Inhalable antibiotic resistomes emitted from hospitals: metagenomic insights into bacterial hosts, clinical relevance, and environmental risks

Abstract

Background Threats of antimicrobial resistance (AMR) to human health are on the rise worldwide. Airborne fine particulate matter (PM2.5), especially those emitted from hospitals, could serve as a substantial yet lesser-known environmental medium of inhalable antibiotic resistomes. A genome-centric understanding of the hosting bacterial taxa, mobility potential, and consequent risks of the resistomes is needed to reveal the health relevance of PM2.5-associated AMR from clinical settings. Results Compared to urban ambient air PM2.5, the hospital samples harbored nearly twice the abundance of antibiotic resistantance genes (ARGs, ~ 0.2 log10(ARGs/16S rRNA gene)) in the summer and winter sampled. The profiled resistome was closely correlated with the human-source-influenced (~ 30% of the contribution) bacterial community (Procrustes test, P < 0.001), reflecting the potential antibiotic-resistant bacteria (PARB), such as the human commensals Staphylococcus spp. and Corynebacterium spp. Despite the reduced abundance and diversity of the assembled metagenomes from summer to winter, the high horizontal transfer potential of ARGs, such as the clinically relevant blaOXA and bacA, in the human virulent PARB remained unaffected in the hospital air PM samples. The occurring patterns of β-lactam resistance genes and their hosting genomes in the studied hospital-emitting PM2.5 were closely related to the in-ward β-lactam-resistant infections (SEM, std = 0.62, P < 0.01). Featured with more abundant potentially virulent PARB (2.89 genome copies/m3-air), the hospital samples had significantly higher resistome risk index scores than the urban ambient air samples, indicating that daily human exposure to virulent PARB via the inhalation of PM2.5 was ten times greater than from the ingestion of drinking water. Conclusions The significance of AMR in the studied hospital-emitting PM2.5 was highlighted by the greater abundance of ARGs, the prevalence of potentially virulent PARB, and the close association with hospital in-ward β-lactam infections. A larger-scale multi-source comparison of genome-resolved antibiotic resistomes is needed to provide a more holistic understanding to evaluate the importance of airborne AMR from the “One-Health” perspective.

Widespread of Potential Pathogen-Derived Extracellular Vesicles Carrying Antibiotic Resistance Genes in Indoor Dust

“…9 ARGs harbored in PM can be a resource providing antibiotic resistance from the "One Health" perspective. 10 As people spend approximately 90% of their time on indoor activities in modern life, 11 the indoor environment is vital for public health. Therefore, understanding the prevalence, status, and transmission mechanism of ARGs in indoor dust is of great importance for assessing the exposure risk of humans to antibiotic resistance.…”

“…Accumulating evidence has revealed that the air environment is a large reservoir of ARGs. − Airborne transmission has been contempered to be a crucial route for ARGs’ spread and exposure. , Particle matter (PM), which is an important airborne contaminant, offers a large volume of adhering sites, thus enhancing the stability of ARGs in the air . ARGs harbored in PM can be a resource providing antibiotic resistance from the “One Health” perspective . As people spend approximately 90% of their time on indoor activities in modern life, the indoor environment is vital for public health.…”

Regionalization and Shaping Factors for Microbiomes and Core Resistomes in Atmospheric Particulate Matters

“…Meanwhile, a lack of correlation was reported between microbiomes and resistomes in the intestinal tracts of migration birds ( 42 ). Few reports have investigated the correlation between APM microbiomes and resistomes, except for a recent publication on Microbiome that collected emitted bioaerosols of a hospital ( n = 19) in Guangzhou city and urban PM 2.5 ( n = 10) in the same city for analysis ( 43 ). A significant correlation was found between APM microbiomes and resistomes in the hospital but not for urban APM samples.…”

Critical review of antibiotic resistance genes in the atmosphere

“…These included rpoB2 (tuberculosis drugs), vanR, ugd, blaOXA, class-a, msrA, tetL, and bacA. 76 These ndings suggest that human activity inside of a hospital, and any indoor environment, could lead to an increase of ARGs in the air, and therefore increase the likelihood of exposure to ARGs.…”

“…Interestingly, they also found that the difference between the relative abundance of ARGs in the urban and hospital settings was much more pronounced in the summertime, especially for MLS and β-lactam. 76 Another hospital study in China showed that the diversity of ARGs was higher during the winter, but the abundances were comparable. In this study, samples were collected from the air filtration system in the hospital and could have been more affected by seasonal changes in operation rather than by the weather itself.…”