Abstract
BackgroundSimulium damnosum sensu lato (s.l.) blackflies transmit Onchocerca volvulus, a filarial nematode that causes human onchocerciasis. Human landing catches (HLCs) is currently the sole method used to estimate blackfly biting rates but is labour-intensive and questionable on ethical grounds. A potential alternative is to measure host antibodies to vector saliva deposited during bloodfeeding. In this study, immunoassays to quantify human antibody responses to S. damnosum s.l. saliva were developed, and the salivary proteome of S. damnosum s.l. was investigated.Methodology/Principal findingsBlood samples from people living in onchocerciasis-endemic areas in Ghana were collected during the wet season; samples from people living in Accra, a blackfly-free area, were considered negative controls and compared to samples from blackfly-free locations in Sudan. Blackflies were collected by HLCs and dissected to extract their salivary glands. An ELISA measuring anti-S. damnosum s.l. salivary IgG and IgM was optimized and used to quantify the humoral immune response of 958 individuals. Both immunoassays differentiated negative controls from endemic participants. Salivary proteins were separated by gel-electrophoresis, and antigenic proteins visualized by immunoblot. Liquid chromatography mass spectrometry (LC–MS/MS) was performed to characterize the proteome of S. damnosum s.l. salivary glands. Several antigenic proteins were recognized, with the major ones located around 15 and 40 kDa. LC–MS/MS identified the presence of antigen 5-related protein, apyrase/nucleotidase, and hyaluronidase.Conclusions/SignificanceThis study validated for the first time human immunoassays that quantify humoral immune responses as potential markers of exposure to blackfly bites. These assays have the potential to facilitate understanding patterns of exposure as well as evaluating the impact of vector control on biting rates. Future studies need to investigate seasonal fluctuations of these antibody responses, potential cross-reactions with other bloodsucking arthropods, and thoroughly identify the most immunogenic proteins.
Highlights
Human onchocerciasis or river blindness is a severely debilitating parasitic disease caused by the filarial nematode Onchocerca volvulus (Nematoda: Filarioidea) and is transmitted via bites of infective haematophagous female blackflies (Diptera: Simuliidae)
We examine the humoral immune response against S. damnosum s.l. in humans living in onchocerciasis-endemic communities in Ghana and propose a novel tool to evaluate blackfly exposure in onchocerciasis epidemiological and vector control studies
We report on the development of immunoassays against S. damnosum s.l. salivary antigens, provide a characterization of its proteome, and discuss the potential use of certain salivary components as host exposure markers, the results of which can be used to improve our understanding of onchocerciasis transmission dynamics towards its control and elimination in African settings
Summary
Human onchocerciasis or river blindness is a severely debilitating parasitic disease caused by the filarial nematode Onchocerca volvulus (Nematoda: Filarioidea) and is transmitted via bites of infective haematophagous female blackflies (Diptera: Simuliidae). Measuring individual heterogeneity in exposure to blackfly bites requires counting the actual number of blackflies landing and successfully feeding on individual villagers during their routine day-time activities [11] These procedures raise ethical concerns about enhanced risk of infection for those involved and are unable to provide robust measures of effective exposure to biting between and within endemic communities. Developing and validating alternative methods for measuring exposure to blackfly bites is highly desirable Data obtained using such methods would improve the parameterization of onchocerciasis transmission models by using independent exposure data, since currently exposure patterns are inferred from parasitological data, which compound exposure to vector bites and infection processes [7]. Immunoassays to quantify human antibody responses to S. damnosum s.l. saliva were developed, and the salivary proteome of S. damnosum s.l. was investigated
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