isolates colonizing residents reported in the United States to date. Although centered in one vSNF, this investigation highlights the interconnectedness of health care facilities through patient sharing and how prolonged, undetected transmission can result in spread through a region. Application of CDC’s multidrug-resistant organisms containment guidance (6), including comprehensive on-site assistance and colonization screening, limited transmission at the index facility despite continued high prevalence. Improved availability of carbapenem resistance mechanism testing and screening tests are critical for early identification of and response to similar clusters. These resources are now available through CDC’s Antibiotic Resistance Laboratory Network.

Corresponding author: Massimo Pacilli,, 312-746-6225.

1Chicago Department of Public Health; 2Epidemic Intelligence Service, CDC; 3Division of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, CDC; 4Rush University Medical Center; Chicago, Illinois; 5APIC Consulting Services, Arlington, Virginia.

All authors have completed and submitted the ICMJE form for disclosure of potential conflicts of interest. Michael Lin reports receiving research support in the form of contributed product from OpGen and Sage Products, and an investigator-initiated grant from CareFusion Foundation (now part of BD). Mary Hayden reports receiving support in the form of contributed product from Sage (now Stryker) and from Molnlycke. Deb Burdsall and Mary Alice Lavin report receiving personal fees from APIC Consulting Services. No other potential conflicts of interest were disclosed.

* Raw sequencing reads were placed under BioProject ID PRJNA474674.


  1. Lolans K, Queenan AM, Bush K, Sahud A, Quinn JP. First nosocomial outbreak of Pseudomonas aeruginosa producing an integron-borne metallo-β-lactamase (VIM-2) in the United States. Antimicrob Agents Chemother 2005;49:3538–40. CrossRefexternal icon PubMedexternal icon
  2. Rankin D, Caicedo L, Dotson N, Gable P, Chu A. Notes from the field: Verona integron-encoded metallo-beta-lactamase–producing Pseudomonas aeruginosa outbreak in a long-term acute care hospital—Orange County, Florida, 2017. MMWR Morb Mortal Wkly Rep 2018;67:611–2. CrossRefexternal icon PubMedexternal icon
  3. Tsakris A, Pournaras S, Woodford N, et al. Outbreak of infections caused by Pseudomonas aeruginosa producing VIM-1 carbapenemase in Greece. J Clin Microbiol 2000;38:1290–2. PubMedexternal icon
  4. Crespo MP, Woodford N, Sinclair A, et al. Outbreak of carbapenem-resistant Pseudomonas aeruginosa producing VIM-8, a novel metallo-beta-lactamase, in a tertiary care center in Cali, Colombia. J Clin Microbiol 2004;42:5094–101. CrossRefexternal icon PubMedexternal icon
  5. Hammami S, Boutiba-Ben Boubaker I, Ghozzi R, Saidani M, Amine S, Ben Redjeb S. Nosocomial outbreak of imipenem-resistant Pseudomonas aeruginosa producing VIM-2 metallo-β-lactamase in a kidney transplantation unit. Diagn Pathol 2011;6:106. CrossRefexternal icon PubMedexternal icon
  6. CDC. Interim guidance for a public health response to contain novel or targeted multidrug-resistant organisms (MDROs). Atlanta, GA: US Department of Health and Human Services, CDC; 2017.
TABLE. Summary of Verona integron-encoded metallo-beta-lactamase–producing carbapenem-resistant Pseudomonas aeruginosa (VIM-CRPA) point prevalence surveys at vSNF A — Chicago, Illinois, November 2016–March 2018Return to your place in the text
Floor Date of PPS Total no. of residents on day of PPS Newly identified VIM-CRPA Newly positive, no previous screening Newly positive, previously screened negative Previously known VIM-CRPA Total no. of residents positive on day of PPS Prevalence, %
SN 11/1/16 72 4 4 0 0 4 6
1/17/17 67 0 0 0 3 3 4
7/10/17 71 0 0 0 0 0 0
VT 11/1/16 69 16 16 0 0 16 23
1/9/17 66 2 0 2 12 14 21
2/27/17 73 3 0 3 19 22 30
5/10/17 73 4 1 3 19 23 32
6/19/17 69 9 0 9 21 30 43
7/5/17 74 0 0 0 30 30 41
7/24/17 68 0 0 0 28 28 41
11/20/17 67 0 0 0 28 28 42
3/28/18 56 0 0 0 24 24 43
Total 38 21 17

Abbreviations: PPS = point prevalence survey; SN = standard skilled nursing floor; vSNF = skilled nursing facility with ventilated residents; VT = floor housing residents with tracheostomies or who were mechanically ventilated.

Suggested citation for this article: Clegg WJ, Pacilli M, Kemble SK, et al. Notes from the Field: Large Cluster of Verona Integron-Encoded Metallo-Beta-Lactamase–Producing Carbapenem-Resistant Pseudomonas aeruginosa Isolates Colonizing Residents at a Skilled Nursing Facility — Chicago, Illinois, November 2016–March 2018. MMWR Morb Mortal Wkly Rep 2018;67:1130–1131. DOI: icon.

MMWR and Morbidity and Mortality Weekly Report are service marks of the U.S. Department of Health and Human Services.
Use of trade names and commercial sources is for identification only and does not imply endorsement by the U.S. Department of Health and Human Services.
References to non-CDC sites on the Internet are provided as a service to MMWR readers and do not constitute or imply endorsement of these organizations or their programs by CDC or the U.S. Department of Health and Human Services. CDC is not responsible for the content of pages found at these sites. URL addresses listed in MMWR were current as of the date of publication.

All HTML versions of MMWR articles are generated from final proofs through an automated process. This conversion might result in character translation or format errors in the HTML version. Users are referred to the electronic PDF version ( and/or the original MMWR paper copy for printable versions of official text, figures, and tables.

Questions or messages regarding errors in formatting should be addressed to

View Page In:pdf icon
Page last reviewed: October 11, 2018