Abstract

BackgroundAlthough malaria control intervention has greatly decreased malaria morbidity and mortality in many African countries, further decline in parasite prevalence has stagnated in western Kenya. In order to assess if malaria transmission reservoir is associated with this stagnation, submicroscopic infection and gametocyte carriage was estimated. Risk factors and associations between malaria control interventions and gametocyte carriage were further investigated in this study.MethodsA total of 996 dried blood spot samples were used from two strata, all smear-positives (516 samples) and randomly selected smear-negatives (480 samples), from a community cross-sectional survey conducted at peak transmission season in 2012 in Siaya County, western Kenya. Plasmodium falciparum parasite presence and density were determined by stained blood smear and by 18S mRNA transcripts using nucleic acid sequence-based amplification assay (NASBA), gametocyte presence and density were determined by blood smear and by Pfs25 mRNA-NASBA, and gametocyte diversity by Pfg377 mRNA RT-PCR and RT-qPCR.ResultsOf the randomly selected smear-negative samples, 69.6 % (334/480) were positive by 18S-NASBA while 18S-NASBA detected 99.6 % (514/516) smear positive samples. Overall, 80.2 % of the weighted population was parasite positive by 18S-NASBA vs 30.6 % by smear diagnosis and 44.0 % of the weighted population was gametocyte positive by Pfs25-NASBA vs 2.6 % by smear diagnosis. Children 5–15 years old were more likely to be parasitaemic and gametocytaemic by NASBA than individuals >15 years old or children <5 years old while gametocyte density decreased with age. Anaemia and self-reported fever within the past 24 h were associated with increased odds of gametocytaemia. Fever was also positively associated with parasite density, but not with gametocyte density. Anti-malarial use within the past 2 weeks decreased the odds of gametocytaemia, but not the odds of parasitaemia. In contrast, recent anti-malarial use was associated with lowered parasite density, but not the gametocyte density. Use of ITNs was associated with lower odds for parasitaemia in part of the study area with a longer history of ITN interventions. In the same part of study area, the odds of having multiple gametocyte alleles were also lower in individuals using ITNs than in those not using ITNs and parasite density was positively associated with gametocyte diversity.ConclusionA large proportion of submicroscopic parasites and gametocytes in western Kenya might contribute to the stagnation in malaria prevalence, suggesting that additional interventions targeting the infectious reservoir are needed. As school aged children and persons with anaemia and fever were major sources for gametocyte reservoir, these groups should be targeted for intervention and prevention to reduce malaria transmission. Anti-malarial use was associated with lower parasite density and odds of gametocytaemia, but not the gametocyte density, indicating a limitation of anti-malarial impact on the transmission reservoir. ITN use had a protective role against parasitaemia and gametocyte diversity in western Kenya.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-016-1482-4) contains supplementary material, which is available to authorized users.

Highlights

  • Malaria control intervention has greatly decreased malaria morbidity and mortality in many African countries, further decline in parasite prevalence has stagnated in western Kenya

  • Given the complex biology and epidemiology of gametocytes that could be influenced by multiple factors including insecticide-treated net (ITN) use and anti-malarial treatment, the objectives of this study were: (1) to estimate the level of submicroscopic infection and gametocyte carriage in circulating blood, measured by molecular tools, in a region of western Kenya, where malaria transmission has stagnated since 2009, (2) to assess the risk factors associated with gametocytaemia, and (3) to determine the associations between malaria control interventions and gametocyte carriage

  • Whatever reasons for the variations between risk and density for parasitaemia and gametocytaemia, the results from this study indicated that children provided a larger gametocyte reservoir compared to adults in the peak transmission season in western Kenya assuming similar numbers of children and adults in population and similar mosquito bite rates received by children and adults

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Summary

Introduction

Malaria control intervention has greatly decreased malaria morbidity and mortality in many African countries, further decline in parasite prevalence has stagnated in western Kenya. The mature gametocytes (stage V) which are responsible for parasite transmission from human to mosquitoes often circulate at low densities [8] In this context, sensitive molecular detection tools could improve detection of low densities of gametocytes and submicroscopic infections to identify potential transmission reservoir. The Pfs25NASBA can detect 3- to 10-fold more gametocytes than microscopy [10] It has been shown by the highly sensitive molecular methods that the gametocyte reservoir is much larger than previously detected or reported [8, 10]

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