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Research Article | Clinical Science and Epidemiology

A Longitudinal Epidemiology Study of Meningococcal Carriage in Students 13 to 25 Years Old in Quebec

Rodica Gilca, Philippe De Wals, Sheila M. Nolan, Nicholas Kitchin, Joseph J. Eiden, Qin Jiang, C. Hal Jones, Kathrin U. Jansen, Annaliesa S. Anderson, Louise Pedneault
Patricia A. Bradford, Editor
Rodica Gilca
Research Center, Centre Hospitalier Universitaire de Québec-Université Laval, Québec City, Quebec, CanadaDepartment of Social and Preventive Medicine, Laval University, Québec City, Quebec, Canada
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Philippe De Wals
Research Center, Centre Hospitalier Universitaire de Québec-Université Laval, Québec City, Quebec, CanadaDepartment of Social and Preventive Medicine, Laval University, Québec City, Quebec, Canada
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Sheila M. Nolan
Vaccine Clinical Research and Development, Pfizer Inc., Pearl River, New York, USA
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Nicholas Kitchin
Vaccine Clinical Research and Development, Pfizer Ltd., Hurley, Berkshire, United Kingdom
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Joseph J. Eiden
Vaccine Clinical Research and Development, Pfizer Inc., Pearl River, New York, USA
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Qin Jiang
Vaccine Clinical Research and Development, Pfizer Inc., Collegeville, Pennsylvania, USA
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C. Hal Jones
Vaccine Research and Development, Pfizer Inc., Pearl River, New York, USA
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Kathrin U. Jansen
Vaccine Research and Development, Pfizer Inc., Pearl River, New York, USA
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Annaliesa S. Anderson
Vaccine Research and Development, Pfizer Inc., Pearl River, New York, USA
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Louise Pedneault
Vaccine Clinical Research and Development, Pfizer Inc., Pearl River, New York, USA
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Patricia A. Bradford
Antimicrobial Development Specialists, LLC
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DOI: 10.1128/mSphere.00427-18
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  • FIG 1
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    FIG 1

    Disposition of subjects (intent-to-treat population).

  • FIG 2
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    FIG 2

    Neisseria meningitidis serogroup B (NmB) carriage prevalence rates at each visit for both cohorts. NmB carriage was determined by seroagglutination, isolate PCR, and direct swab PCR assays at 3 visits and any visit for ninth-grade students (A) and university students (C) and by isolate whole-genome sequencing (WGS), isolate PCR, direct swab PCR, and live cell phenotypic assay (LCPA) for eleventh-grade/college entry students (B). *, P < 0.05. CIs were calculated using the exact method based on Clopper-Pearson (2-sided). The McNemar test using the exact method was used to compare the prevalence rates between PCR analyses and seroagglutination for each visit in ninth-grade/university students.

  • FIG 3
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    FIG 3

    Frequency of Neisseria meningitidis serogroup B (NmB) results by 3 diagnostic methods for both cohorts. The numbers of instances in which NmB was detected for subjects by seroagglutination, isolate PCR, direct swab PCR (ninth-grade and university students); by isolate whole-genome sequencing (WGS), isolate PCR, direct swab PCR, and live cell phenotypic assay (LCPA) (eleventh-grade/college entry students); and by multiple methods are shown as Venn diagrams for ninth-grade students (A), eleventh-grade/college entry students (B), and university students (C).

  • FIG 4
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    FIG 4

    Neisseria meningitidis serogroup B (NmB) and non-NmB carriage analyses for both cohorts. NmB isolates from all 3 visits (n = 45) (A) were characterized by whole-genome sequencing (WGS) to determine multilocus sequence typing (MLST)/clonal complex and factor H binding protein (fHBP) assignment. Results are presented for ninth-grade, eleventh-grade/college entry, and university students. Non-NmB isolates (B) from all 3 visits (n = 143) were characterized by PCR (serogroup assignment, except eleventh grade by WGS) and sequence analysis (fHBP assignment). NT, nontypeable; NG, nongroupable.

Tables

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  • TABLE 1

    Summary of meningococcal carriage prevalence rates at each visit by isolate PCR (ITT population)g

    Visit
    (swab)
    CohortAge group
    (Ne)
    N. meningitidis serogroup detection from throat swab, n (%)a,b
    NmBcNmCNmYNmWNongroupableNmE or
    NmZ
    All
    non-NmBd
    All
    meningococci
    Visit 119th grade (533)4 (0.8)2 (0.4)8 (1.5)4 (0.8)16 (3.0)3 (0.6)33 (6.2)37 (6.9)
    11th gradef (363)4 (1.1)1 (0.3)3 (0.8)1 (0.3)10 (2.8)2 (0.6)17 (4.7)21 (5.8)
    2University (360)20 (5.6)3 (0.8)5 (1.4)8 (2.2)35 (9.7)16 (4.4)67 (18.6)87 (24.2)
    Visit 219th grade (417)7 (1.7)1 (0.2)4 (1.0)1 (0.2)15 (3.6)0 (0.0)21 (5.0)28 (6.7)
    11th grade (363)5 (1.4)1 (0.3)2 (0.6)0 (0.0)8 (2.2)2 (0.6)13 (3.6)18 (5.0)
    2University (356)16 (4.5)3 (0.8)3 (0.8)6 (1.7)31 (8.7)9 (2.5)52 (14.6)68 (19.1)
    Visit 319th grade (526)8 (1.5)1 (0.2)5 (1.0)3 (0.6)14 (2.7)1 (0.2)24 (4.6)32 (6.1)
    College entry (356)4 (1.1)0 (0.0)2 (0.6)1 (0.3)12 (3.4)3 (0.8)18 (5.1)22 (6.2)
    2University (339)17 (5.0)4 (1.2)6 (1.8)7 (2.1)27 (8.0)8 (2.4)52 (15.3)69 (20.4)
    Any visit19th grade (533)11 (2.1)2 (0.4)9 (1.7)5 (0.9)19 (3.6)3 (0.6)39 (7.3)49 (9.2)
    11th grade/college
    entry (363)
    6 (1.7)1 (0.3)4 (1.1)1 (0.3)17 (4.7)3 (0.8)26 (7.2)32 (8.8)
    2University (360)27 (7.5)4 (1.1)8 (2.2)9 (2.5)42 (11.7)15 (4.2)79 (21.9)105 (29.1)
    • ↵a n (%) is the number and percentage of subjects with positive meningococci carriage at that visit.

    • ↵b No NmA or NmX isolates were detected.

    • ↵c NmB PCR data were confirmed by WGS.

    • ↵d All non-NmB meningococci: A, C, X, Y, W, nongroupable, Z, and E.

    • ↵e N is number of subjects who had a culture performed at that visit.

    • ↵f Eleventh-grade/college-entry students are the same (former) ninth-grade students.

    • ↵g Abbreviations: ITT, intent-to-treat; Nm, Neisseria meningitidis; isolate PCR assay was performed by real-time PCR. Non-NmB meningococci include any sample in which the porA and/or ctrA gene(s) was detected but the group B capsule gene was not detected. Missing data were not imputed.

  • TABLE 2

    Carriage rates for nongroupable isolates at any visit

    MethodNo. of subjects with positive non-NmB meningococcal carriage at any visit/no. ofsubjects with ≥1 culture performed at any visit (% [95% CIa]) by cohort:
    Ninth-grade studentsUniversity students
    Seroagglutination36/533 (6.8 [4.8, 9.2])79/360 (21.9 [17.8, 26.6])
    Isolate PCR21/533 (3.9 [2.5, 6.0])44/360 (12.2 [9.0, 16.1])
    P valueb0.001<0.001
    • ↵a 95% Clopper-Pearson 2-sided CI.

    • ↵b McNemar test using exact method is used to compare the prevalence rate between PCR and culture/seroagglutination at each visit.

  • TABLE 3

    Microbiologic analyses of samples by cohort and time point (ITT population)c

    Visit
    (swab)
    CohortAge groupAnalysis method, na
    SeroagglutinationIsolate
    PCR
    Direct
    swab
    PCR
    Isolate
    WGS
    Isolate
    LCPA
    MLST
    Visit 119th grade3636469
    11th grade21361212121
    2University87102327
    Visit 219th grade2828339
    11th grade18363181818
    2University6877342
    Visit 319th grade3334451
    College entry22356222222
    2University3539338
    Any visitb19th grade48533531
    College entry31363313131
    2University99360359
    • ↵a n = number of subjects with specified test performed at that visit.

    • ↵b n = number of subjects with ≥1 specified test performed at any visit.

    • ↵c Abbreviations: ITT, intent-to-treat; LCPA, live cell phenotypic assay; MLST, multilocus sequence typing; WGS, whole-genome sequencing.

  • TABLE 4

    Definitions of meningococcal categories used in PCR analysesa

    CategoryIsolate PCRDirect swab PCRWGS
    All meningococciAny sample in which the porA and/or ctrA gene(s) was detectedAny sample in which the porA and/or ctrA gene(s) and/or the group B capsule gene was detectedAny sample in which the porA and/or ctrA sequences were predicted to encode full-length gene product
    Grouped meningococciAny sample in which the porA and/or ctrA gene(s) and the relevant group capsule gene were detectedPerformed only for NmBAny sample in which the porA and/or ctrA sequences and all the required genes for synthesis and transport of the relevant capsule group were predicted to encode full-length gene products
    Nongroupable meningococciAny sample in which the porA and/or ctrA gene(s) was detected but no capsule gene was detectedNot applicableAny sample in which the porA and ctrA sequences were predicted to encode full-length gene product and lacking any of the required genes for synthesis and transport of the relevant capsule group OR any sample in which the ctrA sequence is incomplete
    Non-NmB meningococciNot applicableAny sample in which the porA and/or ctrA gene(s) was detected but the group B capsule gene was not detectedNot applicable
    Group B meningococciSee “Grouped meningococci” aboveAny sample in which the group B capsule gene was detectedSee “Grouped meningococci” above
    • ↵a Abbreviations: NmB, Neisseria meningitidis serogroup B; WGS, whole-genome sequencing.

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A Longitudinal Epidemiology Study of Meningococcal Carriage in Students 13 to 25 Years Old in Quebec
Rodica Gilca, Philippe De Wals, Sheila M. Nolan, Nicholas Kitchin, Joseph J. Eiden, Qin Jiang, C. Hal Jones, Kathrin U. Jansen, Annaliesa S. Anderson, Louise Pedneault
mSphere Dec 2018, 3 (6) e00427-18; DOI: 10.1128/mSphere.00427-18

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A Longitudinal Epidemiology Study of Meningococcal Carriage in Students 13 to 25 Years Old in Quebec
Rodica Gilca, Philippe De Wals, Sheila M. Nolan, Nicholas Kitchin, Joseph J. Eiden, Qin Jiang, C. Hal Jones, Kathrin U. Jansen, Annaliesa S. Anderson, Louise Pedneault
mSphere Dec 2018, 3 (6) e00427-18; DOI: 10.1128/mSphere.00427-18
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    • ABSTRACT
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KEYWORDS

Neisseria meningitidis
NmB
epidemiology
factor H binding protein
oropharyngeal carriage
serogroup B
vaccines

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