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Epidemiology and Surveillance

Risk Factors for Gastrointestinal Colonization and Acquisition of Carbapenem-Resistant Gram-Negative Bacteria among Patients in Intensive Care Units in Thailand

Anong Kiddee, Kanit Assawatheptawee, Anamai Na-udom, Pornpit Treebupachatsakul, Apirath Wangteeraprasert, Timothy R. Walsh, Pannika R. Niumsup
Anong Kiddee
aDepartment of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok, Thailand
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Kanit Assawatheptawee
aDepartment of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok, Thailand
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Anamai Na-udom
bDepartment of Mathematics, Faculty of Science, Naresuan University, Phitsanulok, Thailand
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Pornpit Treebupachatsakul
cBuddhachinaraj Hospital, Phitsanulok, Thailand
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Apirath Wangteeraprasert
dDepartment of Medicine, Faculty of Medicine, Naresuan University, Phitsanulok, Thailand
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Timothy R. Walsh
eDepartment of Medical Microbiology and Infectious Disease, Division of Infection and Immunity, School of Medicine, Cardiff University, Cardiff, United Kingdom
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Pannika R. Niumsup
aDepartment of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok, Thailand
fCenter of Excellence in Medical Biotechnology, Faculty of Medical Science, Naresuan University, Phitsanulok, Thailand
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DOI: 10.1128/AAC.00341-18
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    FIG 1

    Flowchart of patients included in this study. CR-GNB, carbapenem-resistant Gram-negative bacteria; ICU, intensive care unit; BUH, Buddhachinaraj Hospital; NUH, Naresuan University Hospital.

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  • TABLE 1

    Factors associated with intestinal colonization of CR-GNB among ICU patientse

    CharacteristicNo. (%) of patients in the following groups with the indicated characteristic:Univariate analysis P valueMultivariate logistic regression analysis
    All patients (n = 275)CR-GNB carriers (n = 32)Non-CR-GNB carriers (n = 243)P valueaaOR (95% CI)
    Male patients149 (54.2)14 (43.8)135 (55.6)0.199
    Age >65 yr119 (43.3)16 (50.0)103 (42.4)0.497
    Secondary school educationb190 (69.1)19 (59.4)171 (70.4)0.174
    ≥5 family membersc52 (18.9)4 (12.5)48 (19.8)0.381
    Family income of <10,000 bahtd168 (61.1)18 (56.3)150 (61.7)0.405
    Urban living85 (30.9)11 (34.4)74 (30.5)0.520
    Antibiotic usage within previous 3 mo93 (33.8)17 (53.1)76 (31.3)0.0170.2781.614 (0.679–3.836)
    Hospitalization within previous 6 mo89 (32.4)19 (59.4)70 (28.8)0.0010.0023.818 (1.642–8.878)
    Referral of patients from:
        Home99 (36.0)10 (31.3)89 (36.6)0.722
        Another hospital73 (26.5)7 (21.9)66 (27.2)0.654
        Another ward within hospital92 (33.5)12 (37.5)80 (32.9)0.434
    Principle diagnosis
        Respiratory tract disease69 (25.1)13 (40.6)56 (23.0)0.0340.0512.309 (0.996–5.353)
        Cardiovascular disease35 (12.7)6 (18.8)29 (11.9)0.271
        Renal disease19 (6.9)3 (9.4)16 (6.6)0.477
        Sepsis41 (14.9)4 (12.5)37 (15.2)0.797
    Underlying condition
        Cardiovascular disease130 (47.3)14 (43.8)116 (47.7)0.665
        Diabetes71 (25.8)11 (34.4)60 (24.7)0.233
        Respiratory tract disease35 (12.7)6 (18.8)29 (11.9)0.264
        Renal disease38 (13.8)5 (15.6)33 (13.6)0.784
        Liver disease18 (6.5)1 (3.1)17 (7.0)0.704
    Length of ICU stay (day)
        <8 days165 (60.0)17 (53.1)148 (60.9)0.274
        8–14 days51 (14.5)7 (21.9)44 (18.1)0.666
        15–21 days29 (10.5)5 (15.6)24 (9.9)0.362
        >21 days14 (5.1)2 (6.3)12 (4.9)0.678
    30-day mortality35 (12.7)4 (12.5)31 (12.8)1.000
    • ↵a A P value of <0.05 was considered statistically significant.

    • ↵b Basic education in Thailand consists of 6 years of primary school education and 6 years of secondary school education.

    • ↵c Average number of household members.

    • ↵d The average minimum income per month is 10,000 baht.

    • ↵e Data are for a total of 275 patients.

  • TABLE 2

    Distribution of CR-GNB isolates and types of carbapenemase genes among CR-GNB in carriage and acquisition groups

    OrganismNo. (%) of isolatesNo. of isolates carrying the following carbapenemase gene:
    blaIMPblaNDMblaOXA-23blaOXA-24blaOXA-51blaOXA-58blaOXA-23/51blaOXA-51/58blaOXA-23/51/58blaOXA-24/51/58
    CR-GNB carriage isolates37
        A. baumannii15 (40.5)11212513
        K. pneumoniae9 (24.3)6
        Acinetobacter spp.5 (13.5)11
        Enterobacter spp.3 (8.1)2
        Other CR-GNBa5 (13.5)
    CR-GNB acquisition isolates59
        A. baumannii28 (47.5)415321
        K. pneumoniae13 (22.0)9
        Acinetobacter spp.7 (11.9)211
        P. aeruginosa5 (8.5)3
        Enterobacter spp.1 (1.7)1
        Klebsiella spp.1 (1.7)1
        Other CR-GNBb4 (6.8)
    • ↵a Other CR-GNB isolates included P. aeruginosa (n = 2), Escherichia coli (n = 1), Serratia marcescens (n = 1), and Citrobacter freundii (n = 1).

    • ↵b Other CR-GNB isolates included Klebsiella oxytoca (n = 2), Serratia spp. (n = 1), and Shigella spp. (n = 1).

  • TABLE 3

    Factors associated with acquisition of CR-GNB among patients during ICU stayc

    CharacteristicNo. (%) of patients in the following groups with the indicated characteristic:Univariate analysis P valueMultivariate logistic regression analysis
    All patients (n = 206)CR-GNB acquisition (n = 52)Non-CR-GNB acquisition (n = 154)P valueaaOR (95% CI)
    Male gender113 (54.9)30 (57.7)83 (53.9)0.540
    Age >65 yr84 (40.8)23 (44.2)61 (39.6)0.486
    Mechanical devices
        Central venous catheter29 (14.1)8 (15.4)21 (13.6)0.690
        Indwelling urinary catheter168 (81.6)43 (82.7)125 (81.2)0.485
        Enteral feeding tube153 (74.3)46 (88.5)107 (69.5)0.0020.0085.386 (1.563–18.564)
        Endotracheal tube159 (77.2)46 (88.5)113 (73.4)0.0070.7290.763 (0.165–3.527)
    Antibiotic usage during ICU stay
        First- and second-generation cephalosporins35 (17.0)6 (11.5)29 (18.8)0.258
        Third-generation cephalosporins121 (58.7)37 (71.2)84 (54.5)0.0170.0322.293 (1.074–4.896)
        Carbapenems42 (20.4)16 (30.8)26 (16.9)0.0230.0452.199 (1.019–4.743)
        Penicillinsb4 (1.9)2 (3.8)2 (1.3)0.254
        β-Lactam–β-lactamase inhibitors36 (17.5)10 (19.2)26 (16.9)0.629
        Aminoglycosidesb2 (1.0)1 (1.9)1 (0.6)0.433
        Fluoroquinolones18 (8.7)7 (13.5)11 (7.1)0.156
        Macrolides26 (12.6)8 (15.4)18 (11.7)0.437
        Colistinb7 (3.4)2 (3.8)5 (3.2)0.682
        Vancomycin11 (5.3)4 (7.7)7 (4.5)0.470
        Clindamycin21 (10.2)4 (7.7)17 (11.0)0.531
        Metronidazole12 (5.8)5 (9.6)7 (4.5)0.174
        Fosfomycinb2 (1.0)1 (1.9)1 (0.6)0.433
    Underlying conditions
        Cardiovascular disease97 (47.1)23 (44.2)74 (48.1)0.870
        Respiratory disease25 (12.1)7 (13.5)18 (11.7)0.635
        Renal disease24 (11.7)8 (15.4)16 (10.4)0.264
        Diabetes52 (25.2)14 (26.9)38 (24.7)0.592
        Liver disease14 (6.8)2 (3.8)12 (7.8)0.524
    Length of ICU stay (day)
        <8 days129 (62.6)24 (46.2)105 (68.2)0.0080.4980.730 (0.293–1.815)
        8–14 days34 (16.5)10 (19.2)24 (15.6)0.449
        15–21 days22 (10.7)9 (17.3)13 (8.4)0.0550.1312.144 (0.797–5.767)
        >21 days8 (3.9)4 (7.7)4 (2.6)0.1000.1493.227 (0.657–15.860)
    30-day mortality16 (7.8)5 (9.6)11 (7.1)0.553
    • ↵a A P value of <0.05 was considered statistically significant.

    • ↵b The rate of use was too low to give an accurate P value.

    • ↵c Data are for a total of 206 patients.

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      Supplemental Figures S1 and S2 and Table S1

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Risk Factors for Gastrointestinal Colonization and Acquisition of Carbapenem-Resistant Gram-Negative Bacteria among Patients in Intensive Care Units in Thailand
Anong Kiddee, Kanit Assawatheptawee, Anamai Na-udom, Pornpit Treebupachatsakul, Apirath Wangteeraprasert, Timothy R. Walsh, Pannika R. Niumsup
Antimicrobial Agents and Chemotherapy Jul 2018, 62 (8) e00341-18; DOI: 10.1128/AAC.00341-18

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Risk Factors for Gastrointestinal Colonization and Acquisition of Carbapenem-Resistant Gram-Negative Bacteria among Patients in Intensive Care Units in Thailand
Anong Kiddee, Kanit Assawatheptawee, Anamai Na-udom, Pornpit Treebupachatsakul, Apirath Wangteeraprasert, Timothy R. Walsh, Pannika R. Niumsup
Antimicrobial Agents and Chemotherapy Jul 2018, 62 (8) e00341-18; DOI: 10.1128/AAC.00341-18
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    • ABSTRACT
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KEYWORDS

carbapenem
Gram-negative bacteria
colonization
acquisition
risk factor
blaOXA
blaNDM
carriage

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