Investigating Environmental Determinants of Hookworm Transmission using GPS Tracking and Metagenomics Technologies

Abstract

To identify potential sources of hookworm infections in a Ghanaian community of endemicity that could be targeted to interrupt transmission, we tracked the movements of infected and noninfected persons to their most frequented locations. Fifty-nine participants (29 hookworm positives and 30 negatives) wore GPS trackers for 10 consecutive days. Their movement data were captured in real time and overlaid on a community grid map. Soil samples were collected and divided into two parts: one for determining the physical and chemical properties and the other for culture of helminth larvae. Soil parameters were determined using standard methods, and the number of larvae recovered from Baermann cultures (expressed as larvae per gram of soil) was recorded. We found no significant difference in the larval counts between sites of infected and noninfected participants (P = 0.59). Sandy-loam soil, pH, and effective cation exchange capacity were associated with high larval recovery counts (P <0.001), whereas nitrogen and clay content were associated with low counts (P <0.001). Genomic DNA was extracted from helminth larvae, and species were identified using metagenomic analysis of DNA sequences. The dominant helminth species identified were Panagrolaimus superbus, Parastrongyloides trichosuri, Trichuris trichiura (human whipworm), and Ancylostoma caninum (dog hookworm). Despite Necator americanus being the predominant species in the community, no larvae of this species were identified. This study, however, demonstrates the feasibility of applying molecular tools for identifying environmental factors and places associated with exposure to human and zoonotic helminths, including areas that may be targeted to break transmission in communities where infection is endemic.

Figure 1.

Map of Ghana showing the Kintampo North Municipal area (insert). Kawampe is located on the main trunk road to the north of Ghana. Source: Map created with ArcGIS 10.8 with shapefiles from https://diva-gis.org/data.html.

Figure 2.

Soil factors significantly associated with high and low larval counts. ECEC = effective cation exchange capacity.

Figure 3.

Map of Kawampe showing the soil types at each sampled site. The Lima series soil type (yellow dots) was found mainly to the north of the community, while the Kumayili type (pink triangles) was more widespread and found mostly in the southern part of the community. The map was created with ArcGIS 10.8, and the base map was accessed April 23, 2023.

Figure 4.

(A) A three-dimensional illustration of the participants’ movements across space and time. The green patches are the areas where most participants spent most of their time, whereas the red and blue circles indicate the length of time spent by both hookworm-positive and hookworm-negative participants within these green patches, respectively. (B) A two-dimensional plot illustrates the movement patterns of the hookworm-positive group (brown lines) and the hookworm-negative group (blue lines). Red inverted triangles denote the exact points frequented by positive individuals and where the soils were sampled, whereas blue inverted triangles represent those of the negative individuals.

Figure 5.

Distribution of dominant helminth parasites found in specific areas within the study community: Parastrongyloides trichosuri (blue), Panagrolaimus superbus (green), Trichuris trichiura (yellow), and Ancylostoma caninum (red). The counts are in parentheses. The map was created with ArcGIS 10.8, and the base map was accessed April 23, 2023.