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Public Health Microbiology

Acquisition of Resistance to Extended-Spectrum Cephalosporins by Salmonella enterica subsp. enterica Serovar Newport and Escherichia coli in the Turkey Poult Intestinal Tract

C. Poppe, L. C. Martin, C. L. Gyles, R. Reid-Smith, P. Boerlin, S. A. McEwen, J. F. Prescott, K. R. Forward
C. Poppe
1Laboratory for Foodborne Zoonoses, Public Health Agency of Canada
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  • For correspondence: Cornelius_Poppe@hc-sc.gc.ca
L. C. Martin
1Laboratory for Foodborne Zoonoses, Public Health Agency of Canada
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C. L. Gyles
2Department of Pathobiology
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R. Reid-Smith
1Laboratory for Foodborne Zoonoses, Public Health Agency of Canada
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P. Boerlin
2Department of Pathobiology
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S. A. McEwen
3Department of Population Medicine, University of Guelph, Guelph, Ontario
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J. F. Prescott
2Department of Pathobiology
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K. R. Forward
4Dalhousie University and Queen Elizabeth II HSC, Halifax, Nova Scotia, Canada
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DOI: 10.1128/AEM.71.3.1184-1192.2005
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    FIG. 1.

    Plasmids with the cmy-2 gene in E. coli transferred by conjugation to serovar Newport in the intestinal tracts of poults. Lanes 1, E. coli MPS57 (O168:H7) with 72-MDa plasmid (containing cmy-2 gene) and 66-MDa plasmid; lanes 2, Salmonella serovar Newport 02-6203 before conjugation; lanes 3, serovar Newport 02-6203 after conjugation with E. coli MPS57 containing the 72-MDa plasmid; lanes 4 and 5, E. coli CE332-1 (O168:H7; 72- and 66-MDa plasmids) and serovar Newport CE332-1 (72-MDa plasmid), isolated from the cecal contents of the same poult; lanes 6, reference plasmids of 96, 62, 36, 23, 3.7, 3.4, 2.8, 2.0, and 1.4 MDa; lanes 7 and 8, E. coli CE3313-1 (O168:H7; 72- and 66-MDa plasmids) and serovar Newport CE3313-1 (72-MDa plasmid) isolated from the cecal contents of the same poult; lanes 9 and 10, E. coli CE331-2 (O101:H9; 80-, 72-, 3.6-, 3.0-, and 1.0-MDa plasmids) and serovar Newport CE331-2 (72-MDa plasmid) isolated from the cecal contents of the same poult; lanes 11 and 12, E. coli CE338-2 (O101:H9; 96-, 72-, 3.6-, 3.0-, and 1.0-MDa plasmids) and serovar Newport CE338-2 (72-MDa plasmid) isolated from the cecal contents of the same poult. The isolates with the suffix “-1” were isolated during the first trial; those with the suffix “-2” were isolated during the second trial.

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  • TABLE 1.

    Antimicrobials and concentrations used to test susceptibility of E. coli and Salmonella isolates

    Antimicrobial (abbreviation)Breakpoint concn (μg/ml)a
    SusceptibilityResistance
    Amikacin (AMK)16ND
    Ampicillin (AMP)ND32
    Amoxicillin-clavulanate (AMC)ND64/16b
    Apramycin (APR)cND32d
    Carbadox (CRB)cND30e
    Cephalothin (CEF)ND32
    Ceftriaxone (CRO)8ND
    Ceftiofur (CTF)ND8
    Cefoxitin (FOX)ND32
    Chloramphenicol (CHL)ND32
    Ciprofloxacin (CIP)0.125fND
    Florfenicol (FLO)cND16g
    Gentamicin (GEN)ND16
    Kanamycin (KAN)ND64
    Nalidixic acid (NAL)ND32
    Neomycin (NEO)cND16d
    Nitrofurantoin (NIT)ND64h
    Spectinomycin (SPT)cND64d
    Streptomycin (STR)cND32d
    Sulfisoxazole (SUL)ND512
    Sulfamethoxazole-trimethoprim (SXT)ND76/4
    Tetracycline (TET)ND16
    Tobramycin (TOB)ND8
    Trimethoprim (TMP)ND16
    • ↵ a The breakpoint concentrations to determine susceptibility and resistance are those specified by NCCLS standards M31-A (26) and M100-S12 (27). ND, not determined.

    • ↵ b The strains were considered resistant when growing on agar plates with amoxicillin-clavulanic acid at 64 and 16 μg/ml; respectively.

    • ↵ c There are no interpretive criteria specified by NCCLS standards M31-A (26) or M100-S12 (27) for these drugs.

    • ↵ d Strains were considered resistant to apramycin, neomycin, spectinomycin, and streptomycin at 32, 16, 64, and 32 μg/ml; respectively.

    • ↵ e Strains were considered resistant to carbadox, a veterinary growth promoter for pigs, at 30 μg/ml (12).

    • ↵ f A 0.125-μg/ml concentration of ciprofloxacin determines reduced sensitivity to ciprofloxacin (34).

    • ↵ g Strains were considered resistant to florfenicol at the level of 16 μg/ml (36).

    • ↵ h Strains were considered resistant to nitrofurantoin at 64 μg/ml; human urinary tract isolates are considered resistant at 128 μg/ml (27).

  • TABLE 2.

    Experimental design of study—dosing and treatment of poults

    DayDosing and treatment for poults in pena:
    1234
    1Dosing with antibiotic-susceptible serovar NewportDosing with antibiotic-susceptible serovar NewportDosing with antibiotic-susceptible serovar Newport and ESC-resistant E. coliNo treatment
    2Administration of CTF (0.17 mg in 0.2 ml of saline) subcutaneouslybAdministration of saline (0.2 ml) subcutaneouslyNo treatment with antimicrobialsNo treatment
    • ↵ a The pens were isolation units in an animal isolation building. Pens 1 and 4 contained 12 poults; pens 2 and 3 contained 13 poults. Poults given serovar Newport were dosed orally with 4.2 × 106 (trial 1) or 3.8 × 106 (trial 2) serovar Newport 02-6203 bacteria, an antimicrobial-susceptible strain that did not harbor any plasmids. The poults in pen 3 were also dosed with 2.5 × 106 (trial 1) or 1.4 × 106 (trial 2) bacteria of the ESC-resistant E. coli strain MPS57 that is resistant to AMP, AMC, CEF, CFT, CRO at 8 μg/ml; FOX; CHL, SPT, and SUL and that contains two plasmids of 66 and 72 MDa; the latter plasmid is self-transmissible, contains the cmy-2 gene, and encodes resistance to all the above-mentioned antimicrobials. Saline, phosphate-buffered saline.

    • ↵ b Administered subcutaneously at a dose and route indicated for the prevention of colibacillosis in 1-day-old poults (5).

  • TABLE 3.

    Experimental design of the study—sample collection

    DayTrial(s)Sample type (no. of samples) and time of collectiona
    11 and 2Shavings (4), feed (1), water (1); before poults were placed in pens
    11Cloacal swabsb (12 or 13; 1/poult); when poults were placed in pens and before they were dosed with serovar Newport (pens 1 to 3) and E. coli (pen 3)
    22Cloacal swabs (12 or 13; 1/poult); after poults were dosed with serovar Newport (pens 1 to 3) and E. coli (pen 3) on day 1 but before CTF (pen 1) or saline (pen 2) treatment on day 2
    41 and 2Litter (4), feed with litter (1), water (1), cloacal swabs (12 or 13; 1/poult)
    101 and 2Litter (4), feed with litter (1), water (1), cecal contentsc (12 or 13; 1/poult)
    • ↵ a Samples were taken from 12 or 13 poults in each of four pens.

    • ↵ b Cloacal swabs were taken by inserting a cotton swab wetted with BPW into the cloaca.

    • ↵ c Upon necropsy; cecal contents were taken and examined for the presence of Salmonella and E. coli; one isolate each of E. coli and serovar Newport per sample, if present, was further characterized.

  • TABLE 4.

    Trial 1 antimicrobial resistance patterns and isolation rates of E. coli and Salmonella serovar Newport

    PenDayResistance patterns (no. of isolates) ofa:
    E. coliSerovar Newport
    11AMP-STR (6), AMP-CIP-NAL-(STR)-TET (5), KAN-NEO-SPT-STR-SUL-TET (2)NIb
    4AMP-STR (1), AMP-CIP-NAL-(STR)-(SUL)-TET (15), KAN-NEO-SPT-STR-(SUL)-TET (2)Susc.c (18)
    10AMP-(AMC)-(CEF)-CIP-NAL-(NIT)-(STR)-TET (16), (AMP)-KAN-NEO-SPT-STR-SUL-TET (2)Susc. (16), SPT-STR-SUL (2)
    21AMP-STR (6), AMP-CIP-NAL-(STR)-TET (4), (AMP)-KAN-NEO-SPT-STR-SUL-TET (3)NI
    4AMP-STR (4), AMP-CIP-NAL-STR-(TET) (10), KAN-NEO-SPT-STR-SUL-TET (4)Susc. (18)
    10AMP-STR (4), AMP-CIP-NAL-(STR)-TET (12), KAN-NEO-STR-SUL-TET (2)Susc. (11), SPT-(STR)-SUL (6)
    31AMP-STR (5), AMP-CIP-NAL-(STR)-TET (6), KAN-NEO-SUL-TET (2)NI
    4AMP-STR (2), AMP-CIP-NAL-STR-TET (3), KAN-NEO-(STR)-SUL-TET (8), AMP-(AMC)-CEF-(CRO)-(CTF)-FOX-SPT-SUL (7)Susc. (18), AMP-CEF-CRO-CTF-FOX-CHL-SPT-SUL (1)
    10AMP-STR (2), AMP-CIP-NAL-(STR)-TET (3), KAN-NEO-(SPT)-(STR)-SUL-TET (6), AMP-(AMC)-CEF-CRO-(CTF)-FOX-SPT-SUL (8)Susc. (11), AMP-(AMC)-CEF-(CRO)-(CTF)-FOX-CHL-SPT-SUL (8)
    41AMP-STR (2), AMP-CIP-NAL-(STR)-TET (4), (AMP)-(GEN)-KAN-NEO-SPT-STR-SUL-TET (6)NI
    4AMP-STR (2), AMP-CIP-NAL-(STR)-TET (9), (AMP)-(CIP)-KAN-(NAL)-NEO-(SPT)-STR-SUL-TET (7)NI
    10AMP-STR (1), AMP-CIP-NAL-(SPT)-STR-TET (8), (AMP)-KAN-NEO-SPT-STR-SUL-TET (8)Susc. (1)
    • ↵ a See Table 1 for abbreviations for antimicrobials. Isolates were considered resistant to CIP when growth occurred on MH agar containing 0.125 μg of CIP/ml. Antimicrobials shown in parentheses are those to which the isolates may or may not be additionally resistant.

    • ↵ b NI, none isolated.

    • ↵ c Susc., susceptible.

  • TABLE 5.

    Trial 2 antimicrobial resistance patterns and isolation rates of E. coli and Salmonella serovar Newport

    PenDayResistance pattern(s) (no. of isolates) ofa:
    E. coliSerovar Newport
    12NIbSusc.c(12)
    4NISusc. (17)
    10Susc. (1), AMP-STR (1)Susc. (16), SUL (1)
    22NISusc. (13)
    4NISusc. (18)
    10SPT-SUL (18)Susc. (16), SUL (2)
    32AMP-AMC-CEF-CRO-(CTF)-FOX-SPT-SUL (13)Susc. (13)
    4Susc. (7), AMP-(AMC)-CEF-(CRO)-(CTF)-(FOX)-SPT-SUL-(TET) (11)Susc. (18)
    10Susc. (6), AMP-(AMC)-CEF-(CRO)-(CTF)-FOX-SPT-SUL (12)Susc. (5), AMP-(AMC)-CEF-(CRO)-(CTF)-(FOX)-CHL-SPT-SUL (13)
    42AMP-CIP-NAL-TET (2)NI
    4AMP-CIP-NAL-(STR)-TET (15), KAN-NEO-SUL-TET (2)NI
    10AMP-STR (4), AMP-CIP-NAL-(SPT)-STR-SUL-TET (10), KAN-NEO-(SPT)-STR-SUL-TET (3)NI
    • ↵ a See Table 1 for abbreviations for antimicrobials. Antimicrobials shown in parentheses are those to which the isolates may or may not be additionally resistant.

    • ↵ b NI, none isolated.

    • ↵ c Susc., susceptible.

  • TABLE 6.

    Relationships among serovars, antimicrobial resistances, and plasmid profiles of E. coli isolates

    TrialPenE.coli serovaraAntimicrobial resistance patternbPlasmid profile (MDa)c
    11O8:H9AMP-STR2.8, 1.0
    O77:H18AMP-CIP-NAL-(STR)-(SUL)-TET96, 60, 30, (1.0)
    O92:NM(AMP)-KAN-NEO-SPT-STR-SUL-TET80, 66, 18, 4.8, 2.0
    2O8:H9AMP-STR(80), (66), 2.8, 1.0
    O77:H18AMP-CIP-NAL-(STR)-(TET)96, 60, 30
    O92:NM(AMP)-KAN-NEO-SPT-STR-SUL-TET80, 66, 18, 4.8, 2.0
    3O8:H9AMP-STR80, 66, 2.8, 1.0
    O17:H18KAN-NEO-SUL-TETNONE
    O77:H18AMP-CIP-NAL-(STR)-TET96, 60, 30
    O168:H7AMP-AMC-CEF-CRO-(CFT)-FOX-SPT-SUL 72, 66
    4O8:H9AMP-STR2.8, 1.0
    O77:H18AMP-CIP-NAL-STR-TET96, 60, 30, (1.0)
    O92:NM(AMP)-(GEN)-KAN-NEO-(SPT)-STR-SUL-TET80, 66, 18, 4.8, 2.0
    21O8:H9AMP-STR2.8, 1.0
    O159:H28Susc.None
    2O11:H11SPT-SUL90, 84
    3O101:H9Susc.96, 3.6, 3.0, 1.0
    O101:H9AMP-AMC-CEF-FOX-SPT-SUL96 or 80, 72, 3.6, 3.0, 1.0
    O168:H7AMP-AMC-CEF-CRO-(CTF)-FOX-SPT-SUL 72, 66
    4O8:H9AMP-STR80, 66, 24, 2.8, 1.0
    O17:H18KAN-NEO-SUL-TETNone
    O17:H18AMP-CIP-NAL-TET96, 60, 30
    O92:NMKAN-NEO-(SPT)-STR-SUL-TET80, 66, 18, 2.0
    • ↵ a None of the E. coli isolates were verotoxigenic. NM, nonmotile.

    • ↵ b Antimicrobials shown in parentheses are those to which the isolates may or may not be additionally resistant.

    • ↵ c Those plasmids indicated in parentheses may or may not be present. The 72-MDa plasmid indicated in bold was the only one that hybridized with the cmy-2 probe.

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Acquisition of Resistance to Extended-Spectrum Cephalosporins by Salmonella enterica subsp. enterica Serovar Newport and Escherichia coli in the Turkey Poult Intestinal Tract
C. Poppe, L. C. Martin, C. L. Gyles, R. Reid-Smith, P. Boerlin, S. A. McEwen, J. F. Prescott, K. R. Forward
Applied and Environmental Microbiology Mar 2005, 71 (3) 1184-1192; DOI: 10.1128/AEM.71.3.1184-1192.2005

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Acquisition of Resistance to Extended-Spectrum Cephalosporins by Salmonella enterica subsp. enterica Serovar Newport and Escherichia coli in the Turkey Poult Intestinal Tract
C. Poppe, L. C. Martin, C. L. Gyles, R. Reid-Smith, P. Boerlin, S. A. McEwen, J. F. Prescott, K. R. Forward
Applied and Environmental Microbiology Mar 2005, 71 (3) 1184-1192; DOI: 10.1128/AEM.71.3.1184-1192.2005
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KEYWORDS

Cephalosporin Resistance
Escherichia coli
Salmonella enterica
Turkeys

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