Acinetobacter baumannii: Association

Acinetobacter baumannii : Association between Environmental Contamination of Patient Rooms and Occupant Status Author(s): L. Silvia Munoz-Price, MD; Nicholas Namias, MD; Timothy Cleary, PhD; Yovanit Fajardo-Aquino, MD; Dennise DePascale, MT; Kristopher L. Arheart, EdD; Jesabel I. Rivera, BS; Yohei Doi, MD, PhD Source: Infection Control and Hospital Epidemiology, Vol. 34, No. 5, Special Topic Issue: The Role of the Environment in Infection Prevention (May 2013), pp. 517-520 Published by: The University of Chicago Press on behalf of The Society for Healthcare Epidemiology of America Stable URL: http://www.jstor.org/stable/10.1086/670209 . Accessed: 20/06/2013 14:59 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp

. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

.

The University of Chicago Press and The Society for Healthcare Epidemiology of America are collaborating with JSTOR to digitize, preserve and extend access to Infection Control and Hospital Epidemiology.

http://www.jstor.org

This content downloaded from 170.134.17.9 on Thu, 20 Jun 2013 14:59:58 PM All use subject to JSTOR Terms and Conditions

infection control and hospital epidemiology

may 2013, vol. 34, no. 5

concise communication

Acinetobacter baumannii: Association between Environmental Contamination of Patient Rooms and Occupant Status L. Silvia Munoz-Price, MD;1,2,3 Nicholas Namias, MD;4 Timothy Cleary, PhD;5 Yovanit Fajardo-Aquino, MD;3 Dennise DePascale, MT;3 Kristopher L. Arheart, EdD;2,6 Jesabel I. Rivera, BS;7 Yohei Doi, MD, PhD7

We aimed to determine the association between the presence of Acinetobacter baumannii in patient rooms and the carrier status of the occupants. Fifty-six (39%) of 143 rooms with A. baumannii– positive patients had results positive for A. baumannii. Only 49 (10%) of 485 rooms with A. baumannii–negative patients were positive (odds ratio, 5.72 [95% confidence interval, 3.66–8.96]; P ! .0001). Clinical and environmental isolates shared pulsed-field gel electrophoresis patterns. Infect Control Hosp Epidemiol 2013;34(5):517-520

During the past decade, several reports have highlighted the role that the hospital environment plays as a reservoir for Acinetobacter baumannii.1-5 This pathogen can survive in the environment for extended periods because of its innate resistance to desiccation.6 Additionally, A. baumannii frequently develops resistance to most commercially available antimicrobial agents, and infections caused by these highly resistant strains are associated with a mortality of up to 40%.7-9 To control a prolonged outbreak of A. baumannii infection, a bundle of interventions was implemented. One of the interventions consisted of regular environmental cultures looking for the presence of A. baumannii in patient rooms. Our study investigated the results of these environmental cultures and aimed to determine the association between room contamination with A. baumannii and the corresponding A. baumannii status of the occupants.

methods From January 1, 2011, to January 31, 2012, environmental cultures from inpatient rooms were obtained across 5 adult intensive care units (ICUs) at a county teaching hospital. These units were selected on the basis of their high numbers of new acquisitions of A. baumannii and included trauma (25 beds), medical (18), surgical (40), neurosurgical (20), and progressive (20; medical patients) ICUs. Throughout this project, the facility experienced a hyperendemic situation with carbapenem-resistant A. baumannii. The study was reviewed and approved by the institutional review board of the University of Miami.

Weekly active surveillance cultures (rectal and respiratory samples) were standard among all of our adult ICU patients. The A. baumannii status of patients present in each of the ICUs was available in the patient census and maintained by the Infection Control Department on the basis of microbiology data. A patient with at least 1 culture positive for A. baumannii, including surveillance and clinical cultures, was considered to be positive for A. baumannii. Environmental cultures were performed weekly on a rotating basis (1–2 units/week) across the selected ICUs. The following 4 standard objects were cultured from inpatient rooms: bed rails, bedside tables, intravenous pumps, and ventilator control panels (unless the object was not present). No other objects were analyzed in this project. Approximately 10 # 10 cm of each surface was sampled using premoistened 6-inch cotton swabs (Sterile Cotton-Tipped Applicators; MediChoice). A single swab was used for each individual surface. Swabs were promptly placed in trypticase soy broth (BD Diagnostics) and incubated overnight at 37⬚C. Broths showing turbidity were subcultured onto both blood and MacConkey agar plates. To aid in the detection of resistant gram-negative organisms, ertapenem (10 mg) and meropenem (10 mg) disks were placed on the streaked portion of the MacConkey agar plates (BD Diagnostics). Colonies were selected on the basis of color and morphology and were subcultured for isolation. Identification and susceptibility testing was performed using Vitek II (bioMe´rieux). A positive room was defined as any patient room found to have at least 1 object positive for A. baumannii. During this project, the cleaning policy of the ICUs specified daily cleaning of horizontal surfaces using 1 : 10 bleach (Dispatch; Clorox). Cleaning of the rooms occurred during morning shifts, and environmental cultures were obtained, for the most part, in early afternoon. Concordant pairs of A. baumannii isolates (within a 30day period) were subjected to pulsed-field gel electrophoresis (PFGE). We also included 2 environmental isolates present in rooms without A. baumannii–positive patients. For this procedure, genomic DNA embedded in agarose gel was digested with restriction enzyme ApaI. The resultant fragments were then separated by electrophoresis using a temperaturecontrolled CHEF DR III system as described elsewhere.10 For PFGE pattern analysis, the Bionumerics software, version 6.01, was used to create a dendrogram based on the unweighted pair group method with arithmetic mean with a tolerance of 1.5%. The presence of A. baumannii in a given room was analyzed as a dichotomous variable (yes/no) against the patient’s A. baumannii carrier status on the matching room (A. baumannii positive vs negative). Logistic regression was performed using SAS 9.3 for all analysis.


518


may 2013, vol. 34, no. 5

results During a 13-month period, a total of 628 ICU rooms were cultured; of these, 105 (16.7%) were positive for A. baumannii for at least 1 of the 4 objects cultured (Figure 1). Among all the positive rooms, bed rails were the objects most frequently found to be contaminated with A. baumannii (n p 73; 70%). A. baumannii–positive patients were present in 143 (23%) of the 628 rooms cultured, and 56 (39%) of these 143 rooms were found to be concomitantly positive for A. baumannii. To the contrary, A. baumannii–negative patients were present in 485 (77%) of the cultured rooms, and only 49 (10%) of these rooms had cultures that grew A. baumannii. The odds ratio of environmental contamination of the rooms with A. baumannii–positive occupants versus A. baumannii-negative occupants was 5.7 (95% confidence interval, 3.66–8.96; P ! .0001). Of a total of 105 positive rooms, 86 (82%) had only 1 of 4 objects positive for A. baumannii, and 19 (18%) had 2 or more positive objects. Furthermore, of the latter 19 rooms, 15 (79%) had the bed rails as one of the positive objects. During this project, A. baumannii was identified in a total of 127 objects, including 73 bed rails (57%), 29 intravenous pumps (23%), 13 bed side tables (10%), and 12 ventilator control panels (9%). There were 7 instances in which isolates from both a patient and the corresponding room were available. The PFGE patterns were related by 94.8% or greater in 6 of these 7 pairs (Figure 2).

discussion Throughout this project, we identified the presence of A. baumannii in 16.7% of the 628 patient rooms cultured. The rooms of A. baumannii–positive patients were positive for this organism in 39% of instances. The likelihood of having

a positive room when an occupant was A. baumannii positive was almost 5 times higher than if the occupant was A. baumannii negative. Additionally, bed rails were the objects most frequently found to be contaminated within positive rooms. To the best of our knowledge, this is the first study that shows a differential risk of environmental contamination with A. baumannii on the basis of the status of the room occupants. Furthermore, this is the largest study to identify the presence of A. baumannii in the hospital environment. In this project, we performed environmental cultures using the following 4 objects: bed rails, bedside tables, intravenous pumps, and ventilator control panels. These objects were selected from surfaces previously described as high touch.11 Furthermore, 3 of these 4 objects have been previously shown to have the highest frequency of contamination with A. baumannii among A. baumannii–positive occupants.2 Even though supply carts are also considered high-touch surfaces, we opted not to culture these objects, given that many of our ICUs are open units with supply carts present in common areas. Nevertheless, our findings showed that the objects most frequently contaminated with A. baumannii were the bed rails, followed by intravenous pumps. This finding is consistent with previously published studies.2,10 We found that isolates obtained from a patient and from his or her room environment were highly related by PFGE in all instances but one. Although the isolates from the trauma ICU were related by 79.8% or greater overall, these paired isolates had at least 94.8% similarity with each other (mean similarity, 97.8%). This finding suggested that the room was directly contaminated from the A. baumannii–positive patient or that the patient was colonized directly from the contaminated room, rather than the 2 entities being incidentally contaminated by distinct isolates at the same time. These molecular typing data are also consistent with the overall finding that a room is significantly more likely to be con-

figure 1. Results of the environmental cultures based on room occupant status. Ab, Acinetobacter baumannii; OR, odds ratio.


a. baumannii contamination of patient rooms

519

figure 2. Pulsed-field gel electrophoresis of environmental (E) and clinical (C) Acinetobacter baumannii isolates. Numbers indicate concordant pairs. Isolates 6 and 8 were environmental isolates from rooms occupied by A. baumannii–negative patients. Percentage of relatedness between environmental and clinical isolates in descending order is as follows: 2C–E, 99.5%; 7C–E, 99.0%; 9C–E, 98.1%; 5C– E, 98.0%; 3C–E, 97.4%; 1C–E, 94.8%; 4C–E, 83.0%.

taminated by A. baumannii when it houses a patient known to carry this organism. The limitations of this project include being a single-center experience during an endemic situation with A. baumannii. We did not evaluate the effect on room contamination of other variables, such as the presence of colonization versus infection with A. baumannii, the status of other comorbidities, the number of A. baumannii–positive patients concomitantly present in the unit, the distance between positive patients within the unit and environmental surfaces tested, and the unit’s layout (open vs single-patient rooms). Additionally, we did not factor in the number of days that the patient was A. baumannii positive within the specific room cultured. In a previous study by Thom et al,2 the length of positivity with A. baumannii was not associated with the degree of environmental contamination, although the duration of stay within the same bed (while being A. baumannii positive) was not factored in. Future studies should determine the different extents of transmission from patient to environment versus from environment to patient. In conclusion, a high degree of environmental contamination was detected among A. baumannii–positive occupants. Nevertheless, environmental contamination with A. baumannii was also present among A. baumannii–negative room occupants, although to a lesser degree. Is the latter contami-

nation a result of horizontal transmission from adjacent rooms? If the answer to the last question were yes, then how much would once-a-day cleaning improve recurrent contamination potentially happening throughout the day because of recurrent noncompliance with hand hygiene or disinfection of shared objects? Are these supposedly A. baumannii– negative patients instead subjects who have been misclassified because of the poor sensitivity of the surveillance cultures? What are the clinical implications of A. baumannii–negative patients being exposed to an environment contaminated with A. baumannii? The answers to these questions and the role of the degree of environmental contamination of the variables previously mentioned should be determined in the future.

acknowledgments Potential conflicts of interest. All authors report no conflicts of interest relevant to this article. All authors submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and the conflicts that the editors consider relevant to this article are disclosed here. Affiliations: 1. Department of Medicine, Miller School of Medicine, University of Miami, Miami, Florida; 2. Department of Epidemiology and Public Health, Miller School of Medicine, University of Miami, Miami, Florida; 3. Jackson Memorial Hospital, Miami, Florida; 4. Department of Surgery,


520


may 2013, vol. 34, no. 5

Miller School of Medicine, University of Miami, Miami, Florida; 5. Department of Pathology, Miller School of Medicine, University of Miami, Miami, Florida; 6. Division of Biostatistics, Miller School of Medicine, University of Miami, Miami, Florida; 7. Division of Infectious Diseases, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania. Address correspondence to L. Silvia Munoz-Price, MD, LSMP Park Plaza West L-302, 1611 Northwest 12th Avenue, Miami, FL 33136 ([email protected]). Received September 23, 2012; accepted November 11, 2012; electronically published April 9, 2013. 䉷 2013 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2013/3405-0012$15.00. DOI: 10.1086/670209

references

4.

5. 6. 7.

8.

1. Levin AS, Gobara S, Mendes CM, Cursino MR, Sinto S. Environmental contamination by multidrug-resistant Acinetobacter baumannii in an intensive care unit. Infect Control Hosp Epidemiol 2001;22:717–720. 2. Thom KA, Johnson JK, Lee MS, Harris AD. Environmental contamination because of multidrug-resistant Acinetobacter baumannii surrounding colonized or infected patients. Am J Infect Control 2011;39:711–715. 3. Morgan DJ, Rogawski E, Thom KA, et al. Transfer of multidrugresistant bacteria to healthcare workers’ gloves and gowns after

9. 10.

11.

patient contact increases with environmental contamination. Crit Care Med 2012;40:1045–1051. Hota B. Contamination, disinfection, and cross-colonization: are hospital surfaces reservoirs for nosocomial infection? Clin Infect Dis 2004;39:1182–1189. Weinstein RA. Intensive care unit environments and the fecal patina: a simple problem? Crit Care Med 2012;40:1333–1334. Wendt C, Dietze B, Dietz E, Ru¨den H. Survival of Acinetobacter baumannii on dry surfaces. J Clin Microbiol 1997;35:1394–1397. Munoz-Price LS, Zembower T, Penugonda S, et al. Clinical outcomes of carbapenem-resistant Acinetobacter baumannii bloodstream infections: study of a 2-state monoclonal outbreak. Infect Control Hosp Epidemiol 2010;31:1057–1062. Maragakis LL, Perl TM. Acinetobacter baumannii: epidemiology, antimicrobial resistance, and treatment options. Clin Infect Dis 2008;46:1254–1263. Fishbain J, Peleg AY. Treatment of Acinetobacter infections. Clin Infect Dis 2010;51:79–84. Seifert H, Dolzani L, Bressan R, et al. Standardization and interlaboratory reproducibility assessment of pulsed-field gel electrophoresis-generated fingerprints of Acinetobacter baumannii. J Clin Microbiol 2005;43:4328–4335. Huslage K, Rutala WA, Sickbert-Bennett E, Weber DJ. A quantitative approach to defining “high-touch” surfaces in hospitals. Infect Control Hosp Epidemiol 2010;31:850–853.
