Demographic patterns of human antibody levels to Simulium damnosum s.l. saliva in onchocerciasis-endemic areas: An indicator of exposure to vector bites

Willen, L; Milton, P; Hamley, JID; Walker, M; Osei-Atweneboana, M; Volf, P; Basanez, MG; Courtenay, O

Abstract

BackgroundIn onchocerciasis endemic areas in Africa, heterogenous biting rates by blackfly vectors on humans are assumed to partially explain age- and sex-dependent infection patterns with Onchocerca volvulus. To underpin these assumptions and further improve predictions made by onchocerciasis transmission models, demographic patterns in antibody responses to salivary antigens of Simulium damnosum s.l. are evaluated as a measure of blackfly exposure. Methodology/Principal findingsRecently developed IgG and IgM anti-saliva immunoassays for S. damnosum s.l. were applied to blood samples collected from residents in four onchocerciasis endemic villages in Ghana. Demographic patterns in antibody levels according to village, sex and age were explored by fitting generalized linear models. Antibody levels varied between villages but showed consistent patterns with age and sex. Both IgG and IgM responses declined with increasing age. IgG responses were generally lower in males than in females and exhibited a steeper decline in adult males than in adult females. No sex-specific difference was observed in IgM responses. Conclusions/SignificanceThe decline in age-specific antibody patterns suggested development of immunotolerance or desensitization to blackfly saliva antigen in response to persistent exposure. The variation between sexes, and between adults and youngsters may reflect differences in behaviour influencing cumulative exposure. These measures of antibody acquisition and decay could be incorporated into onchocerciasis transmission models towards informing onchocerciasis control, elimination, and surveillance. Author summaryOnchocerciasis, a disease caused by the helminth parasite Onchocerca volvulus, is transmitted by the bites of female Simulium blackflies. The disease is still endemic in many African countries, and the World Health Organization has proposed elimination of its transmission in 12 countries by 2030. Understanding the heterogeneity in human exposure to vector bites can help discern which portion of the population is at higher risk of acquiring/ transmitting infection and is fundamental to identifying target groups for serological monitoring and transmission control. Traditionally, blackfly biting rates are estimated by performing human landing catches, a method that is often considered unethical and which can be unreliable as a representative measure. Therefore, we used our recently developed immunoassays to measure human antibody responses to antigens contained in the saliva of blackflies and deposited into human skin when they bloodfeed. In onchocerciasis endemic communities in Ghana, we measured antibody responses to understand age- and/or sex-related demographic patterns in vector exposure. We observed lower antibody responses in males compared to in females, and a substantial decline with increasing age, suggesting that high blackfly biting pressure induces desensitization in the human host.

Citation

Willen, L., Milton, P., Hamley, J., Walker, M., Osei-Atweneboana, M., Volf, P., …Courtenay, O. (2022). Demographic patterns of human antibody levels to Simulium damnosum s.l. saliva in onchocerciasis-endemic areas: An indicator of exposure to vector bites. PLoS Neglected Tropical Diseases, 16(1), https://doi.org/10.1371/journal.pntd.0010108

• Journal Article Type: Article
• Acceptance Date: Dec 17, 2021
• Publication Date: 2022
• Deposit Date: Feb 4, 2022
• Publicly Available Date: Feb 4, 2022
• Print ISSN: 1935-2727
• Publisher: Public Library of Science
• Peer Reviewed: Peer Reviewed
• Volume: 16
• Issue: 1
• DOI: https://doi.org/10.1371/journal.pntd.0010108
• Keywords: INFECTION; TRANSMISSION; ELIMINATION; IVERMECTIN; RESPONSES; DYNAMICS; EFFICACY; IGG4; NETS
• Public URL: https://rvc-repository.worktribe.com/output/1557336