Evaluating Molecular Xenomonitoring as a Tool for Lymphatic Filariasis Surveillance in Samoa, 2018-2019

Abstract

Molecular xenomonitoring (MX), the detection of filarial DNA in mosquitoes using molecular methods (PCR), is a potentially useful surveillance strategy for lymphatic filariasis (LF) elimination programs. Delay in filarial antigen (Ag) clearance post-treatment is a limitation of using human surveys to provide an early indicator of the impact of mass drug administration (MDA), and MX may be more useful in this setting. We compared prevalence of infected mosquitoes pre- and post-MDA (2018 and 2019) in 35 primary sampling units (PSUs) in Samoa, and investigated associations between the presence of PCR-positive mosquitoes and Ag-positive humans. We observed a statistically significant decline in estimated mosquito infection prevalence post-MDA at the national level (from 0.9% to 0.3%, OR 0.4) but no change in human Ag prevalence during this time. Ag prevalence in 2019 was higher in randomly selected PSUs where PCR-positive pools were detected (1.4% in ages 5-9; 4.8% in ages ≥10), compared to those where PCR-positive pools were not detected (0.2% in ages 5-9; 3.2% in ages ≥10). Our study provides promising evidence for MX as a complement to human surveys in post-MDA surveillance.

Keywords: elephantiasis; entomology; molecular xenomonitoring; neglected tropical diseases; vector-borne disease.

Figure 1

Map of Samoa showing approximate locations of the 35 primary sampling units (PSUs). Villages included in each PSU are given in Supplementary Figure S1.1. Spatial data on country, island, region, and village boundaries in Samoa were obtained from the Pacific Data Hub (pacificdata.org accessed on 8 July 2020) and DIVA-GIS (diva-gis.org, accessed on 12 August 2019). Regions are Apia Urban Area (AUA), North-West Upolu (NWU), Rest of Upolu (ROU) and Savai’i (SAV).

Figure 2

Timeline of 2018 and 2019 surveys (human and mosquitoes) relative to the rollout of the triple-drug mass drug administration [18] in Samoa.

Figure 3

Presence of female mosquitoes (Ae. polynesiensis and “any species”) PCR-positive for W. bancrofti by primary sampling unit (PSU), Samoa. Data from 2018 shown in the left semicircle, and 2019 in the right semicircle.

Figure 4

Estimated infection prevalence (%) by mosquito species, region and year (using data from the 28 randomly selected primary sampling units (PSUs) surveyed in both 2018 and 2019), Samoa. AUA = Apia Urban Area; NWU = North-West Upolu; ROU = Rest of Upolu; SAV = Savai’i. Values provided in Supplementary Table S3.1.

Figure 5

Adjusted antigen prevalence from human survey in 2018 and 2019 for 30 randomly selected primary sampling units (PSUs) in Samoa for (a) 5–9 year-olds and (b) ≥10 year-olds. Adjusted for selection probability at PSU and individual levels, clustering at the PSU level, finite population correction, and standardized for age and gender.

Figure 6

Estimated Ag prevalence in primary sampling units (PSUs) with and without PCR-positive mosquito pools in (a) 2018 and (b) 2019.

Figure 7

Change in prevalence from 2018 to 2019 in Samoa, expressed as an odds ratio (OR), for mosquito infection prevalence (MX for all species and Ae. polynesiensis), and human antigen prevalence (in those aged ≥10 years, and 5–9 years). Given the low prevalence, the ORs are approximately equal to prevalence ratios. ORs < 1 indicate decrease in infection prevalence in 2019 compared to 2018, ORs > 1 indicate an increase, and OR of 1 indicate no change. OR could not be calculated for 5–9-year-olds in AUA and ROU because no antigen-positive cases were detected in these groups in 2019. AUA = Apia Urban Area; NWU = North-West Upolu; ROU = Rest of Upolu; SAV = Savai’i.