Spatial heterogeneity in Onchocerca volvulus IgG4 seroprevalence around a blackfly (Simulium damnosum s.l.) breeding site in Ghana and its implications for onchocerciasis serosurveillance
Kyomuhangi, I.; Otabil, K. B.; Acheampong, A.; Ofori, D. K.; Kudzordzi, P.-C.; Nyarko, P.; Fronterre, C.; Cheke, R. A.; Basanez, M.-G.; Hawkes, F.
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Progress towards elimination of onchocerciasis transmission is evaluated using entomological and serological indicators. The latter assesses anti-Ov16 IgG4 seroprevalence in children aged <10 years. A seroprevalence of <0.1% suggests that ivermectin Mass Drug Administration (MDA) can be stopped and post-treatment surveillance initiated, according to World Health Organization (WHO) guidelines. Surveillance of populations living in close proximity to vector breeding sites and first-line villages may mask spatial transmission heterogeneity. We mapped anti-Ov16 seroprevalence within a 25-km radius around a known Simulium damnosum s.l. breeding site in Asubende, Ghana, to assess its spatial patterns and their implications for serosurveillance. A cross-sectional survey was conducted in September-November 2024 in 30 settlements. Individuals aged [≥]3 years were recruited through convenience sampling. The Ov16 rapid diagnostic test (RDT) using dry blood spots was used to estimate overall and site-level seroprevalence. Generalized additive models were used to assess seroprevalence trends versus distance from the breeding site. Among 2,479 participants with valid RDT results, overall seroprevalence was 10.0% (95% CI: 8.9%, 11.3%) and increased with age. Seroprevalence varied across sites (0-24.4%) and declined with increasing distance from the breeding site. Among 584 children <10 years old, seroprevalence was 1.5% (95% CI: 0.7%, 2.9%). Adjusting for RDT sensitivity and specificity, seroprevalence in this age-group was 0.7%, (95% CI: 0%, 2.4%). Seropositive children were detected up to 18 km from the breeding site, but none were identified at it. The distance-related decrease in overall seroprevalence is consistent with spatial patterns in vector abundance at Asubende and implies higher cumulative exposure near the breeding site. The small number of children tested limited inference in this WHO target age-group. Detection of seropositive children away from, but not at, the breeding site highlights limitations of surveillance focused on first-line villages and supports broader spatial sampling to strengthen evidence for stop-MDA decisions. Author summaryAfter decades of onchocerciasis control using ivermectin, many countries hope to demonstrate that they have interrupted transmission of this vector-borne parasitic disease using serological surveys. It is unclear whether exposure to infection is spatially clustered around the riverine breeding sites of the blackfly vectors and therefore whether this is where serosurveillance should focus. To address this, we collected dried blood spots from 2,480 consenting participants aged 3-96 years old from 29 communities within a 25-km radius of a known blackfly breeding site in Asubende, Ghana. A rapid diagnostic test was used to test the blood spots for antibodies to the Onchocerca volvulus parasite. We found that overall seropositivity declined with increasing distance from the breeding site, which suggests that cumulative exposure is higher near the breeding site, where vector population is also high. However, seropositivity in children (3-10-year-olds, n= 584), which is indicative of recent transmission, was spatially distributed across the study area and found up to 18 km from the breeding site. These findings are relevant to serosurveillance sampling strategies intended to detect low levels of transmission, which could miss peripheral evidence of ongoing transmission if they are focussed at breeding sites and those villages closest to them.
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