The prevalence of submicroscopic Plasmodium falciparum gametocyte carriage and multiplicity of infection in children, pregnant women and adults in a low malaria transmission area in Southern Ghana

Abstract

BackgroundThe gametocyte stage of Plasmodium falciparum is considered an important target for disrupting malaria transmission. Indications are that various demographic groups, such as children and pregnant women may differ in risk of harbouring gametocytes, which may be crucial for targeted control. In this study, the relationship between the prevalence and multiplicity of P. falciparum, asexual parasite infections and gametocytaemia was assessed in three different demographic groups in an area of southern Ghana with low malaria endemicity. Levels of antibody responses to Pfs230 were also assessed as a proxy for the presence of gametocytes.MethodsThe study involved multiple cross-sectional sampling of children (N = 184, aged 2–15 years), male and non-pregnant female adults (N = 154, aged 16–65 years) and pregnant women (N = 125, aged 18–45 years) from Asutsuare in the Shai Osudoku District of Greater Accra Region in Ghana. Asexual parasitaemia was detected by microscopy and PCR, and gametocytaemia was assessed by Pfs25-real time PCR. Multiclonal P. falciparum infections were estimated by msp2 genotyping and an indirect ELISA was used to measure plasma IgG antibodies to Pfs230 antigen.ResultsOverall, children and pregnant women had higher prevalence of submicroscopic gametocytes (39.5% and 29.7%, respectively) compared to adults (17.4%). Multiplicity of infection observed amongst children (3.1) and pregnant women (3.9) were found to be significantly higher (P = 0.006) compared with adults (2.7). Risk of gametocyte carriage was higher in individuals infected with P. falciparum having both Pfmsp2 3D7 and FC27 parasite types (OR = 5.92, 95% CI 1.56–22.54, P = 0.009) compared with those infected with only 3D7 or FC27 parasite types. In agreement with the parasite prevalence data, anti-Pfs230 antibody levels were lower in gametocyte positive adults (β = − 0.57, 95% CI − 0.81, − 0.34, P < 0.001) compared to children.ConclusionsThese findings suggest that children and pregnant women are particularly important as P. falciparum submicroscopic gametocyte reservoirs and represent important focus groups for control interventions. The number of clones increased in individuals carrying gametocytes compared to those who did not carry gametocytes. The higher anti-gametocyte antibody levels in children suggests recent exposure and may be a marker of gametocyte carriage.Electronic supplementary materialThe online version of this article (10.1186/s12936-018-2479-y) contains supplementary material, which is available to authorized users.

Stage-specific Plasmodium falciparum immune responses in afebrile adults and children living in the Greater Accra Region of Ghana

“…The absence of variation in gametocyte carriage across the dry and rainy season in Asutsuare is supportive of the very low year-round malaria transmission recorded in Asutsuare. The low gametocyte prevalence identified in the participants from Asutsuare supports a recent report that identified low gametocyte prevalence amongst children and adults, including pregnant women in Asutsuare [34].…”

“…As anticipated, the prevalence of asymptomatic carriers was significantly higher in Obom, the high parasite prevalence setting, than in Asutsuare where P. falciparum parasite prevalence has been reported to be very low for over a decade [34,36]. No significant difference was observed in asexual parasite carriage between the dry and rainy season in Asutsuare, mainly because malaria is low and perennial [36] and supports an earlier report on asexual parasite prevalence in another low malaria parasite intensity setting of Ghana [40].…”

“…A few earlier studies have characterized natural antibody responses to both asexual and sexual stage antigens, however these studies have only looked into immune responses in asymptomatic children below the age of 12 years [15] or in a symptomatic population [30]. Other studies on afebrile individuals have characterized antibody responses against sporozoite [31], asexual [32,33] or only sexual stage [34] antibody responses amongst a cohort of Ghanaians. This current study goes further to compare the characteristics of naturally acquired immune responses to asexual parasite antigen MSP3 and sexual stage antigen Pfs230 in both afebrile adults and children living in two communities with different malaria parasite prevalence and transmission intensities.…”

Assessment of the relationship between gametocyte density, multiplicity of infection and mosquito infectivity in Plasmodium falciparum infections

“…Based on the central role of gametocytes in propagating and sustaining malaria transmission, the prevalence of gametocytes is largely used as a parameter of the disease transmission [11,12]. Studies in malaria endemic and high transmission areas have reported high asexual parasite and gametocyte prevalence and densities in children relative to adults [13,14]. In such high malaria transmission settings, due to repeated parasite exposure, older children and adults develop immunity against the parasite [15,16].…”

“…In such high malaria transmission settings, due to repeated parasite exposure, older children and adults develop immunity against the parasite [15,16]. As a result, this category of people are most likely to experience asymptomatic infections harbouring gametocytes at microscopic and sub-microscopic densities thereby serving as efficient parasite reservoirs for sustaining malaria transmission [12,14,17].…”