Skip to main content
NCBI home page
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2013 May 21.
Published in final edited form as: Eur J Clin Microbiol Infect Dis. 2011 Apr 12;30(11):1425–1430. doi: 10.1007/s10096-011-1237-7

Comparison of culture media for detection of Acinetobacter baumannii in surveillance cultures of critically-ill patients

A O Ajao 1,✉, G Robinson 2, M S Lee 3, T D Ranke 4, R A Venezia 5, J P Furuno 6, A D Harris 7, J K Johnson 8,9
PMCID: PMC3660032  NIHMSID: NIHMS389110  PMID: 21487763

Abstract

The objective of this study was to evaluate the performance of CHROMagar Acinetobacter when compared to sheep blood agar, MacConkey agar and MacConkey agar with 6 µg/ml of imipenem for the detection of A. baumannii in surveillance cultures of hospitalized patients. We utilized peri-anal swabs and sputum samples from patients admitted to the University of Maryland Medical Center ICUs from December 7 through December 21, 2009. Samples were plated onto four media in the following order: (1) 5% sheep blood agar (SBA), (2) MacConkey agar, (3) MacConkey agar with 6 µg/ml of imipenem, and (4) CHROMagar Acinetobacter (CHROMagar). SBA was the gold standard to which all media was compared. There were 165 samples collected during the study period. SBA and CHROMagar detected 18 of 18 (100%) Acinetobacter and 11 of 11 (100%) MDR-A. baumannii. MacConkey agar detected 16 of 18 (89%) Acinetobacter and 10 of 11 (91%) MDR- A. baumannii while MacConkey agar with 6 µg/ml imipenem detected 9 of 11 (82%) MDR-A. baumannii. CHROMagar did not differentiate MDR- A. baumannii from non-MDR-A. baumannii. CHROMagar may be useful for rapid detection of patients with MDR-A. baumannii if improved upon to better select for MDR-A. baumannii.

Introduction

Acinetobacter species, especially A. baumannii, has emerged as an important nosocomial pathogen contributing to increased morbidity and mortality among infected patients [1–3]. A. baumannii causes a wide range of infections including hospital-acquired pneumonia, respiratory-tract infection, urinary tract infections, surgical site infections, and bloodstream infections [4]. Furthermore, A. baumannii is resistant to multiple classes of commonly-used antibiotics, thus complicating treatment of these infections [5]. Multiple outbreaks due to A. baumannii have been reported globally [6–11]. These outbreaks have primarily been in intensive care units (ICUs) [7,11]; however, outbreaks have also occurred in surgical wards, burn units and general medical wards [6, 8–10]. Increased morbidity and mortality associated with the outbreaks have prompted some hospitals to begin performing active surveillance in high-risk patients in an attempt to control the spread of A. baumannii [12]. Currently, there is no recommended medium for screening of surveillance and clinical cultures for A. baumannii. Sheep blood agar and MacConkey agar are conventionally used for detection of A. baumannii in clinical cultures; however, these methods are non-selective for A. baumannii. Thus detection and isolation of A. baumannii from surveillance and clinical cultures is laborious and requires several days due to the presence of other bacteria species present in the human flora [13]. In contrast, chromogenic media that can rapidly identify patients colonized or infected with A. baumannii may improve the efficiency of infection control practices, shorten the time to delivery of appropriate antibiotic therapy for infected patients and reduce mortality [14]. The University of Maryland Medical Center (UMMC) utilizes an in-house selective media consisting of MacConkey agar supplemented with 6 µg/ml of imipenem to select for multidrug resistant (MDR)-A. baumannii in surveillance cultures.

Chromogenic media are culture media that are designed for rapid and simple detection of bacteria. They contain chromogenic substrates that are cleaved by enzymes produced by bacteria resulting in unique coloration of the colonies of each bacteria strain allowing for easy identification. Currently, there are numerous chromogenic media that are commercially available and commonly used for rapid detection of colonization with organisms that cause hospital acquired infections such as methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, extended-spectrum beta-lactam-producing bacteria and carbapenem-resistant bacteria [15–21].

CHROMagar Acinetobacter is a recently developed chromogenic media designed for detection and isolation of Acinetobacter species. This media inhibits the growth of most gram-positive cocci and yeast and employs a color-change identification method that allows Acinetobacter species to appear as red colonies. The objective of this study was to evaluate the performance of CHROMagar Acinetobacter when compared to sheep blood agar, MacConkey agar and MacConkey agar with 6 µg/ml of imipenem for detection and isolation of A. baumannii in infection control surveillance cultures of hospitalized patients.

Materials and methods

Sample collection

We utilized leftover peri-anal swabs and sputum samples obtained from a cohort of patients admitted to UMMC medical intensive care unit (MICU) and surgical intensive care unit (SICU) for surveillance of vancomycin-resistant enterococci from December 7, 2009 through December 21, 2009. Peri-anal swabs were obtained routinely from all patients upon ICU admission. Sputum samples were collected in sputum traps from patients who were ventilated during their ICU admission. These samples were collected as part of routine infection control surveillance; therefore, individual informed consent was not sought prior to including their samples in the study. This study was approved by the Institutional Review Board of the University of Maryland, Baltimore.

Media preparation

This study used a formulation of CHROMagar Acinetobacter that was designed for the detection of Acinetobacter species. CHROMagar Acinetobacter was prepared from dehydrated powder and liquid supplement according to manufacturer’s instructions (Chromagar; Paris, France). MacConkey agar with imipenem was prepared in house from dehydrated MacConkey powder according to manufacturer’s instructions (BD, Sparks, MD), and supplemented with 300 µl of 20 mg/ml stock of imipenem solution per one liter of MacConkey solution for a final concentration of 6 µg/ml. An imipenem concentration of 6 µg/ml was chosen to select for intermediate and resistant A. baumannii using Clinical and Laboratory Standard Institute (CLSI) breakpoints [22–24]. MacConkey agar and sheep blood agar plates were purchased directly from the manufacturer (BD, Sparks, MD).

Agar inoculation and comparison

Peri-anal swabs and sputum samples were inoculated directly onto the four agar media in this order: (1) 5% sheep blood agar, (2) MacConkey agar, (3) MacConkey agar with 6ug/ml of imipenem, and (4) CHROMagar Acinetobacter. The same swab was inoculated onto each media and rotated completely. Plates were streaked for isolation and incubated at 37°C for 24 hours. The same laboratory technician evaluated all four plates for a specific patient sample. CHROMagar Acinetobacter and MacConkey agar were compared to sheep blood agar for detection of Acinetobacter species, while CHROMagar Acinetobacter, MacConkey agar, and MacConkey agar with 6 µg/ml of imipenem were compared to sheep blood agar for isolation of MDR-Acinetobacter. Thus, for all comparisons in this study, sheep blood agar was considered the gold standard.

Colony identification and susceptibility testing

Oxidase negative colonies morphologically similar to Acinetobacter were identified using the Vitek II (bioMerieux; Durham, NC). Susceptibilities were performed by disk diffusion method and E-tests (bioMerieux; Durham, NC) and interpreted based on current CLSI guidelines [22]. Acinetobacter isolates were tested against imipenem, doripenem, meropenem, ertapenem, sulfamethoxazole-trimethoprim, ampicillin-sulbactam, piperacillin-tazobactam, ceftazidime, cefepime, ciprofloxacin, amikacin, gentamicin, polymyxin B, and tigecycline. Multidrug resistance was defined as susceptible to two or fewer antibiotics not including polymixin B and tigecycline [24].

Results

There were 165 surveillance samples (153 peri-anal swabs and 12 sputum samples) received at the UMMC microbiology laboratory from 165 unique patients admitted to the MICU and SICU during the 2-week study period. Only 12 sputum samples were collected due to the small number of patients ventilated during their ICU stay. Of the 165 samples collected, 17 samples (10.3%) which consisted of 12 peri-anal swabs and five sputum samples yielded Acinetobacter from sheep blood agar. One peri-anal swab yielded two morphologically different A. baumannii isolates resulting in a total of 18 Acinetobacter species isolated and identified. Of the 18 Acinetobacter isolates, 17 were identified as A. baumannii and one was identified as A. lwoffii. The two morphologically different A. baumannii isolates recovered from the same peri-anal swab had different antibiotic susceptibility profiles. One of the two isolates was identified as an MDR-A. baumannii while the other isolate was identified as a non-MDR-A. baumannii. The non-MDR-A. baumannii isolate was recovered from all four media while the MDR-A. baumannii isolate was recovered from sheep blood agar, MacConkey agar with 6 µg/ml of imipenem and CHROMagar Acinetobacter but not from MacConkey agar. On CHROMagar Acinetobacter, both isolates appeared as red colonies but the MDR-A. baumannii isolate appeared as round and smooth colonies while the non-MDR-A. baumannii isolate appeared as mucoid and spready colonies.

Sheep blood agar and CHROMagar Acinetobacter recovered 18 of 18 (100%) Acinetobacter isolates while MacConkey agar recovered 16 of 18 (89%) Acinetobacter isolates. The isolate identified as Acinetobacter lwoffii was a non-MDR-Acinetobacter and was recovered by sheep blood agar, CHROMagar Acinetobacter and MacConkey agar. Of the 18 Acinetobacter identified, 11 (61%) were identified as MDR-A. baumannii. The 11 MDR-A. baumannii were detected and isolated from eight peri-anal swabs and three sputum samples. Sheep blood agar and CHROMagar Acinetobacter recovered 11 of 11 (100%) MDR-A. baumannii. MacConkey agar recovered 10 of 11 (91%) MDR-A. baumannii. MacConkey agar with 6 µg/ml imipenem recovered 9 of 11 (82%) MDR-A. baumannii. The two MDR-A. baumannii that did not grow on MacConkey agar with 6 µg/ml imipenem had imipenem minimum inhibitory concentration (MIC) of 6 µg/ml. All MDR-A. baumannii identified were resistant to imipenem, doripenem, meropenem, ertapenem, piperacillin tazobactam and ciprofloxacin. Ten of the 11 MDR-A. baumannii (91%) were resistant to ceftazidime, 9 (82%) were resistant to ampicillin-sulbactam, 8 (73%) were resistant to amikacin, 7 (64%) were resistant to cefepime, and 5 of the 11 MDR-A. baumannii (46%) were resistant to gentamicin (Table 1).

Table 1.

Antibiotic susceptibility profile for MDR-A. baumannii isolated using four different culture media

Isolate no. ORG IPM DORI MER ERT SXT SAM AMK GEN TZP CIP CAZ FEP
26.1 A. baumannii R NS R R R R S S R R R R
35.3 A. baumannii R NS R R R R R S R R R R
40 A. baumannii R NS R R R R I R R R R I
43 A. baumannii R NS R R R R I R R R R I
57.1 A. baumannii R NS R R S R R S R R R R
92 A. baumannii R NS R R R R R R R R R R
112 A. baumannii R NS R R R S R S R R R I
122 A. baumannii R NS R R R R R R R R R R
123.2 A. baumannii R NS R R R R R R R R I R
151.2 A. baumannii R NS R R R I R S R R R I
155 A. baumannii R NS R R R R R S R R R R
Open in a new tab

IPM imipenem, DORI doripenem, MER meropenem, ERT ertapenem, SXT sulfamethoxazole-trimethoprim, SAM ampicillin-sulbactam, AMK amikacin, GEN gentamicin, TZP piperacillin tazobactam, CIP ciprofloxacin, CAZ ceftazidime, FEP cefepime, MIC minimum inhibitory concentration, R resistant, S susceptible, NS not susceptible, I intermediate

On CHROMagar Acinetobacter, all Acinetobacter species appeared as bright salmon-red colonies at 24 hours. Colony morphology of MDR and non-MDR-Acinetobacter was indistinguishable on CHROMagar Acinetobacter. CHROMagar Acinetobacter also allowed growth of other red colonies. These red colonies were identified as other gram-negative bacteria other than Acinetobacter and were distinguishable from Acinetobacter colonies by variation of their red color, colony morphology and oxidase reaction. Six isolates appeared as shiny red colonies, tested oxidase-positive and were identified as Pseudomonas species. Three isolates appeared as pinpoint red-orange colonies with clear pheripheral edges, tested oxidase-negative and were identified as Stenotrophomonas maltophilia. Two isolates appeared as pinpoint dark red colonies, tested oxidase-positive and were identified as Achromobacter xylosoxidans (Fig. 1).

Fig. 1.

Fig. 1

Open in a new tab

Appearance of Acinetobacter spp. and other gram-negative bacteria with similar red color as Acinetobacter on CHROMagar Acinetobacter media. a Acinetobacter spp. appeared as bright salmon red colonies. b Pseudomonas spp. appeared as shiny red colonies and tested oxidase-positive. c Stenotrophomonas spp. appeared as red-orange pinpoint colonies with clear pheripheral edges and tested oxidase-negative. d Achromobacter spp. appeared as pinpoint dark red colonies and tested oxidase-positive

Discussion

The objective of this study was to evaluate the performance of CHROMagar Acinetobacter when compared to sheep blood agar, MacConkey agar and MacConkey agar with 6 µg/ml of imipenem for detection and isolation of A. baumannii in infection control surveillance cultures of hospitalized patients. Sheep blood agar, an enriched media that allows for the growth of most bacterial species, was the gold standard to which all other media were compared in this study.

Our study results suggest that CHROMagar Acinetobacter was 100% sensitive for both MDR and non-MDR-Acinetobacter when compared to sheep blood agar. Acinetobacter species appeared as bright salmon red colonies on CHROMagar Acinetobacter facilitating easier identification and isolation. However, CHROMagar Acinetobacter did not differentiate MDR from non-MDR-Acinetobacter and further susceptibility testing is needed to confirm multidrug resistance status. In addition, CHROMagar Acinetobacter allows growth of red colonies that were identified as other gram-negative bacteria besides Acinetobacter; however, these other bacteria could be distinguished from Acinetobacter by variation of their red color, colony morphology and oxidase reaction.

MacConkey agar was 89% sensitive for Acinetobacter species and 91% sensitive for MDR-A. baumannii when compared to sheep blood agar. It is unlikely that depletion of bacteria colonies on the inoculation swab is responsible for the Acinetobacter isolates that were not recovered by MacConkey agar since CHROMagar Acinetobacter was inoculated last and recovered all Acinetobacter isolates. MacConkey agar may be reliable for isolating Acinetobacter species but it is non-selective for Acinetobacter and does not differentiate Acinetobacter from other non-lactose fermenting gram-negative bacteria. Thus differentiating and isolating Acinetobacter from other non-lactose fermenting gram-negative bacteria on MacConkey agar may still be laborious and time-consuming.

MacConkey agar with 6 µg/ml imipenem was 82% sensitive for MDR-A. baumannii when compared to sheep blood agar. The two MDR-A. baumannii that were not recovered by MacConkey agar with 6 µg/ml imipenem had imipenem MICs of 6 µg/ml. It is possible that MDR-Acinetobacter with MIC for imipenem that is close to the breakpoint for intermediate resistance may be missed with 6 µg/ml of imipenem.

Other selective media have been previously developed and compared for the detection and isolation of Acinetobacter species. Jawad et al. compared Herellea agar, Holten agar and Leeds Acinetobacter media (LAM) and reported that both Herellea agar and Holten agar have low sensitivity for Acinetobacter when compared to LAM. The study result suggested that LAM was better at selecting for and differentiating Acinetobacter from other bacteria present in the clinical and environmental samples tested. However, LAM was not commercially available in the United States during our study period and was not included in our comparative study [25].

Previous studies have compared CHROMagar Acinetobacter to other methods for detecting Acinetobacter. Gordon et al. compared CHROMagar Acinetobacter to a molecular method for the ability to detect MDR-A. baumannii in enteric samples of critically ill patients. The CHROMagar evaluated in the study by Gordon et al. was an investigational culture media different from the one evaluated in our study. Their CHROMagar Acinetobacter contained agent that inhibits the growth of most gram-positive bacteria as well as carbapenem-susceptible gram-negative bacteria while allowing Acinetobacter to appear as aqua blue colonies instead of the red colonies in our study. Their study reported that CHROMagar Acinetobacter was both sensitive (91.7%) and specific (89.7%) for MDR-A. baumannii when compared to PCR [26].

Another study by Akers et al. evaluated CHROMagar Acinetobacter for the ability to distinguish carbepenem-resistant and carbepenem-susceptible-A. baumannii. Their study reported that CHROMagar Acinetobacter was unable to distinguish carbepenem-resistant from carbepenem-susceptible-A. baumannii. In addition, various other organisms such as P. aeruginosa, E. cloacae and S. aureus grew on CHROMagar Acinetobacter with the same red or similar red-orange color as A. baumannii. Their study also reported that CHROMagar Acinetobacter was 75% sensitive and 100% specific for A. baumannii. Based on their study result, Akers et. al. advised against the use of CHROMagar Acinetobacter in the absence of confirmatory testing [27].

The study results from Akers et al. was similar to our study result in that MDR-A. baumannii was indistinguishable from non-MDR-A. baumannii on CHROMagar Acinetobacter by colony color or morphology. In our study, S. maltophilia, P. aeruginosa and A. xylosoxidans grew on CHROMagar Acinetobacter with a similar red color as A. baumannii but we did not observe the growth of E. cloacae and S. aureus as reported by Akers et al. This study also reported a lower sensitivity of CHROMagar Acinetobacter for A. baumannii than observed in our study.

CHROMagar Acinetobacter has been recently improved to select for MDR-Acinetobacter. Addition of an optional MDR supplement CR102 specifically selects for MDR-resistant strains defined as strains that are resistant to carbapenems. CHROMagar Acinetobacter specifically designed for identification of MDR-Acinetobacter was recently evaluated by Wareham et. al. This study reported that the addition of the MDR supplement to CHROMagar Acinetobacter prevented the growth of carbapenem-susceptible A. baumannii. However, the authors reported that S. maltophilia still grew on CHROMagar Acinetobacter and appeared with a similar red color as A. baumannii, making it difficult to distinguish from A. baumanii [28].

Excluding the cost of equipment and labor, the cost of CHROMagar Acinetobacter is higher than the cost of sheep blood agar and MacConkey agar. However, there may be additional costs associated with isolation and identification of other bacterial isolates worked up and ultimately found not to be Acinetobacter when using sheep blood agar and MacConkey agar. CHROMagar Acinetobacter may save time when the absence of a red color indicates the absence of Acinetobacter species in a patient sample. However, a comprehensive time and cost-benefit analysis of using CHROMagar Acinetobacter versus sheep blood agar and MacConkey agar for isolating Acinetobacter is beyond the scope of this study. It will be useful for future studies to compare CHROMagar Acinetobacter to other culture media on their time and cost savings.

In summary, our study results and those from prior studies suggest that CHROMagar Acinetobacter is selective for A. baumannii but still allows growth of certain other gram-negative bacteria with a similar red color as A. baumannii. Even though these other bacteria can be distinguished from Acinetobacter by the variation of their red color, colony morphology and oxidase reaction, there is still need for CHROMagar Acinetobacter to better differentiate A. baumannii from these other gram-negative bacteria without further testing to confirm A. baumannii. CHROMagar Acinetobacter may be a useful media for screening and improving infection control strategies aimed at limiting the spread of MDR-A. baumannii if improved upon to better select for MDR-A. baumannii. The addition of MDR supplement to CHROMagar Acinetobacter has demonstrated selectivity for carbapenem-resistant A. baumannii. However, larger studies in different patient populations are needed to evaluate the performance of CHROMagar Acinetobacter with MDR supplement for screening of MDR-A. baumannii. Although a limitation of this study is the small sample size, this study provides useful information on the performance of CHROMagar Acinetobacter when compared to other culture media for detection of A. baumannii for surveillance and control of Acinetobacter species in critically ill patients.

Acknowledgements

CHROMagar (Paris, France) supplied powdered media for the study and supported previous presentation of this data.

Dr. Harris was supported by National Institutes of Health Midcareer Investigator Award 1K24AI079040 and 2R01AI060859-05. Dr. Furuno was supported by National Institutes of Health Career Development Award 1K01AI071015-03 and Agency for Healthcare Research and Quality Contract Number: HHSA290200600020. Dr. Johnson is supported by National Institutes of Health grant 1K12RR023250-03. AO received travel funds to present this data at the 50th ICAAC, Boston, MA, 2010.

Footnotes

Conflict of Interest The authors declare that they have no conflict of interest to report.

Contributor Information

A. O. Ajao, Email: aajao@epi.umaryland.edu, Department of Epidemiology and Public Health, University of Maryland School of Medicine, 685 W. Baltimore St, Baltimore, MD 21201, USA.

G. Robinson, Department of Epidemiology and Public Health, University of Maryland School of Medicine, 685 W. Baltimore St, Baltimore, MD 21201, USA

M. S. Lee, Department of Epidemiology and Public Health, University of Maryland School of Medicine, 685 W. Baltimore St, Baltimore, MD 21201, USA

T. D. Ranke, Department of Epidemiology and Public Health, University of Maryland School of Medicine, 685 W. Baltimore St, Baltimore, MD 21201, USA

R. A. Venezia, Department of Pathology, University of Maryland School of Medicine, 685 W. Baltimore St, Baltimore, MD 21201, USA

J. P. Furuno, Department of Epidemiology and Public Health, University of Maryland School of Medicine, 685 W. Baltimore St, Baltimore, MD 21201, USA

A. D. Harris, Department of Epidemiology and Public Health, University of Maryland School of Medicine, 685 W. Baltimore St, Baltimore, MD 21201, USA

J. K. Johnson, Department of Epidemiology and Public Health, University of Maryland School of Medicine, 685 W. Baltimore St, Baltimore, MD 21201, USA Department of Pathology, University of Maryland School of Medicine, 685 W. Baltimore St, Baltimore, MD 21201, USA.

References

  • 1.Sunenshine RH, Wright MO, Maragakis LL, Harris AD, Song X, Hebden J, Cosgrove SE, Anderson A, Carnell J, Jernigan DB, Kleinbaum DG, Perl TM, Standiford HC, Srinivasan A. Multidrug-resistant Acinetobacter infection mortality rate and length of hospitalization. Emerg Infect Dis. 2007;13(1):97–103. doi: 10.3201/eid1301.060716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Playford EG, Craig JC, Iredell JR. Carbapenem-resistant Acinetobacter baumannii in intensive care unit patients: risk factors for acquisition, infection and their consequences. J Hosp Infect. 2007;65(3):204–211. doi: 10.1016/j.jhin.2006.11.010. [DOI] [PubMed] [Google Scholar]
  • 3.Kwon KT, Oh WS, Song JH, Chang HH, Jung SI, Kim SW, Ryu SY, Heo ST, Jung DS, Rhee JY, Shin SY, Ko KS, Peck KR, Lee NY. Impact of imipenem resistance on mortality in patients with Acinetobacter bacteraemia. J Antimicrob Chemother. 2007;59(3):525–530. doi: 10.1093/jac/dkl499. [DOI] [PubMed] [Google Scholar]
  • 4.Munoz-Price LS, Weinstein RA. Acinetobacter infection. N Engl J Med. 2008;358(12):1271–1281. doi: 10.1056/NEJMra070741. [DOI] [PubMed] [Google Scholar]
  • 5.Urban C, Meyer KS, Mariano N, Rahal JJ, Flamm R, Rasmussen BA, Bush K. Identification of TEM-26 beta-lactamase responsible for a major outbreak of ceftazidime-resistant Klebsiella pneumoniae. Antimicrob Agents Chemother. 1994;38(2):392–395. doi: 10.1128/aac.38.2.392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Kohlenberg A, Brummer S, Higgins PG, Sohr D, Piening BC, de Grahl C, Halle E, Ruden H, Seifert H. Outbreak of carbapenem-resistant Acinetobacter baumannii carrying the carbapenemase OXA-23 in a German university medical centre. J Med Microbiol. 2009;58(Pt 11):1499–1507. doi: 10.1099/jmm.0.012302-0. [DOI] [PubMed] [Google Scholar]
  • 7.Fontana C, Favaro M, Minelli S, Bossa MC, Testore GP, Leonardis F, Natoli S, Favalli C. Acinetobacter baumannii in intensive care unit: a novel system to study clonal relationship among the isolates. BMC Infect Dis. 2008;8:79. doi: 10.1186/1471-2334-8-79. 8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Lolans K, Rice TW, Munoz-Price LS, Quinn JP. Multicity outbreak of carbapenem-resistant Acinetobacter baumannii isolates producing the carbapenemase OXA-40. Antimicrob Agents Chemother. 2006;50(9):2941–2945. doi: 10.1128/AAC.00116-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Heritier C, Dubouix A, Poirel L, Marty N, Nordmann P. A nosocomial outbreak of Acinetobacter baumannii isolates expressing the carbapenem-hydrolysing oxacillinase OXA-58. J Antimicrob Chemother. 2005;55(1):115–118. doi: 10.1093/jac/dkh500. [DOI] [PubMed] [Google Scholar]
  • 10.Maragakis LL, Cosgrove SE, Song X, Kim D, Rosenbaum P, Ciesla N, Srinivasan A, Ross T, Carroll K, Perl TM. An outbreak of multidrug-resistant Acinetobacter baumannii associated with pulsatile lavage wound treatment. JAMA. 2004;292(24):3006–3011. doi: 10.1001/jama.292.24.3006. [DOI] [PubMed] [Google Scholar]
  • 11.Melamed R, Greenberg D, Porat N, Karplus M, Zmora E, Golan A, Yagupsky P, Dagan R. Successful control of an Acinetobacter baumannii outbreak in a neonatal intensive care unit. J Hosp Infect. 2003;53(1):31–38. doi: 10.1053/jhin.2002.1324. [DOI] [PubMed] [Google Scholar]
  • 12.Maragakis LL, Tucker MG, Miller RG, Carroll KC, Perl TM. Incidence and prevalence of multidrug-resistant acinetobacter using targeted active surveillance cultures. JAMA. 2008;299(21):2513–2514. doi: 10.1001/jama.299.21.2513. [DOI] [PubMed] [Google Scholar]
  • 13.Wise KA, Tosolini FA. Epidemiological surveillance of Acinetobacter species. J Hosp Infect. 1990;16(4):319–329. doi: 10.1016/0195-6701(90)90004-8. [DOI] [PubMed] [Google Scholar]
  • 14.Kollef KE, Schramm GE, Wills AR, Reichley RM, Micek ST, Kollef MH. Predictors of 30-day mortality and hospital costs in patients with ventilator-associated pneumonia attributed to potentially antibiotic-resistant gram-negative bacteria. Chest. 2008;134(2):281–287. doi: 10.1378/chest.08-1116. [DOI] [PubMed] [Google Scholar]
  • 15.Flayhart D, Hindler JF, Bruckner DA, Hall G, Shrestha RK, Vogel SA, Richter SS, Howard W, Walther R, Carroll KC. Multicenter evaluation of BBL CHROMagar MRSA medium for direct detection of methicillin-resistant Staphylococcus aureus from surveillance cultures of the anterior nares. J Clin Microbiol. 2005;43(11):5536–5540. doi: 10.1128/JCM.43.11.5536-5540.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Yang HY, Suh JT, Lee HJ. Evaluation of commercial selective agars in screening for methicillin-resistant Staphylococcus aureus. Ann Clin Lab Sci. 2010;40(3):252–256. [PubMed] [Google Scholar]
  • 17.Stamper PD, Shulder S, Bekalo P, Manandhar D, Ross TL, Speser S, Kingery J, Carroll KC. Evaluation of BBL CHROMagar VanRE for detection of vancomycin-resistant Enterococci in rectal swab specimens. J Clin Microbiol. 2010;48(11):4294–4297. doi: 10.1128/JCM.01522-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Saito R, Koyano S, Nagai R, Okamura N, Moriya K, Koike K. Evaluation of a chromogenic agar medium for the detection of extended-spectrum-beta-lactamase-producing Enterobacteriaceae. Lett Appl Microbiol. 2010;51(6):704–706. doi: 10.1111/j.1472-765x.2010.02945.x. [DOI] [PubMed] [Google Scholar]
  • 19.Huang TD, Bogaerts P, Berhin C, Guisset A, Glupczynski Y. Evaluation of Brilliance ESBL agar, a novel chromogenic medium for detection of extended-spectrum-beta-lactamase-producing Enterobacteriaceae. J Clin Microbiol. 2010;48(6):209–2096. doi: 10.1128/JCM.02342-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Randall LP, Kirchner M, Teale CJ, Coldham NG, Liebana E, Clifton-Hadley F. Evaluation of CHROMagar CTX, a novel medium for isolating CTX-M-ESBL-positive Enterobacteriaceae while inhibiting AmpC-producing strains. J Antimicrob Chemother. 2009;63(2):302–308. doi: 10.1093/jac/dkn485. [DOI] [PubMed] [Google Scholar]
  • 21.Panagea T, Galani I, Souli M, Adamou P, Antoniadou A, Giamarellou H. Evaluation of CHROMagar KPC for the detection of carbapenemase-producing Enterobacteriaceae in rectal surveillance cultures. Int J Antimicrob Agents. 2011;37(2):124–128. doi: 10.1016/j.ijantimicag.2010.10.010. [DOI] [PubMed] [Google Scholar]
  • 22.Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; nineteenth informational supplement. CLSI; 2009. [Google Scholar]
  • 23.Thom KA, Hsiao WW, Harris AD, Stine OC, Rasko DA, Johnson JK. Patients with Acinetobacter baumannii bloodstream infections are colonized in the gastrointestinal tract with identical strains. Am J Infect Control. 2010;38(9):751–753. doi: 10.1016/j.ajic.2010.03.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Morgan DJ, Liang SY, Smith CL, Johnson JK, Harris AD, Furuno JP, Thom KA, Snyder GM, Day HR, Perencevich EN. Frequent multidrug-resistant Acinetobacter baumannii contamination of gloves, gowns, and hands of healthcare workers. Infect Control Hosp Epidemiol. 2010;31(7):716–721. doi: 10.1086/653201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Jawad A, Hawkey PM, Heritage J, Snelling AM. Description of Leeds Acinetobacter Medium, a new selective and differential medium for isolation of clinically important Acinetobacter spp., comparison with Herellea agar and Holton’s agar. J Clin Microbiol. 1994;32(10):2353–2358. doi: 10.1128/jcm.32.10.2353-2358.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Gordon NC, Wareham DW. Evaluation of CHROMagar Acinetobacter for detection of enteric carriage of multidrug-resistant Acinetobacter baumannii in samples from critically ill patients. J Clin Microbiol. 2009;47(7):2249–2251. doi: 10.1128/JCM.00634-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Akers KS, Barsoumian A, Beckius ML, Murray CK, Mende K. CHROMagar Acinetobacter is not selective for carbapenem-resistant Acinetobacter baumannii -calcoaceticus complex. Diagn Microbiol Infect Dis. 2010;67(2):209–211. doi: 10.1016/j.diagmicrobio.2010.02.004. [DOI] [PubMed] [Google Scholar]
  • 28.Wareham DW, Gordon NC. Modifications to CHROMagar Acinetobacter for improved selective growth of multi-drug resistant Acinetobacter baumannii. J Clin Microbiol. 2011;47(7):2249–2251. doi: 10.1136/jcp.2010.083469. [DOI] [PubMed] [Google Scholar]

RESOURCES