From contaminated soils to urban communities: Tracing the cryptic transmission routes of Burkholderia pseudomallei ST-1996 in an expanding urban melioidosis hotspot

Abstract

Introduction

Melioidosis, caused by the bacterium Burkholderia pseudomallei, is on the rise globally, rarely emerging in urban centres. In Hong Kong, a dense city battered by typhoons, the novel sequence type B. pseudomallei ST-1996 has caused a deadly outbreak in 2022. Tracing its transmission routes is critical controlling these elusive bacteria.

Material and Methods

This multifaceted investigation built on prior identification of B. pseudomallei in high ground soils. Dye tracing and isolation mapped stormwater drainage connectivity downstream catchpits. Air sampling across varying distances from outlets during rapid rainwater flows assess airborne risks. 5000-L air were drawn onto Ashdown's agar and incubated aerobically at 35°C for 10 days.

In total, 88 clinical isolates from 2015-2023 and 54 environmental samples underwent analysis. Whole-genome sequencing and core-gene SNP phylogenetic analysis assessed genetic relatedness among isolates.

Results

A total of 864 environmental samples were collected across Sham Shui Po district. B. pseudomallei was isolated from 8 soil, 6 water, 41 air samples. Core-gene phylogeny revealed genomic clustering of ST-1996 strains from patient samples and environmental sources, sharing 97.51%-100% SNP identity over 1652 core-genes. Air sampling along the stormwater drainage network detected viable airborne ST-1996 up to 45 meters horizontally and 13 meters vertically from catchpit outlets, with concentrations increasing with rainfall intensity during typhoons. Of Sham Shui Po patients, 63% of cases were presented with pneumonia, supporting investigation of airborne transmission pathways.

Discussion

This integrated study uncovered ST-1996 transmission through interconnected environments, infecting communities via confined stormwater networks and wind-dispersed aerosols, resulting in predominate pneumonia after exposure. Urbanization obscures bacterial routes, but elucidating transmission dynamics through epidemiology, molecular biology and environmental science enables targeted control by guiding policymakers on interventions. With global warming intensifying typhoons, environmental tracing and weather-based preparedness can guide effective public health interventions to safeguard populations in emerging melioidosis hotspots worldwide.