Abstract
Background: Colistin is one of the last-line antimicrobial agents against life-threatening infections. The distribution of the colistin resistance gene mcr-1 has been reported worldwide. However, most studies have focused on the distribution of mcr-1-positive bacteria in humans, animals, food, and sewage; few have focused on their distribution in natural environments. Method: We conducted a large spatial survey of mcr-1-positive Escherichia coli at 119 sites in 48 rivers, covering the entire island of Taiwan. We investigated the relationship between the livestock or poultry density in the surveyed riverine area and the number of mcr-1-positive E. coli in the river water. We then sequenced and characterized the isolated mcr-1-positive plasmids. Results: Seven mcr-1 positive E. coli were isolated from 5.9% of the sampling sites. The mcr-1-positive sites correlated with high chicken and pig stocking densities but not human population density or other river parameters. Four of the mcr-1-positive E. coli strains harbored epidemic IncX4 plasmids, and three of them exhibited identical sequences with a size of 33,309 bp. One of the plasmids contained identical 33,309 bp sequences but carried an additional 5711-bp transposon (Tn3 family). To our knowledge, this is the first demonstration that mcr-1-carrying IncX4 plasmids can contain an insertion of such transposons. All mcr-1-positive isolates belonged to phylogenetic group A and harbored few known virulence genes. Conclusion: This study showed a positive relationship between the number of mcr-1-positive sites and high livestock and poultry density. The sequencing analyses indicated that the epidemic plasmid in the mcr-1 isolates circulates not only in humans, animals, and food but also in the associated environments or natural habitats in Taiwan, suggesting that the surveillance of antibiotics-resistance genes for livestock or poultry farm quality control should include their associated environments.
Highlights
The rapid emergence and dissemination of antibiotic-resistant bacteria has become a serious threat to public health globally
Mcr-1-positive E. coli were found at 5.9% (7/119) of the water sampling sites in the rivers of Taiwan
The cessation of colistin use as a feed additive for animals in China has significantly decreased the prevalence of mcr-1 in farmed pigs nationally, including IncX4 plasmid-carrying mcr-1, which may contribute to a concomitant decline of the distribution of mcr-1 in human carriers [63]. These findings indicate that antibiotic selection pressure is a major driving force of mcr-1 dissemination; the withdrawal of colistin from animal feeds would be an effective strategy for controlling the dissemination of mcr-1 in humans, animals, and the natural environment
Summary
The rapid emergence and dissemination of antibiotic-resistant bacteria has become a serious threat to public health globally. After the first report by Lui in China in 2015, the plasmid-mediated colistin resistance gene mcr-1 has been found to be widespread in five continents [1,2]. Mcr-1 carrying isolates can be found in raw meat, livestock animals, infections, and healthy people [1,4]. A higher number or percentage of mcr-1 carriage in E. coli isolates has been found in raw meat and food animals than in human isolates [1]. A study conducted in China found that 6% of human fecal samples carried the mcr-1 gene [6]. Similar to studies in other countries, the rate of mcr-1 positive isolates from meat and swine/poultry diseases in Taiwan exceeds that in isolates from humans (retail meats: 8.7% in 2015; diseased swine: 33.3% in 2016) [7,10].
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