This is the first population-based survey of nasopharyngeal (NP) carriage of S. pneumoniae
and H. influenzae
conducted in East Africa. The prevalence estimate for pneumococcal carriage in children less than 5 years (50-61%) does not conform with the perception that carriage of the pneumococcus is almost invariable in African children. Much of the variation in carriage prevalence estimates in Africa is attributable to differences in the sampling frames. Studies in Ghana, Zambia, Malawi, and Mozambique have reported the colonization prevalence at 51%, 72%, 84% and 87%, respectively [20
] but each of these studies sampled sick children presenting to hospital. Estimates of carriage prevalence among well children are lower, at 22% in Kenya [24
], 48% in Malawi [25
] and 62% in Uganda [26
] but even in these studies the children were selected because they attended a health facility. In The Gambia in 1989-91 the prevalence of nasopharyngeal carriage in the under-fives was 90% among children who were hospitalized with invasive pneumococcal disease, and 76% among healthy location-matched controls [27
]. More recently in a study of selected villages it was estimated at over 90% [28
]. The carriage prevalence in unselected children aged <5 years in our study was 51-60%. It does appear that the colonisation prevalence in East and Southern Africa is substantially lower than that in The Gambia underlining the premise that pneumococcal epidemiology varies widely by geography.
Previous studies of children have mostly been restricted to those aged <5 years. Our study shows that children aged 5-9 years also have a high prevalence of nasopharyngeal carriage of both S. pneumoniae
and H. influenzae
. In a demographic structure where half of the population is aged <15 years [16
] those in the age group 5-9 years old represent a sizeable fraction of the total population and one that is likely to interact frequently with young children who are most susceptible to disease, facilitating transmission of respiratory pathogens. The distribution of pneumococcal serotypes found in this group with a much lower representation of vaccine serotypes differs substantially from that in younger children.
In our analysis, coryza and rainy season sampling were associated with carriage of S. pneumoniae
and H. influenzae
, independently of the effect of age. It is difficult to determine whether coryza, a marker of viral upper respiratory tract infection, is truly associated with carriage or whether it simply facilitates mucous sampling and thus enhances detection. The interpretation of a seasonal effect is limited by the fact that the survey observed only two short time periods within the annual cycle and because there are numerous hypothetical mechanisms by which season may affect carriage. Rains, like cold weather in temperate climates, encourage indoor living leading to temporary crowding in poorly ventilated structures. In Hong Kong, Vietnamese refugee children with a mean living area of 1.75m2
were compared to Chinese children with a mean living area of 10.2m2
; carriage prevalence of S. pneumoniae
was 56% and 11%, respectively [29
]. The contention that a humid environment better sustains the growth of bacterial pathogens on the mucosal surface is not borne out by evidence from other bacterial pathogens; in West Africa the prevalence of H. influenzae
(and N. meningitidis
) carriage does not vary by season [30
We observed a positive interaction between the presence of one species of pathogen in the nasopharynx and the presence of the other that was independent of age, season and coryza. In the mouse model of colonization by contrast, pre-existing carriage of one serotype of pneumococcus reduced the probability of colonization by a second serotype, indicating a negative interaction, although this was not consistently found [32
]. Although there may be competition between species at the nasal mucosa there is probably also a degree of host susceptibility to colonisation, which is not specific for either pathogen.
Among children aged <5 years the carriage prevalence of H. influenzae
in Kilifi (26%) was within the range observed in Central African Republic (20%) and South Africa (40%) [33
]. Freezing of STGG media has negligible effect on pneumococcal culture sensitivity [17
] but in our hands it reduced the per-swab sensitivity for H. influenzae
by half. As three-quarters of the swabs were processed after freezing, the mean sensitivity of study swabs for H. influenzae
was only approximately 63%. However, even if we take this degree of insensitivity into account, the prevalence of Hib carriage in the population aged <5 years was low and this is likely to be attributable to the Hib vaccine program. In The Gambia introduction of Hib vaccine was associated with a decline in Hib carriage among young children from 12% to 0.25% [35
]. Carriage of non-capsulate H. influenzae
was common in our survey though it should be noted that there has been no concomitant increase in the incidence of non-capsulate invasive disease since the introduction of Hib vaccine [36
In developing countries there are few studies describing the proportion of episodes of invasive pneumococcal disease caused by vaccine serotypes nor describing the extent to which this may be approximated by using nasopharyngeal isolates. Among invasive isolates from children aged <5 years in Kilifi in 1998-2002 the vaccine serotype coverage for the 9-valent vaccine (PCV9), which also includes serotypes 1 and 5, was 70% [1
]. In the same age group the coverage in carried isolates was 47% for both PCV7 and PCV9. We observed only one carried isolate of serotype 1, though it accounts for 23% of all invasive disease episodes in children [1
], and we did not detect serotype 5 at all. For PCV7 therefore, the carried isolates predict the vaccine serotype coverage accurately; for PCV9 they are grossly inaccurate.
A second question of current interest regarding pneumococcal serotypes is whether the direct benefits of introducing PCV7 into routine childhood immunization programs in developing countries would be undermined by an increase in the incidence of non-vaccine type disease. The risk of serotype replacement disease is a function of the exposure frequency and virulence of non-vaccine types in the population. In the USA serotypes 3 and 19A and serogroups 15 and 33 are those that have increased most significantly following vaccine introduction [11
]. Only 9% (18/207) of the carried isolates from young children in Kilifi fell into these groups. However, across all ages there were at least 40 circulating serotypes in a relatively small population sample in Kilifi and 164 (59%) of the carried pneumococci were from serotypes that are not included in PCV7. Operational use of conjugate pneumococcal vaccines in Kenya, justified by strong evidence of efficacy [3
] will provide a natural test of virulence for the many non-vaccine serotypes circulating in this population.