Background
Malaria continues to pose a significant public health threat across Africa. Achievements in increasing coverage of efficacious interventions have changed the landscape of transmission and disease burdens in some areas but this has not been universal between or within countries [
1‐
3]. This impact diversity remains a challenge to the dogma that ‘one size fits all’ regarding the selection and optimization of control approaches.
Understanding the intensity of parasite transmission in a community is a fundamental prerequisite to the design of malaria control [
4]. How transmission intensity changes with increasing coverage of vector control provides a valuable metric of impact, necessary to sustain, increase or revise coverage of intervention tools [
5]. The most widely used metric of malaria transmission intensity is parasite prevalence, measured through cross-sectional surveys. There is a growing recognition of the importance of infection prevalence surveys in the design and evaluation of malaria control initiatives in Africa [
6]. National household sample surveys that include malaria infection measurements are increasing in number; however, they are expensive, labour-intensive undertakings. It has been proposed that where school attendance is high and malaria transmission is stable, the use of school-based malaria surveys offers a cheaper alternative to examine community-acquired infection prevalence and reported coverage of household vector control [
7,
8].
This study reports on a survey of malaria infection among Kenyan schoolchildren living in areas of intense malaria transmission and the relationship between infection in this age group and their reported use of insecticide-treated bed nets (ITN).
Results
Between May and June 2014, 54 schools were sampled across the seven counties including 5188 children with a mean age of 9.6 years (standard deviation 2.6) and 50.3 % of the children were female. Overall, 48.7 % (95 % CI 45.3–57.3) of the children were positive for
P. falciparum and 67.9 % (95 % CI 65.7–74.2) reported having slept under an LLIN the night before the survey. Prevalence varied markedly by school (0–2 %) and by county, the county-level infection prevalence was highest in Busia (66.9 %) and Homa Bay (51.8 %), and lowest in Migori (29.6 %) and Bungoma (35 %) counties. Similarly, the reported use of LLINs varied across the counties with the lowest reported use of LLIN being in Kakamega County (51.9 %), and the highest LLIN use by schoolchildren being in Kisumu County (82 %) (Table
1). In terms of household net ownership, 91.3 % (95 % CI 89.2–93.5) of the children reported having at least one LLIN in their households. Three counties (Kisumu, Homabay, Busia) reported overall net ownership of >90 %, whereas Vihiga County reported the least overall net ownership of 85.5 %. Median reported household coverage of LLIN was above 2.3 persons per one LLIN across all sampled counties (Table
1).
Table 1
Background characteristics of schoolchildren sampled at 54 schools in seven counties of Western Kenya
Bungoma | 6 | 592 (11.4 %) | 9.7 (2.5) | 212 (35.8) [19.9–64.6] | 336 (56.8) [50.0–63.6] | 3.0 (2.7) |
Busia | 11 | 1097 (21.1 %) | 9.8 (2.6) | 734 (66.9) [59.8–74.9] | 796 (72.6) [64.8–80.3] | 2.3 (2.0) |
Homa Bay | 15 | 1389 (26.8 %) | 9.7 (2.9) | 720 (51.8) [41.9–64.2] | 1033 (75.2) [67.6–82.7] | 2.5 (2.3) |
Kakamega | 6 | 585 (11.3 %) | 9.3 (2.5) | 246 (42.1) [26.5–66.7] | 303 (51.9) [42.4–61.3] | 3.0 (2.3) |
Kisumu | 6 | 621 (12.0 %) | 9.7 (2.5) | 273 (44.0) [31.7–61.0] | 503 (82.0) [77.2–86.8] | 2.5 (1.8) |
Migori | 4 | 399 (7.7 %) | 9.5 (2.4) | 118 (29.6) [14.7–59.4] | 268 (67.2) [52.6–81.9] | 3.0 (3.0) |
Vihiga | 6 | 505 (9.7 %) | 9.4 (2.6) | 225 (44.6) [36.9–53.8] | 273 (54.3) [48.4–60.2] | 2.5 (2.5) |
Total | 54 | 5188 | 9.6 (2.6) | 2528 (48.7) [43.2–54.9] | 3512 (67.9) [63.8–72.0] | 2.5 (2.3) |
Factors associated with
P. falciparum infection were investigated using univariable and multivariable mixed effects logistic regression reporting OR at 95 % CI and taking into account two-level hierarchy of the data (county and school). The results from univariable analysis are provided as supplementary information (see Additional file
1: Table S1) while those for multivariable model are shown in Table
2. Age was included in the multivariable model regardless of the effect on infection risk. Whereas, children below 7 years were found to be non-significantly (P = 0.066) more likely to have malaria infection compared to older children (aOR 1.20, 95 % CI 0.99–1.45), there was strong evidence of infection risk (P < 0.001) among children in the age group (7–10) years. Male students were significantly (P < 0.001) more likely to be infected compared to female students (aOR 1.39, 95 %CI 1.23–1.58). In the multivariable model, adjusting for clustering between schools and counties, reported LLIN use by the schoolchild was found to significantly (P = 0.027) reduce the risk of malaria infection, (aOR 0.86, 95 % CI 0.74–0.98).
Table 2
Factors associated with malaria infection prevalence
Age category |
Below 7 years vs above 10 years | 1.20 (0.99–1.45) | 0.066 |
(7–10) years vs above 10 years | 1.28 (1.11–1.46) | 0.000* |
Gender |
Male vs female | 1.39 (1.23–1.58) | 0.000* |
Reported ITN use |
Yes vs no | 0.86 (0.74–0.98) | 0.027* |
Discussion
The reported use of LLIN among schoolchildren in Western Kenya in 2014 was high (67.9 %) and considerably higher than previous reports of 33 % LLIN use among schoolchildren in the lakeside region in 2009–2010 [
17]. This increase in reported LLIN use is a direct consequence of increased investment in this region of Kenya since 2009 to ensure universal coverage [
24] and addresses inequities previously demonstrated in net use within the vulnerable school-age group [
25]. Nevertheless, despite high ownership of LLIN, almost half (48.7 %) of the schoolchildren were infected with malaria, twice the levels of infection prevalence described in the same counties in 2009 [
17]. It is not clear why infection prevalence has escalated over this period and deserves a more detailed epidemiological and entomological investigation.
It should be noted that the survey occurred before the large mass distribution campaign of LLIN in this area in October 2014. It is not possible to gauge how bio-effective the LLINs were as it was not recorded when the nets were issued; the last mass distribution was in 2011. It is possible that many of the nets reported as being used by the schoolchildren might have been at the end of their useful life [
26]. In addition, reduced bio-efficacy to pyrethroids [
14], increasing molecular evidence of pyrethroid resistance [
27] and possible vector behavioural adaptation [
28] have all been recently confirmed in areas close to where the study sampled schoolchildren. Despite these constraints on the impact of LLIN, the study was able to demonstrate a 14 % reduction in the adjusted odds of being infected in this school-aged population living in a high-transmission area of Kenya.
This study’s findings are contrary to previous studies of the impact of treated nets on infection prevalence in this area of Kenya. During one of the pivotal, randomized control trials of ITNs in the 1990s, undertaken in Western Kenya, two cross-sectional surveys among adolescent girls attending 28 schools showed no impact of treated nets on peripheral malaria infection [
29]. Analysis of the impact of LLIN on infection prevalence in schoolchildren during national school surveys undertaken between 2009 and 2010 was unable to show a reduced odds of infection associated with LLIN use among schoolchildren in the lakeside region, despite significant reductions in infection associated with LLIN use in the coast and low-transmission highlands [
17]. Conversely, in support of this study’s observations, in Vihiga and Kakamega Counties between 2005 and 2007, the adjusted period prevalence of
P. falciparum infection was significantly reduced among children reported to have slept under treated nets [
30].
An interesting observation from this study was that males had a higher significant risk of parasitaemia compared with female counterparts. These sex differences in malaria infection were significant in all counties except Kisumu, Homabay and Bungoma. This observation is consistent with findings from other studies [
31], specifically a study in Kakamega County that showed school-aged girls were significantly less likely to be infected than their male counterparts [
32]. Although the cause of these sex differences merits further investigation, including the possibility that males produce more attractive chemicals for mosquitoes [
32], the production of estrogens by females has been shown to augment antiplasmodial immune responses, whereas testosterone suppresses antiplasmodial immune responses [
31].
School surveys provide a rapid means of establishing the use of interventions in the community and the likely impact of these interventions on the risks of malaria infection. They however suffer from the inability to examine the interventions in use in the children’s households and depend on school children’s responses only. In addition, children absent from school on the survey day are not included and these sampling biases might influence estimates of protective effects of ITN. Although such bias is expected to be higher in areas of lower transmission intensity compared to the area selected during the present study.
Conclusion
This study found a significant association between LLIN use and
P. falciparum infection in the lakeside zone with overall significant reduction in the adjusted odds of malaria risk of infection. The results from this study therefore have implications for Kenya’s malaria control programme, which focuses on persons with symptomatic
P. falciparum infection [
11]. Future efforts should target getting bed nets to households through school-attending children; this will effectively address LLIN universal coverage and encourage proper usage among schoolchildren.
One major limitation of the present study was the use of a few selected pupils in a few sampled schools and therefore this might not be representative to county population. This study relied on the affirmative answers of the pupils on the use of nets. Finally, this being a cross-sectional study by nature seasonal fluctuations were not reproduced or captured.
Authors’ contributions
CO participated in the data collection, analysis and developed the draft manuscript. JK and ES were responsible for fieldwork supervision and contributed to the final manuscript. CWG, AMN, RWS, CM, and SMN were responsible for the study design, interpretation and scientific guidance. All authors read and approved the final manuscript.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (
http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (
http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.