risk factores for an outbreak of multi-drug-resistant acinetobacter.chest-1999-husni-1378-82

7/31/2019 Risk Factores for an Outbreak of Multi-drug-resistant Acinetobacter.chest-1999-Husni-1378-82

1/7

DOI 10.1378/chest.115.5.13781999;115;1378-1382Chest

S. Hall, Cynthia Fatica, James K. Stoller and Steven M. GordonRola N. Husni, Lawrence S. Goldstein, Alejandro C. Arroliga, Geraldine *Patients

Nosocomial Pneumonia Among IntubatedMulti-Drug-Resistant AcinetobacterRisk Factors for an Outbreak of

http://chestjournal.chestpubs.org/content/115/5/1378.full.html

services can be found online on the World Wide Web at:The online version of this article, along with updated information and

ISSN:0012-3692)http://chestjournal.chestpubs.org/site/misc/reprints.xhtml(

written permission of the copyright holder.this article or PDF may be reproduced or distributed without the priorDundee Road, Northbrook, IL 60062. All rights reserved. No part ofCopyright1999by the American College of Chest Physicians, 3300Physicians. It has been published monthly since 1935.

is the official journal of the American College of ChestChest

1999 American College of Chest Physiciansby Chiu Ho on May 26, 2012chestjournal.chestpubs.orgDownloaded from
http://chestjournal.chestpubs.org/content/115/5/1378.full.htmlhttp://chestjournal.chestpubs.org/content/115/5/1378.full.htmlhttp://chestjournal.chestpubs.org/content/115/5/1378.full.htmlhttp://chestjournal.chestpubs.org/site/misc/reprints.xhtmlhttp://chestjournal.chestpubs.org/site/misc/reprints.xhtmlhttp://chestjournal.chestpubs.org/http://chestjournal.chestpubs.org/http://chestjournal.chestpubs.org/http://chestjournal.chestpubs.org/http://chestjournal.chestpubs.org/site/misc/reprints.xhtmlhttp://chestjournal.chestpubs.org/content/115/5/1378.full.html


2/7

Risk Factors for an Outbreak of Multi-Drug-ResistantAcinetobacter Nosocomial Pneumonia AmongIntubated Patients*Rola N. Husni, MD; Lawrence S. Goldstein, MD;Alejandro C. Arroliga, MD, FCCP; Geraldine S. Hall, PhD; Cynthia Fatica, RN;

James K. Stoller, MD, FCCP; and Steven M. Gordon, MD

Introduction: Acinetobacter baumanii is a Gram-negative coccobacillus that is normally acommensal pathogen but can be a nosocomial pathogen. An epidemiologic study was performedto investigate an outbreak ofA baumanii that occurred in our medical intensive care unit (MICU)from March to September 1995.Methods: A case-control study was performed by retrospective chart review, comparing case patientsto randomly selected patients who were mechanically ventilated in the MICU for at least 1 weekduring the outbreak. A case patient was defined as any patient with an Acinetobacter infection in

which the epidemic strain was considered to be a pathogen. The epidemic strain was defined by itsantibiogram. Case patients and control patients were compared for age, gender, underlying disease,acute physiology and chronic health evaluation III score, length of MICU stay, prior antibiotic use,presence of fever, sepsis, type of pulmonary infiltrate, and outcome. Environmental and hand-

washing studies also were performed during the period of the outbreak. Molecular typing wasperformed on available bloodstream isolates.Results: There were 15 cases ofA baumanii nosocomial pneumonia. Fifty percent were bacteremic;one chart was unavailable for review. Twenty-nine patients were identified as control patients. Themean age for case patients was 50 (range, 21 to 84). The mean duration of time from admission to theICU to infection was 12.8 days (range, 4 to 40). Sepsis developed in 35% of the case patients.Forty-three percent of the case patients died during their hospitalization, with two of those deathsattributed to Acinetobacter infection. Univariate analysis showed that prior use of ceftazidime wasassociated with infection with Acinetobacter (11/14 case patients compared to 11/29 control patients;p< 0.01). Pulsed-field gel electrophoresis revealed two strains to be responsible for the outbreak.Hand washing was performed before patient contact by only 10% of health-care workers, and only32% washed their hands after patient contact.Conclusion: The use of ceftazidime was associated with an increased risk of nosocomial pneumonia

with resistant strains of Acinetobacter. Health-care workers need to improve compliance withhand-washing recommendations. (CHEST 1999; 115:13781382)

Key words: Acinetobacter baumanii; nosocomial infections; pneumonia

Abbreviations: APACHE acute physiology and chronic health evaluation; MICmean inhibitory concentration;MICUmedical intensive care unit

Acinetobacter1 spp are ubiquitous, small, aerobic,Gram-negative bacilli that prefer moist environ-

ments.1 Acinetobacter spp are usually considered to

be opportunistic pathogens but have been increas-ingly reported as the cause of outbreaks of nosoco-mial pneumonia and bloodstream infections.2 These

organisms can withstand desiccation and may ac-quire resistance to many antimicrobial agents,especially -lactam antibiotics.3 We report an out-

For editorial comment see page 1226

break of nosocomial Acinetobacter spp infectionsamong patients in our MICU associated with use ofa third-generation cephalosporin.

Materials and Methods

Background

The Cleveland Clinic Foundation is a 950-bed tertiary carehospital with a 17-bed MICU. Infection control personnel noted

*From the Departments of Infectious Diseases (Drs. Husni andGordon), Pulmonary and Critical Care Medicine (Drs. Goldstein,Arroliga, and Stoller), Infection Control (Ms. Fatica), and Labo-ratory Medicine (Dr. Hall), Cleveland Clinic Foundation, Cleve-land, OH.Manuscript received March 25, 1998; accepted November 13,1998.Correspondence to: Alejandro C. Arroliga, MD, FCCP, Depart-

ment of Pulmonary and Critical Care Medicine - G62, ClevelandClinic Foundation, Cleveland, OH 44195; e-mail: [email protected]

1378 Clinical Investigations in Critical Care

http://chestjournal.chestpubs.org/http://chestjournal.chestpubs.org/http://chestjournal.chestpubs.org/http://chestjournal.chestpubs.org/


3/7

an increase in the number of nosocomial infections with Acin-etobacter baumanii in MICU patients during the spring andsummer of 1995. To identify risk factors for infection with thisorganism, a case-control study was performed.

Case Definitions

A case patient was defined as any patient in the MICUbetween March and August 1995 with a nosocomial pneumonia

and/or bloodstream infection due to a resistant A baumanii (theepidemic strain). Resistant A baumanii was defined by thefollowing antimicrobial susceptibility pattern: susceptible only toticarcillin/clavulonate (mean inhibitory concentration ([MIC], 16 g/mL) and imipenem (MIC, 4) intermediate to amika-cin (MIC, 32) and resistant to tobramycin (MIC, 8), gentami-cin (MIC, 8), ceftazidime (MIC, 16), and ciprofloxacin(MIC, 2). Acinetobacter pneumonia was defined as includingthe presence of increased respiratory secretions, new lung infil-trate identified on a chest radiograph, and a sputum culturepositive for A baumanii. Fever was defined as an oral tempera-ture of 38C, and sepsis syndrome was determined by previ-ously defined criteria.4

Control Patients

Control patients were defined as all patients mechanicallyventilated in the MICU for 1 week during the epidemicperiod.

Case Ascertainment

Infection control personnel reviewed all microbiology culturesto identify all MICU patients with A baumanii isolated fromclinical cultures. Medical records of all patients were reviewed toidentify case and control patients. Information abstracted in-cluded demographic data, clinical presentation, disease severityscore,5 underlying diseases, prior antibiotics, treatment, andoutcome.

Infection Control Practices

A review of infection control practices was performed byinfection control personnel. Cleaning and disinfecting of flexiblebronchoscopes and ventilators, including the use of disposableand reusable items, was observed. In-service education wasprovided to the physicians, nursing staff, and respiratory thera-pists in regard to A baumanii infections and body substanceisolation.6 Flexible bronchoscopes were routinely cleaned andsterilized by a trained equipment technician (Steris process;Steris Corporation; Mentor, OH). Ventilators were cleaned anddisinfected within the Department of Respiratory Therapy, andreusable items were cleaned and sterilized in the Central ServiceDepartment. All practices were in compliance with our currentpolicy and procedure.

Hand-Washing Survey

A hand-washing survey was conducted in the MICU byinfection control personnel during the outbreak period. Thissurvey consisted of six 2-h observation periods (three on the dayshift and three on the evening shift), during which all health-careproviders (physicians, nurses, and respiratory therapists) wereunaware that they were being observed regarding compliance

with hand washing and glove use as appropriate for bodysubstance isolation.

Culture and DNA Preparation for Pulsed-Field GelElectrophoresis of A baumanii Isolates

After bacterial growth of 18 to 22 h, the isolates wereinoculated into sterile saline to a density approximately equal toMcFarland number 4, sonicated, and centrifuged. The pellet wasresuspended in 1 mL of cold cell-suspension buffer (Bio-Rad;Hercules, CA). Agarose gel plugs were prepared with the soni-cated isolates and digested with SmaI, a restriction enzyme. The

digested DNA plugs were placed in wells of agarose gel molds,and electrophoresis was carried out in a contour-clamped homog-enous electric field apparatus (Gene-Path; Bio-Rad), using a No.12 program that allowed for the separation of molecular weightsof 5 to 300 kb. Gels were stained with ethidium bromide and

were photographed under ultraviolet light. The restriction pat-terns were analyzed following criteria by Tenover et al. 7 If there

were identical banding patterns, the isolates were said to beidentical; if there were one to three band differences betweenisolates, they were considered to be closely related. If theydiffered by more than three bands, they were said to beunrelated.

Data Analysis

The data was subjected to statistical analysis using (Epi-info,version 6.0; Centers for Disease Control and Prevention; Atlanta,GA). Differences between case patients and control patients

were analyzed with the 2 test and Fishers exact test (two-tailed).A p value of 0.05 was chosen to assign statistical significance.

Results

Fifteen cases of A baumanii pneumonia wereidentified in MICU patients between March andAugust 1995 that met the case definition (Fig 1).

One patient was excluded from the study becausethe chart was not available for review.

Characteristics of the Case Patients

The mean age of the case patients was 50 (range,21 to 84 years), and 79% were male (Table 1).Indications for MICU admission included respira-tory failure (eight patients), sepsis (three), cardiactamponade (one), encephalitis (one), and acidosis(one) (Table 2). Underlying chronic diseases in-cluded cirrhosis (four), collagen vascular disease(three), chronic renal failure (one), AIDS (one), andleukopenia (one). The mean acute physiology andchronic health evaluation (APACHE) III score onadmission to the MICU was 95.3. Clinical manifes-tations included fever (79%), sepsis syndrome (35%),and leukocytosis (mean WBC count, 14,634/mL;range, 700 to 26,360). All patients were intubatedand mechanically ventilated. Radiographic evidenceof pneumonia was present in all patients at the timeof the Acinetobacter infection. Lobar infiltrates oc-curred in seven patients (50%), and seven haddiffuse infiltrates. Acinetobacter was isolated from

respiratory secretions in 12 patients (79%). SevenCHEST / 115 / 5 / MAY, 1999 1379



4/7

patients had concomitant bacteremias, accountingfor 15% of all bacteremias in the MICU during thestudy period.

The mean interval from admission to the MICU to

the first respiratory culture for Acinetobacter was12.8 days (range, 4 to 40 days). All case patients wereon antimicrobial agents at the time the Acinetobacterinfections were identified. The most common anti-microbials that patients received at the time ofAcinetobacter infections were vancomycin (100%),ceftazidime (78%), and ciprofloxacin (50%). Antimi-crobial treatment for Acinetobacter infections in-cluded administration of ticarcillin/clavulonate(64%), imipenem (21%), and a combination of both(15%). Amikacin was used in three patients. Themean duration of antimicrobial therapy for Acineto-

bacter infections was 26 days (range, 2 to 71 days).Nine patients (64%) were successfully treated forAcinetobacter infections, while three patients failedtherapy and two were lost to follow-up. Six patients(43%) died during their hospital admissions. In twopatients the death was directly attributed to Acineto-bacter sepsis, and in two other patients Acineto-bacter infection contributed to death.

Case-Control Study

Twenty-nine patients who underwent mechanicalventilation for at least 7 days without developing A

baumanii infection or colonization were included inthe case-control study. The mean age of controlpatients was 60 years, and 41% were male. Indica-tions for MICU admission were acute respiratoryfailure (20 patients), sepsis (4), cardiac disease (2),gastrointestinal disorders (2), and acidosis (1). Themean APACHE III score on admission to the MICUwas 92.4. Twenty-two patients (76%) received van-comycin and 11 (37%) received ceftazidime duringtheir MICU admissions. The only significant riskfactor associated with Acinetobacter infection wasprior use of ceftazidime (11/14 case patients vs 11/29control patients; p 0.01; odds ratio, 6; 95% confi-dence intervals, 1.1 to 35; Table 1). There were nosignificant differences between case patients andcontrol patients in age, gender, indications forMICU admission, underlying diseases, use of otherantimicrobials, or the presence of sepsis syndrome.

Hand-Washing SurveyHand washing was practiced before patient con-

tact in only 10% of the 111 physicians, nurses, andrespiratory therapists observed. After patient con-tact, the rate of hand washing was 32%. Donning ofgloves was practiced by all respiratory therapists, butonly 13 (72%) removed their gloves immediatelyafter completing the patient encounter.

Pulsed-Field Gel Electrophoresis Assay

Of the four A baumanii isolates (all in the blood-

stream) available for pulsed-field gel electrophoresis,two distinct banding patterns were identified.

Discussion

Our study found an association between the prioradministration of ceftazidime and the subsequentdevelopment of A baumanii infections. This findingis in agreement with an earlier study by Mulin et al8

that associated the use of third-generation cephalo-sporins with colonization and infection by A bauma-nii. Other studies have noted an association betweenother antibiotic classes and Acinetobacter infection.One study, interestingly, found an association be-tween the use of cefazolin and Acinetobacter infec-tion but not with higher generation cephalosporins.9

Recently, in a report of three case-control studies ona retrospective cohort study, it was found that epi-demic infections may coexist with endemic infectionsof A baumanii.10 Previous use of a fluoroquinoloneantibiotic (perfloxacin, ofloxacin, norfloxacin, or cip-rofloxacin) was a risk factor found for the develop-ment of endemic A baumanii infection. Other risk

factors for the development of nosocomial Acineto-

Figure 1. Epidemic curve of patients with A baumanii pneu-monia in an MICU, Cleveland Clinic Foundation, 1995.

Table 1Characteristics of Case and Control Patients

Case Patients(n 14)

Control Patients(n 29)

pValue

Mean age, yr 50 60 0.4Men 11 (79%) 12 (41%) 0.05APACHE III score 95.3 92.4 0.79Admitted for acute

respiratory failure8 (57%) 20 (68%) 0.5

Vancomycin received 14 (100%) 22 (76%) 0.08Ceftazidime received 11 (78%) 11 (37%) 0.01Died 6 (43%) 11 (32%) 0.9




5/7

bacter pneumonia in intubated patients includedrecent neurosurgery, head trauma, large aspiration,and ARDS. A case-control study by Baraibar et al11

examined patients who developed A baumanii infec-tions and compared the infections to other etiologiesof ventilator-associated pneumonia; the study couldnot detect risk factors common to both groups. Thatpatient population differed from ours in that theICUs were combined medical-surgical units, with 10of 12 patients being admitted post-trauma or post-operatively. Seventy-seven percent of patients in theBaraibar study had been on antibiotics in the 10 dayspreceding the development of ventilator-associatedpneumonia.

Lortholary et al12 noted that 32 of 40 patients(75%) in an ICU who were colonized or infectedwith Acinetobacter had previously taken antimicro-bials, although in their experience only previousinfection and high severity of illness were statisticallysignificant risk factors for Acinetobacter infection.Because of the difficulty in identifying a specificcause of infection in this patient population, thechoice of antimicrobials is often empiric. At the timeof the outbreak, ceftazidime and ticarcillin/clavulanicacid were the antimicrobials most commonly usedfor empiric Gram-negative rod coverage in ourMICU. This was the most common indication forcase patients to receive ceftazidime. In our study, allof the case patients and most of the control patients(76%) had received vancomycin for empiric Gram-positive bacteria coverage. The p value for thiscomparison was not significant, and it is doubtfulthat the prior use of vancomycin plays any role in the

development of Acinetobacter infection. Our studydid not confirm the findings of Lortholary et al12 thata high disease-severity score was a risk factor forAcinetobacter infection.

Because Acinetobacter resistance is acquiredrather than inherent, prior exposure to antibioticsplays a role in the subsequent acquisition of resistantAcinetobacter.2 All strains of Acinetobacter identi-fied in our epidemic were susceptible to imipenem,which is consistent with prior reports that show rarebut increasing resistance to carbapenams.13 In con-trast, Marques et al14 found that 70% of isolates ofAcinetobacter were resistant to at least two extend-ed-spectrum penicillins and two aminoglycosides butthat imipenem and an aminoglycoside resulted in atleast partial synergy in all of the highly resistantisolates. Unfortunately, detailed descriptions of imi-penem-resistant outbreaks are unavailable. How-ever, the account of one outbreak in New York notedthat the epidemic of imipenem-resistant Acineto-bacter occurred after imipenem had been heavilyprescribed for an outbreak of ceftazidime-resistantAcinetobacter.15

Single-strained nosocomial outbreaks may originatefrom a common environmental source. We cannot ruleout transmission from patient to patient via the handsof health-care workers, especially in light of the hand-washing survey that documented poor adherence to thehand-washing policy by health-care workers before andafter patient contact. However, we did not identify areservoir for Acinetobacter in the MICU, and molec-ular typing suggested that at least two epidemic strainswere present during the outbreak. The availability of

Table 2Characteristics of Case Patients

PatientNo.

Age,yr

Days IntubatedBefore Infection Underlying Disease Prior Use of Antibiotics* Outcome

1 22 24 Pneumonia, respiratory failure A,C,Ci,G,I,M,V,T,Ak,T/S Survived2 74 9 Renal failure, pancytopenia C,Ci,V Survived3 43 40 ARDS, respiratory failure A,C,Ci,E,G,T/S,V Survived4 33 12 Respiratory failure, pulmonary hemosiderosis V,T,To,C Survived5 45 9 Respiratory failure, colon carcinoma E,Cef,A,G,M,T,V Survived

6 62 4 Sepsis, cirrhosis C,V,Ci Survived7 62 8 Sepsis, cirrhosis V,C,To Died8 53 14 Sepsis, cirrhosis, renal failure C,Ci,V Died9 39 15 Respiratory failure, pneumonia, encephalitis A,C,Cef,Ci,V,Cl Survived

10 65 10 Cirrhosis, chronic renal failure, acidosis V,G Survived11 67 11 Alveolar hemorrhage, collagen vascular disease,

respiratory failureV,T,E,C Died

12 84 7 Collagen vascular disease, Pneumocystis cariniipneumonia, respiratory failure

C,E,V,T/S Died

13 37 9 Cardiac tamponade, collagen vascular disease C,V Died14 20 8 AIDS, Pneumocystis carinii pneumonia,

respiratory failure, sepsis syndromeT/S,V,Ci,To Died

*A ampicillin; Ak amikacin; c ceftazidime; cef ceftizoxime or cefuroxime; Ci ciprofloxacin; E erythromycin; G gentamicin;I imipenem; M metronidazole; T ticarcillin/clavulanic acid; To tobramycin; T/S trimethoprim/sulfamethoxazole; V vancomycin.

CHEST / 115 / 5 / MAY, 1999 1381



6/7

only four bacteria for molecular typing is a limitation ofour study and leaves open the possibility that morestrains were responsible for the outbreak, but it doesnot invalidate the finding that some of the outbreaks ofAcinetobacter infections may be caused by severalstrains.10

Our study identified prior use of ceftazidime as arisk factor for acquiring an infection with a resistantAcinetobacter sp. The use of ceftazidime as a first-line antibiotic in treating nosocomial infections hasincreased over the past years because of the in-creased incidence of resistant organisms like Pseudo-monas spp. Now, it seems that ceftazidime has beenoverused, selecting out even more resistant Gram-negative bacteria. Therefore, the empiric use ofthese agents should be reserved for instances wherethere is a high probability of Pseudomonas aerugi-nosa infections. Another goal we recommend isbetter attention to good hand-washing practicesamong health-care workers.

References

1 Gerner-Smidt P. Taxonomy and epidemiology of Acineto-bacter infections. Rev Med Microbiol 1995; 6:186195

2 Towner KJ. Clinical importance and antibiotic resistance ofAcinetobacter spp. J Med Microbiol 1997; 46:721746

3 Bergogne-Berezin E, Decre D, Joly-Guillou ML. Opportu-nistic nosocomial multiply resistant bacterial infections: theirtreatment and prevention. J Antimicrob Chemother 1993;32(suppl A):3947

4 Bone RC, Fisher CJ Jr, Clemmer TP, et al. Sepsis syndrome:a valid clinical entity. Methylprednisolone severe sepsis study

group. Crit Care Med 1989; 17:389393

5 Knaus WA, Wagner DP, Draper EA, et al. The APACHE IIIprognostic system: risk prediction of hospital mortality incritically ill hospitalized patients. Chest 1991; 100:16191636

6 Lynch P, Jackson MM, Cummings J, et al. Rethinking the roleof isolation practices in prevention of nosocomial infections.Ann Intern Med 1987; 107:243246

7 Tenover FC, Arbeit RD, Goering RV, et al. Interpretingchromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing.

J Clin Microbiol 1995; 33:223322398 Mulin B, Talon D, Viel JF, et al. Risk factors for nosocomial

colonization with multiresistant Acinetobacter baumanii. EurJ Clin Microbiol Infect Dis 1995; 14:569576

9 Beck-Sague CM, Sinkowitz RL, Chinn RY, et al. Risk factorsfor ventilator-associated pneumonia in surgical intensive careunit patients. Infect Control Hosp Epidemiol 1996; 17:374376

10 Villers D, Espaze E, Coste-Burel M, et al. NosocomialAcinetobacter baumanii infections: microbiological and clini-cal epidemiology. Ann Intern Med 1998; 129:182189

11 Baraibar J, Correa H, Mariscal D, et al. Risk factors forinfection by Acinetobacter baumanii in intubated patients

with nosocomial pneumonia. Chest 1997; 112:1050 105412 Lortholary O, Fagon JY, Hoi AB, et al. Nosocomial acquisi-

tion of multiresistant Acinetobacter baumanii: risk factors andprognosis. Clin Infect Dis 1995; 20:790796

13 Swartz MN. Hospital-acquired infections: diseases with in-creasingly limited therapies. Proc Natl Acad Sci USA 1994;91:24202427

14 Marques MB, Brookings ES, Moser SA, et al. Comparative invitro antimicrobial susceptibilities of nosocomial isolates ofAcinetobacter baumanii and synergistic activities of nineantimicrobial combinations. Antimicrob Agents Chemother1997; 41:881885

15 Urban C, Go E, Mariano N, et al. Effect of sulbactam oninfections caused by imipenem-resistant Acinetobactercalcoaceticus biotype anitratus. J Infect Dis 1993; 167:

448451




7/7

DOI 10.1378/chest.115.5.1378

1999;115; 1378-1382ChestHall, Cynthia Fatica, James K. Stoller and Steven M. Gordon

Rola N. Husni, Lawrence S. Goldstein, Alejandro C. Arroliga, Geraldine S.

*Nosocomial Pneumonia Among Intubated PatientsRisk Factors for an Outbreak of Multi-Drug-Resistant Acinetobacter

May 26, 2012This information is current as of

http://chestjournal.chestpubs.org/content/115/5/1378.full.htmlUpdated Information and services can be found at:

Updated Information & Services

http://chestjournal.chestpubs.org/content/115/5/1378.full.html#ref-list-1This article cites 15 articles, 10 of which can be accessed free at:

References

http://chestjournal.chestpubs.org/content/115/5/1378.full.html#related-urls

This article has been cited by 17 HighWire-hosted articles:Cited Bys

http://www.chestpubs.org/site/misc/reprints.xhtmlfound online at:Information about reproducing this article in parts (figures, tables) or in its entirety can bePermissions & Licensing

http://www.chestpubs.org/site/misc/reprints.xhtmlInformation about ordering reprints can be found online:

Reprints

"Services" link to the right of the online article.Receive free e-mail alerts when new articles cite this article. To sign up, select the

Citation Alerts

PowerPoint slide format. See any online figure for directions.articles can be downloaded for teaching purposes inCHESTFigures that appear in

Images in PowerPoint format

http://chestjournal.chestpubs.org/content/115/5/1378.full.htmlhttp://chestjournal.chestpubs.org/content/115/5/1378.full.htmlhttp://chestjournal.chestpubs.org/content/115/5/1378.full.htmlhttp://chestjournal.chestpubs.org/content/115/5/1378.full.html#ref-list-1http://chestjournal.chestpubs.org/content/115/5/1378.full.html#ref-list-1http://chestjournal.chestpubs.org/content/115/5/1378.full.html#related-urlshttp://chestjournal.chestpubs.org/content/115/5/1378.full.html#related-urlshttp://www.chestpubs.org/site/misc/reprints.xhtmlhttp://www.chestpubs.org/site/misc/reprints.xhtmlhttp://www.chestpubs.org/site/misc/reprints.xhtmlhttp://www.chestpubs.org/site/misc/reprints.xhtmlhttp://chestjournal.chestpubs.org/http://chestjournal.chestpubs.org/http://chestjournal.chestpubs.org/http://chestjournal.chestpubs.org/http://www.chestpubs.org/site/misc/reprints.xhtmlhttp://www.chestpubs.org/site/misc/reprints.xhtmlhttp://chestjournal.chestpubs.org/content/115/5/1378.full.html#related-urlshttp://chestjournal.chestpubs.org/content/115/5/1378.full.html#ref-list-1http://chestjournal.chestpubs.org/content/115/5/1378.full.html

risk factores for an outbreak of multi-drug-resistant acinetobacter.chest-1999-husni-1378-82

Documents