Environmental Factors Associated With Soil Prevalence of the Melioidosis Pathogen Burkholderia pseudomallei: A Longitudinal Seasonal Study From South West India

Abstract

Melioidosis is a seasonal infectious disease in tropical and subtropical areas caused by the soil bacterium Burkholderia pseudomallei. In many parts of the world, including South West India, most cases of human infections are reported during times of heavy rainfall, but the underlying causes of this phenomenon are not fully understood. India is among the countries with the highest predicted melioidosis burden globally, but there is very little information on the environmental distribution of B. pseudomallei and its determining factors. The present study aimed (i) to investigate the prevalence of B. pseudomallei in soil in South West India, (ii) determine geochemical factors associated with B. pseudomallei presence and (iii) look for potential seasonal patterns of B. pseudomallei soil abundance. Environmental samplings were performed in two regions during the monsoon and post-monsoon season and summer from July 2016 to November 2018. We applied direct quantitative real time PCR (qPCR) together with culture protocols to overcome the insufficient sensitivity of solely culture-based B. pseudomallei detection from soil. A total of 1,704 soil samples from 20 different agricultural sites were screened for the presence of B. pseudomallei. Direct qPCR detected B. pseudomallei in all 20 sites and in 30.2% (517/1,704) of all soil samples, whereas only two samples from two sites were culture-positive. B. pseudomallei DNA-positive samples were negatively associated with the concentration of iron, manganese and nitrogen in a binomial logistic regression model. The highest number of B. pseudomallei-positive samples (42.6%, p < 0.0001) and the highest B. pseudomallei loads in positive samples [median 4.45 × 103 genome equivalents (GE)/g, p < 0.0001] were observed during the monsoon season and eventually declined to 18.9% and a median of 1.47 × 103 GE/g in summer. In conclusion, our study from South West India shows a wide environmental distribution of B. pseudomallei, but also considerable differences in the abundance between sites and within single sites. Our results support the hypothesis that nutrient-depleted habitats promote the presence of B. pseudomallei. Most importantly, the highest B. pseudomallei abundance in soil is seen during the rainy season, when melioidosis cases occur.

Shoulder Shake-up: Unveiling the Unusual Case of Acute Melioidosis

“…The disease is endemic to southeast Asia and northern Australia (1) and is also one of the emerging infections in India, where it is more concentrated in its subtropical, wetter, and peninsular parts while the drier, north-western part is relatively spared (2)(4). Unfortunately, due to a lack of awareness and poor suspicion, the diagnosis of melioidosis is often delayed or overlooked (3). Burkholderia pseudomallei can be found ubiquitously in soil, muddy water from irrigated elds, and animal excreta.…”

Rational design of an acidic erythritol (ACER) medium for the enhanced isolation of the environmental pathogen Burkholderia pseudomallei from soil samples

“…Although molecular detection does not necessarily indicate the presence of viable and culturable bacteria, the high discrepancy between molecular and culture-based B. pseudomallei detection rates points to a remarkable lack of sensitivity of commonly applied culture methods. Moreover, the fact, that culture-based environmental screenings in regions of high melioidosis endemicity have resulted in either no or only very few culture-positive samples ( Benoit et al, 2015 ; Wiersinga et al, 2015 ; Shaw et al, 2022 ), further indicates a potential sensitivity problem of the available culture methods used in those studies, including the currently recommended consensus method using TBSS-C50 ( Limmathurotsakul et al, 2013 ). We recently accomplished a significant improvement in the isolation rate of B. pseudomallei from rice paddy soil samples by introducing TBSS-C50-based erythritol medium in which erythritol is the sole carbon source ( Trinh et al, 2019 ).…”

Melioidosis and Burkholderia pseudomallei: progress in epidemiology, diagnosis, treatment and vaccination

“…Informative case series have been published from Tamil Nadu [18], Kerala [19] and Karnataka [20] in southern India and Odissa in eastern India [21]. An extensive soil sampling study from southwest India showed the wide environmental distribution of B. pseudomallei but with considerable differences in abundance between sites and within single sites, the highest abundance during the rainy season and the presence of B. pseudomallei linked to nutrient-depleted habitats [22 ▪ ].…”