Nasal carriage of Streptococcus pneumoniae serotypes and
Staphylococcus aureus in Streptococcus pneumoniae-vaccinated
and non-vaccinated young children
N. H. T. M. DUKERS-MUIJRERS1,2*, E. STOBBERINGH2, P. BEISSER2,
R. C. H. BOESTEN1, P. JACOBS3AND C. J. P. A. HOEBE1,2
1Department of Sexual Health, Infectious Diseases and Environmental Health, South Limburg Public Health
Service, Geleen, The Netherlands
2Department of Medical Microbiology, School of Public Health and Primary Care (CAPHRI), Maastricht
University Medical Centre (MUMC+), Maastricht, The Netherlands
3Department of Infectious Diseases, Northern Limburg Public Health Service, The Netherlands
Received 13 March 2012; Final revision 26 April 2012; Accepted 14 May 2012
Since the implementation of Streptococcus pneumoniae (SPn) conjugate vaccination (PCV),
non-vaccine types have prevailed in invasive pneumococcal disease (IPD), and an increase in
Staphylococcus aureus (SA) burden has been suggested. Here, we assess the epidemiology of SA
and SPn nasal carriage in 620 children at day-care centres; 141 of these children had received 1–4
PCV7 doses. A higher vaccine dosage was associated with non-vaccine-type SPn carriage. Of all
SPn isolates, 45% were PCV7 types, 1% were additional PCV10 types and 22% were the three
additional PCV13 types. SA carriage was inversely associated with vaccine-type SPn carriage.
SPn serotype 19A showed higher SA co-carriage rates compared to other SPn serotypes. PCV7
implementation does not prevent children from being part of the IPD-related SPn transmission
chain. These results contribute to the monitoring of SA- and SPn-related disease and add to the
debate on the current national vaccination policy that recently included a change from PCV7
Key words: Antibiotic resistance, children, day-care centres, Staphylococcus aureus,
Streptococcus pneumoniae, vaccination.
Streptococcus pneumoniae (SPn) causes about 11% of
all deaths in children aged <5 years and is a leading
cause of bacterial pneumonia, meningitis, and sepsis
in children worldwide . Several countries, including
The Netherlands, have implemented the pneumo-
coccal conjugate vaccine (PCV), which has proved
effective in preventing invasive diseases with SPn in
young children [1–6]. However, the incidence of in-
vasive pneumococcal disease (IPD) caused by non-
vaccine SPn serotypes is substantially increasing. The
most common types found in IPD isolates since the
introduction of PCV7 in Belgium, France, Germany,
Greece, Norway, Portugal, Spain, UK and The
Netherlands are the non-PCV7 serotypes 1, 3, 6A, 7F,
* Author for correspondence: Dr N. H. T. M. Dukers-Muijrers,
Department of Sexual Health, Infectious Diseases and Environ-
mental Health, South Limburg Public Health Service, P.O. Box
2022, 6160 HA Geleen, The Netherlands.
Part of this study was also presented at ECCMID 2008, Barcelona,
Spain and at ESCAIDE 2010, Lisbon, Portugal.
Epidemiol. Infect., Page 1 of 8.
f Cambridge University Press 2012
and 19A; these serotypes are all included in PCV13
[6, 7]. Serotype 19A currently poses a major concern
as its carriage rates have rapidly increased. This sero-
type has emerged as the major cause of otitis media
in children, and in the USA its strains are fre-
quently multiresistant to antibiotics [8, 9]. In the pre-
vaccination era, the most common serotypes found
in IPD isolates were PCV7 types 14, 6B, 19F, and
23F [7, 10].
Invasive disease is preceded by the establishment of
a bacterial population in the nasal passages and the
competition of this population with other bacteria in
the host. Several epidemiological studies have dem-
onstrated lower SPn carriage rates in the presence of
Staphylococcus aureus (SA) nasal carriage [11–15]. In
young children, SA is the main cause of impetigo
contagiosa, which can lead to otitis media, and the
most common cause of severe pneumonia after an
influenza virus infection . Epidemiological studies
in the pre-PCV era demonstrated an inverse relation-
ship between SA and vaccine SPn serotypes but not
for non-vaccine SPn serotypes. One study conducted
after vaccine implementation also showed such in-
verse association for vaccine serotypes . Two other
studies could not demonstrate an inverse effect for
either vaccine or non-vaccine types  or overall SPn
carriage, without analysing the serotypes separately
types replace vaccine types and the carriage rate of
non-vaccine types increases . This mechanism
may lead to a rise in SA carriage rates [12, 15]. The
changing epidemiology of SPn and possibly SA in the
vaccine era requires further monitoring for a better
understanding of the carriage of these bacteria and
related invasive bacterial diseases. This understanding
is relevant not only to the case of PCV7 vaccination
but also to developing strategies for using higher
valent vaccines and preventing serotype replacement
The current cross-sectional study was conducted in
PCV7-vaccinated and non-vaccinated young children.
Our aim is to assess nasal carriage and determinants
of SPn and SA carriage. Therefore, we focus on their
interrelationship and explore the role of serotypes,
age and number of PCV7 doses in SPn and SA car-
MATERIALS AND METHODS
Procedures and study population
In The Netherlands, neonates have been vaccinated
with PCV7 since April 2006 with a four-dose schedule
administered at ages 2, 3, 4, and 11 months; vacci-
nations are registered, and there is no catch-up vac-
cination programme for children born before April
The current cross-sectional study was conducted in
a convenience sample of children (aged 6 weeks to 4
years) who attended 48 randomly chosen day-care
centres out of a total of 150 in the province of
Limburg, The Netherlands. After obtaining written
informed consent from at least one of the parents/
guardians, a nasal swab was taken from the partici-
pating child and a standardized short questionnaire
was completed by the parent. The study population
comprised 620 children. Approval for this study was
obtained from the Medical Ethical Committee of
Maastricht University (no. 104112).
On the same day of collection, the nasal swabs
were forwarded to the Microbiology Laboratory of
University Hospital Maastricht for testing on SA and
SPn using standard biochemical tests. Serotyping was
performed as previously described, using antiserum
from Statens Serum Institute (Denmark) . Of all
the SPn isolates, 20 were unavailable for typing and
six were non-typable.
Table 1. Nasal carriage rates for heptavalent
pneumococcal conjugate vaccine (PCV7) serotypes and
a selection of non-PCV7 types in 620 children aged
between 0 and 4 years attending day-care centres
* Denominator excludes 20 participants with no isolates
available for typing.
# Serotypes additionally included in PCV10.
$ Serotypes additionally included in PCV13.
· Number of isolates was <15 for all serotypes, including
six untypable isolates.
2 N. H. T. M. Dukers-Muijrers and others
Variables and statistical analyses
Univariate and multivariate logistic regression analy-
ses were performed to identify independent determi-
nants for SA and SPn carriage. The determinants of
interest included carriage of SA, SPn and specific SPn
serotypes. Age as a determinant was presented using
polynomials (quintic function) and was tested by
using two first-order splines describing monthly
trends and by constructing two age groups (cut-off at
15 months). Finally, the number of PCV7 doses was
included (continuous variable). Reduced-dose PCV7
schedules have reportedly been effective in reducing
vaccine-type carriage, and schedules with more doses
have been associated with higher serotype 19A car-
riage rates [22–24]. Other determinants, including
gender,householdsize, andpet/cattle ownership, were
not found to be significantly associated with SA or
SPn carriage; thus, these results are not presented.
For the entire group, the correlation between age
and number of vaccine doses was relatively high
(r=0.7) as vaccination was largely dependent on a
child’s age at time of study (only children aged <15
months were eligible for vaccination). Furthermore,
both SA and SPn carriage rates are known to change
substantially with age in young children [11, 25].
Therefore, when evaluating vaccination as a determi-
nant, only children aged <15 months were included
in the analyses (at this age, the correlation between
age and number of vaccine doses is r=0.3). We con-
sidered a P value f0.05 as statistically significant.
Analyses were performed with SPSS package version
14.0.2 (SPSS Inc., USA).
Of the 620 participants, 453 (73.1%) children
were aged o15 months and were born in the pre-
PCV7 vaccination era, and although no data on their
vaccination status are available, these children were
unlikely to have been vaccinated. Of the 167 younger
children, 14 had received one or two PCV7 vaccine
doses, 86 had received three doses, 41 had completed
the four-dose schedule, and 26 were unvaccinated.
Carriage of SA and SPn serotypes
The overall carriage rates were 19.8% (n=123) for
SA and 37.3% (n=231) for SPn; 45% (n=95) of the
Children born during PCV7
Children PCV7 unvaccinated
Carriage rate of SPn ( %)
trend line (dotted): quintic function
Carriage rate of SA ( %)
trend line: quintic function
12 1518 2124 27 30 33 3639 42 45 48
Fig. 1. Age-related Streptococcus pneumoniae (SPn) and Staphylococcus aureus (SA) carriage in 620 children aged between 0
and 4 years attending day-care centres.
S. pneumoniae and S. aureus in (un)vaccinated children3
Table 2. Carriage rates of Streptococcus pneumoniae (SPn) and Staphylococcus aureus (SA) serotypes in relation to the number of received doses of
heptavalent pneumococcal conjugate vaccine (PCV7) and to age in 620 children aged between 0 and 4 years attending day-care centres
(Co-)carriage rate, n (%)#
Age <15 months
1 or 2 PCV7
3 PCV7 doses
4 PCV7 doses
Age <15 months
Age 15–48 months
SPn (all types)
SPn vaccine types
SPn non-vaccine types
SPn vaccine type 6B
SPn vaccine type 14
SPn vaccine type 19F
SPn vaccine type 23F
SPn non-vaccine type 6A
SPn non-vaccine type 19A
SA and SPn
SA and SPn vaccine types
SA and SPn non-vaccine types
# Denominator excludes the 20 isolates that were not typed.
$ x2test for linear trend in the association between number of PCV7 doses and carriage rate.
· x2test of the association between carriage rate and age group.
# Pf0.10, * Pf0.05, ** pf0.01.
N. H. T. M. Dukers-Muijrers and others
SPn isolates were PCV7 types, two (0.9%) were ad-
ditional PCV10 types and 46 (21.8%) were the three
additional PCV13 types. The carriage rates of the
PCV7 types and non-vaccine types were 15.8% and
19.3%, respectively. Vaccine types 6B, 14, 19F, and
23F, and non-vaccine types 6A and 19A were the
most common (Table 1).
Age-related carriage of SA and SPn showed divergent
curvilinear trends (Fig. 1). A significant decrease in
SA carriage was observed in children aged <15
months [odds ratio (OR) per month 0.9, 95% confi-
dence interval (CI) 0.6–1.0]. Compared to the older
children, children aged <15 months (Table 2) had
higher SA carriage rates (OR 1.8, 95% CI 1.2–2.8),
higher co-carriage rates of SA and non-vaccine
SPn types (OR 4.1, 95% CI 1.5–10.8), and lower
carriage rates of SPn vaccine types (OR 0.6, 95% CI
Vaccination and carriage in children aged <15
The number of vaccine doses (Table 2) was not as-
sociatedwithSA carriage, SPncarriageorvaccine-type
carriage. However, an increase in non-vaccine-type
carriage (OR per dose 1.5, 95% CI 1.0–2.1) and in
co-carriage of SA and non-vaccine types (OR per
dose 2.3, 95% CI 0.9–5.8) was observed, although the
latter association had only borderline significance
(P=0.07). Adjusting for age did not substantially
change the association estimates for SPn, although
for SA, the association with number of vaccine doses
became somewhat stronger (adjusted OR 1.44, 95%
CI 0.98–2.11, P=0.06).
Interrelationship between SA and SPn carriage
Of all the children, 32.4% (n=201) exhibited only
SPn carriage, 15% (n=93) had only SA carriage, and
4.8% (n=30) had SA-SPn co-carriage. An inverse as-
sociation was present between SA and SPn carriage,
between SA and vaccine-type SPn carriage, and be-
tween SA and non-vaccine-type SPn carriage, al-
though this last association had only borderline
significance (Table 3). Risk estimates were similar for
the younger and older children (interaction terms
P>0.1) and when adjusting for PCV7 dose or age.
A notable serotype-specific pattern was observed in
that the highest SA co-carriage rate occurred with
serotype 19A (Fig. 2). Compared to children carrying
SPn type 19A, the SA carriage rate was lower in
children carrying SPn type 6A (OR 0.2, 95% CI
0.03–1.0), type 23F (OR 0.1, 95% CI 0.01–1.0), and
type 14 (OR 0.1, 95% CI 0.01–1.2), although this last
serotype had only borderline significance (P=0.06).
Other categories that were non-significant included
SPn-negative children and children carrying type 19F,
type 14, type 6B, other vaccine types and other non-
vaccine types. Adjusting for age did not substantially
change the risk estimates, while subsidiary analysis
adjusting for PCV7 dose in young children was not
possible due to the small number of cases.
The current study assessed nasal carriage rates of
SA and SPn serotypes and their interrelationship
in PCV7-vaccinated and non-vaccinated children
attending day-care centres.The carriageof non-vaccine
types increased with the number of administered
PCV7 doses. The rate of co-carriage between SA and
SPn vaccine types was low; however, SA and non-
vaccine-type SPn co-carriage was associated with
young age and had a tendency to increase with
vaccination. The SA carriage rate was remarkably
high in children carrying non-vaccine-type 19A.
The observed inverse association between SA and
SPn vaccine types agrees with previous studies
[11–15]. Our findings did not provide direct evidence
for the hypothesis [12, 15] that the overall SA carriage
rate would increase with vaccination, although a
tendency to increase was noted after correcting for the
opposing effect of age. Notably, co-carriage with non-
vaccine types tended to occur most frequently in vac-
cinated children. Marked serotype-specific patterns
were also observed. The non-vaccine serotype 19A
Table 3. Univariate associations between
Streptococcus pneumoniae (SPn) and Staphylococcus
aureus carriage in 620 children aged between 0 and 4
years attending day-care centres
Total group (n=620)
OR (95% CI)
SPn (all types)#
SPn vaccine types
SPn non-vaccine types
OR, Odds ratio; CI, confidence interval.
# Of all 233 SPn isolates, 20 were not serotyped.
# Pf0.10, * Pf0.05, ** Pf0.01.
S. pneumoniae and S. aureus in (un)vaccinated children5
showed higher SA carriage rates than did several
other serotypes. Previous studies have found that in
unvaccinated individuals, successful nasal SA colon-
ization is independent of both SA and SPn genotypes
[11, 26]. No major differences between SA clones have
been found regarding their capacity to compete with
SPn types  and no association between the levels
of IgG and IgA in the child vs. colonization status has
been reported . It is possible that the virtual ab-
sence of a pilus-like structure (i.e. an adhesin and in-
flammatory virulence factor) in serotype 19A may
have played a role in this result. Some, but not all,
studies have shown lower odds for co-colonization
with a non-piliated SPn type [26, 29]. The mechanism
of the negative association between SPn and SA
is likely to be multi-factorial, involving both host
immune responses and bacterial characteristics that
may inhibit the other pathogen. In addition, the
serotype-specific associations observed may reflect
an epidemiological association, and further study is
needed to address this interesting phenomenon.
Our study further confirmed an increase in non-
vaccine types after the implementation of PCV7 vac-
cination . SPn serotype 19A rates have been
reported to increase [21–24, 30], but in our study, the
number of cases was too small to demonstrate such
serotype-specific associations. In Europe, the non-
PCV7 types 1, 3, 6A, 7F and 19A have become the
most common IPD isolates, all of which are targeted
by PCV13 [6, 7]. Vaccination does not preclude chil-
dren from becoming part of the IPD-related SPn
transmission chain. For example, in the specific case
of The Netherlands, a country with high vaccination
coverage (y95%), it was recently reported that 3
years after PCV7 implementation, 23% of infants
aged 11 or 24 months carried serotypes targeted by
PCV13 . However, in 2011, The Netherlands
changed to PCV10. PCV10 additionally targets sero-
types 1, 5 and 7F, which show very low carriage rates
in Dutch children, but does not include the important
PCV13 types 3, 6A and 19A. As advised by the Dutch
Health Council  PCV13 rather than PCV10 is
likely to be the better choice in The Netherlands for
preventing IPD .
In our study, vaccination was not associated with
a reduced overall nasal SPn carriage, which is in
agreement with other carriage studies . However,
proceeding further into the vaccination era, some
reports suggest that the decline in PCV7 types may
be starting to outweigh the non-vaccine-type in-
crease, resulting in an overall decrease in SPn carriage
[22, 23, 33].
The current study has several limitations. Some
colonization with SPn may have been overlooked as
the tested samples were taken from the anterior nares
and not from the nasopharyngeal site, which is the
most common sampling site. However, anterior nares
sampling has been previously used to describe the
epidemiology of SPn [17, 34] and our sampling
method was unlikely to result in a substantial bias of
the results. However, the serotype-specific carriage
rates may be slightly underestimated due to the fact
that the serotype could not be determined for 17 un-
vaccinated and three vaccinated children. Finally, the
assessment of the effect of vaccination was somewhat
limited by the small numbers in the young age group;
Type 14 Type 19FType 23F
Non-PCV7 serotypes PCV7 serotypes:
4, 6B, 9V, 14, 18C, 19F, 23F
Fig. 2. Carriage rate of Staphylococcus aureus (SA) stratified by co-carriage of Streptococcus pneumoniae (SPn) (by serotype)
in 620 children aged between 0 and 4 years attending day-care centres.
6 N. H. T. M. Dukers-Muijrers and others
thus, the results for the effect of vaccination should be
interpreted with caution.
In conclusion, vaccinated children are still part of
the IPD-related transmission chain. Current findings
show that, at least on an epidemiological scale, the
dynamics of SPn and SA carriage influence each other
and are influenced by vaccination, and close moni-
toring remains essential for designing and evaluating
infection prevention strategies.
(1) Overall SPn carriage and carriage of non-vaccine
serotypes commonly found in IPD are not re-
duced after PCV7 vaccination.
(2) Although co-carriage rates of SA and SPn are
generally low, co-carriage rates with SA and SPn
non-vaccine types are higher in young children,
especially those vaccinated with PCV7.
(3) The rate of SA co-carriage is highest in children
carrying SPn serotype 19A.
This study was supported by an unrestricted grant
from the Centre for Infectious Disease Control of
the National Institute for Public Health and the
Environment (RIVM), The Netherlands. The authors
thank Kim Ottenheim of the Public Health Services of
North Limburg for collecting samples and organizing
logistics, the staff of the Medical Microbiology
Laboratory, Maastricht University Centre, and Els
Verhaagh, Elisabeth Hospital Tilburg, for conducting
laboratory analyses. We thank RIVM for funding
DECLARATION OF INTEREST
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8 N. H. T. M. Dukers-Muijrers and others