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Risk factors for multidrug-resistant Pseudomonas aeruginosa acquisition. Impact of antibiotic use in a double case–control study

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Risk factors for multidrug-resistant Pseudomonas aeruginosa acquisition. Impact of antibiotic use in a double case–control study
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  See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/40769179 Risk factors for multidrug-resistantPseudomonas aeruginosa acquisition. Impact of antibiotic use in a double case–control study   Article   in  European Journal of Clinical Microbiology · March 2010 DOI: 10.1007/s10096-009-0850-1 · Source: PubMed CITATIONS 14 READS 68 12 authors , including:Milagro MonteroInstitute for Clinical Pharmacodynamics 55   PUBLICATIONS   797   CITATIONS   SEE PROFILE Maria SalaIMIM Hospital del Mar Medical Research Insti… 133   PUBLICATIONS   2,339   CITATIONS   SEE PROFILE Mauricio Orozco-LeviIMIM Hospital del Mar Medical Research Instit… 123   PUBLICATIONS   2,388   CITATIONS   SEE PROFILE Hernando KnobelConsorci MAR Parc de Salut de Barcelona 262   PUBLICATIONS   4,807   CITATIONS   SEE PROFILE All content following this page was uploaded by Francisco Álvarez-Lerma on 09 January 2017. The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the srcinal documentand are linked to publications on ResearchGate, letting you access and read them immediately.  BRIEF REPORT Risk factors for multidrug-resistant  Pseudomonas aeruginosa acquisition. Impact of antibiotic use in a doublecase  –  control study M. Montero  &  M. Sala  &  M. Riu  &  F. Belvis  &  M. Salvado  & S. Grau  &  J. P. Horcajada  &  F. Alvarez-Lerma  & R. Terradas  &  M. Orozco-Levi  &  X. Castells  &  H. Knobel Received: 25 August 2009 /Accepted: 26 November 2009 /Published online: 24 December 2009 # Springer-Verlag 2009 Multidrug-resistant strains of   Pseudomonas aeruginosa (MDRPA) have been increasing in some hospitals [1] andmay become a public health problem [2].The emergence of MDRPA has been related to exposureto antibiotics against   P. aeruginosa  [3, 4]. Most of these studies have focussed on particular environments such asthe intensive care unit (ICU) [5] or particular antibioticresistances, mainly quinolone-resistant   P. aeruginosa  andcarbapenem-resistant   P. aeruginosa  or specific infectionsites such ventilator-associated pneumonia or bacteraemia[6, 7]. Most studies have used case  –  control methodology or have investigated outbreaks, and the case  –  control studieshave usually compared susceptibility to resistant micro-organisms. This methodology may overestimate the associ-ation between the resistance-defining antibiotic or may befalsely implicated as a potential risk factor for theacquisition of this pattern of susceptibility [8, 9]. The aim of this study was to assess the factors related toMDRPA acquisition, especially previous antibiotic expo-sure, using a double case  –  control methodology [10],analysing all types of infections and all hospital wardsduring a long period of follow-up.We conducted a double case  –  control epidemiologicalstudy, exploring the risk factors (host characteristics,invasive procedures and, especially, previous antibioticexposure) associated with the acquisition of MDRPA inhospitalised patients from 1 January 2001 to 31 December 2006 in a University Hospital with 450 beds.  P. aeruginosa was isolated and identified by the microbiology laboratory by means of routine techniques. The susceptibility of  M. Montero ( * ) :  J. P. Horcajada :  H. KnobelDept. of Internal Medicine and Infectious Diseases,Hospital del Mar, Autonomous University of Barcelona,Passeig Marítim 25  –  29,08003 Barcelona, Spaine-mail: 95422@imas.imim.esM. Sala : M. Riu : F. Belvis : R. Terradas : X. CastellsHealth Services Evaluation and Clinical Epidemiology Service,IMIM  —  Hospital del Mar, CIBER de Epidemiología y SaludPública (CIBERESP),Barcelona, SpainM. SalvadoMicrobiology Department,Laboratorio de Referencia de Catalunya,Barcelona, SpainS. GrauPharmacy Department, Hospital del Mar,Barcelona, SpainF. Alvarez-LermaIntensive Care Unit, Hospital del Mar,Barcelona, SpainM. Orozco-LeviRespiratory Department, Hospital del Mar,Barcelona, SpainM. Orozco-LeviExperimental Sciences and Health Department (CEXS),Pompeu Fabra University,Barcelona, SpainM. Orozco-LeviGroup of Research in Injury Immune Response and LungFunction, Municipal Institute of Medical Research (IMIM),Barcelona, SpainEur J Clin Microbiol Infect Dis (2010) 29:335  –  339DOI 10.1007/s10096-009-0850-1  isolates was determined by the MicroScan system (NC36and NC38 panels) or the Kirby  –  Bauer method on Mueller   –  Hinton plates (bioMérieux, Marcy l ’ Etoile, France).Case definition: patients with MDRPA, when themicroorganism was resistant to all agents except colistin and/or amikacin. Control 1: patients withsusceptible  P. aeruginosa  (SPA), when the microorgan-ism was susceptible to all of the agents studied; andcontrol 2: patients randomly selected among thoseadmitted to the hospital during the same period with no positive cultures for   P. aeruginosa  and with a similar length of stay and severity index score to those with a positive culture for   P. aeruginosa .A bivariate analysis was performed to compare thecharacteristics of MDRPA patients with those of SPA andnon-  P. aeruginosa  controls.  P  -values were calculatedusing the Chi-square test for categorical variables andthe Mann  –  Whitney test for continuous variables. Predic-tors of nosocomial acquisition of MDRPA were assessedusing logistic regression models. Two models wereconstructed, one using SPA as controls and another using patients without   P. aeruginosa  isolations as controls.Variables with a  P  -value<0.05 in the bivariate analysiswere included in the logistic regression model. Statisticalanalyses were run using SPSS for Windows, rel. 12.0.0(SPSS Inc., Chicago, Illinois).During the study period, 1,403 incident   P. aeruginosa isolates were identified in hospitalised patients; SPA: 532(37.9%), MDRPA: 345 (24.6%) and  P. aeruginosa  withother susceptibility pattern 526 (37.5%). For study pur- poses, only the SPA and MDRPA patients and 690 patientswithout   P. aeruginosa  were included. The most commonsite of   P. aeruginosa  isolation was the respiratory tract (44.5%), followed by skin and soft tissue (21.6%), and theurinary tract (19.3%). The primary site of isolation was blood in only 3.9% of the study patients.Table 1 shows the clinical and epidemiological charac-teristics of the cases and controls. In the univariate analysis,the most relevant data were that no statistically significant differences were found in the prevalence of most co-morbidities, except for that of chronic obstructive pulmo-nary disease (COPD), which was highest in MDRPA.Mechanical ventilation, haemodialysis and bronchoscopywere more frequent in MDRPA than in SPA or control patients. Previous antibiotic therapy was significantlyassociated with a resistance pattern. The multivariatelogistic regression analysis comparing controls without   P.aeruginosa  isolation with MDRPA showed that adjustedfactors associated with an increased risk of MDRPA weremale sex, more than three previous hospitalisations,simultaneous MDRPA isolates in the hospital, COPD,severity of illness, previous use of quinolones andcarbapenems. When comparing MDRPA isolation versusSPA, the odds ratio (OR) for quinolones was much higher than that observed in the previous model, the OR for carbapenems was similar to that in the previous model andanti-  P. aeruginosa  penicillins were also a risk factor for MDRPA, while COPD disappeared (Table 2).Several risk factors have been previously described to beassociated to MDRPA acquisition, such as ICU stay,mechanical ventilation, higher severity index score, previ-ous hospitalisations and co-morbidities (diabetes mellitus,renal failure, COPD and cystic fibrosis) [5, 6, 11]. In our  study, only COPD, higher severity index score and previoushospitalisations were found to be a risk factor for MDRPA;these differences could be explained by the diverse settingsin which the studies have been carried out.The number of simultaneous detections of MDRPA,considered as a surrogate of colonisation pressure, emergedas a consistent independent factor associated with MDRPA;the role of colonisation pressure in the transmission of multidrug-resistant Gram-negative bacteria has not beenwell established [12]One of the main concerns in the acquisition of resistanceis previous antibiotic exposure. Our study shows that exposure to quinolones and carbapenems was associatedwith MDRPA acquisition in the adjusted analysis using thetwo control groups of patients. Several studies havereported that the emergence of MDRPA occurs after exposure to anti-pseudomonal antibiotics [5, 6]. Another  study performed in critically ill patients with activesurveillance to detect the colonisation of   P. aeruginosa found that quinolones and anti-pseudomonal cephalospor-ins could prevent the acquisition of   P. aeruginosa  and that the use of these agents was not associated with theacquisition of resistance [13].Most of the studies evaluating the risk of MDRPAacquisition have used the case  –  control methodology andhave compared patients with resistant versus susceptiblestrains [14]. Selection of patients with susceptible organ-isms as controls overestimates the contribution of theresistance-defining antibiotic in the development of resis-tance [9, 10, 14]. This effect was also observed in the  present study: when MDRPA were compared with suscep-tible  P. aeruginosa , the adjusted ORs of MDRPA for exposure to quinolones and carbapenems were 15.3 and3.5, respectively, and when MDRPA were compared with acontrol group without   P. aeruginosa  infection, the adjustedORs were 1.8 and 2.3, respectively.The present study has some limitations. First, the patient information was obtained retrospectively. The patientswithout   P. aeruginosa  were randomly selected from thesame population as case patients and had similar length of stay and severity index score to those with MDRPA; asactive surveillance was not carried out, we cannot ascertainthat a proportion of control patients could be colonised by 336 Eur J Clin Microbiol Infect Dis (2010) 29:335  –  339  Table 1  Clinical characteristics of the patients included in the study Non-PA,  n =690 (44%) SPA,  n =532 (34%) MDRPA,  n =345 (22%)  P  -value 1  P  -value 2 DemographicsSexMale 375 (54.3) 316 (59.4) 250 (72.5) <0.001 <0.001Female 315 (45.7) 216 (40.6) 95 (27.5)Age (years)Mean (SD) 67.5 (16.8) 69.1 (16.6) 67.8 (13.5) ns 0.011Related to hospitalisationPrevious hospitalisation None 358 (51.9) 283 (53.2) 119 (34.5) <0.001 <0.0011 151 (21.9) 112 (21.1) 59 (17.1)2 88 (12.8) 54 (10.2) 54 (15.7) ≥ 3 93 (13.5) 83 (15.6) 113 (32.8)Previous ICU stay 3 57 (8.4) 77 (14.8) 83 (24.3) <0.001 <0.001Length of hospital stay (days) 27.1 (15.4) 26.7 (20.9) 43.5 (31.7) <0.001 <0.001Days between admission and isolation  − −  13.1 (11.0) 22.9 (18.9)  −  <0.001Simultaneous MDRPA isolation 2.6 (2.2) 2.6 (2.3) 3.5 (2.1) <0.001 <0.001ComorbiditiesDiabetes 129 (18.7) 86 (16.2) 61 (17.7) ns nsCOPD 116 (16.8) 126 (23.7) 118 (34.2) <0.001 0.001Renal disease 69 (10.0) 54 (10.2) 40 (11.6) ns nsLiver disease 92 (13.3) 36 (6.8) 37 (10.7) ns nsHIV 33 (4.8) 16 (3.0) 12 (3.5) ns nsSolid neoplasia 179 (25.9) 132 (24.8) 68 (19.7) ns nsHaematologic neoplasia 23 (3.3) 18 (3.4) 11 (3.2) ns nsInvasive proceduresMechanical ventilation 32 (4.6) 52 (9.8) 69 (20.0) <0.001 <0.001Haemodialysis 17 (2.5) 7 (1.3) 17 (4.9) 0.036 0.001Bronchoscopy 44 (6.4) 46 (8.6) 44 (12.8) 0.001 0.050Digestive endoscopy 80 (11.6) 37 (7.0) 27 (7.8) ns nsChemotherapy 19 (2.8) 8 (1.5) 7 (2.0) ns nsSurgery 345 (50.0) 276 (51.9) 180 (52.2) ns nsSeverityMean 2.6 (0.68) 2.8 (0.9) 3.1 (1.0) <0.001 <0.0011  –  3 612 (88.7) 393 (74.4) 193 (56.4) <0.001 <0.0014 78 (11.3) 135 (25.6) 149 (43.6)Previous antibiotic therapy No therapy 191 (27.7) 229 (43.0) 55 (15.9)Anti-  P. aeruginosa  drugs 240 (34.8) 60 (11.3) 209 (60.6) <0.001 <0.001 Non-PA = non-  Pseudomonas aeruginosa ; SPA = susceptible  P. aeruginosa ; MDRPA = multidrug-resistant   P. aeruginosa Data are counts (%) or means (standard deviation, SD) 1 Comparison between non-PA and MDRPA. The Chi-square test was used for categorical variables and the Mann  –  Whitney test for continuousvariables 2 Comparison between SPA and MDRPA. The Chi-square test was used for categorical variables and the Mann-Whitney test for continuousvariables 3 Twenty-six missing cases (12 control, 10 SPA, 4 MDRPA) 4 3M ™ APR DRG (All-Patient Refined Diagnosis-Related Group)Eur J Clin Microbiol Infect Dis (2010) 29:335  –  339 337  MDRPA. The selection of the control groups is controver-sial; using patients without   P. aeruginosa  cannot differen-tiate what is a risk for MDRPA from what is a risk from  P.aeruginosa , regardless of the susceptible profile. In thesecond model, we used patients with fully susceptible  P.aeruginosa , because patients with many other non-MDRPA profiles is a very heterogeneous group. When a multivariateanalysis including this group of patients was done,compared to the model with fully susceptible  P. aeruginosa ,the only risk factor that disappeared was the severity indexscore. The results may have been influenced by localepidemiological variables, such as possible environmentalcontamination with MDRPA, which is not applicable toother settings. In contrast, few studies have analysed therisk factors of resistance over such a long period, with alarge number of patients with MDRPA and in a singlehospital, including all hospital wards with a double case  –  control design. In conclusion, the present study suggeststhat, although many factors play a role in the acquisition of MDRPA, previous antibiotic exposure with quinolones and Table 2  Multivariate analysis of risk factors for the isolation of multidrug-resistant   P. aeruginosa Factor Non-PA vs. MDRPA 1 SPA vs. MDRPA 2 Crude OR   P  -value Adjusted OR (95% CI)  P  -value Crude OR   P  -value Adjusted OR (95% CI)  P  -valueSexFemale Ref.  – – – – – – – –  Male 2.21 <0.001 1.67 0.004 1.80 <0.001 1.61 0.016PreviousHospitalization<0.001 <0.001 <0.001 <0.001 None Ref.  – – – – – – – –  1 1.18 0.386 1.30 0.226 1.25 0.246 1.57 0.0652 1.85 0.002 2.15 0.001 2.38 <0.001 2.86 <0.001 Q 3 3.66 <0.001 3.52 <0.001 3.24 <0.001 2.87 <0.001SimultaneousMDRPA isolation0 Ref.  – – – – – – – –  Q 1 3.38 <0.001 3.47 <0.001 4.35 <0.001 3.91 <0.001Severity Index1  –  3 Ref.  – – – – – – – –  4 6.06 <0.001 4.29 <0.001 2.25 <0.001 1.63 0.020Quinolones No Ref.  – – – – – – – –  Yes 2.21 <0.001 1.79 0.001 16.66 <0.001 15.25 <0.001Carbapenems No Ref.  – – – – – – – –  Yes 4.14 <0.001 2.26 0.002 6.87 <0.001 3.53 <0.001Anti-PA Penicillins No Ref.  – – – – – – – –  Yes 2.60 <0.001 1.09 0.816 5.52 <0.001 2.79 0.035COPD No Ref.  – – – – – – – –  Yes 2.57 <0.001 2.02 <0.001 1.68 0.001 1.29 0.226MDRPA = multidrug-resistant   P. aeruginosa ; non-PA = no positive culture for   P. aeruginosa , control 1; SPA sensible  P. aeruginosa , control 2 1 Model adjusted by variables in the table, previous ICU stay, period, solid neoplasm, mechanical ventilation, haemodialysis, bronchoscopy and previous antibiotic therapy with cephalosporins and aminoglycosides. Monobactams and polymyxins, although significant at univariate analysis,were not included in the model because of sparse distribution data. Only significant factors at   P   < 0.05 are shown (except previous treatment withanti-PA penicillins) 2 Model adjusted by variables in the table, previous ICU stay, period, liver disease, mechanical ventilation and previous antibiotic therapy withcephalosporins and aminoglycosides. Haemodialysis, monobactams and polymyxins, although significant at univariate analysis, were not includedin the model because of sparse distribution data. Only significant factors at   P   < 0.05 are shown (except COPD)338 Eur J Clin Microbiol Infect Dis (2010) 29:335  –  339
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