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Epidemiology

Trends in Antibiotic Susceptibility in Staphylococcus aureus in Boston, Massachusetts, from 2000 to 2014

Sanjat Kanjilal, Mohamad R. Abdul Sater, Maile Thayer, Georgia K. Lagoudas, Soohong Kim, Paul C. Blainey, Yonatan H. Grad
Nathan A. Ledeboer, Editor
Sanjat Kanjilal
aDivision of Infectious Diseases, Massachusetts General Hospital, Boston, Massachusetts, USA
bHarvard Medical School, Boston, Massachusetts, USA
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Mohamad R. Abdul Sater
cDepartment of Immunology & Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA
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Maile Thayer
cDepartment of Immunology & Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA
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Georgia K. Lagoudas
dMIT Department of Biological Engineering, Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA
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Soohong Kim
dMIT Department of Biological Engineering, Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA
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Paul C. Blainey
dMIT Department of Biological Engineering, Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA
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Yonatan H. Grad
cDepartment of Immunology & Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA
eDivision of Infectious Diseases, Brigham and Women's Hospital, Boston, Massachusetts, USA
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  • ORCID record for Yonatan H. Grad
Nathan A. Ledeboer
Medical College of Wisconsin
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DOI: 10.1128/JCM.01160-17
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  • FIG 1
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    FIG 1

    Rates of infections by S. aureus per 1,000 inpatients from 2003 to 2014 by subtype (A) and major antibiogram type (B). Estimates adjusted for age, sex, Charlson comorbidity index, type of clinical isolate (blood versus nonblood) and onset (community versus hospital). Lines represent model fits, shaded areas are 95% confidence intervals, and data points represent unadjusted rates. Asterisks indicate the trends are significant. The “other” category for antibiogram type was omitted for clarity.

  • FIG 2
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    FIG 2

    Mean resistances of S. aureus isolates from 2000 to 2014. Estimates adjusted for age, sex, Charlson comorbidity index, type of clinical isolate (blood versus nonblood), and onset (community versus hospital). Lines represent model fits, shaded areas are 95% confidence intervals, and data points represent unadjusted mean resistances. Asterisks indicate trends are significant.

  • FIG 3
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    FIG 3

    Phylogeny of contemporary S. aureus isolates and gain and loss of methicillin resistance at the strain level. (A) Unrooted maximum likelihood phylogeny of 180 S. aureus isolates obtained between 1 January 2016 and 22 July 2016. Select clonal complexes are identified in red circles. (B) Inference of ancestral presence or absence of methicillin resistance in sequence type 5 (CC5) and sequence type 8 (CC8) phylogenies (shown here as dendrograms) estimated using parsimony. Inner rings represent penicillin susceptibility, and outer rings represent methicillin susceptibility. Orange circles represent acquisition of methicillin resistance, and magenta circles represent loss of methicillin resistance. Branch lengths are intended to maximize visual clarity and are not proportional to genetic distance. CC, clonal complex.

Tables

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  • TABLE 1

    Demographic and microbiologic characteristics of patients and S. aureus subtypes

    SubtypeNo. of isolatesMean patient age (yr [SD])% female patientsCCIa (mean [median])Site of infection (%)% community onset infections
    BloodLungSSIOther
    All S. aureus45,70758.8 (18.3)412.8 (2)1634282262
    MRSA22,79961.5 (18.1)423.0 (2)1638252254
    MSSA18,15455.6 (18.2)402.4 (2)1730312269
    PSSA4,75457.8 (18.1)402.6 (2)1632292368
    P valueb
        MRSA vs MSSA<0.00010.005<0.0001<0.0001<0.0001
        MRSA vs PSSA<0.00010.12<0.0001<0.0001<0.0001
        MSSA vs PSSA<0.00010.870.00050.00120.76
    • ↵a CCI, Charlson comorbidity index; SSI, skin and soft tissue infection.

    • ↵b Tests of difference are two-sided and comprised t tests for age, chi-squared tests for sex, site of infection, and onset, and a Mann-Whitney test for CCI.

  • TABLE 2

    Adjusted rates of inpatient infections of S. aureus by subtype and antibiogram type per 1,000 inpatients in 2003 and 2014

    Subtype or antibiogram typeRate of infections/1,000 inpatients (% [95% CI])bAnnual % change (95% CI) in countsbP value
    20032014
    Subtype
        All S. aureus33.4 (23.5–43.3)21.3 (11.5–31.2)−4.2 (−5.6 to −2.7)<0.0001
        MRSA21.1 (17.0–25.1)6.3 (2.2–10.4)−10.9 (−12.6 to −9.3)<0.0001
        MSSA11.1 (9.0–13.3)10.3 (8.2–12.5)−0.6 (−2.1 to 0.9)0.43
        PSSA1.9 (1.2–2.7)4.0 (3.2–4.7)6.1 (4.2 to 8.1)<0.0001
    Antibiogram typea
        PMEL15.8 (12.6–19.0)4.9 (1.7–8.1)−12.1 (−13.6 to −10.5)<0.0001
        PME1.0 (0.1–1.9)1.4 (0.4–2.3)3.0 (−0.1 to 6.2)0.06
        PE3.2 (3.0–3.5)2.8 (2.6–3.1)−1.4 (−3.2 to 0.5)0.14
        P6.2 (4.8–7.6)6.0 (4.6–7.4)−0.3 (−2.3 to 1.8)0.80
        Pansusceptible1.3 (0.8–1.7)2.3 (1.9–2.8)5.3 (3.1 to 7.5)<0.0001
        Other3.9 (1.8–6.0)6.0 (3.9–8.0)3.3 (0.2 to 6.4)0.04
    • ↵a Antibiogram types exclude clindamycin. “Other” category includes all antibiograms not belonging to top 5 most common antibiogram types. PMEL, penicillin-, methicillin-, erythromycin-, and levofloxacin-resistant S. aureus; PME, penicillin-, methicillin-, and erythromycin-resistant S. aureus; PE, penicillin- and erythromycin-resistant S. aureus; P, penicillin-resistant S. aureus.

    • ↵b Percentage estimates adjusted for age, sex, Charlson comorbidity index, type of clinical isolate (blood versus nonblood), and onset (community versus hospital).

  • TABLE 3

    Adjusted mean antibiotic resistances of S. aureus by subtype in 2000 and 2014

    SubtypeMean resistance (no. of antibiotics [95% CI])aAbsolute change (no. of antibiotics [95% CI])P value
    20002014
    All S. aureus3.2 (3.1–3.2)2.3 (2.3–2.4)−0.8 (−0.8 to −0.7)<0.0001
    MRSA4.5 (4.5–4.6)3.7 (3.7–3.8)−0.9 (−1.0 to −0.8)<0.0001
    MSSA1.6 (1.5–1.6)1.5 (1.5–1.6)0.0 (−0.1 to 0.1)0.89
    PSSA0.6 (0.6–0.7)0.6 (0.5–0.6)−0.1 (−0.1 to 0.0)0.05
    • ↵a Estimates adjusted for age, sex, Charlson comorbidity index, type of clinical isolate (blood versus nonblood), and onset (community versus hospital).

Additional Files

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  • Supplemental material

    • Supplemental file 1 -

      Tables S1 (Characteristics of retrospective and prospective samples by subtype and antibiogram type), S2 (Demographic and microbiologic characteristics of S. aureus antibiogram types), and S3 (Distribution of clonal complex by subtype and antibiogram type); Fig. S1 (Adjusted rates of erythromycin, clindamycin, and levofloxacin resistance in S. aureus), S2 (Adjusted rates of S. aureus by major antibiogram type, excluding or including clindamycin, 2010 to 2014), S3 (Mean resistance in S. aureus, excluding or including clindamycin and comparing blood and nonblood isolates), S4 (Complete phylogeny of S. aureus isolates), S5 (Genetic basis for loss of methicillin resistance in ST5/CC5 and ST8/CC8), and S6 (Antibiotic susceptibility testing protocols for S. aureus, 2000 to 2014); and Supplemental methods (Detailed sample preparation for microfluidics platform and bioinformatic analyses)

      PDF, 1.4M

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Trends in Antibiotic Susceptibility in Staphylococcus aureus in Boston, Massachusetts, from 2000 to 2014
Sanjat Kanjilal, Mohamad R. Abdul Sater, Maile Thayer, Georgia K. Lagoudas, Soohong Kim, Paul C. Blainey, Yonatan H. Grad
Journal of Clinical Microbiology Dec 2017, 56 (1) e01160-17; DOI: 10.1128/JCM.01160-17

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Trends in Antibiotic Susceptibility in Staphylococcus aureus in Boston, Massachusetts, from 2000 to 2014
Sanjat Kanjilal, Mohamad R. Abdul Sater, Maile Thayer, Georgia K. Lagoudas, Soohong Kim, Paul C. Blainey, Yonatan H. Grad
Journal of Clinical Microbiology Dec 2017, 56 (1) e01160-17; DOI: 10.1128/JCM.01160-17
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    • ABSTRACT
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KEYWORDS

Staphylococcus aureus
MRSA
antibiotic resistance
genomic epidemiology

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