Baseline meningococcal carriage in Burkina Faso before the introduction of a meningococcal serogroup A conjugate vaccine.
ABSTRACT The serogroup A meningococcal conjugate vaccine MenAfriVac has the potential to confer herd immunity by reducing carriage prevalence of epidemic strains. To better understand this phenomenon, we initiated a meningococcal carriage study to determine the baseline carriage rate and serogroup distribution before vaccine introduction in the 1- to 29-year old population in Burkina Faso, the group chosen for the first introduction of the vaccine. A multiple cross-sectional carriage study was conducted in one urban and two rural districts in Burkina Faso in 2009. Every 3 months, oropharyngeal samples were collected from >5,000 randomly selected individuals within a 4-week period. Isolation and identification of the meningococci from 20,326 samples were performed by national laboratories in Burkina Faso. Confirmation and further strain characterization, including genogrouping, multilocus sequence typing, and porA-fetA sequencing, were performed in Norway. The overall carriage prevalence for meningococci was 3.98%; the highest prevalence was among the 15- to 19-year-olds for males and among the 10- to 14-year-olds for females. Serogroup Y dominated (2.28%), followed by serogroups X (0.44%), A (0.39%), and W135 (0.34%). Carriage prevalence was the highest in the rural districts and in the dry season, but serogroup distribution also varied by district. A total of 29 sequence types (STs) and 51 porA-fetA combinations were identified. The dominant clone was serogroup Y, ST-4375, P1.5-1,2-2/F5-8, belonging to the ST-23 complex (47%). All serogroup A isolates were ST-2859 of the ST-5 complex with P1.20,9/F3-1. This study forms a solid basis for evaluating the impact of MenAfriVac introduction on serogroup A carriage.
- [show abstract] [hide abstract]
ABSTRACT: The epidemiology of infection due to Neisseria meningitidis and Neisseria lactamica was studied in a northern Nigerian community. A low meningococcal carriage rate was observed throughout the two-year survey. Initially, most meningococci isolated from nasopharyngeal carriers belonged to serogroup C or to serogroup Y. Following an outbreak of group A meningococcal disease, more group A meningococcal carriers were detected. Antibody studies indicated that infection with group A meningococci had been more widespread in the community than was suggested by regular carrier surveys. Carriage of meningococci was detected most frequently in children one to nine years of age. Children were identified as the first carriers in households more frequently than adults. The half-life of carriage was three months. The meningococcal carriage rate did not increase during the hot dry season when epidemics of meningococcal disease occur most frequently in Nigeria. Neisseria lactamica was isolated from the nasopharynx of children more frequently than were meningococci.The Journal of Infectious Diseases 12/1982; 146(5):626-37. · 5.85 Impact Factor
- [show abstract] [hide abstract]
ABSTRACT: Meningococcal disease occurs worldwide with incidence rates varying from 1 to 1000 cases per 100,000. The causative organism, Neisseria meningitidis, is an obligate commensal of humans, which normally colonizes the mucosa of the upper respiratory tract without causing invasive disease, a phenomenon known as carriage. Studies using molecular methods have demonstrated the extensive genetic diversity of meningocococci isolated from carriers, in contrast to a limited number of genetic types, known as the hyperinvasive lineages, associated with invasive disease. Population and evolutionary models that invoke positive selection can be used to resolve the apparent paradox of virulent lineages persisting during the global spread of a non-clonal and normally commensal bacterium. The application of insights gained from studies of meningococcal population biology and evolution is important in understanding the spread of disease, as well as in vaccine development and implementation, especially with regard to the challenge of producing comprehensive vaccines based on sub-capsular antigens and measuring their effectiveness.Vaccine 06/2009; 27 Suppl 2:B64-70. · 3.77 Impact Factor
- [show abstract] [hide abstract]
ABSTRACT: Neisseria meningitidis, an obligate commensal of humans, normally colonizes the mucosa of the upper respiratory tract without affecting the host, a phenomenon known as carriage. In Europe, as much as 35% of young adults are carriers at a given time. Recent studies using molecular methods for clone identification have demonstrated the extensive genetic diversity of the strains isolated from carriers, in comparison with a limited number of hypervirulent strains associated with invasive disease. Published studies and new data generated through the framework of the EU-MenNet clearly indicated significant differences in pathogenicity between meningococcal clones and in the distribution of multilocus sequence types among isolates from asymptomatic carriers among European countries; simultaneous carriage of more than one meningococcal strain in the throat is rare, but occasionally occurs; and the commensal association of particular clones with a host is a long-term relationship, often lasting several months. Further investigations of the carrier state are warranted to improve our understanding of the epidemiology and pathogenesis of meningococcal disease, as well as to support the introduction and to measure the impact of mass vaccination.FEMS Microbiology Reviews 02/2007; 31(1):52-63. · 13.23 Impact Factor
CLINICAL AND VACCINE IMMUNOLOGY, Mar. 2011, p. 435–443
Copyright © 2011, American Society for Microbiology. All Rights Reserved.
Vol. 18, No. 3
Baseline Meningococcal Carriage in Burkina Faso before the Introduction of
a Meningococcal Serogroup A Conjugate Vaccine?
Paul A. Kristiansen,1Fabien Diomande ´,2,3Stanley C. Wei,3Rasmata Oue ´draogo,4Lassana Sangare ´,5
Idrissa Sanou,6Denis Kandolo,2,7Pascal Kabore ´,8Thomas A. Clark,3Abdoul-Salam Oue ´draogo,6
Ki Ba Absatou,9Charles D. Oue ´draogo,10Musa Hassan-King,11Jennifer Dolan Thomas,3
Cynthia Hatcher,3Mamoudou Djingarey,2Nancy Messonnier,3Marie-Pierre Pre ´ziosi,12
Marc LaForce,11and Dominique A. Caugant1,13*
Norwegian Institute of Public Health, Oslo, Norway1; WHO Inter Country Support Team, Ouagadougou, Burkina Faso2; Centers for
Disease Control and Prevention, Atlanta, Georgia3; Centre Hospitalier Universitaire Pe ´diatrique Charles de Gaulle4and
Centre Hospitalier Universitaire Yalgado,5Ouagadougou, Burkina Faso; Centre Hospitalier Universitaire Souro Sanou,
Bobo-Dioulasso, Burkina Faso6; WHO Multi Disease Surveillance Center, Ouagadougou, Burkina Faso7; Direction de la
Lutte contre la Maladie, Ministry of Health,8and Laboratoire National de Sante ´ Publique,9Ouagadougou,
Burkina Faso; Centre Hospitalier Re ´gional Kaya, Kaya, Burkina Faso10; Meningitis Vaccine Project,
Ferney, France11; WHO Initiative for Vaccine Research, Geneva, Switzerland12; and
Faculty of Medicine, University of Oslo, Oslo, Norway13
Received 29 October 2010/Returned for modification 1 December 2010/Accepted 17 December 2010
The serogroup A meningococcal conjugate vaccine MenAfriVac has the potential to confer herd immunity by
reducing carriage prevalence of epidemic strains. To better understand this phenomenon, we initiated a
meningococcal carriage study to determine the baseline carriage rate and serogroup distribution before vaccine
introduction in the 1- to 29-year old population in Burkina Faso, the group chosen for the first introduction
of the vaccine. A multiple cross-sectional carriage study was conducted in one urban and two rural districts in
Burkina Faso in 2009. Every 3 months, oropharyngeal samples were collected from >5,000 randomly selected
individuals within a 4-week period. Isolation and identification of the meningococci from 20,326 samples were
performed by national laboratories in Burkina Faso. Confirmation and further strain characterization, in-
cluding genogrouping, multilocus sequence typing, and porA-fetA sequencing, were performed in Norway. The
overall carriage prevalence for meningococci was 3.98%; the highest prevalence was among the 15- to 19-year-
olds for males and among the 10- to 14-year-olds for females. Serogroup Y dominated (2.28%), followed by
serogroups X (0.44%), A (0.39%), and W135 (0.34%). Carriage prevalence was the highest in the rural districts
and in the dry season, but serogroup distribution also varied by district. A total of 29 sequence types (STs) and
51 porA-fetA combinations were identified. The dominant clone was serogroup Y, ST-4375, P1.5-1,2-2/F5-8,
belonging to the ST-23 complex (47%). All serogroup A isolates were ST-2859 of the ST-5 complex with
P1.20,9/F3-1. This study forms a solid basis for evaluating the impact of MenAfriVac introduction on serogroup
After the introduction of vaccines against Haemophilus in-
fluenzae type b, Neisseria meningitidis and Streptococcus pneu-
moniae became the dominant causes of bacterial meningitis. N.
meningitidis is a Gram-negative diplococcus classified into 12
serogroups on the basis of its capsular polysaccharide compo-
sition, with serogroups A, B, C, W135, X, and Y being the main
disease-causing serogroups. Meningococci are transmitted be-
tween individuals by airborne droplets of respiratory or throat
secretions. Healthy humans colonized by meningococci in the
upper respiratory tract are the principal source of spread of the
bacterium in the population (17, 41).
Epidemic meningitis is a significant cause of morbidity and
mortality in sub-Saharan Africa, in an area stretching from
Senegal to Ethiopia. This area is designated the meningitis belt
(15), where epidemic meningitis is primarily caused by sero-
group A meningococci (NmA), with disease incidence peaking
in the dry season every year. In addition to the yearly cycles,
large, multicountry epidemics recur unpredictably every 2 to 10
years (11). The West African country Burkina Faso, with a
population of about 15 million, is located in the middle of the
meningitis belt and has repeatedly been affected by epidemics
of meningitis. The latest epidemic year was 2007, with 26,878
recorded cases and 1,923 deaths. In 2008, 10,401 cases and
1,067 deaths were recorded, and there were 4,723 cases and
629 deaths in 2009 (MDSC Meningitis Weekly Bulletin, http:
//www.who.int/csr/disease/meningococcal). Moreover, Burkina
Faso was the first country to experience a major serogroup
W135 outbreak in 2002 (24), with 13,000 reported cases, of
/w135). The World Health Organization (WHO) currently rec-
ommends reactive mass vaccination to halt ongoing epidemics
(37), and countries can apply for an emergency stockpile of the
A/C or A/C/W polysaccharide vaccine (38). However, the pro-
tective immunity of the polysaccharide vaccines is relatively
* Corresponding author. Mailing address: WHO Collaborating
Center for Reference and Research on Meningococci, Norwegian
Institute of Public Health, P.O. Box 4404, Nydalen, 0403 Oslo,
Norway. Phone: 47 21 07 63 11. Fax: 47 21 07 65 18. E-mail:
?Published ahead of print on 12 January 2011.
brief, and immunogenicity in young children is considered sub-
optimal (29, 32).
Conjugate vaccines are safe and effective not only in pre-
venting disease among those vaccinated but also in preventing
carriage of the disease-causing organisms, leading to reduced
transmission of the disease (10, 19, 20, 28, 35). The Meningitis
Vaccine Project (MVP), a public-private partnership between
WHO and the Program for Appropriate Technology in Health
(PATH), has developed MenAfriVac, an effective monovalent
serogroup A conjugate meningococcal vaccine, at an afford-
able price (14). Clinical trials have been performed in India
and Africa, with very promising results (2, 3, 12, 13, 26).
MenAfriVac has the potential to prevent significant morbidity
and mortality, especially among those aged below 30 years, in
sub-Saharan Africa and to eliminate the devastating serogroup
A meningococcal epidemics that regularly occur in these coun-
tries. A country-wide mass vaccination campaign for the first
introduction of the vaccine was carried out in Burkina Faso in
2010, where the vaccine was offered to all individuals aged 1 to
To assess the indirect effect of the vaccine on protection
from acquisition, carriage studies must be conducted in the
populations that will be targeted by the vaccine. Such an as-
sessment would be easier using population groups with a high
prevalence of carriage. However, risk factors associated with
carriage in other parts of the world might not necessarily rep-
resent the situation in West Africa, since strain distribution
and socioeconomic conditions may be quite different. Previous
carriage studies conducted in Africa have provided variable
information on prevalence and affected age groups (34). To
accurately determine the ability of MenAfriVac to reduce car-
riage of serogroup A N. meningitidis, an initial milestone con-
sists of securing good baseline data on serogroup A carriage
prevalence before the introduction of the vaccine. Therefore,
we conducted a series of carriage studies in Burkina Faso
between October 2008 and December 2009. Carriage preva-
lence of different serogroups of N. meningitidis and molecular
characterization of the retrieved strains are presented here,
together with seasonal and geographical variations, as well as
the age and gender distributions of the asymptomatic carriers.
MATERIALS AND METHODS
Ethics. The study obtained ethical clearance from the Norwegian Regional
Committee for Medical Research Ethics, Southern Norway; the Ethical Com-
mittee for Health Research in Burkina Faso; and the Internal Review Board at
the Centers for Disease Control and Prevention (CDC), Atlanta, GA.
Study population. The study was implemented in three health districts in
Burkina Faso: Bogodogo, an urban district in the capital, Ouagadougou, with
roughly 615,478 inhabitants; Dande ´, a rural district in the west with 214,470
inhabitants; and Kaya, a rural district in the east with 500,207 inhabitants (Fig. 1).
Each study site was supported by a national microbiological laboratory: the
Centre National Pe ´diatrique Charles de Gaulle, Ouagadougou, for Bogodogo;
the Centre Hospitalier Universitaire Souro Sanou, Bobo-Dioulasso, for Dande ´;
and the Centre Hospitalier Universitaire Yalgado, Ouagadougou, for Kaya.
The study was designed as a multiple cross-sectional survey. To account for
seasonal fluctuations in carriage prevalence (1, 5, 16, 22, 27, 34), sampling
campaigns were executed every 3 months, starting in October 2008 (Fig. 2). The
campaigns were conducted simultaneously in all three districts within a 4-week
period. Representative sampling of persons aged 1 to 29 years was accomplished
by multistage cluster design. Eight villages in each rural district were selected by
probability proportional to size. Two additional villages per rural district were
selected as alternates in case the former villages were inaccessible due to rain. All
housing compounds in selected villages were mapped with Global Positioning
System (GPS) coordinates before the study launch. During each sampling cam-
paign, we selected 42 compounds per village by simple random sample and
navigated to them using GPS coordinates. All persons within the target age range
living in the selected compound were asked to participate.
In the urban district, all residential blocks were identified using existing maps.
Sixteen blocks and five alternates per study round were selected by simple
random sample and mapped with GPS coordinates. During each sampling cam-
paign, all the households in the selected blocks were visited. New selections were
done for each sampling campaign.
Inclusion of participants and administration of questionnaires. The village
population was informed about the project through the local health workers and
community leaders. Each randomly selected household was visited by study
personnel, and the purpose of the study was explained. A first questionnaire with
general questions about the compound was administered to the head of the
compound after his written consent. Then, a second questionnaire was admin-
istered to each of the 1- to 29-year-old members of the household after their
individual written consent or, in the case of children below 18 years of age, the
consent of their parent or guardian. Each participant was given a paper wrist-
band with a barcode corresponding to a unique identifier number linked to the
Sample collection. Oropharyngeal samples were obtained by sweeping the
posterior pharyngeal wall behind the uvula and one tonsil with a sterile cotton
swab (Copan, Italy). The swab was immediately plated onto modified Thayer-
FIG. 1. Geographical distribution of the study sites in Burkina Faso
(map source, The World Factbook, Central Intelligence Agency web
FIG. 2. Timelines for sampling campaigns and epidemic curve in
Burkina Faso, 2008 and 2009.
436 KRISTIANSEN ET AL.CLIN. VACCINE IMMUNOL.
Martin VCNT agar, containing 3 mg/liter vancomycin, 7.5 mg/liter colistin, 12.5
U/liter nystatin, 5 mg/liter trimethoprim lactate, and Vitox supplement (manu-
factured by WHO/Multi Disease Surveillance Centre, Burkina Faso). In the field,
inoculated plates were rapidly incubated in humidified and CO2-rich air using
7.0-liter jars (Remel, GA) with a CO2-generating system (CO2GEN; Oxoid,
United Kingdom). Personal digital assistants (PDAs) were used to register the
barcode on the participant’s wristband as well as the barcode label used on the
inoculated plate, creating a link between the person identifier number and
the laboratory specimen number. As soon as possible and within 6 h after
sampling, the jars with the plates were incubated at 37°C in the laboratory.
Between 100 and 110 samples were collected daily at each site, 4 days per week,
during the 4 weeks of each campaign.
Bacterial identification and characterization. Primary identification was per-
formed after 24 and 48 h of incubation. Colonies with a typical morphology of N.
meningitidis were subcultured on blood agar plates and subjected to further
laboratory analysis. Oxidase-positive, Gram-negative diplococci with ?-galacto-
sidase (o-nitrophenyl-?-D-galactopyranoside)-negative activity and ?-glutamyl-
transferase (GGT)-positive activity were considered probable N. meningitidis
isolates and serogrouped by slide agglutination using commercial antisera (Re-
mel). Purified isolates were inoculated into two cryovials containing 0.5 to 1 ml
Greaves solution (8) and stored at ?70°C. After each campaign, one of the vials
was sent to the Norwegian Institute of Public Health (NIPH), Oslo, Norway, on
dry ice for confirmation and further analyses.
The identification tests described above were repeated at NIPH, and sugar
fermentation tests were performed, if necessary. Strains confirmed to be N.
meningitidis were further characterized using molecular methods.
Genotypic characterization. DNA from each strain was isolated by suspending
1 loop of bacteria in 200 ?l Tris-EDTA (TE) buffer, pH 8.0, heating at 95°C for
10 min, and centrifugation at 16,000 ? g for 5 min, and the supernatant was
stored at ?20°C until use. Each strain was assigned to a specific sequence type
(ST), using multilocus sequence typing (MLST), which identifies allelic variation
within seven housekeeping genes (18). Variation in the porA and fetA genes,
coding for the outer membrane proteins PorA and FetA, respectively, was
determined by DNA sequencing, as described previously (30, 33a). New MLST
alleles and STs were submitted to the MLST database (http://pubmlst.org
/neisseria/), together with the strains’ serogroups and porA and fetA sequences.
PCR analysis of the genes coding for the polysaccharide capsule (33) was per-
formed for genogroup determination of nonserogroupable isolates or for con-
firmation of questionable slide agglutination test results.
Amplification of the porA and fetA genes, as well as the genes used in MLST,
was done with 35 cycles of denaturation at 95°C for 1 min, annealing at 52°C for
1 min, and elongation at 72°C for 1 min. Genes used for genogrouping were
amplified with 30 cycles of denaturation at 95°C for 40 s, annealing at 58°C for
1 min, and elongation at 72°C for 40 s. Sequencing reactions were performed
with an ABI Prism BigDye Terminator cycle sequencing ready reaction kit (ABI,
Foster City, CA), according to the manufacturer’s recommendations, using a
epMotion 5070 robot (Eppendorf, Bergman, Oslo, Norway). Sequencing was
performed using an ABI 3730 DNA analyzer (Applied Biosystems).
Data collection and analyses. The databases containing data collected in the
field were uploaded to a computer on a daily basis. In the laboratories in Burkina
Faso and in Norway, results were registered on paper before computerized data
entry into Microsoft Access and Excel databases (Microsoft Corporation, Red-
mond, WA). A combined database with data from all the computer files was used
for the evaluation of the results and the statistical analysis. Some samples were
excluded due to missing or duplicate links between the person and the laboratory
identification or between the person and his or her household. Only samples with
data available in all the databases were included in the analysis. For all the
isolates confirmed to be N. meningitidis at NIPH, all genes described could be
sequenced. Thus, none were excluded at this level. The characteristics of the
retrieved isolates are based on confirmed results obtained at NIPH. Statistical
analyses were performed using the chi-square test with 1 degree of freedom. P
values of ?0.05 were considered significant.
Exclusion of the first sampling campaign. Altogether, five
sampling campaigns were performed at 3-month intervals,
starting in October 2008 (Fig. 2). Results from the first cam-
paign (October and November 2008) yielded an N. meningitidis
carriage prevalence of only 0.87% in the 1- to 29-year-old
Burkinabes (0.75%, 0.51%, and 1.35% in the districts of Bo-
godogo, Dande ´, and Kaya, respectively). Evaluation of the
initial study concluded that the unexpectedly low carriage prev-
alence was due to poor selectivity of the commercial modified
Thayer-Martin agar plates purchased for that campaign, lead-
ing to contamination and difficulties in selecting colonies from
the plates. Improvements of the study standard operating pro-
cedures and quality control procedures were undertaken, and
local production of selective agar plates was successfully estab-
lished in Ouagadougou. The first campaign was therefore con-
sidered a pilot study.
Samples and overall carriage prevalence. The remaining
four sampling campaigns were conducted in 2009 and were
designated S1 through S4. Data collection for each round
occurred in January-February, April-May, July-August, and
October-November for the respective four campaigns. They
yielded a total of 20,326 oropharyngeal samples (range,
5,024 to 5,121 samples per campaign). After isolation and
primary identification in Burkina Faso, 1,049 isolates were
sent to NIPH for confirmation and molecular characteriza-
tion (range, 191 to 357 isolates per campaign). Of these, 811
(77.3%) isolates were confirmed to be N. meningitidis; 809
were registered in all the data sets and could be included in
the data analysis, giving an overall meningococcal carriage
rate of 3.98% (Table 1).
Regional and seasonal variations in carriage prevalence.
The N. meningitidis carriage prevalence rates were 4.10%,
5.27%, 3.37%, and 3.17% at the time points of S1, S2, S3, and
S4, respectively (Fig. 3). Overall carriage prevalence was
higher during the dry season (S1 and S2) than during the rest
of the year (S3 and S4) (P ? 0.001), although the difference
was not significant in the Bogodogo District. Seasonal variation
was also statistically significant between S1 and S2 (P ? 0.01),
TABLE 1. Carriage rate and serogroup prevalence of N. meningitidis in Burkina Faso at four sampling times in 2009
Total no. of samples
No. (%) of N. meningitidis isolates
No. (%) of NmA isolates
No. (%) of NmC isolates
No. (%) of NmW135 isolates
No. (%) of NmX isolates
No. (%) of NmY isolates
No. (%) of nongroupable isolates
VOL. 18, 2011MENINGOCOCCAL CARRIAGE IN BURKINA FASO437
S1 and S4 (P ? 0.05), S2 and S3 (P ? 0.001), and S2 and S4
(P ? 0.001) but not between S1 and S3 or between S3 and S4.
We found a significant difference in carriage rates when the
rate for the urban district (average, 1.82%) was compared to
the rates for the two rural districts (average, 5.07%) (P ?
0.001). The results also showed a geographic variation among
the two rural districts, with the carriage prevalence in Kaya
(average, 6.23%; range, 4.71 to 8.77%) being significantly
higher than that in Dande ´ (average, 3.91%; range, 3.06 to
4.94%) (P ? 0.001) (Fig. 3). This district ranking was the same
for all the campaigns.
Determination of serogroup. Of the 809 isolates, 574 were
assigned to a serogroup on the basis of the result from slide
agglutination, while 235 isolates were nonserogroupable and
further analyzed by capsule gene PCR. After PCR, 102 isolates
remained nonserogroupable, while 16 isolates were NmA, 2
isolates NmC, 18 isolates NmX, 60 isolates NmY, and 37 iso-
lates NmW135. Thus, over half of the isolates that were non-
serogroupable by serum agglutination harbored a capsule gene
that was not expressed phenotypically. In addition, some iso-
lates for which agglutination did not match the other molecular
characteristics were checked by capsule gene PCR. The sero-
group of 14 isolates was then changed according to the PCR
NmA carriage prevalence. NmA carriage prevalence rates at
the time points of S1, S2, S3, and S4 were 0.42%, 0.62%,
0.24%, and 0.29%, respectively (Fig. 4), corresponding to an
average NmA carriage prevalence of 0.39%. Seasonal variation
was statistically significant (P ? 0.01) when the rates during the
dry season (S1 and S2) and the rest of the year (S3 and S4)
were compared. The overall NmA carriage prevalence rates in
each of the districts were 0.06%, 0.21%, and 0.94%, for Bogo-
dogo, Dande ´, and Kaya, respectively. NmA carriage preva-
lence follows the same pattern of variation described for the
overall carriage prevalence, with a higher level in the rural
districts than in the urban district (P ? 0.001) and with signif-
icant differences between the rural districts (P ? 0.05). Inter-
estingly, the NmA carriage prevalence in S4 was the same as
that in the pilot study, executed almost exactly 1 year earlier
(0.29% in both).
Prevalence of other serogroups. The carriage prevalence of
the different serogroups, presented by district and campaign,
showed a predominance of NmY in all three districts at most
time points (Fig. 5). The increase in NmX prevalence seen
between S1 and S2 (Table 1) was significant (P ? 0.01) and was
essentially due to an increase in the district of Kaya. In all the
districts, carriage prevalence of NmA, NmY, and NmX in-
creased from S1 to S2 (significantly for NmY [P ? 0.05] and
NmX [P ? 0.01]) and decreased from S2 to S3 (significantly for
NmA [P ? 0.01] and NmY [P ? 0.01]), while Nm W135 and
nonserogroupable strains had changes in the opposite direc-
tion (significant decrease of NmW135 between S1 and S2 [P ?
Overall, nonserogroupable isolates were significantly more
dominant in the urban district of Bogodogo (33% of the iso-
lates) than in the rural districts of Dande ´ and Kaya (11% and
9%, respectively) (P ? 0.001) (Fig. 6). Kaya had the highest
proportion of serogroup A isolates, as they represented 15% of
all isolates, while the proportions of NmA in Dande ´ and Bo-
godogo were lower and comparable (5% and 3%, respectively).
Although NmY dominated in all three districts, it represented
76% of the isolates in Dande ´ but only 51% in Kaya and 34%
in Bogodogo. The proportions of NmX isolates were compa-
rable in Bogodogo and Kaya (15% and 17%, respectively), but
NmX was almost nonexistent in Dande ´ (?1%, corresponding
to a single carrier).
Molecular characterization. The 809 isolates confirmed to
be N. meningitidis were assigned to 29 different STs, of which
15 STs belonged to 5 different clonal complexes. A total of 51
FIG. 3. Carriage prevalence of N. meningitidis in three districts in
Burkina Faso at four sampling times in 2009.
FIG. 4. Carriage prevalence of serogroup A N. meningitidis in three
districts in Burkina Faso at four sampling times in 2009.
FIG. 5. Serogroup distribution of meningococcal isolates in three
districts in Burkina Faso at four sampling times in 2009.
438 KRISTIANSEN ET AL.CLIN. VACCINE IMMUNOL.
different porA-fetA combinations were identified, and the iso-
lates were assigned to 65 different combinations of serogroup,
ST, and porA-fetA. During the pilot and the carriage studies,
we found 17 new STs, 5 new PorA variants, and 1 new FetA
variant; all have been submitted to the MLST database (http:
All 80 NmA isolates were ST-2859 (ST-5 complex), and all
had the porA-fetA combination P1.20,9/F3-1 (Table 2). This
single clone of serogroup A has been present for the whole
period from October 2008 to November 2009, as all 14 NmA
strains retrieved from the pilot study also had this character-
istic. In addition, two isolates with ST-2859, P1.20,9/F3-1, were
nongroupable both by serogrouping and by PCR.
The four serogroup C isolates originated from the districts
of Bogodogo and Dande ´ at the time point of S2, belonged to
the ST-41/44 clonal complex, and contained the FetA variant
F5-2 (Table 2). Three of these isolates were ST-206, and one
was a new ST (ST-7929), a single-locus variant of ST-206.
During the pilot study, a single NmC isolate was found and
attributed to another new ST (ST-7376) of the ST-41/44 clonal
complex, also a single-locus variant of ST-206.
NmW135 (n ? 70) was represented in all three districts by
the ST-175 complex, almost exclusively by ST-2881 (n ? 69),
but also by a single isolate of a new ST, ST-7928, which is a
single-locus variant (adk) of ST-2881. The porA-fetA combina-
tion P1.5-1,2-36/F5-1 was found for 97% of the NmW135 iso-
The serogroup X isolates (n ? 90) belonged to STs not
assigned to any clonal complex: ST-181, ST-751, and ST-5789.
ST-5789 is a single-locus variant (adk) of ST-181, while ST-751
is a double-locus variant from ST-181 (gdh and phdC). Car-
riage of NmX was mainly observed in the districts of Kaya (n ?
70) and Bogodogo (n ? 19). NmX ST-181 (n ? 67) was present
in both Kaya and Bogodogo, while ST-5789 was present only in
Bogodogo (n ? 12). ST-751 was present only in Kaya (n ? 10)
and Dande ´ (n ? 1). Of the NmX isolates, 96% had the PorA
variant P1.5-1,10-1, of which 63% harbored the F1-31 FetA
variant and 27% harbored F4-23 (Table 2).
The NmY (n ? 457) isolates belonged to the ST-23 complex
(n ? 403) and the ST-167 complex (n ? 54). The ST-23
complex was mainly represented by ST-4375 (n ? 396), the
dominant ST in our study, but 3 new STs were identified, all of
them single-locus variants of ST-4375. Among the isolates as-
signed to ST-4375, eight different porA-fetA combinations were
identified, but 97% of the ST-4375 isolates had the porA-fetA
combination P1.5-1,2-2/F5-8, making this clone the dominant
strain circulating in Burkina Faso during the study period
(47% of all isolates). The ST-167 complex was more diverse,
represented by four STs and 10 porA-fetA combinations. How-
ever, 96% had PorA variant P1.5-1,10-8 and 77% had FetA
Age and gender distribution. Among the 20,326 participants,
43.7% were males and 56.3% were females. Overall carriage
prevalence in males was higher than that in females for NmA
(P ? 0.05), NmY (P ? 0.01), and nonserogroupable meningo-
cocci (P ? 0.05). The only STs with significant differences in
prevalence between genders were ST-2859 (P ? 0.05) and
ST-4375; both were more common among males (P ? 0.01).
Carriage of N. meningitidis was the highest among the 10- to
14-year-olds when both male and female participants were
considered. Among male participants, the 15- to 19-year-olds
had the highest carriage prevalence (Fig. 7). For the female
participants, the carriage prevalence was the highest among
the 10- to 14-year-olds. The difference in age distribution be-
tween genders was mostly due to serogroup Y, since this se-
rogroup dominated, but it was also substantial for serogroup A
and nonserogroupable meningococci.
The highest prevalence of NmA was found among 5- to
9-year-olds (overall, 0.58%; male, 0.66%; female, 0.51%).
Among the 10- to 14-year-olds, males had an even higher
prevalence (0.80%), while the prevalence among females in
the same age group dropped (0.15%). The oldest recorded
person carrying NmA was 26 years of age, although a 29-year-
old NmA carrier was identified during the pilot campaign.
Except for NmC, all the detected serogroups were repre-
sented in all age groups, but the variation by age group was
high for NmY (range, 1.22 to 2.95%) compared to that for the
other serogroups (Fig. 8). The increase in prevalence of non-
serogroupable isolates with age, peaking in the 15- to 19-year-
olds, was observed for both male and female participants.
By investigating the carriage rates in relation to the age, in
years, of the participants, we found a local peak of NmA and
NmY prevalence among 5-year-olds (0.70% and 3.33%, re-
spectively), as well as a local peak of NmA and NmX preva-
lence among 9-year-olds (1.22% and 0.82%, respectively).
Meningococcal carriage. The overall carriage prevalence
rates of meningococci and NmA were low compared to those
found in other African studies, which have reported overall
carriage prevalence rates of between 3 and 30% and NmA
carriage rates of between 0 and 31% (34). Nonetheless, our
results are comparable to those of other longitudinal or cross-
sectional studies performed in West Africa, such as in northern
Ghana, where 6.1% carried N. meningitidis (range, 0.6 to
19.8%) and 1.1% carried NmA (range, 0.3 to 4.3%) over an
8-year period (16), or in northern Nigeria, where 6.2% carried
N. meningitidis (range, 1 to 10%) and 1.1% carried NmA over
1.5 years (4, 9).
It is not clear how the carriage prevalence of N. meningitidis
is linked to epidemic occurrence, but it has been shown that
carriage of outbreak strains can increase significantly during an
FIG. 6. Overall serogroup distribution of meningococcal isolates in
three districts in Burkina Faso in 2009.
VOL. 18, 2011 MENINGOCOCCAL CARRIAGE IN BURKINA FASO439
TABLE 2. Characteristics of N. meningitidis retrieved from the carriers in Burkina Faso according to serogroup
A5 2859 80P1.20,9F3-180
C41/44 2063 P1.5-2,10-2
181 67P1.5-1,10-1 F1-31
Y 23 4375396 P1.5-1,2-2F4-23
198 198 10
192 56 P1.18,42-7a
aNew ST, new PorA variant or new FetA variant.
c—, no gene detected.
440KRISTIANSEN ET AL.CLIN. VACCINE IMMUNOL.
epidemic (23, 34). The low carriage prevalence rate of NmA in
our study is comparable to the rates in other reports of carriage
prevalence of virulent strains of between ?1% and 5% during
endemic or hyperendemic periods (23). During the study pe-
riod, the epidemic situation in Burkina Faso was calm com-
pared to that in earlier years and other countries of the African
meningitis belt, with only 4,723 suspected cases of meningitis in
2009 (39). Only 30% of the cerebrospinal fluid-positive sam-
ples collected from suspected cases contained NmA and 3%
contained NmW135, whereas 66% contained S. pneumoniae
Standardization of operational practices. One of the major
challenges in a large multicenter study is the harmonization of
operational procedures while ensuring a high quality of the
work over a long period of time. Several measures were im-
plemented, including training, pilot studies, wrap-up and brief-
ing meetings between each campaign, the use of written stan-
dard operating procedures, and close supervision by local and,
occasionally, by external supervisors. Laboratory quality con-
trol was also implemented to ensure and document correct
laboratory practices. The sampling technique and the method
of directly plating of the samples that we used are well-known
and recommended to obtain a good yield (7).
Selection bias. Young female participants were overrepre-
sented in the sampled population, a reflection of the society in
general, where women often work at home while the men are
working away from the household. The study included only the
persons physically present at the household at the time of the
visit, with the exception of selected schoolchildren, who were
included during a normal break. This selection bias might lead
to an underestimation of total carriage prevalence, since males
were more frequently carriers and because carriage prevalence
in the youngest age groups was lower. However, the overall
study goal of comparing prevalence before and after vaccina-
tion should not be compromised, as the sampling methods
remained the same throughout the study.
Age and gender distribution. Our results are consistent with
other data showing higher carriage prevalence in males over
females, but with an age distribution different from that seen in
Europe and North America (6). Age-specific carriage preva-
lence likely reflects differences in social behavior, as this has
been hypothesized to be more important than age or sex (17).
Multivariate analysis of risk factors affecting meningococcal
carriage is being done and will be presented in a future pub-
Geographic variation. The variations of carriage prevalence
and serogroup distribution by district can be attributed to dif-
ferences in climate and living conditions. The difference be-
tween rural and urban areas is consistent with previous findings
(9). The district of Kaya is the harshest district in the study and
notably drier than the more agricultural district of Dande ´, but
the living conditions are similar between these rural districts
and the selected villages in each district were not very different.
The district of Bogodogo has a completely different sociolog-
ical context, with smaller families and a higher standard of
living, factors that can affect meningococcal carriage. Easy
access to medicines, such as antibiotics, in the capital might
also be a contributing factor.
Seasonality. A review of longitudinal carriage studies con-
ducted in the meningitis belt has concluded that there is no
association between carriage prevalence and season (34); in
contrast, our data show a significant association with a higher
prevalence of carriage in the dry season. This difference may
be explained by the large sample size in our study (range, 5,024
to 5,121 per time point) compared to the sizes in prior studies
(range, 79 to 525 per time point).
Diversity of strains. The genetic diversity of the isolates in
our material was not very high, with 96% of the isolates be-
longing to 1 of 11 STs. This is consistent with other carriage
studies conducted in Africa (5, 21, 25) but differs from the
genotypic diversity of carrier isolates circulating in Europe (7).
In contrast to other serogroups, all the NmA carrier isolates
were identical: ST-2859, P1.20,9/F3-1. The same molecular
characteristics were also found in all the NmA isolates from
the pilot study. After a large W135 outbreak in Burkina Faso
in 2002-2003 and the subsequent use of a trivalent ACW135
vaccine in 2003 (42), ST-2859 has been the major disease-
causing clone circulating in Burkina Faso (11, 31). All the
ST-2859 isolates reported in the MLST database are P1.20,9
(http://pubmlst.org/neisseria/). Since PorA and FetA are pro-
teins exposed on the surface of the bacteria, they are targeted
by the immune system and have a tendency to adapt by genetic
variation more frequently than the housekeeping genes. The
nonexistent variation of the PorA and FetA composition in the
NmA carrier strains might indicate that this clone is well
FIG. 7. Carriage prevalence of N. meningitidis, NmA, and NmY by
age group and gender.
FIG. 8. Carriage prevalence of each meningococcal serogroup by
VOL. 18, 2011MENINGOCOCCAL CARRIAGE IN BURKINA FASO441
adapted or that these proteins are less exposed on the bacterial
surface than they are in other serogroups.
The other serogroup known to cause disease in Burkina
Faso is NmW135. It was also present and very homogeneous
among the carriage isolates, as 99% of them belonged to ST-
2881. Sporadic cases of meningitis in Burkina Faso from 2008,
as well as 24.4% of genotyped isolates from a carriage study in
Niger in 2003, have been assigned to NmW135 ST-2881 (25;
http://pubmlst.org/neisseria/). This clone is different from the
ST-11 clone, which was associated with outbreaks among Hajj
pilgrims returning from Saudi Arabia in 2000-2001 and which
caused the W135 epidemic in Burkina Faso in 2003 (40). None
of the isolates in our study were ST-11.
Meningococcal carriage was dominated by NmY of the
ST-23 clonal complex, represented by ST-4375, a single-locus
variant (aroE) of ST-23. NmY ST-4375 has previously been
found to be the dominant clone in areas of Burkina Faso with
little disease, and it has been suggested that NmY carriage
might halt the spread of NmA (31). This clone was associated
with sporadic cases of meningitis in Burkina Faso in 2006 and
2007 (http://pubmlst.org/neisseria/). For the past 2 decades,
ST-23 has been increasingly associated with serogroup Y me-
ningococcal disease in the United States, Canada, Israel, and,
to some extent, South Africa, although ST-175 is the predom-
inant NmY clone in South Africa (11, 36). NmY has not yet
caused any epidemic in the meningitis belt.
The dominant serogroup X clone in this study, ST-181, had
been isolated from cases of meningitis in Burkina Faso in 2007
(http://pubmlst.org/neisseria/). This is the same clone respon-
sible for the serogroup X outbreak in Niger in 2006, where a
particularly high seroprevalence of NmX isolates was found in
the southwestern part of the country, close to Burkina Faso.
The relative proximity of the districts of Kaya and Bogodogo
to the borders of Niger could explain why ST-181 was found
only in these two districts. The molecular diversity within the
NmX carrier strains was higher than that among the other
serogroups, as the dominant clone, ST-181, P1.5-1,10-1/F1-31,
represented only 59% of the NmX isolates.
The ST-41/44 complex is a highly diverse clonal complex
which has been, among other things, responsible for a sero-
group B epidemic in New Zealand. ST-206, the dominant ST
belonging to the ST-41/44 in this study, has previously been
reported with serogroups B, C, and Z (http://pubmlst.org
/neisseria/) but expressed only the serogroup C capsule in our
Approximately 50% of strains from carriage studies in Eu-
rope are nonserogroupable, while only 29% of those recovered
in Burkina Faso were nonserogroupable, if we consider the
results from slide agglutination (7). Carriage studies conducted
in the meningitis belt have reported variable proportions of
nonserogroupable strains, many of them lower than 50% (34).
Usually, 16 to 20% of carriage isolates are lacking the gene
coding for the synthesis of the capsule, while we found an
average of 13%, with the differences between urban and rural
areas being significant (6). Most of the new ST and PorA
variants were identified from the pool of nonserogroupable
strains. The diversity of the nonserogroupable strains is likely
an expression of environmental adaptation where the bacteria
lack the protective capsule.
Conclusions. To our knowledge this is the largest meningo-
coccal carriage study ever conducted in Africa. The aggregate
data will form the basis for the assessment of the impact of
MenAfriVac introduction on meningococcal carriage rates.
With a prevaccination NmA carriage prevalence of 0.39%, all
districts and all rounds confounded, and a sample size of
20,326 subjects, we should obtain significant results if the NmA
carriage prevalence is reduced by 50% following vaccine intro-
duction. Due to the low carriage prevalence of NmA, sero-
group replacement is unlikely to occur as a direct result of
MenAfriVac vaccination, in the similar way that replacement
did not occur in the United Kingdom after introduction of a
monovalent serogroup C conjugate vaccine.
We thank the residents in the districts of Bogodogo, Dande ´, and
Kaya for their participation in this study and the public health person-
nel from each district working in the field with mapping, recruitment,
and survey. Special thanks go to the leading laboratory technicians,
Manoudou Tamboura, Maxime Kienou, and Siakka Traore ´, as well as
to the many other laboratory technicians involved in this study. The
technicians at the bacteriology laboratory of MDSC, Eric Sankara and
Idrissa Kamate ´, did a fabulous job making the selective agar plates for
the study. We thank the technicians at the NIPH, Ida Andreasson,
Martha Bjørnstad, Berit Nyland, Torill Alvestad, and Anne-Marie
Klem, for training, supervision in Burkina Faso, and laboratory anal-
ysis. We thank Kader Konde ´, Laurent Toe ´, Stacey Martin, and Lara
Misegades for their contribution and support. We also thank Sylvestre
Tiendrebeogo and Bokar Toure ´ for their support and advice. Special
acknowledgments are given to Flavien Ake ´ for his technical expertise
and engagement in the training, supervision, and technical assistance
to the PDA operators, as well as his role in the data management.
This publication made use of the Neisseria Multi Locus Sequence
Typing website (http://pubmlst.org/neisseria/), sited at the University
of Oxford and funded by the Wellcome Trust and the European
This project was supported by the Norwegian Research Council,
grant no. 185784, to D.A.C.
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