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Epidemiology and Surveillance

Emergence of Imipenem-Resistant Gram-Negative Bacilli in Intestinal Flora of Intensive Care Patients

Laurence Armand-Lefèvre, Cécile Angebault, François Barbier, Emilie Hamelet, Gilles Defrance, Etienne Ruppé, Régis Bronchard, Raphaël Lepeule, Jean-Christophe Lucet, Assiya El Mniai, Michel Wolff, Philippe Montravers, Patrick Plésiat, Antoine Andremont
Laurence Armand-Lefèvre
aFrench National Reference Center for Bacterial Resistance in Commensal Flora, Laboratory of Bacteriology, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
bEA 3964, Denis Diderot University, Paris, France
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Cécile Angebault
aFrench National Reference Center for Bacterial Resistance in Commensal Flora, Laboratory of Bacteriology, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
bEA 3964, Denis Diderot University, Paris, France
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François Barbier
bEA 3964, Denis Diderot University, Paris, France
cMedical Intensive Care Unit, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Emilie Hamelet
aFrench National Reference Center for Bacterial Resistance in Commensal Flora, Laboratory of Bacteriology, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Gilles Defrance
aFrench National Reference Center for Bacterial Resistance in Commensal Flora, Laboratory of Bacteriology, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Etienne Ruppé
aFrench National Reference Center for Bacterial Resistance in Commensal Flora, Laboratory of Bacteriology, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
bEA 3964, Denis Diderot University, Paris, France
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Régis Bronchard
dSurgical Intensive Care Unit, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Raphaël Lepeule
bEA 3964, Denis Diderot University, Paris, France
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Jean-Christophe Lucet
eInfection Control Unit, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Assiya El Mniai
aFrench National Reference Center for Bacterial Resistance in Commensal Flora, Laboratory of Bacteriology, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Michel Wolff
cMedical Intensive Care Unit, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Philippe Montravers
dSurgical Intensive Care Unit, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Patrick Plésiat
fFrench National Reference Center for Pseudomonas Resistance, Jean Minjoz Hospital, EA 3186, Besançon, France
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Antoine Andremont
aFrench National Reference Center for Bacterial Resistance in Commensal Flora, Laboratory of Bacteriology, Bichat-Claude Bernard Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
bEA 3964, Denis Diderot University, Paris, France
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DOI: 10.1128/AAC.01823-12
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    Fig 1

    Rates of intestinal colonization by imipenem-resistant gram-negative bacilli in intensive care patients. Bars indicate observed rates ± standard deviation (SD) (error bars).

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    Fig 2

    Dendrogram and rep-PCR fingerprints of Pseudomonas aeruginosa (a), Stenotrophomonas maltophilia (b), Klebsiella pneumoniae (c), and Acinetobacter baumannii (d).

Tables

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  • Table 1

    Mechanisms of resistance and MICs for imipenem and ertapenem of 56 isolated imipenem-resistant Gram-negative bacilli

    SpeciesNo. of strainsResistance mechanismsaMIC (mg/liter)b
    EnzymesOtherImipenemErtapenem
    P. aeruginosa19OprD−6–>32ND
    6AmpC++OprD−16–>32ND
    4OprD− MexAB efflux ++24–>32ND
    2AmpC++OprD− MexAB efflux ++24–32ND
    1GES-9OprD−>32ND
    4VIM-2>32ND
    Enterobacteriaceae
        K. pneumoniae2DHA-1OMP−24–32>32
    1TEM-1 CTX-M15NP3>32
        E. aerogenes1TEM-24 AmpC++OMP−16>32
        E. cloacae1SHV-12 AmpC++OMP−32>32
        H. alvei1AmpC++NP432
    A. baumannii26–12ND
    S. maltophilia12Wild typeNDND
    • ↵a OprD−, loss of OprD porin; AmpC++, hyperexpression of AmpC chromosomal cephalosporinase; MexAB efflux ++, hyperexpression of MexAB-OprM system efflux; OMP−, loss or reduced expression of outer membrane protein; NP, OMP analysis not performed.

    • ↵b ND, not determined.

  • Table 2

    Univariate and multivariate analysis of risk factors associated with intestinal colonization of imipenem-resistant Gram-negative bacillia

    Characteristic or outcomeNo. of individuals or parameter value (%, unless range is specified)Univariate ORbUnivariate PcMultivariate ORd
    Carrier patients (n = 36)Controls (n = 36)
    Sociodemographic characteristics
        Age, yr [avg (range)]58.3 (30–86)59.9 (37–86)0.57
        Sex ratio (F/M)e0.330.640.31
    Characteristics at admission
        Type of ICU1.00
            Surgical14 (38.9)14 (38.9)1.0
            Medical22 (61.1)22 (61.1)1.0 (0.3–2.9)
        Origin0.69
            Home8 (22.2)10 (27.8)1.0
            Hospital27 (75.0)24 (66.7)1.4 (0.4–4.8)
            Other1 (2.8)2 (5.6)0.6 (0.1–14.4)
        Cancer2 (5.6)2 (5.6)1.0 (0.1–14.5)1.00
        HIV3 (8.3)4 (11.1)0.7 (0.1–4.7)1.00
        Respiratory failure7 (19.4)3 (8.3)2.6 (0.5–17.2)0.31
        Renal failure6 (16.7)1 (2.8)6.8 (0.8–330.4)0.11
        Cardiac failure3 (8.3)4 (11.1)0.7 (0.1–4.7)1.00
        Obesity6 (16.7)6 (16.7)1.0 (0.2–4.2)1.00
        Pulmonary transplantation3 (8.3)2 (5.6)1.5 (0.2–19.5)1.00
        Diabetes mellitus4 (11.1)5 (13.9)0.8 (0.1–4.0)1.00
        Cirrhosis2 (5.6)2 (5.6)1.0 (0.1–14.5)1.00
        McCabe scores0.07
            07 (19.4)15 (41.7)1.0
            ≥129 (80.6)21 (58.3)2.9 (0.9–10.0)
        SAPS II [median (range)]48.5 (13–120)41 (13–104)0.36
    ESBL carriage8 (22.2)6 (16.7)1.4 (0.4–5.7)0.77
    Surveillance period,f days [median (range)]13.5 (3–52)12.5 (3–52)0.97
    Antibiotic treatments
        Exposure time to antibiotics, days [median (range)]11.5 (0–51)9.0 (0–37)0.84
        Penicillin exposure8 (22.2)16 (44.4)0.4 (0.1–1.1)0.080.3 (0.1–0.8)
        Penicillin and β-lactamase inhibitor exposure17 (47.2)20 (55.6)0.7 (0.3–2.0)0.64
        Cephalosporin exposure20 (55.6)17 (47.2)1.4 (0.5–3.9)0.64
        Imipenem exposure28 (77.8)14 (38.9)5.4 (1.8–17.8)<0.01
        Days of imipenem exposure<0.01
            08 (22.2)22 (61.1)1.01.0
            1 to 310 (27.8)6 (16.7)4.4 (1.1–20.5)5.9 (1.5–25.7)
            4 to 2118 (50.0)8 (22.2)6.0 (1.7–23.3)7.8 (2.4–29.8)
        Fluoroquinolone exposure9 (25.0)8 (22.2)1.2 (0.3–4.0)1.00
        Aminoglycoside exposure25 (69.4)21 (58.3)1.6 (0.6–4.8)0.46
        Glycopeptide exposure20 (55.6)11 (30.6)2.8 (1.0–8.4)0.06
        Metronidazole exposure5 (13.9)6 (16.7)0.8 (0.2–3.6)1.00
        Macrolide exposure5 (13.9)3 (8.3)1.8 (0.3–12.3)0.71
        Colistin exposure5 (13.9)2 (5.6)2.7 (0.4–30.4)0.43
    Outcome
        ICU stay, days [median (range)]33.5 (4–173)15.5 (5–137)0.14
        Death13 (36.1)11 (30.6)1.3 (0.4–3.9)0.80
    • ↵a Imipenem-resistant Gram-negative bacilli including Pseudomonas aeruginosa, Stenotrophomonas maltophilia, Enterobacteriaceae, and Acinetobacter baumannii.

    • ↵b Odds ratios (ORs) are given with the 95% confidence intervals in parentheses.

    • ↵c Bivariate analysis was performed using Pearson's chi-squared, Fisher's exact, Wilcoxon, or Welch test (α = 0.05).

    • ↵d Variables with univariate P value of <0.15 were included for multivariate analysis, which was performed using descending stepwise logistic regression.

    • ↵e F, female; M, male.

    • ↵f Period of surveillance, period between admission and acquisition of imipenem-resistant Gram-negative bacilli.

  • Table 3

    Univariate and multivariate analysis of risk factors associated with intestinal colonization of imipenem-resistant Pseudomonas aeruginosa

    Characteristic or outcomeNo. of individuals or parameter value (%, unless range is specified)Univariate ORaUnivariate PbMultivariate ORc
    Carrier patients (n = 22 (%)Controls (n = 22)
    Sociodemographic characteristics
        Age, yr [avg (range)]57.3 (30–74)60.9 (37–80)0.28
        Sex ratio (F/M)d0.570.290.31
    Characteristics at admission
        Type of ICU1.00
            Surgical8 (36.4)8 (36.4)1.0
            Medical14 (63.6)14 (63.6)1.0 (0.2–4.1)
        Origin1.00
            Home6 (27.3)5 (22.7)1.0
            Hospital16 (72.7)17 (77.3)0.8 (0.2–3.8)
            Other
        Cancer1 (4.5)2 (9.1)0.5 (0.1–10.0)1.00
        HIV3 (13.6)1 (4.5)3.2 (0.2–182.0)0.61
        Respiratory failure5 (22.7)2 (9.1)2.9 (0.4–33.8)0.41
        Renal failure3 (13.6)1 (4.5)3.2 (0.2–182.0)0.61
        Cardiac failure2 (9.1)3 (13.6)0.6 (0.1–6.2)1.00
        Obesity4 (18.2)5 (22.7)0.8 (0.1–4.2)1.00
        Pulmonary transplantation
        Diabetes mellitus2 (9.1)4 (18.2)0.5 (0.1–3.6)0.66
        Cirrhosis1 (4.5)1 (4.5)1.0 (0.1–82.1)1.00
        McCabe scores0.12
            05 (22.7)11 (50.0)1.01.0
            ≥117 (77.3)11 (50.0)3.3 (0.8–15.8)5.0 (1.1–29.0)
        SAPS II (median [range])55 (15–120)41 (13–86)0.05
    ESBL carriage3 (13.6)5 (22.7)0.5 (0.1–3.3)0.70
    Surveillance period,e days [median (range)]13 (4–37)13 (3–37)0.91
    Antibiotic treatments
        Exposure time to antibiotics, days [median (range)]10.5 (2–23)8.5 (0–37)0.52
        Penicillin exposure6 (27.3)8 (36.4)0.7 (0.1–2.8)0.75
        Penicillin and β-lactamase inhibitor exposure8 (36.4)12 (54.5)0.5 (0.1–1.9)0.36
        Cephalosporin exposure13 (59.1)12 (54.5)1.2 (0.3–4.7)1.00
        Imipenem exposure17 (77.3)10 (45.5)3.9 (0.9–18.9)0.06
        Days of imipenem exposure0.09
            05 (22.7)12 (54.5)1.01.0
            1 to 38 (36.4)6 (27.3)3.1 (0.6–18.3)5.3 (1.0–38.4)
            4 to 219 (40.9)4 (18.2)5.1 (0.9–35.1)6.8 (1.2–50.2)
        Fluoroquinolone exposure6 (27.3)4 (18.2)1.7 (0.3–9.6)0.72
        Aminoglycoside exposure14 (63.6)12 (54.5)1.4 (0.4–5.8)0.76
        Glycopeptide exposure12 (54.5)5 (22.7)3.9 (0.9–18.9)0.06
        Metronidazole exposure4 (18.2)3 (13.6)1.4 (0.2–10.9)1.00
        Macrolide exposure2 (9.1)1 (4.5)2.1 (0.1–129.6)1.00
        Colistin exposure4 (18.2)2 (9.1)2.2 (0.3–26.9)0.66
    Outcome
        ICU stay, days [median (range)]27.5 (9–173)15.0 (5–137)0.25
        Death11 (50.0)7 (31.8)2.1 (0.5–8.8)0.36
    • ↵a ORs are given with the 95% confidence intervals in parentheses.

    • ↵b Bivariate analysis was performed using Pearson's chi-squared, Fisher's exact, Wilcoxon, or Welch test (α = 0.05).

    • ↵c Variables with univariate P value of <0.15 were included for multivariate analysis, which was performed using descending stepwise logistic regression.

    • ↵d F, female; M, male.

    • ↵e Period of surveillance, period between admission and acquisition of imipenem-resistant P. aeruginosa.

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Emergence of Imipenem-Resistant Gram-Negative Bacilli in Intestinal Flora of Intensive Care Patients
Laurence Armand-Lefèvre, Cécile Angebault, François Barbier, Emilie Hamelet, Gilles Defrance, Etienne Ruppé, Régis Bronchard, Raphaël Lepeule, Jean-Christophe Lucet, Assiya El Mniai, Michel Wolff, Philippe Montravers, Patrick Plésiat, Antoine Andremont
Antimicrobial Agents and Chemotherapy Feb 2013, 57 (3) 1488-1495; DOI: 10.1128/AAC.01823-12

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Emergence of Imipenem-Resistant Gram-Negative Bacilli in Intestinal Flora of Intensive Care Patients
Laurence Armand-Lefèvre, Cécile Angebault, François Barbier, Emilie Hamelet, Gilles Defrance, Etienne Ruppé, Régis Bronchard, Raphaël Lepeule, Jean-Christophe Lucet, Assiya El Mniai, Michel Wolff, Philippe Montravers, Patrick Plésiat, Antoine Andremont
Antimicrobial Agents and Chemotherapy Feb 2013, 57 (3) 1488-1495; DOI: 10.1128/AAC.01823-12
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