MAJOR ARTICLE
Meningococcal Carriage Among Georgia and Maryland High School Students Lee H. Harrison,1,3 Kathleen A. Shutt,3 Kathryn E. Arnold,4,5 Eric J. Stern,6,7 Tracy Pondo,6 Julia A. Kiehlbauch,2 Robert A. Myers,2 Rosemary A. Hollick,1 Susanna Schmink,6 Marianne Vello,4,5 David S. Stephens,4,8,9 Nancy E. Messonnier,6 Leonard W. Mayer,6 and Thomas A. Clark6 1
Department of International Health, Johns Hopkins Bloomberg School of Public Health, and 2Maryland Department of Health and Mental Hygiene, Baltimore, Maryland; 3Infectious Diseases Epidemiology Research Unit, University of Pittsburgh, Pennsylvania; 4Georgia Emerging Infections Program, 5 Division of Public Health, Georgia Department Human of Resources, 6National Center for Immunization and Respiratory Diseases, 7Epidemic Intelligence Service Program, Centers for Disease Control and Prevention, 8Emory University School of Medicine, and 9VA Medical Center, Atlanta, Georgia
Background. Meningococcal disease incidence in the United States is at an all-time low. In a previous study of Georgia high school students, meningococcal carriage prevalence was 7%. The purpose of this study was to measure the impact of a meningococcal conjugate vaccine on serogroup Y meningococcal carriage and to define the dynamics of carriage in high school students. Methods. This was a prospective cohort study at 8 high schools, 4 each in Maryland and Georgia, during a school year. Students at participating schools received quadrivalent meningococcal conjugate vaccine that uses diphtheria toxoid as the protein carrier (MCV4-DT). In each state, 2 high schools were randomly assigned for MCV4-DT receipt by students at the beginning of the study, and 2 were randomly assigned for MCV4-DT receipt at the end. Oropharyngeal swab cultures for meningococcal carriage were performed 3 times during the school year. Results. Among 3311 students, the prevalence of meningococcal carriage was 3.21%–4.01%. Phenotypically nongroupable strains accounted for 88% of carriage isolates. There were only 5 observed acquisitions of serogroup Y strains during the study; therefore, the impact of MCV4-DT on meningococcal carriage could not be determined. Conclusions. Meningococcal carriage rates in US high school students were lower than expected, and the vast majority of strains did not express capsule. These findings may help explain the historically low incidence of meningococcal disease in the United States. Keywords. Neisseria meningitidis; meningococcus; meningococcal; meningococcal conjugate vaccine; oropharyngeal carriage; high school students. Adolescents are at increased risk for infection with Neisseria meningitidis, an important cause of serious invasive disease, including meningitis and septicemia, in the United States [1]. Since 2005, the Advisory Committee on Immunization Practices has recommended quadrivalent meningococcal conjugate vaccine that covers serogroups A, C, W, and Y (MCV4) for all adolescents [2, 3].
Received 4 September 2014; accepted 11 November 2014; electronically published 11 December 2014. Presented in part: 16th International Pathogenic Neisseria Conference, Rotterdam, The Netherlands, September 2008. Correspondence: Lee H. Harrison, MD, 521 Parran Hall, 130 DeSoto St, Pittsburgh, PA 15261 ([email protected]). The Journal of Infectious Diseases® 2015;211:1761–8 © The Author 2014. Published by Oxford University Press on behalf of the Infectious Diseases Society of America. All rights reserved. For Permissions, please e-mail: [email protected]. DOI: 10.1093/infdis/jiu679
Nasopharyngeal carriage of N. meningitidis, a prerequisite for the development of invasive meningococcal disease, is in most cases asymptomatic and results in strain-specific immunity [4]. Meningococcal carriage rates are variable by age, with adolescents and young adults having the highest prevalence [5–14]. Because of high rates of carriage and evidence for transmission within families, adolescents are considered to be a primary reservoir for transmission to other groups, including young children and infants [15]. Polysaccharide-protein conjugate vaccines against Haemophilus influenzae type b and Streptococcus pneumoniae prevent acquisition of carriage, which interrupts transmission and leads to protection of unvaccinated persons [16, 17]. With the implementation of a national serogroup C vaccination program in the United Kingdom, substantial reductions in serogroup C meningococcal carriage and disease were observed in Carriage of N. meningitidis
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vaccinated persons, with similar declines in both carriage and disease occurring in the unvaccinated [5, 18–20]. Similarly, early results from the African meningitis belt suggest that the recently introduced serogroup A conjugate vaccine has led to interruption of transmission of serogroup A meningococcal carriage [21]. Such herd protection can dramatically enhance the public health benefits of conjugate vaccination programs. As a result, the ability of conjugate vaccines to prevent meningococcal carriage has become an important question during postlicensure evaluation. The main purpose of this study was to assess the impact of MCV4 on serogroup Y meningococcal carriage among Georgia and Maryland high school students. Serogroup Y was chosen because it caused approximately one third of the cases of meningococcal disease reported in the United States during 1996–2007 and was the most frequently isolated serogroup in a previous study of carriage among Georgia high school students [22]. We also sought to study the dynamics of carriage in this population. At the time of the study, the incidence of invasive meningococcal disease in the United States was falling to historically low levels [1]. During 2006–2007, MCV4 coverage rates among children 13–17 years old were estimated to be 11%–32% [23, 24]. METHODS Study Design
This study was approved by the institutional review boards of the Centers for Disease Control and Prevention, the Maryland Department of Health and Mental Hygiene, the Johns Hopkins Bloomberg School of Public Health, and the Georgia Department of Human Resources. Written informed consent was obtained for all participating students. For students 1 round. Rate ratios were calculated for serogroup Y carriage at vaccination versus control schools at the time of each survey. To further define the dynamics of carriage in this population, we assessed strain evolution and carriage with different strains among students with carriage during at least 2 surveys. Strain evolution was defined as carriage of an isolate of the same clonal complex (CC) but a different sequence type and/or change in the outer-membrane protein genotype. Strain replacement was defined as carriage of an isolate of a different CC. Genotyping was repeated on isolates to confirm suspected strain evolution. Risk factors for carriage were evaluated by comparing questionnaire answers from students who were carriers and those who were noncarriers. Risk factors were first assessed by stratified univariate logistic regression, using school as the stratification variable to adjust for clustering within schools on demographic, household, and symptom variables. Factors with a P value of 5 isolates each and represented 70% of all isolates recovered. Twenty-seven STs were represented by only 1 isolate each. Among CCs with >10 isolates, the most common CCs and the serogroup that was often associated with each CC ( pubmlst.org/neisseria), were ST-198, nongroupable capsule null locus (cnl) locus (73 isolates); ST-23 (61 isolates), serogroup Y; ST-41/44 (40 isolates), serogroup B; ST-60 (33 isolates), serogroup E; ST-1157 (21 isolates), encapsulated but nongroupable; ST-35 (19 isolates), serogroup B; and ST53 (10 isolates), nongroupable cnl (Figure 1). Among 98 students who had carriage on at least 2 occasions, strain evolution was observed in 5 students: 3 had a change in the porA allele, and 1 each had a change in the porB or fetA allele (Table 4). Two students were observed to have strain replacement. DISCUSSION The most remarkable finding of this study is that the prevalence of meningococcal carriage among Georgia and Maryland high school students was around 3%, which was much lower than expected on the basis of previous studies. For example, in a study among Georgia high school students in 1998 that use similar methods, overall carriage rates were 6.1%–7.7% [22]. Our observed carriage rate was also much lower than has been reported for high school students in Germany and the United Kingdom and for university students in the United Kingdom [5, 27–29]. Another striking finding is that the proportion of isolates that were phenotypically nongroupable was 88%, higher than in previous studies, in which approximately 30% and 60% of isolates from high school students in the United States and United Kingdom, respectively, were phenotypically nongroupable [5, 22]. Thus, the little carriage that we found was caused mostly by commensal meningococci that were not expressing capsule and were therefore unlikely to cause invasive disease. In addition, of the 7 CCs represented by >10 carriage isolates, only CC-41/44 and CC-23 were common causes of invasive disease in the United States during 2000–2005 [26]. A limitation of our study is that the phenotypic
Table 2. Frequency of Meningococcal Carriage Among High School Meningococcal Carriage Study Participants, by Phenotypic Serogroup, State, Vaccination Status of Schools, and Survey Round—Georgia and Maryland, 2006–2007 Round 1
Round 2 a
Serogroup State, School Group
Participants, No.
B
C
Y
Round 3 a
Serogroupa
Serogroup NGb
Totalc
Participants, No.
B
C
Y
NGb
Totalc
Participants, No.
B
C
Y
NGb
Totalc
All Vaccination
1731
0.35 (1.04) 0 (0) 0.35 (0.58) 2.83 (1.91)
3.52
1644
Control
1543
0.19 (1.10) 0 (0) 0.19 (0.39) 2.46 (1.36)
2.85
1469
Total
3274
0.27 (1.07) 0 (0) 0.27 (0.49) 2.66 (1.65)
3.21
3113
0.12 (0.61) 0 (0.12) 0.36 (0.79) 3.28 (2.25)
3.77
1549
0.20 (0.75) 2.52 (1.36)
2.72
1343
0.15 (0.74) 0 (0)
0.22 (0.89) 3.43 (2.16)
3.80
0.06 (0.61) 0 (0.06) 0.29 (0.77) 2.92 (1.83)
3.28
2892
0.07 (0.66) 0 (0.10) 0.28 (0.86) 3.67 (2.39)
4.01
0 (0.61) 0 (0)
0 (0.58) 0 (0.19) 0.32 (0.84) 3.87 (2.58)
4.20
Maryland Vaccination
795
0 (1.13) 0 (0) 0.75 (1.26) 3.65 (2.01)
4.40
758
0 (0.66) 0 (0.13) 0.66 (1.45) 4.49 (2.90)
5.15
709
0 (0.99) 0 (0.28) 0.56 (1.55) 5.22 (2.96)
5.78
Control
611
0 (1.15) 0 (0) 0.33 (0.65) 2.95 (1.47)
3.27
576
0 (0.87) 0 (0)
0.17 (0.52) 3.13 (1.91)
3.30
510
0 (0.98) 0 (0)
0.39 (1.37) 5.69 (3.73)
6.08
1406
0 (1.14) 0 (0) 0.57 (1.00) 3.34 (1.78)
3.91
1334
0 (0.75) 0 (0.07) 0.45 (1.05) 3.90 (2.47)
4.35
1219
0 (0.98) 0 (0.16) 0.49 (1.48) 5.41 (3.28)
5.91
0.23 (0.56) 0 (0.11) 0.11 (0.23) 2.26 (1.69)
Total Georgia
Carriage of N. meningitidis
Vaccination
936
0.64 (0.96) 0 (0)
2.14 (1.82)
2.78
886
Control
932
0.32 (1.07) 0 (0) 0.11 (0.21) 2.15 (1.29)
2.58
893
1868
0.48 (1.02) 0 (0) 0.05 (0.11) 2.14 (1.55)
2.68
1779
Total
0 (0)
2.60
840
0.22 (0.90) 2.13 (1.01)
2.35
833
0.11 (0.51) 0 (0.06) 0.17 (0.56) 2.19 (1.35)
2.47
1673
0 (0.45) 0 (0)
0 (0.24) 0 (0.12) 0.12 (0.24) 2.74 (2.26) 0.24 (0.60) 0 (0)
2.86
0.12 (0.60) 2.04 (1.20)
2.40
0.12 (0.42) 0 (0.06) 0.12 (0.42) 2.39 (1.73)
2.63
•
Abbreviations: NG, nongroupable; PCR, polymerase chain reaction. a The first value represents the percentage of participants with meningococcal carriage. The value in parentheses represents the percentage of participants with isolates that were genotypically groupable by serogroupspecific PCR. b The first value represents the percentage of participants with isolates that were negative by phenotypic serogrouping and are therefore presumed to not express capsule of the serogroups included in the assay (serogroups A, B, C, E, W, X, Y, and Z). The value in parentheses represents the percentage of participants with isolates that were negative by the serogroup-specific PCR assay (which includes groups A, B, C, W, X, and Y); this group likely represents a mix of isolates that are capsule null, belong to groups not included in the serogroup-specific PCR assay, or belong to groups included in the assay but are falsely negative because of polymorphisms in the serogroup-specific PCR primer binding sites. c The value represents the total percentage of participants with meningococcal carriage.
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Table 3. Univariate Analysis of Risk Factors for Carriage Among 189 Students Found to Be Carriers on ≥1 Occasion and 3122 Students Found to be Noncarriers on All Swab Surveys, Stratified by School to Adjust for Clustering Within School Characteristic
Carriers
Noncarriers
P Valuea
ORb(95% CI)
Meningococcal Carriage Among Georgia and Maryland High School Students Lee H. Harrison,1,3 Kathleen A. Shutt,3 Kathryn E. Arnold,4,5 Eric J. Stern,6,7 Tracy Pondo,6 Julia A. Kiehlbauch,2 Robert A. Myers,2 Rosemary A. Hollick,1 Susanna Schmink,6 Marianne Vello,4,5 David S. Stephens,4,8,9 Nancy E. Messonnier,6 Leonard W. Mayer,6 and Thomas A. Clark6 1
Department of International Health, Johns Hopkins Bloomberg School of Public Health, and 2Maryland Department of Health and Mental Hygiene, Baltimore, Maryland; 3Infectious Diseases Epidemiology Research Unit, University of Pittsburgh, Pennsylvania; 4Georgia Emerging Infections Program, 5 Division of Public Health, Georgia Department Human of Resources, 6National Center for Immunization and Respiratory Diseases, 7Epidemic Intelligence Service Program, Centers for Disease Control and Prevention, 8Emory University School of Medicine, and 9VA Medical Center, Atlanta, Georgia
Background. Meningococcal disease incidence in the United States is at an all-time low. In a previous study of Georgia high school students, meningococcal carriage prevalence was 7%. The purpose of this study was to measure the impact of a meningococcal conjugate vaccine on serogroup Y meningococcal carriage and to define the dynamics of carriage in high school students. Methods. This was a prospective cohort study at 8 high schools, 4 each in Maryland and Georgia, during a school year. Students at participating schools received quadrivalent meningococcal conjugate vaccine that uses diphtheria toxoid as the protein carrier (MCV4-DT). In each state, 2 high schools were randomly assigned for MCV4-DT receipt by students at the beginning of the study, and 2 were randomly assigned for MCV4-DT receipt at the end. Oropharyngeal swab cultures for meningococcal carriage were performed 3 times during the school year. Results. Among 3311 students, the prevalence of meningococcal carriage was 3.21%–4.01%. Phenotypically nongroupable strains accounted for 88% of carriage isolates. There were only 5 observed acquisitions of serogroup Y strains during the study; therefore, the impact of MCV4-DT on meningococcal carriage could not be determined. Conclusions. Meningococcal carriage rates in US high school students were lower than expected, and the vast majority of strains did not express capsule. These findings may help explain the historically low incidence of meningococcal disease in the United States. Keywords. Neisseria meningitidis; meningococcus; meningococcal; meningococcal conjugate vaccine; oropharyngeal carriage; high school students. Adolescents are at increased risk for infection with Neisseria meningitidis, an important cause of serious invasive disease, including meningitis and septicemia, in the United States [1]. Since 2005, the Advisory Committee on Immunization Practices has recommended quadrivalent meningococcal conjugate vaccine that covers serogroups A, C, W, and Y (MCV4) for all adolescents [2, 3].
Received 4 September 2014; accepted 11 November 2014; electronically published 11 December 2014. Presented in part: 16th International Pathogenic Neisseria Conference, Rotterdam, The Netherlands, September 2008. Correspondence: Lee H. Harrison, MD, 521 Parran Hall, 130 DeSoto St, Pittsburgh, PA 15261 ([email protected]). The Journal of Infectious Diseases® 2015;211:1761–8 © The Author 2014. Published by Oxford University Press on behalf of the Infectious Diseases Society of America. All rights reserved. For Permissions, please e-mail: [email protected]. DOI: 10.1093/infdis/jiu679
Nasopharyngeal carriage of N. meningitidis, a prerequisite for the development of invasive meningococcal disease, is in most cases asymptomatic and results in strain-specific immunity [4]. Meningococcal carriage rates are variable by age, with adolescents and young adults having the highest prevalence [5–14]. Because of high rates of carriage and evidence for transmission within families, adolescents are considered to be a primary reservoir for transmission to other groups, including young children and infants [15]. Polysaccharide-protein conjugate vaccines against Haemophilus influenzae type b and Streptococcus pneumoniae prevent acquisition of carriage, which interrupts transmission and leads to protection of unvaccinated persons [16, 17]. With the implementation of a national serogroup C vaccination program in the United Kingdom, substantial reductions in serogroup C meningococcal carriage and disease were observed in Carriage of N. meningitidis
•
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1761
vaccinated persons, with similar declines in both carriage and disease occurring in the unvaccinated [5, 18–20]. Similarly, early results from the African meningitis belt suggest that the recently introduced serogroup A conjugate vaccine has led to interruption of transmission of serogroup A meningococcal carriage [21]. Such herd protection can dramatically enhance the public health benefits of conjugate vaccination programs. As a result, the ability of conjugate vaccines to prevent meningococcal carriage has become an important question during postlicensure evaluation. The main purpose of this study was to assess the impact of MCV4 on serogroup Y meningococcal carriage among Georgia and Maryland high school students. Serogroup Y was chosen because it caused approximately one third of the cases of meningococcal disease reported in the United States during 1996–2007 and was the most frequently isolated serogroup in a previous study of carriage among Georgia high school students [22]. We also sought to study the dynamics of carriage in this population. At the time of the study, the incidence of invasive meningococcal disease in the United States was falling to historically low levels [1]. During 2006–2007, MCV4 coverage rates among children 13–17 years old were estimated to be 11%–32% [23, 24]. METHODS Study Design
This study was approved by the institutional review boards of the Centers for Disease Control and Prevention, the Maryland Department of Health and Mental Hygiene, the Johns Hopkins Bloomberg School of Public Health, and the Georgia Department of Human Resources. Written informed consent was obtained for all participating students. For students 1 round. Rate ratios were calculated for serogroup Y carriage at vaccination versus control schools at the time of each survey. To further define the dynamics of carriage in this population, we assessed strain evolution and carriage with different strains among students with carriage during at least 2 surveys. Strain evolution was defined as carriage of an isolate of the same clonal complex (CC) but a different sequence type and/or change in the outer-membrane protein genotype. Strain replacement was defined as carriage of an isolate of a different CC. Genotyping was repeated on isolates to confirm suspected strain evolution. Risk factors for carriage were evaluated by comparing questionnaire answers from students who were carriers and those who were noncarriers. Risk factors were first assessed by stratified univariate logistic regression, using school as the stratification variable to adjust for clustering within schools on demographic, household, and symptom variables. Factors with a P value of 5 isolates each and represented 70% of all isolates recovered. Twenty-seven STs were represented by only 1 isolate each. Among CCs with >10 isolates, the most common CCs and the serogroup that was often associated with each CC ( pubmlst.org/neisseria), were ST-198, nongroupable capsule null locus (cnl) locus (73 isolates); ST-23 (61 isolates), serogroup Y; ST-41/44 (40 isolates), serogroup B; ST-60 (33 isolates), serogroup E; ST-1157 (21 isolates), encapsulated but nongroupable; ST-35 (19 isolates), serogroup B; and ST53 (10 isolates), nongroupable cnl (Figure 1). Among 98 students who had carriage on at least 2 occasions, strain evolution was observed in 5 students: 3 had a change in the porA allele, and 1 each had a change in the porB or fetA allele (Table 4). Two students were observed to have strain replacement. DISCUSSION The most remarkable finding of this study is that the prevalence of meningococcal carriage among Georgia and Maryland high school students was around 3%, which was much lower than expected on the basis of previous studies. For example, in a study among Georgia high school students in 1998 that use similar methods, overall carriage rates were 6.1%–7.7% [22]. Our observed carriage rate was also much lower than has been reported for high school students in Germany and the United Kingdom and for university students in the United Kingdom [5, 27–29]. Another striking finding is that the proportion of isolates that were phenotypically nongroupable was 88%, higher than in previous studies, in which approximately 30% and 60% of isolates from high school students in the United States and United Kingdom, respectively, were phenotypically nongroupable [5, 22]. Thus, the little carriage that we found was caused mostly by commensal meningococci that were not expressing capsule and were therefore unlikely to cause invasive disease. In addition, of the 7 CCs represented by >10 carriage isolates, only CC-41/44 and CC-23 were common causes of invasive disease in the United States during 2000–2005 [26]. A limitation of our study is that the phenotypic
Table 2. Frequency of Meningococcal Carriage Among High School Meningococcal Carriage Study Participants, by Phenotypic Serogroup, State, Vaccination Status of Schools, and Survey Round—Georgia and Maryland, 2006–2007 Round 1
Round 2 a
Serogroup State, School Group
Participants, No.
B
C
Y
Round 3 a
Serogroupa
Serogroup NGb
Totalc
Participants, No.
B
C
Y
NGb
Totalc
Participants, No.
B
C
Y
NGb
Totalc
All Vaccination
1731
0.35 (1.04) 0 (0) 0.35 (0.58) 2.83 (1.91)
3.52
1644
Control
1543
0.19 (1.10) 0 (0) 0.19 (0.39) 2.46 (1.36)
2.85
1469
Total
3274
0.27 (1.07) 0 (0) 0.27 (0.49) 2.66 (1.65)
3.21
3113
0.12 (0.61) 0 (0.12) 0.36 (0.79) 3.28 (2.25)
3.77
1549
0.20 (0.75) 2.52 (1.36)
2.72
1343
0.15 (0.74) 0 (0)
0.22 (0.89) 3.43 (2.16)
3.80
0.06 (0.61) 0 (0.06) 0.29 (0.77) 2.92 (1.83)
3.28
2892
0.07 (0.66) 0 (0.10) 0.28 (0.86) 3.67 (2.39)
4.01
0 (0.61) 0 (0)
0 (0.58) 0 (0.19) 0.32 (0.84) 3.87 (2.58)
4.20
Maryland Vaccination
795
0 (1.13) 0 (0) 0.75 (1.26) 3.65 (2.01)
4.40
758
0 (0.66) 0 (0.13) 0.66 (1.45) 4.49 (2.90)
5.15
709
0 (0.99) 0 (0.28) 0.56 (1.55) 5.22 (2.96)
5.78
Control
611
0 (1.15) 0 (0) 0.33 (0.65) 2.95 (1.47)
3.27
576
0 (0.87) 0 (0)
0.17 (0.52) 3.13 (1.91)
3.30
510
0 (0.98) 0 (0)
0.39 (1.37) 5.69 (3.73)
6.08
1406
0 (1.14) 0 (0) 0.57 (1.00) 3.34 (1.78)
3.91
1334
0 (0.75) 0 (0.07) 0.45 (1.05) 3.90 (2.47)
4.35
1219
0 (0.98) 0 (0.16) 0.49 (1.48) 5.41 (3.28)
5.91
0.23 (0.56) 0 (0.11) 0.11 (0.23) 2.26 (1.69)
Total Georgia
Carriage of N. meningitidis
Vaccination
936
0.64 (0.96) 0 (0)
2.14 (1.82)
2.78
886
Control
932
0.32 (1.07) 0 (0) 0.11 (0.21) 2.15 (1.29)
2.58
893
1868
0.48 (1.02) 0 (0) 0.05 (0.11) 2.14 (1.55)
2.68
1779
Total
0 (0)
2.60
840
0.22 (0.90) 2.13 (1.01)
2.35
833
0.11 (0.51) 0 (0.06) 0.17 (0.56) 2.19 (1.35)
2.47
1673
0 (0.45) 0 (0)
0 (0.24) 0 (0.12) 0.12 (0.24) 2.74 (2.26) 0.24 (0.60) 0 (0)
2.86
0.12 (0.60) 2.04 (1.20)
2.40
0.12 (0.42) 0 (0.06) 0.12 (0.42) 2.39 (1.73)
2.63
•
Abbreviations: NG, nongroupable; PCR, polymerase chain reaction. a The first value represents the percentage of participants with meningococcal carriage. The value in parentheses represents the percentage of participants with isolates that were genotypically groupable by serogroupspecific PCR. b The first value represents the percentage of participants with isolates that were negative by phenotypic serogrouping and are therefore presumed to not express capsule of the serogroups included in the assay (serogroups A, B, C, E, W, X, Y, and Z). The value in parentheses represents the percentage of participants with isolates that were negative by the serogroup-specific PCR assay (which includes groups A, B, C, W, X, and Y); this group likely represents a mix of isolates that are capsule null, belong to groups not included in the serogroup-specific PCR assay, or belong to groups included in the assay but are falsely negative because of polymorphisms in the serogroup-specific PCR primer binding sites. c The value represents the total percentage of participants with meningococcal carriage.
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Table 3. Univariate Analysis of Risk Factors for Carriage Among 189 Students Found to Be Carriers on ≥1 Occasion and 3122 Students Found to be Noncarriers on All Swab Surveys, Stratified by School to Adjust for Clustering Within School Characteristic
Carriers
Noncarriers
P Valuea
ORb(95% CI)
